Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 670670, 12 pages
http://dx.doi.org/10.1155/2014/670670
Research Article

The Effect of Lysophosphatidic Acid during In Vitro Maturation of Bovine Oocytes: Embryonic Development and mRNA Abundances of Genes Involved in Apoptosis and Oocyte Competence

1Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-747 Olsztyn, Poland
2CIISA, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal

Received 12 November 2013; Revised 18 January 2014; Accepted 28 January 2014; Published 4 March 2014

Academic Editor: Anna Chełmonska-Soyta

Copyright © 2014 Dorota Boruszewska et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. X. Ye and J. Chun, “Lysophosphatidic acid (LPA) signaling in vertebrate reproduction,” Trends in Endocrinology and Metabolism, vol. 21, no. 1, pp. 17–24, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. E. J. Goetzl, H. Dolezalova, Y. Kong et al., “Distinctive expression and functions of the type 4 endothelial differentiation gene-encoded G protein-coupled receptor for lysophosphatidic acid in ovarian cancer,” Cancer Research, vol. 59, no. 20, pp. 5370–5375, 1999. View at Google Scholar · View at Scopus
  3. T. C. Spohr, J. W. Choi, S. E. Gardell et al., “Lysophosphatidic acid receptor-dependent secondary effects via astrocytes promote neuronal differentiation,” The Journal of Biological Chemistry, vol. 283, no. 12, pp. 7470–7479, 2008. View at Publisher · View at Google Scholar
  4. J. A. Weiner and J. Chun, “Schwann cell survival mediated by the signaling phospholipid lysophosphatidic acid,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 9, pp. 5233–5238, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. X. Ye, M. K. Skinner, G. Kennedy, and J. Chun, “Age-dependent loss of sperm production in mice via impaired lysophosphatidic acid signaling,” Biology of Reproduction, vol. 79, no. 2, pp. 328–336, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. V. Härmä, M. Knuuttila, J. Virtanen et al., “Lysophosphatidic acid and sphingosine-1-phosphate promote morphogenesis and block invasion of prostate cancer cells in three-dimensional organotypic models,” Oncogene, vol. 31, no. 16, pp. 2075–2089, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. M.-C. Huang, H.-Y. Lee, C.-C. Yeh, Y. Kong, C. J. Zaloudek, and E. J. Goetzl, “Induction of protein growth factor systems in the ovaries of transgenic mice overexpressing human type 2 lysophosphatidic acid G protein-coupled receptor (LPA2),” Oncogene, vol. 23, no. 1, pp. 122–129, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Aoki, “Mechanisms of lysophosphatidic acid production,” Seminars in Cell and Developmental Biology, vol. 15, no. 5, pp. 477–489, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Nakamura, T. Kishimoto, R. Ohkawa et al., “Suppression of lysophosphatidic acid and lysophosphatidylcholine formation in the plasma in vitro: proposal of a plasma sample preparation method for laboratory testing of these lipids,” Analytical Biochemistry, vol. 367, no. 1, pp. 20–27, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Bandoh, J. Aoki, H. Hosono et al., “Molecular cloning and characterization of a novel human G-protein- coupled receptor, EDG7, for lysophosphatidic acid,” The Journal of Biological Chemistry, vol. 274, no. 39, pp. 27776–27785, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. D.-S. Im, C. E. Heise, M. A. Harding et al., “Molecular cloning and characterization of a lysophosphatidic acid receptor, Edg-7, expressed in prostate,” Molecular Pharmacology, vol. 57, no. 4, pp. 753–759, 2000. View at Google Scholar · View at Scopus
