The Role of Androgens in Mammals Folliculogenesis

Authors

  • Livia Brunetti Apolloni Laboratório de Manipulação de Oócitos Inclusos em Folículos Pré-Antrais (LAMOFOPA), Programa de Pós-graduação em Ciências Veterinárias (PPGCV), Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil.
  • Jamily Bezerra Bruno Laboratório de Manipulação de Oócitos Inclusos em Folículos Pré-Antrais (LAMOFOPA), Programa de Pós-graduação em Ciências Veterinárias (PPGCV), Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil.
  • Benner Geraldo Alves Laboratório de Manipulação de Oócitos Inclusos em Folículos Pré-Antrais (LAMOFOPA), Programa de Pós-graduação em Ciências Veterinárias (PPGCV), Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil.
  • José Ricardo de Figueiredo Laboratório de Manipulação de Oócitos Inclusos em Folículos Pré-Antrais (LAMOFOPA), Programa de Pós-graduação em Ciências Veterinárias (PPGCV), Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil.

DOI:

https://doi.org/10.22456/1679-9216.81075

Keywords:

follicles, in vitro culture, androgens, steroidogenesis.

Abstract

Introduction: Steroid hormones production is a physiological process termed steroidogenesis. An important stage of this process is the conversion of androgens into estrogens through aromatase enzyme. Furthermore, androgens are important in the process of folliculogenesis, promoting follicular growth in different species. Thus, the aim of this review was to present the process of synthesis, mechanism of action, and importance of androgens in folliculogenesis. Additionally, the main results of in vitro culture of ovarian cells in the presence of these hormones were emphasized.

Review: Folliculogenesis begins in prenatal life in most of species and can be defined as the process of formation, follicular growth, and oocyte maturation. Preantral follicles represent 95% of the follicular population and assisted reproductive technologies have been developed (e.g., Manipulation of Oocytes Enclosed in Preantral Follicles - MOEPF) in order to avoid the great follicle loss that occurs naturally in vivo by atresia. The MOEPF aim to obtain a large number of competent oocytes from preantral follicles and then subject to in vitro maturation, fertilization, and culture for embryo production. However, the development of an efficient medium to ensure the follicular survival and oocyte maturation is the major challenge of this biotechnology. To achieve the success on in vitro culture, the effects of substances as androgens on follicular development have been evaluated. Androgens are steroid hormones produced in theca cells (TC) that are fundamental for follicular growth. These cells provide all the androgens required by the developing follicles for conversion into estrogens by the granulosa cells (GC). Androgens receptors (AR) are localized in cell cytoplasm of all follicular categories, being more expressed in preantral follicles. The androgen pathway initiates through its connection to its receptor, making a complex androgen-AR, that in the nucleus helps on the process of gene transcription related with follicular survival. This mechanism is androgen receptor genomic activity. In addition to genomic action, there is an androgen receptor non-genomic activity. This occurs through activation of AR and its interaction with different signaling molecules located on the cell membrane, triggering events that aid in the follicular development. Regardless of the androgens actions, ovarian cells of several species subjected to in vitro culture have shown the importance of these hormones on the follicle development. Recent studies demonstrated that androgens addition on the culture medium stimulated the activation of preantral follicles (bovine and caprine), antrum formation (swine), survival (non-primate), and oocyte maturation (antral follicles; bovine). Also, some studies suggest that the addition of these hormones on in vitro culture is dose-dependent and species-specific.

Conclusion: This review shows the role of androgens in different stages of follicular development and its action as a substrate for steroidogenesis and transcription of genes related to follicular survival and oocyte maturation. However, when these hormones should be added during in vitro follicular culture and which concentration is required remains unclear, being necessary more studies to elucidate these aspects.

Downloads

Download data is not yet available.

References

Abir R., Nitkse S., Ben-Harous A. & Fisch B. 2006. In vitro maturation of human primordial ovarian follicles: Clinical significance, progress in mammals, and methods for growth evaluation. Histology and Histopathology. 21(8): 887-898.

Almeida A.P., Saraiva M.V.A., Alves Filho J.G., Silva G.M., Gonçalves R.F.B., Brito I.R., Silva A.W.B., Lima A.K.F., Cunha R.M.S., Silva J.R.V. & Figueiredo J.R. 2012. Gene expression and immunolocalization of fibroblast growth factor 2 in the ovary and its effect on the in vitro culture of caprine preantral ovarian follicles. Reproduction in Domestic Animals. 47(1): 20-25.

