Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T10:23:35.740Z Has data issue: false hasContentIssue false
  • English
  • Français

Involvement of the metabolic hormones leptin, ghrelin, obestatin, IGF-I and of MAP kinase in control of porcine oocyte maturation

Published online by Cambridge University Press:  16 August 2010

A. V. Sirotkin ,
A. Bezáková ,
J. Laurinčík  and
B. Matejovičová
A. V. Sirotkin*
Affiliation:
Department of Zoology and Anthropology, Constantine the Philosopher University, 949 01 Nitra, Slovak Republic Department of Farm Animal Genetics and Reproduction, Animal Production Research Centre Nitra, 951 41 Luzanky near Nitra, Slovak Republic
A. Bezáková
Affiliation:
Department of Zoology and Anthropology, Constantine the Philosopher University, 949 01 Nitra, Slovak Republic Department of Farm Animal Genetics and Reproduction, Animal Production Research Centre Nitra, 951 41 Luzanky near Nitra, Slovak Republic
J. Laurinčík
Affiliation:
Department of Zoology and Anthropology, Constantine the Philosopher University, 949 01 Nitra, Slovak Republic
B. Matejovičová
Affiliation:
Department of Zoology and Anthropology, Constantine the Philosopher University, 949 01 Nitra, Slovak Republic
*
†E-mail: sirotkin@scpv.sk
Get access

Abstract

The general aim of our in vitro experiments was to study the role of the metabolic hormones leptin, ghrelin, obestatin and IGF-I and mitogen-activated protein kinase (MAPK)-dependent intracellular mechanisms in the control of nuclear maturation of porcine oocytes. For this purpose, porcine oocytes were isolated from the ovary and cultured in the presence of leptin, ghrelin, obestatin, IGF-I, MAPK blocker PD98059 and the combinations of hormones with PD98059. Proportions of matured oocytes (at metaphase II of meiosis, determined by DAPI staining) and of oocytes containing MAPK/ERK1-2 (determined by immunocytochemistry) were measured before and after culture. It was observed that the majority of oocytes isolated from the ovary before culture were immature and did not contain visible MAPK, but some oocytes were mature, and the majority of these oocytes contained MAPK. Incubation of oocytes resulted in a significant increase in the proportion of matured oocytes and in the percentage of oocytes containing MAPK in both the matured and not matured groups. Addition of IGF-I to the culture medium increased the proportion of matured oocytes, addition of leptin decreased it, and ghrelin and obestatin did not oocyte maturation. Addition of hormones did not affect the expression of MAPK in either immature or mature oocytes. PD98059, when given alone, suppressed the maturation and accumulation of MAPK in both mature and immature oocytes. When given together with hormones, PD98059 was able to reduce the stimulatory effect of IGF-I, to invert the inhibitory action of leptin to stimulatory and to induce the stimulatory action of ghrelin and obestatin on meiosis. IGF-I, ghrelin and obestatin, but not leptin, when given together with PD98059, increased the accumulation of MAPK in both immature and mature oocytes. Association of nuclear maturation and expression of MAPK in oocytes before, but not after culture, as well as the prevention of oocyte maturation by MAPK blocker suggests the involvement of MAPK-dependent intracellular mechanisms in the promotion of reinitiation, but not completion of meiosis. The effect of hormonal additions on meiosis of oocytes suggests that IGF-I is a stimulator, leptin can be an inhibitor, while ghrelin and obestatin probably do not control oocyte maturation. The ability of PD98059 to modify the effect of hormones on oocyte maturation and on MAPK expression suggests possible interference of hormones and MAPK-dependent intracellular mechanisms in oocytes. However, no influence of hormones on MAPK and lack of association between action of hormones and PD98059 on MAPK and meiosis suggest that MAPK is probably not a mediator of effect of IGF-I, leptin, ghrelin and obestatin on porcine oocyte nuclear maturation.

Keywords

leptinghrelinobestatinMAP kinaseoocyte
Type
Full Paper
Information
animal , Volume 5 , Issue 1 , January 2011 , pp. 94 - 99
Copyright
Copyright © The Animal Consortium 2010

