Melatonin Supplementation Decreases Prolactin Synthesis and Release in Rat Adenohypophysis: Correlation With Anterior Pituitary Redox State and Circadian Clock Mechanisms

REFERENCES

• Alonso-González C, Mediavilla D, Martínez-Campa C, González A, Cos S, Sánchez-Barcelo EJ. (2008). Melatonin modulates the cadmium-induced expression of MT-2 and MT-1 metallothioneins in three lines of human tumor cells (MCF-7, MDA-MB-231 and HeLa). Toxicol. Lett. 181:190–195.
   PubMed Web of Science ®Google Scholar
• Bartness TJ, Powers JB, Hastings MH, Bittman EL, Goldman BD. (1993). The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception, and the photoperiodic control of seasonal responses? J. Pineal Res. 15:161–190.
   PubMed Web of Science ®Google Scholar
• Benarroch EE. (2011). Nitric oxide: a pleiotropic signal in the nervous system. Neurology 77:1568–1576.
   PubMed Web of Science ®Google Scholar
• Beni SM, Kohen R, Reiter RJ, Tan DX, Shohami E. (2004). Melatonin-induced neuroprotection after closed head injury is associated with increased brain antioxidants and attenuated late-phase activation of NF-κB and AP-1. FASEB J. 18:149–151.
   PubMed Web of Science ®Google Scholar
• Bissette G, Griff D, Carnes M, Goodman B, Lavine M, Levant B. (1995). Apparent seasonal rhythms in hypothalamic neuropeptides in rats without photoperiod changes. Endocrinology 136:622–628.
   PubMed Web of Science ®Google Scholar
• Bittman EL, Karsch FJ. (1984). Nightly duration of pineal melatonin secretion determines the reproductive response to inhibitory day length in the ewe. Biol. Reprod. 30:585–593.
   PubMed Web of Science ®Google Scholar
• Bur IM, Zouaoui S, Fontanaud P, Coutry N, Molino F, Martin AO, Mollard P, Bonnefont X. (2010). The comparison between circadian oscillators in mouse liver and pituitary gland reveals different integration of feeding and light schedules. PLoS ONE 5:e15316.
   PubMed Web of Science ®Google Scholar
• Cano P, Cardinali DP, Jiménez-Ortega V, Ríos-Lugo MJ, Scacchi PA, Esquifino AI. (2010). Effect of a high-fat diet on 24-hour pattern in expression of prolactin and redox pathway enzymes in the rat adenohypophysis. Open Obesity J. 2:1–9.
   Google Scholar
• Cardinali DP, García AP, Cano P, Esquifino AI. (2004). Melatonin role in experimental arthritis. Curr. Drug Targets Immune. Endocr. Metabol. Disord. 4:1–10.
   PubMedGoogle Scholar
• Castrillón P, Cardinali DP, Pazo D, Cutrera RA, Esquifino AI. (2001). Effect of superior cervical ganglionectomy on 24-h variations in hormone secretion from anterior hypophysis and in hypothalamic monoamine turnover, during the preclinical phase of Freund's adjuvant arthritis in rats. J. Neuroendocrinol. 13:288–295.
   PubMed Web of Science ®Google Scholar
• Chemineau P, Guillaume D, Migaud M, Thiery JC, Pellicer-Rubio MT, Malpaux B. (2008). Seasonality of reproduction in mammals: intimate regulatory mechanisms and practical implications. Reprod. Domest. Anim. 43( Suppl. 2):40–47.
   PubMed Web of Science ®Google Scholar
• Cohen IR, Mann DR. (1979). Seasonal changes associated with puberty in female rats: effect of photoperiod and ACTH administration. Biol. Reprod. 20:757–762.
   PubMed Web of Science ®Google Scholar
• Dardente H. (2007). Does a melatonin-dependent circadian oscillator in the pars tuberalis drive prolactin seasonal rhythmicity? J. Neuroendocrinol. 19:657–666.
   PubMed Web of Science ®Google Scholar
• De Scremin ER, Scremin OU. (1972). Seasonal variation of reserpine pseudopregnancy in the rat. Experientia 28:1488–1489.
