Genetic Variants Causing Teratozoospermia in Humans

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

It is known that pathogenic variants of genes controlling spermiogenesis can lead to the monomorphic teratozoospermia, which is characterized by the predominance of morphological abnormalities of any one type – globozoospermia, macrozoospermia, sperm acephaly, multiple abnormalities of the sperm flagellum, as well as polymorphic teratozoospermia, when several types of sperm abnormalities occur in the ejaculate. The information obtained as a result of systematization and analysis of information on pathogenic gene variants associated with impaired sperm morphology may be useful for understanding the molecular mechanisms of teratozoospermia. The evidences from 134 literature sources and the databases Malacards, OMIM, KEGG, CTD, DisGeNET were obtained. The information on 109 human genes pathogenic variants of which are associated with the teratozoospermia (globozoospermia, multiple flagellum abnormalities syndrome, dysplasia of the fibrous membrane of the flagellum of spermatozoa, acephaly, macrozoospermia, polymorphic teratozoospermia) was systematized. It was revealed that each type of teratozoospermia is caused by a violation of specific biological processes. However, pathogenic gene variants controlling the processes associated with the organization and functioning of the cytoskeleton and intracellular transport make the greatest contribution genetically determined teratozoospermia.

Full Text

Restricted Access

About the authors

M. A. Kleshchev

Federal Research Center Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences

Author for correspondence.
Email: max82cll@bionet.nsc.ru
Russian Federation, Novosibirsk, 630090

A. V. Osadchuk

Federal Research Center Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences

Email: max82cll@bionet.nsc.ru
Russian Federation, Novosibirsk, 630090

L. V. Osadchuk

Federal Research Center Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences

Email: max82cll@bionet.nsc.ru
Russian Federation, Novosibirsk, 630090

References

  1. Vander Borght M., Wyns C. Fertility and infertility: Definition and epidemiology // Clin. Biochemistry. 2018. V. 62. P. 2–10. https://doi.org/10.1016/j.clinbiochem.2018.03.012
  2. World Health Organization. WHO laboratory manual for the examination and processing of human semen. 6th edn. World Health Organization: Geneva, 2021.
  3. Auger J., Jouannet P., Eustache F. Another look at human sperm morphology // Hum. Reproduction. 2016. V. 31. № 1. P. 10–23. https://doi.org/10.1093/humrep/dev251
  4. Brahem S., Elghezal H., Ghédir H. et al. Cytogenetic and molecular aspects of absolute teratozoospermia: Comparison between polymorphic and monomorphic forms // Urology. 2011. V. 78. № 6. P. 1313–1319. https://doi.org/10.1016/j.urology.2011.08.064.
  5. Krausz C., Riera-Escamilla A. Genetics of male infertility // Nat. Reviews Urology. 2018. V. 15. № 6. P. 369–384. https://doi.org/10.1038/s41585-018-0003-3
  6. Chemes H.E. Phenotypic varieties of sperm pathology: Genetic abnormalities or environmental influences can result in different patterns of abnormal spermatozoa // Animal Reproduction Sci. 2018. V. 194. P. 41–56. https://doi.org/10.1016/j.anireprosci.2018.04.074
  7. Ma Y., Xie N., Xie D. et al. A novel homozygous FBXO43 mutation associated with male infertility and teratozoospermia in a consanguineous Chinese family // Fertility and Sterility. 2019. V. 111. № 5. P. 909–917. https://doi.org/10.1016/j.fertnstert.2019.01.007
  8. Zhao S. Y., Meng L. L., Du Z. et al. A novel loss-of-function variant in PNLDC1 inducing oligo-astheno-teratozoospermia and male infertility // Asian J. Andrology. 2023. V. 25. № 5. P. 643–645. https://doi.org/10.4103/aja20233
  9. de Braekeleer M., Nguyen M. H., Morel F., Perrin A. Genetic aspects of monomorphic teratozoospermia: A review // J. Assisted Reproduction and Genet. 2015. V. 32. № 4. P. 615–623. https://doi.org/10.1007/s10815-015-0433-2
  10. Evgeni E., Lymberopoulos G., Touloupidis S., Asimakopoulos B. Sperm nuclear DNA fragmentation and its association with semen quality in Greek men // Andrologia. 2015. V. 47. № 10. P. 1166–1174. https://doi.org/10.1111/and.12398
  11. Mangiarini A., Paffoni A., Restelli L. et al. Specific sperm defects are differentially correlated with DNA fragmentation in both normozoospermic and teratozoospermic subjects // Andrology. 2013. V. 1. № 6. P. 838–844. https://doi.org/10.1111/j.2047-2927.2013.00138.x
  12. Oumaima A., Tesnim A., Zohra H. et al. Investigation on the origin of sperm morphological defects: oxidative attacks, chromatin immaturity, and DNA fragmentation // Environmental Sci. and Pollution Res. 2018. V. 25. № 14. P. 13775–13786. https://doi.org/10.1007/s11356-018-1417-4
  13. Wang Y., Chen G., Tang Z., Mei X et al. Loss-of-function mutations in IQCN cause male infertility in humans and mice owing to total fertilization failure // Mol. Hum. Reproduction. 2023. V. 29. № 7. https://doi.org/10.1093/molehr/gaad018
  14. Zakrzewski P., Lenartowska M., Buss, F. Diverse functions of myosin VI in spermiogenesis // Histochemistry and Cell Biol. 2021. V. 155. № 3. P. 323–340. https://doi.org/10.1007/s00418-020-01954-x
  15. Wei Y. L., Yang, W. X. The acroframosome-acroplaxome-manchette axis may function in sperm head shaping and male fertility // Gene. 2018. № 660. P. 28–40. https://doi.org/10.1016/j.gene.2018.03.059
  16. Teves M. E., Roldan E. R. S. Sperm bauplan and function and underlying processes of sperm formation and selection // Physiol. Reviews. 2022. V. 102. № 1. P. 7–60. https://doi.org/10.1152/physrev.00009.2020
