Influence of sperm fertilising concentration, sperm selection method and sperm capacitation procedure on the incidence of numerical chromosomal abnormalities in IVF early bovine embryos
Sebastián Demyda-Peyrás A C , Jesús Dorado B , Manuel Hidalgo B and Miguel Moreno-Millán A
+ Author Affiliations
- Author Affiliations
A Meragem Research Group, Department of Genetics, University of Cordoba, Spain.
B Department of Medicine and Animal Surgery, University of Cordoba, Spain.
C Corresponding author. Email: sebass@uco.es
Reproduction, Fertility and Development 27(2) 351-359 https://doi.org/10.1071/RD13285
Submitted: 3 September 2013 Accepted: 21 October 2013 Published: 27 November 2013
Abstract
The occurrence of numerical chromosomal aberrations, widely described as a major cause of mortality in in vitro-produced (IVP) embryos, has been linked to several factors. In the present study we investigated the effect of sperm fertilising concentration and semen handling (sperm selection and capacitation) before IVF on the rate of numerical chromosomal abnormalities in bovine embryos. In all, 466 IVP cattle embryos were karyotyped throughout three sequential experiments, analysing the effects of sperm fertilising concentration (0.1, 1.0 or 10 × 106 spermatozoa mL–1), selection method (unselected or Percoll-selected spermatozoa) and capacitation medium (bovine serum albumin (BSA), heparin or their combination). The percentage of normal (diploid) and aberrant (haploid, polyploid or aneuploid) embryos was noted in each experiment. The rate of numerical chromosomal abnormalities was mainly affected by sperm fertilising concentration (P < 0.01) and, to a lesser extent, by the sperm capacitation medium (P < 0.05). Polyploidy and haploidy rates were only affected by sperm fertilising concentration (P < 0.05). Interestingly, the sperm selection technique used in the present study did not reduce the incidence of chromosome abnormalities in IVP cattle embryos (P > 0.05). Finally, aneuploidy rates were not affected during the experiments (P > 0.05), which suggests that they are not related to sperm-related factors. On the basis of these results, we conclude that sperm fertilising concentration is the ‘paternal’ key factor that affects the rate of numerical chromosomal abnormalities in IVP bovine embryos. By making small adjustments to fertilising protocols, the rate of cytogenetically aberrant embryos can be markedly reduced.
Additional keywords: cattle, paternal influence, spermatozoa.
References
Ballif, B. C., Kashork, C. D., Saleki, R., Rorem, E., Sundin, K., Bejjani, B. A., and Shaffer, L. G. (2006). Detecting sex chromosome anomalies and common triploidies in products of conception by array-based comparative genomic hybridization. Prenat. Diagn. 26, 333–339.| Detecting sex chromosome anomalies and common triploidies in products of conception by array-based comparative genomic hybridization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslegtLY%3D&md5=862d4a28d7aa28822c7a66466100610bCAS | 16491513PubMed |
Barceló-Fimbres, M., Campos-Chillón, L. F., and Seidel, G. E. (2011). In vitro fertilization using non-sexed and sexed bovine sperm: sperm concentration, sorter pressure, and bull effects. Reprod. Domest. Anim. 46, 495–502.
| In vitro fertilization using non-sexed and sexed bovine sperm: sperm concentration, sorter pressure, and bull effects.Crossref | GoogleScholarGoogle Scholar | 20946538PubMed |
Bilodeau-Goeseels, S. (2012). Bovine oocyte meiotic inhibition before in vitro maturation and its value to in vitro embryo production: does it improve developmental competence? Reprod. Domest. Anim. 47, 687–693.
| Bovine oocyte meiotic inhibition before in vitro maturation and its value to in vitro embryo production: does it improve developmental competence?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zmsVSgtA%3D%3D&md5=35c6aefd36decb49313a975295b843c2CAS | 21988654PubMed |
Brackett, B. G., Bousquet, D., Boice, M. L., Donawick, W. J., Evans, J. F., and Dressel, M. A. (1982). Normal development following in vitro fertilization in the cow. Biol. Reprod. 27, 147–158.
