B cell epitope spreading: Mechanisms and contribution to autoimmune diseases

Immunology Letters

Volumn 163, Issue 1, 2015, Pages 56-68

  Cornaby, Caleb ^a   Gibbons, Lauren ^a   Mayhew, Vera ^a   Sloan, Chad S ^a   Welling, Andrew ^a   Poole, Brian D ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

Antibodies; Autoimmune disease; B cells; Epitope spreading

Indexed keywords

ABATACEPT; ADALIMUMAB; ATACICEPT; BELIMUMAB; BLISIBIMOD; CATHEPSIN; EPITOPE; EPRATUZUMAB; GAMMA INTERFERON INDUCIBLE LYSOSOMAL THIOL REDUCTASE; LYSOSOME ENZYME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OCRELIZUMAB; PROTEINASE; RITUXIMAB; TABALUMAB; UNCLASSIFIED DRUG;

ANTIBODY AFFINITY; ANTIGEN PRESENTATION; ARTICLE; AUTOIMMUNE DISEASE; B CELL EPITOPE SPREADING; BULLOUS PEMPHIGOID; CARDIOMYOPATHY; CELL SPREADING; CLINICAL TRIAL (TOPIC); CROSS REACTION; DISEASE COURSE; ENDOCYTOSIS; GRAVES DISEASE; HEYMANN NEPHRITIS; HUMAN; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; INTERMOLECULAR EPITOPE SPREADING; INTRACELLULAR SIGNALING; INTRAMOLECULAR EPITOPE SPREADING; MOLECULAR MIMICRY; MULTICENTER STUDY (TOPIC); MULTIPLE SCLEROSIS; NONHUMAN; PATHOGEN CLEARANCE; PATHOGENESIS; PEMPHIGUS; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); RHEUMATOID ARTHRITIS; SCLERODERMA; SJOEGREN SYNDROME; SOMATIC HYPERMUTATION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; AUTOIMMUNE DISEASES; B LYMPHOCYTE; IMMUNOLOGY; PATHOLOGY; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; ENDOCYTOSIS; EPITOPES, B-LYMPHOCYTE; HUMANS; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; T-LYMPHOCYTES;

EID: 84913582710     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2014.11.001     Document Type: Review

References (129)

1. McCluskey J., Farris A.D., Keech C.L., Purcell A.W., Rischmueller M., Kinoshita G., et al. Determinant spreading: lessons from animal models and human disease. Immunol Rev 1998, 164:209-229.
2. Vanderlugt C.L., Miller S.D. Epitope spreading in immune-mediated diseases: implications for immunotherapy. Nat Rev Immunol 2002, 2:85-95.
3. Steinman L. Multiple sclerosis. Presenting an odd autoantigen. Nature 1995, 375:739-740.
4. Bernard C.C., Johns T.G., Slavin A., Ichikawa M., Ewing C., Liu J., et al. Myelin oligodendrocyte glycoprotein: a novel candidate autoantigen in multiple sclerosis. J Mol Med 1997, 75:77-88.
5. Vanderlugt C.J., Miller S.D. Epitope spreading. Curr Opin Immunol 1996, 8:831-836.
6. Thrasyvoulides A., Lymberi P. Evidence for intramolecular B-cell epitope spreading during experimental immunization with an immunogenic thyroglobulin peptide. Clin Exp Immunol 2003, 132:401-407.
7. Deshmukh U.S., Bagavant H., Sim D., Pidiyar V., Fu S.M. A SmD peptide induces better antibody responses to other proteins within the small nuclear ribonucleoprotein complex than to SmD protein via intermolecular epitope spreading. J Immunol 2007, 178:2565-2571.
8. Kurien B.T., Scofield R.H. Autoimmunity and oxidatively modified autoantigens. Autoimmun Rev 2008, 7:567-573.
9. Deshmukh U.S., Bagavant H., Lewis J., Gaskin F., Fu S.M. Epitope spreading within lupus-associated ribonucleoprotein antigens. Clin Immunol 2005, 117:112-120.
10. Fatenejad S., Mamula M.J., Craft J. Role of intermolecular/intrastructural B- and T-cell determinants in the diversification of autoantibodies to ribonucleoprotein particles. Proc Natl Acad Sci U S A 1993, 90:12010-12014.
11. Singh R.R. Prevention and control of reciprocal T-B cell diversification: implications for lupus-like autoimmunity. Mol Immunol 2004, 40:1137-1145.
