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Balanced chromosomal translocations in men: relationships among semen parameters, chromatin integrity, sperm meiotic segregation and aneuploidy

  • Genetics
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Abstract

Purpose

To analyse relationships between semen parameters, sperm chromatin integrity and frequencies of chromosomally unbalanced, disomic and diploid sperm in 13 Robertsonian and 37 reciprocal translocation carriers and to compare the results with data from 10 control donors.

Methods

Conventional semen analysis, Sperm Chromatin Structure Assay and FISH with probes for chromosomes involved in the individual translocations and for chromosomes X, Y, 7, 8, 13, 18 and 21.

Results

Normal semen parameters were found in 30.8 % of Robertsonian and 59.5 % of reciprocal translocation carriers. The rates of unbalanced sperm were 12.0 % in Robertsonian and 55.1 % in reciprocal translocation carriers with no difference between normospermic patients and those showing altered semen parameters. Significantly increased frequencies of spermatozoa showing defects in chromatin integrity and condensation, aneuploidy for chromosomes not involved in a translocation and diploidy were detected in translocation carriers with abnormal semen parameters. Normospermic reciprocal translocation carriers showed an increase in chromosome 13 disomy compared to the control group. There was no relationship between gametic and somatic aneuploidy in 12 translocation carriers studied by FISH on sperm and lymphocytes. The frequency of motile sperm was negatively correlated with the frequency of sperm showing disomy, diploidy and defective chromatin condensation.

Conclusions

Abnormal semen parameters can serve as indicators of an additional risk of forming spermatozoa with defective chromatin and aneuploidy in translocation carriers.

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References

  1. Anton E, Vidal F, Blanco J. Interchromosomal effect analyses by sperm FISH: incidence and distribution among reorganization carriers. Syst Biol Reprod Med. 2011;57:268–78.

    Article  PubMed  CAS  Google Scholar 

  2. Aston KI, Carrell DT. Emerging evidence for the role of genomic instability in male factor infertility. Syst Biol Reprod Med. 2012;58:71–80.

    Article  PubMed  CAS  Google Scholar 

  3. Benet J, Oliver-Bonet M, Cifuentes P, Templado C, Navarro J. Segregation of chromosomes in sperm of reciprocal translocation carriers: a review. Cytogenet Genome Res. 2005;111:281–90.

    Article  PubMed  CAS  Google Scholar 

  4. Blanco J, Egozcue J, Vidal F. Interchromosomal effects for chromosome 21 in carriers of structural chromosome reorganizations determined by fluorescence in situ hybridization on sperm nuclei. Hum Genet. 2000;106:500–5.

    Article  PubMed  CAS  Google Scholar 

  5. Brugnon F, Van Assche E, Verheyen G, Sion B, Boucher D, Pouly JL, Janny L, Devroey P, Liebaers I, Van Steirteghem A. Study of two markers of apoptosis and meiotic segregation in ejaculated sperm of chromosomal translocation carrier patients. Hum Reprod. 2006;21:685–93.

    Article  PubMed  CAS  Google Scholar 

  6. Bungum M, Humaidan P, Spano M, Jepson K, Bungum L, Giwercman A. The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod. 2004;19:1401–8.

    Article  PubMed  CAS  Google Scholar 

  7. Cans C, Cohen O, Lavergne C, Mermet MA, Demongeot J, Jalbert P. Logistic regression model to estimate the risk of unbalanced offspring in reciprocal translocations. Hum Genet. 1993;92:598–604.

    Article  PubMed  CAS  Google Scholar 

  8. Cassuto NG, Le Foll N, Chantot-Bastaraud S, Balet R, Bouret D, Rouen A, Bhouri R, Hyon C, Siffroi JP. Sperm fluorescence in situ hybridization study in nine men carrying a Robertsonian or a reciprocal translocation: relationship between segregation modes and high-magnification sperm morphology examination. Fertil Steril. 2011;96:826–32.

