A Solution to the Rheumatoid Factor Paradox: Pathologic Rheumatoid Factors Can Be Tolerized by Competition with Natural Rheumatoid Factors

Journal of Immunology

Volumn 159, Issue 4, 1997, Pages 1728-1738

  Stewart, Jeffrey J ^a,e   Agosto, Harvey ^a,f   Litwin, Samuel ^b   Welsh, J Douglas ^a   Shlomchik, Mark ^c   Weigert, Martin ^a   Seiden, Philip E ^a,d,e  

^a PRINCETON UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c YALE NEW HAVEN HOSPITAL   (United States)

^d IBM T J WATSON RESEARCH CENTER   (United States)

^e In Machina Biosciences   (United States)

^f ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RHEUMATOID FACTOR;

ANIMAL; ARTICLE; COMPUTER SIMULATION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MOUSE; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; RHEUMATOID ARTHRITIS;

ANIMALS; ARTHRITIS, RHEUMATOID; COMPUTER SIMULATION; IMMUNE TOLERANCE; MICE; MICE, INBRED MRL LPR; RHEUMATOID FACTOR;

EID: 0031571212     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Coulie, P., and J. Van Snick. 1983. Rheumatoid factors and secondary immune responses in the mouse. II. Incidence, kinetics and induction mechanisms. Eur. J. Immunol. 13:895.
2. Nemazee, D. A., and V. L. Sato. 1983. Induction of rheumatoid antibodies in the mouse: regulated production of autoantibody in the secondary humoral response. J. Exp. Med. 158:529.
3. Coulie, P. G., and J. Van Snick. 1985. Rheumatoid factor (RF) production during anamnestic immune responses in the mouse. III. Activation of RF precursor cells is induced by their interaction with immune complexes and carrier-specific helper T cells. J. Exp. Med. 161:88.
4. Roosnek, E., and A. Lanzavecchia. 1991. Efficient and selective presentation of antigen-antibody complexes by rheumatoid factor B cells. J. Exp. Med. 173:487.
5. Lydyard, P. M., R. Quartey Papafio, B. Broker, L. Mackenzie, J. Jouquan, M. A. Blaschek, J. Steele, M. Petrou, P. Collins, D. Isenberg, and P. Y. Youinou. 1990. The antibody repertoire of early human B cells. I. High frequency of autoreactivity and polyreactivity. Scand. J. Immunol. 31:33.
6. Hartman, A. B., C. P. Mallett, J. Srinivasappa, B. S. Prabhakar, A. L. Notkins, and S. J. Smith Gill. 1989. Organ reactive autoantibodies from nonimmunized adult BALB/c mice are polyreactive and express non-biased VH gene usage. Mol. Immunol. 26:359.
7. Rousseau, P. G., C. P. Mallett, and S. J. Smith Gill. 1989. A substantial proportion of the adult BALB/c available B cell repertoire consists of multireactive B cells. Mol. Immunol. 26:993.
8. Monestier, M., A. Manheimer Lory, B. Bellon, C. Painter, H. Dang, N. Talal, M. Zanetti, R. Schwanz, D. Pisetsky, R. Kuppers, N. Rose, J. Brochier, L. Klareskog, R. Holmdahl, B. Erlanger, F. Alt, and C. Bona. 1986. Shared idiotypes and restricted immunoglobulin variable region heavy chain genes characterize murine autoantibodies of various specificities. J. Clin. Invest. 78:753.
9. Manheimer Lory, A. J., M. Monestier, B. Bellon, F. W. Alt, and C. A. Bona. 1986. Fine specificity, idiotypy, and nature of cloned heavy-chain variable region genes of murine monoclonal rheumatoid factor antibodies. Proc. Natl. Acad. Sci. USA 83:8293.
10. Shlomchik, M. J., D. A. Nemazee, V. L. Sato, J. Van Snick, D. A. Carson, and M. G. Weigert. 1986. Variable region sequences of murine IgM anti-IgG monoclonal autoantibodies (rheumatoid factors): a structural explanation for the high frequency of IgM anti-IgG B cells. J. Exp. Med. 164:407.
