An Overview of Major Genes Affecting Prolificacy in Sheep and Related Mechanisms
الموضوعات :
ام.ام. مستهافا
1
(National Institute of Animal Science and Veterinary Medicine, China Agricultural University, 2 West Yuanmingyuan Road, Beijing 100193,China)
اف.ام.ام.تی. ماریکار
2
(Department of Biochemistry, Faculty of Medicine and Allied Science, University of Rajarata, Saliyapura, Anuradhapura, Sri Lanka)
الکلمات المفتاحية: BMPs, follicular selection, mutated genes, ovulation rate, prolificacy,
ملخص المقالة :
The objective of this review is to explore the current developments on major genes working on prolific sheep breeds and the mechanism behind it, while identifying the future working points. Productivity is the ultimate goal of farm animal production and prolificacy is a key feature in determining productivity in farm animals. Ovulation rate in mammals is an intricate process involving genetics and endocrine pathways. Exceptional reproductive capabilities along with higher ovulation rates were observed in many breeds of sheep from different parts of the world since the discovery of Booroola Merino sheep. These naturally occurring mutations acting on prolificacy are found in chromosomes 5, 6, 11 and X but speculations are around about the presence of more mutations on these genes or different genes on multi ovulating sheep breeds. The exact control mechanism of multiple ovulations and multiple births in prolific sheep breeds is poorly understood. Over the years it has been repeatedly shown that gonadotropins and intra ovarian factors play vital and variety of roles. More specifically, follicular stimulating hormone regulation during folliculogenesis could be a promise for the future studies. Among those intra ovarian factors, bone morphogenic protein system is one of the indispensable components, which exerts enormous enthusiasm among the scientific community towards manipulating ovarian folliculogenesis. Rather surprisingly, biological and physiological roles of bone morphogenic protein subfamily are not thoroughly elucidated and contradictory findings among the mammals make further twists, which will be the gaps to be filled in the near future. Presence of a regulatory control loop between oocyte, granulosa and theca cells throughtransforming growth factor B(TGFB) superfamily is proposed here.
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.
Campbell B.K. (2009). The endocrine and local control of ovarian follicle development in the ewe. Anim. Reprod. Sci. 6, 159-171.
CampbellB.K. and McNeilly A.S. (1996). Follicular dominance and oocyte maturation. Zygote (Cambridge and England). 4, 327-334.
CampbellB.K., Scaramuzzi, R.J. and Webb R. (1996). Induction and maintenance of oestradiol and immunoreactive inhibin production with FSH by ovine granulosa cells cultured in serum-free media. J. Reprod. Fertil. 106, 7-16.
CampbellB.K., Souza C.J.H., Skinner A.J., Webb R. and Baird D.T. (2006). Enhanced response of granulosa and theca cells from sheep carriers of the FecB mutation in vitro to gonadotropins and bone morphogenic protein-2, -4, and -6. Endocrinology. 147, 1608-1620.
Chang H., Brown, C.W. and Matzuk M.M. (2002). Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocrinol. Rev. 23, 787-823.
Davis G.H. (2004). Fecundity genes in sheep. Anim. Reprod. Sci. 82, 247-253.
DavisG.H. (2005). Major genes affecting ovulation rate in sheep. Genet. Sel. Evol. 37, 11-23.
DavisG.H., Dodds K.G. and Bruce G.D. (1999). Combined effect of the Inverdale and Booroola prolificacy genes on ovulation rate in sheep. Proc. Assoc. Advmt. Anim. Breed. Genet. 13, 74-77.
DavisG.H., Dodds K.G., Wheeler R. and Jay N.P. (2001). Evidence that an imprinted gene on the X chromosome increases ovulation rate in sheep. Biol. Reprod. 64, 216-221.
DavisG.H., Galloway S.M., Ross I.K., Gregan S.M., Ward J., Nimbkar B.V., Ghalsasi P.M., Nimbkar C. and Gray G.D. (2002). DNA tests in prolific sheep from eight countries provide new evidence on origin of the Booroola (FecB) mutation. Biol. Reprod. 66, 1869-1874.
