Meat and Livestock Association plenary lecture 2005 oocyte signalling molecules and their effects on reproduction in ruminants

Reproduction, Fertility and Development

Volumn 18, Issue 4, 2006, Pages 403-412

  McNatty, Kenneth P ^a,c   Lawrence, Stephen ^a   Groome, Nigel P ^b   Meerasahib, Mohammed F ^b   Hudson, Norma L ^a   Whiting, Lynda ^a   Heath, Derek A ^a   Juengel, Jennifer L ^a  

^a AGRESEARCH   (New Zealand)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

^c VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Activin like kinase 6; Bone morphogenetic protein 15; Growth differentiation factor 9; Ovary; Ovulation rate

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; GROWTH DIFFERENTIATION FACTOR 9; GROWTH FACTOR; THYMIDINE; TRITIUM;

BOVIDS; BREED; CATTLE; DRUG FORMULATION; FEMALE STERILITY; GENE EXPRESSION; GRANULOSA CELL; HETEROZYGOSITY; IMMUNIZATION; IN VITRO STUDY; LIVESTOCK; MEAT; MOUSE STRAIN; NONHUMAN; ONTOGENY; OOCYTE; OVARY; OVARY FOLLICLE; OVARY FOLLICLE CELL; OVULATION; POINT MUTATION; RAT STRAIN; REPRODUCTION; REVIEW; SHEEP; WILD TYPE;

ANIMALS; CATTLE; FEMALE; GONADOTROPINS, PITUITARY; IMMUNIZATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; OOCYTES; OVARIAN FOLLICLE; POINT MUTATION; REPRODUCTION; RUMINANTS; SHEEP; SIGNAL TRANSDUCTION;

ANIMALIA; BOS TAURUS; BOVIDAE; BOVINAE; MAMMALIA; OVIS; OVIS ARIES; RODENTIA;

EID: 33645569168     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD05104     Document Type: Review

References (61)