   PubMedGoogle Scholar
• Díaz E, Vázquez N, Fernández C, Durand D, Lasaga M, Debeljuk L, Díaz B. (2011). Seasonal variations of Substance P in the striatum of the female rat are affected by maternal and offspring pinealectomy. Neurosci. Lett. 492:71–75.
   PubMed Web of Science ®Google Scholar
• Díaz E, Vázquez N, Fernández C, Jiménez V, Esquifino A, Díaz B. (2012). In vitro seasonal variations of LH, FSH and prolactin secretion of the male rat are dependent on the maternal pineal gland. Neurosci. Lett. 507:16–21.
   PubMed Web of Science ®Google Scholar
• Duncan MJ. (2007). Circannual prolactin rhythms: calendar-like timer revealed in the pituitary gland. Trends Endocrinol. Metab. 18:259–260.
   PubMed Web of Science ®Google Scholar
• Dupre SM. (2011). Encoding and decoding photoperiod in the mammalian pars tuberalis. Neuroendocrinology 94:101–112.
   PubMed Web of Science ®Google Scholar
• Esquifino AI, Pazo D, Cutrera RA, Cardinali DP. (1999). Seasonally-dependent effect of ectopic pituitary grafts on 24-hour rhythms in serum prolactin and gonadotropins in rats. Chronobiol. Int. 16:451–460.
   PubMed Web of Science ®Google Scholar
• Galano A, Tan DX, Reiter RJ. (2011). Melatonin as a natural ally against oxidative stress: a physicochemical examination. J. Pineal Res. 51:1–16.
   PubMed Web of Science ®Google Scholar
• García Bonacho M, Esquifino AI, Castrillón P, Reyes Toso C, Cardinali DP. (2000). Age-dependent effect of Freund's adjuvant on 24-hour rhythms in plasma prolactin, growth hormone, thyrotropin, insulin, follicle-stimulating hormone, luteinizing hormone and testosterone in rats. Life Sci. 66:1969–1977.
   PubMed Web of Science ®Google Scholar
• Girotti M, Weinberg MS, Spencer RL. (2009). Diurnal expression of functional and clock-related genes throughout the rat HPA axis: system-wide shifts in response to a restricted feeding schedule. Am. J. Physiol. Endocrinol. Metab. 296:E888–E897.
   PubMed Web of Science ®Google Scholar
• Gerics B, Szalay F, Hajos F. (2006). Glial fibrillary acidic protein immunoreactivity in the rat suprachiasmatic nucleus: circadian changes and their seasonal dependence. J. Anat. 209:231–237.
   PubMed Web of Science ®Google Scholar
• Glass JD, Lynch GR. (1981). Melatonin: identification of sites of antigonadal action in mouse brain. Science 214:821–823.
   PubMed Web of Science ®Google Scholar
• Hanon EA, Routledge K, Dardente H, Masson-Pévet M, Morgan PJ, Hazlerigg DG. (2010). Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J. Neuroendocrinol. 22:51–55.
   PubMed Web of Science ®Google Scholar
• Hardeland R, Cardinali DP, Srinivasan V, Spence DW, Brown GM, Pandi-Perumal SR. (2011). Melatonin—a pleiotropic, orchestrating regulator molecule. Progr. Neurobiol. 93:350–384.
   PubMed Web of Science ®Google Scholar
• Hegarty CM, Jonassen JA, Bittman EL. (1990). Pituitary hormone gene expression in male golden hamsters: interactions between photoperiod and testosterone. J. Neuroendocrinol. 2:567–573.
   PubMed Web of Science ®Google Scholar
• Jacob C. (2011). Redox signalling via the cellular thiolstat. Biochem. Soc. Trans. 39:1247–1253.
   PubMed Web of Science ®Google Scholar
• Johnston JD, Messager S, Ebling FJ, Williams LM, Barrett P, Hazlerigg DG. (2003). Gonadotrophin-releasing hormone drives melatonin receptor down-regulation in the developing pituitary gland. Proc. Natl. Acad. Sci. U. S. A. 100:2831–2835.
