Hyperexpression of CD40 ligand by B and T cells in human lupus and its role in pathogenic autoantibody production

Journal of Clinical Investigation

Volumn 97, Issue 9, 1996, Pages 2063-2073

  Desai Mehta, Ami ^a   Lu, Liangjun ^a   Ramsey Goldman, Rosalind ^a   Datta, Syamal K ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

anti DNA autoantibodies; autoimmune disease; CD40 ligand expression; immunotherapy; system lupus erythematosus

Indexed keywords

AUTOANTIBODY; CD4 ANTIGEN; CD40 ANTIGEN; CD8 ANTIGEN; DNA ANTIBODY;

ADULT; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HELPER CELL; HUMAN; HUMAN CELL; LUPUS ERYTHEMATOSUS NEPHRITIS; MALE; MONONUCLEAR CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE SUBPOPULATION;

EID: 0029913381     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118643     Document Type: Article

References (69)

1. Rothfield, N.F., and B.D. Stollar. 1967. The relation of immunoglobulin class, pattern of antinuclear antibody, and complement-fixing antibodies to DNA in sera from patients with systemic lupus erythematosus. J. Clin. Invest. 46:1785-1794.
2. Burlingame, R.W., M.L. Boey, G. Starkebaum, and R.L. Rubin. 1994. The central role of chromatin in autoimmune responses to histories and DNA in systematic lupus erythematosus. J. Clin. Invest. 94:184-192.
3. Suzuki, N., T. Harada, Y. Mizushima, and T. Sakane. 1993. Possible pathogenic role of cationic anti-DN A autoantibodies in the development of nephritis in patients with systemic lupus erythematosus. J. Immunol. 151:1128-1136.
4. Suenaga, R., and N.I. Abdou. 1993. Cationic and high affinity serum IgG anti-dsDNA antibodies in active lupus nephritis. Clin. Exp. Immunol. 94:418-422.
5. Diamond, B., J.B. Katz, E. Paul, C. Aranow, D. Lustgarten, and M.D. Scharff. 1992. The role of somatic mutation in the pathogenic anti-DNA response. Annu. Rev. Immunol. 10:731-757.
6. Sabbaga, J., O.G. Pankewycz, V. Lufft, R.S. Schwartz, and M.P. Madaio, 1990. Cross-reactivity distinguishes serum and nephritogenic anti-DNA antibodies in human lupus from their natural counterparts in normal serum. J. Autoimmun. 3:215-235.
7. Rubin, R.L., R.W. Burlingame, and J.E. Arnott. 1995. IgG but not other classes of anti-[〈H2A-H2B〉-DNA] is an early sign of procainamide-induced lupus. J. Immunol. 154:2483-2493.
8. Gavalchin, J., and S.K. Datta. 1987. The NZB X SWR model of lupus nephritis. II. Autoantibodies deposited in renal lesions show a restricted idiotypic diversity. J. Immunol. 138:138-148.
9. Burlingame, R.W., R.L. Rubin, R.S. Balderas, and A.N. Theofilopoulos. 1993. Genesis and evolution of antichromatin autoantibodies in murine lupus implicates immunization with self antigen. J. Clin. Invest. 91:1687-1696.
10. Di Valerio, R., K.A. Bernstein, E. Varghese, and J.B. Lefkowith. 1995. Murine lupus glomerulotropic monoclonal antibodies exhibit differing specificities but bind via a common mechanism. J. Immunol 155:2258-2268.
11. Datta, S.K., H. Patel, and D. Berry. 1987. Induction of a cationic shift in IgG anti-DNA autoantibodies. Role of T helper cells with classical and novel phenotypes in three murine models of lupus nephritis. J. Exp. Med. 165:1252-1268.
12. + T cell lines with selective patterns of autoreactivity as well as CD4 /CD8 T helper cell lines augment the production of idiotypes shared by pathogenic anti-DNA autoantibodies in the NZB X SWR model of lupus nephritis. J. Immunol. 140:2215-2224.
13. + T helper cells in humans augment the production of pathogenic anti-DNA autoantibodies associated with lupus nephritis. J. Immunol. 143:103-112.
14. + T helper cell lines that express the γ/δ T-cell receptor. Proc. Natl. Acad Sci. USA. 87:7020-7024.
15. Desai-Mehta, A., C. Mao, S. Rajagopalan, T. Robinson, and S.K. Datta. 1995. Structure and specificity of T cell receptors expressed by potentially pathogenic anti-DNA autoantibody-inducing T cells in human lupus. J. Clin. Invest. 95:531-541.
16. Adams, S., P. Leblanc, and S.K. Datta. 1991. Junctional region sequences of T-cell receptor β chain genes expressed by pathogenic anti-DNA autoantibody-inducing T helper cells from lupus mice: possible selection by cationic autoantigens. Proc. Natl. Acad. Sci. USA. 88:11271-11275.
17. Mao, C., G.E. Osman, S. Adams, and S.K. Datta. 1993. Nucleosome: a major immunogen for the pathogenic autoantibody-inducing T cells in lupus mice. J. Immunol. 152:1462-1470.
18. Mohan, C., S. Adams, V. Stanik, and S.K. Datta. 1993. Nucleosome: a major immunogen for the pathogenic autoantibody-inducing T cells of lupus. J. Exp. Med. 177:1367-1381.
19. Ando, D.G., E.E. Sercarz, and B.H. Hahn. 1987. Mechanisms of T and B cell collaboration in the in vitro production of anti-DNA antibodies in the NZB/NZW F1 murine SLE model. J. Immunol. 138:3185-3190.
20. Naiki, M., B.-L. Chiang, D. Cawley, A. Ansari, S.J. Rozzo, B.L. Kotzin, A. Zlotnik, and M.E., Gershwin. 1992. Generation and characterization of cloned helper T cell lines for anti-DNA responses in NZB.H-2bml2 mice. J. Immunol. 149:4109-4115.
21. + cells to support autoantibody synthesis. Arthritis & Rheum. 33:1216-1225.
22. Crow, M.K., G. Delguidice-Ash, J.B. Zehetbauer, N. Lawson, H. Brot, H. Weissbach, and K.B. Elkon. 1994. Autoantigen specific T cell proliferation induced by ribosomal P2 protein in patients with systemic lupus erythematosus. J. Clin. Invest. 94:345-352.
23. Kuwana, M., T.A. Medsger, and T.M. Wright. 1995. T and B cell collaboration is essential for autoantibody response to DNA Topoisomerase I in systemic sclerosis. J. Immunol. 155:2703-2714.
24. Mamula, M.J., S. Fatenejad, and J. Craft. 1994. B cells process and present lupus autoantigens that initiate autoimmune T cell responses. J Immunol. 152:1453-1461.
25. Sobel, E.S., V.M. Kakkanaiah, M. Kakkanaiah, R.L. Cheek, P.L. Cohen, and R.A. Eisenberg. 1994. T-B collaboration for autoantibody production in lpr mice is cognate and MHC-restricted. J. Immunol. 152:6011-6016.
26. Klinman, D.M., and A.D. Steinberg. 1987. Systemic autoimmune disease arises from polyclonal B cell activation. J. Exp. Med. 165:1755-1760.
27. Reininger, L., T. Radaszkiewicz, M. Kosco, F. Melchers, and A.G. Rolnik. 1992. Development of autoimmune disease in SCID mice populated with long-term in vitro proliferating (NZB X NZW)F1 pre-B cells. J. Exp. Med. 176:1343-1353.
