Epitope spreading within lupus-associated ribonucleoprotein antigens

Clinical Immunology

Volumn 117, Issue 2, 2005, Pages 112-120

  Deshmukh, Umesh S ^a   Bagavant, Harini ^a   Lewis, Janet ^a   Gaskin, Felicia ^b   Shu, Man Fu ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Autoantibodies; Autoimmunity; Cross reactivity; Epitope spreading; Intermolecular; Intramolecular; Ribonucleoproteins; Ro60; snRNP; Systemic lupus erythematosus

Indexed keywords

ANTIGEN; AUTOANTIBODY; EPITOPE; POLYPEPTIDE; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; RIBONUCLEOPROTEIN;

ANTIBODY PRODUCING CELL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; COMPLEX FORMATION; EXPERIMENTAL ANIMAL; HUMAN; IMMUNIZATION; MUTATION; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SERUM; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; AUTOANTIGENS; EPITOPES; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; RIBONUCLEOPROTEINS;

EID: 26044477194     PISSN: 15216616     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clim.2005.07.002     Document Type: Review

References (78)

1. W.H. Reeves, M. Satoh, and H.B. Richards Origins of antinuclear antibodies R.G. Lahita Systemic Lupus Erythematosus 2004 Elsevier San Diego 401 431
2. M. Reichlin Anticytoplasmic antibodies in SLE: antibodies to cytoplasmic antigens R.G. Lahita Systemic Lupus Erythematosus 2004 Elsevier San Diego 315 324
3. T. Orth, W.J. Mayet, H. Deister, S. Chang, M. Schmitz, and M. Bachmann Analysis of epitope spreading over an eleven-year period in a patient with systemic lupus erythematosus Scand. J. Rheumatol. 27 1998 461 464
4. E.L. Greidinger, and R.W. Hoffman The appearance of U1 RNP antibody specificities in sequential autoimmune human antisera follows a characteristic order that implicates the U1-70 kd and B′/B proteins as predominant U1 RNP immunogens Arthritis Rheum. 44 2001 368 375
5. P.V. Lehmann, T. Forsthuber, A. Miller, and E.E. Sercarz Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen Nature 358 1992 155 157
6. P.V. Lehmann, E.E. Sercarz, T. Forsthuber, C.M. Dayan, and G. Gammon Determinant spreading and the dynamics of the autoimmune T-cell repertoire Immunol. Today 14 1993 203 208
7. J.A. James, and J.B. Harley B-cell epitope spreading in autoimmunity Immunol. Rev. 164 1998 185 200
8. M.R. Arbuckle, M.T. McClain, M.V. Rubertone, R.H. Scofield, G.J. Dennis, J.A. James, and J.B. Harley Development of autoantibodies before the clinical onset of systemic lupus erythematosus N. Engl. J. Med. 349 2003 1526 1533
9. J. McCluskey, A.D. Farris, C.L. Keech, A.W. Purcell, M. Rischmueller, G. Kinoshita, P. Reynolds, and T.P. Gordon Determinant spreading: lessons from animal models and human disease Immunol. Rev. 164 1998 209 229
10. F. Monneaux, and S. Muller Epitope spreading in systemic lupus erythematosus: identification of triggering peptide sequences Arthritis Rheum. 46 2002 1430 1438
11. E.J. McMahon, S.L. Bailey, C.V. Castenada, H. Waldner, and S.D. Miller Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis Nat. Med. 11 2005 335 339
12. M. Reichlin, and J.B. Harley Antibodies to Ro/SSA and La/SSB D.J. Wallace B.H. Hahn Dubois' Lupus Erythematosus 2002 Lippincott Williams and Wilkins Philadelphia 467 480
13. J.P. Hendrick, S.L. Wolin, J. Rinke, M.R. Lerner, and J.A. Steitz Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells Mol. Cell. Biol. 1 1981 1138 1149