Andersen C.Y., Rosendahl M., Byskov A.G., Loft A., Ottosen C., Dueholm M., Schmidt K.L.T., Andersen A.N. & Ernst E. 2008. Two successful pregnancies following autotransplantation of frozen/thawed ovarian tissue. Human Reproduction. 23(10): 2266-2272.

Araújo V.R. 2013. Estudo dos fatores que afetam a eficiência do cultivo in vitro de folículos pré-antrais caprinos e bovinos: efeito do regime de troca, meios de cultivo de base e suplementos. 290f. Fortaleza, CE. Tese (Doutorado em Ciências Veterinárias) - Programa de Pós-graduação em Ciências Veterinárias, Universidade Estadual do Ceará.

Bennett N.C., Gardinerb R.A., Hooperd J.D., Johnsone D.W. & Gobea G.C. 2010. Molecular cell biology of androgen receptor signalling. The International Journal of Biochesmitry & Cell Biology. 42(6): 813-827.

Betteridge K.J., Smith C., Stubbings R.B., Xu K.P. & King W.A. 1989. Potential genetic improvement of cattle by fertilization of fetal oocytes in vitro. Jornal of Reproduction and Fertility. 38: 87-98.

Bristol-Gould S., Woodruff T.K. 2006. Folliculogenesis in the domestic cat (Felis catus). Theriogenology. 66(1): 5-13.

Brito I.R., Silva C.M.G., Duarte A.B.G., Lima I.M.T., Rodrigues G.Q., Rossetto R., Sales A.D., Lobo C.H., Bernuci M.P., Rosa-E-Silva A.C.J.S., Campello C.C., Xu M. & Figueiredo J.R. 2014. Alginate hydrogel matrix stiffness influences the in vitro development of caprine preantral follicles. Molecular Reproduction & Development. 81(7): 636-645.

Bruno J.B. 2006. Utilização de soro no cultivo in vitro de folículos pré-antrais caprinos. 66f. Fortaleza, CE. Dissertação (Mestrado em Ciências Veterinárias) - Programa de Pós-graduação em Ciências Veterinárias, Universidade Estadual do Ceará.

Bruno J.B., Celestino J.J., Lima-Verde I.B., Lima L.F., Matos M.H., Araújo V.R., Saraiva M.V., Martins F.S., Campello C.C. & Figueiredo J.R. 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. Reproduction, Fertility, and Development. 21(5): 679-687.

Bukovski A., Caudle M.R., Svetlikova M. & Upadhyaya N.B. 2004. Origin of germ cells and formation of new primary follicles in adult human ovaries. Reproduction Biology and Endocrinology. 2(20): 1-30.

Cárdenas H. & Pope W.F. 2002. Androgen receptor and follicle-stimulating hormone receptor in the pig ovary during the follicular phase of the estrous cycle. Molecular Reproduction and Development. 62(1): 92-98.

Casson P.R., Santoro N. Elkind-Hirsch K., Carson S.A., Hornsby P.J., Abraham G. & Buster J.E. 1998. Postmenopausal dehydroepiandrosterone administration increases free insulin-like growth factor-I and decreases high-density lipoprotein: a six-month trial. Fertility and Sterility. 70(1): 107-110.

Cato A.C.B. & Peterziel H. 1998. The androgen receptor as mediator of gene expression and signal transduction pathways. Trends in Endocrinology and Metabolism. 9(4): 150-154.

Chadha S., Pache T. D., Huikeshoven F. J. M., Brinkmann A. O. & Van der Kwast T. H. 1994. Androgen receptor expression in human ovarian and uterine tissue of long term androgen-treated transsexual women. Human Pathology. 25(11): 1198-1204.

Chaves R.N., Duarte A.B.G., Rodrigues G.Q., Celestino J.J.H., Silva G.M., Lopes C.A.P., Almeida A.P., Donato M.A.M., Peixoto C.A., Moura A.A.A., Lobo C.H., Locatelli Y., Mermillod P., Campello C.C. & Figueiredo J.R. 2012. The effects of insulin and follicle-stimulating hormone (FSH) during in vitro development of ovarian goat preantral follicles and relative mRNA expression for insulin and FSH receptors and cytochrome P450 aromatase in cultured follicles. Biology of Reproduction. 87(3): 69-80.

