Thyroid hormone limits postnatal sertoli cell proliferation in vivo by activation of its alpha1 isoform receptor (tralpha1) present in these cells and by regulation of Cdk4/jund/c-myc mrna levels in mice

Biology of Reproduction

Volumn 87, Issue 1, 2012, Pages 16-

  Fumel, Betty ^a,b,c   Guerquin, Marie Justine ^d   Livera, Gabriel ^d   Staub, Christophe ^e   Magistrini, Miche'le ^a,b,c   Gauthier, Christophe ^a,b,c   Flamant, Frédéric ^f   Guillou, Florian ^a,b,c   Fouchécourt, Sophie ^a,b,c  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c IFCE   (France)

^d INSERM   (France)

^e CEMAGREF   (France)

^f Univ Lyon 1   (France)

Author keywords

Sertoli cells; T3; Tra1

Indexed keywords

CYCLIN DEPENDENT KINASE 4; MESSENGER RNA; MYC PROTEIN; THYROID HORMONE ALPHA1 ISOFORM RECEPTOR; THYROID HORMONE RECEPTOR ALPHA; TRANSCRIPTION FACTOR JUND; UNCLASSIFIED DRUG; CDK4 PROTEIN, MOUSE; JUND PROTEIN, MOUSE; LIOTHYRONINE; MYC PROTEIN, MOUSE; PROTEIN C JUN; THYROID HORMONE RECEPTOR BETA;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; EXPLANT; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; TESTIS WEIGHT; ANIMAL; CELL COUNT; CELL CYCLE; CYTOLOGY; DOWN REGULATION; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; SIGNAL TRANSDUCTION; TESTIS;

MUS;

ANIMALS; BASE SEQUENCE; CELL COUNT; CELL CYCLE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 4; DOWN-REGULATION; HUMANS; MALE; MICE; MICE, KNOCKOUT; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-JUN; PROTO-ONCOGENE PROTEINS C-MYC; RNA, MESSENGER; SERTOLI CELLS; SIGNAL TRANSDUCTION; TESTIS; THYROID HORMONE RECEPTORS ALPHA; THYROID HORMONE RECEPTORS BETA; TRIIODOTHYRONINE;

EID: 84867117848     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.098418     Document Type: Article

References (53)

