BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Antibodies against Nitric Oxide Damaged Poly L-Tyrosine and 3-Nitrotyrosine Levels in Systemic Lupus Erythematosus

  • Khan, Fozia (Department of Biochemistry, Faculty of Medicine, A.M.U.) ;
  • Ali, Rashid (Department of Biochemistry, Faculty of Medicine, A.M.U.)
  • Received : 2005.10.07
  • Accepted : 2006.01.09
  • Published : 2006.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Alterations in the amino acid structure or sequence can generate neo-epitopes from self-proteins causing autoaggressive immune attack. Reactive nitrogen species are an important factor that induces post-translational modification of proteins by cellular reduction and oxidation mechanism; cysteinyl-nitrosylation or tyrosine nitration leading to potentially pathogenic pathways. It was thought of interest to investigate the immunogenicity of nitrated poly L-tyrosine vis-$\`{a}$-vis its possible role in the induction of antibodies in systemic lupus erythematosus (SLE). Commercially available poly L-tyrosine was exposed to nitrating species and the damage was monitored by UV spectroscopy and alkaline gel electrophoresis. The results indicated the formation of 3-nitrotyrosine. Nitrated poly L-tyrosine induced higher titre antibodies as compared to the native form. Nitrated poly L-tyrosine was recognized by the autoantibodies present in the sera of patients suffering from SLE by enzyme immunoassays and band shift assay. The possible role of nitrated self-proteins has been discussed in the production of circulating anti-DNA antibodies in SLE.