Davis G.H., McEwan J.C., Dodds K.G., Fennessy F. and Farquhar P.A. (1991). Evidance for the presence of a major gene influencing ovulation rate on the X chromosome. Biol. Reprod. 44, 620-624.
Deldar-Tajangookeh H., Shahneh A.Z., Zamiri M.J., Daliri M., Kohram H. and Nejati-Javaremi A. (2009). Study of BMP-15 gene polymorphism in Iranian goats. African J. Biotechnol. 8, 2929-2932.
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, 531-534.
Drouilhet L., Lecerf F., Bodin L., Fabre S. and Mulsant P. (2009). Fine mapping of the FecL locus influencing prolificacy in Lacaune sheep. Anim. Genet. 40, 804-812.
Drouilhet L., Taragnat C., Fontaine J., Duittoz A., Mulsant P., Bodin L. and Fabre S. (2010). Endocrine characterization of the reproductive axis in highly prolific lacaune sheep homozygous for the FecLL mutation. Biol. Reprod. 82, 815-824.
Edson M.A., Nagaraja A.K. and Matzuk M.M. (2009). The mammalian ovary from genesis to revelation. Endocrinol. Rev. 30, 624-712.
Elvin J.A., Yan C. and Matzuk M.M. (2000). Oocyte-expressed TGF-β superfamily members in female fertility. Mol. Cell. Endocrinol. 159, 1-5.
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.
FabreS., Pierre A., Mulsant P., Bodin L., Di Pasquale E., Persani L., Monget P. and Monniaux D. (2006). Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reprod. Biol. Endocrinol. 4, 20-25.
Findlay J.K. and Drummond A. (1999). Regulation of the FSH receptor in the ovary. Trend. Endocrinol. Metab. 10, 183-188.
Findlay J.K., Kerr J.B., Britt K., Liew S.H., Simpson E.R., Rosairo D. and Drummond A. (2009). Ovarian physiology: follicle development, oocyte and hormone relationships. Anim. Reprod. Sci. 6, 16-19.
Galloway S.M., McNatty K.P., Cambridge L.M., Laitinen M.P.E., Juengel J.L., Jokiranta T.S., McLaren R.J., Luiro K., Dodds K.G. and Montgomery G.W. (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.
Ghaderi A., Nasiri M.T.B., Mirzadeh K.H., Fayazi J. and Sadr A.S. (2010). Identification of the GDF9 mutation in two sheep breeds by using polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP ) technique. African J. Biotechnol. 9, 8020-8022.
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.
Hunter M.G., Robinson R.S., Mann G.E. and Webb R. (2004). Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim. Reprod. Sci. 82, 461-477.
Javanmard A., Azadzadeh N. and Esmailizadeh A.K. (2011). Mutations in bone morphogenetic protein 15 and growth differentiation factor 9 genes are associated with increased litter size in Fat-Tailed sheep breeds. Vet. Res. Commun. 35, 157-167.
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. (2004). Physiology of GDF9 and BMP15 signalling molecules. Anim. Reprod. Sci. 82, 447-460.
JuengelJ.L., Hudson N.L., Heath D.A., Smith P., Reader K.L., Lawrence S.B., O’Connell A.R., Laitinen M.P.E., Cranfield M. and Groome N.P. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777-1789.
JuengelJ.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.
JuengelJ.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 (Cambridge and England). 131, 501-513.
Knight P.G. and Glister C. (2001). Potential local regulatory functions of inhibins, activins and follistatin in the ovary. Reproduction (Cambridge and England). 121, 503-512.
Knight P.G. and Glister C. (2003). Local roles of TGF-β superfamily members in the control of ovarian follicle development. Anim. Reprod. Sci. 78, 165-183.
Knight P.G. and Glister C. (2006). TGF-β superfamily members and ovarian follicle development. Reproduction (Cambridge and England). 132, 191-206.
