Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Increased DNA strand breaks in spermatozoa of Pxt1 knockout mice

Bernadetta Pawlicka A , Michał Duliban https://orcid.org/0000-0002-0677-060X B , Mateusz Zięba A , Michał Bochenek C , Kamila Zięba A , Ibrahim Adham D , Maja Studencka-Turski D , Andreas Meinhardt E and Paweł Grzmil https://orcid.org/0000-0001-9780-2007 A *
+ Author Affiliations
- Author Affiliations

A Laboratory of Genetics and Evolutionism, Institute of Zoology and Biomedical Research, Jagiellonian University in Kraków, Kraków, Poland.

B Department of Endocrinology, Institute of Zoology and Biomedical Research, Jagiellonian University in Kraków, Kraków, Poland.

C Malopolska Centre of Biotechnology, Jagiellonian University in Kraków, Kraków, Poland.

D Institute of Human Genetics, University Medical Center Göttingen, Göttingen, Germany.

E Institute of Anatomy and Cell Biology, Justus-Liebig-University, Giessen, Germany.

* Correspondence to: pawel.grzmil@uj.edu.pl

Handling Editor: Jessica Dunleavy

Reproduction, Fertility and Development 35(11) 589-600 https://doi.org/10.1071/RD23061
Published online: 3 July 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: The Pxt1 gene encodes a male germ cell–specific protein and its overexpression results in male germ cell degeneration and male infertility in transgenic mice.

Aims: The analysis of the function of Pxt1 during mouse spermatogenesis.

Methods: The phenotype of Pxt1 knockout mice was characterised by testicular histology, assessment of semen parameters including sperm motility, and DNA fragmentation by flow cytometry. Gene expression was analysed using RT-PCR. Fertility of mutants was checked by standard breeding and competition breeding tests.

Key results: In Pxt1−/− mice, a strong increase in the sperm DNA fragmentation index (DFI) was observed, while other sperm parameters were comparable to those of control animals. Despite enhanced DFI, mutants were fertile and able to mate in competition with wild type males.

Conclusions: Pxt1 induces cell death; thus, the higher sperm DFI of mice with targeted deletion of Pxt1 suggests some function for this gene in the elimination of male germ cells with chromatin damage.

Implications: Ablation of mouse Pxt1 results in enhanced DFI. In humans, the homologous PXT1 gene shares 74% similarity with the mouse gene; thus, it can be considered a candidate for mutation screening in patients with increased DFI.

Keywords: competition breeding test, gene expression, gene knockout, male fertility, Pxt1, spermatogenesis, sperm chromatin damage, sperm DFI.


References

Adham, IM, Eck, TJ, Mierau, K, Müller, N, Sallam, MA, Paprotta, I, Schubert, S, Hoyer-Fender, S, and Engel, W (2005). Reduction of spermatogenesis but not fertility in Creb3l4-deficient mice. Molecular and Cellular Biology 25, 7657–7664.
Reduction of spermatogenesis but not fertility in Creb3l4-deficient mice.Crossref | GoogleScholarGoogle Scholar |

Agarwal, A, Barbăroșie, C, Ambar, R, and Finelli, R (2020). The impact of single- and double-strand DNA breaks in human spermatozoa on assisted reproduction. International Journal of Molecular Sciences 21, 3882.
The impact of single- and double-strand DNA breaks in human spermatozoa on assisted reproduction.Crossref | GoogleScholarGoogle Scholar |

Aguilar, F, Yu, S, Grant, RA, Swanson, S, Ghose, D, Su, BG, Sarosiek, KA, and Keating, AE (2023). Peptides from human BNIP5 and PXT1 and non-native binders of pro-apoptotic BAK can directly activate or inhibit BAK-mediated membrane permeabilization. Structure 31, 265–281.e7.
Peptides from human BNIP5 and PXT1 and non-native binders of pro-apoptotic BAK can directly activate or inhibit BAK-mediated membrane permeabilization.Crossref | GoogleScholarGoogle Scholar |

Aitken, RJ (2018). Not every sperm is sacred; a perspective on male infertility. Molecular Human Reproduction 24, 287–298.
Not every sperm is sacred; a perspective on male infertility.Crossref | GoogleScholarGoogle Scholar |

