Intrinsic quality of goat oocytes already found denuded at collection for in vitro embryo production.

Blastocyst; Cumulus cells; In vitro fertilization; In vitro maturation; Ovum pickup; Animals; Blastocyst/physiology; Cumulus Cells; Embryo Culture Techniques/veterinary; Embryonic Development/physiology; Female; Fertilization in Vitro/veterinary; Goats/embryology; In Vitro Oocyte Maturation Techniques/veterinary; Oocytes/physiology; Tissue and Organ Harvesting/veterinary; Embryo Culture Techniques; Embryonic Development; Fertilization in Vitro; Goats; In Vitro Oocyte Maturation Techniques; Oocytes; Tissue and Organ Harvesting; Small Animals; Food Animals; Animal Science and Zoology; Equine

Abstract :

[en] Although cumulus cells are essential for efficient oocyte maturation, the establishment of protocols that support IVD of embryos obtained from denuded oocytes (DOCs) is important for optimizing the use of reproductive biotechnologies. Thus, this study aimed to establish a protocol for IVD of goat DOC using different strategies of IVM and methods of oocyte activation. Four experiments were performed. Similar developmental competence of slaughterhouse DOC was obtained, regardless of maturation media (complex, semidefined or simplified). However, the ability to reach the blastocyst stage was affected by the activation method. Denuded oocytes subjected to parthenogenetic activation had greater (P < 0.05) development capacity, compared with those undergoing IVF with average cleavage rate of 83% and 75%, blastocyst rate of 49% and 28%, and blastocysts in relation to the cleaved embryos of 59% and 38, respectively. In addition, the quality of embryos evaluated after vitrification/warming was similar between parthenogenetic activation and IVF. Finally, we demonstrated that the coculture of cumulus-oocyte complex (COC) with DOC increased the competence of DOC at a ratio of 1:1 and 1:9 (DOC:COC). We believe that presence of cumulus cells (CCs) is not essential to the meiotic maturation, if at the time of removal of the oocyte from follicular environment, they already acquired competence to development. However, when the oocytes still need to acquire competence, the presence of CC may significantly contribute in their developmental capacity acquisition during IVM. Thus, regardless of the source, these oocytes will require longer time in IVM, contrary to what happens in the absence of CC. In conclusion, although DOC had a lower developmental potential, especially after IVF, they were able to produce blastocysts and the coculture of DOC with COC increased this developmental capacity.

Disciplines :

Animal production & animal husbandry

Author, co-author :

Souza-Fabjan, Joanna Maria Gonçalves; INRA, UMR7247, Physiologie de la Reproduction et des Comportements, INRA, CNRS, Université de Tours, Haras Nationaux, Nouzilly, France, Laboratory of Physiology and Control of Reproduction, Veterinary School, State University of Ceará, Fortaleza, CE, Brazil. Electronic address: joannavet@gmail.com

Locatelli, Yann; INRA, UMR7247, Physiologie de la Reproduction et des Comportements, INRA, CNRS, Université de Tours, Haras Nationaux, Nouzilly, France, Museum National d'Histoire Naturelle, Réserve de la Haute Touche, Obterre, France

Duffard, Nicolas; INRA, UMR7247, Physiologie de la Reproduction et des Comportements, INRA, CNRS, Université de Tours, Haras Nationaux, Nouzilly, France, Museum National d'Histoire Naturelle, Réserve de la Haute Touche, Obterre, France

Corbin, Emilie; INRA, UMR7247, Physiologie de la Reproduction et des Comportements, INRA, CNRS, Université de Tours, Haras Nationaux, Nouzilly, France

Batista, Ribrio Ivan Tavares Pereira; Laboratory of Physiology and Control of Reproduction, Veterinary School, State University of Ceará, Fortaleza, CE, Brazil

de Figueirêdo Freitas, Vicente José; Laboratory of Physiology and Control of Reproduction, Veterinary School, State University of Ceará, Fortaleza, CE, Brazil

Beckers, Jean-François ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF)

Mermillod, Pascal; INRA, UMR7247, Physiologie de la Reproduction et des Comportements, INRA, CNRS, Université de Tours, Haras Nationaux, Nouzilly, France

Language :

English

Title :

Intrinsic quality of goat oocytes already found denuded at collection for in vitro embryo production.

