Hostname: page-component-848d4c4894-r5zm4 Total loading time: 0 Render date: 2024-06-19T04:35:14.334Z Has data issue: false hasContentIssue false
  • English
  • Français

Is p53 controlling spermatogenesis in male mice with the deletion on the Y chromosome?

Published online by Cambridge University Press:  12 July 2011

Tomasz Lech ,
Aniela Golas  and
Jozefa Styrna
Tomasz Lech
Affiliation:
Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Cracow, Poland.
Aniela Golas*
Affiliation:
Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Cracow, Poland.
Jozefa Styrna
Affiliation:
Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Cracow, Poland.
*
All correspondence to: Aniela Golas. Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Cracow, Poland. Tel: +48 12 663 24 34. Fax: +48 12 634 37 16. e-mail: aniela.golas@uj.edu.pl
Get access Rights & Permissions [Opens in a new window]

Summary

The aim of the study was to evaluate the influence of the chromosome Y structure and Trp53 genotype on semen quality parameters. Mice with partial deletion of the Y chromosome (B10.BR-Ydel) have severely altered sperm head morphology when compared with males that possess the complete Y chromosome (B10.BR). Control males from B10.BR and B10.BR-Ydel mice, and mutant males from B10.BR-p53−/− and B10.BR-Ydel-p53−/− experimental groups were used. We assessed testis weight, sperm head abnormalities, viability of spermatozoa (eosin test), percentage of motile and immature sperm, and performed a hypo-osmotic test to detect abnormal tail membrane integrity. Sperm morphology and maturation were controlled by the genes within the deleted region of the Y chromosome. Testis weight was higher in the mutants than in the control males, possibly due to cell accumulation in Trp53-deficient males as the concentration of sperm was significantly increased in the mutants. An elevated percentage of abnormal sperm was noted in B10.BR-p53−/− and B10.BR-Ydel-p53−/− male mice. We suggest that, in Trp53-deficient mice, the sperm cells that escape apoptosis are the ones that have abnormal morphology. The only sperm quality parameter affected by the interplay between Trp53 and chromosome Y genes was sperm motility, which was elevated in B10.BR-p53−/− males, but remained unchanged in B10.BR-Ydel-p53−/− males.

Keywords

p53Semen qualityYdel
Type
Research Article
Information
Zygote , Volume 21 , Issue 1 , February 2013 , pp. 65 - 70
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allan, D.J., Harmon, B.V. & Roberts, S.A. (1992). Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif. 25, 241–50.CrossRefGoogle ScholarPubMed
Beumer, T.L., Roepers-Gajadien, H.L., Gademan, I.S., van Buul, P.P., Gil-Gomez, G., Rutgers, D.H. & de Rooij, D.G. (1998). The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ. 5, 669–77.CrossRefGoogle ScholarPubMed
Burgoyne, PS. (1998). The role of Y-encoded genes in mammalian spermatogenesis. Semin. Cell Dev. Biol. 9, 423–32CrossRefGoogle ScholarPubMed
Embree-Ku, M. & Boekelheide, K. (2002). Absence of p53 and FasL has sexually dimorphic effects on both development and reproduction. Exp. Biol. Med. (Maywood) 227, 545–53.CrossRefGoogle ScholarPubMed
Evans, S.C., Liang, M., Amos, Ch., Gu, X. & Lozano, G. (2004). A novel genetic modifier of p53, mop1, results in embryonic lethality. Mamm. Genome 15, 415–23.CrossRefGoogle ScholarPubMed
Golas, A., Dzieza, A., Kuzniarz, K. & Styrna, J. (2008). Mapping of the genes controlling four parameters of sperm quality in the recombinant inbred strains of mice. Int. J. Dev. Biol. 52, 287–93.CrossRefGoogle ScholarPubMed
Grzmil, P., Golas, A., Müller, C. & Styrna, J. (2007). The influence of the deletion on the long arm of the Y chromosome on sperm motility in mice. Theriogenology 67, 760–6.CrossRefGoogle Scholar
Hasegawa, M., Zhang, Y., Niibe, H., Terry, N.H. & Meistrich, M.L. (1998). Resistance of differentiating spermatogonia to radiation-induced apoptosis and loss in p53-deficient mice. Radiat. Res. 149, 263–70.CrossRefGoogle ScholarPubMed
Krzanowska, H. (1976). Inheritance of sperm head abnormality types in mice – the role of the Y chromosome. Genet. Res. (Camb.) 28, 189–98.CrossRefGoogle ScholarPubMed
Lane, D.P. (1992). p53. Guardian of the genome. Nature 358, 15–16.CrossRefGoogle ScholarPubMed
Liang, M., Ayanga, B., Du, S., Godwin, A.K & Hartsock, J.K. (2008). Ovca1, a candidate gene of the genetic modifier of Tp53, Mop2, affects mouse embryonic lethality. Genes Chromosomes Cancer 47, 315–25.CrossRefGoogle ScholarPubMed
Marty, M.S., Singh, N.P., Holsapple, M.P. & Gollapudi, B.B. (1999). Influence of p53 zygosity on select sperm parameters of the mouse. Mutat. Res. 427, 39–45.CrossRefGoogle ScholarPubMed
Odorisio, T., Rodriguez, T.A., Evans, E.P., Clarke, A.R. & Burgoyne, P.S. (1998). The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat. Genet. 18, 257–61.CrossRefGoogle ScholarPubMed
Ohta, H., Aizawa, S. & Nishimune, Y. (2003). Functional analysis of the p53 gene in apoptosis induced by heat stress or loss of stem cell factor signaling in mouse male germ cells. Biol. Reprod. 68, 2249–54.CrossRefGoogle ScholarPubMed
Oren, M. (1999). Regulation of the p53 tumor suppressor protein. J. Biol. Chem. 247, 36031–4.CrossRefGoogle Scholar
Paul, C., Povey, J.E., Lawrence, N.J., Selfridge, J., Melton, D.W. & Saunders, P.T. (2007). Deletion of genes implicated in protecting the integrity of male germ cell has differential effects on the incidence of DNA breaks and germ cell loss. PloS One 2, e989.CrossRefGoogle ScholarPubMed
Rodriguez, I., Ody, Ch., Araki, K., Garcia, I. & Vassalli, P. (1997). An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J. 16, 2262–70.CrossRefGoogle ScholarPubMed
Rotter, V., Schwartz, D., Almon, E., Goldfinger, N., Kapon, A., Meshorer, A., Donehower, L.A. & Levine, A.J. (1993). Mice with reduced level of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc. Natl. Acad. Sci. USA 90, 9075–9.CrossRefGoogle ScholarPubMed
Salazar, G., Joshi, A., Liu, D., Wei, H., Persson, J.L. & Wolgemuth, D.J. (2005). Induction of apoptosis involving multiple pathways is a primary response to cyclin A1-deficiency in male meiosis. Dev. Dyn. 234, 114–23.CrossRefGoogle ScholarPubMed
Schwartz, D., Goldfinger, N., & Rotter, V. (1993). Expression of p53 protein in spermatogenesis is confined to the tetraploid pachytene primary spermatocytes. Oncogene 8, 1487–94.Google Scholar
Schwartz, D., Goldfinger, N., Kam, Z. & Rotter, V. (1999). p53 controls low DNA damage-dependent premeiotic checkpoint and facilitates DNA repair during spermatogenesis. Cell Growth Differ. 10, 665–75.Google ScholarPubMed
Styrna, J., Imai, H.T. & Moriwaki, K. (1991). An increased level of sperm abnormalities in mice with a partial deletion of the Y chromosome. Genet. Res. (Cambridge) 55, 195–9.CrossRefGoogle Scholar
Styrna, J., Bilinska, B. & Krzanowska, H. (2002). The effect of a partial Y chromosome deletion in B10.BR-Ydel mice on testis morphology, sperm quality and efficiency of fertilization. Reprod. Fertil. Dev. 14, 101–8.CrossRefGoogle ScholarPubMed
Styrna, J., Kilarski, W., Krzanowska, H. (2003). Influence of the CBA genetic background on sperm morphology and fertilization efficiency in mice with partial Y chromosome deletion. Reprod. 126, 579–88.CrossRefGoogle ScholarPubMed
Yan, W., Suominen, J., Samson, M., Jegou, B. & Toppari, J. (2000). Involvement of Bcl-2 family proteins in germ cell apoptosis during testicular development in the rat and pro-survival effect of stem cell factor on germ cells in vitro. Mol. Cell. Endocrinol. 165, 115–29.CrossRefGoogle ScholarPubMed
Yin, Y., DeWolf, W.C. & Morgentaler, A. (1998a). Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and–independent pathways in mice. Biol. Reprod. 58, 492–6.CrossRefGoogle ScholarPubMed
Yin, Y., Stahl, B.C., DeWolf, W.C. & Morgentaler, A. (1998b). p53-mediated germ cell quality control in spermatogenesis. Dev. Biol. 204, 165–71.CrossRefGoogle ScholarPubMed
Yin, Y., Stahl, B.C., DeWolf, W.C. & Morgentaler, A. (2002). p53 and Fas are sequential mechanisms of testicular germ cell apoptosis. J. Androl. 23, 64–70.CrossRefGoogle ScholarPubMed