    Article  PubMed  Google Scholar 

  9. De Braekeleer M, Dao TN. Cytogenetic studies in male infertility: a review. Hum Reprod. 1991;6:245–50.

    PubMed  Google Scholar 

  10. De Palma A, Burrello N, Barone N, D'Agata R, Vicari E, Calogero AE. Patients with abnormal sperm parameters have an increased sex chromosome aneuploidy rate in peripheral leukocytes. Hum Reprod. 2005;20:2153–6.

    Article  PubMed  Google Scholar 

  11. Dohle GR, Halley DJ, Van Hemel JO, van den Ouwel AM, Pieters MH, Weber RF, Govaerts LC. Genetic risk factors in infertile men with severe oligozoospermia and azoospermia. Hum Reprod. 2002;17:13–6.

    Article  PubMed  CAS  Google Scholar 

  12. Douet-Guilbert N, Bris MJ, Amice V, Marchetti C, Delobel B, Amice J, Braekeleer MD, Morel F. Interchromosomal effect in sperm of males with translocations: report of 6 cases and review of the literature. Int J Androl. 2005;28:372–9.

    Article  PubMed  CAS  Google Scholar 

  13. Escudero T, Abdelhadi I, Sandalinas M, Munne S. Predictive value of sperm fluorescence in situ hybridization analysis on the outcome of preimplantation genetic diagnosis for translocations. Fertil Steril. 2003;79 Suppl 3:1528–34.

    Article  PubMed  Google Scholar 

  14. Evenson D, Wixon R. Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod Biomed Online. 2006;12:466–72.

    Article  PubMed  CAS  Google Scholar 

  15. Faraut T, Mermet MA, Demongeot J, Cohen O. Cooperation of selection and meiotic mechanisms in the production of imbalances in reciprocal translocations. Cytogenet Cell Genet. 2000;88:15–21.

    Article  PubMed  CAS  Google Scholar 

  16. Ferfouri F, Selva J, Boitrelle F, Gomes DM, Torre A, Albert M, Bailly M, Clement P, Vialard F. The chromosomal risk in sperm from heterozygous Robertsonian translocation carriers is related to the sperm count and the translocation type. Fertil Steril. 2011;96:1337–43.

    Article  PubMed  Google Scholar 

  17. Fiorentino F, Spizzichino L, Bono S, Biricik A, Kokkali G, Rienzi L, Ubaldi FM, Iammarrone E, Gordon A, Pantos K. PGD for reciprocal and Robertsonian translocations using array comparative genomic hybridization. Hum Reprod. 2011;26:1925–35.

    Article  PubMed  CAS  Google Scholar 

  18. Gazvani MR, Wilson ED, Richmond DH, Howard PJ, Kingsland CR, Lewis-Jones DI. Role of mitotic control in spermatogenesis. Fertil Steril. 2000;74:251–6.

    Article  PubMed  CAS  Google Scholar 

  19. Gianaroli L, Magli MC, Ferraretti AP, Munné S, Balicchia B, Escudero T, Crippa A. Possible interchromosomal effect in embryos generated by gametes from translocation carriers. Hum Reprod. 2002;17:3201–7.

    Article  PubMed  CAS  Google Scholar 

  20. Kennedy C, Ahlering P, Rodriguez H, Levy S, Sutovsky P. Sperm chromatin structure correlates with spontaneous abortion and multiple pregnancy rates in assisted reproduction. Reprod Biomed Online. 2011;22:272–6.

    Article  PubMed  CAS  Google Scholar 

  21. Kirkpatrick G, Ferguson KA, Gao H, Tang S, Chow V, Yuen BH, Ma S. A comparison of sperm aneuploidy rates between infertile men with normal and abnormal karyotypes. Hum Reprod. 2008;23:1679–83.

    Article  PubMed  Google Scholar 

  22. Larson-Cook KL, Brannian JD, Hansen KA, Kasperson KM, Aamold ET, Evenson DP. Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertil Steril. 2003;80:895–902.

    Article  PubMed  Google Scholar 

  23. Machev N, Gosset P, Warter S, Treger M, Schillinger M, Viville S. Fluorescence in situ hybridization sperm analysis of six translocation carriers provides evidence of an interchromosomal effect. Fertil Steril. 2005;84:365–73.