| Normal development following in vitro fertilization in the cow.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2FgtVKgsQ%3D%3D&md5=52cace69a639ec57b3f4395016cdbdf4CAS | 6896830PubMed |
Coy, P., and Avilés, M. (2010). What controls polyspermy in mammals, the oviduct or the oocyte? Biol. Rev. Camb. Philos. Soc. 85, 593–605.
| 20039874PubMed |
Coy, P., Cánovas, S., Mondéjar, I., Saavedra, M. D., Romar, R., Grullón, L., Matás, C., and Avilés, M. (2008). Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc. Natl Acad. Sci. USA 105, 15 809–15 814.
| Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1yitrjL&md5=7d1787d532e060317b71fc446399c206CAS |
Dale, B., and Defelice, L. (2011). Polyspermy prevention: facts and artifacts? J. Assist. Reprod. Genet. 28, 199–207.
| Polyspermy prevention: facts and artifacts?Crossref | GoogleScholarGoogle Scholar | 21104196PubMed |
De Almeida Camargo, L.S., Ferreira de Sá, W., De Moraes Ferreira, A., Moreira Viana, J.H., and Couto Araújo, M.C. (2002). Effect of sperm concentration and incubation period of oocyte-spermatozoa on in vitro fertilization in the Gir breed. Pesq. Agropec. Bras. 37, 709–715.
Demyda-Peyrás, S., Dorado, J., Hidalgo, M., De Luca, L., Muñoz-Serrano, A., and Moreno-Millan, M. (2012). In vitro induction of the acrosome reaction in spermatozoa from endangered Spanish bulls: effect of breed, culture media and incubation time. Livest. Sci. 149, 275–281.
| In vitro induction of the acrosome reaction in spermatozoa from endangered Spanish bulls: effect of breed, culture media and incubation time.Crossref | GoogleScholarGoogle Scholar |
Demyda-Peyrás, S., Dorado, J., Hidalgo, M., Anter, J., De Luca, L., Genero, E., and Moreno-Millán, M. (2013a). Effects of oocyte quality, incubation time and maturation environment on the number of chromosomal abnormalities in IVF-derived early bovine embryos. Reprod. Fertil. Dev. 25, 1077–1084.
| Effects of oocyte quality, incubation time and maturation environment on the number of chromosomal abnormalities in IVF-derived early bovine embryos.Crossref | GoogleScholarGoogle Scholar | 23182337PubMed |
Demyda-Peyrás, S., Hidalgo, M., Dorado, J., Anter, J., Género, E., and Moreno Millán, M. (2013b). In vitro oocyte maturation and fertilization rates in the Spanish Lidia bovine breed. Span. J. Agric. Res. 11, 356–361.
| In vitro oocyte maturation and fertilization rates in the Spanish Lidia bovine breed.Crossref | GoogleScholarGoogle Scholar |
Dias, L.P.B., Sá, W.F., Camargo, L.S.A., Ramos, A.A., Ferreira, A.M., Viana, J.H.M., and Nogueira, L.A.G. (2006). Sperm concentration and incubation period on in vitro fecundation using sperm of Guzera bulls. Arq. Bras. Med. Vet. Zootec. 58, 348–353.
Dinkins, M. B., and Brackett, B. G. (2000). Chlortetracycline staining patterns of frozen–thawed bull spermatozoa treated with β-cyclodextrins, dibutyryl cAMP and progesterone. Zygote 8, 245–256.
| Chlortetracycline staining patterns of frozen–thawed bull spermatozoa treated with β-cyclodextrins, dibutyryl cAMP and progesterone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1OitLk%3D&md5=2d39431fa1cdd66e7760814a376fdf66CAS | 11014504PubMed |
Eichenlaub-Ritter, U. (1998). Genetics of oocyte ageing. Maturitas 30, 143–169.
| Genetics of oocyte ageing.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FovFSktw%3D%3D&md5=2f9536c71ec3aeb3d1ca3fe14f1596f5CAS | 9871909PubMed |
Foote, R. H., and Parks, J. E. (1993). Factors affecting preservation and fertility of bull sperm: a brief review. Reprod. Fertil. Dev. 5, 665–673.