   PubMed Web of Science ®Google Scholar
• Kamberi IA, Mical RS, Porter JC. (1971). Effects of melatonin and serotonin on the release of FSH and prolactin. Endocrinology 88:1288–1293.
   PubMed Web of Science ®Google Scholar
• Khachatur'yan ML, Panchenko LA. (2002). Seasonal variations in rat resistance to hypoxia. Bull. Exp. Biol. Med. 133:300–303.
   PubMed Web of Science ®Google Scholar
• Khodursky AB, Bernstein JA. (2003). Life after transcription—revisiting the fate of messenger RNA. Trends Genet. 19:113–115.
   PubMed Web of Science ®Google Scholar
• Klosen P, Bienvenu C, Demarteau O, Dardente H, Guerrero H, Pevet P, Masson-Pevet M. (2002). The mt1 melatonin receptor and RORβ receptor are co-localized in specific TSH-immunoreactive cells in the pars tuberalis of the rat pituitary. J. Histochem. Cytochem. 50:1647–1657.
   PubMed Web of Science ®Google Scholar
• Konior A, Klemenska E, Brudek M, Podolecka E, Czarnowska E, Beresewicz A. (2011). Seasonal superoxide overproduction and endothelial activation in guinea-pig heart; seasonal oxidative stress in rats and humans. J. Mol. Cell Cardiol. 50:686–694.
   PubMed Web of Science ®Google Scholar
• Kubatka P, Ahlersova E, Ahlers I, Bojkova B, Kalicka K, Adamekova E, Markova M, Chamilova M, Ermakova M. (2002). Variability of mammary carcinogenesis induction in female Sprague-Dawley and Wistar:Han rats: the effect of season and age. Physiol. Res. 51:633–640.
   PubMed Web of Science ®Google Scholar
• Lee TM, McClintock MK. (1986). Female rats in a laboratory display seasonal variation in fecundity. J. Reprod. Fertil. 77:51–59.
   PubMedGoogle Scholar
• Lehman MN, Ladha Z, Coolen LM, Hileman SM, Connors JM, Goodman RL. (2010). Neuronal plasticity and seasonal reproduction in sheep. Eur. J. Neurosci. 32:2152–2164.
   PubMed Web of Science ®Google Scholar
• Levi F, Okyar A, Dulong S, Innominato PF, Clairambault J. (2010). Circadian timing in cancer treatments. Annu. Rev. Pharmacol. Toxicol. 50:377–421
   PubMed Web of Science ®Google Scholar
• Lezoualc'h F, Sparapani M, Behl C. (1998). N-acetyl-serotonin (normelatonin) and melatonin protect neurons against oxidative challenges and suppress the activity of the transcription factor NF-κB. J. Pineal Res. 24:168–178.
   PubMed Web of Science ®Google Scholar
• Lincoln GA, Andersson H, Loudon A. (2003). Clock genes in calendar cells as the basis of annual timekeeping in mammals—a unifying hypothesis. J. Endocrinol. 179:1–13.
   PubMed Web of Science ®Google Scholar
• Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG. (2006). Characterizing a mammalian circannual pacemaker. Science 314:1941–1944.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ Δ C(T)) method. Methods 25:402–408.
   PubMed Web of Science ®Google Scholar
• Locasale JW, Cantley LC. (2011). Metabolic flux and the regulation of mammalian cell growth. Cell Metab. 14:443–451.
   PubMed Web of Science ®Google Scholar
• Lundkvist GB, Sellix MT, Nygard M, Davis E, Straume M, Kristensson K, Block GD. (2010). Clock gene expression during chronic inflammation induced by infection with Trypanosoma brucei brucei in rats. J. Biol. Rhythms 25:92–102.
   PubMed Web of Science ®Google Scholar
• Mancuso C, Scapagini G, Curro D, Giuffrida Stella AM, De Marco C, Butterfield DA, Calabrese V. (2007). Mitochondrial dysfunction, free radical generation and cellular stress response in neurodegenerative disorders. Front. Biosci. 12:1107–1123.
   PubMed Web of Science ®Google Scholar
• Masumura S, Furui H, Hashimoto M, Watanabe Y. (1992). The effects of season and exercise on the levels of plasma polyunsaturated fatty acids and lipoprotein cholesterol in young rats. Biochim. Biophys. Acta 1125:292–296.
   PubMedGoogle Scholar
• Mato E, Santisteban P, Chowen JA, Fornas O, Bouwens M, Puig-Domingo M, Argente J, Webb SM. (1997). Circannual somatostatin gene and somatostatin receptor gene expression in the early post-natal rat pineal gland. Neuroendocrinology 66:368–374.
   PubMed Web of Science ®Google Scholar
• Miler EA, Nudler SI, Quinteros FA, Cabilla JP, Ronchetti SA, Duvilanski BH. (2010). Cadmium induced-oxidative stress in pituitary gland is reversed by removing the contamination source. Hum. Exp. Toxicol. 29:873–880.
   PubMed Web of Science ®Google Scholar
• Mock EJ, Frankel AI. (1978). A shifting circannual rhythm in serum testosterone concentration in male laboratory rats. Biol. Reprod. 19:927–930.
   PubMed Web of Science ®Google Scholar
• Morgan PJ, Barrett P, Howell HE, Helliwell R. (1994). Melatonin receptors: localization, molecular pharmacology and physiological significance. Neurochem. Int. 24:101–146.
   PubMed Web of Science ®Google Scholar
• Mujkosova J, Ferko M, Humenik P, Waczulikova I, Ziegelhoffer A. (2008). Seasonal variations in properties of healthy and diabetic rat heart mitochondria: Mg2+-ATPase activity, content of conjugated dienes and membrane fluidity. Physiol. Res. 57( Suppl 2) :S75–S82.
   PubMed Web of Science ®Google Scholar
• Mukherjee R, Banerjee S, Joshi N, Singh PK, Baxi D, Ramachandran AV. (2011). A combination of melatonin and alpha lipoic acid has greater cardioprotective effect than either of them singly against cadmium-induced oxidative damage. Cardiovasc. Toxicol. 11:78–88.
   PubMed Web of Science ®Google Scholar
• Namdarghanbari M, Wobig W, Krezoski S, Tabatabai NM, Petering DH. (2011). Mammalian metallothionein in toxicology, cancer, and cancer chemotherapy. J. Biol. Inorg. Chem. 16:1087–1101.
   PubMed Web of Science ®Google Scholar
• Nelson W, Tong YL, Lee JK, Halberg F. (1979). Methods for cosinor-rhythmometry. Chronobiologia 6:305–323.
   PubMedGoogle Scholar
• Parrot S, Bert L, Renaud B, Denoroy L. (2001). Large inter-experiment variations in microdialysate aspartate and glutamate in rat striatum may reflect a circannual rhythm. Synapse 39:267–269.
   PubMed Web of Science ®Google Scholar
• Poliandri AH, Esquifino AI, Cano P, Jiménez V, Lafuente A, Cardinali DP, Duvilanski BH. (2006). In vivo protective effect of melatonin on cadmium-induced changes in redox balance and gene expression in rat hypothalamus and anterior pituitary. J. Pineal Res. 41:238–246.
   PubMed Web of Science ®Google Scholar
• Portaluppi F, Smolensky MH, Touitou Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiol. Int. 27:1911–1929.
   PubMed Web of Science ®Google Scholar
• Quinteros FA, Poliandri AH, Machiavelli LI, Cabilla JP, Duvilanski BH. (2007). In vivo and in vitro effects of chromium VI on anterior pituitary hormone release and cell viability. Toxicol. Appl. Pharmacol. 218:79–87.
   PubMed Web of Science ®Google Scholar
• Reiter RJ. (1980). The pineal and its hormones in the control of reproduction in mammals. Endocr. Rev. 1:109–131.
   PubMedGoogle Scholar
• Reiter RJ, Tan DX, Manchester LC, Paredes SD, Mayo JC, Sainz RM. (2009). Melatonin and reproduction revisited. Biol. Reprod. 81:445–456.
   PubMed Web of Science ®Google Scholar
• Revel F., Masson-Pévet M, Pévet P, Mikkelsen JD, Simonneaux V. (2009). Melatonin controls seasonal breeding by a network of hypothalamic targets. Neuroendocrinology 90:1–14.
   PubMed Web of Science ®Google Scholar
• Rodríguez C, Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Reiter RJ. (2004). Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 36:1–9.
   PubMed Web of Science ®Google Scholar
• Scherbarth F, Steinlechner S. (2010). Endocrine mechanisms of seasonal adaptation in small mammals: from early results to present understanding. J. Comp. Physiol. B 180:935–952.
   PubMed Web of Science ®Google Scholar
• Shishkina GT, Borodin PM, Naumenko EV. (1993). Sexual maturation and seasonal changes in plasma levels of sex steroids and fecundity of wild Norway rats selected for reduced aggressiveness toward humans. Physiol. Behav. 53:389–393.
   PubMed Web of Science ®Google Scholar
• Spiwoks-Becker I, Wolloscheck T, Rickes O, Kelleher DK, Rohleder N, Weyer V, Spessert R. (2011). Phosphodiesterase 10A in the rat pineal gland: localization, daily and seasonal regulation of expression and influence on signal transduction. Neuroendocrinology 94:113–123.
   PubMed Web of Science ®Google Scholar
• Steger RW, Bartke A. (1995). Neuroendocrine control of reproduction. Adv. Exp. Med. Biol. 377:15–32.
   PubMedGoogle Scholar
• Stirland JA, Johnston JD, Cagampang FR, Morgan PJ, Castro MG, White MR, Davis JR, Loudon AS. (2001). Photoperiodic regulation of prolactin gene expression in the Syrian hamster by a pars tuberalis-derived factor. J. Neuroendocrinol. 13:147–157.
   PubMed Web of Science ®Google Scholar
• Tinnikov AA, Oskina IN. (1994). Seasonal variations in corticosteroid-binding globulin levels in white laboratory and Norway rats. Horm. Metab. Res. 26:559–560.
   PubMed Web of Science ®Google Scholar
• Utembaeva NT, Pashorina VA, Seliaskin KE, Tyshko NV. (2009). [Methodical approaches to studying effect of seasonal factor on rat reproductive function in experiments on alimentary influence]. Vopr. Pitan. 78:43–48.
   PubMedGoogle Scholar
• Velárdez MO, De Laurentiis A, del Carmen DM, Lasaga M, Pisera D, Seilicovich A, Duvilanski BH. (2000). Role of phosphodiesterase and protein kinase G on nitric oxide-induced inhibition of prolactin release from the rat anterior pituitary. Eur. J. Endocrinol. 143:279–284.
   PubMed Web of Science ®Google Scholar
• Wallen EP, Turek FW. (1981). Photoperiodicity in the male albino laboratory rat. Nature 289:402–404.
   PubMed Web of Science ®Google Scholar
• Weinstock M, Blotnick S, Segal M. (1985). Seasonal variation in the development of stress-induced systolic hypertension in the rat. J. Hypertens. 3 ( Suppl 3) :S107–S109.
   Web of Science ®Google Scholar
• Winyard PG, Spickett CM, Griffiths HR. (2011). Analysis of radicals and radical reaction products in cell signalling and biomolecular damage: the long hard road to gold-standard measures. Biochem. Soc. Trans. 39:1217–1220.
   PubMed Web of Science ®Google Scholar
• Wong CC, Dohler KD, Atkinson MJ, Geerlings H, Hesch RD, von zur MA. (1983). Circannual variations in serum concentrations of pituitary, thyroid, parathyroid, gonadal and adrenal hormones in male laboratory rats. J. Endocrinol. 97:179–185.
   PubMed Web of Science ®Google Scholar
• Yasuo S, Yoshimura T. Ebihara S, Korf HW. (2010). Photoperiodic control of TSH-beta expression in the mammalian pars tuberalis has different impacts on the induction and suppression of the hypothalamo-hypophysial gonadal axis. J. Neuroendocrinol. 22:43–50.
   PubMed Web of Science ®Google Scholar
• Yoshimura T. (2010). Neuroendocrine mechanism of seasonal reproduction in birds and mammals. Anim. Sci. J. 81:403–410.
   PubMed Web of Science ®Google Scholar