  17. Kierszenbaum A.L., Tres L.L. The acrosome-acroplaxome–manchette complex and the shaping of the spermatid head // Arch. of Histology and Cytology. 2004. V. 67. № 4. P. 271–284. https://doi.org/10.1679/aohc.67.271
  18. Lehti M. S., Sironen A. Formation and function of the manchette and flagellum during spermatogenesis // Reproduction. 2016. V. 151. № 4. P. R43–R54. https://doi.org/10.1530/REP-15-0310
  19. Berruti G., Paiard C. The dynamic of the apical ectoplasmic specialization between spermatids and Sertoli cells: The case of the small GTPase Rap1 // Biomed. Res. Int. 2014. https://doi.org/10.1155/2014/635979
  20. Dai J., Zhang,T., Guo J. et al. Homozygous pathogenic variants in ACTL9 cause fertilization failure and male infertility in humans and mice // Am. J. Hum. Genet. 2021. V. 108. № 3. P. 469–481. https://doi.org/10.1016/j.ajhg.2021.02.004
  21. Zhou X., Xi Q., Jia W. et al. A novel homozygous mutation in ACTL7A leads to male infertility // Mol. Genet. and Genomics. 2023. V. 298. № 2. P. 353–360. https://doi.org/10.1007/s00438-022-01985-0
  22. Chang Y., Jiang X., Liu W. et al. Molecular genetic mechanisms of teratozoospermia // Zygote (Cambridge, England). 2023. V. 31. № 2. P. 101–110. https://doi.org/10.1017/S0967199422000594
  23. Kherraf Z. E., Conne B., Amiri-Yekta A., Kent M. C. Creation of knock out and knock in mice by CRISPR/Cas9 to validate candidate genes for human male infertility, interest, difficulties and feasibility // Mol. and Cellular Endocrinology. 2018. V. 46 № 8. P. 70–80. https://doi.org/10.1016/j.mce.2018.03.002
  24. Crafa A., Condorelli R. A., La Vignera S. et al. Globozoospermia: А case report and systematic review of literature // The World J. Men’s Health. 2023. V. 41. № 1. P. 49–80. https://doi.org/10.5534/wjmh.220020
  25. Beurois J., Cazin C., Kherraf Z. E. Genetics of teratozoospermia: back to the head // Best Practice & Res. Clin. Endocrinology & Metabolism. 2020. V. 34. № 6. https://doi.org/10.1016/j.beem.2020.101473
  26. Touré A., Martinez G., Kherraf Z. E., Cazin C. et al. The genetic architecture of morphological abnormalities of the sperm tail // Hum. Genet. 2021. V. 140. № 1. P. 21–42. https://doi.org/10.1007/s00439-020-02113-x
  27. Rappaport N., Twik M., Plaschkes I. et al. MalaCards: An amalgamated human disease compendium with diverse clinical and genetic annotation and structured search // Nucl. Acids Res. 2017. V. 45. P. 877–887. https://doi.org/10.1093/nar/gkw1012
  28. Davis A.P., Wiegers T. C., Johnson R.J. et al. Comparative Toxicogenomics Database (CTD): Update 2023 // Nucl. Acids Res. 2023. V. 51(D1). P. D1257–D1262. https://doi.org/10.1093/nar/gkac833
  29. Demenkov P.S., Ivanisenko T., Kolchanov N. A., Ivanisenko V. A. ANDVisio: A new tool for graphic visualization and analysis of literature mined associative gene networks in the ANDSystem // In Silico Biol. 2011. V. 11. № 3. P. 149–161. https://doi.org/10.3233/ISB-2012-0449
  30. Ricci G., Andolfi L., Zabucchi G. et al. Ultrastructural morphology of sperm from human globozoospermia // BioMed Res. Int. 2015. https://doi.org/10.1155/2015/798754
  31. Sáez-Espinosa P., Robles-Gómez L., Ortega-López L. et al. Immunofluorescence and high-resolution microscopy reveal new insights in human globozoospermia // Int. J. Mol. Sci. 2022. V. 23. № 3. https://doi.org/10.3390/ijms23031729