11. Van Snick, J., and P. Coulie. 1983. Rheumatoid factors and secondary immune responses in the mouse. I. Frequent occurrence of hybridomas secreting IgM anti-IgG1 autoantibodies after immunization with protein antigens. Eur. J. Immunol. 13:890.
12. Dresser, D. W. 1978. Most IgM-producing cells in the mouse secrete autoantibodies (rheumatoid factor). Nature 274:480.
13. Hay, F. C., A. J. Soltys, G. Tribbick, and H. M. Geysen. 1991. Framework peptides from kappa IIIb rheumatoid factor light chains with binding activity for aggregated IgG. Eur. J. Immunol. 21:1837.
14. Weigert, M. 1990. Is the hypothesis alive that IgM anti-IgG, rheumatoid factor specificity is determined by framework regions? Eur. J. Immunol. 20:2529.
15. Mellow, G. H., and A. B. Clarkson, Jr. 1982. Trypanosoma lewisi: enhanced resistance in naive lactating rats and their suckling pups. Exp. Parasitol. 53:217.
16. Heyman, B. 1990. Fc-dependent IgG-mediated suppression of the antibody response: fact or artefact? Scand. J. Immunol. 31:601.
17. Winska Wiloch, H., K. Thompson, A. Young, M. Corbett, M. Shipley, and F. Hay. 1988. IgA and IgM rheumatoid factors as markers of later erosive changes in rheumatoid arthritis (RA). Scand. J. Reumatol. (Suppl. 75):238.
18. Jones, M. G., M. E. Shipley, J. P. Hearn, and F. C. Hay. 1990. Specificity of rheumatoid factors in relation Io the disease state in rheumatoid arthritis. Ann. Rheum. Dis. 49:757.
19. Shlomchik, M., D. Nemazee, J. van Snick, and M. Weigert. 1987. Variable region sequences of murine IgM anti-IgG monoclonal autoantibodies (rheumatoid factors). II. Comparison of hybridomas derived by lipopolysaccharide stimulation and secondary protein immunization. J. Exp. Med. 165:970.
20. Jacobson, B. A., J. Sharon, H. Shan, M. Shlomchik, M. G. Weigert, and A. Marshak Rothstein. 1994. An isotype switched and somatically mutated rheumatoid factor clone isolated from a MRL-lpr/lpr mouse exhibits limited intraclonal affinity maturation. J. Immunol. 152:4489.
21. Berney, T., T. Fulpius, T. Shibata, L. Reininger, J. VanSnick, H. Shan, M. Weigert, A. Marshak-Rothstein, and S. Izui. 1992. Selective pathogenicity of murine rheumatoid factors of the cryoprecipitable IgG3 subclass. Int. Immunol. 4:93.
22. Lydyard, P. M., R. P. Quartey Papafio, B. M. Broker, L. MacKenzie, F. C. Hay, P. Y. Youinou, R. Jefferis, and R. A. Mageed. 1990. The antibody repertoire of early human B cells. III. Expression of cross-reactive idiotopes characteristic of certain rheumatoid factors and identifying V kappa III, VHI, and VHIII gene family products. Scand. J. Immunol. 32:709.
23. Shlomchik, M. J., A. Marshak-Rothstein, C. B. Wolfowicz, T. Rothstein, and M. G. Weigert. 1987. The role of clonal selection and somatic mutation in autoimmunity. Nature 328:805.
24. Taguchi, H., M. Kanoh, N. Takubo, S. Kadota, K. Kanazawa, Y. Hitsumoto, T. Shibata, and S. Utsumi. 1990. IgG isotype and isolype specificity of murine monoclonal IgG rheumatoid factors. Clin. Ext. Immunol. 80:136.
25. Shan, H., M. J. Shlomchik, A. Marshak-Rothstein, D. S. Pisetsky, S. Litwin, and M. G. Weigert. 1994. The mechanism of autoantibody production in an autoimmune MRL/lpr mouse. J. Immunol. 153:5104.
26. Nemazee, D., D. Russell, B. Arnold, G. Haemmerling, J. Allison, J. F. Miller, G. Morahan, and K. Buerki. 1991. Clonal deletion of autospecific B lymphocytes. Immunol. Rev. 122:117.
