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The effect of protein kinase C activator and nitric oxide donor on oocyte activation and cortical granule exocytosis in porcine eggs

Published online by Cambridge University Press:  08 June 2012

L. Tůmová ,
R. Romar ,
J. Petr  and
M. Sedmíková
L. Tůmová*
Affiliation:
Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences in Prague, 165 21 Prague 6-Suchdol, Czech Republic
R. Romar
Affiliation:
Department of Physiology, Faculty of Veterinary, University of Murcia, 30100 Murcia, Spain
J. Petr
Affiliation:
Institute of Animal Science, Přátelství 815, 110 00 Prague 10 - Uhříněves, Czech Republic
M. Sedmíková
Affiliation:
Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences in Prague, 165 21 Prague 6-Suchdol, Czech Republic
*
†E-mail: tumoval@af.czu.cz
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Abstract

Nitric oxide (NO) and protein kinase C (PKC) are involved in the activation of mammalian oocytes, although their role in the exit from the metaphase II stage and cortical granule (CG) exocytosis is still not fully understood. The aim of this study was to verify whether the NO-donor together with specific PKC-activators induce the complete activation of porcine oocytes assessed as meiosis resumption and a cortical reaction. Pig maturated oocytes were treated with the NO-donor S-nitroso-N-acetylpenicillamine (SNAP, 2 mM) or PKC-activators such as phorbol-12-myristate-13-acetate (PMA, 100 nM), 1-oleoyl-2-acetyl-sn-glycerol (OAG, 400 μM) and l-α-phosphatidylinositol-3,4,5-trisphosphate dipalmitoyl heptaammonium salt (DPAM, 2 μM). To study the combined effect of NO-donor and PKC-activators, aliquots of oocytes were also incubated with SNAP (0.5 mM) together with PKC-activators at the same concentration as above (SNAP–DPAM, SNAP–OAG and SNAP–PMA groups). After invitro maturation, an aliquot of oocytes was placed in a fresh medium without NO-donor or PKC-activators (Control group). Another aliquot of oocytes was activated by calcium ionophore A23187 (25 μM, 5 min). The results showed that 0% of the control oocytes reassumed meiosis. However, both the PKC-activators (DPAM 44.0 ± 10.0%, OAG 63.3 ± 1.0% and PMA 45.0 ± 16.5%) as well as the NO-donor alone (48.7 ± 21.0%) significantly induced exit from MII. Interestingly, the combination of PKC-activators and SNAP mainly restrained to the meiosis resumption (SNAP–OAG 0, SNAP–DPAM 17.4 ± 2.5% and SNAP–PMA 38.4 ± 8.5%). Control oocytes did not show a cortical reaction and the area occupied by CG reached 25.9 ± 1.7%, whereas CGs were partially released after Ca2+ ionophore treatment (13.0 ± 3.2%). Treatment with PKC-activators induced a cortical reaction compared with the control group (8.6 ± 2.5, 6.7 ± 1.9 and 0.7 ± 0.4%, respectively, for DPAM, OAG and PMA groups). However, treatment with the NO-donor alone (SNAP group 17.2 ± 2.2%) or combined with any PKC-activator prevented cortical reaction (SNAP–DPAM 20.7 ± 2.6%, SNAP–OAG 16.7 ± 2.9% or SNAP–PMA 20.0 ± 2.4%). Besides, meiosis resumption was not always accompanied by a cortical reaction, indicating that these two activation events are independent. In conclusion, PKC-activators alone induce CG exocytosis to the same degree as calcium ionophore. However, an NO-donor alone or combined with PKC-activators is not able to induce a cortical reaction in pig oocytes.

Keywords

protein kinase Cnitric oxidepig oocyteactivationcortical granules
Type
Physiology and functional biology of systems
Information
animal , Volume 7 , Issue 2 , February 2013 , pp. 279 - 286
Copyright
Copyright © The Animal Consortium 2012

