Gender- and androgen-related influence on the expression of proto- oncogene and apoptotic factor mRNAS in lacrimal glands of autoimmune and non- autoimmune mice

Journal of Steroid Biochemistry and Molecular Biology

Volumn 71, Issue 1-2, 1999, Pages 49-61

  Toda, Ikuko ^a,b   Sullivan, Benjamin D ^a,b   Wickham, L Alexandra ^a,b   Sullivan, David A ^a,b  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; FAS ANTIGEN; FAS LIGAND; MESSENGER RNA; MYC PROTEIN; ONCOPROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; FEMALE; GENDER; GENE EXPRESSION; LACRIMAL GLAND; MALE; MOUSE; NONHUMAN; PROTO ONCOGENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SJOEGREN SYNDROME; TESTICULAR FEMINIZATION;

ANDROGENS; ANIMALS; ANTIGENS, CD95; AUTOIMMUNE DISEASES; BCL-2-ASSOCIATED X PROTEIN; FAS LIGAND PROTEIN; FEMALE; GENE EXPRESSION REGULATION; GENES, MYB; LACRIMAL APPARATUS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED MRL LPR; MICE, INBRED NOD; MICE, INBRED STRAINS; MICE, MUTANT STRAINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENES; RECEPTORS, ANDROGEN; RNA, MESSENGER; SEX FACTORS; TESTOSTERONE; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MURINAE;

EID: 0032760266     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-0760(99)00119-3     Document Type: Article

References (82)

1. Homma M., Sugai S., Tojo T., Miyasaka N., Akizuki M. Sjögren's Syndrome. State of the Art. 1994;Kugler Press, Amsterdam.
2. Ariga H., Edwards J., Sullivan D.A. Androgen control of autoimmune expression in lacrimal glands of MRL/Mp-lpr/lpr mice. Clin. Immunol. Immunopath. 53:1989;499-508.
3. Vendramini A.C., Soo C.H., Sullivan D.A. Testosterone-induced suppression of autoimmune disease in lacrimal tissue of a mouse model (NZB/NZW F1) of Sjögren's syndrome. Invest. Ophthalmol. Vis. Sci. 32:1991;3002-3006.
4. Sato E.H., Sullivan D.A. Comparative influence of steroid hormones and immunosuppressive agents on autoimmune expression in lacrimal glands of a female mouse model of Sjögren's syndrome. Invest. Ophthalmol. Vis. Sci. 35:1994;2632-2642.
5. Rocha F.J., Sato E.H., Sullivan B.D., Sullivan D.A. Effect of androgen analogue treatment and androgen withdrawal on lacrimal gland inflammation in a mouse model (MRL/Mp-lpr/lpr) of Sjögren's syndrome. Reg. Immunol. 6:1994;270-277.
6. D.A. Sullivan, J. Edwards, Androgen stimulation of lacrimal gland function in mouse models of Sjögren's syndrome. J. Ster. Biochem. Mol. Biol. (1997) 237-245.
7. Sullivan D.A. Possible mechanisms involved in the reduced tear secretion in Sjögren's syndrome. Homma M., Sugai S., Tojo T., Miyasaka N., Akizuki M. Sjögren's Syndrome. State of the Art. 1994;13-19 Kugler Press, Amsterdam.
8. I. Toda, E.M. Rocha, L.A. Silveira, L.A. Wickham, D.A. Sullivan, Gender-related difference in the extent of lymphocytic infiltration in lacrimal and salivary glands of mouse models of Sjögren's syndrome. Invest. Ophthalmol. Vis. Sci. Suppl. 34 (1997) S434.
9. Toda I., Wickham L.A., Sullivan D.A. Gender and androgen treatment influences the expression of proto-oncogenes and apoptotic factors in lacrimal and salivary tissues of MRL/lpr mice. Clin. Immunol. Immunopath. 86:1998;59-71.
10. Rocha E.M., Wickham L.A., Huang Z., Toda I., Gao J., da Silveira L.A., Sullivan D.A. Presence and testosterone influence on the levels of anti- and pro-inflammatory cytokines in lacrimal tissues of a mouse model of Sjögren's syndrome. Adv. Exp. Med. Biol. 438:1998;485-491.
11. Jabs D.A., Alexander E.L., Green W.R. Ocular inflammation in autoimmune MRL/Mp mice. Invest. Ophthalmol. Vis. Sci. 26:1985;1223-1229.
12. Ono M., Rocha F.J., Sullivan D.A. Immunocytochemical location and hormonal control of androgen receptors in lacrimal tissues of the female MRL/Mp-lpr/lpr mouse model of Sjögren's syndrome. Exp. Eye Res. 61:1995;659-666.
13. Watanabe-Fukunaga R., Brannan C.I., Copeland N.G., Jenkins N.A., Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 356:1992;314-317.
14. Adachi M., Watanabe-Fukunaga R., Nagata S. Aberrant transcription caused by the insertion of an early transposable element in an intron of the Fas antigen gene of lpr mice. Proc. Natl. Acad. Sci. USA. 90:1993;1756-1760.
15. Drappa J., Brot N., Elkon K.B. The Fas protein is expressed at high levels on CD4+CD8+ thymocytes and activated mature lymphocytes in normal mice but not in the lupus-prone strain, MRL lpr/lpr. Proc. Natl. Acad. Sci. USA. 90:1993;10340-10344.
16. Brann D.W., Hendry L.B., Mahesh V.B. Emerging diversities in the mechanism of action of steroid hormones. J. Steroid Biochem. Mol. Biol. 52:1995;113-133.
17. Kessler H.S. A laboratory model for Sjögren's syndrome. Am. J. Pathol. 52:1968;671-678.
18. Jonsson R.L., Tarkowski A., Backman K., Klareskog L. Immunohistochemical characterization of sialadenitis in NZB×NZW F1 mice. Clin. Immunol. Immunopathol. 42:1987;93-101.
19. Hoffman R.W., Alspaugh M.A., Waggie K.S., Durham J.B., Walker S.E. Sjögren's syndrome in MRL/l and MRL/n mice. Arthr. Rheum. 27:1984;157-165.
20. Jabs D.A., Prendergast R.A. Murine models of Sjögren's syndrome. Invest. Ophthalmol. Vis. Sci. 29:1988;1437-1443.
21. Theofilopoulos A.N., Dixon F.J. Murine models of systemic lupus erythematosus. Adv. Immunol. 37:1985;269-390.
22. Lieberum B., Hartmann K.U. Successive changes of the cellular composition in lymphoid organs of MRL-Mp/lpr/lpr mice during the development of lymphoproliferative disease as investigated in cryosections. Clin. Immunol. Immunopathol. 46:1988;421-431.
23. Tochino Y. The NOD mouse as a model of type 1 diabetes. CRC Crit. Rev. Immun. 8:1987;49-81.
24. Hunger R.E., Müller S., Laissue J.A., Hess M.W., Carnaud C., Garcia I., Mueller C. Inhibition of submandibular and lacrimal gland infiltration in nonobese diabetic mice by transgenic expression of soluble TNF-receptor p55. J. Clin. Invest. 98:1996;954-961.
25. Moore P.A., Bounous D.I., Kaswan R.L., Humphreys-Beher M.G. Histologic examination of the NOD-mouse lacrimal glands, a potential model for idiopathic autoimmune dacryoadenitis in Sjögren's syndrome. Lab. Anim. Sci. 46:1996;125-128.
26. Fox H.S. Androgen treatment prevents diabetes in nonobese diabetic mice. J. Exp. Med. 175:1992;1409-1412.
27. He W.W., Kumar M.V., Tindall D.J. A frame-shift mutation in the androgen receptor gene causes complete androgen insensitivity in the testicular-feminized mouse. Nucleic Acids Res. 19:1991;2373-2378.
28. Sibbitt W.L. Oncogenes, growth factors and autoimmune diseases. Anticancer Res. 11:1991;97-113.
29. Mountz J.D., Steinberg A.D., Klinman D.M., Smith H.R., Mushinski J.F. Autoimunity and increased c-myb transcription. Science. 226:1984;1087-1089.
30. Mountz J.D., Steinberg A.D. Studies of c-myb gene regulation in MRL-lpr/lpr mice. Identification of a 5′ c-myb nuclear protein binding site and high levels of binding factors in nuclear extracts of lpr-lpr lymph node cells. J. Immunol. 142:1989;328-335.
31. Kitajima T., Furukawa F., Kanauchi H., Imamura S., Ogawa K., Sugiyama T. Histological detection of c-myb and c-myc proto-oncogene expression in infiltrating cells in cutaneous lupus erythematosus-like lesions of MRL/l mice by in situ hybridization. Clin. Immunol. Immunopathol. 62:1992;119-123.
32. Skopouli F.N., Kousvelari E.E., Mertz P., Jaffe E.S., Fox P.C., Moutsopoulos H.M. c-Myc mRNA expression in minor salivary glands of patients with Sjögren's Syndrome. J. Rheumatol. 19:1992;693-696.
33. Sugai S., Saito I., Masaki Y., Takeshita S., Shimizu S., Tachibana J., Miyasaka N. Rearrangement of the rheumatoid factor-related germline gene Vg and bcl-2 expression in lymphoproliferative disorders in patients with Sjögren's Syndrome. Clin. Immunol. Immunopathol. 72:1994;181-186.
34. Watanabe D., Suda T., Hashimoto H., Nagata S. Constitutive activation of the Fas ligand gene in mouse lymphoproliferative disorders. EMBO J. 14:1995;12-18.
35. Chu J.L., Ramos P., Rosendorff A., Nikolic-Zugic J., Lacy E., Matsuzawa A., Elkon K.B. Massive upregulation of the Fas ligand in lpr and gld mice: implications for Fas regulation and the graft-versus-host disease-like wasting syndrome. J. Exp. Med. 181:1995;393-398.
36. Ogawa N., Ohashi H. Study of apoptosis in Sjögren's syndrome. Rinsho Byori-Jpn. J. Clin. Pathol. 245:1997;643-648.
37. Kong L., Ogawa N., Nakabayashi T., Liu G.T., D'Souza E., McGuff H.S., Guerrero D., Talal N., Dang H. Fas and Fas ligand expression in the salivary glands of patients with primary Sjögren's syndrome. Arthr. Rheum. 40:1997;87-97.
38. Polihronis M., Tapinos N.I., Theocharis S.E., Economou A., Kittas C., Moutsopoulos H.M. Modes of epithelial cell death in Sjögren's syndrome. J. Rheumatol. Suppl. 50:1997;37.
39. Kong L., Ogawa N., Masago R., Dang H., Talal N. Role of Bcl-2 family of proteins in the apoptotic lesions in Sjögren's syndrome. J. Rheumatol. Suppl. 50:1997;45.
40. Fox R.I., Maruyama T. Pathogenesis and treatment of Sjogren's syndrome. Curr. Opin. Rheumatol. 9:1997;393-399.
41. Emlen W., Niebur J., Kadera R. Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J. Immunol. 152:1994;3685-3692.
42. Chen S.J., Li H., Durand J., Oparil S., Chen Y.F. Estrogen reduces myointimal proliferation after balloon injury of rat carotid artery. Circulation. 93:1996;577-584.
43. Quarmby V.E., Beckman W.C. Jr., Wilson E.M., French F.S. Androgen regulation of c-myc messenger ribonucleic acid levels in rat ventral prostate. Mol. Endocrinol. 1:1987;865-874.
44. Umekita Y., Hiipakka R.A., Kokontis J.M., Liao S. Human prostate tumor growth in athymic mice: inhibition by androgens and stimulation by finasteride. Proc. Natl. Acad. Sci. USA. 93:1996;11802-11807.
45. Yoshimura I., Wu J.M., Chen Y., Ng C., Mallouh C., Backer J.M., Mendola C.E., Tazaki H. Effects of 5 alpha-dihydrotestosterone (DHT) on the transcription of nm23 and c-myc genes in human prostatic LNCaP cells. Biochem. Biophys. Res. Comm. 208:1995;603-609.
46. Musgrove E.A., Lee C.S., Sutherland R.L. Progestins both stimulate and inhibit breast cancer cell cycle progression while increasing expression of transforming growth factor alpha, epidermal growth factor receptor, c-fos, and c-myc genes. Mol. Cell. Biol. 11:1991;5032-5043.
47. Berchem G.J., Bosseler M., Sugars L.Y., Voeller H.J., Zeitlin S., Gelmann E.P. Androgens induce resistance to bcl-2-mediated apoptosis in LNCaP prostate cancer cells. Cancer Res. 55:1995;735-738.
48. Teixeira C., Reed J.C., Pratt M.A. Estrogen promotes chemotherapeutic drug resistance by a mechanism involving Bcl-2 proto-oncogene expression in human breast cancer cells. Cancer Res. 55:1995;3902-3907.
49. Chien C.H., Wang F.F., Hamilton T.C. Transcriptional activation of c-myc proto-oncogene by estrogen in human ovarian cancer cells. Mol. Cell. Endocrinol. 99:1994;11-19.
50. Suzuki A., Enari M., Eguchi Y., Matsuzawa A., Nagata S., Tsujimoto Y., Iguchi T. Involvement of Fas in regression of vaginal epithelia after ovariectomy and during an estrous cycle. EMBO J. 15:1996;211-215.
51. Suzuki A., Matsuzawa A., Iguchi T. Down regulation of Bcl-2 is the first step on Fas-mediated apoptosis of male reproductive tract. Oncogene. 13:1996;31-37.
52. Tao X.J., Tilly K.I., Maravei D.V., Shifren J.L., Krajewski S., Reed J.C., Tilly J.L., Isaacson K.B. Differential expression of members of the bcl-2 gene family in proliferative and secretory human endometrium: glandular epithelial cell apoptosis is associated with increased expression of Bax. J. Clin. Endocr. Metab. 82:1997;2738-2746.
53. McDonnell T.J., Troncoso P., Brisbay S.M., Longothetis C., Chung L.W.K., Hsieh J.T., Tu S.M., Campbell M.L. Expression of the proto-oncogene bcl-2 in the prostate and its association with emergence of androgen-independent prostate cancer. Cancer Res. 52:1992;6940-6944.
54. Wang T.T., Phang J.M. Effects of estrogen on apoptotic pathways in human breast cancer cell line MCF-7. Cancer Res. 55:1995;2487-2489.
55. Pecci A., Scholz A., Pelster D., Beato M. Progestins prevent apoptosis in a rat endometrial cell line and increase the ratio of bcl-XL to bcl-XS. J. Biol. Chem. 2272:1997;11791-11798.
56. Saegusa M., Okayasu I. Down-regulation of bcl-2 expression is closely related to squamous differentiation and progesterone therapy in endometrial carcinomas. J. Pathol. 182:1997;429-436.
57. Hann L.E., Kelleher R.S., Sullivan D.A. Influence of culture conditions on the androgen control of secretory component production by acinar cells from the lacrimal gland. Invest. Ophthalmol. Vis. Sci. 32:1991;2610-2621.
58. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
59. Lai K.N., Ho R.T.H., Leung J.C.K., Chui Y.L., Lim P.L., Lui S.F., Li P.K.T. CD4-positive cells from patients with IgA nephropathy demonstrate increased mRNA of cytokines that induce the IgA switch and differentiation. J. Pathol. 174:1994;13-22.
60. Zheng J., Rudra-Ganguly N., Miller G.J., Moffat K.A., Colte R.J., Roy-Burman P. Steroid hormone induction and expression patterns of L-plastin in normal and carcinomatous prostates. Am. J. Pathol. 150:1997;2009-2018.
61. Gaspar M.L., Meo T., Tosi M. Structure and size distribution of the androgen receptor mRNA in wild-type and Tfm/Y mutant mice. Mol. Endocrinol. 4:1990;1600-1610.
62. Lubahn D.B., Joseph D.R., Sullivan P.R., Willard H.F., French F.S., Wilson E.M. Cloning of human androgen receptor complementary DNA and localization to the X chromosome. Science. 240:1988;327-330.
63. Sullivan D.A., Wickham L.A., Rocha E.M., Kelleher R.S., da Silveira L.A., Toda I. Influence of gender, sex steroid hormones and the hypothalamic-pituitary axis on the structure and function of the lacrimal gland. Adv. Exp. Med. Biol. 438:1998;11-42.
64. Verheul H.A., Verveld M., Hoefakker S., Schuurs A.H. Effects of ethinylestradiol on the course of spontaneous autoimmune disease in NZB/W and NOD mice. Immunopharmacol. Immunotoxicol. 17:1995;163-180.
65. Pearce R.B., Formby B., Healy K., Peterson C.M. Association of an androgen-responsive T cell phenotype with murine diabetes and Idd2. Autoimmunity. 20:1995;247-258.
66. Wu J., Wang M., Li X., Sheng Y. Conformation changes of p53 proteins in regulation of murine T lymphocyte proliferation. Cell. Mol. Biol. Res. 39:1993;27-31.
67. Garchon H.J., Luan J.J., Eloy L., Bedossa P., Bach J.F. Genetic analysis of immune dysfunction in non-obese diabetic (NOD) mice: mapping of a susceptibility locus close to the Bcl-2 gene correlates with increased resistance of NOD T cells to apoptosis induction. Eur. J. Immunol. 24:1994;380-384.
68. Sullivan D.A., Hann L.E. Hormonal influence on the secretory immune system of the eye: endocrine impact on the lacrimal gland accumulation and secretion of IgA and IgG. J. Steroid Biochem. 34:1989;253-262.
69. Giordano C., Stassi G., Todaro M., De Maria R., Richiusa P., Scorsone A., Giordano M., Galluzzo A. Low bcl-2 expression and increased spontaneous apoptosis in T-lymphocytes from newly-diagnosed IDDM patients. Diabetologia. 38:1995;953-958.
70. Riu E., Bosch F., Valera A. Prevention of diabetic alterations in transgenic mice overexpressing Myc in the liver. Proc. Natl. Acad. Sci. USA. 93:1996;2198-2202.
71. Thompson D.B., de Gregorio M., Sommercorn J. Insulin regulation of multiple ribonucleic acid species in human skeletal muscle in insulin-sensitive and insulin-resistant subjects. J. Clin. Endocrinol. Metab. 81:1996;519-523.
72. Chen Z.P., Yeung D.C. Regulation of p53 expression in HeLa cells. Biochem. Mol. Biol. Int. 38:1996;607-616.
73. Krajewski S., Krajewska M., Shabaik A., Miyashita T., Wang H.G., Reed J.C. Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145:1994;1323-1336.
74. Murphy L., O'Shaughnessy P.J. Testicular steroidogenesis in the testicular feminized (Tfm) mouse: loss of 17α-hydroxylase activity. J. Endocrinol. 131:1991;443-449.
75. Sullivan D.A. Sex hormones and Sjögren's syndrome. J. Rheumatol. 24:(Suppl. 50):1997;17-32.
76. K. Skarstein, R. Jonsson. The apoptosis related APO-1/Fas (CD95) receptor is expressed in MRL/lpr mice despite defects in the Fas gene. Clin. Rheum. Suppl. 14 (1995) 27.
77. Bargou R.C., Daniel P.T., Mapara M.Y., Bommert K., Wagener C., Kallinich B., Royer H.D., Dorken B. Expression of the bcl-2 gene family in normal and malignant breast tissue: low Bax-alpha expression in tumor cells correlates with resistance towards apoptosis. Int. J. Cancer. 60:1995;854-859.
78. Lanoix J., D'Agati V., Szabolcs M., Trudel M. Dysregulation of cellular proliferation and apoptosis mediates human autosomal dominant polycystic kidney disease (ADPKD). Oncogene. 13:1996;1153-1160.
79. French L.E., Tschopp J. Constitutive Fas ligand expression in several non-lymphoid mouse tissues: implications for immune-protection and cell turnover. Behring Inst. Mitt. 97:1996;156-160.
80. Vaux D.L., Strasser A. The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA. 93:1996;2239-2244.
81. Tan E.M. Autoimmunity and apoptosis. J. Exp. Med. 179:1994;1083-1086.
82. Negrini M., Silini E., Kozak C., Tsujimoto Y., Croce C.M. Molecular analysis of mbcl-2: structure and expression of the murine gene homologous to the human gene involved in follicular lymphoma. Cell. 49:1987;455-463.