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Equine bone marrow mesenchymal or amniotic epithelial stem cells as feeder in a model for the in vitro culture of bovine embryos

Published online by Cambridge University Press:  21 December 2010

Anna Lange-Consiglio ,
Valentina Maggio ,
Laura Pellegrino  and
Fausto Cremonesi
Anna Lange-Consiglio
Affiliation:
Università degli Studi di Milano, Reproduction Unit, Large Animal Hospital, Faculty of Veterinary Medicine, Via dell'Università 6, 26900 Lodi, Italy.
Valentina Maggio
Affiliation:
Università degli Studi di Milano, Reproduction Unit, Large Animal Hospital, Faculty of Veterinary Medicine, Via dell'Università 6, 26900 Lodi, Italy.
Laura Pellegrino
Affiliation:
Università degli Studi di Milano, Reproduction Unit, Large Animal Hospital, Faculty of Veterinary Medicine, Via dell'Università 6, 26900 Lodi, Italy.
Fausto Cremonesi*
Affiliation:
Università degli Studi di Milano, Reproduction Unit, Large Animal Hospital, Faculty of Veterinary Medicine, Via dell'Università 6, 26900 Lodi, Italy.
*
All correspondence to: Fausto Cremonesi. Università degli Studi di Milano, Reproduction Unit, Large Animal Hospital, Faculty of Veterinary Medicine, Via dell'Università 6, 26900 Lodi, Italy. Tel: +39 02 50331150. Fax: +39 02 50331115. e-mail: [email protected]
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Summary

Various studies have shown that the in vitro culture environment is one of the key determinants of the blastocyst output. In the present study we investigated the effects of co-culturing bovine embryos with equine bone marrow mesenchymal stem cells (BM-MSCs) or equine amniotic epithelial stem cells (AE-SCs) on in vitro blastocysts development. BM specimens were obtained aseptically from sternal aspirates of horses under local anaesthesia and the isolated cells were resuspended in Dulbecco Modified Earle's Medium supplemented with 10 ng/ml of basic fibroblast growth factor (bFGF). Amniotic membranes were obtained from fresh placentas and, to release the AE cells, amniotic fragments were incubated with 0.05% trypsin for 45 min. Separated AE cells were plated in standard culture medium containing 10 ng/ml epidermal growth factor (EGF). Seven hundred and five cumulus–oocyte complexes were used and, after IVM and IVF, cumulus-free presumptive zygotes were randomly transferred into one of three co-culture systems in which they were cultured up to day 7: (1) co-culture with cumulus cells (control); (2) co-culture with BM-MSCs; and (3) co-culture with AE-SCs. Statistical analyses were performed by ANOVA. Blastocyst developmental rates were significantly different (p < 0.001) between control, AE-SCs and BM-MSCs (respectively 35.45, 41.84 and 30.09%). In conclusion, the AE-SC monolayer create a more suitable microenvironment necessary for inducing local cell activation and proliferation of the growing embryos in comparison with BM-MSCs and cumulus cells. It can be suggested that these cells secrete biologically active substances, including signalling molecules and growth factors of epithelial nature, different to those of the BM cells of mesenchymal origin.

Keywords

Amniotic cellsBovine embryosCo-cultureHorseMesenchymal cells
Type
Research Article
Information
Zygote , Volume 20 , Issue 1 , February 2012 , pp. 45 - 51
Copyright
Copyright © Cambridge University Press 2010