Cheng X.B., Jimenez M., Desai R., Middleton L.J., Joseph S.R., Ning G., Allan C.M., Smith J.T., Handelsman D.J. & Walters K.A. 2013. Characterizing the neuroendocrine and ovarian defects of androgen receptor-knockout female mice. American Journal of Physiology Endocrinology and Metabolism. 305(6): 717-726.

Compagnone N.A., Zhang P., Vigne J.L. & Mellon S.H. 2000. Novel role for the nuclear phosphoprotein SET in transcriptional activation of P450c17 and initiation of neurosteroidogenesis. Molecular Endocrinology. 14(6): 875-888.

Demeestere I., Centner J., Gervy Y. & Delbaere A. 2005. Impact of various endocrine and paracrine factors on culture of preantral follicles in rodents. Reproduction. 130(2): 147-156.

Demeestere I., Simon P., Emiliani S., Delbaere A. & Englert Y. 2007. Fertility preservation: Successful transplantation of cryopreserved ovarian tissue in a young patient previously treated for Hodgkin’s disease. Oncologist. 12(12): 1437-1442.

Detera-Wadleigh S.D. & Fanning T.G. 1994. Phylogeny of the steroid receptor superfamily. Molecular Phylogenetics and Evolution. 3(3): 192-205.

Dode M.A. & Graves C.N. 2003. Role of estradiol-17 on nuclear and cytoplasmic maturation of pig oocytes. Animal Reproduction Science. 78(1-2): 99-110.

Drummond A. E. 2006. The role of steroids in follicular growth. Reproductive Biology and Endocrinology. 4(16): 1-11.

Duarte A.B.G., Araújo V.R., Chaves R.N., Silva G.M., Magalhães-Padilha D.M., Satrapa R.A., Donato M.A.M., Peixoto C.A., Campello C.C., Matos M.H.T., Barros C.M. & Figueiredo J.R. 2011. Bovine dominant follicular fluid promotes the in vitro development of goat preantral follicles. Reproduction, Fertility, and Development. 24(3): 490-500.

Erickson G.F. 1986. An analysis of follicle development and ovum maturation. Semin Reproduction Endocrinology. 4(3): 233-254.

Fatehi R., Ebrahimi B., Shahhosseini M., Farrokhi A. & Fathi R. 2013. Effect of ovarian tissue vitrification method on mice preantral follicular development and gene expression. Theriogenology. 81(2): 302-308.

Faustino L.R., Rossetto R., Lima I.M., Silva C.M., Saraiva M.V., Lima L.F., Silva A.W., Donato M.A., Campello C.C., Peixoto C.A., Figueiredo J.R. & Rodrigues A.P. 2011. Expression of keratinocyte growth factor in goat ovaries and its effects on preantral follicles within cultured ovarian cortex. Reproductive Sciences. 18(12): 1222-1229.

Figueiredo J.R., Rodrigues A.P.R., Amorim C.A. & Silva J.R.V. 2008. Manipulação de oócitos inclusos em folículos ovarianos pré-antrais - MOIFOPA. In: Gonçalves P.B.D., Figueiredo J.R. & Freitas V.J.F. (Eds). Biotécnicas aplicadas à reprodução animal. 2.ed. São Paulo: Roca, pp.303-327.

Franks S. 1995. Polycystic ovary syndrome. New England Journal of Medicine. 333(13): 853-861.

Gilling-Smith C., Willis D.S., Beard R.W. & Franks S. 1994. Hypersecretion of androstenedione by isolated thecal cells from polycystic ovaries. Journal of Clinical Endocrinology and Metabolism. 79(4): 1158-1165.

Giometti I.C., Castilho A.C.S., Sá-Filho O.G., Papa P.C. & Buratini Jr. J. 2009. Controle local e endócrino do desenvolvimento e da regressão do corpo lúteo bovino. Revista Brasileira de Reprodução Animal. 33(1): 34-52.

Goodarzi M.O., Dumesic D.A., Chazenbalk G. & Azziz R. 2011. Polycystic ovary syndrome: etiology, pathogenesis and diagnosis. Nature Reviews Endocrinology. 7(4): 219-231.

