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:

Besides the hypothalamus and pituitary, melatonin action at the testicuiar level has been recently suggested. Therefore, we investigated in the Syrian hamster, a well-characterized seasonal breeder, melatonin action on Leydig cells, testicular expression of melatonergic receptors, and possible interactions between melatonin receptors and the previously identified testicular serotoninergic and CRH systems. In isolated Leydig cells from active testes of adult hamsters kept in a long-day (14 h light, 10 h dark) photoperiod and from regressed testes of adult animals exposed to a short-day photoperiod during 16 wk (6 h light, 18 h dark), melatonin significantly reduced human chorionic gonadotropin-stimulated production of cAMP and the main androgens: testosterone and androstane-3α,17β-diol, respectively, and decreased the expression of steroidogenic acute regulatory protein, P450 side chain cleavage, 3β-hydroxysteroid dehydrogenase and 17β-hydroxysteroid dehydrogenase. In Leydig cells exposed to a short-day photoperiod during 16 wk, melatonin stimulated the conversion of testosterone into 5α-reduced androgens by inducing 5α-reductase isoform 1, and controlled androstane-3α,17β-diol production by inhibiting 3α- hydroxysteroid dehydrogenase expression. Melatonin subtype (mella) receptors were detected in Leydig cells. Although the local serotonin system did not mediate melatonin action on androgen production, melatonergic effect on steroidogenesis involved the interaction between mella receptors and the inhibitory CEH system. Moreover, melatonin significantly increased CRH mRNA levels and production in hamster Leydig cells expressing CRH subtype 1 receptors. Our studies indicate that melatonin may act as a local inhibitor of human chorionic gonadotropin-stimulated cAMP and androgen production through mella receptors, down-regulation of steroidogenic acute regulatory protein, and key steroidogenic enzymes expression and its interaction with the local CRH system.

Registro:

Documento: Artículo
Título:Direct effect of melatonin on Syrian hamster testes: Melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system
Autor:Frungieri, M.B.; Mayerhofer, A.; Zitta, K.; Pignataro, O.P.; Calandra, R.S.; Gonzalez-Calvar, S.I.
Filiación:Inst. de Biol. y Med. Experimental, Consejo Nac. de Invest. Cie. y Tec., 1428 Buenos Aires, Argentina
Anatomical Institute, Ludwig Maximilians University, D-80802 Munich, Germany
Facultad de Medicina, Universidad de Buenos Aires, 1121 Buenos Aires, Argentina
Cátedra de Endocrinologia, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, 1900 La Plata, Argentina
Inst. Multidisc. de Biologia Celular, 1900 La Plata, Argentina
Inst. de Biol. y Med. Experimental, Consejo Nac. de Invest. Cie. y Tec., Vuelta de Obligado 2490, (1428) Buenos Aires, Argentina
Palabras clave:3(or 17)beta hydroxysteroid dehydrogenase; 3alpha hydroxysteroid dehydrogenase; androgen; androstanediol; cholesterol monooxygenase (side chain cleaving); chorionic gonadotropin; corticotropin releasing factor; corticotropin releasing factor receptor 1; cyclic AMP; melatonin; melatonin 1 receptor; melatonin 1A receptor; messenger RNA; serotonin; steroid 5alpha reductase; steroidogenic acute regulatory protein; testosterone; testosterone 17beta dehydrogenase; unclassified drug; androgen release; animal cell; animal experiment; animal