| Factors affecting preservation and fertility of bull sperm: a brief review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3ptFWqtQ%3D%3D&md5=1a4f78ab1b5b60a5dfcc39f8fbd3bbf3CAS | 9627727PubMed |
Frumkin, T., Malcov, M., Yaron, Y., and Ben-Yosef, D. (2008). Elucidating the origin of chromosomal aberrations in IVF embryos by preimplantation genetic analysis. Mol. Cell. Endocrinol. 282, 112–119.
| Elucidating the origin of chromosomal aberrations in IVF embryos by preimplantation genetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVegtrY%3D&md5=0cf70ffa9600d6ea7cc1c91498b2f730CAS | 18177997PubMed |
Gianaroli, L., Magli, M. C., and Ferraretti, A. P. (2005). Sperm and blastomere aneuploidy detection in reproductive genetics and medicine. J. Histochem. Cytochem. 53, 261–267.
| Sperm and blastomere aneuploidy detection in reproductive genetics and medicine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisFSqtrg%3D&md5=63e7f76d22e4254393393c51f014ee95CAS | 15749998PubMed |
Hansen, P. J. (2006). Realizing the promise of IVF in cattle: an overview. Theriogenology 65, 119–125.
| Realizing the promise of IVF in cattle: an overview.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnjtFSmsw%3D%3D&md5=77369a2e2aead52684aee1924e0b5cffCAS | 16253320PubMed |
Harper, J. C., and Sengupta, S. B. (2012). Preimplantation genetic diagnosis: state of the ART 2011. Hum. Genet. 131, 175–186.
| Preimplantation genetic diagnosis: state of the ART 2011.Crossref | GoogleScholarGoogle Scholar | 21748341PubMed |
Hawk, H. W., and Wall, R. J. (1994). Improved yields of bovine blastocysts from in vitro-produced oocytes. II. Media and co-culture cells. Theriogenology 41, 1585–1594.
| Improved yields of bovine blastocysts from in vitro-produced oocytes. II. Media and co-culture cells.Crossref | GoogleScholarGoogle Scholar |
Ho, P. C., Yeung, W. S. B., Chan, Y. F., So, W. W. K., and Chan, S. T. H. (1994). Factors affecting the incidence of polyploidy in a human in vitro fertilization program. Int. J. Fertil. 39, 14–19.
| 1:STN:280:DyaK2c3itFSqsA%3D%3D&md5=0e7adeed7606f256daddc40f39c21aedCAS |
Hornak, M., Hulinska, P., Musilova, P., Kubickova, S., and Rubes, J. (2009). Investigation of chromosome aneuploidies in early porcine embryos using comparative genomic hybridization. Cytogenet. Genome Res. 126, 210–216.
| Investigation of chromosome aneuploidies in early porcine embryos using comparative genomic hybridization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MfjvV2ksw%3D%3D&md5=7d7a147ccc0ba7828fe891e9dedbe555CAS | 20016172PubMed |
Hornak, M., Oracova, E., Hulinska, P., Urbankova, L., and Rubes, J. (2012). Aneuploidy detection in pigs using comparative genomic hybridization: from the oocytes to blastocysts. PLoS One 7, e30335.
| Aneuploidy detection in pigs using comparative genomic hybridization: from the oocytes to blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XitFensLw%3D&md5=ea7f2673556e4f9fe529a154e8baa9f9CAS | 22291937PubMed |
Hunter, R. H. F., and Rodriguez-Martinez, H. (2002). Analysing mammalian fertilisation: reservations and potential pitfalls with an in vitro approach. Zygote 10, 11–15.
| Analysing mammalian fertilisation: reservations and potential pitfalls with an in vitro approach.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383islejtQ%3D%3D&md5=f216f8f5269bd6e78c0457c25c22fa40CAS |
Hyttel, P., Viuff, D., Laurincik, J., Schmidt, M., Thomsen, P. D., Avery, B., Callesen, H., Rath, D., Niemann, H., Rosenkranz, C., Schellander, K., Ochs, R. L., and Greve, T. (2000). Risks of in-vitro production of cattle and swine embryos: aberrations in chromosome numbers, ribosomal RNA gene activation and perinatal physiology. Hum. Reprod. 15, 87–97.
| Risks of in-vitro production of cattle and swine embryos: aberrations in chromosome numbers, ribosomal RNA gene activation and perinatal physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlKns7k%3D&md5=ec76cf78b4aacc62ad6363ba8d76e1d4CAS | 11263540PubMed |
Iannuzzi, L., and Di Berardino, D. (2008). Tools of the trade: diagnostics and research in domestic animal cytogenetics. J. Appl. Genet. 49, 357–366.
| Tools of the trade: diagnostics and research in domestic animal cytogenetics.Crossref | GoogleScholarGoogle Scholar | 19029683PubMed |
International Embryo Transfer Society (IETS) (2012). Data Retrieval Comittee Report. (IETS: IL, USA.)