  32. Dam A. H., Ramos L., Dijkman H. B. et al. Morphology of partial globozoospermia // J. Andrology. 2011. V. 32. № 2. P. 199–206. https://doi.org/10.2164/jandrol.109.009530
  33. Moreno R. D. Human globozoospermia-related genes and their role in acrosome biogenesis // WIREs Mechanisms of Disease. 2023. V. 15 № 2. https://doi.org/10.1002/wsbm.1589
  34. Elinati E., Kuentz P., Redin C. et al. Globozoospermia is mainly due to dpy19l2 deletion via non-allelic homologous recombination involving two recombination hotspots // Hum. Mol. Genet. 2012. V. 21. № 16. P. 3695–3702. https://doi.org/10.1093/hmg/dds200
  35. Pierre V., Martinez G., Coutton C. et al. Absence of Dpy19l2, a new inner nuclear membrane protein, causes globozoospermia in mice by preventing the anchoring of the acrosome to the nucleus // Development (Cambridge). 2012. V. 139. № 16. P. 2955–2965. https://doi.org/10.1242/dev.077982
  36. Ghédir H., Braham A., Viville S. et al. Comparison of sperm morphology and nuclear sperm quality in SPATA16- and DPY19L2-mutated globozoospermic patients // Andrologia. 2019. V. 51. № 6. https://doi.org/10.1111/and.13277
  37. Dam A. H. D. M., Koscinski I., Kremer J. A. M. et al. Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia // Am. J. Hum. Genet. 2007. V. 81. № 4. P. 813–820. https://doi.org/10.1086/521314
  38. Fujihara Y., Satouh Y., Inoue N., Isotani A. SPACA1-deficient male mice are infertile with abnormally shaped sperm heads reminiscent of globozoospermia // Development (Cambridge). 2012. V. 139. № 19. P. 3583–3589. https://doi.org/10.1242/dev.081778
  39. Chen P., Saiyin H., Shi R. et al. Loss of SPACA1 function causes autosomal recessive globozoospermia by damaging the acrosome-acroplaxome complex // Hum. Reproduction. 2021. V. 36. № 9. P. 2587–2596. https://doi.org/10.1093/humrep/deab144
  40. Liu G., Sh Q. W., Lu G. X. A newly discovered mutation in PICK1 in a human with globozoospermia // Asian J. Andrology. 2010. V. 12. № 4. P. 556–560. https://doi.org/10.1038/aja.2010.47
  41. Xiao N., Kam C., Shen C. et al. PICK1 deficiency causes male infertility in mice by disrupting acrosome formation // J. Clin. Investigation. 2009. V. 119. № 4. P. 802–812. https://doi.org/10.1172/JCI36230
  42. Oud M. S., Okutman Ö., Hendricks L. A. et al. Exome sequencing reveals novel causes as well as new candidate genes for human globozoospermia // Hum. Reproduction (Oxford, England). 2020. V. 35 № 1. P. 240–252. https://doi.org/10.1093/humrep/dez246
  43. Yatsenko A. N., O’Neil D. S., Roy A. et al. Association of mutations in the zona pellucida binding protein 1 (ZPBP1) gene with abnormal sperm head morphology in infertile men // Mol. Hum. Reproduction. 2012. V. 18. № 1. P. 14–21. https://doi.org/10.1093/molehr/gar057
  44. Lin Y.-N., Roy A., Yan W. et al. Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis // Mol. and Cellular Biol. 2007. V. 27. № 19. P. 6794–6805. https://doi.org/10.1128/mcb.01029-07
  45. Li Y., Li C., Lin S. et al. A nonsense mutation in Ccdc62 gene is responsible for spermiogenesis defects and male infertility in repro29/repro29 mice // Biol. of Reproduction. 2017. V. 96. № 3. P. 587–597. https://doi.org/10.1095/biolreprod.116.141408
  46. Li Y., Wang Y., Wen Y. et al. Whole-exome sequencing of a cohort of infertile men reveals novel causative genes in teratozoospermia that are chiefly related to sperm head defects // Hum. Reproduction. 2022. V. 37. № 1. P. 152–177. https://doi.org/10.1093/humrep/deab229
  47. Refik-Rogers J., Manova K., Koff A. Misexpression of cyclin B3 leads to aberrant spermatogenesis // Cell Cycle. 2006. V. 5. № 17. P. 1966–1973. https://doi.org/10.4161/cc.5.17.3137