Aouacheria, A, Combet, C, Tompa, P, and Hardwick, JM (2015). Redefining the BH3 death domain as a ‘Short Linear Motif’. Trends in Biochemical Sciences 40, 736–748.
Redefining the BH3 death domain as a ‘Short Linear Motif’.Crossref | GoogleScholarGoogle Scholar |

Auger, J, Mesbah, M, Huber, C, and Dadoune, JP (1990). Aniline blue staining as a marker of sperm chromatin defects associated with different semen characteristics discriminates between proven fertile and suspected infertile men. International Journal of Andrology 13, 452–462.
Aniline blue staining as a marker of sperm chromatin defects associated with different semen characteristics discriminates between proven fertile and suspected infertile men.Crossref | GoogleScholarGoogle Scholar |

Ausejo, R, Martínez, JM, Soler-Llorens, P, Bolarín, A, Tejedor, T, and Falceto, MV (2021). Seasonal changes of nuclear DNA fragmentation in boar spermatozoa in Spain. Animals 11, 465.
Seasonal changes of nuclear DNA fragmentation in boar spermatozoa in Spain.Crossref | GoogleScholarGoogle Scholar |

Barbonetti, A, Castellini, C, Di Giammarco, N, Santilli, G, Francavilla, S, and Francavilla, F (2016). In vitro exposure of human spermatozoa to bisphenol A induces pro-oxidative/apoptotic mitochondrial dysfunction. Reproductive Toxicology 66, 61–67.
In vitro exposure of human spermatozoa to bisphenol A induces pro-oxidative/apoptotic mitochondrial dysfunction.Crossref | GoogleScholarGoogle Scholar |

Birkhead TR (2001) ‘Promiscuity: an evolutionary history of sperm competition.’ (Harvard University Press: Cambridge, MA, USA)

Bochenek, M, Smorąg, Z, and Pilch, J (2001). Sperm chromatin structure assay of bulls qualified for artificial insemination. Theriogenology 56, 557–567.
Sperm chromatin structure assay of bulls qualified for artificial insemination.Crossref | GoogleScholarGoogle Scholar |

Casciola-Rosen, L, Rosen, A, Petri, M, and Schlissel, M (1996). Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus. Proceedings of the National Academy of Sciences 93, 1624–1629.
Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus.Crossref | GoogleScholarGoogle Scholar |

Dean, MD, Ardlie, KG, and Nachman, MW (2006). The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Molecular Ecology 15, 4141–4151.
The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus).Crossref | GoogleScholarGoogle Scholar |

Deenadayal Mettler, A, Govindarajan, M, Srinivas, S, Mithraprabhu, S, Evenson, D, and Mahendran, T (2020). Male age is associated with sperm DNA/chromatin integrity. The Aging Male 23, 822–829.
Male age is associated with sperm DNA/chromatin integrity.Crossref | GoogleScholarGoogle Scholar |

De Felici, M, and Klinger, FG (2015). Programmed cell death in mouse primordial germ cells. The International Journal of Developmental Biology 59, 41–49.
Programmed cell death in mouse primordial germ cells.Crossref | GoogleScholarGoogle Scholar |

Du, L, Chen, W, Cheng, Z, Wu, S, He, J, Han, L, He, Z, and Qin, W (2021). Novel gene regulation in normal and abnormal spermatogenesis. Cells 10, 666.
Novel gene regulation in normal and abnormal spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

Evenson DP (2013) Sperm chromatin structure assay (SCSA). In ‘Spermatogenesis’. Methods in Molecular Biology, Vol. 927. (Eds D Carrell, K Aston) pp. 147–164. (Humana Press: New York, NY, USA) 10.1007/978-1-62703-038-0_14

Evenson, DP (2016). The Sperm Chromatin Structure Assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Animal Reproduction Science 169, 56–75.
The Sperm Chromatin Structure Assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility.Crossref | GoogleScholarGoogle Scholar |

Evenson, DP (2017). Evaluation of sperm chromatin structure and DNA strand breaks is an important part of clinical male fertility assessment. Translational Andrology and Urology 6, S495–S500.
Evaluation of sperm chromatin structure and DNA strand breaks is an important part of clinical male fertility assessment.Crossref | GoogleScholarGoogle Scholar |