Publication date :

November 2016

Journal title :

Theriogenology

ISSN :

0093-691X

eISSN :

1879-3231

Publisher :

Elsevier Inc., United States

Volume :

Issue :

Pages :

1989 - 1998

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0093691X16302795?httpAccept=text/xml

Name of the research project :

CAPES-COFECUB

Funders :

Région Center

Funding text :

This work was supported by a grant from Région Center , France (PIVER program, #200800030493, 2008–2011) and from CAPES-COFECUB bilateral framework (grant 728/11 , 2011–2014).J.M.G. Souza-Fabjan was supported by CAPES and Ceará State University. The authors wish to thank CAPES-COFECUB bilateral framework for financial support of collaboration between the Ceará State University and INRA on goat IVP (grant 728/11, 2011–2013).

Available on ORBi :

since 08 January 2023

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Bibliography

[1] Sirard, M.A., Richard, F., Blondin, P., Robert, C., Contribution of the oocyte to embryo quality. Theriogenology 65 (2006), 126–136.
[2] Sohel, M.M., Hoelker, M., Noferesti, S.S., Salilew-Wondim, D., Tholen, E., Looft, C., et al. Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One, 8, 2013, e78505.
[3] Eppig, J.J., The relationship between cumulus cell-oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev Biol 89 (1982), 268–272.
[4] Macaulay, A.D., Gilbert, I., Caballero, J., Barreto, R., Fournier, E., Tossou, P., et al. The gametic synapse: RNA transfer to the bovine oocyte. Biol Reprod, 91, 2014, 90.
[5] Sasseville, M., Gagnon, M.C., Guillemette, C., Sullivan, R., Gilchrist, R.B., Richard, F.J., Regulation of gap junctions in porcine cumulus-oocyte complexes: contributions of granulosa cell contact, gonadotropins, and lipid rafts. Mol Endocrinol 23 (2009), 700–710.
[6] Salustri, A., Yanagishita, M., Hascall, V., Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev Biol 138 (1990), 26–32.
[7] Ball, G.D., Bellin, M.E., Ax, R.L., First, N.L., Glycosaminoglycans in bovine cumulus-oocyte complexes: morphology and chemistry. Mol Cell Endocrinol 28 (1982), 113–122.
[8] Tanghe, S., Van Soom, A., Mehrzad, J., Maes, D., Duchateau, L., de Kruif, A., Cumulus contributions during bovine fertilization in vitro. Theriogenology 60 (2003), 135–149.
[9] Schroeder, A.C., Eppig, J.J., The developmental capacity of mouse oocytes that matured spontaneously in vitro is normal. Dev Biol 102 (1984), 493–497.
[10] Vanderhyden, B.C., Armstrong, D.T., Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod 40 (1989), 720–728.
[11] Zhang, L., Jiang, S., Wozniak, P.J., Yang, X., Godke, R.A., Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro. Mol Reprod Dev 40 (1995), 338–344.
[12] Wongsrikeao, P., Kaneshige, Y., Ooki, R., Taniguchi, M., Agung, B., Nii, M., et al. Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod Domest Anim 40 (2005), 166–170.
[13] Liu, L., Trimarchi, J.R., Oldenbourg, R., Keefe, D.L., Increased birefringence in the meiotic spindle provides a new marker for the onset of activation in living oocytes. Biol Reprod 63 (2000), 251–258.
[14] Modina, S., Beretta, M., Lodde, V., Lauria, A., Luciano, A.M., Cytoplasmic changes and developmental competence of bovine oocytes cryopreserved without cumulus cells. Eur J Haematol Suppl 48 (2004), 337–346.
[15] Chang, H.C., Liu, H., Zhang, J., Grifo, J., Krey, L.C., Developmental incompetency of denuded mouse oocytes undergoing maturation in vitro is ooplasmic in nature and is associated with aberrant Oct-4 expression. Hum Reprod 20 (2005), 1958–1968.
