Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-25T22:09:21.473Z Has data issue: false hasContentIssue false
  • English
  • Français

Promotion of glucose utilization by insulin enhances granulosa cell proliferation and developmental competence of porcine oocyte grown in vitro

Published online by Cambridge University Press:  13 December 2016

Nobuhiko Itami ,
Yasuhisa Munakata ,
Koumei Shirasuna ,
Takehito Kuwayama  and
Hisataka Iwata
Nobuhiko Itami
Affiliation:
Department of Animal Science, Tokyo University of Agriculture, Kanagawa 243–0034, Japan.
Yasuhisa Munakata
Affiliation:
Department of Animal Science, Tokyo University of Agriculture, Kanagawa 243–0034, Japan.
Koumei Shirasuna
Affiliation:
Department of Animal Science, Tokyo University of Agriculture, Kanagawa 243–0034, Japan.
Takehito Kuwayama
Affiliation:
Department of Animal Science, Tokyo University of Agriculture, Kanagawa 243–0034, Japan.
Hisataka Iwata*
Affiliation:
Department of Animal Science, Tokyo, University of Agriculture, Kanagawa 243-0034, Japan.
*
All correspondence to: Hisataka Iwata. Department of Animal Science, Tokyo, University of Agriculture, Kanagawa 243-0034, Japan. Tel: +81 46 270 6587. Fax: +81 46 270 6587. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In vitro culture of the oocyte granulosa cell complexes (OGCs) from early antral follicles (EAFs) shows granulosa cell (GC) proliferation, but to a lesser extent than that observed in vivo during follicle development. As the number of GCs closely relates to energy sufficiency of the oocytes, enhancement of GC proliferation influences oocyte development. GC proliferation depends on glycolysis and insulin-mediated AKT/mTOR signaling pathway; therefore, addition of culture medium containing insulin and glucose may potentially promote GC proliferation and hence improve oocyte development. In the present study, we assessed the effect of exogenous insulin and glucose concentration on GC proliferation and oocyte energy status as well as developmental abilities of porcine oocytes grown in vitro. In the presence of 5.5 mM of glucose (Low), a comparison of 10 versus 20 μg/ml insulin showed that high insulin enhanced GC proliferation but exhausted glucose from the medium, which resulted in low energy status including lipid and adenosine triphosphate of the oocyte. Whereas, in the presence of 20 μg/ml insulin, medium with 11 mM glucose (High) enhanced GC proliferation and oocyte energy status as well as developmental ability up to the blastocyst stage. Considering that there was no difference in OGCs development observed with medium (10 μg/ml insulin) containing 5.5 versus 11 mM glucose, we concluded that the combination of high insulin and glucose enhanced GC proliferation and energy status of oocytes as well as the developmental ability of the oocytes grown in vitro.

Keywords

InsulinGlucoseGranulosa cellsProliferationOocytes
Type
Research Article
Information
Zygote , Volume 25 , Issue 1 , February 2017 , pp. 65 - 74
Copyright
Copyright © Cambridge University Press 2016 