1. Anderson, L. L. (1977). Development in calves and heifers after hypophysical stalk transection or hypophysectomy. Am. J. Physiol. 232, E497-E503.
2. Baird, D. T., and McNeilly, A. S. (1981). Gonadotrophin control of follicular development and function during the oestrous cycle of the ewe. J. Reprod. Fertil. Suppl. 30, 119-133.
3. Bodensteiner, K. J., Clay, C. M., Moeller, C. L., and 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, 381-386. doi:10.1095/BIOLREPROD60.2.381
4. Bodin, L., Lecerf, F., Pisselet, C., San Cristhal, M., Bibe, M., and Mulsant, P. (2003). How many mutations are associated with increased ovulation rate and little size in progeny of Lacaune meat sheep. In 'Proceedings of the International Workshop on Major Genes and QTL in Sheep and Goats'. (Ed. L. Bodin.) pp. 2-11. (Institut National De La Recherche Agronomique: Toulouse, France.)
5. Braw-Tal, R., and 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.
6. I) are devoid of secondary and tertiary follicles but contain many abnormal structures. Biol. Reprod. 49, 895-907. doi:10.1095/BIOLREPROD49.5.895
7. Chang, H., Brown, C. W., and Matzuk, M. M. (2002). Genetic analysis of the mammalian transforming growth factor-β superfamily. Endocr. Rev. 23, 787-823. doi:10.1210/ER.2002-0003
8. Davis, G. H., Dodds, K. G., and Bruce, G. D. (1999). Combined effect of the Inverdale and Booroola prolificacy genes on ovulation rates. Proc. Adv. Anim. Breed. Genet. 13, 74-77.
9. H) sheep. Proc. Assoc. Adv. Anim. Breed. Genet. 14, 175-178.
10. Di Pasquale, E., Beck-Peccoz, P., and Persani, E. (2004). Hyper-gonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am. J. Hum. Genet. 75, 106-111. doi:10.1086/422103
11. Dong, J., Albertini, D. F., Nishimori, K., Kumar, T. R., Lu, N., and Matzuk, M. M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531-535. doi:10.1038/383531A0
12. Fabre, S., Pierre, A., Pisselet, C., Mulsant, P., Lecerf, F., Pohl, J., Monget, P., and Monniaux, D. (2003). The Booroola mutation in sheep is associated with an alteration of the bone morphogenetic protein receptor-IB functionality. J. Endocrinol. 177, 435-444. doi:10.1677/JOE.0.1770435
13. Galloway, S. M., McNatty, K. P., Cambridge, L. M., Laitinen, M. P. E., Juengel, J. L., et al. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279-283. doi:10.1038/77033
14. Glister, C., Kemp, C. F., and Knight, P. G. (2004). Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian cells: action of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 by phosphorylation by follistatin. Reproduction 127, 239-254. doi:10.1530/REP1. 00090
15. Gougeon, A., and Chainy, G. B. N. (1987). Morphometric studies of small follicles in ovaries of women at different ages. J. Reprod. Fertil. 81, 433-442.
16. Govan, A. D. T. (1968). The human ovary during early pregnancy. J. Endocrinol. 40, 421-428.
17. Hanrahan, J. P., Gregan, S. M., Mulsant, P., Mullen, M., Davis, G. H., Powell, R., and Galloway, S. M. (2004). Mutations in the genes for oocyte derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 70, 900-909. doi:10.1095/BIOLREPROD.103.023093
18. Hashimoto, O., Moore, R. K., and Shimasaki, S. (2005). Posttranslational processing of mouse and human BMP15: potential implication in the determination of ovulation quota. Proc. Natl Acad. Sci. USA 102, 5426-5431. doi:10.1073/PNAS.0409533102
19. Henderson, K. M., McNatty, K. P., O'Keefe, L. E., Lun, S., Heath, D. A., and Prisk, M. D. (1987). Differences in gonadotrophin-stimulated cyclic AMP production by granulosa cells from Booroola x Merino ewes which were homozygous, heterozygous or non-carriers of a fecundity gene influencing their ovulation rate. J. Reprod. Fertil. 81, 395-402.
20. 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
21. Juengel, J. L., and McNatty, K. P. (2005). The role of proteins of the transforming growth factor-β superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 11, 143-160.
22. Juengel, J. L., Quirke, L. D., Tisdall, D. J., Smith, P., Hudson, N. L., and McNatty, K. P. (2000). Gene expression in abnormal ovarian structures of ewes homozygous for the Inverdale prolificacy gene. Biol. Reprod. 62, 1467-1478. doi:10.1095/BIOLREPROD62.6.1467
23. Juengel, J. L., Hudson, N. L., Heath, D. A., Smith, P., Reader, K. L., et al. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777-1789. doi:10.1095/BIOLREPROD.102.007146
