Female and male sex hormones differentially regulate expression of Ifi202, an interferon-inducible lupus susceptibility gene within the Nba2 interval

Journal of Immunology

Volumn 183, Issue 11, 2009, Pages 7031-7038

  Panchanathan, Ravichandran ^a   Shen, Hui ^a   Bupp, Melanie Gubbels ^b,d   Gould, Karen A ^c   Choubey, Divaker ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d ROCHE BIOSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ANDROSTANOLONE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; ANDROGEN; ESTROGEN; IFI202B PROTEIN, MOUSE; SEX HORMONE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DRUG ACTIVITY; DRUG PROTEIN BINDING; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEX DIFFERENCE; SPLEEN CELL; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; UPREGULATION; ANIMAL; BIOSYNTHESIS; CHROMATIN IMMUNOPRECIPITATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; METABOLISM; NEW ZEALAND BLACK MOUSE; ORCHIECTOMY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT; WESTERN BLOTTING;

ANDROGENS; ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; DIHYDROTESTOSTERONE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GONADAL STEROID HORMONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MICE, INBRED NZB; ORCHIECTOMY; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX CHARACTERISTICS; T-LYMPHOCYTES;

EID: 73349110966     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802665     Document Type: Article

References (51)

1. Whitacre, C. C. 2001. Sex differences in autoimmune disease. Nat. Immunol. 2: 777-780.
2. Rider, V., and N. I. Abdou. 2001. Gender differences in autoimmunity: molecular basis for estrogen effects in systemic lupus erythematosus. Int. Immunopharmacol. 1: 1009-1024. (Pubitemid 32434421)
3. Cohen-Solal, J. F., V. Jeganathan, C. M. Grimaldi, E. Peeva, and B. Diamond. 2006. Sex hormones and SLE: influencing the fate of autoreactive B cells. Curr. Top. Microbiol. Immunol. 305: 67-88.
4. Zandman-Goddard, G., E. Peeva, and Y. Shoenfeld. 2007. Gender and autoimmunity. Autoimmun. Rev. 6: 366-372.
5. Tsokos, G. C., and G. M. Kammer. 2000. Molecular aberrations in human systemic lupus erythematosus. Mol. Med. Today 6: 418-424.
6. Kotzin, B. L. 1996. Systemic lupus erythematosus. Cell 85: 303-306.
7. Banchereau, J., and V. Pascual. 2006. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 25: 383-392. (Pubitemid 44354221)
8. Jorgensen, T. N., M. R. Gubbels, and B. L. Kotzin. 2004. New insights into disease pathogenesis from mouse lupus genetics. Curr. Opin. Immunol. 16: 787-793. (Pubitemid 39423670)
9. Zhu, J., and C. Mohan. 2007. SLE 1, 2, 3 ... genetic dissection of lupus. Adv. Exp. Med. Biol. 601: 85-95.
10. Haywood, M. E. K., S. J. Rose, S. Horswell, M. J. Lees, G. Fu, M. J. Walport, and B. J. Morley. 2006. Overlapping BXSB congenic intervals, in combination with microarray gene expression, reveal novel lupus candidate genes. Genes Immun. 7: 250-263.
11. Liu, J., G. Karypis, A. L. Vegoe, P. Ruiz, G. S. Gilkeson, and T. W. Behrens. 2006. Genomic view of systemic autoimmunity in MRL/lpr mice. Genes Immun. 7: 156-168. (Pubitemid 43336058)
12. Theofilopoulos, A. N., R. Baccala, B. Beutler, and D. H. Kono. 2005. Type I interferon (α/β) in immunity and autoimmunity. Annu. Rev. Immunol. 23: 307-336.
13. Roubinian, J. R., R. Papoian, and N. Talal. 1977. Androgenic hormones modulate autoantibody response and improve survival in murine lupus. J. Clin. Invest. 59: 1066-1070.
14. 1 mice. J. Exp. Med. 147: 1568-1583.
15. Carroll, J. S., and M. Brown. 2006. Estrogen receptor target gene: an evolving concept. Mol. Endocrinol. 20: 1707-1714. (Pubitemid 44148078)
16. Deroo, B. J., and K. S. Korach. 2006. Estrogen receptors and human disease. J. Clin. Invest. 116: 561-570.
