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Current Medicinal Chemistry

Author(s): Marian Vincenzi, Flavia Anna Mercurio and Marilisa Leone*

DOI: 10.2174/0929867327666200702131032

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NMR Spectroscopy in the Conformational Analysis of Peptides: An Overview

Page: [2729 - 2782] Pages: 54

  • * (Excluding Mailing and Handling)

Abstract

Background: NMR spectroscopy is one of the most powerful tools to study the structure and interaction properties of peptides and proteins from a dynamic perspective. Knowing the bioactive conformations of peptides is crucial in the drug discovery field to design more efficient analogue ligands and inhibitors of protein-protein interactions targeting therapeutically relevant systems.

Objective: This review provides a toolkit to investigate peptide conformational properties by NMR.

Methods: Articles cited herein, related to NMR studies of peptides and proteins were mainly searched through PubMed and the web. More recent and old books on NMR spectroscopy written by eminent scientists in the field were consulted as well.

Results: The review is mainly focused on NMR tools to gain the 3D structure of small unlabeled peptides. It is more application-oriented as it is beyond its goal to deliver a profound theoretical background. However, the basic principles of 2D homonuclear and heteronuclear experiments are briefly described. Protocols to obtain isotopically labeled peptides and principal triple resonance experiments needed to study them, are discussed as well.

Conclusion: NMR is a leading technique in the study of conformational preferences of small flexible peptides whose structure can be often only described by an ensemble of conformations. Although NMR studies of peptides can be easily and fast performed by canonical protocols established a few decades ago, more recently we have assisted to tremendous improvements of NMR spectroscopy to investigate instead large systems and overcome its molecular weight limit.

Keywords: NMR, structural biology, peptides, proteins, conformational ensemble, distance and angular restraints, bioactive conformation.

[1]
Gauto, D.F.; Estrozi, L.F.; Schwieters, C.D.; Effantin, G.; Macek, P.; Sounier, R.; Sivertsen, A.C.; Schmidt, E.; Kerfah, R.; Mas, G.; Colletier, J.P.; Güntert, P.; Favier, A.; Schoehn, G.; Schanda, P.; Boisbouvier, J. Integrated NMR and cryo-EM atomic-resolution structure determination of a half-megadalton enzyme complex. Nat. Commun., 2019, 10(1), 2697.
[http://dx.doi.org/10.1038/s41467-019-10490-9] [PMID: 31217444]
[2]
Cerofolini, L.; Fragai, M.; Ravera, E.; Diebolder, C.A.; Renault, L.; Calderone, V. Integrative approaches in structural biology: a more complete picture from the combination of individual techniques. Biomolecules, 2019, 9(8), E370.
[http://dx.doi.org/10.3390/biom9080370] [PMID: 31416261]
[3]
Acharya, K.R.; Lloyd, M.D. The advantages and limitations of protein crystal structures. Trends Pharmacol. Sci., 2005, 26(1), 10-14.
[http://dx.doi.org/10.1016/j.tips.2004.10.011] [PMID: 15629199]
[4]
Tugarinov, V.; Hwang, P.M.; Ollerenshaw, J.E.; Kay, L.E. Cross-correlated relaxation enhanced 1H[bond]13C NMR spectroscopy of methyl groups in very high molecular weight proteins and protein complexes. J. Am. Chem. Soc., 2003, 125(34), 10420-10428.
[http://dx.doi.org/10.1021/ja030153x] [PMID: 12926967]
[5]
Tugarinov, V.; Sprangers, R.; Kay, L.E. Line narrowing in methyl-TROSY using zero-quantum 1H-13C NMR spectroscopy. J. Am. Chem. Soc., 2004, 126(15), 4921-4925.
[http://dx.doi.org/10.1021/ja039732s] [PMID: 15080697]
[6]
Schanda, P.; Ernst, M. Studying dynamics by magic-angle spinning solid-state NMR spectroscopy: principles and applications to biomolecules. Prog. Nucl. Magn. Reson. Spectrosc., 2016, 96, 1-46.
[http://dx.doi.org/10.1016/j.pnmrs.2016.02.001] [PMID: 27110043]
[7]
Andreas, L.B.; Le Marchand, T.; Jaudzems, K.; Pintacuda, G. High-resolution proton-detected NMR of proteins at very fast MAS. J. Magn. Reson., 2015, 253, 36-49.
[http://dx.doi.org/10.1016/j.jmr.2015.01.003] [PMID: 25797003]
[8]
Ohno, A.; Inomata, K.; Tochio, H.; Shirakawa, M. Application of NMR spectroscopy in medicinal chemistry and drug discovery. Curr. Top. Med. Chem., 2011, 11(1), 68-73.
[http://dx.doi.org/10.2174/156802611793611878] [PMID: 20809894]
[9]
Danielson, M.A.; Falke, J.J. Use of 19F NMR to probe protein structure and conformational changes. Annu. Rev. Biophys. Biomol. Struct., 1996, 25, 163-195.
[http://dx.doi.org/10.1146/annurev.bb.25.060196.001115] [PMID: 8800468]
[10]
Boeszoermenyi, A.; Chhabra, S.; Dubey, A.; Radeva, D.L.; Burdzhiev, N.T.; Chanev, C.D.; Petrov, O.I.; Gelev, V.M.; Zhang, M.; Anklin, C.; Kovacs, H.; Wagner, G.; Kuprov, I.; Takeuchi, K.; Arthanari, H. Aromatic 19F-13C TROSY: a background-free approach to probe biomolecular structure, function, and dynamics. Nat. Methods, 2019, 16(4), 333-340.
[http://dx.doi.org/10.1038/s41592-019-0334-x] [PMID: 30858598]
[11]
Leone, M.; Rodriguez-Mias, R.A.; Pellecchia, M. Selective incorporation of 19F-labeled Trp side chains for NMR-spectroscopy-based ligand-protein interaction studies. Chem. Bio. Chem., 2003, 4(7), 649-650.
[http://dx.doi.org/10.1002/cbic.200300597] [PMID: 12851935]
[12]
Comparison of crystallography, NMR and EM. Available at: https://www.creative-biostructure.com/comparison-of-crystallography-nmr-and-em_6.htm [Accessed date: 15th March 2020].
[13]
Renaud, J.P.; Chari, A.; Ciferri, C.; Liu, W.T.; Rémigy, H.W.; Stark, H.; Wiesmann, C. Cryo-EM in drug discovery: achievements, limitations and prospects. Nat. Rev. Drug Discov., 2018, 17(7), 471-492.
[http://dx.doi.org/10.1038/nrd.2018.77] [PMID: 29880918]
[14]
Lau, J.L.; Dunn, M.K. Therapeutic peptides: historical perspectives, current development trends, and future directions. Bioorg. Med. Chem., 2018, 26(10), 2700-2707.
[http://dx.doi.org/10.1016/j.bmc.2017.06.052] [PMID: 28720325]
[15]
Hinds, M.G.; Norton, R.S. NMR spectroscopy of peptides and proteins. Practical considerations. Mol. Biotechnol., 1997, 7(3), 315-331.
[http://dx.doi.org/10.1007/BF02740822] [PMID: 9219245]
[16]
D’Hondt, M.; Bracke, N.; Taevernier, L.; Gevaert, B.; Verbeke, F.; Wynendaele, E.; De Spiegeleer, B. Related impurities in peptide medicines. J. Pharm. Biomed. Anal., 2014, 101, 2-30.
[http://dx.doi.org/10.1016/j.jpba.2014.06.012] [PMID: 25044089]
[17]
King, G.F.; Mobli, M. Derivation of peptide and protein structures using NMR spectroscopy. In: Comprehensive natural products II - Chemistry and biology; Mander, L; Liu, H.-W, Eds.; Elsevier Science & Technology Books: Oxford, England, ,2010, 9, pp. 279-325.
[http://dx.doi.org/10.1016/B978-008045382-8.00653-5]
[18]
Zerbe, O.; Bader, R. Peptide NMR. Available at: http://www.chem.uzh.ch/zerbe/ [Accessed date: 15th March 2020].
[19]
Wishart, D.S.; Bigam, C.G.; Yao, J.; Abildgaard, F.; Dyson, H.J.; Oldfield, E.; Markley, J.L.; Sykes, B.D. 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR, 1995, 6(2), 135-140.
[http://dx.doi.org/10.1007/BF00211777] [PMID: 8589602]
[20]
Vincenzi, M.; Mercurio, F.A.; Leone, M. About TFE: old and new findings. Curr. Protein Pept. Sci., 2019, 20(5), 425-451.
[http://dx.doi.org/10.2174/1389203720666190214152439] [PMID: 30767740]
[21]
Hinds, M.G.; Norton, R.S. NMR spectroscopy of peptides and proteins. Methods Mol. Biol., 1994, 36, 131-154.
[http://dx.doi.org/10.1385/0-89603-274-4:131] [PMID: 7697108]
[22]
Cavanagh, J.; Fairbrother, W.J.; Palmer, A.G. III.; Skelton, N.J. Water suppression techniques. In: Protein NMR Spectroscopy principles and practice, 1st ed; Academic Press: San Diego, 1996; pp. 146-158.
[23]
Hore, P.J. Nuclear magnetic resonance. Solvent suppression. Methods Enzymol., 1989, 176, 64-77.
[http://dx.doi.org/10.1016/0076-6879(89)76005-5] [PMID: 2811699]
[24]
Eads, T.M.; Kennedy, S.D.; Bryant, R.G. Solvent suppression in high-resolution proton nuclear magnetic resonance based on control of transverse relaxation rate. Anal. Chem., 1986, 58(8), 1752-1756.
[http://dx.doi.org/10.1021/ac00121a034] [PMID: 3752509]
[25]
Liu, M.; Mao, X.; Ye, C.; Huang, H.; Nicholson, J.K.; Lindon, J.C. Improved WATERGATE pulse sequences for solvent suppression in NMR spectroscopy. J. Magn. Reson., 1998, 132(1), 125-129.
[http://dx.doi.org/10.1006/jmre.1998.1405] [PMID: 9469907]
[26]
Hwang, T.L.; Shaka, A.J. Water suppression that works - excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson. A, 1995, 112(2), 275-279.
[http://dx.doi.org/10.1006/jmra.1995.1047]
[27]
Pellecchia, M.; Sem, D.S.; Wüthrich, K. NMR in drug discovery. Nat. Rev. Drug Discov., 2002, 1(3), 211-219.
[http://dx.doi.org/10.1038/nrd748] [PMID: 12120505]
[28]
Riek, R.; Pervushin, K.; Wüthrich, K. TROSY and CRINEPT: NMR with large molecular and supramolecular structures in solution. Trends Biochem. Sci., 2000, 25(10), 462-468.
[http://dx.doi.org/10.1016/S0968-0004(00)01665-0] [PMID: 11050425]
[29]
Koenig, B.W.; Rogowski, M.; Louis, J.M. A rapid method to attain isotope labeled small soluble peptides for NMR studies. J. Biomol. NMR, 2003, 26(3), 193-202.
