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Development, molecular composition and freeze tolerance of bovine embryos cultured in TCM-199 supplemented with hyaluronan

Published online by Cambridge University Press:  01 February 2008

A.T. Palasz*
Affiliation:
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain.
P. Beltrán Breña
Affiliation:
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain.
Marcelo F. Martinez
Affiliation:
Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK Canada S7N 5B4.
S.S. Perez-Garnelo
Affiliation:
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain.
M.A. Ramirez
Affiliation:
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain.
A. Gutiérrez-Adán
Affiliation:
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain.
J. De la Fuente
Affiliation:
Dpto. de Reproducción Animal y Conservación de Recursos Zoogenéticos, INIA, Ctra de la Coruña Km 5.9, Madrid 28040, Spain.
*
1All correspondence to: A.T. Palasz. Ministerio De Educación y Ciencia, INIA, Ctra. de La Coruna km 5, 9 Madrid 28040, Spain. Tel: +34 91 347 40 23. Fax: +34 91 347 40 14. e-mail: Palasz@inia.es

Summary

Hyaluronan (HA) is glycosaminoglycan that is present from the start of embryonic development and its role and concentration increases with embryo development. The objective of this study was to evaluate if the presence of HA in TCM-199 culture medium had an effect on the development and quality of bovine embryos. There was no effect of HA on the total number of zygotes developing to blastocysts on day 7, however more expanded and hatched blastocyst stages were observed on days 8 and 9 in the group supplemented with HA (p < 0.05). Following freeze/thawing, significantly more (p < 0.05) embryos cultured in medium supplemented with HA hatched than those cultured in TCM-199 alone or those with BSA. Medium supplemented with HA and BSA significantly increased the level of expression of glucose metabolism Glut-1 gene and embryo compaction Cx43 gene (p < 0.05), and had no effect on Glut-5 and IGF-II expression. In addition, HA presence in culture decreased the level of expression of apoptosis Bax and oxidative stress SOX genes (p < 0.05). There was significant difference in total number of nuclei between TCM-199 medium only and the remaining media containing BSA or HA plus BSA, between which there was no difference. In summary, our results indicate that the addition of high molecular weight HA to TCM-199 medium that contains BSA on day 4 of culture improved embryo development to hatching and hatched blastocysts and the quality of produced embryos, which were superior to embryos cultured without HA addition.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

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References

Assmann, V., Jenkinson, D., Marshall, J.F. & Hart, IR. (1999). The intracellular hyaluronan receptor RHAMM/IHABP interacts with microtubules and actin filaments. J. Cell Sci. 112, 3943–54.Google Scholar
Barnes, D. & Sato, G. (1980). Serum-free cell culture: a unifying approach. Cell 22, 649–55.CrossRefGoogle ScholarPubMed
Bavister, B.D. (1992). Co-culture for embryo development: is it really necessary? Hum. Reprod. 10, 1339–41.Google Scholar
Bavister, B.D., Rose-Hellekant, T.A. & Pinyopummintr, T. (1992). Development of in vitro matured/in vitro fertilized bovine embryos into morulae and blastocysts in defined culture media. Theriogenology 37, 111–26.CrossRefGoogle Scholar
