Hostname: page-component-848d4c4894-p2v8j Total loading time: 0 Render date: 2024-06-08T21:29:54.597Z Has data issue: false hasContentIssue false

Molecular genetic mechanisms of teratozoospermia

Published online by Cambridge University Press:  06 February 2023

Ying Chang
Affiliation:
Jilin Medical University, jilin, 132013, China
Xin Jiang
Affiliation:
Jilin Medical University, jilin, 132013, China
Wei Liu
Affiliation:
Jilin Medical University, jilin, 132013, China
Dongfang Zhang
Affiliation:
Jilin Medical University, jilin, 132013, China
Shubao Yang*
Affiliation:
Jilin Medical University, jilin, 132013, China
Donghai Zhao*
Affiliation:
Jilin Medical University, jilin, 132013, China
*
Authors for correspondence: Donghai Zhao, Jilin Medical University, jilin, 132013, China. E-mail: zdh751027@126.com; Shubao Yang, Jilin Medical University, jilin, 132013, China. E-mail: 18721325@qq.com
Authors for correspondence: Donghai Zhao, Jilin Medical University, jilin, 132013, China. E-mail: zdh751027@126.com; Shubao Yang, Jilin Medical University, jilin, 132013, China. E-mail: 18721325@qq.com

Summary

In recent years, the incidence of teratospermia has been increasing, and it has become a very important factor leading to male infertility. The research on the molecular mechanism of teratospermia is also progressing rapidly. This article briefly summarizes the clinical incidence of teratozoospermia, and makes a retrospective summary of related studies reported in recent years. Specifically discussing the relationship between gene status and spermatozoa, the review aims to provide the basis for the genetic diagnosis and gene therapy of teratozoospermia.

Type
Review Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press

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.)

Footnotes

a

These authors contributed equally to this work.

References

Abu-Halima, M., Ayesh, B. M., Hart, M., Alles, J., Fischer, U., Hammadeh, M., Keller, A., Huleihel, M. and Meese, E. (2019). Differential expression of miR-23a/b-3p and its target genes in male patients with subfertility. Fertility and Sterility, 112(2), 323335.e2. doi: 10.1016/j.fertnstert.2019.03.025 CrossRefGoogle ScholarPubMed
Aydos, O. S. E., Hekmatshoar, Y., Altınok, B., Özkan, T., Şakirağaoğlu, O., Karadağ, A., Kaplan, F., Ilgaz, S., Taşpınar, M., Yükselen, I., Sunguroğlu, A. and Aydos, K. (2018). Genetic polymorphisms in PRM1, PRM2, and YBX2 genes are associated with male factor infertility. Genetic Testing and Molecular Biomarkers, 22(1), 5561. doi: 10.1089/gtmb.2017.0040 CrossRefGoogle ScholarPubMed
Ben Khelifa, M., Coutton, C., Zouari, R., Karaouzène, T., Rendu, J., Bidart, M., Yassine, S., Pierre, V., Delaroche, J., Hennebicq, S., Grunwald, D., Escalier, D., Pernet-Gallay, K., Jouk, P. S., Thierry-Mieg, N., Touré, A., Arnoult, C. and Ray, P. F. (2014). Mutations in DNAH1, which encodes an inner arm heavy chain dynein, lead to male infertility from multiple morphological abnormalities of the sperm flagella. American Journal of Human Genetics, 94(1), 95104. doi: 10.1016/j.ajhg.2013.11.017 CrossRefGoogle ScholarPubMed
Bao, J., Zhang, J., Zheng, H., Xu, C., & Yan, W. (2010). UBQLN1 interacts with SPEM1 and participates in spermiogenesis. Molecular and Cellular Endocrinology, 327(1), 8997.CrossRefGoogle ScholarPubMed
Bao, J., Wu, Q., Song, R., Jie, Z., Zheng, H., Xu, C. and Yan, W. (2011). RANBP17 is localized to the XY body of spermatocytes and interacts with SPEM1 on the manchette of elongating spermatids. Molecular and Cellular Endocrinology, 333(2), 134142. doi: 10.1016/j.mce.2010.12.021.CrossRefGoogle Scholar
Bhanmeechao, C., Srisuwatanasagul, S., Prapaiwan, N. and Ponglowhapan, S. (2018). Reproductive aging in male dogs: The epididymal sperm defects and expression of androgen receptor in reproductive tissues. Theriogenology, 108, 7480. doi: 10.1016/j.theriogenology.2017.11.011 CrossRefGoogle ScholarPubMed
Blendy, J. A., Kaestner, K. H., Weinbauer, G. F., Nieschlag, E. and Schütz, G. (1996). Severe impairment of spermatogenesis in mice lacking the CREM gene. Nature, 380(6570), 162165. doi: 10.1038/380162a0 CrossRefGoogle ScholarPubMed
Bracke, A., Peeters, K., Punjabi, U., Hoogewijs, D. and Dewilde, S. (2018) A search for molecular mechanisms underlying male idiopathic infertility. Reproductive Biomedicine Online, 36(3), 327339. doi: 10.1016/j.rbmo.2017.12.005 CrossRefGoogle ScholarPubMed
Chianese, C., Fino, M. G., Riera Escamilla, A., López Rodrigo, O., Vinci, S., Guarducci, E., Daguin, F., Muratori, M., Tamburrino, L., Lo Giacco, D., Ars, E., Bassas, L., Costa, M., Pisatauro, V., Noci, I., Coccia, E., Provenzano, A., Ruiz-Castañé, E., Giglio, S., et al. (2015). Comprehensive investigation in patients affected by sperm macrocephaly and globozoospermia. Andrology, 3(2), 203212. doi: 10.1111/andr.12016 CrossRefGoogle ScholarPubMed
Coutton, C., Escoffier, J., Martinez, G., Arnoult, C. and Ray, P. F. (2015). Teratozoospermia: Spotlight on the main genetic actors in the human. Human Reproduction Update, 21(4), 455485. doi: 10.1093/humupd/dmv020 CrossRefGoogle ScholarPubMed
Coutton, C., Vargas, A. S., Amiri-Yekta, A., Kherraf, Z. E., Ben Mustapha, S. F., Le Tanno, P., Wambergue-Legrand, C., Karaouzène, T., Martinez, G., Crouzy, S., Daneshipour, A., Hosseini, S. H., Mitchell, V., Halouani, L., Marrakchi, O., Makni, M., Latrous, H., Kharouf, M., Deleuze, J. F., Boland, A., et al. (2018). Mutations in CFAP43 and CFAP44 cause male infertility and flagellum defects in Trypanosoma and human. Nature Communications, 9(1), 686. doi: 10.1038/s41467-017-02792-7 CrossRefGoogle ScholarPubMed
Coveney, C. R., Collins, I., Mc Fie, M., Chanalaris, A., Yamamoto, K. and Wann, A. K. T. (2018). Cilia protein IFT88 regulates extracellular protease activity by optimizing LRP-1-mediated endocytosis. FASEB Journal, 32(12), fj201800334. doi: 10.1096/fj.201800334 CrossRefGoogle ScholarPubMed
Dam, A. H., Koscinski, I., Kremer, J. A., Moutou, C., Jaeger, A. S., Oudakker, A. R., Tournaye, H., Charlet, N., Lagier-Tourenne, C., van Bokhoven, H. and Viville, S. (2007). Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia. American Journal of Human Genetics, 81(4), 813820. doi: 10.1086/521314 CrossRefGoogle ScholarPubMed
Dávila Garza, S. A. and Patrizio, P. (2013). Reproductive outcomes in patients with male infertility because of Klinefelter’s syndrome, Kartagener’s syndrome, round-head sperm, dysplasia fibrous sheath, and “stump”‘stump’ tail sperm: An updated literature review. Current Opinion in Obstetrics and Gynecology, 25(3), 229246. doi: 10.1097/GCO.0b013e32835faae5 CrossRefGoogle ScholarPubMed
De Braekeleer, M., Nguyen, M. H., Morel, F. and Perrin, A. (2015). Genetic aspects of monomorphic teratozoospermia: A review. Journal of Assisted Reproduction and Genetics, 32(4), 615623. doi: 10.1007/s10815-015-0433-2 CrossRefGoogle ScholarPubMed
Dehghanpour, F., Tabibnejad, N., Fesahat, F., Yazdinejad, F. and Talebi, A. R. (2017). Evaluation of sperm protamine deficiency and apoptosis in infertile men with idiopathic teratozoospermia. Clinical and Experimental Reproductive Medicine, 44(2), 7378. doi: 10.5653/cerm.2017.44.2.73 CrossRefGoogle ScholarPubMed
Dong, F. N., Amiri-Yekta, A., Martinez, G., Saut, A., Tek, J., Stouvenel, L., Lorès, P., Karaouzène, T., Thierry-Mieg, N., Satre, V., Brouillet, S., Daneshipour, A., Hosseini, S. H., Bonhivers, M., Gourabi, H., Dulioust, E., Arnoult, C., Touré, A., et al. (2018). Absence of CFAP69 causes male infertility due to multiple morphological abnormalities of the flagella in human and mouse. American Journal of Human Genetics, 102(4), 636648. doi: 10.1016/j.ajhg.2018.03.007 CrossRefGoogle ScholarPubMed
El Kerch, F., Lamzouri, A., Laarabi, F. Z., Zahi, M., Ben Amar, B. and Sefiani, A. (2011). Confirmation of the high prevalence in Morocco of the homozygous mutation c.144delC in the aurora kinase C gene (AURKC) in the teratozoospermia with large-headed spermatozoa. Journal de Gynecologie, Obstetrique et Biologie de la Reproduction, 40(4), 329333. doi: 10.1016/j.jgyn.2010.09.003 CrossRefGoogle ScholarPubMed
Elinati, E., Kuentz, P., Redin, C., Jaber, S., Vanden Meerschaut, F., Makarian, J., Koscinski, I., Nasr-Esfahani, M. H., Demirol, A., Gurgan, T., Louanjli, N., Iqbal, N., Bisharah, M., Pigeon, F. C., Gourabi, H., De Briel, D., Brugnon, F., Gitlin, S. A., Grillo, J. M., et al. (2012). Globozoospermia is mainly due to DPY19L2 deletion via non-allelic homologous recombination involving two recombination hotspots. Human Molecular Genetics, 21(16), 36953702. doi: 10.1093/hmg/dds200 CrossRefGoogle ScholarPubMed
Elisen, M. G., van Kooij, R. J., Nolte, M. A., Marquart, J. A., Lock, T. M., Bouma, B. N. and Meijers, J. C. (1998). Protein C inhibitor may modulate human sperm-oocyte interactions. Biology of Reproduction, 58(3), 670677. doi: 10.1095/biolreprod58.3.670 CrossRefGoogle ScholarPubMed
