Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The dynamic equilibrium between spermatogonial proliferation and testicular apoptosis determines the progression of spermatogenesis in amphibians. Estrogens and their receptors play a central role in regulating spermatogenesis in vertebrates, and in some species of anurans, estradiol (E2) is involved in the regulation of spermatogonial proliferation and apoptosis of germ cells. Bidder's organ (BO) is a structure characteristic of Bufonidae that has historically been compared to an undeveloped ovary. In adult Rhinella arenarum males, BO is one of the main sources of plasma E2. The aim of this study was 1) to describe the seasonal variations in testicular apoptosis, spermatogonial proliferation, and cellular proliferation in BO; and 2) to analyze the presence and localization of estrogen receptor β (ERβ) in the testes and BO of R. arenarum. Testicular fragments and BOs from animals collected during the year were labeled with 5-bromo-2′-deoxyuridine (BrdU) and BrdU incorporation was determined using immunohistochemistry. Apoptosis in testicular sections was detected using the TUNEL method, and ERβ localization was assessed using immunohistochemistry in testes and BOs. The results indicate that spermatogonial proliferation is highest during the reproductive season and that cysts of spermatocytes and spermatids undergo apoptosis during the postreproductive season. Furthermore, the proliferation of follicular cells is highest during the reproductive and postreproductive seasons. ERβ was primarily detected by immunolocalization in Sertoli cells, follicular cells, and oocytes. Taken together, these results suggest that cysts that do not form spermatozoa are removed from testes by apoptosis and that estrogens regulate both spermatogenesis and oogenesis in adult males of R. arenarum. © 2016 Wiley Periodicals, Inc.

Registro:

Documento: Artículo
Título:Apoptosis, proliferation and presence of estradiol receptors in the testes and Bidder's organ of the toad Rhinella arenarum (Amphibia, Anura)
Autor:Scaia, M.F.; Czuchlej, S.C.; Cervino, N.; Ceballos, N.R.
Filiación:Laboratorio De Endocrinología Comparada, Departamento De Biodiversidad Y Biologia Experimental, Facultad De Ciencias Exactas Y Naturales, Universidad De Buenos Aires, Consejo Nacional De Investigaciones Cientificas Y Técnicas, Buenos Aires, Argentina
Palabras clave:Amphibians; Bufonidae; Estrogens; Reproduction; Spermatogenesis; estradiol receptor; estrogen receptor beta; anatomy and histology; animal; apoptosis; Bufonidae; cell proliferation; cytology; male; metabolism; physiology; Sertoli cell; spermatogenesis; testis; Animals; Apoptosis; Bufonidae; Cell Proliferation; Estrogen Receptor beta; Male; Receptors, Estradiol; Sertoli Cells; Spermatogenesis; Testis
Año:2016
Volumen:277
Número:4
Página de inicio:412
Página de fin:423
DOI: http://dx.doi.org/10.1002/jmor.20507
Título revista:Journal of Morphology
Título revista abreviado:J. Morphol.
ISSN:03622525
CODEN:JOMOA
CAS:Estrogen Receptor beta; Receptors, Estradiol
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03622525_v277_n4_p412_Scaia

Referencias:

  • Burgos, M.H., Mancini, R.E., Ciclo espermatogénico anual del Bufo arenarum (1948) Hensel Rev Soc Arg Biol, 24, pp. 328-336
  • Caneguim, B.H., Luz, J.S., Valentini, S.R., Cerri, P.S., Sasso-Cerri, E., Immunoexpression of aromatase and estrogen receptors in stem spermatogonia of bullfrogs indicates a role of estrogen in the seasonal spermatogonial mitotic activity (2013) Gen Comp Endocrinol, 182, pp. 65-72
  • Canosa, L.F., Pozzi, A.G., Ceballos, N.R., Pregnenolone and progesterone metabolism by the testes of Bufo arenarum (1998) J Comp Physiol B, 168, pp. 491-496
  • Canosa, L.F., Ceballos, N.R., Effects of different steroid-biosynthesis inhibitors on the testicular steroidogenesis of the toad Bufo arenarum (2001) J Comp Physiol B, 171, pp. 519-526
  • Canosa, L.F., Ceballos, N.R., Seasonal changes in testicular steroidogenesis in the toad Bufo arenarum H (2002) Gen Comp Endocrinol, 125, pp. 426-434
  • Canosa, L.F., Pozzi, A.G., Rosemblit, C., Ceballos, N.R., Steroid production in toads (2003) J Steroid Biochem Mol Biol, 85, pp. 227-233
  • Chieffi, P., Minucci, S., Cobellis, G., Fasano, S., Pierantoni, R., Changes in proto oncogene activity in the testis of the frog, Rana esculenta, during the annual reproductive cycle (1995) Gen Comp Endocrinol, 99, pp. 127-136
  • Chieffi, P., Franco, R., Fulgione, D., Staibano, S., PCNA in the testis of the frog, Rana esculenta: A molecular marker of the mitotic testicular epithelium proliferation (2000) Gen Comp Endocrinol, 119, pp. 11-16
  • Chieffi, P., Colucci-D'Amato, G.L., Staibano, S., Franco, R., Tramontano, D., Estradiol-induced mitogen activated protein kinase (extracellular signal-regulated kinase 1 and 2) activity in the frog (Rana esculenta) testis (2000) J Endocrinol, 167, pp. 77-84
  • Cobellis, G., Pierantoni, R., Minucci, S., Pernas-Alonso, R., Meccariello, R., Fasano, S., C-fos activity in Rana esculenta testis: Seasonal and estradiol-induced changes (1999) Endocrinology, 140, pp. 3238-3244
  • Colombo, L., Colombo Belvedere, P., Steroid hormone biosynthesis by male Bidder's organs of the toad Bufo bufo bufo (1980) Gen Comp Endocrinol, 40, pp. 320-321
  • Duellman, W.E., Trueb, L., (1994) Biology of Amphibians, , New York: McGraw-Hill
  • Fan, W., Yanase, T., Morinaga, H., Gondo, S., Okabe, T., Nomura, M., Komatsu, T., Nawata, H., Atrazine-induced aromatase expression is SF-1 dependent: Implications for endocrine disruption in wildlife and reproductive cancers in humans (2007) Environ Health Perspect, 115, pp. 720-727
  • Fasano, S., Minucci, S., Di Matteo, L., D'Antonio, M., Pierantoni, R., Intratesticular feedback mechanisms in the regulation of steroid profiles in the frog, Rana esculenta (1989) Gen Comp Endocrinol, 75, pp. 335-342
  • Fernández Solari, J.J., Pozzi, A.G., Ceballos, N.R., Seasonal changes in the activity of cytochrome P450 c17 from the testis of Bufo arenarum (2002) J Comp Physiol, 172, pp. 685-690
  • Ferrara, D., Palmiero, C., Branco, M., Pierantoni, R., Minucci, S., Testicular activity of Mos in the frog, Rana esculenta: A new role in spermatogonial proliferation (2004) Biol Reprod, 70, pp. 1782-1789
  • Freitas, J.S., Franco-Belussi, L., De Oliveira, C., Morphological and histochemical studies of Biddeŕs organ in Rhinella schneideri (Amphibia: Anura) males (2015) Ital J Zool 82:479-488.
  • Galas, J., Slomczynska, M., Pierscinski, A., Effect of photoperiod on the distribution patterns of androgen receptors and steroid hormone concentrations in ovaries of bank voles (2003) Acta Histochem, 105, pp. 175-181
  • Gentz, E.J., Medicine and surgery of amphibians (2007) Ilar J, 48, pp. 255-259
  • Ghosh, P.K., Gosh, A.K., Biswas, N.M., Effect of cadmium chloride on steroidogenic enzymes in the Bidder's organ of the toad (Bufo melanostictus) (1984) Experientia., 40, pp. 91-92
  • Hayes, T., Haston, K., Tsui, M., Hoang, A., Haeffele, C., Vonk, A., Herbicides: Feminization of male frogs in the wild (2002) Nature, 419, pp. 895-896
  • Hayes, T.B., Collins, A., Lee, M., Mendoza, M., Noriega, N., Stuart, A.A., Vonk, A., Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses (2002) Proc Natl Acad Sci USA, 99, pp. 5476-5480
  • Hayes, T.B., Khoury, V., Naravan, A., Nazir, M., Park, A., Brown, T., Adame, L., Gallipeau, S., Atrazine induces complete femilization and chemical castration in male African clawed frogs (Xenopus laevis) (2010) Proc Natl Acad Sci USA, 107, pp. 4612-4617
  • Lofts, B., Reproduction (1974) Physiology of the Amphibian, pp. 107-218. , In: Lofts B, editor. . New York: Academic Press
  • Lofts, B., Testicular function (1987) Hormones and Reproduction in Fishes, Amphibians, and Reptiles, pp. 283-325. , In: Norris DO, Jones RE, editors. . New York: Plenum Press
  • McCoy, K.A., Bortnick, L.J., Campbell, C.M., Hamlin, H.J., Guillette, L.J., St Marry, C.M., Agriculture alters gonadal form and function in the toad Bufo marinus (2008) Environ Health Perspect, 116, pp. 1526-1532
  • Minucci, S., Di Matteo, L., Chieffi, P., Pierantoni, R., Fasano, S., 17 β - estradiol effects on mast cell number and spermatogonial mitotic index in the testis of the frog, Rana esculenta (1997) J Exp Zool, 278, pp. 93-100
  • Pancak-Roessler, M.K., Norris, D.O., The effects of orchidectomy and gonadotropins on steroidogenesis and oogenesis in Biddeŕs Organs of the toad Bufo woodhousii (1991) J Exper Zool, 260, pp. 323-336
  • Pudney, J., Spermatogenesis in nonmammalian vertebrates (1995) Microsc Res Tech, 32, pp. 459-497
  • Rastogi, R.K., Iela, L., Saxena, P.K., Chieffi, G., The control of spermatogenesis in the green frog, Rana esculenta (1976) J Exp Zool, 196, pp. 151-166
  • Raucci, F., Di Fiore, M.M., The c-kit receptor protein in the testis of green frog Rana esculenta: seasonal changes in relationship to testosterone titres and spermatogonial proliferation (2007) Reproduction, 133, pp. 51-60
  • Ricote, M., Alfaro, J.M., García-Tuñón, I., Arenas, M.I., Fraile, B., Paniagua, R., Royuela, M., Control of the annual testicular cycle of the marbled-newt by p53, 21, and Rb gene products (2002) Mol Reprod Dev, 32, pp. 202-209
  • Sasso-Cerri, E., Faria, F.P., Freymüller, E., Miraglia, S.M., Testicular morphological changes during the seasonal reproductive cycle of the bullfrog Rana catesbeiana (2004) J Exp Zool, 301, pp. 249-260
  • Sasso-Cerri, E., Cerri, P.S., Freymüller, E., Miraglia, S.M., Apoptosis during the seasonal spermatogenic cycle of Rana catesbeiana (2006) J Anat, 209, pp. 21-29
  • Scaia, M.F., Regueira, E., Sassone, A.G., Volonteri, M.C., Ceballos, N.R., The Biddeŕs organ of the toad Rhinella arenarum (Amphibia, Anura). Presence of steroidogenic enzymes (2011) J Exp Zool A, 15, pp. 439-446
  • Scaia, M.F., Regueira, E., Volonteri, M.C., Ceballos, N.R., Estradiol production by the Biddeŕs organ of the toad Rhinella arenarum (Amphibia, Anura). Seasonal variations in plasma estradiol (2013) J Exp Zool A, 319, pp. 355-364
  • Scaia, M.F., Volonteri, M.C., Czuchlej, S.C., Ceballos, N.R., Effect of estradiol on apoptosis, proliferation and steroidogenic enzymes in the testes of the toad Rhinella arenarum (Amphibia, Anura) (2015) Gen Comp Endocrinol, 221, pp. 244-254
  • Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis (2012) Nat Methods, 9, pp. 671-675
  • Smita, M., Beyo, R.S., George, J.M., Akbarsha, M.A., Oommen, O.V., Seasonal variation in spermatogenic and androgenic activities in a caecilian testis (Ichthyophis tricolor) (2005) J Zool Lond, 267, pp. 45-53
  • Stabile, V., Russo, M., Chieffi, P., 17 beta - estradiol induces Akt-1 through estrogen receptor-beta in the frog (Rana esculenta) male germ cells (2006) Reproduction, 132, pp. 477-484
  • Tsai, P.-S., Lunden, J.B., Jones, J.T., Effects of steroid hormones on spermatogenesis and GnRH release in male Leopard frogs, Rana pipiens (2003) Gen Comp Endocrinol, 134, pp. 330-338
  • Van Oordt, P.G.W.J., The influence of the internal and external factors in the regulation of the spermatogenic cycle in amphibia (1960) Zool Soc Lond Symp, 2, pp. 29-52
  • Varriale, B., Pierantoni, R., Di Matteo, L., Minucci, S., Fasano, S., D'Antonio, M., Chieffi, G., Plasma and testicular estradiol and plasma androgen profile in the male frog Rana esculenta during the annual cycle (1986) Gen Comp Endocrinol, 64, pp. 401-404
  • Wake, M.H., Evolutionary morphology of the caecilian urogenital system. I. The gonads and the fat bodies (1969) J Morphol, 126, pp. 191-331
  • Yazawa, T., Yamamoto, K., Kikuyama, S., Abé, S.I., Elevation of plasma prolactin concentrations by low temperature is the cause of spermatogonial cell death in the newt, Cynops pyrrhogaster (1999) Gen Comp Endocrinol, 113, pp. 302-311
  • Zhao, Y., Yang, D., Zhang, Y., Liu, S.-S., Li, D.-D., Li, S.-F., Yan, Y.-Q., Comparison of estradiol receptor β expression in the ovary of mice and pigs (2008) Acta Anat Sin, 39, pp. 747-750

Citas:

---------- APA ----------
Scaia, M.F., Czuchlej, S.C., Cervino, N. & Ceballos, N.R. (2016) . Apoptosis, proliferation and presence of estradiol receptors in the testes and Bidder's organ of the toad Rhinella arenarum (Amphibia, Anura). Journal of Morphology, 277(4), 412-423.
http://dx.doi.org/10.1002/jmor.20507
---------- CHICAGO ----------
Scaia, M.F., Czuchlej, S.C., Cervino, N., Ceballos, N.R. "Apoptosis, proliferation and presence of estradiol receptors in the testes and Bidder's organ of the toad Rhinella arenarum (Amphibia, Anura)" . Journal of Morphology 277, no. 4 (2016) : 412-423.
http://dx.doi.org/10.1002/jmor.20507
---------- MLA ----------
Scaia, M.F., Czuchlej, S.C., Cervino, N., Ceballos, N.R. "Apoptosis, proliferation and presence of estradiol receptors in the testes and Bidder's organ of the toad Rhinella arenarum (Amphibia, Anura)" . Journal of Morphology, vol. 277, no. 4, 2016, pp. 412-423.
http://dx.doi.org/10.1002/jmor.20507
---------- VANCOUVER ----------
Scaia, M.F., Czuchlej, S.C., Cervino, N., Ceballos, N.R. Apoptosis, proliferation and presence of estradiol receptors in the testes and Bidder's organ of the toad Rhinella arenarum (Amphibia, Anura). J. Morphol. 2016;277(4):412-423.
http://dx.doi.org/10.1002/jmor.20507