Generic placeholder image

Current Topics in Medicinal Chemistry

Author(s): Guo-Ping Zhou*, Si-Ming Liao, Dong Chen and Ri-Bo Huang*

DOI: 10.2174/1568026619666191121145924

DownloadDownload PDF Flyer Cite As
The Cooperative Effect between Polybasic Region (PBR) and Polysialyltransferase Domain (PSTD) within Tumor-Target Polysialyltranseferase ST8Sia II

Page: [2831 - 2841] Pages: 11

  • * (Excluding Mailing and Handling)

Abstract

ST8Sia II (STX) is a highly homologous mammalian polysialyltransferase (polyST), which is a validated tumor-target in the treatment of cancer metastasis reliant on tumor cell polysialylation. PolyST catalyzes the synthesis of α2,8-polysialic acid (polySia) glycans by carrying out the activated CMP-Neu5Ac (Sia) to N- and O-linked oligosaccharide chains on acceptor glycoproteins. In this review article, we summarized the recent studies about intrinsic correlation of two polybasic domains, Polysialyltransferase domain (PSTD) and Polybasic region (PBR) within ST8Sia II molecule, and suggested that the critical amino acid residues within the PSTD and PBR motifs of ST8Sia II for polysialylation of Neural cell adhesion molecules (NCAM) are related to ST8Sia II activity. In addition, the conformational changes of the PSTD domain due to point mutations in the PBR or PSTD domain verified an intramolecular interaction between the PBR and the PSTD. These findings have been incorporated into Zhou’s NCAM polysialylation/cell migration model, which will provide new perspectives on drug research and development related to the tumor-target ST8Sia II.

Keywords: Tumor metastasis, Polysialic acid (polySia), Polysialyltransferase domain (PSTD), Polybasic region (PBR), ST8Sia II (STX), ST8Sia IV (PST), Neural cell adhesion molecules (NCAM), Polysialylation, Protein 3D structure, Phyre2 sever.

Graphical Abstract

[1]
Fukuda, M. Molecular and Cellular Glycobiology; Fukuda, M; Hindsgaul, O., Ed.; Oxford University Press: Oxford, United Kingdom, 2000, pp. 1-61.
[2]
Angata, K.; Fukuda, M. Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie, 2003, 85(1-2), 195-206.
[http://dx.doi.org/10.1016/S0300-9084(03)00051-8] [PMID: 12765789]
[3]
Schachner, M.; Martini, R. Glycans and the modulation of neural-recognition molecule function. Trends Neurosci., 1995, 18(4), 183-191.
[http://dx.doi.org/10.1016/0166-2236(95)93899-9] [PMID: 7539963]
[4]
Park, K.H.; Yeo, S.W.; Troy, F.A., II Expression of polysialylated neural cell adhesion molecules on adult stem cells after neuronal differentiation of inner ear spiral ganglion neurons. Biochem. Biophys. Res. Commun., 2014, 453(2), 282-287.
[http://dx.doi.org/10.1016/j.bbrc.2014.05.035] [PMID: 24845385]
[5]
Inoue, S.; Iwasaki, M. Isolation of a novel glycoprotein from the eggs of rainbow trout: occurrence of disialosyl groups on all carbohydrate chains. Biochem. Biophys. Res. Commun., 1978, 83(3), 1018-1023.
[http://dx.doi.org/10.1016/0006-291X(78)91497-3] [PMID: 708420]
[6]
Eckhardt, M.; Mühlenhoff, M.; Bethe, A.; Koopman, J.; Frosch, M.; Gerardy-Schahn, R. Molecular characterization of eukaryotic polysialyltransferase-1. Nature, 1995, 373(6516), 715-718.
[http://dx.doi.org/10.1038/373715a0] [PMID: 7854457]
[7]
Nakayama, J.; Fukuda, M.N.; Fredette, B.; Ranscht, B.; Fukuda, M. Expression cloning of a human polysialyltransferase that forms the polysialylated neural cell adhesion molecule present in embryonic brain. Proc. Natl. Acad. Sci. USA, 1995, 92(15), 7031-7035.
[http://dx.doi.org/10.1073/pnas.92.15.7031] [PMID: 7624364]
[8]
Mendiratta, S.S.; Sekulic, N.; Hernandez-Guzman, F.G.; Close, B.E.; Lavie, A.; Colley, K.J. A novel alpha-helix in the first fibronectin type III repeat of the neural cell adhesion molecule is critical for N-glycan polysialylation. J. Biol. Chem., 2006, 281(47), 36052-36059.
[http://dx.doi.org/10.1074/jbc.M608073200] [PMID: 17003032]
[9]
Thompson, M.G.; Foley, D.A.; Swartzentruber, K.G.; Colley, K.J. Sequences at the interface of the fifth immunoglobulin domain and first fibronectin type III repeat of the neural cell adhesion molecule are critical for its polysialylation. J. Biol. Chem., 2011, 286(6), 4525-4534.
[http://dx.doi.org/10.1074/jbc.M110.200386] [PMID: 21131353]
[10]
Thompson, M.G.; Foley, D.A.; Colley, K.J. The polysialyltransferases interact with sequences in two domains of the neural cell adhesion molecule to allow its polysialylation. J. Biol. Chem., 2013, 288(10), 7282-7293.
[http://dx.doi.org/10.1074/jbc.M112.438374] [PMID: 23341449]
[11]
Finne, J. Occurrence of unique polysialosyl carbohydrate units in glycoproteins of developing brain. J. Biol. Chem., 1982, 257(20), 11966-11970.
[PMID: 7118922]
[12]
Edelman, G.M. Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu. Rev. Neurosci., 1984, 7, 339-377.
[http://dx.doi.org/10.1146/annurev.ne.07.030184.002011] [PMID: 6201120]
[13]
Rutishauser, U.; Landmesser, L. Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci., 1996, 19(10), 422-427.
[http://dx.doi.org/10.1016/S0166-2236(96)10041-2] [PMID: 8888519]
[14]
Kiss, J.Z.; Rougon, G. Cell biology of polysialic acid. Curr. Opin. Neurobiol., 1997, 7(5), 640-646.
