Generic placeholder image

Protein & Peptide Letters

Author(s): Md. Asad Khan*, Md. Faiz Akram, Khursheed Alam, Haseeb Ahsan and Moshahid A. Rizvi

DOI: 10.2174/0929866527666200427213722

DownloadDownload PDF Flyer Cite As
Peroxynitrite-Mediated Structural Changes in Histone H2A: Biochemical and Biophysical Analysis

Page: [989 - 998] Pages: 10

  • * (Excluding Mailing and Handling)

Explore Articles
About Journal
For Authors
For Editors
For Reviewers

Abstract

Background: Peroxynitrite, a nitrating and oxidizing agent, is formed by the interaction between nitric oxide and superoxide radicals. H2A histone is a basic nucleoprotein and is one of the major core histones responsible for packaging DNA. It has been shown that they are highly sensitive to oxidizing and nitrating agents.

Objective: Nitration of tyrosine residues in proteins by peroxynitrite is regarded as a marker of nitrosative damage. The dityrosine bond, an oxidative covalent cross-link between two tyrosines in protein, is increasingly identified as a marker of oxidative stress, aging and neurodegerative diseases.

Methods: Peroxinitrite-mediated nitration and dinitration in H2A histone was assessed by various biophysical techniques.

Results: The data presented in this study showed that the dityrosine content was found to be elevated in H2A histone modified with peroxynitrite. The formation of dityrosine showed a decrease in fluorescence intensity, generation of a new peak in FT-IR, increase in hydrodynamic size, and loss of secondary and tertiary structure of H2A resulting in a partially folded structure.

Conclusion: We report that H2A may undergo conformational and structural changes under nitrosative and oxidative stress from the deleterious effects of peroxynitrite.

Keywords: H2A histone, peroxynitrite, dityrosine, fluorescence, protein nitration, nitration.