12. Poole B.D., Gross T., Maier S., Harley J.B., James J.A. Lupus-like autoantibody development in rabbits and mice after immunization with EBNA-1 fragments. J Autoimmun 2008, 31:362-371.
13. Maeda J.Y., Moura A.K., Maruta C.W., Santi C.G., Prisayanh P.S., Aoki V. Changes in the autoimmune blistering response: a clinical and immunopathological shift from pemphigus foliaceus to bullous pemphigoid. Clin Exp Dermatol 2006, 31:653-655.
14. Peterson J.D., Chang A.J., Chan L.S. Clinical evidence of an intermolecular epitope spreading in a patient with pemphigus foliaceus converting into bullous pemphigoid. Arch Dermatol 2007, 143:272-274.
15. Milich D.R., McLachlan A., Thornton G.B., Hughes J.L. Antibody production to the nucleocapsid and envelope of the hepatitis B virus primed by a single synthetic T cell site. Nature 1987, 329:547-549.
16. Craft J., Fatenejad S. Self antigens and epitope spreading in systemic autoimmunity. Arthritis Rheum 1997, 40:1374-1382.
17. Datta S.K., Kaliyaperumal A., Desai-Mehta A. T cells of lupus and molecular targets for immunotherapy. J Clin Immunol 1997, 17:11-20.
18. Li N., Aoki V., Hans-Filho G., Rivitti E.A., Diaz L.A. The role of intramolecular epitope spreading in the pathogenesis of endemic pemphigus foliaceus (fogo selvagem). J Exp Med 2003, 197:1501-1510.
19. Poole B.D., Schneider R.I., Guthridge J.M., Velte C.A., Reichlin M., Harley J.B., et al. Early targets of nuclear RNP humoral autoimmunity in human systemic lupus erythematosus. Arthritis Rheum 2009, 60:848-859.
20. Leech S. Molecular mimicry in autoimmune disease. Arch Dis Childhood 1998, 79:448-451.
21. Cusick M.F., Libbey J.E., Fujinami R.S. Molecular mimicry as a mechanism of autoimmune disease. Clin Rev Allergy Immunol 2012, 42:102-111.
22. Ohtaki A., Kieber-Emmons T., Murali R. Structure-based peptide mimicry of tumor-associated antigens. Monoclon Antibod Immunodiagn Immunother 2013, 32:1-5.
23. Fields B.A., Goldbaum F.A., Ysern X., Poljak R.J., Mariuzza R.A. Molecular basis of antigen mimicry by an anti-idiotope. Nature 1995, 374:739-742.
24. Braden B.C., Fields B.A., Ysern X., Dall'Acqua W., Goldbaum F.A., Poljak R.J., et al. Crystal structure of an Fv-Fv idiotope-anti-idiotope complex at 1.9 A resolution. J Mol Biol 1996, 264:137-151.
25. Poole B.D., Scofield R.H., Harley J.B., James J.A. Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity 2006, 39:63-70.
26. Amigorena S., Bonnerot C. Fc receptor signaling and trafficking: a connection for antigen processing. Immunol Rev 1999, 172:279-284.
27. Amigorena S., Bonnerot C. Fc receptors for IgG and antigen presentation on MHC class I and class II molecules. Semin Immunol 1999, 11:385-390.
28. Binder M., Muller F., Jackst A., Lechenne B., Pantic M., Bacher U., et al. B-cell receptor epitope recognition correlates with the clinical course of chronic lymphocytic leukemia. Cancer 2011, 117:1891-1900.
29. Watts C. Capture and processing of exogenous antigens for presentation on MHC molecules. Annu Rev Immunol 1997, 15:821-850.
30. McGovern E.M., Moquin A.E., Caballero A., Drake J.R. The effect of B cell receptor signaling on antigen endocytosis and processing. Immunol investig 2004, 33:143-156.
31. Lankar D., Vincent-Schneider H., Briken V., Yokozeki T., Raposo G., Bonnerot C. Dynamics of major histocompatibility complex class II compartments during B cell receptor-mediated cell activation. J Exp Med 2002, 195:461-472.
32. Aluvihare V.R., Khamlichi A.A., Williams G.T., Adorini L., Neuberger M.S. Acceleration of intracellular targeting of antigen by the B-cell antigen receptor: importance depends on the nature of the antigen-antibody interaction. EMBO J 1997, 16:3553-3562.