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References

Bement, WM, Capco, DG 1989. Activators of protein kinase-C trigger cortical granule exocytosis, cortical contraction, and cleavage furrow formation in Xenopus-laevis oocytes and eggs. Journal of Cell Biology 108, 885–892.CrossRefGoogle ScholarPubMed
Bement, WM, Capco, DG 1991. Parallel pathways of cell-cycle control during Xenopus egg activation. Proceedings of the National Academy of Sciences of the United States of America 88, 5172–5176.Google Scholar
Bleil, JD, Beall, CF, Wassarman, PM 1981. Mammalian sperm–egg interaction: fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2. Developmental Biology 86, 189–197.CrossRefGoogle ScholarPubMed
Campagna, C, Bailey, JL, Sirard, MA, Ayotte, P, Maddox-Hyttel, P 2006. An environmentally-relevant mixture of organochlorines and its vehicle control, dimethylsulfoxide, induce ultrastructural alterations in porcine oocytes. Molecular Reproduction and Development 73, 83–91.CrossRefGoogle ScholarPubMed
Che, L, Lalonde, A, Bordignon, V 2007. Chemical activation of parthenogenetic and nuclear transfer porcine oocytes using ionomycin and strontium chloride. Theriogenology 67, 1297–1304.Google Scholar
Colonna, R, Tatone, C, Francione, A, Rosati, F, Callaini, G, Corda, D, Difrancesco, L 1997. Protein kinase C is required for the disappearance of MPF upon artificial activation in mouse eggs. Molecular Reproduction and Development 48, 292–299.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Coy, P, Gadea, J, Romar, R, Matas, C, Garcia, E 2002. Effect of in vitro fertilization medium on the acrosome reaction, cortical reaction, zona pellucida hardening and in vitro development in pigs. Reproduction 124, 279–288.Google Scholar
Ducibella, T, LeFevre, L 1997. Study of protein kinase C antagonists on cortical granule exocytosis and cell-cycle resumption in fertilized mouse eggs. Molecular Reproduction and Development 46, 216–226.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Eliyahu, E, Tsaadon, A, Shtraizent, N, Shalgi, R 2005. The involvement of protein kinase C and actin filaments in cortical granule exocytosis in the rat. Reproduction 129, 161–170.Google Scholar
Fan, HY, Tong, C, Li, MY, Lian, L, Chen, DY, Schatten, H, Sun, QY 2002. 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
Funahashi, H, Cantley, TC, Day, BN 1997. Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biology of Reproduction 57, 49–53.Google Scholar
Green, KM, Kim, JH, Wang, WH, Day, BN, Prather, RS 1999. Effect of myosin light chain kinase, protein kinase A, and protein kinase C inhibition on porcine oocyte activation. Biology of Reproduction 61, 111–119.Google Scholar
Ito, J, Shimada, M, Terada, T 2003. Effect of protein kinase C activator on mitogen-activated protein kinase and p34 (cdc2) kinase activity during parthenogenetic activation of porcine oocytes by calcium ionophore. Biology of Reproduction 69, 1675–1682.Google Scholar
Jílek, F, Hüttelová, R, Petr, J, Holubová, M, Rozinek, J 2000. Activation of pig oocytes using calcium ionophore: effect of protein synthesis inhibitor cycloheximide. Animal Reproduction Science 63, 101–111.Google Scholar
Jílek, F, Hüttelová, R, Petr, J, Holubová, M, Rozinek, J 2001. Activation of pig oocytes using calcium ionophore: effect of the protein kinase inhibitor 6-dimethyl aminopurine. Reproduction in Domestic Animals 36, 139–145.Google Scholar
Koo, OJ, Jang, G, Kwon, DK, Kang, JT, Kwon, OS, Park, HJ, Kang, SK, Lee, BC 2008. Electrical activation induces reactive oxygen species in porcine embryos. Theriogenology 70, 1111–1118.Google Scholar
Kuo, RK, Baxter, GT, Thompson, SH, Stricker, SA, Patton, C, Bonaventura, J, Epel, D 2000. NO is necessary and sufficient for egg activation at fertilization. Nature 406, 633–636.Google Scholar
Liu, WS, Heckman, CA 1998. The sevenfold way of PKC regulation. Cellular Signalling 10, 529–542.Google Scholar
Lorca, T, Cruzalegui, FH, Fesquet, D, Cavadore, JC, Méry, J, Means, A, Dorée, M 1993. Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature 366, 270–273.Google Scholar
Moore, GD, Kopf, GS, Schultz, RM 1995. Differential effect of activators of protein-kinase-C on cytoskeletal changes in mouse and hamster eggs. Developmental Biology 170, 519–530.Google Scholar
Okada, K, Miyano, T, Miyake, M 2003. Activation of pig oocytes by intracytoplasmic injection of strontium and barium. Zygote 11, 159–165.Google Scholar
Petr, J, Rozinek, J, Jílek, F, Urbánková, D 2000. Activation of porcine oocytes using cyclopiazonic acid, an inhibitor of calcium-dependent ATPases. Journal of Experimental Zoology 287, 304–315.Google Scholar
Petr, J, Krejčová, M, Rajmon, R, Jílek, F 2011. Activation of protein kinase C suppresses fragmentation of pig oocytes aged in vitro. Animal 5, 565–571.Google Scholar
Petr, J, Chmelíková, E, Dörflerová, A, Ješeta, M, Kuthanová, Z 2007. Effects of protein kinase C on parthenogenetic activation of pig oocytes using calcium ionophore or nitric oxide-donor. Czech Journal of Animal Science 52, 415–422.Google Scholar