24. Juengel, J. L., Hudson, N. L., Whiting, L., and McNatty, K. P. (2004a). Effects of immunization against bone morphogenetic protein 15 and growth differentiation factor 9 on ovulation rate, fertilization and pregnancy in ewes. Biol. Reprod. 70, 557-561. doi:10.1095/BIOLREPROD.103.023333
25. Juengel, J. L., Bodensteiner, K. J., Heath, D. A., Hudson, N. L., Moeller, C. L., Smith, P., Galloway, S. M., Davis, G. H., Sawyer, H. R., and McNatty, K. P. (2004b). Physiology of GDF9 and BMP15 signalling molecules. Anim. Reprod. Sci. 82-83, 447-460. doi:10.1016/J.ANIREPROSCI.2004.04.021
26. Juengel, J. L., Bibby, A. H., Reader, K. L., Lun, S., Quirke, L. D., Haydon, L. J., and McNatty, K. P. (2004c). The role of transforming growth factor-β (TGF-β) during ovarian follicular development in sheep. Reprod. Biol. Endocrinol. 2, 78. doi:10.1186/1477-7827-2-78
27. Juengel, J. L., Reader, K. L., Bibby, A. H., Lun, S., Ross, I., Haydon, L. J., and McNatty, K. P. (2006). The role of bone morphogenetic proteins 2, 4, 6 and 7 during ovarian follicular development in sheep: contrast to rat. Reproduction 131, 501-513. doi:10.1530/REP.1.00958
28. Kaivo-Oja, N., Bondestam, J., Kamarainen, M., Koskimies, J., Vitt, U., et al. (2003). Growth differentiation factor-9 induces Smad2 activation and inhibin B production in cultured human granulosaluteal cells. J. Clin. Endocrinol. Metab. 88, 755-762. doi:10.1210/JC.2002-021317
29. Kumar, T. R., Wang, Y., Lu, N., and Matzuk, M. M. (1997). Follicle stimulating hormone is required for ovarian follicle maturation but not for male fertility. Nat. Genet. 15, 201-204. doi:10.1038/NG0297-201
30. Liao, W. X., Moore, R. K., Otsuka, F., and Shimasaki, S. (2003). Effect of intracellular interactions on the processing and secretion of bone morphogenetic protein-15 (BMP-15) and growth differentiation factor-9. Implication of the aberrant ovarian phenotype of BMP-15 mutant sheep. J. Biol. Chem. 278, 3713-3719. doi:10.1074/JBC.M210598200
31. Lundy, T., Smith, P., O'Connell, A., Hudson, N. L., and McNatty, K. P. (1999). Populations of granulosa cells in small follicles of the sheep ovary. J. Reprod. Fertil. 115, 251-262.
32. Matthews, C. H., Borgato, S., Beck-Peccoz, O., Adams, M., Tone, Y., Gambino, G., Casagrande, S., Tedeschini, G., Benedetti, A., and Chatterjee, V. K. K. (1993). Primary amenorrhoea and infertility due to a mutation in the β-subunit of follicle-stimulating hormone. Nat. Genet. 5, 83-86. doi:10.1038/NG0993-83
33. Matzuk, M. M., Burns, K. H., Viveros, M. M., and Eppig, J. J. (2002). Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178-2180. doi:10.1126/SCIENCE.1071965
34. Mazerbourg, S., Klein, C., Roh, J., Kaivo-Oja, N., Mottershead, D. G., Korchynskyi, O., Ritvos, O., and Hsueh, A. J. (2004). Growth differentiation factor-9 signalling is mediated by the type 1 receptor activin-like kinase 5. Mol. Endocrinol. 18, 653-665. doi:10.1210/ME.2003-0393
35. McNatty, K. P. (1982). Ovarian follicular development from the onset of luteal regression in humans and sheep. In 'Follicular Maturation and Ovulation'. (Eds R. Rolland, E. V. van Hall, S. G. Hillier, K. P. McNatty and J. Schoemaker.) pp. 1-18. (Excerpta Medica: Amsterdam, the Netherlands.)
36. McNatty, K. P., Hillier, S. G., van den Boogaard, A. M. J., Trimbos-Kemper, T. C. M., Reichert, L. E., and van Hall, E. V. (1983). Follicular development during the luteal phase of the human menstrual cycle. J. Clin. Endocrinol. Metab. 56, 1022-1031.
37. McNatty, K. P., Heath, D. A., Lun, S., Fannin, J. M., McDiarmid, J. M., and Henderson, K. M. (1984). Steroidogenesis by bovine theca interna in an in vitro perifusion system. Biol. Reprod. 30, 159-170. doi:10.1095/BIOLREPROD30.1. 159
38. McNatty, K. P., Lun, S., Heath, D. A., Ball, K., Smith, P., Hudson, N. L., McDiarmid, J., Gibb, M., and Henderson, K. M. (1986). Differences in ovarian activity between Booroola x Merino ewes which were homozygous, heterozygous or non-carriers of a major gene(s) influencing their ovulation rate. J. Reprod. Fertil. 86, 27-38.
39. McNatty, K. P., Heath, D. A., Hudson, N. and Clarke, I. J. (1990). Effect of long-term hypophysectomy on ovarian follicle populations and gonadotrophin-induced adenosine cyclic 3′,5′-monophosphate output from follicles from Booroola ewes with or without the F gene. J. Reprod. Fertil. 90, 515-522.
40. McNatty, K. P., Heath, D. A., Lundy, T., Fidler, A. E., Quirke, L., O'Connell, A., Smith, P., Groome, N., and Tisdall, D. J. (1999). Control of early ovarian follicular development. J. Reprod. Fertil. Suppl. 54, 3-16.
