Overexpression of activation-induced cytidine deaminase in B cells is associated with production of highly pathogenic autoantibodies

Journal of Immunology

Volumn 178, Issue 8, 2007, Pages 5357-5365

  Hsu, Hui Chen ^a   Wu, Yalei ^b   Yang, PingAr ^a   Wu, Qi ^a   Job, Godwin ^a   Chen, Jian ^a   Wang, John ^a   Accavitti Loper, Mary Ann V ^c   Grizzle, William E ^d   Carter, Robert H ^a,e   Mountz, John D ^a,e,f  

^a The University of Alabama at Birmingham   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

^e BIRMINGHAM VA MEDICAL CENTER   (United States)

^f UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; AUTOANTIBODY; CD28 ANTIBODY; CD28 ANTIGEN; CD3 ANTIBODY; CD4 ANTIGEN; CD86 ANTIGEN; CYTIDINE DEAMINASE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE MODEL; ENZYME INDUCTION; FEMALE; GENETIC RECOMBINATION; GERMINAL CENTER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SOMATIC HYPERMUTATION;

EID: 34247141537     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.8.5357     Document Type: Article

References (59)

1. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377.
2. Yurasov, S., H. Wardemann, J. Hammersen, M. Tsuiji, E. Meffre, V. Pascual, and M. C. Nussenzweig. 2005. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201: 703-711.
3. Samuels, J., Y. S. Ng, C. Coupillaud, D. Paget, and E. Meffre. 2005. Impaired early B cell tolerance in patients with rheumatoid arthritis. J. Exp. Med. 201: 1659-1667.
4. Melchers, P., and A. R. Rolink. 2006. B cell tolerance-how to make it and how to break it. Curr. Top. Microbiol. Immunol. 305: 1-23.
5. Taylor, B. A., C. Wnek, B. S. Kotlus, N. Roemer, T. MacTaggart, and S. J. Phillips. 1999. Genotyping new BXD recombinant inbred mouse strains and comparison of BXD and consensus maps. Mamm. Genome 10: 335-348.
6. Morse, H. C., III, T. M. Chused, J. W. Hartley, B. J. Mathieson, S. O. Sharrow, and B. A. Taylor. 1979. Expression of xenotropic murine leukemia viruses as cell-surface gp70 in genetic crosses between strains DBA/2 and C57BL/6. J. Exp. Med. 149: 1183-1196.
7. Mountz, J. D., P. Yang, Q. Wu, J. Zhou, A. Tousson, A. Fitzgerald, J. Allen, X. Wang, S. Cartner, W. E. Grizzle, et al. 2005. Genetic segregation of spontaneous erosive arthritis and generalized autoimmune disease in the BXD2 recombinant inbred strain of mice. Scand. J. Immunol 61: 128-138.
8. Hsu, H. C., T. Zhou, H. Kim, S. Barnes, P. Yang, Q. Wu, J. Zhou, B. A. Freeman, M. Luo, and J. D. Mountz. 2006. Production of a novel class of polyreactive pathogenic autoantibodies in BXD2 mice causes glomerulonephritis and arthritis. Arthritis Rheum. 54: 343-355.
9. Muramatsu, M., V. S. Sankaranand, S. Anant, M. Sugai, K. Kinoshita, N. O. Davidson, and T. Honjo. 1999. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274: 18470-18476.
10. Willenbrock, K., B. Jungnickel, M. L. Hansmann, and R. Kuppers. 2005. Human splenic marginal zone B cells lack expression of activation-induced cytidine deaminase. Eur. J. Immunol. 35: 3002-3007.
11. Okazaki, I. M., K. Kinoshita, M. Muramatsu, K. Yoshikawa, and T. Honjo. 2002. The AID enzyme induces class switch recombination in fibroblasts. Nature 416: 340-345.
12. Yoshikawa, K., I. M. Okazaki, T. Eto, K. Kinoshita, M. Muramatsu, H. Nagaoka, and T. Honjo. 2002. AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science 296: 2033-2036.
13. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
14. Kettleborough, C. A., J. Saldanha, K. H. Ansell, and M. M. Bendig. 1993. Optimization of primers for cloning libraries of mouse immunoglobulin genes using the polymerase chain reaction. Eur. J. Immunol. 23: 206-211.
15. Giudicelli, V., P. Duroux, C. Ginestoux, G. Folch, J. Jabado-Michaloud, D. Chaume, and M. P. Lefranc. 2006. IMGT/LIGM-DB, the IMGT comprehensive database of immunoglobulin and T cell receptor nucleotide sequences. Nucleic Acids Res. 34: D781-D784.
16. Lefranc, M. P., V. Giudicelli, C. Ginestoux, J. Bodmer, W. Muller, R. Bontrop, M. Lemaitre, A. Malik, V. Barbie, and D. Chaume. 1999. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res. 27: 209-212.