14. M.R. Lerner, J.A. Boyle, J.A. Hardin, and J.A. Steitz Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus Science 211 1981 400 402
15. M.J. Fritzler, and E.K.L. Chan Antibodies to nonhistone antigens in systemic lupus erythematosus R.G. Lahita Systemic Lupus Erythematosus 2004 Elsevier San Diego 349 376
16. M. Rischmueller, S. Lester, Z. Chen, G. Champion, R. Van Den Berg, R. Beer, T. Coates, J. McCluskey, and T. Gordon HLA class II phenotype controls diversification of the autoantibody response in primary Sjogren's syndrome (pSS) Clin. Exp. Immunol. 111 1998 365 371
17. E. Ben-Chetrit, E.K. Chan, K.F. Sullivan, and E.M. Tan A 52-kD protein is a novel component of the SS-A/Ro antigenic particle J. Exp. Med. 167 1988 1560 1571
18. G. Boire, M. Gendron, N. Monast, B. Bastin, and H.A. Menard Purification of antigenically intact Ro ribonucleoproteins; biochemical and immunological evidence that the 52-kD protein is not a Ro protein Clin. Exp. Immunol. 100 1995 489 498
19. Y.T. Yu, E.C. Scharl, C.M. Smith, and J.A. Steitz The Growing World of Small Nuclear Ribonucleoprotein 1999 Cold Spring laboratory Press Cold Spring Harbor
20. J.E. Craft Anti-snRNP antibodies D.J. Wallace B.H. Hahn Dubois' Lupus Erythematosus 2002 Lippincott Williams and Wilkins Philadelphia 481 494
21. E. Benito-Garcia, P.H. Schur, and R. Lahita Guidelines for immunologic laboratory testing in the rheumatic diseases: anti-Sm and anti-RNP antibody tests Arthritis Rheum. 51 2004 1030 1044
22. W.H. Reeves, D.E. Fisher, R.G. Lahita, and H.G. Kunkel Autoimmune sera reactive with Sm antigen contain high levels of RNP-like antibodies J. Clin. Invest. 75 1985 580 587
23. D.E. Fisher, W.H. Reeves, R. Wisniewolski, R.G. Lahita, and N. Chiorazzi Temporal shifts from Sm to ribonucleoprotein reactivity in systemic lupus erythematosus Arthritis Rheum. 28 1985 1348 1355
24. 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. U. S. A. 92 1995 875 879
25. C.L. Keech, T.P. Gordon, and J. McCluskey The immune response to 52-kDa Ro and 60-kDa Ro is linked in experimental autoimmunity J. Immunol. 157 1996 3694 3699
26. C.E. Tseng, E.K. Chan, E. Miranda, M. Gross, F. Di Donato, and J.P. Buyon The 52-kd protein as a target of intermolecular spreading of the immune response to components of the SS-A/Ro-SS-B/La complex Arthritis Rheum. 40 1997 936 944
27. M.E. Miranda-Carus, M. Boutjdir, C.E. Tseng, F. DiDonato, E.K. Chan, and J.P. Buyon Induction of antibodies reactive with SSA/Ro-SSB/La and development of congenital heart block in a murine model J. Immunol. 161 1998 5886 5892
28. G. Kinoshita, C.L. Keech, R.D. Sontheimer, A. Purcell, J. McCluskey, and T.P. Gordon Spreading of the immune response from 52 kDa Ro and 60 kDa Ro to calreticulin in experimental autoimmunity Lupus 7 1998 7 11
29. 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 responses to Ro60 and its peptides in mice: I. The nature of the immunogen and endogenous autoantigen determine the specificities of the induced autoantibodies J. Exp. Med. 189 1999 531 540
30. G. Kinoshita, A.W. Purcell, C.L. Keech, A.D. Farris, J. McCluskey, and T.P. Gordon Molecular chaperones are targets of autoimmunity in Ro(SS-A) immune mice Clin. Exp. Immunol. 115 1999 268 274
31. T. Paisansinsup, U.S. Deshmukh, V.R. Chowdhary, H.S. Luthra, S.M. Fu, and C.S. David HLA class II influences the immune response and antibody diversification to Ro60/Sjogren's syndrome-A: heightened antibody responses and epitope spreading in mice expressing HLA-DR molecules J. Immunol. 168 2002 5876 5884