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

Acevedo, N., Ding, J. & Smith, G.D. (2007). Insulin signaling in mouse oocytes. Biol. Reprod. 77, 872–9.CrossRefGoogle ScholarPubMed
Biggers, J.D., Whittingham, D.G. & Donahue, R.P. (1967). The pattern of energy metabolism in the mouse oocyte and zygote. Proc. Natl. Acad. Sci. USA 58, 560–7.CrossRefGoogle ScholarPubMed
Brower, P.T. & Schultz, R.M. (1982). Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev. Biol. 90, 144–53.CrossRefGoogle ScholarPubMed
Cetica, P., Pintos, L., Dalvit, G. & Beconi, M. (2002). Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro . Reproduction 124, 675–81.CrossRefGoogle ScholarPubMed
Cheng, Y., Kim, J., Li, X.X. & Hsueh, A.J. (2015). Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators. PLoS One 24, e0117769.Google Scholar
Choi, J., Jo, M., Lee, E. & Choi, D. (2013). AKT is involved in granulosa cell autophagy regulation via mTOR signaling during rat follicular development and atresia. Reproduction 20, 73–80.Google Scholar
Dunning, K.R., Akison, L.K., Russell, D.L., Norman, R.J. & Robker, R.L. (2011). Increased beta-oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice. Biol. Reprod. 85, 548–55.CrossRefGoogle ScholarPubMed
Dunning, K.R., Cashman, K., Russell, D.L., Thompson, J.G., Norman, R.J. & Robker, R.L. (2010). Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol. Reprod. 83, 909–18.Google Scholar
Eppig, J.J. & O'Brien, M.J. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.Google Scholar
Fair, T., Hulshof, S.C., Hyttel, P., Greve, T. & Boland, M. (1997). Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat. Embryol. (Berl.) 195, 327–36.CrossRefGoogle ScholarPubMed
Ferguson, E.M. & Leese, H.J. (2006). A potential role for triglyceride as an energy source during bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 73, 1195–201.Google Scholar
Gilula, N.B., Epstein, M.L. & Beers, W.H. (1978). Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J. Cell. Biol. 78, 58–75.Google Scholar
Goto, M., Iwase, A., Harata, T., Takigawa, S., Suzuki, K., Manabe, S. & Kikkawa, F. (2009). IGF1-induced AKT phosphorylation and cell proliferation are suppressed with the increase in PTEN during luteinization in human granulosa cells. Reproduction 137, 835–42.CrossRefGoogle ScholarPubMed
Gougeon, A. (1996). Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 17, 121–55.Google Scholar
Hein, G.J., Panzani, C.G., Rodríguez, F.M., Salvetti, N.R., Díaz, P.U., Gareis, N.C., Benítez, G.A., Ortega, H.H. & Rey, F. (2015). Impaired insulin signaling pathway in ovarian follicles of cows with cystic ovarian disease. Anim. Reprod. Sci. 156, 64–74.Google Scholar
Hirao, Y., Itoh, T., Shimizu, M., Iga, K., Aoyagi, K., Kobayashi, M., Kacchi, M., Hoshi, H. & Takenouchi, N. (2004). In vitro growth and development of bovine oocyte-granulosa cell complexes on the flat substratum: effects of high polyvinylpyrrolidone concentration in culture medium. Biol. Reprod. 70, 83–91.Google Scholar
Irusta, G., Abramovich, D., Parborell, F. & Tesone, M. (2010). Direct survival role of vascular endothelial growth factor (VEGF) on rat ovarian follicular cells. Mol. Cell. Endocrinol. 30, 93–100.Google Scholar
Itami, N., Shirasuna, K., Kuwayama, T. & Iwata, H. (2015a). Resveratrol improves the quality of pig oocytes derived from early antral follicles through sirtuin 1 activation. Theriogenology. 83, 1360–7.Google Scholar
Itami, N., Shiratsuki, S., Shirasuna, K., Kuwayama, T. & Iwata, H. (2015b). Mitochondrial biogenesis and degradation are induced by CCCP treatment of porcine oocytes. Reproduction 150, 97–104.Google Scholar
Iwata, H., Goto, H., Tanaka, H., Sakaguchi, Y., Kimura, K., Kuwayama, T. & Monji, Y. (2011). Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes. Reprod. Fertil. Dev. 23, 424–32.Google Scholar
Jeong, W.J., Cho, S.J., Lee, H.S., Deb, G.K., Lee, Y.S., Kwon, T.H. & Kong, I.K. (2009). Effect of cytoplasmic lipid content on in vitro developmental efficiency of bovine IVP embryos. Theriogenology 72, 584–9.Google Scholar
Kadakia, R., Arraztoa, J.A., Bondy, C. & Zhou, J. (2001). Granulosa cell proliferation is impaired in the Igf1 null ovary. Growth Horm. IGF Res. 11, 220–4.Google Scholar