17. Jabara, H., D. Laouini, E. Tsitsikov, E. Mizoguchi, A. Bhan, E. Castigli, F. Dedeoglu, V. Pivniouk, S. Brodeur, and R. Geha. 2002. The binding site for TRAF2 and TRAF3 but not for TRAF6 is essential for CD40-mediated immunoglobulin class switching. Immunity 17: 265-276.
18. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629.
19. Zhou, T., C. K. Edwards III, and J. D. Mountz. 1995. Prevention of age-related T cell apoptosis defect in CD2-fas-transgenic mice. J. Exp. Med. 182: 129-137.
20. Bonham, C. A., L. Peng, X. Liang, Z. Chen, L. Wang, L. Ma, H. Hackstein, P. D. Robbins, A. W. Thomson, J. J. Fung, et al. 2002. Marked prolongation of cardiac allograft survival by dendritic cells genetically engineered with NF-κB oligodeoxyribonucleotide decoys and adenoviral vectors encoding CTLA4-Ig. J. Immunol. 169: 3382-3391.
21. Chen, J., Q. Wu, P. Yang, H. C. Hsu, and J. D. Mountz. 2006. Determination of specific CD4 and CD8 T cell epitopes after AAV2- and AAV8-hF.IX gene therapy. Mol. Ther. 13: 260-269.
22. Hao, Z., and K. Rajewsky. 2001. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J. Exp. Med. 194: 1151-1164.
23. Martin, F., and J. F. Kearney. 2000. B-cell subsets and the mature preimmune repertoire: marginal zone and B1 B cells as part of a "natural immune memory". Immunol. Rev. 175: 70-79.
24. Breitfeld, D., L. Ohl, E. Kremmer, J. Ellwart, F. Sallusto, M. Lipp, and R. Forster. 2000. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J. Exp. Med. 192: 1545-1552.
25. Koncz, G., C. Bodor, D. Kovesdi, R. Gati, and G. Sarmay. 2002. BCR mediated signal transduction in immature and mature B cells. Immunol. Lett. 82: 41-49.
26. Chaudhuri, J., C. Khuong, and F. W. Alt. 2004. Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature 430: 992-998.
27. Honjo, T., M. Muramatsu, and S. Fagarasan. 2004. AID: how does it aid antibody diversity? Immunity 20: 659-668.
28. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553-563.
29. Bransteitter, R., J. L. Sneeden, S. Allen, P. Pham, and M. F. Goodman. 2006. First AID (activation-induced cytidine deaminase) is needed to produce high affinity isotype-switched antibodies. J. Biol. Chem. 281: 16833-16836.
30. Kotani, A., I. M. Okazaki, M. Muramatsu, K. Kinoshita, N. A. Begum, T. Nakajima, H. Saito, and T. Honjo. 2005. A target selection of somatic hypermutations is regulated similarly between T and B cells upon activation-induced cytidine deaminase expression. Proc. Natl. Acad. Sci. USA 102: 4506-4511.
31. Losses, I. S., R. Levy, and A. A. Alizadeh. 2004. AID is expressed in germinal center B-cell-like and activated B-cell-like diffuse large-cell lymphomas and is not correlated with intraclonal heterogeneity. Leukemia 18: 1775-1779.
32. Hardianti, M. S., E. Tatsumi, M. Syampurnawati, K. Furuta, K. Saigo, Y. Nakamachi, S. Kumagai, H. Ohno, S. Tanabe, M. Uchida, and N. Yasuda. 2004. Activation-induced cytidine deaminase expression in follicular lymphoma: association between AID expression and ongoing mutation in FL. Leukemia 18: 826-831.
33. Okazaki, I. M., H. Hiai, N. Kakazu, S. Yamada, M. Muramatsu, K. Kinoshita, and T. Honjo. 2003. Constitutive expression of AID leads to tumorigenesis. J. Exp. Med. 197: 1173-1181.
34. Ruckerl, F., B. Busse, and J. Bachl. 2006. Episomal vectors to monitor and induce somatic hyperrnutation in human Burkitt-Lymphoma cell lines. Mol. Immunol. 43: 1645-1652.
35. Martin, A., and M. D. Scharff. 2002. Somatic hypermutation of the AID transgene in B and non-B cells. Proc. Natl. Acad. Sci. USA 99: 12304-12308.
36. Faber, C., H. Morbach, S. K. Singh, and H. J. Girschick. 2006. Differential expression patterns of recombination-activating genes in individual mature B cells in juvenile idiopathic arthritis. Ann. Rheum. Dis. 65: 1351-1356.
37. lpr mice. J. Immunol. 172: 3913-3921.
38. Retter, M. W., P. L. Cohen, R. A. Eisenberg, and S. H. Clarke. 1996. Both Sm and DNA are selecting antigens in the anti-Sm B cell response in autoimmune MRL/lpr mice. J. Immunol. 156: 1296-1306.