Goyeneche A.A., Calvo V., Gibori G. & Telleria C.M. 2002. Androstenedione interfere in luteal regression by inhibiting apoptosis and stimulating progesterone production. Biology of Reproduction. 66(5): 1540-1547.

Hampton J.H., Manikkam M., Lubahn D.B., Smith M.F. & Garverick H.A. 2004. Androgen receptor mRNA expression in the bovine ovary. Domestic Animal Endocrinology. 27(1): 81-88.

He B., Kemppainen J.A., Voegel J.J., Gronemeyer H. & Wilson E.M. 1999. Activation function 2 in the human androgen receptor ligand binding domain mediates interdomain communication with the NH(2)-terminal domain. Journal of Biological Chemistry. 274(52): 37219-37225.

Heinlein C.A. & Chang C. 2002. Androgen receptor (AR) coregulators: an overview. Endocrinology Review. 23(2): 175-200.

Hild-Petito S., West N. B., Brenner R. M. & Stouffer R. L. 1991. Localization of androgen receptor in the follicle and corpus luteum of the primate ovary during the menstrual cycle. Biology of Reproduction. 44(3): 561-568.

Horie K., Takakura K., Imai K., Liao S. & Mori T. 1992. Immunohistochemical localization of androgen receptor in the human endometrium, decidua, placenta and pathological conditions of the endometrium. Human Reproduction. 7(10): 1461-1466.

Isachenko V., Isachenko E., Weiss J.M., Todorov P. & Kreienberg R. 2009. Cryobanking of human ovarian tissue for anti-cancer treatment: comparison of vitrification and conventional freezing. Cryoletters. 30(6): 449-454.

Jenster G. 1998. Coactivatiors and corepressors as mediators of nuclear receptor function: an update. Molecular and Cellular Endocrinology. 143(1-2): 1-7.

Johnson J., Bagley J., Skaznik-Wikiel M., Lee H.J., Adams G.B., Niikura Y., Tschudy K.S., Tilly J.C., Cortes M.L., Forkert R., Spitzer T., Iacomini J., Scadden D.T. & Tilly J.L. 2004. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 122(2): 303-315.

Juengel J.L., Heath D.A., Quirke L.D. & McNatty K.P. 2006. Oestrogen receptor α and β, androgen receptor and progesterone receptor mRNA and protein localization within the developing ovary and in small growing follicles of sheep. Reproduction. 131(1): 81-92.

Lenie S. & Smitz J. 2009. Functional AR signaling is evident in an in vitro mouse follicle culture bioassay that encompasses most stages of folliculogenesis. Biology of Reproduction. 80(4): 685-695.

Li M., Xue K., Ling J., Diao F.Y., Cui Y.G. & Liu J.Y. 2010. The orphan nuclear receptor NR4A1 regulates transcription of key steroidogenic enzymes in ovarian theca cells. Molecular and Cellular Endocrinology. 319(1-2): 39-46.

Lima-Verde I.B., Rosseto R. & Figueiredo J.R. 2011. Influência dos hormônios esteroides na foliculogênse. Revista Brasileira Reprodução Animal. 35(4): 472-482.

Lima-Verde I.B., Rossetto R., Matos M.H.T., Celestino J.J.H., Bruno J.B., Silva C.M.G., Faustino L.R., Mororó M.B.S., Araújo V.R., Campello C.C. & Figueiredo J.R. 2010. Androstenedione and follicle stimulating hormone involvement in the viability and development of goat preantral follicles in vitro. Animal Reproduction. 7(2): 80-89.

Loy C.J., Sim K.S. & Yong E.L. 2003. Filamin-A fragment localizes to the nucleus to regulate androgen receptor and coactivator functions. PNAS. 100(8): 4562-4567.

Lucci C.M., Amorim C.A., Báo S.N., Figueiredo J.R., Rodrigues A.P.R., Silva J.R. & Gonçalves P.B.D. 1999. Effect of the interval of serial sections of ovarian in the tissue chopper on the number of isolated caprine preantral follicles. Animal Reproduction Science. 56(1): 39-49.

Lucci C.M., Silva R.V., Carvalho C.A., Figueiredo J.R. & Báo S.N. 2001. Light microscopical and ultrastrutural characterization of goat preantral follicles. Small Ruminant Research. 41(1): 61-69.

