Genetic variability in equine GDF9 and BMP15 genes in Arabian and Thoroughbred mares

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., Rit- vos O. (1999). Human growth differentiation factor 9 (GDF9) and its novel homolog GDF9Bare expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab., 84: 2744-2750.Search in Google Scholar

Albertini D.F., Combelles C.M., Benecchi E., Carabatsos M.J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction, 121: 647-653.Search in Google Scholar

Alves K.A., Alves B.G., Gastal G.D.A.,de Tarso S.G.S., Gastal M.O., Figueire - do J.R., Gambarini M.L., Gastal E.L. (2016). The mare model to study the effects of ovarian dynamics on preantral follicle features. PLo S ONE, 11(2): e0149693. doi:10.1371/journal. pone.0149693Search in Google Scholar

Barrett J.C., Fry B., Maller J., Daly M.J. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics, 21: 263-265.10.1093/bioinformatics/bth45715297300Open DOISearch in Google Scholar

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: 381-386.10.1095/biolreprod60.2.3819916005Open DOISearch in Google Scholar

Bodensteiner K.J., Mc Natty K.P., Clay C.M., Moeller C.L., Sawyer H.R. (2000). Expression of growth and differentiation factor-9 in the ovaries of fetal sheep homozygous or heterozygous for the inverdale prolificacy gene (Fec X(I)). Biol. Reprod., 62: 1479-1485.10.1095/biolreprod62.6.147910819747Open DOISearch in Google Scholar

Bresińska A., Wachowska L., Szwaczkowski T. (2004). Genetic and environmental effects on twin pregnancy and length of reproduction in Thoroughbred mares. Arch. Tierzucht., 47: 119-127.Search in Google Scholar

Campos-Chillon F., Farmerie T.A., Bouma G.J., Clay C.M., Carnevale E.M. (2015). Effects of aging on gene expression and mitochondrial DNAin the equine oocyte and follicle cells. Reprod. Fertil. Dev., 27: 925-933.Search in Google Scholar

Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., Frisch M., Bayerlein M., Werner T. (2005). Mat Inspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics, 21: 2933-2942.10.1093/bioinformatics/bti47315860560Open DOISearch in Google Scholar

Castro F.C. de, Cruz M.H., Leal C.L. (2015). Role of growth differentiation factor 9 and bone morphogenetic protein 15 in ovarian function and their importance in mammalian female fertility - a review. Asian-Australas. J. Anim. Sci., 29: 1065-1074.Search in Google Scholar

Chowdhary B.P. (2013). Equine genomics. Texas A&M University College Station, Texas, USA, 202 pp.10.1002/9781118522158Search in Google Scholar

Coutinhoda Silva M.A. (2008). When shouldamare go for assisted reproduction? Theriogenology, 70: 441-444.10.1016/j.theriogenology.2008.05.03918534673Open DOISearch in Google Scholar

Crawford J.L., Mc Natty K.P. (2012). The ratio of growth differentiation factor 9: bone morphogenetic protein 15 m RNAexpression is tightly co-regulated and differs between species overawide range of ovulation rates. Mol. Cell Endocrinol., 348: 339-343.Search in Google Scholar

Di Pasquale E., Beck- Peccoz P., 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.Search in Google Scholar

Di Pasquale E., Rossetti R., Marozzi A., Bodega B., Borgato S., Cavallo L., Ei- naudi S., Radetti G., Russo G., Sacco M., Wasniewska M., Cole T. (2006). Identification of new variants of human BMP15 gene inalarge cohort of women with premature ovarian failure. J. Clin. Endocrinol. Metab., 91: 1976-1979.10.1210/jc.2005-265016464940Open DOISearch in Google Scholar

Dixit H., Rao L.K., Padmalatha V., Kanakavalli M., Deenadayal M., Gupta N., Chakravarty B., Singh L. (2005). Mutational screening of the coding region of growth differentiation factor 9 gene in Indian women with ovarian failure. Menopause, 12: 749-754.10.1097/01.gme.0000184424.96437.7a16278619Open DOISearch in Google Scholar

