Time-course changes of steroidogenic gene expression and steroidogenesis of rat leydig cells after acute immobilization stress

International Journal of Molecular Sciences

Volumn 15, Issue 11, 2014, Pages 21028-21044

  Lin, Han ^a   Yuan, Kai Ming ^a   Zhou, Hong Yu ^a   Bu, Tiao ^a   Su, Huina ^a   Liu, Shiwen ^a   Zhu, Qiqi ^a   Wang, Yiyan ^a   Hu, Yuanyuan ^a   Shan, Yuanyuan ^a   Lian, Qing Quan ^a   Wu, Xiao Yun ^b   Ge, Ren Shan ^a  

^a WENZHOU MEDICAL UNIVERSITY   (China)

^b Huzhou Maternity and Child Care Hospital   (China)

Author keywords

Acute stress; Corticosterone; Leydig cell; Rat; StAR; Steroidogenic enzymes

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; 3BETA HYDROXY DELTA5 STEROID DEHYDROGENASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CORTICOSTERONE; CYTOCHROME P450 17; GLUCOCORTICOID RECEPTOR; INDUCIBLE NITRIC OXIDE SYNTHASE; LUTEINIZING HORMONE; MIFEPRISTONE; SCAVENGER RECEPTOR BI; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG; HORMONE; STEROID;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; IMMOBILIZATION STRESS; LEYDIG CELL; NONHUMAN; PROTEIN ANALYSIS; RADIOIMMUNOASSAY; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEROIDOGENESIS; UPREGULATION; WESTERN BLOTTING; ANIMAL; BLOOD; CELL CULTURE; EXERCISE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; CELLS, CULTURED; CORTICOSTERONE; GENE EXPRESSION REGULATION; HORMONES; LEYDIG CELLS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; STEROIDS;

EID: 84910134522     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms151121028     Document Type: Article

References (52)

