Wt1 is involved in leydig cell steroid hormone biosynthesis by regulating paracrine factor expression in mice

Biology of Reproduction

Volumn 90, Issue 4, 2014, Pages

  Chen, Min ^a   Wang, Xiaona ^a,b   Wang, Yanbo ^a,b   Zhang, Lianjun ^a,b   Xu, Binyang ^a,b   Lv, Limin ^a   Cui, Xiuhong ^a   Li, Wei ^a   Gao, Fei ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Gene regulation; Leydig cells; Spermatogenesis; Testis; Testosterone

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; CYTOCHROME P450; CYTOCHROME P450 17; LUTEINIZING HORMONE; SONIC HEDGEHOG PROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TAMOXIFEN; TESTOSTERONE; WT1 PROTEIN; LUTEINIZING HORMONE RECEPTOR; STEROID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXPLANT; GENE CONTROL; GENE DELETION; GENE EXPRESSION; HORMONE BLOOD LEVEL; IN VITRO STUDY; LEYDIG CELL; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE; SERTOLI CELL; STEROIDOGENESIS; TESTIS; 129 MOUSE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; FEMALE; GENETICS; MALE; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SPERMATOGENESIS; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; FEMALE; HEDGEHOG PROTEINS; LEYDIG CELLS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; PARACRINE COMMUNICATION; RECEPTORS, LH; SEMINIFEROUS TUBULES; SERTOLI CELLS; SPERMATOGENESIS; STEROIDS; TESTIS; TESTOSTERONE; WT1 PROTEINS;

EID: 84903778677     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.114702     Document Type: Article

References (34)

