Multiple effects of retinoids on the development of Sertoli, germ, and Leydig cells of fetal and neonatal rat testis in culture

Biology of Reproduction

Volumn 62, Issue 5, 2000, Pages 1303-1314

  Livera, G ^a   Rouiller Fabre, V ^a   Durand, P ^b   Habert, René ^a,c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b HÔPITAL DEBROUSSE   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; LUTEINIZING HORMONE; RETINOID;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL LABELING; CONCEPTION; DOSE RESPONSE; GERM CELL; LEYDIG CELL; LUTEINIZING HORMONE BLOOD LEVEL; MITOSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SERTOLI CELL; SEX DIFFERENCE; TESTIS;

ANIMALIA;

EID: 0034007028     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod62.5.1303     Document Type: Article

References (57)

1. George F, Wilson J. Sex determination and differentiation. In: Knobil E, Neill J (eds.), The Physiology of Reproduction. Vol. 1. New York: Raven Press; 1994: 3-28.
2. Jost A, Magre S. Sexual differentiation. In: Thibault C, Levasseur M, Hunter RHF (eds.), Reproduction in Mammals and Man. Paris: Ellipses; 1993: 197-226.
3. Magre S, Josi A. The initial phases of testicular organogenesis in the rat. An electron microscopy study. Arch Anat Microsc Morphol Exp 1980; 69:297-318.
4. Pelliniemi LJ, Fröjdman K, Paranko J. Embryological and prenatal development and function of Sertoli cells. In: Russell LD. Griswold MD (eds.), The Sertoli Cell. Vienna, IL: Cache River Press; 1993: 88-113.
5. Beaumont HM, Mandl AM. A quantitative study of primordial germ cells in the rat. J Embryol Exp Morphol 1963; 11:715-740.
6. Boulogne B, Olaso R, Levacher C, Durand P, Habert R. Apoptosis and mitosis in the gonocytes of the rat testis during fetal and neonatal development. Int J Androl 1999; 22:356-365.
7. Lejeune H, Habert R, Saez J. Origin, proliferation and differentiation of Leydig cells. J Mol Endocrinol 1998; 20:1-25.
8. Warren DW, Haltmeyer GC, Eik-Nes KB. Testosterone in the fetal rat testis. Biol Reprod 1973; 8:560-565.
9. Habert R, Picon R. Testosterone, dihydrotestosterone and estradiol 17β levels in maternal and fetal plasma and in fetal testes in the rat. J Steroid Biochem 1984; 21:193-198.
10. Habert R, Brignaschi P. Developmental changes in vitro testosterone production by dispersed Leydig cells during fetal life in rats. Arch Androl 1991; 27:65-71.
11. Habert R. In vivo acute testicular testosterone response to injection of luteinizing hormone in the rat fetus. Acta Endocrinol 1993; 128:268-273.
12. Chytil F. Retinoids in lung development. FASEB J 1996; 10:986-992.
13. Lelièvre-Pégorier M, Vilar J, Ferrier M, Moreau E, Freund N, Gilbert T, Merlet-Bénichou C. Mild vitamin A deficiency leads to inborn nephron deficit in the rat. Kidney int 1998; 54:1455-1462.
14. Van Pelt AM, de Rooij DG. Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol Reprod 1990; 43:363-367.
15. Gaemers IC, Van Pelt AMM, De Rooij DG. All-trans-4-oxo-retinoic acid: a potent inducer of in vivo proliferation of growth arrested A spermatogonia in the vitamin A-deficient mouse testis. Endocrinology 1996; 1996:479-485.
16. Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, Le Meur M, Chambon P. High postnatal lethality and testis degeneration in retinoic acid receptor α mutant mice. Dev Biol 1993; 90:7225-7229.
17. Kastner P, Mark M, Mark L, Dierich A, Chambon P. Abnormal spermatogenesis in RXRβ mutant mice. Gene Dev 1996; 10:80-92.
18. Zheng WL, Bucco RA, Schmit MC, Wardlaw SA, Ong DE. Localisation of cellular retinoic acid-binding protein (CRABP) II and CRABP in developing rat testis. Endocrinology 1996; 137:5028-5035.
