Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Genome-wide analysis of sperm DNA methylation from monozygotic twin bulls

Habib A. Shojaei Saadi A B , Éric Fournier A B , Christian Vigneault C , Patrick Blondin C , Janice Bailey B and Claude Robert A B D
+ Author Affiliations
- Author Affiliations

A Laboratory of Functional Genomics of Early Embryonic Development, Institut sur la nutrition et les aliments fonctionnels, Faculté des sciences de l’agriculture et de l’alimentation, Pavillon des services, Université Laval, Québec G1V 0A6, Canada.

B Centre de recherche en biologie de la reproduction, Département des sciences animales, Faculté des sciences de l’agriculture et de l’alimentation, Université Laval, Québec G1V 0A6, Canada.

C Semex Alliance 130 Stone Road West, Guelph, Ontario N1G 3Z2, Canada.

D Corresponding author. Email: claude.robert@fsaa.ulaval.ca

Reproduction, Fertility and Development 29(4) 838-843 https://doi.org/10.1071/RD15384
Submitted: 1 August 2015  Accepted: 3 December 2015   Published: 12 January 2016

Abstract

Monozygotic (MZ) twins are of great interest to elucidate the contributions of pre- and postnatal environmental factors on epigenetics in the expression of complex traits and diseases. Progeny testing recently revealed that MZ twin bulls do not necessarily lead to identical genetic merit estimates (i.e. breeding values). Therefore, to explain differences in offspring productivity of MZ twin bulls despite their identical genetic backgrounds, we hypothesised that paternal sperm epigenomes vary between MZ twin bulls. In the present study, semen characteristics and global sperm DNA methylome were profiled for four pairs of MZ twin bulls. Some MZ twin pairs had divergent semen quality (sperm morphology, motility and viability). Comparative genome-wide DNA methylome surveys were performed using methyl-sensitive enrichment and microarray identification. Between 2% and 10% of all probes (400 000) were differentially methylated between MZ twin pairs. In addition, there were 580 loci differentially methylated across all pairs of MZ twins. Furthermore, enrichment analysis indicated a significant enrichment for fertility associated quantitative trait loci (P = 0.033). In conclusion, differences in the sperm epigenome may contribute to incongruous diverging performances of daughters sired by bulls that are MZ twins.

Additional keywords: quantitative trait loci, spermatozoa.


References

Bell, J. T., and Spector, T. D. (2011). A twin approach to unraveling epigenetics. Trends Genet. 27, 116–125.
A twin approach to unraveling epigenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsV2htr8%3D&md5=6cd74d868380f62e02f809ea87fa3b0bCAS | 21257220PubMed |

Braun, J., Schams, D., and Brem, G. (1990). [The reproductive function in experimentally-produced monozygotic twin bulls.] Berl. Munch. Tierarztl. Wochenschr. 103, 213–217.
| 1:STN:280:DyaK3czktlOitA%3D%3D&md5=be8949c844556161863207800b3d79d4CAS | 2383230PubMed |

Brenseke, B., Prater, M. R., Bahamonde, J., and Gutierrez, J. C. (2013). Current thoughts on maternal nutrition and fetal programming of the metabolic syndrome. J. Pregnancy 2013, Article ID 368461.
Current thoughts on maternal nutrition and fetal programming of the metabolic syndrome.Crossref | GoogleScholarGoogle Scholar |

Campagna, C., Guillemette, C., Ayotte, P., and Bailey, J. L. (2009). Effects of an environmentally relevant organochlorine mixture and a metabolized extract of this mixture on porcine sperm parameters in vitro. J. Androl. 30, 317–324.
Effects of an environmentally relevant organochlorine mixture and a metabolized extract of this mixture on porcine sperm parameters in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFOjtbc%3D&md5=61fe2ba0d348d4fe6f0b78de4ee732ebCAS | 19136392PubMed |

Chagas, L. M., Bass, J. J., Blache, D., Burke, C. R., Kay, J. K., Lindsay, D. R., Lucy, M. C., Martin, G. B., Meier, S., Rhodes, F. M., Roche, J. R., Thatcher, W. W., and Webb, R. (2007). Invited review: new perspectives on the roles of nutrition and metabolic priorities in the subfertility of high-producing dairy cows. J. Dairy Sci. 90, 4022–4032.
Invited review: new perspectives on the roles of nutrition and metabolic priorities in the subfertility of high-producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsleqtb0%3D&md5=66bd8cfe459206bec605f470053f51a0CAS | 17699018PubMed |

Czyz, W., Morahan, J., Ebers, G., and Ramagopalan, S. (2012). Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences. BMC Med. 10, 93.
Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences.Crossref | GoogleScholarGoogle Scholar | 22898292PubMed |

Dance, A., Thundathil, J., Wilde, R., Blondin, P., and Kastelic, J. (2015). Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls. J. Dairy Sci. 98, 987–998.
Enhanced early-life nutrition promotes hormone production and reproductive development in Holstein bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFKnu73P&md5=27012cdeeb2996fb3c97a51ef22f78d5CAS | 25497791PubMed |

Daxinger, L., and Whitelaw, E. (2012). Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 13, 153–162.
| 1:CAS:528:DC%2BC38XhsVOru7c%3D&md5=791224fb726eeb88c5ab60e20c00698aCAS | 22290458PubMed |

Evans, A. C., Mossa, F., Walsh, S. W., Scheetz, D., Jimenez-Krassel, F., Ireland, J. L., Smith, G. W., and Ireland, J. J. (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reprod. Domest. Anim. 47, 31–37.
Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring.Crossref | GoogleScholarGoogle Scholar | 22827347PubMed |

Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., Boix-Chornet, M., Sanchez-Aguilera, A., Ling, C., Carlsson, E., Poulsen, P., Vaag, A., Stephan, Z., Spector, T. D., Wu, Y.-Z., Plass, C., and Esteller, M. (2005). Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA 102, 10 604–10 609.
Epigenetic differences arise during the lifetime of monozygotic twins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVSiur0%3D&md5=4bb8164bad3e464b557a6a1eea69054cCAS |

Galli, A., Bornaghi, V., Previtali, C., Balduzzi, D., and Moretti, M. (1997). Brief communication: andrological study of two young identical twin bulls. Andrologia 29, 115–116.
Brief communication: andrological study of two young identical twin bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3ms1SrsA%3D%3D&md5=4b6f437bbd5ca6352a3a6d09394f959fCAS | 9111885PubMed |

Gaskins, A. J., Colaci, D. S., Mendiola, J., Swan, S. H., and Chavarro, J. E. (2012). Dietary patterns and semen quality in young men. Hum. Reprod. 27, 2899–2907.
Dietary patterns and semen quality in young men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlymsbfF&md5=9bfda91704f93f9e4b00b21928acc460CAS | 22888168PubMed |

Gluckman, P. D., Hanson, M. A., Cooper, C., and Thornburg, K. L. (2008). Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359, 61–73.
Effect of in utero and early-life conditions on adult health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotFSit7o%3D&md5=651aaeb2724a3b7990f326f486c0e439CAS | 18596274PubMed |

Heard, E., and Martienssen, R. A. (2014). Transgenerational epigenetic inheritance: myths and mechanisms. Cell 157, 95–109.
Transgenerational epigenetic inheritance: myths and mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtVCnurs%3D&md5=6e68c6b8a4cce63488cf47382428ad00CAS | 24679529PubMed |

Hogg, K., Wood, C., McNeilly, A. S., and Duncan, W. C. (2011). The in utero programming effect of increased maternal androgens and a direct fetal intervention on liver and metabolic function in adult sheep. PLoS One 6, e24877.
The in utero programming effect of increased maternal androgens and a direct fetal intervention on liver and metabolic function in adult sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Onu7fJ&md5=67f8b609aa7a6bad9381a3321c2aed25CAS | 21935484PubMed |

Kaminsky, Z. A., Tang, T., Wang, S.-C., Ptak, C., Oh, G. H. T., Wong, A. H. C., Feldcamp, L. A., Virtanen, C., Halfvarson, J., Tysk, C., McRae, A. F., Visscher, P. M., Montgomery, G. W., Gottesman, I. I., Martin, N. G., and Petronis, A. (2009). DNA methylation profiles in monozygotic and dizygotic twins. Nat. Genet. 41, 240–245.
DNA methylation profiles in monozygotic and dizygotic twins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGjtQ%3D%3D&md5=da774fb5537bdc8627f69eb80e704b94CAS | 19151718PubMed |

Lessard, C., Masseau, I., Bilodeau, J.-F., Kroetsch, T., Twagiramungu, H., Bailey, J. L., Leclerc, P., and Sullivan, R. (2003). Semen characteristics of genetically identical quadruplet bulls. Theriogenology 59, 1865–1877.
Semen characteristics of genetically identical quadruplet bulls.Crossref | GoogleScholarGoogle Scholar | 12566158PubMed |

