Follicular oocyte growth and acquisition of developmental competence

Animal Reproduction Science

Volumn 78, Issue 3-4, 2003, Pages 203-216

  Fair, Trudee ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Follicle cells; Mammals; Meiosis; Morphology; Oogenesis

Indexed keywords

MAMMALIA;

EID: 0042785544     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-4320(03)00091-5     Document Type: Article

References (110)

1. Aaltonen, J., Laitinen, M.P., Vuojolainen, K., Jaatinen, R., Horelli-Kuitunen, N., Seppa, L., Louhio, H., Tuuri, T., Sjoberg, J., Butzow, R., Hovata, O., Dale, L., Ritvos, O., 1999. Human growth differentiation factor-9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab. 84, 2744-2750.
2. Ackert, C.L., Gittens, J.E.I., O'Brien, M.J., Eppig, J.J., Kidder, G.M., 2001. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev. Biol. 233, 258-270.
3. Adams, G.P., Matteri, R.L., Kastelic, J.P., Ko, J.C.H., Ginther, O., 1992. Association between surges of follicle-stimulating hormone and the emergence of follicular waves in heifers. J. Reprod. Fertil. 94, 177-188.
4. Adashi, E.Y., 1992. Intraovarian regulation: the IGF-I example. Reprod. Fertil. Dev. 4, 497-504.
5. Assey, R.J., Hyttel, P., Greve, T., Purwantara, B., 1994. Oocyte morphology in dominant and subordinate follicles. Mol. Reprod. Dev. 37, 335-344.
6. Baker, T.G., Franchi, L.L., 1967. The fine structure of chromosomes in bovine primordial oocytes. J. Reprod. Fertil. 14, 511-513.
7. Baker, T.G., Hunter, R.H.F., 1978. Oogenesis and follicular growth in the cow: implications for superovulation. In: Sreenan J.M. (Ed.), Control of Reproduction in the Cow. CEC Publications, Luxembourg, pp. 34-49.
8. Bao, B., Garverick, H.A., 1998. Expression of steroidogenic enzyme and gonadotrophin receptor genes in bovine follicles during ovarian follicular waves: a review. J. Anim. Sci. 76, 1466-1473.
9. Blondin, P., Guibault, L., Sirard, M.A., 1997. The time interval between FSH-P administration and slaughter can influence the developmental competence of beef heifer oocytes. Theriogenology 48, 803-813.
10. Blondin, P., Bousquet, D., Twagiramungu, H., Barnes, F., Sirard, M.A., 2002. Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38-43.
11. Bodensteiner, K.J., Clay, C.M., Moeller, C.L., Sawyer, H.R., 1999. Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 60, 381.
12. Braw-Tal, R., Yossefi, S., 1997. Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165-171.
13. Brower, P.T., Schultz, R.M., 1982. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev. Biol. 84, 455-464.
14. Buccione, R., Cecconi, S., Tatone, C., Mangia, F., Colonna, R., 1987. Follicle cell regulation of mammalian oocyte growth. J. Exp. Zool. 242, 351-354.
15. Buccione, R., Vanderhyden, B.C., Caron, P.J., Eppig, J.J., 1990. FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev. Biol. 138, 16-25.
16. Byskov, A.G., Skakkebaek, N.E., Stafanger, G., Peters, H., 1977. Influence of ovarian surface epithelium and rete ovarii on follicle formation. J. Anat. 123, 77-86.
17. Campbell, B.K., Picton, H.M., Mann, G.E., McNeilly, A.S., Baird, D.T., 1991. Effect of steroid- and inhibin-free ovine follicular fluid on ovarian follicles and ovarian hormone secretion. J. Reprod. Fert. 93, 81-96.
18. Carabatsos, M.J., Sellitto, C., Goodenough, D.A., Albertini, D.F., 2000. Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev. Biol. 226, 167-179.
19. Cecconi, S., Tatone, C., Buccione, R., Mangia, F., Colonna, R., 1991. Granulosa cell-oocyte interactions: the phosphorylation of specific proteins in mouse oocytes at the germinal vesicle stage is dependent on the differentiative state of companion somatic cells. J. Exp. Zool. 258, 249-254.
20. Crozet, N., Kanka, J., Motlik, J., Fulka, J., 1986. Nucleolar fine structure and RNA synthesis in bovine oocytes from antral follicles. Gamete Res. 14, 65-73.
21. Dong, J.W., Albertini, D.F., Nishimori, K., Kumar, T.R., Lu, N.E, Matzuk, M.M., 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531-535.