28. Datta, S.K., F.L. Owen, J.E. Womack, and R.J. Riblet. 1982. Analysis of recombinant inbred lines derived from autoimmune (NZB) and high leukemia (C58) strains: independent multigenic systems control B cell hyperactivity, retrovirus expression and autoimmunity. J. Immunol. 129:1539-1544.
29. Merino, R., M. Iwamoto, L. Fossati, and S. Izui. 1993. Polyclonal B cell activation arises from different mechanisms in lupus-prone (NZB X NZW)F1 and MRL/Mpj-lpr/lpr mice. J. Immunol. 151:6509-6516.
30. Noelle, R.J., M. Roy, D.M. Shepherd, I. Stamencovic, J.A. Ledbetter, and A. Aruffo. 1992. A novel ligand on activated helper T cells binds CD40 and transduces the signal for the cognate activation of B cells. Proc. Natl. Acad. Sci. USA. 89:6550-6554.
31. Lederman, S., M.J. Yellin, G. Inghirami, J.J. Lee, D.M. Knowles, and L. Chess. 1992. Molecular interaction mediating T-B lymphocyte collaboration in human lymphoid follicles. Role T cell-B cell activating molecule (5c8 antigen) and CD40 in contact-dependent help. J Immunol. 149:3817-3826.
32. Clark, E. A., and J.A. Ledbetter. 1994. How B and T cells talk to each other. Nature (Lond.). 367:425-428.
33. Roy, M., T. Waldschmidt, A. Aruffo, J.A. Ledbetter, and R.J. Noelle. 1993. The regulation of the expression of gp39, the CD40 ligand, on normal and cloned CD4+ T cells. J. Immunol. 151:2497-2510.
34. Ren, C.L., T. Morio, S.M. Fu, and R.S. Geha. 1994. Signal transduction via CD40 involves activation of lyn kinase and phosphalidylinositol-3-kinase, and phosphorylation of phospholipase Cγ2. J. Exp. Med. 179:673-680.
35. Faris, M., F. Gaskin, J.T. Parsons, and S.M. Fu. 1994. CD40 signaling pathway: anti-CD40 monoclonal antibody induces rapid dephosphorylation and phosphorylation of Tyrosine-phosphorylated proteins including protein tyrosine kinase Lyn, Fyn, and Syk and the appearance of a 28-kD tyrosine phosphorylated protein. J. Exp. Med. 179:1923-1931.
36. Banchereau, J., F. Bazan, D. Blanchard, F. Briere, J.P. Galizi, C. van Kooten, Y.J. Liu. F. Rousset, and S. Saeland. 1994. The CD40 antigen and its ligand. Annu. Rev. Immunol. 12:881-922.
37. Spriggs, M.K., R.J. Armitage, L. Stockbine, K.N. Clifford, B.M. Macduff, T.A. Sato, C.R. Maliszewski, and W.C. Fanslow. 1992. Recombinant human CD40 ligand stimulates B cell proliferation and immunoglobulin E secretion. J. Exp. Med. 176:1543-1550.
38. Lederman, S., M.J. Yellin, A.M. Cleary, A. Pernis, G. Inghirami, L.E. Chon, L.R. Covey, J.L. Lee, P. Rothman, and L. Chess. 1994. T-BAM/CD40-L on helper T lymphocytes augments lymphokine-induced B cell 1g isotype switch recombination and rescues B cells from programmed cell death. J. Immunol. 152:2163-2171.
39. Foy, T.M., J.D. Laman, J.A. Ledbetter, A. Aruffo, E. Claassen, and R.J. Noelle. 1994. gp39-CD40 interactions are essential for germinal center formation and the development of B cell memory. J. Exp. Med. 180:157-163.
40. Liu, Y.-J., D.E. Joshua, G.T. Williams, C.A. Smith, J. Gordon, and I.C.M. MacLennan. 1989. Mechanism of antigen driven selection in germinal centers. Nature (Lond.). 342:929-931.
