Androgen action via testicular arteriole smooth muscle cells is important for leydig cell function, vasomotion and testicular fluid dynamics

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Welsh, Michelle ^a   Sharpe, Richard M ^a   Moffat, Lindsey ^a   Atanassova, Nina ^b   Saunders, Philippa T K ^a   Kilter, Sigrid ^c   Bergh, Anders ^c   Smith, Lee B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Institute of Experimental Morphology and Anthropology Bulgarian Academy of Sciences   (Bulgaria)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; FOLLITROPIN; LUTEINIZING HORMONE; TESTOSTERONE; PRIMER DNA;

ADULTHOOD; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BREEDING; CELL FUNCTION; CONTROLLED STUDY; FEMALE; FERTILITY; GERM CELL; HORMONE DETERMINATION; LEYDIG CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SPERMATOGENESIS; TESTIS BLOOD FLOW; TESTIS FUNCTION; TESTIS WEIGHT; ANIMAL; GENETIC TRANSCRIPTION; GENETICS; IMMUNOHISTOCHEMISTRY; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TESTIS; VASCULAR SMOOTH MUSCLE; VASCULARIZATION;

MUS;

ANDROGENS; ANIMALS; ARTERIOLES; BASE SEQUENCE; DNA PRIMERS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TESTIS; TRANSCRIPTION, GENETIC;

EID: 78149444074     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013632     Document Type: Article

References (50)

