Action mechanism of inhibin α-subunit on the development of sertoli cells and first wave of spermatogenesis in mice

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Cai, Kailai ^a   Hua, Guohua ^a   Ahmad, Sibtain ^a,b   Liang, Aaixin ^a   Han, Li ^a   Wu, Canjie ^a   Yang, Feifei ^a   Yang, Liguo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF AGRICULTURE   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN E; INHIBIN; INHIBIN ALPHA SUBUNIT; MESSENGER RNA; UNCLASSIFIED DRUG; INHBB PROTEIN, MOUSE; INHIBIN-ALPHA SUBUNIT; RECOMBINANT DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL MATURATION; CONTROLLED STUDY; CYP11A1 GENE; DHH GENE; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; IGF1 GENE; INHA GENE; INHBA GENE; INHBB GENE; KITL GENE; LEYDIG CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PDGFA GENE; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SERTOLI CELL; SPERMATOGENESIS; TGFBRS GENE; TJP1 GENE; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL CYCLE; CYTOLOGY; GENETICS; METABOLISM; PLASMID; REPRODUCIBILITY; RNA INTERFERENCE; SPERMATOZOON;

ANIMALIA; MUS;

ANIMALS; CELL CYCLE; DNA, RECOMBINANT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INHIBIN-BETA SUBUNITS; INHIBINS; MALE; MICE; PLASMIDS; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; RNA, MESSENGER; SERTOLI CELLS; SPERMATOGENESIS; SPERMATOZOA;

EID: 80053592373     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025585     Document Type: Article

References (57)