  48. Christensen G. L., Ivanov I. P., Atkins J. F. et al. Identification of polymorphisms in the Hrb, GOPC, and Csnk2a2 genes in two men with globozoospermia // J. Andrology. 2006. V. 27. № 1. P. 11–15. https://doi.org/10.2164/jandrol.05087
  49. Celse T., Cazin C., Mietton F. et al. Genetic analyses of a large cohort of infertile patients with globozoospermia, DPY19L2 still the main actor, GGN confirmed as a guest player // Hum. Genet. 2021. V. 140. № 1. P. 43–57. https://doi.org/10.1007/s00439-020-02229-0
  50. Liu Y., Li Y., Meng L. et al. Bi-allelic human TEKT3 mutations cause male infertility with oligoasthenoteratozoospermia owing to acrosomal hypoplasia and reduced progressive motility // Hum. Mol. Genet. 2023. V. 32 № 10. P. 1730–1740. https://doi.org/10.1093/hmg/ddad013
  51. Roy A., Lin Y. N., Agno J. E. et al. Tektin 3 is required for progressive sperm motility in mice // Mol. Reproduction and Development. 2009. V. 76. № 5. P. 453–459. https://doi.org/10.1002/mrd.20957
  52. Wang J., Wang W., Shen L. et al. Clinical detection, diagnosis and treatment of morphological abnormalities of sperm flagella: A review of literature // Frontiers in Genet. 2022. V. 13. https://doi.org/10.3389/fgene.2022.1034951
  53. Wang W. L., Tu C. F., Tan Y. Q. Insight on multiple morphological abnormalities of sperm flagella in male infertility: What is new? // Asian J. Andrology. 2020. V. 22. № 3. P. 236–245. https://doi.org/10.4103/aja.aja_53_19
  54. Sha Y., Yang X., Mei L. et al. DNAH1 gene mutations and their potential association with dysplasia of the sperm fibrous sheath and infertility in the Han Chinese population // Fertility and Sterility. 2017. V. 107. № 6. P. 1312–1318.
  55. Oud M.S., Houston B.J., Volozonoka L. et al. Exome sequencing reveals variants in known and novel candidate genes for severe sperm motility disorders // Hum. Reproduction. 2021. V. 36. № 9. P. 2597–2611.
  56. Horani A., Ferkol T. W. Understanding primary ciliary dyskinesia and other ciliopathies // J. of Pediatrics. 2021. V. 230. P. 15-22.e1. https://doi.org/10.1016/j.jpeds.2020.11.040
  57. Sironen A., Shoemark A., Patel M., Loebinger M. R. Sperm defects in primary ciliary dyskinesia and related causes of male infertility // Cellular and Mol. Life Sci. CMLS. 2020. V. 77. № 11. P. 2029–2048. https://doi.org/10.1007/s00018-019-03389-7
  58. Li L., Sha Y. W., Xu X. et al. DNAH6 is a novel candidate gene associated with sperm head anomaly // Andrologia. 2018. V. 50. № 4. https://doi.org/10.1111/and.12953
  59. Shao Z.-M., Zhu Y.-T., Gu M. et al. Novel variants in DNAH6 cause male infertility associated with multiple morphological abnormalities of the sperm flagella (MMAF) and ICSI outcomes // Asian J. Andrology. 2023. https://doi.org/10.4103/aja202328
  60. Tu C., Nie H., Meng L. et al. Identification of DNAH6 mutations in infertile men with multiple morphological abnormalities of the sperm flagella // Sci. Reports. 2019. V. 9. № 1. https://doi.org/10.1038/s41598-019-52436-7
  61. Lei C., Yang D., Wang R. et al. DRC1 deficiency caused primary ciliary dyskinesia and MMAF in a Chinese patient // J. Hum. Genet. 2022. V. 67. № 4. P. 197–201. https://doi.org/10.1038/s10038-021-00985-z
  62. Zhang J., He X., Wu H. et al. Loss of DRC1 function leads to multiple morphological abnormalities of the sperm flagella and male infertility in human and mouse // Hum. Mol. Genet. 2021. V. 30. № 21. P. 1996–2011. https://doi.org/10.1093/hmg/ddab171