1. Stocco, D.M. Tracking the role of a StAR in the sky of the new millenium. Mol. Endocrinol. 2001, 15, 1245-1254.
2. Ge, R.S.; Hardy, M.P. Regulation of Leydig cells during pubertal development. In The Leydig Cell in Health and Disease; Payne, A.H., Hardy, M.P., Eds.; Humana Press: Totowa, NJ, USA, 2007; pp. 55-70.
3. Veldhuis, J.D.; Dufau, M.L. Steroidal regulation of biologically active luteinizing hormone secretion in men and women. Hum. Reprod. 1993, 8, 84-96.
4. Ge, R.S.; Hardy, D.O.; Catterall, J.F.; Hardy, M.P. Developmental changes in glucocorticoid receptor and 11β-hydroxysteroid dehydrogenase oxidative and reductive activities in rat Leydig cells. Endocrinology 1997, 138, 5089-5095.
5. Schultz, R.; Isola, J.; Parvinen, M.; Honkaniemi, J.; Wikstrom, A.C.; Gustafsson, J.A.; Pelto-Huikko, M. Localization of the glucocorticoid receptor in testis and accessory sexual organs of male rat. Mol. Cell Endocrinol. 1993, 95, 115-120.
6. Macho, L.; Kvetnansky, R.; Fickova, M.; Popova, I.A.; Grigoriev, A. Effects of exposure to space flight on endocrine regulations in experimental animals. Endocr. Regul. 2001, 35, 101-114.
7. Chrousos, G.P.; Gold, P.W. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 1992, 267, 1244-1252.
8. Munck, A.; Guyre, P.M.; Holbrook, N.J. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrinol. Rev. 1984, 5, 25-43.
9. Hardy, M.P.; Gao, H.B.; Dong, Q.; Ge, R.; Wang, Q.; Chai, W.R.; Feng, X.; Sottas, C. Stress hormone and male reproductive function. Cell. Tissue Res. 2005, 322, 147-153.
10. Stojkov, N.J.; Janjic, M.M.; Baburski, A.Z.; Mihajlovic, A.I.; Drljaca, D.M.; Sokanovic, S.J.; Bjelic, M.M.; Kostic, T.S.; Andric, S.A. Sustained in vivo blockade of α1-adrenergic receptors prevented some of stress-triggered effects on steroidogenic machinery in Leydig cells. Am. J. Physiol. Endocrinol. Metab 2013, 305, E194-E204.
11. Stojkov, N.J.; Janjic, M.M.; Bjelic, M.M.; Mihajlovic, A.I.; Kostic, T.S.; Andric, S.A. Repeated immobilization stress disturbed steroidogenic machinery and stimulated the expression of cAMP signaling elements and adrenergic receptors in Leydig cells. Am. J. Physiol. Endocrinol. Metab 2012, 302, E1239-E1251.
12. Hales, D.B.; Payne, A.H. Glucocorticoid-mediated repression of P450scc mRNA and de novo synthesis in cultured Leydig cells. Endocrinology 1989, 124, 2099-2104.
13. Orr, T.E.; Taylor, M.F.; Bhattacharyya, A.K.; Collins, D.C.; Mann, D.R. Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17α-hydroxylase and 17,20-lyase without affecting the binding of LH/hCG receptors. J. Androl. 1994, 15, 302-308.
14. Ge, R.S.; Dong, Q.; Sottas, C.M.; Chen, H.; Zirkin, B.R.; Hardy, M.P. Gene expression in rat Leydig cells during development from the progenitor to adult stage: A cluster analysis. Biol. Reprod. 2005, 72, 1405-1415.
15. Ge, R.S.; Gao, H.B.; Nacharaju, V.L.; Gunsalus, G.L.; Hardy, M.P. Identification of a kinetically distinct activity of 11β-hydroxysteroid dehydrogenase in rat Leydig cells. Endocrinology 1997, 138, 2435-2442.
16. Ge, R.S.; Dong, Q.; Niu, E.M.; Sottas, C.M.; Hardy, D.O.; Catterall, J.F.; Latif, S.A.; Morris, D.J.; Hardy, M.P. 11β-Hydroxysteroid dehydrogenase 2 in rat Leydig cells: Its role in blunting glucocorticoid action at physiological levels of substrate. Endocrinology 2005, 146, 2657-2664.
17. Fenster, L.; Katz, D.F.; Wyrobek, A.J.; Pieper, C.; Rempel, D.M.; Oman, D.; Swan, S.H. Effects of psychological stress on human semen quality. J. Androl. 1997, 18, 194-202.
18. Hjollund, N.H.; Bonde, J.P.; Henriksen, T.B.; Giwercman, A.; Olsen, J. Job strain and male fertility. Epidemiology 2004, 15, 114-117.