[http://dx.doi.org/10.1023/A:1023887412387] [PMID: 12766417]
[30]
Mac, T.T.; Beyermann, M.; Pires, J.R.; Schmieder, P.; Oschkinat, H. High yield expression and purification of isotopically labelled human endothelin-1 for use in NMR studies. Protein Expr. Purif., 2006, 48(2), 253-260.
[http://dx.doi.org/10.1016/j.pep.2006.01.022] [PMID: 16584890]
[31]
Seo, E.S.; Vargues, T.; Clarke, D.J.; Uhrín, D.; Campopiano, D.J. Preparation of isotopically labelled recombinant beta-defensin for NMR studies. Protein Expr. Purif., 2009, 65(2), 179-184.
[http://dx.doi.org/10.1016/j.pep.2008.11.007] [PMID: 19063971]
[32]
Tapaneeyakorn, S.; Ross, S.; Attrill, H.; Watts, A. Heterologous high yield expression and purification of neurotensin and its functional fragment in Escherichia coli. Protein Expr. Purif., 2010, 74(1), 65-68.
[http://dx.doi.org/10.1016/j.pep.2010.06.014] [PMID: 20600945]
[33]
Wagstaff, J.L.; Howard, M.J.; Williamson, R.A. Production of recombinant isotopically labelled peptide by fusion to an insoluble partner protein: generation of integrin αvβ6 binding peptides for NMR. Mol. Biosyst., 2010, 6(12), 2380-2385.
[http://dx.doi.org/10.1039/c0mb00105h] [PMID: 20953501]
[34]
Mercurio, F.A.; Scaloni, A.; Caira, S.; Leone, M. The antimicrobial peptides casocidins I and II: Solution structural studies in water and different membrane-mimetic environments. Peptides, 2019, 114, 50-58.
[http://dx.doi.org/10.1016/j.peptides.2018.09.004] [PMID: 30243923]
[35]
Mercurio, F.A.; Di Natale, C.; Pirone, L.; Vincenzi, M.; Marasco, D.; De Luca, S.; Pedone, E.M.; Leone, M. Exploring the ability of cyclic peptides to target SAM domains: a computational and experimental study. Chem. Bio. Chem., 2020, 21(5), 702-711.
[http://dx.doi.org/10.1002/cbic.201900444] [PMID: 31538690]
[36]
Mandaliti, W.; Nepravishta, R.; Sinibaldi Vallebona, P.; Pica, F.; Garaci, E.; Paci, M. Thymosin α1 interacts with exposed phosphatidylserine in membrane models and in cells and uses serum albumin as a carrier. Biochemistry, 2016, 55(10), 1462-1472.
[http://dx.doi.org/10.1021/acs.biochem.5b01345] [PMID: 26909491]
[37]
Diaferia, C.; Mercurio, F.A.; Giannini, C.; Sibillano, T.; Morelli, G.; Leone, M.; Accardo, A. Self-assembly of PEGylated tetra-phenylalanine derivatives: structural insights from solution and solid state studies. Sci. Rep., 2016, 6, 26638.
[http://dx.doi.org/10.1038/srep26638] [PMID: 27220817]
[38]
Zhang, M. Recent developments of methyl-labeling strategies in Pichia pastoris for NMR spectroscopy. Protein Expr. Purif., 2020, 166, 105521.
[http://dx.doi.org/10.1016/j.pep.2019.105521] [PMID: 31654735]
[39]
Cavanagh, J.; Fairbrother, W.J.; Palmer, A.G. III.; Skelton, N.J. Sequential assignments and structure calculations. In: Protein NMR Spectroscopy principles and practice; Academic Press: San Diego, 1996; pp. 532-556.
[40]
Wuthrich, K. NMR of Proteins and Nucleic Acids; Wiley: New York, 1986.
[http://dx.doi.org/10.1051/epn/19861701011]
[41]
Piantini, U.; Sorensen, O.W.; Ernst, R.R. Multiple quantum filters for elucidating NMR coupling networks. J. Am. Chem. Soc., 1982, 104(24), 6800-6801.
[http://dx.doi.org/10.1021/ja00388a062]
[42]
Griesinger, C.; Otting, G.; Wuthrich, K.; Ernst, R.R. Clean TOCSY for proton spin system identification in macromolecules. J. Am. Chem. Soc., 1988, 110(23), 7870-7872.
[http://dx.doi.org/10.1021/ja00231a044]
[43]
Kumar, A.; Ernst, R.R.; Wüthrich, K. A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun., 1980, 95(1), 1-6.
[http://dx.doi.org/10.1016/0006-291X(80)90695-6] [PMID: 7417242]
[44]
Bax, A.; Davis, D.G. Practical aspects of two-dimensional transverse NOE spectroscopy. J. Magn. Reson., 1985, 63(1), 207-213.
[http://dx.doi.org/10.1016/0022-2364(85)90171-4]
[45]
Keeler, J. Chapter 7- Important 2D NMR experiments. In: Solving Problems with NMR Spectroscopy, 2nd ed.; Atta-ur- Rahman, Choudhary; M.I, Atia-tul-Wahab, Eds.; Academic Press (Elsevier), 2016, pp. 265-386.
[http://dx.doi.org/10.1016/B978-0-12-411589-7.00007-3]
[46]
Williamson, M.P. Nuclear magnetic resonance specroscopy - nuclear overhauser effect. Encyclopedia of Analytical Science, 2nd ed; Elsevier, 2005, pp. 342-349.
[http://dx.doi.org/10.1016/B0-12-369397-7/00412-X]
[47]
Hore, P.J.; Jones, J.A.; Wimperis, S. NMR: The Toolkit; Oxford University Press Inc.: New York, 2000.
[48]
Mandal, P.K.; Majumdar, A. A comprehensive discussion of HSQC and HMQC pulse sequences. Concept. Magn. Reson. A, 2004, 20(1), 1-23.
[http://dx.doi.org/10.1002/cmr.a.10095]
[49]
Uhrin, D.; Liptaj, T.; Kover, K.E. Modified bird pulses and design of heteronuclear pulse sequences. J. Magn. Reson. A, 1993, 101(1), 41-46.
[http://dx.doi.org/10.1006/jmra.1993.1005] [PMID: 26298081]
[50]
Pervushin, K. Impact of transverse relaxation optimized spectroscopy (TROSY) on NMR as a technique in structural biology. Q. Rev. Biophys., 2000, 33(2), 161-197.
[http://dx.doi.org/10.1017/S0033583500003619] [PMID: 11131563]
[51]
Schanda, P.; Kupce, E.; Brutscher, B. SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J. Biomol. NMR, 2005, 33(4), 199-211.
[http://dx.doi.org/10.1007/s10858-005-4425-x] [PMID: 16341750]
[52]
Schanda, P.; Brutscher, B. Very fast two-dimensional NMR spectroscopy for real-time investigation of dynamic events in proteins on the time scale of seconds. J. Am. Chem. Soc., 2005, 127(22), 8014-8015.
[http://dx.doi.org/10.1021/ja051306e] [PMID: 15926816]
[53]
Leopold, M.F.; Urbauer, J.L.; Wand, A.J. Resonance assignment strategies for the analysis of NMR spectra of proteins. Mol. Biotechnol., 1994, 2(1), 61-93.
[http://dx.doi.org/10.1007/BF02789290] [PMID: 7866869]
[54]
Biological magnetic resonance data bank. A repository for data from NMR spectroscopy on proteins, peptides, nucleic acids, and other biomolecules. Available at: http://www. bmrb.wisc.edu/ [Accessed date: 15th March 2020].
[55]
Romero, P.R.; Kobayashi, N.; Wedell, J.R.; Baskaran, K.; Iwata, T.; Yokochi, M.; Maziuk, D.; Yao, H.; Fujiwara, T.; Kurusu, G.; Ulrich, E.L.; Hoch, J.C.; Markley, J.L. BioMagResBank (BMRB) as a resource for structural biology. Methods Mol. Biol., 2020, 2112, 187-218.
[http://dx.doi.org/10.1007/978-1-0716-0270-6_14] [PMID: 32006287]
[56]
Ulrich, E.L.; Akutsu, H.; Doreleijers, J.F.; Harano, Y.; Ioannidis, Y.E.; Lin, J.; Livny, M.; Mading, S.; Maziuk, D.; Miller, Z.; Nakatani, E.; Schulte, C.F.; Tolmie, D.E.; Kent Wenger, R.; Yao, H.; Markley, J.L. BioMagResBank. Nucleic Acids Res., 2008, 36(Database issue), D402-D408.
[http://dx.doi.org/10.1093/nar/gkm957] [PMID: 17984079]
[57]
Full Chemical Shift Statistics. Statistics calculated for all chemical shifts from atoms in the 20 common amino acids. Available at: http://www.bmrb.wisc.edu/ftp/pub/bmrb/statistics/chem_shifts/full/statful_prot.txt [Accessed date: 15th March 2020].
[58]
Mercurio, F.A.; Di Natale, C.; Pirone, L.; Scognamiglio, P.L.; Marasco, D.; Pedone, E.M.; Saviano, M.; Leone, M. Peptide fragments of Odin-Sam1: conformational analysis and interaction studies with EphA2-sam. Chem. Bio. Chem., 2015, 16(11), 1629-1636.
[http://dx.doi.org/10.1002/cbic.201500197] [PMID: 26120079]
[59]
Güntert, P. Automated NMR structure calculation with CYANA. Methods Mol. Biol., 2004, 278, 353-378.
[http://dx.doi.org/10.1385/1-59259-809-9:353] [PMID: 15318003]
[60]
Dyson, H.J.; Palmer, A.G. III. Introduction to solution-state NMR spectroscopy. In: Comprehensive Biophysics. Biophysical Techniques for Structural Characterization of Macromolecules, 1st ed; Egelman, E.H., Ed.; Academic Press: Oxford, 2012; pp. 136-159.
[http://dx.doi.org/10.1016/B978-0-12-374920-8.00113-2]
[61]
Xu, J.; Weber, P.L.; Borer, P.N. Computer-assisted assignment of peptides with non-standard amino acids. J. Biomol. NMR, 1995, 5(2), 183-192.
[http://dx.doi.org/10.1007/BF00208809] [PMID: 7703701]
[62]
Artimo, P.; Jonnalagedda, M.; Arnold, K.; Baratin, D.; Csardi, G.; de Castro, E.; Duvaud, S.; Flegel, V.; Fortier, A.; Gasteiger, E.; Grosdidier, A.; Hernandez, C.; Ioannidis, V.; Kuznetsov, D.; Liechti, R.; Moretti, S.; Mostaguir, K.; Redaschi, N.; Rossier, G.; Xenarios, I.; Stockinger, H. Ex- PASy: SIB bioinformatics resource portal. Nucleic Acids Res., 2012, 40(Web Server issue), W597-603.
