Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-19T21:11:23.342Z Has data issue: false hasContentIssue false
  • English
  • Français

Exposure to follicular fluid during oocyte maturation and oviductal fluid during post-maturation does not improve in vitro embryo production in the horse

Published online by Cambridge University Press:  20 September 2017

Cécile Douet ,
Olivia Parodi ,
Nicola Antonio Martino ,
Giovanni Michele Lacalandra ,
Michele Nicassio ,
Fabrice Reigner ,
Stefan Deleuze ,
Maria Elena Dell'Aquila  and
Ghylène Goudet
Cécile Douet
Affiliation:
PRC, INRA, CNRS, IFCE, Université de Tours, 37380 Nouzilly, France.
Olivia Parodi
Affiliation:
PRC, INRA, CNRS, IFCE, Université de Tours, 37380 Nouzilly, France.
Nicola Antonio Martino
Affiliation:
Istituto Zooprofilattico Sperimentale per la Puglia e la Basilicata, Foggia, Italy. Università degli Studi di Bari Aldo Moro, Dipartimento di Bioscienze, Biotecnologie e Biofarmaceutica, 70010, Polo di Valenzano, Bari, Italy.
Giovanni Michele Lacalandra
Affiliation:
Università degli Studi di Bari Aldo Moro, Dipartimento dell'Emergenza e Trapianti d'Organo (DETO), 70010 Polo di Valenzano, BariItaly.
Michele Nicassio
Affiliation:
Università degli Studi di Bari Aldo Moro, Dipartimento dell'Emergenza e Trapianti d'Organo (DETO), 70010 Polo di Valenzano, BariItaly.
Fabrice Reigner
Affiliation:
PAO, INRA, 37380, Nouzilly, France.
Stefan Deleuze
Affiliation:
Faculté de Médecine vétérinaire, Département des Sciences Cliniques-Clinique Equine, Université de Liège, B-4000 Liège, Belgium.
Maria Elena Dell'Aquila
Affiliation:
Università degli Studi di Bari Aldo Moro, Dipartimento di Bioscienze, Biotecnologie e Biofarmaceutica, 70010, Polo di Valenzano, Bari, Italy.
Ghylène Goudet*
Affiliation:
INRA, UMR 85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France.
*
All correspondence to: Ghylène Goudet, INRA, UMR 85, Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France. Tel:+33 2 47 42 79 41. Fax: +33 2 47 42 77 43. E-mail: ghylene.goudet@inra.fr
Get access Rights & Permissions [Opens in a new window]

Summary

Most wild equids and many domestic horse breeds are at risk of extinction, so there is an urgent need for genome resource banking. Embryos cryopreservation allows the preservation of genetics from male and female and is the fastest method to restore a breed. In the equine, embryo production in vitro would allow the production of several embryos per cycle. Intracytoplasmic sperm injection (ICSI) is used to generate horse embryos, but it requires expensive equipment and expertise in micromanipulation, and blastocyst development rates remain low. No conventional in vitro fertilization (IVF) technique for equine embryo production is available. The development of culture conditions able to mimic the maturation of the oocyte in preovulatory follicular fluid (pFF) and the post-maturation in oviductal fluid (OF) may improve embryo production in vitro. Our aim was to analyse the effect of in vitro maturation in pFF and incubation in OF on in vitro maturation of equine oocytes, fertilization using conventional IVF or ICSI, and embryo development after culture in synthetic oviductal fluid (SOF) or DMEM-F12. Oocytes collected from slaughtered mares or by ovum pick up were matured in vitro in pFF or semi-synthetic maturation medium (MM). The in vitro maturation, fertilization and development rates were not statistically different between pFF and MM. After in vitro maturation, oocytes were incubated with or without OF. Post-maturation in OF did not significantly improve the fertilization and development rates. Thus, in our study, exposure to physiological fluids for oocyte maturation and post-maturation does not improve in vitro embryo production in the horse.

