Degree of modification of Ro60 by the lipid peroxidation by-product 4-hydroxy-2-nonenal may differentially induce Sjögren syndrome or systemic lupus erythematosus in BALB/c mice

Free Radical Biology and Medicine

Volumn 50, Issue 10, 2011, Pages 1222-1233

  Kurien, Biji T ^a,b   Porter, Andrew ^a   Dorri, Yaser ^a,b   Iqbal, Saqib ^a   D'Souza, Anil ^a,b   Singh, Anil ^b   Asfa, Sima ^b   Cartellieri, Marc ^c   Mathias, Kristen ^d   Matsumoto, Hiroyuki ^b   Bachmann, Michael ^c   Hensley, Kenneth ^e   Scofield, R Hal ^a,b,f  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d Oklahoma School of Science and Mathematics   (United States)

^e MEDICAL COLLEGE OF OHIO   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

4 Hydroxy 2 nonenal; Antigens; Autoantibodies; Autoimmunity; Epitope spreading; Free radicals; Oxidative damage; Sj gren syndrome; SLE

Indexed keywords

4 HYDROXYNONENAL; AMYLASE; ANTINUCLEAR ANTIBODY; DOUBLE STRANDED DNA ANTIBODY; FREUND ADJUVANT; LA ANTIBODY; LA ANTIGEN; PROTEIN ANTIBODY; RIBONUCLEOPROTEIN; RO60 ANTIBODY; RO60 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETIC MANIPULATION; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; IMMUNOLOGICAL TOLERANCE; LIPID PEROXIDATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN MODIFICATION; SALIVATION; SJOEGREN SYNDROME; SYSTEMIC LUPUS ERYTHEMATOSUS;

ALDEHYDES; ANIMALS; AUTOIMMUNITY; FEMALE; LIPID PEROXIDATION; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; RIBONUCLEOPROTEINS; SALIVARY GLANDS; SJOGREN'S SYNDROME;

MUS; ORYCTOLAGUS CUNICULUS;

EID: 79955462938     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.10.687     Document Type: Article

References (68)