Keywords

References

  1. Ali, R. and Alam, K. (2002) Evaluation of antibodies against oxygen free radical-modified DNA by ELISA. Methods Mol. Biol. 186, 171-181
  2. Arnett, F. C., Edworthy, S. M., Bloch, D. A., McShane, D. J., Fries, J. F., Cooper, N. S., Healey, L. A., Kaplan, S. R., Liang, M. H. and Luthra, H. S. (1998) The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arth. Rheum. 31, 315-324
  3. Belmont, H. M., Levartovsky, D., Goel, A., Amin, A., Giorno, R., Rediske, J., Skovron, M. L. and Abramson, S. B. (1997) Increased nitric oxide production accompanied by the upregulation of inducible nitric oxide synthase in vascular endothelium from patients with systemic lupus erythematosus. Arth. Rheum. 40, 1810-1816 https://doi.org/10.1002/art.1780401013
  4. Brito, C., Naviliat, M., Tiscornia, A. C., Vuillier, F., Gualco, G., Dighiero, G., Radi, R. and Cayota, A. M. (1999) Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J. Immunol. 162, 3356-3366
  5. Brown, G. C., McBride, A. G., Fox, E. J., McNaught, K. S. and Borutaite, V. (1997) Nitric oxide and oxygen metabolism. Biochem. Soc. Trans. 25, 901-904 https://doi.org/10.1042/bst0250901
  6. Cassina, A. and Radi, R. (1996) Differential inhibitory action of nitric oxide and peroxynitrite on mitochondrial electron transport. Arch. Biochem. Biophys. 328, 309-316 https://doi.org/10.1006/abbi.1996.0178
  7. Crow, J. P. (1999) Measurement and significance of free and protein-bound 3-nitrotyrosine, 3-chlorotyrosine, and free 3- nitro-4-hydroxyphenylacetic acid in biologic samples: A highperformance liquid chromatography method using electrochemical detection. Methods Enzymol. 301, 151-160 https://doi.org/10.1016/S0076-6879(99)01078-2
  8. Davies, K. J. (1987) Protein damage and degradation by oxygen radicals. I. general aspects. J. Biol. Chem. 262, 9895-9901
  9. Davies, K. J. and Delsignore, M. E. (1987) Protein damage and degradation by oxygen radicals. III. Modification of secondary and tertiary structure. J. Biol. Chem. 262, 9908-9913
  10. Davies, K. J., Delsignore, M. E. and Lin, S. W. (1987) Protein damage and degradation by oxygen radicals. II. Modification of amino acids. J. Biol. Chem. 262, 9902-9907
  11. Dixit, K. and Ali, R. (2004) Role of nitric oxide modified DNA in the etiopathogenesis of systemic lupus erythematosus. Lupus. 13, 95-100 https://doi.org/10.1191/0961203304lu492oa
  12. Dixit, K., Ahsan, H. and Ali, A. (2003) Polydeoxyribonucleotide C photoconjugated with lysine or arginine present unique epitopes for human anti-DNA autoantibodies. Hum. Immunol. 64, 880-886 https://doi.org/10.1016/S0198-8859(03)00144-7
  13. Gilkeson, G., Cannon, C., Oates, J., Reilly, C., Goldman, D. and Petri, M. (1999) Correlation of serum measures of nitric oxide production with lupus disease activity. J. Rheumatol. 26, 318- 324 https://doi.org/10.1093/rheumatology/26.4.318
  14. Gunther, M. R., Sturgeon, B. E. and Mason, R. P. (2002) Nitric oxide trapping of the tyrosyl radical-chemistry and biochemistry. Toxicology 177, 1-9 https://doi.org/10.1016/S0300-483X(02)00191-9
  15. Hal, S. R., Kurien, B. T., Ganick, S., McClain, M. T., Pye, Q., James, J. A., Schneider, R. I., Broyles, R. H., Bachmann, M. and Hensley, K. (2005) Modification of lupus-associated 60- kDa Ro protein with the lipid oxidation product 4-hydroxy-2- nonenal increases antigenicity and facilitates epitope spreading. Free Radic. Biol. Med. 38, 719-728 https://doi.org/10.1016/j.freeradbiomed.2004.11.001
  16. Hasan, R. and Ali, R. (1990) Antibody recognition of common epitopes on Z-DNA and native DNA brominated under high salt. Biochem. Int. 20, 1077-1088
  17. Hasan, R., Ali, A. and Ali, R. (1991) Antibodies against DNApsoralen crosslink recognize unique conformation. Biochim. Biophys. Acta. 1073, 509-513 https://doi.org/10.1016/0304-4165(91)90223-4
  18. Jacob, L., Lety, M. A., Bach, J. F. and Louvard, D. (1986) Human systemic lupus erythematosus sera contain antibodies against cell-surface protein(s) that share(s) epitope(s) with DNA. Proc. Natl. Acad. Sci. USA 83, 6970-6974 https://doi.org/10.1073/pnas.83.18.6970
  19. Kaur, H. and Halliwell, B. (1994) Evidence for nitric oxidemediated oxidative damage in chronic inflammation. Nitrotyrosine in serum and synovial fluid from rheumatoid patients. FEBS Lett. 350, 9-12 https://doi.org/10.1016/0014-5793(94)00722-5
  20. Khan, J., Brennand, D. M., Bradley, N., Gao, B., Bruckdorfer, R., and Jacobs, M. (1998) 3-Nitrotyrosine in the proteins of human plasma determined by an ELISA method. Biochem. J. 332, 807-808
  21. Lepoivre, M., Fieschi, F., Coves, J., Thelander, L. and Fontecave, M. (1991) Inactivation of ribonucleotide reductase by nitric oxide. Biochem. Biophys. Res. Commun. 179, 442-448 https://doi.org/10.1016/0006-291X(91)91390-X
  22. Lopez-Nevot, M. A., Ramal, L., Jimenez-Alonso, J. and Martin, J. (2003) The inducible nitric oxide synthase promoter polymorphism does not confer susceptibility to systemic lupus erythematosus. Rheumatology 42, 113-116 https://doi.org/10.1093/rheumatology/keg044
  23. Mansoor, F., Ali, A. and Ali, R. (2005) Binding of circulating SLE autoantibodies to oxygen free radical damaged chromatin. Autoimmunity 38, 431-438 https://doi.org/10.1080/08916930500288596
  24. Nguyen, T., Brunson, D., Crespi, C. L., Penman, B. W., Wishnok, J. S. and Tannenbaum, S. R. (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. USA 89, 3030-3034 https://doi.org/10.1073/pnas.89.7.3030
  25. Oates, J. C., Christensen, E. F., Reilly, C. M., Self, S. E. and Gilkeson, G. S. (1999) Prospective measure of serum 3- nitrotyrosine levels in systemic lupus erythematosus: correlation with disease activity. Proc. Assoc. Am. Physicians. 111, 611- 621 https://doi.org/10.1046/j.1525-1381.1999.99110.x
  26. Ohmori, H., Oka, M., Nishikawa, Y., Shigemitsu, H., Takeuchi, M., Magari, M. and Kanayama, N. (2005) Immunogenicity of autologous IgG bearing the inflammation-associated marker 3- nitrotyrosine. Immunol. Lett. 96, 47-54 https://doi.org/10.1016/j.imlet.2004.07.004
  27. Ohshima, H., Friesen, M., Brouet, I. and Bartsch, H. (1990) Nitrotyrosine as new marker for endogenous nitrosation and nitration of proteins. Food Chem. Toxicol. 28, 647-652 https://doi.org/10.1016/0278-6915(90)90173-K
  28. Reynolds, M. R., Berry, R. W. and Binder, L. I. (2005) Site- Specific Nitration and oxidative dityrosine bridging of the tau protein by peroxynitrite: implications for Alzheimer's disease. Biochemistry 44, 1690-1700 https://doi.org/10.1021/bi047982v
  29. Robert, P. and Kimberly, M. D. (2001) Research advances in systemic lupus erythematosus. J. Am. Med. Assn. 285, 650-651 https://doi.org/10.1001/jama.285.5.650
  30. Tsikas, D. and Caidahl, K. (2005) Recent methodological advances in the mass spectrometric analysis of free and protein-associated 3-nitrotyrosine in human plasma. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 814, 1-9 https://doi.org/10.1016/j.jchromb.2004.10.003
  31. Wanchu, A., Khullar, M., Deodhar, S. D., Bambery, P. and Sud, A. (1998) Nitric oxide synthesis is increased in patients with systemic lupus erythematosus. Rheumatol. Int. 18, 41-43 https://doi.org/10.1007/s002960050055
  32. Waris, G. and Alam, K. (2004) Immunogenicity of superoxide radical modified-DNA: Studies on induced antibodies and SLE anti-DNA autoantibodies. Life Sci. 75, 2633-2642 https://doi.org/10.1016/j.lfs.2004.04.034
  33. Xiao, G. G., Nel, A. E. and Loo, J. A. (2005) Nitrotyrosinemodified proteins and oxidative stress induced by diesel exhaust particles. Electrophoresis 26, 280-292 https://doi.org/10.1002/elps.200406145
  34. Yoshie, Y. and Ohshima, H. (1997) Synergistic induction of DNA strand breakage caused by nitric oxide together with catecholamine: implications for neurodegenerative disease. Chem. Res. Toxicol. 10, 1015-1022 https://doi.org/10.1021/tx970025k