Keywords

EquineIVMIVFOocyteSpermatozoa
Type
Research Article
Information
Zygote , Volume 25 , Issue 5 , October 2017 , pp. 612 - 630
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, G. P., Ratto, M. H., Collins, C. W. & Bergfelt, D.R. (2009). Artificial insemination in South American camelids and wild equids. Theriogenology 71, 166–75.Google Scholar
Alm, H., Torner, H., Blottner, S., Nurnberg, G. & Kanitz, W. (2001). Effect of sperm cryopreservation and treatment with calcium ionophore or heparin on in vitro fertilization of horse oocytes. Theriogenology 56, 817–29.Google Scholar
Ambruosi, B., Accogli, G., Douet, C., Canepa, S., Pascal, G., Monget, P., Moros, C., Holmskov, U., Mollenhauer, J., Robbe-Masselot, C., Vidal, O., Desantis, S. & Goudet, G. (2013). Deleted in malignant brain tumor 1 is secreted in the oviduct and involved in the mechanism of fertilization in equine and porcine species. Reproduction 146, 119–33.Google Scholar
Ambruosi, B., Lacalandra, G. M., Iorga, A. I., De Santis, T., Mugnier, S., Matarrese, R., Goudet, G. & Dell'aquila, M.E. (2009). Cytoplasmic lipid droplets and mitochondrial distribution in equine oocytes: Implications on oocyte maturation, fertilization and developmental competence after ICSI. Theriogenology 71, 1093–104.CrossRefGoogle ScholarPubMed
Aviles, M., Gutierrez-Adan, A. & Coy, P. (2010). Oviductal secretions: will they be key factors for the future ARTs? Mol. Hum. Reprod. 16, 896–906.Google Scholar
Bézard, J., Magistrini, M., Duchamp, G. & Palmer, E. (1989). Chronology of equine fertilisation and embryonic development in vivo and in vitro . Equine Vet. J. Suppl. 8, 105–10.Google Scholar
Caillaud, M., Dell'aquila, M. E., De Santis, T., Nicassio, M., Lacalandra, G. M., Goudet, G. & Gerard, N. (2008). In vitro equine oocyte maturation in pure follicular fluid plus interleukin-1 and fertilization following ICSI. Anim. Reprod. Sci. 106, 431–9.Google Scholar
Carrasco, L. C., Romar, R., Aviles, M., Gadea, J. & Coy, P. (2008). Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle. Reproduction 136, 833–42.CrossRefGoogle ScholarPubMed
Choi, Y. H., Love, C. C., Varner, D. D. & Hinrichs, K. (2006). Equine blastocyst development after intracytoplasmic injection of sperm subjected to two freeze-thaw cycles. Theriogenology 65, 808–19.Google Scholar
Choi, Y. H., Varner, D. D., Love, C. C., Hartman, D. L. & Hinrichs, K. (2011). Production of live foals via intracytoplasmic injection of lyophilized sperm and sperm extract in the horse. Reproduction 142, 529–38.Google Scholar
Conforti, V. A., Vanderwall, D. K. & Woods, G.L. (2005). Effect of homologous follicular fluid from medium-sized and large follicles on in vitro maturation of equine cumulus–oocyte complexes. Reprod. Fertil. Dev. 17, 651–8.Google Scholar
Coy, P., Garcia-Vazquez, F. A., Visconti, P. E. & Aviles, M. (2012). Roles of the oviduct in mammalian fertilization. Reproduction 144, 649–60.Google Scholar
Deleuze, S., Goudet, G., Caillaud, M., Lahuec, C. & Duchamp, G. (2009). Efficiency of embryonic development after intrafollicular and intraoviductal transfer of in vitro and in vivo matured horse oocytes. Theriogenology 72, 203–9.CrossRefGoogle ScholarPubMed
Dell'Aquila, M. E., Albrizio, M., Maritato, F., Minoia, P. & Hinrichs, K. (2003). Meiotic competence of equine oocytes and pronucleus formation after intracytoplasmic sperm injection (ICSI) as related to granulosa cell apoptosis. Biol. Reprod. 68, 2065–72.Google Scholar