33. Amigorena S., Bonnerot C. Role of B-cell and Fc receptors in the selection of T-cell epitopes. Curr Opin Immunol 1998, 10:88-92.
34. Bonnerot C., Lankar D., Hanau D., et al. Role of B cell receptor Ig alpha and Ig beta subunits in MHC class II-restricted antigen presentation. Immunity 1995, 3:335-347.
35. Lennon-Dumenil A.M., Bakker A.H., Wolf-Bryant P., Ploegh H.L., Lagaudriere-Gesbert C. A closer look at proteolysis and MHC-class-II-restricted antigen presentation. Curr Opin Immunol 2002, 14:15-21.
36. Fiebiger E., Meraner P., Weber E., Fang I.F., Stingl G., Ploegh H., et al. Cytokines regulate proteolysis in major histocompatibility complex class II-dependent antigen presentation by dendritic cells. J Exp Med 2001, 193:881-892.
37. Drakesmith H., O'Neil D., Schneider S.C., Binks M., Medd P., Sercarz E., et al. In vivo priming of T cells against cryptic determinants by dendritic cells exposed to interleukin 6 and native antigen. Proc Natl Acad Sci U S A 1998, 95:14903-14908.
38. Rammensee H.G. Chemistry of peptides associated with MHC class I and class II molecules. Curr Opin Immunol 1995, 7:85-96.
39. Escola J.M., Grivel J.C., Chavrier P., Gorvel J.P. Different endocytic compartments are involved in the tight association of class II molecules with processed hen egg lysozyme and ribonuclease A in B cells. J Cell Sci 1995, 108(Pt 6):2337-2345.
40. Griffin J.P., Chu R., Harding C.V. Early endosomes and a late endocytic compartment generate different peptide-class II MHC complexes via distinct processing mechanisms. J Immunol 1997, 158:1523-1532.
41. Clark H.L., Banks R., Jones L., et al. Characterization of MHC-II antigen presentation by B cells and monocytes from older individuals. Clin Immunol 2012, 144:172-177.
42. Lindner R., Unanue E.R. Distinct antigen MHC class II complexes generated by separate processing pathways. EMBO J 1996, 15:6910-6920.
43. Lake P., Mitchison N.A. Regulatory mechanisms in the immune response to cell-surface antigens. Cold Spring Harbor Symp Quantitat Biol 1977, 41(Pt 2):589-595.
44. Di Noia J.M., Neuberger M.S. Molecular mechanisms of antibody somatic hypermutation. Annu Rev Biochem 2007, 76:1-22.
45. Ray S.K., Putterman C., Diamond B. Pathogenic autoantibodies are routinely generated during the response to foreign antigen: a paradigm for autoimmune disease. Proc Natl Acad Sci U S A 1996, 93:2019-2024.
46. Sokolove J., Bromberg R., Deane K.D., et al. Autoantibody epitope spreading in the pre-clinical phase predicts progression to rheumatoid arthritis. PLoS ONE 2012, 7:e35296.
47. Schellekens G.A., de Jong B.A., van den Hoogen F.H., van de Putte L.B., van Venrooij W.J. Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies. J Clin Invest 1998, 101:273-281.
48. McInnes I.B., Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011, 365:2205-2219.
49. Nielen M.M., van Schaardenburg D., Reesink H.W., van de Stadt R.J., van der Horst-Bruinsma I.E., de Koning M.H., et al. Specific autoantibodies precede the symptoms of rheumatoid arthritis: a study of serial measurements in blood donors. Arthritis Rheum 2004, 50:380-386.
50. Rantapaa-Dahlqvist S., de Jong B.A., Berglin E., Hallmans G., Wadell G., Stenlund H., et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum 2003, 48:2741-2749.
51. Snir O., Widhe M., von Spee C., Lindberg J., Padyukov L., Lundberg K., et al. Multiple antibody reactivities to citrullinated antigens in sera from patients with rheumatoid arthritis: association with HLA-DRB1 alleles. Ann Rheum Dis 2009, 68:736-743.
52. Kidd B.A., Ho P.P., Sharpe O., Zhao X., Tomooka B.H., Kanter J.L., et al. Epitope spreading to citrullinated antigens in mouse models of autoimmune arthritis and demyelination. Arthritis Res Ther 2008, 10:R119.
