Mouse Testis Development and Function Are Differently Regulated by Follicle-Stimulating Hormone Receptors Signaling During Fetal and Prepubertal Life

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Migrenne, Stéphanie ^a,b,c   Moreau, Evelyne ^a,b,c   Pakarinen, Pirjo ^d   Dierich, Andrée ^e,f   Merlet, Jorge ^a,b,c   Habert, René ^a,b,c   Racine, Chrystèle ^a,b,c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^c Universite Paris Sud   (France)

^d UNIVERSITY OF TURKU   (Finland)

^e INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^f INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CLAUDIN 11; FOLLICLE STIMULATING HORMONE RECEPTOR; FOLLITROPIN; HORMONE RECEPTOR; LUTEINIZING HORMONE; MESSENGER RNA; SONIC HEDGEHOG PROTEIN; STEROID 17ALPHA MONOOXYGENASE; TRANSFERRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CLAUDIN 11 GENE; CONTROLLED STUDY; DESERT HEDGEHOG GENE; DOWN REGULATION; GENE OVEREXPRESSION; GERM CELL; HORMONE ACTION; HORMONE BLOOD LEVEL; HORMONE DETERMINATION; INTRACELLULAR SIGNALING; LEYDIG CELL; MALE; MOUSE; NONHUMAN; P450 17ALPHA HYDROXYLASE GENE; SERTOLI CELL; STEROIDOGENIC ACUTE REGULATORY PROTEIN GENE; TESTIS DEVELOPMENT; TESTIS FUNCTION; TRANSFERRIN GENE; WILD TYPE;

ANIMALS; FOLLICLE STIMULATING HORMONE; LEYDIG CELLS; MALE; MICE; MICE, KNOCKOUT; RECEPTORS, FSH; SERTOLI CELLS; SIGNAL TRANSDUCTION; TESTIS; TESTOSTERONE;

ERINACEIDAE; MUS; RATTUS;

EID: 84871665170     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053257     Document Type: Article

References (56)

