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Published in: Journal of Assisted Reproduction and Genetics 3/2019

01-03-2019 | Gamete Biology

Simulated physiological oocyte maturation has side effects on bovine oocytes and embryos

Authors: Eduardo M. Razza, Hanne S. Pedersen, Lotte Stroebech, Patricia K. Fontes, Haja N. Kadarmideen, Henrik Callesen, Maria Pihl, Marcelo F. G. Nogueira, Poul Hyttel

Published in: Journal of Assisted Reproduction and Genetics | Issue 3/2019

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Abstract

Purpose

Oocyte maturation is a complex process involving nuclear and cytoplasmic modulations, during which oocytes acquire their ability to become fertilized and support embryonic development. The oocyte is apparently “primed” for maturation during its development in the dominant follicle. As bovine oocytes immediately resume meiosis when cultured, it was hypothesized that delaying resumption of meiosis with cyclic nucleotide modulators before in vitro maturation (IVM) would allow the oocytes to acquire improved developmental competence.

Methods

We tested the Simulated Physiological Oocyte Maturation (SPOM) system that uses forskolin and 3-isobutyl-1-methylxanthine for 2 h prior to IVM against two different systems of conventional IVM (Con-IVM). We evaluated the ultrastructure of matured oocytes and blastocysts and also assessed the expression of 96 genes related to embryo quality in the blastocysts.

Results

In summary, the SPOM system resulted in lower blastocyst rates than both Con-IVM systems (30 ± 9.1 vs. 35 ± 8.7; 29 ± 2.6 vs. 38 ± 2.8). Mature SPOM oocytes had significantly increased volume and number of vesicles, reduced volume and surface density of large smooth endoplasmic reticulum clusters, and lower number of mitochondria than Con-IVM oocytes. SPOM blastocysts showed only subtle differences with parallel undulations of adjacent trophectoderm plasma membranes and peripherally localized ribosomes in cells of the inner cell mass compared with Con-IVM blastocysts. SPOM blastocysts, however, displayed significant downregulation of genes related to embryonic developmental potential when compared to Con-IVM blastocysts.

