Androgen receptor signalling in peritubular myoid cells is essential for normal differentiation and function of adult Leydig cells

International Journal of Andrology

Volumn 35, Issue 1, 2012, Pages 25-40

  Welsh, M ^a   Moffat, L ^a   Belling, K ^b   de Franca L R ^c   Segatelli, T M ^c   Saunders, P T K ^a   Sharpe, R M ^a   Smith, L B ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Androgen receptor; Hormone receptors; Hormones; Leydig cell; Peritubular cells; Steroidogenic enzymes; Testosterone

Indexed keywords

ANDROGEN RECEPTOR; HORMONE RECEPTOR; LUTEINIZING HORMONE RECEPTOR; SOMATOMEDIN C; STEROIDOGENIC FACTOR 1; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; HORMONE DETERMINATION; IN VITRO STUDY; IN VIVO STUDY; LEYDIG CELL; MALE; MOUSE; NONHUMAN; PERITUBULAR MYOID CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TESTIS CELL;

ANIMALS; CELL DIFFERENTIATION; LEYDIG CELLS; MALE; MICE; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION;

EID: 84855701499     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2011.01150.x     Document Type: Article

References (58)

1. Baker PJ & O'Shaughnessy PJ. (2001a) Expression of prostaglandin D synthetase during development in the mouse testis. Reproduction 122, 553-559.
2. Baker PJ & O'Shaughnessy PJ. (2001b) Role of gonadotrophins in regulating numbers of Leydig and Sertoli cells during fetal and postnatal development in mice. Reproduction 122, 227-234.
3. Baker PJ, Johnston H, Abel M, Charlton HM & O'Shaughnessy PJ. (2003) Differentiation of adult-type Leydig cells occurs in gonadotrophin-deficient mice. Reprod Biol Endocrinol 1, 4. doi:10.1186/1477-7827-1-4.
4. Christensen AK & Fawcett DW. (1966) The fine structure of testicular interstitial cells in mice. Am J Anat 118, 551-571.
5. Clark AM, Garland KK et al. (2000) Desert hedgehog (Dhh) gene is required in the mouse testis for formation of adult-type Leydig cells and normal development of peritubular cells and seminiferous tubules. Biol Reprod 63, 1825-1838.
6. Corker CS & Davidson DW. (1978) A radioimmunoassay for testosterone in various biological fluids without chromatography. J Steroid Biochem 9, 373-374.
7. De Gendt K, Swinnen JV et al. (2004) A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA 101, 1327-1332.
8. De Gendt K, Atanassova N et al. (2005) Development and function of the adult generation of Leydig cells in mice with Sertoli cell-selective or total ablation of the androgen receptor. Endocrinology 146, 4117-4126.
9. Ferlin A, Pepe A et al. (2009) New roles for INSL3 in adults. Ann N Y Acad Sci 1160, 215-218.
10. Fisher JS, Macpherson S et al. (2003) Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate. Hum Reprod 18, 1383-1394.
11. Foresta C, Bettella A et al. (2004) A novel circulating hormone of testis origin in humans. J Clin Endocrinol Metab 89, 5952-5958.
12. Ge RS, Shan LX et al. (1996) Pubertal development of Leydig cells. In: The Leydig Cell (eds AH Payne, M Hardy & LD Russell), pp. 160-172. Cache River Press, Vienna, IL.
13. Gnessi L, Basciani S et al. (2000) Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 149, 1019-1026.
14. Habert R, Lejeune H et al. (2001) Origin, differentiation and regulation of fetal and adult Leydig cells. Mol Cell Endocrinol 179, 47-74.
15. Haider SG. (2004) Cell biology of Leydig cells in the testis. Int Rev Cytol 233, 181-241.
16. Handelsman DJ. (2008) Androgens. In: Endocrinology of Male Reproduction (ed. R. McLachlan), Available at: http://www.endotext.org/male/index.htm.
17. Hardy MP, Zirkin BR et al. (1989) Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 124, 762-770.
18. Hiroi H, Christenson LK et al. (2004) Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification. Mol Cell Endocrinol 215, 119-126.
19. Hoivik EA, Lewis AE et al. (2010) Molecular aspects of steroidogenic factor 1 (SF-1). Mol Cell Endocrinol 315, 27-39.
20. Huhtaniemi I & Toppari J. (1995) Endocrine, paracrine and autocrine regulation of testicular steroidogenesis. Adv Exp Med Biol 377, 33-54.
21. Ikeda Y, Shen WH et al. (1994) Developmental expression of mouse steroidogenic factor-1, an essential regulator of the steroid hydroxylases. Mol Endocrinol 8, 654-662.
22. Ivell R & Bathgate RA. (2002) Reproductive biology of the relaxin-like factor (RLF/INSL3). Biol Reprod 67, 699-705.
23. Keeney DS, Mendis-Handagama SM et al. (1988) Effect of long term deprivation of luteinizing hormone on Leydig cell volume, Leydig cell number, and steroidogenic capacity of the rat testis. Endocrinology 123, 2906-2915.
24. Keeney DS, Sprando RL et al. (1990) Reversal of long-term LH deprivation on testosterone secretion and Leydig cell volume, number and proliferation in adult rats. J Endocrinol 127, 47-58.
25. Khan S, Teerds K et al. (1992) Growth factor requirements for DNA synthesis by Leydig cells from the immature rat. Biol Reprod 46, 335-341.