Evenson DP (2018) Sperm Chromatin Structure Assay (SCSAVR): evolution from origin to clinical utility. In ‘A clinician’s guide to sperm DNA and chromatin damage’. (Eds A Zini, A Agarwal) pp. 65–89. (Springer International: Cham, Switzerland) https://doi.org/10.1007/978-3-319-71815-6

Evenson, DP, Witkin, SS, de Harven, E, and Bendich, A (1978). Ultrastructure of partially decondensed human spermatozoal chromatin. Journal of Ultrastructure Research 63, 178–187.
Ultrastructure of partially decondensed human spermatozoal chromatin.Crossref | GoogleScholarGoogle Scholar |

Evenson, DP, Darzynkiewicz, Z, and Melamed, MR (1980a). Comparison of human and mouse sperm chromatin structure by flow cytometry. Chromosoma 78, 225–238.
Comparison of human and mouse sperm chromatin structure by flow cytometry.Crossref | GoogleScholarGoogle Scholar |

Evenson, DP, Darzynkiewicz, Z, and Melamed, MR (1980b). Relation of mammalian sperm chromatin heterogeneity to fertility. Science 210, 1131–1133.
Relation of mammalian sperm chromatin heterogeneity to fertility.Crossref | GoogleScholarGoogle Scholar |

Evenson, DP, Larson, KL, and Jost, LK (2002). Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. Journal of Andrology 23, 25–43.
Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques.Crossref | GoogleScholarGoogle Scholar |

Evenson, DP, Djira, G, Kasperson, K, and Christianson, J (2020). Relationships between the age of 25,445 men attending infertility clinics and sperm chromatin structure assay (SCSA®) defined sperm DNA and chromatin integrity. Fertility and Sterility 114, 311–320.
Relationships between the age of 25,445 men attending infertility clinics and sperm chromatin structure assay (SCSA®) defined sperm DNA and chromatin integrity.Crossref | GoogleScholarGoogle Scholar |

Fraga, CG, Motchnik, PA, Wyrobek, AJ, Rempel, DM, and Ames, BN (1996). Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 351, 199–203.
Smoking and low antioxidant levels increase oxidative damage to sperm DNA.Crossref | GoogleScholarGoogle Scholar |

Gogol, P, Bochenek, M, and Smorag, Z (2002). Effect of rabbit age on sperm chromatin structure. Reproduction in Domestic Animals 37, 92–95.
Effect of rabbit age on sperm chromatin structure.Crossref | GoogleScholarGoogle Scholar |

Grizard, G, Ouchchane, L, Roddier, H, Artonne, C, Sion, B, Vasson, M-P, and Janny, L (2007). In vitro alachlor effects on reactive oxygen species generation, motility patterns and apoptosis markers in human spermatozoa. Reproductive Toxicology 23, 55–62.
In vitro alachlor effects on reactive oxygen species generation, motility patterns and apoptosis markers in human spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Grzmil, P, Burfeind, C, Preuss, T, Dixkens, C, Wolf, S, Engel, W, and Burfeind, P (2007). The putative peroxisomal gene Pxt1 is exclusively expressed in the testis. Cytogenetic and Genome Research 119, 74–82.
The putative peroxisomal gene Pxt1 is exclusively expressed in the testis.Crossref | GoogleScholarGoogle Scholar |

Grzmil, P, Boinska, D, Kleene, KC, Adham, I, Schlüter, G, Kämper, M, Buyandelger, B, Meinhardt, A, Wolf, S, and Engel, W (2008). Prm3, the fourth gene in the mouse protamine gene cluster, encodes a conserved acidic protein that affects sperm motility. Biology of Reproduction 78, 958–967.
Prm3, the fourth gene in the mouse protamine gene cluster, encodes a conserved acidic protein that affects sperm motility.Crossref | GoogleScholarGoogle Scholar |

Guérin, J-F, and Benchaïb, M (2004). Tests d’exploration de la qualité nucléaire du spermatozoïde: relations avec la fertilité et la qualité du conceptus [Assays for assessment of sperm DNA integrity: relationships with fertility and conceptus quality]. Gynécologie Obstétrique & Fertilité 32, 799–802.
Tests d’exploration de la qualité nucléaire du spermatozoïde: relations avec la fertilité et la qualité du conceptus [Assays for assessment of sperm DNA integrity: relationships with fertility and conceptus quality].Crossref | GoogleScholarGoogle Scholar |