Conclusions

Our results show that the use of the current version of the SPOM system may have adverse effects on oocytes and blastocysts calling for optimized protocols for improving oocyte competence.
Appendix
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Literature
1.
go back to reference Pincus G, Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro : I. the activation of ovarian eggs. J Exp Med. 1935;62:665–75.CrossRefPubMedPubMedCentral Pincus G, Enzmann EV. The comparative behavior of mammalian eggs in vivo and in vitro : I. the activation of ovarian eggs. J Exp Med. 1935;62:665–75.CrossRefPubMedPubMedCentral
2.
go back to reference Edwards RG. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature. 1965;208:349–51.CrossRefPubMed Edwards RG. Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature. 1965;208:349–51.CrossRefPubMed
3.
go back to reference Fair T, Hyttel P, Greve T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev. 1995;42:437–42.CrossRefPubMed Fair T, Hyttel P, Greve T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev. 1995;42:437–42.CrossRefPubMed
4.
go back to reference Hyttel P, Fair T, Callesen H, Greve T. Oocyte growth, capacitation and final maturation in cattle. Theriogenology. 1997;47:23–32.CrossRef Hyttel P, Fair T, Callesen H, Greve T. Oocyte growth, capacitation and final maturation in cattle. Theriogenology. 1997;47:23–32.CrossRef
5.
go back to reference Assey RJ, Hyttel P, Greve T, Purwantara B. Oocyte morphology in dominant and subordinate follicles. Mol Reprod Dev. 1994;37:335–44.CrossRefPubMed Assey RJ, Hyttel P, Greve T, Purwantara B. Oocyte morphology in dominant and subordinate follicles. Mol Reprod Dev. 1994;37:335–44.CrossRefPubMed
6.
go back to reference Holm P, Callesen H. In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application. Reprod Nutr Dev. 1998;38:579–94.CrossRefPubMed Holm P, Callesen H. In vivo versus in vitro produced bovine ova: similarities and differences relevant for practical application. Reprod Nutr Dev. 1998;38:579–94.CrossRefPubMed
7.
go back to reference Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. United States 2010. p. 366–9. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. United States 2010. p. 366–9.
8.
go back to reference Vaccari S, Weeks JL, Hsieh M, Menniti FS, Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod. 2009;81:595–604.CrossRefPubMedPubMedCentral Vaccari S, Weeks JL, Hsieh M, Menniti FS, Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod. 2009;81:595–604.CrossRefPubMedPubMedCentral
9.
go back to reference Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, et al. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development. 2009;136:1869–78.CrossRefPubMedPubMedCentral Norris RP, Ratzan WJ, Freudzon M, Mehlmann LM, Krall J, Movsesian MA, et al. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development. 2009;136:1869–78.CrossRefPubMedPubMedCentral
10.
go back to reference Richard FJ, Tsafriri A, Conti M. Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod. 2001;65:1444–51.CrossRefPubMed Richard FJ, Tsafriri A, Conti M. Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod. 2001;65:1444–51.CrossRefPubMed
11.
12.
go back to reference Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool. 1974;187:383–6.CrossRefPubMed Cho WK, Stern S, Biggers JD. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J Exp Zool. 1974;187:383–6.CrossRefPubMed
13.
go back to reference Oliveira e Silva I, Vasconcelos RB, Caetano JV, Gulart LV, Camargo LS, Báo SN, et al. Induction of reversible meiosis arrest of bovine oocytes using a two-step procedure under defined and nondefined conditions. Theriogenology. 2011;75:1115–24.CrossRefPubMed Oliveira e Silva I, Vasconcelos RB, Caetano JV, Gulart LV, Camargo LS, Báo SN, et al. Induction of reversible meiosis arrest of bovine oocytes using a two-step procedure under defined and nondefined conditions. Theriogenology. 2011;75:1115–24.CrossRefPubMed
14.
go back to reference Thomas RE, Thompson JG, Armstrong DT, Gilchrist RB. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol Reprod. 2004;71:1142–9.CrossRefPubMed Thomas RE, Thompson JG, Armstrong DT, Gilchrist RB. Effect of specific phosphodiesterase isoenzyme inhibitors during in vitro maturation of bovine oocytes on meiotic and developmental capacity. Biol Reprod. 2004;71:1142–9.CrossRefPubMed
15.