17. Erlandsson, M. C., C. Ohlsson, J. A. Gustafsson, and H. Carlsten. 2001. Role of oestrogen receptors-α and -β in immune organ development and in oestrogenmediated effects on thymus. Immunology 103: 17-25.
18. Svenson, J. L., J. Eudaly, P. Ruiz, K. S. Korach, and G. S. Gilkeson. 2008. Impact of estrogen receptor deficiency on disease expression in the NZM2410 lupus prone mouse. Clin. Immunol. 128: 259-268.
19. Li, J., and R.W. McMurray. 2007. Effects of estrogen receptor subtype-selective agonists on autoimmune disease in lupus-prone NZB/NZW F1 mouse model. Clin. Immunol. 123: 219-226. (Pubitemid 46591958)
20. Bynoté, K. K., J. M. Hackenberg, K. S. Korach, D. B. Lubahn, P. H. Lane, and K. A. Gould. 2008. Estrogen receptor-α deficiency attenuates autoimmune disease in (NZB x NZW)F1 mice. Genes Immun. 9: 137-152.
21. Kato, S., L. Tora, J. Yamauchi, S. Masushige, M. Bellard, and P. Chambon. 1992. A far upstream estrogen response element of the ovalbumin gene contains several half-palindromic 5′-TGACC-3′ motifs acting synergistically. Cell 68: 731-742.
22. Heemers, H. V., and D. J. Tindall. 2007. Androgen receptor (AR) coregulators: a diversity of functions converging on and regulating the AR transcriptional complex. Endocr. Rev. 28: 778-808.
23. Liva, S. M., and R. R. Voskuhl. 2001. Testosterone acts directly on CD4 T lymphocytes to increase IL-10 production. J. Immunol. 167: 2060-2067.
24. Choubey, D., J. Snoddy, V. Chaturvedi, E. Toniato, G. Opdenakker, A. Thakur, H. Samanta, D. A. Engel, and P. Lengyel. 1989. Interferons as gene activators: indications for repeated gene duplication during the evolution of a cluster of interferon-activatable genes on murine chromosome 1. J. Biol. Chem. 264: 17182-17189. (Pubitemid 19255549)
25. Choubey, D. 2000. p202: an interferon-inducible negative regulator of cell growth. J. Biol. Regul. Homeost. Agents 14: 187-192.
26. Choubey, D., and B. L. Kotzin. 2002. Interferon-inducible p202 in the susceptibility to systemic lupus. Front. Biosci. 7: e252-e262.
27. Wang, C., G. Chatterjee, J. J. Meyer, C. J. Liu, N. A. Manunath, P. Bray-Ward, and P. Lengyel. 1999. Characteristics of three homologous 202 genes (Ifi202a, Ifi202b, and Ifi202c) from the murine interferon-activatable gene 200 cluster. Genomics 60: 281-294.
28. Ludlow, L. E., R. W. Johnstone, and C. J. Clark. 2005. The HIN-200 family: more than interferon-inducible genes? Exp. Cell Res. 308: 1-17. (Pubitemid 40984758)
29. Roberts, T. L., A. Idris, J. A. Dunn, G. M. Kelly, C. M. Burnton, S. Hodgson, L. L. Hardy, V. Garceau, M. J. Sweet, I. L. Ross, et al. 2009. Hin-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323: 1057-1060.
30. Bürckstümmer, T., C. Baumann, S. Blüml, E. Dixit, G. Dürnberger, H. Jahn, M. Planyavsky, M. Bilban, J. Colinge, K. L. Bennett, and G. Superti-Furga. 2009. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10: 266-272.
31. Choubey, D., and P. Lengyel. 1993. Interferon action: cytoplasmic and nuclear localization of the interferon-inducible 52-kD protein that is encoded by the Ifi202 gene from the gene 200 cluster. J. Interferon Res. 13: 43-52. (Pubitemid 23078365)
32. Rozzo, S. J., J. D. Allard, D. Choubey, T. J. Vyse, S. Izui, G. Peltz, and B. L. Kotzin. 2001. Evidence for an interferon-inducible gene, Ifi202, in the susceptibility to systemic lupus. Immunity 15: 435-443.
33. Choubey, D. 2008. Comment on: The candidate lupus susceptibility gene Ifi202a is largely dispensable for B-cell function. Rheumatology 47: 558-559.
34. Gubbels, M. R., T. N. Jorgensen, T. E. Metzger, K. Menze, H. Steele, S. A. Flannery, S. J. Rozzo, and B. L. Kotzin. 2005. Effects of MHC and gender on lupus-like autoimmunity in Nba2 congenic mice. J. Immunol. 175: 6190-6196.