Jakobsen, A. S., Thomsen, P. D., and Avery, B. (2006). Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro. Theriogenology 65, 870–881.
| Few polyploid blastomeres in morphologically superior bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 16115669PubMed |
Januskauskas, A., Gil, J., Söderquist, L., Håård, M. G. M., Håård, M. C., Johannisson, A., and Rodriguez-Martinez, H. (1999). Effect of cooling rates on post-thaw sperm motility, membrane integrity, capacitation status and fertility of dairy bull semen used for artificial insemination in Sweden. Theriogenology 52, 641–658.
| Effect of cooling rates on post-thaw sperm motility, membrane integrity, capacitation status and fertility of dairy bull semen used for artificial insemination in Sweden.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVGgug%3D%3D&md5=94e922bfa457cb751625b59fed36cc82CAS | 10734363PubMed |
Kawarsky, S. J., Basrur, P. K., Stubbings, R. B., Hansen, P. J., and King, W. A. (1996). Chromosomal abnormalities in bovine embryos and their influence on development. Biol. Reprod. 54, 53–59.
| Chromosomal abnormalities in bovine embryos and their influence on development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtVSisLrJ&md5=7d21e722c07c96e327076361a0ac2047CAS | 8838000PubMed |
King, W. A. (1990). Chromosome abnormalities and pregnancy failure in domestic animals. Adv. Vet. Sci. Comp. Med. 34, 229–250.
| Chromosome abnormalities and pregnancy failure in domestic animals.Crossref | GoogleScholarGoogle Scholar |
King, W. A. (2008). Chromosome variation in the embryos of domestic animals. Cytogenet. Genome Res. 120, 81–90.
| Chromosome variation in the embryos of domestic animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1czgs1yltA%3D%3D&md5=acfd9007408f77f11bcec90212cad087CAS | 18467828PubMed |
Magli, M. C., Gianaroli, L., Ferraretti, A. P., Gordts, S., Fredericks, V., and Crippa, A. (2009). Paternal contribution to aneuploidy in preimplantation embryos. Reprod. Biomed. Online 18, 536–542.
| Paternal contribution to aneuploidy in preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MzgvVaiuw%3D%3D&md5=21ad5201e69770fc868e196012b6fa4fCAS | 19400996PubMed |
Matás, C., Sansegundo, M., Ruiz, S., García-Vázquez, F. A., Gadea, J., Romar, R., and Coy, P. (2010). Sperm treatment affects capacitation parameters and penetration ability of ejaculated and epididymal boar spermatozoa. Theriogenology 74, 1327–1340.
| Sperm treatment affects capacitation parameters and penetration ability of ejaculated and epididymal boar spermatozoa.Crossref | GoogleScholarGoogle Scholar | 20688369PubMed |
Munné, S. (2002). Preimplantation genetic diagnosis of numerical and structural chromosome abnormalities. Reprod. Biomed. Online 4, 183–196.
| Preimplantation genetic diagnosis of numerical and structural chromosome abnormalities.Crossref | GoogleScholarGoogle Scholar | 12470583PubMed |
Munné, S. (2012). Preimplantation genetic diagnosis for aneuploidy and translocations using array comparative genomic hybridization. Curr. Genomics 13, 463–470.
| Preimplantation genetic diagnosis for aneuploidy and translocations using array comparative genomic hybridization.Crossref | GoogleScholarGoogle Scholar | 23448851PubMed |
Munné, S., Sandalinas, M., Escudero, T., Márquez, C., and Cohen, J. (2002). Chromosome mosaicism in cleavage-stage human embryos: evidence of a maternal age effect. Reprod. Biomed. Online 4, 223–232.