tissue; article; cell isolation; controlled study; down regulation; hormone action; hormone receptor interaction; hypophysis; hypothalamus; Leydig cell; male; nonhuman; nucleotide sequence; photoperiodicity; priority journal; protein expression; protein protein interaction; protein synthesis; serotoninergic system; steroidogenesis; Syrian hamster; testis; testosterone metabolism; 3-Hydroxysteroid Dehydrogenases; Androgens; Animals; Corticotropin-Releasing Hormone; Cricetinae; Cyclic AMP; DNA Primers; Immunoblotting; Immunoenzyme Techniques; Immunohistochemistry; Leydig Cells; Light; Male; Melatonin; Mesocricetus; Receptors, Melatonin; Reverse Transcriptase Polymerase Chain Reaction; Testis; Testosterone; Time Factors; Tryptamines
Año:2005
Volumen:146
Número:3
Página de inicio:1541
Página de fin:1552
DOI: http://dx.doi.org/10.1210/en.2004-0990
Título revista:Endocrinology
Título revista abreviado:Endocrinology
ISSN:00137227
CODEN:ENDOA
CAS:3(or 17)beta hydroxysteroid dehydrogenase, 9015-81-0; 3alpha hydroxysteroid dehydrogenase, 9028-56-2; androstanediol, 1852-53-5, 25126-76-5, 67332-38-1; cholesterol monooxygenase (side chain cleaving), 37292-81-2; chorionic gonadotropin, 9002-61-3; corticotropin releasing factor, 9015-71-8; cyclic AMP, 60-92-4; melatonin, 73-31-4; serotonin, 50-67-9; steroidogenic acute regulatory protein, 168183-61-7; testosterone 17beta dehydrogenase, 9028-62-0; testosterone, 58-22-0; 3-Hydroxysteroid Dehydrogenases, EC 1.1.-; Androgens; Corticotropin-Releasing Hormone, 9015-71-8; Cyclic AMP, 60-92-4; DNA Primers; luzindole, 117946-91-5; Melatonin, 73-31-4; Receptors, Melatonin; Testosterone, 58-22-0; Tryptamines
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00137227_v146_n3_p1541_Frungieri

Referencias:

  • Minneman, K.P., Wurtmann, R.J., Effects of pineal compounds on mammals (1975) Life Sci, 17, pp. 1189-1200
  • Reiter, R.J., The pineal and its hormones in the control of reproduction in mammals (1980) Endocr Rev, 1, pp. 109-131
  • Moore, R.Y., The innervation of the mammalian pineal gland (1978) The Pineal and Reproduction, Progress in Reproductive Biology, 4, p. 1. , Reiter RJ, ed. Basel: Karger
  • Reiter, R.J., Hester, R.J., Interrelationships of the pineal gland, the superior cervical ganglia and the photoperiod in the regulation of the endocrine systems of hamsters (1966) Endocrinology, 79, pp. 1168-1170
  • Dubocovich, M.L., Masana, M.I., Iacob, S., Sauri, D.M., Melatonin receptor antagonists that differentiate between the human Mel1a and Mel1b recombinant subtypes are used to assess the pharmacological profile of the rabbit retina ML1 presynaptic heteroreceptor (1997) Naunyn Schmiedebergs Arch Pharmacol, 355, pp. 365-375
  • Reppert, S.M., Weaver, D.R., Ebisawa, T., Cloning and characterization of a mammalian melatonin receptor that mediates reproductive and arcadian responses (1994) Neuron, 13, pp. 1177-1185
  • Kokkola, T., Laitinen, J.T., Melatonin receptor genes (1998) Ann Med, 30, pp. 88-94
  • Reppert, S.M., Godson, C., Mahle, C.D., Weaver, D.R., Slaugenhaupt, S.A., Gusella, J.F., Molecular characterization of a second melatonin receptor expressed in human retina and brain: The Mel1b melatonin receptor (1995) Proc Natl Acad Sci USA, 92, pp. 8734-8738
  • Wiechmann, A.F., Campbell, L.D., Defoe, D.M., Melatonin receptor RNA expression in Xenopus retina (1999) Brain Res Mol Brain Res, 63, pp. 297-303
  • Arendt, J., Melatonin (1988) Clin Endocrinol (Oxf), 29, pp. 205-229