Loke, Y. J., Novakovic, B., Ollikainen, M., Wallace, E. M., Umstad, M. P., Permezel, M., Morley, R., Ponsonby, A. L., Gordon, L., Galati, J. C., Saffery, R., and Craig, J. M. (2013). The Peri/postnatal Epigenetic Twins Study (PETS). Twin Res. Hum. Genet. 16, 13–20.
The Peri/postnatal Epigenetic Twins Study (PETS).Crossref | GoogleScholarGoogle Scholar | 23171547PubMed |

Ollikainen, M., Smith, K. R., Joo, E. J.-H., Ng, H. K., Andronikos, R., Novakovic, B., Abdul Aziz, N. K., Carlin, J. B., Morley, R., Saffery, R., and Craig, J. M. (2010). DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum. Mol. Genet. 19, 4176–4188.
DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1KqurnL&md5=59d9159b421576befd8f17ff0e836dd1CAS | 20699328PubMed |

Shojaei Saadi, H. A., and Robert, C. (2015). Modern reproductive technologies and breed improvement. In ‘The genetics of cattle’. 2nd edn. (Eds D. J. Garrick and A. Ruvinsky.) pp. 284–317. (Centre for Agriculture and Biosciences International (CABI) UK.)

Shojaei Saadi, H. A., van Riemsdijk, E., Dance, A. L., Rajamanickam, G. D., Kastelic, J. P., and Thundathil, J. C. (2013). Proteins associated with critical sperm functions and sperm head shape are differentially expressed in morphologically abnormal bovine sperm induced by scrotal insulation. J. Proteomics 82, 64–80.
Proteins associated with critical sperm functions and sperm head shape are differentially expressed in morphologically abnormal bovine sperm induced by scrotal insulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmslehurs%3D&md5=176e5d66d6e9618a816ee6c5e5a0de9cCAS | 23500133PubMed |

Shojaei Saadi, H. A., O’Doherty, A. M., Gagne, D., Fournier, E., Grant, J. R., Sirard, M.-A., and Robert, C. (2014). An integrated platform for bovine DNA methylome analysis suitable for small samples. BMC Genomics 15, 451.
An integrated platform for bovine DNA methylome analysis suitable for small samples.Crossref | GoogleScholarGoogle Scholar | 24912542PubMed |

Storgaard, L., Bonde, J. P., Ernst, E., Andersen, C. Y., Spanô, M., Christensen, K., Petersen, H. C., and Olsen, J. (2006). Genetic and environmental correlates of semen quality: a twin study. Epidemiology 17, 674–681.
Genetic and environmental correlates of semen quality: a twin study.Crossref | GoogleScholarGoogle Scholar | 17003685PubMed |

Tan, Q., Christiansen, L., von Bornemann Hjelmborg, J., and Christensen, K. (2015). Twin methodology in epigenetic studies. J. Exp. Biol. 218, 134–139.
Twin methodology in epigenetic studies.Crossref | GoogleScholarGoogle Scholar | 25568460PubMed |

van Dongen, J., Ehli, E. A., Slieker, R. C., Bartels, M., Weber, Z. M., Davies, G. E., Slagboom, P. E., Heijmans, B. T., and Boomsma, D. I. (2014). Epigenetic variation in monozygotic twins: a genome-wide analysis of DNA methylation in buccal cells. Genes (Basel) 5, 347–365.
Epigenetic variation in monozygotic twins: a genome-wide analysis of DNA methylation in buccal cells.Crossref | GoogleScholarGoogle Scholar | 24802513PubMed |

Vujkovic, M., de Vries, J. H., Dohle, G. R., Bonsel, G. J., Lindemans, J., Macklon, N. S., van der Spek, P. J., Steegers, E. A. P., and Steegers-Theunissen, R. P. M. (2009). Associations between dietary patterns and semen quality in men undergoing IVF/ICSI treatment. Hum. Reprod. 24, 1304–1312.
Associations between dietary patterns and semen quality in men undergoing IVF/ICSI treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlKqtbw%3D&md5=eefae34720cf1cf3b726dc22088eb05cCAS | 19228759PubMed |

Wei, Y., Schatten, H., and Sun, Q.-Y. (2015). Environmental epigenetic inheritance through gametes and implications for human reproduction. Hum. Reprod. Update 21, 194–208.
Environmental epigenetic inheritance through gametes and implications for human reproduction.Crossref | GoogleScholarGoogle Scholar | 25416302PubMed |