27. Nemazee, D. and K. Buerki. 1989. Clonal deletion of autoreactive B lymphocytes in bone marrow chimeras. Proc. Natl. Acad. Sci. USA 86:8039.
28. Hartley, S. B., J. Crosbie. R. Brink, A. B. Kantor, A. Basten, and C. C. Goodnow. 1991. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353:765.
29. Nossal, G. J., and B. L. Pike. 1978. Mechanisms of clonal abortion tolerogenesis. I. Response of immature hapten-specific B lymphocytes. J. Exp. Med. 148:1161.
30. Gay, D., T. Saunders, S. Camper, and M. Weigert. 1993. Receptor editing: an approach by autoreactive B cells to escape tolerance. J. Exp. Med. 177:999.
31. Tiegs, S. L., D. M. Russell, and D. Nemazee. 1993. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177:1009.
32. Nossal, G. V. J., and B. L. Pike. 1980. Clonal anergy: persistence in tolerant mice of antigen-binding B lymphocytes incapable of responding to antigen or mitogen. Proc. Natl. Acad. Sci. USA 77:1602.
33. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith Gill, R. A. Brink, H. Pritchard Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, R. J. Trent, and A. Basten. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334:676.
34. Brink, R., C. C. Goodnow, J. Crosbie, E. Adams, J. Eris, D. Y. Mason, S. B. Hartley, and A. Basten. 1992. Immunoglobulin M and D antigen receptors are both capable of mediating B lymphocyte activation, deletion, or anergy after interaction with specific antigen. J. Exp. Med. 176:991.
35. Linton, P. J., A. Rudie, and N. R. Klinman. 1991. Tolerance susceptibility of newly generating memory B cells. J. Immunol. 146:4099.
36. Han, S., K. Hathcock, B. Zheng, T. B. Kepler, R. Hodes, and G. Kelsoe. 1995. Cellular interaction in germinal centers: roles of CD40 ligand and B7-2 in established germinal centers. J. Immunol. 155:556.
37. Pulendran, B., K. G. Smith, and G. J. Nossal. 1995. Soluble antigen can impede affinity maturation and the germinal center reaction but enhance extrafollicular immunoglobulin production. J. Immunol. 155:1141.
38. Nossal, G. J., M. Karvelas, and B. Pulendran. 1993. Soluble antigen profoundly reduces memory B-cell numbers even when given after challenge immunization. Proc. Natl. Acad. Sci. USA 90:3088.
39. Shlomchik, M. J., D. Zharhary, T. Saunders, S. A. Camper, and M. G. Weigert. 1993. A rheumatoid factor transgenic mouse model of autoantibody regulation. Int. Immunol. 5:1329.
40. Hannum, L. G., D. Ni, A. M. Haberman, M. G. Weigert, and M. Shlomchik. 1996. A disease-related rheumatoid factor autoantibody is not tolerized in a normal mouse: implications for the origins of autoantibodies in autoimmune disease. J. Exp. Med. 184:1269.
41. Seiden, P. E., and F. Celada. 1992. A model for simulating cognate recognition and response in the immune system. J. Theor. Biol. 158:329.
42. Celada, F., and P. E. Seiden. 1992. A computer model of cellular interactions in the immune system. Immunol. Today 13:56.
43. Celada, F., and P. E. Seiden. 1996. Affinity maturation and hypermutation in a simulation of the humoral immune response. Eur. J. Immunol. 26:1150.
44. Randen, I., D. Brown, K. M. Thompson, N. Hughes Jones, V. Pascual, K. Victor, J. D. Capra, O. Forre, and J. B. Natvig. 1992. Clonally related IgM rheumatoid factors undergo affinity maturation in the rheumatoid synovial tissue. J. Immunol. 148:3296.