go back to reference Ponderato N, Crotti G, Turini P, Duchi R, Galli C, Lazzari G. Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF. Mol Reprod Dev. 2002;62:513–8.CrossRefPubMed Ponderato N, Crotti G, Turini P, Duchi R, Galli C, Lazzari G. Embryonic and foetal development of bovine oocytes treated with a combination of butyrolactone I and roscovitine in an enriched medium prior to IVM and IVF. Mol Reprod Dev. 2002;62:513–8.CrossRefPubMed
16.
go back to reference Luciano AM, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod. 2004;70:465–72.CrossRefPubMed Luciano AM, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod. 2004;70:465–72.CrossRefPubMed
17.
go back to reference Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina SC, Fadini R, et al. Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod. 2014;91:61.CrossRefPubMed Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina SC, Fadini R, et al. Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod. 2014;91:61.CrossRefPubMed
18.
go back to reference Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod. 2010;25:2999–3011.CrossRefPubMed Albuz FK, Sasseville M, Lane M, Armstrong DT, Thompson JG, Gilchrist RB. Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum Reprod. 2010;25:2999–3011.CrossRefPubMed
19.
go back to reference Gilchrist RB, Luciano AM, Richani D, Zeng HT, Wang X, Vos MD, et al. Oocyte maturation and quality: role of cyclic nucleotides. Reproduction. 2016;152:R143–57.CrossRefPubMed Gilchrist RB, Luciano AM, Richani D, Zeng HT, Wang X, Vos MD, et al. Oocyte maturation and quality: role of cyclic nucleotides. Reproduction. 2016;152:R143–57.CrossRefPubMed
20.
go back to reference Hyttel P, Madsen I. Rapid method to prepare mammalian oocytes and embryos for transmission electron microscopy. Acta Anat (Basel). 1987;129:12–4.CrossRef Hyttel P, Madsen I. Rapid method to prepare mammalian oocytes and embryos for transmission electron microscopy. Acta Anat (Basel). 1987;129:12–4.CrossRef
22.
go back to reference Dadarwal D, Adams GP, Hyttel P, Brogliatti GM, Caldwell S, Singh J. Organelle reorganization in bovine oocytes during dominant follicle growth and regression. Reprod Biol Endocrinol. 2015;13:124.CrossRefPubMedPubMedCentral Dadarwal D, Adams GP, Hyttel P, Brogliatti GM, Caldwell S, Singh J. Organelle reorganization in bovine oocytes during dominant follicle growth and regression. Reprod Biol Endocrinol. 2015;13:124.CrossRefPubMedPubMedCentral
23.
go back to reference Zoller LC. A quantitative electron microscopic analysis of the membrana granulosa of rat preovulatory follicles. Acta Anat (Basel). 1984;118:218–23.CrossRef Zoller LC. A quantitative electron microscopic analysis of the membrana granulosa of rat preovulatory follicles. Acta Anat (Basel). 1984;118:218–23.CrossRef
24.
go back to reference Baddeley AJ, Gundersen HJ, Cruz-Orive LM. Estimation of surface area from vertical sections. J Microsc. 1986;142:259–76.CrossRefPubMed Baddeley AJ, Gundersen HJ, Cruz-Orive LM. Estimation of surface area from vertical sections. J Microsc. 1986;142:259–76.CrossRefPubMed
25.
go back to reference Robertson I, Nelson R. Certification of the embryos. In: SM S, editor. Manual of the International Embryo Transfer Society. Savoy: Stringfellow DAS; 1998. p. 103–34. Robertson I, Nelson R. Certification of the embryos. In: SM S, editor. Manual of the International Embryo Transfer Society. Savoy: Stringfellow DAS; 1998. p. 103–34.
26.
go back to reference Li HJ, Sutton-McDowall ML, Wang X, Sugimura S, Thompson JG, Gilchrist RB. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum Reprod. 2016;31:810–21.CrossRefPubMed Li HJ, Sutton-McDowall ML, Wang X, Sugimura S, Thompson JG, Gilchrist RB. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum Reprod. 2016;31:810–21.CrossRefPubMed
27.
go back to reference Shu YM, Zeng HT, Ren Z, Zhuang GL, Liang XY, Shen HW, et al. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reprod. 2008;23:504–13.CrossRefPubMed Shu YM, Zeng HT, Ren Z, Zhuang GL, Liang XY, Shen HW, et al. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reprod. 2008;23:504–13.CrossRefPubMed
28.
go back to reference Zeng HT, Ren Z, Guzman L, Wang X, Sutton-McDowall ML, Ritter LJ, et al. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum Reprod. 2013;28:1536–45.CrossRefPubMed Zeng HT, Ren Z, Guzman L, Wang X, Sutton-McDowall ML, Ritter LJ, et al. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum Reprod. 2013;28:1536–45.CrossRefPubMed
29.
go back to reference Zeng HT, Richani D, Sutton-McDowall ML, Ren Z, Smitz JE, Stokes Y, et al. Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol Reprod. 2014;91:47.CrossRefPubMed Zeng HT, Richani D, Sutton-McDowall ML, Ren Z, Smitz JE, Stokes Y, et al. Prematuration with cyclic adenosine monophosphate modulators alters cumulus cell and oocyte metabolism and enhances developmental competence of in vitro-matured mouse oocytes. Biol Reprod. 2014;91:47.CrossRefPubMed
30.
go back to reference Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB, Thompson JG. Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol Reprod. United States 2012. p. 87. Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB, Thompson JG. Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic protein 15. Biol Reprod. United States 2012. p. 87.
31.
go back to reference Kawashima I, Okazaki T, Noma N, Nishibori M, Yamashita Y, Shimada M. Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro. Reproduction. 2008;136:9–21.CrossRefPubMed Kawashima I, Okazaki T, Noma N, Nishibori M, Yamashita Y, Shimada M. Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro. Reproduction. 2008;136:9–21.CrossRefPubMed
32.
go back to reference Rose RD, Gilchrist RB, Kelly JM, Thompson JG, Sutton-McDowall ML. Regulation of sheep oocyte maturation using cAMP modulators. Theriogenology. 2013;79:142–8.CrossRefPubMed Rose RD, Gilchrist RB, Kelly JM, Thompson JG, Sutton-McDowall ML. Regulation of sheep oocyte maturation using cAMP modulators. Theriogenology. 2013;79:142–8.CrossRefPubMed
33.
go back to reference Guimarães AL, Pereira SA, Leme LO, Dode MA. Evaluation of the simulated physiological oocyte maturation system for improving bovine in vitro embryo production. Theriogenology. 2015;83:52–7.CrossRefPubMed Guimarães AL, Pereira SA, Leme LO, Dode MA. Evaluation of the simulated physiological oocyte maturation system for improving bovine in vitro embryo production. Theriogenology. 2015;83:52–7.CrossRefPubMed
34.
go back to reference Ulloa SM, Heinzmann J, Herrmann D, Timmermann B, Baulain U, Großfeld R, et al. Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote. 2015;23:367–77.CrossRefPubMed Ulloa SM, Heinzmann J, Herrmann D, Timmermann B, Baulain U, Großfeld R, et al. Effects of different oocyte retrieval and in vitro maturation systems on bovine embryo development and quality. Zygote. 2015;23:367–77.CrossRefPubMed
35.
go back to reference Bernal-Ulloa SM, Heinzmann J, Herrmann D, Hadeler KG, Aldag P, Winkler S, et al. Cyclic AMP affects oocyte maturation and embryo development in prepubertal and adult cattle. PLoS One. 2016;11:e0150264.CrossRefPubMedPubMedCentral Bernal-Ulloa SM, Heinzmann J, Herrmann D, Hadeler KG, Aldag P, Winkler S, et al. Cyclic AMP affects oocyte maturation and embryo development in prepubertal and adult cattle. PLoS One. 2016;11:e0150264.CrossRefPubMedPubMedCentral
36.
go back to reference Hyttel P, Callesen H, Greve T. Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J Reprod Fertil. 1986;76:645–56.CrossRefPubMed Hyttel P, Callesen H, Greve T. Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J Reprod Fertil. 1986;76:645–56.CrossRefPubMed
37.
go back to reference Burkart A, Xiong B, Baibakov B, Jiménez-Movilla M, Dean J. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J Cell Biol. 2012;197:37–81.CrossRefPubMedPubMedCentral Burkart A, Xiong B, Baibakov B, Jiménez-Movilla M, Dean J. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J Cell Biol. 2012;197:37–81.CrossRefPubMedPubMedCentral
39.
go back to reference Reynier P, May-Panloup P, Chrétien MF, Morgan CJ, Jean M, Savagner F, et al. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–9.CrossRefPubMed Reynier P, May-Panloup P, Chrétien MF, Morgan CJ, Jean M, Savagner F, et al. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–9.CrossRefPubMed
40.
go back to reference Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol. 2010;224:672–80.CrossRefPubMedPubMedCentral Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol. 2010;224:672–80.CrossRefPubMedPubMedCentral
41.
go back to reference Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, et al. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol Reprod. 2001;64:904–9.CrossRefPubMed Stojkovic M, Machado SA, Stojkovic P, Zakhartchenko V, Hutzler P, Goncalves PB, et al. Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol Reprod. 2001;64:904–9.CrossRefPubMed
42.
go back to reference Mohr LR, Trounson AO. Structural changes associated with freezing of bovine embryos. Biol Reprod. 1981;25:1009–25.CrossRefPubMed Mohr LR, Trounson AO. Structural changes associated with freezing of bovine embryos. Biol Reprod. 1981;25:1009–25.CrossRefPubMed
43.
go back to reference Mohr LR, Trounson AO. Comparative ultrastructure of hatched human, mouse and bovine blastocysts. J Reprod Fertil. 1982;66:499–504.CrossRefPubMed Mohr LR, Trounson AO. Comparative ultrastructure of hatched human, mouse and bovine blastocysts. J Reprod Fertil. 1982;66:499–504.CrossRefPubMed
44.
go back to reference Vedeler A, Pryme IF, Hesketh JE. Insulin and step-up conditions cause a redistribution of polysomes among free, cytoskeletal-bound and membrane-bound fractions in Krebs II ascites cells. Cell Biol Int Rep. 1990;14:211–8.CrossRefPubMed Vedeler A, Pryme IF, Hesketh JE. Insulin and step-up conditions cause a redistribution of polysomes among free, cytoskeletal-bound and membrane-bound fractions in Krebs II ascites cells. Cell Biol Int Rep. 1990;14:211–8.CrossRefPubMed
45.
go back to reference Hesketh JE, Horne Z, Campbell GP. Immunohistochemical evidence for an association of ribosomes with microfilaments in 3T3 fibroblasts. Cell Biol Int Rep. 1991;15:141–50.CrossRefPubMed Hesketh JE, Horne Z, Campbell GP. Immunohistochemical evidence for an association of ribosomes with microfilaments in 3T3 fibroblasts. Cell Biol Int Rep. 1991;15:141–50.CrossRefPubMed
46.
go back to reference Larsen TH, Saetersdal T. Translocation of 60S ribosomal subunit in spreading cardiac myocytes. J Histochem Cytochem. 1998;46:963–70.CrossRefPubMed Larsen TH, Saetersdal T. Translocation of 60S ribosomal subunit in spreading cardiac myocytes. J Histochem Cytochem. 1998;46:963–70.CrossRefPubMed
48.
go back to reference Tiffin GJ, Rieger D, Betteridge KJ, Yadav BR, King WA. Glucose and glutamine metabolism in pre-attachment cattle embryos in relation to sex and stage of development. J Reprod Fertil. 1991;93:125–32.CrossRefPubMed Tiffin GJ, Rieger D, Betteridge KJ, Yadav BR, King WA. Glucose and glutamine metabolism in pre-attachment cattle embryos in relation to sex and stage of development. J Reprod Fertil. 1991;93:125–32.CrossRefPubMed
49.
go back to reference Johnson MH, Nasr-Esfahani MH. Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? BioEssays. 1994;16:31–8.CrossRefPubMed Johnson MH, Nasr-Esfahani MH. Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? BioEssays. 1994;16:31–8.CrossRefPubMed
50.
go back to reference Dovolou E, Clemente M, Amiridis GS, Messinis IE, Kallitsaris A, Gutierrez-Adan A, et al. Effects of guaiazulene on in vitro bovine embryo production and on mRNA transcripts related to embryo quality. Reprod Domest Anim. 2011;46:862–9.CrossRefPubMed Dovolou E, Clemente M, Amiridis GS, Messinis IE, Kallitsaris A, Gutierrez-Adan A, et al. Effects of guaiazulene on in vitro bovine embryo production and on mRNA transcripts related to embryo quality. Reprod Domest Anim. 2011;46:862–9.CrossRefPubMed
51.
go back to reference Ghanem N, Salilew-Wondim D, Gad A, Tesfaye D, Phatsara C, Tholen E, et al. Bovine blastocysts with developmental competence to term share similar expression of developmentally important genes although derived from different culture environments. Reproduction. England 2011. p. 551–64. Ghanem N, Salilew-Wondim D, Gad A, Tesfaye D, Phatsara C, Tholen E, et al. Bovine blastocysts with developmental competence to term share similar expression of developmentally important genes although derived from different culture environments. Reproduction. England 2011. p. 551–64.
52.
go back to reference Zhang K, Haversat JM, Mager J. CTR9/PAF1c regulates molecular lineage identity, histone H3K36 trimethylation and genomic imprinting during preimplantation development. Dev Biol. 2013;383:15–27.CrossRefPubMedPubMedCentral Zhang K, Haversat JM, Mager J. CTR9/PAF1c regulates molecular lineage identity, histone H3K36 trimethylation and genomic imprinting during preimplantation development. Dev Biol. 2013;383:15–27.CrossRefPubMedPubMedCentral
53.
go back to reference Smith C, Berg D, Beaumont S, Standley NT, Wells DN, Pfeffer PL. Simultaneous gene quantitation of multiple genes in individual bovine nuclear transfer blastocysts. Reproduction. England 2007. p. 231-42. Smith C, Berg D, Beaumont S, Standley NT, Wells DN, Pfeffer PL. Simultaneous gene quantitation of multiple genes in individual bovine nuclear transfer blastocysts. Reproduction. England 2007. p. 231-42.
54.
go back to reference Harvey AJ, Navarrete Santos A, Kirstein M, Kind KL, Fischer B, Thompson JG. Differential expression of oxygen-regulated genes in bovine blastocysts. Mol Reprod Dev. 2007;74:290–9.CrossRefPubMed Harvey AJ, Navarrete Santos A, Kirstein M, Kind KL, Fischer B, Thompson JG. Differential expression of oxygen-regulated genes in bovine blastocysts. Mol Reprod Dev. 2007;74:290–9.CrossRefPubMed
