Expression of the aromatase cytochrome p450 enzyme, α and β estrogen receptors, and androgens in cells of the spermatogenic lineage, Leydig and Sertoli of Hydrochoerus hydrochaeris (Linnaeus, 1766)
DOI:
https://doi.org/10.5380/avs.v29i3.94273Palavras-chave:
Capybara, Reproduction, Spermatogenesis, Androgen, EstrogenResumo
Capybaras (Hydrochoerus hydrochaeris) are the biggest rodents in the world and have a huge importance in conservation, can be a rodent model in reproduction and have a huge role in the food chain in South America. Molecular studies of the reproduction of this animal are important for all animal class conservation, mainly rodents. In this way, hormone signaling can be useful to understand external and internal mechanisms of reproduction. In this work, estrogen receptors α and β, aromatase cytochrome P450 enzyme, and androgens were detected by immunohistochemistry on Leydig cells, Sertoli cells, myoid cells, and seminiferous epithelium H. hydrochaeris testis. Nine animals were sacrificed and it was collected the testicles, and for each staining (hematoxylin and eosin, Mallory, and immunohistochemistry for four antibodies) it was made 5 slides per animal, after that a qualitative analysis was performed. The presence of estrogen receptors α and β in germinal epithelial cells, with stronger expression in spermatogonia and spermatocytes, may indicate the action of these hormones in the initial process of sperm cell development, needing more studies to investigate this first evidence. In other animals is believed that the aromatase cytochrome P450 enzyme can promote the transformation of androgens into estrogen, and in H. hydrochaeris is observed in those cells and androgen receptors. Sertoli cells exhibited moderate immunostaining for androgen and estrogen receptors α and β in the cytoplasm, with poor labeling for the aromatase cytochrome P450 enzyme in the nucleus in H. hydrochaeris. It is suggested that Sertoli cells may be responsible for producing estrogen in adult animals.
Referências
Alvarez RM. Criação em cativeiro de capivaras na Venezuela, R. Bras. Zootec. 40:44-47, 2011.
Berensztein EB, Baquedano MS, Gonzalez CR, Saraco NI, Rodriguez J, Ponzio R, Rivarola M, Belgorosky A. Expression of Aromatase, Estrogen Receptor α and β, Androgen Receptor, and Cytochrome P-450scc in the Human Early Prepubertal Testis. Pediatr Res. 60(6):740–744, 2006. https://doi.org/10.1203/01.pdr.0000246072.04663.bb
Bonagura TW, Zhou H, Babischkin JS, Pepe GJ, Albrecht ED. Expression of P-450 aromatase, estrogen receptor α and β, and α-inhibin in the
fetal baboon testis after estrogen suppression during the second half of gestation. Endocrine. 2011. 39(1):75-82. https://doi.org/10.1007/s12020-010-9414-5
Bremner WJ, Millar MR, Sharpe RM, Saunders PT. Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens. Endocr, 1994. 135(3): 1227-1234. https://doi.org/10.1210/endo.135.3.8070367
Carreau S, Bois C, Zanatta L, Silva FRMB, Bouraima-Lelong H, Delalande C, Estrogen signaling in testicular cells. Life Sci.;89:584–587, 2011. https://doi.org/10.1016/j.lfs.2011.06.004
Carreta Júnior M. Estudo comparativo do processo espermatogênico e duração do ciclo do epitélio seminífero através da técnica de imunoistoquímica com bromodeoxiuridina de três diferentes espécies de roedores da subordem Hystricomorfa: Cutia (Dasyprocta leporina), paca (Cuniculus paca), capivara (Hydrochoerus hydrochaeris). [Tese]. Viçosa: Universidade Federal de Viçosa, 2012.
