Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0077
Animal Reproduction (AR)
Conference Paper

Oocyte related factors impacting on embryo quality: relevance for in vitro embryo production

Fabienne Nuttinck

Downloads: 0
Views: 799

Abstract

The outcome of pregnancy is closely linked to early events that occur during the onset of embryogenesis. The first stages in embryonic development are mainly governed by the storage of maternal factors present in the oocyte at the time of fertilisation. In this review, we outline the different classes of oocyte transcripts that may be involved in activation of the embryonic genome as well as those associated with epigenetic reprogramming, imprinting maintenance or the control of transposon mobilisation during preimplantation development. We also report the influence of cumulus-oocyte crosstalk during the maturation process on the oocyte transcriptome and how in vitro procedures can affect these interactions.

Keywords

cumulus cells, germinal-somatic interactions, maternal RNAs, oocyte maturation, preimplantation development.

References

Artus J, Chazaud C. 2014. A close look at the mammalian blastocyst: epiblast and primitive endoderm formation. Cell Mol Life Sci, 71:3327-3338.

Assou S, Al-edani T, Haouzi D, Philippe N, Lecellier CH, Piquemal D, Commes T, Ait-Ahmed O, Dechaud H, Hamamah S. 2013. MicroRNAs: new candidates for the regulation of the human cumulus- oocyte complex. Hum Reprod, 28:3038-3049.

Barckmann B, Simonelig M. 2013 Control of maternal mRNA stability in germ cells and early embryos. Biochim Biophys Acta, 1829:714-724.

Berg DK, van Leeuwen J, Beaumont S, Berg M, Pfeffer PL. 2010. Embryo loss in cattle between days 7 and 16 of pregnancy. Theriogenology, 73:250-260.

Bettegowda A, Yao J, Sen A, Li Q, Lee KB, Kobayashi Y, Patel OV, Coussens PM, Ireland JJ, Smith GW. 2007. JY-1, an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle. Proc Natl Acad Sci USA, 104:17602-17607.

Bogliotti YS, Ross PJ. 2012. Mechanisms of histone H3 lysine 27 trimethylation remodeling during early mammalian development. Epigenetics, 7:976-981.

Bouckenheimer J, Assou S, Riquier S, Hou C, Philippe N, Sansac C, Lavabre-Bertrand T, Commes T, Lemaitre JM, Boureux A, De Vos J. 2016. Long non-coding RNAs in human early embryonic development and their potential in ART. Hum Reprod Update, 23:19-40.

Bouckenheimer J, Fauque P, Lecellier CH, Bruno C, Commes T, Lemaitre JM, De Vos J, Assou S. 2018. Differential long non-coding RNA expression profiles in human oocytes and cumulus cells. Sci Rep, 8:2202. doi: 10.1038/s41598-018-20727-0.

Brown HM, Dunning KR, Sutton-McDowall M, Gilchrist RB, Thompson JG, Russell DL. 2017. Failure to launch: aberrant cumulus gene expression during oocyte in vitro maturation. Reproduction, 153:R109-R120.

Bui LC, Evsikov AV, Khan DR, Archilla C, Peynot N, Henaut A, Le Bourhis D, Vignon X, Renard JP, Duranthon V. 2009. Retrotransposon expression as a defining event of genome reprogramming in fertilized and cloned bovine embryos. Reproduction, 138:289- 299.

Cakmak H, Franciosi F, Zamah AM, Cedars MI, Conti M. 2016. Dynamic secretion during meiotic reentry integrates the function of the oocyte and cumulus cells. Proc Natl Acad Sci USA, 113:2424-2429.

Canovas S, Cibelli JB, Ross PJ. 2012. Jumonji domain-containing protein 3 regulates histone 3 lysine 27 methylation during bovine preimplantation development. Proc Natl Acad Sci USA, 109:2400-2405.

Canovas S, Ross PJ. 2016. Epigenetics in preimplantation mammalian development. Theriogenology, 86:69-79.