22. Driancourt, M.A., 1991. Follicular dynamics in sheep and cattle. Theriogenology 35, 55-68.
23. Driancourt, M.A., Reynand, K., Cortvrindt, R., Smitz, J., 2000. Roles of KIT and KIT LIGAND in ovarian function. Rev. Reprod. 5, 143-152.
24. Dube, J.L., Wang, P., Elvin, J., Lyons, K.M., Celeste, A.J., Matzuk, M.M., 1998. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 12, 1809-1817.
25. Durlinger, A.L., Visser, J.A., Themmen, A.P., 2002. Regulation of ovarian function: the role of anti-mullerian hormone. Reproduction 124, 601-609.
26. Elvin, J.A., Clark, A.T., Wang, P., Nishimori, K., Matzuk, M.M., 1999. Molecular charcterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol. 13, 1018-1034.
27. Eppig, J.J., 1979. A comparison between oocytes growth in culture with granulose cells and oocytes with granuslosa cell-oocyte junctional contact maintained in vitro. J. Exp. Zool. 209, 345-353.
28. Eppig, J.J., 1991. Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13, 569-574.
29. Eppig, J.J., Peters, A.H.F.M., Telfer, E.E., Wigglesworth, K., 1993. Production of cumulus expansion enabling factor by mouse oocytes grown in vitro: preliminary characterization of the factor. Mol. Reprod. Dev. 34, 450-456.
30. Eppig, J.J., 2001. Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829-938.
31. Erickson, B.H., 1966. Development and senescence of the post natal bovine ovary. J. Anim. Sci. 25, 800-805.
32. Espey, L.L., 1994. Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol. Reprod. 50, 233-238.
33. Faerge, I., Mayes, M., Hyttel, P., Sirard, M.A., 2001. Nuclear ultrastmcture in bovine oocytes after inhibition of meiosis by chemical and biological inhibitors. Mol. Reprod. Dev. 59, 459-467.
34. Fair, T., Hyttel, P., Greve, T., 1995. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437-442.
35. Fair, T., Hyttel, P., Greve, T., Boland, M., 1996. Nucleus structure and transcriptional activity in relation to oocyte diameter in cattle. Mol. Reprod. Dev. 43, 503-512.
36. Fair, T., Hulshof, S.C.J., Hyttel, P., Boland, M., Greve, T., 1997a. Bovine oocyte ultrastructure in primordial to tertiary follicles. Anat. Embryol. 195, 327-336.
37. Fair, T., Hulshof, S.C.J., Hyttel, P., Boland, M., Greve, T., 1997b. Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Mol. Reprod. Devel. 46, 208-215.
38. Fair, T., Hyttel, P., 1997. Oocyte growth in cattle - ultrastructure, transcription and developmental competence. In: Motta P.M. (Ed.), Microscopy of Reproduction and Development: A Dynamic Approach. Antonio Delfino, Rome, pp. 109-118.
39. Fair, T., Hyttel, P., Motlik, J., Boland, M.P., Lonergan, P., 2002. Maintenance of meiotic arrest in bovine oocytes in vitro using butyrolactone I: effects on oocyte ultrastructure and nucleolus function. Mol. Reprod. Dev. 62, 375-386.
40. Flaws, J.A., Hirshfield, A.N., Hewitt, J.A., Babus, J.K., Furth, P.A., 2001. Effect of Bcl-2 on the primordial follicle endowment in the mouse ovary. Biol. Reprod. 64, 1153-1159.
41. Hagemann, L.J., 1999. Influence of the dominant follicle on oocytes from subordinate follicles. Theriogenology 51, 449-459.
42. Hashimoto, S., Minami, N., Takakura, R., Imai, H., 2002. Bovine immature oocytes acquire developmental competence during meiotic arrest in vitro. Biol. Reprod. 66, 1696-1701.
43. Hayashi, M., McGee, E.A., Min, G., Klein, C., Rose, U.M., van Duin, M., Hseueh, A.J., 1999. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236-1244.
44. Herlands, R.L., Schultz, R.M., 1984. Regulation of mouse oocyte growth: probable nutritional role for intercellular communication between follicle cells and oocytes in oocyte growth. J. Exp. Zool. 229, 317-325.
45. Hulshof, S.C.J., Bevers, M.M., van der Donk, H.A., van den Hurk, R., 1992. The isolation and characterization of preantral follicles from foetal bovine ovaries. In: Proceedings of the 12th International Congress on Animal Reproduction, vol. 1, The Hague, pp. 336-338.
46. Hsu, C.J., Holmes, S.D., Hammond, J.M., 1987. Ovarian epidermal growth factor-like activity. Concentrations in porcine follicular fluid during follicular enlargement. Biochem. Biophys. Res. Commun. 147, 242-247.