1. Mackay S, (2000) Gonadal development in mammals at the cellular and molecular levels. In: Jeon KW, editors. International Review of Cytology Volume 200 Academic Press Inc.; Academic Press Ltd pp. 47-99.
2. McLaren A, (2000) Germ and somatic cell lineages in the developing gonad. Molecular and Cellular Endocrinology 163: 3-9.
3. 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.
4. Anawalt BD, Bebb RA, Matsumoto AM, Groome NP, Illingworth PJ, et al. (1996) Serum inhibin B levels reflect Sertoli cell function in normal men and men with testicular dysfunction. J Clin Endocrinol Metab 81: 3341-3345.
5. Majdic G, McNeilly AS, Sharpe RM, Evans LR, Groome NP, et al. (1997) Testicular expression of inhibin and activin subunits and follistatin in the rat and human fetus and neonate and during postnatal development in the rat. Endocrinology 138: 2136-2147.
6. Roberts V, Meunier H, Sawchenko PE, Vale W, (1989) Differential production and regulation of inhibin subunits in rat testicular cell types. Endocrinology 125: 2350-2359.
7. de Kretser DM, Buzzard JJ, Okuma Y, O'Connor AE, Hayashi T, et al. (2004) The role of activin, follistatin and inhibin in testicular physiology. Molecular and Cellular Endocrinology 225: 57-64.
8. Findlay JK, Drummond AE, Britt KL, Dyson M, Wreford NG, et al. (2000) The roles of activins, inhibins and estrogen in early committed follicles. Molecular and Cellular Endocrinology 163: 81-87.
9. Knight PG, (1996) Roles of inhibins, activins, and follistatin in the female reproductive system. Front Neuroendocrinol 17: 476-509.
10. Mann GE, Campbell BK, McNeilly AS, Baird DT, (1992) The role of inhibin and oestradiol in the control of FSH secretion in the sheep. J Endocrinol 133: 381-391.
11. Greep RO, Fevold HL, (1937) The spermatogenic and secretory function of the gonads of hypophysectomized adult rats treated with pituitary FSH and LH. Endocrinology 21: 611-618.
12. Kerr JB, Maddocks S, Sharpe RM, (1992) Testosterone and FSH have independent, synergistic and stage-dependent effects upon spermatogenesis in the rat testis. Cell Tissue Res 268: 179-189.
13. Mason AJ, Hayflick JS, Ling N, Esch F, Ueno N, et al. (1985) Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor-beta. Nature 318: 659-663.
14. Luisi S, Florio P, Reis FM, Petraglia F, (2005) Inhibins in female and male reproductive physiology: role in gametogenesis, conception, implantation and early pregnancy. Human Reproduction Update 11: 123-135.
15. Medras M, Trzmiel-Bira A, Jozkow P, Terpilowski L, Zagocka E, et al. (2010) Inhibin B and FSH as markers of Sertoli cell function in impaired spermatogenesis. Endokrynol Pol 61: 695-698.
16. Mehta MN, Mahale SD, Iyer KS, Vanage GR, Raghavan VR, et al. (2003) Effect of active immunization with the C-terminal 67-94 (R-28) region of human seminal plasma inhibin on the fecundity of adult male rabbits. American Journal of Reproductive Immunology 49: 42-50.
17. Bame JH, Dalton JC, Degelos SD, Good TE, Ireland JL, et al. (1999) Effect of long-term immunization against inhibin on sperm output in bulls. Biol Reprod 60: 1360-1366.
18. Schanbacher BD, (1991) Pituitary and testicular responses of beef bulls to active immunization against inhibin alpha. J Anim Sci 69: 252-257.
19. Martin TL, Williams GL, Lunstra DD, Ireland JJ, (1991) Immunoneutralization of inhibin modifies hormone secretion and sperm production in bulls. Biol Reprod 45: 73-77.
20. Voge JL, Wheaton JE, (2007) Effects of immunization against two inhibin antigens on daily sperm production and hormone concentrations in ram lambs. Journal of Animal Science 85: 3249-3255.
21. Hammond SM, Caudy AA, Hannon GJ, (2001) Post-transcriptional gene silencing by double-stranded RNA. Nature Reviews Genetics 2: 110-119.
22. Shen WG, (2004) RNA interference and its current application in mammals. Chinese Medical Journal 117: 1084-1091.
23. Sliva K, Schnierle BS, (2010) Selective gene silencing by viral delivery of short hairpin RNA. Virology Journal 7: 11.
24. Spiliotis M, Mizukami C, Oku Y, Kiss F, Brehm K, et al. (2010) Echinococcus multilocularis primary cells: Improved isolation, small-scale cultivation and RNA interference. Molecular and Biochemical Parasitology 174: 83-87.
25. Zhou WB, Li JD, Wang XC, Hu RM, (2010) Stable knockdown of TPPP3 by RNA interference in Lewis lung carcinoma cell inhibits tumor growth and metastasis. Molecular and Cellular Biochemistry 343: 231-238.
26. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, et al. (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17: 969-973.
27. Yomgogida K, (2008) Mammalian testis: A target of in vivo electroporation. Development Growth & Differentiation 50: 513-515.
28. Falender AE, Freiman RN, Geles KG, Lo KC, Hwang K, et al. (2005) Maintenance of spermatogenesis requires TAF4b, a gonad-specific subunit of TFIID. Genes Dev 19: 794-803.
29. Beamer WG, Cunliffe-Beamer TL, Shultz KL, Langley SH, Roderick TH, (1988) Juvenile spermatogonial depletion (jsd): a genetic defect of germ cell proliferation of male mice. Biol Reprod 38: 899-908.
30. Chen C, Ouyang W, Grigura V, Zhou Q, Carnes K, et al. (2005) ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 436: 1030-1034.
31. Barakat B, O'Connor AE, Gold E, de Kretser DM, Loveland KL, (2008) Inhibin, activin, follistatin and FSH serum levels and testicular production are highly modulated during the first spermatogenic wave in mice. Reproduction 136: 345-359.
32. Loveland KL, Dias V, Meachem S, Meyts ERD, (2007) The transforming growth factor-beta superfamily in early spermatogenesis: potential relevance to testicular dysgenesis. International Journal of Andrology 30: 377-384.
33. Mazerbourg S, Sangkuhl K, Luo CW, Sudo S, Klein C, et al. (2005) Identification of receptors and signaling pathways for orphan bone morphogenetic protein/growth differentiation factor ligands based on genomic analyses. Journal of Biological Chemistry 280: 32122-32132.
34. Looyenga BD, Wiater E, Vale W, Hammer GD, (2010) Inhibin-A Antagonizes TGF beta 2 Signaling by Down-Regulating Cell Surface Expression of the TGF beta Coreceptor Betaglycan. Molecular Endocrinology 24: 608-620.
35. Kananen K, Markkula M, Mikola M, Rainio EM, McNeilly A, et al. (1996) Gonadectomy permits adrenocortical tumorigenesis in mice transgenic for the mouse inhibin alpha-subunit promoter/simian virus 40 T-antigen fusion gene: evidence for negative autoregulation of the inhibin alpha-subunit gene. Mol Endocrinol 10: 1667-1677.
36. Joyce KL, Porcelli J, Cooke PS, (1993) Neonatal goitrogen treatment increases adult testis size and sperm production in the mouse. J Androl 14: 448-455.
37. Orth JM, Gunsalus GL, Lamperti AA, (1988) Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 122: 787-794.
38. Hess RA, Cooke PS, Bunick D, Kirby JD, (1993) Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased sertoli and germ cell numbers. Endocrinology 132: 2607-2613.
39. Vanamala J, Reddivari L, Radhakrishnan S, Tarver C, (2010) Resveratrol suppresses IGF-1 induced human colon cancer cell proliferation and elevates apoptosis via suppression of IGF-1R/Wnt and activation of p53 signaling pathways. BMC Cancer 10: 238.
40. Alao JP, Gamble SC, Stavropoulou AV, Pomeranz KM, Lam EWF, et al. (2006) The cyclin D1 proto-oncogene is sequestered in the cytoplasm of mammalian cancer cell lines. Molecular Cancer 5: 11.
41. Ohtsubo M, Theodoras AM, Schumacher J, Roberts JM, Pagano M, (1995) Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol Cell Biol 15: 2612-2624.
42. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ, (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816.
43. Bitgood MJ, Shen L, McMahon AP, (1996) Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 6: 298-304.
44. Byers S, Graham R, Dai HN, Hoxter B, (1991) Development of Sertoli cell junctional specializations and the distribution of the tight-junction-associated protein ZO-1 in the mouse testis. Am J Anat 191: 35-47.
45. Gnessi L, Basciani S, Mariani S, Arizzi M, Spera G, et al. (2000) Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. Journal of Cell Biology 149: 1019-1025.
46. Manova K, Huang EJ, Angeles M, De Leon V, Sanchez S, et al. (1993) The expression pattern of the c-kit ligand in gonads of mice supports a role for the c-kit receptor in oocyte growth and in proliferation of spermatogonia. Dev Biol 157: 85-99.
47. Morita K, Sasaki H, Fujimoto K, Furuse M, Tsukita S, (1999) Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 145: 579-588.
48. Munsterberg A, Lovell-Badge R, (1991) Expression of the mouse anti-mullerian hormone gene suggests a role in both male and female sexual differentiation. Development 113: 613-624.
49. Yao HHC, Whoriskey W, Capel B, (2002) Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes & Development 16: 1433-1440.
50. Kawai Y, Noguchi J, Akiyama K, Takeno Y, Fujiwara Y, et al. (2011) A missense mutation of the Dhh gene is associated with male pseudohermaphroditic rats showing impaired Leydig cell development. Reproduction 141: 217-225.
51. Brennan J, Tilmann C, Capel B, (2003) Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes & Development 17: 800-810.
52. Cheng CY, Mruk DD, (2002) Cell junction dynamics in the testis: sertoli-germ cell interactions and male contraceptive development. Physiological Reviews 82: 825-874.
53. Russell LD, Peterson RN, (1985) Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 94: 177-211.
54. Yan W, Suominen J, Toppari J, (2000) Stem cell factor protects germ cells from apoptosis in vitro. Journal of Cell Science 113: 161-168.
55. Elbashir SM, Lendeckel W, Tuschl T, (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes and Development 15: 188-200.
56. Ding Y, Chan CY, Lawrence CE, (2004) Sfold web server for statistical folding and rational design of nucleic acids. Nucleic Acids Research 32: W135-W141.
57. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DELTADELTACT method. Methods (Orlando) 25: 402-408.