Lunardi F.O., Araújo V.R., Faustino L.R., Carvalho A.A., Gonçalves R.F.B., Bass C.S., Báo S.N., Name K.P.O., Campello C.C., Figueiredo J.R. & Rodrigues A.P.R. 2012. Morphologic, viability and ultrastructural analysis of vitrified sheep preantral follicles enclosed in ovarian tissue. Small Ruminant Research. 107(3): 121-130.

Lunardi F.O., Chaves R.N., Lima L.F., Araújo V.R., Brito I.R., Souza C.E.A., Donato M.A.M., Peixoto C.A., Dinnyes A., Campello C.C., Figueiredo J.R. & Rodrigues A.P.R. 2015. Vitrified sheep isolated secondary follicles are able to grow and form antrum after a short period of in vitro culture. Cell and Tissue Research. 362(1): 241-251.

Luz V.B., Araújo V.R., Duarte A.B.G., Silva G.M., Chaves R.N., Brito I.R., Serafim M.K.B., Campello C.C., Feltrin C., Bertolini M., Almeida A.P., Santos R.R. & Figueiredo J.R. 2013. Kit ligand and insulin-like growth factor I affect the in vitro development of ovine preantral follicles. Small Ruminant Research. 115(2-3): 99-102.

Macaulay A.D., Hamilton C.K., King W. A. & Bartlewski P.M. 2013. Influence of physiological concentrations of androgens on the developmental competence and sex ratio of in vitro produced bovine embryos. Reproductive Biology. 13(1): 41-50.

Machelon V., Nome F. & Tesarik J. 1998. Nongenomic effects of androstenedione on human granulosa luteinizing cells. Journal of Clinical Endocrinology and Metabolism. 83(1): 263-269.

Magalhães D.M., Duarte A.B.G., Araújo V.R., Brito I.R., Soares T.G., Lima I.M.T., Lopes C.A.P., Campello C.C., Rodrigues A.P.R. & Figueiredo J.R. 2011. In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology. 75(1): 182-188.

Matos M.H.T., Van den Hurk R., Lima-Verde I.B., Luque M.C.A., Santos K.D.B., Martins F.S., Báo S.N., Lucci C.M. & Figueiredo J.R. 2007. Effects of fibroblast growth factor-2 on the in vitro culture of caprine preantral follicles. Cells Tissues Organs. 186(2): 112-120.

Mlodawska W. & Okolski A. 2014. Immunolocalization of androgen receptors and assessment of steroidogenic activity of the ovaries in prepubertal and pubertal mare. Journal of Equine Veterinary Science. 34(1): 113-114.

Montgomery J.S., Price D.K. & Figg W.D. 2001. The androgen receptor gene and its influence on the development and progression of prostate cancer. Journal of Pathology. 195(2):138-146.

Murayama C., Miyazaki H., Miyamoto A. & Shimizu T. 2012. Luteinizing hormone (LH) regulates production of androstenedione and progesterone via control of histone acetylation of StAR and CYP17 promoters in ovarian theca cells. Molecular and Cellular Endocrinology. 350(1): 1-9.

Murray A. A., Gosden R. G., Allison V. & Spears N. 1998. Effect of androgens on the development of mouse follicles growing in vitro. Journal of Reproduction and Fertility. 113(1): 27-33.

Murray A.A., Molinek M.D., Baker S.J., Kojima F.N., Smith M.F., Hillier S.G. & Spears N. 2001. Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro. Reproduction. 121(1): 89-96.

Narkwichean A., Jayaprakasan K., Maalouf W.E., Hernandez-Medrano J.H., Pincott-Allen C. & Campbell B.K. 2014. Effects of dehydroepiandrosterone on in vivo ovine follicular development. Human Reproduction. 29(1): 146-154.

O’brien M.J., Pendola J.K. & Eppig J.J. 2003. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biology of Reproduction. 68(5): 1682-1686.

O’malley B.W. & Tsai M.J. 1992. Molecular pathway of steroid receptor action. Biology of Reproduction. 46(2): 163-167.

Okutsu Y., Itoh M.T., Takahashi N. & Ishizuka B. 2010. Exogenous androstenedione induces formation of follicular cysts and premature luteinization of granulosa cells in the ovary. Fertility and Sterility. 93(3): 927-935.

