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Activation of protein kinase C suppresses fragmentation of pig oocytes aged in vitro

Published online by Cambridge University Press:  02 November 2010

J. Petr ,
M. Krejčová ,
R. Rajmon  and
F. Jílek
J. Petr*
Affiliation:
Research Institute of Animal Production, Přátelství 815, 10401 Prague 10-Uhříněves, Czech Republic
M. Krejčová
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic
R. Rajmon
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic
F. Jílek
Affiliation:
Faculty of Agrobiology, Food and Natural Resources, Department of Veterinary Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Prague 6 – Suchdol, Czech Republic
*
†E-mail: [email protected]
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Abstract

When cultured for an extended time, pig oocytes that matured in vitro to the stage of metaphase II undergo the complex process designated as ageing. Under our conditions, some pig oocytes aged 3 days remained at the stage of metaphase II (22%), but others underwent spontaneous parthenogenetic activation (45%), and still others perished through fragmentation (28%) or lysis (5%). Activation of protein kinases C (PKCs) using phorbol-12-myristate-13-acetate (PMA) protects oocytes from fragmentation. None of the oocytes were fragmented after 3 days of aging in 50 nM of PMA. A similar effect (8% of fragmented oocytes) was observed after a 3-day treatment of aging oocytes with 100 μM of 1-stearoyl-2arachidonoyl-sn-glycerol (STEAR). PMA and STEAR activate both calcium-dependent and calcium-independent PKCs. This combined effect on PKCs seems to be essential for the protection of oocytes from fragmentation. Neither the specific activator of calcium-dependent PKCs 1-oleoyl-2-acetyl-sn-glycerol (OLE) nor the specific activator of calcium-independent PKCs dipalmitoyl-l-α-phosphatidylinositol-3,4,5-triphosphate heptaammonium salt (DIPALM) suppressed the fragmentation of aging pig oocytes. Twenty-one percentage of oocytes fragmented when aged for 3 days in 10 μM OLE and 26% of aged oocytes fragmented in 100 nM of DIPALM. However, fragmentation was significantly suppressed to 7% when the oocytes were exposed to the combination of both 10 μM OLE and 100 nM DIPALM. Aging pig oocytes cultured for 1 day with PMA maintained a high capability of being parthenogenetically activated (86% of activated oocytes), using calcium ionophore with 6-dimethylaminopurine. Ageing oocytes treated with PMA also had high capability of cleavage (82%) after their artificial parthenogenetic activation. However, their ability to develop to the stage of blastocyst (12%) was suppressed when compared with oocytes activated immediately after their maturation (29%).

Keywords

pig oocyteoocyteageingoocyte fragmentationprotein kinase C
Type
Full Paper
Information
animal , Volume 5 , Issue 4 , 23 February 2011 , pp. 565 - 571
Copyright
Copyright © The Animal Consortium 2010