  63. Pereira R., Oliveira J., Ferraz L., Barros A. Mutation analysis in patients with total sperm immotility // J. Assisted Reproduction and Genet. 2015. V. 32. № 6. P. 893–902.
  64. Niemeyer J., Mentrup T., Heidasch R. et al. The intramembrane protease SPPL2c promotes male germ cell development by cleaving phospholamban // EMBO Reports. 2019. V. 20. № 3.
  65. Papadopoulou A.A., Müller S.A., Mentrup T. et al. Signal peptide peptidase-like 2c impairs vesicular transport and cleaves SNARE proteins // EMBO Reports. 2019. V. 20. № 3. doi: 10.15252/embr.201846451.
  66. Sha Y., Liu W., Li L., Serafimovski M. Pathogenic variants in ACTRT1 cause acephalic spermatozoa syndrome // Frontiers in Cell and Developmental Biol. 2021. № 9. 676246.
  67. Nie H., Tang Y., Qin W. Beyond acephalic spermatozoa: the complexity of intracytoplasmic sperm injection outcomes // BioMed Res. Int. 2020. 6279795.
  68. Zhu F., Wang F., Yang X. et al. Biallelic SUN5 mutations cause autosomal-recessive acephalic spermatozoa syndrome // Am. J. Hum. Genet. 2016. V. 99. № 4. P. 942–949. https://doi.org/10.1016/j.ajhg.2016.08.004
  69. Wang Y., Xiang M. F. Genetic pathogenesis of acephalic spermatozoa syndrome: past, present, and future // Asian J. Andrology. 2022. V. 24. № 3. P. 231–237. https://doi.org/10.4103/aja202198
  70. Zhang D., Huang W. J., Chen G. Y. et al. Pathogenesis of acephalic spermatozoa syndrome caused by SUN5 variant // Mol. Hum. Reproduction. 2021. V. 27. № 5. https://doi.org/10.1093/molehr/gaab028
  71. Shang Y., Zhu F., Wang L. et al. Essential role for SUN5 in anchoring sperm head to the tail // eLife. 2017. V. 6. https://doi.org/10.7554/eLife.28199
  72. Zhu F., Liu C., Wang F. et al. Mutations in PMFBP1 cause acephalic spermatozoa syndrome. // Am. J. of Hum. Genet. 2018. V. 103. № 2. P. 188–199. https://doi.org/10.1016/j.ajhg.2018.06.010
  73. Moghaddam M., Mazaheri Moghaddam M., Hamzeiy H. et al. Genetic basis of acephalic spermatozoa syndrome, and intracytoplasmic sperm injection outcomes in infertile men: A systematic scoping review // J. of Assisted Reproduction and Genet. 2021. V. 38. № 3. P. 573–586.
  74. Sha Y. W., Wang X., Xu X. et al. Biallelic mutations in PMFBP1 cause acephalic spermatozoa // Clin. Genet. 2019. V. 95. № 2. P. 277–286. https://doi.org/10.1111/cge.13461
  75. Luo G., Hou M., Wang B. et al. Tsga10 is essential for arrangement of mitochondrial sheath and male fertility in mice // Andrology. 2021. V. 9. № 1. P. 368–375. https://doi.org/10.1111/andr.1288
  76. Sha Y. W., Sha Y. K., Ji Z. Y. et al. TSGA10 is a novel candidate gene associated with acephalic spermatozoa // Clin. Genet. 2018. V. 93. № 4. P. 776–783. https://doi.org/10.1111/cge.13140
  77. Li L., Sha Y., Wang X., Li P. Whole-exome sequencing identified a homozygous BRDT mutation in a patient with acephalic spermatozoa // Oncotarget. 2017. V. 8. № 12. P. 19914–19922. https://doi.org/10.18632/oncotarget.15251
  78. Chen H., Zhu Y., Zhu Z., Zhi E. Detection of heterozygous mutation in hook microtubule-tethering protein 1 in three patients with decapitated and decaudated spermatozoa syndrome // J. Med. Genet. 2018. V. 55. № 3. P. 150–157. https://doi.org/10.1136/jmedgenet-2016-104404
  79. Maldonado-Báez L., Cole N. B., Krämer H., Donaldson J. G. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1 // J. Cell Biol. 2013. V. 201. № 2. P. 233–247. https://doi.org/10.1083/jcb.201208172
  80. Sha Y., Wang X., Yuan J. T., Zhu X. Loss-of-function mutations in centrosomal protein 112 is associated with human acephalic spermatozoa phenotype // Clin. Genet. 2020. V. 97. № 2. P. 321–328. https://doi.org/10.1111/cge.13662
