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In anurans, two types of gonadotropins were described in several species of Ranidae and Pipidae families but only in one of the Bufonidae family. Rhinella arenarum is a bufonid that have the lowest concentration of plasma androgens during the breeding. The objective of this paper was to characterize the cDNA sequence of β subunit of LH and FSH from toad pituitary and study seasonal variation in gonadotropins mRNA using quantitative real-time RT-PCR. The LHβ cDNA is a 636. bp sequence containing an open reading frame (ORF), 45. bp of 5'-untranslated region (UTR) and 174. bp of 3'-UTR. The ORF encodes for a signal peptide of 26 amino acids and a mature protein of 113 amino acids with one N-glycosylation site at the 34th position. The FSHβ cDNA sequence is a 535. bp fragment containing an ORF, 8. bp of 5'-UTR and 152. bp of 3'-UTR. The ORF encodes for a signal peptide of 20 amino acids and a mature protein of 104 amino acids with two N-glycosylation sites at 25th and 42nd positions. Multiple alignments of aminoacid deduced sequences of LHβ and FSHβ (teleosts, amphibians, birds, mammals) showed that all the tetrapods studied conserve 12 cysteins and one (LH) or two (FSH) N-Glycosylation sites. LHβ is closer to teleosts than to mammals and birds while FSHβ is closer to mammals. The analysis of seasonal changes in LHβ and FSHβ mRNA indicates that transcript levels have seasonal variations and that the profile of androgens is opposite to that of the gonadotropins mRNA. © 2013 Elsevier Inc.


Documento: Artículo
Título:Characterization and seasonal changes in LHβ and FSHβ mRNA of Rhinella arenarum (Amphibia, Anura)
Autor:Volonteri, M.C.; Regueira, E.; Scaia, M.F.; Ceballos, N.R.
Filiación:Lab. de Endocrinología Comparada, Departamento de Biodiversidad y Biologia Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Palabras clave:Androgens; Gonadotropins; Pituitary; Seasonal variations; Toad; amino acid; complementary DNA; cysteine; follitropin beta subunit; luteinizing hormone; luteinizing hormone beta; messenger RNA; unclassified drug; 3' untranslated region; 5' untranslated region; Amphibia; Anura; article; bird; controlled study; gene sequence; human; male; mammal; mouse; nonhuman; nucleotide sequence; open reading frame; priority journal; protein glycosylation; quantitative analysis; reverse transcription polymerase chain reaction; Rhinella arenarum; seasonal variation; sequence alignment; signal transduction; teleost; tetrapod
Página de inicio:95
Página de fin:103
Título revista:General and Comparative Endocrinology
Título revista abreviado:Gen. Comp. Endocrinol.
CAS:amino acid, 65072-01-7; cysteine, 4371-52-2, 52-89-1, 52-90-4; luteinizing hormone, 39341-83-8, 9002-67-9


  • Abe, S.-I., Ji, Z.-S., Initiation and stimulation of spermatogenesis in vitro by mammalian follicle-stimulating hormone in the Japanese newt, Cynops pyrrhogaster (1994) Int. J. Dev. Biol., 38, pp. 201-208
  • Baenziger, J.U., Kumar, S., Brodbeck, R.M., Smith, P.L., Beranek, M.C., Circulatory half-life but not interaction with the lutropin/chorionic gonadotropin receptor is modulated by sulfation of bovine lutropin oligosaccharides (1992) Proc. Natl. Acad. Sci., 89, pp. 334-338