47. Hyttel, P., Callesen, H., Greve, T., 1986. Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J. Reprod. Fertil. 76, 645-656.
48. Hyttel, P., Greve, T., Callesen, H., 1989. Ultrastructural aspects of oocyte maturation and fertilization in cattle. J. Reprod. Fertil. 38 (Suppl.), 35-47.
49. Hyttel, P., Fair, T., Callesen, H., Greve, T., 1997. Oocyte growth. Theriogenology 47, 23-32.
50. Itahana, K., Morikazu, Y., Takeya, T., 1996. Differential expression of four connexin genes, Cx-26, Cx-303, Cx-32 and Cx-43, in the porcine ovarian follicle. Endocrinology 137, 5036-5044.
51. Itoh, T., Kacchi, M., Abe, H., Sendai, Y., Hoshi, H., 2002. Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol. Reprod. 67, 1099-1105.
52. Jaatinen, R., Laitinen, M.P., Vuojolainen, K., Aaltonen, J., Louhio, H., Heikinheimo, M., Ritvos, O., 1999. Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homologue GDF-9B. Mol. Cell. Endocrinol. 156, 189-193.
53. Johnson, M.L., Redmer, D.A., Reynolds, L.P., Grazul-Bilska, A.T., 1999. Expression of gap junctional proteins connexin 43, 32 and 26 throughout follicular development and atresia in cows. Endocrine 10, 43-51.
54. Juneja, S.C., Barr, K.J., Enders, G.C., Kidder, G.M., 1999. Defects in germ line and gonads of mice lacking connexin 43. Biol. Reprod. 60, 1263-1270.
55. Kitagawa, M., Okabe, T., Ogino, H., Matsumoto, H., Suzuki-Takahashi, I., Kokubo, T., Higashi, H., Saitoh, S., Taya, Y., Yasuda, H., Ohba, Y., Nishimura, S., Tanaka, N., Okuyama, A., 1993. Butyrolactone I, a selective inhibitor of cdk2 and cdc2 kinase. Oncogene 8, 2425-2432.
56. Kubelka, M., Motlik, J., Schultz, R.M., Pavlok, A., 2000. Butyrolactone I reversibly inhibits meiotic maturation of bovine oocytes without influencing chromosome condensation activity. Biol. Reprod. 62, 292-301.
57. Law, A.S., Logue, D.N., O'Shea, T., Webb, R., 1992. Evidence for the action of bovine follicular fluid factor(s) other than inhibin in suppressing follicular development and delaying estrous in heifers. J. Reprod. Fert. 96, 603-616.
58. Lee, W.S., Otsuka, F., Moore, R.K., Shimasaki, S., 2001. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol. Reprod. 65, 994-999.
59. Liang, L., Soyal, S.M., Dean, J., 1997. FIGalpha, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 24, 4939-4947.
60. Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P., Gordon, I., 1994. Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48-53.
61. Lonergan, P., Dinnyes, A., Fair, T., Yang, X., Boland, M., 2000. Bovine oocyte and embryo development following meiotic inhibition with butyrolactone I. Mol. Reprod. Dev, 57, 204-209.
62. Lonergan, P., Faerge, I., Maddox Hyttel, P., Boland, M.P., Fair, T., 2003. Ultrastructural modifications in bovine oocytes maintained in meiotic arrest in vitro using roscovitine or butyrolactone I. Mol. Reprod. Dev. 64, 69-78.
63. Lussier, J.G., Matton, P., Dufour, J.J., 1987. Growth rates of follicles in the ovary of the cow. J. Reprod. Fertil. 81, 301-307.
64. Matton, P., Adelakoun, V., Couture, Y., Dufour, J.J., 1981. Growth and replacement of bovine ovarian follicles during the estrous cycle. J. Anim. Sci. 37, 48-53.
65. McGrath, S.A., Esquela, A.F., Lee, S.J., 1995. Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9, 131-136.
66. McNatty, K.P., Smith, P., Hudson, N.L., Heath, D.A., Tisdall, D.J., W-S.O., Braw-Tal, R. 1995. Development of the sheep ovary during fetal and early neonatal life and the effect of fecundity genes. J. Reprod. Fertil. 49 (Suppl.) 123-135.
67. Meijer, L., Kim, S.H., 1997. Chemical inhibitors of cyclin-dependent kinases. Methods Enzymol. 283, 113-128.
68. Mermillod, P., Tomanek, M., Marchal, R., Meijer, L., 2000. High developmental competence of cattle oocytes maintained at the germinal vesicle stage for 24 h culture by specific inhibition of MPF kinase activity. Mol. Reprod. Dev. 55, 89-95.
