B-lymphocyte depletion reduces skin fibrosis and autoimmunity in the tight-skin mouse model for systemic sclerosis

American Journal of Pathology

Volumn 169, Issue 3, 2006, Pages 954-966

  Hasegawa, Minoru ^a   Hamaguchi, Yasuhito ^c   Yanaba, Koichi ^c   Bouaziz, Jean David ^c   Uchida, Junji ^c   Fujimoto, Manabu ^a   Matsushita, Takashi ^a   Matsushita, Yukiyo ^a   Horikawa, Mayuka ^a   Komura, Kazuhiro ^a   Takehara, Kazuhiko ^a   Sato, Shinichi ^b   Tedder, Thomas F ^a,c  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^b NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIBODY; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; DISEASE COURSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN FIBROSIS; SYSTEMIC SCLEROSIS; TH1 CELL; TH2 CELL;

EID: 33748788266     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.060205     Document Type: Article

References (62)

1. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger Jr TA, Rowell N, Wollheim F: Scleroderma (systemic sclerosis): classification, subsets, and pathogenesis. J Rheumatol 1988, 15:202-205
2. Abraham JD, Varga J: Scleroderma: from cell and molecular mechanisms to disease models. Trends Immunol 2005, 26:587-595
3. Fleischmajer R, Perlish JS, Reeves JRT: Cellular infiltrates in scleroderma skin. Arthritis Rheum 1977, 20:975-984
4. Famularo G, Giacomelli R, Alesse E, Cifone MG, Morrone S, Boirivant M, Danese C, Perego MA, Santoni A, Tonietti G: Polyclonal B lymphocyte activation in progressive systemic sclerosis. J Clin Lab Immunol 1989, 29:59-63
5. Sato S, Fujimoto M, Hasegawa M, Takehara K: Altered blood B lymphocyte homeostasis in systemic sclerosis. Expanded naive B cells and diminished but activated memory B cells. Arthritis Rheum 2004, 50:1918-1927
6. Whitfield ML, Finlay DR, Murray JI, Troyanskaya OG, Chi JT, Pergamenschikov A, McCalmont TH, Brown PO, Botstein D, Connolly MK: Systemic and cell type-specific gene expression patterns in scleroderma skin. Proc Natl Acad Sci USA 2003, 100:12319-12324
7. Steen VD, Powell DL, Medsger Jr TA: Clinical correlations and prognosis based on serum autoantibodies in patients with systemic sclerosis. Arthritis Rheum 1988, 31:196-203
8. Kuwana M, Kaburaki J, Mimori T, Tojo T, Homma M: Antoantibody reactive with three classes of RNA polymerases in sera from patients with systemic sclerosis. J Clin Invest 1993, 91:1399-1404
9. Tan FK, Arnett FC, Antohi S, Saito S, Mirarchi A, Spiera H, Sasaki T, Shoichi O, Takeuchi K, Pandey JP, Silver RM, LeRoy C, Postlethwaite AE, Bona CA: Autoantibodies to the extracellular matrix microfibrillar protein, fibrillin-1, in patients with scleroderma and other connective tissue diseases. J Immunol 1999, 163:1066-1072
10. Zhou X, Tan FK, Milewicz DM, Guo X, Bona CA, Arnett FC: Autoantibodies to fibrillin-1 activate normal human fibroblasts in culture through the TGF-pathway to recapitulate the "scleroderma phenotype." J Immunol 2005, 175:4555-4560
11. Sato S, Hasegawa M, Fujimoto M, Tedder TF, Takehara K: Quantitative genetic variation in CD19 expression correlates with autoimmunity in mice and humans. J Immunol 2000, 165:6635-6643