  • Stankov, B., Reiter, R.J., Melatonin receptors: Current status, facts and hypothesis (1990) Life Sci, 44, pp. 971-982
  • Lincoln, G.A., Neuroendocrine regulation of seasonal gonadotrophin and prolactin rhythms: Lessons from the Soay ram model (2002) Reprod Suppl, 59, pp. 131-147
  • Reiter, R.J., Pineal melatonin: Cell biology of its synthesis and of its physiological interactions (1991) Endocr Rev, 12, pp. 151-180
  • Cardinali, D.P., Lynch, H.J., Wurtman, R.J., Binding of melatonin to human and rat plasma proteins (1972) Endocrinology, 91, pp. 1213-1218
  • Reiter, R.J., The melatonin rhythm: Both a clock and a calendar (1993) Experientia, 49, pp. 654-664
  • Tijmes, M., Pedraza, R., Valladares, L., Melatonin in the rat testes: Evidence of local synthesis (1996) Steroids, 61, pp. 65-68
  • Kato, H., Fu, Z., Kotera, N., Sugahara, K., Kubo, T., Regulation of the expression of serotonin N-acetyltransferase gene in Japanese quail (Coturnix japonica): I. Rhythmic pattern and effect of light (1999) J Pineal Res, 27, pp. 24-33
  • Fu, Z., Kato, H., Kotera, N., Noguchi, T., Sugahara, K., Kubo, T., Regulation of hydroxyindole-O-methyltransferase gene expression in Japanese quail (Coturnix japonica) (2001) Biosci Biotechnol Biochem, 65, pp. 2504-2511
  • Stefulj, J., Hortner, M., Ghosh, M., Schauenstein, K., Rinner, I., Wolfler, A., Semmler, J., Liebmann, P.M., Gene expression of the key enzymes of melatonin synthesis in extrapineal tissues of the rat (2001) J Pineal Res, 30, pp. 243-247
  • Olivares, A.N., Valladares, L.E., Bustos-Obregon, E., Nunez, S.M., Testicular function of sexually immature rats chronically treated with melatonin (1989) Arch Biol Med Exp (Santiago), 22, pp. 387-393
  • Niedziela, M., Lukaszyk, A., Melatonin inhibits forskolin stimulated testosterone secretion by hamster Leydig cells in primary culture (1993) Melatonin and the Pineal Gland: From Basic Science to Clinical Application, pp. 285-288. , Touitou J, Arendt J, Pévet P, eds. Amsterdam: Elsevier
  • Valenti, S., Guido, R., Giusti, M., Giordano, G., In vitro acute and prolonged effects of melatonin on purified rat Leydig cell steroidogenesis and adenosine 3′,5′-monophosphate production (1995) Endocrinology, 136, pp. 5357-5362
  • Ayre, E.A., Pang, S.F., 2-(125I)iodomelatonin binding sites in the testis and ovary: Putative melatonin receptors in the gonads (1994) Biol Signals, 3, pp. 71-84
  • Vera, H., Tijmes, M., Valladares, L.E., Melatonin and testicular function: Characterization of binding sites for 2-[125I]-iodomelatonin in immature rat testes (1997) Steroids, 62, pp. 226-229
  • Valenti, S., Fazzuoli, L., Giordano, G., Giusti, M., Changes in binding of iodomelatonin to membranes of Leydig steroidogenesis after prolonged in vitro exposure to melatonin (2001) Int J Androl, 24, pp. 80-86
  • Bartke, A., Male hamster reproductive endocrinology (1985) The Hamster, pp. 73-98. , Siegel HI, ed. New York: Plenum
  • Berndtson, W.E., Desjardins, C., Circulating. LH and FSH levels and testicular function in hamsters during light deprivation and subsequent photoperiod stimulation (1974) Endocrinology, 95, pp. 195-205
  • Frungieri, M.B., Gonzalez-Calvar, S.I., Calandra, R.S., Influence of photoinhibition on GABA and glutamic acid levels, and on glutamate decarboxylase activity in the testis and epididymis of the golden hamster (1996) Int J Androl, 19, pp. 171-178
  • Frungieri, M.B., Gonzalez-Calvar, S.I., Calandra, R.S., Polyamine levels in testes and seminal vesicles from adult golden hamsters during gonadal regression-recrudescence (1996) J Androl, 17, pp. 683-691
  • Fabbri, A., Tinajero, J.C., Dufau, M.L., Corticotropin-releasing factor is produced by rat Leydig cells and has a major local antireproductive role in the testis (1990) Endocrinology, 127, pp. 1541-1543
  • Dufau, M.L., Tinajero, J.C., Fabbri, A., Corticotropin-releasing factor: An antireproductive hormone of the testis (1993) FASEB J, 7, pp. 299-307
  • Frungieri, M.B., Zitta, K., Pignataro, O.P., Gonzalez-Calvar, S.I., Calandra, R.S., Interactions between testicular serotonergic, catecholaminergic and corticotropin-releasing factor systems modulating the cAMP and testosterone production in the Golden hamster (2002) Neuroendocrinology, 76, pp. 35-46
  • Levy, H., Deane, H.W., Rubin, B.L., Visualization of steroid 3 β-ol-dehydrogenase activity in tissues of intact and hypophysectomized rats (1959) Endocrinology, 65, pp. 932-943
  • Frungieri, M.B., Weidinger, S., Meineke, V., Köhn, F.M., Mayerhofer, A., Proliferative action of mast-cell tryptase is mediated by PAR2, COX2, prostaglandins, and PPARγ: Possible relevance to human fibrotic disorders (2002) Proc Natl Acad Sci USA, 99, pp. 15072-15077
  • Gamel-Didelon, K., Kunz, L., Fohr, K.J., Gratzl, M., Mayerhofer, A., Molecular and physiological evidence for functional γ-aminobutyric acid (GABA)-C receptors in growth hormone-secreting cells (2003) J Biol Chem, 278, pp. 20192-20195
  • Frungieri, M.B., Gonzalez-Calvar, S.I., Rubio, M., Ozu, M., Lustig, L., Calandra, R.S., Serotonin in golden hamster testes: Testicular levels, immunolocalization and role during sexual development and photoperiodic regression-recrudescence transition (1999) Neuroendocrinology, 69, pp. 299-308
  • Del Punta, K., Charreau, E.H., Pignataro, O.P., Nitric oxide inhibits Leydig cell steroidogenesis (1996) Endocrinology, 137, pp. 5337-5343
  • Birnbaumer, L., Techniques in cyclic nucleotide research (1980) Laboratory Methods Manual for Hormone Action and Molecular Endocrinology. 4th Ed., pp. 9-16. , Schrader WT, O'Malley BW, eds. Houston: Baylor College of Medicine, Department of Cell Biology
  • Brooker, G., Harper, J.F., Terasaki, W.L., Moylan, R.D., Radioimmunoassay of cyclic AMP and cyclic GMP (1979) Advances in Cyclic Nucleotide Research, pp. 1-32. , Brooker G, Greengard P, eds. New York: Raven Press
  • Cagnacci, A., Volpe, A., Influence of melatonin and photoperiod on animal and human reproduction (1996) J Endocrinol Invest, 19, pp. 382-411
  • Gunduz, B., Daily rhythm in serum melatonin and leptin levels in the Syrian hamster (Mesocricetus auratus) (2002) Comp Biochem and Physiol A Mol Integr Physiol, 132, pp. 393-401
  • Wurtman, R.J., Axelrod, J., The physiologic effects of melatonin and the control of its biosynthesis (1966) Probl Actuels Endocrinol Nutr, 10, pp. 189-200
  • Reiter, R.J., Pineal control of reproduction (1981) Prog Clin Biol Res, 59 B, pp. 349-355
  • Frungieri, M.B., Gonzalez-Calvar, S.I., Bartke, A., Calandra, R.S., Influence of age and photoperiod on steroidogenic function of the testis in the golden hamster (1999) Int J Androl, 22, pp. 243-252
  • Wu, C.S., Leu, S.F., Yang, H.Y., Huang, B.M., Melatonin inhibits the expression of steroidogenic acute regulatory protein and steroidogenesis in MA-10 cells (2001) J Androl, 22, pp. 245-254