Dell'Aquila, M. E., Cho, Y. S., Minoia, P., Traina, V., Fusco, S., Lacalandra, G. M. & Maritato, F. (1997a). Intracytoplasmic sperm injection (ICSI) versus conventional IVF on abattoir-derived and in vitro-matured equine oocytes. Theriogenology 47, 1139–56.Google Scholar
Dell'Aquila, M. E., Cho, Y. S., Minoia, P., Traina, V., Lacalandra, G. M. & Maritato, F. (1997b). Effects of follicular fluid supplementation of in-vitro maturation medium on the fertilization and development of equine oocytes after in-vitro fertilization or intracytoplasmic sperm injection. Hum. Reprod. 12, 2766–72.Google Scholar
Dell'Aquila, M. E., Fusco, S., Lacalandra, G. M. & Maritato, F. (1996). In vitro maturation and fertilization of equine oocytes recovered during the breeding season. Theriogenology 45, 547–60.Google Scholar
Dell'Aquila, M. E., Masterson, M., Maritato, F. & Hinrichs, K. (2001). Influence of oocyte collection technique on initial chromatin configuration, meiotic competence, and male pronucleus formation after intracytoplasmic sperm injection (ICSI) of equine oocytes. Mol. Reprod. Dev. 60, 79–88.Google Scholar
Galli, C., Crotti, G., Turini, P., Duchi, R., Mari, G., Zavaglia, G., Duchamp, G., Daels, P. & Lazzari, G. (2002). Frozen–thawed embryos produced by ovum pick up of immature oocytes and ICSI are capable to establish pregnancies in the horse. Theriogenology 58, 705–8.Google Scholar
Goudet, G. (2011). Fertilisation in the horse and paracrine signalling in the oviduct. Reprod. Fertil. Dev. 23, 941–51.Google Scholar
Goudet, G., Belin, F., Mlodawska, W. & Bezard, J. (2000). Influence of epidermal growth factor on in vitro maturation of equine oocytes. J. Reprod. Fertil. Suppl. 56, 483–92.Google Scholar
Goudet, G., Bézard, J., Duchamp, G., Gérard, N. & Palmer, E. (1997). Equine oocyte competence for nuclear and cytoplasmic in vitro maturation: effect of follicle size and hormonal environment. Biol. Reprod. 57, 232–45.Google Scholar
Hawley, L. R., Enders, A. C. & Hinrichs, K. (1995). Comparison of equine and bovine oocyte–cumulus morphology within the ovarian follicle. Biol. Reprod. Monograph Series 1, 243–52.CrossRefGoogle Scholar
Hinrichs, K. (2012). Assisted reproduction techniques in the horse. Reprod. Fertil. Dev. 25, 80–93.Google Scholar
Hinrichs, K., Choi, Y. H., Love, L. B., Varner, D. D., Love, C. C. & Walckenaer, B.E. (2005). Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence. Biol. Reprod. 72, 1142–50.Google Scholar
Hinrichs, K., Love, C. C., Brinsko, S. P., Choi, Y. H. & Varner, D.D. (2002). In vitro fertilization of in vitro-matured equine oocytes: effect of maturation medium, duration of maturation, and sperm calcium ionophore treatment, and comparison with rates of fertilization in vivo after oviductal transfer. Biol. Reprod. 67, 256–62.Google Scholar
Kawashima, I., Okazaki, T., Noma, N., Nishibori, M., Yamashita, Y. & Shimada, M. (2008). 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 136, 9–21.CrossRefGoogle ScholarPubMed
Lange Consiglio, A., Dell'Aquila, M. E., Fiandanese, N., Ambruosi, B., Cho, Y. S., Bosi, G., Arrighi, S., Lacalandra, G. M. & Cremonesi, F. (2009). Effects of leptin on in vitro maturation, fertilization and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse. Reprod . Biol. Endocrinol. 7, 113.Google Scholar