[16] Xiong, B., Li, S., Ai, J.S., Yin, S., Yang, Y.C., Sun, S.C., et al. BRCA1 is required for meiotic spindle assembly and spindle assembly checkpoint activation in mouse oocytes. Biol Reprod 79 (2008), 718–726.
[17] Averty, B., Brandenhof, H.R., Greve, T., Development of in vitro matured and fertilized bovine embryos, cultured from day 1–5 post insemination in either menezo-B2 medium or in HECM-6 medium. Theriogenology 44 (1995), 935–945.
[18] Wani, N.A., Wani, G.M., Khan, M.Z., Sidiqi, M.A., Effect of different factors on the recovery rate of oocytes for in vitro maturation and in vitro fertilization procedures in sheep. Small Ruminant Res 34 (1999), 71–76.
[19] Paramio, M.T., Izquierdo, D., Current status of in vitro embryo production in sheep and goats. Reprod Domest Anim 49 (2014), 37–48.
[20] Chian, R.C., Niwa, K., Sirard, M.A., Effects of cumulus cells on male pronuclear formation and subsequent early development of bovine oocytes in vitro. Theriogenology 41 (1994), 1499–1508.
[21] Keskintepe, L., Darwish, G.M., Kenimer, A.T., Brackett BGTerm development of caprine embryos derived from immature oocytes in vitro. Theriogenology 42 (1994), 527–535.
[22] Tajik, P., Shams Esfandabadi, N., In vitro maturation of caprine oocytes in different culture media. Small Ruminant Res 47 (2003), 155–158.
[23] Rao, B.S., Naaidu, K.S., Amarnath, D., Vagdevi, R., Rao, A.S., Brahmaioh, K.V., et al. In vitro maturation of sheep oocytes in different media during breeding and non breeding season. Small Ruminant Res 43 (2002), 31–36.
[24] Sagirkaya, H., Misirlioglu, M., Kaya, A., First, N.L., Parrish, J.J., Memili, E., Developmental potential of bovine oocytes cultured in different maturation and culture conditions. Anim Reprod Sci 101 (2007), 225–240.
[25] Souza-Fabjan, J.M.G., Locatelli, Y., Duffard, N., Corbin, E., Touzé, J.L., Perreau, C., et al. In vitro embryo production in goats: slaughterhouse and laparoscopic ovum pick up–derived oocytes have different kinetics and requirements regarding maturation media. Theriogenology 81 (2014), 1021–1031.
[26] Souza, J.M.G., Duffard, N., Bertoldo, M.J., Locatelli, Y., Corbin, E., Fatet, A., et al. Influence of heparin or the presence of cumulus cells during fertilization on the in vitro production of goat embryos. Anim Reprod Sci 138 (2013), 82–89.
[27] Souza-Fabjan, J.M.G., Panneau, B., Duffard, N., Locatelli, Y., Figueiredo, J.R., Freitas, V.J.F., et al. In vitro production of small ruminant embryos: late improvements and further research. Theriogenology 81 (2014), 1149–1162.
[28] Guignot, F., Bouttier, A., Baril, G., Salvetti, P., Pignon, P., Beckers, J.F., et al. Improved vitrification method allowing direct transfer of goat embryos. Theriogenology 66 (2006), 1004–1011.
[29] Dinnyes, A., Carolan, C., Lonergan, P., Massip, A., Mermillod, P., Survival of frozen or vitrified bovine blastocysts produced in vitro in synthetic oviduct fluid. Theriogenology 46 (1996), 1425–1439.
[30] Brower, P.T., Schultz, R.M., Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 90 (1982), 140–153.
[31] Dode, M.A., Graves, C., Involvement of steroid hormones on in vitro maturation of pig oocytes. Theriogenology 57 (2002), 811–821.
[32] Cognie, Y., Baril, G., Poulin, N., Mermillod, P., Current status of embryo technologies in sheep and goat. Theriogenology 59 (2003), 171–188.
[33] Tibary, A., Anouassi, A., Khatir, H., Update on reproductive biotechnologies in small ruminants and camelids. Theriogenology 64 (2005), 618–638.