Elkhatib, R. A., Paci, M., Longepied, G., Saias-Magnan, J., Courbière, B., Guichaoua, M. R., Lévy, N., Metzler-Guillemain, C. and Mitchell, M. J. (2017). Homozygous deletion of SUN5 in three men with decapitated spermatozoa. Human Molecular Genetics, 26(16), 31673171. doi: 10.1093/hmg/ddx200 Google ScholarPubMed
Fellmeth, J. E., Ghanaim, E. M. and Schindler, K. (2016). Characterization of macrozoospermia-associated AURKC mutations in a mammalian meiotic system. Human Molecular Genetics, 25(13), 26982711. doi: 10.1093/hmg/ddw128 Google Scholar
Ford, W. C. (2010). Comments on the release of the 5th edition of the WHO Laboratory Manual for the examination and processing of human semen. Asian Journal of Andrology, 12(1), 5963. doi: 10.1038/aja.2008.57 CrossRefGoogle ScholarPubMed
Ganguly, I., Gaur, G. K., Kumar, S., Mandal, D. K., Kumar, M., Singh, U., Kumar, S. and Sharma, A. (2013). Differential expression of protamine 1 and 2 genes in mature spermatozoa of normal and motility impaired semen producing crossbred Frieswal (HFxSahiwal) bulls. Research in Veterinary Science, 94(2), 256262. doi: 10.1016/j.rvsc.2012.09.001 CrossRefGoogle ScholarPubMed
Ghazavi, F., Peymani, M., Hashemi, M. S., Ghaedi, K. and Nasr-Esfahani, M. H. (2019). Embryos derived from couples with consanguineous marriages with globozoospermia should be screened for gender or DPY19L2 deletion. Andrologia, 51(4), e13221. doi: 10.1111/and.13221 CrossRefGoogle ScholarPubMed
Ghédir, H., Ibala-Romdhane, S., Okutman, O., Viot, G., Saad, A. and Viville, S. (2016). Identification of a new DPY19L2 mutation and a better definition of DPY19L2 deletion breakpoints leading to globozoospermia. Molecular Human Reproduction, 22(1), 3545. doi: 10.1093/molehr/gav061 CrossRefGoogle Scholar
Ghédir, H., Braham, A., Viville, S., Saad, A. and Ibala-Romdhane, S. (2019). Comparison of sperm morphology and nuclear sperm quality in SPATA16- and DPY19L2-mutated globozoospermic patients. Andrologia, 51(6), e13277. doi: 10.1111/and.13277 CrossRefGoogle ScholarPubMed
Haigis, M. C. and Sinclair, D. A. (2010). Mammalian sirtuins: Biological insights and disease relevance. Annual Review of Pathology, 5(1), 253295. doi: 10.1146/annurev.pathol.4.110807.092250 CrossRefGoogle ScholarPubMed
He, J., Xia, M., Tsang, W. H., Chow, K. L. and Xia, J. (2015). ICA1L forms BAR-domain complexes with PICK1 and is crucial for acrosome formation in spermiogenesis. Journal of Cell Science, 128(20), 38223836. doi: 10.1242/jcs.173534 Google ScholarPubMed
He, X., Li, W., Wu, H., Lv, M., Liu, W., Liu, C., Zhu, F., Li, C., Fang, Y., Yang, C., Cheng, H., Zhang, J., Tan, J., Chen, T., Tang, D., Song, B., Wang, X., Zha, X., Wang, H., et al. (2019). Novel homozygous CFAP69 mutations in humans and mice cause severe asthenoteratospermia with multiple morphological abnormalities of the sperm flagella. Journal of Medical Genetics, 56(2), 96103. doi: 10.1136/jmedgenet-2018-105486 CrossRefGoogle ScholarPubMed
Hetherington, L., Schneider, E. K., Scott, C., DeKretser, D., Muller, C. H., Hondermarck, H., Velkov, T. and Baker, M. A. (2017). Deficiency in outer dense fiber 1 is a marker and potential driver of idiopathic male infertility. Molecular and Cellular Proteomics, 16(6), 1172. doi: 10.1074/mcp.A116.060343 CrossRefGoogle ScholarPubMed
Hu, J. H., Zhang, J. F., Ma, Y. H., Jiang, J., Yang, N., Li, X. B., Yu Chi, Z. G., Fei, J. and Guo, L. H. (2004). Impaired reproduction in transgenic mice overexpressing gamma-aminobutyric acid transporter I (GAT1). Cell Research, 14(1), 5459. doi: 10.1038/sj.cr.7290202 CrossRefGoogle ScholarPubMed
Huynh, L. M., Shinagawa, T. and Ishii, S. (2016). Two histone variants TH2A and TH2B enhance human induced pluripotent stem cell generation. Stem Cells and Development, 25(3), 251258. doi: 10.1089/scd.2015.0264 CrossRefGoogle ScholarPubMed
Ike, A., Yamada, S., Tanaka, H., Nishimune, Y. and Nozaki, M. (2002). Structure and promoter activity of the gene encoding ornithine decarboxylase antizyme expressed exclusively in haploid germ cells in testis (OAZt/Oaz3). Gene, 298(2), 183193. doi: 10.1016/s0378-1119(02)00978-2 CrossRefGoogle ScholarPubMed
Jedidi, I., Ouchari, M. and Yin, Q. (2018). Autosomal single-gene disorders involved in human infertility. Saudi Journal of Biological Sciences, 25(5), 881887. doi: 10.1016/j.sjbs.2017.12.005 CrossRefGoogle ScholarPubMed
Jiang, X., Wang, X., Zhang, X., Xiao, Z., Zhang, C., Liu, X., Xu, J., Li, D. and Shen, Y. (2019a). A homozygous RNF220 mutation leads to male infertility with small-headed sperm. Gene, 688, 1318. doi: 10.1016/j.gene.2018.11.074 CrossRefGoogle ScholarPubMed
Jiang, S., Liang, C., Gao, Y., Liu, Y., Han, Y., Wang, J. and Zhang, J. (2019b). Fluoride exposure arrests the acrosome formation during spermatogenesis via down-regulated Zpbp1, Spaca1 and Dpy19l2 expression in rat testes. Chemosphere, 226, 874882. doi: 10.1016/j.chemosphere.2019.04.019 CrossRefGoogle ScholarPubMed
Kang-Decker, N., Mantchev, G. T., Juneja, S. C., McNiven, M. A. and van Deursen, J. M. (2001). Lack of acrosome formation in Hrb-deficient mice. Science, 294(5546), 15311533. doi: 10.1126/science.1063665 CrossRefGoogle ScholarPubMed
Karaca, N., Yilmaz, R., Kanten, G. E., Kervancioglu, E., Solakoglu, S. and Kervancioglu, M. E. (2014). First successful pregnancy in a globozoospermic patient having homozygous mutation in SPATA16. Fertility and Sterility, 102(1), 103107. doi: 10.1016/j.fertnstert.2014.04.002 CrossRefGoogle Scholar
Kierszenbaum, A. L., Tres, L. L., Rivkin, E., Kang-Decker, N. and van Deursen, J. M. (2004). The acroplaxome is the docking site of Golgi-derived myosin Va/Rab27a/b- containing proacrosomal vesicles in wild-type and Hrb mutant mouse spermatids. Biology of Reproduction, 70(5), 14001410. doi: 10.1095/biolreprod.103.025346 CrossRefGoogle ScholarPubMed
Kierszenbaum, A. L., Rivkin, E. and Tres, L. L. (2011a). Cytoskeletal track selection during cargo transport in spermatids is relevant to male fertility. Spermatogenesis, 1(3), 221230. doi: 10.4161/spmg.1.3.18018 CrossRefGoogle ScholarPubMed
Kierszenbaum, A. L., Rivkin, E., Tres, L. L., Yoder, B. K., Haycraft, C. J., Bornens, M. and Rios, R. M. (2011b). GMAP210 and IFT88 are present in the spermatid Golgi apparatus and participate in the development of the acrosome–acroplaxome complex, head-tail coupling apparatus and tail. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 240(3), 723736. doi: 10.1002/dvdy.22563 CrossRefGoogle ScholarPubMed
Kopp, C., Sukura, A., Tuunainen, E., Gustavsson, I., Parvinen, M. and Andersson, M. (2007). Multinuclear-multiflagellar sperm defect in a bull—A new sterilizing sperm defect. Reproduction in Domestic Animals = Zuchthygiene, 42(2), 208213. doi: 10.1111/j.1439-0531.2006.00754.x CrossRefGoogle Scholar
Koscinski, I., Elinati, E., Fossard, C., Redin, C., Muller, J., Velez de la Calle, J., Schmitt, F., Ben Khelifa, M., Ray, P. F., Kilani, Z., Barratt, C. L. and Viville, S. (2011). DPY19L2 deletion as a major cause of globozoospermia. American Journal of Human Genetics, 88(3), 344350. doi: 10.1016/j.ajhg.2011.01.018 CrossRefGoogle Scholar
Kramer, I. M., Koornneef, I., de Laat, S. W. and van den Eijnden-van Raaij, A. J. (1991). TGF-beta 1 induces phosphorylation of the cyclic AMP responsive element binding protein in ML-CCl64 cells. EMBO Journal, 10(5), 10831089. doi: 10.1002/j.1460-2075.1991.tb08048.x CrossRefGoogle ScholarPubMed
Krausz, C. and Sassone-Corsi, P. (2005). Genetic control of spermiogenesis: Insights from the CREM gene and implications for human infertility. Reproductive Biomedicine Online, 10(1), 6471. doi: 10.1016/s1472-6483(10)60805-x CrossRefGoogle ScholarPubMed
Li, Y., Li, C., Lin, S., Yang, B., Huang, W., Wu, H., Chen, Y., Yang, L., Luo, M., Guo, H., Chen, J., Wang, T., Ma, Q., Gu, Y., Mou, L., Jiang, Z., Xia, J. and Gui, Y. (2017). A nonsense mutation in Ccdc62 gene is responsible for spermiogenesis defects and male infertility in repro29/repro29 mice. Biology of Reproduction, 96(3), 587597. doi: 10.1095/biolreprod.116.141408 CrossRefGoogle ScholarPubMed
Li, X., Wu, Y., Huang, L., Yang, L. and Xing, X. (2019). SPAG4L/SPAG4Lbeta interacts with Nesprin2 to participate in the meiosis of spermatogenesis. Acta Biochimica et Biophysica Sinica, 51(7), 669676. doi: 10.1093/abbs/gmz051 CrossRefGoogle ScholarPubMed
Lin, Y. N., Roy, A., Yan, W., Burns, K. H. and Matzuk, M. M. (2007). Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Molecular and Cellular Biology, 27(19), 67946805. doi: 10.1128/MCB.01029-07 CrossRefGoogle ScholarPubMed