Gupta, S, Finelli, R, Agarwal, A, and Henkel, R (2021). Total antioxidant capacity – relevance, methods and clinical implications. Andrologia 53, e13624.
Total antioxidant capacity – relevance, methods and clinical implications.Crossref | GoogleScholarGoogle Scholar |

Januskauskas, A, Söderquist, L, Håård, MG, Ch, M, Lundeheim, N, and Rodriguez-Martinez, H (1996). Influence of sperm number per straw on the post-thaw sperm viability and fertility of Swedish red and white A.I. bulls. Acta Veterinaria Scandinavica 37, 461–470.
Influence of sperm number per straw on the post-thaw sperm viability and fertility of Swedish red and white A.I. bulls.Crossref | GoogleScholarGoogle Scholar |

Joyner AL (1993) ‘Gene targeting: a practical approach.’ p. 234. (Oxford University Press: UK) 10.1093/oso/9780199637928.001.0001

Jurewicz, J, Radwan, M, Wielgomas, B, Sobala, W, Piskunowicz, M, Radwan, P, Bochenek, M, and Hanke, W (2015). The effect of environmental exposure to pyrethroids and DNA damage in human sperm. Systems Biology in Reproductive Medicine 61, 37–43.
The effect of environmental exposure to pyrethroids and DNA damage in human sperm.Crossref | GoogleScholarGoogle Scholar |

Kaczmarek, K, Studencka, M, Meinhardt, A, Wieczerzak, K, Thoms, S, Engel, W, and Grzmil, P (2011). Overexpression of peroxisomal testis-specific 1 protein induces germ cell apoptosis and leads to infertility in male mice. Molecular Biology of the Cell 22, 1766–1779.
Overexpression of peroxisomal testis-specific 1 protein induces germ cell apoptosis and leads to infertility in male mice.Crossref | GoogleScholarGoogle Scholar |

Khan, S, Jan, MH, Kumar, D, and Telang, AG (2015). Firpronil induced spermotoxicity is associated with oxidative stress, DNA damage and apoptosis in male rats. Pesticide Biochemistry and Physiology 124, 8–14.
Firpronil induced spermotoxicity is associated with oxidative stress, DNA damage and apoptosis in male rats.Crossref | GoogleScholarGoogle Scholar |

Kikukawa, Y, Minami, R, Shimada, M, Kobayashi, M, Tanaka, K, Yokosawa, H, and Kawahara, H (2005). Unique proteasome subunit Xrpn10c is a specific receptor for the antiapoptotic ubiquitin-like protein Scythe. FEBS Journal 272, 6373–6386.
Unique proteasome subunit Xrpn10c is a specific receptor for the antiapoptotic ubiquitin-like protein Scythe.Crossref | GoogleScholarGoogle Scholar |

Kleene, KC (2005). Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells. Developmental Biology 277, 16–26.
Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells.Crossref | GoogleScholarGoogle Scholar |

Lane, M, McPherson, NO, Fullston, T, Spillane, M, Sandeman, L, Kang, WX, and Zander-Fox, DL (2014). Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring. PLoS ONE 9, e100832.
Oxidative stress in mouse sperm impairs embryo development, fetal growth and alters adiposity and glucose regulation in female offspring.Crossref | GoogleScholarGoogle Scholar |

Lim, D, Jin, S, Shin, H-C, Kim, W, Choi, JS, Oh, D-B, Kim, SJ, Seo, J, and Ku, B (2022). Structural and biochemical analyses of Bcl-xL in complex with the BH3 domain of peroxisomal testis-specific 1. Biochemical and Biophysical Research Communications 625, 174–180.
Structural and biochemical analyses of Bcl-xL in complex with the BH3 domain of peroxisomal testis-specific 1.Crossref | GoogleScholarGoogle Scholar |

Lolis, D, Georgiou, I, Syrrou, M, Zikopoulos, K, Konstantelli, M, and Messinis, I (1996). Chromomycin A3-staining as an indicator of protamine deficiency and fertilization. International Journal of Andrology 19, 23–27.
Chromomycin A3-staining as an indicator of protamine deficiency and fertilization.Crossref | GoogleScholarGoogle Scholar |