35. Gubbels, M. R., T. N. Jorgensen, and B. L. Kotzin. 2008. Identification of candidate genes that influence sex hormone-dependent disease phenotypes in mouse lupus. Genes Immun. 9: 47-56.
36. Xin, H., S. D'Souza, T. N. Jorgensen, A. T. Vaughan, P. Lengyel, B. L. Kotzin, and D. Choubey. 2006. Increased expression of Ifi202, an IFN-activatable gene, in B6.Nba2 lupus susceptible mice inhibits p53-mediated apoptosis. J. Immunol. 176: 5863-5870.
37. Zinser, G. M., K. McEleney, and J. Welsh. 2003. Characterization of mammary tumor cell lines from wild type and vitamin D3 receptor knockout mice. Mol. Cell. Endocrinol. 200: 67-80.
38. Stefano, G. B., V. Prevot, J. C. Beauvillain, C. Fimiani, I. Welters, P. Cadet, C. Breton, J. Pestel, M. Salzet, and T. V. Bilfinger. 1999. Estradiol coupling to human monocytes nitric oxide release is dependent on intracellular calcium transients: evidence for an estrogen surface receptor. J. Immunol. 163: 3758-3763.
39. Tora, L., J. White, C. Brou, D. Tasset, N. Webster, E. Scheer, and P. Chambon. 1989. The human estrogen receptor has two independent non-acidic transcriptional activation functions. Cell 59: 477-487. (Pubitemid 19284461)
40. Xin, H., Y. Geng, R. Pramanik, and D. Choubey. 2003. Induction of p202, a modulator of apoptosis, during oncogenic transformation of NIH 3T3 cells by activated H-Ras (Q61L) contributes to cell survival. J. Cell. Biochem. 88: 191-204. (Pubitemid 36015088)
41. Panchanathan, R., H. Xin, and D. Choubey. 2008. Disruption of mutually negative regulatory feedback loop between interferon-inducible p202 protein and the E2F family of transcription factors in lupus-prone mice. J. Immunol. 180: 5927-5934.
42. Nalbandian, G., V. Paharkova-Vatchkova, A. Mao, S. Nale, and S. Kovats. 2005. The selective estrogen receptor modulators, tamoxifen and raloxifene, impair dendritic cell differentiation and activation. J. Immunol. 175: 2666-2675. (Pubitemid 41113882)
43. Bynoe, M. S., C. M. Grimaldi, and B. Diamond. 2000. Estrogen up-regulates Bcl-2 and blocks tolerance induction of naive B cells. Proc. Natl. Acad. Sci. USA 97: 2703-2708.
44. Grimaldi, C. M., D. J. Michael, and B. Diamond. 2001. Expansion and activation of a population of auto-reactive marginal zone B cells in a model of estrogeninduced lupus. J. Immunol. 167: 1886-1890.
45. Grimaldi, C. M., J. Cleary, A. S. Dagtas, D. Moussai, and B. Diamond. 2002. Estrogen alters thresholds for B cell apoptosis and activation. J. Clin. Invest. 109: 1625-1633.
46. D'Souza, S., H. Xin, S. Walter, and D. Choubey. 2001. The gene encoding p202, an interferon-inducible negative regulator of the p53 tumor suppressor, is a target of p53-mediated transcriptional repression. J. Biol. Chem. 276: 298-305. (Pubitemid 32050320)
47. Couse, J. F., M. M. Yates, V. R. Walker, and K. S. Korach. 2003. Characterization of the hypothalamic-pituitary-gonadal axis in estrogen receptor (ER) null mice reveals hypergonadism and endocrine sex reversal in females lacking ERα but not ERβ. Mol. Endocrinol. 17: 1039-1053.
48. Li, J., and R. W. McMurray. 2006. Effects of estrogen receptor subtype-selective agonists on immune functions in ovariectomized mice. Int. Immunopharmacol. 6: 1413-1423. (Pubitemid 44038682)
49. Siracusa, M. C., M. G. Overstreet, F. Housseau, A. L. Scott, and S. L. Klein. 2008. 17β-Estradiol alters the activity of conventional and IFN-producing killer dendritic cells. J. Immunol. 180: 1423-1431.
50. Peeva, E., J. Venkatesh, and B. Diamond. 2005. Tamoxifen blocks estrogen induced B cell maturation but not survival. J. Immunol. 175: 1415-1423. (Pubitemid 41023040)
51. Olsen, N. J., X. Gu, and W. J. Kovacs. 2001. Bone marrow stromal cells mediate androgenic suppression of B lymphocyte development. J. Clin. Invest. 108: 1697-1704.