19. Cupp A, Dufour J, Kim G, Skinner M, Kim K. Action of retinoids on embryonic and early postnatal testis development. Endocrinology 1999; 140:2343-2352.
20. Boulogne B, Levacher C, Durand P, Habert R. Retinoic acid receptors and retinoid X receptors in the rat testis during fetal and postnatal development: immunolocalization and implication in the control of the number of gonocytes. Biol Reprod 1999; 61:1548-1557.
21. Marinos E, Kulukussa M, Zotos A, Kittas C. Retinoic acid affects basement membrane formation of the seminiferous cords in 14-day male rat gonads in vitro. Differentiation 1995; 59:87-94.
22. Magre S, Jost A. Sertoli cells and testicular differentiation in the rat fetus. J Electron Microsc Tech 1991; 19:172-188.
23. Olaso R, Pairault C, Boulogne B, Durand P, Habert R. Transforming growth factor β1 and β2 reduce the number of gonocytes by increasing apoptosis. Endocrinology 1998; 139:733-740.
24. Habert R, Devif I, Gangncrau MN, Lecert L. Ontogenesis of the in vitro response of rat testis to gonadotropin-releasing hormone. Mol Cell Endocrinol 1991; 82:199-206.
25. Mannaerts B, Deleeuv R, Geelen J, Van Ravestein A, Van Wezenbcck P, Schuursa A, Kloosterboer H. Comparative in vitro and in vivo studies on biological characteristics of recombinant human follicle-stimulating hormone. Endocrinology 1991; 129:2623-2630.
26. Abercrombie M. Estimation of nuclear population from microtome sections. Anal Rec 1946; 94:238-248.
27. Vigier B, Tran D, Du Mesnil du Buisson F, Heyman Y, Josso N. Use of monoclonal antibody techniques to study the ontogeny of bovine anti-Müllerian hormone. J Reprod Fertil 1983; 69:207-214.
28. Harper J, Brooker G. Fentomole sensitive radioimmunoassay for cyclic AMP and GMP after 2′-O-acctylation by acetic anhydride in aqueous solution. J Cyclic Nucleic Res 1975; 1:207-218.
29. Orth JM. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anal Rec 1982; 203:485-492.
30. Aubert M, Begeot M, Winiger B, Morel G, Sizonenko P, Dubois P. Ontogeny of hypothalamic luteinizing hormone-releasing hormone (GnRH) and pituitary GnRH receptors in fetal and neonatal rats. Endocrinology 1985; 116:1565-1575.
31. Orth JM. The role of follicle-stimulating hormone in controlling sertoli cell proliferation in testes of fetal rats. Endocrinology 1984; 115: 1248-1255.
32. De Miguel MP, de Boer-Brouwer M, de Rooij DG, Paniagua R, van Dissel-Emiliani FMF. Ontogeny and localization of an oncostatin M-like protein in the rat testis: its possible role at the start of spermatogenesis. Cell Growth Differ 1997; 8:611-618.
33. Habert R, Picon R. Control of testicular steroidogenesis in fetal rat: effect of decapitation on testosterone and plasma luteinizing hormone-like activity. Acta Endocrinol 1982; 99:466-473.
34. Vilar J, Gilbert T, Moreau E, Merlet-Bénichou C. Metanephros organogenesis is highly stimulated by vitamin A derivatives in organ culture. Kidney Int 1996; 49:1478-1487.
35. Moro Balbas J, Gato A, Alonso Revuelta M, Pastor J, Repressa J, Barbosa E. Retinoic acid induces changes in the rhombencephalic neural crest cells migration and extracellular matrix composition in chick embryos. Teratology 1993; 48:197-206.
36. Braunhut S, Moses M. Retinoids modulate endothelial cell production of matrix-degrading proteases and tissue inhibitors of metalloproteinases (TIMP). J Biol Chem 1994; 1994:13472-13479.
37. Jost A, Perlman S, Valentino O, Castanier M, Scholler R, Magre S. Experimental control of the differentiation of Leydig cells in the rat fetal testis. Proc Natl Acad Sci USA 1988; 85:8094-8097.
38. Merchant H. Rat gonadal and ovarian organogenesis with and without germ cells. An ultrastructural study. Dev Biol 1975; 44:1-21.