  12. K. Noguchi, S. Ishii, and T. Shimizu, “Identification of p2y9/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family,” The Journal of Biological Chemistry, vol. 278, no. 28, pp. 25600–25606, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Aoki, A. Inoue, and S. Okudaira, “Two pathways for lysophosphatidic acid production,” Biochimica et Biophysica Acta, vol. 1781, no. 9, pp. 513–518, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. T. M. McIntyre, A. V. Pontsler, A. R. Silva et al., “Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARγ agonist,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 1, pp. 131–136, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Okudaira, H. Yukiura, and J. Aoki, “Biological roles of lysophosphatidic acid signaling through its production by autotaxin,” Biochimie, vol. 92, no. 6, pp. 698–706, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. A. Jarvis, C. Cain, and E. A. Dennis, “Purification and characterization of a lysophospholipase from human amnionic membranes,” The Journal of Biological Chemistry, vol. 259, no. 24, pp. 15188–15195, 1984. View at Google Scholar · View at Scopus
  17. E. Liszewska, P. Reinaud, E. Billon-Denis, O. Dubois, P. Robin, and G. Charpigny, “Lysophosphatidic acid signaling during embryo development in sheep: involvement in prostaglandin synthesis,” Endocrinology, vol. 150, no. 1, pp. 422–434, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Woclawek-Potocka, I. Kowalczyk-Zieba, and D. J. Skarzynski, “Lysophosphatidic acid action during early pregnancy in the cow: in vivo and in vitro studies,” The Journal of Reproduction and Development, vol. 56, no. 4, pp. 411–420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. I. Woclawek-Potocka, J. Komiyama, J. S. Saulnier-Blache et al., “Lysophosphatic acid modulates prostaglandin secretion in the bovine uterus,” Reproduction, vol. 137, no. 1, pp. 95–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. I. Kowalczyk-Zieba, D. Boruszewska, J. S. Saulnier-Blache et al., “Lysophosphatidic acid action in the bovine corpus luteum—an in vitro study,” The Journal of Reproduction and Development, vol. 58, no. 6, pp. 661–671, 2012. View at Publisher · View at Google Scholar
  21. D. Boruszewska, E. Sinderewicz, I. Kowalczyk-Zieba, D. J. Skarzynski, and I. Woclawek-Potocka, “Influence of lysophosphatidic acid on estradiol production and follicle stimulating hormone action in bovine granulosa cells,” Reproductive Biology, vol. 13, no. 4, pp. 344–347, 2013. View at Publisher · View at Google Scholar
  22. I. Woclawek-Potocka, K. Kondraciuk, and D. J. Skarzynski, “Lysophosphatidic acid stimulates prostaglandin E2 production in cultured stromal endometrial cells through LPA1 receptor,” Experimental Biology and Medicine, vol. 234, no. 8, pp. 986–993, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. R. A. Sorensen and P. M. Wassarman, “Relationship between growth and meiotic maturation of the mouse oocyte,” Developmental Biology, vol. 50, no. 2, pp. 531–536, 1976. View at Google Scholar · View at Scopus
  24. D. Wickramasinghe, K. M. Ebert, and D. F. Albertini, “Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes,” Developmental Biology, vol. 143, no. 1, pp. 162–172, 1991. View at Publisher · View at Google Scholar · View at Scopus
  25. J. J. Eppig, R. M. Schultz, M. O'Brien, and F. Chesnel, “Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes,” Developmental Biology, vol. 164, no. 1, pp. 1–9, 1994. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Payne and G. Schatten, “Golgi dynamics during meiosis are distinct from mitosis and are coupled to endoplasmic reticulum dynamics until fertilization,” Developmental Biology, vol. 264, no. 1, pp. 50–63, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Torner, K.-P. Brüssow, H. Alm et al., “Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation,” Theriogenology, vol. 61, no. 9, pp. 1675–1689, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. C. de Vantéry, A. C. Gavin, J. D. Vassalli, and S. Schorderet-Slatkine, “An accumulation of p34cdc2 at the end of mouse oocyte growth correlates with the acquisition of meiotic competence,” Developmental Biology, vol. 174, no. 2, pp. 335–344, 1996. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Krischek and B. Meinecke, “In vitro maturation of bovine oocytes requires polyadenylation of mRNAs coding proteins for chromatin condensation, spindle assembly, MPF and MAP kinase activation,” Animal Reproduction Science, vol. 73, no. 3-4, pp. 129–140, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. M. J. Carabatsos, C. Sellitto, D. A. Goodenough, and D. F. Albertini, “Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence,” Developmental Biology, vol. 226, no. 2, pp. 167–179, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. R. de La Fuente and J. J. Eppig, “Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling,” Developmental Biology, vol. 229, no. 1, pp. 224–236, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Reynaud, R. Cortvrindt, J. Smitz, and M. A. Driancourt, “Effects of Kit Ligand and anti-Kit antibody on growth of cultured mouse preantral follicles,” Molecular Reproduction and Development, vol. 56, no. 4, pp. 483–494, 2000. View at Google Scholar
