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The effects of extracellular ATP and its receptor antagonists on pig oocytes during in vitro maturation

Published online by Cambridge University Press:  02 December 2014

Erika Wakizoe
Affiliation:
Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
Koji Ashizawa
Affiliation:
Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
Shinsuke H. Sakamoto
Affiliation:
Division of Bio-Resources, Frontier Research Center, University of Miyazaki889–1692, Japan.
Koichiro Hemmi
Affiliation:
Sumiyoshi Livestock Station, Field Science Center, Faculty of Agriculture, University of Miyazaki, Miyazaki 880–0121, Japan.
Ikuo Kobayashi
Affiliation:
Sumiyoshi Livestock Station, Field Science Center, Faculty of Agriculture, University of Miyazaki, Miyazaki 880–0121, Japan.
Yasuhiro Tsuzuki*
Affiliation:
Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan. Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan.
*
All correspondence to: Yasuhiro Tsuzuki. Animal Reproduction Laboratory, Faculty of Agriculture, University of Miyazaki, Miyazaki 889–2192, Japan. e-mail: a01207u@cc.miyazaki-u.ac.jp

Summary

We measured the ATP concentrations in the porcine follicular fluid derived from three sizes of follicles (small: <3 mm, medium: 3–6 mm, large: >6 mm in diameter). Then, the effects of pre-treatment (100 μM each for 30 min before maturation) with antagonists for extracellular ATP receptor P2X or P2Y on the nuclear maturation rate of cumulus-cell-enclosed (COs) or -denuded oocytes (DOs) up to the preovulatory stage in the presence or absence of 20 nM ATP (a similar concentration to that of medium-sized follicle fluid) were investigated. The antagonists used were pyridoxalphosphate-6-azophenyl-2′,4′-disulfonic acid (PPADS) or reactive blue 2 (RB2), for extracellular ATP receptor P2X and P2Y, respectively. In addition, the embryonic development rates of COs pre-treated with RB2 were also evaluated. It was found that when the follicular sizes increased, the ATP concentrations significantly decreased (P < 0.05). No differences were observed in the nuclear maturation rates among all COs, regardless of pre-treatment with (+) or without (–) PPADS and in the presence (+) or absence (–) of ATP during maturation. In contrast, the nuclear maturation rate of the COs, but not DOs, in the ATP(–) RB2(+) group was significantly lower (P < 0.05) than that of the ATP(–) RB2(–) and ATP(+)RB2(–) groups. The pronuclear formation and blastocyst formation rates by parthenogenetic activation in the ATP(–) RB2(+) and ATP(+) RB2(+) groups were significantly lower (P < 0.05) than those in the ATP(–) RB2(–) group. In conclusion, it is suggested that the nuclear maturation of porcine oocytes may be influenced by the ATP receptor P2Y present in the cumulus cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Amadio, S., Apolloni, S., D’Ambrosi, N. & Volonté, C. (2011). Purinergic signaling at the plasma membrane: a multipurpose and multidirectional mode to deal with amyotrophic lateral sclerosis and multiple sclerosis. J. Neurochem. 116, 796805.CrossRefGoogle ScholarPubMed
Antosik, P., Kempisty, B., Bukowska, D., Jackowska, M., Włdarczyk, R., Budna, J., Brūssow, K.P., Lianeri, M., Jagodriński, P.P. & Jaśkowski, J.M. (2009). Follicular size is associated with the levels of transcripts and proteins of selected molecules responsible for the fertilization ability of oocytes of puberal gilts. J. Reprod. Dev. 55, 588–93.CrossRefGoogle ScholarPubMed
Arellano, R.O., Martínez-Torres, A. & Garay, E. (2002). Ionic currents activated via purinergic receptors in the cumulus cell-enclosed mouse oocyte. Biol. Reprod. 67, 837–46.CrossRefGoogle ScholarPubMed
Bagg, M.A., Nottle, M.B., Armstrong, D.T. & Grupen, C.G. (2007). Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reprod. Fertil. Dev. 19, 797803.CrossRefGoogle ScholarPubMed