32. T.P. Gordon, G. Kinoshita, D. Cavill, C. Keech, A. Farris, K. Kaufman, J. McCluskey, and A. Purcell Restricted specificity of intermolecular spreading to endogenous La (SS-B) and 60 kDa Ro (SS-A) in experimental autoimmunity Scand. J. Immunol. 56 2002 168 173
33. R.H. Scofield, W.E. Henry, B.T. Kurien, J.A. James, and J.B. Harley Immunization with short peptides from the sequence of the systemic lupus erythematosus-associated 60-kDa Ro autoantigen results in anti-Ro ribonucleoprotein autoimmunity J. Immunol. 156 1996 4059 4066
34. P. Reynolds, T.P. Gordon, A.W. Purcell, D.C. Jackson, and J. McCluskey Hierarchical self-tolerance to T cell determinants within the ubiquitous nuclear self-antigen La (SS-B) permits induction of systemic autoimmunity in normal mice J. Exp. Med. 184 1996 1857 1870
35. R.H. Scofield, K.M. Kaufman, U. Baber, J.A. James, J.B. Harley, and B.T. Kurien Immunization of mice with human 60-kd Ro peptides results in epitope spreading if the peptides are highly homologous between human and mouse Arthritis Rheum. 42 1999 1017 1024
36. A.D. Farris, L. Brown, P. Reynolds, J.B. Harley, J.A. James, R.H. Scofield, J. McCluskey, and T.P. Gordon Induction of autoimmunity by multivalent immunodominant and subdominant T cell determinants of La (SS-B) J. Immunol. 162 1999 3079 3087
37. U.S. Deshmukh, J.E. Lewis, F. Gaskin, P.K. Dhakephalkar, C.C. Kannapell, S.T. Waters, and S.M. Fu Ro60 peptides induce antibodies to similar epitopes shared among lupus-related autoantigens J. Immunol. 164 2000 6655 6661
38. 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
39. R.R. Graham, W.A. Ortmann, C.D. Langefeld, D. Jawaheer, S.A. Selby, P.R. Rodine, E.C. Baechler, K.E. Rohlf, K.B. Shark, K.J. Espe, L.E. Green, R.P. Nair, P.E. Stuart, J.T. Elder, R.A. King, K.L. Moser, P.M. Gaffney, T.L. Bugawan, H.A. Erlich, S.S. Rich, P.K. Gregersen, and T.W. Behrens Visualizing human leukocyte antigen class II risk haplotypes in human systemic lupus erythematosus Am. J. Hum. Genet. 71 2002 543 553
40. M. Reichlin, A. Martin, E. Taylor-Albert, K. Tsuzaka, W. Zhang, M.W. Reichlin, E. Koren, F.M. Ebling, B. Tsao, and B.H. Hahn Lupus autoantibodies to native DNA cross-react with the A and D SnRNP polypeptides J. Clin. Invest. 93 1994 443 449
41. K. Tsuzaka, A.K. Leu, M.B. Frank, B.F. Movafagh, M. Koscec, T.H. Winkler, J.R. Kalden, and M. Reichlin Lupus autoantibodies to double-stranded DNA cross-react with ribosomal protein S1 J. Immunol. 156 1996 1668 1675
42. H. Hasegawa, T. Uchiumi, T. Sato, M. Arakawa, and R. Kominami Anti-Sm autoantibodies cross-react with ribosomal protein S10: a common structural unit shared by the small nuclear RNP proteins and the ribosomal protein Arthritis Rheum. 41 1998 1040 1046
43. S. Kumar, J. Kalsi, K. Bunting, C.T. Ravirajan, D.S. Latchman, L.H. Pearl, and D.A. Isenberg Fine binding characteristics of human autoantibodies-Partial molecular characterization Mol. Immunol. 41 2004 495 510
44. R.W. Hoffman, T. Gazitt, M.F. Foecking, R.A. Ortmann, M. Misfeldt, R. Jorgenson, S.L. Young, and E.L. Greidinger U1 RNA induces innate immunity signaling Arthritis Rheum. 50 2004 2891 2896
45. J. Ma, J. Xu, M.P. Madaio, Q. Peng, J. Zhang, I.S. Grewal, R.A. Flavell, and J. Craft Autoimmune lpr/lpr mice deficient in CD40 ligand: spontaneous Ig class switching with dichotomy of autoantibody responses J. Immunol. 157 1996 417 426