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References

Adams, JM, Cory, S 1998. The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322–1326.CrossRefGoogle ScholarPubMed
Aderem, A 1995. The MARCKS family of protein kinase-C substrates. Biochemical Society Transactions 23, 587–591.CrossRefGoogle ScholarPubMed
Baines, CP, Song, CX, Zheng, YT, Wang, GW, Zhang, J, Wang, OL, Guo, Y, Bolli, R, Cardwell, EM, Ping, P 2003. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circulation Research 92, 873–880.CrossRefGoogle ScholarPubMed
Downs, SM, Cottom, J, Hunzicker-Dunn, M 2001. Protein kinase C and meiotic regulation in isolated mouse oocytes. Molecular Reproduction and Development 58, 101–115.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Eliyahu, E, Shalgi, R 2002. A role for protein kinase C during rat egg activation. Biology of Reproduction 67, 189–195.CrossRefGoogle ScholarPubMed
Fan, HY, Tong, C, Chen, DY, Sun, QY 2003. Roles of protein kinase C in oocyte meiotic maturation and fertilization. Progress in Natural Science 13, 401–406.Google Scholar
Fan, HY, Li, MY, Tong, C, Chen, DY, Xia, GL, Song, XF, Schatten, H, Sun, QY 2002a. Inhibitory effects of cAMP and protein kinase C on meiotic maturation and MAP kinase phosphorylation in porcine oocytes. Molecular Reproduction and Development 63, 480–487.CrossRefGoogle ScholarPubMed
Fan, HY, Tong, C, Li, MY, Lian, L, Chen, DY, Schatten, H, Sun, QY 2002b. Translocation of the classic protein kinase C isoforms in porcine oocytes: implications of protein kinase C involvement in the regulation of nuclear activity and cortical granule exocytosis. Experimental Cell Research 277, 183–191.CrossRefGoogle ScholarPubMed
Fissore, RA, Kurokawa, M, Knott, J, Zhang, M, Smyth, J 2002. Mechanisms underlying oocyte activation and postovulatory ageing. Reproduction 124, 745–754.CrossRefGoogle ScholarPubMed
Gangeswaran, R, Jones, KT 1997. Unique protein kinase C profile in mouse oocytes: lack of calcium-dependent conventional isoforms suggested by rtPCR and Western blotting. Febs Letters 412, 309–312.CrossRefGoogle ScholarPubMed
Hall, VJ, Compton, D, Stojkovic, P, Nesbitt, M, Herbert, M, Murdoch, A, Stojkovic, M 2007. Developmental competence of human in vitro aged oocytes as host cells for nuclear transfer. Human Reproduction 22, 52–62.CrossRefGoogle Scholar
Jílek, F, Huttelova, R, Petr, J, Holubova, M, Rozinek, J 2001. Activation of pig oocytes using calcium ionophore: effect of the protein kinase inhibitor 6-dimethyl aminopurine. Reproduction in Domestic Animal 36, 139–145.Google ScholarPubMed
Jolliff, WJ, Prather, RS 1997. Parthenogenic development of in vitro-matured, in vivo-cultured porcine oocytes beyond blastocyst. Biology of Reproduction 56, 544–548.CrossRefGoogle ScholarPubMed
Kikuchi, K, Kashiwazaki, N, Nagai, T, Nakai, M, Somfai, T, Noguchi, J, Kaneko, H 2008. Selected aspects of advanced porcine reproductive technology. Reproduction in Domestic Animal 43 (suppl. 2), 401–406.CrossRefGoogle ScholarPubMed
Kikuchi, K, Naito, K, Noguchi, J, Shimada, A, Kaneko, H, Yamashita, M, Aoki, F, Tojo, H, Toyoda, Y 2000. Maturation/M-phase promoting factor: a regulator of aging in porcine oocytes. Biology of Reproduction 63, 715–722.CrossRefGoogle ScholarPubMed
Liu, WS, Heckman, CA 1998. The sevenfold way of PKC regulation. Cellular Signalling 10, 529–542.CrossRefGoogle ScholarPubMed
Luria, A, Tennenbaum, T, Sun, QY, Rubinstein, S, Breitbart, H 2000. Differential localization of conventional protein kinase C isoforms during mouse oocyte development. Biology of Reproduction 62, 1564–1570.CrossRefGoogle ScholarPubMed
Ma, W, Koch, JA, Viveiros, MM 2008. Protein kinase C delta (PKCdelta) interacts with microtubule organizing center (MTOC)-associated proteins and participates in meiotic spindle organization. Developmental Biology 320, 414–425.CrossRefGoogle ScholarPubMed
Nagano, M, Katagiri, S, Takahashi, Y 2006. Relationship between bovine oocyte morphology and in vitro developmental potential. Zygote 14, 53–61.CrossRefGoogle ScholarPubMed