39. Wilson, P. C., O. de Bouteiller, Y. J. Liu, K. Potter, J. Banchereau, J. D. Capra, and V. Pascual. 1998. Somatic hypermutation introduces insertions and deletions into immunoglobulin V genes. J. Exp. Med. 187: 59-70.
40. L segments of monoreactive and polyreactive IgA autoantibodies to DNA in patients with systemic lupus erythematosus. J. Immunol. 152: 3137-3151.
41. H CDR3 structures. J. Immunol. 155: 2248-2257.
42. Putterman, C., B. Deocharan, and B. Diamond. 2000. Molecular analysis of the autoantibody response in peptide-induced autoimmunity. J. Immunol. 164: 2542-2549.
43. Deshmukh, U. S., H. Bagavant, and S. M. Fu. 2006. Role of anti-DNA antibodies in the pathogenesis of lupus nephritis. Autoimmun. Rev. 5: 414-418.
44. Li, Q. Z., C. Xie, T. Wu, M. Mackay, C. Aranow, C. Putterman, and C. Mohan. 2005. Identification of autoantibody clusters that best predict lupus disease activity using glomerular proteome arrays. J. Clin. Invest. 115: 3428-3439.
45. H gene repertoire of splenic B cells and somatic hypermutation in systemic lupus erythematosus. Arthritis Res. Ther. 5: R114-R121.
46. Harada, Y., M. Muramatsu, T. Shibata, T. Honjo, and K. Kuroda. 2003. Unmutated immunoglobulin M can protect mice from death by influenza virus infection. J. Exp. Med. 197: 1779-1785.
47. Muto, T., I. M. Okazaki, S. Yamada, Y. Tanaka, K. Kinoshita, M. Muramatsu, H. Nagaoka, and T. Honjo. 2006. Negative regulation of activation-induced cytidine deaminase in B cells. Proc. Natl. Acad. Sci. USA 103: 2752-2757.
48. Wu, X., P. Geraldes, J. L. Platt, and M. Cascalho. 2005. The double-edged sword of activation-induced cytidine deaminase. J. Immunol. 174: 934-941.
49. Liossis, S. N., and P. P. Sfikakis. 2004. Costimulation blockade in the treatment of rheumatic diseases. Bio. Drugs 18: 95-102.
50. Noel, P. J., L. H. Boise, and C. B. Thompson. 1996. Regulation of T cell activation by CD28 and CTLA4. Adv. Exp. Med. Biol. 406: 209-217.
51. Daikh, D. I., B. K. Finck, P. S. Linsley, D. Hollenbaugh, and D. Wofsy. 1997. Long-term inhibition of murine lupus by brief simultaneous blockade of the B7/CD28 and CD40/gp39 costimulation pathways. J. Immunol. 159: 3104-3108.
52. Ramanujam, M., X. Wang, W. Huang, L. Schiffer, C. Grimaldi, A. Akkerman, B. Diamond, M. P. Madaio, and A. Davidson. 2004. Mechanism of action of transmembrane activator and calcium modulator ligand interactor-Ig in murine systemic lupus erythematosus. J. Immunol. 173: 3524-3534.
53. Bijl, M., G. Horst, P. C. Limburg, and C. G. Kallenberg. 2001. Expression of costimulatory molecules on peripheral blood lymphocytes of patients with systemic lupus erythematosus. Ann. Rheum. Dis. 60: 523-526.
54. Nagafuchi, H., Y. Shimoyama, J. Kashiwakura, M. Takeno, T. Sakane, and N. Suzuki. 2003. Preferential expression of B7.2 (CD86), but not B7.1 (CD80), on B cells induced by CD40/CD40L interaction is essential for anti-DNA autoantibody production in patients with systemic lupus erythematosus. Clin. Exp. Rheumatol. 21: 71-77.
55. Dedeoglu, F., B. Horwitz, J. Chaudhuri, F. W. Alt, and R. S. Geha. 2004. Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NFκB. Int. Immunol. 16: 395-404.
56. Marquez, V. E., J. A. Kelley, R. Agbaria, T. Ben-Kasus, J. C. Cheng, C. B. Yoo, and P. A. Jones. 2005. Zebularine: a unique molecule for an epigenetically based strategy in cancer chemotherapy. Ann. NY Acad. Sci. 1058: 246-254.
57. Cheng, J. C., D. J. Weisenberger, F. A. Gonzales, G. Liang, G. L. Xu, Y. G. Hu, V. E. Marquez, and P. A. Jones. 2004. Continuous zebularine treatment effectively sustains demethylation in human bladder cancer cells. Mol. Cell. Biol. 24: 1270-1278.
58. Morita, T., A. Matsuzaki, S. Kurokawa, and A. Tokue. 2003. Forced expression of cytidine deaminase confers sensitivity to capecitabine. Oncology 65: 267-274.
59. Loder, F., B. Mutschler, R. J. Ray, C. J. Paige, P. Sideras, R. Torres, M. C. Lamers, and R. Carsetti. 1999. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190: 75-89.