Eickbush T.H., Malik H.S. (2002). Origins and evolution of retrotransposons. In: Mobile DNA II, Craig N.L., Craigie R., Gellert M., Lambowitz A.M. (eds). ASM Press, Washington DC, pp. 1111-1144.10.1128/9781555817954.ch49Search in Google Scholar

Erickson G.F., Shimasaki S. (2003). The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod. Biol. Endocrinol., 1: 9.Search in Google Scholar

Fabre S., Pierre A., Mulsant P., Bodin L., Di Pasquale E., Persani L., Monget P., Monniaux D. (2006). Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reprod. Biol. Endocrinol., 4: 20.Search in Google Scholar

Gilchrist R.B., Lane M., Thompson J.G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update., 14: 159-177.10.1093/humupd/dmm040Open DOISearch in Google Scholar

Ginther O.J. (1982). Twinning in mares:areview of recent studies. J. Equine. Vet. Sci., 2: 127-135.10.1016/S0737-0806(82)80005-1Open DOISearch in Google Scholar

Ginther O.J., Bergfelt D.R. (1992). Associations between FSHconcentrations and major and minor follicular waves in pregnant mares. Theriogenology, 38: 807-821.10.1016/0093-691X(92)90157-MOpen DOISearch in Google Scholar

Haag K.T., Magalhães-Padilha D.M., Fonseca G.R., Wischral A., Gastal M.O., King S.S., Jones K.L., Figueiredo J.R., Gastal E.L. (2013 a). Equine preantral follicles obtained via the Biopsy Pick-Up method: histological evaluation and validation ofamechanical isolation technique. Theriogenology, 79: 735-743.10.1016/j.theriogenology.2012.10.02323352704Open DOISearch in Google Scholar

Haag K.T., Magalhães-Padilha D.M., Gastal M.O., Figueiredo J.R., Gastal E.L. (2013 b). Equine preantral follicle harvesting processing and in vitro culture: the journey has already started. Anim. Reprod., 10: 187-198.Search in Google Scholar

Han H., Lei Q., Zhou Y., Gao J., Liu W., Li F., Zhang Q., Lu Y., Cao D. (2015). Association between BMP15 gene polymorphism and reproduction traits and its tissues expression characteristics in chicken. PLo S One., 10 e0143298.10.1371/journal.pone.0143298464849826574748Search in Google Scholar

Han J.S. (2010). Non-long terminal repeat (non-LTR) retrotransposons: mechanisms, recent developments and unanswered questions. Mob. DNA, 1: 15. Search in Google Scholar

Hanrahan J.P., Gregan S.M., Mulsant P., Mullen M., Davis G.H., Powell R., Gal- loway 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: 900-909.10.1095/biolreprod.103.02309314627550Open DOISearch in Google Scholar

Hill E.W., Gu J., Eivers S.S., Fonseca R.G., Mc Givney B.A., Govindarajan P., Orr N., Katz L.M., Mac Hugh D.E. (2010). Asequence polymorphism in MSTNpredicts sprinting ability and racing stamina in thoroughbred horses. PLo S One, 5: e8645.Search in Google Scholar

Hosoe M., Kaneyama K., Ushizawa K., Hayashi K.G., Takahashi T. (2011). Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod. Biol. Endocrinol., 9: 33.Search in Google Scholar

Jurka J., Kapitonov V.V., Pavlicek A., Klonowski P., Kohany O., Walichie - wicz J. (2005). Repbase Update:adatabase of eukaryotic repetitive elements. Cytogenet. Genome. Res., 110: 462-467.Search in Google Scholar

Kohany O., Gentles A.J., Hankus L., Jurka J. (2006). Annotation, submission and screening of repetitive elements in Repbase: Repbase Submitter and Censor. BMC Bioinformatics, 25: 7-474.10.1186/1471-2105-7-474163475817064419Open DOISearch in Google Scholar