12. Tsuchiya N, Kuroki K, Fujimoto M, Murakami Y, Tedder TF, Tokunaga K, Takehara K, Sato S: Association of a functional CD19 polymorphism with susceptibility to systemic sclerosis (scleroderma). Arthritis Rheum 2004, 50:4002-4007
13. Tedder TF, Poe JC, Fujimoto M, Haas KM, Sato S: The CD19-CD21 signal transduction complex of B lymphocytes regulates the balance between health and autoimmune disease: systemic sclerosis as a model system. Curr Dir Autoimmunity 2005, 8:55-90
14. Green MC, Sweet HO, Bunker LE: Tight-skin, a new mutation of the mouse causing excessive growth of connective tissue and skeleton. Am J Pathol 1976, 82:493-512
15. Jimenez SA, Williams CJ, Myers JC, Bashey RI: Increased collagen biosynthesis and increased expression of type I and type III procollagen genes in tight skin (TSK) mouse fibroblasts. J Biol Chem 1986, 261:657-662
16. Osborn TG, Bauer NE, Ross SC, Moore TL, Zucker J: The tight-skin mouse: physical and biochemical properties of the skin. J Rheumatol 1983, 10:793-796
17. Siracusa LD, McGrath R, Ma Q, Moskow JJ, Manne J, Christner PJ, Buchberg AM, Jimenez SA: A tandem duplication within the fibrillin 1 gene is associated with the mouse tight skin mutation. Genome Res 1996, 6:300-313
18. Kasturi KN, Hatakeyama A, Murai C, Gordon R, Phelps RG, Bona CA: B-cell deficiency does not abrogate development of cutaneous hyperplasia in mice inheriting the defective fibrillin-1 gene. J Autoimmun 1997, 10:505-517
19. Phelps RG, Murai C, Saito S, Hatakeyama A, Andrikopoulos K, Kasturi KN, Bona CA: Effect of targeted mutation in collagen Vα2 gene on development of cutaneous hyperplasia in tight skin mice. Mol Med 1998, 4:356-360
20. Gayraud B, Keene DR, Sakai LY, Ramirez F: New insights into the assembly of extracellular microfibrils from the analysis of the fibrillin 1 mutation in the tight skin mouse. J Cell Biol 2000, 150:667-680
21. Lemaire R, Korn JH, Schiemann WP, Lafyatis R: Fibulin-2 and fibulin-5 alterations in tsk mice associated with disorganized hypodermal elastic fibers and skin tethering. J Invest Dermatol 2004, 123:1063-1069
22. Phelps RG, Daian C, Shibata S, Fleischmajer R, Bona CA: Induction of skin fibrosis and autoantibodies by infusion of immunocompetent cells from tight skin mice into C57BL/6 Pa/Pa mice. J Autoimmun 1993, 6:701-718
23. + T cells in the pathogenesis of skin fibrosis in tight skin mice. Eur J Immunol 1994, 24:1463-1466
24. Everett ET, Pablos JL, Harley RA, LeRoy EC, Norris JS: The role of mast cells in the development of skin fibrosis in tight-skin mutant mice. Comp Biochem Physiol 1995, 110A: 159-165
25. Bocchieri MH, Christner PJ, Henriksen PD, Jimenez SA: Immunological characterization of (tight skin/NZB)F1 hybrid mice with connective tissue and autoimmune features resembling human systemic sclerosis. J Autoimmun 1993, 6:337-351
26. Walker MA, Harley RA, DeLustro FA, LeRoy EC: Adoptive transfer of Tsk skin fibrosis to +/+ recipients by Tsk bone marrow and spleen cells. Proc Soc Exp Biol Med 1989, 192:196-200
27. Ong CJ, Ip S, Teh S-J, Wong C, Jirik FR, Grusby MJ, Teh HS: A role for T helper 2 cells in mediating skin fibrosis in tight-skin mice. Cell Immunol 1999, 196:60-68
28. McGaha TL, Bona CA: Role of profibrogenic cytokines secreted by T cells in fibrotic processes in scleroderma. Autoimmunity Rev 2002, 1:174-181