Lomonosova, E, and Chinnadurai, G (2008). BH3-only proteins in apoptosis and beyond: an overview. Oncogene 27, S2–S19.
BH3-only proteins in apoptosis and beyond: an overview.Crossref | GoogleScholarGoogle Scholar |

Lu, Y, Lin, M, and Aitken, RJ (2017). Exposure of spermatozoa to dibutyl phthalate induces abnormal embryonic development in a marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae). Aquatic Toxicology 191, 189–200.
Exposure of spermatozoa to dibutyl phthalate induces abnormal embryonic development in a marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae).Crossref | GoogleScholarGoogle Scholar |

Lyon MF, Searle AG (1989) ‘Genetic variants and strains of the laboratory mouse.’ 2nd edn. pp. XIV, 876. (Oxford University Press: UK) https://doi.org/10.1002/jobm.3620300716

Mannan, AU, Nayernia, K, Mueller, C, Burfeind, P, Adham, IM, and Engel, W (2003). Male mice lacking the Theg (testicular haploid expressed gene) protein undergo normal spermatogenesis and are fertile. Biology of Reproduction 69, 788–796.
Male mice lacking the Theg (testicular haploid expressed gene) protein undergo normal spermatogenesis and are fertile.Crossref | GoogleScholarGoogle Scholar |

Martinot, E, Sèdes, L, Baptissart, M, Holota, H, Rouaisnel, B, Damon-Soubeyrand, C, De Haze, A, Saru, J-P, Thibault-Carpentier, C, Keime, C, Lobaccaro, J-MA, Baron, S, Benoit, G, Caira, F, Beaudoin, C, and Volle, DH (2017). The bile acid nuclear receptor FXRα is a critical regulator of mouse germ cell fate. Stem Cell Reports 9, 315–328.
The bile acid nuclear receptor FXRα is a critical regulator of mouse germ cell fate.Crossref | GoogleScholarGoogle Scholar |

Matzuk, MM, and Lamb, DJ (2002). Genetic dissection of mammalian fertility pathways. Nature Cell Biology 8, s41–s49.
Genetic dissection of mammalian fertility pathways.Crossref | GoogleScholarGoogle Scholar |

Matzuk, MM, and Lamb, DJ (2008). The biology of infertility: research advances and clinical challenges. Nature Medicine 14, 1197–1213.
The biology of infertility: research advances and clinical challenges.Crossref | GoogleScholarGoogle Scholar |

Miciński, P, Pawlicki, K, Wielgus, E, Bochenek, M, and Tworkowska, I (2009). The sperm chromatin structure assay (SCSA) as prognostic factor in IVF/ICSI program. Reproductive Biology 9, 65–70.
The sperm chromatin structure assay (SCSA) as prognostic factor in IVF/ICSI program.Crossref | GoogleScholarGoogle Scholar |

Mund, T, Gewies, A, Schoenfeld, N, Bauer, MKA, and Grimm, S (2003). Spike, a novel BH3-only protein, regulates apoptosis at the endoplasmic reticulum. The FASEB Journal 17, 696–698.
Spike, a novel BH3-only protein, regulates apoptosis at the endoplasmic reticulum.Crossref | GoogleScholarGoogle Scholar |

Nayernia, K, Adham, IM, Shamsadin, R, Müller, C, Sancken, U, and Engel, W (2002). Proacrosin-deficient mice and zona pellucida modifications in an experimental model of multifactorial infertility. Molecular Human Reproduction 8, 434–440.
Proacrosin-deficient mice and zona pellucida modifications in an experimental model of multifactorial infertility.Crossref | GoogleScholarGoogle Scholar |

Nayernia, K, Drabent, B, Adham, IM, Möschner, M, Wolf, S, Meinhardt, A, and Engel, W (2003). Male mice lacking three germ cell expressed genes are fertile. Biology of Reproduction 69, 1973–1978.
Male mice lacking three germ cell expressed genes are fertile.Crossref | GoogleScholarGoogle Scholar |

Ni, W, Liu, K, Hou, G, Pan, C, Wu, S, Zheng, J, Cao, J, Chen, Q, and Huang, X (2019). Diurnal variation in sperm DNA fragmentation: analysis of 11,382 semen samples from two populations and in vivo animal experiments. Chronobiology International 36, 1455–1463.
Diurnal variation in sperm DNA fragmentation: analysis of 11,382 semen samples from two populations and in vivo animal experiments.Crossref | GoogleScholarGoogle Scholar |