41. McNatty, K. P., Juengel, J. L., Wilson, T., Galloway, S. M., and Davis, G. H. (2001). Genetic mutations influencing ovulation rate in sheep. Reprod. Fertil. Dev. 13, 549-555. doi:10.1071/RD01078
42. McNatty, K. P., Juengel, J. L., Wilson, T., Galloway, S. M., Davis, G. H., et al. (2003). Oocyte-derived growth factors and ovulation rate in sheep. Reprod. Suppl. 61, 339-351.
43. McNatty, K. P., Smith, P., Moore, L. G., Reader, K., Lun, S., Hanrahan, J. P., Groome, N. P., Laitinen, M., Ritvos, O., and Juengel, J. L. (2005a). Oocyte-expressed genes affecting ovulation rate. Mol. Cell. Endocrinol. 234, 57-66. doi:10.1016/J.MCE.2004.08.013
44. McNatty, K. P., Juengel, J. L., Reader, K. L., Lun, S., Myllymaa, S., et al. (2005b). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129, 473-480. doi:10.1530/REP.1.0511
45. McNatty, K. P., Juengel, J. L., Reader, K. L., Lun, S., Myllymaa, S., et al. (2005c). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 129, 481-487. doi:10.1530/REP.1.00517
46. Monget, P., Fabre, S., Mulsant, P., Lecerf, F., Elsen, J. M., Mazerbourg, S., Pisselet, C., and Monniaux, D. (2002). Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. Domest. Anim. Endocrinol. 23, 139-154. doi:10.1016/S0739-7240(02)00152-2
47. Montgomery, G. W., Galloway, S. M., Davis, G. H., and McNatty, K. P. (2001). Genes controlling ovulation rate in sheep. Reproduction 121, 843-852. doi:10.1530/REP.0.1210843
48. Moore, R. K., Otsuka, F., and Shimasaki, S. (2003). Molecular basis of bone morphogenetic protein-15 signalling in granulosa cells. J. Biol. Chem. 278, 304-310. doi:10.1074/JBC.M207362200
49. Moore, R. K., Erickson, G. F., and Shimasaki, S. (2004). Are BMP-15 and GDF-9 primary determinants of ovulation quota in mammals? Trends Endocrinol. Metab. 15, 356-361. doi:10.1016/J.TEM.2004.08.008
50. Nohe, A., Keating, E., Knaus, P., and Petersen, N. O. (2004). Signal transduction of bone morphogenetic protein receptors. Cell. Signal. 16, 291-299. doi:10.1016/J.CELLSIG.2003.08.011
51. Otsuka, F., Moore, R. K., Wang, X., Sharma, S., Miyoshi, T., and Shimasaki, S. (2005). Essential role of the oocyte in estrogen amplication of follicle-stimulating hormone signalling in granulosa cells. Endocrinology 146, 3362-3367. doi:10.1210/EN.2005-0349
52. Roh, J. S., Bondestam, J., Mazerbourg, S., Kaivo-Oja, Groome, N. P., Ritvos, O., and Hsueh, A. J. (2003). Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 144, 172-178. doi:10.1210/EN.2002-220618
53. I) on the X chromosome that influences ovulation rate. Biol. Reprod. 48, 1150-1156. doi:10.1095/BIOLREPROD48.5.1150
54. Shimasaki, S., Moore, R. K., Otsuka, F., and Erickson, G. F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72-101. doi:10.1210/ER.2003-0007
55. Smith, P., Braw-Tal, R., Corrigan, K., Hudson, N. L., Heath, D. A., and McNatty, K. P. (1994). Ontogeny of ovarian follicle development in Booroola sheep fetuses that are homozygous carriers or non-carriers of the FecB gene. J. Reprod. Fertil. 100, 485-490.
56. Smith, P., O, W.-S., Corrigan, K. A., Lundy, T., Davis, G. H., and McNatty, K. P. (1997). Ovarian morphology and endocrine characteristics of female sheep fetuses that are heterozygous or homozygous for the Inverdale prolificacy gene (FecXI). Biol. Reprod. 57, 1183-1192. doi:10.1095/BIOLREPROD57. 5.1183
57. Vitt, U. A., Mazerbourg, S., Klein, C., and Hsueh, A. J. (2002). Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol. Reprod. 67, 473-480. doi:10.1095/BIOLREPROD67.2.473
58. Wilson, T., Wu, X. Y., Juengel, J. L., Ross, I. K., Lumsden, J. M., et al. (2001). Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod. 64, 1225-1235. doi:10.1095/BIOLREPROD64.4.1225
59. Xia, Y., Sidis, Y., Mukherjee, A., Samad, T. A., Brenner, G., Woolf, C. J., Lin, H. Y., and Schneyer, A. (2005). Location and action of Dragon (RGMb), a novel BMP co-receptor throughout the reproductive axis. Endocrinology 146, 3614-3621.
60. Yan, C., Wang, P., De Mayo, J., DeMayo, F. J., Elvin, J. A., et al. (2001). Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15, 854-866. doi:10.1210/ME.15.6.854
61. Zeleznik, A. J., and Kubik, C. J. (1986). Ovarian responses in macaques to pulsatile infusion of follicle-stimulating hormone and luteinising hormone: increased sensitivity of the maturing follicle to FSH. Endocrinology 119, 2025-2032.