Chen J, Torcia S, Xie F, Lin CJ, Cakmak H, Franciosi F, Horner K, Onodera C, Song JS, Cedars MI, Ramalho-Santos M, Conti M. 2013. Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat Cell Biol, 15:1415- 1423.

Conti M, Hsieh M, Zamah AM, Oh JS. 2012. Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol, 356:65- 73.

Conti M, Franciosi F. 2018. Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Hum Reprod Update, 24:245- 266.

Coticchio G, Dal Canto M, Mignini Renzini M, Guglielmo MC, Brambillasca F, Turchi D, Novara PV, Fadini R. 2015. Oocyte maturation: gametesomatic cells interactions, meiotic resumption, cytoskeletal dynamics and cytoplasmic reorganization. Hum Reprod Update, 21:427-454.

Dallaire A, Simard MJ. 2016. The implication of microRNAs and endo-siRNAs in animal germline and early development. Dev Biol, 416:18-25.

Deutsch DR, Frohlich T, Otte KA, Beck A, Habermann FA, Wolf E, Arnold GJ. 2014. Stagespecific proteome signatures in early bovine embryo development. J Proteome Res, 13:4363-4376.

Elhamamsy AR. 2017. Role of DNA methylation in imprinting disorders: an updated review. J Assist Reprod Genet, 34:549-562.

Gad A, Hoelker M, Besenfelder U, Havlicek V, Cinar U, Rings F, Held E, Dufort I, Sirard MA, Schellander K, Tesfaye D. 2012. Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod, 87:100. doi: 10.1095/biolreprod.112.099697.

Graf A, Krebs S, Zakhartchenko V, Schwalb B, Blum H, Wolf E. 2014. Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc Natl Acad Sci USA, 111:4139-4144.

Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature, 466:835-840.

Guo J, Zhang T, Guo Y, Sun T, Li H, Zhang X, Yin H, Cao G, Yin Y, Wang H, Shi L, Guo X, Sha J, Eppig JJ, Su YQ. 2018. Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice. Proc Natl Acad Sci USA, 115:E5326- E5333.

Kim JH, Richter JD. 2007. RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev, 21:2571-2579.

Kouzarides T. 2007. Chromatin modifications and their function. Cell, 128:693-705.

Lee KB, Wee G, Zhang K, Folger JK, Knott JG, Smith GW. 2014. Functional role of the bovine oocytespecific protein JY-1 in meiotic maturation, cumulus expansion, and subsequent embryonic development. Biol Reprod, 90:69. doi: 10.1095/biolreprod.113.115071.

Li R, Albertini DF. 2013. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol, 14:141-152.

Lodde V, Luciano AM, Franciosi F, Labrecque R, Sirard MA. 2017. Accumulation of chromatin remodelling enzyme and histone transcripts in bovine oocytes. Results Probl Cell Differ, 63:223-255.

Lonergan P, Fair T, Forde N, Rizos D. 2016. Embryo development in dairy cattle. Theriogenology, 86:270- 277.

Macaulay AD, Gilbert I, Caballero J, Barreto R, Fournier E, Tossou P, Sirard MA, Clarke HJ, Khandjian EW, Richard FJ, Hyttel P, Robert C. 2014. The gametic synapse: RNA transfer to the bovine oocyte. Biol Reprod, 91:90. doi: 10.1095/biolreprod.114.119867.

Macaulay AD, Gilbert I, Scantland S, Fournier E, Ashkar F, Bastien A, Saadi HA, Gagne D, Sirard MA, Khandjian EW, Richard FJ, Hyttel P, Robert C. 2016. Cumulus cell transcripts transit to the bovine oocyte in preparation for maturation. Biol Reprod, 94:16. doi: 10.1095/biolreprod.114.127571.

Mattick JS, Rinn JL. 2015. Discovery and annotation of long noncoding RNAs. Nat Struct Mol Biol, 22:5-7.

May-Panloup P, Chretien MF, Malthiery Y, Reynier P. 2007. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol, 77:51-83.

McGinnis LK, Limback SD, Albertini DF. 2013. Signaling modalities during oogenesis in mammals. Curr Top Dev Biol, 102:227-242.