Nozawa, K, Fritzler, MJ, Takasaki, Y, Wood, MR, and Chan, EKL (2009). Co-clustering of Golgi complex and other cytoplasmic organelles to crescentic region of half-moon nuclei during apoptosis. Cell Biology International 33, 148–157.
Co-clustering of Golgi complex and other cytoplasmic organelles to crescentic region of half-moon nuclei during apoptosis.Crossref | GoogleScholarGoogle Scholar |

Oleszczuk, K, Giwercman, A, and Bungum, M (2016). Sperm chromatin structure assay in prediction of in vitro fertilization outcome. Andrology 4, 290–296.
Sperm chromatin structure assay in prediction of in vitro fertilization outcome.Crossref | GoogleScholarGoogle Scholar |

Ozaki, T, Hanaoka, E, Naka, M, Nakagawara, A, and Sakiyama, S (1999). Cloning and characterization of rat BAT3 cDNA. DNA and Cell Biology 18, 503–512.
Cloning and characterization of rat BAT3 cDNA.Crossref | GoogleScholarGoogle Scholar |

Rosahl, TW, Spillane, D, Missler, M, Herz, J, Selig, DK, Wolff, JR, Hammer, RE, Malenka, RC, and Südhof, TC (1995). Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375, 488–493.
Essential functions of synapsins I and II in synaptic vesicle regulation.Crossref | GoogleScholarGoogle Scholar |

Shukla, KK, Mahdi, AA, and Rajender, S (2012). Apoptosis, spermatogenesis and male infertility. Frontiers in Bioscience 4, 746–754.
Apoptosis, spermatogenesis and male infertility.Crossref | GoogleScholarGoogle Scholar |

Sinha Hikim, AP, Wang, C, Lue, Y, Johnson, L, Wang, X-H, and Swerdloff, RS (1998). Spontaneous germ cell apoptosis in humans: evidence for ethnic differences in the susceptibility of germ cells to programmed cell death. The Journal of Clinical Endocrinology & Metabolism 83, 152–156.
Spontaneous germ cell apoptosis in humans: evidence for ethnic differences in the susceptibility of germ cells to programmed cell death.Crossref | GoogleScholarGoogle Scholar |

Taylor, JD, Baumgartner, A, Schmid, TE, and Brinkworth, MH (2019). Responses to genotoxicity in mouse testicular germ cells and epididymal spermatozoa are affected by increased age. Toxicology Letters 310, 1–6.
Responses to genotoxicity in mouse testicular germ cells and epididymal spermatozoa are affected by increased age.Crossref | GoogleScholarGoogle Scholar |

Tripathi, R, Mishra, DP, and Shaha, C (2009). Male germ cell development: turning on the apoptotic pathways. Journal of Reproductive Immunology 83, 31–35.
Male germ cell development: turning on the apoptotic pathways.Crossref | GoogleScholarGoogle Scholar |

Wang, R, and Liew, C-C (1994). The human BAT3 ortholog in rodents is predominantly and developmentally expressed in testis. Molecular and Cellular Biochemistry 136, 49–57.
The human BAT3 ortholog in rodents is predominantly and developmentally expressed in testis.Crossref | GoogleScholarGoogle Scholar |

Westerman, R (2020). Biomarkers for demographic research: sperm counts and other male infertility biomarkers. Biodemography and Social Biology 65, 73–87.
Biomarkers for demographic research: sperm counts and other male infertility biomarkers.Crossref | GoogleScholarGoogle Scholar |

Wu, Y-H, Shih, S-F, and Lin, J-Y (2004). Ricin triggers apoptotic morphological changes through caspase-3 cleavage of BAT3. Journal of Biological Chemistry 279, 19264–19275.
Ricin triggers apoptotic morphological changes through caspase-3 cleavage of BAT3.Crossref | GoogleScholarGoogle Scholar |

Yatsenko, AN, Iwamori, N, Iwamori, T, and Matzuk, MM (2010). The power of mouse genetics to study spermatogenesis. Journal of Andrology 31, 34–44.
The power of mouse genetics to study spermatogenesis.Crossref | GoogleScholarGoogle Scholar |