69. Mihm, M., Bagusi, A., Boland, M.P., Roche, J.F., 1994. Association between the duration of dominance of the ovulatory follicle and pregnancy rate in beef heifers. J. Reprod. Fertil. 102, 123-130.
70. Mihm, M., Curran, N., Hyttel, P., Knight, P.G., Boland, M.P., Roche, J.F., 1999. Effect of dominant follicle persistence on follicular fluid oestradiol and inhibin and on oocyte maturation in heifers. J. Reprod. Fertil. 116, 293-304.
71. Mitchell, P.A., Burghardt, R.C., 1986. The ontogeny of nexuses (gap junctions) in the ovary of the fetal mouse. Anat. Rec. 214, 283-288.
72. Monniaux, D., Pisselet, C., 1992. Control of proliferation and differentiation of ovine granulose cells by insulin-like growth factor-I and follicle stimulating hormone in vitro. Biol. Reprod. 46, 109-119.
73. Motro, B., Bernstein, A., 1993. Dynamic changes in ovarian c-kit and steel expression during the estrous reproductive cycle. Dev. Dyn. 197, 69-79.
74. Nilsson, E.E., Parrot, J.A., Skinner, M.K., 2001. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol. Cell. Endocrinol. 175, 123-130.
75. Nilsson, E.E., Kezele, P., Skinner, M.K., 2002a. Leukeamia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol. Cell. Endocrinol. 188, 65-73.
76. Nilsson, E.E., Skinner, M.K., 2002b. Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol. Reprod. 67, 1018-1024.
77. Nuttinck, F., Peynot, N., Humblot, P., Massip, A., Dessy, F., Flechon, J.E., 2000. Comparative immunohistochemical distribution of connexin 37 and connexin 43 throughout folliculogenesis in the bovine ovary. Mol. Reprod. Dev. 57, 60-66.
78. O'Shea, T., Hilliard, M.A., Anderson, T., Bindon, B.M., Findlay, J.K., Tsonis, C.G., Wilkins, J.F., 1994. Inhibin immunization for increasing ovulation rate and superovulation. Theriogenology 41, 3-17.
79. Otsuka, F., Yao, Z., Lee, T., Yamamoto, S., Erickson, G.F., Shimasakai, S., 2000. Bone morphogenetic protein-15. J. Bio. Chem. 275, 39523-39528.
80. Oussaid, B., Lonergan, P., Khatir, H., Guler, A., Monniaux, D., Touze, J.L., Beckers, J.F., Cognie, Y., Mermillod, P., 2000. Effect of GnRH antagonist-induced prolonged follicular phase on follicular atresia and oocyte developmental competence in vitro in superovulated heifers. J. Reprod. Fertil. 118, 137-144.
81. Parrott, J.A., Skinner, M.K., 1997. Direct actions of kit-ligand on theca cell growth and differentiation during follicle development. Endocrinology 138, 3819-3827.
82. Parrott, J.A., Skinner, M.K., 2000. Kit-ligand actions on ovarian stromal cells: effects on theca cell recruitment and steroid production. Mol. Reprod. Dev. 55, 55-64.
83. Pavlok, A., Lucas-Hahn, A., Niemann, H., 1992. Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63-67.
84. Pavlok, A., Kopecny, V., Lucas-Hahn, A., Niemann, H., 1993. Transcriptional activity and nuclear ultrastructure of 8-cell embryos developed by in vitro maturation and fertilization of oocytes from different growth categories of antral follicles. Mol. Reprod. Dev. 35, 233-243.
85. Pavlok, A., Kanka, J., Motlik, J., Vodicka, P., 2000. Culture of bovine oocytes from small antral follicles in meiosis-inhibiting medium with butyrolactone I: RNA synthesis. Anim. Reprod. Sci. 64, 1-11.
86. Ponderato, N., Lagutina, I., Crotti, G., Turini, P., Galli, C., Lazzari, G., 2001. Bovine oocytes treated prior to in vitro maturation with a combination of butyrolactone I and roscovitine at low doses maintain a normal developmental capacity. Mol. Reprod. Dev. 60, 579-585.
87. Presl, J., Pospisil, J., Figarova, V., Krabec, Z., 1974. Stage-dependent changes in binding of iodinated FSH during ovarian follicle maturation in rats. Endocrinol. Exp. 8 (4), 291-298.
88. Rajokoski, E., 1960. The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical and left-right variations. Acta Endocrinol. 52, 1-68.