[http://dx.doi.org/10.1016/S0959-4388(97)80083-9] [PMID: 9384537]
[15]
Seki, T.; Arai, Y. Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci. Res., 1993, 17(4), 265-290.
[http://dx.doi.org/10.1016/0168-0102(93)90111-3] [PMID: 8264989]
[16]
Hu, H.; Tomasiewicz, H.; Magnuson, T.; Rutishauser, U. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron, 1996, 16(4), 735-743.
[http://dx.doi.org/10.1016/S0896-6273(00)80094-X] [PMID: 8607992]
[17]
Gómez-Climent, M.A.; Castillo-Gómez, E.; Varea, E.; Guirado, R.; Blasco-Ibáñez, J.M.; Crespo, C.; Martínez-Guijarro, F.J.; Nácher, J. A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb. Cortex, 2008, 18(10), 2229-2240.
[http://dx.doi.org/10.1093/cercor/bhm255] [PMID: 18245040]
[18]
Gómez-Climent, M.A.; Guirado, R.; Castillo-Gómez, E.; Varea, E.; Gutierrez-Mecinas, M.; Gilabert-Juan, J.; García-Mompó, C.; Vidueira, S.; Sanchez-Mataredona, D.; Hernández, S.; Blasco-Ibáñez, J.M.; Crespo, C.; Rutishauser, U.; Schachner, M.; Nacher, J. The polysialylated form of the neural cell adhesion molecule (PSA-NCAM) is expressed in a subpopulation of mature cortical interneurons characterized by reduced structural features and connectivity. Cereb. Cortex, 2011, 21(5), 1028-1041.
[http://dx.doi.org/10.1093/cercor/bhq177] [PMID: 20843898]
[19]
Gomez-Climent, M.A.; Guirado, R.; Varea, E.; Nàcher, J. Arrested development. Immature, but not recently generated, neurons in the adult brain. Arch. Ital. Biol., 2010, 148(2), 159-172.
[PMID: 20830977]
[20]
Close, B.E.; Colley, K.J. In vivo autopolysialylation and localization of the polysialyltransferases PST and STX. J. Biol. Chem., 1998, 273(51), 34586-34593.
[http://dx.doi.org/10.1074/jbc.273.51.34586] [PMID: 9852130]
[21]
Seki, T.; Rutishauser, U. Removal of polysialic acid-neural cell adhesion molecule induces aberrant mossy fiber innervation and ectopic synaptogenesis in the hippocampus. J. Neurosci., 1998, 18(10), 3757-3766.
[http://dx.doi.org/10.1523/JNEUROSCI.18-10-03757.1998] [PMID: 9570806]
[22]
Namba, T.; Mochizuki, H.; Suzuki, R.; Onodera, M.; Yamaguchi, M.; Namiki, H.; Shioda, S.; Seki, T. Time-lapse imaging reveals symmetric neurogenic cell division of GFAP-expressing progenitors for expansion of postnatal dentate granule neurons. PLoS One, 2011, 6(9)e25303
[http://dx.doi.org/10.1371/journal.pone.0025303] [PMID: 21966492]
[23]
Seki, T. From embryonic to adult neurogenesis in the dentate gyrus.In:Neurogenesis in the adult brain I, Neurobiology; Seki, T.; Sawamoto, K.; Parent, J.; Alvarez-Buylla, A., Eds.; SpringerL Berlin, 2011, pp. 193-216.
[http://dx.doi.org/10.1007/978-4-431-53933-9_7]
[24]
Liu, Y.; Namba, T.; Liu, J.; Suzuki, R.; Shioda, S.; Seki, T. GFAP-expressing neural progenitors give rise to immature neurons via early intermediate progenitors expressing both GFAP and neuronal markers in the adult hippocampus. Neuroscience, 2010, 166, 241-251.
[http://dx.doi.org/10.1016/j.neuroscience.2009.12.026] [PMID: 20026190]
[25]
Burgess, A.; Wainwright, S.R.; Shihabuddin, L.S.; Rutishauser, U.; Seki, T.; Aubert, I. Polysialic acid regulates the clustering, migration, and neuronal differentiation of progenitor cells in the adult hippocampus. Dev. Neurobiol., 2008, 68(14), 1580-1590.
[http://dx.doi.org/10.1002/dneu.20681] [PMID: 18844212]
[26]
Nakata, D.; Troy, F.A., II Degree of polymerization (DP) of polysialic acid (polySia) on neural cell adhesion molecules (N-CAMS): development and application of a new strategy to accurately determine the DP of polySia chains on N-CAMS. J. Biol. Chem., 2005, 280(46), 38305-38316.
[http://dx.doi.org/10.1074/jbc.M508762200] [PMID: 16172115]
[27]
McCoy, R.D.; Vimr, E.R.; Troy, F.A., II CMP-NeuNAc:poly-α-2,8-sialosyl sialyltransferase and the biosynthesis of polysialosyl units in neural cell adhesion molecules. J. Biol. Chem., 1985, 260(23), 12695-12699.
[PMID: 4044605]
[28]
Kitazume, S.; Kitajima, K.; Inoue, S.; Inoue, Y.; Troy, F.A., II Developmental expression of trout egg polysialoglycoproteins and the prerequisite α 2,6-, and α 2,8-sialyl and α 2,8-polysialyltransferase activities required for their synthesis during oogenesis. J. Biol. Chem., 1994, 269(14), 10330-10340.
[PMID: 8144614]
[29]
Kojima, N.; Tachida, Y.; Yoshida, Y.; Tsuji, S. Characterization of mouse ST8Sia II (STX) as a neural cell adhesion molecule-specific polysialic acid synthase. Requirement of core alpha1,6-linked fucose and a polypeptide chain for polysialylation. J. Biol. Chem., 1996, 271(32), 19457-19463.
[http://dx.doi.org/10.1074/jbc.271.32.19457] [PMID: 8702635]
[30]
Close, B.E.; Mendiratta, S.S.; Geiger, K.M.; Broom, L.J.; Ho, L.L.; Colley, K.J. The minimal structural domains required for neural cell adhesion molecule polysialylation by PST/ST8Sia IV and STX/ST8Sia II. J. Biol. Chem., 2003, 278(33), 30796-30805.