[http://dx.doi.org/10.1093/nar/gks400] [PMID: 22661580]
[63]
Wilkins, M.R.; Gasteiger, E.; Bairoch, A.; Sanchez, J.C.; Williams, K.L.; Appel, R.D.; Hochstrasser, D.F. Protein identification and analysis tools in the ExPASy server. Methods Mol. Biol., 1999, 112, 531-552.
[http://dx.doi.org/10.1385/1-59259-584-7:531] [PMID: 10027275]
[64]
Mercurio, F.A.; Scognamiglio, P.L.; Di Natale, C.; Marasco, D.; Pellecchia, M.; Leone, M. CD and NMR conformational studies of a peptide encompassing the Mid Loop interface of Ship2-Sam. Biopolymers, 2014, 101(11), 1088-1098.
[http://dx.doi.org/10.1002/bip.22512] [PMID: 24889333]
[65]
Vuister, G.W.; Bax, A.; Quantitative, J. Correlation: a new approach for measuring homonuclear 3-bond JHNH(Alpha) coupling-constants in 15N-enriched proteins. J. Am. Chem. Soc., 1993, 115(17), 7772-7777.
[http://dx.doi.org/10.1021/ja00070a024]
[66]
Archer, S.J.; Ikura, M.; Torchia, D.A.; Bax, A. An alternative 3D NMR technique for correlating backbone 15N with side-chain H-beta-resonances in larger proteins. J. Magn. Reson., 1991, 95(3), 636-641.
[http://dx.doi.org/10.1016/0022-2364(91)90182-S]
[67]
Düx, P.; Whitehead, B.; Boelens, R.; Kaptein, R.; Vuister, G.W. Measurement of (15)N- (1)H coupling constants in uniformly (15)N-labeled proteins: application to the photoactive yellow protein. J. Biomol. NMR, 1997, 10(3), 301-306.
[http://dx.doi.org/10.1023/A:1018393225804] [PMID: 20700833]
[68]
Leone, M.; Cellitti, J.; Pellecchia, M. The Sam domain of the lipid phosphatase Ship2 adopts a common model to interact with Arap3-Sam and EphA2-Sam. BMC Struct. Biol., 2009, 9, 59.
[http://dx.doi.org/10.1186/1472-6807-9-59] [PMID: 19765305]
[69]
Olejniczak, E.T.; Xu, R.X.; Fesik, S.W.A.A. 4D HCCH-TOCSY experiment for assigning the side chain 1H and 13C resonances of proteins. J. Biomol. NMR, 1992, 2(6), 655-659.
[http://dx.doi.org/10.1007/BF02192854] [PMID: 1283353]
[70]
Leone, M.; Cellitti, J.; Pellecchia, M. NMR studies of a heterotypic Sam-Sam domain association: the interaction between the lipid phosphatase Ship2 and the EphA2 receptor. Biochemistry, 2008, 47(48), 12721-12728.
[http://dx.doi.org/10.1021/bi801713f] [PMID: 18991394]
[71]
Mercurio, F.A.; Marasco, D.; Pirone, L.; Pedone, E.M.; Pellecchia, M.; Leone, M. Solution structure of the first Sam domain of Odin and binding studies with the EphA2 receptor. Biochemistry, 2012, 51(10), 2136-2145.
[http://dx.doi.org/10.1021/bi300141h] [PMID: 22332920]
[72]
Grzesiek, S.; Bax, A. Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins. J. Biomol. NMR, 1993, 3(2), 185-204.
[http://dx.doi.org/10.1007/BF00178261] [PMID: 8477186]
[73]
Hiller, S.; Fiorito, F.; Wüthrich, K.; Wider, G. Automated projection spectroscopy (APSY). Proc. Natl. Acad. Sci. USA, 2005, 102(31), 10876-10881.
[http://dx.doi.org/10.1073/pnas.0504818102] [PMID: 16043707]
[74]
Hiller, S.; Wider, G. Automated projection spectroscopy and its applications. Top. Curr. Chem., 2012, 316, 21-47.
[http://dx.doi.org/10.1007/128_2011_189] [PMID: 21710379]
[75]
Murrali, M.G.; Schiavina, M.; Sainati, V.; Bermel, W.; Pierattelli, R.; Felli, I.C. 13C APSY-NMR for sequential assignment of intrinsically disordered proteins. J. Biomol. NMR, 2018, 70(3), 167-175.
[http://dx.doi.org/10.1007/s10858-018-0167-4] [PMID: 29492731]
[76]
Wishart, D.S.; Sykes, B.D.; Richards, F.M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry, 1992, 31(6), 1647-1651.
[http://dx.doi.org/10.1021/bi00121a010] [PMID: 1737021]
[77]
Baxter, N.J.; Williamson, M.P. Temperature dependence of 1H chemical shifts in proteins. J. Biomol. NMR, 1997, 9(4), 359-369.
[http://dx.doi.org/10.1023/A:1018334207887] [PMID: 9255942]
[78]
Trainor, K.; Palumbo, J.A.; MacKenzie, D.W.S.; Meiering, E.M. Temperature dependence of NMR chemical shifts: tracking and statistical analysis. Protein Sci., 2020, 29(1), 306-314.
[http://dx.doi.org/10.1002/pro.3785] [PMID: 31730280]
[79]
Rothemund, S.; Weisshoff, H.; Beyermann, M.; Krause, E.; Bienert, M.; Mügge, C.; Sykes, B.D.; Sönnichsen, F.D. Temperature coefficients of amide proton NMR resonance frequencies in trifluoroethanol: a monitor of intramolecular hydrogen bonds in helical peptides. J. Biomol. NMR, 1996, 8(1), 93-97.
[http://dx.doi.org/10.1007/BF00198143] [PMID: 8810526]
[80]
Rennella, E.; Solyom, Z.; Brutscher, B. Measuring hydrogen exchange in proteins by selective water saturation in (1)H- (15)N SOFAST/BEST-type experiments: advantages and limitations. J. Biomol. NMR, 2014, 60(2-3), 99-107.
[http://dx.doi.org/10.1007/s10858-014-9857-8] [PMID: 25173410]
[81]
Huang, S.; Umemoto, R.; Tamura, Y.; Kofuku, Y.; Uyeda, T.Q.; Nishida, N.; Shimada, I. Utilization of paramagnetic relaxation enhancements for structural analysis of actin-binding proteins in complex with actin. Sci. Rep., 2016, 6, 33690.
[http://dx.doi.org/10.1038/srep33690] [PMID: 27654858]
[82]
Zangger, K.; Respondek, M.; Göbl, C.; Hohlweg, W.; Rasmussen, K.; Grampp, G.; Madl, T. Positioning of micelle-bound peptides by paramagnetic relaxation enhancements. J. Phys. Chem. B, 2009, 113(13), 4400-4406.
[http://dx.doi.org/10.1021/jp808501x] [PMID: 19256533]
[83]
Dames, S.A.; Aregger, R.; Vajpai, N.; Bernado, P.; Blackledge, M.; Grzesiek, S. Residual dipolar couplings in short peptides reveal systematic conformational preferences of individual amino acids. J. Am. Chem. Soc., 2006, 128(41), 13508-13514.
[http://dx.doi.org/10.1021/ja063606h] [PMID: 17031964]
[84]
Yao, S.; Weber, D.K.; Separovic, F.; Keizer, D.W. Measuring translational diffusion coefficients of peptides and proteins by PFG-NMR using band-selective RF pulses. Eur. Biophys. J., 2014, 43(6-7), 331-339.
[http://dx.doi.org/10.1007/s00249-014-0965-x] [PMID: 24824112]
[85]
Hafsa, N.E.; Arndt, D.; Wishart, D.S. CSI 3.0: a web server for identifying secondary and super-secondary structure in proteins using NMR chemical shifts. Nucleic Acids Res., 2015, 43(W1), W370-W377.
[http://dx.doi.org/10.1093/nar/gkv494] [PMID: 25979265]
[86]
Wishart, D.S. Chemical shift index. In: Encyclopedia of Biophysics; Roberts, G.C.K, Ed.; European Biophysical Societies’ Association (EBSA), 2013, pp. 279-280.
[http://dx.doi.org/10.1007/978-3-642-16712-6_317]
[87]
Hafsa, N.E.; Wishart, D.S. CSI 2.0: a significantly improved version of the Chemical Shift Index. J. Biomol. NMR, 2014, 60(2-3), 131-146.
[http://dx.doi.org/10.1007/s10858-014-9863-x] [PMID: 25273503]
[88]
Kabsch, W.; Sander, C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 1983, 22(12), 2577-2637.
[http://dx.doi.org/10.1002/bip.360221211] [PMID: 6667333]
[89]
CSI 2.0. Available at: http://csi.wishartlab.com [Accessed date: 15th March 2020].
[90]
Jones, D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol., 1999, 292(2), 195-202.
[http://dx.doi.org/10.1006/jmbi.1999.3091] [PMID: 10493868]
[91]
Berjanskii, M.V.; Wishart, D.S. Application of the random coil index to studying protein flexibility. J. Biomol. NMR, 2008, 40(1), 31-48.
[http://dx.doi.org/10.1007/s10858-007-9208-0] [PMID: 17985196]
[92]
Wishart, D.S.; Nip, A.M. Protein chemical shift analysis: a practical guide. Biochem. Cell Biol., 1998, 76(2-3), 153-163.
[http://dx.doi.org/10.1139/o98-038] [PMID: 9923684]
[93]
Wang, Y.; Jardetzky, O. Investigation of the neighboring residue effects on protein chemical shifts. J. Am. Chem. Soc., 2002, 124(47), 14075-14084.
[http://dx.doi.org/10.1021/ja026811f] [PMID: 12440906]
[94]
Schwarzinger, S.; Kroon, G.J.; Foss, T.R.; Chung, J.; Wright, P.E.; Dyson, H.J. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc., 2001, 123(13), 2970-2978.
[http://dx.doi.org/10.1021/ja003760i] [PMID: 11457007]
[95]
Shen, Y.; Bax, A. Protein backbone and sidechain torsion angles predicted from NMR chemical shifts using artificial neural networks. J. Biomol. NMR, 2013, 56(3), 227-241.
[http://dx.doi.org/10.1007/s10858-013-9741-y] [PMID: 23728592]
[96]
Berjanskii, M.V.; Wishart, D.S. A simple method to predict protein flexibility using secondary chemical shifts. J. Am. Chem. Soc., 2005, 127(43), 14970-14971.
[http://dx.doi.org/10.1021/ja054842f] [PMID: 16248604]
[97]
Berjanskii, M.V.; Wishart, D.S. A simple method to measure protein side-chain mobility using NMR chemical shifts. J. Am. Chem. Soc., 2013, 135(39), 14536-14539.
[http://dx.doi.org/10.1021/ja407509z] [PMID: 24032347]
[98]
Wishart, D.S.; Sykes, B.D. The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR, 1994, 4(2), 171-180.