89. Ralph, J.H., Telfer, E.E., Wilmut, I., 1995. Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol. Reprod. Dev. 42, 248-253.
90. Richard, F.J., Sirard, M.A., 1996. Effects of follicular cells on oocyte maturation. II. Theca cell inhibition of bovine oocyte maturation in vitro. Biol. Reprod. 54, 22-28.
91. Rizos, D., Lonergan, P., Ward, F., Duffy, P., Boland, M.P., 2002. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234-248.
92. Russe, I., 1983. Oogenesis in cattle and sheep. Bibl. Anat. 24, 77-92.
93. Salustri, A., Yanagishita, M., Hascall, V.C., 1990. Mouse oocytes regulate hyaluronic acid synthesis and mucification by FSH-stimulated cumulus cells. Dev. Biol. 138, 26-32.
94. Savio, J.D., Keenan, L., Boland, M.P., Roche, J.F., 1988. Pattern of growth of dominant follicles during the oestrous cycle of heifers. J. Reprod. Fertil. 83, 663-671.
95. Simon, A.M., Goodenough, D.A., Li, E., Paul, D.L., 1997. Female infertility in mice lacking connexin 37. Nature 385, 525-529.
96. Sirard, M.A., Blondin, P., 1996. Oocyte maturation and IVF in cattle. Anim. Reprod. Sci. 42, 417-426.
97. Sirard, M.A., Richard, F., Mayes, M., 1998. Controlling meiotic resumption in bovine oocytes: a review. Theriogenology 49.
98. Sirard, M.A., 2001. Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241-1254.
99. Tanaka, Y., Nakada, K., Moriyoshi, M., Sawamukai, Y., 2001. Appearance and number of follicles and change in the concentration of serum FSH in female bovine fetuses. Reproduction 121, 777-782.
100. Tisdall, D.J., Watanabe, K., Hudson, N.L., Smith, P., McNatty, K.P., 1995. FSH receptor gene expression during ovarian follicle development in sheep. J. Mol. Endocrinol. 15, 273-281.
101. van de Leemput, E.E., Vos, P.L.A.M., Zeinstra, E.C., Bevers, M.M., van der Weijden, G.C., Dieleman, S.J., 1999. Improved in vitro embryo development using in vivo matured oocytes from heifers superiovulated with a controlled preovulatory LH surge. Theriogenology 52, 335-349.
102. Vanderhyden, B.C., Caron, P.J., Buccione, R., Eppig, J.J., 1990. Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307-317.
103. Vitt, U.A., Mazerbourg, S., Klein, C., Hsueh, A.J., 2002. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol. Reprod. 67, 473-480.
104. Vitt, U.A., McGee, E.A., Hayashi, M., Hsueh, A.J.W., 2000. In vivo treatment GDF-9 stimulates primordial and primary follicle progression and theca cell marker CyP17 in ovaries of immature rats. Endocrinology 141, 3814-3820.
105. Vozzi, C., Formenton, A., Chanson, A., Senn, A., Sahli, R., Shaw, P., Nicod, P., Germond, M., Haefliger, J.A., 2001. Involvement of connexin 43 in meiotic maturation of bovine oocytes. Reproduction 122, 619-628.
106. Wright, C., Becker, D.L., Lin, J.S., Warner, A.E.K.H., 2001. Stage-specific and differential expression of gap junctions in the mouse ovary: connexiu-specific roles in follicular regulation. Reproduction 121, 77-88.
107. Webb, R., Campbell, B.K., Garverick, H.A., Gong, J.G., Gutierrez, C.G., Armstrong, D.G., 1999. Molecular mechanisms regulating follicular recruitment and selection. J. Reprod. Fertil. 54 (Suppl.), 33-48.
108. Wolfsdorf, K.E., Diaz, T., Schmitt, E.J.P., Thatcher, M.J., Drost, M., Thatcher, W.W., 1997. The dominant follicle exerts an interovarian inhibition on FSH-induced follicular development. Theriogenology 48, 435-447.
109. Wood, S.C., Glencross, R.G., Bleach, E.C., Lovell, R., Beard, A.J., Knight, P.J., 1993. The ability of steroid - free bovine follicular fluid to suppress FSH secretion and delay ovulation persists in heifers actively immunized against inhibin. J. Endocrinol. 136, 137-148.
110. Xu, Z.Z., Garverick, H.A., Smith, G.W., Smith, M.F., Hamilton, S.A., Younquist, R.S., 1995. Expression of follicle stimulating hormone and luteinizing hormone receptor messenger fibonucleic acids in bovine follicles during the first follicular wave. Biol. Reprod. 53, 951-957.