  • Valenti, S., Giusti, M., Guido, R., Giordano, G., Melatonin receptors are present in adult rat Leydig cells and are coupled through a pertussis toxin-sensitive G-protein (1997) Eur J Endocrinol, 136, pp. 633-639
  • Maitra, S.K., Ray, A.K., Role of light in the mediation of acute effects of a single afternoon melatonin injection on steroidogenic activity of testis in the rat (2000) J Biosci, 25, pp. 253-256
  • Pratis, K., O'Donnell, L., Ooi, G.T., Stanton, P.G., McLachlan, R.I., Robertson, D.M., Differential regulation of rat testicular 5α-reductase type 1 and 2 isoforms by testosterone and FSH (2003) J Endocrinol, 176, pp. 393-403
  • Ji, Q., Chang, L., VanDenBerg, D., Stanczyk, F.Z., Stolz, A., Selective reduction of AKR1C2 in prostate cancer and its role in DHT metabolism (2003) Prostate, 54, pp. 275-289
  • Saez, J.M., Leydig cells: Endocrine, paracrine and autocrine regulation (1994) Endocr Rev, 15, pp. 574-626
  • Valenti, S., Thellung, S., Florio, T., Giusti, M., Schettini, G., Giordano, G., A novel mechanism for the melatonin inhibition of testosterone secretion by rat Leydig cells: Reduction of GnRH-induced increase in cytosolic Ca2+ (1999) J Mol Endocrinol, 23, pp. 299-306
  • Reiter, R.J., Tan, D.X., Mayo, J.C., Sainz, R.M., Leon, J., Czarnocki, Z., Melatonin as an antioxidant: Biochemical mechanisms and pathophysiological implications in humans (2003) Acta Biochim Pol, 50, pp. 1129-1146
  • Sainz, R.M., Mayo, J.C., Tan, D.X., Lopez-Burillo, S., Natarajan, M., Reiter, R.J., Antioxidant activity of melatonin in Chinese hamster ovarian cells: Changes in cellular proliferation and differentiation (2003) Biochem Biophys Res Commun, 302, pp. 625-634
  • Pickering, H., Sword, S., Vonhoff, S., Jones, R., Sugden, D., Analogues of diverse structure are unable to differentiate native melatonin receptors in the chicken retina, sheep pars tuberalis and Xenopus melanophores (1996) Br J Pharmacol, 119, pp. 379-387
  • Reppert, S.M., Melatonin receptors: Molecular biology of a new family of G protein-coupled receptors (1997) J Biol Rhythms, 12, pp. 528-531
  • Lee, C.K., Rang, H.S., Lee, B.J., Kang, H.M., Choi, W.S., Kang, S.G., Effects of dopamine and melatonin on the regulation of the PIT-1 isotype, placental growth hormone and lactogen gene expressions in the rat placenta (1999) Mol Cells, 9, pp. 646-651
  • Marelli, M.M., Limonta, P., Maggi, R., Motta, M., Moretti, R.M., Growth-inhibitory activity of melatonin on human androgen-independent DU 145 prostate cancer cells (2000) Prostate, 45, pp. 238-244
  • Shiu, S.Y., Li, L., Siu, S.W., Xi, S.C., Fong, S.W., Pang, S.F., Biological basis and possible physiological implications of melatonin receptor-mediated signalling in the rat epididymis (2000) Biol Signals Recept, 9, pp. 172-187
  • Lee, C.J., Do, B.R., Lee, Y.H., Park, J.H., Kim, S.J., Kim, J.K., Roh, S.I., Yoon, H.S., Ovarian expression of melatonin Mel(1a) receptor mRNA during mouse development (2001) Mol Reprod Dev, 59, pp. 126-132
  • Dugovic, C., Leysen, J.E., Wauquier, A., Melatonin modulates the sensitivity of 5-hydroxytryptamine-2-receptor- media ted sleep-wakefulness regulation in the rat (1989) Neurosci Lett, 104, pp. 320-325
  • Yocca, F.D., Wright, R.N., Margraf, R.R., Eison, A.S., 8-OH-DPAT and buspirone analogs inhibit the ketanserin-sensitive quipazine-induced head shake response in rats (1990) Pharmacol Biochem Behav, 35, pp. 252-254
