Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-04T03:06:05.012Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of hyaluronan accumulation during cumulus expansion on in vitro porcine oocyte maturation

Published online by Cambridge University Press:  01 November 2008

Masaki Yokoo ,
Naoko Kimura ,
Hiroyuki Abe  and
Eimei Sato
Masaki Yokoo*
Affiliation:
Innovation of New Biomedical Engineering Centre, Tohoku University, 1–1 Seiryou-machi, Aoba-ku, Sendai 980–8575, Japan. Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan. Division of Biofunctional Science, Tohoku University Biomedical Engineering Research Organization (TUBERO), 2–1 Seiryou-machi, Aoba-ku, Sendai 980–8575, Japan.
Naoko Kimura
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
Hiroyuki Abe
Affiliation:
Division of Biofunctional Science, Tohoku University Biomedical Engineering Research Organization (TUBERO), 2–1 Seiryou-machi, Aoba-ku, Sendai 980–8575, Japan.
Eimei Sato
Affiliation:
Laboratory of Animal Reproduction, Graduate School of Agricultural Science, Tohoku University, Sendai 981–8555, Japan.
*
All correspondence to: Masaki Yokoo. Innovation of New Biomedical Engineering Centre, Tohoku University, 1–1 Seiryou-machi, Aoba-ku, Sendai 980–8575, Japan. Tel: +81 22 717 7122. Fax: +81 22 717 7104. e-mail: myokoo@m.tains.tohoku.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

During oocyte maturation, the cumulus–oocyte complexes (COCs) expand dramatically. This phenomenon, which is known as cumulus expansion, is the result of the synthesis and accumulation of hyaluronan in the extracellular space between cumulus cells. The purpose of this study was to investigate the effect of 6-diazo-5-oxo-l-norleucine (DON), an inhibitor of hyaluronan synthesis, on cumulus expansion during in vitro porcine oocyte maturation and hyaluronan accumulation within COCs. Further, this study aimed to examine the influence of hyaluronan accumulation within COCs on the rate of oocyte maturation. Cumulus expansion was observed during in vitro maturation. However, the addition of DON to the maturation medium significantly inhibited cumulus expansion. The total inhibition of hyaluronan accumulation within COCs was observed with the use of confocal microscopy. Moreover, a positive correlation between the area of cumulus expansion and the rate of oocyte maturation was observed. These results demonstrate that the hyaluronan accumulation within the COCs during oocyte maturation affects oocyte maturation. On the basis of these results, we propose that hyaluronan accumulation within the COCs during cumulus expansion is a necessary step in the porcine oocyte maturation process.

Keywords

Cumulus expansionHyaluronanOocyteOocyte maturationPig
Type
Research Article
Information
Zygote , Volume 16 , Issue 4 , November 2008 , pp. 309 - 314
Copyright
Copyright © Cambridge University Press 2008

