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Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos

Olga Tšuiko, Maaike Catteeuw UGent, Masoud Zamani Esteki, Aspasia Destouni, Osvaldo Américo Bogado Pascottini, Urban Besenfelder, Vitezslav Havlicek, Katrien Smits UGent, Ants Kurg, Andres Salumets, et al. (2017) HUMAN REPRODUCTION. 32(11). p.2348-2357
abstract
STUDY QUESTION: Is the rate and nature of chromosome instability (CIN) similar between bovine in vivo-derived and in vitro-cultured cleavage-stage embryos? SUMMARY ANSWER: There is a major difference regarding chromosome stability of in vivo-derived and in vitro-cultured embryos, as CIN is significantly lower in in vivo-derived cleavage-stage embryos compared to in vitro-cultured embryos. WHAT IS KNOWN ALREADY: CIN is common during in vitro embryogenesis and is associated with early embryonic loss in humans, but the stability of in vivo-conceived cleavage-stage embryos remains largely unknown. STUDY DESIGN, SIZE, DURATION: Because human in vivo preimplantation embryos are not accessible, bovine (Bos taurus) embryos were used to study CIN in vivo. Five young, healthy, cycling Holstein Friesian heifers were used to analyze single blastomeres of in vivo embryos, in vitro embryos produced by ovum pick up with ovarian stimulation (OPU-IVF), and in vitro embryos produced from in vitro matured oocytes retrieved without ovarian stimulation (IVM-IVF). PARTICIPANTS/MATERIALS, SETTING, METHODS: Single blastomeres were isolated from embryos, whole-genome amplified and hybridized on Illumina BovineHD BeadChip arrays together with the bulk DNA from the donor cows (mothers) and the bull (father). DNA was also obtained from the parents of the bull and from the parents of the cows (paternal and maternal grandparents, respectively). Subsequently, genome-wide haplotyping and copy-number profiling was applied to investigate the genomic architecture of 171 single bovine blastomeres of 16 in vivo, 13 OPU-IVF and 13 IVM-IVF embryos. MAIN RESULTS AND THE ROLE OF CHANCE: The genomic stability of single blastomeres in both of the in vitro-cultured embryo cohorts was severely compromised (P < 0.0001), and the frequency of whole chromosome or segmental aberrations was higher in embryos produced in vitro than in embryos derived in vivo. Only 18.8% of in vivo-derived embryos contained at least one blastomere with chromosomal anomalies, compared to 69.2% of OPU-IVF embryos (P < 0.01) and 84.6% of IVM-IVF embryos (P < 0.001). LARGE SCALE DATA: Genotyping data obtained in this study has been submitted to NCBI Gene Expression Omnibus (GEO; accession number GSE95358) LIMITATIONS REASONS FOR CAUTION: There were two main limitations of the study. First, animal models may not always reflect the nature of human embryogenesis, although the use of an animal model to investigate CIN was unavoidable in our study. Second, a limited number of embryos were obtained, therefore more studies are warranted to corroborate the findings. WIDER IMPLICATIONS OF THE FINDINGS: Although CIN is also present in in vivo-developed embryos, in vitro procedures exacerbate chromosomal abnormalities during early embryo development. Hence, the present study highlights that IVF treatment compromises embryo viability and should be applied with care. Additionally, our results encourage to refine and improve in vitro culture conditions and assisted reproduction technologies.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
in vivo embryo, preimplantation embryo, chromosome instability, CIN, haplarithmisis, CONFINED PLACENTAL MOSAICISM, DIPLOID-TRIPLOID MIXOPLOIDY, HYDATIDIFORM MOLE, CHROMOSOMAL-ABNORMALITIES, HORMONAL-STIMULATION, ANTAGONIST PROTOCOL, PERINATAL OUTCOMES, OOCYTE MATURATION, TWIN PREGNANCY, FERTILIZATION
journal title
HUMAN REPRODUCTION
Hum. Reprod.
volume
32
issue
11
pages
2348 - 2357
Web of Science type
Article
Web of Science id
000413450900023
ISSN
0268-1161
1460-2350
DOI
10.1093/humrep/dex286
language
English
UGent publication?
yes
classification
A1
additional info
the first three authors contributed equally to this work
copyright statement
I have transferred the copyright for this publication to the publisher
id
8547349
handle
http://hdl.handle.net/1854/LU-8547349
date created
2018-02-01 13:54:19
date last changed
2018-03-02 10:03:01
@article{8547349,
  abstract     = {STUDY QUESTION: Is the rate and nature of chromosome instability (CIN) similar between bovine in vivo-derived and in vitro-cultured cleavage-stage embryos? 
SUMMARY ANSWER: There is a major difference regarding chromosome stability of in vivo-derived and in vitro-cultured embryos, as CIN is significantly lower in in vivo-derived cleavage-stage embryos compared to in vitro-cultured embryos. 
WHAT IS KNOWN ALREADY: CIN is common during in vitro embryogenesis and is associated with early embryonic loss in humans, but the stability of in vivo-conceived cleavage-stage embryos remains largely unknown. 
