Gender differences in autoimmunity: Molecular basis for estrogen effects in systemic lupus erythematosus

International Immunopharmacology

Volumn 1, Issue 6, 2001, Pages 1009-1024

  Rider, Virginia ^a   Abdou, Nabih I ^b,c  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b Allerg Immunol St Luke's H   (United States)

^c Pittsburg Stt Univ 1701 S B   (United States)

Author keywords

Calcineurin; Estrogen; Estrogen receptors; SLE; T cells

Indexed keywords

AUTOANTIBODY; CALCINEURIN; CYCLOHEXIMIDE; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; MESSENGER RNA; PHOSPHATASE;

ADOLESCENT; ADULT; ANTIBODY PRODUCTION; AUTOIMMUNITY; B LYMPHOCYTE; CLINICAL ARTICLE; ENZYME ACTIVITY; FEMALE; GENDER; GENETIC TRANSCRIPTION; HUMAN; LYMPHOCYTE ACTIVATION; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE;

ANIMALS; AUTOIMMUNITY; CALCINEURIN; ESTROGENS; FEMALE; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; RNA, MESSENGER; SEX CHARACTERISTICS;

EID: 0035036345     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1567-5769(01)00046-7     Document Type: Review

References (81)

1. Hess E.V. Lupus, the clinical entity. Kammer G.M., Tsokos G.C. Lupus: Molecular and Cellular Pathogenesis. 1999;1-12 Humana Press, Totowa, NJ.
2. Abdou N.I., Wall G., Lindsley H.B., Halsey J.F., Suzuki T. The network theory in autoimmunity: in vitro supersession of serum anti-DNA antibody binding to DNA by anti-idiotypic antibody in systemic lupus erythematosus. J. Clin. Invest. 67:1981;1297-1304.
3. Mongey A.-B., Hess E.V. The role of environment in systemic lupus erythematosus and associated disorders. Wallace D.J., Hahn B.H. Dubois' Lupus Erythematosus. 1997;31-37 Williams & Wilkins, Baltimore, MD.
4. Arnett F.C. The genetics of human lupus. Wallace D.J., Hahn B.H. Dubois' Lupus Erythematosus. 1997;77-117 Williams & Wilkins, Baltimore, MD.
5. Cooper G.S., Dooley M.A., Treadwell E.L., St. Clair E.W., Parks C.G., Gilkeson G.S. Hormonal environment and infectious risk factors for developing systemic lupus erythematosus. Arthritis Rheum. 41:1998;1714-1724.
6. Jungers P.F., Kuttenn F., Liote G., Pelissier N., Athea M.C.et al. Hormonal modulation in SLE. Arthritis Rheum. 28:1985;1243-1250.
7. Garovich M., Agudelo C., Pisko E. Oral contraceptives and systemic lupus erythematosus. Arthritis Rheum. 23:1980;1396-1398.
8. Bruce I.N., Laskin C.A. Sex hormones in systemic lupus erythematosus: a controversy for modern times. J. Rheumatol. 24:1997;1461-1463.
9. Arden N.K., Spector T.D. Oestrogens, bones and systemic lupus erythematosus. Lupus. 2:1993;381-382.
10. Petri M., Courtland R. Oral contraceptives and systemic lupus erythematosus. Arthritis Rheum. 40:1997;797-803.
11. Mund A.J., Simson J., Rothefield N. Effect of pregnancy on course of systemic lupus erythematosus. JAMA, J. Am. Med. Assoc. 183:1963;109-112.
12. Roubinian J.R., Talal N., Greenspan J.S., Goodman J.R., Siiteri P.K. Effect of castration and sex hormone treatment on survival, anti-nucleic acid antibodies, and glomerulonephritis in NZB/NZW F1 mice. J. Exp. Med. 147:1978;1568-1583.
13. Carson-Juricka M.A., Schrader W.T., O'Malley B.W. Steroid receptor family: structure and functions. Endocr. Rev. 11:1990;201-220.
14. Kuiper G.G., Gustafsson J.A. The novel estrogen receptor-β subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogen. FEBS Lett. 410:1997;87-90.
15. McInerney E.M., Weis K.E., Sum J., Mosselman S., Katzenellenbogen B.S. Transcription activation by the human estrogen receptor subtype β (ERβ) studies with ERβ and ERα receptor chimeras. Endocrinology. 1998;4513-4522.
16. Smith C.L., Onate S.A., Tsai M.-J., O'Malley B.W. CREB binding protein acts synergistically with steroid receptor coactivator-1 to enhance steroid receptor-dependent transcription. Proc. Natl. Acad. Sci. U. S. A. 93:1996;8884-8888.
