Bone Morphogenetic Protein (BMP15) Gene and its Relationship with Prolificacy in Sheep

(Review Paper)

  • Hassan Isahag Hassan Haren Department of Animal Production, Faculty of Agriculture, Omdurman Islamic University, Omdurman, Sudan
Keywords: BMP-15 gene, Relationship, Prolificacy, Sheep

Abstract

This review aims to study the Bone Morphogenetic Protein (BMP-15) gene and its association with ovulation rate and litter size in sheep. Fecundity traits such as ovulation rate and litter size are genetically regulated by many genes with small effects, and sometimes also by a single gene with major effects. BMP15 is essential for activation of the primordial follicle and subsequently in all stages of normal follicular development, maturation and ovulation. Mutations in the BMP-15 gene have been observed to be associated with increased ovulation rate and litter size in many sheep breeds worldwide.

References

Abdoli, R., Zamani, P., Mirhoseini, S., Ghavi Hossein-Zadeh, N., and Nadri, S (201). A review on prolificacy genes in sheep, Reproduction in Domestic Animals, 51, 631–637, 2016.

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.

Bodin L. Di, Pasquale E, Fabre S, (2007) A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. J Endocrinol 2007; 148:393–400.

Chu, M. X., Liu, Z. H., Jiao, C. L., He, Y. Q., Fang, L.,Ye, S. C., Chen, G. H. and Wang, J. Y. (2007) Mutations in BMPR-IB and BMP-15 genes are associated with litter size in Small Tailed Han sheep (Ovisaries). J. Anim. Sci. 85:598–603.

Crawford, J. L., Heath, D.A., Reader, K.L., Quirke, L. D., Hudson, N.L. and Juengel, J.L. and McNatty, K.P. (2011) Oocytes in sheep homozygous for a mutation in bone morphogenetic protein receptor 1B express lower mRNA levels of bone morphogenetic protein 15 but not growth differentiation factor 9. Reproduction. 142: 53–61.

Davis GH, Dodds KG, Bruce GD. (1999).Combined effect of the Inverdale and Booroola prolificacy genes on ovulation rate in sheep. Proc AssocAdvmtAnim Breed Genet. 13:74–77.

Davis GH, Bruce GD, Dodds KG.(2001).Ovulation rate and litter size of prolific Inverdale (FecXI) and Hanna (FecXH) sheep.Proc Assoc Adv Anim Breed Genet 2001, 13:74-77.

Davis GH (2004).Fecundity genes in sheep. Anim.Reprod. Sci. 8283:247-253.

Davis GH, Balakrishnan L, Ross IK, Wilson T, Galloway SM, Lumsden BM, Hanrahan JP, Mullen M, Mao XZ, Wang GL, Zhao ZS, Zeng YQ, Robinson JJ, Mavrogenis AP, Papachristoforou C, Peter C, Baumung R, Cardyn P, Boujenane I, Cockett NE, Ey-thorsdottir E, Arranz JJ, Notter D (2006). Investigation of the Booroola (FecB) and Inverdale (FecXI) mutations in 21 prolific breeds and strains of sheep sampled in 13 countries.Anim. Reprod. Sci. 92:87-96.

Davis, G.H. (2005). Major genes affecting ovulation rate in sheep. Genetics Selection Evolution, vol. 37, ss.11–23.

Demars, J., Fabre, S., Sarry, J., Rossetti, R., Gilbert, H., Persani, L., Tosser-Klopp, G., Mulsant, P., Nowak, Z., Drobik, W., Martyniuk, E. and Bodin, L. (2013) Genome Wide Association Studies Identify Two Novel BMP15 Mutations Responsible for an Atypical Hyperprolificacy Phenotype in Sheep. 9:4.

Di Pasquale, E., Beck-Peccoz, P., and Persani, L. (2004). Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene, Am. J. Hum. Genet., 75, 106–111.

Dixit, H., Rao, L., Padmalatha, V., Kanakavalli, M., Deenadayal, M., Gupta, N., Chakrabarty, B. and Singh, L. (2006). Missense mutations in the BMP15 gene are associated with ovarian failure. Human Genetics 119(4): 408-415.

Drouilhet, L., Lecerf, F., Bodin, L., Fabre, S., Mulsant, P. (2009). Fine mapping of the FecL locus influencing prolificacy in Lacaunesheep.Animal Genetics, doi:10.1111/j.1365-2052.2009.01919.x.

Drouilhet, L., Mansanet, C., Sarry, J., Tabet, K., Bardou, P.,Woloszyn, F., Lluch, J., Harichaux, G., Viguie´, C., Monniaux, D., Bodin, L., Mulsant, P., Fabre, S. (2013). The Highly Prolific Phenotype of Lacaune Sheep Is Associated with an Ectopic Expression of the B4GALNT2 Gene within the Ovary. PLoS Genetics, vol. 9(9): e1003809.

Dube, J. L., Wang, P., Elvin, J., Lyons, K. M., Celeste, A. J. and Matzuk, M. M. (1998). The Bone Morphogenetic Protein 15 Gene Is X-Linked and Expressed in Oocytes. Molecular Endocrinology 12(12): 1809-1817.

Duguma, G., Cloete, S.W.P., Schoeman, S.J., Jordaan, G.F., (2002). Genetic parameters of testicular measurements in Merino rams and the influence of scrotal circumference on total flock fertility. S. Afr. J. Anim. Sci. 32, 76-82.