Liska, F., Gosele, C., Rivkin, E., Tres, L., Cardoso, M. C., Domaing, P., Krejcí, E., Snajdr, P., Lee-Kirsch, M. A., de Rooij, D. G., Kren, V., Krenová, D., Kierszenbaum, A. L. and Hubner, N. (2009). Rat hd Mutation Reveals an Essential Role of Centrobin in spermatid Head Shaping and Assembly of the Head-Tail Coupling Apparatus. Biology of Reproduction, 81(6), 11961205. doi: 10.1095/biolreprod.109.078980 CrossRefGoogle ScholarPubMed
Liu, D. Y. and Baker, H. W. (2003). Frequency of defective sperm-zona pellucida interaction in severely teratozoospermic infertile men. Human Reproduction, 18(4), 802807. doi: 10.1093/humrep/deg164 CrossRefGoogle ScholarPubMed
Liu, D. Y., Stewart, T. and Baker, H. W. (2003). Normal range and variation of the zona pellucida-induced acrosome reaction in fertile men. Fertility and Sterility, 80(2), 384389. doi: 10.1016/s0015-0282(03)00603-4 CrossRefGoogle ScholarPubMed
Liu, G., Shi, Q. W. and Lu, G. X. (2010). A newly discovered mutation in PICK1 in a human with globozoospermia. Asian Journal of Andrology, 12(4), 556560. doi: 10.1038/aja.2010.47 CrossRefGoogle Scholar
Liu, R. Z., Wu, J. and Wang, R. X. (2013). Molecular genetic mechanisms of teratozoospermia. Zhonghua Nan Ke Xue, 19(12), 10591067.Google ScholarPubMed
Liu, Y., Liang, C., Gao, Y., Jiang, S., He, Y., Han, Y., Olfati, A., Manthari, R. K., Wang, J. and Zhang, J. (2019). Fluoride interferes with the sperm fertilizing ability via downregulated SPAM1, ACR, and PRSS21 expression in rat epididymis. Journal of Agricultural and Food Chemistry, 67(18), 52405249. doi: 10.1021/acs.jafc.9b01114 CrossRefGoogle ScholarPubMed
Martínez-Rodríguez, C., Alvarez, M., López-Urueña, E., Gomes-Alves, S., Anel-López, L., Tizado, J. E., Anel, L. and de Paz, P. (2015). Head morphology of ram spermatozoa is associated with their ability to migrate in vitro and correlates with fertility. Reproduction, Fertility, and Development, 28(11), 18251837. doi: 10.1071/RD15022 CrossRefGoogle Scholar
Milatiner, D., Halle, D., Huerta, M., Margalioth, E. J., Cohen, Y., Ben-Chetrit, A., Gal, M., Mimoni, T. and Eldar-Geva, T. (2004). Associations between androgen receptor CAG repeat length and sperm morphology. Human Reproduction, 19(6), 14261430. doi: 10.1093/humrep/deh251 CrossRefGoogle ScholarPubMed
Modarres, P., Tanhaei, S., Tavalaee, M., Ghaedi, K., Deemeh, M. R. and Nasr-Esfahani, M. H. (2016). Assessment of DPY19L2 deletion in familial and non-familial individuals with globozoospermia and DPY19L2 genotyping. International Journal of Fertility and Sterility, 10(2), 196207. doi: 10.22074/ijfs.2016.4910 Google ScholarPubMed
Netzel-Arnett, S., Bugge, T. H., Hess, R. A., Carnes, K., Stringer, B. W., Scarman, A. L., Hooper, J. D., Tonks, I. D., Kay, G. F. and Antalis, T. M. (2009). The glycosylphosphatidylinositol-anchored serine protease PRSS21 (testisin) imparts murine epididymal sperm cell maturation and fertilizing ability. Biology of Reproduction, 81(5), 921932. doi: 10.1095/biolreprod.109.076273 CrossRefGoogle ScholarPubMed
Nsota Mbango, J., Coutton, C., Arnoult, C., Ray, P. F. and Touré, A. (2019). Genetic causes of male infertility: Snapshot on morphological abnormalities of the sperm flagellum. Basic and Clinical Andrology, 29(1), 2. doi: 10.1186/s12610-019-0083-9 CrossRefGoogle ScholarPubMed
Odet, F., Guyot, R., Leduque, P. and Le Magueresse-Battistoni, B. (2004). Evidence for similar expression of protein C inhibitor and the urokinase-type plasminogen activator system during mouse testis development. Endocrinology, 145(3), 14811489. doi: 10.1210/en.2003-0955 CrossRefGoogle ScholarPubMed
Ogungbenro, Y. A., Tena, T. C., Gaboriau, D., Lalor, P., Dockery, P., Philipp, M. and Morrison, C. G. (2018). Centrobin controls primary ciliogenesis in vertebrates. Journal of Cell Biology, 217(4), 12051215. doi: 10.1083/jcb.201706095 CrossRefGoogle ScholarPubMed
Ounis, L., Zoghmar, A., Coutton, C., Rouabah, L., Hachemi, M., Martinez, D., Martinez, G., Bellil, I., Khelifi, D., Arnoult, C., Fauré, J., Benbouhedja, S., Rouabah, A. and Ray, P. F. (2015). Mutations of the aurora kinase C gene causing macrozoospermia are the most frequent genetic cause of male infertility in Algerian men. Asian Journal of Andrology, 17(1), 6873. doi: 10.4103/1008-682X.136441 Google ScholarPubMed
Pandey, A., Yadav, S. K., Vishvkarma, R., Singh, B., Maikhuri, J. P., Rajender, S. and Gupta, G. (2019). The dynamics of gene expression during and post meiosis sets the sperm agenda. Molecular Reproduction and Development, 86(12), 19211939. doi: 10.1002/mrd.23278 CrossRefGoogle ScholarPubMed
Pasch, E., Link, J., Beck, C., Scheuerle, S. and Alsheimer, M. (2015). The LINC complex component Sun4 plays a crucial role in sperm head formation and fertility. Biology Open, 4(12), 17921802. doi: 10.1242/bio.015768 CrossRefGoogle Scholar
Perrin, A., Coat, C., Nguyen, M. H., Talagas, M., Morel, F., Amice, J. and De Braekeleer, M. (2013). Molecular cytogenetic and genetic aspects of globozoospermia: A review. Andrologia, 45(1), 19. doi: 10.1111/j.1439-0272.2012.01308.x CrossRefGoogle ScholarPubMed
Pirrello, O., Machev, N., Schimdt, F., Terriou, P., Ménézo, Y. and Viville, S. (2005). Search for mutations involved in human globozoospermia. Human Reproduction, 20(5), 13141318. doi: 10.1093/humrep/deh799 CrossRefGoogle ScholarPubMed
Quartuccio, S. M. and Schindler, K. (2015). Functions of Aurora kinase C in meiosis and cancer. Frontiers in Cell and Developmental Biology, 3, 50. doi: 10.3389/fcell.2015.00050 CrossRefGoogle ScholarPubMed
Ravel, C., Chantot-Bastaraud, S., El Houate, B., Berthaut, I., Verstraete, L., De Larouziere, V., Lourenço, D., Dumaine, A., Antoine, J. M., Mandelbaum, J., Siffroi, J. P. and McElreavey, K. (2007). Mutations in the protamine 1 gene associated with male infertility. Molecular Human Reproduction, 13(7), 461464. doi: 10.1093/molehr/gam031 CrossRefGoogle ScholarPubMed
Ray, P. F., Touré, A., Metzler-Guillemain, C., Mitchell, M. J., Arnoult, C. and Coutton, C. (2017). Genetic abnormalities leading to qualitative defects of sperm morphology or function. Clinical Genetics, 91(2), 217232. doi: 10.1111/cge.12905 CrossRefGoogle ScholarPubMed
Rondanino, C., Duchesne, V., Escalier, D., Jumeau, F., Verhaeghe, F., Peers, M. C., Mitchell, V. and Rives, N. (2015). Evaluation of sperm nuclear integrity in patients with different percentages of decapitated sperm in ejaculates. Reproductive Biomedicine Online, 31(1), 8999. doi: 10.1016/j.rbmo.2015.04.002 CrossRefGoogle ScholarPubMed
Roy, A., Lin, Y. N. and Matzuk, M. M. (2006). Shaping the sperm head: An ER enzyme leaves its mark. Journal of Clinical Investigation, 116(11), 28602863. doi: 10.1172/JCI30221 CrossRefGoogle ScholarPubMed
Ruan, Y., Cheng, M., Ou, Y., Oko, R. and van der Hoorn, F. A. (2011). Ornithine decarboxylase antizyme Oaz3 modulates protein phosphatase activity. Journal of Biological Chemistry, 286(33), 2941729427. doi: 10.1074/jbc.M111.274647 CrossRefGoogle ScholarPubMed
Schwarz, T., Prieler, B., Schmid, J. A., Grzmil, P. and Neesen, J. (2017). Ccdc181 is a microtubule-binding protein that interacts with Hook1 in haploid male germ cells and localizes to the sperm tail and motile cilia. European Journal of Cell Biology, 96(3), 276288. doi: 10.1016/j.ejcb.2017.02.003 CrossRefGoogle Scholar
Sha, Y. W., Ding, L., Wu, J. X., Lin, S. B., Wang, X., Ji, Z. Y. and Li, P. (2017a). Headless spermatozoa in infertile men. Andrologia, 49(8), e12716. doi: 10.1111/and.12716 CrossRefGoogle ScholarPubMed
Sha, Y., Yang, X., Mei, L., Ji, Z., Wang, X., Ding, L., Li, P. and Yang, S. (2017b). DNAH1 gene mutations and their potential association with dysplasia of the sperm fibrous sheath and infertility in the Han Chinese population. Fertility and Sterility, 107(6), 13121318.e2. doi: 10.1016/j.fertnstert.2017.04.007 CrossRefGoogle ScholarPubMed
Sha, Y. W., Wang, X., Xu, X., Su, Z. Y., Cui, Y., Mei, L. B., Huang, X. J., Chen, J., He, X. M., Ji, Z. Y., Bao, H., Yang, X., Li, P. and Li, L. (2019). Novel mutations in CFAP44 and CFAP43 cause multiple morphological abnormalities of the sperm flagella (MMAF). Reproductive Sciences, 26(1), 2634. doi: 10.1177/1933719117749756 CrossRefGoogle ScholarPubMed
Shang, Y., Zhu, F., Wang, L., Ouyang, Y. C., Dong, M. Z., Liu, C., Zhao, H., Cui, X., Ma, D., Zhang, Z., Yang, X., Guo, Y., Liu, F., Yuan, L., Gao, F., Guo, X., Sun, Q. Y., Cao, Y. and Li, W. (2017). Essential role for SUN5 in anchoring sperm head to the tail. eLife, 6, e28199. doi: 10.7554/eLife.28199 CrossRefGoogle ScholarPubMed
Shang, Y., Yan, J., Tang, W., Liu, C., Xiao, S., Guo, Y., Yuan, L., Chen, L., Jiang, H., Guo, X., Qiao, J. and Li, W. (2018). Mechanistic insights into acephalic spermatozoa syndrome-associated mutations in the human SUN5 gene. Journal of Biological Chemistry, 293(7), 23952407. doi: 10.1074/jbc.RA117.000861 CrossRefGoogle ScholarPubMed
Shinagawa, T., Huynh, L. M., Takagi, T., Tsukamoto, D., Tomaru, C., Kwak, H. G., Dohmae, N., Noguchi, J. and Ishii, S. (2015). Disruption of Th2a and Th2b genes causes defects in spermatogenesis. Development, 142(7), 12871292. doi: 10.1242/dev.121830 Google ScholarPubMed
Sironen, A., Shoemark, A., Patel, M., Loebinger, M. R. and Mitchison, H. M. (2020). Sperm defects in primary ciliary dyskinesia and related causes of male infertility. Cellular and Molecular Life Sciences: CMLS, 77(11), 20292048. doi: 10.1007/s00018-019-03389-7 CrossRefGoogle ScholarPubMed
Stafuzza, N. B., Silva, Costa E, E. V. D., Silva, R. M. O., Costa Filho, L. C. C. D., Barbosa, F. B., Macedo, G. G., Lobo, R. B. and Baldi, F. (2020). Genome-wide association study for age at puberty in young Nelore bulls. Journal of Animal Breeding and Genetics, 137(2), 234244. doi: 10.1111/jbg.12438 CrossRefGoogle ScholarPubMed
Steger, K., Fink, L., Klonisch, T., Bohle, R. M. and Bergmann, M. (2002). Protamine-1 and −2 mRNA in round spermatids is associated with RNA-binding proteins. Histochemistry and Cell Biology, 117(3), 227234. doi: 10.1007/s00418-002-0385-3 CrossRefGoogle ScholarPubMed
Sujit, K. M., Singh, V., Trivedi, S., Singh, K., Gupta, G. and Rajender, S. (2020). Increased DNA methylation in the spermatogenesis-associated (SPATA) genes correlates with infertility. Andrology, 8(3), 602609. doi: 10.1111/andr.12742 CrossRefGoogle ScholarPubMed
Suzuki-Toyota, F., Ito, C., Toyama, Y., Maekawa, M., Yao, R., Noda, T., Iida, H. and Toshimori, K. (2007). Factors maintaining normal sperm tail structure during epididymal maturation studied in Gopc−/− mice. Biology of Reproduction, 77(1), 7182. doi: 10.1095/biolreprod.106.058735 CrossRefGoogle ScholarPubMed
Swegen, A., Smith, N. D., Gibb, Z., Curry, B. J. and Aitken, R. J. (2019). The serine protease testisin is present on the surface of capacitated stallion spermatozoa and interacts with key zona pellucida binding proteins. Andrology, 7(2), 199212. doi: 10.1111/andr.12569 CrossRefGoogle ScholarPubMed
Takeda, N., Yoshinaga, K., Furushima, K., Takamune, K., Li, Z., Abe, S., Aizawa, S. and Yamamura, K. (2016). Viable offspring obtained from Prm1-deficient sperm in mice. Scientific Reports, 6, 27409. doi: 10.1038/srep27409 CrossRefGoogle ScholarPubMed
Tapia Contreras, C. C. and Hoyer-Fender, S. (2019). CCDC42 localizes to manchette, HTCA and tail and interacts with ODF1 and ODF2 in the formation of the male germ cell cytoskeleton. Frontiers in Cell and Developmental Biology, 7, 151. doi: 10.3389/fcell.2019.00151 CrossRefGoogle ScholarPubMed
Tokuhiro, K., Isotani, A., Yokota, S., Yano, Y., Oshio, S., Hirose, M., Wada, M., Fujita, K., Ogawa, Y., Okabe, M., Nishimune, Y. and Tanaka, H. (2009). OAZ-t/OAZ3 is essential for rigid connection of sperm tails to heads in mouse. PLOS Genetics, 5(11), e1000712. doi: 10.1371/journal.pgen.1000712 CrossRefGoogle Scholar
Touré, A., Martinez, G., Kherraf, Z. E., Cazin, C., Beurois, J., Arnoult, C., Ray, P. F. and Coutton, C. (2021). The genetic architecture of morphological abnormalities of the sperm tail. Human Genetics, 140(1), 2142. doi: 10.1007/s00439-020-02113-x CrossRefGoogle ScholarPubMed
Tut, T. G., Ghadessy, F. J., Trifiro, M. A., Pinsky, L. and Yong, E. L. (1997). Long polyglutamine tracts in the androgen receptor are associated with reduced trans-activation, impaired sperm production, and male infertility. Journal of Clinical Endocrinology and Metabolism, 82(11), 37773782. doi: 10.1210/jcem.82.11.4385 Google ScholarPubMed
Tüttelmann, F., Křenková, P., Römer, S., Nestorovic, A. R., Ljujic, M., Stambergová, A., Macek, M., Macek, M., Nieschlag, E., Gromoll, J. and Simoni, M. (2010). A common haplotype of protamine 1 and 2 genes is associated with higher sperm counts. International Journal of Andrology, 33(1), e240e248. doi: 10.1111/j.1365-2605.2009.01003.x CrossRefGoogle Scholar
Uhrin, P., Dewerchin, M., Hilpert, M., Chrenek, P., Schöfer, C., Zechmeister-Machhart, M., Krönke, G., Vales, A., Carmeliet, P., Binder, B. R. and Geiger, M. (2000). Disruption of the protein C inhibitor gene results in impaired spermatogenesis and male infertility. Journal of Clinical Investigation, 106(12), 15311539. doi: 10.1172/JCI10768 CrossRefGoogle ScholarPubMed
Utsuno, H., Miyamoto, T., Oka, K. and Shiozawa, T. (2014). Morphological alterations in protamine-deficient spermatozoa. Human Reproduction, 29(11), 23742381. doi: 10.1093/humrep/deu225 CrossRefGoogle ScholarPubMed
