Genetic causes of macrozoospermia and proposal for an optimized genetic diagnosis strategy based on sperm parameters

Alicia Coudert; Caroline Cazin; Amir Amiri-Yekta; Selima Fourati Ben Mustapha; Raoudha Zouari; Julien Bessonat; Abdelali Zoghmar; Antoine Clergeau; Catherine Metzler-Guillemain; Chema Triki; Hervé Lejeune; Nathalie Sermondade; Eva Pipiras; Nadia Prisant; Isabelle Cedrin; Isabelle Koscinski; Leila Keskes; Florence Lestrade; Laetitia Hesters; Nathalie Rives; Béatrice Dorphin; Agnes Guichet; Catherine Patrat; Emmanuel Dulioust; Aurélie Feraille; François Robert; Sophie Brouillet; Frédéric Morel; Aurore Perrin; Nathalie Rougier; Eric Bieth; Arthur Sorlin; Jean-Pierre Siffroi; Mariem Ben Khelifa; Florence Boiterelle; Sylvianne Hennebicq; Veronique Satre; Christophe Arnoult; Charles Coutton; Anne-Laure Barbotin; Nicolas Thierry-Mieg; Zine-Eddine Kherraf; Pierre F. Ray

doi:10.1016/j.jgg.2023.04.007

Volume 50 Issue 7

Jul. 2023

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2023 > 50(7): 536-540

PDF( 642 KB)

Genetic causes of macrozoospermia and proposal for an optimized genetic diagnosis strategy based on sperm parameters

doi: 10.1016/j.jgg.2023.04.007

1. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, UniversitéGrenoble Alpes, 38000, Grenoble, France;
2. CHU Grenoble Alpes, UM GI-DPI, 38000, Grenoble, France;
3. CHU Grenoble Alpes, UM de Génétique Chromosomique, 38000, Grenoble, France;
4. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, UniversitéGrenoble Alpes, 38000, Grenoble, France;
5. CHU Grenoble Alpes, UM GI-DPI, 38000, Grenoble, France;
6. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, UniversitéGrenoble Alpes, 38000, Grenoble, France;
7. CHU Grenoble Alpes, UM GI-DPI, 38000, Grenoble, France;
8. Department of Genetics, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran;
9. Polyclinique les Jasmins, Centre d'Aide Médicaleàla Procréation, Centre Urbain Nord, 1003, Tunis, Tunisia;
10. CHU Grenobles Alpes, UF de Biologie de la Procréation, 38000, Grenoble, France;
11. Reproduction Sciences and Surgery Clinique, Ibn Rochd, Constantine, Algeria;
12. CHU Caen, CECOS de Caen, Département de Biologie, Unitéde Biologie de la Reproduction, 14033, Caen, France;
13. APHM Hôpital La-Conception, Pôle Femmes-parents-enfants, Centre Clinico-biologique d'assistance Médicaleàla Procréation-CECOS, 13385 Marseille, France;
14. Aix-Marseille Univ, Inserm, MMG, U1251, 13385 Marseille Medical Genetics, 13385 Marseille, France;
15. Clinique Hannibal, Centre d'AMP, Les Berges du Lac, 1053, Tunis, Tunisia;
16. Reproductive Medicine Department, Hospices Civil de Lyon, Lyon, France;
17. Hôpital Jean Verdier, UniversitéSorbonne Paris Nord, Paris, France;
18. CHU de Pointe-à-Pitre/Abymes, Guadeloupe, France;
19. Service de Médecine de la Reproduction, CHU Jean Verdier, Paris, France;
20. CECOS Alsace, Biologie de la Reproduction, 67303, Schiltigheim, France;
21. Facultéde Médecine de Sfax, Sfax, Tunisia;