| Chromosome mosaicism in cleavage-stage human embryos: evidence of a maternal age effect.Crossref | GoogleScholarGoogle Scholar | 12709271PubMed |
Nagaoka, S. I., Hassold, T. J., and Hunt, P. A. (2012). Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 13, 493–504.
| Human aneuploidy: mechanisms and new insights into an age-old problem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos12ht78%3D&md5=a192eda0d9a86e05388de27e1622d2ecCAS | 22705668PubMed |
Nijs, M., De Jonge, C., Cox, A., Janssen, M., Bosmans, E., and Ombelet, W. (2011). Correlation between male age, WHO sperm parameters, DNA fragmentation, chromatin packaging and outcome in assisted reproduction technology. Andrologia 43, 174–179.
| Correlation between male age, WHO sperm parameters, DNA fragmentation, chromatin packaging and outcome in assisted reproduction technology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntlKnt7s%3D&md5=95e9a3e71a540a8cf032ee323a63ed9bCAS | 21561463PubMed |
Palma, G. A., and Sinowatz, F. (2004). Male and female effects on the in vitro production of bovine embryos. Anat. Histol. Embryol. 33, 257–262.
| Male and female effects on the in vitro production of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvksFCgsg%3D%3D&md5=d2b7c082e8224d069f34a755b4a8edc6CAS | 15352877PubMed |
Parrish, J. J., Krogenaes, A., and Susko-Parrish, J. L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–869.
| Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVGgug%3D%3D&md5=162b4ec4dddf4398e84b8c88373cce16CAS | 16727781PubMed |
Pauciullo, A., Nicodemo, D., Peretti, V., Marino, G., Iannuzzi, A., Cosenza, G., Di Meo, G. P., Ramunno, L., Iannuzzi, L., Rubes, J., and Di Berardino, D. (2012). X–Y aneuploidy rate in sperm of two ‘minor’ breeds of cattle (Bos taurus) by using dual color fluorescent in situ hybridization (FISH). Theriogenology 78, 688–695.
| X–Y aneuploidy rate in sperm of two ‘minor’ breeds of cattle (Bos taurus) by using dual color fluorescent in situ hybridization (FISH).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rltFWitQ%3D%3D&md5=9a73e2b9f8dab4a165550c85fff084cbCAS | 22503844PubMed |
Pers-Kamczyc, E., Pawlak, P., Rubes, J., and Lechniak, D. (2012). Early cleaved bovine embryos show reduced incidence of chromosomal aberrations and higher developmental potential on Day 4.5 post-insemination. Reprod. Domest. Anim. 47, 899–906.
| Early cleaved bovine embryos show reduced incidence of chromosomal aberrations and higher developmental potential on Day 4.5 post-insemination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vhvFyisA%3D%3D&md5=9bbea2b1cda9d695d36d1af167984961CAS | 22304363PubMed |
Plachot, M., Mandelbaum, J., Junca, A. M., De Grouchy, J., Salat-Baroux, J., and Cohen, J. (1989). Cytogenetic analysis and developmental capacity of normal and abnormal embryos after IVF. Hum. Reprod. 4, 99–103.
| Cytogenetic analysis and developmental capacity of normal and abnormal embryos after IVF.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7jtFSjsw%3D%3D&md5=4730c51a55fafba58d0c56752734ce35CAS | 2613880PubMed |
Pontes, J. H. F., Silva, K. C. F., Basso, A. C., Rigo, A. G., Ferreira, C. R., Santos, G. M. G., Sanches, B. V., Porcionato, J. P. F., Vieira, P. H. S., Faifer, F. S., Sterza, F. A. M., Schenk, J. L., and Seneda, M. M. (2010). Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm. Theriogenology 74, 1349–1355.
| Large-scale in vitro embryo production and pregnancy rates from Bos taurus, Bos indicus, and indicus-taurus dairy cows using sexed sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfntlyqsA%3D%3D&md5=b3a823e282a66be883a80dd175ddca89CAS |
Rambags, B. P. B., Krijtenburg, P. J., Van Drie, H. F., Lazzari, G., Galli, C., Pearson, P. L., Colenbrander, B., and Stout, T. A. E. (2005). Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 72, 77–87.
| Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntlClsL4%3D&md5=da21bb2f523ce18a79374d3c22c8c089CAS |
Rodriguez-Martinez, H., and Larsson, B. (1998). Assessment of sperm fertilizing ability in farm animals. Acta Agr. Scand. A-An. 29, 12–18.
