Follistatin-like 3 (FSTL3) mediated silencing of transforming growth factor β (tgfβ) signaling is essential for testicular aging and regulating testis size

Endocrinology

Volumn 154, Issue 3, 2013, Pages 1310-1320

  Oldknow, Karla J ^a   Seebacher, Jan ^b   Goswami, Tapasree ^b   Villen, Judit ^b   Pitsillides, Andrew A ^a   O'Shaughnessy, Peter J ^c   Gygi, Steven P ^b   Schneyer, Alan L ^d   Mukherjee, Abir ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FSTL3 PROTEIN; GLYCOPROTEIN; PROTEIN KINASE B; SIRTUIN 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; GENE DELETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS FUNCTION; TESTIS SIZE;

AGING; ANIMALS; CELL COUNT; FOLLISTATIN-RELATED PROTEINS; LIGANDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SIZE; PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SERTOLI CELLS; SIGNAL TRANSDUCTION; SIRTUIN 1; SPERMATOGENESIS; TESTIS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84874583799     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1886     Document Type: Article

References (46)

1. Steeno OP. Clinical and physical evaluation of the infertile male: Testicular measurement or orchidometry. Andrologia. 1989;21: 103-112.
2. Turek FW, Campbell CS. Photoperiodic regulation of neuroendocrine-gonadal activity. Biol Reprod. 1979;20:32-50.
3. Salisbury GW, Hart RG. Gamete aging and its consequences. Biol Reprod Suppl. 1970;2:1-13.
4. Hardwick RJ, Tretyakov MV, Dubrova YE. Age-related accumulation of mutations supports a replication-dependent mechanism of spontaneous mutation at tandem repeatDNAloci in mice. Mol Biol Evol. 2009;26:2647-2654.
5. Wilhelm D, Palmer S, Koopman P. Sex determination and gonadal development in mammals. Physiol Rev. 2007;87:1-28.
6. Itman C, Mendis S, Barakat B, Loveland KL. All in the family: TGF-beta family action in testis development. Reproduction. 2006; 132:233-246.
7. Sidis Y, Mukherjee A, Keutmann H, Delbaere A, Sadatsuki M, Schneyer A. Biological activity of follistatin isoforms and follistatinlike-3 is dependent on differential cell surface binding and specificity for activin, myostatin, and bone morphogenetic proteins. Endocrinology. 2006;147:3586-3597.
8. Tsuchida K, Arai KY, Kuramoto Y, Yamakawa N, Hasegawa Y, Sugino H. Identification and characterization of a novel follistatinlike protein as a binding protein for the TGF-beta family. J Biol Chem. 2000;275:40788-40796.
9. Mukherjee A, Sidis Y, Mahan A, et al. FSTL3 deletion reveals roles for TGF-beta family ligands in glucose and fat homeostasis in adults. Proc Natl Acad Sci U S A. 2007;104:1348-1353.
10. Baker PJ, O'Shaughnessy PJ. Role of gonadotrophins in regulating numbers of Leydig and Sertoli cells during fetal and postnatal development in mice. Reproduction. 2001;122:227-234.
11. Wreford NG. Theory and practice of stereological techniques applied to the estimation of cell number and nuclear volume in the testis. Microsc Res Tech. 1995;32:423-436.
12. Gill R, Hitchins L, Fletcher F, Dhoot GK. Sulf1A and HGF regulate satellite-cell growth. J Cell Sci. 2010;123:1873-1883.
13. Bastow ER, Lamb KJ, Lewthwaite JC, et al. Selective activation of the MEK-ERK pathway is regulated by mechanical stimuli in forming joints and promotes pericellular matrix formation. J Biol Chem. 2005;280:11749-11758.
14. Coultas L, Bouillet P, Loveland KL, et al. Concomitant loss of proapoptotic BH3-only Bcl-2 antagonists Bik and Bim arrests spermatogenesis. EMBO J. 2005;24:3963-3973.
15. Tolonen AC, Haas W, Chilaka AC, Aach J, Gygi SP, Church GM. Proteome-wide systems analysis of a cellulosic biofuel-producing microbe. Mol Syst Biol. 2011;7:461.
16. Parvinen M. Regulation of the seminiferous epithelium. Endocr Rev. 1982;3:404-417.
17. Dierich A, Sairam MR, Monaco L, et al. 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 USA. 1998;95:13612-13617.
18. Archambeault DR, Yao HH. Activin A, a product of fetal Leydig cells, is a unique paracrine regulator of Sertoli cell proliferation and fetal testis cord expansion. Proc Natl Acad Sci USA. 2010;107: 10526-10531.
19. Nef S, Verma-Kurvari S, Merenmies J, et al. Testis determination requires insulin receptor family function in mice. Nature. 2003;426: 291-295.
20. Johnston H, Baker PJ, Abel M, et al. Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse. Endocrinology. 2004;145: 318-329.
21. Kumar TR, Palapattu G, Wang P, et al. Transgenic models to study gonadotropin function: The role of follicle-stimulating hormone in gonadal growth and tumorigenesis. Mol Endocrinol. 1999;13:851-865.
22. Tanimoto Y, Tanimoto K, Sugiyama F, et al. Male sterility in transgenic mice expressing activin betaA subunit gene in testis. Biochem Biophys Res Commun. 1999;259:699-705.
23. MatzukMM,DeMayo FJ, Hadsell LA, Kumar TR. Overexpression of human chorionic gonadotropin causes multiple reproductive defects in transgenic mice. Biol Reprod. 2003;69:338-346.
24. Lee NP, Mruk DD, Conway AM, Cheng CY. Zyxin, axin, and Wiskott-Aldrich syndrome protein are adaptors that link the cadherin/ catenin protein complex to the cytoskeleton at adherens junctions in the seminiferous epithelium of the rat testis. J Androl. 2004;25:200-215.
25. Fujita Y, Yamaguchi A, Hata K, Endo M, Yamaguchi N, Yamashita T. Zyxin is a novel interacting partner for SIRT1. BMC Cell Biol. 2009;10:6.
26. Cohen HY, Miller C, Bitterman KJ, et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science. 2004;305:390-392.
27. Coussens M, Maresh JG, Yanagimachi R, Maeda G, Allsopp R. SIRT1 deficiency attenuates spermatogenesis and germ cell function. PLoS One. 2008;3:e1571.
28. Kato T, Muraski J, Chen Y, et al. Atrial natriuretic peptide promotes cardiomyocyte survival by cGMP-dependent nuclear accumulation of zyxin and Akt. J Clin Invest. 2005;115:2716-2730.
29. Chan CB, Liu X, Tang X, Fu H, Ye K. Akt phosphorylation of zyxin mediates its interaction with acinus-S and prevents acinus-triggered chromatin condensation. Cell Death Differ. 2007;14:1688-1699.
30. Xia Y, Sidis Y, Schneyer A. Overexpression of follistatin-like 3 in gonads causes defects in gonadal development and function in transgenic mice. Mol Endocrinol. 2004;18:979-994.
31. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction. 2003;125:769-784.
32. Brehm R, Zeiler M, Rüttinger C, et al. A sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am J Pathol. 2007;171:19-31.
33. St-Pierre N, Dufresne J, Rooney AA, Cyr DG. Neonatal hypothyroidism alters the localization of gap junctional protein connexin 43 in the testis and messenger RNA levels in the epididymis of the rat. Biol Reprod. 2003;68:1232-1240.
34. Cooke PS, Porcelli J, Hess RA. Induction of increased testis growth and sperm production in adult rats by neonatal administration of the goitrogen propylthiouracil (PTU): The critical period. Biol Reprod. 1992;46:146-154.
35. Cooke PS, Hess RA, Porcelli J, Meisami E. Increased sperm production in adult rats after transient neonatal hypothyroidism. Endocrinology. 1991;129:244-248.
36. 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.
37. Besset V, Le Magueresse-Battistoni B, Collette J, Benahmed M. Tumor necrosis factor alpha stimulates insulin-like growth factor binding protein 3 expression in cultured porcine Sertoli cells. Endocrinology. 1996;137:296-303.
38. Bartholin L, Destaing O, Forissier S, et al. FLRG, a new ADAM12-associated protein, modulates osteoclast differentiation. Biol Cell. 2005;97:577-588.
39. Kato M, Putta S, Wang M, et al. TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol. 2009;11:881-889.
40. DoTV,KubbaLA, AntenosM,RademakerAW,SturgisCD,Woodruff TK. The role of activin A and Akt/GSK signaling in ovarian tumor biology. Endocrinology. 2008;149:3809-3816.
41. Bakker CE, Verheij CE, Willemsen R, et al. Fmr1 knockout mice: A model to study fragile X mental retardation. Cell. 1994;78:23-33.
42. Yang B, Song Y, Zhao D, Verkman AS. Phenotype analysis of aquaporin-8 null mice. Am J Physiol Cell Physiol. 2005;288:C1161-1170.
43. Slegtenhorst-Eegdeman KE, de Rooij DG, Verhoef-Post M, et al. Macroorchidism in FMR1 knockout mice is caused by increased Sertoli cell proliferation during testicular development. Endocrinology. 1998;139:156-162.
44. Kooy RF, D'Hooge R, Reyniers E, et al. Transgenic mouse model for the fragile X syndrome. Am J Med Genet. 1996;64:241-245.
45. Shang L, Zhou H, Xia Y, et al. Serum withdrawal up-regulates human SIRT1 gene expression in a p53-dependent manner. J Cell Mol Med. 2009;13:4176-4184.
46. Noriega LG, Feige JN, Canto C, et al.CREBandChREBPoppositely regulate SIRT1 expression in response to energy availability.EMBO Rep. 2011;12:1069-1076.