53. Prasad S., Kohm A.P., McMahon J.S., Luo X., Miller S.D. Pathogenesis of NOD diabetes is initiated by reactivity to the insulin B chain 9-23 epitope and involves functional epitope spreading. J Autoimmun 2012, 39:347-353.
54. Tian J., Zekzer D., Lu Y., Dang H., Kaufman D.L. B cells are crucial for determinant spreading of T cell autoimmunity among beta cell antigens in diabetes-prone nonobese diabetic mice. J Immunol 2006, 176:2654-2661.
55. Serreze D.V., Leiter E.H., Kuff E.L., Jardieu P., Ishizaka K. Molecular mimicry between insulin and retroviral antigen p73. Development of cross-reactive autoantibodies in sera of NOD and C57BL/KsJ db/db mice. Diabetes 1988, 37:351-358.
56. Brooks-Worrell B., Gersuk V.H., Greenbaum C., Palmer J.P. Intermolecular antigen spreading occurs during the preclinical period of human type 1 diabetes. J Immunol 2001, 166:5265-5270.
57. Hemmer B., Nessler S., Zhou D., Kieseier B., Hartung H.P. Immunopathogenesis and immunotherapy of multiple sclerosis. Nat Clin Pract Neurol 2006, 2:201-211.
58. Cao L., Sun D., Whitaker J.N. Citrullinated myelin basic protein induces experimental autoimmune encephalomyelitis in Lewis rats through a diverse T cell repertoire. J Neuroimmunol 1998, 88:21-29.
59. Kuerten S., Schickel A., Kerkloh C., Recks M.S., Addicks K., Ruddle N.H., et al. Tertiary lymphoid organ development coincides with determinant spreading of the myelin-specific T cell response. Acta Neuropathol 2012, 124:861-873.
60. Pollinger B., Krishnamoorthy G., Berer K., Lassmann H., Bosl M.R., Dunn R., et al. Spontaneous relapsing-remitting EAE in the SJL/J mouse: MOG-reactive transgenic T cells recruit endogenous MOG-specific B cells. J Exp Med 2009, 206:1303-1316.
61. Lehmann P.V., Forsthuber T., Miller A., Sercarz E.E. Spreading of T-cell autoimmunity to cryptic determinants of an autoantigen. Nature 1992, 358:155-157.
62. Miller S.D., Vanderlugt C.L., Begolka W.S., et al. Persistent infection with Theiler's virus leads to CNS autoimmunity via epitope spreading. Nat Med 1997, 3:1133-1136.
63. Klippel J.H., Weyand C.M., Wortmann R.L. Primer on the rheumatic diseases 1997, Arthritis Foundation, Atlanta, Georgia.
64. Taylor K.E., Chung S.A., Graham R.R., Ortmann W.A., Lee A.T., Langefeld C.D., et al. Risk alleles for systemic lupus erythematosus in a large case-control collection and associations with clinical subphenotypes. PLoS Genet 2011, 7:e1001311.
65. Arbuckle M.R., McClain M.T., Rubertone M.V., Scofield R.H., Dennis G.J., James J.A., et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N Engl J Med 2003, 349:1526-1533.
66. Deshmukh U.S., Kannapell C.C., Fu S.M. 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 2002, 168:5326-5332.
67. van Bavel C.C., Dieker J.W., Tamboer W.P., van der Vlag J., Berden J.H. Lupus-derived monoclonal autoantibodies against apoptotic chromatin recognize acetylated conformational epitopes. Mol Immunol 2010, 48:248-256.
68. Scofield R.H., Kurien B.T., Ganick S., McClain M.T., Pye Q., James J.A., et al. Modification of lupus-associated 60-kDa Ro protein with the lipid oxidation product 4-hydroxy-2-nonenal increases antigenicity and facilitates epitope spreading. Free Radical Biol Med 2005, 38:719-728.
69. Kurien B.T., Dsouza A., Igoe A., Lee Y.J., Maier-Moore J.S., Gordon T., et al. Immunization with 60kD Ro peptide produces different stages of preclinical autoimmunity in a Sjogren's syndrome model among multiple strains of inbred mice. Clin Exp Immunol 2013, 173:67-75.
70. Kivity S., Arango M.T., Ehrenfeld M., Tehori O., Shoenfeld Y., Anaya J.M., et al. Infection and autoimmunity in Sjogren's syndrome: a clinical study and comprehensive review. J Autoimmun 2014, 51:17-22. 10.1016/j.jaut.2014.02.008.
