Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: Temporal effects of follicular fluid during IVM

Reproduction, Fertility and Development

Volumn 22, Issue 7, 2010, Pages 1100-1109

  Grupen, Christopher G ^a   Armstrong, David T ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

blastocyst; cumulus expansion; embryo development; fertilisation; meiosis

Indexed keywords

PROGESTERONE;

APOPTOSIS; ARTICLE; BLASTOCYST; CELL EXPANSION; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; CUMULUS CELL; EMBRYO; FEMALE; FERTILIZATION IN VITRO; MEIOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE FLUID; OXIDATIVE STRESS; PREPUBERTY; STEROIDOGENESIS; SWINE;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CUMULUS CELLS; FEMALE; FERTILIZATION IN VITRO; FOLLICULAR FLUID; IN SITU NICK-END LABELING; LOGISTIC MODELS; MALE; MEIOSIS; OOCYTES; PREGNANCY; PROGESTERONE; SWINE;

SUIDAE; SUS;

EID: 77956259205     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09307     Document Type: Article

References (42)

1. Algriany, O., Bevers, M., Schoevers, E., Colenbrander, B., and Dieleman, S. (2004). Follicle size-dependent effects of sow follicular fluid on in vitro cumulus expansion, nuclear maturation and blastocyst formation of sow cumulus oocytes complexes. Theriogenology 62, 1483-1497. doi:10.1016/J.THERIOGENOLOGY. 2004.02.008
2. Armstrong, D. T., Xia, P., de Gannes, G., Tekpetey, F. R., and Khamsi, F. (1996). Differential effects of insulin-like growth factor-I and folliclestimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells. Biol. Reprod. 54, 331-338. doi:10.1095/BIOLREPROD54.2.331
3. Bagg, M. A., Nottle, M. B., Grupen, C. G., and Armstrong, D. T. (2006). Effect of dibutyrylcAMPon thecAMPcontent, meiotic progression, and developmental potential of in vitro matured pre-pubertal and adult pig oocytes. Mol. Reprod. Dev. 73, 1326-1332. doi:10.1002/MRD.20555
4. Bagg, M. A., Nottle, M. B., Armstrong, D. T., and Grupen, C. G. (2009). Effect of follicle size and dibutyryl cAMP on the cAMP content and gap junctional communication of porcine prepubertal cumulus-oocyte complexes during IVM. Reprod. Fertil. Dev. 21, 796-804. doi:10.1071/RD08165
5. Baltsen, M., and Byskov, A. G. (1999). Quantitation of meiosis activating sterols in human follicular fluid using HPLC and photodiode array detection. Biomed. Chromatogr. 13, 382-388. doi:10.1002/(SICI)1099-0801(199910)13:6o382:: AID-BMC89643.0.CO;2-D
6. Basini, G., Simona, B., Santini, S. E., and Grasselli, F. (2008). Reactive oxygen species and anti-oxidant defences in swine follicular fluids. Reprod. Fertil. Dev. 20, 269-274. doi:10.1071/RD07147
7. Bavister, B. D. (1989). A consistently successful procedure for in vitro fertilization of golden hamster eggs. Gamete Res. 23, 139-158. doi:10.1002/MRD.1120230202
8. Bijttebier, J., Van Soom, A., Meyer, E., Mateusen, B., and Maes, D. (2008). Preovulatory follicular fluid during in vitro maturation decreases polyspermic fertilization of cumulus-intact porcine oocytes: in vitro maturation of porcine oocytes. Theriogenology 70, 715-724. doi:10.1016/J.THERIOGENOLOGY. 2008.04.046
9. Byskov, A. G., Andersen, C. Y., and Leonardsen, L. (2002). Role of meiosis activating sterols, MAS, in induced oocyte maturation. Mol. Cell. Endocrinol. 187, 189-196. doi:10.1016/S0303-7207(01)00707-9
10. Carbone, M. C., Tatone, C., Delle Monache, S., Marci, R., Caserta, D., Colonna, R., and Amicarelli, F. (2003). Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Mol. Hum. Reprod. 9, 639-643. doi:10.1093/MOLEHR/GAG090
11. Conley, A. J., Howard, H. J., Slanger, W. D., and Ford, J. J. (1994). Steroidogenesis in the preovulatory porcine follicle. Biol. Reprod. 51, 655-661. doi:10.1095/BIOLREPROD51.4.655