22. CHR Metz-Thionville, Service d'Assistance Médicaleàla Procréation, 57530, Ars-Laquenexy, France;
23. Unit of Reproductive Biology, Antoine Béclère University Hospital, University Paris Sud, Clamart, Paris-Sud University, Le Kremlin Bicêtre, France;
24. Univ Rouen Normandie, Inserm U1239, NorDIC, Adrenal and Gonadal Pathophysiology, Reproductive Biology Laboratory-CECOS, Rouen University Hospital, 76031, Rouen Cedex, France;
25. CHAL Centre Hospitalier Alpes Leman, Centre AMP74, 74130, Contamine-sur-Arve, France;
26. CHU Angers, Service de Gen etique, 49933, Angers, INSERM U1083, France;
27. Service de Biologie de la Reproduction e CECOS Hopital Cochin, 74014, Paris, France;
28. Univ Rouen Normandie, Inserm U1239, NorDIC, Adrenal and Gonadal Pathophysiology, Reproductive Biology LaboratoryCECOS, Rouen University Hospital, 76031, Rouen Cedex, France;
29. IRH Medicentre, Clinique du Val d'Ouest, 39 Chemin de la Vernique, 69 130, Ecully, France;
30. CHU Arnaud De Villeneuve, Biologie de la Reproduction, 34000, Montpellier, France;
31. Faculte de M edecine et des Sciences de la Sant e, Universit e de Brest, EFS, UMR1078, GGB, Brest, Franc;
32. Service de Gen etique M edicale et Biologie de la Reproduction, CHU de Brest, Brest, France;
33. CHRU Nîmes, Laboratoire d'Assistance Medicale a la Procr eation, 30029, Nîmes, France;
34. CHU Toulouse, Service de Gen etique, 31059, Toulouse, France;
35. Laboratoire National de Sante,;
1 Rue Louis Rech, L-3555, Dudelange, Luxembourg;
36. Sorbonne Universite, INSERM, UMRS_933, AP-HP, H opital Armand^Trousseau, F-75012, Paris, France;
37. Centre Fertillia, Clinique La Rose, 2035, Tunis, Tunisia;
38. Reproductive Biology, Fertility Preservation, Andrology, CECOS, Poissy Hospital, 78300 Poissy, France;
39. UVSQ, INRAE, BREED, Paris Saclay University, 78350 Jouy-enJosas, France;
40. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, Universite Grenoble Alpes, 38000, Grenoble, France;
41. CHU Grenobles Alpes, UF de Biologie de la Procreation, 38000, Grenoble, France;
42. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, Universite Grenoble Alpes, 38000, Grenoble, France;
43. CHU Grenoble Alpes, UM de Gen etique Chromosomique, 38000, Grenoble, France;
44. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, Universite Grenoble Alpes, 38000, Grenoble, France;
45. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, Universite Grenoble Alpes, 38000, Grenoble, France;
46. CHU Grenoble Alpes, UM de Gen etique Chromosomique, 38000, Grenoble, France;
47. CHU Lille, Hopital Jeanne De Flandre, Laboratoire de Biologie de la^Reproduction-Spermiologie, 59037, Lille, France;
48. Univ. Grenoble Alpes, CNRS, TIMC-IMAG, F-38000, Grenoble, France;
49. Genetic Epigenetic and Therapies of Infertility Team, Institute for Advanced Biosciences, Inserm U 1209, CNRS UMR 5309, Universite Grenoble Alpes, 38000, Grenoble, France;
50. CHU Grenoble Alpes, UM GI-DPI, 38000, Grenoble, France