71. Scofield R.H., Asfa S., Obeso D., Jonsson R., Kurien B.T. 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 2005, 175:8409-8414.
72. Gottenberg J.E., Busson M., Loiseau P., Cohen-Solal J., Lepage V., Charron D., et al. In primary Sjogren's syndrome, HLA class II is associated exclusively with autoantibody production and spreading of the autoimmune response. Arthritis Rheum 2003, 48:2240-2245.
73. Paisansinsup T., Deshmukh U.S., Chowdhary V.R., Luthra H.S., Fu S.M., David C.S. 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 2002, 168:5876-5884.
74. Routsias J.G., Kyriakidis N., Latreille M., Tzioufas A.G. RNA recognition motif (RRM) of La/SSB: the bridge for interparticle spreading of autoimmune response to U1-RNP. Mol Med 2010, 16:19-26.
75. Prabhakar B.S., Bahn R.S., Smith T.J. Current perspective on the pathogenesis of Graves' disease and ophthalmopathy. Endocrine Rev 2003, 24:802-835.
76. Genovese B.M., Noureldine S.I., Gleeson E.M., Tufano R.P., Kandil E. What is the best definitive treatment for Graves' disease? A systematic review of the existing literature. Ann Surg Oncol 2013, 20:660-667.
77. Lazarus J.H. Epidemiology of Graves' orbitopathy (GO) and relationship with thyroid disease. Best Pract Res Clin Endocrinol Metab 2012, 26:273-279.
78. Vlase H., Nakashima M., Graves P.N., Tomer Y., Morris J.C., Davies T.F. Defining the major antibody epitopes on the human thyrotropin receptor in immunized mice: evidence for intramolecular epitope spreading. Endocrinology 1995, 136:4415-4423.
79. Schwarz-Lauer L., Pichurin P.N., Chen C.R., Nagayama Y., Paras C., Morris J.C., et al. The cysteine-rich amino terminus of the thyrotropin receptor is the immunodominant linear antibody epitope in mice immunized using naked deoxyribonucleic acid or adenovirus vectors. Endocrinology 2003, 144:1718-1725.
80. Inaba H., Pan D., Shin Y.H., Martin W., Buchman G., De Groot L.J. Immune response of mice transgenic for human histocompatibility leukocyte Antigen-DR to human thyrotropin receptor-extracellular domain. Thyroid 2009, 19:1271-1280.
81. Inaba H., Moise L., Martin W., et al. Epitope recognition in HLA-DR3 transgenic mice immunized to TSH-R protein or peptides. Endocrinology 2013, 154:2234-2243.
82. Chung L., Utz P.J. Antibodies in scleroderma: direct pathogenicity and phenotypic associations. Curr Rheumatol Rep 2004, 6:156-163.
83. Henry P.A., Atamas S.P., Yurovsky V.V., Luzina I., Wigley F.M., White B. Diversity and plasticity of the anti-DNA topoisomerase I autoantibody response in scleroderma. Arthritis Rheum 2000, 43:2733-2742.
84. Asano Y., Ihn H., Yamane K., Kubo M., Tamaki K. The prevalence and clinical significance of anti-U1 RNA antibodies in patients with systemic sclerosis. J Investig Dermatol 2003, 120:204-210.
85. Gavanescu I., Vazquez-Abad D., McCauley J., Senecal J.L., Doxsey S. Centrosome proteins: a major class of autoantigens in scleroderma. J Clin Immunol 1999, 19:166-171.
86. Rose N.R. Myocarditis: infection versus autoimmunity. J Clin Immunol 2009, 29:730-737.
87. Neumann D.A., Burek C.L., Baughman K.L., Rose N.R., Herskowitz A. Circulating heart-reactive antibodies in patients with myocarditis or cardiomyopathy. J Am Coll Cardiol 1990, 16:839-846.
88. Caforio A.L., Marcolongo R., Jahns R., Fu M., Felix S.B., Iliceto S. Immune-mediated and autoimmune myocarditis: clinical presentation, diagnosis and management. Heart Failure Rev 2013, 18:715-732.
89. Nishimura H., Okazaki T., Tanaka Y., Nakatani K., Hara M., Matsumori A., et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001, 291:319-322.
90. Caforio A.L., Mahon N.G., Baig M.K., Tona F., Murphy R.T., Elliott P.M., et al. Prospective familial assessment in dilated cardiomyopathy: cardiac autoantibodies predict disease development in asymptomatic relatives. Circulation 2007, 115:76-83.