[34] Paramio, M.T., In vivo and in vitro embryo production in goats. Small Ruminant Res 89 (2010), 144–148.
[35] Magalhães-Padilha, D.M., Duarte, A.B., Araujo, V.R., Saraiva, M.V., Almeida, A.P., Rodrigues, G.Q., et al. Steady-state level of insulin-like growth factor-I (IGF-I) receptor mRNA and the effect of IGF-I on the in vitro culture of caprine preantral follicles. Theriogenology 77 (2012), 206–213.
[36] Cognie, Y., Poulin, N., Locatelli, Y., Mermillod, P., State-of-the-art production, conservation and transfer of in-vitro-produced embryos in small ruminants. Reprod Fertil Dev 16 (2004), 437–445.
[37] Locatelli, Y., Poulin, N., Baril, G., Touze, J., Fatet, A., Beckers, J., et al. In vitro maturation treatment affects developmental competence of laparoscopic ovum pickup-derived oocytes in follicle- stimulating hormone-stimulated goats. Reprod Fertil Dev 20 (2008), 182–183.
[38] Han, Y.M., Wang, W.H., Abeydeera, L.R., Peterson, A.L., Kim, J.H., Murphy, C., Pronuclear location before the first cell division determines ploidy of polyspermic pig embryos. Biol Reprod 61 (1999), 1340–1346.
[39] Ducibella, T., Anderson, E., Albertini, D.F., Aalberg, J., Rangarajan, S., Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev Biol 130 (1988), 184–197.
[40] Ducibella, T., Kurasawa, S., Rangarajan, S., Kopf, G.S., Schultz, R.M., Precocious loss of cortical granules during mouse oocyte meiotic maturation and correlation with an egg-induced modification of the zona pellucida. Dev Biol 137 (1990), 46–55.
[41] Dell'Aquila, M.E., De Felici, M., Massari, S., Maritatos, F., Minoia, P., Effects of fetuin on zona pellucida hardening and fertilizability of equine oocytes matured in vitro. Biol Reprod 61 (1999), 533–540.
[42] Zhang, X., Rutledge, J., Armstrong, D.T., Studies on zona hardening in rat oocytes that are matured in vitro in a serum-free medium. Mol Reprod Dev 28 (1991), 292–296.
[43] Downs, S.M., Schroeder, A.C., Eppig, J.J., Serum maintains the fertilizability of mouse oocytes matured in vitro by preventing the hardening of the zona pellucida. Gam Res 15 (1986), 115–122.
[44] Galeati, G., Modina, S., Lauria, A., Mattioli, M., Follicle somatic cells influence pig oocyte penetrability and cortical granule distribution. Mol Reprod Dev 29 (1991), 40–46.
[45] Fatehi, A.N., Zeinstra, E.C., Kooij, R.V., Colenbrander, B., Bevers, M.M., Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 57 (2002), 1347–1355.
[46] Nyholt de Prada, J.K., Lee, Y.S., Latham, K.E., Chaffin, C.L., Vande-Voort, C.A., Role for cumulus cell-produced EGF-like ligands during primate oocyte maturation in vitro. Am J Physiol Endocrinol Metab 296 (2009), E1049–E1058.
[47] Abbas, M.M., Evans, J.J., Sin, I.L., Gooneratne, A., Hill, A., Benny, P.S., Vascular endothelial growth factor and leptin: regulation in human cumulus cells and in follicles. Acta Obstet Gynecol Scand Suppl 82 (2003), 997–1003.
[48] Luciano, A.M., Lodde, V., Beretta, M.S., Colleoni, S., Lauria, A., Modina, S., Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 3',5'-monophosphate, and glutathione. Mol Reprod Dev 71 (2005), 389–397.
[49] Perreault, S.D., Barbee, R.R., Slott, V.L., Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol 125 (1988), 181–186.
[50] Yoshida, M., Ishigaki, K., Nagai, T., Chikyu, M., Pursel, V.G., Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod 49 (1993), 89–94.
[51] Sutovsky, P., Schatten, G., Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol Reprod 56 (1997), 1503–1512.