  33. A. Torres, M. Batista, P. Diniz, L. Mateus, and L. Lopes-da-Costa, “Embryo-luteal cells co-culture: an in vitro model to evaluate steroidogenic and prostanoid bovine early embryo-maternal interactions,” In Vitro Cellular & Developmental Biology, vol. 49, no. 2, pp. 134–146, 2013. View at Publisher · View at Google Scholar
  34. A. Tokumura, M. Miyake, Y. Nishioka, S. Yamano, T. Aono, and K. Fukuzawa, “Production of lysophosphatidic acids by lysophospholipase D in human follicular fluids of in vitro fertilization patients,” Biology of Reproduction, vol. 61, no. 1, pp. 195–199, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Komatsu, S. Yamano, A. Kuwahara, A. Tokumura, and M. Irahara, “The signaling pathways linking to lysophosphatidic acid-promoted meiotic maturation in mice,” Life Sciences, vol. 79, no. 5, pp. 506–511, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Hinokio, S. Yamano, K. Nakagawa et al., “Lysophosphatidic acid stimulates nuclear and cytoplasmic maturation of golden hamster immature oocytes in vitro via cumulus cells,” Life Sciences, vol. 70, no. 7, pp. 759–767, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Holm, P. J. Booth, M. H. Schmidt, T. Greve, and H. Callesen, “High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins,” Theriogenology, vol. 52, no. 4, pp. 683–700, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. Z. Liu and D. R. Armant, “Lysophosphatidic acid regulates murine blastocyst development by transactivation of receptors for heparin-binding EGF-like growth factor,” Experimental Cell Research, vol. 296, no. 2, pp. 317–326, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. L. A. van Meeteren, P. Ruurs, C. Stortelers et al., “Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development,” Molecular and Cellular Biology, vol. 26, no. 13, pp. 5015–5022, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Boruszewska, I. Kowalczyk-Zieba, K. Piotrowska-Tomala et al., “Which bovine endometrial cells are source and target for lysophosphatidic acid?” Reproductive Biology, vol. 13, no. 1, pp. 100–103, 2013. View at Publisher · View at Google Scholar
  41. H. A. Amer, A.-R. O. Hegab, and S. M. Zaabal, “Some studies on the morphological aspects of buffalo oocytes in relation to the ovarian morphology and culture condition,” In Vitro Cellular & Developmental Biology, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Buccione, B. C. Vanderhyden, P. J. Caron, and J. J. Eppig, “FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte,” Developmental Biology, vol. 138, no. 1, pp. 16–25, 1990. View at Publisher · View at Google Scholar · View at Scopus
  43. J. A. Elvin, A. T. Clark, P. Wang, N. M. Wolfman, and M. M. Matzuk, “Paracrine actions of growth differentiation factor-9 in the mammalian ovary,” Molecular Endocrinology, vol. 13, no. 6, pp. 1035–1048, 1999. View at Google Scholar · View at Scopus
  44. B. C. Vanderhyden and A. M. Tonary, “Differential regulation of progesterone and estradiol production by mouse cumulus and mural granulosa cells by a factor(s) secreted by the oocyte,” Biology of Reproduction, vol. 53, no. 6, pp. 1243–1250, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Li, R. J. Norman, D. T. Armstrong, and R. B. Gilchrist, “Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells,” Biology of Reproduction, vol. 63, no. 3, pp. 839–845, 2000. View at Google Scholar · View at Scopus
