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

  • Erika Wakizoe (a1), Koji Ashizawa (a1), Shinsuke H. Sakamoto (a2), Koichiro Hemmi (a3), Ikuo Kobayashi (a3) and Yasuhiro Tsuzuki (a4) (a1)...

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.

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Corresponding author

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

References

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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.
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.
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.
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.
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.
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.
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.
Burnstock, G. (2007). Purine and pyrimidine receptors. Cell. Mol. Life Sci. 64, 1471–83.
Burnstock, G. (2009). Purinergic signaling: past, present and future. Brazil. J. Med. Biol. Res. 42, 38.
Burnstock, G. & Ulrich, H. (2011). Purinergic signaling in embryonic and stem cell development. Cell. Mol. Life Sci. 68, 1369–94.
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.
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.
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.
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.
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.
Erb, L., Liao, Z., Seye, C.I. & Weisman, G.A. (2006). P2 receptors: intracellular signaling. Eur. J. Physiol. 452, 552–62.
Erlinge, D. & Burnstock, G. (2008). P2 receptors in cardiovascular regulation and disease. Purinergic Signal. 4, 120.
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.
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.
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.
Gorman, M.W., Feigl, E.O. & Buffington, C.W. (2007). Human plasma ATP concentration. Clin. Chem. 53, 318–25.
Holzer, A.M. & Granstein, R.D. (2004). Role of extracellular adenosine triphosphate in human skin. J. Cutan. Med. Surg. 8, 90–6.
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.
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.
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.
Lecca, D. & Ceruti, S. (2008). Uracil nucleotides: from metabolic intermediates to neuroprotection and neuroinflammation. Biochem. Pharmacol. 75, 1869–81.
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.
Machaca, K. (2007). Ca2+ signaling differentiation during oocyte maturation. J. Cell. Physiol. 213, 331–40.
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.
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.
Ribeiro, J.A. (1978). ATP; related nucleotides and adenosine on neurotransmission. Life Sci. 22, 1373–80.
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.
Schwiebert, E.M. & Zsembery, A. (2003). Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta 1615, 732.
Stagg, J. & Smyth, M.J. (2010). Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29, 5346–58.
St John, J.C. (2002). The transmission of mitochondrial DNA following assisted reproductive techniques. Theriogenology 57, 109–23.
Trautmann, A. (2009). Extracellular ATP in the immune system: more than just a “danger signal.” Sci. Signal. 2, e6.
Tsuda, M., Tozaki-Saitoh, H. & Inoue, K. (2010). Pain and purinergic signaling. Brain Res. Rev. 63, 222–32.
Uehara, Y., Yauchi, M. & Kumasaka, K. (2004). Evaluation of renal damage using urinary ATP analysis. Jpn. J. Nephrol. 46, 693–99. (in Japanese)
Wakai, T. & Fissore, R.A. (2013). Ca2+ homeostasis and regulation of ER Ca2+ in mammalian oocytes/eggs. Cell Calcium 53, 6376.
Watson, A.J. (2007). Oocyte cytoplasmic maturation: a key mediator of oocyte and embryo developmental competence. J. Anim. Sci. 85, E1E3.
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.
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.
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.
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.
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.

Keywords

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

  • Erika Wakizoe (a1), Koji Ashizawa (a1), Shinsuke H. Sakamoto (a2), Koichiro Hemmi (a3), Ikuo Kobayashi (a3) and Yasuhiro Tsuzuki (a4) (a1)...

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