Mondou E, Dufort I, Gohin M, Fournier E, Sirard MA. 2012. Analysis of microRNAs and their precursors in bovine early embryonic development. Mol Hum Reprod, 18:425-434.

Nuttinck F, Reinaud P, Tricoire H, Vigneron C, Peynot N, Mialot JP, Mermillod P, Charpigny G. 2002. Cyclooxygenase-2 is expressed by cumulus cells during oocyte maturation in cattle. Mol Reprod Dev, 61:93-101.

Nuttinck F, Marquant-Le Guienne B, Clement L, Reinaud P, Charpigny G, Grimard B. 2008. Expression of genes involved in prostaglandin E2 and progesterone production in bovine cumulus-oocyte complexes during in vitro maturation and fertilization. Reproduction, 135:593-603.

Nuttinck F, Gall L, Ruffini S, Laffont L, Clement L, Reinaud P, Adenot P, Grimard B, Charpigny G, Marquant-Le Guienne B. 2011. PTGS2-related PGE2 affects oocyte MAPK phosphorylation and meiosis progression in cattle: late effects on early embryonic development. Biol Reprod, 84:1248-1257.

Nuttinck F, Jouneau A, Charpigny G, Hue I, Richard C, Adenot P, Ruffini S, Laffont L, Chebrout M, Duranthon V, Guienne BM. 2017. Prosurvival effect of cumulus prostaglandin G/H synthase 2/prostaglandin2 signaling on bovine blastocyst: impact on in vivo posthatching development. Biol Reprod, 96:531-541.

Prochazka R, Blaha M, Nemcova L. 2017. Significance of epidermal growth factor receptor signaling for acquisition of meiotic and developmental competence in mammalian oocytes. Biol Reprod, 97:537-549.

Ribeiro ES, Greco LF, Bisinotto RS, Lima FS, Thatcher WW, Santos JE. 2016. Biology of preimplantation conceptus at the onset of elongation in dairy cows. Biol Reprod, 94:97. doi: 10.1095/biolreprod.115.134908.

Richani D, Gilchrist RB. 2018 The epidermal growth factor network: role in oocyte growth, maturation and developmental competence. Hum Reprod Update, 24:1- 14.

Richter JD. 2007. CPEB: a life in translation. Trends Biochem Sci, 32:279-285.

Rocha JC, Passalia F, Matos FD, Maserati MP, Jr., Alves MF, Almeida TG, Cardoso BL, Basso AC, Nogueira MF. 2016. Methods for assessing the quality of mammalian embryos: how far we are from the gold standard? JBRA Assist Reprod, 20:150-158.

Roovers EF, Rosenkranz D, Mahdipour M, Han CT, He N, Chuva de Sousa Lopes SM, van der Westerlaken LA, Zischler H, Butter F, Roelen BA, Ketting RF. 2015. Piwi proteins and piRNAs in mammalian oocytes and early embryos. Cell Rep, 10:2069-2082.

Ruiz-Orera J, Messeguer X, Subirana JA, Alba MM. 2014. Long non-coding RNAs as a source of new peptides. Elife, 3:e03523. doi: 10.7554/eLife.03523.

Russell SJ, Stalker L, Gilchrist G, Backx A, Molledo G, Foster RA, LaMarre J. 2016. Identification of PIWIL1 isoforms and their expression in bovine testes, oocytes, and early embryos. Biol Reprod, 94:75. doi: 10.1095/biolreprod.115.136721.

Russell SJ, Patel M, Gilchrist G, Stalker L, Gillis D, Rosenkranz D, LaMarre J. 2017 Bovine piRNA-like RNAs are associated with both transposable elements and mRNAs. Reproduction, 153:305-318.

Saha P, Verma S, Pathak RU, Mishra RK. 2017. Long noncoding RNAs in mammalian development and diseases. Adv Exp Med Biol, 1008:155-198.

Schroder SS, Tsikolia N, Weizbauer A, Hue I, Viebahn C. 2016. Paraxial nodal expression reveals a novel conserved structure of the left-right organizer in four mammalian species. Cells Tissues Organs, 201:77- 87.