19. Hjollund, N.H.; Bonde, J.P.; Henriksen, T.B.; Giwercman, A.; Olsen, J. Reproductive effects of male psychologic stress. Epidemiology 2004, 15, 21-27.
20. Eskiocak, S.; Gozen, A.S.; Yapar, S.B.; Tavas, F.; Kilic, A.S.; Eskiocak, M. Glutathione and free sulphydryl content of seminal plasma in healthy medical students during and after exam stress. Hum. Reprod. 2005, 20, 2595-2600.
21. Campagne, D.M. Should fertilization treatment start with reducing stress? Hum. Reprod. 2006, 21, 1651-1658.
22. Gao, H.B.; Tong, M.H.; Hu, Y.Q.; Guo, Q.S.; Ge, R.; Hardy, M.P. Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 2002, 143, 130-138.
23. Chen, Y.; Wang, Q.; Wang, F.F.; Gao, H.B.; Zhang, P. Stress induces glucocorticoid-mediated apoptosis of rat Leydig cells in vivo. Stress 2012, 15, 74-84.
24. Spencer, R.L.; Miller, A.H.; Moday, H.; McEwen, B.S.; Blanchard, R.J.; Blanchard, D.C.; Sakai, R.R. Chronic social stress produces reductions in available splenic type II corticosteroid receptor binding and plasma corticosteroid binding globulin levels. Psychoneuroendocrinology 1996, 21, 95-109.
25. Blanchard, D.C.; Spencer, R.L.; Weiss, S.M.; Blanchard, R.J.; McEwen, B.; Sakai, R.R. Visible burrow system as a model of chronic social stress: Behavioral and neuroendocrine correlates. Psychoneuroendocrinology 1995, 20, 117-134.
26. Ge, R.S.; Hardy, M.P. Initial predominance of the oxidative activity of type I 11β-hydroxysteroid dehydrogenase in primary rat Leydig cells and transfected cell lines. J. Androl. 2000, 21, 303-310.
27. Monder, C.; Miroff, Y.; Marandici, A.; Hardy, M.P. 11β-Hydroxysteroid dehydrogenase alleviates glucocorticoid-mediated inhibition of steroidogenesis in rat Leydig cells. Endocrinology 1994, 134, 1199-1204.
28. Martin, L.J.; Tremblay, J.J. Glucocorticoids antagonize cAMP-induced StAR transcription in Leydig cells through the orphan nuclear receptor NR4A1. J. Mol. Endocrinol. 2008, 41, 165-175.
29. Xiao, Y.C.; Huang, Y.D.; Hardy, D.O.; Li, X.K.; Ge, R.S. Glucocorticoid suppresses steroidogenesis in rat progenitor Leydig cells. J. Androl. 2010, 31, 365-371.
30. Stocco, D.M.; Clark, B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 1996, 17, 221-244.
31. Dong, Q.; Salva, A.; Sottas, C. M.; Niu, E.; Holmes, M.; Hardy, M.P. Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J. Androl. 2004, 25, 973-981.
32. Gao, H.B.; Shan, L.X.; Monder, C.; Hardy, M.P. Suppression of endogenous corticosterone levels in vivo increases the steroidogenic capacity of purified rat Leydig cells in vitro. Endocrinology 1996, 137, 1714-1718.
33. Monder, C.; Hardy, M.P.; Blanchard, R.J.; Blanchard, D.C. Comparative aspects of 11β-hydroxysteroid dehydrogenase. Testicular 11β-hydroxysteroid dehydrogenase: Development of a model for the mediation of Leydig cell function by corticosteroids. Steroids 1994, 59, 69-73.
34. Orr, T.E.; Mann, D.R. Effects of restraint stress on plasma LH and testosterone concentrations, Leydig cell LH/hCG receptors, and in vitro testicular steroidogenesis in adult rats. Horm. Behav. 1990, 24, 324-341.
35. Akibami, M.A.; Mann, D.R. Mechanism of stress-induced attenuation of the testicular response to gonadotropin: Possible involvement of testicular opioids, a pertussis toxin-sensitive G-protein, and phosphodiesterase. J. Androl. 1996, 17, 10-16.
36. Kostic, T.; Andric, S.; Kovacevic, R.; Maric, D. The involvement of nitric oxide in stress-impaired testicular steroidogenesis. Eur. J. Pharmacol. 1998, 346, 267-273.
37. Andric, S.A.; Janjic, M.M.; Stojkov, N.J.; Kostic, T.S. Testosterone-induced modulation of nitric oxide-cGMP signaling pathway and androgenesis in the rat Leydig cells. Biol. Reprod. 2010, 83, 434-442.
38. Weissman, B.A.; Sottas, C.M.; Zhou, P.; Iadecola, C.; Hardy, M.P. Testosterone production in mice lacking inducible nitric oxide synthase expression is sensitive to restraint stress. Am. J. Physiol. Endocrinol. Metab 2007, 292, E615-E620.
39. Weissman, B.A.; Sottas, C.M.; Holmes, M.; Zhou, P.; Iadecola, C.; Hardy, D.; Ge, R.S.; Hardy, M.P. Normal responses to restraint stress in mice lacking the gene for neuronal nitric oxide synthase. J. Androl. 2009, 30, 614-620.
40. Yun, C.C.; Chen, Y.; Lang, F. Glucocorticoid activation of Na+/H+ exchanger isoform 3 revisited. the roles of SGK1 and NHERF2. J. Biol. Chem. 2002, 277, 7676-7683.
41. Maddocks, S.; Sharpe, R.M. Interstitial fluid volume in the rat testis: Androgen-dependent regulation by the seminiferous tubules? J. Endocrinol. 1989, 120, 215-222.
42. Klinefelter, G.R.; Hall, P.F.; Ewing, L.L. Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multi-step procedure. Biol. Reprod. 1987, 36, 769-783.
43. Payne, A.H.; Downing, J.R.; Wong, K.L. Luteinizing hormone receptor and testosterone synthesis in two distinct populations of Leydig cells. Endocrinology 1980, 106, 1424-1429.
44. Kumar, N.; Didolkar, A.K.; Monder, C.; Bardin, C.W.; Sundaram, K. The biological activity of 7α-methyl-19-nortestosterone is not amplified in male reproductive tract as is that of testosterone. Endocrinology 1992, 130, 3677-3683.
45. Cochran, R.C.; Ewing, L.L.; Niswender, G.D. Serum levels of follicle-stimulating hormone, prolactin, testosterone, 5α-dihydrotestosterone, 5α-androstane-3α, 17β-diol, 5α-androstane-3β, 17b-diol and 17β-estradiol from male beagles with spontaneous or induced benign prostatic hyperplasia. Invest. Urol. 1981, 19, 142-147.
46. Lin, H.; Ge, R.S.; Chen, G.R.; Hu, G.X.; Dong, L.; Lian, Q.Q.; Hardy, D.O.; Sottas, C.M.; Li, X.K.; Hardy, M.P. Involvement of testicular growth factors in fetal Leydig cell aggregation after exposure to phthalate in utero. Proc. Nat. Acad. Sci. USA 2008, 105, 7218-7222.
47. Guo, J.; Zhou, H.; Su, Z.; Chen, B.; Wang, G.; Wang, C. Q.; Xu, Y.; Ge, R.S. Comparison of cell types in the rat Leydig cell lineage after ethane dimethanesulfonate treatment. Reproduction 2013, 145, 371-380.
48. Zhang Y.F.; Yuan K.M.; Liang Y.; Chu Y.H.; Lian Q.Q.; Ge Y.F.; Zhen W.; Sottas C.M.; Su Z.J.; Ge R.S. Alterations of gene profiles in Leydig-cell-regenerating adult rat testis after ethane dimethane sulfonate-treatment. Asian J. Androl. 2014, doi:10.4103/1008-682X.136447.
49. Huyghe, S.; Schmalbruch, H.; de Gendt, K.; Verhoeven, G.; Guillou, F.; van Veldhoven, P.P.; Baes, M. Peroxisomal multifunctional protein 2 is essential for lipid homeostasis in Sertoli cells and male fertility in mice. Endocrinology 2006, 147, 2228-2236.
50. Corton, J.C.; Bocos, C.; Moreno, E.S.; Merritt, A.; Marsman, D.S.; Sausen, P.J.; Cattley, R.C.; Gustafsson, J.A. Rat 17β-hydroxysteroid dehydrogenase type IV is a novel peroxisome proliferator-inducible gene. Mol. Pharmacol. 1996, 50, 1157-1166.
51. Hu, G.X.; Zhou, H.Y.; Li, X.W.; Chen, B.B.; Xiao, Y.C.; Lian, Q.Q.; Liang, G.; Kim, H.H.; Zheng, Z.Q.; Hardy, D.O.; Ge, R.S. The (+)-and (−)-gossypols potently inhibit both 3β-hydroxysteroid dehydrogenase and 17β-hydroxysteroid dehydrogenase 3 in human and rat testes. J. Steroid Biochem. Mol. Biol. 2009, 115, 14-19.
52. Li, L.; Chen, X.; Zhu, Q.; Chen, D.; Guo, J.; Yao, W.; Dong, Y.; Wei, J.; Lian, Q.; Ge, R.S.; Yuan, B. Disrupting androgen production of Leydig cells by resveratrol via direct inhibition of human and rat 3β-hydroxysteroid dehydrogenase. Toxicol. Lett. 2014, 226, 14-19.