Bertoldo, M.J., Nadal-Desbarats, L., Gérard, N., Dubois, A., Holyoake, P.K. & Grupen, C.G. (2013). Differences in the metabolomic signatures of porcine follicular fluid collected from environments associated with good and poor oocyte quality. Reproduction 146, 221–31.CrossRefGoogle ScholarPubMed
Bonora, M., Patergnani, S., Rimessi, A., de Marchi, E., Suski, J.M., Bononi, A., Giorgi, C., Marchi, S., Missiroli, S., Poletti, F., Wieckowski, M.R. & Pinton, P. (2012). ATP synthesis and storage. Purinergic Signal. 8, 343–57.CrossRefGoogle ScholarPubMed
Brevini, T.A.L., Cillo, F., Antonini, S. & Gandolfi, F. (2007). Cytoplasmic remodeling and acquisition of developmental competence in pig oocytes. Anim. Reprod. Sci. 98, 2338.CrossRefGoogle ScholarPubMed
Burnstock, G. (2007). Purine and pyrimidine receptors. Cell. Mol. Life Sci. 64, 1471–83.CrossRefGoogle ScholarPubMed
Burnstock, G. (2009). Purinergic signaling: past, present and future. Brazil. J. Med. Biol. Res. 42, 38.CrossRefGoogle ScholarPubMed
Burnstock, G. & Ulrich, H. (2011). Purinergic signaling in embryonic and stem cell development. Cell. Mol. Life Sci. 68, 1369–94.CrossRefGoogle ScholarPubMed
Catala, M.G., Izquierdo, D. & Rodriguez-Prado, M. (2012). Effect of oocyte quality on blastocyst development after in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI) in a sheep model. Fertil. Steril. 97, 1004–8.CrossRefGoogle Scholar
Che, L., Lalonde, A. & Bordignon, V. (2007). Chemical activation of parthenogenetic and nuclear transfer porcine oocytes using ionomycin and strontium chloride. Theriogenology 67, 1297–304.CrossRefGoogle ScholarPubMed
Conn, R.B., Charache, P. & Chappelle, E.W. (1975). Limits of applicability of the firefly luminescence ATP assay for the detection of bacteria in clinical specimens. Am. J. Clin. Pathol. 63, 493501.CrossRefGoogle ScholarPubMed
Downs, S.M., Coleman, D.L., Ward-Bailey, P.F. & Eppig, J. (1985). Hypoxanthine is the principal inhibitor of murine oocyte maturation in a low molecular weight fraction of porcine follicular fluid. Proc. Natl. Acad. Sci. USA 82, 454–8.CrossRefGoogle Scholar
Dubyak, G.R. & El-Moatassim, C. (1993). Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am. J. Physiol. 265 (3 Pt 1), C577–606.CrossRefGoogle ScholarPubMed
Erb, L., Liao, Z., Seye, C.I. & Weisman, G.A. (2006). P2 receptors: intracellular signaling. Eur. J. Physiol. 452, 552–62.CrossRefGoogle ScholarPubMed
Erlinge, D. & Burnstock, G. (2008). P2 receptors in cardiovascular regulation and disease. Purinergic Signal. 4, 120.CrossRefGoogle ScholarPubMed
Farias, M. 3rd, Gorman, M.W., Savage, M.V. & Feigl, E.O. (2005). Plasma ATP during exercise: possible role in regulation of coronary blood flow. Am. J. Physiol. Heart Circ. Physiol. 288, 1046–55.CrossRefGoogle ScholarPubMed
Fricke, P.M., Ford, J.J., Reynolds, L.P. & Redmer, D.A. (1996). Growth and cellular proliferation of antral follicles throughout the follicular phase of the estrous cycle in Meishan gilts. Biol. Reprod. 54, 879–87.CrossRefGoogle ScholarPubMed
Gever, J.R., Cockayne, D.A., Dillon, M., Burnstock, G. & Ford, A.P.D.W. (2006). Pharmacology of P2X channels. Pflugers Arch. 452, 513–37.CrossRefGoogle ScholarPubMed
Gorman, M.W., Feigl, E.O. & Buffington, C.W. (2007). Human plasma ATP concentration. Clin. Chem. 53, 318–25.CrossRefGoogle ScholarPubMed
Holzer, A.M. & Granstein, R.D. (2004). Role of extracellular adenosine triphosphate in human skin. J. Cutan. Med. Surg. 8, 90–6.CrossRefGoogle ScholarPubMed
Ito, M., Iwata, H., Kitagawa, M., Kon, Y., Kuwayama, T. & Monji, Y. (2008). Effect of follicular fluid collected from various diameter follicles on the progression of nuclear and developmental competence of pig oocytes. Anim. Reprod. Sci. 106, 421–30.CrossRefGoogle ScholarPubMed
Kamada, S., Kubota, T., Hirata, Y., Taguchi, M., Eguchi, S., Marumo, F. & Aso, T. (1992). Direct effect of endothelin-1 on the granulose cells of the porcine ovary. J. Endocrinol. 134, 5966.CrossRefGoogle Scholar
Kamada, S., Blackmore, P.F., Oehninger, S., Gordon, K. & Hodgen, G.D. (1994). Existence of P2-purinoceptors on human and porcine granulose cells. J. Clin. Endocrinol. Metab. 78, 650–6.Google Scholar
Lecca, D. & Ceruti, S. (2008). Uracil nucleotides: from metabolic intermediates to neuroprotection and neuroinflammation. Biochem. Pharmacol. 75, 1869–81.CrossRefGoogle ScholarPubMed
Lohman, A.W., Billaud, M. & Isakson, B.E. (2012). Mechanisms of ATP release and signaling in the blood vessel wall. Cardiovasc. Res. 95, 269–80.CrossRefGoogle ScholarPubMed
Machaca, K. (2007). Ca2+ signaling differentiation during oocyte maturation. J. Cell. Physiol. 213, 331–40.CrossRefGoogle ScholarPubMed
Mehri, S., Levi Setti, P.E., Greco, K., Sakkas, D., Martinez, G. & Patrizio, P. (2014). Correlation between follicular diameters and flushing versus no flushing on oocyte maturity, fertilization rate and embryo quality. J. Assist. Reprod. Genet. 31, 73–7.CrossRefGoogle ScholarPubMed
Ohnishi, T., Matsumura, S. & Ito, S. (2009). Translocation of neuronal nitric oxide synthase to the plasma membrane by ATP is mediated by P2X and P2Y receptors. Mol. Pain 5, 40.CrossRefGoogle Scholar
Ribeiro, J.A. (1978). ATP; related nucleotides and adenosine on neurotransmission. Life Sci. 22, 1373–80.CrossRefGoogle ScholarPubMed
R Development Core Team. (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Schwiebert, E.M. & Zsembery, A. (2003). Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta 1615, 732.CrossRefGoogle ScholarPubMed
Stagg, J. & Smyth, M.J. (2010). Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29, 5346–58.CrossRefGoogle ScholarPubMed
St John, J.C. (2002). The transmission of mitochondrial DNA following assisted reproductive techniques. Theriogenology 57, 109–23.CrossRefGoogle ScholarPubMed
Trautmann, A. (2009). Extracellular ATP in the immune system: more than just a “danger signal.” Sci. Signal. 2, e6.CrossRefGoogle ScholarPubMed
Tsuda, M., Tozaki-Saitoh, H. & Inoue, K. (2010). Pain and purinergic signaling. Brain Res. Rev. 63, 222–32.CrossRefGoogle ScholarPubMed
Uehara, Y., Yauchi, M. & Kumasaka, K. (2004). Evaluation of renal damage using urinary ATP analysis. Jpn. J. Nephrol. 46, 693–99. (in Japanese)Google ScholarPubMed
Wakai, T. & Fissore, R.A. (2013). Ca2+ homeostasis and regulation of ER Ca2+ in mammalian oocytes/eggs. Cell Calcium 53, 6376.CrossRefGoogle ScholarPubMed
Watson, A.J. (2007). Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J. Anim. Sci. 85, E1E3.CrossRefGoogle ScholarPubMed
Webb, R.J., Bains, H., Cruttwell, C. & Carroll, J. (2002). Gap-junctional communication in mouse cumulus–oocyte complexes: implications for mechanism of meiotic maturation. Reproduction 123, 4152.CrossRefGoogle ScholarPubMed
Yamanaka, K., Sugimura, S., Wakai, T., Kawahara, M. & Sato, E. (2009). Difference in sensitivity to culture condition between in vitro fertilized and somatic cell nuclear transfer embryos in pigs. J. Reprod. Dev. 55, 299304.CrossRefGoogle ScholarPubMed
Yamashiro, H., Toyomizu, M., Toyama, N., Aono, N., Sakurai, M., Hiradate, Y., Yokoo, M., Moisyadi, S. & Sato, E. (2010). Extracellular ATP and dibutyl cAMP enhance the freezability of rat epidermal sperm. J. Am. Assoc. Lab. Anim. Sci. 49, 167–72.Google Scholar
Yoshioka, K., Suzuki, C. & Onishi, A. (2008). Defined system for in vitro production of porcine embryos using a single basic medium. J. Reprod. Dev. 54, 208–13.CrossRefGoogle ScholarPubMed
Yi, Y.J., Park, C.S., Kim, E.S., Song, E.S., Jeong, J.H. & Sutovsky, P. (2009). Sperm-surface ATP in boar spermatozoa is required for fertilization: relevance to sperm proteasomal function. Syst. Biol. Reprod. Med. 55, 8596.CrossRefGoogle ScholarPubMed