Eppig, J.J., (2001). Oocyte control of ovarian follicular development and function in mammals.Reproduction. 122, 829-838.

Feary, E.S., Juengel, J.L., Smith, P., French, M.C., O'Connell, A.R., Lawrence, S.B., Galloway, S.M., Davis, G.H and McNatty, K.P. (2007) Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B, and BMPR2 during follicular development and characterization of ovarian follicular populations in ewe carrying the Woodlands FecX2W mutation. Biol. Reprod. 77 (6): 990–998.

Fogarty, N. M. (2009). A review of the effects of the Booroola gene (FecB) on sheep production. Small Ruminant Research, vol. 85, ss. 75-84.

Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P.E., Juengel, J.L., Jokiranta, S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W., Beattie, A.E., Davis, G.H. &Ritvos, O., (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.

Hanrahan JP, Gregan SM, Mulsant P, (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 (Ovisaries). BiolReprod 2004; 70:900–909.

Iagaki, K. and Shimasaki, S.(2010). Impaired production of BMP-15 and GDF-9 mature proteins derived from proproteins with mutations in the proregion, Mol. Cell. Endocrinol., 328, 1–7.

Juengel JL, Sawyer HR, Smith PR, Quirke LD, Heath DA, Lun S, Wakefield SJ, McNatty KP. (2002). Origins of follicular cells and ontogeny of steroidogenesis in ovine fetal ovaries. Mol Cell Endocrinol 191:1-10

Laitinen, M., Vuojolainen, K., Jaatinen, R., Ketola, I., Aaltonen, J., Lehtonen, E., Heikinheimo, M. and Ritvos, O. (1998). A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mechanisms of Development 78(1-2): 135-140.

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.

Mandon-Pepin B, Oustry-Vaiman A, Vigier B, Piumi F, Cribiu E, Cotinot C, (2003). xpression profiles and chromosomal localization of genes controlling meiosis and follicular development in the sheep ovary. BiolReprod 2003, 68:E985-995.

McNatty, K. P., Juengel, J. L., Reader, K. L., Lun, S., Myllymaa, S., Lawrence, S. B., Western, A., Meerasahib, M. F., Mottershead, D. G., Groome, N. P., Ritvos, O. and Laitinen, M. P. E. (2005a). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129(4): 473-480.

Monteagudo LV, Ponz R, Tejedor MT, Lavina A, Sierra I (2009) A 17 bp deletion in the Bone Morphogenetic Protein 15 (BMP15) gene is associated to increased prolificacy in the Rasa Aragonesa sheep breed. AnimReprodSci 110:139–146.

Montgomery, G. W., Galloway, S. M., Davis, G. H., McNatty, K. P. (2001). Genes controlling ovulation rate in sheep. Reproduction, vol. 121, ss. 843-852.

Olivier, W.J., Snyman, M.A., Olivier, J.J., Van Wyk, J.B., Erasmus, G.J., (2001). Direct and correlated responses to selection for total weight of lamb weaned in Merino sheep. S. Afr. J. Anim. Sci. 31, 115-121.

Otsuka, F. and Shimasaki, S. (2002). A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: Its role in regulating granulosa cell mitosis. Proceedings of the National Academy of Sciences of the United States of America 99(12): 8060-8065.

Pramod KR, Sharma SK, Kumar R, Rajan A (2013). Genetics of ovulation rate in farm animals. Vet. World 6(11):833-838.

Saito S, Yano K, Sharma S, Mcmahon HE, Shimasaki S (2008). Characterization of the post-translational modification of recombinant human BMP-15 mature protein. Protein Sci 2008;17:362–370.

SanCristobal-Gaudy, M., Bodin, L., Elsen, J-M., Chevalet, C. (2001). Genetic components of litter size variability in sheep. Genetics Selection Evolution, vol. 33, ss. 249-271.

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.

Souza, C. J., MacDougall, C., Campbell, B. K., McNeilly, A.S., Baird, D. T. (2001). The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. Journal of Endocrinology, vol. 169, ss. R1–6.

Sun, R.Z., Lei, L., Cheng, L., Jin, Z.F., Zu, S.J., Shan, Z.Y., Wang, Z.D., Zhang, J.X. and Liu, Z.H. (2010). Expression of GDF-9, BMP-15 and their receptors in mammalian ovary follicles. J. Mol. Histol. 41: 325–332.

Våge, D. I., Husdal, M., Kent, M. P., Klemetsdal, G. and Boman, I. A. (2013) A missense mutation in growth differentiation factor 9 (GDF9) is strongly associated with litter size in sheep. BMC Genet. 14 (1): 1.

Wang, Weimin., Shijia Liu., Fadi Li., Xiangyu Pan., Chong Li., Xiaoxue Zhang., Youji Ma., Yongfu La., Rui Xi., and Tingfu Li. (2015). Polymorphisms of the Ovine BMPR-IB, BMP-15 and FSHR and Their Associations with Litter Size in Two Chinese Indigenous Sheep Breeds. Int. J. Mol. Sci. 2015, 16, 11385-11397; doi:10.3390/ijms160511385.

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.

Zhang, R.; Zhang, S.; Zhu, X.; Zhou, Y.; Wu, X. (2015).Follicle-stimulating hormone receptor (FSHR) in Chinese alligator, Alligator sinensis: Molecular characterization, tissue distribution and mRNA expression changes during the female reproductive cycle. Anim. Reprod. Sci. 2015, 156, 40–50.

Published
2022-10-30