29. Shen Y, Ichino M, Nakazawa M, Minami M: CpG oligodeoxynucleotides prevent the development of scleroderma-like syndrome in tight-skin mice by stimulating a Th1 immune response. J Invest Dermatol 2005, 124:1141-1148
30. Tsuji-Yamada J, Nakazawa M, Takahashi K, Iijima K, Hattori S, Okuda K, Minami M, Ikezawa Z, Sasaki T: Effect of IL-12 encoding plasmid administration on tight-skin mouse. Biochem Biophys Res Commun 2001, 280:707-712
31. McGaha TL, Le M, Kodera T, Stoica C, Zhu J, Paul WE, Bona CA: Molecular mechanisms of interleukin-4-induced up-regulation of type I collagen gene expression in murine fibroblasts. Arthritis Rheum 2003, 48:2275-2284
32. McGaha T, Saito S, Phelps RG, Gordon R, Noben-Trauth N, Paul WE, Bona C: Lack of skin fibrosis in tight skin (TSK) mice with targeted mutation in the interleukin-4Rα and transforming growth factor-β genes. J Invest Dermatol 2001, 116:136-143
33. Kodera T, McGaha TL, Phelps R, Paul WE, Bona CA: Disrupting the IL-4 gene rescues mice homozygous for the tight-skin mutation from embryonic death and diminishes TGF-β production by fibroblasts. Proc Natl Acad Sci USA 2002, 99:3800-3805
34. Ong C, Wong C, Roberts CR, Teh HS, Jirik FR: Anti-IL-4 treatment prevents dermal collagen deposition in the tight-skin mouse model of scleroderma. Eur J Immunol 1998, 28:2619-2629
35. Saito E, Fujimoto M, Hasegawa M, Komura K, Hamaguchi Y, Kaburagi Y, Nagaoka T, Takehara K, Tedder TF, Sato S: CD19-dependent B lymphocyte signaling thresholds influence skin fibrosis and autoimmunity in the tight-skin mouse. J Clin Invest 2002, 109:1453-1462
36. Asano N, Fujimoto M, Yazawa N, Shirasawa S, Hasegawa M, Okochi H, Tamaki K, Tedder TF, Sato S: B lymphocyte signaling established by the CD19/CD22 loop regulates autoimmunity in the tight-skin mouse. Am J Pathol 2004, 165:641-650
37. Bona C, Rothfield N: Autoantibodies in scleroderma and tightskin mice. Curr Opin Immunol 1994, 6:931-937
38. Murai C, Saito S, Kasturi KN, Bona CA: Spontaneous occurrence of anti-fibrillin-1 autoantibodies in tight-skin mice. Autoimmunity 1998, 28:151-155
39. Hatakeyama A, Kasturi KN, Wolf I, Phelps RG, Bona CA: Correlation between the concentration of serum anti-topoisomerase I autoantibodies and histological and biochemical alterations in the skin of tight skin mice. Cell Immunol 1996, 167:135-140
40. Edwards JCW, Cambridge G: Prospects for B-cell-targeted therapy in autoimmune disease. Rheumatology 2005, 44:151-156
41. Uchida J, Lee Y, Hasegawa M, Liang Y, Bradney A, Oliver JA, Bowen K, Steeber DA, Haas KM, Poe JC, Tedder TF: Mouse CD20 expression and function. Int Immunol 2004, 16:119-129
42. Uchida J, Hamaguchi Y, Oliver JA, Ravetch JV, Poe JC, Haas KM, Tedder TF: The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 2004, 199:1659-1669
43. Hamaguchi Y, Uchida J, Cain DW, Venturi GM, Poe JC, Haas KM, Tedder TF: The peritoneal cavity provides a protective niche for B1 and conventional B lymphocytes during anti-CD20 immunotherapy in mice. J Immunol 2005, 7:4389-4399
44. Hamaguchi Y, Xiu Y, Komura K, Nimmerjahn F, Tedder TF: Antibody isotype-specific engagement of Fcγ receptors regulates B lymphocyte depletion during CD20 immunotherapy. J Exp Med 2006, 203:743-753
