Aspectos qualitativos e quantitativos da atresia durante a foliculogênese em mamíferos
Palavras-chave:
Folículos ovarianos, fatores de crescimento, métodos de análises, vacúolosResumo
Durante a foliculogênese ovariana, cerca de 99,9% dos folículos morrem pelo processo de atresia folicular. O processo de atresia pode ocorrer pelas vias degenerativa ou apoptótica. Este processo compromete todos os estágios de desenvolvimento folicular, sendo os folículos antrais os mais afetados. Por outro lado, os folículos pré-antrais são mais resistentes, em função de sua menor taxa metabólica, bem como do número reduzido de células e camadas de células somáticas, células da granulosa e/ou da teca. Embora folículos pré-antrais sejam menos afetados pelo processo de atresia, quando este evento ocorre, pode-se classificá-lo de duas formas, degeneração do tipo I e degeneração do tipo II. Na degeneração do tipo I, o oócito é o compartimento mais comprometido, apresentando núcleo picnótico, embora suas células da granulosa apresentem-se bem organizadas e sem picnose nuclear. Já na degeneração do tipo II, os folículos apresentam oócito retraído e células da granulosa edemaciadas, desorganizadas e sem aderência à membrana basal e ao oócito. É importante destacar que a degeneração do tipo I é mais comum em folículos primordiais e primários, enquanto folículos secundários apresentam mais degeneração do tipo II, ou seja, a medida que os folículos evoluem, a degeneração do tipo II é mais frequente. Considerando todos os aspectos aqui relacionados, essa revisão de literatura abordará aspectos relacionados aos processos de foliculogênese e atresia folicular, bem como as substâncias que induzem a atresia durante a foliculogenesein vitro e in vivo e, ainda, os métodos e parâmetros para análise da atresia em folículos ovarianos. Isto se deve a necessidade de desenvolvimento de protocolos mais eficientes de recuperação dos folículos ovarianos, prevenindo essa grande perda folicular e otimizando as possibilidades de utilização desses materiais biológicos no futuro.
Referências
ABRAMOVICH, D.; PARBORELL, F.; TESONE, M. Effect of a vascular endothelial growth factor (VEGF) Inhibitory treatment on the folliculogenesis and ovarian apoptosis in gonadotropin-treated prepubertal rats. Biology of Reproduction, v.75, p.434-441, 2006.
ABRAMOVICH, D.; IRUSTA, G.; PARBORELL, F.; TESONE, M. Intrabursal injection of vascular endothelial growthfactor trap in eCG-treated prepubertal rats inhibitsproliferation and increases apoptosis of follicular cellsinvolving the PI3K/AKT signaling pathway. Fertility and Sterility,v.93, p.1369-1377, 2010.
AERTS, J.M.; BOLS, P.E. Ovarian follicular dynamics: a review with emphasis on thebovine species. Part I: Folliculogenesis and pre-antral follicle development. Reproduction in Domestic Animals,v.45, p.171-179, 2010.
ARAÚJO, V.R.; LIMA-VERDE, I.B.; NAME, K.P.O.; BÁO S.N.; CAMPELO, C.C.; SILVA, J.R.V.; RODRIGUES, A.P.R.; FIGUEIREDO, J.R. Bone Morphogenetic Protein-6 (BMP-6) induces atresia in goat primordial follicles cultured in vitro. Pesquisa Veterinária Brasileira, v.30, p.770-776, 2010.
ARAÚJO, V.R.; GASTAL, M. O.; FIGUEIREDO, J.R.; GASTAL, E. L. In vitrocultureofbovinepreantralfollicles: a review. Reproductive Biology and Endocrinology,v.12, p.78, 2014.
ARAÚJO, V.R.; GASTAL, M. O.; WISCHRAL, A.; FIGUEIREDO, J.R.; GASTAL, E. L.
Long-term in vitro culture of bovine preantral follicles: Effect of base medium and medium replacement methods,Animal Reproduction Science,v.161, p.23-31,2015.
ARAÚJO, V.R.; SILVA, G.M.; FIGUEIREDO, J.R. Only VEGF is necessary to stimulate the meiotic competence of caprine oocytes during in vitro maturation. Ciência Animal (UECE), v.27, p.31-40, 2017.
BAO, B.; GARVERICK, H.A.; SMITH, G.W.; SMITH, M.F.; SALFEN, B.E.; YOUNGQUIST, R.S. Changes in messenger ribonucleic acid encoding luteinizing hormone receptor, cytochrome P450-side chain cleavage, and aromatase are associated with recruitment and selection of bovine ovarian follicles. Biology of Reproduction, v.56, p.1158-1168, 1997.
BHATIA, M. Apoptosis versus necrosis. American Journal of Physiology-Renal Physiology v.284, p.608-627, 2004.
BONZ, A.; SIEGMUND, B.; LADILOV, Y.; VAHL, C.F.; PIPER, H.M. Metabolic recovery of isolated adult rat cardiomyocytes after energy depletion: existence of an ATP threshold? Journal of Molecular and Cellular Cardiology, v.30, p.2111-2119, 1998.
BOONE, D.L.; TSANG, B. K. Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression, Biology of Reproduction, v.58, p.1533-1539, 1998.
BOSSY-WETZEL, E.; GREEN, D.R. Detection of apoptosis by Annexin V labeling, Methods in Enzymology, v.322, p.15-18, 2000.
BRISTOL-GOULD, S.; WOODRUFF, T. K. Folliculogenesis in the domestic cat (Felis catus). Theriogenology, v.66, p.5-13, 2006.
BRUNO, J.B.; LIMA-VERDE, I.B.; MARTINS, F.S.; MATOS, M.H.T.; LOPES, C.A.P.; MAIA-JR, J.E.; BÁO, S.N.; NOBRE-JUNIOR, H.V.; MAIA F.D.; PESSOA, C.; MORAES, M.O.; SILVA, J.R.V.; FIGUEIREDO, J.R.; RODRIGUES, A.P.R. Característica histológica, ultra-estrutural e produção de nitrito de folículos pré-antrais caprinos cultivados in vitro na ausência ou presença de soro. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, v.60, p.1329-1337, 2008.
CELESTINO, J.J.H.; CHAVES, R.N.; MATOS, M.H.T.; SARAIVA, M.V.A.; SILVA, J.R.V.; BRUNO, J.B.; MAIA-JÚNIOR, J.E.; FIGUEIREDO, J.R. Mechanismsof atresia in ovarianfollicles. Animal Reproduction, v.6, p.495-508, 2009.
CUNHA, E.R.; MARTINS, C.F.; SILVA, C.G.; BESSLER, H.C.; BÁO, S.N.Effects of prolonged in vitro culture and cryopreservation on viability, DNA fragmentation, chromosome stability and ultrastructure of bovine cells from amniotic fluid and umbilical cord. Reproduction and Domestic Animals,v.49, p.806-812, 2014.
De los REYES, M.; VILLAGRÁN, M.L.; CEPEDA, R.; DUCHENS, M.; PARRAGUEZ, V.; URQUIETA, B. Histological characteristics and steroid concentration of ovarian follicles at different stages of development in pregnant and non-pregnant dairy cows. Veterinary Research Communications, v.30, p.161-173, 2006.
ELMORE, S. Apoptosis: a review of programmed cell death. Toxicologic Pathology, v.35, p.495-516, 2007.
FIGUEIREDO, J.R.; HULSHOF, S.C.J.; VAN DEN HURK, R.; BEVERS, M.M.; THIRY, M.; NUSGENS, B.; BECKERS, J.F. The physiological status of the ovarian donor affects the in vitro development of isolated bovine preantral follicles. Theriogenology, v.42, p.1303-1310, 1994.
GARLID, K.D. Cation transport in mitochondria-the potassium cycle. Biochimica et Biophysica Acta, v.1275, p.123-126, 1996.