Rubeš, J., Machatková, M., Jokešová, E., and Zudová, D. (1999). A potential relationship between the 16;20 and 14;20 Robertsonian translocations and low in vitro embryo development. Theriogenology 52, 171–180.
| A potential relationship between the 16;20 and 14;20 Robertsonian translocations and low in vitro embryo development.Crossref | GoogleScholarGoogle Scholar | 10734415PubMed |
Rybar, R., Kopecka, V., Prinosilova, P., Kubickova, S., Veznik, Z., and Rubes, J. (2010). Fertile bull sperm aneuploidy and chromatin integrity in relationship to fertility. Int. J. Androl. 33, 613–622.
| 1:STN:280:DC%2BC3cnosFajsQ%3D%3D&md5=f87cfc962937a019805170406bbce784CAS | 19751362PubMed |
Sandalinas, M., Sadowy, S., Alikani, M., Calderon, G., Cohen, J., and Munné, S. (2001). Developmental ability of chromosomally abnormal human embryos to develop to the blastocyst stage. Hum. Reprod. 16, 1954–1958.
| Developmental ability of chromosomally abnormal human embryos to develop to the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvosFOkug%3D%3D&md5=9e3ff0941d319969a279cad2eae89c32CAS | 11527904PubMed |
Sapienza, F., Verheyen, G., Tournaye, H., Janssens, R., Pletincx, I., Derde, M., and Van Steirteghem, A. (1993). An auto-controlled study in in-vitro fertilization reveals the benefit of Percoll centrifugation to swim-up in the preparation of poor-quality semen. Hum. Reprod. 8, 1856–1862.
| 1:STN:280:DyaK2c7hslKksw%3D%3D&md5=128854ecedf807b15ab0248cb398aefdCAS | 8288751PubMed |
Sloter, E., Nath, J., Eskenazi, B., and Wyrobek, A. J. (2004). Effects of male age on the frequencies of germinal and heritable chromosomal abnormalities in humans and rodents. Fertil. Steril. 81, 925–943.
| Effects of male age on the frequencies of germinal and heritable chromosomal abnormalities in humans and rodents.Crossref | GoogleScholarGoogle Scholar | 15066442PubMed |
Staessen, C., and Van Steirteghem, A. C. (1997). The chromosomal constitution of embryos developing from abnormally fertilized oocytes after intracytoplasmic sperm injection and conventional in-vitro fertilization. Hum. Reprod. 12, 321–327.
| The chromosomal constitution of embryos developing from abnormally fertilized oocytes after intracytoplasmic sperm injection and conventional in-vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3isVWltQ%3D%3D&md5=e53080565338f2536e0ca2e5eeaec1ceCAS | 9070720PubMed |
Stewart-Savage, J. (1993). Effect of bovine serum albumin concentration and source on sperm capacitation in the golden hamster. Biol. Reprod. 49, 74–81.
| Effect of bovine serum albumin concentration and source on sperm capacitation in the golden hamster.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkvFahtLk%3D&md5=531ba1cd5a77011d0eb3761564933966CAS | 8353192PubMed |
Tajik, P., Niwa, K., and Murase, T. (1993). Effects of different protein supplements in fertilization medium on in vitro penetration of cumulus-intact and cumulus-free bovine oocytes matured in culture. Theriogenology 40, 949–958.
| Effects of different protein supplements in fertilization medium on in vitro penetration of cumulus-intact and cumulus-free bovine oocytes matured in culture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVWgtQ%3D%3D&md5=1cedfd2d3f4145a77f7f0595aacf0fe8CAS | 16727377PubMed |
Takahashi, K., Matsui, H., Takahashi, I., Matsumoto, H., Fukui, E., Motoyama, M., and Yoshizawa, M. (2010). Effects of in vitro aging of mouse oocytes on metaphase II spindle morphology, in vitro fertilization and subsequent embryonic development. J. Mamm. Ova 27, 42–50.