    Article  PubMed  CAS  Google Scholar 

  24. Manvelyan M, Hunstig F, Bhatt S, Mrasek K, Pellestor F, Weise A, Simonyan I, Aroutiounian R, Liehr T. Chromosome distribution in human sperm—a 3D multicolor banding-study. Mol Cytogenet. 2008;1:25.

    Article  PubMed  Google Scholar 

  25. Martin RH. Cytogenetic determinants of male fertility. Hum Reprod Update. 2008;14:379–90.

    Article  PubMed  CAS  Google Scholar 

  26. Morel F, Douet-Guilbert N, Le Bris MJ, Amice V, Le Martelot MT, Roche S, Valéri A, Derrien V, Amice J, De Braekeleer M. Chromosomal abnormalities in couples undergoing intracytoplasmic sperm injection. A study of 370 couples and review of the literature. Int J Androl. 2004;27:178–82.

    Article  PubMed  CAS  Google Scholar 

  27. Morel F, Douet-Guilbert N, Le Bris MJ, Herry A, Amice V, Amice J, De Braekeleer M. Meiotic segregation of translocations during male gametogenesis. Int J Androl. 2004;27:200–12.

    Article  PubMed  Google Scholar 

  28. Munné S. Analysis of chromosome segregation during preimplantation genetic diagnosis in both male and female translocation heterozygotes. Cytogenet Genome Res. 2005;111:305–9.

    Article  PubMed  Google Scholar 

  29. Navarro J, Vidal F, Benet J, Templado C, Marina S, Egozcue J. XY-trivalent association and synaptic anomalies in a male carrier of a Robertsonian t(13;14) translocation. Hum Reprod. 1991;6:376–81.

    PubMed  CAS  Google Scholar 

  30. Nicopoullos JD, Gilling-Smith C, Almeida PA, Homa S, Nice L, Tempest H, Ramsay JW. The role of sperm aneuploidy as a predictor of the success of intracytoplasmic sperm injection? Hum Reprod. 2008;23:240–50.

    Article  PubMed  CAS  Google Scholar 

  31. Nielsen J, Wohlert M. Chromosome abnormalities found among 34,910 newborn children: results from a 13-year incidence study in Arhus, Denmark. Hum Genet. 1991;87:81–3.

    Article  PubMed  CAS  Google Scholar 

  32. Oliver-Bonet M, Benet J, Sun F, Navarro J, Abad C, Liehr T, Starke H, Greene C, Ko E, Martin RH. Meiotic studies in two human reciprocal translocations and their association with spermatogenic failure. Hum Reprod. 2005;20:683–8.

    Article  PubMed  CAS  Google Scholar 

  33. Pellestor F, Imbert I, Andréo B, Lefort G. Study of the occurrence of interchromosomal effect in spermatozoa of chromosomal rearrangement carriers by fluorescence in-situ hybridization and primed in-situ labelling techniques. Hum Reprod. 2001;16:1155–64.

    Article  PubMed  CAS  Google Scholar 

  34. Perrin A, Caer E, Oliver-Bonet M, Navarro J, Benet J, Amice V, De Braekeleer M, Morel F. DNA fragmentation and meiotic segregation in sperm of carriers of a chromosomal structural abnormality. Fertil Steril. 2009;92:583–9.

    Article  PubMed  Google Scholar 

  35. Pujol A, Benet J, Staessen C, Van Assche E, Campillo M, Egozcue J, Navarro J. The importance of aneuploidy screening in reciprocal translocation carriers. Reproduction. 2006;131:1025–35.

    Article  PubMed  CAS  Google Scholar 

  36. Rius M, Obradors A, Daina G, Ramos L, Pujol A, Martínez-Passarell O, Marquès L, Oliver-Bonet M, Benet J, Navarro J. Detection of unbalanced chromosome segregations in preimplantation genetic diagnosis of translocations by short comparative genomic hibridization. Fertil Steril. 2011;96:134–42.

    Article  PubMed  CAS  Google Scholar 

  37. Robbins WA, Segraves R, Pinkel D, Wyrobek AJ. Detection of aneuploid human sperm by fluorescence in situ hybridization–evidence for a donor difference in frequency of sperm disomic for chromosomes-I and chromosomes-Y. Am J Hum Genet. 1993;52:799–807.

    PubMed  CAS  Google Scholar 

  38. Roux C, Tripogney C, Morel F, Joanne C, Fellmann F, Clavequin MC, Bresson JL. Segregation of chromosomes in sperm of Robertsonian translocation carriers. Cytogenet Genome Res. 2005;111:291–6.

    Article  PubMed  CAS  Google Scholar 

  39. Rubes J, Vozdova M, Robbins WA, Rezacova O, Perreault SD, Wyrobek AJ. Stable variants of sperm aneuploidy among healthy men show associations between germinal and somatic aneuploidy. Am J Hum Genet. 2002;70:1507–19.

    Article  PubMed  CAS  Google Scholar 

  40. Rubes J, Vozdova M, Oracova E, Perreault SD. Individual variation in the frequency of sperm aneuploidy in humans. Cytogenet Genome Res. 2005;111:229–36.

    Article  PubMed  CAS  Google Scholar 

  41. Rubio C, Gil-Salom M, Simón C, Vidal F, Rodrigo L, Mínguez Y, Remohí J, Pellicer A. Incidence of sperm chromosomal abnormalities in a risk population: relationship with sperm quality and ICSI outcome. Hum Reprod. 2001;16:2084–92.

    Article  PubMed  CAS  Google Scholar 

  42. Rybar R, Markova P, Veznik Z, Faldikova L, Kunetkova M, Zajicova A, Kopecka V, Rubes J. Sperm chromatin integrity in young men with no experiences of infertility and men from idiopathic infertility couples. Andrologia. 2009;41:141–9.

    Article  PubMed  CAS  Google Scholar 

  43. Sciurano RB, Rahn MI, Rey-Valzacchi G, Coco R, Solari AJ. The role of asynapsis in human spermatocyte failure. Int J Androl. 2012;35:541–9.

    Article  PubMed  CAS  Google Scholar 

  44. Sills ES, Fryman JT, Perloe M, Michels KB, Tucker MJ. Chromatin fluorescence characteristics and standard semen analysis parameters: correlations observed in andrology testing among 136 males referred for infertility evaluation. J Obstet Gynaecol. 2004;24:74–7.

    Article  PubMed  Google Scholar 

  45. Stern C, Pertile M, Norris H, Hale L, Baker HW. Chromosome translocations in couples with in-vitro fertilization implantation failure. Hum Reprod. 1999;14:2097–101.

    Article  PubMed  CAS  Google Scholar 

  46. Templado C, Bosch M, Benet J. Frequency and distribution of chromosome abnormalities in human spermatozoa. Cytogenet Genome Res. 2005;111:199–205.

    Article  PubMed  CAS  Google Scholar 

  47. Vegetti W, Van Assche E, Frias A, Verheyen G, Bianchi MM, Bonduelle M, Liebaers I, Van Steirteghem A. Correlation between semen parameters and sperm aneuploidy rates investigated by fluorescence in-situ hybridization in infertile men. Hum Reprod. 2000;15:351–65.

    Article  PubMed  CAS  Google Scholar 

  48. Vincent MC, Daudin M, De MP, Massat G, Mieusset R, Pontonnier F, Calvas P, Bujan L, Bourrouillout G. Cytogenetic investigations of infertile men with low sperm counts: a 25-year experience. J Androl. 2002;23:18–22.

    PubMed  Google Scholar 

  49. Virro MR, Larson-Cook KL, Evenson DP. Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril. 2004;81:1289–95.

    Article  PubMed  Google Scholar 

  50. Vozdova M, Oracova E, Horinova V, Rubes J. Sperm fluorescence in situ hybridization study of meiotic segregation and an interchromosomal effect in carriers of t(11;18). Hum Reprod. 2008;23:581–8.

    Article  PubMed  CAS  Google Scholar 

  51. Vozdova M, Oracova E, Gaillyova R, Rubes J. Sperm meiotic segregation and aneuploidy in a 46,X,inv(Y),t(10;15) carrier: case report. Fertil Steril. 2009;92:1748.e9–1748.e13.