Otala M., Makinen S., Tuuri T., Sjoberg J., Pentikainen V., Matikainen T. & Dunkel L. 2004. Effects of testosterone, dihydrotestosterone, and 17β-estradiol onhumanovarian tissue survival in culture. Fertility and Sterility. 82(3): 1077-1085.

Ozanne D.M., Brady M.E., Cook S., Gaughan L., Neal D.E. & Robson C.N. 2000. Androgen receptor nuclear translocation is facilitated by the f-actin cross-linking protein filamin. Molecular Endocrinology. 14(10): 1618-1626.

Pasquali R., Stener-Victorin E., Yildiz B.O., Duleba A.J., Hoeger K., Mason H., Homburg R., Hickey T., Franks S., Tapanainen J.S., Balen A., Abbott D.H., Diamati-Kandarakis E. & Legro R.S. 2011. PCOS Forum: research in polycystic ovary syndrome today and tomorrow. Clinical Endocrinology. 74(4): 424-433.

Pradeep P.K., Li X., Peegel H. & Menon K.M. 2002. Dihydrotestosterone inhibits granulosa cell proliferation by decreasing the cyclin D2 mRNA expression and cell cycle arrest at G phase. Endocrinology. 143(8): 2930-2935.

Prizant H., Gleicher N. & Sen A. 2014. Androgen actions in the ovary: balance is key. Journal of Endocrinology. 222(3): 141-151.

Ricarte A.R.F. & Silva A.R. 2010. Morfofisiologia da reprodução de caprinos: revisão. Acta Veterinaria Brasilica. 4(1): 8-13.

Rocha R.M.P., Lima L.F., Alves A.M.C.V., Celestino J.J.H., Matos M.H.T., Lima-Verde I.B., Bernuci M.P., Lopes C.A.P., Báo S.N., Campello C.C., Rodrigues A.P.R. & Figueiredo J.R. 2013. Interaction between melatonin and follicle-stimulating hormone promotes in vitro development of caprine preantral follicles. Domestic Animal Endocrinology. 44(1): 1-9.

Rodrigues G.Q., Silva C.M.G., Faustino L.R., Bruno J.B., Pinto L.C., Lopes C.A.P., Campello C.C. & Figueiredo J.R. 2010. Efeito de diferentes concentrações de hormônio folículo-estimulante recombinante sobre o desenvolvimento in vitro de folículos pré-antrais caprinos e ovinos isolados. Acta Veterinaria Brasileira. 4(3): 144-152.

Rodrigues J.K., Navarro P.A., Zelinski M.B., Stouffer R.L. & Xu J. 2015. Direct actions of androgens on the survival, growth and secretion of steroids and anti-Mullerian hormone by individual macaque follicle during three-dimensional culture. Human Reproduction. 30(3): 1-11.

Romero S. & Smitz J. 2010. Exposing cultured mouse ovarian follicles under increased gonadotropin tonus to aromatizable androgens influences the steroid balance and reduces oocyte meiotic capacity. Endocrinology. 38(2): 243-253.

Salvetti N.R., Alfaro N.S. & Velázquez M.M. 2012. Alteration in localization of steroid hormone receptors and coregulatory proteins in follicles from cows with induced ovarian follicular cysts. Reproduction. 144(6): 723-735.

Saraiva M.V.A., Celestino J.J.H., Araújo V.R., Chaves R.N., Almeida A.P., Lima-Verde I.B., Duarte A.B.G., Silva G.M., Martins F.S., Bruno J.B., Matos M.H.T., Campello C.C., Silva J.R.V. & Figueiredo J.R. 2010. Expression of follicle-stimulating hormone receptor (FSHR) in goat ovarian follicles and the impact of sequential culture medium on in vitro development of caprine preantral follicles. Zygote. 19(3): 205-214.

Sen A., Prizant H., Light A., Biswas A., Hayes E., Lee H.J., Barad D., Gleicher N. & Hammes S.R. 2014. Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. PNAS. 111(8): 3008-3013.

Shaw J.M., Oranratnachai A. & Trounson A.O. 2000. Fundamental cryobiology of mammalian oocytes and ovarian tissue. Theriogenology. 53(1): 59-72.