45. Thompson, K. M., M. Borretzen, I. Randen, O. Forre, and J. B. Natvig. 1995. V-gene repertoire and hypermutaiion of rheumatoid factors produced in rheumatoid synovial inflammation and immunized healthy donors. Ann. NY Acad. Sci. 764:440.
46. Langman, R. E., and M. Cohn. 1987. The E-T (elephant-tadpole) paradox necessitates the concept of a unit of B-cell function: the protecion. Mol. Immunol. 24:675.
47. Fazekas, G., E. Rajnavolgyi, I. Kurucz, E. Sintar, K. Kiss, G. Laszlo, and J. Gergely. 1990. Isolation and characterization of IgG2a-reactive autoantibodies from influenza virus-infected BALB/c mice. Eur. J. Immunol. 20:2719.
48. Takahashi, T., M. Tanaka, C. I. Brannan, N. A. Jenkins, N. G. Copeland, T. Suda, and S. Nagata. 1994. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76:969.
49. Watanabe-Fukunaga, R., C. I. Brannan, N. G. Copeland, N. A. Jenkins, and S. Nagata. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356.
50. Cohen, P. L., and R. A. Eisenberg. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9:243.
51. Itoh, N., S. Yonehara, A. Ishii, M. Yonehara, S-I. Mizushima, M. Samashima, A. Hase, Y. Seta, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 65:233.
52. Rubio, C. F., J. Kench, D. M. Russell, R. Yawger, and D. Nemazee. 1996. Analysis of central B cell tolerance in autoimmune-prone MRL/lpr mice bearing autoantibody transgenes. J. Immunol. 157:65.
53. Jacobson, B. A., D. J. Panka, K. A. Nguyen, J. Erikson, A. K. Abbas, and A. Marshak Rothstein. 1995. Anatomy of autoantibody production: dominant localization of antibody-producing cells to T cell zones in Fas-deficient mice. Immunity 3:509.
54. Schroder, A. E., A. Greiner, C. Seyfert, and C. Berek. 1996. Differentiation of B cells in the nonlymphoid tissue of the synovial membrane of patients with rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 93:221.
55. Randen, I., O. J. Mellbye, O. Forre, and J. B. Natvig. 1995. The identification of germinal centres and follicular dendritic cell networks in rheumatoid synovial tissue. Scand. J. Immunol. 41:481.
56. Welch, M. J., S. Fong, J. Vaughan, and D. Carson. 1983. Increased frequency of rheumatoid factor precursor B lymphocytes after immunization of normal adults with tetanus toxoid. Clin. Exp. Immunol. 51:299.
57. Tighe, H., K. Warnatz, D. Brinson, M. Corr, W. O. Weigle, S. M. Baird, and D. A. Carson. 1997. Peripheral deletion of rheumatoid factor B cells after abortive activation by IgG. Proc. Natl. Acad. Sci. USA 94:646.
58. Matzinger, P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12:991.
59. Ohashi, P. S., S. Oehen, K. Buerki, H. Pircher, C. T. Ohashi, B. Odermatt, B. Malissen, R. M. Zinkemagel, and H. Hengartner. 1991. Ablation of "tolerance" and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65:305.
60. Rolink, A. G., T. Radaszkiewicz, and F. Melchers. 1987. The autoantigen-binding B cell repertoires of normal and of chronically graft-versus-host-diseased mice. J. Exp. Med. 165:1675.
61. Van Snick, J. L., and P. Coulie. 1982. Monoclonal anti-IgG autoantibodies derived from lipopolysaccharide-activated spleen cells of 129/Sv mice. J. Exp. Med. 155:219.
62. Conger, J. D., B. L. Pike, and G. J. Nossal. 1987. Clonal analysis of the anti-DNA repertoire of murine B lymphocytes. Proc. Natl. Acad. Sci. USA 84:2931.
63. Gilkeson, G. S., P. Ruiz, A. M. Pippen, A. L. Alexander, J. B. Lefkowith, and D. S. Pisetsky. 1996. Modulation of renal disease in autoimmune NZB/NZW mice by immunization with bacterial DNA. J. Exp. Med. 183:1389.