Kido, Y., Nakae, J. & Accili, D. (2001). Clinical review 125: The insulin receptor and its cellular targets. J. Clin. Endocrinol. Metab. 86, 972–9.Google Scholar
Kubo, N., Cayo-Colca, I.S. & Miyano, T. (2015). Effect of estradiol-17β during in vitro growth culture on the growth, maturation, cumulus expansion and development of porcine oocytes from early antral follicles. Anim. Sci. J. 86, 251–9.Google Scholar
Makker, A., Goel, M.M. & Mahdi, A.A. (2014). PI3K/PTEN/Akt and TSC/mTOR signaling pathways, ovarian dysfunction, and infertility: an update. J. Mol. Endocrinol. 53, R103–18.CrossRefGoogle ScholarPubMed
Munakata, Y., Kawahara-Miki, R., Shiratsuki, S., Tasaki, H., Itami, N., Shirasuna, K., Kuwayama, T. & Iwata, H. (2016a). Gene expression patterns in granulosa cells and oocytes at various stages of follicle development as well as in in vitro grown oocyte-and-granulosa cell complexes. J. Reprod. Dev. 62, 359–66.CrossRefGoogle ScholarPubMed
Munakata, Y., Ichinose, T., Ogawa, K., Itami, N., Tasaki, H., Shirasuna, K., Kuwayama, T. & Iwata, H. (2016b). Relationship between the number of cells surrounding oocytes and energy states of oocytes. Theriogenology 86, 1789–98.CrossRefGoogle ScholarPubMed
Oi, A., Tasaki, H., Munakata, Y., Shirasuna, K., Kuwayama, T. & Iwata, H. (2015). Effects of reaggregated granulosa cells and oocytes derived from early antral follicles on the properties of oocytes grown in vitro . J. Reprod. Dev. 61, 191–7.Google Scholar
Peluso, J.J., Delidow, B.C., Lynch, J. & White, B.A. (1991). Follicle-stimulating hormone and insulin regulation of 17 beta-estradiol secretion and granulosa cell proliferation within immature rat ovaries maintained in perifusion culture. Endocrinology. 128, 191–6.Google Scholar
Prates, E.G., Nunes, J.T. & Pereira, R.M. (2014). A role of lipid metabolism during cumulus-oocyte complex maturation: impact of lipid modulators to improve embryo production. Mediators Inflamm. 692067.CrossRefGoogle Scholar
Purcell, S.H., Chi, M.M., Lanzendorf, S. & Moley, K.H. (2012). Insulin-stimulated glucose uptake occurs in specialized cells within the cumulus oocyte complex. Endocrinology 153, 2444–54.CrossRefGoogle ScholarPubMed
Salfi, V., Ventura, T. & Caraceni, D. (1979). Follicles development in the foetal human ovary. Experientia 15, 543–4.CrossRefGoogle Scholar
Sato, D., Itami, N., Tasaki, H., Takeo, S., Kuwayama, T. & Iwata, H. (2014). Relationship between mitochondrial DNA copy number and SIRT1 expression in porcine oocytes. PLoS One 18, e94488.CrossRefGoogle Scholar
Savion, N., Lui, G.M., Laherty, R. & Gospodarowicz, D. (1981). Factors controlling proliferation and progesterone production by bovine granulosa cells in serum-free medium. Endocrinology 109, 409–20.Google Scholar
Serafim, M.K., Silva, G.M., Duarte, A.B., Araújo, V.R., Silva, T.F., Lima, A.K., Chaves, R.N., Campello, C.C., Silva, L.D. & Figueiredo, J.R. (2013). High insulin concentrations promote the in vitro growth and viability of canine preantral follicles. Reprod. Fertil. Dev. 25, 927–34.Google Scholar
Shiratsuki, S, Hara, T, Munakata, Y, Shirasuna, K, Kuwayama, T, Iwata, H. (2016). Low oxygen level increases proliferation and metabolic changes in bovine granulosa cells. Mol. Cell. Endocrinol. 9, 75–85.CrossRefGoogle Scholar
Sugiura, K. & Eppig, J.J. (2005). Society for Reproductive Biology Founders’ Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reprod. Fertil. Dev. 17, 667–74.Google Scholar
Sutton-McDowall, M.L., Gilchrist, R.B. & Thompson, J.G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–95.Google Scholar
Tasaki, H., Munakata, Y., Arai, S., Murakami, S., Kuwayama, T. & Iwata, H. (2015). The Effect of High Glucose Concentration on the Quality of Oocytes Derived from Different Growth Stages of Follicles. J. Mamm. Ova Res. 32, 41–48.CrossRefGoogle Scholar
Tsutsumi, O, Yano, T, Satoh, K, Mizuno, M, Kato, T. (1990). Studies of hexokinase activity in human and mouse oocyte. Am. J. Obstet. Gynecol. 162, 1301–4.Google Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.CrossRefGoogle Scholar
Zhang, D., Fei, Q., Li, J., Zhang, C., Sun, Y., Zhu, C., Wang, F. & Sun, Y. (2016). 2-Deoxyglucose reverses the promoting effect of insulin on colorectal cancer cells in vitro . PLoS One 3, e0151115.Google Scholar