[http://dx.doi.org/10.1074/jbc.M305390200] [PMID: 12791681]
[31]
Kojima, N.; Yoshida, Y.; Tsuji, S. A developmentally regulated member of the sialyltransferase family (ST8Sia II, STX) is a polysialic acid synthase. FEBS Lett., 1995, 373(2), 119-122.
[http://dx.doi.org/10.1016/0014-5793(95)01024-9] [PMID: 7589448]
[32]
Scheidegger, E.P.; Sternberg, L.R.; Roth, J.; Lowe, J.B. A human STX cDNA confers polysialic acid expression in mammalian cells. J. Biol. Chem., 1995, 270(39), 22685-22688.
[http://dx.doi.org/10.1074/jbc.270.39.22685] [PMID: 7559389]
[33]
Foley, D.A.; Swartzentruber, K.G.; Colley, K.J. Identification of sequences in the polysialyltransferases ST8Sia II and ST8Sia IV that are required for the protein-specific polysialylation of the neural cell adhesion molecule, NCAM. J. Biol. Chem., 2009, 284(23), 15505-15516.
[http://dx.doi.org/10.1074/jbc.M809696200] [PMID: 19336400]
[34]
Kitazume-Kawaguchi, S.; Kabata, S.; Arita, M. Differential biosynthesis of polysialic or disialic acid Structure by ST8Sia II and ST8Sia IV. J. Biol. Chem., 2001, 276(19), 15696-15703.
[http://dx.doi.org/10.1074/jbc.M010371200] [PMID: 11278664]
[35]
Sevigny, M.B.; Ye, J.; Kitazume-Kawaguchi, S.; Troy, F.A., II Developmental expression and characterization of the alpha2,8-polysialyltransferase activity in embryonic chick brain. Glycobiology, 1998, 8(9), 857-867.
[http://dx.doi.org/10.1093/glycob/8.9.857] [PMID: 9675218]
[36]
Peng, L.X.; Liu, X.H.; Lu, B.; Liao, S.M.; Zhou, F.; Huang, J.M.; Chen, D.; Troy, F.A., II; Zhou, G.P.; Huang, R.B. The inhibition of polysialyltranseferase st8siaiv through heparin binding to polysialyltransferase domain (PSTD). Med. Chem., 2019, 15(5), 486-495.
[http://dx.doi.org/10.2174/1573406415666181218101623] [PMID: 30569872]
[37]
Bhide, G.P.; Prehna, G.; Ramirez, B.E.; Colley, K.J. The polybasic region of the polysialyltransferase ST8Sia-IV binds directly to the neural cell adhesion Molecule, NCAM. Biochemistry, 2017, 56(10), 1504-1517.
[http://dx.doi.org/10.1021/acs.biochem.6b01221] [PMID: 28233978]
[38]
Isomura, R.; Kitajima, K.; Sato, C. Structural and functional impairments of polysialic acid by a mutated polysialyltransferase found in schizophrenia. J. Biol. Chem., 2011, 286(24), 21535-21545.
[http://dx.doi.org/10.1074/jbc.M111.221143] [PMID: 21464126]
[39]
Zhou, G.P.; Troy, F.A. Characterization by NMR and molecular modeling of the binding of polyisoprenols (PI) and polyisoprenyl recognition sequence (PIRS) peptides: three-dimensional structure of the complexes reveals sites of specific interactions. Glycobiology, 2003, 13, 51-71.
[http://dx.doi.org/10.1093/glycob/cwg008] [PMID: 12626407]
[40]
Zhou, G.P.; Troy, F.A. II NMR study of the preferred membrane orientation of polyisoprenols (dolichol) and the impact of their complex with polyisoprenyl recognition sequence peptides on membrane structure. Glycobiology, 2005, 15(4), 347-359.
[http://dx.doi.org/10.1093/glycob/cwi016] [PMID: 15563715]
[41]
Zhou, G.P.; Troy, F.A. II NMR studies on how the binding complex of polyisoprenol recognition sequence peptides and polyisoprenols can modulate membrane structure. Curr. Protein Pept. Sci., 2005, 6(5), 399-411.
[http://dx.doi.org/10.2174/138920305774329377] [PMID: 16248792]
[42]
Nakayama, J.; Fukuda, M.N.; Hirabayashi, Y.; Kanamori, A.; Sasaki, K.; Nishi, T.; Fukuda, M. Expression cloning of a human GT3 synthase. GD3 AND GT3 are synthesized by a single enzyme. J. Biol. Chem., 1996, 271(7), 3684-3691.
[http://dx.doi.org/10.1074/jbc.271.7.3684] [PMID: 8631981]
[43]
Kelley, L.A.; Sternberg, M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc., 2009, 4(3), 363-371.
[http://dx.doi.org/10.1038/nprot.2009.2] [PMID: 19247286]
[44]
Zhou, G.P.; Huang, R.B.; Troy, F.A. II 3D structural conformation and functional domains of polysialyltransferase ST8Sia IV required for polysialylation of neural cell adhesion molecules. Protein Pept. Lett., 2015, 22(2), 137-148.
[http://dx.doi.org/10.2174/0929866521666141019192221] [PMID: 25329332]
[45]
Huang, R.B.; Cheng, D.; Liao, S.M.; Lu, B.; Wang, Q.Y.; Xie, N.Z.; Troy Ii, F.A.; Zhou, G.P. The Intrinsic Relationship Between Structure and Function of the Sialyltransferase ST8Sia Family Members. Curr. Top. Med. Chem., 2017, 17(21), 2359-2369.
[http://dx.doi.org/10.2174/1568026617666170414150730] [PMID: 28413949]
[46]
Fu, Q.; Piai, A.; Chen, W.; Xia, K.; Chou, J.J. Structure determination protocol for transmembrane domain oligomers. Nat. Protoc., 2019, 14(8), 2483-2520.
[http://dx.doi.org/10.1038/s41596-019-0188-9] [PMID: 31270510]
[47]
Kang, J.; Low, W.; Norberg, T.; Meisenhelder, J.; Hansson, K.; Stenflo, J.; Zhou, G.P.; Imperial, J.; Olivera, B.M.; Rigby, A.C.; Craig, A.G. Total chemical synthesis and NMR characterization of the glycopeptide tx5a, a heavily post-translationally modified conotoxin, reveals that the glycan structure is α-D-Gal-(1-->3)-α-D-GalNAc. Eur. J. Biochem., 2004, 271(23-24), 4939-4949.
[http://dx.doi.org/10.1111/j.1432-1033.2004.04464.x] [PMID: 15606782]
[48]
Schnell, J.R.; Zhou, G.P.; Zweckstetter, M.; Rigby, A.C.; Chou, J.J. Rapid and accurate structure determination of coiled-coil domains using NMR dipolar couplings: application to cGMP-dependent protein kinase Ialpha. Protein Sci., 2005, 14(9), 2421-2428.
[http://dx.doi.org/10.1110/ps.051528905] [PMID: 16131665]
[49]
Zhou, G.P.; Surks, H.K.; Schnell, J.R.; Chou, J.J.; Mendelsohn, M.E.; Rigby, A.C. The three-dimensional structure of the cGMP-dependent protein kinase I - α leucine zipper domain and its interaction with the myosin binding subunit. Blood, 2004, 104, 3539-3539.
[http://dx.doi.org/10.1182/blood.V104.11.3539.3539]
[50]
Zhou, G.P.; Huang, R.B. The pH-triggered conversion of the PrP(c) to PrP(sc.). Curr. Top. Med. Chem., 2013, 13(10), 1152-1163.
[http://dx.doi.org/10.2174/15680266113139990003] [PMID: 23647538]
[51]
Zhou, G.P.; Chen, D.; Liao, S.; Huang, R.B. Recent progresses in studying helix-helix interactions in proteins by incorporating the wenxiang diagram into the NMR spectroscopy. Curr. Top. Med. Chem., 2016, 16(6), 581-590.
[http://dx.doi.org/10.2174/1568026615666150819104617] [PMID: 26286215]
[52]
Zhou, G.P. The structural determinations of the leucine zipper coiled-coil domains of the cGMP-dependent protein kinase Iα and its interaction with the myosin binding subunit of the myosin light chains phosphase. Protein Pept. Lett., 2011, 18(10), 966-978.
[http://dx.doi.org/10.2174/0929866511107010966] [PMID: 21592084]
[53]
Zhou, G.P. The disposition of the LZCC protein residues in wenxiang diagram provides new insights into the protein-protein interaction mechanism. J. Theor. Biol., 2011, 284(1), 142-148.
[http://dx.doi.org/10.1016/j.jtbi.2011.06.006] [PMID: 21718705]
[54]
Brunger, A.T. Version 1.2 of the crystallography and NMR system. Nat. Protoc., 2007, 2(11), 2728-2733.
[http://dx.doi.org/10.1038/nprot.2007.406] [PMID: 18007608]
[55]
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]
[56]
Cheung, M.S.; Maguire, M.L.; Stevens, T.J.; Broadhurst, R.W. DANGLE: A Bayesian inferential method for predicting protein backbone dihedral angles and secondary structure. J. Magn. Reson., 2010, 202(2), 223-233.
[http://dx.doi.org/10.1016/j.jmr.2009.11.008] [PMID: 20015671]
[57]
Chen, W.; Cai, Y.; Fu, Q.; Chen, B.; Guo, J.; Chou, J.J. Unidirectional presentation of membrane proteins in nanoparticle-supported liposomes. Angew. Chem. Int. Ed. Engl., 2019, 58(29), 9866-9870.
[http://dx.doi.org/10.1002/anie.201903093] [PMID: 30990942]
[58]
Chen, W.; OuYang, B.; Chou, J.J. Reply to 'Re-evaluating the p7 viroporin structure. Nature, 2018, 562(7727), E19-E20.
[http://dx.doi.org/10.1038/s41586-018-0562-8] [PMID: 30333581]
[59]
Fu, Q.; Shaik, M.M.; Cai, Y.; Ghantous, F.; Piai, A.; Peng, H.; Rits-Volloch, S.; Liu, Z.; Harrison, S.C.; Seaman, M.S.; Chen, B.; Chou, J.J. Structure of the membrane proximal external region of HIV-1 envelope glycoprotein. Proc. Natl. Acad. Sci. USA, 2018, 115(38), E8892-E8899.
[http://dx.doi.org/10.1073/pnas.1807259115] [PMID: 30185554]
[60]
Volkers, G.; Worrall, L.J.; Kwan, D.H.; Yu, C.C.; Baumann, L.; Lameignere, E.; Wasney, G.A.; Scott, N.E.; Wakarchuk, W.; Foster, L.J.; Withers, S.G.; Strynadka, N.C. Structure of human ST8SiaIII sialyltransferase provides insight into cell-surface polysialylation. Nat. Struct. Mol. Biol., 2015, 22(8), 627-635.
[http://dx.doi.org/10.1038/nsmb.3060] [PMID: 26192331]
[61]
Falconer, R.A.; Errington, R.J.; Shnyder, S.D.; Smith, P.J.; Patterson, L.H. Polysialyltransferase: a new target in metastatic cancer. Curr. Cancer Drug Targets, 2012, 12(8), 925-939.
[http://dx.doi.org/10.2174/156800912803251225] [PMID: 22463390]
[62]
Viprey, V.; Springett, B.R.; Al-Saraireh, Y.; Northrop, M.; Sutherland, M.; Saeed, R.; Loadman, P.M.; Patterson, L.H.; Shnyder, S.D.; Falconer, R.A. Polysialyltransferase ST8SiaII: a new target for the treatment of metastatic tumors, Experimental and Molecular Therapeutics. Cancer Res., 2014, 74(19), 1774.
[63]
Elkashef, S.M.; Saeed, R.F.; Morais, G.R.; Guo, X.; Sini, M.; Viprey, V.F.; Sutherland, M.; Loadman, P.M.; Patterson, L.H.; Shnyder, S.D.; Falconer, R.A. Polysialyltransferase ST8SiaII as a target for neuroblastoma dissemination. Cancer Res., 2016, 76(19), 1270.
