17β-estradiol and interferon tau interact in the regulation of the immune response in a model of experimental autoimmune orchitis

Journal of Interferon and Cytokine Research

Volumn 31, Issue 11, 2011, Pages 825-837

  Maj, Tomasz ^a   Sławek, Anna ^a   Kaleta Kuratewicz, Katarzyna ^b   Chełmońska Soyta, Anna ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b WROC AW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; TAU INTERFERON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE ORCHITIS; GERM CELL TUMOR; HYPERSENSITIVITY; IMMUNE RESPONSE; MALE; MOUSE; NONHUMAN; ORCHITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; SPLEEN CELL;

ANIMALS; AUTOIMMUNE DISEASES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ESTRADIOL; INTERFERON TYPE I; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; ORCHITIS; PREGNANCY PROTEINS;

MUS;

EID: 80955136675     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2010.0147     Document Type: Article

References (61)

1. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. 2000. Immunobiology of dendritic cells. Annu Rev Immunol 18:767-811. (Pubitemid 30365397)
2. Bebo BF Jr., Fyfe-Johnson A, Adlard K, Beam AG, Vandenbark AA, Offner H. 2001. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J Immunol 166:2080-2089. (Pubitemid 32114698)
3. Bossie A, Brooks KH, Krammer PH, Vitetta ES. 1987. Activation of murine B cells from different tissues with different mitogens. II. Isotype distribution of secreted immunoglobulins in the presence and absence of IL-4-containing T cell supernatants. J Mol Cell Immunol 3:221-226.
4. Carreras E, Turner S, Paharkova-Vatchkova V, Mao A, Dascher C, Kovats S. 2008. Estradiol acts directly on bone marrow myeloid progenitors to differentially regulate GM-CSF or Flt3 ligand-mediated dendritic cell differentiation. J Immunol 180:727-738.
5. Chao T, Alten PV, Greager JA, Walters RJ. 1995. Steroid sex hormones regulate the release of tumor necrosis factor by macrophages. Cell Immunol 160:43-49.
6. Chaouat G, Assal Meliani A, Martal J, Raghupathy R, Elliott JF, Mosmann T, Wegmann TG. 1995. IL-10 prevents naturally occurring fetal loss in the CBA x DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-Tau. J Immunol 154:4261-4268.
7. Cook J, Johnson L, O'Connor JC, Biegel LB, Krams CH, Frame SR, Hurtt ME.1988. Effects of dietary 17 β- estradiol exposure on serum hormoe concentrations and testicular parameters in male Crl:CD BR rats. Toxicol Sci 44:155-168.
8. Dai R, Phillips RA, Karpuzoglu E, Khan D, Ahmed SA. 2009. Estrogen regulates transcription factors STAT-1 and NF-kB to promote inducible nitric oxide synthase and inflammatory responses. J Immunol 183:6998-7005.
9. Dhaher YY, Greenstein BD, Khamashta MA, Hughes GR. 2001. Effects of oestradiol and the oestrogen antagonist ICI 182,780 on the delayed type hypersensitivity (DTH) index and on serum levels of IgM and IgG in ovariectomised Balb/C and MRL/Mp-Lpr/Lpr mice, a model of systemic lupus erythematosus (SLE). Autoimmunity 33:237-243. (Pubitemid 32834215)
10. Douin-Echinard V, Laffont S, Seillet C, Delpy L, Krust A, Chambon P, Gourdy P, Arnal JF, Guery JC. 2008. Estrogen receptor a, but not b, is required for optimal dendritic cell differentiation and CD40-induced cytokine production. J Immunol 180:3661-3669.
11. Delpy L, Douin-Echinard V, Garidou L, Bruand C, Saoudi A, Guery JC. 2005. Estrogen enhances susceptibility to experimental autoimmune myasthenia gravis by promoting type 1- polarized immune responses. J Immunol 175:5050-5057. (Pubitemid 41456388)
12. Dulos J, Hofstra CL, Joosten LAB, Veening-Griffioen DH, Lucassen MA, Doorn CM, Graaf JH, Miltenburg AMM, Dijcks FA, Ederveen TH, Bootset AMH. 2006. A selective estrogen receptor alpha agonist (Org 37663) suppresses inflammation and arthritis in mouse models. Ann Rheum Dis 65(SupplII): 1289.
13. EllosoMM, Phiel K, Henderson RA, Harris HA, Adelman SJ. 2005. Suppression of experimental autoimmune encephalomyelitis using estrogen receptor-selective ligands. J Endocrinol 182:243-252. (Pubitemid 40691791)
14. Facchetti F, Tironi A, Marocolo D, Capucci A, Ruggeri G, Bellotti D, Rossi G. 1997. Histopathological changes in bone marrow biopsies from patients with chronic myeloid leukaemia after treatment with recombinant alpha-interferon. Histopathology 31:3-11. (Pubitemid 27314499)
15. Feng F, Nyland J, Banyai M, Tatum A, Silverstone AE, Gavalchin J. 2010. The induction of the lupus phenotype by estrogen is via an estrogen receptor-Alpha-dependent pathway. Clin Immunol 134:226-236.
16. Fleming JGW, Choi Y, Johnson GA, Spencer TE, Bazer FW. 2001. Cloning of the ovine estrogen receptor-A promoter and functional regulation by ovine interferon-T. Endocrinology 142: 2879-2887. (Pubitemid 32575523)
17. Goodin DS. 2005. Treatment of multiple sclerosis with human beta interferon. Int MS J 12:96-108. (Pubitemid 41712027)
18. Gordon MN, Osterburg HH, May PC, Finch CE. 1986. Effective oral administration of 17-beta-estradiol to female C57BL/6J mice through the drinking water. Biol Reprod 35:1088-1095. (Pubitemid 17010451)
19. Gourdy P, Araujo LM, Zhu R, Garmy-Susini B, Diem S, Laurell H, Leite-de-Moraes M, Dy M, Arnal JF, Bayard F, Herbelin A. 2005. Relevance of sexual dimorphism to regulatory T cells: Estradiol promotes IFN-γ production by invariant natural killer T cells. Blood 105:2415-2420. (Pubitemid 40387040)
20. Hemelaar M, Kenemans P, Schalkwijk CG, Braat DD, Van Der Mooren MJ. 2006. No increase in C-reactive protein levels during intranasal compared to oral hormone therapy in healthy post-menopausal women. Hum Reprod 21:1635-1642. (Pubitemid 44445048)
21. Hosoda T, Mito N, Yoshino H, Sato K. 2004. Estrogen altered oral tolerance induction in type II collagen-induced murine arthritis. Int Arch Allergy Immunol 133:19-28. (Pubitemid 38199396)
22. Huber SA, Kupperman J, Newell MK. 1999. Estradiol prevents and testosterone promotes Fas-dependent apoptosis in CD4+ Th2 cells by altering Bcl-2 expression. Lupus 8:384-387. (Pubitemid 29378019)
23. Ito A, Bebo B Jr., Matejuk A, Zamora A, Silverman M, Fyfe-Johnson A, Offner H. 2006. Estrogen treatment downregulates TNF-Alpha production and reduces the severity of experimental autoimmune encephalomyelitis in cytokine knockout mice. J Immunol 167:542-552. (Pubitemid 32567822)
24. Itoh M, Hiramine C, Hojo K. 1991. A new murine model of autoimmune orchitis induced by immunization with viable syngeneic testicular germ cells alone. I. Immunological and histological studies. Clin Exp Immunol 83:137-142.
25. Itoh M, Yano A, Xie Q, Iwahashi K, Takeuchi Y, Meroni PL, Nicoletti F. 1998. Essential pathogenic role for endogenous interferon-gamma (IFN-γamma) during disease onset phase of murine experimental autoimmune orchitis. I. In vivo studies. Clin Exp Immunol 111:513-520. (Pubitemid 28160893)
26. Kaneko T, Itoh M, Nakamura Y, Iimura A, Hayashi S, Takahashi K, Stivala F, Bendtzen K, Nicoletti F. 2003. Proinflammatory effects of exogenously administered IL-10 in experimental autoimmune orchitis. Cytokine 22:50-53.
27. Kawasaki T, Choudhry MA, Suzuki T, Schwacha MG, Bland KI, Chaudry IH. 2008. 17beta-Estradiol's salutary effects on splenic dendritic cell functions following trauma-hemorrhage are mediated via estrogen receptor-Alpha. Mol Immunol 45:376-385. (Pubitemid 47332641)
28. Lengi AJ, Phillips RA, Karpuzoglu E, Ahmed SA. 2006. 17ß- Estradiol downregulates interferon regulatory factor-1 in murine splenocytes. J Mol Endocirnol 37:421-432. (Pubitemid 46085168)
29. Li J, McMurray RW. 2006. Effects of estrogen receptor subtypeselective agonists on immune functions in ovariectomized mice. Int Immunopharmacol 6:1413-1423. (Pubitemid 44038682)
30. Liu HY, Buenafe AC, Matejuk A, Ito A, Zamora A, Dwyer J, Vandenbark AA, Offner H. 2002. Estrogen inhibition of EAE involves effects on dendritic cell function. J Neurosci Res 70:238-248.
31. Lutz MB, Kukutsch N, Ogilvie AL, RÖssner S, Koch F, Romani N, Schuler G. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223:77-92. (Pubitemid 29096240)
32. Maggiolini M, Picard D. 2010. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J Endocrinol 204: 105-114.
33. Matsuzaki G, Sonoda KH, Mukasa A, Yamada H, Nakamura T, Ikebe H, Hamano S, Nomoto K. 1997. The characterization of testicular cell (TC)-specific T-cell clones induced by intratesticular Listeria monocytogenes infection: TC-specific T cells with atypical cytokine profile transfer orchitis. Immunology 91:520-528. (Pubitemid 27312332)
34. McCombe PA, Greer JM, Mackay IR. 2009. Sexual dimorphism in autoimmune disease. Curr Mol Med 9:1058-1079.
35. Mukasa A, Yoshida H, Kobayashi N, Matsuzaki G, Nomoto K. 1998. Gamma delta T cells in infection-induced and autoimmune- induced testicular inflammation. Immunology 95:395-401. (Pubitemid 28505696)
36. Panchanathan R, Shen H, Bupp MG, Gould KA, Choubey D. 2009. Female and male sex hormones differentially regulate expression of Ifi202, an interferon-inducible lupus susceptibility gene within the Nba2 interval. J Immunol 183:7031-7038.
37. Polanczyk M, Zamora A, Subramanian S, Matejuk A, Hess DL, Blankenhorn EP, Teuscher C, Vandenbark AA, Offner H. 2003. The protective effect of 17beta-estradiol on experimental autoimmune encephalomyelitis is mediated through estrogen receptor-Alpha. Am J Pathol 2163:1599-1605. (Pubitemid 37175106)
38. Polanczyk MJ, Jones RE, Subramanian S, Afentoulis M, Rich C, Zakroczymski M, Cooke P, Vandenbark AA, Offner H. 2004. T lymphocytes do not directly mediate the protective effect of estrogen on experimental autoimmune encephalomyelitis. Am J Pathol 165:2069-2077. (Pubitemid 39578384)
39. Ramanujam M, Kahn P, Huang W, Tao H, Madaio MP, Factor SM, Davidson A. 2009. Interferon-Alpha treatment of female (NZW x BXSB)F(1) mice mimics some but not all features associated with the Yaa mutation. Arthritis Rheum 60:1096-1101.
40. Rival C, Guazzone VA, von Wulffen W, Hackstein H, Schneider E, Lustig L, Meinhardt A, Fijak M. 2007. Expression of costimulatory molecules, chemokine receptors and proinflammatory cytokines in dendritic cells from normal and chronically inflamed rat testis. Mol Hum Reprod 13:853-861.
41. Rosenthal GJ, Stranahan RP III, Thompson M, Blair P, Germolec DR, Comment CE, Schwab K, Luster MI. 1989. Organ-specific hematopoietic changes induced by a recombinant human interferon-Alpha in mice. Fundam Appl Toxicol 14:666-675.
42. Roubinian JR, Talal N, Greenspan JS, Goodman JR, Siiteri PK. 1978. Effect of castration and sex hormone treatment on survival, anti-nucleic acid antibodies, and glomerulonephritis in NZB/NZW F1 mice. J Exp Med 147:1568-1583. (Pubitemid 8372952)
43. Shifren JL, Rifai N, Desindes S, McIlwain M, Doros G, Mazer NA. 2008. A comparison of the short-Term effects of oral conjugated equine estrogens versus transdermal estradiol on C-reactive protein, other serum markers of inflammation, and other hepatic proteins in naturally menopausal women. J Clin Endocrinol Metab 93:1702-1710. (Pubitemid 351656508)
44. Snapper CM, Paul WE. 1987. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236:944-947. (Pubitemid 17107942)
45. Sobel DO, Ahvazi B, Amjad F, Mitnaul L, Pontzer C. 2008. Interferon-Tau inhibits the development of diabetes in NOD mice. Autoimmunity 41:543-553.
46. Soos JM, Mujtaba MG, Subramaniam PS, Streit WJ, Johnson HM. 1997. Oral feeding of interferon tau can prevent the acute and chronic relapsing forms of experimental allergic encephalomyelitis. J Neuroimmunol 75:43-50. (Pubitemid 27170301)
47. Soos JM, Stüve O, Youssef S, Bravo M, Johnson HM, Weiner HL, Zamvil SS. 2002. Cutting edge: Oral type I IFN-T promotes a Th2 bias and enhances suppression of autoimmune encephalomyelitis by oral glatiramer acetate. J Immunol 169:2231-2235. (Pubitemid 34920961)
48. Spencer TE, Bazer FW. 1996. Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinology 137:1144-1147. (Pubitemid 26074139)
49. Stevens TL, Bossie A, Sanders VM, Fernandez-Botran R, Coffman RL, Mosmann TR, Vitetta ES. 1998. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334:255-258.
50. Stübgen JP. 2009. Interferon alpha and neuromuscular disorders. J Neuroimmunol 207: 3-17.
51. Subramaniam PS, Khan SA, Pontzer CH, Johnson HM. 1995. Differential recognition of the type I interferon receptor by interferons tau and alpha is responsible for their disparate cytotoxicities. PNAS 92:12270-12274. (Pubitemid 26014052)
52. Suzuki T, Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH. 2007a. Estrogen receptor-Alpha predominantly mediates the salutary effects of 17beta-estradiol on splenic macrophages following trauma-hemorrhage. Am J Physiol Cell Physiol 293:C978-C984. (Pubitemid 47437387)
53. Suzuki T, Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Chaudry IH. 2007b. Salutary effects of 17beta-estradiol on T-cell signaling and cytokine production after trauma-hemorrhage are mediated primarily via estrogen receptor-Alpha. Am J Physiol Cell Physiol 292:C2103-C2111. (Pubitemid 47080523)
54. Tadokoro CE, Abrahamsohn IA. 2001. Bone marrow-derived macrophages grown in GM-CSF or M-CSF differ in their ability to produce IL-12 and to induce IFN-γ production after stimulation with Trypanosoma cruzi antigens. Immunol Lett 77:31-38. (Pubitemid 32434413)
55. Tokunaga Y, Terayama H, Naito M, Qu N, Hirai S, Ogawa Y, Yi SQ, Itoh M. 2008. Splenic cytokines in mice immunized with testicular germ cells. Int J Androl 31:471-476.
56. Toyama Y, Hosoi I, Ichikawa S, Maruoka M, Yashiro E, Ito H, Yuasa S. 2001. β-estradiol 3-benzoate affects spermatogenesis in the adult mouse. Mol Cell Endocrinol 178:161-168. (Pubitemid 32519604)
57. Van Holten J, Reedquist K, Sattonet-Roche P, Smeets TJM, Plater-Zyberk C, Vervooldeldonk MJ, Tak PP. 2004. Treatment with recombinant interferon-beta reduces inflammation and slows cartilage destruction in the collagen-induced arthritis model of rheumatoid arthritis. Arthritis Res Ther 6:R239-R249.
58. Webb P, Lopez GN, Greene GL, Baxter JD, Kushner PJ. 1992. The limits of the cellular capacity to mediate an estrogen response. Mol Endocrinol 6:157-167.
59. Whitacre CC. 2001. Sex differences in autoimmune disease. Nat Immunol 2:777-780.
60. Yoshimoto T, Okada K, Morishima N, Kamiya S, Owaki T, Asakawa M, Iwakura Y, Fukai F, Mizuguchi J. 2004. Induction of IgG2a Class Switching in B Cells by IL-27. J Immunol 173:2479-2485. (Pubitemid 39063105)
61. Zhu WH, Huang YM, Link H, Xiao BG. 2007. A putative mechanism on remission of multiple sclerosis during pregnancy: Estrogen-induced indoleamine 2,3-dioxygenase by dendritic cells. Multiple Sclerosis 13:33-40. (Pubitemid 46152759)