1. R.H. Scofield, S. Asfa, D. Obeso, R. Jonsson, and B.T. Kurien Immunization with short peptides from the 60-kDa Ro antigen recapitulates the serological and pathological findings as well as the salivary gland dysfunction of Sjogren's syndrome J. Immunol. 175 2005 8409 8414 (Pubitemid 41798408)
2. S.A. Mathews, B.T. Kurien, and R.H. Scofield Oral manifestations of Sjögren's syndrome J. Dent. Res. 87 2008 308 318
3. A.D. Farris, J.K. Gross, J.S. Hanas, and J.B. Harley Genes for murine Y1 and Y3 Ro RNAs have class 3 RNA polymerase III promoter structures and are unlinked on mouse chromosome 6 Gene 174 1996 35 42 (Pubitemid 26326848)
4. C.A. O'Brien, and S.L. Wolin A possible role for the 60-kDa Ro autoantigen in a discard pathway for defective 5 S rRNA precursors Genes Dev. 8 1994 2891 2903 (Pubitemid 24374673)
5. R.H. Scofield, B.T. Kurien, F. Zhang, P. Mehta, K. Kaufman, T. Gross, M. Bachmann, T. Gordon, and J.B. Harley Protein-protein interaction of the Ro-ribonucleoprotein particle using multiple antigenic peptides Mol. Immunol. 36 1999 1093 1106 (Pubitemid 30078911)
6. R.H. Scofield, B.T. Kurien, J.K. Gross, N.B. Reed, A.K. Taylor, N. Dominguez, P. Mehta, J.M. Guthridge, and M. Bachmann Interaction of calcium and Ro60: increase of antigenicity Mol. Immunol. 41 2004 809 816 (Pubitemid 38953638)
7. T.P. Gordon, A.I. Bolstad, M. Rischmueller, R. Jonsson, and S.A. Waterman Autoantibodies in primary Sjogren's syndrome: new insights into mechanisms of autoantibody diversification and disease pathogenesis Autoimmunity 34 2001 123 132 (Pubitemid 34149800)
8. R.H. Scofield Genetics of systemic lupus erythematosus and Sjögren's syndrome Curr. Opin. Rheumatol. 21 2009 448 453
9. M.N. Manoussakis, and H.M. Moutsopoulos Sjogren's syndrome: current concepts Adv. Intern. Med. 47 2001 191 217
10. R.H. Scofield, B.T. Kurien, and M. Reichlin Immunologically restricted and inhibitory anti-Ro/SSA in monozygotic twins Lupus 6 1997 395 398 (Pubitemid 27232135)
11. A.I. Bolstad, H.J. Haga, R. Wassmuth, and R. Jonsson Monozygotic twins with primary Sjögren's syndrome J. Rheumatol. 27 2000 2264 2266
12. S.C. Huang, R.H. Scofield, B.T. Kurien, and J.B. Harley Human anti-Ro autoantibodies bind multiple conformational epitopes of 60-kD Ro autoantigen Clin. Immunol. 17 1997 212 219 (Pubitemid 27261694)
13. R.H. Scofield, F.C. Zhang, B.T. Kurien, and J.B. Harley Anti-Ro fine specificity defined by multiple antigenic peptides identifies components of tertiary epitopes Clin. Exp. Immunol. 109 1997 480 487 (Pubitemid 27402317)
14. J.B. Harley, R.H. Scofield, and M. Reichlin Anti-Ro in Sjögren's syndrome and systemic lupus erythematosus Rheum. Dis. Clin. North Am. 18 1992 337 358
15. J.B. Harley, A.S. Sestak, L.G. Willis, S.M. Fu, J.A. Hansen, and M. Reichlin A model for disease heterogeneity in systemic lupus erythematosus: relationships between histocompatibility antigens, autoantibodies and lymphopenia or renal disease Arthritis Rheum. 32 1989 826 836 (Pubitemid 19181004)
16. B.T. Kurien, J.G. Newland, C. Paczkowski, K.L. Moore, and R.H. Scofield Anti-Ro mediates neutropenia in systemic lupus erythematosus by binding a 60, 000 MW antigen on the surface of neutrophils Clin. Exp. Immunol. 120 2000 209 217 (Pubitemid 30176921)
17. S. Kanagasegar, R. Cimaz, B.T. Kurien, A. Brucato, and R.H. Scofield Neonatal lupus manifests as isolated neutropenia and mildly abnormal liver functions J. Rheumatol. 29 2002 187 191 (Pubitemid 34041878)