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 and differentiation factor-9. Implication of the aberrant ovarian phenotype of BMP-15 mutant sheep. J. Biol. Chem. 278, 3713-3719.
Lin S.J., Lerch T.F., Cook R.W., Jardetzky T.S. and Woodruff T.K. (2006). The structural basis of TGF-β, bone morphogenetic protein, and activin ligand binding. Reproduction (Cambridge and England). 132, 179-190.
Martinez-Royo A., Jurado J.J., Smulders J.P., Martí J.I., Alabart J.L., Roche A., Fantova E., Bodin L., Mulsant P. and Serrano M. (2008). A deletion in the bone morphogenetic protein 15 gene causes sterility and increased prolificacy in Rasa Aragonesa sheep. Anim. Genet. 39, 294-297.
McIntosh C.J., Lun S., Lawrence S., Western A.H., McNatty K.P. and Juengel J.L. (2008). The proregion of mouse BMP15 regulates the cooperative interactions of BMP15 and GDF9. Biol. Reprod. 79, 889-896.
McNatty K.P., Galloway S.M., Wilson T., Smith P., Hudson N.L., O’Connell A.R., Bibby A.H., Heath D.A., Davis G.H. and Hanrahan J.P. (2005a). Physiological effects of major genes affecting ovulation rate in sheep. Genet. Sel. Evol. 37,25-38.
McNattyK.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, 377-392.
McNattyK.P., Juengel J.L., Wilson T., Galloway S.M., Davis G.H., Hudson N.L., Moeller C.L., Cranfield M., Reader K.L. and Laitinen M.P.E. (2003). Oocyte-derived growth factors and ovulation rate in sheep. Reprod. Suppl. 61, 339-351.
McNattyK.P., Kieboom L.E., McDiarmid J., Heath D.A. and Lun S. (1986a). Adenosine cyclic 3’,5'-monophosphate and steroid production by small ovarian follicles from Booroola ewes with and without a fecundity gene.J. Reprod. Fertil. 76, 471-480.
McNattyK.P., Lun S., Heath D.A, Ball K., Smith P., Hudson N.L., McDiarmid J., Gibb M. and Henderson K.M. (1986b). Differences in ovarian activity between Booroola X Merino ewes which were homozygous, heterozygous and non-carriers of a major gene influencing their ovulation rate.J. Reprod. Fertil. 77, 193-205.
McNattyK.P., Smith P., Moore L.G., Reader K., Lun S., Hanrahan J.P., Groome N.P., Laitinen M.P.E., Ritvos O. and Juengel J.L. (2005b). Oocyte-expressed genes affecting ovulation rate. Mol. Cell. Endocrinol. 234, 57-66.
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.
Montgomery G.W., Galloway S.M., Davis G.H. and McNatty K.P. (2001). Genes controlling ovulation rate in sheep. Reproduction. 121, 843-852.
Mulsant P., Lecerf F., Fabre S., Schibler L., Monget P., Lanneluc I., Pisselet C., Riquet J., Monniaux D. and Callebaut I. (2001). Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Mérino ewes. Proc. Natl. Acad. Sci. USA. 98, 5104-5109.
Nassiry M.R., Tahmoorespour M., Javadmanesh A., Soltani M. and Far S.F. (2006). Calpastatin polymorphism and its association with daily gain in Kurdi sheep. Iranian J. Biotechnol. 4, 188-192.
Orisaka M., Tajima K., Tsang B.K. and Kotsuji F. (2009). Oocyte-granulosa-theca cell interactions during preantral follicular development. J. Ovarian Res. 2, 9-15.
Otsuka F., McTavish K.J. and Shimasaki S. (2011). Integral role of GDF-9 and BMP-15 in ovarian function. Mol. Reprod. Dev. 78, 9-21.
OtsukaF., Yamamoto S., Erickson G.F. and Shimasaki S. (2001). Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J. Biol. Chem. 276, 11387-11392.
OtsukaF., Yao Z., Lee T., Yamamoto S., Erickson G.F. and Shimasaki S. (2000). Bone morphogenetic protein-15.J. Biol. Chem. 275, 39523-39528.