  46. M. J. Carabatsos, J. Elvin, M. M. Matzuk, and D. F. Albertini, “Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice,” Developmental Biology, vol. 204, no. 2, pp. 373–384, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Otsuka, Z. Yao, T.-H. Lee, S. Yamamoto, G. F. Erickson, and S. Shimasaki, “Bone morphogenetic protein-15: identification of target cells and biological functions,” The Journal of Biological Chemistry, vol. 275, no. 50, pp. 39523–39528, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. J. L. Juengel, N. L. Hudson, D. A. Heath et al., “Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep,” Biology of Reproduction, vol. 67, no. 6, pp. 1777–1789, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Pennetier, S. Uzbekova, C. Perreau, P. Papillier, P. Mermillod, and R. Dalbiès-Tran, “Spatio-temporal expression of the germ cell marker genes MATER, ZAR1, GDF9, BMP15, and VASA in adult bovine tissues, oocytes, and preimplantation embryos,” Biology of Reproduction, vol. 71, no. 4, pp. 1359–1366, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Gendelman, A. Aroyo, S. Yavin, and Z. Roth, “Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos,” Reproduction, vol. 140, no. 1, pp. 73–82, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Gendelman and Z. Roth, “In vivo vs. in vitro models for studying the effects of elevated temperature on the GV-stage oocyte, subsequent developmental competence and gene expression,” Animal Reproduction Science, vol. 134, no. 3, pp. 125–134, 2012. View at Publisher · View at Google Scholar
  52. T. S. Hussein, J. G. Thompson, and R. B. Gilchrist, “Oocyte-secreted factors enhance oocyte developmental competence,” Developmental Biology, vol. 296, no. 2, pp. 514–521, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. O. V. Patel, A. Bettegowda, J. J. Ireland, P. M. Coussens, P. Lonergan, and G. W. Smith, “Functional genomics studies of oocyte competence: evidence that reduced trascript abundance for follistatin is associated with poor developmental competence of bovine oocytes,” Reproduction, vol. 133, no. 1, pp. 95–106, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. K.-B. Lee, A. Bettegowda, G. Wee, J. J. Ireland, and G. W. Smith, “Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis,” Endocrinology, vol. 150, no. 5, pp. 2463–2471, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Fukui and Y. Sakuma, “Maturation of bovine oocytes cultured in vitro: relation to ovarian activity, follicular size and the presence or absence of cumulus cells,” Biology of Reproduction, vol. 22, no. 3, pp. 669–673, 1980. View at Google Scholar · View at Scopus
  56. A. N. Fatehi, E. C. Zeinstra, R. V. Kooij, B. Colenbrander, and M. M. Bevers, “Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate,” Theriogenology, vol. 57, no. 4, pp. 1347–1355, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. M. L. Sutton-McDowall, R. B. Gilchrist, and J. G. Thompson, “Cumulus expansion and glucose utilisation by bovine cumulus-oocyte complexes during in vitro maturation: the influence of glucosamine and follicle-stimulating hormone,” Reproduction, vol. 128, no. 3, pp. 313–319, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. K. A. Preis, G. Seidel Jr., and D. K. Gardner, “Metabolic markers of developmental competence for in vitro-matured mouse oocytes,” Reproduction, vol. 130, no. 4, pp. 475–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. D. G. de Matos, C. C. Furnus, and D. F. Moses, “Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells,” Biology of Reproduction, vol. 57, no. 6, pp. 1420–1425, 1997. View at Google Scholar · View at Scopus
  60. A. Bettegowda, O. V. Patel, K.-B. Lee et al., “Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications,” Biology of Reproduction, vol. 79, no. 2, pp. 301–309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. C. M. Corn, C. Hauser-Kronberger, M. Moser, G. Tews, and T. Ebner, “Predictive value of cumulus cell apoptosis with regard to blastocyst development of corresponding gametes,” Fertility and Sterility, vol. 84, no. 3, pp. 627–633, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. F. de Loos, P. Kastrop, P. van Maurik, T. H. van Beneden, and T. A. Kruip, “Heterologous cell contacts and metabolic coupling in bovine cumulus oocyte complexes,” Molecular Reproduction and Development, vol. 28, no. 3, pp. 255–259, 1991. View at Google Scholar · View at Scopus