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References

Abe, H., Yamashita, S., Satoh, T. & Hoshi, H. (2002). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Mol. Reprod. Dev. 61, 57–66.CrossRefGoogle ScholarPubMed
Ali, A.A., Bilodeau, J.F. & Sirard, M.A. (2003). Antioxidant requirements for bovine oocytes vary during in vitro maturation, fertilization and development. Theriogenology 59, 939–49.CrossRefGoogle Scholar
Battut, I., Bezard, J. & Palmer, E. (1991). Establishment of equine oviduct cell monolayers for co-culture with early equine embryos. J. Reprod. Fertil. Suppl. 44, 393–403.Google ScholarPubMed
Cheng, L., Gearing, D.P., White, L.S., Compton, D.L., Schooley, K. & Donovan, P.J. (1994). Role of leukemia inhibitory factor and its receptor in mouse primordial germ cell growth. Development 120, 3145–53.CrossRefGoogle ScholarPubMed
Choi, Y.H., Chung, Y.G., Seidel, G.E. Jr. & Squires, E.L. (2001). Developmental capacity of equine oocytes matured and cultured in equine trophoblast-conditioned media. Theriogenology 56, 329–39.CrossRefGoogle ScholarPubMed
Choi, Y.H., Love, C.C., Varner, D.D. & Hinrichs, K. (2006a). Equine blastocyst development after intracytoplasmic injection of sperm subjected to two freeze–thaw cycles. Theriogenology 6, 808–19.CrossRefGoogle Scholar
Choi, Y.H., Love, L.B., Varner, D.D., & Hinrichs, K. (2006b). Holding immature equine oocytes in the absence of meiotic inhibitors: effect on germinal vesicle chromatin and blastocyst development after intracytoplasmic sperm injection. Theriogenology 66, 955–63.CrossRefGoogle ScholarPubMed
Costa Pereira, D., Nunes Dodeb, M.A. & Rumpf, R. (2005). Evaluation of different culture systems on the in vitro production of bovine embryos. Theriogenology 63, 1131–41.CrossRefGoogle Scholar
Cremonesi, F., Maggio, V. & Lange Consiglio, A. (2009). Equine amniotic epithelial or bone marrow mesenchymal stem cells differently support in vitro embryo development in a bovine IVC model. 35th Annual Conference of International Embryo Transfer Society (IETS) Conference, 3–7 January, San Diego, California CSIRO Publishing, Sidney, Australia. Reprod., Fertil. Dev. 21, 156.CrossRefGoogle Scholar
Cremonesi, F., Violini, S., Lange Consiglio, A., Ramelli, P., Ranzenigo, G. & Mariani, P. (2008). Isolation, in vitro culture and characterization of foal umbilical cord cells at birth. Vet. Res. Commun. 32 (Suppl. 1), S139–42.CrossRefGoogle ScholarPubMed
Dell'Aquila, M.E., Cho, Y.S., Minoia, P., Traina, V., Lacalandra, G.M. & Maritato, F. (1997). 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.CrossRefGoogle ScholarPubMed
Dolci, S., Williams, D.E., Ernst, M.K., Resnick, J.L., Brannan, C.I., Lock, L.F., Lyman, S.D., Boswell, H.S. & Donovan, P.J. (1991). Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352, 809–11.CrossRefGoogle ScholarPubMed
Donnay, I., Van Langendonckt, A., Auquier, P., Grisart, B., Vansteenbrugge, A. & Massip, A. (1997). Effects of coculture and embryo number on the in vitro development of bovine embryos. Theriogenology 47, 1549–61.CrossRefGoogle ScholarPubMed
Duszewska, A.M., Reklewski, Z., Pienkowski, M., Karasiewicz, J. & Modlinski, J.A. (2000). Development of bovine embryos on Vero/BRL cell monolayers (mixed co-culture). Theriogenology 54, 1239–47.CrossRefGoogle ScholarPubMed
Galli, C. & Lazzari, G. (2001). In vitro and in vivo culture in the sheep oviduct of equine embryos obtained by IVM and ICSI. In Proceedings of the Second Meeting of the European Equine Gamete Group (eds. Stout, T.A.E. & Wade, J.F.), pp. 55–6. Loosdrecht, The Netherlands Newmarket: R&W Publications.Google Scholar
Galli, C., Crotti, G., Duchi, R., Mari, G. & Lazzari, G. (2000). Embryonic development of equine oocytes fertilised by ICSI. In Proceedings of the Fifth International Symposium on Equine Embryo Transfer (eds. Katila, T. & Wade, J.F.), pp. 32–34. Havemeyer Foundation Monograph Series no. 3, Finland, Saari Unit of Helsinki University, July 6–9, Newmarket: R&W Publications.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 pickup of immature oocytes and ICSI are capable to establish pregnancies in the horse. Theriogenology 58, 705–8.Google Scholar
Galli, C., Colleoni, S., Duchi, R., Lagutina, I. & Lazzari, G. (2007). Developmental competence of equine oocytes and embryos obtained by in vitro procedures ranging from in vitro maturation and ICSI to embryo culture, cryopreservation and somatic cell nuclear transfer. Anim. Reprod. Sci. 98, 39–55.CrossRefGoogle ScholarPubMed
Gardner, D.K. (2008). Dissection of culture media for embryos: the most important and less important components and characteristics. Reprod. Fertil. Dev. 20, 9–18.CrossRefGoogle ScholarPubMed
Gardner, D.K. & Lane, M. (2000). Embryo culture systems. In Handbook of In Vitro Fertilization (eds. Trounson, A.O. & Gardner, D.K.) 2nd edn p. 558. Bocca Raton: CRC Press.Google Scholar