Sepulveda-Rincon LP, Solanas Edel L, SerranoRevuelta E, Ruddick L, Maalouf WE, Beaujean N. 2016. Early epigenetic reprogramming in fertilized, cloned, and parthenogenetic embryos. Theriogenology, 86:91-98.

Shimada M, Umehara T, Hoshino Y. 2016. Roles of epidermal growth factor (EGF)-like factor in the ovulation process. Reprod Med Biol, 15:201-216.

Sinha PB, Tesfaye D, Rings F, Hossien M, Hoelker M, Held E, Neuhoff C, Tholen E, Schellander K, Salilew-Wondim D. 2017. MicroRNA-130b is involved in bovine granulosa and cumulus cells function, oocyte maturation and blastocyst formation. J Ovarian Res, 10:37. doi: 10.1186/s13048-017-0336-1.

Sirard MA, Richard F, Blondin P, Robert C. 2006. Contribution of the oocyte to embryo quality. Theriogenology, 65:126-136.

Sirois J. 1994 Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology, 135:841- 848.

Sousa Martins JP, Liu X, Oke A, Arora R, Franciosi F, Viville S, Laird DJ, Fung JC, Conti M. 2016. DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation. J Cell Sci, 129:1271-1282.

Susor A, Jansova D, Anger M, Kubelka M. 2016. Translation in the mammalian oocyte in space and time. Cell Tissue Res, 363:69-84.

Svoboda P. 2017. Long and small noncoding RNAs during oocyte-to-embryo transition in mammals. Biochem Soc Trans, 45:1117-1124.

Tadros W, Lipshitz HD. 2009. The maternal-to- zygotic transition: a play in two acts. Development, 136:3033-3042.

Taylor DH, Chu ET, Spektor R, Soloway PD. 2015. Long non-coding RNA regulation of reproduction and development. Mol Reprod Dev, 82:932-956.

Tejomurtula J, Lee KB, Tripurani SK, Smith GW, Yao J. 2009. Role of importin alpha8, a new member of the importin alpha family of nuclear transport proteins, in early embryonic development in cattle. Biol Reprod, 81:333-342.

Telford NA, Watson AJ, Schultz GA. 1990. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev, 26:90-100.

Tesfaye D, Gebremedhn S, Salilew-Wondim D, Hailay T, Hoelker M, Grosse-Brinkhaus C, Schellander K. 2017. MicroRNAs: tiny molecules with significant role in mammalian follicular and oocyte development. Reproduction, 155:R121-R135.

Tripurani SK, Lee KB, Wang L, Wee G, Smith GW, Lee YS, Latham KE, Yao J. 2011a. A novel functional role for the oocyte-specific transcription factor newborn ovary homeobox (NOBOX) during early embryonic development in cattle. Endocrinology, 152:1013-1023.

Tripurani SK, Lee KB, Wee G, Smith GW, Yao J. 2011b. MicroRNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis. BMC Dev Biol, 11:25. doi: 10.1186/1471-213X-11-25.

Vigneault C, Gravel C, Vallee M, McGraw S, Sirard MA. 2009. Unveiling the bovine embryo transcriptome during the maternal-to-embryonic transition. Reproduction, 137:245-257.

Weill L, Belloc E, Bava FA, Mendez R. 2012. Translational control by changes in poly(A) tail length: recycling mRNAs. Nat Struct Mol Biol, 19:577-585.

Zhang H, Liu J, Tai Y, Zhang X, Zhang J, Liu S, Lv J, Liu Z, Kong Q. 2017. Identification and characterization of L1-specific endo-siRNAs essential for early embryonic development in pig. Oncotarget, 8:23167-23176.

Zheng H, Huang B, Zhang B, Xiang Y, Du Z, Xu Q, Li Y, Wang Q, Ma J, Peng X, Xu F, Xie W. 2016. genetic memory by reprogramming of histone modifications in mammals. Mol Cell, 63:1066- 1079.

5b76c5250e8825cb6c8068aa animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections