Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development

Theriogenology

Volumn 81, Issue 9, 2014, Pages 1163-1173

  Cordova, A ^a,b   Perreau, C ^a   Uzbekova, S ^a   Ponsart, C ^b   Locatelli, Y ^a,c   Mermillod, P ^a  

^a CEMAGREF   (France)

^b UNCEIA Union Nationale des Cooperatives d'Elevage et d'Insemination Animale   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Apoptosis; Blastocyst; BOEC; Glucose; Methylation; Oxygen

Indexed keywords

BOVINAE;

ANIMAL; BLASTOCYST; BOVINE; COCULTURE; CYTOLOGY; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYOLOGY; EPITHELIUM CELL; FEMALE; FERTILIZATION IN VITRO; PHYSIOLOGY; PROCEDURES; UTERINE TUBE; VETERINARY;

ANIMALS; BLASTOCYST; CATTLE; COCULTURE TECHNIQUES; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; EPITHELIAL CELLS; FALLOPIAN TUBES; FEMALE; FERTILIZATION IN VITRO;

EID: 84899911529     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2014.01.012     Document Type: Article

References (64)

1. Watson A.J., Natale D.R., Barcroft L.C. Molecular regulation of blastocyst formation. Anim Reprod Sci 2004, 82-83:583-592.
2. Duszewska A.M., Reklewski Z., Pienkowski M., Karasiewicz J., Modlinski J.A. Development of bovine embryos on Vero/BRL cell monolayers (mixed co-culture). Theriogenology 2000, 54:1239-1247.
3. Eyestone W.H., First N.L. Co-culture of early cattle embryos to the blastocyst stage with oviducal tissue or in conditioned medium. J Reprod Fertil 1989, 85:715-720.
4. Goovaerts I.G., Leroy J.L., Rizos D., Bermejo-Alvarez P., Gutierrez-Adan A., Jorssen E.P., et al. Single in vitro bovine embryo production: coculture with autologous cumulus cells, developmental competence, embryo quality and gene expression profiles. Theriogenology 2011, 76:1293-1303.
5. Harvey M.B., Arcellana-Panlilio M.Y., Zhang X., Schultz G.A., Watson A.J. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture. Biol Reprod 1995, 53:532-540.
6. Johnson M.H., Nasr-Esfahani M.H. Radical solutions and cultural problems: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro?. Bioessays 1994, 16:31-38.
7. Rief S., Sinowatz F., Stojkovic M., Einspanier R., Wolf E., Prelle K. Effects of a novel co-culture system on development, metabolism and gene expression of bovine embryos produced in vitro. Reproduction 2002, 124:543-556.
8. Rieger D., Grisart B., Semple E., Van Langendonckt A., Betteridge K.J., Dessy F. Comparison of the effects of oviductal cell co-culture and oviductal cell-conditioned medium on the development and metabolic activity of cattle embryos. J Reprod Fertil 1995, 105:91-98.
9. Al Darwich A., Perreau C., Petit M.H., Papillier P., Dupont J., Guillaume D., et al. Effect of PUFA on embryo cryoresistance, gene expression and AMPKalpha phosphorylation in IVF-derived bovine embryos. Prostaglandins Other Lipid Mediat 2010, 93:30-36.
10. Pedersen M.E., Ozdas O.B., Farstad W., Tverdal A., Olsaker I. Effects of bovine oviduct epithelial cells, fetal calf serum and bovine serum albumin on gene expression in single bovine embryos produced in the synthetic oviduct fluid culture system. Reprod Fertil Dev 2005, 17:751-757.
11. Tse P.K., Lee Y.L., Chow W.N., Luk J.M., Lee K.F., Yeung W.S. Preimplantation embryos cooperate with oviductal cells to produce embryotrophic inactivated complement-3b. Endocrinology 2008, 149:1268-1276.
12. Edwards L.J., Batt P.A., Gandolfi F., Gardner D.K. Modifications made to culture medium by bovine oviduct epithelial cells: changes to carbohydrates stimulate bovine embryo development. Mol Reprod Dev 1997, 46:146-154.
13. Lonergan P., Rizos D., Kanka J., Nemcova L., Mbaye A.M., Kingston M., et al. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction 2003, 126:337-346.
14. Rizos D., Lonergan P., Boland M.P., Arroyo-García R., Pintado B., de la Fuente J., et al. Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol Reprod 2002, 66:589-595.
15. Enright B.P., Lonergan P., Dinnyes A., Fair T., Ward F.A., Yang X., et al. Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology 2000, 54:659-673.
16. Rizos D., Ward F., Duffy P., Boland M.P., Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 2002, 61:234-248.
17. Driver A.M., Penagaricano F., Huang W., Ahmad K.R., Hackbart K.S., Wiltbank M.C., et al. RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics 2012, 13:118.
18. Dovolou E., Clemente M., Amiridis G.S., Messinis I.E., 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 Dom Anim 2011, 46:862-869.
19. Rizos D., Clemente M., Bermejo-Alvarez P., de La Fuente J., Lonergan P., Gutierrez-Adan A. Consequences of in vitro culture conditions on embryo development and quality. Reprod Dom Anim 2008, 43(Suppl 4):44-50.
20. Ju S., Rui R., Lu Q., Lin P., Guo H. Analysis of apoptosis and methyltransferase mRNA expression in porcine cloned embryos cultured in vitro. J Assist Reprod Genet 2010, 27:49-59.
21. Pantaleon M., Ryan J.P., Gil M., Kaye P.L. An unusual subcellular localization of GLUT1 and link with metabolism in oocytes and preimplantation mouse embryos. Biol Reprod 2001, 64:1247-1254.
22. Guerin P., El Mouatassim S., Menezo Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 2001, 7:175-189.
23. Melka M.G., Rings F., Holker M., Tholen E., Havlicek V., Besenfelder U., et al. Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos. Reprod Dom Anim 2010, 45:915-921.
24. Huang H.F., He R.H., Sun C.C., Zhang Y., Meng Q.X., Ma Y.Y. Function of aquaporins in female and male reproductive systems. Hum Reprod Update 2006, 12:785-795.
25. Donnay I., Faerge I., Grondahl C., Verhaeghe B., Sayoud H., Ponderato N., et al. Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology 2004, 62:1093-1107.
26. Holm P., Booth P.J., Schmidt M.H., Greve T., Callesen H. High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 1999, 52:683-700.
27. Goossens K., Van Poucke M., Van Soom A., Vandesompele J., Van Zeveren A., Peelman L.J. Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev Biol 2005, 5:27.
28. Goossens K., Van Soom A., Van Poucke M., Vandaele L., Vandesompele J., Van Zeveren A., et al. Identification and expression analysis of genes associated with bovine blastocyst formation. BMC Dev Biol 2007, 7:64.
29. Khan D.R., Dube D., Gall L., Peynot N., Ruffini S., Laffont L., et al. Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One 2012, 7:e34110.
30. Thibodeaux J.K., Menezo Y., Roussel J.D., Hansel W., Goodeaux L.L., Thompson D.L., et al. Coculture of in vitro fertilized bovine embryos with oviductal epithelial cells originating from different stages of the estrous cycle. J Dairy Sci 1992, 75:1448-1455.
31. Plourde D., Vigneault C., Lemay A., Breton L., Gagne D., Laflamme I., et al. Contribution of oocyte source and culture conditions to phenotypic and transcriptomic variation in commercially produced bovine blastocysts. Theriogenology 2012, 78:116-131. e111-113.
32. Takahashi M. Oxidative stress and redox regulation on in vitro development of mammalian embryos. J Reprod Dev 2012, 58:1-9.
33. Bavister B.D. Culture of preimplantation embryos: facts and artifacts. Hum Reprod Update 1995, 1:91-148.
34. Barnett D.K., Bavister B.D. What is the relationship between the metabolism of preimplantation embryos and their developmental competence?. Mol Reprod Dev 1996, 43:105-133.
35. Harvey A.J. The role of oxygen in ruminant preimplantation embryo development and metabolism. Anim Reprod Sci 2007, 98:113-128.
36. Harvey A.J., Kind K.L., Thompson J.G. Regulation of gene expression in bovine blastocysts in response to oxygen and the iron chelator desferrioxamine. Biol Reprod 2007, 77:93-101.
37. Joo B.S., Kim M.K., Na Y.J., Moon H.S., Lee K.S., Kim H.D. The mechanism of action of coculture on embryo development in the mouse model: direct embryo-to-cell contact and the removal of deleterious components. Fertil Steril 2001, 75:193-199.
38. Bavister B. Oxygen concentration and preimplantation development. Reprod Biomed Online 2004, 9:484-486.
39. Vandaele L., Mateusen B., Maes D., de Kruif A., Van Soom A. Is apoptosis in bovine in vitro produced embryos related to early developmental kinetics and in vivo bull fertility?. Theriogenology 2006, 65:1691-1703.
40. Gandolfi F., Moor R.M. Stimulation of early embryonic development in the sheep by co-culture with oviduct epithelial cells. J Reprod Fertil 1987, 81:23-28.
41. Desai N., Goldfarb J. Co-cultured human embryos may be subjected to widely different microenvironments: pattern of growth factor/cytokine release by Vero cells during the co-culture interval. Hum Reprod 1998, 13:1600-1605.
42. Gutierrez-Adan A., Rizos D., Fair T., Moreira P.N., Pintado B., de la Fuente J., et al. Effect of speed of development on mRNA expression pattern in early bovine embryos cultured in vivo or in vitro. Mol Reprod Dev 2004, 68:441-448.
43. Betts D.H., King W.A. Genetic regulation of embryo death and senescence. Theriogenology 2001, 55:171-191.
44. Fear J.M., Hansen P.J. Developmental changes in expression of genes involved in regulation of apoptosis in the bovine preimplantation embryo. Biol Reprod 2011, 84:43-51.
45. Lu W.J., Lee N.P., Kaul S.C., Lan F., Poon R.T., Wadhwa R., et al. Mortalin-p53 interaction in cancer cells is stress dependent and constitutes a selective target for cancer therapy. Cell Death Differ 2011, 18:1046-1056.
46. Matwee C., Kamaruddin M., Betts D.H., Basrur P.K., King W.A. The effects of antibodies to heat shock protein 70 in fertilization and embryo development. Mol Hum Reprod 2001, 7:829-837.
47. Dix D.J., Garges J.B., Hong R.L. Inhibition of hsp70-1 and hsp70-3 expression disrupts preimplantation embryogenesis and heightens embryo sensitivity to arsenic. Mol Reprod Dev 1998, 51:373-380.
48. Ufer C., Wang C.C. The roles of glutathione peroxidases during embryo development. Front Mol Neurosci 2011, 4:12.
49. Roy M., Gauvreau D., Bilodeau J.F. Expression of superoxide dismutases in the bovine oviduct during the estrous cycle. Theriogenology 2008, 70:836-842.
50. Correa G.A., Rumpf R., Mundim T.C., Franco M.M., Dode M.A. Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim Reprod Sci 2008, 104:132-142.
51. Flentjar N.J., Crack P.J., Boyd R., Malin M., de Haan J.B., Hertzog P., et al. Mice lacking glutathione peroxidase-1 activity show increased TUNEL staining and an accelerated inflammatory response in brain following a cold-induced injury. Exp Neurol 2002, 177:9-20.
52. Kind K.L., Collett R.A., Harvey A.J., Thompson J.G. Oxygen-regulated expression of GLUT-1, GLUT-3, and VEGF in the mouse blastocyst. Mol Reprod Dev 2005, 70:37-44.
53. Thompson J.G., McNaughton C., Gasparrini B., McGowan L.T., Tervit H.R. Effect of inhibitors and uncouplers of oxidative phosphorylation during compaction and blastulation of bovine embryos cultured in vitro. J Reprod Fertil 2000, 118:47-55.
54. Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 2002, 64:993-998.
55. Deb G.K., Jin J.I., Kwon T.H., Choi B.H., Bang J.I., Dey S.R., et al. Improved blastocyst development of single cow OPU-derived presumptive zygotes by group culture with agarose-embedded helper embryos. Reprod Biol Endocrinol 2011, 9:121.
56. Shi L., Wu J. Epigenetic regulation in mammalian preimplantation embryo development. Reprod Biol Endocrinol 2009, 7:59.
57. Oron E., Ivanova N. Cell fate regulation in early mammalian development. Phys Biol 2012, 9:045002.
58. Leonhardt H., Page A.W., Weier H.U., Bestor T.H. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 1992, 71:865-873.
59. Okano M., Bell D.W., Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
60. Duranthon V., Watson A.J., Lonergan P. Preimplantation embryo programming: transcription, epigenetics, and culture environment. Reproduction 2008, 135:141-150.
61. Sagirkaya H., Misirlioglu M., Kaya A., First N.L., Parrish J.J., Memili E. Developmental and molecular correlates of bovine preimplantation embryos. Reproduction 2006, 131:895-904.
62. Barrera D., Garcia E.V., Sinowatz F., Palma G.A., Jimenez-Diaz M.A., Miceli D.C. Expression of DNA methyltransferase genes in four-cell bovine embryos cultured in the presence of oviductal fluid. Anat Histol Embryol 2013, 42:312-315.
63. Henault M.A., Killian G.J. Synthesis and secretion of lipids by bovine oviduct mucosal explants. J Reprod Fertil 1993, 98:431-438.
64. Agre P., Kozono D. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett 2003, 555:72-78.