GOUGEON, A. Dynamics of follicular growth in the human: a model from preliminary results. Human Reproduction, v.1, p.81-87, 1986.
GOUGEON, A. Human ovarian follicular development: From activation of resting follicles to preovulatory maturation. Annales d’Endocrinologie, v.71, p.132-143, 2010.
HAZZARD, T.M.; XU, F.; STOUFFER, R.L. Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biology of Reproduction,v. 67, p. 1305-1312, 2002.
HERNANDEZ-MEDRANO, J.H.; CAMPBELL, B.K.; WEBB, R. Nutritional Influences on Folliculogenesis. Reproduction in Domestic Animals,v.47, p.274-282, 2012.
HIRSHFIELD, A.N. Effect of low dose of pregnant mar’s serum gonadotropin on follicular recruitment and atresia in cycling rats. Biology of Reproduction, v.35, p 113-118, 1986.
HIRSHFIELD, A.N. Size-frequency analysis of atresia in cycling rats. Biology of Reproduction, v.38, p.1181-1188, 1988.
HOU, L.; LIU, K.; LI, Y.; MA, S.; JI, X.; LIU, L. Necrotic pyknosis is a morphologically and biochemically distinct event from apoptotic pyknosis. Journal of Cell Science, v.129, p.3084-3090, 2016.
HUONG, P.L.T.;KOLK, A.H.J.; EGGELTE, T.A.; VERSTIJNEN, C.P.H.J.; GILIS, H.; HENDRIKS, J.T. Journal of Immunological Methods, v.140, p 243-248, 1991.
HUGHES JR. F.M.; GOROPE, W.C. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology, v.129, p.2415-2422, 1991.
INOUE, N.; MATSUDA, F.; GOTO, Y.; MANABE, N. Role of cell-death ligand-receptor system of granulosa cells in selective follicular atresia in porcine ovary. Journal of Reproduction and Development,v.57, p.169-175, 2011.
KAIPIA, A.; CHUN, S. Y.; EISENHAUER, K.; HSUEH, A. W. J. Tumor necrosis factor- and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles. Endocrinology, v.137, p.4864-4870, 1996.
KUROSAKA, K.; TAKAHASHI, M.; WATANABE, N.; KOBAYASHI, Y. Silent cleanup of very early apoptotic cells by macrophages. Journal of Immunology, v.171, p.4672-4679, 2003.
LOPES, C.A.P.; SANTOS, R.R.; CELESTINO, J.J.H.; MELO, M.A.P.; CHAVES, R.N.; CAMPELLO, C.C.; SILVA, J.R.V.; BÁO, S.N.; JEWGENOW, K., FIGUEIREDO, J.R. Short-term preservation of canine preantral follicles: Effects of temperature, medium and time. Animal Reproduction Science, v.115, p.201-214, 2009.
LIMA-VERDE, I.B.; MATOS, M.H.T.; BRUNO, J.B.; MARTINS, F.S.; SANTOS, R.R.; BÁO, S.N.; LUQUE, M.C.A.; VIEIRA, G.A.B.; SILVEIRA, E.R.; RODRIGUES, A.P.R.; FIGUEIREDO, J.R.; OLIVEIRA, M.A.L.; LIMA, P.F. Effects of α-tocopherol and ternatin antioxidants on morphology and activation of goat preantral follicles in vitro cultured. ArquivoBrasileiro de Medicina Veterinária e Zootecnia, v.61, p.57-65, 2009.
MANABE, N.; MYOUMOTO, A.; TAJIMA, C.; FUKUMOTO, M.; NAKAYAMA, M.; UCHIO, K.; YAMAGUCHI, M.; MIYAMOTO, H. Immunochemical characteristics of a novel cells death receptor and a decoy receptor on granulosa cells of porcine ovarian follicles. Cytotechnology, v.33, p.189-201, 2000.