41. Tsubata, T., J. Wu, and T. Honjo. 1993. B cell apoptosis induced by antigen receptor crosslinking is blocked by a T cell signal through CD40. Nature (Lond). 364:645-648.
42. Wang, Z., J.G. Karras, R.G. Howard, and T.L. Rothstein. 1995. Induction of bcl-x by CD40 engagement rescues sIg-induced apoptosis in murine B cells. J. Immunol. 155:3722-3725.
43. Liang, M.H., S.A. Socher, M.G. Larson, and P.H. Schur. 1989. Reliability and validity of six systems for the clinical assessment of disease activity in systemic lupus erythematosus. Arthritis & Rheum. 32:1107-1118.
44. Grammer, A.C., M.C. Bergman, Y. Miura, K. Fujita, L.S. Davis, and P.E. Lipsky. 1995. The CD40 ligand expressed by human B cells costimulates B cell responses. J. Immunol. 154:4996-5010.
45. Castle, B.E., K. Kishimoto, C. Stearns, M.L. Brown, and M.R. Kehry. 1993. Regulation of expression of the ligand for CD40 on T helper lymphocytes. J. Immunol. 151:1777-1788.
46. Yellin, M.J., K. Sippel, G. Inghirami, L.R. Covey, J.J. Lee, J. Sinning, E.A. Clark, L. Chess, and S. Lederman. 1994. CD40 molecules induce down-modulation and endocytosis of T cell surface Tcell-B cell activating molecule/ CD40-L. J. Immunol. 152:598-608.
47. van Kooten, C.V., C. Gaillard, J.-P. Gallizi, P. Hermann, F. Fossiez, J. Banchereau, and D. Blanchard. 1994. B cells regulate expression of CD40 ligand on activated T cells by lowering the mRNA level and through the release of soluble CD40. Eur. J. Immunol. 24:787-792.
48. Mohan, C., Y. Shi, J.D. Laman, and S.K. Datta. 1995. Interaction between CD40 and its ligand gp39 in the development of murine lupus nephritis. J. Immunol. 154:1470-1480.
49. Gyllensten, U.B., and H.A. Erlich. 1988. Generation of single stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus. Proc. Natl. Acad. Sci. USA. 85:7652-7656.
50. Nonoyama, S., L.A. Penix, C.P. Edwards, D.B. Lewis, S. Ito, A. Aruffo, C.B. Wilson, and H.D. Ochs. 1995. Diminished expression of CD40 ligand by activated neonatal T cells. J. Clin. Invest. 95:66-75.
51. Vassilopoulos, D., B. Kovacs, and G.C. Tsokos. 1995. TCR/CD3 complex-mediated signal transduction pathway in T cells and T cell lines from patients with systemic lupus erythematosus. J. Immunol. 155:2269-2281.
52. Kammer, G.M., I. Khan, and C. Malemud. 1994. Deficient type I protein kinase A isozyme activity in systemic lupus erythematosus T lymphocytes. J. Clin. Invest. 94:422-430.
53. Maggi, E., M.G. Giudizi, R. Biagiotti, F. Annunziato, R. Manetti, M-P. Piccinni, P. Parronchi, S. Sampognaro, L. Giannarini, G. Zuccati, and S. Romagnani. 1994. Th2-like CD8+ T cells showing B cell helper function and reduced cytolytic activity in human immunodeficiency virus type 1 infection. J. Exp. Med. 180:489-495.
54. Buhlmann, J.E., T.M. Foy, A. Aruffo, K.M. Crassi, J.A. Ledbetter, W.R. Green, J.C. Xu, L.D. Schultz, D. Roopesian, R.A. Flavell, et al. 1995. In the absence of a CD40 signal B cells are tolerogenic. Immunity. 2:645-653.
55. Tsitsikov, E.N., N. Ramesh, and R.S. Geha. 1994. Structure of the CD40 ligand gene. Mol. Immunol. 31:895-900.
56. Facchetti, F., C. Appiani, L. Salvi, J. Levy, and L.D. Notarangelo. 1995. Immunohistologic analysis of ineffective CD40-CD40 Ligand interaction in lymphoid tissues from patients with X-linked immunodeficiency with hyper-IgM. Abortive germinal center cell reaction and severe depletion of follicular dendritic cells. J. Immunol. 154:6624-6633.
57. Ware, C.F., P.D. Crowe, T.L. Vanarsdale, M.H. Grayson, R. Jerzy, C.A. Smith, and R.G. Goodwin. 1991. Tumor necrosis factor (TNF) receptor family expression in T lymphocytes. Differential regulation of the type I TNF receptor during activation of resting and effector T cells. J. Immunol. 147:4229-4238.
58. Ranheim, E.A., and T.J. Kipps. 1993. Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal. J. Exp. Med. 177:925-935.
59. Kennedy, M.K., K.M. Mohler, K.D. Shanebeck, P.R. Baum, K.S. Picha, C.A. Ottene-Evans, C.A. Janeway, and K.H. Grabstein. 1994. Induction of B cell costimulatory function by recombinant murine CD40 ligand. Eur. J. Immunol. 24:116-123.
60. Singh, R.R., V. Kumar, F.M. Ebling, S. Southwood, A. Sette, E.E. Sercarz, and B.H. Hahn. 1995. T cell determinants from autoantibodies to DNA can upregulate autoimmunity in murine SLE. J. Exp. Med. 181:2017-2027.
61. Sercarz, E.E., and S.K. Datta. 1994. Mechanisms of autoimmunization: perspective from the mid-90s. Curr. Opin. Immunol. 6:875-881.
62. Gleichmann, E., E.H. van Elven, and J.P.W. van der Veen. 1982. A systemic lupus erythematosus (SLE) like disease in mice induced by abnormal T-B cell cooperation. Preferential formation of autoantibodies characteristic of SLE. Eur. J. Immunol. 12:152-159.
63. James, J.A., T. Gross, R.H. Scofield, and J.B. Harley. 1995. Immunoglobulin epitope spreading and autoimmune disease after peptide immunization: Sm B/B'-derived PPPGMRPP and PPPGIRGP induce spliceosome autoimmunity. J. Exp. Med. 181:453-461.
64. Desai, D.D., M.R. Krishnan, J.T. Swindle, and T.N. Marion. 1993. Antigen-specific induction of antibodies against native mammalian DNA in nonautoimmune mice. J. Immunol. 151:1614-1626.
65. Moens, U., O.-M. Seterenes, A.W. Hey, Y. Silsand, T. Traavik, B. Johansen, and O.P. Rekvig. 1995. In vivo expression of a single viral DNA-binding protein generates systemic lupus erythematosus-related autoimmunity to double-stranded DNA and histones. Proc. Natl. Acad. Sci. USA. 92:12393-12397.
66. Schattner, E.J., K.B. Elkon, D.-H. Yoo, J. Tumang, P.H. Krammer, M.K. Crow, and S.H. Friedman. 1995. CD40 ligation induces Apo-1/Fas expression on human B lymphocytes and facilitates apoptosis through the Apo-1/Fas pathway. J. Exp. Med. 182:1557-1566.
67. Finck, B.K., P.S. Linsley, and D. Wofsy. 1994. Treatment of murine lupus with CTLA4Ig. Science (Wash. DC). 265:1225-1227.
68. Klaus, S.J., L.M. Pinchuk, H.D. Ochs, C.-L. Law, W.C. Fanslow, R.J. Armitage, and E.A. Clark. 1994. Costimulation through CD28 enhances T cell-dependent B cell activation via CD40-CD40L interaction. J. Immunol. 152: 5643-5652.
69. Datta, S.K., C. Mohan, and A. Desai-Mehta. 1995. Mechanisms of the pathogenic autoimmune response in lupus: Prospects for specific immunotherapy. Immunol. Res. 14:132-147.