26. Kroft TL, Patterson J et al. (2001) GLI1 localization in the germinal epithelial cells alternates between cytoplasm and nucleus: upregulation in transgenic mice blocks spermatogenesis in pachytene. Biol Reprod 65, 1663-1671.
27. Mariani S, Basciani S et al. (2002) PDGF and the testis. Trends Endocrinol Metab 13, 11-17.
28. Matsui H & Takahashi T. (2001) Mouse testicular Leydig cells express Klk21, a tissue kallikrein that cleaves fibronectin and IGF-binding protein-3. Endocrinology 142, 4918-4929.
29. Matsui H, Moriyama A et al. (2000) Cloning and characterization of mouse klk27, a novel tissue kallikrein expressed in testicular Leydig cells and exhibiting chymotrypsin-like specificity. Eur J Biochem 267, 6858-6865.
30. Matsui H, Takano N et al. (2005) Characterization of mouse glandular kallikrein 24 expressed in testicular Leydig cells. Int J Biochem Cell Biol 37, 2333-2343.
31. McLachlan RI, O'Donnell L, Meacham SJ, Stanton PG, de Krester DM, Pratis K & Robertson DM. (2002) Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 57, 149-179.
32. McNeilly JR, Saunders PT 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.
33. Mendis-Handagama SM & Ariyaratne HB. (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65, 660-671.
34. Mendis-Handagama SM, Ariyaratne HB et al. (2007) Expression of insulin-like peptide 3 in the postnatal rat Leydig cell lineage: timing and effects of triiodothyronine-treatment. Reproduction 133, 479-485.
35. Miller WL. (1998) Early steps in androgen biosynthesis: from cholesterol to DHEA. Baillieres Clin Endocrinol Metab 12, 67-81.
36. Murphy L, Jeffcoate IA et al. (1994) Abnormal Leydig cell development at puberty in the androgen-resistant Tfm mouse. Endocrinology 135, 1372-1377.
37. Nef S, Shipman T et al. (2000) A molecular basis for estrogen-induced cryptorchidism. Dev Biol 224, 354-361.
38. O'Shaughnessy PJ, Johnston H et al. (2002) Failure of normal adult Leydig cell development in androgen-receptor-deficient mice. J Cell Sci 115(Pt 17), 3491-3496.
39. Payne AH, Downing JR et al. (1980) Luteinizing hormone receptors and testosterone synthesis in two distinct populations of Leydig cells. Endocrinology 106, 1424-1429.
40. Pusch W, Balvers M et al. (1996) Molecular cloning and expression of the relaxin-like factor from the mouse testis. Endocrinology 137, 3009-3013.
41. Quigley CA, De Bellis A et al. (1995) Androgen receptor defects: historical, clinical, and molecular perspectives. Endocr Rev 16, 271-321.
42. Qureshi SJ & Sharpe RM. (1993) Evaluation of possible determinants and consequences of Leydig cell heterogeneity in man. Int J Androl 16, 293-305.
43. Schill WB & Miska W. (1992) Possible effects of the kallikrein-kinin system on male reproductive functions. Andrologia 24, 69-75.
44. Scott HM, Mason JI et al. (2009) Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr Rev 30, 883-925.
45. Shan LX & Hardy MP. (1992) Developmental changes in levels of luteinizing hormone receptor and androgen receptor in rat Leydig cells. Endocrinology 131, 1107-1114.
46. Shan LX, Phillips DM et al. (1993) Differential regulation of steroidogenic enzymes during differentiation optimizes testosterone production by adult rat Leydig cells. Endocrinology 133, 2277-2283.
47. Sharpe RM. (1994) Regulation of spermatogenesis. In: The Physiology of Reproduction (eds E Knobil & JD Neill), pp. 1363-2434. Raven, New York.
48. Tan KA, De Gendt K et al. (2005) The role of androgens in Sertoli cell proliferation and functional maturation: studies in mice with total or Sertoli cell-selective ablation of the androgen receptor. Endocrinology 146, 2674-2683.
49. Vergouwen RP, Jacobs SG et al. (1991) Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice. J Reprod Fertil 93, 233-243.
50. Wang GM, O'Shaughnessy PJ et al. (2003) Effects of insulin-like growth factor I on steroidogenic enzyme expression levels in mouse leydig cells. Endocrinology 144, 5058-5064.
51. Welsh M, Sharpe RM et al. (2010) Androgen action via testicular arteriole smooth muscle cells is important for Leydig cell function, vasomotion and testicular fluid dynamics. PLoS ONE 5, e13632.
52. Welsh M, Saunders PT et al. (2006) Androgen-dependent mechanisms of Wolffian duct development and their perturbation by flutamide. Endocrinology 147, 4820-4830.
53. Welsh M, Saunders PT et al. (2009) Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J 23, 4218-4230.
54. Wu X, Arumugam R et al. (2010) Androgen profiles during pubertal Leydig cell development in mice. Reproduction 140, 113-121.
55. Xin HB, Deng KY et al. (2002) Smooth muscle expression of Cre recombinase and eGFP in transgenic mice. Physiol Genomics 10, 211-215.
56. Yao HH, Whoriskey W et al. (2002) Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16, 1433-1440.
57. Zhang FP, Poutanen M et al. (2001) Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol Endocrinol 15, 172-183.
58. Zhang FP, Pakarainen T et al. (2004) Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 145, 1453-1463.