18. A. Fujisaku, M.B. Frank, B. Neas, M. Reichlin, and J.B. Harley HLA-DQ gene complement and other histocompatibility relationships in man with the anti-Ro/SSA autoantibody response in systemic lupus erythematosus J. Clin. Invest. 86 1989 606 611 (Pubitemid 20271897)
19. R.H. Scofield, M.B. Frank, B.R. Neas, R.M. Horowitz, K.L. Hardgrave, A. Fujisaku, R. McArthur, and J.B. Harley Cooperative association of T cell beta receptor and HLA-DQ alleles in the production of anti-Ro in systemic lupus erythematosus Clin. Immunol. Immunopathol. 72 1994 335 341 (Pubitemid 24275212)
20. R.H. Scofield, W.D. Dickey, K.L. Hardgrave, B.R. Neas, R.M. Horowitz, R.A. McArthur, A. Fujisaku, M.B. Frank, and J.B. Harley Immunogenetics of epitopes of the carboxyl terminus of the human 60-kDa Ro autoantigen Clin. Exp. Immunol. 99 1995 256 261
21. J.D. Reveille, M.J. MaCLeod, K. Whittington, and F.C. Arnett Specific amino acid residues in the second hypervariable region of HLA-DQA1 and DQB1 chain genes promote the Ro (SS-A)/La (SS-B) autoantibody responses J. Immunol. 146 1991 3871 3876
22. R.H. Scofield, and J.B. Harley Association of anti-Ro (SS-A) autoantibodies with glutamine in position 34 of DQA1 and leucine in position 26 of DQB1 Arthritis Rheum. 37 1994 961 962 (Pubitemid 24184554)
23. R.H. Scofield, W.E. Henry, B.T. Kurien, J.A. James, and J.B. Harley Immunization with short peptides derived from the systemic lupus erythematosus associated 60 kDa Ro autoantigen results in autoimmunity directed towards the Ro ribonucleoprotein J. Immunol. 156 1996 4059 4066 (Pubitemid 26139946)
24. R.H. Scofield, K.M. Kaufman, U. Baber, J.A. James, J.B. Harley, and B.T. Kurien Immunization of mouse with 60 kDa Ro peptides results in epitope spreading if peptides are highly homologous between man and mouse Arthritis Rheum. 42 1999 1017 1024 (Pubitemid 29215014)
25. R.H. Scofield, P.G. Pierce, J.A. James, K.M. Kaufman, and B.T. Kurien Immunization with peptides from 60 kDa Ro in diverse mouse strains Scand. J. Immunol. 56 2002 477 483 (Pubitemid 35373684)
26. F. Topfer, T. Gordon, and J. McCluskey Intra- and intermolecular spreading of autoimmunity involving the nuclear self antigens La (SS-B) and Ro (SS-A) Proc. Natl Acad. Sci. USA 92 1995 875 879
27. P. Michel, W. Eggert, H. Albrecht-Nebe, and T. Grune Increased lipid peroxidation in children with autoimmune diseases Acta Paediatr. 86 1997 609 612 (Pubitemid 27330424)
28. M.G. Serban, and S. Tanaseanu Lipid peroxidation in autoimmune systemic vasculitides: effect of corticoid treatment on lipid peroxidation. Antioxidant protection with vitamin E Rom. J. Intern. Med. 32 1994 137 142 (Pubitemid 24322041)
29. T. Grune, P. Michel, N. Sitte, W. Eggert, H. Albrecht-Nebe, H. Esterbauer, and W.G. Siems Increased levels of 4-hydroxynonenal modified proteins in plasma of children with autoimmune diseases Free Radic. Biol. Med. 23 1997 357 360 (Pubitemid 27276770)
30. S. Turi, I. Nemeth, A. Torkos, L. Saghy, I. Vargha, B. Matcovics, and J. Nagy Oxidative stress and antioxidant defense mechanism in glomerular diseases Free Radic. Biol. Med. 22 1997 161 168
31. M.G. Serban, S. Tanaseanu, and C. Bara Oxidant stress and antioxidant protection in lupus nephropathy Rom. J. Intern. Med. 34 1996 105 109
32. T.B. Kurien, and R. Selvam Induction of lipid-peroxidation in calcium-oxalate stone formation Ind. J. Exp. Biol. 27 1989 450 453 (Pubitemid 20054424)
33. G. Jurgens, H.B. Hoff, G.M. Chisolm, and H. Esterbauer Modification of human serum low density lipoprotein by oxidation: characterization and pathophysiological implications Chem. Phys. Lipids 45 1987 315 336 (Pubitemid 17152339)