Cooke, PS; Walker WH, Male fertility in mice requires classical and nonclassical androgen signaling. Cell Reports. Volume 36, Issue 7, 109557, 2021. https://doi.org/10.1016/j.celrep.2021.109557
Delbès G, Levacher C, Pairault C, Racine C, Duquenne C, Krust A, Habert1er R. ß-mediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endo.145(7):3395-403. 2004. https://doi.org/10.1210/en.2003-1479
Dewaele, A; Dujardin, E; André, M; Albina, A; Jammes, H; Giton, F; Sellem, E; Jolivet, G; Pailhoux, E; Pannetier, M,. Absence of Testicular Estrogen Leads to Defects in Spermatogenesis and Increased Semen Abnormalities in Male Rabbits. Genes (Basel). Nov 8;13(11):2070, 2022. https://doi.org/10.3390/genes13112070
França LR, Hess RA, Dufour JM, Hofmann MC, Griswold MD. The Sertoli cell: one hundred fifty years of beauty and plasticity. Andrology, 2016. 4:189–212. https://doi.org/10.1111/andr.12165
Gadda, TMC, Souza, JMT, Paula, GAR, Van Kaick, TS, Gervásio, JHDB. The International Biodiversity Agenda at the Local Level: the Case of Capybaras in Curitiba, Brazil. Ambiente & Sociedade, 24, 2021. https://doi.org/10.1590/1809-4422asoc20180283r2vu2021L1AO
Galuszka A, Pawlicki P, Pardyak L, Chmurska-Gąsowska M, Pietsch-Fulbiszewska A, Duliban M, Turek W, Dubniewicz K, Ramisz G, Kotula-Balak M, Abundance of estrogen receptors involved in non-canonical signaling in the dog testis. Anim Reprod Sci., 2021. doi: 10.1016/j.anireprosci.2021.106888.
Gould ML, Hurst PR, Nicholson HD. The effects of oestrogen receptors A and B on testicular cell number and steroidogenesis in mice. Reproduction, 2007. 134:271–279. https://doi.org/10.1530/REP-07-0025
Guimarães LC, Rodrigues FHG, Scotti MR. Strategies for herbivory mitigation by capybaras Hydrochoerus hydrochaeris in a riparian forest under restoration in the São Francisco river basin Brazil, Wildlife Biol., 20:136–144, 2014. https://doi.org/10.2981/wlb.13065
Hess, RA; Sharpe, RM; Hinton, BT. Estrogens and Development of the Rete Testis, Efferent Ductules, Epididymis and Vas Deferens. Differentiation, 118, 41–71, 2021. https://doi.org/10.1016/j.diff.2020.11.004
Kamińska, A, Marek, S, Pardyak, L, Brzoskwinia M, Pawlicki P, Bilinska B, Hejmej A. Disruption of androgen signaling during puberty affects Notch pathway in rat seminiferous epithelium. Reprod Biol Endocrinol 18, 30, 2020. https://doi.org/10.1186/s12958-020-00582-3
Lin J, Zhu J, Li X, Li S, Lan Z, Ko J, Lei Z. Expression of Genomic Functional Estrogen Receptor 1 in Mouse Sertoli Cells. Reprod Sci. 21(11):1411–1422, 2014. https://doi.org/10.1177/1933719114527355
Lucas TFG, Pimenta MT, Pisolato R, Lazari MFM, Porto CS. 17β-estradiol Signaling and Regulation of Sertoli Cell Function. Spermatogenesis. 1(4):318-324, 2011. https://doi.org/10.4161/spmg.1.4.18903
