Regulation of Folliculogenesis by Growth Factors in Piglet Ovary Exposed Prenatally to β-Hydroxy-β-Methylbutyrate (HMB)

Aaron J.W., Hsueh A.J.W., Kawamura K., Cheng Y., Fauser B.C.J.M. (2015). Intraovarian control of early folliculogenesis. Endocr. Rev., 36: 1–24.10.1210/er.2014-1020Search in Google Scholar

Baker, J., Hardy, M.P., Zhou, J., Bondy, C., Lupu, F., Bellvé, A.R., Efstratiadis A. (1996). Effects of an IGF-I gene null mutation on mouse reproduction. Mol. Endocrinol., 10: 903–918.10.1210/mend.10.7.8813730Search in Google Scholar

Behl R., Kaul R. (2002). Insulin like growth factor 1 and regulation of ovarian function in mammals. Indian J. Exp. Biol., 40: 25–30.Search in Google Scholar

Bielańska-Osuchowska Z. (2006). Oogenesis in pig ovaries during the prenatal period: ultrastructure and morphometry. Reprod. Biol., 6: 161–193.Search in Google Scholar

Blicharski T., Tomaszewsk, E., Dobrowolski P., Hułas-Stasiak M., Muszyński S. (2017). A metabolite of leucine (β-hydroxy-β-methylbutyrate) given to sows during pregnancy alters bone development of their newborn offspring by hormonal modulation. PLoS One, 12, e0179693.10.1371/journal.pone.0179693547231628617846Search in Google Scholar

Bradford M.M. (1976). A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-die binding. Anal. Biochem., 72: 248–254.10.1016/0003-2697(76)90527-3Search in Google Scholar

Chan K.A., Tsoulis M.W., Sloboda D.M. (2015). Early-life nutritional effects on the female reproductive system. J. Endocrinol., 224: R45–R62.10.1530/JOE-14-0469Search in Google Scholar

Childs A.J., Kinnell H.L., Collins C.S., Hogg K.R., Bayne A.L., Green S.J., McNeilly A.S., Anderson R.A. (2010). BMP signaling in the human fetal ovary is developmentally regulated and promotes primordial germ cell apoptosis. Stem Cells, 28: 1368–1378.10.1002/stem.440Search in Google Scholar

Cieślak D., Nieradka-Iwanicka B. (2018). β-Hydroxy- β-methylbutyrate (HMB) supplementation during pregnancy and perinatal period in animals studies and possible application in humans. J. Educ. Health Sport, 8: 11–18.Search in Google Scholar

da Cunha E.V., de Souza G.B., Passos J.R.S., Silva A.W.B., Dau A.M., Saraiva M.V.A., Lobo R.N.B., Silva J.R.V. (2017). Effects of bone morphogenetic protein 4 (BMP4) on in vitro development and survival of bovine preantral follicles enclosed in fragments ovarian tissue. Zygote, 25: 256–264.10.1017/S0967199417000089Search in Google Scholar

Doneda L., Klinger F.G., Larizza L., De Felici M. (2002). KL/KIT co-expression in mouse fetal oocytes. Int. J. Dev. Biol., 46: 1015–1021.Search in Google Scholar

Driancourt M.A., Reynaud K., Cortvrindt R., Smitz J. (2000). Roles of KIT and KIT LIGAND in ovarian function. Rev. Reprod., 5: 143–152.10.1530/ror.0.0050143Search in Google Scholar

Dupont C., Cordier A.G., Junien C., Mandon-Pépin B., Levy R., Chavatte-Palmer P. (2012). Maternal environment and the reproductive function of the offspring. Theriogenology, 78: 1405–1414.10.1016/j.theriogenology.2012.06.016Search in Google Scholar

Evans A.C., Mossa F., Walsh S.W., Scheetz D., Jimenez-Krassel F., Ireland J.L., Smith G.W., Ireland J.J. (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reprod. Domest. Anim., 47 Suppl 4: 31–37.10.1111/j.1439-0531.2012.02052.xSearch in Google Scholar

Flummer C., Kristensen N.B., Theil P.K. (2012). Body composition of piglets from sows fed the leucine metabolite β-hydroxy-β-methylbutyrate in late gestation. J. Anim. Sci., 90: 442–444.10.2527/jas.53923Search in Google Scholar

Gospodarowicz D., Bialecki H. (1979). Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine, and human origin. Endocrinology, 104: 757–764.10.1210/endo-104-3-757Search in Google Scholar

Høyer P.E., Byskov A.G., Møllgård K. (2005). Stem cell factor and c-Kit in human primordial germ cells and fetal ovaries. Mol. Cell Endocrinol., 234: 1–10.10.1016/j.mce.2004.09.012Search in Google Scholar

Hułas-Stasiak M., Jakubowicz-Gil J., Dobrowolski P., Tomaszewska E., Muszyński S. (2019). Maternal β-hydroxy-β-methylbutyrate (HMB) supplementation during pregnancy affects early folliculogenesis in the ovary of newborn piglets. Theriogenology, 128: 91–100.10.1016/j.theriogenology.2019.02.003Search in Google Scholar

Hussein M.R. (2005). Apoptosis in the ovary: molecular mechanisms. Hum. Reprod., 11: 162–178.10.1093/humupd/dmi001Search in Google Scholar

Hut K.J., McLaughlin E.A., Holland M.K. (2006). Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol. Hum. Reprod., 12: 61–69.10.1093/molehr/gal010Search in Google Scholar

Jin X., Han C.S., Yu F.Q., Wei P., Hu Z.Y., Liu Y.X. (2004). Anti-apoptotic action of stem cell factor on oocytes in primordial follicles and its signal transduction. Mol. Reprod. Dev., 70: 82–90.10.1002/mrd.20142Search in Google Scholar

Kang J.S., Lee C.J., Lee J.M., Rha J.Y., Song K.W., Park M.H. (2003). Follicular expression of c-Kit/SCF and inhibin-alpha in mouse ovary during development. J. Histochem. Cytochem., 51: 1447–1458.10.1177/002215540305101105Search in Google Scholar

Kezele, P.R., Nilsson, E.E., Skinner, M.K. (2002). Insulin but not insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol. Cell. Endocrinol., 192: 37–43.10.1016/S0303-7207(02)00114-4Search in Google Scholar

Krawczyk A., Rycerz K., Jaworska-Adamu J., Tomaszewska E., Dobrowolski P. (2016). Calretinin expression in hippocampus of mouse offspring from dams treated with β-hydroxy-β-methylbutyrate. Med. Weter., 72: 423–429.10.21521/mw.5535Search in Google Scholar

Lavranos T.C., Rodgers H.F., Bertoncello I., Rodgers R.J. (1994). Anchorage-independent culture of bovine granulosa cells: The effects of basic fibroblast growth factor and dibutyryl cAMP on cell division and differentiation. Exp. Cell Res., 211: 245–251.10.1006/excr.1994.1084Search in Google Scholar

Lu C.L., Yan J., Zhi X., Xia X., Wang T.R., Yan L.Y., Yu Y., Ding T., Gao J.M., Li R., Qiao J. (2015). Basic fibroblast growth factor promotes macaque follicle development in vitro. Reproduction, 149: 425–433.10.1530/REP-14-0557Search in Google Scholar

Martins F.S., Saraiva M.V.A., Celestino J.J.H., Bruno J.B., Almeida A.P., Cunha R.M.S., Silva J.R.V., Campello C.C., Lucci C.M., Matos M.H.T., Figueiredo J.R. (2010). Expression of protein and mRNA encoding insulin growth factor-I (IGF-I) in goat ovarian follicles and the influence of IGF-I on in vitro development and survival of caprine preantral follicles. Anim. Reprod., 7: 349–361.Search in Google Scholar

Monniaux D., Pisselet C. (1992). Control of proliferation and differentiation of ovine granulosa cells by insulin-like growth factor-I and follicle-stimulating hormone in vitro. Biol. Reprod., 46: 109–111.10.1095/biolreprod46.1.109Search in Google Scholar

Morita Y., Manganaro T.F., Tao X.J., Martimbeau S., Donahoe P.K., Tilly J.L. (1999). Requirement for phosphatidylinositol-3’-kinase in cytokine-mediated germ cell survival during fetal oogenesis in the mouse. Endocrinology, 140: 941–949.10.1210/endo.140.2.6539Search in Google Scholar

Morita Y., Tilly J.L. (1999). Oocyte apoptosis: like sand through and hourglass. Dev. Biol., 213: 1–17.10.1006/dbio.1999.9344Search in Google Scholar

Nilsson E., Parrott J.A., Skinner M.K. (2001). Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol. Cell. Endocrinol., 175: 123–130.10.1016/S0303-7207(01)00391-4Search in Google Scholar

Nilsson E.E., Kezele P., Skinner M.K. (2002). Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol. Cell. Endocrinol., 188: 65–73.10.1016/S0303-7207(01)00746-8Search in Google Scholar

Nilsson E.E., Skinner M.K. (2003). Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol. Reprod., 69: 1265–1272.10.1095/biolreprod.103.018671Search in Google Scholar

Nilsson E.E., Skinner M.K. (2004). Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol. Cell. Endocrinol., 214: 19–25.10.1016/j.mce.2003.12.001Search in Google Scholar

NRC, National Research Council (2012). Nutrient Requirements of Swine.National Academy Press,Washington, USA, 11th ed., pp.420.Search in Google Scholar

Ortega S., Ittmann M., Tsang S.H., Erlich M., Basilico C. (1998). Neuronal defects and wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci., USA 95: 5672–5677.10.1073/pnas.95.10.5672Search in Google Scholar

Parrot J.A., Skinner M.K., (1999). Kit ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology, 140: 4262–4271.10.1210/endo.140.9.6994Search in Google Scholar

Pedersen T., Peters H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. Reproduction, 17: 555–557.10.1530/jrf.0.0170555Search in Google Scholar

Poljicanin A., Filipovic N., Vukusic Pusic T., Soljic V., Caric A., Saraga-Babic M., Vukojevic K. (2015). Expression pattern of RAGE and IGF-1 in the human fetal ovary and ovarian serous carcinoma. Acta Histochem., 117: 468–476.10.1016/j.acthis.2015.01.004Search in Google Scholar

Quennell J.H., Stanton J.A.L., Hurst P.R. (2004). Basic fibroblast growth factor expression in isolated small human ovarian follicles. Mol. Hum. Reprod., 10: 623–628.10.1093/molehr/gah083Search in Google Scholar

Resnick J.L., Ortiz M., Keller J.R., Donovan P.J. (1998). Role of fibroblast growth factors and their receptors in mouse primordial germ cell growth. Biol. Reprod., 59: 1224–1229.10.1095/biolreprod59.5.1224Search in Google Scholar

Reynaud K., Cortvrindt R., Smitz J., Driancourt M.A. (2000). Effects of Kit Ligand and anti-Kit antibody on growth of cultured mouse preantral follicles. Mol. Reprod. Dev., 56: 483–494.10.1002/1098-2795(200008)56:4<483::AID-MRD6>3.0.CO;2-OSearch in Google Scholar

Roberts R.D., Ellis R.C.L. (1999). Mitogenic effects of fibroblast growth factors on chicken granulosa cell and theca cells in vitro. Biol. Reprod., 61: 1387–1392.10.1095/biolreprod61.6.1387Search in Google Scholar

Ross A. J., Tilman C., Yao H., MacLaughlin D., Capela B. (2003). AMH induces mesonephric cell migration in XX gonads. Mol. Cell. Endocrinol., 211: 1–7.10.1016/j.mce.2003.09.021Search in Google Scholar

Shimizu T., Yokoo M., Miyake Y., Sasada H., Sato E. (2004). Differential expression of bone morphogenetic protein 4-6 (BMP-4,5 and 6) and growth differentation factor-9 (GDF-9) during ovarian development in neonatal pigs. Domest. Anim. Enocrinol., 27: 397–405.10.1016/j.domaniend.2004.04.001Search in Google Scholar

Stubbs S.A., Webber L.J., Stark J., Rice S., Margara R., Lavery S., Trew G.H., Hardy K., Franks S. (2013). Role of insulin-like growth factors in initiation of follicle growth in normal and polycystic human ovaries. J. Clin. Endocrinol. Metab., 98: 3298–3305.10.1210/jc.2013-1378Search in Google Scholar

Świetlicka I., Muszyński S., Tomaszewska E., Dobrowolsk, P., Kwaśniewska A., Świetlicki M., Skic A., Gołacki K. (2016). Prenatally administered HMB modifies the enamel surface roughness in spiny mice offspring: An Atomic Force Microscopy study. Arch. Oral Biol., 70: 24–31.10.1016/j.archoralbio.2016.06.001Search in Google Scholar

Tatara M.R., Śliwa E., Krupski, W. (2007). Prenatal programming of skeletal development in the offspring: effects of maternal treatment with β-hydroxy-β-methylbutyrate (HMB) on femur properties in pigs at slaughter age. Bone, 40: 1615–1622.10.1016/j.bone.2007.02.018Search in Google Scholar

Tingen C., Kim A., Woodruf, T.K. (2009). The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol. Hum. Reprod., 15: 795–803.10.1093/molehr/gap073Search in Google Scholar

van Wezel I.L., Umapathysivam K., Tilley W.D., Rodgers R.J. (1995). Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Mol. Cell. Endocrinol., 115: 133–140.10.1016/0303-7207(95)03678-4Search in Google Scholar

Wan H.F., Zhu J.T., Shen Y., Xiang X., Yin H.J., Fang Z.F., Che L.Q., Lin Y., Xu S.Y., Feng B., Wu D. (2016a). Effects of dietary supplementation of β-hydroxy-β-methylbutyrate on sow performance and mRNA expression of myogenic markers in skeletal muscle of neonatal piglets. Reprod. Domest. Anim., 51: 134–142.10.1111/rda.1265726698926Search in Google Scholar

Wan H., Zhu J., Su G., Liu Y., Hua L., Hu L., Wu C., Zhang R., Zhou P., Shen Y., Lin Y., Xu S., Fang Z., Che L., Feng B., Wu D. (2016b). Dietary supplementation with β-hydroxy-β-methylbutyrate calcium during the early postnatal period accelerates skeletal muscle fiber growth and maturity in intra-uterine growth-retarded and normal-birth-weight piglets. Br. J. Nutr., 115: 1360–1309.10.1017/S000711451600046526917333Search in Google Scholar

Wan H., Zhu J., Wu C., Zhou P., Shen Y., Lin Y., Xu S., Che L., Feng B., Li J., Fang Z., Wu D. (2017). Transfer of β-hydroxy-β-methylbutyrate from sows to their offspring and its impact on muscle fibre type transformation and performance in pigs. J. Anim. Sci. Biotechnol., 8: 2.10.1186/s40104-016-0132-6Search in Google Scholar

Wang T., Yan L., Yan J., Lu C., Xia X., Yin T.L., Zhu X.H., Gao J.M., Ding T., Hu W.H., Guo H.Y., Li R., Qiao J. (2014). Basic fibroblast growth factor promotes the development of human ovarian early follicle during growth in vitro. Hum. Reprod., 29: 568–576.10.1093/humrep/det465Search in Google Scholar

Wilson G.J., Wilson J.M., Manninen A.H. (2008). Effects of beta-hydroxy-beta-methylbutyrate (HMB) on exercise performance and body composition across varying levels of age, sex, and training experience: a review. Nutr. Metab., 5: 1.10.1186/1743-7075-5-1Search in Google Scholar

Wilson J.M., Fitschen P.J., Campbell B., Wilson G.J., Zanchi N., Taylor L. Wilborn C., Kalman D.S., Stout J.R., Hoffman J.R., Ziegenfuss T.N., Lopez H.L., Kreider R.B., Smith-Ruan A.E., Antonio J. (2013). International Society of Sports Nutrition Position Stand: beta-hydroxy-beta-methylbutyrate (HMB). J. Int. Soc. Sports Nutr., 10: 6.10.1186/1550-2783-10-6Search in Google Scholar

Yamamoto S., Konishi I., Nanbu K., Komatsu T., Mandai M., Kuroda H., Matsushita K., Mori T. (1997). Immunohistochemical localization of basic fibroblast growth factor (bFGF) during folliculogenesis in the human ovary. Gynecol. Endocrinol., 11: 223–230.10.3109/09513599709152538Search in Google Scholar

Zhao J., Tavene M.A., Van Der Weijden G.C., Bevers M.M., Van Den Hurk R. (2001). Insulin-like growth factor-I (IGF-I) stimulates the development of cultured rat pre-antral follicles. Mol. Reprod. Develop., 58: 287–296.10.1002/1098-2795(200103)58:3<287::AID-MRD7>3.0.CO;2-GSearch in Google Scholar