1. Stanley E, Lin CY, Jin S, Liu J, Sottas CM, Ge R, Zirkin BR, Chen H. Identification, proliferation, and differentiation of adult Leydig stem cells. Endocrinology 2012; 153:5002-5010.
2. Lei ZM, Mishra S, Zou W, Xu B, Foltz M, Li X, Rao CV. Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol Endocrinol 2001; 15:184-200.
3. Themmen AP. An update of the pathophysiology of human gonadotrophin subunit and receptor gene mutations and polymorphisms. Reproduction 2005; 130:263-274.
4. Zhang FP, Poutanen M, Wilbertz J, Huhtaniemi I. Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol Endocrinol 2001; 15:172-183.
5. Wu N, Murono EPA. Sertoli cell-secreted paracrine factor(s) stimulates proliferation and inhibits steroidogenesis of rat Leydig cells. Mol Cell Endocrinol 1994; 106:99-109.
6. Perrard-Sapori MH, Chatelain PC, Rogemond N, Saez JM. Modulation of Leydig cell functions by culture with Sertoli cells or with Sertoli cellconditioned medium: effect of insulin, somatomedin-C and FSH. Mol Cell Endocrinol 1987; 50:193-201.
7. Onoda M, Djakiew D, Papadopoulos V. Pachytene spermatocytes regulate the secretion of Sertoli cell protein(s) which stimulate Leydig cell steroidogenesis. Mol Cell Endocrinol 1991; 77:207-216.
8. Mishra J, Gautam M, Dadhich R, Kowtharapu BS, Majumdar SS. Peritubular cells may modulate Leydig cell-mediated testosterone production through a nonclassic pathway. Fertil Steril 2012; 98: 1308-1317.e1.
9. Gao F, Maiti S, Alam N, Zhang Z, Deng JM, Behringer RR, Lecureuil C, Guillou F, Huff V. The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc Natl Acad Sci U S A 2006; 103:11987-11992.
10. Wang XN, Li ZS, Ren Y, Jiang T, Wang YQ, Chen M, Zhang J, Hao JX, Wang YB, Sha RN, Huang Y, Liu X, et al. The Wilms tumor gene, Wt1, is critical for mouse spermatogenesis via regulation of Sertoli cell polarity and is associated with non-obstructive azoospermia in humans. PLoS Genet 2013; 9:e1003645.
11. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, Jaenisch R. WT-1 is required for early kidney development. Cell 1993; 74: 679-691.
12. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002; 244:305-318.
13. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M, Taketo MM. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 1999; 18:5931-5942.
14. Mason-Garcia M, Vigh S, Comaru-Schally AM, Redding TW, Somogyvari-Vigh A, Horvath J, Schally AV. Radioimmunoassay for 6-Dtryptophan analog of luteinizing hormone-releasing hormone: measurement of serum levels after administration of long-acting microcapsule formulations. Proc Natl Acad Sci U S A 1985; 82:1547-1551.
15. Gao F, Maiti S, Sun G, Ordonez NG, Udtha M, Deng JM, Behringer RR, Huff V. The Wt1+/R394W mouse displays glomerulosclerosis and earlyonset renal failure characteristic of human Denys-Drash syndrome. Mol Cell Biol 2004; 24:9899-9910.
16. van der Wee KS, Johnson EW, Dirami G, Dym TM, Hofmann MC. Immunomagnetic isolation and long-term culture of mouse type A spermatogonia. J Androl 2001; 22:696-704.
17. Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, Kubota Y, Ogawa T. In vitro production of functional sperm in cultured neonatal mouse testes. Nature 2011; 471:504-507.
18. Zhang FP, Pakarainen T, Zhu F, Poutanen M, Huhtaniemi I. Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 2004; 145: 1453-1463.
19. Bitgood MJ, McMahon AP. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 1995; 172:126-138.
20. Clark AM, Garland KK, Russell LD. 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 2000; 63:1825-1838.
21. Basciani S, Mariani S, Arizzi M, Ulisse S, Rucci N, Jannini EA, Della Rocca C, Manicone A, Carani C, Spera G, Gnessi L. Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor-alpha and -beta during human testicular development and disease. J Clin Endocrinol Metab 2002; 87:2310-2319.
22. Brennan J, Tilmann C, Capel B. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 2003; 17:800-810.
23. Gnessi L, Basciani S, Mariani S, Arizzi M, Spera G, Wang C, Bondjers C, Karlsson L, Betsholtz C. Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 2000; 149:1019-1026.
24. Hatano O, Takayama K, Imai T, Waterman MR, Takakusu A, Omura T, Morohashi K. Sex-dependent expression of a transcription factor, Ad4BP, regulating steroidogenic P-450 genes in the gonads during prenatal and postnatal rat development. Development 1994; 120:2787-2797.
25. Colvin JS, Green RP, Schmahl J, Capel B, Ornitz DM. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 2001; 104: 875-889.
26. Lin D, Sugawara T, Strauss JF III, Clark BJ, Stocco DM, Saenger P, Rogol A, Miller WL. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 1995; 267:1828-1831.
27. Bose HS, Sugawara T, Strauss JF III, Miller WL. The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. N Engl J Med 1996; 335:1870-1878.
28. Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997; 15:201-204.
29. Bitgood MJ, Shen L, McMahon AP. Sertoli cell signaling by desert hedgehog regulates the male germline. Curr Biol 1996; 6:298-304.
30. Yao HH, Whoriskey W, Capel B. Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 2002; 16:1433-1440.
31. Val P, Lefrancois-Martinez AM, Veyssiere G, Martinez A. SF-1 a key player in the development and differentiation of steroidogenic tissues. Nucl Recept 2003; 1:8.
32. Luo X, Ikeda Y, Parker KL. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. Cell 1994; 77:481-490.
33. Barsoum IB, Bingham NC, Parker KL, Jorgensen JS, Yao HH. Activation of the Hedgehog pathway in the mouse fetal ovary leads to ectopic appearance of fetal Leydig cells and female pseudohermaphroditism. Dev Biol 2009; 329:96-103.
34. Park SY, Tong M, Jameson JL. Distinct roles for steroidogenic factor 1 and desert hedgehog pathways in fetal and adult Leydig cell development. Endocrinology 2007; 148:3704-3710.