46. S.L. Peng, M.P. Madaio, D.P. Hughes, I.N. Crispe, M.J. Owen, L. Wen, A.C. Hayday, and J. Craft Murine lupus in the absence of alpha beta T cells J. Immunol. 156 1996 4041 4049
47. S. Fatenejad, W. Brooks, A. Schwartz, and J. Craft Pattern of anti-small nuclear ribonucleoprotein antibodies in MRL/Mp-lpr/lpr mice suggests that the intact U1 snRNP particle is their autoimmunogenic target J. Immunol. 152 1994 5523 5531
48. S. Fatenejad, M.J. Mamula, and J. Craft Role of intermolecular/ intrastructural B- and T-cell determinants in the diversification of autoantibodies to ribonucleoprotein particles Proc. Natl. Acad. Sci. U. S. A. 90 1993 12010 12014
49. M.J. Mamula, S. Fatenejad, and J. Craft B cells process and present lupus autoantigens that initiate autoimmune T cell responses J. Immunol. 152 1994 1453 1461
50. J.A. James, T. Gross, R.H. Scofield, and J.B. Harley Immunoglobulin epitope spreading and autoimmune disease after peptide immunization: Sm B/B′-derived PPPGMRPP and PPPGIRGP induce spliceosome autoimmunity J. Exp. Med. 181 1995 453 461
51. J.A. James, and J.B. Harley A model of peptide-induced lupus autoimmune B cell epitope spreading is strain specific and is not H-2 restricted in mice J. Immunol. 160 1998 502 508
52. S. Fatenejad, M. Bennett, J. Moslehi, and J. Craft Influence of antigen organization on the development of lupus autoantibodies Arthritis Rheum. 41 1998 603 612
53. L.J. Mason, L.M. Timothy, D.A. Isenberg, and J.K. Kalsi Immunization with a peptide of Sm B/B′ results in limited epitope spreading but not autoimmune disease J. Immunol. 162 1999 5099 5105
54. F. Monneaux, and S. Muller Key sequences involved in the spreading of the systemic autoimmune response to spliceosomal proteins Scand. J. Immunol. 54 2001 45 54
55. U.S. Deshmukh, C.C. Kannapell, and S.M. Fu Immune responses to small nuclear ribonucleoproteins: antigen-dependent distinct B cell epitope spreading patterns in mice immunized with recombinant polypeptides of small nuclear ribonucleoproteins J. Immunol. 168 2002 5326 5332
56. L.K. Bockenstedt, R.J. Gee, and M.J. Mamula Self-peptides in the initiation of lupus autoimmunity J. Immunol. 154 1995 3516 3524
57. U.S. Deshmukh, F. Gaskin, J.E. Lewis, C.C. Kannapell, and S.M. Fu Mechanisms of autoantibody diversification to SLE-related autoantigens Ann. N. Y. Acad. Sci. 987 2003 91 98
58. H. Bagavant, U.S. Deshmukh, F. Gaskin, and S.M. Fu Lupus glomerulonephritis revisited 2004: autoimmunity and end-organ damage Scand. J. Immunol. 60 2004 52 63
59. E. Koren, M. Koscec, M. Wolfson-Reichlin, F.M. Ebling, B. Tsao, B.H. Hahn, and M. Reichlin Murine and human antibodies to native DNA that cross-react with the A and D SnRNP polypeptides cause direct injury of cultured kidney cells J. Immunol. 154 1995 4857 4864
60. S.X. Deng, E. Hanson, and I. Sanz In vivo cell penetration and intracellular transport of anti-Sm and anti-La autoantibodies Int. Immunol. 12 2000 415 423
61. M.T. McClain, L.D. Heinlen, G.J. Dennis, J. Roebuck, J.B. Harley, and J.A. James Early events in lupus humoral autoimmunity suggest initiation through molecular mimicry Nat. Med. 11 2005 85 89
62. H.A. Doyle, R.J. Gee, and M.J. Mamula A failure to repair self-proteins leads to T cell hyperproliferation and autoantibody production J. Immunol. 171 2003 2840 2847