55.
go back to reference Dafni H, Larson PE, Hu S, Yoshihara HA, Ward CS, Venkatesh HS, et al. Hyperpolarized 13C spectroscopic imaging informs on hypoxia-inducible factor-1 and myc activity downstream of platelet-derived growth factor receptor. Cancer Res. 2010;70:7400–10.CrossRefPubMedPubMedCentral Dafni H, Larson PE, Hu S, Yoshihara HA, Ward CS, Venkatesh HS, et al. Hyperpolarized 13C spectroscopic imaging informs on hypoxia-inducible factor-1 and myc activity downstream of platelet-derived growth factor receptor. Cancer Res. 2010;70:7400–10.CrossRefPubMedPubMedCentral
56.
go back to reference Cagnone GL, Dufort I, Vigneault C, Sirard MA. Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biol Reprod. 2012;86:50.CrossRefPubMed Cagnone GL, Dufort I, Vigneault C, Sirard MA. Differential gene expression profile in bovine blastocysts resulting from hyperglycemia exposure during early cleavage stages. Biol Reprod. 2012;86:50.CrossRefPubMed
58.
go back to reference Zhao YH, Zhou M, Liu H, Ding Y, Khong HT, Yu D, et al. Upregulation of lactate dehydrogenase a by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene. 2009;28:3689–701.CrossRefPubMed Zhao YH, Zhou M, Liu H, Ding Y, Khong HT, Yu D, et al. Upregulation of lactate dehydrogenase a by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene. 2009;28:3689–701.CrossRefPubMed
59.
go back to reference Hosseini SM, Dufort I, Caballero J, Moulavi F, Ghanaei HR, Sirard MA. Transcriptome profiling of bovine inner cell mass and trophectoderm derived from in vivo generated blastocysts. BMC Dev Biol. 2015;15:49.CrossRefPubMedPubMedCentral Hosseini SM, Dufort I, Caballero J, Moulavi F, Ghanaei HR, Sirard MA. Transcriptome profiling of bovine inner cell mass and trophectoderm derived from in vivo generated blastocysts. BMC Dev Biol. 2015;15:49.CrossRefPubMedPubMedCentral
60.
go back to reference Razza EM, Sudano MJ, Fontes PK, Franchi FF, Belaz KRA, Santos PH, et al. Treatment with cyclic adenosine monophosphate modulators prior to in vitro maturation alters the lipid composition and transcript profile of bovine cumulus? Oocyte complexes and blastocysts. Reprod Fertil Dev. 2018;30:1314.CrossRefPubMed Razza EM, Sudano MJ, Fontes PK, Franchi FF, Belaz KRA, Santos PH, et al. Treatment with cyclic adenosine monophosphate modulators prior to in vitro maturation alters the lipid composition and transcript profile of bovine cumulus? Oocyte complexes and blastocysts. Reprod Fertil Dev. 2018;30:1314.CrossRefPubMed
61.
go back to reference Ferguson EM, Leese HJ. Triglyceride content of bovine oocytes and early embryos. J Reprod Fertil. 1999;116:373–8.CrossRefPubMed Ferguson EM, Leese HJ. Triglyceride content of bovine oocytes and early embryos. J Reprod Fertil. 1999;116:373–8.CrossRefPubMed
62.
go back to reference Sturmey RG, Reis A, Leese HJ, McEvoy TG. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim. 2009;44(Suppl 3):50–8.CrossRefPubMed Sturmey RG, Reis A, Leese HJ, McEvoy TG. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Reprod Domest Anim. 2009;44(Suppl 3):50–8.CrossRefPubMed
63.
go back to reference Yao H, Ye J. Long chain acyl-CoA synthetase 3-mediated phosphatidylcholine synthesis is required for assembly of very low density lipoproteins in human hepatoma Huh7 cells. J Biol Chem. 2008;283:849–54.CrossRefPubMed Yao H, Ye J. Long chain acyl-CoA synthetase 3-mediated phosphatidylcholine synthesis is required for assembly of very low density lipoproteins in human hepatoma Huh7 cells. J Biol Chem. 2008;283:849–54.CrossRefPubMed
64.
65.
go back to reference Miyazaki M, Dobrzyn A, Sampath H, Lee SH, Man WC, Chu K, et al. Reduced adiposity and liver steatosis by stearoyl-CoA desaturase deficiency are independent of peroxisome proliferator-activated receptor-alpha. J Biol Chem. 2004;279:35017–24.CrossRefPubMed Miyazaki M, Dobrzyn A, Sampath H, Lee SH, Man WC, Chu K, et al. Reduced adiposity and liver steatosis by stearoyl-CoA desaturase deficiency are independent of peroxisome proliferator-activated receptor-alpha. J Biol Chem. 2004;279:35017–24.CrossRefPubMed
Metadata
Title
Simulated physiological oocyte maturation has side effects on bovine oocytes and embryos
Authors
Eduardo M. Razza
Hanne S. Pedersen
Lotte Stroebech
Patricia K. Fontes
Haja N. Kadarmideen
Henrik Callesen
Maria Pihl
Marcelo F. G. Nogueira
Poul Hyttel
Publication date
01-03-2019
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 3/2019
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-018-1365-4

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