Meiotic Heterogeneity of Trivalent Structure and Interchromosomal Effect in Blastocysts With Robertsonian Translocations

Overview

Journal Front Genet

Date 2021 Mar 8

PMID 33679881

Citations 5

Authors

Shuo Zhang

Caixia Lei

Junping Wu

Jing Zhou

Min Xiao

Saijuan Zhu

Yanping Xi

Jing Fu

Yijuan Sun

Congjian Xu

Xiaoxi Sun

Affiliations

Soon will be listed here.

Abstract

Background: Robertsonian translocations are common structural rearrangements and confer an increased genetic reproductive risk due to the formation of trivalent structure during meiosis. Studies on trivalent structure show meiotic heterogeneity between different translocation carriers, although the factors causing heterogeneity have not been well elaborated in blastocysts. It is also not yet known whether interchromosomal effect (ICE) phenomenon occurs in comparison with suitable non-translocation control patients. Herein, we aimed to evaluate the factors that cause meiotic heterogeneity of trivalent structure and the ICE phenomenon.

Methods: We designed a retrospective study, comprising 217 Robertsonian translocation carriers and 134 patients with the risk of transmitting monogenic inherited disorders (RTMIDs) that underwent preimplantation genetic testing (PGT). Data was collected between March 2014 and December 2019. The segregation products of trivalent structure were analyzed based on the carrier's gender, age and translocation type. In addition, to analyze ICE phenomenon, aneuploidy abnormalities of non-translocation chromosomes from Robertsonian translocation carriers were compared with those from patients with RTMIDs.

Results: We found that the percentage of male carriers with alternate segregation pattern was significantly higher [ < 0.001, odds ratio (OR) = 2.95] than that in female carriers, while the percentage of adjacent segregation pattern was lower ( < 0.001, OR = 0.33). By contrast, no difference was observed between young and older carriers when performing stratified analysis by age. Furthermore, segregation pattern was associated with the D;G chromosomes involved in Robertsonian translocation: the rate of alternate segregation pattern in Rob(13;14) carriers was significantly higher ( = 0.010, OR = 1.74) than that in Rob(14;21) carriers, whereas the rate of adjacent segregation pattern was lower ( = 0.032, OR = 0.63). Moreover, the results revealed that the trivalent structure could significantly increase the frequencies of chromosome aneuploidies 1.30 times in Robertsonian translocation carriers compared with patients with RTMIDs ( = 0.026), especially for the male and young subgroups ( = 0.030, OR = 1.35 and = 0.012, OR = 1.40), while the mosaic aneuploidy abnormalities presented no statistical difference.

Conclusions: Our study demonstrated that meiotic segregation heterogeneity of trivalent structure is associated with the carrier's gender and translocation type, and it is independent of carrier's age. ICE phenomenon exists during meiosis and then increases the frequencies of additional chromosome abnormalities.

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References

Wang J, Zeng Y, Ding C, Cai B, Lu B, Li R . Preimplantation genetic testing of Robertsonian translocation by SNP array-based preimplantation genetic haplotyping. Prenat Diagn. 2018; . DOI: 10.1002/pd.5258. View

Ko D, Cho J, Lee H, Kim J, Kang I, Yang K . Preimplantation genetic diagnosis outcomes and meiotic segregation analysis of robertsonian translocation carriers. Fertil Steril. 2013; 99(5):1369-76. DOI: 10.1016/j.fertnstert.2012.12.010. View

Gianaroli L, Magli M, Ferraretti A, Munne S, Balicchia B, Escudero T . Possible interchromosomal effect in embryos generated by gametes from translocation carriers. Hum Reprod. 2002; 17(12):3201-7. DOI: 10.1093/humrep/17.12.3201. View

Godo A, Blanco J, Vidal F, Sandalinas M, Garcia-Guixe E, Anton E . Altered segregation pattern and numerical chromosome abnormalities interrelate in spermatozoa from Robertsonian translocation carriers. Reprod Biomed Online. 2015; 31(1):79-88. DOI: 10.1016/j.rbmo.2015.04.003. View

Ghevaria H, SenGupta S, Shmitova N, Serhal P, Delhanty J . The origin and significance of additional aneuploidy events in couples undergoing preimplantation genetic diagnosis for translocations by array comparative genomic hybridization. Reprod Biomed Online. 2016; 32(2):178-89. DOI: 10.1016/j.rbmo.2015.11.017. View

Scriven P, Handyside A, Ogilvie C . Chromosome translocations: segregation modes and strategies for preimplantation genetic diagnosis. Prenat Diagn. 1999; 18(13):1437-49. View

Zhang L, Jiang W, Zhu Y, Chen H, Yan J, Chen Z . Effects of a carrier's sex and age on the segregation patterns of the trivalent of Robertsonian translocations. J Assist Reprod Genet. 2019; 36(9):1963-1969. PMC: 6730718. DOI: 10.1007/s10815-019-01534-6. View

Xie Y, Xu Y, Wang J, Miao B, Zeng Y, Ding C . Preliminary analysis of numerical chromosome abnormalities in reciprocal and Robertsonian translocation preimplantation genetic diagnosis cases with 24-chromosomal analysis with an aCGH/SNP microarray. J Assist Reprod Genet. 2017; 35(1):177-186. PMC: 5758468. DOI: 10.1007/s10815-017-1045-9. View

Anton E, Blanco J, Vidal F . Meiotic behavior of three D;G Robertsonian translocations: segregation and interchromosomal effect. J Hum Genet. 2010; 55(8):541-5. DOI: 10.1038/jhg.2010.67. View

10.

Wiland E, Olszewska M, Wozniak T, Kurpisz M . How much, if anything, do we know about sperm chromosomes of Robertsonian translocation carriers?. Cell Mol Life Sci. 2020; 77(23):4765-4785. PMC: 7658086. DOI: 10.1007/s00018-020-03560-5. View

11.

Wang B, Nie B, Tang D, Li R, Liu X, Song J . Analysis of Meiotic Segregation Patterns and Interchromosomal Effects in Sperm from 13 Robertsonian Translocations. Balkan J Med Genet. 2017; 20(1):43-50. PMC: 5596821. DOI: 10.1515/bjmg-2017-0003. View

12.

Bernicot I, Schneider A, Mace A, Hamamah S, Hedon B, Pellestor F . Analysis using fish of sperm and embryos from two carriers of rare rob(13;21) and rob(15;22) robertsonian translocation undergoing PGD. Eur J Med Genet. 2012; 55(4):245-51. DOI: 10.1016/j.ejmg.2012.02.003. View

13.

Zhang S, Zhao D, Zhang J, Mao Y, Kong L, Zhang Y . BasePhasing: a highly efficient approach for preimplantation genetic haplotyping in clinical application of balanced translocation carriers. BMC Med Genomics. 2019; 12(1):52. PMC: 6423798. DOI: 10.1186/s12920-019-0495-6. View

14.

Rodriguez-Purata J, Lee J, Whitehouse M, Moschini R, Knopman J, Duke M . Embryo selection versus natural selection: how do outcomes of comprehensive chromosome screening of blastocysts compare with the analysis of products of conception from early pregnancy loss (dilation and curettage) among an assisted reproductive.... Fertil Steril. 2015; 104(6):1460-66.e1-12. DOI: 10.1016/j.fertnstert.2015.08.007. View

15.

Deleye L, Dheedene A, De Coninck D, Sante T, Christodoulou C, Heindryckx B . Shallow whole genome sequencing is well suited for the detection of chromosomal aberrations in human blastocysts. Fertil Steril. 2015; 104(5):1276-85.e1. DOI: 10.1016/j.fertnstert.2015.07.1144. View

16.

Tulay P, Gultomruk M, Findikli N, Yagmur E, Bahceci M . Is the interchromosomal effect present in embryos derived from Robertsonian and reciprocal translocation carriers particularly focusing on chromosome 10 rearrangements?. Zygote. 2014; 23(6):908-15. DOI: 10.1017/S0967199414000628. View

17.

Munne S, Cohen J . Advanced maternal age patients benefit from preimplantation genetic diagnosis of aneuploidy. Fertil Steril. 2017; 107(5):1145-1146. DOI: 10.1016/j.fertnstert.2017.03.015. View

18.

Hajlaoui A, Slimani W, Kammoun M, Sallem A, Braham S, Bibi M . Sperm fluorescent in situ hybridisation study of interchromosomal effect in six Tunisian carriers of reciprocal and Robertsonian translocations. Andrologia. 2018; . DOI: 10.1111/and.12949. View

19.

Wang J, Li D, Xu Z, Diao Z, Zhou J, Lin F . Analysis of meiotic segregation modes in biopsied blastocysts from preimplantation genetic testing cycles of reciprocal translocations. Mol Cytogenet. 2019; 12:11. PMC: 6390622. DOI: 10.1186/s13039-019-0423-7. View

20.

Zhang L, Wei D, Zhu Y, Gao Y, Yan J, Chen Z . Rates of live birth after mosaic embryo transfer compared with euploid embryo transfer. J Assist Reprod Genet. 2018; 36(1):165-172. PMC: 6338591. DOI: 10.1007/s10815-018-1322-2. View