SirT1 is required in the male germ cell for differentiation and fecundity in mice

Development (Cambridge)

Volumn 141, Issue 18, 2014, Pages 3495-3504

  Bell, Eric L ^a   Nagamori, Ippei ^b,c   Williams, Eric O ^a   Del Rosario, Amanda M ^a   Bryson, Bryan D ^a,d   Watson, Nicki ^e   White, Forest M ^a,d   Sassone Corsi, Paolo ^b   Guarente, Leonard ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d Massachusetts Institute of Technology Cambridge   (United States)

^e WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Male germ cell; Reproduction; SirT1

Indexed keywords

MALE GERM CELL; REPRODUCTION; SIRT1;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATOGRAPHY, LIQUID; FEMALE; FERTILITY; FLUORESCENT ANTIBODY TECHNIQUE; GERM CELLS; HISTONES; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIRTUIN 1; SPERMATOGENESIS; TANDEM MASS SPECTROMETRY; TESTIS;

EID: 84906871840     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.110627     Document Type: Article

References (35)

1. Baarends, W. M., Hoogerbrugge, J. W., Roest, H. P., Ooms, M., Vreeburg, J., Hoeijmakers, J. H. J. and Grootegoed, J. A. (1999). Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev. Biol. 207, 322-333.
2. Balhorn, R. (1982). A model for the structure of chromatin in mammalian sperm. J. Cell Biol. 93, 298-305.
3. Bhardwaj, A., Rao, M. K., Kaur, R., Buttigieg, M. R. and Wilkinson, M. F. (2008). GATA factors and androgen receptor collaborate to transcriptionally activate the Rhox5 homeobox gene in Sertoli cells. Mol. Cell. Biol. 28, 2138-2153.
4. Brykczynska, U., Hisano, M., Erkek, S., Ramos, L., Oakeley, E. J., Roloff, T. C., Beisel, C., Schübeler, D., Stadler, M. B. and Peters, A. H. F. M. (2010). Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687.
5. Caron, C., Pivot-Pajot, C., van Grunsven, L. A., Col, E., Lestrat, C., Rousseaux, S. and Khochbin, S. (2003). Cdyl: a new transcriptional co-repressor. EMBO Rep. 4, 877-882.
6. Chen, Y., Zhao, W., Yang, J. S., Cheng, Z., Luo, H., Lu, Z., Tan, M., Gu, W. and Zhao, Y. (2012). Quantitative acetylome analysis reveals the roles of SIRT1 in regulating diverse substrates and cellular pathways. Mol. Cell. Proteomics 11, 1048-1062.
7. Cheng, H.-L., Mostoslavsky, R., Saito, S. i., Manis, J. P., Gu, Y., Patel, P., Bronson, R., Appella, E., Alt, F. W. and Chua, K. F. (2003). Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc. Natl. Acad. Sci. USA 100, 10794-10799.
8. Cho, C., Willis, W. D., Goulding, E. H., Jung-Ha, H., Choi, Y.-C., Hecht, N. B. and Eddy, E. M. (2001). Haploinsufficiency of protamine-1 or-2 causes infertility in mice. Nat. Genet. 28, 82-86.
9. Coussens, M., Maresh, J. G., Yanagimachi, R., Maeda, G. and Allsopp, R. (2008). Sirt1 deficiency attenuates spermatogenesis and germ cell function. PLoS ONE 3, e1571.
10. Dobbin, M. M., Madabhushi, R., Pan, L., Chen, Y., Kim, D., Gao, J., Ahanonu, B., Pao, P.-C., Qiu, Y. and Zhao, Y. et al. (2013). SIRT1 collaborates with ATM and HDAC1 to maintain genomic stability in neurons. Nat. Neurosci. 16, 1008-1015.
11. Ford, W. C. L., North, K., Taylor, H., Farrow, A., Hull, M. G. R. and Golding, J. and
12. Gaucher, J., Boussouar, F., Montellier, E., Curtet, S., Buchou, T., Bertrand, S., Hery, P., Jounier, S., Depaux, A. and Vitte, A.-L. et al. (2012). Bromodomaindependent stage-specific male genome programming by Brdt. EMBO J. 31, 3809-3820.
13. Giwercman, A., Lindstedt, L., Larsson, M., Bungum, M., Spano, M., Levine, R. J. and Rylander, L. (2010). Sperm chromatin structure assay as an independent predictor of fertility in vivo: a case-control study. Int. J. Androl. 33, e221-e227.
14. Godmann, M., Auger, V., Ferraroni-Aguiar, V., Sauro, A. D., Sette, C., Behr, R. and Kimmins, S. (2007). Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis. Biol. Reprod. 77, 754-764.
15. Guarente, L. (1999). Diverse and dynamic functions of the Sir silencing complex. Nat. Genet. 23, 281-285.
16. Haigis, M. C. and Sinclair, D. A. (2010). Mammalian sirtuins: biological insights and disease relevance. In Annual Review of Pathology-Mechanisms of Disease, Vol. 5, pp. 253-295.
