Persistence of androgenic effects on the production of proinflammatory cytokines by circulating antigen-presenting cells after withdrawal of testosterone treatment in aging type 2 diabetic men with partial androgen deficiency

Fertility and Sterility

Volumn 92, Issue 1, 2009, Pages 311-319

  Corrales, Juan José ^a   Almeida, María ^a   Miralles, José Manuel ^a   Orfao, Alberto ^a  

^a HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

Author keywords

aging; androgens; Dendritic cells; hypogonadism; immune response; inflammatory cytokines; monocytes; testosterone; testosterone deprivation

Indexed keywords

CD16 ANTIGEN; CD33 ANTIGEN; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TESTOSTERONE ENANTATE; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; AGING; ANDROGEN DEFICIENCY; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL SUBPOPULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DIABETIC PATIENT; DRUG WITHDRAWAL; EX VIVO STUDY; HORMONE SUBSTITUTION; HUMAN; HUMAN CELL; MALE; MONOCYTE; NATURAL KILLER CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; PATIENT COMPLIANCE; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROSPECTIVE STUDY; T LYMPHOCYTE;

AGED; ANDROGENS; ANTIGEN-PRESENTING CELLS; CYTOKINES; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 2; HORMONE REPLACEMENT THERAPY; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MIDDLE AGED; MONOCYTES; PROSPECTIVE STUDIES; REFERENCE VALUES; TESTOSTERONE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 67649099766     PISSN: 00150282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2008.05.040     Document Type: Article

References (46)