1. Magre S, Jost A, (1991) Sertoli cells and testicular differentiation in the rat fetus. J Electron Microsc Tech 19: 172-188.
2. Orth JM, (1982) Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 203: 485-492.
3. Vergouwen RP, Jacobs SG, Huiskamp R, Davids JA, de Rooij DG, (1991) Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice. J Reprod Fertil 93: 233-243.
4. Vergouwen RP, Huiskamp R, Bas RJ, Roepers-Gajadien HL, Davids JA, et al. (1993) Postnatal development of testicular cell populations in mice. J Reprod Fertil 99: 479-485.
5. Saez JM, (1994) Leydig cells: endocrine, paracrine, and autocrine regulation. Endocr Rev 15: 574-626.
6. Habert R, Lejeune H, Saez JM, (2001) Origin, differentiation and regulation of fetal and adult Leydig cells. Mol Cell Endocrinol 179: 47-74.
7. Svechnikov K, Soder O, (2008) Ontogeny of gonadal sex steroids. Best Pract Res Clin Endocrinol Metab 22: 95-106.
8. Scott HM, Mason JI, Sharpe RM, (2009) Steroidogenesis in the fetal testis and its susceptibility to disruption by exogenous compounds. Endocr Rev 30: 883-925.
9. Warren DW, Haltmeyer GC, Eik-Nes KB, (1973) Testosterone in the fetal rat testis. Biol Reprod 8: 560-565.
10. Habert R, Picon R, (1984) Testosterone, dihydrotestosterone and estradiol-17 beta levels in maternal and fetal plasma and in fetal testes in the rat. J Steroid Biochem 21: 193-198.
11. Livera G, Rouiller-Fabre V, Durand P, Habert R, (2000) Multiple effects of retinoids on the development of Sertoli, germ, and Leydig cells of fetal and neonatal rat testis in culture. Biol Reprod 62: 1303-1314.
12. Livera G, Delbes G, Pairault C, Rouiller-Fabre V, Habert R, (2006) Organotypic culture, a powerful model for studying rat and mouse fetal testis development. Cell Tissue Res 324: 507-521.
13. Kerr JB, Knell CM, (1988) The fate of fetal Leydig cells during the development of the fetal and postnatal rat testis. Development 103: 535-544.
14. Baker PJ, Sha JA, McBride MW, Peng L, Payne AH, et al. (1999) Expression of 3beta-hydroxysteroid dehydrogenase type I and type VI isoforms in the mouse testis during development. Eur J Biochem 260: 911-917.
15. O'Shaughnessy PJ, Fowler PA, (2011) Endocrinology of the mammalian fetal testis. Reproduction 141: 37-46.
16. Nef S, Shipman T, Parada LF, (2000) A molecular basis for estrogen-induced cryptorchidism. Dev Biol 224: 354-361.
17. Huhtaniemi I, (1989) Endocrine function and regulation of the fetal and neonatal testis. Int J Dev Biol 33: 117-123.
18. McLean DJ, Friel PJ, Pouchnik D, Griswold MD, (2002) Oligonucleotide microarray analysis of gene expression in follicle-stimulating hormone-treated rat Sertoli cells. Mol Endocrinol 16: 2780-2792.
19. Krishnamurthy H, Kats R, Danilovich N, Javeshghani D, Sairam MR, (2001) Intercellular communication between Sertoli cells and Leydig cells in the absence of follicle-stimulating hormone-receptor signaling. Biol Reprod 65: 1201-1207.
20. Baker PJ, Pakarinen P, Huhtaniemi IT, Abel MH, Charlton HM, et al. (2003) Failure of normal Leydig cell development in follicle-stimulating hormone (FSH) receptor-deficient mice, but not FSHbeta-deficient mice: role for constitutive FSH receptor activity. Endocrinology 144: 138-145.
21. Kerr JB, Sharpe RM, (1985) Stimulatory effect of follicle-stimulating hormone on rat Leydig cells. A morphometric and ultrastructural study. Cell Tissue Res 239: 405-415.
22. Teerds KJ, Closset J, Rommerts FF, de Rooij DG, Stocco DM, et al. (1989) Effects of pure FSH and LH preparations on the number and function of Leydig cells in immature hypophysectomized rats. J Endocrinol 120: 97-106.
23. Barakat B, Itman C, Mendis SH, Loveland KL, (2012) Activins and inhibins in mammalian testis development: New models, new insights. Mol Cell Endocrinol 359: 66-77.
24. Rannikki AS, Zhang FP, Huhtaniemi IT, (1995) Ontogeny of follicle-stimulating hormone receptor gene expression in the rat testis and ovary. Mol Cell Endocrinol 107: 199-208.
25. Lecerf L, Rouiller-Fabre V, Levacher C, Gautier C, Saez JM, et al. (1993) Stimulatory effect of follicle-stimulating hormone on basal and luteinizing hormone-stimulated testosterone secretions by the fetal rat testis in vitro. Endocrinology 133: 2313-2318.
26. Orth JM, (1984) The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats. Endocrinology 115: 1248-1255.
27. Migrenne S, Racine C, Guillou F, Habert R, (2003) Pituitary hormones inhibit the function and differentiation of fetal Sertoli cells. Endocrinology 144: 2617-2622.
28. Japon MA, Rubinstein M, Low MJ, (1994) In situ hybridization analysis of anterior pituitary hormone gene expression during fetal mouse development. J Histochem Cytochem 42: 1117-1125.
29. Baker PJ, O'Shaughnessy PJ, (2001) Role of gonadotrophins in regulating numbers of Leydig and Sertoli cells during fetal and postnatal development in mice. Reproduction 122: 227-234.