Silber S.J., DeRosa M., Pineda J., Lenahan K., Grenia D., Gorman K. & Gosden, R.G. 2008. A series of monozygotic twins discordant for ovarian failure: ovary transplantation (cortical versus microvascular) and cryopreservation. Human Reproduction. 23(7): 1531-1537.

Silva C.M.G. 2013. Utilização do hormônio luteinizante (LH), fator de crescimento epidermal (EGF) e ativina-A no cultivo in vitro de folículos pré-antrais caprinos isolados. 191f. Fortaleza, CE. Tese (Doutorado em Ciências Veterinárias) - Programa de Pós-graduação em Ciências Veterinárias, Universidade Estadual do Ceará.

Silva C.M.G., Castro S.V., Faustino L.R., Rodrigues G.Q., Brito I.R., Saraiva M.V.A., Rossetto R., Silva T.F.P., Campello C.C. & Figueiredo J.R. 2011. Moment of addition of LH to the culture medium improves in vitro survival and development of secondary goat pre-antral follicles. Reproduction in Domestic Animals. 46(4): 579-584. F.I: 1.151

Silva J.R.V., van den Hurk R., van Tol H.T.A., Roelen B.A.J. & Figueiredo J.R. 2004. Gene expression and protein localization for activin-A, follistatin and activin receptors in goat ovaries. Journal of Endocrinology. 183(1): 405-415.

Slomczynska M. & Tabarowski Z. 2001. Localization of androgen receptor and cytochrome P450 aromatase in the follicle and corpus luteum of the porcine ovary. Animal Reproduction Science. 65(1-2): 127-134.

Spears N., Murray A. A., Allison V., Boland N.I. & Gosden R.G. 1998. Role of gonadotropins and ovarian steroids in the development of mouse follicles in vitro. Journal of Reproduction and Fertility. 113(1): 19-26.

Suzuki T., Sasano H., Kimura N., Tamura M., Fukaya T., Yajima A. & Nagura H. 1994. Immunohistochemical distribution of progesterone, androgen and oestrogen receptors in the human ovary during the menstrual cycle: relationship to expression of steroidogenic enzymes. Human Reproduction. 9(9): 1589-1595.

Szoltys M. & Slomczynska M. 2000. Changes in distribution of androgen receptor during maturation of rat ovarian follicles. Experimental and Clinical Endocrinology & Diabetes. 108(3) 228-234.

Taketsuru H., Hirao Y., Takenouchi N., Kosuke I. & Miyano T. 2011. Effect of androstenedione on the growth and meiotic competence of bovine oocytes from early antral follicles. Zygote. 20(4): 407-415.

Taniguchi F., Couse J.F., Rodriguez K.F., Emmen J.M.A., Poirier D. & Korach K.S. 2007. Estrogen receptor-α mediates an intraovarian negative feedback loop on thecal cell steroidogenesis via modulation of Cyp17α1 (cytochrome P450, steroid 17α-hydroxylase/17,20 lyase) expression. FASEB J. 21(2): 586-595.

Tarumi W., Itoh M.T. & Suzuki N. 2014. Effects of 5α-dihydrotestosterone and 17β-estradiol on the mouse ovarian follicle development and oocyte maturation. PLoS ONE. 9(6): 1-7.

Tarumi W., Tsukamoto S., Okutsu Y., Takahashi N., Horiuchi T., Masanori T.I. & Ishizuka B. 2012. Androstenedione induces abnormalities in morphology and function of developing oocytes, which impairs oocyte meiotic competence. Fertility and Sterility. 97(2): 469-476.

Tasaki H., Iwata H., Sato D., Monjy Y. & Kuwayama T. 2013. Estradiol has a major role in antrum formation of porcine preantral follicles cultured in vitro. Theriogenology. 79(5): 809-814.

Telfer E.E., Mclaughlin M., Ding C. & Thong K.J. 2008. A two-step serum free culture system supports development of human oocytes from primordial follicles in the presence of activin. Human Reproduction. 23(5): 1151-1158.

Valdez K.E., Cuneo S.P., Gorden P.J. & Turzillo A.M. 2005. The role of thecal androgen production in the regulation of estradiol biosynthesis by dominant bovine follicles during the first follicular wave. Journal of Animal Science. 83(3): 597-603.

Van Den Hurk R. & Zhao J. 2005. Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology. 63(6): 1717-1751.