39. Magre S, Agelopoulou R, Jost A. Action du sérum de foetus de veau sur la différenciation in vitro ou le maintien des cordons séminifères du testicule du foetus de rat. C R Acad Sci (Paris) 1981; 292:85-89.
40. Taketo T, Thau R, Adeyemo O, Koide S. Influence of adenosine 3′: 5′-cyclic monophosphate analogues on testicular organization of fetal mouse gonads in vitro. Biol Reprod 1984; 30:189-198.
41. Jaillard C, Chatelain PG, Saez JM. In vitro regulation of pig Sertoli cell growth and function: effects of fibroblast growth factor and somatomedin-C. Biol Reprod 1987; 37:665-674.
42. Lecerf L, Rouiller-Fabre V, Levacher C, Gautier C, Saez J, Habert R. Stimulatory effect of follicle-stimulating hormone on basal and luteinizing hormone-stimulated testosterone secretion by fetal rat testis in vitro. Endocrinology 1993; 133:2313-2318.
43. Rannikki AS, Zhang FP, Huhtaniemi IT. Ontogeny of follicle-stimulating hormone receptor gene expression in the rat testis and ovary. Mol Cell Endocrinol 1995; 107:199-208.
44. Eskola V, Nikula H, Huhtaniemi I. Age-related variation of follicle-stimulating hormone-stimulated cAMP production, protein kinase C activity and their interactions in the rat testis. Mol Cell Endocrinol 1993; 93:143-148.
45. Galdieri M, Nistico L. Retinoids regulate gonadotropin action in cultured rat Sertoli cells. Biol Reprod 1994; 50:171-177.
46. Mehta K, McQueen T, Neamali N, Collins S, Andreeff M. Activation of retinoid receptors RARα and RXRα induces differentiation and apoptosis, respectively, in HL-60 cells. Cell Growth Differ 1996; 7: 179-186.
47. Szondy Z, Reichert U, Bernardon JM, Michel S, Toth R, Ancian P, Ajzner E, Fesus L. Induction of apoptosis by retinoic acid receptor γ-selective compounds in mouse thymocytes through a novel apoptosis pathway. Mol Pharmacol 1997; 51:972-982.
48. McCoshen JA, McCallion DJ. A study of the primordial germ cells during their migratory phase in Steel mutant mice. Experientia 1975; 31:589-590.
49. Koshimizu U, Watanabe M, Nakatuji N. Retinoic acid is a potent growth activator of Mouse primordial germ cells in vitro. Dev Biol 1995; 168:683-685.
50. Kerr JB, Knell CM. The fate of foetal Leydig cells during the development of foetal and postnatal rat testis. Development 1988; 103:535-544.
51. Rich KA, Kerr JB, Kretser DM. Evidence for Leydig cell dysfunction in rals with seminiferous tubule damage. Mol Cell Endocrinol 1979; 13:123-135.
52. Appling DR, Chytil F Evidence of a role for retinoic acid (vitamin A-acid) in the maintenance of testosterone production in male rats. Endocrinology 1981; 108:2120-2123.
53. Chaudhary LR, Hutson JC, Stocco DM. Effect of retinol and retinoic acid on testosterone production by rat Leydig cells in primary culture. Biochem Biophys Res Commun 1989; 158:400-406.
54. Chaudhary LR, Stocco DM. An in vitro cell model system to study the action of retinoids on Leydig cell steroidogenesis. Biochem Int 1990; 21:1033-1042.
55. Lefevre A, Rogier E, Astraudo C, Duquenne C, Finaz C. Regulation by retinoids of luteinizing hormone/chorionic gonadotropin receptor, cholesterol side-chain cleavage cytochrome P-450, 3β-hydroxysteroid dehydrogenase/Δ5-4-isomerase and 17α-hydroxylase/C17-20 lyase cytochrome P-450 messenger ribonucleic acid levels in the K9 mouse Leydig cell line. Mol Cell Endocrinol 1994; 106:31-39.
56. Morera AM, Esposito G, Ghiglieri C, Chauvin MA, Hartman DJ, Benahmed M. Transforming growth factor β1 inhibits gonadotropin action in cultured porcine Sertoli cells. Endocrinology 1992; 130:831-836.
57. Gautier C, Levacher C, Saez JM, Habert R. Transforming growth factor β1 inhibits steroidogenesis in dispersed fetal testicular cells in culture. Mol Cell Endocrinol 1997; 131:21-30.