Molecular Mechanisms and Pathways Involved in Bovine Embryonic Genome Activation and Their Regulation by Alternative In Vivo and In Vitro Culture Conditions1

Gad, Ahmed; Hoelker, M.; Besenfelder, U.; Havlíček, V.; Cinar, U; Rings, F.; Held, Eva; Dufort, Isabelle; Sirard, Marc‐André; Schellander, K.; Tesfaye, Dawit

doi:10.1095/biolreprod.112.099697

Cited by 146 publications

(172 citation statements)

References 49 publications

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“…Further, to date there is no systematic study addressing the activation of specific genes during several stages of early bovine embryo development. Detailed insight into the time course of embryonic genome activation is important, because embryos are particularly susceptible during the period of EGA (e.g., to changing culture conditions) (7). However, the underlying mechanisms are only partially understood, and new molecular readouts, such as effects on the timing of EGA, are required.…”

mentioning

confidence: 99%

Fine mapping of genome activation in bovine embryos by RNA sequencing

Graf

Krebs

Zakhartchenko³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

270

300

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During maternal-to-embryonic transition control of embryonic development gradually switches from maternal RNAs and proteins stored in the oocyte to gene products generated after embryonic genome activation (EGA). Detailed insight into the onset of embryonic transcription is obscured by the presence of maternal transcripts. Using the bovine model system, we established by RNA sequencing a comprehensive catalogue of transcripts in germinal vesicle and metaphase II oocytes, and in embryos at the four-cell, eight-cell, 16-cell, and blastocyst stages. These were produced by in vitro fertilization of Bos taurus taurus oocytes with sperm from a Bos taurus indicus bull to facilitate parent-specific transcriptome analysis. Transcripts from 12.4 to 13.7 × 10 3 different genes were detected in the various developmental stages. EGA was analyzed by (i) detection of embryonic transcripts, which are not present in oocytes; (ii) detection of transcripts from the paternal allele; and (iii) detection of primary transcripts with intronic sequences. These strategies revealed (i) 220, (ii) 937, and (iii) 6,848 genes to be activated from the four-cell to the blastocyst stage. The largest proportion of gene activation [i.e., (i) 59%, (ii) 42%, and (iii) 58%] was found in eight-cell embryos, indicating major EGA at this stage. Gene ontology analysis of genes activated at the four-cell stage identified categories related to RNA processing, translation, and transport, consistent with preparation for major EGA. Our study provides the largest transcriptome data set of bovine oocyte maturation and early embryonic development and detailed insight into the timing of embryonic activation of specific genes.

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mentioning

confidence: 99%

Fine mapping of genome activation in bovine embryos by RNA sequencing

Graf

Krebs

Zakhartchenko³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

270

300

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“…Some of the problems with the in vitro-produced embryo could result from selection of incompetent oocytes or inadequate oocyte maturation. However, the importance of the maternal environment during development is indicated by observations that transfer of in vitro-produced embryos to the oviduct after fertilization limits some of the abnormalities associated with in vitro production (9,21).…”

mentioning

confidence: 99%

Maternal embryokines that regulate development of the bovine preimplantation embryo

Hansen¹,

Denicol²,

Dobbs³

2014

Turk J Vet Anim Sci

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The zygote contains within its genome and epigenome the program to direct development through the embryonic, fetal, and postnatal periods. The execution of that program is dependent on the embryo's nongenetic inheritance from the oocyte and sperm (1,2) as well as on the environment in which development proceeds. Variation in the maternal environment can affect the ability of the preimplantation embryo to establish pregnancy. In cattle, the focus of this review, competence of the preimplantation embryo for growth and survival can be affected by maternal parity (3), lactational status (4), and circulating concentrations of progesterone (5). Moreover, patterns of gene expression in the endometrium are associated with survival of an embryo transferred to the uterus in the next ovulatory cycle (6,7).Development of the bovine embryo to the blastocyst in the absence of maternal signals (i.e. through in vitro production procedures) results in embryos with aberrant gene expression (8,9), lipid content (10,11), DNA methylation (12), and, as shown in the Table, reduced competence to establish pregnancy after transfer into recipients (13-17). Additionally, an increased proportion of embryos produced in vitro have developmental abnormalities that lead to increased neonatal death losses (18-20). Some of the problems with the in vitro-produced embryo could result from selection of incompetent oocytes or inadequate oocyte maturation. However, the importance of the maternal environment during development is indicated by observations that transfer of in vitro-produced embryos to the oviduct after fertilization limits some of the abnormalities associated with in vitro production (9,21).One function of the reproductive tract is to secrete bioactive molecules that regulate the embryo, oviduct, or endometrium. Genes for 115 ligands expressed in the endometrium had the corresponding receptor gene expressed by the embryo (22). Regulatory molecules produced by the oviduct and endometrium, which include hormones, growth factors, and cytokines, are referred to as embryokines when they function to regulate embryonic growth and development (23).It is likely that some of the variation in the ability of the reproductive tract to support embryonic development represents variation in secretion of embryokines. Indeed, several genes that were overexpressed in the endometrium of cows that subsequently became pregnant after embryo transfer as compared to cows that did not establish pregnancy are potential embryokines. These include NGF,

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“…For example, Dattena et al [192] confirmed higher sheep embryo cryosurvival results when including BSA and hyaluronan during IVC, and Gad et al [197] realized that altered culture conditions at different time points of the preimplantation period lead to adaptations of the embryos, changing their gene expression and developmental ability. As referred, the initial stages of development are those with higher cryosensitivity, from oocytes to late embryo, with the acquisition of cryotolerance in an intermediate stage of development.…”

Section: Methods Of Improving the Cryopreservation Of Sheep Embryosmentioning

confidence: 99%

“…Mitochondrial changes, namely, a reduced total number and an increase in the proportion of immature mitochondria [18,187], have been observed in poor-quality and IVP embryos and were associated with culture in serum-containing medium [210]. These changes have been also associated with inefficient lipid metabolism, with the presence of cytoplasmic vesicles and lipid drops and fewer lysosome-like vesicles [18], compromising ATP production [108,197,204].…”

Section: Methods Of Improving the Cryopreservation Of Sheep Embryosmentioning

confidence: 99%

Cryopreservation of Sheep Produced Embryos – Current and Future Perspectives

Romão¹,

Marques²,

Bettencourt³

et al. 2016

Insights From Animal Reproduction

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Due to economical and scientific limitations, sheep embryo reproductive technologies are less commercially applied than in other animal species. However, it is very clear that, in the near future, those techniques are expected to have a central role in animal production as a consequence of genetic and reproductive demands. One drawback is that results obtained after sheep embryo cryopreservation are unattractive for commercial purposes. It is expected that a successful cryopreservation of sheep embryos can push forward all other reproductive biotechnologies in this species, such as multiple ovulation and embryo transfer (MOET), artificial insemination, or in vitro production of embryos. This paper tries to discuss the current and future perspectives of cryopreservation of in vivo-and in vitro-produced sheep embryos concerning advantages and limitations for its practical use and possible solutions for improving methods to allow a higher survival rate of cryopreserved embryos.

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Molecular Mechanisms and Pathways Involved in Bovine Embryonic Genome Activation and Their Regulation by Alternative In Vivo and In Vitro Culture Conditions1

Cited by 146 publications

References 49 publications

Fine mapping of genome activation in bovine embryos by RNA sequencing

Fine mapping of genome activation in bovine embryos by RNA sequencing

Maternal embryokines that regulate development of the bovine preimplantation embryo

Cryopreservation of Sheep Produced Embryos – Current and Future Perspectives

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