12. Conti, M., Andersen, C. B., Richard, F., Mehats, C., Chun, S. Y., Horner, K., Jin, C., and Tsafriri, A. (2002). Role of cyclic nucleotide signaling in oocyte maturation. Mol. Cell. Endocrinol. 187, 153-159. doi:10.1016/S0303- 7207(01)00686-4
13. Downs, S. M. (1993). Purine control of mouse oocyte maturation: evidence that nonmetabolized hypoxanthine maintains meiotic arrest. Mol. Reprod. Dev. 35, 82-94. doi:10.1002/MRD.1080350114
14. Faerge, I., Strejcek, F., Laurincik, J., Rath, D., Niemann, H., Schellander, K., Rosenkranz, C., Hyttel, P. M., and Grondahl, C. (2006). The effect of FF-MAS on porcine cumulus-oocyte complex maturation, fertilization and pronucleus formation in vitro. Zygote 14, 189-199. doi:10.1017/ S0967199406003765
15. Flores-Alonso, J. C., Lezama-Monfil, L., Sanchez-Vazquez, M. L., Reyes, R., and Delgado, N. M. (2008). Heparin effect on in vitro nuclear maturation of bovine oocytes. Zygote 16, 1-8. doi:10.1017/S0967199407004418
16. Friberg, P. A., Larsson, D. G., and Billig, H. (2009). Dominant role of nuclear progesterone receptor in the control of rat periovulatory granulose cell apoptosis. Biol. Reprod. 80, 1160-1167. doi:10.1095/BIOLREPROD.108.073932
17. Funahashi, H., Cantley, T., and Day, B. N. (1994). Different hormonal requirements of pig oocyte-cumulus complexes during maturation in vitro. J. Reprod. Fertil. 101, 159-165. doi:10.1530/JRF.0.1010159
18. Funahashi, H., Cantley, T. C., and Day, B. N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol.Reprod. 57, 49-53. doi:10.1095/BIOLREPROD57.1.49
19. Garmey, J. C., Guthrie, H. D., Garrett, W. M., Stoler, M. H., and Veldhuis, J. D. (2000). Localization and expression of low-density lipoprotein receptor, steroidogenic acute regulatory protein, cytochrome P450 side-chain cleavage and P450 17-alpha-hydroxylase/C17-20 lyase in developing swine follicles: in situ molecular hybridization and immunocytochemical studies. Mol. Cell. Endocrinol. 170, 57-65. doi:10.1016/S0303-7207(00)00332-4
20. Grupen, C. G., Nagashima, H., and Nottle, M. B. (1997). Role of epidermal growth factor and insulin-like growth factor-I on porcine oocyte maturation and embryonic development in vitro. Reprod. Fertil. Dev. 9, 571-575. doi:10.1071/R96115
21. Grupen, C. G., McIlfatrick, S. M., Ashman, R. J., Boquest, A. C., Armstrong, D. T., and Nottle, M. B. (2003). Relationship between donor animal age, follicular fluid steroid content and oocyte developmental competence in the pig. Reprod. Fertil. Dev. 15, 81-87. doi:10.1071/RD02086
22. Grupen, C. G., Fung, M., and Armstrong, D. T. (2006). Effects of milrinone and butyrolactone-I on porcine oocyte meiotic progression and developmental competence. Reprod. Fertil. Dev. 18, 309-317. doi:10.1071/RD05125
23. Guérin, P., El Mouatassim, S., and Menezo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175-189. doi:10. 1093/HUMUPD/7.2.175
24. Hashimoto, S., Minami, N., Takakura, R., and Imai, H. (2002). Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro. Biol. Reprod. 66, 1696-1701. doi:10.1095/BIOLREPROD66.6.1696
25. Hong, J., and Lee, E. (2007). Intrafollicular amino acid concentration and the effect of amino acids in a defined maturation medium on porcine oocyte maturation, fertilization, and preimplantation development. Theriogenology 68, 728-735. doi:10.1016/J.THERIOGENOLOGY.2007.06.002
26. Høst, E., Gabrielsen, A., Lindenberg, S., and Smidt-Jensen, S. (2002). Apoptosis in human cumulus cells in relation to zona pellucida thickness variation, maturation stage, and cleavage of the corresponding oocyte after intracytoplasmic sperm injection. Fertil. Steril. 77, 511-515. doi:10.1016/S0015-0282(01)03006-0
27. Hussein, T. S., Froiland, D. A., Amato, F., Thompson, J. G., and Gilchrist, R. B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257-5268. doi:10.1242/JCS.02644
