Genetic factors of early embryo developmental arrest in in vitro fertilization programs

1. Корсак В.С., Смирнова А.А., Шурыгина О.В. Регистр ВРТ Общероссийской общественной организации «Российская Ассоциация Репродукции Человека». Отчет за 2021 год. Проблемы репродукции. 2023; 29(6): 25-40. [Korsak V.S., Smirnova A.A., Shurygina O.V. ART Register of RAHR, 2021. Russian Journal of Human Reproduction. 2023; 29(6): 25-40. (in Russian)]. https://dx.doi.org/10.17116/repro20232906125.
2. Mohebi M., Ghafouri-Fard S. Embryo developmental arrest: Review of genetic factors and pathways. Gene Rep. 2019; 17:100479. https://dx.doi.org/10.1016/j.genrep.2019.100479.
3. ESHRE Special Interest Group of Embryology and Alpha Scientists in Reproductive Medicine. Electronic address: coticchio.biogenesi@grupposandonato.it. The Vienna consensus: report of an expert meeting on the development of ART laboratory performance indicators. Reprod. Biomed. Online. 2017; 35(5): 494-510. https://dx.doi.org/10.1016/j.rbmo.2017.06.015.
4. Sfakianoudis K., Maziotis E., Karantzali E., Kokkini G., Grigoriadis S., Pantou A. et al. Molecular drivers of developmental arrest in the human preimplantation embryo: A systematic review and critical analysis leading to mapping future research. Int. J. Mol. Sci. 2021; 22(15): 8353. https://dx.doi.org/10.3390/ijms22158353.
5. Alpha Scientists in Reproductive Medicine and ESHRE Special Interest Group of Embryology. The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum. Reprod. 2011; 26(6): 1270-83. https://dx.doi.org/10.1093/humrep/der037.
6. Cívico S., Agell N., Hernández L., Campo E., Bachs O., Balasch J. Increased messenger ribonucleic acid expression of the cyclin-dependent kinase inhibitor p27Kip1 in cleavage-stage human embryos exhibiting developmental arrest. Fertil. Steril. 2008; 89(5 Suppl.): 1557-62. https://dx.doi.org/10.1016/j.fertnstert.2007.06.003.
7. La Salle S. Growing fast or slow: what makes the best embryo? Biol. Reprod. 2012; 86(5): 142, 1-2. https://dx.doi.org/10.1095/biolreprod.112.100289.
8. Weremowicz S., Sandstrom D.J., Morton C.C., Niedzwiecki C.A., Sandstrom M.M., Bieber F.R. Fluorescence in situ hybridization (FISH) for rapid detection of aneuploidy: experience in 911 prenatal cases. Prenat. Diagn. 2001; 21(4): 262-9. https://dx.doi.org/10.1002/pd.39.
9. Бейк Е.П., Коротченко О.Е., Гвоздева А.Д., Сыркашева А.Г., Долгушина Н.В. Роль преимплантационного генетического скрининга в повышении эффективности программ вспомогательных репродуктивных технологий у пациенток позднего репродуктивного возраста. Акушерство и гинекология. 2018; 4: 78-84. [Beik E.P., Korotchenko O.E., Gvozdeva A.D., Syrkasheva A.G., Dolgushina N.V. Role of preimplantation genetic screening in enhancing the effectiveness of assisted reproductive technology programs in late reproductive-aged patients. Obstetrics and Gynecology. 2018; (4): 78-84. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.4.78-84.
10. Checa M.A., Alonso-Coello P., Solà I., Robles A., Carreras R., Balasch J. IVF/ICSI with or without preimplantation genetic screening for aneuploidy in couples without genetic disorders: a systematic review and meta-analysis. J. Assist. Reprod. Genet. 2009; 26(5): 273-83. https://dx.doi.org/10.1007/s10815-009-9328-4.
11. Dahdouh E.M., Balayla J., Audibert F., Genetics Committee, Wilson R.D., Audibert F. et al. RETIRED: Technical Update: Preimplantation genetic diagnosis and screening. J. Obstet. Gynaecol. Can. 2015; 37(5): 451-63. https://dx.doi.org/10.1016/s1701-2163(15)30261-9.
12. Александрова Н.В., Шубина Е.С., Екимов А.Н., Кодылева Т.А., Мукосей И.С., Макарова Н.П., Кулакова Е.В., Левков Л.А., Барков И.Ю., Трофимов Д.Ю., Сухих Г.Т. Сравнительные результаты предимплантационного генетического скрининга с помощью array comparative genomic hybridization и секвенирования нового поколения. Молекулярная биология. 2017; 51(2): 308-13. [Aleksandrova N.V., Shubina E.S., Ekimov A.N., Kodyleva T.A., Mukosey I.S., Makarova N.P., Kulakova E.V., Levkov L.A., Barkov I.Y., Trofimov D.Y., Sukhikh G.T. Comparative results of preimplantation genetic screening by array comparative genomic hybridization and new-generation sequencing]. Mol. Biol. (Mosk). 2017; 51(2): 308-13. (in Russian)]. https://dx.doi.org/10.7868/S0026898417010025.
13. Wells D., Alfarawati S., Fragouli E. Use of comprehensive chromosomal screening for embryo assessment: microarrays and CGH. Mol. Hum. Reprod. 2008; 14(12): 703-10. https://dx.doi.org/10.1093/molehr/gan062.
14. Treff N.R., Thompson K., Rafizadeh M., Chow M., Morrison L., Tao X. et al. SNP array-based analyses of unbalanced embryos as a reference to distinguish between balanced translocation carrier and normal blastocysts. J. Assist. Reprod. Genet. 2016; 33(8): 1115-9. https://dx.doi.org/10.1007/s10815-016-0734-0.
15. Munné S., Kaplan B., Frattarelli J.L., Child T., Nakhuda G., Shamma F.N. et al. Preimplantation genetic testing for aneuploidy versus morphology as selection criteria for single frozen-thawed embryo transfer in good-prognosis patients: a multicenter randomized clinical trial. Fertil. Steril. 2019; 112(6): 1071-1079.e7. https://dx.doi.org/10.1016/j.fertnstert.2019.07.1346.
16. Pirtea P., De Ziegler D., Tao X., Sun L., Zhan Y., Ayoubi J.M. et al. Rate of true recurrent implantation failure is low: results of three successive frozen euploid single embryo transfers. Fertil. Steril. 2021; 115(1): 45-53. https://dx.doi.org/10.1016/j.fertnstert.2020.07.002.
17. Braude P., Bolton V., Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature. 1988; 332(6163): 459-61. https://dx.doi.org/10.1038/332459a0.
18. Xu Y., Shi Y., Fu J., Yu M., Feng R., Sang Q. et al. Mutations in PADI6 cause female infertility characterized by early embryonic arrest. Am. J. Hum. Genet. 2016; 99(3): 744-52. https://dx.doi.org/10.1016/j.ajhg.2016.06.024.
19. Zheng W., Hu H., Zhang S., Xu X., Gao Y., Gong F. et al. The comprehensive variant and phenotypic spectrum of TUBB8 in female infertility. J. Assist. Reprod. Genet. 2021; 38(9): 2261-72. https://dx.doi.org/10.1007/s10815-021-02219-9.
20. Jia Y., Li K., Zheng C., Tang Y., Bai D., Yin J. et al. Identification and rescue of a novel TUBB8 mutation that causes the first mitotic division defects and infertility. J. Assist. Reprod. Genet. 2020; 37(11): 2713-22. https://dx.doi.org/10.1007/s10815-020-01945-w.
21. Feng R., Sang Q., Kuang Y., Sun X., Yan Z., Zhang S. et al. Mutations in TUBB8 and human oocyte meiotic arrest. N. Engl. J. Med. 2016; 374(3): 223-32. https://dx.doi.org/10.1056/NEJMoa1510791.
22. Zhao L., Xue S., Yao Z., Shi J., Chen B., Wu L. et al. Biallelic mutations in CDC20 cause female infertility characterized by abnormalities in oocyte maturation and early embryonic development. Protein Cell. 2020; 11(12): 921-7. https://dx.doi.org/10.1007/s13238-020-00756-0.
23. Zhang Z., Li B., Fu J., Li R., Diao F., Li C. et al. Bi-allelic missense pathogenic variants in TRIP13 cause female infertility characterized by oocyte maturation arrest. Am. J. Hum. Genet. 2020; 107(1): 15-23. https://dx.doi.org/10.1016/j.ajhg.2020.05.001.