Laissue P., Christin-Maitre S., Touraine P., Kuttenn F., Ritvos O., Aittoma- ki K., Bourcigaux N., Jacquesson L., Bouchard P., Frydman R., Dewailly D., Reyss A.C. (2006). Mutations and sequence variants in GDF9 and BMP15 in patients with premature ovarian failure. Eur. J. Endocrinol., 154: 739-744.Search in Google Scholar

Lin Z.L., Li Y.H., Xu Y.N., Wang Q.L., Namgoong S., Cui X.S., Kim N.H. (2104). Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes. Reprod. Domest. Anim., 49: 219-227.Search in Google Scholar

Liu K., Muse S.V. (2005). Power Marker: an integrated analysis environment for genetic marker analysis. Bioinformatics, 21: 2128-2129.10.1093/bioinformatics/bti28215705655Open DOISearch in Google Scholar

Marchitelli C., Nardone A. (2015). Mutations and sequence variants in GDF9, BMP15, and BMPR1Bgenes in Maremmana cattle breed with single and twin births. Rend. Fis. Acc. Lincei, 26, suppl. 3: 553-560.Search in Google Scholar

Mlodawska W., Slomczynska M. (2010). Immunohistochemical localization of aromatase during the development and atresia of ovarian follicles in prepubertal horses. Theriogenology, 74: 1707-1712.10.1016/j.theriogenology.2010.04.01920932560Open DOISearch in Google Scholar

Monestier O., Servin B., Auclair S., Bourquard T., Poupon A., Pascal G., Fa- bre S. (2014). Evolutionary origin of bone morphogenetic protein 15 and growth and differentiation factor 9 and differential selective pressure between mono- and polyovulating species. Biol. Rep., 91: 1-13.Search in Google Scholar

Montgomery G.W., Zhao Z.Z., Marsh A.J., Mayne R., Treloar S.A., James M., Mar- tin N.G., Boomsma D.I., Duffy D.L. (2004). Adeletion mutation in GDF9 in sisters with spontaneous DZtwins. Twin. Res., 7: 548-555.Search in Google Scholar

Morel M.C., Newcombe J.R., Swindlehurst J.C. (2005). The effect of age on multiple ovulation rates, multiple pregnancy rates and embryonic vesicle diameter in the mare. Theriogenology, 63: 2482-2493.10.1016/j.theriogenology.2004.09.05815910928Open DOISearch in Google Scholar

Mottershead D.G., Sugimura S., Al- Musawi S.L., Li J.J., Richani D., White M.A., Martin G.A., Trotta A.P., Ritter L.J., Shi J., Mueller T.D., Harrison C.A., Gil- christ R.B. (2015). Cumulin, an oocyte-secreted heterodimer of the transforming growth factor-β family, isapotent activator of granulosa cells and improves oocyte quality. J. Biol. Chem., 290: 24007-24020.Search in Google Scholar

Mucha S., Wolc A., Szwaczkowski T. (2012). Bayesian and REMLanalysis of twinning and fertility in Thoroughbred horses. Livest. Sci., 144: 82-88.Search in Google Scholar

Otsuka F., Mc Tavish K.J., Shimasaki S. (2011). Integral role of GDF-9 and BMP-15 in ovarian function. Mol. Rep. Dev., 78: 9-21.10.1002/mrd.21265305183921226076Open DOISearch in Google Scholar

Palmer J.S., Zhao Z.Z., Hoekstra C., Hayward N.K., Webb P.M., Whiteman D.C., Martin N.G., Boomsma D.I., Duffy D.L., Montgomery G.W. (2006). Novel variants in growth differentiation factor 9 in mothers of dizygotic twins. J. Clin. Endocrinol. Metab., 91: 4713-4716.10.1210/jc.2006-097016954162Open DOISearch in Google Scholar

Peng J., Li Q., Wigglesworth K., Rangarajan A., Kattamuri C., Peterson R.T., Eppig J.J., Thompson T.B., Matzuk M.M. (2013). Growth differentiation factor 9: bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc. Natl. Acad. Sci. USA, 110: 776-785.Search in Google Scholar