Gardner, D.K. & Lane, M. (2003). Towards a single embryo transfer. Reprod. Biomed. Online 6, 470–81.CrossRefGoogle ScholarPubMed
Gardner, D.K. & Lane, M. (2005). Ex vivo early embryo development and effects on gene expression and imprinting. Reprod. Fertil. Dev. 17, 361–70.CrossRefGoogle ScholarPubMed
Geshi, M., Yonai, M., Sakaguchi, M. & Nagai, T. (1999). Improvement of in vitro co-culture systems for bovine embryos using a low concentration of carbon dioxide and medium supplemented with β-mercaptoethanol. Theriogenology 51, 551–8.CrossRefGoogle ScholarPubMed
Harlow, G.M. & Quinn, P. (1982). Development of preimplantation mouse embryos in vivo and in vitro. Aust. J. Biol. Sci. 35, 187–93.CrossRefGoogle ScholarPubMed
Hatoya, S., Sugiyama, Y., Torii, R., Wijewardana, V., Kumagai, D., Sugiura, K., Kida, K., Kawate, N., Tamada, H., Sawada, T. & Inaba, T. (2006). Effect of co-culturing with embryonic fibroblasts on IVM, IVF and IVC of canine oocytes. Theriogenology 66, 1083–90.CrossRefGoogle ScholarPubMed
Hendriksen, P.J.M., Bevers, M.M. & Dieleman, S.J. (1999). Single IVP using BRL cell co-culture and serum yields a lower blastocyst rate than group culture. Theriogenology 5, 319.CrossRefGoogle Scholar
Koizumi, N.J., Inatomi, T.J. & Sotozono, T.J. (2000). Growth factor mRNA and protein in preserved human amniotic membrance. Cirr. Eye Res. 20, 173–7.CrossRefGoogle Scholar
Lange Consiglio, A., Corradetti, B., Bizzarro, D., Cassano, M. & Cremonesi, F. (2010). Horse amnion: a source of mesenchymal (amscs) and epithelial stem cells (aescs). 36th Annual Conference of International Embryo Transfer Society (IETS) Conference, 9–12 gennaio, Cordoba, Argentina. Reprod. Fertil. Dev. 22, 349. CSIRO Publishing, Sidney, Australia.CrossRefGoogle 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
Li, X., Morris, L.H-A. & Allen, W.R. (2001). Influence of co-culture during maturation on the developmental potential of equine oocytes fertilized by intracytoplasmic sperm injection (ICSI). Reproduction 121, 925–32.CrossRefGoogle ScholarPubMed
Li, A., Chandrakanthan, V., Chami, O. & O'Neill, C. (2007). Culture of zygotes increases TRP53 expression in B6 mouse embryos, which reduces embryo viability. Biol. Reprod. 76, 362–7.CrossRefGoogle ScholarPubMed
Lonergan, P., Fair, T., Corcoran, D. & Evans, A.C.O. (2006). Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos. Theriogenology 65, 137–52.CrossRefGoogle ScholarPubMed
Majumdar, M.K. (2000). Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J. Hematother. Stem Cell Res. 9, 841–8.CrossRefGoogle ScholarPubMed
Matsui, Y., Toksoz, D., Nishikawa, S., Nishikawa, S., Williams, D., Zsebo, K. & Hogan, B.L. (1991). Effect of Steel factor and leukaemia inhibitory factor on murine primordial germ cells in culture. Nature 353, 750–2.CrossRefGoogle ScholarPubMed
Park, J.S., Han, Y.M., Lee, C.S., Kim, S.J., Kim, Y.H., Lee, K.J., Lee, K. S. & Lee, K.K. (2000). Improved development of DNA-injected bovine embryos co-cultured with mouse embryonic fibroblast cells. Anim. Reprod. Sci. 59, 13–22.CrossRefGoogle ScholarPubMed
Rexroad, C.E. Jr & Powell, A.M. (1993). Development of ovine embryos co-cultured on oviductal cells, embryonic fibroblasts, or STO cell monolayers. Biol. Reprod. 49, 789–93.CrossRefGoogle ScholarPubMed
Rizos, D., Ward, F., Duffy, P., Boland, M.P. & Lonergan, P. (2002). 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. 61, 234–48.CrossRefGoogle ScholarPubMed
Rizos, D., Gutierrez-Adan, A., Perez-Garnelo, S., de la Fuente, J., Boland, M.P. & Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance, and messenger RNA expression. Biol. Reprod. 68, 236–43.CrossRefGoogle ScholarPubMed
Rosati, I., Berlinguer, F., Bogliolo, L., Leoni, G., Ledda, S. & Naitana, S. (2002). The effect of co-culture on the development of in vitro matured equine oocytes after intracytoplasmic sperm injection. Equine Vet. J. 34, 673–8.CrossRefGoogle Scholar
Vajta, G., Peura, T.T., Holm, P., Paldi, A., Greve, T., Trounson, A.O. & Callessen, H. (2000). New method for culture of zona-included or zona-free embryos: the well of the well (WOW) system. Mol. Reprod. Dev. 55, 256–64.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Van Soom, A., Yuan, Y.Q., Peelman, L.J., de Matos, D.G., Dewulf, J., Laevens, H. & De Kruif, A. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology 57, 1453–65.CrossRefGoogle ScholarPubMed
White, K.L., Hehnke, K., Rickords, L.F., Southern, L.L., Thompson, D.L. Jr & Wood, T.C. (1989). Early embryonic development in vitro by co-culture with oviductal epithelial cells in pigs. Biol. Reprod. 41, 425–30.CrossRefGoogle Scholar
www.vet-stem.com/technologies/regenerativecells.phpGoogle Scholar
Xie, C.Q., Lin, G., Luo, K.L., Luo, S.W. & Lu, G.X. (2004). Newly expressed proteins of mouse embryonic fibroblasts irradiated to be inactive. Biochem. Biophys. Res. Commun. 315, 581–8.CrossRefGoogle ScholarPubMed