17. Sabbah M., Courilleau D., Mester J., Redeuilh G. Estrogen induction of the cyclin D1 promoter: involvement of a cAMP response-like element. Proc. Natl. Acad. Sci. U. S. A. 96:1999;11217-11222.
18. Enmark E., Pelto-Huikko M., Gradien K., Lagercrantz S., Lagercrantz J.et al. Human estrogen receptor β-gene structure, chromosomal localization and expression pattern. J. Clin. Endocrinol. Metab. 82:1997;4258-4265.
19. Rood M.J., Vander Velde E.A., Cate R.T., Breedveld F.C., Huizinga T.W.J. Female sex hormones at the onset of systemic lupus erythematosus affect survival. Br. J. Rheumatol. 37:1998;1009-1010.
20. Whitacre C.C., Reingold S.C., O'Looney P.A. A gender gap in autoimmunity. Science. 283:1999;1277-1278.
21. Lahita R.G. The role of sex hormones in systemic lupus erythematosus. Curr. Opin. Rheumatol. 11:1999;352-356.
22. Ahmed S.A., Hissong B.D., Verthelyi D., Donner K., Becker K., Karpuzoglu-Sahin E. Gender and risk of autoimmune diseases: possible role of estrogenic compounds. Environ. Health Perspect. 107:1999;681-686.
23. Sagawa A., Abdou N.I. Suppressor cell dysfunction in systemic lupus erythematosus. Cells involved and in vitro correction. J. Clin. Invest. 62:1978;789-798.
24. Dayal A.K., Kammer G.M. The T cell enigma in lupus. Arthritis Rheum. 39:1996;23-33.
25. Tsokos G.C., Liossis S.N.C. Immune cell signaling defects in lupus: activation, anergy and death. Immunol. Today. 20:1999;119-124.
26. Rider V., Foster R.T., Evans M., Suenaga R., Abdou N.I. Gender differences in autoimmune diseases: estrogen increases calcineurin expression in systemic lupus erythematosus. Clin. Immunol. Immunopathol. 89:1998;171-180.
27. Guerini D., Klee C.B. Cloning of human calcineurin A: evidence for two isozymes and identification of a polypropylene structural domain. Proc. Natl. Acad. Sci. U. S. A. 86:1989;9183-9187.
28. Weiss A., Litman D.R. Signal transduction by lymphocyte antigen receptors. Cell. 76:1994;263-274.
29. Weiss A. Molecular and genetic insights into T cell antigen receptor structure and function. Annu. Rev. Genet. 25:1991;487-510.
30. Clipstone N.A., Crabtree G.R. Identification of calcineurin as a key signaling enzyme in T lymphocyte activation. Nature. 357:1992;695-697.
31. Bierer B.E., Hollander G., Fruman D., Burakoff S.J. Cyclosporin A and FK506: molecular mechanism of immunosuppression and probes for transplantation biology. Curr. Opin. Immunol. 5:1993;763-773.
32. Thomson A.W., Bonham C.A., Zeevi A. Mode of action of tacrolimus (FK506): molecular and cellular mechanisms. Ther. Drug Monit. 17:1995;584-591.
33. Klee C.B., Ren H., Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurinn. J. Biol. Chem. 22:1998;13367-13370.
34. Kiani A., Rao A., Aramburu J. Manipulating immune responses with immunosuppressive agents that target NFAT. Immunity. 12:2000;359-372.
35. Feske S., Draeger R., Peter H.H., Eichmann K., Rao A. The duration of nuclear residence of NFAT determines the pattern of cytokine expression in human SCID T cells. J. Immunol. 165:2000;297-305.
36. Aramburu J., Garcia-Cozar F., Raghavan A., Okamure H., Rao A., Hoan P.G. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site for NFAT. Mol. Cell. 1:1998;627-637.
37. Vassilopoulos D., Kovacs B., Tsokos G.C. TCR/CD3 complex-mediate signal transduction pathway in T cells and T cell lines from patients with systemic lupus erythematosus. J. Immunol. 155:1995;2269-2281.
38. Katagiri C., Kawamura T., Matsuzawa S.I., Mizuno Y., Matsumura S., Kikuchi K. Increase in protein phosphatase 2B activity in lymphoid tissues and T lymphocytes of autoimmune MRL/MpJ-lpr/lpr mice. J. Biochem. 114:1993;874-878.
39. + T cells, cytokine gene expression and disease activity in MRL/MpJ-lrp/lpr mice. Clin. Exp. Immunol. 100:1995;118-125.
40. Tan E.M., Cohen A.S., Fries J.F., Masi A.T., McShane D.J.et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25:1982;1271-1277.
41. Rider V., Jones S.R., Evans M., Abdou N.I. Molecular mechanisms involved in the estrogen-dependent regulation of calcineurin in systemic lupus erythematosus T cells. Clin. Immunol. 95:2000;124-134.
42. Rider V., Carlone D.L., Foster R.T. Oestrogen and progesterone regulate basic fibroblast growth factor messenger RNA in the rat uterus. J. Endocrinol. 154:1997;75-84.
43. Tumlin J.A., Someren J.T., Swanson C.E., Lea J.P. Expression of calcineurin activity and α-subunit isoforms in specific segments of the rat nephron. Am. J. Physiol. 269:1995;F558-F563.
44. Tumlin J.A., Lea J.P., Swanson C.E., Smith C.L., Edge S.S., Sorensen J.S. Aldosterone and dexamethasone stimulate calcineurin activity though a transcription-independent mechanism involving steroid receptor-associated heat shock proteins. J. Clin. Invest. 99:1997;1217-1223.
45. Rider V., Peterson C.J. Activation of uteroglobin gene expression by progesterone is modulated by uterine-specific promoter-binding proteins. Mol. Endocrinol. 5:1991;911-920.
46. Evans M.J., MacLaughlin S., Marvin R.D., Abdou N.I. Estrogen decreases in vitro apoptosis of peripheral blood mononuclear cells from women with normal menstrual cycles and decreases TNF-α production in SLE but not in normal cultures. Clin. Immunol. Immunopath. 82:1997;258-262.
47. Rider V., Piva M., Cohen M.E., Carlone D.L. Alternative splicing and differential targeting of fibroblast growth factor receptor 1 (FGFR1) in the pregnant rat uterus. Endocrinology. 136:1995;3137-3145.
48. Shimmoyama T., Everett S.M., Dixon M.F., Axon A.T.R., Crabtree J.E. Chemokine mRNA expression in gastric mucosa is associated with Helicobacter pylori cagA positivity and severity of gastritis. J. Clin. Pathol. 51:1998;765-770.
49. Suenaga R., Evans M.J., Mitamura K., Rider V., Abdou N.I. Peripheral blood T cells and monocytes, and B cell lines derived from lupus patients express estrogen receptor transcripts similar to those of normal controls. J. Rheumatol. 25:1998;1305-1312.
50. Van den Brink H.R., van Wijk M.J., Bijlsma J.W. Influence of steroid hormones on proliferation of peripheral blood mononuclear cells in patients with rheumatoid arthritis. Br. J. Rheumatol. 31:1992;663-667.
51. Dean D.M., Sanders M.M. Ten years after: reclassification of steroid-responsive genes. Mol. Endocrinol. 10:1996;1489-1495.
52. Coligan J.E., Kruisbee A.M., Marguiles D.H., Shevack E.M., Strober W. Current Protocols in Immunology. 1994;Wiley.
53. Wordsworth P., Pile K. Rheumatoid arthritis: etiology. Klippel J.H., Dieppo P.A. Rheumatology. 1994;3-8.1 P.A. Mosby, St. Louis.
54. Kumar V., Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell. 55:1988;145-156.
55. Hyder S.M., Stancel G.M. In vitro interaction of uterine estrogen receptor with the estrogen response element present in the 3′-flanking region of the murine c-fos protooncogene. J. Steroid Biochem. Mol. Biol. 48:1991;69-79.
56. Paech K., Webb P., Kuiper G.G., Nilsson S., Gustafsson J.et al. Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science. 277:1997;1508-1510.
57. Qin C., Singh P., Safe S. Transcriptional activation of insulin-like growth factor-binding protein-4 by 17β-estradiol in MCF-7 cells: role of estrogen receptor-Sp1 complexes. Endocrinology. 140:1999;2501-2508.
58. Suenaga R., Mitamura K., Evans M.J., Abdou N.I. Binding affinity and quantity of estrogen receptor in peripheral blood monocytes of pateints with systemic lupus erythematosus. Lupus. 5:1996;227-231.