1. Harman S.M., Metter E.J., Tobin J.D., Pearson J., and Blackman M.R. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. J Clin Endocrinol Metab 86 (2001) 724-731
2. Feldman H.A., Longcope C., Derby C.A., Johannes C.B., Araujo A.B., Coviello A.D., et al. Age trends in the level of serum testosterone and other hormones in middle-aged men: longitudinal results from the Massachusetts Male Aging Study. J Clin Endocrinol Metab 87 (2002) 589-598
3. Anderson B., Marin P., Lissner L., Vermeulen A., and Bjorntorp P. Testosterone concentrations in women and men with NIDDM. Diabetes Care 17 (1994) 405-411
4. Barrett-Connor E., Khaw K.T., and Yen S.S.C. Endogenous sex hormone levels in older adult men with diabetes mellitus. Am J Epidemiol 132 (1990) 895-901
5. Dhindsa S., Prabhakar S., Sethi M., Bandyopadhyay A., Chaudhuri A., and Dandona P. Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 89 (2004) 5462-5468
6. Hajjar R.R., Kaiser F.E., and Morley J.E. Outcomes of long-term testosterone replacement in older hypogonadal males: a retrospective analysis. J Clin Endocrinol Metab 82 (1997) 3793-3796
7. Snyder P.J., Peachey H., Hannoush P., Berlin J.A., Loh L., Lenrow D.A., et al. Effect of testosterone treatment on body composition and muscle strength in men over 65 years of age. J Clin Endocrinol Metab 84 (1999) 2647-2653
8. Page S.T., Amory J.K., Bowman F.D., Anawalt B.D., Matsumoto A.M., Bremner W.J., et al. Exogenous testosterone (T) alone or with finasteride increases physical performance, grip strength, and lean body mass in older men with low serum T. J Clin Endocrinol Metab 90 (2005) 1502-1510
9. Nieschlag E., Behre H.M., Bouchard P., Corrales J.J., Jones T.H., Stalla G.K., et al. Testosterone replacement therapy: current trends and future directions. Hum Reprod Update 10 (2004) 409-419
10. Kaufman J.M., and Vermeulen A. The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocrin Rev 26 (2005) 833-876
11. Nieschlag E., Swerdloff R., Behre H.M., Gooren L.J., Kaufman J.M., Legros J.J., et al. Investigation, treatment, and monitoring of late-onset hypogonadism in males: ISA, ISSAM, and EAU recommendations. J Androl 27 (2006) 135-137
12. American Society for Reproductive Medicine. The Practice Committee of the American Society for Reproductive Medicine. Treatment of androgen deficiency in the aging male. Fertil Steril 81 (2004) 1437-1440
13. Snyder P.J. Hypogonadism in elderly men. What to do until the evidence comes. N Engl J Med 350 (2004) 440-442
14. Tanriverdi F., Silveira L.F.G., MacColl G.S., and Bouloux P.M.G. The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. J Endocrinol 176 (2003) 293-304
15. Jacobson D.L., Gange S.J., Rose N.R., and Graham N.M.H. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol 84 (1997) 223-243
16. Corrales J.J., Almeida M., Burgo R., Mories M.T., Miralles J.M., and Orfao A. Androgen-replacement therapy depresses the ex vivo production of inflammatory cytokines by circulating antigen-presenting cells in aging type-2 diabetic men with partial androgen deficiency. J Endocrinol 189 (2006) 595-604
17. Cutolo M., Sulli A., Capellino S., Villaggio B., Montagna P., Seriolo B., et al. Sex hormones influence on the immune system: basic and clinical aspects of autoimmunity. Lupus 13 (2004) 635-638
18. Ellis T.M., Moser M.T., Le P.T., Flanigan R.C., and Kwon E.D. Alterations in peripheral B cells and B cell progenitors following androgen ablation in mice. Int Immunol 13 (2001) 553-558
19. Roden A.C., Moser M.T., Tri S.D., Mercader M., Kuntz S.M., Dong H., et al. Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol 173 (2004) 6098-6108
20. French M.A.H., and Hughes P. Systemic lupus erythematosus and Klinefelter's syndrome. Ann Rheum Dis 42 (1983) 471-473
21. Musabak U., Bolu E., Ozata M., Oktenli C., Sengul A., Inal A., et al. Gonadotropin treatment restores in vitro interleukin-1β and tumour necrosis factor-α production by stimulated peripheral blood mononuclear cells from patients with idiopathic hypogonadotropic hypogonadism. Clin Exp Immunol 132 (2003) 265-270
22. Yesilova Z., Ozata M., Kocar I.H., Turan M., Pekel A., Sengul A., et al. The effects of gonadotropin treatment on the immunological features of male patients with idiopathic hypogonadotropic hypogonadism. J Clin Endocrinol Metab 85 (2000) 66-70
23. Khosla S., Atkinson E.J., Dunstan C.R., and O'Fallon W.M. Effect of estrogen versus testosterone on circulating osteoprotegerin and other cytokine levels in normal elderly men. J Clin Endocrinol Metab 87 (2002) 1550-1554
24. Page S.T., Plymate S.R., Bremmer W.J., Matsumoto A.M., Hess D.L., Lin D.W., et al. Effect of medical castration on CD4+CD25+ T cells, CD8+ T cell IFN-γ expression, and NK cells: physiological role of testosterone and/or its metabolites. Am J Physiol Endocrinol Metab 290 (2006) E856-E863