Pfaffl M.W. (2001). Anew mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29: e45. doi: 10.1093/nar/29.9.e45.Search in Google Scholar

Roser J.F., Meyers-Brown G. (2012). Superovulation in the mare:awork in progress. J. Equine Vet. Sci., 32: 376-386.10.1016/j.jevs.2012.05.055Open DOISearch in Google Scholar

Sakagami M., Ohshima K., Mukoyama H., Yasue H., Okada N. (1994). Anovel t RNA species as an origin of short interspersed repetitive elements (SINEs). Equine SINEs may have originated from t RNA(Ser). J. Mol. Biol., 239: 731-735.Search in Google Scholar

Santagostino M., Khoriauli L., Gamba R., Bonuglia M., Klipstein O., Piras F.M., Vella F., Russo A., Badiale C., Mazzagatti A., Raimondi E., Nergadze S.G., Giulotto E. (2015). Genome-wide evolutionary and functional analysis of the Equine Repetitive Element 1: an insertion in the myostatin promoter affects gene expression. BMC Genet., 16: 126.Search in Google Scholar

Silva B.D., Castro E.A., Souza C.J., Paiva S.R., Sartori R., Franco M.M., Azeve-do H.C., Silva T.A., Vieira A.M., Neves J.P., Melo E.O. (2011). Anew polymorphism in the growth and differentiation factor 9 (GDF9) gene is associated with increased ovulation rate and prolificacy in homozygous sheep. Anim. Genet., 42: 89-92.Search in Google Scholar

Silva J.R.,vanden Hurk R.,van Tol H.T., Roelen B.A., Figueiredo J.R. (2005). Expression of growth differentiation factor 9 (GDF9) bone morphogenetic protein 15 (BMP15) and BMPreceptors in the ovaries of goats. Mol. Reprod., 70: 11-19.Search in Google Scholar

Simpson C.M., Stanton P.G., Walton K.L., Chan K.L., Ritter L.J., Gilchrist R.B., Harrison C.A. (2012). Activation of latent human GDF9 byasingle residue change (Gly 391 Arg) in the mature domain. Endocrinology, 153: 1301-1310.Search in Google Scholar

Sun R.Z., Lei L., Cheng L., Jin Z.F., Zu S.J., Shan Z.Y., Wang Z.D., Zhang J.X., Liu Z.H. (2010). Expression of GDF-9 BMP-15 and their receptors in mammalian ovary follicles. J. Mol. Histol., 41: 325-332.10.1007/s10735-010-9294-220857181Open DOISearch in Google Scholar

Tran J.T-U., Gąsior S. (2010). SINEsubfamilies from horse. Repbase Reports., 10: 240-240.Search in Google Scholar

Wheelan S.J., Aizawa Y., Han J.S., Boeke J.D. (2005). Gene-breaking:anew paradigm for human retrotransposon-mediated gene evolution. Genome Res., 15: 1073-1078.10.1101/gr.3688905118221916024818Open DOISearch in Google Scholar

Wolc A., Bresińska A., Szwaczkowski T. (2006). Genetic and permanent environmental variability of twinning in Thoroughbred horses estimated via three threshold models. J. Anim. Breed. Genet., 123: 186-190.Search in Google Scholar

Zhang D.X., Park W.J., Sun S.C., Xu Y.N., Li Y.H., Cui X.S., Kim N.H. (2011). Regulation of maternal gene expression by MEK/MAPKand MPFsignaling in porcine oocytes during in vitro meiotic maturation. J. Reprod. Dev., 57: 49-56.Search in Google Scholar

Zhao Z.Z., Painter J.N., Palmer J.S., Webb P.M., Hayward N.K., Whiteman D.C., Boomsma D.I., Martin N.G., Duffy D.L., Montgomery G.W. (2008). Variation in bone morphogenetic protein 15 is not associated with spontaneous human dizygotic twinning. Hum. Reprod., 23: 2372-2379.10.1093/humrep/den268272172318614612Open DOISearch in Google Scholar