17. Palo Alto: Annual Reviews. Hazzouri, M., Pivot-Pajot, C., Faure, A.-K., Usson, Y., Pelletier, R., Sèle, B., Khochbin, S. and Rousseaux, S. (2000). Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone-deacetylases. Eur. J. Cell Biol. 79, 950-960.
18. Inoue, S., Tomasini, R., Rufini, A., Elia, A. J., Agostini, M., Amelio, I., Cescon, D., Dinsdale, D., Zhou, L. and Harris, I. S. et al. (2014). TAp73 is required for spermatogenesis and the maintenance of male fertility. Proc. Natl. Acad. Sci. USA 111, 1843-1848.
19. Kimmins, S. and Sassone-Corsi, P. (2005). Chromatin remodelling and epigenetic features of germ cells. Nature 434, 583-589.
20. Kolthur-Seetharam, U., Teerds, K., Rooij, D. G. d., Wendling, O., McBurney, M., Sassone-Corsi, P. and Davidson, I. (2009). The histone deacetylase SIRT1 controls male fertility in mice through regulation of hypothalamic-pituitary gonadotropin signaling. Biol. Reprod. 80, 384-391.
21. Kotaja, N., Kimmins, S., Brancorsini, S., Hentsch, D., Vonesch, J.-L., Davidson, I., Parvinen, M. and Sassone-Corsi, P. (2004). Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat. Methods 1, 249-254.
22. Kyrönlahti, A., Euler, R., Bielinska, M., Schoeller, E. L., Moley, K. H., Toppari, J., Heikinheimo, M. andWilson, D. B. (2011). GATA4 regulates Sertoli cell function and fertility in adult male mice. Mol. Cell. Endocrinol. 333, 85-95.
23. Mali, P., Kaipia, A., Kangasniemi, M., Toppari, J., Sandberg, M., Hecht, N. B. and Parvinen, M. (1989). Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod. Fertil. Dev. 1, 369-382.
24. McBurney, M.W., Yang, X., Jardine, K., Hixon, M., Boekelheide, K., Webb, J. R., Lansdorp, P. M. and Lemieux, M. (2003). The mammalian SIR2α protein has a role in embryogenesis and gametogenesis. Mol. Cell. Biol. 23, 38-54.
25. Meng, J., Holdcraft, R.W., Shima, J. E., Griswold, M. D. and Braun, R. E. (2005). Androgens regulate the permeability of the blood-testis barrier. Proc. Natl. Acad. Sci. USA 102, 16696-16700.
26. Montellier, E., Boussouar, F., Rousseaux, S., Zhang, K., Buchou, T., Fenaille, F., Shiota, H., Debernardi, A., Hery, P. and Curtet, S. et al. (2013). Chromatinto-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev. 27, 1680-1692.
27. Morinière, J., Rousseaux, S., Steuerwald, U., Sóler-Lopez, M., Curtet, S., Vitte, A.-L., Govin, J., Gaucher, J., Sadoul, K. and Hart, D. J. et al. (2009). Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461, 664-668.
28. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
29. Nakane, H., Hirota, S., Brooks, P. J., Nakabeppu, Y., Nakatsu, Y., Nishimune, Y., Iino, A. and Tanaka, K. (2008). Impaired spermatogenesis and elevated spontaneous tumorigenesis in xeroderma pigmentosum group A gene (Xpa)-deficient mice. DNA Repair 7, 1938-1950.
30. Pasqualotto, F. F., Sobreiro, B. P., Hallak, J., Pasqualotto, E. B. and Lucon, A.M. (2005). Sperm concentration and normal sperm morphology decrease and folliclestimulating hormone level increases with age. BJU Int. 96, 1087-1091.
31. Pradeepa, M. M., Nikhil, G., Hari Kishore, A., Bharath, G. N., Kundu, T. K. and Rao, M. R. S. (2009). Acetylation of Transition Protein 2 (TP2) by KAT3B (p300) Alters Its DNA Condensation Property and Interaction with Putative Histone Chaperone NPM3. J. Biol. Chem. 284, 29956-29967.
32. Rolf, C., Behre, H. M. and Nieschlag, E. (1996). Reproductive parameters of older compared to younger men of infertile couples. Int. J. Androl. 19, 135-142.
33. Russell, L. D., Ettlin, R. A., Sinha Hikim, A. P. and Clegg, E. D. (1990). Histological and Histopathological Evaluation of The Testis, pp. 62-193. Clearwater, FL: Cache River Press.
34. Sadate-Ngatchou, P. I., Payne, C. J., Dearth, A. T. and Braun, R. E. (2008). Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 46, 738-742.
35. Verdin, E., Hirschey, M. D., Finley, L. W. S. and Haigis, M. C. (2010). Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends Biochem. Sci. 35, 669-675.