91. Matsumoto Y., Park I.K., Kohyama K. B-cell epitope spreading is a critical step for the switch from C-protein-induced myocarditis to dilated cardiomyopathy. Am J Pathol 2007, 170:43-51.
92. Salant D.J., Quigg R.J., Cybulsky A.V. Heymann nephritis: mechanisms of renal injury. Kidney Int 1989, 35:976-984.
93. Raychowdhury R., Niles J.L., McCluskey R.T., Smith J.A. Autoimmune target in Heymann nephritis is a glycoprotein with homology to the LDL receptor. Science 1989, 244:1163-1165.
94. Shah P., Tramontano A., Makker S.P. Intramolecular epitope spreading in Heymann nephritis. J Am Soc Nephrol 2007, 18:3060-3066.
95. Farquhar M.G., Saito A., Kerjaschki D., Orlando R.A. The Heymann nephritis antigenic complex: megalin (gp330) and RAP. J Am Soc Nephrol 1995, 6:35-47.
96. Wang Y., Wang Y.M., Wang Y., Zheng G., Zhang G.Y., Zhou J.J., et al. DNA vaccine encoding CD40 targeted to dendritic cells in situ prevents the development of Heymann nephritis in rats. Kidney Int 2013, 83:223-232.
97. Wu H., Walters G., Knight J.F., Alexander S.I. DNA vaccination against specific pathogenic TCRs reduces proteinuria in active Heymann nephritis by inducing specific autoantibodies. J Immunol 2003, 171:4824-4829.
98. Galichet A., Borradori L., Muller E.J. A new light on an old disease: adhesion signaling in pemphigus vulgaris. J Investig Dermatol 2014, 134:8-10.
99. Groves R.W. Pemphigus: a brief review. Clin Med 2009, 9:371-375.
100. Salato V.K., Hacker-Foegen M.K., Lazarova Z., Fairley J.A., Lin M.S. Role of intramolecular epitope spreading in pemphigus vulgaris. Clin Immunol 2005, 116:54-64.
101. Bowen G.M., Peters N.T., Fivenson D.P., Su L.D., Nousari H.C., Anhalt G.J., et al. Lichenoid dermatitis in paraneoplastic pemphigus: a pathogenic trigger of epitope spreading?. Arch Dermatol 2000, 136:652-656.
102. Chan L.S. Epitope spreading in paraneoplastic pemphigus: autoimmune induction in antibody-mediated blistering skin diseases. Arch Dermatol 2000, 136:663-664.
103. Stanley J.R., Hawley-Nelson P., Yuspa S.H., Shevach E.M., Katz S.I. Characterization of bullous pemphigoid antigen: a unique basement membrane protein of stratified squamous epithelia. Cell 1981, 24:897-903.
104. Chan L.S., Vanderlugt C.J., Hashimoto T., Nishikawa T., Zone J.J., Black M.M., et al. Epitope spreading: lessons from autoimmune skin diseases. J Investig Dermatol 1998, 110:103-109.
105. Schmidt E., Zillikens D. Pemphigoid diseases. Lancet 2013, 381:320-332.
106. Kershenovich R., Hodak E., Mimouni D. Diagnosis and classification of pemphigus and bullous pemphigoid. Autoimmun Rev 2014, 13:477-481.
107. Walmsley N., Hampton P. Bullous pemphigoid triggered by swine flu vaccination: case report and review of vaccine triggered pemphigoid. J Dermatol Case Rep 2011, 5:74-76.
108. Di Zenzo G., Thoma-Uszynski S., Calabresi V., Fontao L., Hofmann S.C., Lacour J.P., et al. Demonstration of epitope-spreading phenomena in bullous pemphigoid: results of a prospective multicenter study. J Investig Dermatol 2011, 131:2271-2280.
109. Fairley J.A., Woodley D.T., Chen M., Giudice G.J., Lin M.S. A patient with both bullous pemphigoid and epidermolysis bullosa acquisita: an example of intermolecular epitope spreading. J Am Acad Dermatol 2004, 51:118-122.
110. Recke A., Rose C., Schmidt E., Brocker E.B., Zillikens D., Sitaru C. Transition from pemphigus foliaceus to bullous pemphigoid: intermolecular B-cell epitope spreading without IgG subclass shifting. J Am Acad Dermatol 2009, 61:333-336.
111. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 2008, 358:676-688.