[64]
Al-Saraireh, Y.M.; Sutherland, M.; Springett, B.R.; Freiberger, F.; Ribeiro Morais, G.; Loadman, P.M.; Errington, R.J.; Smith, P.J.; Fukuda, M.; Gerardy-Schahn, R.; Patterson, L.H.; Shnyder, S.D.; Falconer, R.A. Pharmacological inhibition of polysialyltransferase ST8SiaII modulates tumour cell migration. PLoS One, 2013, 8(8)e73366
[http://dx.doi.org/10.1371/journal.pone.0073366] [PMID: 23951351]
[65]
Chou, K.C.; Jones, D.; Heinrikson, R.L. Prediction of the tertiary structure and substrate binding site of caspase-8. FEBS Lett., 1997, 419(1), 49-54.
[http://dx.doi.org/10.1016/S0014-5793(97)01246-5] [PMID: 9426218]
[66]
Chou, K.C.; Tomasselli, A.G.; Heinrikson, R.L. Prediction of the tertiary structure of a caspase-9/inhibitor complex. FEBS Lett., 2000, 470(3), 249-256.
[http://dx.doi.org/10.1016/S0014-5793(00)01333-8] [PMID: 10745077]
[67]
Chou, K.C.; Howe, W.J. Prediction of the tertiary structure of the beta-secretase zymogen. Biochem. Biophys. Res. Commun., 2002, 292(3), 702-708.
[http://dx.doi.org/10.1006/bbrc.2002.6686] [PMID: 11922623]
[68]
Chou, K.C. Insights from modeling three-dimensional structures of the human potassium and sodium channels. J. Proteome Res., 2004, 3(4), 856-861.
[http://dx.doi.org/10.1021/pr049931q] [PMID: 15359741]
[69]
Chou, K.C. Insights from modelling the 3D structure of the extracellular domain of alpha7 nicotinic acetylcholine receptor. Biochem. Biophys. Res. Commun., 2004, 319(2), 433-438.
[http://dx.doi.org/10.1016/j.bbrc.2004.05.016] [PMID: 15178425]
[70]
Chou, K.C. Coupling interaction between thromboxane A2 receptor and alpha-13 subunit of guanine nucleotide-binding protein. J. Proteome Res., 2005, 4(5), 1681-1686.
[http://dx.doi.org/10.1021/pr050145a] [PMID: 16212421]
[71]
Chou, K.C. Insights from modeling the tertiary structure of human BACE2. J. Proteome Res., 2004, 3(5), 1069-1072.
[http://dx.doi.org/10.1021/pr049905s] [PMID: 15473697]
[72]
Chou, K.C. Modelling extracellular domains of GABA-A receptors: subtypes 1, 2, 3, and 5. Biochem. Biophys. Res. Commun., 2004, 316(3), 636-642.
[http://dx.doi.org/10.1016/j.bbrc.2004.02.098] [PMID: 15033447]
[73]
Chou, K.C. Molecular therapeutic target for type-2 diabetes. J. Proteome Res., 2004, 3(6), 1284-1288.
[http://dx.doi.org/10.1021/pr049849v] [PMID: 15595739]
[74]
Chou, K.C. Modeling the tertiary structure of human cathepsin-E. Biochem. Biophys. Res. Commun., 2005, 331(1), 56-60.
[http://dx.doi.org/10.1016/j.bbrc.2005.03.123] [PMID: 15845357]
[75]
Chou, K.C. Insights from modeling the 3D structure of DNA-CBF3b complex. J. Proteome Res., 2005, 4(5), 1657-1660.
[http://dx.doi.org/10.1021/pr050135+] [PMID: 16212418]
[76]
Wang, S.Q.; Du, Q.S.; Huang, R.B.; Zhang, D.W.; Chou, K.C. Insights from investigating the interaction of oseltamivir (Tamiflu) with neuraminidase of the 2009 H1N1 swine flu virus. Biochem. Biophys. Res. Commun., 2009, 386(3), 432-436.
[http://dx.doi.org/10.1016/j.bbrc.2009.06.016] [PMID: 19523442]
[77]
Wang, J.F.; Chou, K.C. Insights from studying the mutation-induced allostery in the M2 proton channel by molecular dynamics. Protein Eng. Des. Sel., 2010, 23(8), 663-666.
[http://dx.doi.org/10.1093/protein/gzq040] [PMID: 20571121]
[78]
Wang, J.F.; Chou, K.C. Insights from modeling the 3D structure of New Delhi metallo-β-lactamse and its binding interactions with antibiotic drugs. PLoS One, 2011, 6(4)e18414
[http://dx.doi.org/10.1371/journal.pone.0018414] [PMID: 21494599]
[79]
Wang, J.F.; Chou, K.C. Insights into the mutation-induced HHH syndrome from modeling human mitochondrial ornithine transporter-1. PLoS One, 2012, 7(1)e31048
[http://dx.doi.org/10.1371/journal.pone.0031048] [PMID: 22292090]
[80]
Chou, K.C. Structural bioinformatics and its impact to biomedical science. Curr. Med. Chem., 2004, 11(16), 2105-2134.
[http://dx.doi.org/10.2174/0929867043364667] [PMID: 15279552]
[81]
Chou, K.C.; Wei, D.Q.; Zhong, W.Z. Binding mechanism of coronavirus main proteinase with ligands and its implication to drug design against SARS. Biochem. Biophys. Res. Commun., 2003, 308(1), 148-151.
[http://dx.doi.org/10.1016/S0006-291X(03)01342-1] [PMID: 12890493]
[82]
Liao, Q.H.; Gao, Q.Z.; Wei, J.; Chou, K.C. Docking and molecular dynamics study on the inhibitory activity of novel inhibitors on epidermal growth factor receptor (EGFR). Med. Chem., 2011, 7(1), 24-31.