Bergqvist, A.S., Yokoo, M., Heldin, P., Frendin, J., Sato, E. & Rodríguez-Martínez, H. (2005). Hyaluronan and its binding proteins in the epithelium and intraluminal fluid of the bovine oviduct. Zygote 13, 207–18.CrossRefGoogle ScholarPubMed
Brachet, A. (1913). Recherches sur le determinisme herditaire de l'oeuf des mammiferes. Development in vitro de jeunes vesicules blastdermiques du lapin. Arch. Biol. 28, 4478–504.Google Scholar
Brill, A., Torchinsky, A., Carp, H. & Toder, V. (1999). The role of apoptosis in normal and abnormal embryonic development. J. Assis. Reprod. Gen. 16, 512–9.Google Scholar
Cukierman, E., Pankov, R. & Yamada, K.M. (2002). Cell interactions with three-dimensional matrices. Curr. Biol. 14, 633–9.CrossRefGoogle ScholarPubMed
Diez, C., Heyman, Y., Le Bourhis, D., Guyader-Joly, C., Degrouard, J. & Renard, J.P. (2001). Delipidating in vitro-produced bovine zygotes: effect on further development and consequences for freezability. Theriogenology 55, 923–36.Google Scholar
Enright, B.P., Lonergan, P., Dinnyes, A., Fair, T., Ward, F.A., Yang, X. & Boland, M.P. (2000). Culture of in vitro produced bovine zygotes in vitro vs in vivo: implications for early embryo development and quality. Theriogenology 54, 659–73.CrossRefGoogle ScholarPubMed
Entwistle, J., Hall, C.L. & Turley, E.A. (1996). HA receptors: regulators of signaling to the cytoskeleton. J. Cell Chem. 61, 569–77.Google Scholar
Eppig, J.J. (1981). Regulation by sulfated glycosaminoglycans of the expansion of cumuli oophori isolated from mice. Biol. Reprod. 25, 599608.CrossRefGoogle ScholarPubMed
Fair, T., Lonergan, P., Dinnyes, A., Cottell, D., Hyttel, P., Ward, F.A. & Boland, M.P. (2001). Ultrastructure of bovine blastocysts following cryopreservation: effect of method of embryo production on blastocyst quality. Mol. Reprod. Dev. 58, 186–95.3.0.CO;2-N>CrossRefGoogle Scholar
Fenderson, B.A., Stamenkovic, I. & Aruffo, A. (1993). Localization of hyaluronan in mouse embryo during implantation, gastrulation and organogenesis. Differentiation 54, 8598.CrossRefGoogle ScholarPubMed
Furnus, C.C., de Matos, D.G. & Martínez, A.G. (1998). Effect of hyaluronic acid on development of in vitro produced bovine embryos. Theriogenology 49, 1489–99.Google Scholar
Furnus, C.C., Valcarcel, A., Dulout, F.N. & Errecalde, A.L. (2003). The hyaluronic acid receptor (CD44) is expressed in bovine oocytes and early stage embryos. Theriogenology 60, 1633–44.CrossRefGoogle ScholarPubMed
Gjorret, J.O., Avery, B., Larsson, L.I., Schellander, K. & Hyttel, P. (2001). Apoptosis in bovine blastocysts produced in vivo and in vitro. Theriogenology 55, 321.Google Scholar
Guerin, P., El Mouatassim, S. & Menozo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175–89.Google Scholar
Hansen, P.J. (2006). Realizing the promise of IVF in cattle – an overview. Theriogenology 65, 119–25.CrossRefGoogle ScholarPubMed
Harvey, A.J., Kind, K.L., Pantaleon, M., Armstrong, D.T. & Thompson, J.G. (2004). Oxygen-regulated gene expression in bovine blastocysts. Biol. Reprod. 71, 1108–19.Google Scholar
Keskintepe, L., Burnely, C.A. & Brackett, B.G. (1995). Production of viable bovine blastocysts in defined in vitro conditions. Biol. Reprod. 52, 1410–7.CrossRefGoogle ScholarPubMed
Knudson, W., Aguiar, D.J., Hua, Q. & Knudson, C.B. (1996). CD44-anchored hyaluronan-rich pericellular matrices: an ultrastructural and biochemical analysis. Exp. Cell Res. 228, 216–28.CrossRefGoogle ScholarPubMed
Kobayashi, Y., Okarnoto, A. & Nishinari, K. (1994). Viscoelasticity of hyaluronic acid with different molecular weight. Biorheology 31, 235–44.CrossRefGoogle Scholar