STUDY DESIGN, SIZE, DURATION: Because human in vivo preimplantation embryos are not accessible, bovine (Bos taurus) embryos were used to study CIN in vivo. Five young, healthy, cycling Holstein Friesian heifers were used to analyze single blastomeres of in vivo embryos, in vitro embryos produced by ovum pick up with ovarian stimulation (OPU-IVF), and in vitro embryos produced from in vitro matured oocytes retrieved without ovarian stimulation (IVM-IVF). 
PARTICIPANTS/MATERIALS, SETTING, METHODS: Single blastomeres were isolated from embryos, whole-genome amplified and hybridized on Illumina BovineHD BeadChip arrays together with the bulk DNA from the donor cows (mothers) and the bull (father). DNA was also obtained from the parents of the bull and from the parents of the cows (paternal and maternal grandparents, respectively). Subsequently, genome-wide haplotyping and copy-number profiling was applied to investigate the genomic architecture of 171 single bovine blastomeres of 16 in vivo, 13 OPU-IVF and 13 IVM-IVF embryos. 
MAIN RESULTS AND THE ROLE OF CHANCE: The genomic stability of single blastomeres in both of the in vitro-cultured embryo cohorts was severely compromised (P {\textlangle} 0.0001), and the frequency of whole chromosome or segmental aberrations was higher in embryos produced in vitro than in embryos derived in vivo. Only 18.8\% of in vivo-derived embryos contained at least one blastomere with chromosomal anomalies, compared to 69.2\% of OPU-IVF embryos (P {\textlangle} 0.01) and 84.6\% of IVM-IVF embryos (P {\textlangle} 0.001). 
LARGE SCALE DATA: Genotyping data obtained in this study has been submitted to NCBI Gene Expression Omnibus (GEO; accession number GSE95358) 
LIMITATIONS REASONS FOR CAUTION: There were two main limitations of the study. First, animal models may not always reflect the nature of human embryogenesis, although the use of an animal model to investigate CIN was unavoidable in our study. Second, a limited number of embryos were obtained, therefore more studies are warranted to corroborate the findings. 
WIDER IMPLICATIONS OF THE FINDINGS: Although CIN is also present in in vivo-developed embryos, in vitro procedures exacerbate chromosomal abnormalities during early embryo development. Hence, the present study highlights that IVF treatment compromises embryo viability and should be applied with care. Additionally, our results encourage to refine and improve in vitro culture conditions and assisted reproduction technologies.},
  author       = {T\v{s}uiko, Olga and Catteeuw, Maaike and Zamani Esteki, Masoud and Destouni, Aspasia and Bogado Pascottini, Osvaldo Am{\'e}rico and Besenfelder, Urban and Havlicek, Vitezslav and Smits, Katrien and Kurg, Ants and Salumets, Andres and D{\textquoteright}Hooghe, Thomas and Voet, Thierry and Van Soom, Ann and Vermeesch, Joris Robert},
  issn         = {0268-1161},
  journal      = {HUMAN REPRODUCTION},
  keyword      = {in vivo embryo,preimplantation embryo,chromosome instability,CIN,haplarithmisis,CONFINED PLACENTAL MOSAICISM,DIPLOID-TRIPLOID MIXOPLOIDY,HYDATIDIFORM MOLE,CHROMOSOMAL-ABNORMALITIES,HORMONAL-STIMULATION,ANTAGONIST PROTOCOL,PERINATAL OUTCOMES,OOCYTE MATURATION,TWIN PREGNANCY,FERTILIZATION},
  language     = {eng},
  number       = {11},
  pages        = {2348--2357},
  title        = {Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos},
  url          = {http://dx.doi.org/10.1093/humrep/dex286},
  volume       = {32},
  year         = {2017},
}

Chicago
Tšuiko, Olga, Maaike Catteeuw, Masoud Zamani Esteki, Aspasia Destouni, Osvaldo Américo Bogado Pascottini, Urban Besenfelder, Vitezslav Havlicek, et al. 2017. “Genome Stability of Bovine in Vivo-conceived Cleavage-stage Embryos Is Higher Compared to in Vitro-produced Embryos.” Human Reproduction 32 (11): 2348–2357.
APA
Tšuiko, O., Catteeuw, M., Zamani Esteki, M., Destouni, A., Bogado Pascottini, O. A., Besenfelder, U., Havlicek, V., et al. (2017). Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos. HUMAN REPRODUCTION, 32(11), 2348–2357.
Vancouver
1.
Tšuiko O, Catteeuw M, Zamani Esteki M, Destouni A, Bogado Pascottini OA, Besenfelder U, et al. Genome stability of bovine in vivo-conceived cleavage-stage embryos is higher compared to in vitro-produced embryos. HUMAN REPRODUCTION. 2017;32(11):2348–57.
MLA
Tšuiko, Olga, Maaike Catteeuw, Masoud Zamani Esteki, et al. “Genome Stability of Bovine in Vivo-conceived Cleavage-stage Embryos Is Higher Compared to in Vitro-produced Embryos.” HUMAN REPRODUCTION 32.11 (2017): 2348–2357. Print.