| Effects of in vitro aging of mouse oocytes on metaphase II spindle morphology, in vitro fertilization and subsequent embryonic development.Crossref | GoogleScholarGoogle Scholar |
Tarín, J. J., Trounson, A. O., and Sathananthan, H. (1999). Origin and ploidy of multipronuclear zygotes. Reprod. Fertil. Dev. 11, 273–279.
| Origin and ploidy of multipronuclear zygotes.Crossref | GoogleScholarGoogle Scholar | 10898292PubMed |
Taşkin, S., and Sönmezer, M. (2012). Fertility preservation in women: an update. Exp. Rev. Obstet. Gynecol. 7, 595–603.
| Fertility preservation in women: an update.Crossref | GoogleScholarGoogle Scholar |
Taylor, A. S., and Braude, P. R. (1994). The early development and DNA content of activated human oocytes and parthenogenetic human embryos. Hum. Reprod. 9, 2389–2397.
| 1:STN:280:DyaK2M3ivFyqtg%3D%3D&md5=3ee08bd2e289a3a5aefeb8af15f22440CAS | 7714163PubMed |
Ulloa Ulloa, C. M., Yoshizawa, M., Komoriya, E., Mitsui, A., Nagai, T., and Kikuchi, K. (2008a). The blastocyst production rate and incidence of chromosomal abnormalities by developmental stage in in vitro produced porcine embryos. J. Reprod. Dev. 54, 22–29.
| The blastocyst production rate and incidence of chromosomal abnormalities by developmental stage in in vitro produced porcine embryos.Crossref | GoogleScholarGoogle Scholar |
Ulloa Ulloa, C. M., Yoshizawa, M., Yamashita, A., Hama, S., Mitsui, A., Hashi, C., Abe, H., Hoshi, H., Fukui, E., and Matsumoto, H. (2008b). Blastocyst production from in vitro-produced day-2 bovine embryos classified by cleavage stage, and cytogenetical evaluation of the resultant day-8 blastocysts. J. Reprod. Dev. 54, 465–472.
| Blastocyst production from in vitro-produced day-2 bovine embryos classified by cleavage stage, and cytogenetical evaluation of the resultant day-8 blastocysts.Crossref | GoogleScholarGoogle Scholar | 18957827PubMed |
van der Heijden, G. W., van den Berg, I. M., Baart, E. B., Derijck, A. A. H. A., Martini, E., and de Boer, P. (2009). Parental origin of chromatin in human monopronuclear zygotes revealed by asymmetric histone methylation patterns, differs between IVF and ICSI. Mol. Reprod. Dev. 76, 101–108.
| Parental origin of chromatin in human monopronuclear zygotes revealed by asymmetric histone methylation patterns, differs between IVF and ICSI.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFemtL3K&md5=55646c597694fa241cc3d5a709f56fadCAS | 18481364PubMed |
Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A., and Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology 68, S131–S137.
| Gamete origin in relation to early embryo development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaitLk%3D&md5=ec20a46b1d97742c14c07f01a95b29a4CAS | 17467789PubMed |
Vegetti, W., Van Assche, E., Frias, A., Verheyen, G., Bianchi, M. M., Bonduelle, M., Liebaers, I., and Van Steirteghem, A. (2000). Correlation between semen parameters and sperm aneuploidy rates investigated by fluorescence in-situ hybridization in infertile men. Hum. Reprod. 15, 351–365.
| Correlation between semen parameters and sperm aneuploidy rates investigated by fluorescence in-situ hybridization in infertile men.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7it1ertg%3D%3D&md5=50ad005a3f2716bcd9e8155ddbf5d26aCAS | 10655307PubMed |
Visconti, P. E., and Kopf, G. S. (1998). Regulation of protein phosphorylation during sperm capacitation. Biol. Reprod. 59, 1–6.
| Regulation of protein phosphorylation during sperm capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFaksLw%3D&md5=dabded89a0bf24a8d6ecb8c520214529CAS | 9674985PubMed |
Visconti, P. E., Galantino-Homer, H., Ning, X., Moore, G. D., Valenzuela, J. P., Jorgez, C. J., Alvarez, J. G., and Kopf, G. S. (1999). Cholesterol efflux-mediated signal transduction in mammalian sperm: β- cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. J. Biol. Chem. 274, 3235–3242.