[http://dx.doi.org/10.1007/BF00175245] [PMID: 8019132]
[99]
Wishart, D.S.; Sykes, B.D.; Richards, F.M. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol., 1991, 222(2), 311-333.
[http://dx.doi.org/10.1016/0022-2836(91)90214-Q] [PMID: 1960729]
[100]
Kjaergaard, M.; Poulsen, F.M. Sequence correction of random coil chemical shifts: correlation between neighbor correction factors and changes in the Ramachandran distribution. J. Biomol. NMR, 2011, 50(2), 157-165.
[http://dx.doi.org/10.1007/s10858-011-9508-2] [PMID: 21604143]
[101]
Kjaergaard, M.; Brander, S.; Poulsen, F.M. Random coil chemical shift for intrinsically disordered proteins: effects of temperature and pH. J. Biomol. NMR, 2011, 49(2), 139-149.
[http://dx.doi.org/10.1007/s10858-011-9472-x] [PMID: 21234644]
[102]
Maltsev, A.S.; Ying, J.; Bax, A. Deuterium isotope shifts for backbone 1H, 15N and 13C nuclei in intrinsically disordered protein α-synuclein. J. Biomol. NMR, 2012, 54(2), 181-191.
[http://dx.doi.org/10.1007/s10858-012-9666-x] [PMID: 22960996]
[103]
Mercurio, F.A.; Pirone, L.; Di Natale, C.; Marasco, D.; Pedone, E.M.; Leone, M. Sam domain-based stapled peptides: Structural analysis and interaction studies with the Sam domains from the EphA2 receptor and the lipid phosphatase Ship2. Bioorg. Chem., 2018, 80, 602-610.
[http://dx.doi.org/10.1016/j.bioorg.2018.07.013] [PMID: 30036816]
[104]
Mercurio, F.A.; Di Natale, C.; Pirone, L.; Iannitti, R.; Marasco, D.; Pedone, E.M.; Palumbo, R.; Leone, M. The Sam-Sam interaction between Ship2 and the EphA2 receptor: design and analysis of peptide inhibitors. Sci. Rep., 2017, 7(1), 17474.
[http://dx.doi.org/10.1038/s41598-017-17684-5] [PMID: 29234063]
[105]
Random coil chemical shifts for intrinsically disordered proteins. Available at: https://www1.bio.ku.dk/english/research/bms/research/sbinlab/groups/mak/randomcoil/script/ [Accessed date: 15th March 2020].
[106]
Pimenta, J.; Viegas, A.; Sardinha, J.; Martins, I.C.; Cabrita, E.J.; Fontes, C.M.; Prates, J.A.; Pereira, R.M. NMR solution structure and SRP54M predicted interaction of the N-terminal sequence (1-30) of the ovine Doppel protein. Peptides, 2013, 49, 32-40.
[http://dx.doi.org/10.1016/j.peptides.2013.08.013] [PMID: 23973967]
[107]
Feenstra, K.A.; Peter, C.; Scheek, R.M.; van Gunsteren, W.F.; Mark, A.E. A comparison of methods for calculating NMR cross-relaxation rates (NOESY and ROESY intensities) in small peptides. J. Biomol. NMR, 2002, 23(3), 181-194.
[http://dx.doi.org/10.1023/A:1019854626147] [PMID: 12238590]
[108]
Raghothama, S. NMR of peptides. J. Indian Inst. Sci., 2010, 90(1), 145-161.
[109]
Leone, M.; Freeze, H.H.; Chan, C.S.; Pellecchia, M. The nuclear overhauser effect in the lead identification process. Curr. Drug Discov. Technol., 2006, 3(2), 91-100.
[http://dx.doi.org/10.2174/157016306778108884] [PMID: 16925517]
[110]
Wüthrich, K.; Billeter, M.; Braun, W. Polypeptide secondary structure determination by nuclear magnetic resonance observation of short proton-proton distances. J. Mol. Biol., 1984, 180(3), 715-740.
[http://dx.doi.org/10.1016/0022-2836(84)90034-2] [PMID: 6084719]
[111]
Short sequential and medium-range 1H-1H distance in polypeptide secondary structures. Available at: www.bmrb.wisc.edu/referenc/noe-table.shtml [Accessed date: 15th March 2020].
[112]
Wu, C.H.; Das, B.B.; Opella, S.J. (1)H-(13)C Hetero-nuclear dipole-dipole couplings of methyl groups in stationary and magic angle spinning solid-state NMR experiments of peptides and proteins. J. Magn. Reson., 2010, 202(2), 127-134.
[http://dx.doi.org/10.1016/j.jmr.2009.10.007] [PMID: 19896874]
[113]
Pellecchia, M.; Bertini, I.; Cowburn, D.; Dalvit, C.; Giralt, E.; Jahnke, W.; James, T.L.; Homans, S.W.; Kessler, H.; Luchinat, C.; Meyer, B.; Oschkinat, H.; Peng, J.; Schwalbe, H.; Siegal, G. Perspectives on NMR in drug discovery: a technique comes of age. Nat. Rev. Drug Discov., 2008, 7(9), 738-745.
[http://dx.doi.org/10.1038/nrd2606] [PMID: 19172689]
[114]
Sem, D.S.; Pellecchia, M. NMR in the acceleration of drug discovery. Curr. Opin. Drug Discov. Devel., 2001, 4(4), 479-492.
[PMID: 11727313]
[115]
Becattini, B.; Culmsee, C.; Leone, M.; Zhai, D.; Zhang, X.; Crowell, K.J.; Rega, M.F.; Landshamer, S.; Reed, J.C.; Plesnila, N.; Pellecchia, M. Structure-activity relationships by interligand NOE-based design and synthesis of antiapoptotic compounds targeting Bid. Proc. Natl. Acad. Sci. USA, 2006, 103(33), 12602-12606.
[http://dx.doi.org/10.1073/pnas.0603460103] [PMID: 16891420]
[116]
Becattini, B.; Pellecchia, M. SAR by ILOEs: an NMR-based approach to reverse chemical genetics. Chemistry, 2006, 12(10), 2658-2662.
[http://dx.doi.org/10.1002/chem.200500636] [PMID: 16121405]
[117]
Rega, M.F.; Wu, B.; Wei, J.; Zhang, Z.; Cellitti, J.F.; Pellecchia, M. SAR by interligand nuclear overhauser effects (ILOEs) based discovery of acylsulfonamide compounds active against Bcl-x(L) and Mcl-1. J. Med. Chem., 2011, 54(17), 6000-6013.
[http://dx.doi.org/10.1021/jm200826s] [PMID: 21797225]
[118]
Doyle, C.M.; Rumfeldt, J.A.; Broom, H.R.; Sekhar, A.; Kay, L.E.; Meiering, E.M. Concurrent increases and decreases in local stability and conformational heterogeneity in Cu, Zn superoxide dismutase variants revealed by temperature-dependence of amide chemical shifts. Biochemistry, 2016, 55(9), 1346-1361.
[http://dx.doi.org/10.1021/acs.biochem.5b01133] [PMID: 26849066]
[119]
Hong, J.; Jing, Q.; Yao, L. The protein amide 1H(N) chemical shift temperature coefficient reflects thermal expansion of the N-H•••O=C hydrogen bond. J. Biomol. NMR, 2013, 55(1), 71-78.
[http://dx.doi.org/10.1007/s10858-012-9689-3] [PMID: 23202986]
[120]
Veltri, T.; de Oliveira, G.A.P.; Bienkiewicz, E.A.; Palhano, F.L.; Marques, M.A.; Moraes, A.H.; Silva, J.L.; Sorenson, M.M.; Pinto, J.R. Amide hydrogens reveal a temperature-dependent structural transition that enhances site-II Ca2+-binding affinity in a C-domain mutant of cardiac troponin C. Sci. Rep., 2017, 7(1), 691.
[http://dx.doi.org/10.1038/s41598-017-00777-6] [PMID: 28386062]
[121]
Wang, C.K.; Northfield, S.E.; Colless, B.; Chaousis, S.; Hamernig, I.; Lohman, R.J.; Nielsen, D.S.; Schroeder, C.I.; Liras, S.; Price, D.A.; Fairlie, D.P.; Craik, D.J. Rational design and synthesis of an orally bioavailable peptide guided by NMR amide temperature coefficients. Proc. Natl. Acad. Sci. USA, 2014, 111(49), 17504-17509.
[http://dx.doi.org/10.1073/pnas.1417611111] [PMID: 25416591]
[122]
Mahalakshmi, R.; Raghothama, S.; Balaram, P. NMR analysis of aromatic interactions in designed peptide beta-hairpins. J. Am. Chem. Soc., 2006, 128(4), 1125-1138.
[http://dx.doi.org/10.1021/ja054040k] [PMID: 16433528]
[123]
Vijayalakshmi, S.; Rao, R.B.; Karle, I.L.; Balaram, P. Comparison of helix-stabilizing effects of alpha,alpha-dialkyl glycines with linear and cycloalkyl side chains. Biopolymers, 2000, 53(1), 84-98.
[http://dx.doi.org/10.1002/(SICI)1097-0282(200001)53:1<84:AID-BIP8>3.0.CO;2-W] [PMID: 10644953]
[124]
Khandelwal, P.; Seth, S.; Hosur, R.V. CD and NMR investigations on trifluoroethanol-induced step-wise folding of helical segment from scorpion neurotoxin. Eur. J. Biochem., 1999, 264(2), 468-478.
[http://dx.doi.org/10.1046/j.1432-1327.1999.00641.x] [PMID: 10491093]
[125]
Merutka, G.; Dyson, H.J.; Wright, P.E. ‘Random coil’ 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR, 1995, 5(1), 14-24.
[http://dx.doi.org/10.1007/BF00227466] [PMID: 7881270]
[126]
Contreras, M.A.; Haack, T.; Royo, M.; Giralt, E.; Pons, M. Temperature coefficients of peptides dissolved in hexafluoroisopropanol monitor distortions of helices. Lett. Pept. Sci., 1997, 4(1), 29-39.
[http://dx.doi.org/10.1007/BF02443552]
[127]
Alexandrescu, A.T. Amide proton solvent protection in amylin fibrils probed by quenched hydrogen exchange NMR. PLoS One, 2013, 8(2), e56467.
[http://dx.doi.org/10.1371/journal.pone.0056467] [PMID: 23457571]
[128]
Kim, K.S.; Fuchs, J.A.; Woodward, C.K. Hydrogen exchange identifies native-state motional domains important in protein folding. Biochemistry, 1993, 32(37), 9600-9608.
[http://dx.doi.org/10.1021/bi00088a012] [PMID: 7690587]
[129]
Kuwajima, K.; Baldwin, R.L. Exchange behavior of the H-bonded amide protons in the 3 to 13 helix of ribonuclease S. J. Mol. Biol., 1983, 169(1), 299-323.