25. Mercader M., Bodner B.K., Moser M.T., Kwon P.S., Park E.S.Y., Manecke R.G., et al. T cell infiltration of the prostate induced by androgen withdrawal in patients with prostate cancer. Proc Natl Acad Sci U S A 98 (2001) 14565-14570
26. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 27 Suppl 1 (2004) S5-10
27. Corrales J.J., Burgo R.M., García-Berrocal B., Almeida M., Alberca I., González Buitrago J.M., et al. Partial androgen deficiency in aging type 2 diabetic men and its relationship to glycemic control. Metabolism 53 (2004) 666-672
28. Corrales J.J., Burgo R.M., Mories M.T., Fraile A., and Miralles J.M. Andropausia en pacientes con diabetes mellitus de tipo 2. Análisis de criterios clínicos y bioquímicos para su identificación. Endocrinología y Nutrición 50 Suppl 2 (2003) 8-9
29. Corrales J.J., Burgo R.M., Miralles J.M., and Villar E. Abnormalities in sperm acid glycosidases from infertile men with idiopathic oligoasthenoteratozoospermia. Fertil Steril 73 (2000) 470-478
30. Kaufman J.M., and Vermeulen A. Declining gonadal function in elderly men. Baillieres Clin Endocrinol Metab 11 (1997) 289-309
31. Menéndez P., Prósper F., Bueno C., Arbona C., San Miguel J.F., García-Conde J., et al. Sequential analysis of CD34+ and CD34- cell subsets in peripheral blood and leukapheresis products from breast cancer patients mobilized with SCF plus G-CSF and cyclophosphamide. Leukemia 15 (2001) 430-439
32. Almeida J., Bueno C., Algueró M.C., Sánchez M.L., De Santiago M., Escribano L., et al. Comparative analysis of the morphological, cytochemical, immunophenotypical, and functional characteristics of normal human peripheral blood lineage-/CD16+/HLA-DR+/CD14-/lo cells, CD14+ monocytes, and CD16- dendritic cells. Clin Immunol 100 (2001) 325-338
33. Almeida J., Bueno C., Algueró M.C., Sánchez M.L., Cañizo M.C., Fernández M.E., et al. Extensive characterization of the immunophenotype and pattern of cytokine production by distinct subpopulations of normal human peripheral blood MHCII+/lineage- cells. Clin Exp Immunol 118 (1999) 392-401
34. National Committee of Clinical Laboratory Standards. Performance of single cell immune response assays: approved guideline. NCCLS document I/LA26-A. [ISBN 1-56238-546-1]. Wayne, PA: NCCLS (2004)
35. Bueno C., Almeida J., Algueró M.C., Sánchez M.L., Vaquero J.M., Laso F.J., et al. Flow cytometric analysis of cytokine production by normal human peripheral blood dendritic cells and monocytes: comparative analysis of different stimuli, secretion-blocking agents and incubation periods. Cytometry 46 (2001) 33-40
36. Malkin C.J., Pugh P.J., Jones R.D., Kapoor D., Channer K.S., and Jones T.H. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J Clin Endocrinol Metab 89 (2004) 3313-3318
37. Bebo Jr. B.F., Zelinka-Vincent E., Adamus G., Admundson D., Vandenbark A.A., and Offner H. Gonadal hormones influence the immune response to PLP 139-151 and the clinical course of relapsing experimental autoimmune encephalomyelitis. J Neuroimmunol 84 (1997) 122-130
38. Messingham K.A.N., Shirazi M., Duffner L.A., Emanuele M.A., and Kovacs E.J. Testosterone receptor blockade restores cellular immunity in male mice after burn injury. J Endocrinol 169 (2001) 299-308
39. Morishita M., Migayi M., and Iwamoto Y. Effects of sex hormones on production of interleukin-1 by human peripheral monocytes. J Periodontol 70 (1999) 757-760
40. Bouman A., Schipper M., Heinemann M.J., and Faas M.M. Gender difference in the non-specific and specific immune response in humans. Am J Reprod Immunol 52 (2004) 19-26
41. Posma P.E., Moes H., Heineman M.J., and Faas M.M. The effect of testosterone on cytokine production in the specific and non-specific immune response. Am J Reprod Immunol 52 (2004) 237-243
42. Behre H.M., Wang C., Handelsman D.J., and Nieschlag E. Pharmacology of testosterone preparations. In: Nieschlag E., and Behre H.M. (Eds). Testosterone action, deficiency, substitution (2004), Cambridge University Press, Cambridge, United Kingdom 405-444
43. Schroeder E.T., Zheng L., Ong M.D., Martinez C., Flores C., Stewart Y., et al. Effects of androgen therapy on adipose tissue and metabolism in older men. J Clin Endocrinol Metab 89 (2004) 4863-4872
44. Matejuk A., Hopke C., Vandenbark A.A., Hurn P.D., and Offner H. Middle-age male mice have increased severity of experimental autoimmune encephalomyelitis and are unresponsive to testosterone therapy. J Immunol 174 (2005) 2387-2395
45. Hammer F., Drescher D.G., Schneider S.B., Quinkler M., Stewart P.M., Allolio B., et al. Sex steroid metabolism in human peripheral blood mononuclear cells changes with aging. J Clin Endocrinol Metab 90 (2005) 6283-6290
46. Corrales J.J., Almeida M., Burgo R.M., Hernández P., Miralles J.M., and Orfao A. Decreased production of inflammatory cytokines by circulating monocytes and dendritic cells in type 2 diabetic men with atherosclerotic complications. J Diab Compl 21 (2007) 41-49