MARKSTRÖM, E.; SVENSSON, E.C.; SHAO, R.; SVANBERG, B.; BILLIG, H. Survival factors regulating ovarian apoptosis – dependence on follicle differentiation. Reproduction, v.123, p.23-30, 2002.
MARTINS, F.S.; van den HURK, R.; SANTOS, R.R.; SILVA, J.R.V.; MATOS, M.H.T.; CELESTINO, J.J.H.; RODRIGUES, A.P.R.; PESSOA, C.; FERREIRA, F.V.A.; FIGUEIREDO, J.R. Development of goat primordial follicles after in vitro culture of ovarian tissue in Minimal Essential Medium supplemented with coconut water. Animal Reproduction, v.2, p.106-113, 2005.
MATOS, M.H.T.; van den HURK, R.; MARTINS, F.S.; SANTOS, R.R.; LUQUE, M.C.A.; SILVA, J.R.V.; CELESTINO, J.J.H.; BÁO, S.N.; FIGUEIREDO, J.R. Histological and ultrastructural features of caprine preantral follicles after in vitro culture in the presence or absence of indole-3-acetic acid. Animal Reproduction, v.3, p.415-422, 2006.
McCGEE, E.A.; HSUEH, A.J.W. Initial and cyclic recruitment of ovarian follicles. Endocrine Reviews, v.21, p.200-214, 2000.
MHAWI, A.J.; KANKA, J.; MOTL´IK, J. Follicle and oocyte growth in early postnatal calves: cytochemical, autoradiographical and electron microscopical studies. Reproduction Nutrition Development, v.31, p.115-126, 1991.
MLODAWSKA, W.; SLOMCZYNSKA, M. Immunohistochemical localization of aromatase during the development and atresia of ovarian follicles in prepubertal horses, Theriogenology, v.74, p.1707-1712, 2010.
NAKAYAMA, M.; MANABE, N.; NISHIHARA, S.; MIYAMOTO, H. Species specific differences in apoptotic cell localization in granulosa and theca internal cells during follicular atresia in porcine and bovine ovaries. Journal of Reproduction and Development, v.46, p.147-156, 2000.
PARBORELL, F.; PECCI, A.; GONZALEZ, O.; VITALE, A.; TESONE, M. Effects of a gonadotropin-releasing hormone agonist on rat ovarian follicle apoptosis: regulation by EGF and the expression of Bcl-2-related genes. Biology of Reproduction, v.67, p.481-486, 2002.
PRANGE-KIEL, J.; KREUTZKAMM, C.; WEHRENBERG, U.; RUNE, G.M. Role of tumor necrosis factor in preovulatory follicles of swine. Biology of Reproduction,v.65, p.928-935, 2001.
QU, J.P.; GODIN, P.A.; NISOLLE, M.; DONNEZ, J. Distribution of epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation. Human Reproduction, v.15, p.302-310, 2000.
RODRIGUES, A.P.R.; COSTA, S.H.F.; SANTOS, R.R.; AMORIM, C.A.; LUCCI, C.M.; BÁO, S.N.; NUNES, J.F.; RONDINA, D.; FIGUEIREDO, J.R. In vitro culture of cryopreserved caprine ovarian tissue pieces and isolated follicles. Cell Pres, v.4, p.290-298, 2006.
SANTOS, R.R.; THARASANIT, T.; VAN, H.T.; FIGUEIREDO, J.R.; SILVA, J.R.V.; van den HURK, R. Vitrification of goat preantral follicles enclosed in ovarian tissue by using conventional and solid-surface vitrification methods. Cell and Tissue Research, v.327, p.167-176, 2007.
SAVILL, J.; FADOK, V. Corpse clearance defines the meaning of cell death. Nature, v.407, p.784-788, 2000.
OCHATT, S.J. Flow cytometry (ploidy determination, cell cycle analysis, DNA content per nucleus). In: – The Medicago truncatula handbook. Ardmore, OK: Noble Research Institute, 2006, 1-13 p.