  • Araneda, R., Andrade, R., 5-Hydroxytryptamin-2 and 5-hydroxytryptamin-1A receptors mediate opposing responses on membrane excitability in rat association cortex (1991) Neuroscience, 40, pp. 399-412
  • Yocca, F.D., Eison, A.S., Hyslop, D.K., Ryan, E., Taylor, D.P., Gianutsos, G., Unique modulation of central 5-HT2 receptor binding sites and 5-HT2 receptor-mediated behavior by continuous gepirone treatment (1991) Life Sci, 49, pp. 1777-1785
  • Eison, A.S., Freeman, R.P., Guss, V.B., Mullins, L., Wright, R.N., Melatonin agonists modulate 5-HT2A receptor-mediated neurotransmission: Behavioral and biochemical studies in the rat (1995) J Pharmacol Exp Ther, 273, pp. 304-308
  • Esquifino, A.I., Arce, A., Villanua, M.A., Cardinali, D.P., Twenty-four hour rhythms of serum prolactin, growth hormone and luteinizing hormone levels, and of medial basal hypothalamic corticotropin-releasing hormone levels and dopamine and serotonin metabolism in rats neonatally administered melatonin (1997) J Pineal Res, 22, pp. 52-58
  • Konakchieva, R., Mitev, Y., Almeida, O.F., Patchev, V.K., Chronic melatonin treatment counteracts glucocorticoid-induced dysregulation of the hypothalamic-pituitary-adrenal axis in the rat (1998) Neuroendocrinology, 67, pp. 171-180
  • Heinrich, N., Meyer, M.R., Furkert, J., Sasse, A., Beyermann, M., Bonigk, W., Berger, H., Corticotropin-releasing factor (CRF) agonists stimulate testosterone production in mouse Leydig cells through CRF receptor-1 (1998) Endocrinology, 139, pp. 651-658
  • Tsai-Morris, Ch.H., Buczko, E., Geng, Y., Gamboa-Pinto, A., Dufau, M.L., The genomlc structure of the rat corticotropin releasing factor receptor (1996) J Biol Chem, 271, pp. 14519-14525
  • Reiter, R.J., Rudeen, P.K., Sackman, J.W., Vaughan, M.K., Johnson, L.Y., Little, J.C., Subcutaneous melatonin implants inhibit reproductive atrophy in male hamsters induced by daily melatonin injections (1977) Endocr Res Commun, 4, pp. 35-44
  • Gorman, M.R., Independence of circadian entrainment state and responses to melatonin in male Siberian hamsters (2003) BMC Physiol, 3, p. 10

Citas:

---------- APA ----------
Frungieri, M.B., Mayerhofer, A., Zitta, K., Pignataro, O.P., Calandra, R.S. & Gonzalez-Calvar, S.I. (2005) . Direct effect of melatonin on Syrian hamster testes: Melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system. Endocrinology, 146(3), 1541-1552.
http://dx.doi.org/10.1210/en.2004-0990
---------- CHICAGO ----------
Frungieri, M.B., Mayerhofer, A., Zitta, K., Pignataro, O.P., Calandra, R.S., Gonzalez-Calvar, S.I. "Direct effect of melatonin on Syrian hamster testes: Melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system" . Endocrinology 146, no. 3 (2005) : 1541-1552.
http://dx.doi.org/10.1210/en.2004-0990
---------- MLA ----------
Frungieri, M.B., Mayerhofer, A., Zitta, K., Pignataro, O.P., Calandra, R.S., Gonzalez-Calvar, S.I. "Direct effect of melatonin on Syrian hamster testes: Melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system" . Endocrinology, vol. 146, no. 3, 2005, pp. 1541-1552.
http://dx.doi.org/10.1210/en.2004-0990
---------- VANCOUVER ----------
Frungieri, M.B., Mayerhofer, A., Zitta, K., Pignataro, O.P., Calandra, R.S., Gonzalez-Calvar, S.I. Direct effect of melatonin on Syrian hamster testes: Melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system. Endocrinology. 2005;146(3):1541-1552.
http://dx.doi.org/10.1210/en.2004-0990