Pangas S.A. and Matzuk M.M. (2004). Genetic models for transforming growth factor beta superfamily signaling in ovarian follicle development. Mol. Cell. Endocrinol. 225, 83-91.
Scaramuzzi R.J., Adams N.R., Baird D.T., Campbell B.K., Downing J.A., Findlay J.K., Henderson K.M., Martin G.B., McNatty K.P. and McNeilly A.S. (1993). A model for follicle selection and the determination of ovulation rate in the ewe. Reprod. Fertil. Dev. 5, 459-478.
Shimasaki S. (2006). BMP-15 regulation of ovulation quota in mammals.Reprod. Med. Biol. 5, 245-248.
ShimasakiS., Moore R.K., Otsuka F. and Erickson G.F. (2004). The none morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72-101.
ShimasakiS., Zachow R.J., Li D., Kim H., Iemura S., Ueno N., Sampath K., Chang R.J. and Erickson G.F. (1999). A functional bone morphogenetic protein system in the ovary. Proc. Natl. Acad. Sci. USA. 96, 7282-7287.
Souza C.J.H., Campbell B.K., McNeilly A.S. and Baird D.T. (2002). Effect of bone morphogenetic protein 2 (BMP2) on oestradiol and inhibin A production by sheep granulosa cells, and localization of BMP receptors in the ovary by immunohistochemistry. Reproduction (Cambridge and England). 123, 363-369.
SouzaC.J.H., González-Bulnes A., Campbell B.K., McNeilly A.S. and Baird D.T. (2004). Mechanisms of action of the principal prolific genes and their application to sheep production. Reprod. Fertil. Dev. 16, 395-401.
Trombly D.J., Woodruff T.K. and Mayo K.E. (2010). Roles for transforming growth factor β superfamily proteins in early folliculogenesis. Semin. Reprod. Med. 27, 14-23.
Vireque A.A., Reis R.M., Rosa e Silva A.A.M., Resende L.O.T., Ferreira E.M., Rosa e Silva A.C.J.S. and Ferriani R.A. (2008). Involvement of bone morphogenetic proteins (BMPs) in ovarian function and infertility. Open. Reprod. Sci. J. 1, 11-15.
Vitt U.A., Hayashi M., Klein C. and Hsueh A.J.W. (2000). Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol. Reprod. 62, 370-377.
Webb R., Garnsworthy P.C., Campbell B.K. and Hunter M.G. (2007). Intra-ovarian regulation of follicular development and oocyte competence in farm animals. Theriogenology. 68, 22-29.
WebbR., Garnsworthy P.C., Gong J. and Armstrong D.G. (2004). Control of follicular growth: local interactions and nutritional influences.J. Anim. Sci. 82, 63-74.
Wilson T., Wu X., Juengel J.L., Ross I.K., Lumsden J.M., Lord E.A., Dodds K.G., Walling G.A., McEwan J.C. and O’Connell A.R. (2001). Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK6) that is expressed in both oocytes and granulosa cells 1. Biol. Reprod. 64, 1225-1235.
Wu X., and Matzuk M.M. (2002). GDF9 and BMP15: oocyte organizers. Rev. Endocrinol. Metab. Disord. 3, 27-32.
Xu Y., Li E., Han Y., Chen L. and Xie Z. (2010). Differential expression of mRNAs encoding BMP / Smad pathway molecules in antral follicles of high- and low-fecundity Hu sheep. Anim. Reprod. Sci. 120, 47-55.
Young J.M., Juengel J.L., Dodds K.G., Laird M., Dearden P.K., McNeilly A.S., McNatty K.P. and Wilson T. (2008). The activin receptor-like kinase 6 Booroola mutation enhances suppressive effects of bone morphogenetic protein 2 (BMP2), BMP4, BMP6 and growth and differentiation factor-9 on FSH release from ovine primary pituitary cell cultures. J. Endocrinol. 196, 251-261.