[http://dx.doi.org/10.2174/157340611794072698] [PMID: 21235516]
[83]
Li, X.B.; Wang, S.Q.; Xu, W.R.; Wang, R.L.; Chou, K.C. Novel inhibitor design for hemagglutinin against H1N1 influenza virus by core hopping method. PLoS One, 2011, 6(11)e28111
[http://dx.doi.org/10.1371/journal.pone.0028111] [PMID: 22140516]
[84]
Ma, Y.; Wang, S.Q.; Xu, W.R.; Wang, R.L.; Chou, K.C. Design novel dual agonists for treating type-2 diabetes by targeting peroxisome proliferator-activated receptors with core hopping approach. PLoS One, 2012, 7(6)e38546
[http://dx.doi.org/10.1371/journal.pone.0038546] [PMID: 22685582]
[85]
Fan, Y.N.; Xiao, X.; Min, J.L.; Chou, K.C. iNR-Drug: predicting the interaction of drugs with nuclear receptors in cellular networking. Int. J. Mol. Sci., 2014, 15(3), 4915-4937.
[http://dx.doi.org/10.3390/ijms15034915] [PMID: 24651462]
[86]
Min, J.L.; Xiao, X.; Chou, K.C. iEzy-drug: a web server for identifying the interaction between enzymes and drugs in cellular networking. BioMed Res. Int., 2013, 2013701317
[http://dx.doi.org/10.1155/2013/701317] [PMID: 24371828]
[87]
Xiao, X.; Min, J.L.; Wang, P.; Chou, K.C. iGPCR-drug: a web server for predicting interaction between GPCRs and drugs in cellular networking. PLoS One, 2013, 8(8)e72234
[http://dx.doi.org/10.1371/journal.pone.0072234] [PMID: 24015221]
[88]
Xiao, X.; Min, J.L.; Wang, P.; Chou, K.C. iCDI-PseFpt: identify the channel-drug interaction in cellular networking with PseAAC and molecular fingerprints. J. Theor. Biol., 2013, 337, 71-79.
[http://dx.doi.org/10.1016/j.jtbi.2013.08.013] [PMID: 23988798]
[89]
Xiao, X.; Min, J.L.; Lin, W.Z.; Liu, Z.; Cheng, X.; Chou, K.C. iDrug-Target: predicting the interactions between drug compounds and target proteins in cellular networking via benchmark dataset optimization approach. J. Biomol. Struct. Dyn., 2015, 33(10), 2221-2233.
[http://dx.doi.org/10.1080/07391102.2014.998710] [PMID: 25513722]
[90]
Chou, K.C.; Elrod, D.W. Bioinformatical analysis of G-protein-coupled receptors. J. Proteome Res., 2002, 1(5), 429-433.
[http://dx.doi.org/10.1021/pr025527k] [PMID: 12645914]
[91]
Chou, K.C. Pseudo amino acid composition and its applications in bioinformatics, proteomics and system biology. Curr. Prot., 2009, 6, 262-274.
[http://dx.doi.org/10.2174/157016409789973707]
[92]
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]
[93]
Gizachew, D.; Dratz, E. Transferred NOESY NMR studies of biotin mimetic peptide (FSHPQNT) bound to streptavidin: a structural model for studies of peptide-protein interactions. Chem. Biol. Drug Des., 2011, 78(1), 14-24.
[http://dx.doi.org/10.1111/j.1747-0285.2011.01096.x] [PMID: 21294848]
[94]
Gizachew, D.; Moffett, D.B.; Busse, S.C.; Westler, W.M.; Dratz, E.A.; Teintze, M. NMR studies on the conformation of the CD4 36-59 peptide bound to HIV-1 gp120. Biochemistry, 1998, 37(30), 10616-10625.
[http://dx.doi.org/10.1021/bi980652o] [PMID: 9692951]
[95]
Adams, E.R.; Dratz, E.A.; Gizachew, D.; Deleo, F.R.; Yu, L.; Volpp, B.D.; Vlases, M.; Jesaitis, A.J.; Quinn, M.T. Interaction of human neutrophil flavocytochrome b with cytosolic proteins: transferred-NOESY NMR studies of a gp91phox C-terminal peptide bound to p47phox. Biochem. J., 1997, 325(Pt 1), 249-257.
[http://dx.doi.org/10.1042/bj3250249] [PMID: 9224653]
[96]
Burritt, J.B.; Busse, S.C.; Gizachew, D.; Siemsen, D.W.; Quinn, M.T.; Bond, C.W.; Dratz, E.A.; Jesaitis, A.J. Antibody imprint of a membrane protein surface. Phagocyte flavocytochrome b. J. Biol. Chem., 1998, 273(38), 24847-24852.
[http://dx.doi.org/10.1074/jbc.273.38.24847] [PMID: 9733789]
[97]
Jesaitis, A.J.; Gizachew, D.; Dratz, E.A.; Siemsen, D.W.; Stone, K.C.; Burritt, J.B. Actin surface structure revealed by antibody imprints: evaluation of phage-display analysis of anti-actin antibodies. Protein Sci., 1999, 8(4), 760-770.
[http://dx.doi.org/10.1110/ps.8.4.760] [PMID: 10211822]
[98]
Gizachew, D.; Oswald, R.E. Concerted motion of a protein-peptide complex: backbone dynamics studies of an (15)N-labeled peptide derived from P(21)-activated kinase bound to Cdc42Hs.GMPPCP. Biochemistry, 2001, 40(48), 14368-14375.
[http://dx.doi.org/10.1021/bi010989h] [PMID: 11724548]
[99]
Landowski, T.H.; Dratz, E.A.; Starkey, J.R. Studies of the structure of the metastasis-associated 67 kDa laminin binding protein: fatty acid acylation and evidence supporting dimerization of the 32 kDa gene product to form the mature protein. Biochemistry, 1995, 34(35), 11276-11287.
[http://dx.doi.org/10.1021/bi00035a037] [PMID: 7669786]
[100]
Keren-Aviram, G.; Dachet, F.; Bagla, S.; Balan, K.; Loeb, J.A.; Dratz, E.A. Proteomic analysis of human epileptic neocortex predicts vascular and glial changes in epileptic regions. PLoS One, 2018, 13(4)e0195639
[http://dx.doi.org/10.1371/journal.pone.0195639] [PMID: 29634780]
[101]
Kraft, P.; Mills, J.; Dratz, E. Mass spectrometric analysis of cyanogen bromide fragments of integral membrane proteins at the picomole level: application to rhodopsin. Anal. Biochem., 2001, 292(1), 76-86.
