Enhancement of developmental capacity of meiotically inhibited bovine oocytes by retinoic acid

Human Reproduction

Volumn 17, Issue 10, 2002, Pages 2706-2714

  Duque, P ^a   Diez C ^a   Royo, L ^a   Lorenzo, P L ^b   Carneiro, G ^c   Hidalgo, C O ^a   Facal, N ^a   Gomez E ^a  

^a Área de Cultivos Hortofrutícolas y Forestales   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bovine; In vitro; Oocyte; Retinoic; Roscovitine

Indexed keywords

ALITRETINOIN; RETINOIC ACID; ROSCOVITINE;

ANIMAL CELL; ARTICLE; ASPIRATION; BLASTOCYST; CATTLE; CELL COUNT; CELL LABELING; CELL MIGRATION; CELL SURVIVAL; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; COW; CRYOPRESERVATION; CUMULUS OOPHORUS; CYTOPLASM; DRUG EFFECT; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPY; GRANULE CELL; IN VITRO STUDY; MEIOSIS; MITOSIS INHIBITION; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVIDUCT; SPECIES DIFFERENCE; VITRIFICATION; WARMING;

ANIMALIA; BOS TAURUS; BOVINAE; FALLOPIA;

EID: 0036796212     PISSN: 02681161     EISSN: None     Source Type: Journal    
DOI: 10.1093/humrep/17.10.2706     Document Type: Article

References (71)