1. Orth JM, Gunsalus GL, Lamperti AA. Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 1988; 122: 787-794.
2. Steinberger A, Steinberger E. Replication pattern of Sertoli cells in maturing rat testis in vivo and in organ culture. Biol Reprod 1971; 4: 84-87.
3. Nagy F. An autoradiographic study of the post-natal changes in (3H)leucine incorporation by Sertoli cell nuclei in rat testes. J Reprod Fertil 1974; 37: 353-359.
4. Vitale R, Fawcett DW, Dym M. The normal development of the bloodtestis barrier and the effects of clomiphene and estrogen treatment. Anat Rec 1973; 176: 331-344.
5. Ahmed EA, Barten-van Rijbroek AD, Kal HB, Sadri-Ardekani H, Mizrak SC, van Pelt AM, de Rooij DG. Proliferative activity in vitro and DNA repair indicate that adult mouse and human Sertoli cells are not terminally differentiated, quiescent cells. Biol Reprod 2009; 80: 1084-1091.
6. Mazaud-Guittot S, Meugnier E, Pesenti S, Wu X, Vidal H, Gow A, Le Magueresse-Battistoni B. Claudin 11 deficiency in mice results in loss of the Sertoli cell epithelial phenotype in the testis. Biol Reprod 2010; 82: 202-213.
7. Griswold M, Mably E, Fritz IB. Stimulation by follicle stimulating hormone and dibutyryl cyclic AMP of incorporation of 3H-thymidine into nuclear DNA of cultured Sertoli cell-enriched preparations from immature rats. Curr Top Mol Endocrinol 1975; 2: 413-420.
8. Griswold MD, Solari A, Tung PS, Fritz IB. Stimulation by folliclestimulating hormone of DNA synthesis and of mitosis in cultured Sertoli cells prepared from testes of immature rats. Mol Cell Endocrinol 1977; 7: 151-165.
9. Orth JM. The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats. Endocrinology 1984; 115: 1248-1255.
10. Meachem SJ, McLachlan RI, de Kretser DM, Robertson DM, Wreford NG. Neonatal exposure of rats to recombinant follicle stimulating hormone increases adult Sertoli and spermatogenic cell numbers. Biol Reprod 1996; 54: 36-44.
11. Singh J, Handelsman DJ. Neonatal administration of FSH increases Sertoli cell numbers and spermatogenesis in gonadotropin-deficient (hpg) mice. J Endocrinol 1996; 151: 37-48.
12. Jannini EA, Ulisse S, D'Armiento M. Thyroid hormone and male gonadal function. Endocr Rev 1995; 16: 443-459.
13. Cooke PS, Hess RA, Porcelli J, Meisami E. Increased sperm production in adult rats after transient neonatal hypothyroidism. Endocrinology 1991; 129: 244-248.
14. Cooke PS, Zhao YD, Bunick D. Triiodothyronine inhibits proliferation and stimulates differentiation of cultured neonatal Sertoli cells: possible mechanism for increased adult testis weight and sperm production induced by neonatal goitrogen treatment. Biol Reprod 1994; 51: 1000-1005.
15. van Haaster LH, de Jong FH, Docter R, de Rooij DG. High neonatal triiodothyronine levels reduce the period of Sertoli cell proliferation and accelerate tubular lumen formation in the rat testis, and increase serum inhibin levels. Endocrinology 1993; 133: 755-760.
16. Cooke PS, Meisami E. Early hypothyroidism in rats causes increased adult testis and reproductive organ size but does not change testosterone levels. Endocrinology 1991; 129: 237-243.
17. Palmero S, Prati M, Bolla F, Fugassa E. Tri-iodothyronine directly affects rat Sertoli cell proliferation and differentiation. J Endocrinol 1995; 145: 355-362.
18. Joyce KL, Porcelli J, Cooke PS. Neonatal goitrogen treatment increases adult testis size and sperm production in the mouse. J Androl 1993; 14: 448-455.
19. Marchlewska K, Kula K, Walczak-Jedrzejowska R, Oszukowska E, Filipiak E, Slowikowska-Hilczer J. Role of FSH and triiodothyronine in Sertoli cell development expressed by formation of connexin 43-based gap junctions. J Exp Zool A Ecol Genet Physiol 2011; 315: 329-336.
20. Hadj-Sahraoui N, Seugnet I, Ghorbel MT, Demeneix B. Hypothyroidism prolongs mitotic activity in the post-natal mouse brain. Neurosci Lett 2000; 280: 79-82.
21. Kress E, Samarut J, Plateroti M. Thyroid hormones and the control of cell proliferation or cell differentiation: paradox or duality? Mol Cell Endocrinol 2009; 313: 36-49.
22. Holsberger DR, Kiesewetter SE, Cooke PS. Regulation of neonatal Sertoli cell development by thyroid hormone receptor alpha1. Biol Reprod 2005; 73: 396-403.
23. Kirby JD, Arambepola N, Porkka-Heiskanen T, Kirby YK, Rhoads ML, Nitta H, Jetton AE, Iwamoto G, Jackson GL, Turek FW, Cooke PS. Neonatal hypothyroidism permanently alters follicle-stimulating hormone and luteinizing hormone production in the male rat. Endocrinology 1997; 138: 2713-2721.
24. Antony FF, Aruldhas MM, Udhayakumar RC, Maran RR, Govindarajulu P. Inhibition of Leydig cell activity in vivo and in vitro in hypothyroid rats. J Endocrinol 1995; 144: 293-300.
25. Quignodon L, Vincent S, Winter H, Samarut J, Flamant F. A point mutation in the activation function 2 domain of thyroid hormone receptor alpha1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol Endocrinol 2007; 21: 2350-2360.
26. Lecureuil C, Fontaine I, Crepieux P, Guillou F. Sertoli and granulosa cellspecific Cre recombinase activity in transgenic mice. Genesis 2002; 33: 114-118.