Petr, J, Urbánková, D, Tománek, M, Rozinek, J, Jílek, F 2002. Activation of in vitro matured pig oocytes using activators of inositol triphosphate or ryanodine receptors. Animal Reproduction Science 70, 235–249.Google Scholar
Petr, J, Chmelíková, E, Krejčová, T, Řehák, D, Novotná, B, Jílek, F 2010. Parthenogenetic activation of pig oocytes using pulsatile treatment with a nitric oxide donor. Reproduction in Domestic Animals 45, 493–499.Google Scholar
Petr, J, Rajmon, R, Chmelíková, E, Tománek, M, Lánská, V, Pribanová, M, Jílek, F 2006. Nitric-oxide-dependent activation of pig oocytes: the role of the cGMP-signalling pathway. Zygote 14, 9–16.Google Scholar
Petr, J, Rajmon, R, Rozinek, J, Sedmíková, M, Ješeta, M, Chmelíková, E, Švestková, D, Jílek, F 2005. Activation of pig oocytes using nitric oxide donors. Molecular Reproduction and Development 71, 115–122.CrossRefGoogle ScholarPubMed
Petters, RM, Wells, KD 1993. Culture of pig embryos. Journal of Reproduction and Fertility 48, 61–73.Google Scholar
Romar, R, Coy, P, Rath, D 2012. Maturation conditions and boar affect timing of cortical reaction in porcine oocytes. Theriogenology, in press. doi:10.1016/j.theriogenology.2012.05.009.Google Scholar
Romar, R, Coy, P, Gadea, J, Rath, D 2005. Effect of oviductal and cumulus cells on zona pellucida and cortical granules of porcine oocytes fertilized in vitro with epididymal spermatozoa. Animal Reproduction Science 85, 287–300.Google Scholar
Ruth, P, Wang, GX, Boekhoff, I, May, B, Pfeifer, A, Penner, R, Korth, M, Breer, H, Hofmann, F 1993. Transfected cGMP-dependent protein-kinase suppresses calcium transients by inhibition of inositol 1,4,5-trisphosphate production. Proceedings of the National Academy of Sciences of the United States of America 90, 2623–2627.CrossRefGoogle ScholarPubMed
Saunders, CM, Larman, MG, Parrington, J, Cox, LJ, Royse, J, Blayney, LM, Swann, K, Lai, FA 2002. PLC zeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533–3544.Google Scholar
Sedmíková, M, Rajmon, R, Petr, J, Švestková, D, Chmelíková, 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 305A, 376–382.Google Scholar
Sethi, JK, Empson, RM, Galione, A 1996. Nicotinamide inhibits cyclic ADP-ribose-mediated calcium signalling in Sea Urchin eggs. Biochemical Journal 319, 613–617.Google Scholar
Shimada, M, Maeda, T, Terada, T 2001. Dynamic changes of connexin-43, gap junctional protein, in outer layers of cumulus cells are regulated by PKC and Pi 3-kinase during meiotic resumption in porcine oocytes. Biology of Reproduction 64, 1255–1263.Google Scholar
Sitsapesan, R, Williams, AJ 1995. Cyclic ADP-ribose activation of the sheep skeletal ryanodine receptor Ca2+-release channel is dependent upon luminal Ca2+. British Journal of Pharmacology 114, 246pp.Google Scholar
Su, YQ, Xia, GL, Byskov, AG, Fu, CD, Yang, CR 1999. Protein kinase C and intracellular calcium are involved in follicle-stimulating hormone-mediated meiotic resumption of cumulus cell-enclosed porcine oocytes in hypoxanthine-supplemented medium. Molecular Reproduction and Development 53, 51–58.Google Scholar
Sun, FZ, Hoyland, J, Huang, X, Mason, W, Moor, RM 1992. A comparison of intracellular changes in porcine eggs after fertilization and electroactivation. Development 115, 947–956.Google Scholar
Sun, QY, Wang, WH, Hosoe, H, Taniguchi, T, Chen, DY, Shioya, Y 1997. Activation of protein kinase C induces cortical granule exocytosis in a Ca2+-independent manner, but not the resumption of cell cycle in porcine eggs. Development, Growth & Differentiation 39, 523–529.Google Scholar
Wang, WH, Abeydeera, LR, Prather, RS, Day, BN 1998. Functional analysis of activation of porcine oocytes by spermatozoa, calcium ionophore, and electrical pulse. Molecular Reproduction and Development 51, 346–353.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Wang, WH, Sun, QY, Hosoe, M, Shioya, Y, Day, BN 1997. Quantified analysis of cortical granule distribution and exocytosis of porcine oocytes during meiotic maturation and activation. Biology of Reproduction 56, 1376–1382.Google Scholar
Williams, CJ 2002. Signalling mechanisms of mammalian oocyte activation. Human Reproduction Update 8, 313–321.Google Scholar
Willmott, N, Sethi, JK, Walseth, TF, Lee, HC, White, AM, Galione, A 1996. Nitric oxide-induced mobilization of intracellular calcium via the cyclic ADP-ribose signaling pathway. Journal of Biological Chemistry 271, 3699–3705.Google Scholar
Wu, XQ, Zhang, X, Li, XH, Cheng, HH, Kuai, YR, Wang, S, Guo, YL 2006. Translocation of classical PKC and cortical granule exocytosis of human oocyte in germinal vesicle and metaphase II stage. Acta Pharmacologica Sinica 27, 1353–1358.CrossRefGoogle ScholarPubMed
Yoshida, M, Cran, DG, Pursel, VG 1993. Confocal and fluorescence microscopic study using lectins of the distribution of cortical granules during the maturation and fertilization of pig oocytes. Molecular Reproduction and Development 36, 462–468.Google Scholar