1. Besenfelder, U.L., Solti, J., Seregi, M., Müller, M. and Brem, G. (1996) Different roles for B-carotene and vitamin A in the reproduction of rabbits. Theriogenology, 45, 1583-1591.
2. Bevers, M.M., Dieleman, S.J., van der Hurk, R. and Izadyar, F. (1997) Regulation and modulation of oocyte maturation in the bovine. Theriogenology, 47, 13-22.
3. Blondin, P., Conene, K., Guilbault, L.A. and Sirard, M.A. (1997) In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology, 47, 1061-1075.
4. Bucco, R.A., Melner, M.H., Gordon, D.S., Leers-Sucheta, S. and Ong, D.E. (1995) Inducible expression of cellular retinoic acid-binding protein II in rat ovary: gonadotropin regulation during luteal development. Endocrinology, 136, 2730-2740.
5. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J., 10, 940-954.
6. Cran, D.G. and Esper, C.R. (1990) Cortical granules and the cortical reaction in mammals. Journal of Reprod. Fertil., 42 (Suppl.), 177-188.
7. Damiani, P., Fissore, R.A., Cibelli, J.B., Long, C.R., Balise, J.J., Robl, J.M. and Duby, R.T. (1996) Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev., 45, 521-534.
8. Donnay, I., Auquier, Ph., Kaidi, S., Carolan, C., Lonergan, P., Mermillod, P. and Massip, A. (1998) Vitrification of in vitro produced bovine blastocysts: methodological studies and developmental capacity. Anim. Reprod. Sci., 52, 93-104.
9. Ducibella, T., Anderson, E., Albertini, D.F., Aalberg, J. and Rangarajan, S. (1988) Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev. Biol., 130, 184-197.
10. Duque, P., Gómez, E., Hidalgo, C., Facal, N., Fernández, I. and Díez, C. (2002) Retinoic acid during in vitro maturation of bovine oocytes promotes embryonic development and early differentiation. Theriogenology, 57, 364 (abstract).
11. Eberhardt, D.M., Will, W.A. and Godkin, J.D. (1999) Retinol administration to superovulated ewes improves in vitro embryonic viability. Biol. Reprod., 60, 1483-1487.
12. Edwards, R.G. (1965) Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature, 208, 349-351.
13. Ellington, J.E., Carney, E.W., Farrell, P.B., Simkin, M.E. and Foote, R.H. (1990) Bovine 1-2 cell embryo development using a simple medium in three oviduct epithelial cell coculture systems. Biol. Reprod., 43, 97-104.
14. Flament, S., Bodart, J.F., Bertout, M., Browaeys, E., Rousseau, A. and Vilain, J.P. (2000) Differential effects of 6-DMAP, olomoucine and roscovitine on Xenopus oocytes and eggs. Zygote, 8, 3-14.
15. Fouladi Nashta, A.A., Waddington, D. and Campbell, K.H.S. (1998) Maintenance of bovine oocytes in meiotic arrest and subsequent development in vitro: a comparative evaluation of antral follicle culture with other methods. Biol. Reprod., 59, 255-262.
16. Griffith, M. and Zile, M.H. (2000) Retinoic acid, midkine and defects of secondary neurulation. Teratology, 62, 123-133.
17. Hattori, M., Takesue, K., Nishida, N., Kato, Y. and Fujihara, N. (2000) Inhibitory effect of retinoic acid on the development of immature porcine granulosa cells to mature cells. J. Mol. Endocrinol., 25, 53-61.
18. Hidalgo, C., Díez, C., Duque, P., Facal, N., Prendes, J.M., Fernández, I. and Gómez, E. (2002) Improved cumulus-oocyte complex yields from heifers treated with retinol. Theriogenology, 57, 672 (abstract).
19. Holm, P., Booth, P.J., Schmidt, M.H., Greve, T. and Callesen, H. (1999) 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, 52, 683-700.
20. Hosoe, M. and Shioya, Y. (1997) Distribution of cortical granules in bovine oocytes classified by cumulus complex. Zygote, 5, 371-376.
21. Hyttel, P., Xu, K.P. and Greve, T. (1988) Ultrastructural abnormalities of in vitro fertilization of in vitro matured bovine oocytes. Anat. Embryol. (Berl.), 178, 47-52.
22. Hyttel, P., Fair, T., Callesen, H. and Greve, T. (1997) Oocyte growth, capacitation and final maturation in cattle. Theriogenology, 47, 23-32.
23. Ikeda, S., Nishikimi, A., Ichihara-Tanaka, K., Muramatsu, T. and Yamada, M. (2000a) cDNA cloning of bovine midkine and production of the recombinant protein, which affects in vitro maturation of bovine oocytes. Mol. Reprod. Dev., 57, 99-107.
24. Ikeda, S., Ichihar-Tanaka, K., Azuma, T., Muramatsu, T. and Yamada, M. (2000b) Effects of midkine during in vitro maturation of bovine oocytes on subsequent developmental competence. Biol. Reprod., 63, 1067-1074.
25. Johansson, S., Dencker, L. and Dantzer, V. (2001) Immunohistochemical localization of retinoid binding proteins at the materno-fetal interface of the porcine epitheliochorial placenta. Biol. Reprod., 64, 60-68.