45. Sato S, Ono N, Steeber DA, Pisetsky DS, Tedder TF: CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J Immunol 1996, 157:4371-4378
46. Sato S, Miller AS, Inaoki M, Bock CB, Jansen PJ, Tang MLK, Tedder TF: CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 1996, 5:551-562
47. Engel P, Zhou L-J, Ord DC, Sato S, Koller B, Tedder TF: Abnormal B lymphocyte development, activation and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 1995, 3:39-50
48. Meijerink J, Mandigers C, van de Locht L, Tonnissen E, Goodsaid F, Raemaekers J: A novel method to compensate for different amplification efficiencies between patient DNA samples in quantitative real-time PCR. J Mol Diag 2001, 3:55-61
49. Dodig TD, Mack KT, Cassarino DF, Clark SH: Development of the tight-skin phenotype in immune-deficient mice. Arthritis Rheum 2001, 44:723-727
50. Hultin LE, Hausner MA, Hultin PM, Giorgi JV: CD20 (pan-B cell) antigen is expressed at a low level on a subpopulation of human T lymphocytes. Cytometry 1993, 14:196-204
51. Algino KM, Thomason RW, King DE, Montiel MM, Craig FE: CD20 (pan-B cell antigen) expression on bone marrow-derived T cells. Am J Clin Pathol 1996, 106:78-81
52. Quintanilla-Martinez L, Preffer F, Rubin D, Ferry JA, Harris NL: CD20+ T-cell lymphoma. Neoplastic transformation of a normal T-cell subset. Am J Clin Pathol 1994, 102:483-489
53. Leandro MJ, Cambridge G, Ehrenstein MR, Edwards JC: Reconstitution of peripheral blood B cells after depletion with rituximab in patients with rheumatoid arthritis. Arthritis Rheum 2006, 54:613-620
54. Postlethwaite AE, Holness MA, Katai H, Raghow R: Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J Clin Invest 1992, 90:1479-1485
55. Duncan MR, Berman B: Stimulation of collagen and glycosaminoglycan production in cultured human adult dermal fibroblasts by recombinant human interleukin 6. J Invest Dermatol 1991, 97:686-692
56. H2 paradigm. Nat Rev Immunol 2004, 4:583-594
57. Skok J, Poudrier J, Gray D: Dendritic cell-derived IL-12 promotes B cell induction of Th2 differentiation: a feedback regulation of Th1 development. J Immunol 1999, 163:4284-4291
58. Siracusa LD, McGrath R, Fisher JK, Jimenez SA: The mouse tight skin (Tsk) phenotype is not dependent on the presence of mature T and B lymphocytes. Mamm Genome 1998, 9:907-909
59. Baxter RM, Crowell TP, McCrann ME, Frew EM, Gardner H: Analysis of the tight skin (Tsk1/+) mouse as a model for testing antifibrotic agents. Lab Invest 2005, 85:1199-1209
60. Saito S, Nishimura H, Phelps RG, Wolf I, Suzuki M, Honjo T, Bona C: Induction of skin fibrosis in mice expressing a mutated fibrillin-1 gene. Mol Med 2000, 6:825-836
61. McGaha TL, Phelps RG, Spiera H, Bona C: Halofuginone, an inhibitor of type-1 collagen synthesis and skin sclerosis, blocks transforming-growth-factor- β-mediated Smad3 activation in fibroblasts. J Invest Dermatol 2002, 118:461-470
62. Zhou L-J, Tedder TF: CD20 workshop panel report. Leukocyte Typing V. White Cell Differentiation Antigens. Edited by Schlossman SF, Boumsell L, Gilks W, Harlan JM, Kishimoto T, Morimoto C, Ritz J, Shaw S, Silverstein R, Springer T, Tedder TF, Todd RF. Oxford, Oxford University Press, 1995, pp 511-514