Graphical Abstract

[1]
Porter-Peden, L.; Kamper, S.G.; Wal, M.V.; Blankespoor, R.; Sinniah, K. Estimating kinetic and thermodynamic parameters from single molecule enzyme-inhibitor interactions. Langmuir, 2008, 24(20), 11556-11561.
[http://dx.doi.org/10.1021/la801477a] [PMID: 18808161]
[2]
Povarova, O.I.; Kuznetsova, I.M.; Turoverov, K.K. Differences in the pathways of proteins unfolding induced by urea and guanidine hydrochloride: Molten globule state and aggregates. PLoS One, 2010, 5(11), e15035.
[http://dx.doi.org/10.1371/journal.pone.0015035] [PMID: 21152408]
[3]
Siddiqui, K.S.; Cavicchioli, R. Improved thermal stability and activity in the cold-adapted lipase B from Candida antarctica following chemical modification with oxidized polysaccharides. Extremophiles, 2005, 9(6), 471-476.
[http://dx.doi.org/10.1007/s00792-005-0464-1] [PMID: 15999221]
[4]
Akhtar, M.S.; Ahmad, A.; Bhakuni, V. Guanidinium chloride- and urea-induced unfolding of the dimeric enzyme glucose oxidase. Biochemistry, 2002, 41(11), 3819-3827.
[http://dx.doi.org/10.1021/bi0116700] [PMID: 11888301]
[5]
Rabbani, G.; Ahmad, E.; Zaidi, N.; Fatima, S.; Khan, R.H. pH-Induced molten globule state of Rhizopus niveus lipase is more resistant against thermal and chemical denaturation than its native state. Cell Biochem. Biophys., 2012, 62(3), 487-499.
[http://dx.doi.org/10.1007/s12013-011-9335-9] [PMID: 22215307]
[6]
Anfinsen, C.B.; Scheraga, H.A. Experimental and theoretical aspects of protein folding. Adv. Protein Chem., 1975, 29, 205-300.
[http://dx.doi.org/10.1016/S0065-3233(08)60413-1] [PMID: 237413]
[7]
Beckman, J.S.; Beckman, T.W.; Chen, J.; Marshall, P.A.; Freeman, B.A. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA, 1990, 87(4), 1620-1624.
[http://dx.doi.org/10.1073/pnas.87.4.1620] [PMID: 2154753]
[8]
Alvarez, B.; Radi, R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids, 2003, 25(3-4), 295-311.
[http://dx.doi.org/10.1007/s00726-003-0018-8] [PMID: 14661092]
[9]
Jacob, C.; Giles, G.I.; Giles, N.M.; Sies, H. Sulfur and selenium: The role of oxidation state in protein structure and function. Angew. Chem. Int. Ed. Engl., 2003, 42(39), 4742-4758.
[http://dx.doi.org/10.1002/anie.200300573] [PMID: 14562341]
[10]
Ohshima, H.; Friesen, M.; Brouet, I.; Bartsch, H. Nitrotyrosine as a new marker for endogenous nitrosation and nitration of proteins. Food Chem. Toxicol., 1990, 28(9), 647-652.
[http://dx.doi.org/10.1016/0278-6915(90)90173-K] [PMID: 2272563]
[11]
Ferrer-Sueta, G.; Campolo, N.; Trujillo, M.; Bartesaghi, S.; Carballal, S.; Romero, N.; Alvarez, B.; Radi, R. Biochemistry of peroxynitrite and protein tyrosine nitration. Chem. Rev., 2018, 118(3), 1338-1408.
[http://dx.doi.org/10.1021/acs.chemrev.7b00568] [PMID: 29400454]
[12]
Bartesaghi, S.; Radi, R. Fundamentals on the biochemistry of peroxynitrite and protein tyrosine nitration. Redox Biol., 2018, 14, 618-625.
[http://dx.doi.org/10.1016/j.redox.2017.09.009] [PMID: 29154193]
[13]
Ahsan, H. 3-Nitrotyrosine: A biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions. Hum. Immunol., 2013, 74(10), 1392-1399.
[http://dx.doi.org/10.1016/j.humimm.2013.06.009] [PMID: 23777924]
[14]
Berlett, B.S.; Levine, R.L.; Stadtman, E.R. Carbon dioxide stimulates peroxynitrite-mediated nitration of tyrosine residues and inhibits oxidation of methionine residues of glutamine synthetase: Both modifications mimic effects of adenylylation. Proc. Natl. Acad. Sci. USA, 1998, 95(6), 2784-2789.
[http://dx.doi.org/10.1073/pnas.95.6.2784] [PMID: 9501167]
[15]
Yilmaz, I.A.; Akçay, T.; Cakatay, U.; Telci, A.; Ataus, S.; Yalçin, V. Relation between bladder cancer and protein oxidation. Int. Urol. Nephrol., 2003, 35(3), 345-350.
[http://dx.doi.org/10.1023/B:UROL.0000022920.93994.ba] [PMID: 15160536]
[16]
Khan, M.A.; Alam, K.; Dixit, K.; Rizvi, M.M.A. Role of peroxynitrite induced structural changes on H2B histone by physicochemical method. Int. J. Biol. Macromol., 2016, 82, 31-38.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.10.085] [PMID: 26536630]
[17]
Khan, M.A.; Dixit, K.; Jabeen, S. Moinuddin; Alam, K. Impact of peroxynitrite modification on structure and immunogenicity of H2A histone. Scand. J. Immunol., 2009, 69(2), 99-109.
[http://dx.doi.org/10.1111/j.1365-3083.2008.02200.x] [PMID: 19144075]
[18]
Luger, K.; Mäder, A.W.; Richmond, R.K.; Sargent, D.F.; Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 1997, 389(6648), 251-260.
[http://dx.doi.org/10.1038/38444] [PMID: 9305837]
[19]
Arents, G.; Burlingame, R.W.; Wang, B.C.; Love, W.E.; Moudrianakis, E.N. The nucleosomal core histone octamer at 3.1 A resolution: A tripartite protein assembly and a left-handed superhelix. Proc. Natl. Acad. Sci. USA, 1991, 88(22), 10148-10152.
[http://dx.doi.org/10.1073/pnas.88.22.10148] [PMID: 1946434]
[20]
Arents, G.; Moudrianakis, E.N. The histone fold: A ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA, 1995, 92(24), 11170-11174.
[http://dx.doi.org/10.1073/pnas.92.24.11170] [PMID: 7479959]
[21]
Munishkina, L.A.; Fink, A.L.; Uversky, V.N. Conformational prerequisites for formation of amyloid fibrils from histones. J. Mol. Biol., 2004, 342(4), 1305-1324.