[http://dx.doi.org/10.1016/S0022-2836(83)80185-5] [PMID: 6312052]
[130]
Kuwajima, K.; Baldwin, R.L. Nature and locations of the most slowly exchanging peptide NH protons in residues 1 to 19 of ribonuclease S. J. Mol. Biol., 1983, 169(1), 281-297.
[http://dx.doi.org/10.1016/S0022-2836(83)80184-3] [PMID: 6312051]
[131]
Landreh, M.; Astorga-Wells, J.; Johansson, J.; Bergman, T.; Jörnvall, H. New developments in protein structure-function analysis by MS and use of hydrogen-deuterium exchange microfluidics. FEBS J., 2011, 278(20), 3815-3821.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08215.x] [PMID: 21668648]
[132]
Whittemore, N.A.; Mishra, R.; Kheterpal, I.; Williams, A.D.; Wetzel, R.; Serpersu, E.H. Hydrogen-deuterium (H/D) exchange mapping of Abeta 1-40 amyloid fibril secondary structure using nuclear magnetic resonance spectroscopy. Biochemistry, 2005, 44(11), 4434-4441.
[http://dx.doi.org/10.1021/bi048292u] [PMID: 15766273]
[133]
Uchida, K.; Markley, J.L.; Kainosho, M. Carbon-13 NMR method for the detection of correlated hydrogen exchange at adjacent backbone peptide amides and its application to hydrogen exchange in five antiparallel beta strands within the hydrophobic core of Streptomyces subtilisin inhibitor (SSI). Biochemistry, 2005, 44(35), 11811-11820.
[http://dx.doi.org/10.1021/bi050467s] [PMID: 16128582]
[134]
Calce, E.; Leone, M.; Monfregola, L.; De Luca, S. Chemical modifications of peptide sequences via S-alkylation reaction. Org. Lett., 2013, 15(20), 5354-5357.
[http://dx.doi.org/10.1021/ol402637d] [PMID: 24090306]
[135]
Leone, M.; Di Lello, P.; Ohlenschläger, O.; Pedone, E.M.; Bartolucci, S.; Rossi, M.; Di Blasio, B.; Pedone, C.; Saviano, M.; Isernia, C.; Fattorusso, R. Solution structure and backbone dynamics of the K18G/R82E Alicyclobacillus acidocaldarius thioredoxin mutant: a molecular analysis of its reduced thermal stability. Biochemistry, 2004, 43(20), 6043-6058.
[http://dx.doi.org/10.1021/bi036261d] [PMID: 15147188]
[136]
Wang, A.C.; Bax, A. Determination of the backbone dihedral angles φ in human ubiquitin from reparametrized empirical karplus equations. J. Am. Chem. Soc., 1996, 118(10), 2483-2494.
[http://dx.doi.org/10.1021/ja9535524]
[137]
Pardi, A.; Billeter, M.; Wüthrich, K. Calibration of the angular dependence of the amide proton-C alpha proton coupling constants, 3JHN alpha, in a globular protein. Use of 3JHN alpha for identification of helical secondary structure. J. Mol. Biol., 1984, 180(3), 741-751.
[http://dx.doi.org/10.1016/0022-2836(84)90035-4] [PMID: 6084720]
[138]
Wang, Y.; Nip, A.M.; Wishart, D.S. A simple method to quantitatively measure polypeptide JHNH alpha coupling constants from TOCSY or NOESY spectra. J. Biomol. NMR, 1997, 10(4), 373-382.
[http://dx.doi.org/10.1023/A:1018315729609] [PMID: 9460242]
[139]
Jeannerat, D.; Bodenhausen, G. Determination of coupling constants by deconvolution of multiplets in NMR. J. Magn. Reson., 1999, 141(1), 133-140.
[http://dx.doi.org/10.1006/jmre.1999.1845] [PMID: 10527750]
[140]
Szyperski, T.; Güntert, P.; Otting, G.; Wüthrich, K. Determination of scalar coupling constants by inverse Fourier transformation of in phase multiplets. J. Magn. Reson., 1992, 99(3), 552-560.
[http://dx.doi.org/10.1016/0022-2364(92)90209-P]
[141]
Gattin, Z.; Zaugg, J.; van Gunsteren, W.F. Structure determination of a flexible cyclic peptide based on NMR and MD simulation 3J-coupling. Chem. Phys. Chem, 2010, 11(4), 830-835.
[http://dx.doi.org/10.1002/cphc.200900501] [PMID: 20162655]
[142]
Berjanskii, M.V.; Neal, S.; Wishart, D.S. PREDITOR: a web server for predicting protein torsion angle restraints. Nucleic Acids Res., 2006, 34(Web Server issue), W63-W69.
[http://dx.doi.org/10.1093/nar/gkl341] [PMID: 16845087]
[143]
Shen, Y.; Bax, A. Protein structural information derived from NMR chemical shift with the neural network program TALOS-N. Methods Mol. Biol., 2015, 1260, 17-32.
[http://dx.doi.org/10.1007/978-1-4939-2239-0_2] [PMID: 25502373]
[144]
Shen, Y.; Delaglio, F.; Cornilescu, G.; Bax, A. TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J. Biomol. NMR, 2009, 44(4), 213-223.
[http://dx.doi.org/10.1007/s10858-009-9333-z] [PMID: 19548092]
[145]
PREDITOR. Dihedral angles from chemical shifts and/or homology. Available at: http://wishart.biology.ualberta.ca/shiftor/cgi-bin/preditor_current.py [Accessed date: 15th March 2020].
[146]
Chen, K.; Tjandra, N. The use of residual dipolar coupling in studying proteins by NMR. Top. Curr. Chem., 2012, 326, 47-67.
[http://dx.doi.org/10.1007/128_2011_215] [PMID: 21952837]
[147]
Prestegard, J.H.; al-Hashimi, H.M.; Tolman, J.R. NMR structures of biomolecules using field oriented media and residual dipolar couplings. Q. Rev. Biophys., 2000, 33(4), 371-424.
[http://dx.doi.org/10.1017/S0033583500003656] [PMID: 11233409]
[148]
Bax, A.; Kontaxis, G.; Tjandra, N. Dipolar couplings in macromolecular structure determination. Methods Enzymol., 2001, 339, 127-174.
[http://dx.doi.org/10.1016/S0076-6879(01)39313-8] [PMID: 11462810]
[149]
Prestegard, J.H.; Mayer, K.L.; Valafar, H.; Benison, G.C. Determination of protein backbone structures from residual dipolar couplings. Methods Enzymol., 2005, 394, 175-209.
[http://dx.doi.org/10.1016/S0076-6879(05)94007-X] [PMID: 15808221]
[150]
Tolman, J.R.; Ruan, K. NMR residual dipolar couplings as probes of biomolecular dynamics. Chem. Rev., 2006, 106(5), 1720-1736.
[http://dx.doi.org/10.1021/cr040429z] [PMID: 16683751]
[151]
Losonczi, J.A.; Prestegard, J.H. Improved dilute bicelle solutions for high-resolution NMR of biological macromolecules. J. Biomol. NMR, 1998, 12(3), 447-451.
[http://dx.doi.org/10.1023/A:1008302110884] [PMID: 9835051]
[152]
Zweckstetter, M. NMR: prediction of molecular alignment from structure using the PALES software. Nat. Protoc., 2008, 3(4), 679-690.
[http://dx.doi.org/10.1038/nprot.2008.36] [PMID: 18388951]
[153]
Valafar, H.; Prestegard, J.H. REDCAT: a residual dipolar coupling analysis tool. J. Magn. Reson., 2004, 167(2), 228-241.
[http://dx.doi.org/10.1016/j.jmr.2003.12.012] [PMID: 15040978]
[154]
Koenig, B.W.; Kontaxis, G.; Mitchell, D.C.; Louis, J.M.; Litman, B.J.; Bax, A. Structure and orientation of a G protein fragment in the receptor bound state from residual dipolar couplings. J. Mol. Biol., 2002, 322(2), 441-461.
[http://dx.doi.org/10.1016/S0022-2836(02)00745-3] [PMID: 12217702]
[155]
Farley, K.A.; Che, Y.; Navarro-Vázquez, A.; Limberakis, C.; Anderson, D.; Yan, J.; Shapiro, M.; Shanmugasundaram, V.; Gil, R.R. Cyclic peptide design guided by residual dipolar couplings, J-couplings, and intramolecular hydrogen bond analysis. J. Org. Chem., 2019, 84(8), 4803-4813.
[http://dx.doi.org/10.1021/acs.joc.8b02811] [PMID: 30605335]
[156]
Morris, K.F.; Johnson, C.S.J. Diffusion-ordered two-dimensional nuclear magnetic resonance spectroscopy. J. Am. Chem. Soc., 1992, 114(8), 3139-3141.
[http://dx.doi.org/10.1021/ja00034a071]
[157]
Neufeld, R.; Stalke, D. Accurate molecular weight determination of small molecules via DOSY-NMR by using external calibration curves with normalized diffusion coefficients. Chem. Sci. (Camb.), 2015, 6(6), 3354-3364.
[http://dx.doi.org/10.1039/C5SC00670H] [PMID: 29142693]
[158]
Price, W.S. Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part 1. Basic theory. Concepts Magn. Reson., 1997, 9(5), 299-366.
[http://dx.doi.org/10.1002/(SICI)1099-0534(1997)9:5<299:AID-CMR2>3.0.CO;2-U]
[159]
Crutchfield, C.A.; Harris, D.J. Molecular mass estimation by PFG NMR spectroscopy. J. Magn. Reson., 2007, 185(1), 179-182.
[http://dx.doi.org/10.1016/j.jmr.2006.12.004] [PMID: 17188920]
[160]
Yao, S.; Howlett, G.J.; Norton, R.S. Peptide self-association in aqueous trifluoroethanol monitored by pulsed field gradient NMR diffusion measurements. J. Biomol. NMR, 2000, 16(2), 109-119.
[http://dx.doi.org/10.1023/A:1008382624724] [PMID: 10723990]
[161]
Wang, C.K.; Northfield, S.E.; Swedberg, J.E.; Harvey, P.J.; Mathiowetz, A.M.; Price, D.A.; Liras, S.; Craik, D.J. Translational diffusion of cyclic peptides measured using pulsed-field gradient NMR. J. Phys. Chem. B, 2014, 118(38), 11129-11136.
[http://dx.doi.org/10.1021/jp506678f] [PMID: 25184622]
[162]
Augé, S.; Schmit, P.O.; Crutchfield, C.A.; Islam, M.T.; Harris, D.J.; Durand, E.; Clemancey, M.; Quoineaud, A.A.; Lancelin, J.M.; Prigent, Y.; Taulelle, F.; Delsuc, M.A. NMR measure of translational diffusion and fractal dimension. Application to molecular mass measurement. J. Phys. Chem. B, 2009, 113(7), 1914-1918.
[http://dx.doi.org/10.1021/jp8094424] [PMID: 19173563]
[163]
Wilkins, D.K.; Grimshaw, S.B.; Receveur, V.; Dobson, C.M.; Jones, J.A.; Smith, L.J. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry, 1999, 38(50), 16424-16431.