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

Craig, JA, Zhu, H, Dyce, PW, Wen, L, Li, J 2005. Leptin enhances porcine preimplantation embryo development in vitro. Molecular and Cellular Endocrinology 229, 141–147.CrossRefGoogle ScholarPubMed
Ebeling, S, Schuon, C, Meinecke, B 2007. Mitogen-activated protein kinase phosphorylation patterns in pig oocytes and cumulus cells during gonadotrophin-induced resumption of meiosis in vitro. Zygote 15, 139–147.CrossRefGoogle ScholarPubMed
Illera, MJ, Lorenco, PL, Illera, JC, Petters, RM 1998. Developmental competence of immature pig oocytes under the influence of EGF, IGF-I, folicular fluid and gonadotropins during IVM-IVF. Developmental Biology 48, 1169–1172.Google Scholar
Inoue, M, Naito, K, Aoki, F, Tayoda, Y, Sato, E 1995. Activation of mitogen-activated protein kinase during meiotic maturation in porcine oocytes. Zygote 3, 265–271.CrossRefGoogle ScholarPubMed
Inoue, M, Naito, K, Nakayama, T, Sato, E 1998. Mitogen-activated protein kinase translocates into the germinal vesicle and induces germinal vesicle breakdown in porcine oocytes. Biology of Reproduction 58, 130–136.CrossRefGoogle ScholarPubMed
Jin, YX, Cui, XS, Han, YJ, Kim, NH 2009. Leptin accelerates pronuclear formation following intracytoplasmic isperm injection of porcine oocytes: possible role for MAP kinase inactivation. Animal Reproducton Science 115, 137–482.CrossRefGoogle Scholar
Kimura, N, Hoshino, Y, Totsukawa, K, Sato, E 2007. Cellular and molecular events during oocyte maturation in mammals: molecules of cumulus-oocyte complex matrix and signalling pathways regulating meiotic progression. Society of Reproduction and Fertility 63, 327–342.Google ScholarPubMed
Kun, Z, Shaohua, W, Yufang, M, Yankun, L, Hengxi, W, Xiuzhu, S, Yonghui, Z, Yan, L, Yunping, D, Lei, Z, Ning, L 2007. Effects of leptin supplementation in in vitro maturation medium on meiotic maturation of oocytes and preimplantation development of parthenogenetic and cloned embryos in pigs. Animal Reproduction Science 101, 85–96.CrossRefGoogle ScholarPubMed
Lee, J, Miyano, T, Moor, RM 2000. Localisation of phosphorylated MAP kinase during the transition from meiosis I to meiosis II in pig oocytes. Zygote 8, 119–125.CrossRefGoogle Scholar
Li, M, Liang, CG, Xiong, B, Xu, BZ, Lin, SL, Hou, Y, Chen, DY, Schatten, H, Sun, QY 2008. PI3-kinase and mitogen-activated protein kinase in cumulus cells mediate EGF-induced meiotic resumption of porcine oocyte. Domestic Animal Endocrinology 34, 360–371.CrossRefGoogle ScholarPubMed
Makarevich, AV, Markkula, M 2002. Apoptosis and cell proliferation potential of bovine embryos stimulated with insulin-like growth factor I during in vitro maturation and culture. Biology of Reproduction 66, 386–392.CrossRefGoogle ScholarPubMed
Motlik, J, Pavlok, A, Kubelka, M, Kalous, J, Kalab, P 1998. Interplay between cdc2 kinase and map kinase pathway during maturation of mammalian oocytes. Theriogenology 49, 461–469.CrossRefGoogle ScholarPubMed
Nebreda, AR, Ferby, I 2000. Regulation of the meiotic cell cycle in oocytes. Current Opinion in Cell Biology 12, 666–675.CrossRefGoogle ScholarPubMed
Sirotkin, AV, Dukesova, J, Makarevich, AV, Kubek, A, Bulla, J, Hetenyi, L 2000. Evidence that growth factors IGF-I, IGF-II and EGF can stimulate nuclear maturation of porcine oocytes via intracellular protein kinase A. Reproduction, Nutrition, Development 40, 559–569.CrossRefGoogle ScholarPubMed
Suzuki, H, Sasaki, Y, Shimizu, M, Matsuzaki, M, Hashizume, T, Kuwayama, H 2009. Ghrelin and leptin did not improve meiotic maturation of porcine oocytes cultured in vitro. Reproduction in Domestic Animals 28 March 2009 [Epub ahead of print, PMID: 19416485].CrossRefGoogle Scholar
Wehrend, A, Meinecke, B 2001. Kinetics of meiotic progression, Mphase promoting factor (MPF) and mitogen-activated protein kinase (MAP kinase) activities during in vitromaturation of porcine and bovine oocytes: species specific differences in the length of the meiotic stages. Animal Reproduction Science 66, 175–184.CrossRefGoogle Scholar
Xia, P, Tekpetey, F, Armstrong, D 1994. Effect of IGF-I on pig oocyte maturation, fertilization and early embryonic development in vitro, and on granulosa and cumulus cell biosynthetic activity. Molecular Reproduction and Development 38, 373–379.CrossRefGoogle ScholarPubMed
Ye, J, Coleman, J, Hunter, MG, Craigon, J, Campbell, KH, Luck, MR 2007. Physiological temperature variants and culture media modify meiotic progression and developmental potential of pig oocytes in vitro. Reproduction 133, 877–886.CrossRefGoogle ScholarPubMed