59. Olsen N.J., Kovacs W.J. Gonadal steroids and immunity. Endocrinol. Rev. 17:1996;369-384.
60. Miller L., Hunt J.S. Sex steroids, hormones and macrophage function. Life Sci. 59:1996;1-14.
61. Kanda N., Tamaki K. Estrogen enhances immunoglobulin production by human PBMCs. J. Allergy Clin. Immunol. 103:1999;282-288.
62. Cutulo M., Sulli A., Villaggio B., Seriolo B., Accardo S. Relations between steroid hormones and cytokines in rheumatoid arthritis and systemic lupus erythematosus. Ann. Rheum. Dis. 57:1998;573-577.
63. Kanda N., Tsuchida T., Tamaki K. Estrogen enhancement of anti-double stranded DNA antibody and immunoglobulin production in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Arthritis Rheum. 42:1999;328-337.
64. Griffith J.S., Jensen S.M., Lunceford J.K., Kahn W., Zheng Y.et al. Evidence for the genetic control of estradiol-regulated responses. Am. J. Pathol. 150:1997;2223-2230.
65. Lahita R.G., Bradlow H.L., Kunkel H.G., Fisheman J. Increased 16 alpha-hydroxylation of estradiol in SLE. J. Clin. Endocrinol. Metab. 53:1981;174-178.
66. Lahita R.G. Sex hormones as immune modulators of disease. Ann. N. Y. Acad. Sci. 685:1993;278-287.
67. Jungers P., Nahoul K., Pelissier C., Dougados M., Tron F., Bach J. Low plasma androgens in women with active or quiescent systemic lupus erythematosus. Arthritis Rheum. 25:1982;454-457.
68. Arnalich F., Benito-Urbina S., Gonzalez-Gancedo P., Iglesias E., de Miguel E., Gijon-Banos J. Inadequate production of progesterone in women with systemic lupus erythematosus. Br. J. Rheumatol. 31:1992;247-251.
69. Turner R.T., Riggs B.L., Spelsberg T.C. Skeletal effects of estrogens. Endocr. Rev. 15:1994;275-300.
70. Farhat M.Y., Lavigne M.C., Ramwell P.W. The vascular protective effects of estrogen. FASEB J. 10:1996;615-624.
71. Kammer G.M. High prevalence of T cell type I protein kinase A deficiency in systemic lupus erythematosus. Arthritis Rheum. 42:1999;1458-1465.
72. Kato S., Endoh H., Masuhiro Y., Kitamoto T., Uchiyama S.et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 270:1995;1491-1494.
73. Chen D., Pace P.E., Coombes R.C., Ali S. Phosphorylation of human estrogen receptor alpha by protein kinase A regulates dimerization. Mol. Cell Biol. 19:1999;1002-1015.
74. Hall J.M., McDonnell D.P. The estrogen receptor β-isoform (ERβ) of the human estrogen receptor modulates ERα transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology. 140:1999;5566-5578.
75. Lahita R.G., Bradlow H.L., Kunkel H.G., Fishman J. Increased oxidation of testosterone in systemic lupus erythematosus. Arthritis Rheum. 26:1983;1517-1521.
76. Suenaga R., Rider V., Evans M., Abdou N.I. Estrogen receptor (ER) proteins in cultured T cell extracts from SLE patients and normal donors bind to the human estrogen response element (ERE). Arthritis Rheum. 42:1999;S311.
77. Chang C.-D., Takeda T., Mukai H., Shunton H., Takayoshi K., Tanaka C. Molecular cloning and characterization of the promoter region of the calcineurin Aα gene. Biochem. J. 288:1992;801-805.
78. Dong L., Wang W., Wang F., Stoner M., Reed J.C.et al. Mechanisms of transcriptional activation of bcl-2 gene expression by 17β-estradiol in breast cancer cells. J. Biol. Chem. 45:1999;32099-32107.
79. Loose-Mitchell D.S., Chiapetta C., Stancel G.M. Estrogen regulation of c-fos messenger ribonucleic acid. Mol. Endocrinol. 2:1988;946-951.
80. Powell J.D., Lerner C.G., Ewoldt G.R., Schwartz R.H. The -180 site of the IL-2 promoter is the target of CREB/CREM binding in T cell anergy. J. Immunol. 163:1999;6631-6639.
81. Shibata H., Spencer T.E., Onate S.A., Jenster G., Tsai T.Y., Tsai M.J.et al. Role of co-activators and co-repressors in the mechanism of steroid/thyroid receptor action. Recent Prog. Horm. Res. 52:1997;141-164.