SILVA, J.R.V.; FERREIRA, M.A.L.; COSTA, S.H.F.; SANTOS, R.R.; CARVALHO, F.C.A.; RODRIGUES A.P.R.; LUCCI, C.M.; BÁO, S.N.; FIGUEIREDO, J.R. Degeneration rate of preantral follicles in the ovaries of goats.Small Ruminant Research, v.43, p.203-209, 2002.
SILVA, J.R.V.; van den HURK, R.; van TOL, H.T.; ROELEN, B.A.; FIGUEIREDO, J.R. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP-15), and BMP receptors in the ovaries of goats. Molecular Reproduction and Development, v.70, p.11-19, 2005.
SILVA, J.R.V.; THARASANIT, T.; TAVERNE, M.A.M.; van der WEIJDEN, G.C.; SANTOS, R.R.; FIGUEIREDO, J.R.; van den HURK, R. The activin-follistatin system and in vitro early follicle development in goats. Journal of Endocrinology, v.189, p.113-125, 2006.
SVANBERG, B.; BILLIG, H. Isolation of differentially expressed mRNA in ovaries after estrogen withdrawal in hypophysectomized diethylstilbestrol-treated rats: increased expression during apoptosis. Journal of Endocrinology, v.163, p.309-316, 1999.
SVENSSON, P-A.; JOHNSON, M.S.C.; LING, C.; CARLSSON, L.M.S.; BILLIG, H.; CARLSSON. B. Scavenger receptor class B type I in the rat ovary: possible role in high density lipoprotein cholesterol uptake and in the recognition of apoptotic granulosa cells. Endocrinology, v.140, p.2494-2500, 1999.
TABAROWSKI, Z.; SZOLTYS, M.; BIK, M.; SLOMCZYNSKA, M. Atresia of large ovarian follicles of the rat. Folia Histochemica et Cytobiologica, v.43, p.43-50, 2005.
TINGEN, C.; KIM, A.; WOODRUFF, T. K. The primordial pool of follicles and nest breakdown in mammalian ovaries. Molecular human reproduction, v.15, p.795-803, 2009.
TILLY, J.L.; KOWALSKI, K. I.; JOHNSON, A. L.; HSUEH, A. J. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology, v.129, p.2799-2801, 1991.
TILLY, J. L.; KOWALSKI, K.I.; SCHOMBERG, D.W.; HSUEH, A. J. Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology, v.131, p.1670-1676, 1992.
van den HURK, R.; ZHAO, J. Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology, v.63, p.1717-1751, 2005.
YEUNG, C. K.; WANG, G.; YAO, Y.; LIANG, J.; TENNY CHUNG, C. Y.; CHUAI, M.; LEE, K. K.; YANG, X. BRE modulates granulosa cell death to affect ovarian follicle development and atresia in the mouse. Cell death & disease, v.8, p.e2697, 2017.
YUAN, J.H.; WANG, J.Z.; LAN, G.C.; SUI, H.S.; YU, J.N.; TAN, J.H. Expression of steroidogenic enzymes and synthesis of steroid hormones during development of ovarian follicles in prepubertal goats. Domestic Animal Endocrinology, v.34, p.451-460, 2008.
ZHANG, W.; HUANG, L.; ZHUANG, Y.; WANG, W. The effect of mifepristone on apoptosis and caspase-3 activation in human ovarian luteinized granulosa cells. European Journal of Obstetrics & Gynecology and Reproductive Biology,v.141, p.131-136, 2008.
WANG, J.J.; GE, W.; LIU, J.C.; KLINGER, F.G.; DYCE, P.W.; De FELICI, M.; SHEN, W. Complete in vitro oogenesis: retrospects and prospects. Cell Death Differ. V.24, p.1845-1852, 2017.
WILLIAMS, C.J.; ERICKSON, G.F. Morphology and Physiology of the Ovary. [Updated 2012 Jan 30]. In: Feingold KR, Anawalt B, Boyce A, et al., editors. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.; 2000-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK278951/
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