  • Burgos, M.H., Mancini, R.E., Ciclo espermatogénico anual del Bufo arenarum Hensel (1948) Rev. Soc. Arg. Biol., 24, pp. 328-336
  • 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., Ceballos, N.R., In vitro hCG and human recombinant FSH actions on testicular steroidogenesis in the toad Bufo arenarum (2002) Gen. Comp. Endocrinol., 126, pp. 318-324
  • Canosa, L.F., Pozzi, A.G., Ceballos, N.R., Pregnenolone and progesterone metabolism by testes of Bufo arenarum (1998) J. Comp. Physiol. B, 168, pp. 491-496
  • 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
  • Chien, J.T., Shen, S.T., Lin, Y.S., Yu, J.Y., Molecular cloning of the cDNA encoding follicle-stimulating hormone beta subunit of the Chinese soft-shell turtle Pelodiscus sinensis, and its gene expression (2005) Gen. Comp. Endocrinol., 141, pp. 190-200
  • Cobellis, G., Cacciola, G., Chioccarelli, T., Izzo, G., Meccariello, R., Pierantoni, R., Estrogen regulation of the male reproductive tract in the frog, Rana esculenta: a role in Fra-1 activation in peritubular myoid cells and in sperm release (2008) Gen. Comp. Endocrinol., 155, pp. 838-846
  • Denari, D., Ceballos, N.R., 11-hydroxysteroid dehydrogenase in the testis of Bufo arenarum, changes in its seasonal activity (2005) Gen. Comp. Endocrinol., 143, pp. 113-120
  • Fernandez Solari, J.J., Pozzi, A.G., Ceballos, N.R., Seasonal changes in the activity of the cytochrome P450c17 from the testis of Bufo arenarum (2002) J. Comp. Physiol. B, 172, pp. 685-690
  • Gentz, E.J., Medicine and surgery of amphibians (2007) ILAR J., 48, pp. 255-259
  • Guarino, F.M., Di Fiore, M.M., Caputo, V., Angelini, F., Iela, L., Rastogi, R.K., Seasonal analysis of the reproductive cycle in two wild populations of Rana italica Dubois (1985) Anim. Biol., 2 (1985), pp. 25-43
  • Hall, P.F., Testicular steroid synthesis: organization and regulation (1994) The Physiology of Reproduction, 1, pp. 1335-1362. , Raven Press, New York
  • Han, Y.S., Liao, I.C., Tzeng, W.N., Yu, J.Y.L., Cloning of the cDNA for thyroid stimulating hormone beta subunit and changes in activity of the pituitary-thyroid axis during silvering of the Japanese eel, Anguilla japonica (2004) J. Mol. Endocrinol., 32, pp. 179-194
  • Hanaoka, Y., Hayashi, H., Takahashi, H., Isolation and characterization of bullfrog gonadotropins (1984) Gunma Symp. Endocrinol., 21, pp. 63-77
  • Hayashi, H., Hayashi, T., Hanaoka, Y., Amphibian lutropin from the bullfrog Rana catesbeiana. Complete amino acid sequence of the subunit (1992) Eur. J. Biochem., 205, pp. 105-110
  • Hayashi, T., Hanaoka, Y., Hayashi, H., The complete amino acid sequence of the follitropin beta-subunit of the bullfrog, Rana catesbeiana (1992) Gen. Comp. Endocrinol., 88, p. 144
  • Huang, H., Cai, L., Remo, B.F., Brown, D.D., Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis (2001) Proc. Natl. Acad. Sci. USA, 98, pp. 7348-7353
  • Itoh, M., Inoue, M., Ishii, S., Annual cycle of pituitary and plasma gonadotropins and sex steroids in a wild population of the toad, Bufo japonicus (1990) Gen. Comp. Endocrinol., 78, pp. 242-253
  • Itoh, M., Ishii, S., Changes in plasma levels of gonadotropins and sex steroids in the toad, Bufo japonicus, in association with behavior during the breading season (1990) Gen. Comp. Endocrinol., 80, pp. 451-464
