Platelet-derived growth factor-BB (PDGF-BB) improves follicular survival, oocyte and follicular diameters, in a dose-dependent manner, after the in vitro culture of goat preantral follicles enclosed in ovarian tissue fragments
Renato Félix da Silva, Ivina Rocha Brito, Laritza Ferreira de Lima, Francisco Léo Nascimento de Aguiar, Giovanna Quintino Rodrigues, Ivila Lorrine Castro do Nascimento, Rebeca Magalhães Pedrosa Rocha, Francielli Weber Santos Cibin, Matthew Bryan Wheeler, Claudio Cabral Campello, Ana Paula Ribeiro Rodrigues, José Ricardo de Figueiredo
Abstract
The aims of this study were to investigate the effects of different concentrations of Platelet-derived growth factor-BB (PDGF-BB) on the survival, activation, levels of ROS, and growth of goat preantral follicles enclosed in ovarian tissue. For this, ovarian fragments were cultured for 7 days in Alpha Minimum Essential Medium (α-MEM+ ) with or without PDGF-BB (0, 25, 50 and 100 ng/ml). The results showed that both the 25 ng/ml PDGF and the 50 ng/ml PDGF treatments maintained the percentage of morphologically normal follicles from day 1 to day 7. In addition, the 25 ng/ml PDGF treatment showed a significantly higher percentage of morphologically normal follicles when compared to the other treatments. At day 7, greater (P < 0.05) follicular and oocyte diameters were observed in the 25 ng/ml PDGF and the 50 ng/ml PDGF treatments when compared to the cultured control treatment. On day 7 of culture, all the treatments tested had a significant increase in the percentage of developing follicles when compared to the non-cultured control. However, the percentage of follicle activation, as well as ROS production, were similar (P < 0.05) among the treatments, irrespective of culture time. In conclusion, PDGF-BB improved, in a concentration-dependent manner, follicular survival as well as oocyte and follicular diameter after in vitro culture of goat preantral follicle-enclosed in ovarian tissue fragments.
Keywords
References
Aguiar FLN, Lunardi FO, Lima LF, Rocha RMP, Bruno JB, Magalhães-Padilha DM, Cibin FWS, Nunes-Pinheiro DCS, Gastal MO, Rodrigues APR, Apgar GA, Gastal EL, Figueiredo JR. 2016a. FSH supplementation to culture medium is beneficial for activation and survival of preantral follicles enclosed in equine ovarian tissue. Theriogenology, 85:1106-1112.
Aguiar FLN, Lunardi FO, Lima LF, Rocha RMP, Bruno JB, Magalhães-Padilha DM, Cibin FWS, Rodrigues APR, Gastal MO, Gastal EL, Figueiredo JR. 2016b. Insulin improves in vitro survival of equine preantral follicles enclosed in ovarian tissue and reduces reactive oxygen species production after culture. Theriogenology, 85:1063-1069.
Aguiar FLN, Lunardi FO, Lima LF, Bruno JB, Alves BG, Magalhães-Padilha DM, Cibin FWS, Berioni L, Apgar GA, Lo Turco EG, Gastal EL, Figueiredo JR. 2017. Role of EGF on in situ culture of equine preantral follicles and metabolomics profile. Res Vet Sci, 115:155-164.
Bagavant H, Adams S, Terranova P, Chang A, Kraemer FW, Lou Y, Kasai K, Luo AM, Tung KSK. 1999. Autoimmune ovarian inflammation triggered by Proinflammatory (Th1) T cells is compatible with normal ovarian function in mice. Biol Reprod, 61:635- 642.
Berridge MJ. 1993. Inositol triphosphate and calcium signalling. Nature, 361:315-332.
Brito IR, Lima IMT, Saraiva MVA, Silva CMG, Magalhães-Padilha DM, Araújo VR, Barreto Luz V, Barbalho Silva AW, Campello CC, Silva JRV, Figueiredo JR. 2012. Expression levels of mRNAencoding PDGF receptors in goat ovaries and the influence of PDGF on the in vitro development of caprine pre-antral follicles. Reprod Domest Anim, 47:695-703.
Brito IR, Silva CMG, Duarte ABG, Lima IMT, Rodrigues GQ, Rossetto R, Sales AD, Lobo CH, Bernuci MP, Rosa-e-Silva ACJS, Campello CC, Xu M, Figueiredo JR. 2014. Alginate hydrogel matrix stiffness influences the in vitro development of caprine preantral follicles. Mol Reprod Dev, 81:636-645.
Brito IR, Sales AD, Rodrigues GQ, Lobo CH, Castro SV, Silva AWB, Moura AAA, Silva JRV, Rodrigues APR, Figueiredo JR. 2015. Differential gene expression and immunolocalization of platelet-derived growth factors and their receptors in caprine ovaries. Domest Anim Endocrinol, 51:46-55.
