Advertisement

Kisspeptin: A key link to seasonal breeding

  • Florent G. Revel
  • Laura Ansel
  • Paul Klosen
  • Michel Saboureau
  • Paul Pévet
  • Jens D. Mikkelsen
  • Valérie SimonneauxEmail author
Article

Abstract

In seasonal species, photoperiod (i.e. daylength) tightly regulates reproduction to ensure that birth occurs at the most favorable time of year. In mammals, a distinct photoneuroendocrine circuit controls this process via the pineal hormone melatonin. This hormone is responsible for the seasonal regulation of reproduction, but the anatomical substrate and the cellular mechanism through which melatonin modulates sexual activity is far from understood. The Syrian hamster is widely used to explore the photoneuroendocrine system, because it is a seasonal model in which sexual activity is promoted by long summer days (LD) and inhibited by short winter days (SD). Recent evidences indicate that the products of the KiSS-1 gene, kisspeptins, and their specific receptor GPR54, represent potent stimulators of the sexual axis. We have shown that melatonin impacts on KiSS-1 expression to control reproduction in the Syrian hamster. In this species, KiSS-1 is expressed in the antero-ventral-periventricular and arcuate nuclei of the hypothalamus at significantly higher levels in hamsters kept in LD as compared to SD. In the arcuate nucleus, the downregulation of KiSS-1 expression in SD appears to be mediated by melatonin and not by secondary changes in gonadal hormones. Remarkably, a chronic administration of kisspeptin restores testicular activity in SD hamsters, despite persisting photoinhibitory conditions. Overall, these findings are consistent with a role of KiSS-1/GPR54 in the seasonal control of reproduction. We propose that the photoperiod, via melatonin, modulates KiSS-1 neurons to drive the reproductive axis.