Krisher, R.L., Gibbons, J.R. & Gwazdauskas, F.C. (1998). Effectiveness of Menuzo's B2 medium with buffalo rat liver cells for development of in vitro matured/in vitro fertilized bovine oocytes. J. Ass. Reprod. Genetics 15, 50–3.CrossRefGoogle ScholarPubMed
Lane, M., Gardner, D.K., Hasler, M.J. & Hasler, J.F. (2003a). Use of G1.2/G2.2 media for commercial bovine embryo culture: equivalent development and pregnancy rates compared to co-culture. Theriogenology 60, 407–19.Google Scholar
Lane, M., Maybach, J.M., Hooper, K., Hasler, J.F. & Gardner, D.K. (2003b). Cryo-survival and development of bovine blastocysts are enhanced by culture with recombinant albumin and hyaluronan. Mol. Reprod. Dev. 64, 70–8.Google Scholar
Leppens-Luisier, G., Urner, F. & Sakkas, D. (2001). Facilitated glucose transporters play a crucial role throughout mouse preimplantation embryo development. Hum. Reprod. 16, 1229–36.Google Scholar
Lonergan, P., Crolan, C., Van Langendonck, T., Donnay, I., Kathir, H. & Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development. Biol. Reprod. 54, 1420–9.Google Scholar
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Moreira, P.M., Pintado, B., de la Fuente, J. & Boland, M.P. (2003). Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol. Reprod. 69, 1424–31.CrossRefGoogle ScholarPubMed
Nuttinck, F., Peynot, N., Humblot, P., Massip, A., Dessy, F. & Flechon, J.E. (2000). Comparative immunohistochemical distribution of connexin 37 and connexin 43 throughout folliculogenesis in the bovine ovary. Mol. Reprod. Dev. 57, 60–6.Google Scholar
Palasz, A.T., Alkemade, S. & Mapletoft, R. (1993). The use of sodium hyaluronate in freezing media for bovine and murine embryos. Cryobiology 30, 172–8.Google Scholar
Palasz, A.T., Alkemade, S. & Mapletoft, R.J. (1996). Selection of bull spermatozoa for in vitro fertilization with sodium hyaluronate in a swim-up test. Proc. 13th Int. Cong. Anim. Reprod. Sydney, Australia, V-2, P88.Google Scholar
Palasz, A.T., Rodriguez-Martinez, H., Beltran-Breña, P., Perez-Garnelo, S., Martinez, M.F., Gutierrez-Adan, A. & De la Fuente, J. (2006). The effect of hyaluronan, BSA and serum on bovine embryo in vitro development, ultrastructure and gene expression patterns. Mol. Reprod. Dev. 73, 1503–11.Google Scholar
Parrish, J.J., Susko-Parrish, J., Winer, M.A. & First, N.L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–80.CrossRefGoogle ScholarPubMed
Pollack, G.H. (2001). A new unifying approach to cell function. In: The Cells, Gels and the Engines of Life (eds Ebner & Sons), pp. 3946. Seattle, WA USA.Google Scholar
Pollard, J.W. & Leibo, S.P. (1994). Chilling sensitivity of mammalian embryos. Theriogenology 41, 101–6.Google Scholar
Prehm, P. (1984). Hyaluronate is synthesized at plasma membranes. Bioch. J. 220, 597600.CrossRefGoogle ScholarPubMed
Presti, D. & Scott, J.E. (1994). Hyaluronan-mediated protective effect against cell damage caused by enzymatically produced hydroxyl (OH*) radicals is dependent on hyaluronan molecular mass. Cell Bioch. Function 12, 281–8.CrossRefGoogle ScholarPubMed
Rizos, D., Lonergan, P., Boland, M.P., Arroyo-Garcia, R., Pintado, B., de la Fuente, J. & Gutierrez-Adan, A. (2002). Analysis of different messenger RNA expression between bovine blastocysts produced in different culture systems: implication for blastocyst quality. Biol. Reprod. 66, 589–95.Google Scholar
Ruoslahti, E. & Yamaguchi, Y. (1991). Proteoglycans as modulators of growth factor activities. Cell 64, 867–9.Google Scholar