24. Hu H., Zhang S., Guo J., Meng F., Chen X., Gong F. et al. Identification of novel variants of thyroid hormone receptor interaction protein 13 that cause female infertility characterized by zygotic cleavage failure. Front. Physiol. 2022; 13: 899149. https://dx.doi.org/10.3389/fphys.2022.899149.
25. Zheng W., Zhou Z., Sha Q., Niu X., Sun X., Shi J. et al. Homozygous mutations in BTG4 cause zygotic cleavage failure and female infertility. Am. J. Hum. Genet. 2020; 107(1): 24-33. https://dx.doi.org/10.1016/j.ajhg.2020.05.010.
26. Wang X., Song D., Mykytenko D., Kuang Y., Lv Q., Li B. et al. Novel mutations in genes encoding subcortical maternal complex proteins may cause human embryonic developmental arrest. Reprod. Biomed. Online. 2018; 36(6):698-704. https://dx.doi.org/10.1016/j.rbmo.2018.03.009.
27. Tong X., Jin J., Hu Z., Zhang Y., Fan H.-Y., Zhang Y.-L. et al. Mutations in OOEP and NLRP5 identified in infertile patients with early embryonic arrest. Hum. Mutat. 2022; 43(12): 1909-20. https://dx.doi.org/10.1002/humu.24448.
28. World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen. 2010.
29. Nallella K.P., Sharma R.K., Aziz N., Agarwal A. Significance of sperm characteristics in the evaluation of male infertility. Fertil. Steril. 2006; 85(3): 629-34. https://dx.doi.org/10.1016/j.fertnstert.2005.08.024.
30. Perdrix A., Travers A., Chelli M.H., Escalier D., Do Rego J.L., Milazzo J.P. et al. Assessment of acrosome and nuclear abnormalities in human spermatozoa with large vacuoles. Hum. Reprod. 2011; 26(1): 47-58. https://dx.doi.org/10.1093/humrep/deq297.
31. Bichara C., Berby B., Rives A., Jumeau F., Letailleur M., Setif V. et al. Sperm chromatin condensation defects, but neither DNA fragmentation nor aneuploidy, are an independent predictor of clinical pregnancy after intracytoplasmic sperm injection. J. Assist. Reprod. Genet. 2019; 36(7):1387-99. https://dx.doi.org/10.1007/s10815-019-01471-4.
32. Desai N., AbdelHafez F., Sabanegh E., Goldfarb J. Paternal effect on genomic activation, clinical pregnancy and live birth rate after ICSI with cryopreserved epididymal versus testicular spermatozoa. Reprod. Biol. Endocrinol. 2009; 7: 142. https://dx.doi.org/10.1186/1477-7827-7-142.
33. Nanassy L., Carrell D.T. Paternal effects on early embryogenesis. J. Exp. Clin. Assist. Reprod. 2008; 5: 2. https://dx.doi.org/10.1186/1743-1050-5-2.
34. Desai N., Gill P., Tadros N.N., Goldberg J.M., Sabanegh E., Falcone T. Azoospermia and embryo morphokinetics: testicular sperm-derived embryos exhibit delays in early cell cycle events and increased arrest prior to compaction. J. Assist. Reprod. Genet. 2018; 35(7): 1339-48. https://dx.doi.org/10.1007/s10815-018-1183-8.
35. Sacha C.R., Dimitriadis I., Christou G., James K., Brock M.L., Rice S.T. et al. The impact of male factor infertility on early and late morphokinetic parameters: a retrospective analysis of 4126 time-lapse monitored embryos. Hum. Reprod. 2020; 35(1): 24-31. https://dx.doi.org/10.1093/humrep/dez251.
36. Neyer A., Zintz M., Stecher A., Bach M., Wirleitner B., Zech N.H. et al. The impact of paternal factors on cleavage stage and blastocyst development analyzed by time-lapse imaging-a retrospective observational study. J. Assist. Reprod. Genet. 2015; 32(11): 1607-14. https://dx.doi.org/10.1007/s10815-015-0558-3.
37. Wdowiak A., Bakalczuk S., Bakalczuk G. The effect of sperm DNA fragmentation on the dynamics of the embryonic development in intracytoplasmatic sperm injection. Reprod. Biol. 2015; 15(2): 94-100. https://dx.doi.org/10.1016/j.repbio.2015.03.003.
38. Mangoli E., Khalili M.A., Talebi A.R., Ghasemi-Esmailabad S., Hosseini A. Is there any correlation between sperm parameters and chromatin quality with embryo morphokinetics in patients with male infertility? Andrologia. 2018; 50(5): e12997. https://dx.doi.org/10.1111/and.12997.
39. Xin A., Qu R., Chen G., Zhang L., Chen J., Tao C. et al. Disruption in ACTL7A causes acrosomal ultrastructural defects in human and mouse sperm as a novel male factor inducing early embryonic arrest. Sci. Adv. 2020; 6(35): eaaz4796. https://dx.doi.org/10.1126/sciadv.aaz4796.
40. Wang J., Zhang J., Sun X., Lin Y., Cai L., Cui Y. et al. Novel bi-allelic variants in ACTL7A are associated with male infertility and total fertilization failure. Hum. Reprod. 2021; 36(12): 3161-9. https://dx.doi.org/10.1093/humrep/deab228.
41. Yang T.-Y., Chen Y., Chen G.-W., Sun Y.-S., Li Z.-C., Shen X.-R. et al. Sperm-specific protein ACTL7A as a biomarker for fertilization outcomes of assisted reproductive technology. Asian J. Androl. 2022; 24(3): 260-5. https://dx.doi.org/10.4103/aja2021111.
42. Lin Y., Huang Y., Li B., Zhang T., Niu Y., Hu S. et al. Novel mutations in PLCZ1 lead to early embryonic arrest as a male factor. Front. Cell. Dev. Biol. 2023; 11: 1193248. https://dx.doi.org/10.3389/fcell.2023.1193248.
43. Kashir J., Jones C., Lee H.C., Rietdorf K., Nikiforaki D., Durrans C. et al. Loss of activity mutations in phospholipase C zeta (PLCζ) abolishes calcium oscillatory ability of human recombinant protein in mouse oocytes. Hum. Reprod. 2011; 26(12): 3372-87. https://dx.doi.org/10.1093/humrep/der336.
44. Dai J., Dai C., Guo J., Zheng W., Zhang T., Li Y. et al. Novel homozygous variations in PLCZ1 lead to poor or failed fertilization characterized by abnormal localization patterns of PLCζ in sperm. Clin. Genet. 2020; 97(2): 347-51. https://dx.doi.org/10.1111/cge.13636.
45. Kashir J., Mistry B. V, BuSaleh L., Abu-Dawas R., Nomikos M., Ajlan A. et al. Phospholipase C zeta profiles are indicative of optimal sperm parameters and fertilisation success in patients undergoing fertility treatment. Andrology. 2020; 8(5): 1143-59. https://dx.doi.org/10.1111/andr.12796.
46. Yan Z., Fan Y., Wang F., Yan Z., Li M., Ouyang J. et al. Novel mutations in PLCZ1 cause male infertility due to fertilization failure or poor fertilization. Hum. Reprod. 2020; 35(2): 472-81. https://dx.doi.org/10.1093/humrep/dez282.
47. Wei Y., Wang J., Qu R., Zhang W., Tan Y., Sha Y. et al. Genetic mechanisms of fertilization failure and early embryonic arrest: a comprehensive review. Hum. Reprod. Update. 2024; 30(1): 48-80. https://dx.doi.org/10.1093/humupd/dmad026.
48. Mu J., Zhang Z., Wu L., Fu J., Chen B., Yan Z. et al. The identification of novel mutations in PLCZ1 responsible for human fertilization failure and a therapeutic intervention by artificial oocyte activation. Mol. Hum. Reprod. 2020; 26(2): 80-7. https://dx.doi.org/10.1093/molehr/gaaa003.
49. Betts D.H., Madan P. Permanent embryo arrest: molecular and cellular concepts. Mol. Hum. Reprod. 2008; 14(8): 445-53. https://dx.doi.org/10.1093/molehr/gan035.