Bruno JB, Celestino JJ, Lima-Verde IB, Lima LF, Matos MH, Araújo VR, Saraiva MV, Martins FS, Campello CC, Figueiredo JR. 2009. Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF. Reprod Fertil Dev, 21:679-687.
Carvalho AA, Faustino LR, Silva CMG, Castro SV, Lobo CH, Santos FW, Santos RR, Campello CC, Bordignon V, Figueiredo JR, Rodrigues APR. 2014.
Catalase addition to vitrification solutions maintains goat ovarian preantral follicles stability. Res Vet Sci, 97:140-147.
Castro SV, Carvalho AA, Silva CMG, Santos FW, Campello CC, Figueiredo JR, Rodrigues APR. 2014. Fresh and vitrified bovine preantral follicles have different nutritional requirements during in vitro culture. Cell Tissue Bank, 15:591-601.
Chaves RN, Martins FS, Saraiva MVA, Celestino JJH, Lopes CAP, Correia JC, Lima-Verde IB, Matos MHT, Báo SN, Name KPO, Campello CC, Silva JRV, Figueiredo JR. 2008. Chilling ovarian fragments during transportation improves viability and growth of goat preantral follicles cultured in vitro. Reprod Fertil Dev, 20:640-647.
Chaves RN, Alves AMCV, Duarte ABG, Araújo VR, Celestino JJH, Matos MHT, Lopes CAP, Campello CC, Name KPO, Báo SN, Figueiredo JR. 2010. Nerve growth factor promotes the survival of goat preantral follicles cultured in vitro. Cells Tissues Organs, 192:272-282.
Cushman RA, Wahl CM, Fortune JE. 2002. Bovine ovarian cortical pieces grafted to chick embryonic membranes: a model for studies on the activation of primordial follicles. Hum Reprod, 174:48-54.
Duleba AJ, Spaczynski RZ, Arici A, Carbone R, Behrman HR. 1999. Proliferation and differentiation of rat theca-interstitial cells: comparison of effects induced by platelet-derived growth factor and insulin-like growth factor-I. Biol Reprod, 60:546-550.
Fortune JE, Kito SA, Wandji VS. 1998. Activation of bovine and baboon primordial follicles in vitro. Theriogenology, 49:441-449.
Fortune JE, Cushman RA, Wahl CM, Kito S. 2000. The primordial to primary follicle transition. Mol Cell Endocrinol, 163:53-60.
Fortune JE. 2003. The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci, 78:135- 163.
Gaultier CJ, Michel JB. 1999. Angiogenic growth factors. In: Levy BI, Tedgui A (Ed.). Biology of the Arterial Wall. Norwell, MA: Kluwer Academic Publishers. pp. 101-111.
Haag KT, Magalhães-Padilha DM, Fonseca GR, Wischral A, Gastal MO, King SS, Jones KL, Figueiredo JR, Gastal EL. 2013. Quantification, morphology, and viability of equine preantral follicles obtained via the biopsy pick-up method. Theriogenology, 79:599-609.
Hwu YM, Li SH, Lee RK, Lin MH, Tsai YH, Yeh TS. 2009. Luteinizing hormone increases-platelet derived growth factor-D gene expression in human granulosa-luteal cells. Fertil Steril, 92:2065-2068.
Kim JY. 2012. Control of ovarian primordial follicle activation. Clin Exp Reprod Med, 39:10-14.
Lee VH. 2000. Expression of rabbit zona pellucida-1 messenger ribonucleic acid during early follicular development. Biol Reprod, 63:401-408.
Lopes CAP, Santos RR, Celestino JJH, Melo MAP, Chaves RN, Campello CC, Silva JRV, Báo SN, Jewgenow K, Figueiredo JR. 2008. Short-term preservation of canine preantral follicles: effects of temperature, medium and time. Anim Reprod Sci, j115:201-214.
Lopes CAP, Alves AMCV, Jewgenow K, Báo SN, Figueiredo JR. 2016. Cryopreservation of canine ovarian cortex using DMSO or 1,3-propanediol. Theriogenology, 86:1165-1174.
Liu X. 2014. Overstimulation can create health problems due to increases in PI3K/Akt/GSK3 insensitivity and GSK3 activity. Springerplus, 3:356- 368.
Loetchutinat C, Kothan S, Dechsupa S, Meesungnoen J, Jay-Gerin JP, Mankhetkorn S. 2005. Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drugresistant cancer cells using the 2’,7’- dichlorofluorescein diacetate assay. Radiat Phys Chem, 72:323-331.
Lucci CM, Amorim CA, Báo SN, Figueiredo JR, Rodrigues APR, Silva JRV, Gonçalves PBD. 1999. Effect of the interval of serial sections of ovarian tissue in the tissue chopper on the number of isolated caprine preantral follicles. Anim Reprod Sci, 56:39-49.
Lunardi FO, Araújo VR, Faustino LR, Carvalho AA, Gonçalves RFB, Bass CS, Báo SN, Name KPO, Campello CC, Figueiredo JR, Rodrigues APR. 2012.
Morphologic, viability and ultrastructural analysis of vitrified sheep preantral follicles enclosed in ovarian tissue. Small Rumin Res, 107:121-130.
Magalhães-Padilha DM, Geisler-Lee J, Wischral A, Gastal MO, Fonseca GR, Eloy YRG, Geisler M, Figueiredo JR, Gastal EL. 2013. Gene expression during early folliculogenesis in goats using microarray analysis. Biol Reprod, 89:19. doi: 10.1095/biolreprod.112.106096.
Martinho NA, Dell’Aquila ME, Uranio MF, Rutigliano L, Nicassio M, Lacalandra GM, Hinrichs K. 2014. Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential. Reprod Biol Endocrinol, 12:99. doi: 10.1186/1477-7827-12-99.
McLaughlin EA, McIver SC. 2008. Awakening the oocyte: controlling primordial follicle development. Reproduction, 137:1-11. doi: 10.1530/REP-08-0118.
Nilsson EE, Detzel C, Skinner MK. 2006. Plateletderived growth factor modulates the primordial to primary follicle transition. Reproduction, 131:1007- 1015.
Oktem O, Oktay K. 2008. The ovary: anatomy and function throughout human life. Sciences (New York), 1127:1-9. doi: 10.1196/annals.1434.009.
Ou XH, Li S, Wang ZB, Li M, Quan S, Xing F, Guo L, Chao SB, Chen Z, Liang XW, Hou Y, Schatten H, Sun QY. 2012. Maternal insulin resistance causes oxidative stress and mitochondrial dysfunction in mouse oocytes. Hum Reprod, 27:2130-2145.
Paes VM, Vieira LA, Correia HHV, Sa NAR, Moura AAA, Sales AD, Rodrigues APR, Magalhães-Padilha DM, Santos FW, Apgar GA, Campello CC, Camargo LSA, Figueiredo JR. 2016. Effect of heat stress on the survival and development of in vitro cultured bovine preantral follicles and on in vitro maturation of cumulus–oocyte complex. Theriogenology, 86:994- 1003.
Rigacci S, Iantomasi T, Marraccini P, Berti A, Vincenzini MT, Ramponi G. 1997. Evidence for glutathione involvement in platelet-derived growthfactor mediated signal transduction. Biochem J, 324:791-796.
Rizzo A, Roscino MT, Binetti F, Sciorsci RL. 2012. Roles of reactive oxygen species in female reproduction. Reprod Domest Anim, 47:344-352.
Rubin K, Tingstro AM, Hansson GK, Larsson E, Nnstrand L, Klareskog L, Claesson-Welsh L, Heldin CH, Fellstro BM, Terracio L. 1988. Induction of Btype receptors for platelet-derived growth factor in vascular inflammation: possible implications for development of vascular proliferative lesions. Lancet, 1:1353-1356. Sá NAR, Araújo VR, Correia HHV, Ferreira ACA, Guerreiro DD, Sampaio AM, Escobar E, Santos FW, Moura AA, Lôbo CH, Ceccatto VM, Campello CC, Rodrigues APR, Leal-Cardoso JH, Figueiredo JR. 2017. Anethole improves the in vitro development of isolated caprine secondary follicles. Theriogenology, 89:226-234.
Silva JRV, Van Den Hurk R., Matos MHT, Santos RR, Pessoa C, Moraes MO, Figueiredo JR. 2004. Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology, 61:1691-1704.
Sleer LS, Taylor CC. 2007. Cell-type localization of platelet-derived growth factors and receptors in the postnatal rat ovary and follicle. Biol Reprod, 76:379- 390.
Talebi A, Zavareh S, Kashani MH, Lashgarbluki T, Karimi I. 2012. The effect of alpha lipoic acid on the developmental competence of mouse isolated preantral follicles. J Assist Reprod Genet, 29:175-183.
Taylor CC. 2000. Platelet-derived growth factor activates porcine thecal cellphosphatidylinositol-3- kinase-Akt/PKB and ras-extracellular signal-regulated kinase-1/2 kinase signaling pathways via the plateletderived growth factor-beta receptor. Endocrinology, 141:1545-1553.
Van Den Hurk R, Zhao J. 2005. Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology, 63:1717-1751.
Vanhaesebroeck B, Leevers SJ, Panayotou G, Waterfield MD. 1997. Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem Sci, 7:267-272.
Winterbourn CC. 2014. The challenges of using fluorescent probes to detect and quantify specific reactive oxygen species in living cells. Biochim Biophys Acta, 1840:730-738.
Young RM, Mendonza AE, Collins T, Orkin SH. 1990. Alternatively spliced platelet-derived growth factor A-chain transcripts are not tumor specific but encode normal cellular proteins. Mol Cell Biol, 11:6051-6054.
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