1. George FW, Wilson, J (1994) Gonads and ducts in mammals. In: Knobil E, Neill, JD, eds. The Physiology of Reproduction. 2nd ed. New York: Raven Press. pp 3-27.
2. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, et al. (2002) Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 57: 149-179.
3. Sharpe RM (1994) The Physiology of Reproduction. In: Knobil EaN JD, ed. New York: Raven. pp 1363-2434.
4. Quigley CA, De Bellis A, Marschke KB, el-Awady MK, Wilson EM, et al. (1995) Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 16: 271-321.
5. Bremner WJ, Millar MR, Sharpe RM, Saunders PT (1994) Immunohistochem-ical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens. Endocrinology 135: 1227-1234.
6. Bergh A, Damber JE (1992) Immunohistochemical demonstration of androgen receptors on testicular blood vessels. Int J Androl 15: 425-434.
7. De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, et al. (2004) A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci U S A 101: 1327-1332.
8. Welsh M, Saunders PT, Atanassova N, Sharpe RM, Smith LB (2009) Androgen action via testicular peritubular myoid cells is essential for male fertility. Faseb J 23: 4218-4230.
9. Chang C, Chen YT, Yeh SD, Xu Q, Wang RS, et al. (2004) Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells. Proc Natl Acad Sci U S A 101: 6876-6881.
10. Johnston DS, Russell LD, Friel PJ, Griswold MD (2001) Murine germ cells do not require functional androgen receptors to complete spermatogenesis following spermatogonial stem cell transplantation. Endocrinology 142: 2405-2408.
11. Tsai MY, Yeh SD, Wang RS, Yeh S, Zhang C, et al. (2006) Differential effects of spermatogenesis and fertility in mice lacking androgen receptor in individual testis cells. Proc Natl Acad Sci U S A 103: 18975-18980.
12. Ergun S, Kilic N, Harneit S, Paust HJ, Ungefroren H, et al. (1997) Microcirculation and the vascular control of the testis. Adv Exp Med Biol 424: 163-180.
13. Coveney D, Cool J, Oliver T, Capel B (2008) Four-dimensional analysis of vascularization during primary development of an organ, the gonad. Proc Natl Acad Sci U S A 105: 7212-7217.
14. Brennan J, Karl J, Capel B (2002) Divergent vascular mechanisms downstream of Sry establish the arterial system in the XY gonad. Dev Biol 244: 418-428.
15. Damber JE, Janson PO (1978) Testicular blood flow and testosterone concentration in spermatic venous blood of anaesthetized rats. J Reprod Fertil 52: 265-269.
16. Free MJ, Jaffe RA (1972) Dynamics of circulation in the testis of the conscious rat. Am J Physiol 223: 241-248.
17. Bergh A, Damber JE (1993) Vascular controls in testicular physiology. In: de Kretser D, ed. Molecular Biology of the Male Reproductive System. New York: Academic Press. pp 439-468.
18. Anand RJ, Paust HJ, Altenpohl K, Mukhopadhyay AK (2003) Regulation of vascular endothelial growth factor production by Leydig cells in vitro: the role of protein kinase A and mitogen-activated protein kinase cascade. Biol Reprod 68: 1663-1673.
19. Ergun S, Kilic N, Fiedler W, Mukhopadhyay AK (1997) Vascular endothelial growth factor and its receptors in normal human testicular tissue. Mol Cell Endocrinol 131: 9-20.
20. Collin O, Zupp JL, Setchell BP (2000) Testicular vasomotion in different mammals. Asian J Androl 2: 297-300.
21. Damber JE, Bergh A, Fagrell B, Lindahl O, Rooth P (1986) Testicular microcirculation in the rat studied by videophotometric capillaroscopy, fluorescence microscopy and laser Doppler flowmetry. Acta Physiol Scand 126: 371-376.
22. Collin O, Bergh A, Damber JE, Widmark A (1993) Control of testicular vasomotion by testosterone and tubular factors in rats. J Reprod Fertil 97: 115-121.
23. Widmark A, Damber JE, Bergh A (1986) Relationship between human chorionic gonadotrophin-induced changes in testicular microcirculation and the formation of testicular interstitial fluid. J Endocrinol 109: 419-425.
24. Widmark A, Damber JE, Bergh A (1989) High and low doses of luteinizing hormone induce different changes in testicular microcirculation. Acta En-docrinol (Copenh) 121: 621-627.
25. Setchell BP (1990) Local control of testicular fluids. Reprod Fertil Dev 2: 291-309.
26. Damber JE, Maddocks S, Widmark A, Bergh A (1992) Testicular blood flow and vasomotion can be maintained by testosterone in Leydig cell-depleted rats. Int J Androl 15: 385-393.
27. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, et al. (2002) Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci U S A 99: 7142-7147.
28. Welsh M, Saunders PT, Marchetti NI, Sharpe RM (2006) Androgen-dependent mechanisms of Wolffian duct development and their perturbation by flutamide. Endocrinology 147: 4820-4830.
29. McNeilly JR, Saunders PT, Taggart M, Cranfield M, Cooke HJ, et al. (2000) Loss of oocytes in Dazl knockout mice results in maintained ovarian steroidogenic function but altered gonadotropin secretion in adult animals. Endocrinology 141: 4284-4294.
30. Corker CS, Davidson DW (1978) A radioimmunoassay for testosterone in various biological fluids without chromatography. J Steroid Biochem 9: 373-374.
31. Fisher JS, Macpherson S, Marchetti N, Sharpe RM (2003) Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate. Hum Reprod 18: 1383-1394.
32. Sharpe RM, Cooper I (1983) Testicular interstitial fluid as a monitor for changes in the intratesticular environment in the rat. J Reprod Fertil 69: 125-135.
33. Sharpe RM (1979) Gonadotrophin-induced accumulation of 'interstitial fluid' in the rat testis. J Reprod Fertil 55: 365-371.
34. Welsh M, Saunders PT, Atanassova N, Sharpe RM, Smith LB. (2009) Androgen action via testicular peritubular myoid cells is essential for male fertility. Faseb J.
35. Zhang C, Yeh S, Chen YT, Wu CC, Chuang KH, et al. (2006) Oligozoospermia with normal fertility in male mice lacking the androgen receptor in testis peritubular myoid cells. Proc Natl Acad Sci U S A 103: 17718-17723.
36. Frutkin AD, Shi H, Otsuka G, Leveen P, Karlsson S, et al. (2006) A critical developmental role for tgfbr2 in myogenic cell lineages is revealed in mice expressing SM22-Cre, not SMMHC-Cre. J Mol Cell Cardiol 41: 724-731.
37. Kotite NJ, Nayfeh SN, French FS (1978) FSH and androgen regulation of Sertoli cell function in the immature rat. Biol Reprod 18: 65-73.
38. Denolet E, De Gendt K, Allemeersch J, Engelen K, Marchal K, et al. (2006) The effect of a sertoli cell-selective knockout of the androgen receptor on testicular gene expression in prepubertal mice. Mol Endocrinol 20: 321-334.
39. Bergh A (1988) Treatment with human chorionic gonadotropin induces inflammation-like changes in the testicular microcirculation in adult unilaterally cryptorchid rats. Horm Res 30: 207-209.
40. Maddocks S, Setchell BP (1989) Effect of a single injection of human chorionic gonadotrophin on testosterone levels in testicular interstitial fluid, and in testicular and peripheral venous blood in adult rats. J Endocrinol 121: 311-316.
41. Setchell BP, Sharpe RM (1981) Effect of injected human chorionic gonadotro-phin on capillary permeability, extracellular fluid volume and the flow of lymph and blood in the testes of rats. J Endocrinol 91: 245-254.
42. Liu PY, Death AK, Handelsman DJ (2003) Androgens and cardiovascular disease. Endocr Rev 24: 313-340.
43. Weidemann W, Hanke H (2002) Cardiovascular effects of androgens. Cardiovasc Drug Rev 20: 175-198.
44. Stallone JN, Salisbury RL, Fulton CT (2001) Androgen-receptor defect abolishes sex differences in nitric oxide and reactivity to vasopressin in rat aorta. J Appl Physiol 91: 2602-2610.
45. Jones RD, Pugh PJ, Hall J, Channer KS, Jones TH (2003) Altered circulating hormone levels, endothelial function and vascular reactivity in the testicular feminised mouse. Eur J Endocrinol 148: 111-120.
46. Paul C, Teng S, Saunders PT (2009) A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 80: 913-919.
47. Lissbrant E, Collin O, Bergh A (1997) Localization and effects of calcitonin gene-related peptide in the testicular vasculature of the rat. J Androl 18: 385-392.
48. Sharpe RM, Kerr JB, McKinnell C, Millar M (1994) Temporal relationship between androgen-dependent changes in the volume of seminiferous tubule fluid, lumen size and seminiferous tubule protein secretion in rats. J Reprod Fertil 101: 193-198.
49. Jegou B, Le Gac F, de Kretser DM (1982) Seminiferous tubule fluid and interstitial fluid production. I. Effects of age and hormonal regulation in immature rats. Biol Reprod 27: 590-595.
50. Walker WH, Cheng J (2005) FSH and testosterone signaling in Sertoli cells. Reproduction 130: 15-28.