50. Bamberger A., Sudahl S., Bamberger C.M., Schulte H.M., Löning T. Expression patterns of the cell-cycle inhibitor p27 and the cell-cycle promoter cyclin E in the human placenta throughout gestation: implications for the control of proliferation. Placenta. 1999; 20(5-6): 401-6. https://dx.doi.org/10.1053/plac.1999.0396.
51. Civico S., Agell N., Bachs O., Vanrell J.A., Balasch J. Increased expression of the cyclin-dependent kinase inhibitor p27 in cleavage-stage human embryos exhibiting developmental arrest. Mol. Hum. Reprod. 2002; 8(10): 919-22. https://dx.doi.org/10.1093/molehr/8.10.919.
52. Мартиросян Я.О., Назаренко Т.А., Кадаева А.И., Краснова В.Г., Бирюкова А.М., Погосян М.Т. Новые подходы к изучению регуляции преимплантационного развития эмбрионов. Акушерство и гинекология. 2023; 6: 29-37. [Martirosyan Ya.O., Nazarenko T.A., Kadaeva A.I., Krasnova V.G., Biryukova A.M., Pogosyan M.T. New approaches to studying the regulation of preimplantation embryonic development. Obstetrics and Gynecology. 2023; (6): 29-37. (in Russian)]. https://dx.doi.org/10.18565/aig.2023.10.
53. Magli M.C., Gianaroli L., Ferraretti A.P., Lappi M., Ruberti A., Farfalli V. Embryo morphology and development are dependent on the chromosomal complement. Fertil. Steril. 2007; 87(3): 534-41. https://dx.doi.org/10.1016/j.fertnstert.2006.07.1512.
54. Mantzouratou A., Delhanty J.D.A. Aneuploidy in the human cleavage stage embryo. Cytogenet. Genome Res. 2011; 133(2-4): 141-8. https://dx.doi.org/10.1159/000323794.
55. Munné S., Chen S., Colls P., Garrisi J., Zheng X., Cekleniak N. et al. Maternal age, morphology, development and chromosome abnormalities in over 6000 cleavage-stage embryos. Reprod. Biomed. Online. 2007; 14(5): 628-34. https://dx.doi.org/10.1016/s1472-6483(10)61057-7.
56. Rubio C., Simón C., Vidal F., Rodrigo L., Pehlivan T., Remohí J. et al. Chromosomal abnormalities and embryo development in recurrent miscarriage couples. Hum. Reprod. 2003; 18(1): 182-8. https://dx.doi.org/10.1093/humrep/deg015.
57. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007; 447(7143): 425-32. https://dx.doi.org/10.1038/nature05918.
58. Li X., Zhou W., Li X., Gao M., Ji S., Tian W. et al. SOX19b regulates the premature neuronal differentiation of neural stem cells through EZH2-mediated histone methylation in neural tube development of zebrafish. Stem. Cell. Res. Ther. 2019; 10(1): 389. https://dx.doi.org/10.1186/s13287-019-1495-3.
59. Swiercz R., Cheng D., Kim D., Bedford M.T. Ribosomal protein rpS2 is hypomethylated in PRMT3-deficient mice. J. Biol. Chem. 2007; 282(23): 16917-23. https://dx.doi.org/10.1074/jbc.M609778200.
60. Zhang W., Li S., Li K., Li L.I., Yin P., Tong G. The role of protein arginine methyltransferase 7 in human developmentally arrested embryos cultured in vitro. Acta Biochim. Biophys. Sin. (Shanghai). 2021; 53(7): 925-32. https://dx.doi.org/10.1093/abbs/gmab068.
61. Погосян М.Т., Назаренко Т.А., Гайсин Э.А. Анализ клинико-лабораторных характеристик пациенток с остановкой развития эмбрионов в раннем эмбриональном периоде программ экстракорпорального оплодотворения. Акушерство и гинекология. 2024; 2: 89-96. [Pogosyan M.T., Nazarenko T.A., Gaysin E.A. Clinical and laboratory characteristics of patients with embryonic arrest in the early embryonic period of in vitro fertilization programs. Obstetrics and Gynecology. 2024; (2): 89-96 (in Russian)]. https://dx.doi.org/10.18565/aig.2023.271.

Received 22.04.2024

Accepted 01.08.2024