[http://dx.doi.org/10.1021/bi991765q] [PMID: 10600103]
[164]
Roman, E.A.; Rosi, P.; González Lebrero, M.C.; Wuilloud, R.; González Flecha, F.L.; Delfino, J.M.; Santos, J. Gain of local structure in an amphipathic peptide does not require a specific tertiary framework. Proteins, 2010, 78(13), 2757-2768.
[http://dx.doi.org/10.1002/prot.22789] [PMID: 20607854]
[165]
Wang, Y.; Truex, N.L.; Vo, N.D.P.; Nowick, J.S. Effects of charge and hydrophobicity on the oligomerization of peptides derived from IAPP. Bioorg. Med. Chem., 2018, 26(6), 1151-1156.
[http://dx.doi.org/10.1016/j.bmc.2017.10.001] [PMID: 29074350]
[166]
Wang, Y.; Kreutzer, A.G.; Truex, N.L.; Nowick, J.S. A tetramer derived from islet amyloid polypeptide. J. Org. Chem., 2017, 82(15), 7905-7912.
[http://dx.doi.org/10.1021/acs.joc.7b01116] [PMID: 28661686]
[167]
Westermark, P.; Wernstedt, C.; O’Brien, T.D.; Hayden, D.W.; Johnson, K.H. Islet amyloid in type 2 human diabetes mellitus and adult diabetic cats contains a novel putative polypeptide hormone. Am. J. Pathol., 1987, 127(3), 414-417.
[PMID: 3296768]
[168]
Clark, T.D.; Bartolotti, L.; Hicks, R.P. The application of DOSY NMR and molecular dynamics simulations to explore the mechanism(s) of micelle binding of antimicrobial peptides containing unnatural amino acids. Biopolymers, 2013, 99(8), 548-561.
[http://dx.doi.org/10.1002/bip.22215] [PMID: 23712491]
[169]
Eichstaedt, K.; Szpotkowski, K.; Grajda, M.; Gilski, M.; Wosicki, S.; Jaskólski, M.; Szumna, A. Self-assembly and ordering of peptide-based cavitands in water and DMSO: the power of hydrophobic effects combined with neutral hydrogen bonds. Chemistry, 2019, 25(12), 3091-3097.
[http://dx.doi.org/10.1002/chem.201805353] [PMID: 30548937]
[170]
Wan, Y.; Baltaze, J.P.; Kouklovsky, C.; Miclet, E.; Alezra, V. Unexpected dimerization of a tripeptide comprising a β,γ-diamino acid. J. Pept. Sci., 2019, 25(2), e3143.
[http://dx.doi.org/10.1002/psc.3143] [PMID: 30575201]
[171]
Mayer, M.; Meyer, B. Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angew. Chem. Int. Ed. Engl., 1999, 38(12), 1784-1788.
[http://dx.doi.org/10.1002/(SICI)1521-3773(19990614)38:12<1784:AID-ANIE1784>3.0.CO;2-Q] [PMID: 29711196]
[172]
Becker, W.; Bhattiprolu, K.C.; Gubensäk, N.; Zangger, K. Investigating protein-ligand interactions by solution nuclear magnetic resonance spectroscopy. ChemPhysChem, 2018, 19(8), 895-906.
[http://dx.doi.org/10.1002/cphc.201701253] [PMID: 29314603]
[173]
Mayer, M.; Meyer, B. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor. J. Am. Chem. Soc., 2001, 123(25), 6108-6117.
[http://dx.doi.org/10.1021/ja0100120] [PMID: 11414845]
[174]
Huang, R.; Bonnichon, A.; Claridge, T.D.; Leung, I.K. Protein-ligand binding affinity determination by the waterLOGSY method: an optimised approach considering ligand rebinding. Sci. Rep., 2017, 7, 43727.
[http://dx.doi.org/10.1038/srep43727] [PMID: 28256624]
[175]
Walpole, S.; Monaco, S.; Nepravishta, R.; Angulo, J. STD NMR as a technique for ligand screening and structural studies. Methods Enzymol., 2019, 615, 423-451.
[http://dx.doi.org/10.1016/bs.mie.2018.08.018] [PMID: 30638536]
[176]
Ji, Z.; Yao, Z.; Liu, M. Saturation transfer difference nuclear magnetic resonance study on the specific binding of ligand to protein. Anal. Biochem., 2009, 385(2), 380-382.
[http://dx.doi.org/10.1016/j.ab.2008.11.022] [PMID: 19070584]
[177]
Angulo, J.; Enríquez-Navas, P.M.; Nieto, P.M. Ligand-receptor binding affinities from saturation transfer difference (STD) NMR spectroscopy: the binding isotherm of STD initial growth rates. Chemistry, 2010, 16(26), 7803-7812.
[http://dx.doi.org/10.1002/chem.200903528] [PMID: 20496354]
[178]
Nieto, P.M. The use of NMR to study transient carbohydrate-protein interactions. Front. Mol. Biosci., 2018, 5, 33.
[http://dx.doi.org/10.3389/fmolb.2018.00033] [PMID: 29696146]
[179]
Bhunia, A.; Bhattacharjya, S. Mapping residue-specific contacts of polymyxin B with lipopolysaccharide by saturation transfer difference NMR: insights into outer-membrane disruption and endotoxin neutralization. Biopolymers, 2011, 96(3), 273-287.
[http://dx.doi.org/10.1002/bip.21530] [PMID: 20683937]
[180]
Monaco, S.; Tailford, L.E.; Juge, N.; Angulo, J. Differential epitope mapping by STD NMR spectroscopy to reveal the nature of protein-ligand contacts. Angew. Chem. Int. Ed. Engl., 2017, 56(48), 15289-15293.
[http://dx.doi.org/10.1002/anie.201707682] [PMID: 28977722]
[181]
Nepravishta, R.; Walpole, S.; Tailford, L.; Juge, N.; Angulo, J. Deriving ligand orientation in weak protein-ligand complexes by DEEP-STD NMR spectroscopy in the absence of protein chemical-shift assignment. Chem. Bio. Chem., 2019, 20(3), 340-344.
[http://dx.doi.org/10.1002/cbic.201800568] [PMID: 30379391]
[182]
Meinecke, R.; Meyer, B. Determination of the binding specificity of an integral membrane protein by saturation transfer difference NMR: RGD peptide ligands binding to integrin alphaIIbbeta3. J. Med. Chem., 2001, 44(19), 3059-3065.
[http://dx.doi.org/10.1021/jm0109154] [PMID: 11543674]
[183]
Molina, M.L.; Barrera, F.N.; Encinar, J.A.; Renart, M.L.; Fernández, A.M.; Poveda, J.A.; Santoro, J.; Bruix, M.; Gavilanes, F.; Fernández-Ballester, G.; Neira, J.L.; González-Ros, J.M. N-type inactivation of the potassium channel KcsA by the Shaker B “ball” peptide: mapping the inactivating peptide-binding epitope. J. Biol. Chem., 2008, 283(26), 18076-18085.
[http://dx.doi.org/10.1074/jbc.M710132200] [PMID: 18430729]
[184]
Hurtado-Gómez, E.; Abián, O.; Muñoz, F.J.; Hernáiz, M.J.; Velázquez-Campoy, A.; Neira, J.L. Defining the epitope region of a peptide from the Streptomyces coelicolor phosphoenolpyruvate: sugar phosphotransferase system able to bind to the enzyme I. Biophys. J., 2008, 95(3), 1336-1348.
[http://dx.doi.org/10.1529/biophysj.107.126664] [PMID: 18456829]
[185]
Sivertsen, A.; Isaksson, J.; Leiros, H.K.; Svenson, J.; Svendsen, J.S.; Brandsdal, B.O. Synthetic cationic antimicrobial peptides bind with their hydrophobic parts to drug site II of human serum albumin. BMC Struct. Biol., 2014, 14, 4.
[http://dx.doi.org/10.1186/1472-6807-14-4] [PMID: 24456893]
[186]
Palmioli, A.; Ceresa, C.; Tripodi, F.; La Ferla, B.; Nicolini, G.; Airoldi, C. On-cell saturation transfer difference NMR study of Bombesin binding to GRP receptor. Bioorg. Chem., 2020, 99, 103861.
[http://dx.doi.org/10.1016/j.bioorg.2020.103861] [PMID: 32339813]
[187]
Sorge, J.L.; Wagstaff, J.L.; Rowe, M.L.; Williamson, R.A.; Howard, M.J. Q2DSTD NMR deciphers epitope-mapping variability for peptide recognition of integrin αvβ6. Org. Biomol. Chem., 2015, 13(29), 8001-8007.
[http://dx.doi.org/10.1039/C5OB01237F] [PMID: 26119198]
[188]
Claasen, B.; Axmann, M.; Meinecke, R.; Meyer, B. Direct observation of ligand binding to membrane proteins in living cells by a saturation transfer double difference (STDD) NMR spectroscopy method shows a significantly higher affinity of integrin alpha(IIb)beta3 in native platelets than in liposomes. J. Am. Chem. Soc., 2005, 127(3), 916-919.
[http://dx.doi.org/10.1021/ja044434w] [PMID: 15656629]
[189]
Megy, S.; Bertho, G.; Gharbi-Benarous, J.; Baleux, F.; Benarous, R.; Girault, J.P. STD and TRNOESY NMR studies for the epitope mapping of the phosphorylation motif of the oncogenic protein beta-catenin recognized by a selective monoclonal antibody. FEBS Lett., 2006, 580(22), 5411-5422.
[http://dx.doi.org/10.1016/j.febslet.2006.08.084] [PMID: 16996060]
[190]
Calvanese, L.; Focà, A.; Sandomenico, A.; Focà, G.; Caporale, A.; Doti, N.; Iaccarino, E.; Leonardi, A.; D’Auria, G.; Ruvo, M.; Falcigno, L. Structural insights into the interaction of a monoclonal antibody and Nodal peptides by STD-NMR spectroscopy. Bioorg. Med. Chem., 2017, 25(24), 6589-6596.
[http://dx.doi.org/10.1016/j.bmc.2017.10.036] [PMID: 29113739]
[191]
Benie, A.J.; Moser, R.; Bäuml, E.; Blaas, D.; Peters, T. Virus-ligand interactions: identification and characterization of ligand binding by NMR spectroscopy. J. Am. Chem. Soc., 2003, 125(1), 14-15.
[http://dx.doi.org/10.1021/ja027691e] [PMID: 12515488]
[192]
Takeuchi, K.; Baskaran, K.; Arthanari, H. Structure determination using solution NMR: is it worth the effort? J. Magn. Reson., 2019, 306, 195-201.
[http://dx.doi.org/10.1016/j.jmr.2019.07.045] [PMID: 31345771]
[193]
Herrmann, T.; Güntert, P.; Wüthrich, K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 2002, 319(1), 209-227.
[http://dx.doi.org/10.1016/S0022-2836(02)00241-3] [PMID: 12051947]
[194]
CYANA wiki. Sequence file. Available at: http://www.cyana.org/wiki/index.php/Sequence_file [Accessed date: 15th March 2020].
[195]
CYANA wiki. Defining non-standard residues. Available at: http://www.cyana.org/wiki/index.php/Defining_non-standard_residues [Accessed date: 15th March 2020].
[196]
Yilmaz, E.M.; Güntert, P. NMR structure calculation for all small molecule ligands and non-standard residues from the PDB chemical component dictionary. J. Biomol. NMR, 2015, 63(1), 21-37.
[http://dx.doi.org/10.1007/s10858-015-9959-y] [PMID: 26123317]
[197]
Bartels, C.; Xia, T.H.; Billeter, M.; Güntert, P.; Wüthrich, K. The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR, 1995, 6(1), 1-10.
[http://dx.doi.org/10.1007/BF00417486] [PMID: 22911575]
[198]
Güntert, P.; Braun, W.; Wüthrich, K. Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol., 1991, 217(3), 517-530.
[http://dx.doi.org/10.1016/0022-2836(91)90754-T] [PMID: 1847217]
[199]
Mumenthaler, C.; Güntert, P.; Braun, W.; Wüthrich, K. Automated combined assignment of NOESY spectra and three-dimensional protein structure determination. J. Biomol. NMR, 1997, 10(4), 351-362.
[http://dx.doi.org/10.1023/A:1018383106236] [PMID: 9460241]
[200]
DYANA version 1.5 User's manual. Available at: https://www.las.jp/english/products/cyana/DyanaManual.-pdf [Accessed date: 15th March 2020].
[201]
Scudiero, O.; Nigro, E.; Cantisani, M.; Colavita, I.; Leone, M.; Mercurio, F.A.; Galdiero, M.; Pessi, A.; Daniele, A.; Salvatore, F.; Galdiero, S. Design and activity of a cyclic mini-β-defensin analog: a novel antimicrobial tool. Int. J. Nanomedicine, 2015, 10, 6523-6539.
[http://dx.doi.org/10.2147/IJN.S89610] [PMID: 26508857]
[202]
Williamson, M.P.; Havel, T.F.; Wüthrich, K. Solution conformation of proteinase inhibitor IIA from bull seminal plasma by 1H nuclear magnetic resonance and distance geometry. J. Mol. Biol., 1985, 182(2), 295-315.
[http://dx.doi.org/10.1016/0022-2836(85)90347-X] [PMID: 3839023]
[203]
Güntert, P.; Billeter, M.; Ohlenschläger, O.; Brown, L.R.; Wüthrich, K. Conformational analysis of protein and nucleic acid fragments with the new grid search algorithm FOUND. J. Biomol. NMR, 1998, 12(4), 543-548.
[http://dx.doi.org/10.1023/A:1008391403193] [PMID: 20012763]
[204]
Würz, J.M.; Kazemi, S.; Schmidt, E.; Bagaria, A.; Güntert, P. NMR-based automated protein structure determination. Arch. Biochem. Biophys., 2017, 628, 24-32.
[http://dx.doi.org/10.1016/j.abb.2017.02.011] [PMID: 28263718]
[205]
Welcome to Cara. Available at: http://www.cara.nmr.ch [Accessed date: 15th March 2020].
[206]
Johnson, B.A.; Blevins, R.A. NMR view: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR, 1994, 4(5), 603-614.
[http://dx.doi.org/10.1007/BF00404272] [PMID: 22911360]
[207]
Helgstrand, M.; Kraulis, P.; Allard, P.; Härd, T. Ansig for Windows: an interactive computer program for semiautomatic assignment of protein NMR spectra. J. Biomol. NMR, 2000, 18(4), 329-336.
[http://dx.doi.org/10.1023/A:1026729404698] [PMID: 11200527]
[208]
Lee, W.; Tonelli, M.; Markley, J.L. NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy. Bioinformatics, 2015, 31(8), 1325-1327.
[http://dx.doi.org/10.1093/bioinformatics/btu830] [PMID: 25505092]
[209]
Vranken, W.F.; Boucher, W.; Stevens, T.J.; Fogh, R.H.; Pajon, A.; Llinas, M.; Ulrich, E.L.; Markley, J.L.; Ionides, J.; Laue, E.D. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins, 2005, 59(4), 687-696.
[http://dx.doi.org/10.1002/prot.20449] [PMID: 15815974]
[210]
Koradi, R.; Billeter, M.; Engeli, M.; Güntert, P.; Wüthrich, K. Automated peak picking and peak integration in macromolecular NMR spectra using AUTOPSY. J. Magn. Reson., 1998, 135(2), 288-297.
[http://dx.doi.org/10.1006/jmre.1998.1570] [PMID: 9878459]
[211]
Garrett, D.S.; Powers, R.; Gronenborn, A.M.; Clore, G.M. A common sense approach to peak picking in two-, three-, and four-dimensional spectra using automatic computer analysis of contour diagrams. 1991. J. Magn. Reson., 2011, 213(2), 357-363.
[http://dx.doi.org/10.1016/j.jmr.2011.09.007] [PMID: 22152355]
[212]
Herrmann, T.; Güntert, P.; Wüthrich, K. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR, 2002, 24(3), 171-189.
[http://dx.doi.org/10.1023/A:1021614115432] [PMID: 12522306]
[213]
Liu, Z.; Abbas, A.; Jing, B.Y.; Gao, X. WaVPeak: picking NMR peaks through wavelet-based smoothing and volume-based filtering. Bioinformatics, 2012, 28(7), 914-920.
[http://dx.doi.org/10.1093/bioinformatics/bts078] [PMID: 22328784]
[214]
Alipanahi, B.; Gao, X.; Karakoc, E.; Donaldson, L.; Li, M. PICKY: a novel SVD-based NMR spectra peak picking method. Bioinformatics, 2009, 25(12), i268-i275.
[http://dx.doi.org/10.1093/bioinformatics/btp225] [PMID: 19477998]
[215]
Schmidt, E.; Güntert, P. A new algorithm for reliable and general NMR resonance assignment. J. Am. Chem. Soc., 2012, 134(30), 12817-12829.
[http://dx.doi.org/10.1021/ja305091n] [PMID: 22794163]
[216]
Bartels, C.; Billeter, M.; Güntert, P.; Wüthrich, K. Automated sequence-specific NMR assignment of homologous proteins using the program GARANT. J. Biomol. NMR, 1996, 7(3), 207-213.
[http://dx.doi.org/10.1007/BF00202037] [PMID: 22911044]
[217]
Zimmerman, D.E.; Kulikowski, C.A.; Huang, Y.; Feng, W.; Tashiro, M.; Shimotakahara, S.; Chien, C.; Powers, R.; Montelione, G.T. Automated analysis of protein NMR assignments using methods from artificial intelligence. J. Mol. Biol., 1997, 269(4), 592-610.
[http://dx.doi.org/10.1006/jmbi.1997.1052] [PMID: 9217263]
[218]
Rieping, W.; Habeck, M.; Bardiaux, B.; Bernard, A.; Malliavin, T.E.; Nilges, M. ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics, 2007, 23(3), 381-382.
[http://dx.doi.org/10.1093/bioinformatics/btl589] [PMID: 17121777]
[219]
Huang, Y.J.; Mao, B.; Xu, F.; Montelione, G.T. Guiding automated NMR structure determination using a global optimization metric, the NMR DP score. J. Biomol. NMR, 2015, 62(4), 439-451.
[http://dx.doi.org/10.1007/s10858-015-9955-2] [PMID: 26081575]
[220]
Gronwald, W.; Moussa, S.; Elsner, R.; Jung, A.; Ganslmeier, B.; Trenner, J.; Kremer, W.; Neidig, K.P.; Kalbitzer, H.R. Automated assignment of NOESY NMR spectra using a knowledge based method (KNOWNOE). J. Biomol. NMR, 2002, 23(4), 271-287.
[http://dx.doi.org/10.1023/A:1020279503261] [PMID: 12398348]
[221]
Zhang, Z.; Porter, J.; Tripsianes, K.; Lange, O.F. Robust and highly accurate automatic NOESY assignment and structure determination with Rosetta. J. Biomol. NMR, 2014, 59(3), 135-145.
[http://dx.doi.org/10.1007/s10858-014-9832-4] [PMID: 24845473]
[222]
Vranken, W.F.; Vuister, G.W.; Bonvin, A.M. NMR-based modeling and refinement of protein 3D structures. Methods Mol. Biol., 2015, 1215, 351-380.
[http://dx.doi.org/10.1007/978-1-4939-1465-4_16] [PMID: 25330971]
[223]
Güntert, P.; Mumenthaler, C.; Wüthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol., 1997, 273(1), 283-298.
[http://dx.doi.org/10.1006/jmbi.1997.1284] [PMID: 9367762]
[224]
Guntert, P. Structure calculation using automated techniques. BioNMR in Drug Research; Zerbe, O., Ed.; WILEY-VCH: Weinheim, 2002, Vol. 16, pp. 39-66.
[http://dx.doi.org/10.1002/3527600663.ch2]
[225]
López-Méndez, B.; Güntert, P. Automated protein structure determination from NMR spectra. J. Am. Chem. Soc., 2006, 128(40), 13112-13122.
[http://dx.doi.org/10.1021/ja061136l] [PMID: 17017791]
[226]
Williamson, M.P. Peptide structure determination by NMR. In: Spectroscopic Methods and Analyses; Jones, C.; Mulloy, B.; Thomas, A.H., Eds.; Humana Press: Totowa, N.J., 1993; Vol. 17, pp. 69-85.
[http://dx.doi.org/10.1385/0-89603-215-9:69]
[227]
Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera--a visualization system for exploratory research and analysis. J. Comput. Chem., 2004, 25(13), 1605-1612.
[http://dx.doi.org/10.1002/jcc.20084] [PMID: 15264254]
[228]
Koradi, R.; Billeter, M.; Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph., 1996, 14(1), 51-55.
[http://dx.doi.org/10.1016/0263-7855(96)00009-4] [PMID: 8744573]
[229]
Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph., 1996, 14(1), 33-38.
[http://dx.doi.org/10.1016/0263-7855(96)00018-5] [PMID: 8744570]
[230]
DeLano, W.L. Pymol: An open-source molecular graphics tool. CCP4 Newsletter On Protein Crystallography, 2002, 40, 82-92. http://legacy.ccp4.ac.uk/newsletters.php
[231]
PyMOL by Schrödinger. Available at: http://www.pymol. org [Accesed date: 15th March 2020].
[232]
Maiorov, V.N.; Crippen, G.M. Significance of root-mean-square deviation in comparing three-dimensional structures of globular proteins. J. Mol. Biol., 1994, 235(2), 625-634.
[http://dx.doi.org/10.1006/jmbi.1994.1017] [PMID: 8289285]
[233]
Kelley, L.A.; Gardner, S.P.; Sutcliffe, M.J. An automated approach for clustering an ensemble of NMR-derived protein structures into conformationally related subfamilies. Protein Eng., 1996, 9(11), 1063-1065.