| Cholesterol efflux-mediated signal transduction in mammalian sperm: β- cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXpsVCisQ%3D%3D&md5=ae4c7da66a007acac2d12ebbb5746968CAS | 9915865PubMed |
Viuff, D., Rickords, L., Offenberg, H., Hyttel, P., Avery, B., Greve, T., Olsaker, I., Williams, J. L., Callesen, H., and Thomsen, P. D. (1999). A high proportion of bovine blastocysts produced in vitro are mixoploid. Biol. Reprod. 60, 1273–1278.
| A high proportion of bovine blastocysts produced in vitro are mixoploid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVaqtbw%3D&md5=2dca1c990e7d71ca06e4717770e79a8eCAS | 10330080PubMed |
Viuff, D., Greve, T., Avery, B., Hyttel, P., Brockhoff, P. B., and Thomsen, P. D. (2000). Chromosome aberrations in in vitro-produced bovine embryos at Days 2–5 post-insemination. Biol. Reprod. 63, 1143–1148.
| Chromosome aberrations in in vitro-produced bovine embryos at Days 2–5 post-insemination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslylurw%3D&md5=3b95b1e2f6bf96f8cbe2cd75a7252220CAS | 10993838PubMed |
Viuff, D., Hendriksen, P. J. M., Vos, P. L. A. M., Dieleman, S. J., Bibbiy, B. M., Greve, T., Hyttel, P., and Thomsen, P. D. (2001). Chromosomal abnormalities and developmental kinetics in in vivo-developed cattle embryos at Days 2 to 5 after ovulation. Biol. Reprod. 65, 204–208.
| Chromosomal abnormalities and developmental kinetics in in vivo-developed cattle embryos at Days 2 to 5 after ovulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWhtbg%3D&md5=c29bf51276f6233e91b206572db73bccCAS | 11420241PubMed |
Viuff, D., Palsgaard, A., Rickords, L., Lawson, L. G., Greve, T., Schmidt, M., Avery, B., Hyttel, P., and Thomsen, P. D. (2002). Bovine embryos contain a higher proportion of polyploid cells in the trophectoderm than in the embryonic disc. Mol. Reprod. Dev. 62, 483–488.
| Bovine embryos contain a higher proportion of polyploid cells in the trophectoderm than in the embryonic disc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Klsrs%3D&md5=1b766daf57f100b99f20985e6ec6dffdCAS | 12112581PubMed |
Viville, S., Mollard, R., Bach, M. L., Falquet, C., Gerlinger, P., and Warter, S. (2000). Do morphological anomalies reflect chromosomal aneuploidies? Hum. Reprod. 15, 2563–2566.
| Do morphological anomalies reflect chromosomal aneuploidies?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FoslWnug%3D%3D&md5=0c5e0ec696f63a62f34bb64b05b1a49cCAS | 11098027PubMed |
Wang, W. H., Day, B. N., and Wu, G. M. (2003). How does polyspermy happen in mammalian oocytes? Microsc. Res. Tech. 61, 335–341.
| How does polyspermy happen in mammalian oocytes?Crossref | GoogleScholarGoogle Scholar | 12811738PubMed |
Yoo, J. G., and Smith, L. C. (2007). Extracellular calcium induces activation of Ca2+/calmodulin-dependent protein kinase II and mediates spontaneous activation in rat oocytes. Biochem. Biophys. Res. Commun. 359, 854–859.
| Extracellular calcium induces activation of Ca2+/calmodulin-dependent protein kinase II and mediates spontaneous activation in rat oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvV2ju7Y%3D&md5=09aba44fba7af2321763ef67526184b4CAS | 17570344PubMed |
Yoshizawa, M., Ulloa, C. M. U., Hufana-Duran, D., Atabay, E., Duran, P. G., Cruz, L. C., Kanai, Y., and Takahashi, Y. (2010). Incidence of chromosomal abnormalities in early-stage river buffalo embryos derived from in vitro fertilization. J. Mamm. Ova 27, 157–160.
| Incidence of chromosomal abnormalities in early-stage river buffalo embryos derived from in vitro fertilization.Crossref | GoogleScholarGoogle Scholar |