27. Fauquier T, Romero E, Picou F, Chatonnet F, Nguyen XN, Quignodon L, Flamant F. Severe impairment of cerebellum development in mice expressing a dominant-negative mutation inactivating thyroid hormone receptor alpha1 isoform. Dev Biol 2011; 356: 350-358.
28. De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, Claessens F, Lecureuil C, Heyns W, Carmeliet P, et al. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci U S A 2004; 101: 1327-1332.
29. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, Wegner M, Scherer G. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 2009; 327: 301-312.
30. Weider K, Bergmann M, Giese S, Guillou F, Failing K, Brehm R. Altered differentiation and clustering of Sertoli cells in transgenic mice showing a Sertoli cell specific knockout of the connexin 43 gene. Differentiation 2011; 82: 38-49.
31. Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, Willott JF, Sundin V, Roux JP, Malaval L, Hara M, Samarut J, et al. Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol 2001; 21: 4748-4760.
32. Lecureuil C, Staub C, Fouchecourt S, Maurel MC, Fontaine I, Martinat N, Gauthier C, Daudignon A, Delaleu B, Sow A, Jegou B, Guillou F. Transferrin overexpression alters testicular function in aged mice. Mol Reprod Dev 2007; 74: 197-206.
33. Hochereau-de Reviers MT, Perreau C, Pisselet C, Fontaine I, Monet-Kuntz C. Comparisons of endocrinological and testis parameters in 18-month-old Ile de France and Romanov rams. Domest Anim Endocrinol 1990; 7: 63-73.
34. Livera G, Delbes G, Pairault C, Rouiller-Fabre V, Habert R. Organotypic culture, a powerful model for studying rat and mouse fetal testis development. Cell Tissue Res 2006; 324: 507-521.
35. Merlet J, Moreau E, Habert R, Racine C. Development of fetal testicular cells in androgen receptor deficient mice. Cell Cycle 2007; 6: 2258-2262.
36. Oakberg EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 1956; 99: 507-516.
37. Zhang Q, Xiao X, Feng K, Wang T, Li W, Yuan T, Sun X, Sun Q, Xiang H, Wang H. Berberine moderates glucose and lipid metabolism through multipathway mechanism. Evid Based Complement Alternat Med 2011; 2011.
38. Xiao L, Rao JN, Zou T, Liu L, Marasa BS, Chen J, Turner DJ, Passaniti A, Wang JY. Induced JunD in intestinal epithelial cells represses CDK4 transcription through its proximal promoter region following polyamine depletion. Biochem J 2007; 403: 573-581.
39. Hernandez JM, Floyd DH, Weilbaecher KN, Green PL, Boris-Lawrie K. Multiple facets of junD gene expression are atypical among AP-1 family members. Oncogene 2008; 27: 4757-4767.
40. Haas K, Staller P, Geisen C, Bartek J, Eilers M, Moroy T. Mutual requirement of CDK4 and Myc in malignant transformation: evidence for cyclin D1/CDK4 and p16INK4A as upstream regulators of Myc. Oncogene 1997; 15: 179-192.
41. Hermeking H, Rago C, Schuhmacher M, Li Q, Barrett JF, Obaya AJ, O'Connell BC, Mateyak MK, Tam W, Kohlhuber F, Dang CV, Sedivy JM, et al. Identification of CDK4 as a target of c-MYC. Proc Natl Acad Sci U S A 2000; 97: 2229-2234.
42. Hess RA, Cooke PS, Bunick D, Kirby JD. Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased Sertoli and germ cell numbers. Endocrinology 1993; 132: 2607-2613.
43. Jannini EA, Dolci S, Ulisse S, Nikodem VM. Developmental regulation of the thyroid hormone receptor alpha 1 mRNA expression in the rat testis. Mol Endocrinol 1994; 8: 89-96.
44. Canale D, Agostini M, Giorgilli G, Caglieresi C, Scartabelli G, Nardini V, Jannini EA, Martino E, Pinchera A, Macchia E. Thyroid hormone receptors in neonatal, prepubertal, and adult rat testis. J Androl 2001; 22: 284-288.
45. Zamoner A, Pessoa-Pureur R, Silva FR. Membrane-initiated actions of thyroid hormones on the male reproductive system. Life Sci 2011; 89: 507-514.
46. Wrutniak-Cabello C, Casas F, Cabello G. Thyroid hormone action in mitochondria. J Mol Endocrinol 2001; 26: 67-77.
47. Rao JN, Liang JY, Chakraborti P, Feng P. Effect of thyroid hormone on the development and gene expression of hormone receptors in rat testes in vivo. J Endocrinol Invest 2003; 26: 435-443.
48. Tsutsui T, Hesabi B, Moons DS, Pandolfi PP, Hansel KS, Koff A, Kiyokawa H. Targeted disruption of CDK4 delays cell cycle entry with enhanced p27(Kip1) activity. Mol Cell Biol 1999; 19: 7011-7019.
49. Holsberger DR, Jirawatnotai S, Kiyokawa H, Cooke PS. Thyroid hormone regulates the cell cycle inhibitor p27Kip1 in postnatal murine Sertoli cells. Endocrinology 2003; 144: 3732-3738.
50. Choksi NY, Jahnke GD, St Hilaire C, Shelby M. Role of thyroid hormones in human and laboratory animal reproductive health. Birth Defects Res B Dev Reprod Toxicol 2003; 68: 479-491.
51. Koibuchi N, Iwasaki T. Regulation of brain development by thyroid hormone and its modulation by environmental chemicals. Endocr J 2006; 53: 295-303.
52. Zoeller RT, Bansal R, Parris C. Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology 2005; 146: 607-612.
53. Zoeller RT. Environmental chemicals as thyroid hormone analogues: new studies indicate that thyroid hormone receptors are targets of industrial chemicals? Mol Cell Endocrinol 2005; 242: 10-15.