Funds:

et de la Recherche Mé

This work was funded by the French National Research Agency (ANR), projects MAS FLAGELLA (ANR-14-CE15-0002), FLAGEL-OME (ANR-19-CE17-0014), and the INSERM (Institut National de la Santé

dicale) and Bettencourt Foundation.

Received Date: 2023-01-03
Accepted Date: 2023-04-16
Rev Recd Date: 2023-04-14
Publish Date: 2023-07-28

Abstract

FullText(HTML)

References(20)

References

[1]	Arafah, K., Lopez, F., Cazin, C., Kherraf, Z.-E., Tassistro, V., Loundou, A., Arnoult, C., Thierry-Mieg, N., Bulet, P., Guichaoua, M.-R., Ray, P.F., 2021. Defect in the nuclear pore membrane glycoprotein 210-like gene is associated with extreme uncondensed sperm nuclear chromatin and male infertility: a case report. Hum. Reprod. 36, 693-701.
[2]	Bai, S., Hu, X., Zhao, Y., Li, W., Wan, Y., Jin, R., Wang, Y., Guo, T., Tong, X., Xu, B., 2020. Compound heterozygosity for novel AURKC mutations in an infertile man with macrozoospermia. Andrologia 52, e13663.
[3]	Khelifa, M.B., Coutton, C., Blum, M.G.B., Abada, F., Harbuz, R., Zouari, R., May-Panloup, P., Triki, C., Merdassi, G., Vialard, F., et al., 2012. Identification of a new recurrent Aurora kinase C mutation in both European and African men with macrozoospermia. Hum. Reprod. 27, 3337-3346.
[4]	Choi, S.H., Cho, K., Kim, E.S., Yoo, H.Y., 2022. Proline-serine-threonine-repeat region of MDC1 mediates Chk1 phosphorylation and the DNA double-strand break repair. Int. J. Biochem. Cell Biol. 143, 106152.
[5]	Chukrallah, L.G., Badrinath, A., Vittor, G.G., Snyder, E.M., 2022. ADAD2 regulates heterochromatin in meiotic and post-meiotic male germ cells via translation of MDC. J. Cell Sci. 35, jcs259196.
[6]	Dieterich, K., Rifo, R.S., Faure, A.K., Hennebicq, S., Amar, B.B., Zahi, M., Perrin, J., Martinez, D., Sele, B., Jouk, P.-S., Ohlmann, T., Rousseaux, S., Lunardi, J., Ray, P.F., 2007. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat. Genet. 39, 661-665.
[7]	Dieterich, K., Zouari, R., Harbuz, R., Bellayou, H., Prisant, N., Zoghmar, A., Guichaoua, M.R., Koscinski, I., Kharouf, M., Noruzinia, M., et al., 2009. The Aurora Kinase C c.144delC mutation causes meiosis I arrest in men and is frequent in the North African population. Hum. Mol. Genet. 18, 1301-1309.
[8]	Galander, S., Barton, R.E., Borek, W.E., Robertson, D., Rappsilber, J., Marston, A.L., 2019. Reductional meiosis I chromosome segregation is established by coordination of key meiotic kinases. Dev. Cell 49, 526-541.
[9]	Galander, S., Marston, A.L., 2020. Meiosis I kinase regulators: conserved orchestrators of reductional chromosome segregation. Bioessays 42, e2000018
[10]	Kherraf, Z.-E., Cazin, C., Lestrade, F., Muronova, J., Coutton, C., Arnoult, C., Thierry-Mieg, N., Ray, P.F., 2021. From azoospermia to macrozoospermia, a phenotypic continuum due to mutations in the ZMYND15 gene. Asian J. Androl. 24, 243-247.
[11]	Kim, J., Ishiguro, K., Nambu, A., Akiyoshi, B., Yokobayashi, S., Kagami, A., Ishiguro, T., Pendas, A.M., Takeda, N., Sakakibara, Y., et al., 2015. Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature 517, E23.
[12]	Kimmins, S., Crosio, C., Kotaja, N., Hirayama, J., Monaco, L., Hoog, C., van Duin, M., Gossen, J.A., Sassone-Corsi, P., 2007. Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol. Endocrinol. 21, 726-739.
[13]	Kobesiy, M.M., Foda, B.M., Ali, O.S.M., Fahmy, I., Ismail, S.M., 2020. Mutational analysis of Aurora kinase C gene in Egyptian patients with macrozoospermia. Andrologia 52, e13619.
[14]	Krausz, C., Riera-Escamilla, A., Moreno-Mendoza, D., Holleman, K., Cioppi, F., Algaba, F., Pybus, M., Friedrich, C., Wyrwoll, M.J., Casamonti, E., et al., 2021. Genetic dissection of spermatogenic arrest through exome analysis: clinical implications for the management of azoospermic men. Genet. Med. 22, 1956-1966.
[15]	Lou, Z., Minter-Dykhouse, K., Franco, S., Gostissa, M., Rivera, M.A., Celeste, A., Manis, J.P., van Deursen, J., Nussenzweig, A., Paull, T.T., et al., 2006. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell, 2006 187-200.
[16]	Miyazaki, S., Kim, J., Sakuno, T., Watanabe, Y., 2017. Hierarchical regulation of centromeric cohesion protection by meikin and shugoshin during meiosis I. Cold Spring Harb. Symp. Quant. Biol. 82, 259-266.
[17]	Oud, M.S., Houston, B.J., Volozonoka, L., Mastrorosa, F.K., Holt, G.S., Alobaidi, B.K.S., Mclachlan, R.I., O'Bryan, M.K., Veltman, J.A., Chemes, H.E., et al., 2021. Exome sequencing reveals variants in known and novel candidate genes for severe sperm motility disorders. Hum. Reprod. 36, 2597-2611.
[18]	Ray, P.F., Toure, A., Metzler-Guillemain, C., Mitchell, M.J., Arnoult, C., Coutton, C., 2017. Genetic abnormalities leading to qualitative defects of sperm morphology or function. Clin. Genet. 91, 217-232.
[19]	Snyder, E., Chukrallah, L.G., Seltzer, K., Goodwin, L., Braun, R.E., 2020. ADAD1 and ADAD2, testis-specific adenosine deaminase domain-containing proteins, are required for male fertility. Sci. Rep. 10, 11536.
[20]	Wellard, S.R., Schindler, K., Jordan, P.W., 2020. Aurora B and C kinases regulate chromosome desynapsis and segregation during mouse and human spermatogenesis. J. Cell Sci. 133, jcs248831.