Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

The contribution of p53 and Y chromosome long arm genes to regulation of apoptosis in mouse testis

Tomasz Lech A D , Józefa Styrna B and Katarzyna Kotarska B C
+ Author Affiliations
- Author Affiliations

A Department of Microbiology, Faculty of Commodity Science, Cracow University of Economics, Rakowicka 27, PL 31-510, Krakow, Poland.

B Department of Genetics and Evolution, Institute of Zoology, Jagiellonian University, Gronostajowa 9, PL 30-387, Krakow, Poland.

C Department of Experimental Neuroendocrinology, Institute of Pharmacology, Polish Academy of Sciences, Smetna 12, PL 31-343 Krakow, Poland.

D Corresponding author. Email: tomasz.lech@uek.krakow.pl

Reproduction, Fertility and Development 30(3) 469-476 https://doi.org/10.1071/RD17217
Submitted: 28 February 2017  Accepted: 15 July 2017   Published: 2 August 2017

Abstract

Apoptosis of excessive or defective germ cells is a natural process occurring in mammalian testes. Tumour suppressor protein p53 is involved in this process both in developing and adult male gonads. Its contribution to testicular physiology is known to be modified by genetic background. The aim of this study was to evaluate the combined influence of the p53 and Y chromosome long arm genes on male germ cell apoptosis. Knockout of the transformation related protein 53 (Trp53) gene was introduced into congenic strains: B10.BR (intact Y chromosome) and B10.BR-Ydel (Y chromosome with a deletion in the long arm). The level of apoptosis in the testes of 19-day-old and 3-month-old male mice was determined using the terminal deoxynucleotidyl transferase-mediated deoxyuridine triphosphate in situ nick-end labelling (TUNEL) method. The study revealed that although p53 is involved in germ cell apoptosis in peripubertal testes, this process can also be mediated by p53-independent mechanisms. However, activation of p53-independent apoptotic pathways in the absence of the p53 protein requires engagement of the multicopy Yq genes and was not observed in gonads of B10.BR-Ydel-p53−/− males. The role of Yq genes in the regulation of testicular apoptosis seems to be restricted to the initial wave of spermatogenesis and is not evident in adult gonads. The study confirmed, instead, that p53 does participate in spontaneous apoptosis in mature testes.

Additional keywords: male germ cells, p53 knockout, spermatogenesis, Yq deletion.


References

Almon, E., Goldfinger, N., Kapon, A., Schwartz, D., Levine, A. J., and Rotter, V. (1993). Testicular tissue-specific expression of the p53 suppressor gene. Dev. Biol. 156, 107–116.
Testicular tissue-specific expression of the p53 suppressor gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFSisbY%3D&md5=e3748dec802189ca1cbc1e06383e9399CAS |

Bayram, S., Kizilay, G., and Topcu-Tarladacalisir, Y. (2016). Evaluation of the Fas/FasL signaling pathway in diabetic rat testis. Biotech. Histochem. 91, 204–211.
Evaluation of the Fas/FasL signaling pathway in diabetic rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktlGqtb0%3D&md5=7c8bff3c776fbcb76b0b5bdc2a55d754CAS |

Beumer, T. L., Roepers-Gajadien, H. L., Gademan, I. S., van Buul, P. P., Gil-Gomez, G., Rutgers, D. H., and de Rooij, D. G. (1998). The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ. 5, 669–677.
The role of the tumor suppressor p53 in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlslWgtrg%3D&md5=8be7b66de29285e2b12314a3cf4529ffCAS |

Billig, H., Furuta, I., Rivier, C., Tapanainen, J., Parvinen, M., and Hsueh, A. J. (1995). Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136, 5–12.
Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjt1Knsbw%3D&md5=b34c7c9b89e718ad4e033d360112dda8CAS |

Bishop, C. E., and Hatat, D. (1987). Molecular cloning and sequence analysis of a mouse Y chromosome RNA transcript expressed in the testis. Nucleic Acids Res. 15, 2959–2969.
Molecular cloning and sequence analysis of a mouse Y chromosome RNA transcript expressed in the testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlsVygsb4%3D&md5=bf654695095251390f75dd0bdb1a6148CAS |

Burgoyne, P. S., Mahadevaiah, S. K., Sutcliffe, M. J., and Palmer, S. J. (1992). Fertility in mice requires X–Y pairing and a Y-chromosomal “spermiogenesis” gene mapping to the long arm. Cell 71, 391–398.
Fertility in mice requires X–Y pairing and a Y-chromosomal “spermiogenesis” gene mapping to the long arm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsleiug%3D%3D&md5=69dbf327026c2bae7c1e4a559461d218CAS |

Cocquet, J., Ellis, P. J., Yamauchi, Y., Mahadevaiah, S. K., Affara, N. A., Ward, M. A., and Burgoyne, P. S. (2009). The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Biol. 7, e1000244.
The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis.Crossref | GoogleScholarGoogle Scholar |

Comptour, A., Moretti, C., Serrentino, M. E., Auer, J., Ialy-Radio, C., Ward, M. A., Touré, A., Vaiman, D., and Cocquet, J. (2014). SSTY proteins co-localize with the post-meiotic sex chromatin and interact with regulators of its expression. FEBS J. 281, 1571–1584.
SSTY proteins co-localize with the post-meiotic sex chromatin and interact with regulators of its expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlCisrs%3D&md5=085866b0db61ebb021ddfef9d275d24bCAS |

Conway, S. J., Mahadevaiah, S. K., Darling, S. M., Capel, B., Rattigan, A. M., and Burgoyne, P. S. (1994). Y353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome. Mamm. Genome 5, 203–210.
Y353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnslSi&md5=32e690baaf7da054aedf417a6f4e95e3CAS |

Ellis, P. J., Ferguson, L., Clemente, E. J., and Affara, N. A. (2007). Bidirectional transcription of a novel chimeric gene mapping to mouse chromosome Yq. BMC Evol. Biol. 7, 171.
Bidirectional transcription of a novel chimeric gene mapping to mouse chromosome Yq.Crossref | GoogleScholarGoogle Scholar |

Elmore, S. (2007). Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35, 495–516.
Apoptosis: a review of programmed cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlWmtb4%3D&md5=67fcd67aa06c38c5af34adc66c838b96CAS |

Golas, A., Lech, T., Janula, M., Bederska, D., Lenartowicz, M., and Styrna, J. (2011). Semen quality parameters and embryo lethality in mice deficient for Trp53 protein. Reprod. Biol. 11, 250–263.
Semen quality parameters and embryo lethality in mice deficient for Trp53 protein.Crossref | GoogleScholarGoogle Scholar |

Green, M. R., and Sambrook, J. (2017). Isolation of high-molecular-weight DNA using organic solvents. Cold Spring Harb. Protoc. 2017, .
Isolation of high-molecular-weight DNA using organic solvents.Crossref | GoogleScholarGoogle Scholar |

Grzmil, P., Gołas, A., Müller, C., and Styrna, J. (2007). The influence of the deletion on the long arm of the Y chromosome on sperm motility in mice. Theriogenology 67, 760–766.
The influence of the deletion on the long arm of the Y chromosome on sperm motility in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlCksLk%3D&md5=f72163ef68dd74c5e5f7a058a9270020CAS |

Guan, Y., Liang, G., Hawken, P. A., Malecki, I. A., Cozens, G., Vercoe, P. E., Martin, G. B., and Guan, L. L. (2015). Roles of small RNAs in the effects of nutrition on apoptosis and spermatogenesis in the adult testis. Sci. Rep. 5, 10372–10386.
Roles of small RNAs in the effects of nutrition on apoptosis and spermatogenesis in the adult testis.Crossref | GoogleScholarGoogle Scholar |

Jahnukainen, K., Chrysis, D., Hou, M., Parvinen, M., Eksborg, S., and Söder, O. (2004). Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis. Biol. Reprod. 70, 290–296.
Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslyrtw%3D%3D&md5=b528f680c5dad1b152d633f02706e77cCAS |

Jaiswal, M. K., Agrawal, V., Katara, G. K., Pamarthy, S., Kulshrestha, A., Chaouat, G., Gilman-Sachs, A., and Beaman, K. D. (2015). Male fertility and apoptosis in normal spermatogenesis are regulated by vacuolar-ATPase isoform a2. J. Reprod. Immunol. 112, 38–45.
Male fertility and apoptosis in normal spermatogenesis are regulated by vacuolar-ATPase isoform a2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Gru7vO&md5=fc860c4e2b9715db654243eaf49701a6CAS |

Kotarska, K., and Lenartowicz, M. (2011). Sperm migration and selection in the reproductive tract of female mice is mostly affected by male genotype. Folia Biol. (Krakow) 59, 71–75.
Sperm migration and selection in the reproductive tract of female mice is mostly affected by male genotype.Crossref | GoogleScholarGoogle Scholar |

Kotarska, K., Galas, J., Przybyło, M., Bilińska, B., and Styrna, J. (2015). Increased progesterone production in cumulus–oocyte complexes of female mice sired by males with the Y-chromosome long arm deletion and its potential influence on fertilization efficiency. Reprod. Sci. 22, 242–249.
Increased progesterone production in cumulus–oocyte complexes of female mice sired by males with the Y-chromosome long arm deletion and its potential influence on fertilization efficiency.Crossref | GoogleScholarGoogle Scholar |

Kotula-Balak, M., Grzmil, P., Styrna, J., and Bilińska, B. (2004). Immunodetection of aromatase in mice with a partial deletion in the long arm of the Y chromosome. Acta Histochem. 106, 55–64.
Immunodetection of aromatase in mice with a partial deletion in the long arm of the Y chromosome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsVGhtb0%3D&md5=fb040300a9dc22d2184d9eec33bb1087CAS |

Lawen, A. (2003). Apoptosis – an introduction. BioEssays 25, 888–896.
Apoptosis – an introduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1Sis7s%3D&md5=f96551091240b09a872c8bb99dfffa01CAS |

Lech, T., Golas, A., and Styrna, J. (2013). Is p53 controlling spermatogenesis in male mice with the deletion on the Y chromosome? Zygote 21, 65–70.
Is p53 controlling spermatogenesis in male mice with the deletion on the Y chromosome?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVamtbg%3D&md5=5f9241c73b00d54005b87ff8d031db40CAS |

Lin, Y. C., Yao, P. L., and Richburg, J. H. (2010). FasL gene-deficient mice display a limited disruption in spermatogenesis and inhibition of mono-(2-ethylhexyl) phthalate-induced germ cell apoptosis. Toxicol. Sci. 114, 335–345.
FasL gene-deficient mice display a limited disruption in spermatogenesis and inhibition of mono-(2-ethylhexyl) phthalate-induced germ cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsleisbo%3D&md5=c7161d0ce5e9ef85040e107321bc25caCAS |

Lizama, C., Alfaro, I., Reyes, J. G., and Moreno, R. D. (2007). Up-regulation of CD95 (Apo-1/Fas) is associated with spermatocyte apoptosis during the first round of spermatogenesis in the rat. Apoptosis 12, 499–512.
Up-regulation of CD95 (Apo-1/Fas) is associated with spermatocyte apoptosis during the first round of spermatogenesis in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitFKmsrY%3D&md5=c1ad464f255492f9ebf9f323cb39c57dCAS |

Matsuda, Y., Hirobe, T., and Chapman, V. M. (1991). Genetic basis of X–Y chromosome dissociation and male sterility in interspecific hybrids. Proc. Natl. Acad. Sci. USA 88, 4850–4854.
Genetic basis of X–Y chromosome dissociation and male sterility in interspecific hybrids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ntFaqsg%3D%3D&md5=8a6720160f6725d5f82ad16e9bfe5dfeCAS |

Odorisio, T., Rodriguez, T. A., Evans, E. P., Clarke, A. R., and Burgoyne, P. S. (1998). The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat. Genet. 18, 257–261.
The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlKktbc%3D&md5=9afe497962c7ba3f909c8e3b2863597fCAS |

Ohta, H., Aizawa, S., and 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, 2249–2254.
Functional analysis of the p53 gene in apoptosis induced by heat stress or loss of stem cell factor signaling in mouse male germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1Ggtrw%3D&md5=c9e4fcc2e78c8752dfd4e718483944acCAS |

Oren, M. (2003). Decision making by p53: life, death and cancer. Cell Death Differ. 10, 431–442.
Decision making by p53: life, death and cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt1GjsLg%3D&md5=e162a9b98a09d76e1148ad561e9f398cCAS |

Paul, C., Povey, J. E., Lawrence, N. J., Selfridge, J., Melton, D. W., and Saunders, P. T. (2007). Deletion of genes implicated in protecting the integrity of male germ cells has differential effects on the incidence of DNA breaks and germ cell loss. PLoS One 2, e989.
Deletion of genes implicated in protecting the integrity of male germ cells has differential effects on the incidence of DNA breaks and germ cell loss.Crossref | GoogleScholarGoogle Scholar |

Prado, V. F., Lee, C. H., Zahed, L., Vekemans, M., and Nishioka, Y. (1992). Molecular characterization of a mouse Y chromosomal repetitive sequence that detects transcripts in the testis. Cytogenet. Cell Genet. 61, 87–90.
Molecular characterization of a mouse Y chromosomal repetitive sequence that detects transcripts in the testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvVCkurc%3D&md5=08df2f619384501c1f1c337919e90ea7CAS |

Reynard, L. N., Cocquet, J., and Burgoyne, P. S. (2009). The multi-copy mouse gene Sycp3-like Y-linked (Sly) encodes an abundant spermatid protein that interacts with a histone acetyltransferase and an acrosomal protein. Biol. Reprod. 81, 250–257.
The multi-copy mouse gene Sycp3-like Y-linked (Sly) encodes an abundant spermatid protein that interacts with a histone acetyltransferase and an acrosomal protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVaitLk%3D&md5=5fd53cdc35bb057d49e1c474af58c9a4CAS |

Richburg, J. H. (2000). The relevance of spontaneous- and chemically-induced alterations in testicular germ cell apoptosis to toxicology. Toxicol. Lett. 112–113, 79–86.
The relevance of spontaneous- and chemically-induced alterations in testicular germ cell apoptosis to toxicology.Crossref | GoogleScholarGoogle Scholar |

Riel, J. M., Yamauchi, Y., Sugawara, A., Li, H. Y., Ruthig, V., Stoytcheva, Z., Ellis, P. J., Cocquet, J., and Ward, M. A. (2013). Deficiency of the multi-copy mouse Y gene Sly causes sperm DNA damage and abnormal chromatin packaging. J. Cell Sci. 126, 803–813.
Deficiency of the multi-copy mouse Y gene Sly causes sperm DNA damage and abnormal chromatin packaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXns1Ggtr0%3D&md5=831664d8d81615b95b43402bbc093ee8CAS |

Rodriguez, I., Ody, C., Araki, K., Garcia, I., and Vassalli, P. (1997). An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J. 16, 2262–2270.
An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsV2nu7Y%3D&md5=9ee5c10f326629bc1ddd12458bed5788CAS |

Rotter, V., Schwartz, D., Almon, E., Goldfinger, N., Kapon, A., Meshorer, A., Donehower, L. A., and Levine, A. J. (1993). Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc. Natl. Acad. Sci. USA 90, 9075–9079.
Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVOhs78%3D&md5=e93ed8f9f9e78c699c37dee86fbb29f2CAS |

Russell, L. D., Chiarini-Garcia, H., Korsmeyer, S. J., and Knudson, C. M. (2002). Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol. Reprod. 66, 950–958.
Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCltb8%3D&md5=174f5e73beca076ad3808c93735449cdCAS |

Schwartz, D., Goldfinger, N., and Rotter, V. (1993). Expression of p53 protein in spermatogenesis is confined to the tetraploid pachytene primary spermatocytes. Oncogene 8, 1487–1494.
| 1:CAS:528:DyaK3sXkvFahsLk%3D&md5=8c0ed22d5d68bc9473fd92c0357542e2CAS |

Schwartz, D., Goldfinger, N., Kam, Z., and Rotter, V. (1999). p53 controls low DNA damage-dependent premeiotic checkpoint and facilitates DNA repair during spermatogenesis. Cell Growth Differ. 10, 665–675.
| 1:CAS:528:DyaK1MXntFCksLg%3D&md5=117e6b6632afa6bf38f50d9f2dff936cCAS |

Shaha, C., Tripathi, R., and Mishra, D. P. (2010). Male germ cell apoptosis: regulation and biology. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365, 1501–1515.
Male germ cell apoptosis: regulation and biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaisr3J&md5=c5e3460d70a2389708102a844c0b6399CAS |

Soh, Y. Q. S., Alföldi, J., Pyntikova, T., Brown, L. G., Graves, T., Minx, P. J., Fulton, R. S., Kremitzki, C., Koutseva, N., Mueller, J. L., Rozen, S., Hughes, J. F., Owens, E., Womack, J. E., Murphy, W. J., Cao, Q., de Jong, P., Warren, W. C., Wilson, R. K., Skaletsky, H., and Page, D. C. (2014). Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell 159, 800–813.
Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVGks7nP&md5=e7dbbf51e1bbc3cfbe02a4e1ae842f0dCAS |

Styrna, J., Imai, H. T., and Moriwaki, K. (1991a). An increased level of sperm abnormalities in mice with a partial deletion of the Y chromosome. Genet. Res. 57, 195–199.
An increased level of sperm abnormalities in mice with a partial deletion of the Y chromosome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3ns1ahuw%3D%3D&md5=bc0c580416cce099b9ca09719a960c02CAS |

Styrna, J., Klag, J., and Moriwaki, K. (1991b). Influence of partial deletion of the Y chromosome on mouse sperm phenotype. J. Reprod. Fertil. 92, 187–195.
Influence of partial deletion of the Y chromosome on mouse sperm phenotype.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M3nvVShug%3D%3D&md5=04c8179ce83cb91ec3262d66b2eff812CAS |

Styrna, J., Bilińska, B., and 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, 101–108.
The effect of a partial Y chromosome deletion in B10.BR-Ydel mice on testis morphology, sperm quality and efficiency of fertilization.Crossref | GoogleScholarGoogle Scholar |

Sutcliffe, M. J., Darling, S. M., and Burgoyne, P. S. (1991). Spermatogenesis in XY, XYSxra, and XOSxra mice: a quantitative analysis of spermatogenesis throughout puberty. Mol. Reprod. Dev. 30, 81–89.
Spermatogenesis in XY, XYSxra, and XOSxra mice: a quantitative analysis of spermatogenesis throughout puberty.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2Fmt1CitQ%3D%3D&md5=d2ceb493ca29be7d5ff1dac824cae082CAS |

Touré, A., Szot, M., Mahadevaiah, S. K., Rattigan, Á., Ojarikre, O. A., and Burgoyne, P. S. (2004). A new deletion of the mouse Y chromosome long arm associated with the loss of Ssty expression, abnormal sperm development and sterility. Genetics 166, 901–912.
A new deletion of the mouse Y chromosome long arm associated with the loss of Ssty expression, abnormal sperm development and sterility.Crossref | GoogleScholarGoogle Scholar |

Touré, A., Clemente, E. J., Ellis, P., Mahadevaiah, S. K., Ojarikre, O. A., Ball, P. A., Reynard, L., Loveland, K. L., Burgoyne, P. S., and Affara, N. A. (2005). Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol. 6, R102.
Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm.Crossref | GoogleScholarGoogle Scholar |

Wang, H., Zhao, R., Guo, C., Jiang, S., Yang, J., Xu, Y., Liu, Y., Fan, L., Xiong, W., Ma, J., Peng, S., Zeng, Z., Zhou, Y., Li, X., Li, Z., Li, X., Schmitt, D. C., Tan, M., Li, G., and Zhou, M. (2016). Knockout of BRD7 results in impaired spermatogenesis and male infertility. Sci. Rep. 6, 21776.
Knockout of BRD7 results in impaired spermatogenesis and male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XislOqtrY%3D&md5=486bf23c1df9a84a032adfc7b87dfa3eCAS |

Xian, M., Azuma, S., Naito, K., Kunieda, T., Moriwaki, K., and Toyoda, Y. (1992). Effect of a partial deletion of Y chromosome on in vitro fertilizing ability of mouse spermatozoa. Biol. Reprod. 47, 549–553.
Effect of a partial deletion of Y chromosome on in vitro fertilizing ability of mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2Fgtl2isQ%3D%3D&md5=a1e462729f10e0da463829dc166586cbCAS |

Xu, Y. R., Dong, H. S., and Yang, W. X. (2016). Regulators in the apoptotic pathway during spermatogenesis: killers or guards? Gene 582, 97–111.
Regulators in the apoptotic pathway during spermatogenesis: killers or guards?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisVegtLk%3D&md5=7800a6e686254c4498601761f9938786CAS |

Yan, W., Suominen, J., Samson, M., Jégou, B., and 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, 115–129.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjsLw%3D&md5=935468a1a88ee1ee6154df4df044e7abCAS |

Yin, Y., DeWolf, W. C., and Morgentaler, A. (1998a). Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice. Biol. Reprod. 58, 492–496.
Experimental cryptorchidism induces testicular germ cell apoptosis by p53-dependent and -independent pathways in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXot1SrtQ%3D%3D&md5=ad0c2b3517f8b0a955076d72709082c7CAS |

Yin, Y., Stahl, B. C., DeWolf, W. C., and Morgentaler, A. (1998b). p53-mediated germ cell quality control in spermatogenesis. Dev. Biol. 204, 165–171.
p53-mediated germ cell quality control in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotFSju78%3D&md5=226fac1ec3151ed0f62fc17482db4329CAS |

Yin, Y., Stahl, B. C., DeWolf, W. C., and Morgentaler, A. (2002). P53 and Fas are sequential mechanisms of testicular germ cell apoptosis. J. Androl. 23, 64–70.
P53 and Fas are sequential mechanisms of testicular germ cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksFGjug%3D%3D&md5=d972f622f5bf1b0f980c4a92be6ea38aCAS |