  63. S. Tanghe, A. van Soom, H. Nauwynck, M. Coryn, and A. de Kruif, “Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization,” Molecular Reproduction and Development, vol. 61, no. 3, pp. 414–424, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Tatemoto, N. Sakurai, and N. Muto, “Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells,” Biology of Reproduction, vol. 63, no. 3, pp. 805–810, 2000. View at Google Scholar · View at Scopus
  65. A. L. Mikkelsen, E. Høst, and S. Lindenberg, “Incidence of apoptosis in granulosa cells from immature human follicles,” Reproduction, vol. 122, no. 3, pp. 481–486, 2001. View at Google Scholar · View at Scopus
  66. S. Kölle, M. Stojkovic, G. Boie, E. Wolf, and F. Sinowatz, “Growth hormone-related effects on apoptosis, mitosis, and expression of connexin 43 in bovine in vitro maturation cumulus-oocyte complexes,” Biology of Reproduction, vol. 68, no. 5, pp. 1584–1589, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Szołtys, Z. Tabarowski, and A. Pawlik, “Apoptosis of postovulatory cumulus granulosa cells of the rat,” Anatomy and Embryology, vol. 202, no. 6, pp. 523–529, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. N. Manabe, Y. Imai, H. Ohno, Y. Takahagi, M. Sugimoto, and H. Miyamoto, “Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in pig ovaries,” Experientia, vol. 52, no. 7, pp. 647–651, 1996. View at Google Scholar · View at Scopus
  69. M. Y. Yang and R. Rajamahendran, “Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells,” Biology of Reproduction, vol. 62, no. 5, pp. 1209–1217, 2000. View at Google Scholar · View at Scopus
  70. S. Bilodeau-Goeseels and P. Panich, “Effects of oocyte quality on development and transcriptional activity in early bovine embryos,” Animal Reproduction Science, vol. 71, no. 3-4, pp. 143–155, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. H. J. Li, D. J. Liu, M. Cang et al., “Early apoptosis is associated with improved developmental potential in bovine oocytes,” Animal Reproduction Science, vol. 114, no. 1–3, pp. 89–98, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Y. Yang and R. Rajamahendran, “Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro,” Animal Reproduction Science, vol. 70, no. 3-4, pp. 159–169, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Q. Yuan, A. van Soom, J. L. M. R. Leroy et al., “Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence,” Theriogenology, vol. 63, no. 8, pp. 2147–2163, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. E. Warzych, E. Pers-Kamczyc, A. Krzywak, S. Dudzińska, and D. Lechniak, “Apoptotic index within cumulus cells is a questionable marker of meiotic competence of bovine oocytes matured in vitro,” Reproductive Biology, vol. 13, no. 1, pp. 82–87, 2013. View at Publisher · View at Google Scholar
  75. T. S. Hussein, D. A. Froiland, F. Amato, J. G. Thompson, and R. B. Gilchrist, “Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins,” Journal of Cell Science, vol. 118, no. 22, pp. 5257–5268, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. I. Woclawek-Potocka, I. Kowalczyk-Zieba, M. Tylingo, D. Boruszewska, E. Sinderewicz, and D. J. Skarzynski, “Effects of lysophopatidic acid on tumor necrosis factor α and interferon γ action in the bovine corpus luteum,” Molecular and Cellular Endocrinology, vol. 377, no. 1-2, pp. 103–111, 2013. View at Publisher · View at Google Scholar
  77. X. Ye, K. Hama, J. J. A. Contos et al., “LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing,” Nature, vol. 435, no. 7038, pp. 104–108, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. T. Kobayashi, “Effect of lysophosphatidic acid on the preimplantation development of mouse embryos,” FEBS Letters, vol. 351, no. 1, pp. 38–40, 1994. View at Publisher · View at Google Scholar · View at Scopus
  79. J. W. Jo, B. C. Jee, C. S. Suh, and S. H. Kim, “Addition of lysophosphatidic acid to mouse oocyte maturation media can enhance fertilization and developmental competence,” Human Reproduction, vol. 29, no. 2, pp. 234–241, 2014. View at Publisher · View at Google Scholar