112. Lichtman E.I., Helfgott S.M., Kriegel M.A. Emerging therapies for systemic lupus erythematosus - focus on targeting interferon-alpha. Clin Immunol 2012, 143:210-221.
113. Dreyfus D.H. Autoimmune disease: a role for new anti-viral therapies?. Autoimmun Rev 2011, 11:88-97.
114. Leshem Y.A., David M., Hodak E., Waitman D.A., Vardy D., Israeli M., et al. A prospective study on clinical response and cell-mediated immunity of pemphigus patients treated with rituximab. Arch Dermatol Res 2014, 306:67-74.
115. Leandro M.J., Cambridge G., Edwards J.C., Ehrenstein M.R., Isenberg D.A. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology (Oxford) 2005, 44:1542-1545.
116. Bekar K.W., Owen T., Dunn R., Ichikawa T., Wang W., Wang R., et al. Prolonged effects of short-term anti-CD20 B cell depletion therapy in murine systemic lupus erythematosus. Arthritis Rheum 2010, 62:2443-2457.
117. Kamal A. The efficacy of novel B cell biologics as the future of SLE treatment: a review. Autoimmun Rev 2014.
118. Looney R.J., Anolik J.H., Campbell D., et al. B cell depletion as a novel treatment for systemic lupus erythematosus: a phase I/II dose-escalation trial of rituximab. Arthritis Rheum 2004, 50:2580-2589.
119. La Cava A. Targeting B cells with biologics in systemic lupus erythematosus. Exp Opin Biol Ther 2010, 10:1555-1561.
120. Furie R., Petri M., Zamani O., et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum 2011, 63:3918-3930.
121. Furie R.A., Leon G., Thomas M., Petri M.A., Chu A.D., Hislop C., et al. A phase 2, randomised, placebo-controlled clinical trial of blisibimod, an inhibitor of B cell activating factor, in patients with moderate-to-severe systemic lupus erythematosus, the PEARL-SC study. Ann Rheum Dis 2014, 10.1136/annrheumdis-2013-205144.
122. Isenberg D., Gordon C., Licu D., Copt S., Rossi C.P., Wofsy D. Efficacy and safety of atacicept for prevention of flares in patients with moderate-to-severe systemic lupus erythematosus (SLE): 52-week data (APRIL-SLE randomised trial). Ann Rheum Dis 2014, pii:annrheumdis-2013-205067.
123. Genovese M.C., Kinnman N., de La Bourdonnaye G., Pena Rossi C., Tak P.P. Atacicept in patients with rheumatoid arthritis and an inadequate response to tumor necrosis factor antagonist therapy: results of a phase II, randomized, placebo-controlled, dose-finding trial. Arthritis Rheum 2011, 63:1793-1803.
124. Kappos L., Hartung H.P., Freedman M.S., Boyko A., Radu E.W., Mikol D.D., et al. Atacicept in multiple sclerosis (ATAMS): a randomised, placebo-controlled, double-blind, phase 2 trial. Lancet Neurol 2014, 13:353-363.
125. Weinblatt M.E., Schiff M., Valente R., van der Heijde D., Citera G., Zhao C., et al. Head-to-head comparison of subcutaneous abatacept versus adalimumab for rheumatoid arthritis: findings of a phase IIIb, multinational, prospective, randomized study. Arthritis Rheum 2013, 65:28-38.
126. Merrill J.T., Burgos-Vargas R., Westhovens R., Chalmers A., D'Cruz D., Wallace D.J., et al. The efficacy and safety of abatacept in patients with non-life-threatening manifestations of systemic lupus erythematosus: results of a twelve-month, multicenter, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum 2010, 62:3077-3087.
127. Mease P., Genovese M.C., Gladstein G., Kivitz A.J., Ritchlin C., Tak P.P., et al. Abatacept in the treatment of patients with psoriatic arthritis: results of a six-month, multicenter, randomized, double-blind, placebo-controlled, phase II trial. Arthritis Rheum 2011, 63:939-948.
128. Choi J., Kim S.T., Craft J. The pathogenesis of systemic lupus erythematosus - an update. Curr Opin Immunol 2012, 24:651-657.
129. Hashimoto T., Tsuruta D., Dainichi T., Hamada T., Furumura M., Ishii N. Demonstration of epitope spreading in bullous pemphigoid: results of a prospective multicenter study. J Investig Dermatol 2011, 131:2175-2177.