30. Johnston H, Baker PJ, Abel M, Charlton HM, Jackson G, et al. (2004) Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse. Endocrinology 145: 318-329.
31. O'Shaughnessy PJ, Monteiro A, Abel M, (2012) Testicular development in mice lacking receptors for follicle stimulating hormone and androgen. PLoS One 7: e35136.
32. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, et al. (1998) Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A 95: 13612-13617.
33. Merlet J, Racine C, Moreau E, Moreno SG, Habert R, (2007) Male fetal germ cells are targets for androgens that physiologically inhibit their proliferation. Proc Natl Acad Sci U S A 104: 3615-3620.
34. Habert R, Picon R, (1982) Control of testicular steroidogenesis in foetal rat: effect of decapitation on testosterone and plasma luteinizing hormone-like activity. Acta Endocrinol (Copenh) 99: 466-473.
35. Kero J, Poutanen M, Zhang FP, Rahman N, McNicol AM, et al. (2000) Elevated luteinizing hormone induces expression of its receptor and promotes steroidogenesis in the adrenal cortex. J Clin Invest 105: 633-41.
36. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, et al. (2000) The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 141: 1795-803.
37. Delbes G, Levacher C, Pairault C, Racine C, Duquenne C, et al. (2004) Estrogen receptor beta-mediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endocrinology 145: 3395-3403.
38. Delbes G, Levacher C, Duquenne C, Racine C, Pakarinen P, et al. (2005) Endogenous estrogens inhibit mouse fetal Leydig cell development via estrogen receptor alpha. Endocrinology 146: 2454-2461.
39. Tan KA, De Gendt K, Atanassova N, Walker M, Sharpe RM, 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.
40. Ketola I, Rahman N, Toppari J, Bielinska M, Porter-Tinge SB, et al. (1999) Expression and regulation of transcription factors GATA-4 and GATA-6 in developing mouse testis. Endocrinology 140: 1470-1480.
41. Heikinheimo M, Ermolaeva M, Bielinska M, Rahman NA, Narita N, et al. (1997) Expression and hormonal regulation of transcription factors GATA-4 and GATA-6 in the mouse ovary. Endocrinology 138: 3505-3514.
42. Skinner MK, Griswold MD, (1980) Sertoli cells synthesize and secrete transferrin-like protein. J Biol Chem 255: 9523-9525.
43. Norton JN, Skinner MK, (1989) Regulation of Sertoli cell function and differentiation through the actions of a testicular paracrine factor P-Mod-S. Endocrinology 124: 2711-2719.
44. Gow A, Southwood CM, Li JS, Pariali M, Riordan GP, et al. (1999) CNS myelin and Sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99: 649-659.
45. Al-Attar L, Noel K, Dutertre M, Belville C, Forest MG, et al. (1997) Hormonal and cellular regulation of Sertoli cell anti-Mullerian hormone production in the postnatal mouse. J Clin Invest 100: 1335-1343.
46. Kuroda T, Lee MM, Haqq CM, Powell DM, Manganaro TF, et al. (1990) Mullerian inhibiting substance ontogeny and its modulation by follicle-stimulating hormone in the rat testes. Endocrinology 127: 1825-1832.
47. Migrenne S, Pairault C, Racine C, Livera G, Geloso A, et al. (2001) Luteinizing hormone-dependent activity and luteinizing hormone-independent differentiation of rat fetal Leydig cells. Mol Cell Endocrinol 172: 193-202.
48. Abel MH, Baban D, Lee S, Charlton HM, O'Shaughnessy PJ, (2009) Effects of FSH on testicular mRNA transcript levels in the hypogonadal mouse. J Mol Endocrinol 42: 291-303.
49. Yao HH, Whoriskey W, Capel B, (2002) Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16: 1433-1440.
50. Park SY, Tong M, Jameson JL, (2007) Distinct roles for steroidogenic factor 1 and desert hedgehog pathways in fetal and adult Leydig cell development. Endocrinology 148: 3704-3710.
51. Racine C, Rey R, Forest MG, Louis F, Ferre A, et al. (1998) Receptors for anti-mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci U S A 95: 594-599.
52. Rouiller-Fabre V, Carmona S, Merhi RA, Cate R, Habert R, et al. (1998) Effect of anti-Mullerian hormone on Sertoli and Leydig cell functions in fetal and immature rats. Endocrinology 139: 1213-1220.
53. Picon R, Habert R, (1981) A sensitive bioassay for luteinizing hormone-like activity applied to systemic plasmas of foetal rats. Acta Endocrinol (Copenh) 97: 176-180.
54. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG, et al. (2000) The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 141: 1795-1803.
55. Sharpe RM, Skakkebaek NE, (2008) Testicular dysgenesis syndrome: mechanistic insights and potential new downstream effects. Fertil Steril 89: e33-38.
56. Habert R, Muczynski V, Lehraiki A, Lambrot R, Lecureuil C, et al. (2009) Adverse effects of endocrine disruptors on the foetal testis development: focus on the phthalates. Folia Histochem Cytobiol 47: S67-74.