Lazzari, G., Crotti, G., Turini, P., Duchi, R., Mari, G., Zavaglia, G., Barbacini, S. & Galli, C. (2002). Equine embryos at the compacted morula and blastocyst stage can be obtained by intracytoplasmic sperm injection (ICSI) of in vitro matured oocytes with frozen–thawed spermatozoa from semen of different fertilities. Theriogenology 58, 709–12.Google Scholar
Leemans, B., Gadella, B. M., Stout, T. A., Heras, S., Smits, K., Ferrer-Buitrago, M., Claes, E., Heindryckx, B., De Vos, W. H., Nelis, H., Hoogewijs, M. & Van Soom, A. (2015). Procaine induces cytokinesis in horse oocytes via a pH-dependent mechanism. Biol. Reprod. 93, 23.Google Scholar
Lopera-Vasquez, R., Hamdi, M., Maillo, V., Lloreda, V., Coy, P., Gutierrez-Adan, A., Bermejo-Alvarez, P. & Rizos, D. (2015). Effect of bovine oviductal fluid on development and quality of bovine embryos produced in vitro . Reprod. Fertil. Dev. doi: 10.1071/RD15238. [Epub ahead of print]Google Scholar
Martino, N. A., Marzano, G., Nicassio, M., Minervini, F., Cardinali, A., Lacalandra, G. M., Hinrichs, K. & Dell'aquila, M.E. (2016). Effects of verbascoside treatment during oocyte in vitro maturation on blastocyst development and bioenergetic/oxidative status after ICSI in the horse. J. Equine Vet. Sci. 41, 66.Google Scholar
McPartlin, L. A., Suarez, S. S., Czaya, C. A., Hinrichs, K. & Bedford-Guaus, S.J. (2009). Hyperactivation of stallion sperm is required for successful in vitro fertilization of equine oocytes. Biol. Reprod. 81, 199–206.Google Scholar
Meyers-Brown, G., Bidstrup, L. A., Famula, T. R., Colgin, M. & Roser, J.F. (2011). Treatment with recombinant equine follicle stimulating hormone (reFSH) followed by recombinant equine luteinizing hormone (reLH) increases embryo recovery in superovulated mares. Anim. Reprod. Sci. 128, 52–9.Google Scholar
Mugnier, S., Kervella, M., Douet, C., Canepa, S., Pascal, G., Deleuze, S., Duchamp, G., Monget, P. & Goudet, G. (2009). The secretions of oviduct epithelial cells increase the equine in vitro fertilization rate: are osteopontin, atrial natriuretic peptide A and oviductin involved? Reprod. Biol. Endocrinol. 7, 129.Google Scholar
Palmer, E., Bezard, J., Magistrini, M. & Duchamp, G. (1991). In vitro fertilization in the horse. A retrospective study. J. Reprod. Fertil. Suppl. 44, 375–84.Google Scholar
Smits, K., Govaere, J., Hoogewijs, M., Piepers, S. & Van Soom, A. (2012a). A pilot comparison of laser-assisted vs piezo drill ICSI for the in vitro production of horse embryos. Reprod. Domest. Anim. 47, e1–3.Google Scholar
Smits, K., Hoogewijs, M., Woelders, H., Daels, P. & Van Soom, A. (2012b). Breeding or assisted reproduction? Relevance of the horse model applied to the conservation of endangered equids. Reprod. Domest. Anim. 47 (Suppl. 4), 239–48.Google Scholar
Tremoleda, J. L., Stout, T. A., Lagutina, I., Lazzari, G., Bevers, M. M., Colenbrander, B. & Galli, C. (2003). Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation. Biol. Reprod. 69, 1895–906.Google Scholar
Zhang, J. J., Boyle, M. S., Allen, W. R. & Galli, C. (1989). Recent studies on in vivo fertilization of in vitro matured horse oocytes. Equine Vet. J. Suppl. 8, 101–4.Google Scholar
Zhang, J. J., Muzs, L. Z. & Boyle, M.S. (1990). In vitro fertilization of horse follicular oocytes matured in vitro . Mol. Reprod. Dev. 26, 361–5.Google Scholar