Keywords

KiSS-1 GPR54 Reproduction Photoperiod Syrian hamster Melatonin 

References

  1. 1.
    Sisk CL, Foster DL. The neural basis of puberty and adolescence. Nat Neurosci 2004;7:1040–7.PubMedCrossRefGoogle Scholar
  2. 2.
    Clarke IJ, Pompolo S. Synthesis and secretion of GnRH. Anim Reprod Sci 2005;88:29–55.PubMedCrossRefGoogle Scholar
  3. 3.
    Pevet P. The role of the pineal gland in the photoperiodic control of reproduction in different hamster species. Reprod Nutr Dev 1988;28:443–58.PubMedGoogle Scholar
  4. 4.
    Goldman BD. Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J Biol Rhythms 2001;16:283–301.PubMedCrossRefGoogle Scholar
  5. 5.
    Malpaux B, Migaud M, Tricoire H, Chemineau P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. J Biol Rhythms 2001;16:336–47.PubMedCrossRefGoogle Scholar
  6. 6.
    Schwartz WJ, de la Iglesia HO, Zlomanczuk P, Illnerova H. Encoding le quattro stagioni within the mammalian brain: photoperiodic orchestration through the suprachiasmatic nucleus. J Biol Rhythms 2001;16:302–11.PubMedCrossRefGoogle Scholar
  7. 7.
    Simonneaux V, Ribelayga C. Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev 2003;55:325–95.PubMedCrossRefGoogle Scholar
  8. 8.
    Gaston S, Menaker M. Photoperiodic control of hamster testis. Science 1967;158:925–8.PubMedCrossRefGoogle Scholar
  9. 9.
    Brackmann M, Hoffmann K. Pinealectomy and photoperiod influence testicular development in the Djungarian hamster. Naturwissenschaften 1977;64:341–2.PubMedCrossRefGoogle Scholar
  10. 10.
    Bartke A, Steger RW. Seasonal changes in the function of the hypothalamic-pituitary-testicular axis in the Syrian hamster. Proc Soc Exp Biol Med 1992;199:139–48.PubMedGoogle Scholar
  11. 11.
    Hoffman RA, Reiter RJ. Pineal gland: influence on gonads of male hamsters. Science 1965;148:1609–11.PubMedCrossRefGoogle Scholar
  12. 12.
    Vitale PM, Darrow JM, Duncan MJ, Shustak CA, Goldman BD. Effects of photoperiod, pinealectomy and castration on body weight and daily torpor in Djungarian hamsters (Phodopus sungorus). J Endocrinol 1985;106:367–75.PubMedGoogle Scholar
  13. 13.
    Bartness TJ, Powers JB, Hastings MH, Bittman EL, Goldman BD. 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 1993;15:161–90.PubMedCrossRefGoogle Scholar
  14. 14.
    Pitrosky B, Pevet P. The photoperiodic response in Syrian hamsters depends upon a melatonin-driven rhythm of sensitivity to melatonin. Biol Signals 1997;6:264–71.PubMedGoogle Scholar
  15. 15.
    Bittman EL, Kaynard AH, Olster DH, Robinson JE, Yellon SM, Karsch FJ. Pineal melatonin mediates photoperiodic control of pulsatile luteinizing hormone secretion in the ewe. Neuroendocrinology 1985;40:409–18.PubMedGoogle Scholar
  16. 16.
    Urbanski HF, Doan A, Pierce M. Immunocytochemical investigation of luteinizing hormone-releasing hormone neurons in Syrian hamsters maintained under long or short days. Biol Reprod 1991;44:687–92.PubMedCrossRefGoogle Scholar
  17. 17.
    Ronchi E, Krey LC, Pfaff DW. Steady state analysis of hypothalamic GnRH mRNA levels in male Syrian hamsters: influences of photoperiod and androgen. Neuroendocrinology 1992;55:146–55.PubMedGoogle Scholar
  18. 18.
    Ronchi E, Aoki C, Krey LC, Pfaff DW. Immunocytochemical study of GnRH and GnRH-associated peptide in male Syrian hamsters as a function of photoperiod and gonadal alterations. Neuroendocrinology 1992;55:134–45.PubMedGoogle Scholar
  19. 19.
    Lehman MN, Goodman RL, Karsch FJ, Jackson GL, Berriman SJ, Jansen HT. The GnRH system of seasonal breeders: anatomy and plasticity. Brain Res Bull 1997;44:445–57.PubMedCrossRefGoogle Scholar
  20. 20.
    Bernard DJ, Abuav-Nussbaum R, Horton TH, Turek FW. Photoperiodic effects on gonadotropin-releasing hormone (GnRH) content and the GnRH-immunoreactive neuronal system of male Siberian hamsters. Biol Reprod 1999;60:272–6.PubMedCrossRefGoogle Scholar
  21. 21.
    Brown DI, Garyfallou VT, Urbanski HF. Photoperiodic modulation of GnRH mRNA in the male Syrian hamster. Brain Res Mol Brain Res 2001;89:119–25.PubMedCrossRefGoogle Scholar
  22. 22.
    Pickard GE, Silverman AJ. Effects of photoperiod on hypothalamic luteinizing hormone releasing hormone in the male hamster. J Endocrinol 1979;83:421–8.PubMedGoogle Scholar
  23. 23.
    Chen HJ. Luteinizing hormone releasing hormone prevents testicular atrophy in golden hamsters exposed to a short photoperiod: temporal difference in effectiveness of administration of luteinizing hormone releasing hormone. J Endocrinol 1983;96:147–54.PubMedGoogle Scholar
  24. 24.
    Pieper DR. Effects of photoperiod, castration, and gonadotropin-releasing hormone (GnRH) on the number of GnRH receptors in male golden hamsters. Endocrinology 1984;115:1857–62.PubMedCrossRefGoogle Scholar
  25. 25.
    Goldman BD. The circadian timing system and reproduction in mammals. Steroids 1999;64:679–85.PubMedCrossRefGoogle Scholar
  26. 26.
    Karsch FJ, Dahl GE, Evans NP, Manning JM, Mayfield KP, Moenter SM, et al. Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biol Reprod 1993;49:1377–83.PubMedCrossRefGoogle Scholar
  27. 27.
    Tamarkin L, Hutchison JS, Goldman BD. Regulation of serum gonadotropins by photoperiod and testicular hormone in the Syrian hamster. Endocrinology 1976;99:1528–33.PubMedGoogle Scholar
  28. 28.
    Goodman RL, Bittman EL, Foster DL, Karsch FJ. Alterations in the control of luteinizing hormone pulse frequency underlie the seasonal variation in estradiol negative feedback in the ewe. Biol Reprod 1982;27:580–9.PubMedCrossRefGoogle Scholar
  29. 29.
    Bittman EL, Goldman BD. Serum levels of gonadotrophins in hamsters exposed to short photoperiods: effects of adrenalectomy and ovariectomy. J Endocrinol 1979;83:113–8.PubMedGoogle Scholar
  30. 30.
    Hastings MH, Walker AP, Roberts AC, Herbert J. Intra-hypothalamic melatonin blocks photoperiodic responsiveness in the male Syrian hamster. Neuroscience 1988;24:987–91.PubMedCrossRefGoogle Scholar
  31. 31.
    Lincoln GA, Maeda K. Effects of placing micro-implants of melatonin in the mediobasal hypothalamus and preoptic area on the secretion of prolactin and beta-endorphin in rams. J Endocrinol 1992;134:437–48.PubMedCrossRefGoogle Scholar
  32. 32.
    Malpaux B, Daveau A, Maurice F, Gayrard V, Thiery JC. Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod 1993;48:752–60.PubMedCrossRefGoogle Scholar
  33. 33.
    Maywood ES, Hastings MH. Lesions of the iodomelatonin-binding sites of the mediobasal hypothalamus spare the lactotropic, but block the gonadotropic response of male Syrian hamsters to short photoperiod and to melatonin. Endocrinology 1995;136:144–53.PubMedCrossRefGoogle Scholar
  34. 34.
    Bae HH, Mangels RA, Cho BS, Dark J, Yellon SM, Zucker I. Ventromedial hypothalamic mediation of photoperiodic gonadal responses in male Syrian hamsters. J Biol Rhythms 1999;14:391–401.PubMedCrossRefGoogle Scholar
  35. 35.
    Lewis D, Freeman DA, Dark J, Wynne-Edwards KE, Zucker I. Photoperiodic control of oestrous cycles in Syrian hamsters: mediation by the mediobasal hypothalamus. J Neuroendocrinol 2002;14:294–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001;411:613–7.PubMedCrossRefGoogle Scholar
  37. 37.
    Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, et al. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 2001;276:28969–75.PubMedCrossRefGoogle Scholar
  38. 38.
    Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001;276:34631–6.PubMedCrossRefGoogle Scholar
  39. 39.
    Terao Y, Kumano S, Takatsu Y, Hattori M, Nishimura A, Ohtaki T, et al. Expression of KiSS-1, a metastasis suppressor gene, in trophoblast giant cells of the rat placenta. Biochim Biophys Acta 2004;1678:102–10.PubMedGoogle Scholar
  40. 40.
    Stafford LJ, Xia C, Ma W, Cai Y, Liu M. Identification and characterization of mouse metastasis-suppressor KiSS1 and its G-protein-coupled receptor. Cancer Res 2002;62:5399–404.PubMedGoogle Scholar
  41. 41.
    Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Jr., Shagoury JK, et al. The GPR54 gene as a regulator of puberty. N Engl J Med 2003;349:1614–27.PubMedCrossRefGoogle Scholar
  42. 42.
    de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 2003;100:10972–6.PubMedCrossRefGoogle Scholar
  43. 43.
    Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, et al. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003;312:1357–63.PubMedCrossRefGoogle Scholar
  44. 44.
    Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, et al. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004;145:4073–7.PubMedCrossRefGoogle Scholar
  45. 45.
    Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005;102:2129–34.PubMedCrossRefGoogle Scholar
  46. 46.
    Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, et al. Involvement of central metastin in the regulation of preovulatory LH surge and estrous cyclicity in female rats. Endocrinology 2005;146:4431–6.PubMedCrossRefGoogle Scholar
  47. 47.
    Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005;146:3686–92.PubMedCrossRefGoogle Scholar
  48. 48.
    Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005;146:2976–84.PubMedCrossRefGoogle Scholar
  49. 49.
    Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006;401:225–30.PubMedCrossRefGoogle Scholar
  50. 50.
    Clarkson J, Herbison AE. Postnatal development Of Kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006;147:5817–25.PubMedCrossRefGoogle Scholar
  51. 51.
    Mikkelsen JD, Revel FG, Larsen L, Caraty A, Simonneaux V: Distribution and function of kisspeptins and their receptor GPR54 in the rodent brain (“Abstract”). Society for Neuroscience’s 36th Annual Meeting, Atlanta, USA, 2006Google Scholar
  52. 52.
    Revel FG, Saboureau M, Masson-Pevet M, Pevet P, Mikkelsen JD, Simonneaux V. KiSS-1: a likely candidate for the photoperiodic control of reproduction in seasonal breeders. Chronobiol Int 2006;23:277–87.PubMedCrossRefGoogle Scholar
  53. 53.
    Revel FG, Saboureau M, Masson-Pevet M, Pevet P, Mikkelsen JD, Simonneaux V. Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol 2006;16:1730–5.PubMedCrossRefGoogle Scholar
  54. 54.
    Parhar IS, Ogawa S, Sakuma Y. Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology 2004;145:3613–8.PubMedCrossRefGoogle Scholar
  55. 55.
    Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004;80:264–72.PubMedCrossRefGoogle Scholar
  56. 56.
    Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci U S A 2005;102:1761–6.PubMedCrossRefGoogle Scholar
  57. 57.
    Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, et al. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005;25:11349–56.PubMedCrossRefGoogle Scholar
  58. 58.
    Lee DK, Nguyen T, O’Neill GP, Cheng R, Liu Y, Howard AD, et al. Discovery of a receptor related to the galanin receptors. FEBS Lett 1999;446:103–7.PubMedCrossRefGoogle Scholar
  59. 59.
    Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, et al. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004;145:4565–74.PubMedCrossRefGoogle Scholar
  60. 60.
    Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 2006;26:6687–94.PubMedCrossRefGoogle Scholar
  61. 61.
    Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, et al. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 2004;561:379–86.PubMedCrossRefGoogle Scholar
  62. 62.
    Roa J, Vigo E, Castellano JM, Navarro VM, Fernandez-Fernandez R, Casanueva FF, et al. Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female Rat. Endocrinology 2006;147:2864–78.PubMedCrossRefGoogle Scholar
  63. 63.
    Castellano JM, Navarro VM, Fernandez-Fernandez R, Nogueiras R, Tovar S, Roa J, et al. Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by Kisspeptin in undernutrition. Endocrinology 2005;146:3917–25.PubMedCrossRefGoogle Scholar
  64. 64.
    Smith JT, Acohido BV, Clifton DK, Steiner RA. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J Neuroendocrinol 2006;18:298–303.PubMedCrossRefGoogle Scholar
  65. 65.
    Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 2004;320:383–8.PubMedCrossRefGoogle Scholar
  66. 66.
    Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, et al. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004;16:850–8.PubMedCrossRefGoogle Scholar
  67. 67.
    Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, et al. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005;146:1689–97.PubMedCrossRefGoogle Scholar
  68. 68.
    Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, et al. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005;146:156–63.PubMedCrossRefGoogle Scholar
  69. 69.
    Maywood ES, Bittman EL, Hastings MH. Lesions of the melatonin- and androgen-responsive tissue of the dorsomedial nucleus of the hypothalamus block the gonadal response of male Syrian hamsters to programmed infusions of melatonin. Biol Reprod 1996;54:470–7.PubMedCrossRefGoogle Scholar
  70. 70.
    Hoffmann K. Effects of short photoperiods on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J Reprod Fertil 1978;54:29–35.PubMedCrossRefGoogle Scholar
  71. 71.
    Ebling FJ, Foster DL. Pineal melatonin rhythms and the timing of puberty in mammals. Experientia 1989;45:946–54.PubMedCrossRefGoogle Scholar
  72. 72.
    Shaw D, Goldman BD. Influence of prenatal and postnatal photoperiods on postnatal testis development in the Siberian hamster (Phodopus sungorus). Biol Reprod 1995;52:833–8.PubMedCrossRefGoogle Scholar
  73. 73.
    Bronson FH, Heideman PD. Seasonal regulation of reproduction in mammals. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York: Raven; 1994. p. 541–83.Google Scholar
  74. 74.
    Smith JT, Clay CM, Caraty A, Clarke IJ. KiSS-1 mRNA expression in the Hypothalamus of the Ewe is regulated by sex steroids and season. Endocrinology doi  10.1210/en. 2006;1435.
  75. 75.
    Pompolo S, Pereira A, Estrada KM, Clarke IJ. Co-localisation of Kisspeptin and gonadotropin releasing hormone in the ovine brain. Endocrinology 2006;147:804–10.PubMedCrossRefGoogle Scholar
  76. 76.
    Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ. Elevated KiSS-1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotrophin-releasing hormone/lutenising hormone surge in the ewe suggests a stimulatory role for kisspeptin in oestrogen-positive feedback. J Neuroendocrinol 2006;18:806–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P. Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 1998;139:1508–16.PubMedCrossRefGoogle Scholar
  78. 78.
    Chabot V, Caldani M, de Reviers MM, Pelletier J. Localization and quantification of melatonin receptors in the diencephalon and posterior telencephalon of the sheep brain. J Pineal Res 1998;24:50–7.PubMedCrossRefGoogle Scholar
  79. 79.
    Ubuka T, Bentley GE, Ukena K, Wingfield JC, Tsutsui K. Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc Natl Acad Sci U S A 2005;102:3052–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Ross AW, Webster CA, Mercer JG, Moar KM, Ebling FJ, Schuhler S, et al. Photoperiodic regulation of hypothalamic retinoid signaling: association of retinoid X receptor gamma with body weight. Endocrinology 2004;145:13–20.PubMedCrossRefGoogle Scholar
  81. 81.
    Watanabe M, Yasuo S, Watanabe T, Yamamura T, Nakao N, Ebihara S, et al. Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology 2004;145:1546–9.PubMedCrossRefGoogle Scholar
  82. 82.
    Revel FG, Saboureau M, Pevet P, Mikkelsen JD, Simonneaux V. Melatonin regulates type 2 deiodinase gene expression in the Syrian hamster. Endocrinology 2006;147:4680–7.PubMedCrossRefGoogle Scholar
  83. 83.
    Barrett P, Ross AW, Balik A, Littlewood PA, Mercer JG, Moar KM, et al. Photoperiodic regulation of histamine H3 receptor and VGF messenger ribonucleic acid in the arcuate nucleus of the Siberian hamster. Endocrinology 2005;146:1930–9.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Florent G. Revel
    • 1
  • Laura Ansel
    • 1
  • Paul Klosen
    • 1
  • Michel Saboureau
    • 1
  • Paul Pévet
    • 1
  • Jens D. Mikkelsen
    • 2
  • Valérie Simonneaux
    • 1
    Email author
  1. 1.Institut des Neurosciences Cellulaires et Intégratives, Département de Neurobiologie des RythmesUMR-7168/LC2 CNRS-Université Louis PasteurStrasbourgFrance
  2. 2.Department of Translational NeurobiologyNeuroSearch A/SBallerupDenmark

Personalised recommendations