[http://dx.doi.org/10.1006/abio.2001.5072] [PMID: 11319820]
[102]
Piscitelli, C.L.; Angel, T.E.; Bailey, B.W.; Hargrave, P.; Dratz, E.A.; Lawrence, C.M. Equilibrium between metarhodopsin-I and metarhodopsin-II is dependent on the conformation of the third cytoplasmic loop. J. Biol. Chem., 2006, 281(10), 6813-6825.
[http://dx.doi.org/10.1074/jbc.M510175200] [PMID: 16407202]
[103]
Li, A.; Guo, H.; Luo, X.; Sheng, J.; Yang, S.; Yin, Y.; Zhou, J.; Zhou, J. Apomorphine-induced activation of dopamine receptors modulates FGF-2 expression in astrocytic cultures and promotes survival of dopaminergic neurons. FASEB J., 2006, 20(8), 1263-1265.
[http://dx.doi.org/10.1096/fj.05-5510fje] [PMID: 16636101]
[104]
Nandy, S.B.; Mohanty, S.; Singh, M.; Behari, M.; Airan, B. Fibroblast Growth Factor-2 alone as an efficient inducer for differentiation of human bone marrow mesenchymal stem cells into dopaminergic neurons. J. Biomed. Sci., 2014, 21, 83.
[http://dx.doi.org/10.1186/s12929-014-0083-1] [PMID: 25248378]
[105]
Woodbury, M.E.; Ikezu, T. Fibroblast growth factor-2 signaling in neurogenesis and neurodegeneration. J. Neuroimmune Pharmacol., 2014, 9(2), 92-101.
[http://dx.doi.org/10.1007/s11481-013-9501-5] [PMID: 24057103]
[106]
Johnson, C.P.; Fujimoto, I.; Rutishauser, U.; Leckband, D.E. Direct evidence that neural cell adhesion molecule (NCAM) polysialylation increases intermembrane repulsion and abrogates adhesion. J. Biol. Chem., 2005, 280(1), 137-145.
[http://dx.doi.org/10.1074/jbc.M410216200] [PMID: 15504723]
[107]
El Maarouf, A.; Petridis, A.K.; Rutishauser, U. Use of polysialic acid in repair of the central nervous system. Proc. Natl. Acad. Sci. USA, 2006, 103(45), 16989-16994.
[http://dx.doi.org/10.1073/pnas.0608036103] [PMID: 17075041]
[108]
Rutishauser, U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci., 2008, 9(1), 26-35.
[http://dx.doi.org/10.1038/nrn2285] [PMID: 18059411]
[109]
Sato, C.; Kitajima, K. Disialic, oligosialic and polysialic acids: distribution, functions and related disease. J. Biochem., 2013, 154(2), 115-136.
[http://dx.doi.org/10.1093/jb/mvt057] [PMID: 23788662]
[110]
Crocker, P.R.; Paulson, J.C.; Varki, A. Siglecs and their roles in the immune system. Nat. Rev. Immunol., 2007, 7(4), 255-266.
[http://dx.doi.org/10.1038/nri2056] [PMID: 17380156]
[111]
Mühlenhoff, M.; Rollenhagen, M.; Werneburg, S.; Gerardy-Schahn, R.; Hildebrandt, H. Polysialic acid: versatile modification of NCAM, SynCAM 1 and neuropilin-2. Neurochem. Res., 2013, 38(6), 1134-1143.
[http://dx.doi.org/10.1007/s11064-013-0979-2] [PMID: 23354723]
[112]
Acheson, A.; Sunshine, J.L.; Rutishauser, U. NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol., 1991, 114(1), 143-153.
[http://dx.doi.org/10.1083/jcb.114.1.143] [PMID: 2050739]
[113]
Schnaar, R.L.; Gerardy-Schahn, R.; Hildebrandt, H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol. Rev., 2014, 94(2), 461-518.
[http://dx.doi.org/10.1152/physrev.00033.2013] [PMID: 24692354]
[114]
Doherty, P.; Cohen, J.; Walsh, F.S. Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron, 1990, 5(2), 209-219.
[http://dx.doi.org/10.1016/0896-6273(90)90310-C] [PMID: 2200449]
[115]
Weinhold, B.; Seidenfaden, R.; Röckle, I.; Mühlenhoff, M.; Schertzinger, F.; Conzelmann, S.; Marth, J.D.; Gerardy-Schahn, R.; Hildebrandt, H. Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem., 2005, 280(52), 42971-42977.
[http://dx.doi.org/10.1074/jbc.M511097200] [PMID: 16267048]
[116]
Lu, B.; Liu, X.H.; Lia, S.M.; Lu, Z.L.; Chen, D. A Troy Ii, F.; Huang, R.B.; Zhou, G.P. A possible modulation mechanism of intramolecular and intermolecular interactions for NCAM polysialylation and cell Migration. Curr. Top. Med. Chem., 2019, 19(25), 2271-2282.
[http://dx.doi.org/10.2174/1568026619666191018094805] [PMID: 31648641]
[117]
Angata, K.; Suzuki, M.; Fukuda, M. ST8Sia II and ST8Sia IV polysialyltransferases exhibit marked differences in utilizing various acceptors containing oligosialic acid and short polysialic acid. The basis for cooperative polysialylation by two enzymes. J. Biol. Chem., 2002, 277(39), 36808-36817.
[http://dx.doi.org/10.1074/jbc.M204632200] [PMID: 12138100]
[118]
Mahal, L.K.; Charter, N.W.; Angata, K.; Fukuda, M.; Koshland, D.E., Jr; Bertozzi, C.R. A small-molecule modulator of poly-alpha 2,8-sialic acid expression on cultured neurons and tumor cells. Science, 2001, 294(5541), 380-381.
[http://dx.doi.org/10.1126/science.1062192] [PMID: 11598302]
[119]
Scheidegger, E.P.; Lackie, P.M.; Papay, J.; Roth, J. In vitro and in vivo growth of clonal sublines of human small cell lung carcinoma is modulated by polysialic acid of the neural cell adhesion molecule. Lab. Invest., 1994, 70(1), 95-106.