Cited by

  1. Regulation of the Neurodegenerative Process Associated to Parkinson’s Disease by CD4+ T-cells vol.10, pp.4, 2015, https://doi.org/10.1007/s11481-015-9618-9
  2. Autoimmune Profiling Reveals Peroxiredoxin 6 as a Candidate Traumatic Brain Injury Biomarker vol.32, pp.22, 2015, https://doi.org/10.1089/neu.2014.3736
  3. Role of peroxynitrite-modified H2A histone in the induction and progression of rheumatoid arthritis vol.41, pp.6, 2012, https://doi.org/10.3109/03009742.2012.698300
  4. 3-Nitrotyrosine: A biomarker of nitrogen free radical species modified proteins in systemic autoimmunogenic conditions vol.74, pp.10, 2013, https://doi.org/10.1016/j.humimm.2013.06.009
  5. Autoantibody Determination in the Diagnosis of Systemic Lupus Erythematosus vol.64, pp.3, 2006, https://doi.org/10.1111/j.1365-3083.2006.01819.x
  6. Immune response to chemically modified proteome vol.8, pp.1-2, 2014, https://doi.org/10.1002/prca.201300068
  7. Protein Nitration in Placenta – Functional Significance vol.29, pp.12, 2008, https://doi.org/10.1016/j.placenta.2008.09.003
  8. Neuroimmune regulation of microglial activity involved in neuroinflammation and neurodegenerative diseases vol.274, pp.1-2, 2014, https://doi.org/10.1016/j.jneuroim.2014.07.012
  9. Loss of CD4 T-cell-dependent tolerance to proteins with modified amino acids vol.108, pp.31, 2011, https://doi.org/10.1073/pnas.1110042108
  10. Tyrosine-Nitrated Proteins: Proteomic and Bioanalytical Aspects vol.26, pp.7, 2017, https://doi.org/10.1089/ars.2016.6787
  11. Effect of peroxynitrite on human serum albumin: a multi technique approach vol.35, pp.9, 2017, https://doi.org/10.1080/07391102.2016.1206489
  12. Measurement and Significance of 3-Nitrotyrosine in Systemic Lupus Erythematosus vol.64, pp.5, 2006, https://doi.org/10.1111/j.1365-3083.2006.01794.x
  13. Nitrite correlates with 3-nitrotyrosine but not with the F2-isoprostane 15(S)-8-iso-PGF2α in urine of rheumatic patients vol.21, pp.3-4, 2009, https://doi.org/10.1016/j.niox.2009.09.001
  14. Role of peroxynitrite-modified biomolecules in the etiopathogenesis of systemic lupus erythematosus vol.14, pp.1, 2014, https://doi.org/10.1007/s10238-012-0222-5
  15. Circulating free nitrotyrosine and cognitive decline vol.122, pp.3, 2010, https://doi.org/10.1111/j.1600-0404.2009.01286.x
  16. The Emerging Role of Autoimmunity in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/cfs) vol.49, pp.2, 2014, https://doi.org/10.1007/s12035-013-8553-0
  17. Strategies for comprehensive analysis of amino acid biomarkers of oxidative stress vol.33, pp.1, 2007, https://doi.org/10.1007/s00726-007-0542-z
  18. Protein kinase Cδ oxidation contributes to ERK inactivation in lupus T cells vol.64, pp.9, 2012, https://doi.org/10.1002/art.34503
  19. The biology of nitric oxide and other reactive intermediates in systemic lupus erythematosus vol.121, pp.3, 2006, https://doi.org/10.1016/j.clim.2006.06.001
  20. The biology of reactive intermediates in systemic lupus erythematosus vol.43, pp.1, 2010, https://doi.org/10.3109/08916930903374683