    Article  Google Scholar 

  52. Vozdova M, Oracova E, Musilova P, Kasikova K, Prinosilova P, Gaillyova R, Rubes J. Sperm and embryo analysis of similar t(7;10) translocations transmitted in two families. Fertil Steril. 2011;96:e66–70.

    Article  PubMed  Google Scholar 

  53. Vozdova M, Kasikova K, Oracova E, Prinosilova P, Rybar R, Horinova V, Gaillyova R, Rubes J. The effect of the swim-up and hyaluronan-binding methods on the frequency of abnormal spermatozoa detected by FISH and SCSA in carriers of balanced chromosomal translocations. Hum Reprod. 2012;27:930–7.

    Article  PubMed  CAS  Google Scholar 

  54. Wiland E, Midro AT, Panasiuk B, Kurpisz M. The analysis of meiotic segregation patterns and aneuploidy in the spermatozoa of father and son with translocation t(4;5)(p15.1;p12) and the prediction of the individual probability rate for unbalanced progeny at birth. J Androl. 2007;28:262–72.

    Article  PubMed  Google Scholar 

  55. Wiland E, Zegało M, Kurpisz M. Interindividual differences and alterations in the topology of chromosomes in human sperm nuclei of fertile donors and carriers of reciprocal translocations. Chromosome Res. 2008;16:291–305.

    Article  PubMed  CAS  Google Scholar 

  56. World Health Organization (1999) WHO laboratory manual for the examination of human semen and semen-cervical mucus interaction, 4th edn. Cambridge University Press, Cambridge, UK. ISBN 9780521645997

  57. World Health Organization (2010) WHO laboratory manual for the examination and processing of human semen, 5th edn. World Health Organization, Geneva, Switzerland. ISBN 978 92 4 154778 9

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Acknowledgments

We are grateful to the patients for their participation in the study. We wish to thank Mr. Paul Veater (Bristol, United Kingdom) for proofreading the translated manuscript. Supported by the Grant Agency of the Czech Ministry of Health, grant No. NS9842-4/2008 and CEITEC–Central European Institute of Technology (ED1.1.00/02.0068) from the European Regional Development Fund.

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Authors and Affiliations

  1. Department of Genetics and Reproduction, Veterinary Research Institute, Hudcova 70, 621 00, Brno, Czech Republic

    Miluse Vozdova, Eva Oracova, Petra Prinosilova, Roman Rybar & Jiri Rubes

  2. Sanatorium Repromeda, 615 00, Brno, Czech Republic

    Eva Oracova & Jiri Rubes

  3. Department of Medical Genetics, University Hospital Brno, 625 00, Brno, Czech Republic

    Katerina Kasikova & Renata Gaillyova

  4. Department of Preventive Medicine, Faculty of Medicine, Masaryk University, 602 00, Brno, Czech Republic

    Katerina Kasikova

  5. Sanatorium Helios SIVF, 602 00, Brno, Czech Republic

    Vera Horinova

  6. Biological Institute, Faculty of Medicine, Masaryk University, 602 00, Brno, Czech Republic

    Renata Gaillyova

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  1. Miluse Vozdova
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  2. Eva Oracova
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  3. Katerina Kasikova
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  4. Petra Prinosilova
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  5. Roman Rybar
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  6. Vera Horinova
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  7. Renata Gaillyova
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  8. Jiri Rubes
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Corresponding author

Correspondence to Miluse Vozdova.

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Capsule

Translocation carriers showing abnormal semen parameters are at increased risk of forming gametes with additional numerical chromosomal aberrations and defective chromatin condensation.

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Vozdova, M., Oracova, E., Kasikova, K. et al. Balanced chromosomal translocations in men: relationships among semen parameters, chromatin integrity, sperm meiotic segregation and aneuploidy. J Assist Reprod Genet 30, 391–405 (2013). https://doi.org/10.1007/s10815-012-9921-9

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  • DOI: https://doi.org/10.1007/s10815-012-9921-9

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