Verdin, E., Hirschey, M. D., Finley, L. W. and Haigis, M. C. (2010). Sirtuin regulation of mitochondria: Energy production, apoptosis, and signaling. Trends in Biochemical Sciences, 35(12), 669675. doi: 10.1016/j.tibs.2010.07.003 CrossRefGoogle ScholarPubMed
Walden, C. M., Sandhoff, R., Chuang, C. C., Yildiz, Y., Butters, T. D., Dwek, R. A., Platt, F. M. and van der Spoel, A. C. (2007). Accumulation of glucosylceramide in murine testis, caused by inhibition of beta-glucosidase 2: implications for spermatogenesis. Journal of Biological Chemistry, 282(45), 3265532664. doi: 10.1074/jbc.M702387200 CrossRefGoogle ScholarPubMed
Wang, H., Wan, H., Li, X., Liu, W., Chen, Q., Wang, Y., Yang, L., Tang, H., Zhang, X., Duan, E., Zhao, X., Gao, F. and Li, W. (2014). Atg7 is required for acrosome biogenesis during spermatogenesis in mice. Cell Research, 24(7), 852869. doi: 10.1038/cr.2014.70 CrossRefGoogle ScholarPubMed
Xiao, N., Kam, C., Shen, C., Jin, W., Wang, J., Lee, K. M., Jiang, L. and Xia, J. (2009). PICK1 deficiency causes male infertility in mice by disrupting acrosome formation. Journal of Clinical Investigation, 119(4), 802812. doi: 10.1172/JCI36230 CrossRefGoogle ScholarPubMed
Yang, K., Grzmil, P., Meinhardt, A. and Hoyer-Fender, S. (2014). Haplo-deficiency of ODF1/HSPB10 in mouse sperm causes relaxation of head-to-tail linkage. Reproduction, 148(5), 499506. doi: 10.1530/REP-14-0370 CrossRefGoogle ScholarPubMed
Yang, K., Adham, I. M., Meinhardt, A. and Hoyer-Fender, S. (2018). Ultra-structure of the sperm head-to-tail linkage complex in the absence of the spermatid-specific LINC component SPAG4. Histochemistry and Cell Biology, 150(1), 4959. doi: 10.1007/s00418-018-1668-7 CrossRefGoogle ScholarPubMed
Yao, R., Ito, C., Natsume, Y., Sugitani, Y., Yamanaka, H., Kuretake, S., Yanagida, K., Sato, A., Toshimori, K. and Noda, T. (2002). Lack of acrosome formation in mice lacking a Golgi protein, GOPC. Proceedings of the National Academy of Sciences of the United States of America, 99(17), 1121111216. doi: 10.1073/pnas.162027899 CrossRefGoogle ScholarPubMed
Yatsenko, A. N., O’Neil, D. S., Roy, A., Arias-Mendoza, P. A., Chen, R., Murthy, L. J., Lamb, D. J. and Matzuk, M. M. (2012). Association of mutations in the zona pellucida binding protein 1 (ZPBP1) gene with abnormal sperm head morphology in infertile men. Molecular Human Reproduction, 18(1), 1421. doi: 10.1093/molehr/gar057 CrossRefGoogle ScholarPubMed
Yeh, C. H., Wang, Y. Y., Wee, S. K., Chen, M. F., Chiang, H. S., Kuo, P. L. and Lin, Y. H. (2019). Testis-specific Sept12 expression affects SUN protein localization and is involved in mammalian spermiogenesis. International Journal of Molecular Sciences, 20(5), 1163. doi: 10.3390/ijms20051163 CrossRefGoogle ScholarPubMed
Yu, Y., Vanhorne, J. and Oko, R. (2009). The origin and assembly of a zona pellucida binding protein, IAM38, during spermiogenesis. Microscopy Research and Technique, 72(8), 558565. doi: 10.1002/jemt.20696 CrossRefGoogle ScholarPubMed
Zhang, J., Gui, Y., Yuan, T., Bian, C. and Guo, L. (2009). Expression of GAT1 in male reproductive system and its effects on reproduction in mice. Systems Biology in Reproductive Medicine, 55(5–6), 175180. doi: 10.3109/19396360903030500 CrossRefGoogle ScholarPubMed
Zhou, J., Du, Y. R., Qin, W. H., Hu, Y. G., Huang, Y. N., Bao, L., Han, D., Mansouri, A. and Xu, G. L. (2009). RIM-BP 3 is a manchette-associated protein essential for spermiogenesis. Development, 136(3), 373382. doi: 10.1242/dev.030858 CrossRefGoogle Scholar
Zhu, F., Gong, F., Lin, G. and Lu, G. (2013). DPY19L2 gene mutations are a major cause of globozoospermia: Identification of three novel point mutations. Molecular Human Reproduction, 19(6), 395404. doi: 10.1093/molehr/gat018 CrossRefGoogle Scholar
Zhu, F., Wang, F., Yang, X., Zhang, J., Wu, H., Zhang, Z., Zhang, Z., He, X., Zhou, P., Wei, Z., Gecz, J. and Cao, Y. (2016). Biallelic SUN5 mutations cause autosomal-recessive acephalic spermatozoa syndrome. American Journal of Human Genetics, 99(4), 942949. doi: 10.1016/j.ajhg.2016.08.004 CrossRefGoogle ScholarPubMed
Zhu, F., Liu, C., Wang, F., Yang, X., Zhang, J., Wu, H., Zhang, Z., He, X., Zhang, Z., Zhou, P., Wei, Z., Shang, Y., Wang, L., Zhang, R., Ouyang, Y. C., Sun, Q. Y., Cao, Y. and Li, W. (2018). Mutations in PMFBP1 cause acephalic spermatozoa syndrome. American Journal of Human Genetics, 103(2), 188199. doi: 10.1016/j.ajhg.2018.06.010 CrossRefGoogle ScholarPubMed