Lucas TFG, Siu ER, Esteves CA, Monteiro HP, Oliveira CA, Porto CS, Lazari MFM. 17Beta-Estradiol Induces the Translocation of the Estrogen Receptors ESR1 and ESR2 to the Cell Membrane, MAPK3/1 Phosphorylation and Proliferation of Cultured Immature Rat Sertoli Cells. Biol Reprod. 78:101–114, 2008. https://doi.org/10.1095/biolreprod.107.063909
Madhabananda S, Dennis B, Lubahn FS, Wilson FEM. Immunohistochemical Localization of the Androgen Receptor in Rat and Human Tissues. Endocr. 1990. 127(6): 3180-3186. https://doi.org/10.1210/endo-127-6-3180
Miranda, LB. Aspectos morfofisiológicos do aparelho genital masculino de capivara (Hydrochoerus hydrochaeris), Botucatu- SP, 2003. Doi: 10.11606/D.10.2003.tde-06082007-100037
Mutembei HM, Pesch S, Schuler G, Hoffmann B. Expression of Oestrogen Receptors a and b and of Aromatase in the Testis of Immature and Mature Boars. Reprod Dom Anim. 40:228–236, 2005. https://doi.org/10.1111/j.1439-0531.2005.00586.x
Nie R, Zhou Q, Jassim E, Saunders TKP, Hess RA. Differential Expression of Estrogen Receptors a and b in the Reproductive Tracts of Adult Male Dogs and Cats, Biol Reprod. 66:1161–1168, 2002. https://doi.org/10.1095/biolreprod66.4.1161
Nittat H, Bunick D, Hess RA, Janulis L, Newton SC, Millette CF, Osawa C, Shizuta Y, Toda K, Bahr JM. Germ Cells of the Mouse Testis Express P450 Aromatase. Endo. 132(3):1396-401, 1993. doi: 10.1210/endo.132.3.8440194.
Nogueira-Filho SLG, Nogueira SSC. Criação Comercial de Animais Silvestres: Produção e Comercialização da Carne e de Subprodutos na Região Sudeste do Brasil. Rev. Econ. Nordeste.; 31:188-195, 2000.
O'Shaughnessy PJ. Hormonal control of germ cell development and spermatogenesis. Seminars in Cell & Developmental Biology. 29:55-65. https://doi.org/10.1016/j.semcdb.2014.02.010
Paula TAR, Costa DS, da Matta SLP. Avaliação histológica quantitativa do testículo de capivaras (Hydrochoerus hydrochaeris) adultas. Biosci. J.; 18(1). 2006.
Pearl, CA, Mason H, Roser JF. Immunolocalization of estrogen receptor alpha, estrogen receptor beta, and androgen receptor in the pre-, peri- and post-pubertal stallion testis, Anim Reprod Sci. 125:103– 111, 2011.
Pelletier G, Labrie C, Labrie F. Localization of oestrogen receptor α, oestrogen receptor β, and androgen receptors in the rat reproductive organs. J Endo.;165:359–370, 2000. https://doi.org/10.1677/joe.0.1650359
Rago V, Maggiolini M, Vivacqua A, Palma A, Carpino A. Differential Expression of Estrogen Receptors (ERα/ERβ) in Testis of Mature and Immature Pigs. Anat Rec. 281A:1234–1239, 2004. https://doi.org/10.1002/ar.a.20131
Rinaldi RA. Ecologia de Capivaras (Hydrochoerus hydrochaeris, Linnaeus, 1766) em região alterada pela formação de um reservatório hidrelétrico. [Dissertação]. Curitiba-PR: UFPR, 2014.
Rodrigues MN, Oliveira GB, Albuquerque JFG, Menezes DJA, Assis Neto AC, Miglino MA, Oliveira MF. Aspectos anatômicos do aparelho genital masculino de preás adultos (Galea spixii Wagler, 1831), Biotemas, 2013. 26:181-188. https://doi.org/10.5007/2175-7925.2013v26n1p181
Schlatta S, Ehmcke J. Regulation of spermatogenesis: An evolutionary biologist’s perspective. Semin Cell Dev Biol.;29:2–16, 2014. https://doi.org/10.1016/j.semcdb.2014.03.007
Schulster M, Bernie AM, Ramasamy R. The role of estradiol in male reproductive function. Asian J. Androl.;18:435–440, 2016. doi: 10.4103/1008-682X.173932
Simpson ER, Mahendroof MS, Means GD, Kilgoref MW, Hinshelwoodf MM, Lorence SG, Amarneh B, Ito Y, Fisher CR, Michael MD, Mendelson CR, Bulun SE. Aromatase Cytochrome P450, The Enzyme Responsible for Estrogen Biosynthesis. Endocr. Rev. 15(3):342-355, 1994. https://doi.org/10.1210/edrv-15-3-342
Silva SFM, Silva CHS, Dias FCR, Cordero-Schmidt E, Vargas-Mena JC, Silva IGM, Bao SN, Carvalho TG, Araujo Junior RF, Moura CEBM, Melo FCSA, Matta SLP, Morais DB. Testicular characterization and spermatogenesis of the hematophagous bat Diphylla ecaudata. Plos One, 14(12): e0226558, 2019. https://doi.org/10.1371/journal.pone.0226558
Sipahutar H, Sourdaine P, Moslemi S, Plainfossé B, Séralini GE. Immunolocalization of Aromatase in Stallion Leydig Cells and Seminiferous Tubules. J Histochem Cytochem. 51(3):311–318, 2003. https://doi.org/10.1177/002215540305100306
Smith LB, Walker WH. Hormone Signaling in the Testis. In: Plant TM, Zeleznik AJ. In: Knobil and Neill’s Physiology of Reproduction. Elsevier Inc; 4ª ed. San Diego, CA, USA. pp. 637–690, 2015.
Soto CF. Efecto de un inhibidor de la aromatasa sobre la espermatogénesis, la conducta sexual y la fertilidad de la rata macho adulta. [Tese] Distrito Federal- México, 2012. https://doi.org/10.24275/uami.jm214p21q
Srisuwatanasagul K, Prapaiwan N, Srisuwatanasagul S, Kunavongkrit A, Roongsitthichai A. Immunohistochemical study of Ki-67 protein, androgen receptor, and estrogen receptor beta in testicular tissues of male pigs immunocastrated with different times of GnRH vaccination. Anat Histol Embryol, 2018. Oct;47(5):475-480. doi: 10.1111/ahe.12386.
Sugita N, Choijookhuu N, Yano K, Lee D, Ikenoue M, Fidya, Taniguchi N, Chosa E, Hishikawa Y. Depletion of high-mobility group box 2 causes seminiferous tubule atrophy via aberrant expression of androgen and estrogen receptors in mouse testis. Biol Reprod. Dec 20;105(6):1510-1520, 2021. doi: 10.1093/biolre/ioab187.
Van Pelt AM, Rooij DG, Van der Burg B, Van der Saag PT, Gustafsson JA, Kuiper GG. Ontogeny of estrogen receptor-beta expression in rat testis. Endocrinology. 140(1):478-83, 1999. https://doi.org/10.1210/endo.140.1.6438
Walker HW. Testosterone signaling and the regulation of spermatogenesis, Spermatogenesis.;1(2):116-120, 2011. https://doi.org/10.4161/spmg.1.2.16956
Yan HHN, Mruk DD, Lee WM, Cheng CY. Blood-testis barrier dynamics are regulated by testosterone and cytokines via their differential effects on the kinetics of protein endocytosis and recycling in Sertoli cells. Faseb J.2(22):1945-1959, 2008. https://doi.org/10.1096/fj.06-070342
Zhou Q, Nie R, Prins GS, Saunders TKP, Katzenellenbogen BS, Hess RA. Localization of Androgen and Estrogen Receptors in Adult Male Mouse Reproductive Tract. J Androl. 23(6):870-881, 2002. https://doi.org/10.1002/j.1939-4640.2002.tb02345.x
Zhou X, Kudo A, Kawakami H, Hirano H. Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development. Anat Rec. 245, 509-518, 1996. https://doi.org/10.1002/(SICI)1097-0185(199607)245:3<509::AID-AR7>3.0.CO;2-M.
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