  • Kano, Y., Nakano, T., Kumakura, M., Wasa, T., Suzuki, M., Yamauchi, K., Seasonal expression of LHβ and FSHβ in the male newt pituitary gonadotrophs (2005) Gen. Comp. Endocrinol., 141, pp. 248-258
  • Kawauchi, H., Sower, S.A., The dawn and evolution of hormones in the adenohypophysis (2006) Gen. Comp. Endocrinol., 148, pp. 3-14
  • Kim, J.W., Im, W.-B., Choi, H.H., Ishii, S., Kwon, H.B., Seasonal fluctuations in pituitary gland and plasma levels of gonadotropic hormones in Rana (1998) Gen. Comp. Endocrinol., 109, pp. 13-23
  • Kobayashi, T., Sakai, N., Adachi, S., Asahina, K., Iwasawa, H., Nagahama, Y., 17, 20-dihydroxy-4-pregnen-3-one is the naturally occurring spermiation inducing hormone in the testis of a frog, Rana nigromaculata (1993) Endocrinology, 133, pp. 321-327
  • Komoike, Y., Ishii, S., Cloning of cDNAs encoding the three pituitary glycoprotein hormone subunit precursor molecules in the Japanese toad, Bufo japonicus (2003) Gen. Comp. Endocrinol., 132, pp. 333-347
  • Levavi-Sivan, B., Bogerd, J., Mañanós, E.L., Gómez, A., Lareyre, J.J., Perspectives on fish gonadotropins and their receptors (2010) Gen. Comp. Endocrinol., 165, pp. 412-437
  • Licht, P., McCreery, B.R., Barnes, R., Pang, R., Seasonal and stress related changes in plasma gonadotropins, sex steroids, and corticosterone in the bullfrog, Rana catesbeiana (1983) Gen. Comp. Endocrinol., 50, p. 124
  • Licht, P., Papkoff, H., Separation of two distinct gonadotropins from the pituitary gland of the bullfrog Rana catesbeiana (1974) Endocrinology, 94, pp. 1587-1594
  • Licht, P., Papkoff, H., Farmer, S.W., Muller, C.H., Tsui, H.W., Crews, D., Evolution of gonadotropin structure and function (1977) Recent Prog. Horm. Res., 33, pp. 169-248
  • Manna, P.R., Joshi, L., Reinhold, V.N., Aubert, M.L., Suganuma, N., Pettersson, K., Synthesis, purification and structural and functional characterization of recombinant form of a common genetic variant of human luteinizing hormone (2002) Hum. Mol. Genet., 11, pp. 301-315
  • Nagahama, Y., Testis (1986) Vertebrates Endocrinology: Fundamentals and Biomedical Implications, 1, pp. 399-437. , Academic Press, New York
  • Norris, D.O., (2007) Vertebrate Endocrinology, , Academic Press, San Diego
  • Papkoff, H., Farmer, S.W., Licht, P., Isolation and characterization of luteinizing hormone from amphibian (Rana catesbeiana) pituitaries (1976) Life Sci., 18, pp. 245-250
  • Pierce, J.G., Parsons, T.F., Glycoprotein hormones: structure and function (1981) Ann. Rev. Biochem., 50 (1981), pp. 465-495
  • Pinelli, C., Fiorentino, M., D'Aniello, B., Tanaka, S., Rastogi, R.K., Immunohistochemical demonstration of FSH and LH in the pituitary of the developing frog, Rana esculenta (1996) Gen. Comp. Endocrinol., 104, pp. 189-196
  • Polzonetti-Magni, A.M., Mosconi, G., Carnevali, O., Yamamoto, K., Hanaoka, Y., Kikuyama, S., Gonadotropins and reproductive function in the anuran amphibian Rana esculenta (1998) Biol. Reprod., 58, pp. 88-93
  • Pozzi, A.G., Rosemblit, C., Ceballos, N.R., Effect of human gonadotropins on spermiation and androgen biosynthesis in testes of Bufo arenarum (2006) J. Exp. Zool., 305 A, pp. 96-102