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

Ball, G.D., Leibfried, M.L., Lenz, R.W., Ax, R.L., Bavister, B.D. & First, N.L. (1983). Factors affecting successful in vitro fertilization of bovine follicular oocytes. Biol. Reprod. 28, 717–25.CrossRefGoogle ScholarPubMed
Chen, L., Russell, P.T. & Larsen, W.J. (1993). Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Mol. Reprod. Dev. 34, 87–93.CrossRefGoogle ScholarPubMed
Chen, L., Wert, S.E., Hendrix, E.M., Russell, P.T., Cannon, M. & Larsen, W.J. (1990). Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Mol. Reprod. Dev. 26, 236–47.CrossRefGoogle ScholarPubMed
Daen, F.P., Sato, E., Naito, K. & Toyoda, Y. (1994). Morphometrical assessment of the expanded porcine oocyte–cumulus complexes matured in vitro: comparison of measuring methods. J Mamm Ova Res, 11, 203–8.Google Scholar
Fulop, C., Salustri, A. & Hascall, V.C. (1997). Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus–oocyte complex. Arch. Biochem. Biophys. 337, 261–6.CrossRefGoogle ScholarPubMed
Gutnisky, C., Dalvit, G.C., Pintos, L.N., Thompson, J.G., Beconi, M.T. & Cetica, P.D. (2007). Influence of hyaluronic acid synthesis and cumulus mucification on bovine oocyte in vitro maturation, fertilization and embryo development. Reprod. Fertil. Dev. 19, 488–97.CrossRefGoogle ScholarPubMed
Hess, K.A., Chen, L. & Larsen, W.J. (1999). Inter-alphainhibitor binding to hyaluronan in the cumulus extracellular matrix is required for optimal ovulation and development of mouse oocytes. Biol. Reprod. 61, 436–43.CrossRefGoogle ScholarPubMed
Kimura, N., Konno, Y., Miyoshi, K., Matsumoto, H. & Sato, E. (2002). Expression of hyaluronan synthases and CD44 messenger RNAs in porcine cumulus–oocyte complexes during in vitro maturation. Biol. Reprod. 66, 707–17.CrossRefGoogle ScholarPubMed
Lee, J.Y. & Spicer, A.P. (2000). Hyaluronan: a multifunctional, megaDalton, stealth molecule. Curr. Opin. Cell Biol. 12, 581–6.CrossRefGoogle ScholarPubMed
Nagai, T., Ding, J. & Moor, R.M. (1993). Effect of follicle cells and steroidogenesis on maturation and fertilization in vitro of pig oocytes. J. Exp. Zool. 266, 146–51.CrossRefGoogle ScholarPubMed
Nagyova, E., Prochazka, R. & Vanderhyden, B.C. (1999). Oocytectomy does not influence synthesis of hyaluronic acid by pig cumulus cells: retention of hyaluronic acid after insulin-like growth factor-I treatment in serum-free medium. Biol. Reprod. 61, 569–74.CrossRefGoogle Scholar
Nemcova, L., Nagyova, E., Petlach, M., Tomanek, M. & Prochazka, R. (2007). Molecular mechanisms of insulin-like growth factor 1 promoted synthesis and retention of hyaluronic acid in porcine oocyte–cumulus complexes. Biol. Reprod. 76, 1016–24.CrossRefGoogle ScholarPubMed
Petr, J., Zetova, L., FulkaJ., Jr J., Jr & Jilek, F. (1989). Quantitative inhibitory influence of porcine cumulus cells upon the maturation of pig and cattle oocytes in vitro. Reprod. Nutr. Dev. 29, 541–9.CrossRefGoogle ScholarPubMed
Qian, Y., Shi, W. Q., Ding, J.T., Sha, J.H. & Fan, B.Q. (2003). Predictive value of the area of expanded cumulus mass on development of porcine oocytes matured and fertilized in vitro. J. Reprod. Dev. 49, 167–74.CrossRefGoogle ScholarPubMed
Salustri, A., Yanagishita, M. & Hascall, V.C. (1990). Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev. Biol. 138, 26–32.CrossRefGoogle ScholarPubMed
Schoenfelder, M. & Einspanier, R. (2003). Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol. Reprod. 69, 269–77.CrossRefGoogle ScholarPubMed
Somfai, T., Kikuchi, K., Onishi, A., Iwamoto, M., Fuchimoto, D., Papp, A.B., Sato, E. & Nagai, T. (2004). Relationship between the morphological changes of somatic compartment and the kinetics of nuclear and cytoplasmic maturation of oocytes during in vitro maturation of porcine follicular oocytes. Mol. Reprod. Dev. 68, 484–91.CrossRefGoogle ScholarPubMed
Spicer, A.P. & McDonald, J.A. (1998). Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family. J. Biol. Chem. 273, 1923–32.CrossRefGoogle ScholarPubMed
Wallach-Dayan, S.B., Grabovsky, V., Moll, J., Sleeman, J., Herrlich, P., Alon, R. & Naor, D. (2001). CD44-dependent lymphoma cell dissemination: a cell surface CD44 variant, rather than standard CD44, supports in vitro lymphoma cell rolling on hyaluronic acid substrate and its in vivo accumulation in the peripheral lymph nodes. J. Cell Sci. 114, 3463–77.CrossRefGoogle ScholarPubMed
Yang, L.S., Kadam, A.L. & Koide, S.S. (1993). Identification of a cAMP-dependent protein kinase in bovine and human follicular fluids. Biochem. Mol. Biol. Int. 31, 521–5.Google ScholarPubMed
Yokoo, M., Miyahayashi, Y., Naganuma, T., Kimura, N., Sasada, H. & Sato, E. (2002a). Identification of hyaluronic acid-binding proteins and their expressions in porcine cumulus–oocyte complexes during in vitro maturation. Biol. Reprod. 67, 1165–71.CrossRefGoogle ScholarPubMed
Yokoo, M., Tientha, P., Kimura, N., Niwa, K., Sato, E. & Rodriguez-Martinez, H. (2002b). Localization of the hyaluronan receptor CD44 in porcine cumulus cells during in vivo and in vitro maturation. Zygote 10, 317–26.CrossRefGoogle ScholarPubMed
Yokoo, M., Shimizu, T., Kimura, N., Tunjung, W.A., Matsumoto, H., Abe, H., Sasada, H., Rodriguez-Martinez, H. & Sato, E. (2007). Role of the hyaluronan receptor CD44 during porcine oocyte maturation. J. Reprod. Dev. 53, 263–70.CrossRefGoogle ScholarPubMed
Zhang, S., Chang, M.C., Zylka, D., Turley, S., Harrison, R. & Turley, E.A. (1998). The hyaluronan receptor RHAMM regulates extracellular-regulated kinase. J. Biol. Chem. 273, 11342–8.CrossRefGoogle ScholarPubMed
Zhuo, L., Yoneda, M., Zhao, M., Yingsung, W., Yoshida, N., Kitagawa, Y., Kawamura, K., Suzuki, T. & Kimata, K. (2001). Defect in SHAP–hyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice. J. Biol. Chem. 276, 7693–6.CrossRefGoogle ScholarPubMed
Zhuo, L., Kanamori, A., Kannagi, R., Itano, N., Wu, J., Hamaguchi, M., Ishiguro, N. & Kimata, K. (2006). SHAP potentiates the CD44-mediated leukocyte adhesion to the hyaluronan substratum. J. Biol. Chem. 281, 20303–14.CrossRefGoogle Scholar