Salustri, A., Yanagishita, M., Underhill, C.B., Laurent, T.C. & Hascall, V.C. (1992). Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle. Dev. Biol. 151, 541–51.Google Scholar
Scott, J.E., Cummings, C., Brass, A. & Chen, Y. (1991). Secondary and tertiary structures of hyaluronan in aqueous solution, investigated by rotary shadowing-electron microscopy and computer simulation. Hyaluronan is a very efficient network-forming polymer. Bioch. J. 274, 699705.CrossRefGoogle ScholarPubMed
Scott, J.E. & Presti, D. (1994). Hyaluronan-mediated protective effect against cell damage caused by enzymatically produced hydroxyl radicals is dependent on hyaluronan molecular mass. Cell Bioch. Function 12, 281–8.Google Scholar
Shu, X.Z., Liu, Y., Luo, Y., Roberts, M.C. & Prestwich, G.D. (2002). Disulfide cross-linked hyaluronan hydrogels. Biomacromolecules 3, 1304–11.CrossRefGoogle ScholarPubMed
Stojkovic, M., Krebs, O., Kolle, S., Prelle, K., Assmann, V., Zakhartchenko, V., Sinowatz, F. & Wolf, E. (2003). Developmental regulation of hyaluronan-binding protein (RHAMM/IHABP) expression in early embryos. Biol. Reprod. 68, 60–6.Google Scholar
Tammi, R., Ripellino, J.A., Margolis, R.U., Maibach, H.I., Tammi, M. (1989). Hyaluronate accumulation in human epidermis treated with retinoic acid in skin organ culture. J. Invest. Dermatol. 92, 326–32.Google Scholar
Thompson, J.G., Partridge, R.J., Houghton, F.D., Cox, C.I., Leese, H.J. (1996). Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos. J. Reprod. Fert. 106, 299306.CrossRefGoogle ScholarPubMed
Tian, W.M., Hou, S.P., Ma, J., Zhang, C.L., Xu, Q.Y., Lee, I.S., Li, H.D., Spector, M. & Cui, F.Z. (2005). Hyaluronic acid–poly-d-lysine-based three-dimensional hydrogel for traumatic brain injury. Tissue Eng. 11, 513–25.Google Scholar
Tirone, E., D'Alessandris, C., Hascall, V.C., Siracusa, G. & Salustri, A. (1997). Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocytes factor (or transforming growth factor beta1). J. Biol. Chem. 21, 4787–94.CrossRefGoogle Scholar
Toole, B.P. (1981). Glycosaminoglycans in morphogenesis. In: The Cell Biology of the Extracellular Matrix (ed. Hay, ), pp. 259–94. New York: Plenum Press.Google Scholar
Turley, E.A., Austen, L., Vandelight, K. & Clary, C. (1991). Hyaluronan and a cell-hyaluronan binding protein regulate the locomotion of rat-transformed cells. J. Cell Biol. 112, 1041–7.Google Scholar
Watson, A.J., Hogan, A., Hahner, A., Wiemer, K.E. & Schultz, G.A. (1992). Expression of growth factor ligand and receptors genes in the preimplantation bovine embryo. Mol. Reprod. Dev. 31, 8795.Google Scholar
Whitten, W.K. (1957). Culture of tubal ova. Nature 25, 1081–2.CrossRefGoogle Scholar
Wrenzycki, C., Herrmann, D., Carnwath, J.W. & Niemann, H. (1999). Alterations in the relative abundance of gene transcripts in preimplantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol. Reprod. Dev. 53, 818.Google Scholar
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A. Jr, Sirisathien, S., Brackett, B. & Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16, 893901.Google Scholar
Xu, K.P., Yadav, B.R., Rorie, R.W., Plante, L., Betteridge, K.J. & King, W.A. (1992). Development and viability of bovine embryos derived from oocytes matured and fertilized in vitro and co-cultured with bovine oviducal epithelial cells. J. Reprod. Fert. 94, 3343.CrossRefGoogle ScholarPubMed
Zhang, S. (2004). Beyond the Petri dish. Nature Biotech. 22, 151–2.CrossRefGoogle ScholarPubMed