  • Pozzi, A.G., Ceballos, N.R., Human chorionic gonadotropin-induced spermiation in Bufo arenarum is not mediated by steroid biosynthesis (2000) Gen. Comp. Endocrinol., 119, pp. 164-171
  • Quérat, B., Sellouk, A., Salmon, C., Phylogenetic analysis of the vertebrate glycoprotein hormone family including new sequences of sturgeon (Acipenser baeri) beta subunits of the two gonadotropins and the thyroid-stimulating hormone (2000) Biol. Reprod., 63, pp. 222-228
  • Quérat, B., Tonnerre-Doncarli, C., Genies, F., Salmon, C., Duality of gonadotropins in gnathostomes (2001) Gen. Comp. Endocrinol., 124, pp. 308-314
  • Quérat, B., Arai, Y., Henry, A., Akama, Y., Longhurst, T.J., Jo, J.M.P., Pituitary glycoprotein hormone b subunits in the australian lungfish and estimation of the relative evolution rate of these subunits within vertebrates (2004) Biol. Reprod., 70, pp. 356-363
  • Rastogi, R.K., Iela, L., Delrio, G., Bagnara, J.T., Reproduction in the mexican leaf frog, Pachymedusa dacnicolor II. The male (1986) Gen. Comp. Endocrinol., 62, pp. 23-35
  • Takada, K., Ishii, S., Purification of bullfrog gonadotropin: presence of two subspecies of luteinizing hormone with high isoelectric points (1984) Zool. Sci., 1, pp. 617-629
  • Takahashi, H., Hanaoka, Y., Isolation and characterization of multiple components of basic gonadotropin from bullfrog (Rana catesbeiana) pituitary gland (1981) J. Biochem., 90, pp. 1333-1340
  • Takahashi, H., Hanaoka, Y., Characterization of bullfrog gonadotropins molecules in comparison with mammalian hormones (1985) Current Trends in Comparative Endocrinology, pp. 187-188. , Hong Kong University Press, Hong Kong, B. Lofts, W.H. Holmes (Eds.)
  • Tanaka, S., Sakai, M., Hattori, M., Kikuyama, S., Wakabayashi, K., Hanaoka, Y., Effect of bullfrog LH and FSH on newt testes under different temperatures (2004) Gen. Comp. Endocrinol., 138, pp. 1-7
  • Yazawa, T., Yamamoto, T., Jin, Y., Abe, S.-I., Follicle stimulating hormone is indispensable for the last spermatogonial mitosis preceding meiosis initiation in newts (Cynops pyrrhogaster) (2002) Biol. Reprod., 66, pp. 14-20
  • Zhang, L., Kessler, A.E., Tsai, P.-S., Characterization and steroidal regulation of gonadotropin beta subunits in the male leopard frog, Rana pipiens (2007) Gen. Comp. Endocrinol., 150, pp. 66-74


---------- APA ----------
Volonteri, M.C., Regueira, E., Scaia, M.F. & Ceballos, N.R. (2013) . Characterization and seasonal changes in LHβ and FSHβ mRNA of Rhinella arenarum (Amphibia, Anura). General and Comparative Endocrinology, 187, 95-103.
---------- CHICAGO ----------
Volonteri, M.C., Regueira, E., Scaia, M.F., Ceballos, N.R. "Characterization and seasonal changes in LHβ and FSHβ mRNA of Rhinella arenarum (Amphibia, Anura)" . General and Comparative Endocrinology 187 (2013) : 95-103.
---------- MLA ----------
Volonteri, M.C., Regueira, E., Scaia, M.F., Ceballos, N.R. "Characterization and seasonal changes in LHβ and FSHβ mRNA of Rhinella arenarum (Amphibia, Anura)" . General and Comparative Endocrinology, vol. 187, 2013, pp. 95-103.
---------- VANCOUVER ----------
Volonteri, M.C., Regueira, E., Scaia, M.F., Ceballos, N.R. Characterization and seasonal changes in LHβ and FSHβ mRNA of Rhinella arenarum (Amphibia, Anura). Gen. Comp. Endocrinol. 2013;187:95-103.