Vanacker J., Camboni A., Dath C., Langendonckt A.V., Dolmans M.M., Donnez J. & Amorim C.A. 2011. Enzymatic isolation of human primordial and primary ovarian follicles with Liberase DH: protocol for application in a clinical setting. Fertility Preservation. 96(2): 379-383.

Veldscholte J., Berrevoets C.A., Zegers N.D., van der Kwast T.H., Grootegoed J.A. & Mulder E. 1992. Hormoneinduced dissociation of the androgen receptor-heat-shock protein complex: use of a new monoclonal antibody to distinguish transformed from nontransformed receptors. Biochemistry. 31(32): 7422-7430.

Vendola K., Zhou J., Wang J. & Bondy C.A. 1999. Androgens promote insulin-like growth factor-I and insulin-like growth factor-I receptor gene expression in the primate ovary. Human Reproduction. 14(9): 2328-2332.

Walters K.A. 2015. Role of androgens in normal and pathological ovarian function. Reproduction and Fertility. 149(4): 193-218.

Walters K.A., Allan C.M. & Handelsman D.J. 2008. Androgen actions and the ovary. Biology of Reproduction. 78(3): 380-389.

Walters K.A., Middleton L.J., Joseph S.R., Hazra R., Jimenez M., Simanainen U., Allan C.M. & Handelsman D.J. 2012. Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Biology of Reproduction. 87(6): 151-162.

Wang R.S., Chang H.Y., Kao H.S., Kao C.H., Wu Y.C., Yeh S., Tzeng C.R. & Chang C. 2015. Abnormal mitochondrial function and impaired granulosa cell differentiation in androgen receptor knockout mice. International Journal of Molecular Sciences. 16(5): 9831-9849.

Weil S., Vendola K., Zhou J. & Bondy C.A. 1999. Androgen and follicle-stimulating hormone interactions in primate ovarian follicle development. Journal of Clinical Endocrinology. 84(8): 2951-2956.

Wu Y.G., Bennett J., Talla D. & Stocco C. 2011. Testosterone, not 5α-Dihydrotestosterone, stimulates LRH-1 leading to FSH-independent expression of Cyp19 and P450scc in granulosa cells. Molecular Endocrinology. 25(4): 656-668.

White Y.A.R., Woods D.C., Ishihara Y.T.O., Seki H. & Tilly. J.L. 2012. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nature Medicine. 18(3): 413-421.

Xu B., Gao L., Cui Y., Gao L., Dai X., Li M., Zhang Y., Ma X., Diao F. & Liu J. 2013. SET protein up-regulated testosterone production in the cultured preantral follicles. Reproductive Biology and Endocrinology. 11(9): 1-7.

Yang M.Y. & Fortune J.E. 2006. Testosterone stimulates the primary to secondary follicle transition in bovine follicles in vitro. Biology of Reproduction. 75(6): 924-932.

Yazawa T., Kawabe S., Kanno M., Mizutani T., Imamichi Y., Ju Y., Matsumura T., Yamazaki Y., Usami Y., Kuribayashi M., Shimada M., Kitano T., Umezawa A. & Miyamoto K. 2013. Androgen/androgen receptor pathway regulates expression of the genes for cyclooxygenase-2 and amphiregulin in periovulatory granulosa cells. Molecular and Cellular Endocrinology. 369(1-2): 42-51.

Zeleznik A.J., Little-Ihrig L. & Ramasawamy S. 2004. Administration of dihydrotestosterone to rhesus monkeys inhibits gonadotropin-stimulated ovarian steroidogenesis. Journal of Clinical Endocrinology and Metabolism. 89(2): 860-866.

Zou K., Yuan Z., Yang Z., Luo H., Sun K., Zhou L., Xiang J., Shi L., Yu Q., Zhang Y., Hou R. & Wu J. 2009. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nature Cell Biology. 11(5): 631-636.

Published

2016-01-01

How to Cite

Apolloni, L. B., Bruno, J. B., Alves, B. G., & Figueiredo, J. R. de. (2016). The Role of Androgens in Mammals Folliculogenesis. Acta Scientiae Veterinariae, 44(1), 15. https://doi.org/10.22456/1679-9216.81075

Issue

Section

Articles

Most read articles by the same author(s)