[http://dx.doi.org/10.1093/protein/9.11.1063] [PMID: 8961360]
[234]
Geng, H.; Chen, F.; Ye, J.; Jiang, F. Applications of molecular dynamics simulation in structure prediction of peptides and proteins. Comput. Struct. Biotechnol. J., 2019, 17, 1162-1170.
[http://dx.doi.org/10.1016/j.csbj.2019.07.010] [PMID: 31462972]
[235]
Shin, H.H.; Yoon, W.S. Non-equilibrium molecular dynamics simulation of nanojet injection with adaptive-spatial decomposition parallel algorithm. J. Nanosci. Nanotechnol., 2008, 8(7), 3661-3673.
[http://dx.doi.org/10.1166/jnn.2008.18332] [PMID: 19051924]
[236]
Luginbühl, P.; Güntert, P.; Billeter, M.; Wüthrich, K. The new program OPAL for molecular dynamics simulations and energy refinements of biological macromolecules. J. Biomol. NMR, 1996, 8(2), 136-146.
[http://dx.doi.org/10.1007/BF00211160] [PMID: 8914272]
[237]
Duan, Y.; Wu, C.; Chowdhury, S.; Lee, M.C.; Xiong, G.; Zhang, W.; Yang, R.; Cieplak, P.; Luo, R.; Lee, T.; Caldwell, J.; Wang, J.; Kollman, P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem., 2003, 24(16), 1999-2012.
[http://dx.doi.org/10.1002/jcc.10349] [PMID: 14531054]
[238]
Cornell, W.D.; Cieplak, P.; Bayly, C.I.; Gould, I.R.; Merz, K.M.J.; Ferguson, D.M.; Spellmeyer, D.C.; Fox, T.; Caldwell, J.W.; Kollman, P.A. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc., 1995, 117(19), 5179-5197.
[http://dx.doi.org/10.1021/ja00124a002]
[239]
Hinsen, K. The molecular modeling toolkit: a new approach to molecular simulations. J. Comput. Chem., 2000, 21(2), 79-85.
[http://dx.doi.org/10.1002/(SICI)1096-987X(20000130)21:2<79:AID-JCC1>3.0.CO;2-B]
[240]
Montelione, G.T.; Nilges, M.; Bax, A.; Güntert, P.; Herrmann, T.; Richardson, J.S.; Schwieters, C.D.; Vranken, W.F.; Vuister, G.W.; Wishart, D.S.; Berman, H.M.; Kleywegt, G.J.; Markley, J.L. Recommendations of the wwPDB NMR validation task force. Structure, 2013, 21(9), 1563-1570.
[http://dx.doi.org/10.1016/j.str.2013.07.021] [PMID: 24010715]
[241]
Billeter, M. A consensus on protein structure accuracy in NMR? Structure, 2015, 23(2), 255-256.
[http://dx.doi.org/10.1016/j.str.2015.01.007] [PMID: 25651058]
[242]
Brand, G.D.; Ramada, M.H.S.; Manickchand, J.R.; Correa, R.; Ribeiro, D.J.S.; Santos, M.A.; Vasconcelos, A.G.; Abrão, F.Y.; Prates, M.V.; Murad, A.M.; Cardozo Fh, J.L.; Leite, J.R.S.A.; Magalhães, K.G.; Oliveira, A.L.; Bloch, C., Jr Intragenic antimicrobial peptides (IAPs) from human proteins with potent antimicrobial and anti-inflammatory activity. PLoS One, 2019, 14(8), e0220656.
[http://dx.doi.org/10.1371/journal.pone.0220656] [PMID: 31386688]
[243]
Laskowski, R.A.; Rullmannn, J.A.; MacArthur, M.W.; Kaptein, R.; Thornton, J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 1996, 8(4), 477-486.
[http://dx.doi.org/10.1007/BF00228148] [PMID: 9008363]
[244]
Moseley, H.N.; Sahota, G.; Montelione, G.T. Assignment validation software suite for the evaluation and presentation of protein resonance assignment data. J. Biomol. NMR, 2004, 28(4), 341-355.
[http://dx.doi.org/10.1023/B:JNMR.0000015420.44364.06] [PMID: 14872126]
[245]
Wang, L.; Markley, J.L. Empirical correlation between protein backbone 15N and 13C secondary chemical shifts and its application to nitrogen chemical shift re-referencing. J. Biomol. NMR, 2009, 44(2), 95-99.
[http://dx.doi.org/10.1007/s10858-009-9324-0] [PMID: 19436955]
[246]
Shen, Y.; Bax, A. SPARTA+: a modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network. J. Biomol. NMR, 2010, 48(1), 13-22.
[http://dx.doi.org/10.1007/s10858-010-9433-9] [PMID: 20628786]
[247]
Wang, B.; Wang, Y.; Wishart, D.S. A probabilistic approach for validating protein NMR chemical shift assignments. J. Biomol. NMR, 2010, 47(2), 85-99.
[http://dx.doi.org/10.1007/s10858-010-9407-y] [PMID: 20446018]
[248]
Han, B.; Liu, Y.; Ginzinger, S.W.; Wishart, D.S. SHIFTX2: significantly improved protein chemical shift prediction. J. Biomol. NMR, 2011, 50(1), 43-57.
[http://dx.doi.org/10.1007/s10858-011-9478-4] [PMID: 21448735]
[249]
Rieping, W.; Vranken, W.F. Validation of archived chemical shifts through atomic coordinates. Proteins, 2010, 78(11), 2482-2489.
[http://dx.doi.org/10.1002/prot.22756] [PMID: 20602353]
[250]
Heller, D.M.; Giorgetti, A. NMR constraints analyser: a web-server for the graphical analysis of NMR experimental constraints. Nucleic Acids Res, 2010, 38(Web Server issue), W628-632.
[http://dx.doi.org/10.1093/nar/gkq48] [PMID: 20513646]
[251]
Bhattacharya, A.; Tejero, R.; Montelione, G.T. Evaluating protein structures determined by structural genomics consortia. Proteins, 2007, 66(4), 778-795.
[http://dx.doi.org/10.1002/prot.21165] [PMID: 17186527]
[252]
Doreleijers, J.F.; Sousa da Silva, A.W.; Krieger, E.; Nabuurs, S.B.; Spronk, C.A.; Stevens, T.J.; Vranken, W.F.; Vriend, G.; Vuister, G.W. CING: an integrated residue-based structure validation program suite. J. Biomol. NMR, 2012, 54(3), 267-283.
[http://dx.doi.org/10.1007/s10858-012-9669-7] [PMID: 22986687]
[253]
Doreleijers, J.F.; Vranken, W.F.; Schulte, C.; Markley, J.L.; Ulrich, E.L.; Vriend, G.; Vuister, G.W. NRG-CING: integrated validation reports of remediated experimental biomolecular NMR data and coordinates in wwPDB. Nucleic Acids Res., 2012, 40(Database issue), D519-D524.
[http://dx.doi.org/10.1093/nar/gkr1134] [PMID: 22139937]
[254]
Tejero, R.; Snyder, D.; Mao, B.; Aramini, J.M.; Montelione, G.T. PDBStat: a universal restraint converter and restraint analysis software package for protein NMR. J. Biomol. NMR, 2013, 56(4), 337-351.
[http://dx.doi.org/10.1007/s10858-013-9753-7] [PMID: 23897031]
[255]
Vriend, G. WHAT IF: a molecular modeling and drug design program. J. Mol. Graph., 1990, 8(1), 52-56.
[http://dx.doi.org/10.1016/0263-7855(90)80070-V] [PMID: 2268628]
[256]
Chen, V.B.; Arendall, W.B. III; Headd, J.J.; Keedy, D.A.; Immormino, R.M.; Kapral, G.J.; Murray, L.W.; Richardson, J.S.; Richardson, D.C. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr., 2010, 66(Pt 1), 12-21.
[http://dx.doi.org/10.1107/S0907444909042073] [PMID: 20057044]
[257]
Bagaria, A.; Jaravine, V.; Huang, Y.J.; Montelione, G.T.; Güntert, P. Protein structure validation by generalized linear model root-mean-square deviation prediction. Protein Sci., 2012, 21(2), 229-238.
[http://dx.doi.org/10.1002/pro.2007] [PMID: 22113924]
[258]
Benkert, P.; Kunzli, M.; Schwede, T. QMEAN server for protein model quality estimation. Nucleic Acids Res., 2009, 37(Web Server issue), W510-514.
[http://dx.doi.org/10.1093/nar/gkp322] [PMID: 19429685]
[259]
Hendrickx, P.M.; Gutmanas, A.; Kleywegt, G.J. Vivaldi: visualization and validation of biomacromolecular NMR structures from the PDB. Proteins, 2013, 81(4), 583-591.
[http://dx.doi.org/10.1002/prot.24213] [PMID: 23180575]
[260]
Pugalenthi, G.; Shameer, K.; Srinivasan, N.; Sowdhamini, R. Harmony: a server for the assessment of protein structures. Nucleic Acids Res, 2006, 34(Web Server issue), W231-W234.
[http://dx.doi.org/10.1093/nar/gkl314] [PMID: 16844999]
[261]
Pervushin, K. The use of TROSY for detection and suppression of conformational exchange NMR line broadening in biological macromolecules. J. Biomol. NMR, 2001, 20(3), 275-285.
[http://dx.doi.org/10.1023/A:1011208109853] [PMID: 11519750]
[262]
Brutscher, B.; Felli, I.C.; Gil-Caballero, S.; Hošek, T.; Kümmerle, R.; Piai, A.; Pierattelli, R.; Sólyom, Z. NMR methods for the study of instrinsically disordered proteins structure, dynamics, and interactions: general overview and practical guidelines. Adv. Exp. Med. Biol., 2015, 870, 49-122.
[http://dx.doi.org/10.1007/978-3-319-20164-1_3] [PMID: 26387100]
[263]
Lee, J.H.; Okuno, Y.; Cavagnero, S. Sensitivity enhancement in solution NMR: emerging ideas and new frontiers. J. Magn. Reson., 2014, 241, 18-31.
[http://dx.doi.org/10.1016/j.jmr.2014.01.005] [PMID: 24656077]
[264]
Tzeng, S.R.; Pai, M.T.; Kalodimos, C.G. NMR studies of large protein systems. Meth. Mol. Biol., 2012, 831, 133-140.
[http://dx.doi.org/10.1007/978-1-61779-480-3_8] [PMID: 22167672]
[265]
OneDep System. Available at: https://validate-rcsb-1.wwpdb.org/ (Accessed date: 15th March 2020).
[266]
SAVES v6.0. https://saves.mbi.ucla.edu/ (Accessed date: 15th March 2020).
[267]
JCSG. https://smb.slac.stanford.edu/jcsg/QC/ (Accessed date: 15th March 2020).