26. Kaidi, S., Donnay, I., Massip, A. and Dessy, F. (2000) Effect of freezing or vitrification on the quality of in vitro-produced bovine blastocysts. Theriogenology, 53, 257.
27. Karino, S., Minegishi, T., Ohyama, Y., Tano, M., Nakamura, K., Miyamoto, K., Tanaka, S. and Ibuki, Y. (1995) Regulation and localization of midkine in rat ovary. FEBS Lett., 362, 147-150.
28. Kasinathan, P., Knott, J.G., Spell, A.R., King, T.L. and Robl, J.M. (2001) Effect of roscovitine delayed maturation on development of nuclear transplant embryos. Theriogenology, 55, 273 (abstract).
29. Kastrop, P.M.M., Bevers, M.M., Destree, O.H.J. and Kruip, Th.A.M. (1990) Analysis of protein synthesis in morphologically classified bovine follicular oocytes before and after maturation in vitro. Mol. Reprod. Dev., 26, 222-226.
30. cdc2 prevents chromosome condensation in porcine oocytes. Theriogenology, 53, 457 (abstract).
31. Kubelka, M., Motlik, J., Fulka, J.Jr., Prochazka, R., Rimkevikova, Z. and Fulka, J. (1988) Time sequence of germinal vesicle breakdown in pig oocytes after cycloheximide and p-aminobenzamidine block. Gamete Res., 19, 423-431.
32. Lane, M.A., Chen, A.C., Roman, S.D., Derguini, F. and Gudas, L.J. (1999) Removal of LIF (leukemia inhibitory factor) results in increased vitamin A (retinol) metabolism to 4-oxoretinol in embryonic stem cells. Proc. Natl. Acad. Sci. USA, 96, 13524-13529.
33. Long, C.R., Damiani, P., Pinto-Correia, C., MacLean, R.A., Duby, R.T. and Robl, J.M. (1994) Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization. J. Reprod. Fertil., 102, 361-369.
34. Lorenzo, P.L., Illera, M.J., Illera, J.C. and Illera, M. (1994) Enhancement of cumulus expansion and nuclear maturation during bovine oocyte maturation in vitro by the addition of epidermal growth factor and insulin-like growth factor I. J. Reprod. Fertil., 101, 697-701.
35. Mangelsdorf, D.J., Umesono, K. and Evans, R.M. (1994) The retinoid receptors. In Sporn, M.B., Roberts, A.B. and Goodman, D.S. (eds), The Retinoids: Biology, Chemistry and Medicine. Raven Press, New York, pp. 319-349.
36. Marchal, R., Tomanek, M., Terqui, M. and Mermillod, P. (2001) Effects of cell cycle dependent kinases inhibitor on nuclear and cytoplasmic maturation of porcine oocytes. Mol. Reprod. Dev., 60, 65-73.
37. Mermillod, P., Tomanek, M., Marchal, R. and Meijer, L. (2000) High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 h in culture by specific inhibition of MPF kinase activity. Mol. Reprod. Dev., 55, 89-95.
38. Minegishi, T., Karino, S., Tano, M., Ibuki, Y. and Miyamoto, K. (1996) Regulation of midkine messenger ribonucleic acid levels in cultured rat granulosa cells. Biochem. Biophys. Res. Commun., 229, 799-805.
39. Minegishi, T., Hirakawa, T., Kishi, H., Abe, K., Tano, M., Abe, Y. and Miyamoto, K. (2000) The mechanisms of retinoic acid-induced regulation on the follicle-stimulating hormone receptor in rat granulosa cells. Biochim. Biophys. Acta, 1495, 203-211.
40. Mitalipov, S.M., Nusser, K.D. and Wolf, D.P. (2001) Parthenogenetic activation of rhesus monkey oocytes and reconstructed embryos. Biol. Reprod., 65, 253-259.
41. Mohan, M., Malayer, J.R., Geisert, R.D. and Morgan, G.L. (2001) Expression of retinol-binding protein messenger RNA and retinoic acid receptors in preattachment bovine embryos. Mol. Reprod. Dev., 60, 289-296.
42. Mohan, M., Malayer, J.R., Geisert, R.D. and Morgan, G.L. (2002) Expression patterns of retinoid X receptors, retinaldehyde dehydrogenase, and peroxisome proliferator activated receptor gamma in bovine preattachment embryos. Biol. Reprod., 66, 692-700.
43. Morris-Kay, G.M. and Ward, S.J. (1999) Retinoids and mammalian development. Int. Rev. Cytol., 188, 73-131.
44. Nagano, M., Takahashi, Y. and Katagiri, S. (1999) In vitro fertilization and cortical granule distribution of bovine oocytes having heterogeneous ooplasm with dark clusters. J. Vet. Med. Sci., 61, 531-535.
45. Nicosia, S.V., Woil, D.P. and Inoe, M. (1977) Cortical granule distribution and cell surface characteristics in mouse eggs. Dev. Biol., 57, 56-74.
46. Ohyama, Y., Miyamoto, K., Minamino, N. and Matsuo, H. (1994) Isolation and identification of midkine and pleiotrophin in bovine follicular fluid. Mol. Cell. Endocrinol., 105, 203-208.
47. Okada, A., Yanagimachi, R. and Yanagimachi, M. (1986) Development of a cortical granule-free area of cortex and the perivitelline space in the hamster oocyte during maturation and following ovulation. J. Submicrosc. Cytol., 18, 233-247.
48. Old, R.W., Smith, D.P., Mason, C.S., Marklew, S. and Jones E.A. (1995) Effects of retinoic acid on Xenopus embryos. Biochem. Soc. Symp., 62, 157-175.
49. Ong, D.F. and Page, D.L. (1986) Quantitation of cellular retinol-binding protein in human organs. Am. J. Clin. Nutr., 44, 425-430.
50. Parrish, J.J., Susko-Parrish, J.L., Leibifried-Ruthledge, M.L., Critser, S.E., Eyestone, W.H. and First, N.L. (1986) Bovine in vitro fertilization with frozen-thawed semen. Theriogenology, 25, 591-600.
51. Pavlok, A., Kalab, P. and Bobak, P. (1997) Fertilization competence of bovine normally matured or aged oocytes derived from different antral follicles: morphology, protein synthesis, H1 and MBP kinase activity. Zygote, 5, 235-246.
52. Pavlok, A., Kanaka, J., Motlik, J. and Vodicka, P. (2000) Culture of bovine oocytes from small antral follicles in meiosis-inhibiting medium with butyrolactone I: RNA synthesis, nucleolar morphology and meiotic competence. Anim. Reprod. Sci., 64, 1-11.
53. Sapin, V., Chaib, S., Blanchon, L., Alexandre-Gouabau, M.C., Lemery, D., Charbonne, F., Gallot, D., Jacquetin, B., Dastugue, B. and Azais-Braesco, V. (2000) Esterification of vitamin A by the human placenta involves villous mesenchymal fibroblasts. Pediatr. Res., 48, 565-572.
54. Shaw, D.W., Farin, P.W., Washburn, S.P. and Britt, J.H. (1995) Effect of retinol palmitate on ovulation rate and embryo quality in superovulated cattle. Theriogenology, 44, 51-58.
55. Sirard, M.-A., Richard, F. and Mayes, M. (1998) Controlling meiotic resumption in bovine oocytes: a review. Theriogenology, 49, 483-497.
56. Szollosi, D. (1967) Development of cortical granules and cortical reaction in rat and hamster eggs. Anat. Rec., 159, 431-466.
57. Thaller, C., Hofmann, C. and Eichele, G. (1993) 9-cis-retinoic acid, a potent inducer of digit pattern duplications in the chick wing bud. Development, 118, 957-965.
58. Thompson, J.G., Gardner, D.K., Pugh, P.A., McMillan, W.H. and Tervit, H.R. (1995) Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos. Biol. Reprod., 53, 1385-1391.
59. Trounson, A., Anderiesz, C. and Jones, G. (2001) Maturation of human oocytes in vitro and their developmental competence. Reproduction, 121, 51-75.
60. Van de Leemput, E.E., Vos, P.L.A.M., Zeinstra, E.C., Bevers, M.M., van der Weijden, G.C. and Dieleman, S.J. (1999) Improved in vitro embryo development using in vivo matured oocytes from heifers superovulated with a controlled preovulatory LH surge. Theriogenology, 52, 335-349.
61. Van Soom, A., Boerjan, M., Ysebaert, M.T. and De Kruif, A. (1996) Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol. Reprod. Dev., 45, 171-182.
62. Van Wagtendonk-De Leeuw, A.M., Den Daas, J.H.G., Kruip, T.H.A.M. and Rall, W.F. (1995) Comparison of the efficacy of conventional slow freezing and rapid cryopreservation methods for bovine embryos. Cryobiology, 32, 157-167.
63. Wang, W.-H., Sun, Q.-Y., Hosoe, M., Shioya, Y. and Day, B.N. (1997a) Quantified analysis of cortical granule distribution and exocytosis of porcine oocytes during meiotic maturation and activation. Biol. Reprod., 56, 1376-1383.
64. Wang, W., Hosoe, M., Li, R. and Shioya, Y. (1997b) Development of the competence of bovine oocytes to release cortical granules and block polyspermy after meiotic maturation. Dev. Growth. Differ., 39, 607-615.
65. Wardlaw, S.A., Bucco, R.A., Zheng, W.L. and Ong, D.E. (1997) Variable expression of cellular retinol- and cellular retinoic acid-binding proteins in the rat uterus and ovary during the estrous cycle. Biol. Reprod., 56, 125-132.
66. Wellik, D.M., Norback, D.H. and Deluca, H.F. (1997) Retinol is specifically required during midgestation for neonatal survival. Am. J. Physiol., 272, E25-E29.
67. Whaley, S.L., Hedgpeth, V.S. and Britt, J.H. (1997) Evidence that injection of vitamin A before mating may improve embryo survival in gilts fed normal or high energy diets. J. Anim. Sci., 75, 1071-1077.
68. Whaley, S.L., Hedgpeth, V.S., Farin, C.E., Martus, N.S., Jayes, F.C.L. and Britt, J.H. (2000) Influence of vitamin A injection before mating on oocyte development, follicular hormones, and ovulation in gilts fed high-energy diets. J. Anim. Sci., 78, 1598-1607.
69. Yanagimachi, R. (1994) Mammalian fertilization. In Knobil E. and Neill, J.D. (eds), The Physiology of Reproduction. Raven Press, New York, pp. 189-317.
70. Zheng, W.L., Bucco, R.A., Sierra-Rievera, E., Osteen, K.G., Melner, M.H. and Ong, D.E. (1999) Synthesis of retinoic acid by rat ovarian cells that express cellular retinoic acid-binding protein-II. Biol. Reprod., 60, 110-114.
71. Zile, M.H. (2001) Function of vitamin A in vertebrate embryonic development. J. Nutr., 131, 705-708.