[http://dx.doi.org/10.1016/j.jmb.2004.06.094] [PMID: 15351653]
[22]
Alvarez, B.; Ferrer-Sueta, G.; Freeman, B.A.; Radi, R. Kinetics of peroxynitrite reaction with amino acids and human serum albumin. J. Biol. Chem., 1999, 274(2), 842-848.
[http://dx.doi.org/10.1074/jbc.274.2.842] [PMID: 9873023]
[23]
Koppenol, W.H.; Kissner, R.; Beckman, J.S. Syntheses of peroxynitrite: To go with the flow or on solid grounds? Methods Enzymol., 1996, 269, 296-302.
[http://dx.doi.org/10.1016/S0076-6879(96)69030-2] [PMID: 8791658]
[24]
Yoshie, Y.; Ohshima, H. Nitric oxide synergistically enhances DNA strand breakage induced by polyhydroxyaromatic compounds, but inhibits that induced by the Fenton reaction. Arch. Biochem. Biophys., 1997, 342(1), 13-21.
[http://dx.doi.org/10.1006/abbi.1997.0100] [PMID: 9185609]
[25]
Ischiropoulos, H.; al-Mehdi, A.B. Peroxynitrite-mediated oxidative protein modifications. FEBS Lett., 1995, 364(3), 279-282.
[http://dx.doi.org/10.1016/0014-5793(95)00307-U] [PMID: 7758583]
[26]
DiMarco, T.; Giulivi, C. Current analytical methods for the detection of dityrosine, a biomarker of oxidative stress, in biological samples. Mass Spectrom. Rev., 2007, 26(1), 108-120.
[http://dx.doi.org/10.1002/mas.20109] [PMID: 17019703]
[27]
Chen, Y.H.; Yang, J.T.; Martinez, H.M. Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion. Biochemistry, 1972, 11(22), 4120-4131.
[http://dx.doi.org/10.1021/bi00772a015] [PMID: 4343790]
[28]
Oberg, K.A.; Fink, A.L. A new attenuated total reflectance Fourier transform infrared spectroscopy method for the study of proteins in solution. Anal. Biochem., 1998, 256(1), 92-106.
[http://dx.doi.org/10.1006/abio.1997.2486] [PMID: 9466802]
[29]
Khan, M.A.; Dixit, K. Moinuddin; Arif, Z.; Alam, K. Studies on peroxynitrite-modified H1 histone: Implications in systemic lupus erythematosus. Biochimie, 2014, 97, 104-113.
[http://dx.doi.org/10.1016/j.biochi.2013.09.026] [PMID: 24113317]
[30]
Neurath, H. In: Protein Folding; R. Jaenicke (Ed.), Elsevier/North-Holland Biomedical Press: Amsterdam/New York, 1980, pp. 501-504.
[31]
Dixit, K.; Khan, M.A.; Sharma, Y.D. Moinuddin; Alam, K. Physicochemical studies on peroxynitrite-modified H3 histone. Int. J. Biol. Macromol., 2010, 46(1), 20-26.
[http://dx.doi.org/10.1016/j.ijbiomac.2009.10.009] [PMID: 19878690]
[32]
Eftink, M.R. The use of fluorescence methods to monitor unfolding transitions in proteins. Biophys. J., 1994, 66(2 Pt 1), 482-501.
[http://dx.doi.org/10.1016/S0006-3495(94)80799-4] [PMID: 8161701]
[33]
Zhao, X.; He, G.; Chen, Y.R.; Pandian, R.P.; Kuppusamy, P.; Zweier, J.L. Endothelium-derived nitric oxide regulates postischemic myocardial oxygenation and oxygen consumption by modulation of mitochondrial electron transport. Circulation, 2005, 111(22), 2966-2972.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.104.527226] [PMID: 15939832]
[34]
Han, Z.; Chen, Y.R.; Jones, C.I., III; Meenakshisundaram, G.; Zweier, J.L.; Alevriadou, B.R. Shear-induced reactive nitrogen species inhibit mitochondrial respiratory complex activities in cultured vascular endothelial cells. Am. J. Physiol. Cell Physiol., 2007, 292(3), C1103-C1112.
[http://dx.doi.org/10.1152/ajpcell.00389.2006] [PMID: 17020931]
[35]
Goldstein, S.; Czapski, G.; Lind, J.; Merényi, G. Tyrosine nitration by simultaneous generation of (.)NO and O-(2) under physiological conditions. How the radicals do the job. J. Biol. Chem., 2000, 275(5), 3031-3036.
[http://dx.doi.org/10.1074/jbc.275.5.3031] [PMID: 10652282]
[36]
Zeng, L.; Mathew, A.V.; Byun, J.; Atkins, K.B.; Brosius, F.C., III; Pennathur, S. Myeloperoxidase-derived oxidants damage artery wall proteins in an animal model of chronic kidney disease-accelerated atherosclerosis. J. Biol. Chem., 2018, 293(19), 7238-7249.
[http://dx.doi.org/10.1074/jbc.RA117.000559] [PMID: 29581235]
[37]
Deeg, K.J.; Katsikas, L.; Schnabel, W. High energy radiation effects in single histones. I. Preparation of histones and irradiation of histone H2B. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 1987, 51(3), 527-540.
[http://dx.doi.org/10.1080/09553008714551001] [PMID: 3494701]
[38]
Lackowicz, J. Principals of fluorescence spectroscopy. Kluwer Academic/Plenum Publishers: New York, 1999.
[http://dx.doi.org/10.1007/978-1-4757-3061-6]
[39]
Uversky, V.N.; Yamin, G.; Munishkina, L.A.; Karymov, M.A.; Millett, I.S.; Doniach, S.; Lyubchenko, Y.L.; Fink, A.L.; Finka, A. Effects of nitration on the structure and aggregation of alpha-synuclein. Brain Res. Mol. Brain Res., 2005, 134(1), 84-102.
[http://dx.doi.org/10.1016/j.molbrainres.2004.11.014] [PMID: 15790533]
[40]
Khyami-Horani, H. Thermotolerant strain of Bacillus licheniformis producing lipase. World J. Microbiol. Biotechnol., 1996, 12(4), 399-401.
[http://dx.doi.org/10.1007/BF00340219] [PMID: 24415318]
[41]
Fontana, A.; Polverino de Laureto, P.; De Filippis, V.; Scaramella, E.; Zambonin, M. Probing the partly folded states of proteins by limited proteolysis. Fold. Des., 1997, 2(2), R17-R26.
[http://dx.doi.org/10.1016/S1359-0278(97)00010-2] [PMID: 9135978]