28. Ikeda, S., Saeki, K., Imai, H., and Yamada, M. (2006). Abilities of cumulus and granulosa cells to enhance the developmental competence of bovine oocytes during in vitro maturation period are promoted by midkine; a possible implication of its apoptosis suppressing effects. Reproduction 132, 549-557. doi:10.1530/REP.1.01066
29. Ito, M., Iwata, H., Kitagawa, M., Kon, Y., Kuwayama, T., and Monji, Y. (2008). Effect of follicular fluid collected from various diameter follicles on the progression of nuclear maturation and developmental competence of pig oocytes. Anim. Reprod. Sci. 106, 421-430. doi:10.1016/J.ANIREPROSCI.2007.06.003
30. Kawashima, I., Okazaki, T., Noma, N., Nishibori, M., Yamashita, Y., and Shimada, M. (2008). Sequential exposure of porcine cumulus cells to FSH and/or LH is critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vitro. Reproduction 136, 9-21. doi:10.1530/REP-08-0074
31. Luciano, A. M., Modina, S., Gandolfi, F., Lauria, A., and Armstrong, D. T. (2000). Effect of cell-to-cell contact on in vitro deoxyribonucleic acid synthesis and apoptosis responses of bovine granulosa cells to insulinlike growth factor-I and epidermal growth factor. Biol. Reprod. 63, 1580-1585. doi:10.1095/BIOLREPROD63.6.1580
32. Naito, K., Fukuda, Y., and Toyoda, Y. (1988). Effects of porcine follicular fluid on male pronucleus formation in porcine oocytes matured in vitro. Gamete Res. 21, 289-295. doi:10.1002/MRD.1120210310
33. Nandi, S., Girish Kumar, V., Manjunatha, B. M., Ramesh, H. S., and Gupta, P. S. (2008). Follicular fluid concentrations of glucose, lactate and pyruvate in buffalo and sheep, and their effects on cultured oocytes, granulosa and cumulus cells. Theriogenology 69, 186-196. doi:10.1016/J.THERIOGENOLOGY.2007.08. 036
34. Nestler, D., Risch, M., Fischer, B., and Pocar, P. (2007). Regulation of aryl hydrocarbon receptor activity in porcine cumulus-oocyte complexes in physiological and toxicological conditions: the role of follicular fluid. Reproduction 133, 887-897. doi:10.1530/REP-06-0246
35. Papanikolaou, T., Amiridis, G. S., Dimitriadis, I., Vainas, E., and Rekkas, C. A. (2008). Effect of plasmin, plasminogen activators and a plasmin inhibitor on bovine in vitro embryo production. Reprod. Fertil. Dev. 20, 320-327. doi:10.1071/RD07108
36. Peluso, J. J., Liu, X., Gawkowska, A., and Johnston-MacAnanny, E. (2009). Progesterone activates a progesterone receptor membrane component 1-dependent mechanism that promotes human granulosa/luteal cell survival but not progesterone secretion. J. Clin. Endocrinol. Metab. 94, 2644-2649. doi:10.1210/JC.2009-0147
37. Petters, R. M., and Wells, K. D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 61-73.
38. Shimada, M., Ito, J., Yamashita, Y., Okazaki, T., and Isobe, N. (2003). Phosphatidylinositol 3-kinase in cumulus cells is responsible for both suppression of spontaneous maturation and induction of gonadotropinstimulated maturation of porcine oocytes. J. Endocrinol. 179, 25-34. doi:10.1677/JOE.0. 1790025
39. Shimada, M., Yamashita, Y., Ito, J., Okazaki, T., Kawahata, K., and Nishibori, M. (2004). Expression of two progesterone receptor isoforms in cumulus cells and their roles during meiotic resumption of porcine oocytes. J. Mol. Endocrinol. 33, 209-225. doi:10.1677/JME.0.0330209
40. Tatemoto, H., Muto, N., Sunagawa, I., Shinjo, A., and Nakada, T. (2004). Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol. Reprod. 71, 1150-1157. doi:10.1095/BIOLREPROD.104.029264
41. Vanderhyden, B. C., Caron, P. J., Buccione, R., and Eppig, J. J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulose cell differentiation. Dev. Biol. 140, 307-317. doi:10.1016/0012-1606 (90)90081-S
42. Vatzias, G., and Hagen, D. R. (1999). Effects of porcine follicular fluid and oviduct-conditioned media on maturation and fertilization of porcine oocytes in vitro. Biol. Reprod. 60, 42-48. doi:10.1095/BIOLREPROD60.1.42