34. W. Palinski, and J.L. Witztum Immune response to oxidative neoepitopes on LDL and phospholipids modulate the development of atherosclerosis J. Intern. Med. 247 2000 371 380 (Pubitemid 30180039)
35. J.A. Berliner, M. Navab, A.M. Fogelman, J.S. Frank, L.L. Demer, P.A. Edwards, A.D. Watson, and A.J. Luis Atherosclerosis: basic mechanisms. Oxidation, inflammation and genetics Circulation 91 1995 2488 2496
36. D. Steinberg Oxidative modification of LDL and atherosclerosis Circulation 95 1997 1062 1071
37. K. Uchida, M. Kanamatsu, Y. Morimitsu, T. Osawa, N. Noguchi, and E. Niki Acrolein is a product of lipid peroxidation: formation of free acrolein and its conjugation with lysine residues in oxidized low density lipoproteins J. Biol. Chem. 273 1998 16058 16066 (Pubitemid 28311374)
38. M. Comporti Lipid peroxidation and biogenic aldehydes: from the identification of 4-hydroxynonenal to further achievements in biopathology Free Radic. Res. 28 1998 623 635 (Pubitemid 28454255)
39. R.H. Scofield, B.T. Kurien, S. Ganick, M.T. McClain, Q. Pye, J.A. James, R.I. Schneider, R.H. Broyles, M. Bachmann, and K. Hensley 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 2005 719 728 (Pubitemid 40249742)
40. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
41. Y. Dorri, B.T. Kurien, and R.H. Scofield A simpler and faster version of two-dimensional gel electrophoresis using vertical, mini SDS-PAGE apparatus Iran. J. Chem. Chem. Eng. 28 2009 51 56
42. H. Towbin, T. Staehelin, and T. Gordon Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some application Proc. Natl Acad. Sci. USA 76 1979 4350 4354 (Pubitemid 9256559)
43. B.T. Kurien, and R.H. Scofield Protein blotting J. Immunol. Meth. 274 2003 1 15
44. H. Matsumoto, and N. Komori Ocular proteomics: cataloging photoreceptor proteins by two-dimensional gel electrophoresis and mass spectrometry Meth. Enzymol. 316 2000 492 511 (Pubitemid 30235689)
45. D.J. Pappin, P. Hojrup, and A.J. Bleasby Rapid identification of proteins by peptide-mass fingerprinting Curr. Biol. 3 1993 327 332
46. B.T. Kurien, and R.H. Scofield Heat mediated quick Coomassie blue protein staining and destaining of SDS-PAGE gels Indian J. Biochem. Biophys. 35 1998 385 389 (Pubitemid 128376853)
47. Y. Dorri, and B.T. Kurien Environmentally safe removal/disposal of Coomassie brilliant blue from gel destain and used gel stain Anal. Biochem. 404 2010 193 196
48. E.L. Alexander, K. Malinow, J.E. Lejewski, M.S. Jerdan, T.T. Provost, and G.E. Alexander Primary Sjögren's syndrome with central nervous system disease mimicking multiple sclerosis Ann. Intern. Med. 104 1986 323 330 (Pubitemid 16163608)
49. E.L. Alexander Neurologic disease in Sjögren's syndrome: mononuclear inflammatory vasculopathy affecting central/peripheral nervous system and muscle. A clinical review and update of immunopathogenesis Rheum. Dis. Clin. North Am. 19 1993 869 908 (Pubitemid 23347416)
50. A.N. Scofield, B.T. Kurien, T.P. Gordon, and R.H. Scofield Can B cell epitopes of 60 kD Ro distinguish systemic lupus erythematosus from Sjogren's syndrome Lupus 10 2001 547 553 (Pubitemid 32777651)
51. M.J. Mamula Epitope spreading: the role of self peptides and autoantigen processing by B lymphocytes Immunol. Rev. 164 1998 231 239 (Pubitemid 28438411)
52. F. Topfer, T. Gordon, and J. McCluskey Intra- and inter-molecular spreading of autoimmunity involving the nuclear self-antigens La (SS-B) and Ro (SS-A) Proc. Natl Acad. Sci. USA 92 1995 875 879
53. K. Kawahata, Y. Misaki, Y. Komagata, K. Setoguchi, S. Tsunekawa, Y. Yoshikawa, J. Miyazaki, and K. Yamamoto Altered expression level of a systemic nuclear autoantigen determines the fate of immune response to self J. Immunol. 162 1999 6482 6491 (Pubitemid 29309370)
54. U.S. Deshmukh, J.E. Lewis, F. Gaskin, C.C. Kannapell, S.T. Waters, Y.H. Lou, K.S. Tung, and S.M. Fu Immune response to Ro60 and its peptides in mice. I. The nature of the immunogen and endogenous autoantigen determine the specificities of the induced antibodies J. Exp. Med. 189 1999 531 540 (Pubitemid 29187375)
55. B.T. Kurien, and R.H. Scofield Autoantibody determination in the diagnosis of systemic lupus erythematosus Scand. J. Immunol. 64 2006 227 235 (Pubitemid 44215112)
56. B.T. Kurien, and R.H. Scofield Free radical mediated peroxidative damage in systemic lupus erythematosus Life Sci. 73 2003 1655
57. H. Esterbauer, R.G. Schaur, and H. Zollner Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radic. Biol. Med. 11 1991 81 128 (Pubitemid 121003917)
58. W. Palinski, and J.L. Witztum Immune response to oxidative neoepitopes on LDL and phospholipids modulate the development of atherosclerosis J. Intern. Med. 247 2000 371 380 (Pubitemid 30180039)
59. E. Maggi, R. Chiesa, G. Melisano, R. Castellano, G. Astore, A. Grossi, G. Finardi, and G. Bellomo LDL oxidation in patients with atherosclerosis: a study of in vitro and in vivo oxidation markers Arterioscler. Thromb. Vasc. Biol. 14 1995 1892
60. C. Bergmark, R. Wu, U. de Faire, A.K. Lefvert, and J. Swedenborg Patients with early onset peripheral vascular disease have increased levels of autoantibodies against oxidized LDL Arterioscler. Thromb. Vasc. Biol. 15 1995 441
61. P. Holvoet, G. Perez, Z. Zhao, E. Brouwers, H. Bernar, and D. Collen Malondialdehyde-modified LDL in patients with atherosclerotic disease J. Clin. Invest. 95 1995 2611
62. T. Lehtimaki, S. Lehtinen, T. Solakivi, M. Nikkila, O. Jaakkola, H. Jokela, S. Yla-Herttuala, J.S. Luoma, T. Koivula, and T. Nikkari Autoantibodies against oxidized low density lipoprotein in patients with angiographically verified coronary artery disease Arterioscler. Thromb. Vasc. Biol. 19 1990 23
63. H. Itabe, S. Jimi, S. Kamimura, K. Suzuki, N. Uesugi, T. Imanaka, H. Shijo, and T. Tanako Appearance of cross linked proteins in human atheroma and rat pre-fibrotic liver detected by a new monoclonal antibody Biochim. Biophys. Acta 1406 1998 28
64. M.K. Chang, C. Bergmark, A. Laurila, S. Horkko, K.H. Han, P. Friedman, E.A. Dennis, and J.L. Witztum Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition Proc. Natl Acad. Sci. USA 96 1999 6353
65. E. Mottaran, S.F. Stewart, R. Rolla, D. Vay, V. Cipriani, M.G. Moretti, M. Vidali, M. Sartori, C. Rigamonti, C.P. Day, and E. Albano Lipid peroxidation contributes to immune reactions associated with alcoholic liver disease Free Radic. Biol. Med. 32 2002 38
66. S.M. Trigwell, P.M. Radford, S.R. Page, A.C. Loweth, R.F. James, N.G. Morgan, and I. Todd Islet glutamic acid decarboxylase modified by reactive oxygen species is recognized by antibodies from patients with type 1 diabetes mellitus Clin. Exp. Immunol. 126 2001 242
67. J.H. Reed, M.W. Jackson, and T.P. Gordon A B cell apotope of Ro 60 in systemic lupus erythematosus Arthritis Rheum. 58 2008 1125 1129 (Pubitemid 351564015)
68. J.H. Reed, M.W. Jackson, and T.P. Gordon A Ro60 apotope is cryptic on the intracellular ribonucleoprotein complex Lupus 19 2010 107 108