[PMID: 8302024]
[120]
Tanaka, F.; Otake, Y.; Nakagawa, T.; Kawano, Y.; Miyahara, R.; Li, M.; Yanagihara, K.; Nakayama, J.; Fujimoto, I.; Ikenaka, K.; Wada, H. Expression of polysialic acid and STX, a human polysialyltransferase, is correlated with tumor progression in non-small cell lung cancer. Cancer Res., 2000, 60(11), 3072-3080.
[PMID: 10850459]
[121]
Robbins, J.B.; McCracken, G.H.J., Jr; Gotschlich, E.C.; Ørskov, F.; Ørskov, I.; Hanson, L.A. Escherichia coli K1 capsular polysaccharide associated with neonatal meningitis. N. Engl. J. Med., 1974, 290(22), 1216-1220.
[http://dx.doi.org/10.1056/NEJM197405302902202] [PMID: 4133095]
[122]
Angata, K.; Long, J.M.; Bukalo, O.; Lee, W.; Dityatev, A.; Wynshaw-Boris, A.; Schachner, M.; Fukuda, M.; Marth, J.D. Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem., 2004, 279(31), 32603-32613.
[http://dx.doi.org/10.1074/jbc.M403429200] [PMID: 15140899]
[123]
Woodard-Grice, A.V.; McBrayer, A.C.; Wakefield, J.K.; Zhuo, Y.; Bellis, S.L. Proteolytic shedding of ST6Gal-I by BACE1 regulates the glycosylation and function of alpha4beta1 integrins. J. Biol. Chem., 2008, 283(39), 26364-26373.
[http://dx.doi.org/10.1074/jbc.M800836200] [PMID: 18650447]
[124]
Liu, Y.; Pan, D.; Bellis, S.L.; Song, Y. Effect of altered glycosylation on the structure of the I-like domain of beta1 integrin: a molecular dynamics study. Proteins, 2008, 73(4), 989-1000.
[http://dx.doi.org/10.1002/prot.22126] [PMID: 18536010]
[125]
Büll, C.; den Brok, M.H.; Adema, G.J. Sweet escape: sialic acids in tumor immune evasion. Biochim. Biophys. Acta, 2014, 1846(1), 238-246.
[PMID: 25026312]
[126]
Peracaula, R.; Tabarés, G.; López-Ferrer, A.; Brossmer, R.; de Bolós, C.; de Llorens, R. Role of sialyltransferases involved in the biosynthesis of Lewis antigens in human pancreatic tumour cells. Glycoconj. J., 2005, 22(3), 135-144.
[http://dx.doi.org/10.1007/s10719-005-0734-2] [PMID: 16133834]
[127]
Zhao, Y.Y.; Takahashi, M.; Gu, J.G.; Miyoshi, E.; Matsumoto, A.; Kitazume, S.; Taniguchi, N. Functional roles of N-glycans in cell signaling and cell adhesion in cancer. Cancer Sci., 2008, 99(7), 1304-1310.
[http://dx.doi.org/10.1111/j.1349-7006.2008.00839.x] [PMID: 18492092]
[128]
Hakomori, S. Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10231-10233.
[http://dx.doi.org/10.1073/pnas.172380699] [PMID: 12149519]
[129]
Smith, L.J.; Fiebig, K.M.; Schwalbe, H.; Dobson, C.M. The concept of a random coil. Residual structure in peptides and denatured proteins. Fold. Des., 1996, 1(5), R95-R106.
[http://dx.doi.org/10.1016/S1359-0278(96)00046-6] [PMID: 9080177]
[130]
Nakata, D.; Zhang, L.; Troy, F.A., II Molecular basis for polysialylation: a novel polybasic polysialyltransferase domain (PSTD) of 32 amino acids unique to the α 2,8-polysialyltransferases is essential for polysialylation. Glycoconj. J., 2006, 23(5-6), 423-436.
[http://dx.doi.org/10.1007/s10719-006-6356-5] [PMID: 16897183]
[131]
Bhide, G.P.; Zapater, J.L.; Colley, K.J. Autopolysialylation of polysialyltransferases is required for polysialylation and polysialic acid chain elongation on select glycoprotein substrates. J. Biol. Chem., 2018, 293(2), 701-716.
[http://dx.doi.org/10.1074/jbc.RA117.000401] [PMID: 29183999]
[132]
Close, B.E.; Tao, K.; Colley, K.J. Polysialyltransferase-1 autopolysialylation is not requisite for polysialylation of neural cell adhesion molecule. J. Biol. Chem., 2000, 275(6), 4484-4491.
[http://dx.doi.org/10.1074/jbc.275.6.4484] [PMID: 10660622]
[133]
Close, B.E.; Wilkinson, J.M.; Bohrer, T.J.; Goodwin, C.P.; Broom, L.J.; Colley, K.J. The polysialyltransferase ST8Sia II/STX: posttranslational processing and role of autopolysialylation in the polysialylation of neural cell adhesion molecule. Glycobiology, 2001, 11(11), 997-1008.
[http://dx.doi.org/10.1093/glycob/11.11.997] [PMID: 11744634]
[134]
Liu, B.; Wang, S.; Long, R.; Chou, K.C. iRSpot-EL: identify recombination spots with an ensemble learning approach. Bioinformatics, 2017, 33(1), 35-41.
[http://dx.doi.org/10.1093/bioinformatics/btw539] [PMID: 27531102]
[135]
Chou, K.C. Progresses in predicting post-translational modification. Int. J. Pept. Res. Ther., 2019, 1-16.
[http://dx.doi.org/10.1007/s10989-019-09893-5]
[136]
Chou, K.C. Impacts of bioinformatics to medicinal chemistry. Med. Chem., 2015, 11(3), 218-234.
[http://dx.doi.org/10.2174/1573406411666141229162834] [PMID: 25548930]
[137]
Chou, K.C. An unprecedented revolution in medicinal chemistry driven by the progress of biological science. Curr. Top. Med. Chem., 2017, 17(21), 2337-2358.
[http://dx.doi.org/10.2174/1568026617666170414145508] [PMID: 28413951]