  81. Kim J., Kwon J. T., Jeong J. et al. SPATC1L maintains the integrity of the sperm head‐tail junction // EMBO Reports. 2018. V. 19. № 9. https://doi.org/10.15252/embr.201845991
  82. Li Y. Z., Li N., Liu W. S., Sha Y. W. Biallelic mutations in spermatogenesis and centriole-associated 1 like (SPATC1L) cause acephalic spermatozoa syndrome and male infertility // Asian J. Andrology. 2022. V. 24. № 1. P. 67–72. https://doi.org/10.4103/aja.aja_56_21
  83. Wang X., Jiang C., Dai S. et al. Identification of nonfunctional SPATA20 causing acephalic spermatozoa syndrome in humans // Clin. Genet. 2023. V. 103. № 3. P. 310–319. https://doi.org/10.1111/cge.14268
  84. Martinez G., Metzler-Guillemain C., Cazin C. et al. Expanding the sperm phenotype caused by mutations in SPATA20: А novel splicing mutation in an infertile patient with partial globozoospermia // Clin. Genet. 2023. V. 103. № 5. P. 612–614. https://doi.org/10.1111/cge.14284
  85. Sujit K. M., Singh V., Trivedi S. et al. Increased DNA methylation in the spermatogenesis-associated (SPATA) genes correlates with infertility // Andrology. 2020. V. 8. № 3. P. 602–609. https://doi.org/10.1111/andr.12742
  86. Wellard S. R., Schindler K., Jordan P.W. Aurora B and C kinases regulate chromosome desynapsis and segregation during mouse and human spermatogenesis // J. Cell Sci. 2020. V. 133. № 23.
  87. Carmignac V., Dupont J.M., Fierro R. C. et al. Diagnostic genetic screening for assisted reproductive technologies patients with macrozoospermia // Andrology. 2017. V. 5. № 2. P. 370–380.
  88. Bai S., Hu X., Zhao Y. et al. Compound heterozygosity for novel AURKC mutations in an infertile man with macrozoospermia // Andrologia. 2020. V. 52. № 9.
  89. Hua J., Wan Y. Y. Whole-exome sequencing identified a novel mutation of AURKC in a Chinese family with macrozoospermia // J. Assisted Reproduction and Genet. 2019. V. 36. № 3. P. 529–534.
  90. Kimmins S., Crosio C., Kotaja N. et al. Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis // Mol. Endocrinology. 2007. V. 21. № 3. P. 726–739.
  91. Kherraf Z.E., Cazin C., Lestrade F. et al. From azoospermia to macrozoospermia, a phenotypic continuum due to mutations in the ZMYND15 gene // Asian J. Andrology. 2022. V. 24. № 3. P. 243–247.
  92. Yan W., Si Y., Slaymaker S. et al. Zmynd15 encodes a histone deacetylase-dependent transcriptional repressor essential for spermiogenesis and male fertility // The J. Biol. Chemistry. 2010. V. 285. № 41. P. 31418–31426.
  93. Kierszenbaum A. L., Rivkin E., Tres L. L. Molecular biology of sperm head shaping // Society Reproduction and Fertility Supplement. 2007. V. 65. P. 33–43.
  94. Osadchuk L., Shantanova L., Troev I.et al. Regional and ethnic differences in semen quality and reproductive hormones in Russia: А Siberian population-based cohort study of young men // Andrology. 2021. V. 9. № 5. P. 1512–1525.
  95. Kleshchev M., Osadchuk A., Osadchuk L. Impaired semen quality, an increase of sperm morphological defects and DNA fragmentation associated with environmental pollution in urban population of young men from Western Siberia, Russia // PLoS Оne. 2021. V. 16. № 10.
  96. Kolmykov S., Vasiliev G., Osadchuk L. et al. Whole-exome sequencing analysis of human semen quality in Russian multiethnic population // Frontiers in Genet. 2021. V. 12.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Appendix 1
Download (37KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences