Effect of medical castration on CD4+CD25+ T cells, CD8+ T cell IFN-γ expression, and NK cells: A physiological role for testosterone and/or its metabolites

American Journal of Physiology - Endocrinology and Metabolism

Volumn 290, Issue 5, 2006, Pages

  Page, Stephanie T ^a   Plymate, Stephen R ^a,b   Bremner, William J ^a   Matsumoto, Alvin M ^a,b   Hess, David L ^c   Lin, Daniel W ^a   Amory, John K ^a   Nelson, Peter S ^d   Wu, Jennifer D ^a,e  

^a UNIVERSITY OF WASHINGTON   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e Box 359625 ^*  (United States)

Author keywords

Gonadotropin releasing hormone antagonist; Interferon ; Regulatory T cells; Testosterone replacement

Indexed keywords

ACYLINE; ANDROSTANOLONE; CHEMOKINE RECEPTOR CXCR1; ESTRADIOL; GAMMA INTERFERON; GONADORELIN ANTAGONIST; NATURAL KILLER CELL RECEPTOR NKG2D; PLACEBO; TESTOSTERONE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BLOOD SAMPLING; CASTRATION; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFECT; HORMONE BLOOD LEVEL; HORMONE SUBSTITUTION; HUMAN; HUMAN EXPERIMENT; MALE; NATURAL KILLER CELL; NORMAL HUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; CD4-CD8 RATIO; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DIHYDROTESTOSTERONE; ESTRADIOL; GONADOTROPIN-RELEASING HORMONE; HUMANS; INTERFERON TYPE II; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; OLIGOPEPTIDES; RECEPTORS, IMMUNOLOGIC; RECEPTORS, INTERLEUKIN-2; RECEPTORS, INTERLEUKIN-8A; T-LYMPHOCYTE SUBSETS; TESTOSTERONE; TETRADECANOYLPHORBOL ACETATE;

EID: 33646432202     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00484.2005     Document Type: Article

References (49)

1. + T cells: optimal soldiers in the war against viruses and tumors. Immunol Res 31: 13-24, 2005.
2. Bach JF. Organ-specific autoimmunity. Immunol Today 16: 353-355, 1995.
3. + cells. Clin Immunol 115: 10-18, 2005.
4. + T cells in the thymus of patients with autoimmune myasthenia gravis. Blood 105: 735-741, 2005.
5. Bizzarro A, Valentini G, Di Martino G, DaPonte A, De Bellis A, and Iacono G. Influence of testosterone therapy on clinical and immunological features of autoimmune diseases associated with Klinefelter's syndrome. J Clin Endocrinol Metab 64: 32-36, 1987.
6. Cohen JH, Danel L, Cordier G, Saez S, and Revillard JP. Sex steroid receptors in peripheral T cells: absence of androgen receptors and restriction of estrogen receptors to OKT8-positive cells. J Immunol 131: 2767-2771, 1983.
7. Crispin JC, Martinez A, and Alcocer-Varela J. Quantification of regulatory T cells in patients with systemic lupus erythematosus. J Autoimmun 21: 273-276, 2003.
8. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, and Straub RH. Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus 13: 635-638, 2004.
9. + Tregs and immune control. J Clin Invest 114: 1209-1217, 2004.
10. Fox HS, Bond BL, and Parslow TG. Estrogen regulates the IFN-gamma promoter. J Immunol 146: 4362-4367, 1991.
11. Giltay EJ, Fonk JC, von Blomberg BM, Drexhage HA, Schalkwijk C, and Gooren LJ. In vivo effects of sex steroids on lymphocyte responsiveness and immunoglobulin levels in humans. J Clin Endocrinol Metab 85: 1648-1657, 2000.
12. Griffen JE and Wilson JD. The testis. In: Metabolic Control and Disease (8th ed.), edited by Bondy PK and Rosenberg LE. Philadelphia, PA: Saunders, 1980, p. 1525.
13. Hamerman JA, Ogasawara K, and Lanier LL. NK cells in innate immunity. Curr Opin Immunol 17: 29-35, 2005.
14. Herbst KL, Anawalt BD, Amory JK, and Bremner WJ. Acyline: the first study in humans of a potent, new gonadotropin-releasing hormone antagonist. J Clin Endocrinol Metab 87: 3215-3220, 2002.
15. Herbst KL, Coviello AD, Page S, Amory JK, Anawalt BD, and Bremner WJ. A single dose of the potent gonadotropin-releasing hormone antagonist acyline suppresses gonadotropins and testosterone for 2 weeks in healthy young men. J Clin Endocrinol Metab 89: 5959-5965, 2004.
16. Jacobson DL, Gange SJ, Rose NR, and Graham NM. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol 84: 223-243, 1997.
17. Khosla S, Atkinson EJ, Dunstan CR, and O'Fallon WM. Effect of estrogen versus testosterone on circulating osteoprotegerin and other cytokine levels in normal elderly men. J Clin Endocrinol Metab 87: 1550-1554, 2002.
18. Klein SL. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26: 247-264, 2004.
19. Kocar IH, Yesilova Z, Ozata M, Turan M, Sengul A, and Ozdemir I. The effect of testosterone replacement treatment on immunological features of patients with Klinefelter's syndrome. Clin Exp Immunol 121: 448-452, 2000.
20. Kronenberg M and Rudensky A. Regulation of immunity by self-reactive T cells. Nature 435: 598-604, 2005.
21. Lang K, Drell TL, Niggemann B, Zanker KS, and Entschladen F. Neurotransmitters regulate the migration and cytotoxicity in natural killer cells. Immunol Lett 90: 165-172, 2003.
22. + T-cells from patients with type 1 diabetes. Diabetes 54: 92-99, 2005.
23. Malkin CJ, Pugh PJ, Jones RD, Kapoor D, Channer KS, and Jones TH. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J Clin Endocrinol Metab 89: 3313-3318, 2004.
24. Maloy KJ and Powrie F. Regulatory T cells in the control of immune pathology. Nat Immunol 2: 816-822, 2001.
25. Marks LS, Hess DL, Dorey FJ, Luz Macairan M, Cruz Santos PB, and Tyler VE. Tissue effects of saw palmetto and finasteride: use of biopsy cores for in situ quantification of prostatic androgens. Urology 57: 999-1005, 2001.
26. Matejuk A, Hopke C, Vandenbark AA, Hurn PD, and Offner H. Middle-age male mice have increased severity of experimental autoimmune encephalomyelitis and are unresponsive to testosterone therapy. J Immunol 174: 2387-2395, 2005.
27. high T cells in inflammatory bowel disease. Gastroenterology 128: 1868-1878, 2005.
28. Olsen NJ and Kovacs WJ. Gonadal steroids and immunity. Endocr Rev 17: 369-384, 1996.
29. Petri MA, Mease PJ, Merrill JT, Lahita RG, Iannini MJ, Yocum DE, Ginzler EM, Katz RS, Gluck OS, Genovese MC, Van Vollenhoven R, Kalunian KC, Manzi S, Greenwald MW, Buyon JP, Olsen NJ, Schiff MH, Kavanaugh AF, Caldwell JR, Ramsey-Goldman R, St Clair EW, Goldman AL, Egan RM, Polisson RP, Moder KG, Rothfield NF, Spencer RT, Hobbs K, Fessler BJ, Calabrese LH, Moreland LW, Cohen SB, Quarles BJ, Strand V, Gurwith M, and Schwartz KE. Effects of prasterone on disease activity and symptoms in women with active systemic lupus erythematosus. Arthritis Rheum 50: 2858-2868, 2004.
30. + regulatory T cell compartment. J Immunol 173: 2227-2230, 2004.
31. Resko JA, Ellinwood WE, Pasztor LM, and Huhl AE. Sex steroids in the umbilical circulation of fetal rhesus monkeys from the time of gonadal differentiation. J Clin Endocrinol Metab 50: 900-905, 1980.
32. Robertson MJ. Role of chemokines in the biology of natural killer cells. J Leukoc Biol 71: 173-183, 2002.
33. Roden AC, Moser MT, Tri SD, Mercader M, Kuntz SM, Dong H, Hurwitz AA, McKean DJ, Celis E, Leibovich BC, Allison JP, and Kwon ED. Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol 173: 6098-6108, 2004.
34. + regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6: 345-352, 2005.
35. + regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 182: 18-32, 2001.
36. Schroder K, Hertzog PJ, Ravasi T, and Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75: 163-189, 2004.
37. Seaman WE, Blackman MA, Gindhart TD, Roubinian JR, Loeb JM, and Talal N. Beta-estradiol reduces natural killer cells in mice. J Immunol 121: 2193-2198, 1978.
38. Shevach EM. Regulatory T cells in autoimmmunity. Annu Rev Immunol 18: 423-449, 2000.
39. Sorachi K, Kumagai S, Sugita M, Yodoi J, and Imura H. Enhancing effect of 17 beta-estradiol on human NK cell activity. Immunol Lett 36: 31-35, 1993.
40. Stimson WH. Oestrogen and human T lymphocytes: presence of specific receptors in the T-suppressor/cytotoxic subset. Scand J Immunol 28: 345-350, 1988.
41. Sulke AN, Jones DB, and Wood PJ. Hormonal modulation of human natural killer cell activity in vitro. J Reprod Immunol 7: 105-110, 1985.
42. Tanriverdi F, Silveira LF, MacColl GS, and Bouloux PM. The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. J Endocrinol 176: 293-304, 2003.
43. Teixeira LK, Fonseca BP, Barboza BA, and Viola JP. The role of interferon-gamma on immune and allergic responses. Mem Inst Oswaldo Cruz 100, Suppl 1: 137-144, 2005.
44. Tengstrand B, Carlstrom K, Fellander-Tsai L, and Hafstrom I. Abnormal levels of serum dehydroepiandrosterone, estrone, and estradiol in men with rheumatoid arthritis: high correlation between serum estradiol and current degree of inflammation. J Rheumatol 30: 2338-2343, 2003.
45. + regulatory T cells in patients with multiple sclerosis. J Exp Med 199: 971-979, 2004.
46. Wildin RS, Ramsdell F, Peake J, Faravelli F, Casanova JL, Buist N, Levy-Lahad E, Mazzella M, Goulet O, Perroni L, Bricarelli FD, Byrne G, McEuen M, Proll S, Appleby M, and Brunkow ME. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet 27: 18-20, 2001.
47. Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, and Plymate SR. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J Clin Invest 114: 560-568, 2004.
48. Wunderlich F, Benten WP, Lieberherr M, Guo Z, Stamm O, Wrehlke C, Sekeris CE, and Mossmann H. Testosterone signaling in T cells and macrophages. Steroids 67: 535-538, 2002.
49. Yesilova Z, Ozata M, Kocar IH, Turan M, Pekel A, Sengul A, and Ozdemir IC. The effects of gonadotropin treatment on the immunological features of male patients with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 85: 66-70, 2000.