63. M.J. Mamula, R.J. Gee, J.I. Elliott, A. Sette, S. Southwood, P.J. Jones, and P.R. Blier Isoaspartyl post-translational modification triggers autoimmune responses to self-proteins J. Biol. Chem. 274 1999 22321 22327
64. M.J. Shlomchik, J.E. Craft, and M.J. Mamula From T to B and back again: positive feedback in systemic autoimmune disease Nat. Rev., Immunol. 1 2001 147 153
65. J. Craft, and S. Fatenejad Self antigens and epitope spreading in systemic autoimmunity Arthritis Rheum. 40 1997 1374 1382
66. M.J. Mamula Epitope spreading: the role of self peptides and autoantigen processing by B lymphocytes Immunol. Rev. 164 1998 231 239
67. S. Shinde, R. Gee, S. Santulli-Marotto, L.K. Bockenstedt, S.H. Clarke, and M.J. Mamula T cell autoimmunity in Ig transgenic mice J. Immunol. 162 1999 7519 7524
68. J. Yan, and M.J. Mamula B and T cell tolerance and autoimmunity in autoantibody transgenic mice Int. Immunol. 14 2002 963 971
69. 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
70. C.L. Keech, A.D. Farris, D. Beroukas, T.P. Gordon, and J. McCluskey Cognate T cell help is sufficient to trigger anti-nuclear autoantibodies in naive mice J. Immunol. 166 2001 5826 5834
71. A. Yada, S. Ebihara, K. Matsumura, S. Endo, T. Maeda, A. Nakamura, K. Akiyama, S. Aiba, and T. Takai Accelerated antigen presentation and elicitation of humoral response in vivo by Fc[gamma]RIIB- and Fc[gamma]RI/III-mediated immune complex uptake Cell. Immunol. 225 2003 21
72. R.A. Eisenberg, D.S. Pisetsky, S.Y. Craven, J.P. Grudier, M.A. O'Donnell, and P.L. Cohen Regulation of the anti-Sm autoantibody response in systemic lupus erythematosus mice by monoclonal anti-Sm antibodies J. Clin. Invest. 85 1990 86 92
73. M. Houdayer, J.P. Bouvet, A. Wolff, C. Magnac, J.C. Guillemot, L. Borche, and G. Dighiero Simultaneous presence, in one serum, of four monoclonal antibodies that might correspond to different steps in a clonal evolution from polyreactive to monoreactive antibodies J. Immunol. 150 1993 311 319
74. M. Okawa-Takatsuji, S. Aotsuka, S. Uwatoko, M. Takaono, K. Iwasaki, M. Kinoshita, and M. Sumiya Endothelial cell-binding activity of anti-U1-ribonucleoprotein antibodies in patients with connective tissue diseases Clin. Exp. Immunol. 126 2001 345 354
75. M. Okawa-Takatsuji, S. Aotsuka, S. Uwatoko, M. Kinoshita, and M. Sumiya Increase of cytokine production by pulmonary artery endothelial cells induced by supernatants from monocytes stimulated with autoantibodies against U1-ribonucleoprotein Clin. Exp. Rheumatol. 17 1999 705 712
76. M. Okawa-Takatsuji, S. Aotsuka, M. Fujinami, S. Uwatoko, M. Kinoshita, and M. Sumiya Up-regulation of intercellular adhesion molecule-1 (ICAM-1), endothelial leucocyte adhesion molecule-1 (ELAM-1) and class II MHC molecules on pulmonary artery endothelial cells by antibodies against U1-ribonucleoprotein Clin. Exp. Immunol. 116 1999 174 180
77. J.L. Suen, Y.H. Chuang, and B.L. Chiang In vivo tolerance breakdown with dendritic cells pulsed with U1A protein in non-autoimmune mice: the induction of a high level of autoantibodies but not renal pathological changes Immunology 106 2002 326 335
78. G. Riemekasten, A. Kawald, C. Weiss, A. Meine, J. Marell, R. Klein, B. Hocher, C. Meisel, G. Hausdorf, R. Manz, T. Kamradt, G.R. Burmester, and F. Hiepe Strong acceleration of murine lupus by injection of the SmD1(83-119) peptide Arthritis Rheum. 44 2001 2435 2445