Pauken, CM, Capco, DG 2000. The expression and stage-specific localization of protein kinase C isotypes during mouse preimplantation development. Developmental Biology 223, 411–421.CrossRefGoogle ScholarPubMed
Pavlok, A, Kalab, P, Bobak, P 1997. Fertilisation competence of bovine normally matured or aged oocytes derived from different antral follicles: morphology, protein synthesis, H1 and MBP kinase activity. Zygote 5, 235–246.CrossRefGoogle ScholarPubMed
Perez, GI, Tao, XJ, Tilly, JL 1999. Fragmentation and death (a.k.a. apoptosis) of ovulated oocytes. Molecular Human Reproduction 5, 414–420.CrossRefGoogle ScholarPubMed
Petters, RM, Wells, KD 1993. Culture of pig embryos. Journal of Reproduction Fertility 48 (suppl.), 61–73.Google ScholarPubMed
Petrová, I, Sedmíková, M, Chmelikova, E, Svestkova, D, Rajmon, R 2004. In vitro aging of porcine oocytes. Czech Journal of Animal Science 49, 93–98.CrossRefGoogle Scholar
Raz, T, Eliyahu, E, Yesodi, V, Shalgi, R 1998. Profile of protein kinase C isozymes and their possible role in mammalian egg activation. FEBS Letters 431, 415–418.CrossRefGoogle ScholarPubMed
Sadler, KC, Yuce, O, Hamaratoglu, F, Verge, V, Peaucellier, G, Picard, A 2004. MAP kinases regulate unfertilized egg apoptosis and fertilization suppresses death via Ca2+ signaling. Molecular Reproduction and Development 67, 366–383.CrossRefGoogle ScholarPubMed
Sedmíková, M, Rajmon, R, Petr, J, Svestkova, D, Chmelikova, E, Bantirgu, A, Rozinek, J, Jílek, F 2006. Effect of protein kinase C inhibitors on porcine oocyte activation. Journal of Experimental Zoology Part A – Comparative Experimental Biology 305, 376–382.CrossRefGoogle ScholarPubMed
Takahashi, T, Saito, H, Hiroi, M, Doi, K, Takahashi, E 2000. Effects of aging on inositol 1,4,5-triphosphate-induced Ca2+ release in unfertilized mouse oocytes. Molecular Reproduction and Development 55, 299–306.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Tarin, JJ, Perez-Albala, S, Cano, A 2001. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biology of Reproduction 65, 141–150.CrossRefGoogle ScholarPubMed
Tatone, C, Delle Monache, S, Francione, A, Gioia, L, Barboni, B, Colonna, R 2003. Ca2+-independent protein kinase C signalling in mouse eggs during the early phases of fertilization. International Journal of Developmental Biology 47, 327–333.Google ScholarPubMed
Viveiros, MM, Hirao, Y, Eppig, JJ 2001. Evidence that protein kinase C (PKC) participates in the meiosis I to meiosis II transition in mouse oocytes. Developmental Biology 235, 330–342.CrossRefGoogle ScholarPubMed
Viveiros, MM, O’Brien, M, Wigglesworth, K, Eppig, JJ 2003. Characterization of protein kinase C-delta in mouse oocytes throughout meiotic maturation and following egg activation. Biology of Reproduction 69, 1494–1499.CrossRefGoogle ScholarPubMed
Wassarman, PM 1988. The mammalian ovum. In The physiology of reproduction (ed. E Knobil and J Neill), pp. 69–102. Raven Press, New York.Google Scholar
Webb, M, Howlett, SK, Maro, B 1986. Parthenogenesis and cytoskeletal organization in ageing mouse eggs. Journal of Embryology and Experimental Morphology 95, 131–145.Google ScholarPubMed
Wilding, M, Dale, B, Marino, M, di Matteo, L, Alviggi, C, Pisaturo, ML, Lombardi, L, De Placido, G 2001. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Human Reproduction 16, 909–917.CrossRefGoogle ScholarPubMed
Winkel, GK, Ferguson, JE, Takeichi, M, Nuccitelli, R 1990. Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. Developmental Biology 138, 1–15.CrossRefGoogle ScholarPubMed
Yu, BZ, Zheng, J, Yu, AM, Shi, XY, Liu, Y, Wu, DD, Fu, W, Yang, J 2004. Effects of protein kinase C on M-phase promoting factor in early development of fertilized mouse eggs. Cell Biochemistry and Function 22, 291–298.CrossRefGoogle ScholarPubMed
Yuce, O, Sadler, KC 2001. Postmeiotic unfertilized starfish eggs die by apoptosis. Developmental Biology 237, 29–44.CrossRefGoogle ScholarPubMed