Activation of growth hormone secretagogue receptor induces time-dependent clock phase delay in mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 307, Issue 6, 2014, Pages E515-E526

  Zhou, Lan ^a   Gao, Qian ^a   Zhang, Peng ^a   Guo, Shu ^a   Gu, Jingli ^a   Hao, Wei ^a   Cao, Ji Min ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

Author keywords

Growth hormone releasing peptide 6; Growth substances; Nonphotic cues; Phase shift; Prokineticins

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GHRELIN RECEPTOR; GLUTAMIC ACID; GROWTH FACTOR; HISTIDYL DEXTRO TRYPTOPHYLALANYLTRYPTOPHYL DEXTRO PHENYLALANYLLYSINAMIDE; MESSENGER RNA; PER1 PROTEIN; PROKINETICIN 2; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG; CIRCADIAN RHYTHM SIGNALING PROTEIN; GROWTH PROMOTOR; PER1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENERGY METABOLISM; GABAERGIC TRANSMISSION; HORMONE RELEASE; IMMUNOREACTIVITY; IN VIVO STUDY; LIGHT DARK CYCLE; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; ANIMAL; C57BL MOUSE; DRUG EFFECT; DRUG POTENTIATION; FLOW CYTOMETRY; GROWTH HORMONE RELEASING PEPTIDE-6; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; NERVE CELL; NONPHOTIC CUES; PHASE SHIFT; PHYSIOLOGY; PROKINETICINS; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL ANALYSIS;

GROWTH HORMONE RELEASING PEPTIDE-6; GROWTH SUBSTANCES; NONPHOTIC CUES; PHASE SHIFT; PROKINETICINS;

ANIMALS; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DATA INTERPRETATION, STATISTICAL; FLOW CYTOMETRY; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MICE, INBRED C57BL; NEURONS; PERIOD CIRCADIAN PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, GHRELIN; SUPRACHIASMATIC NUCLEUS;

EID: 84907722533     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00535.2013     Document Type: Article

References (54)

1. Bodosi B, Gardi J, Hajdu I, Szentirmai E, Obal F Jr, Krueger JM. Rhythms of ghrelin, leptin, and sleep in rats: effects of the normal diurnal cycle, restricted feeding, and sleep deprivation. Am J Physiol Regul Integr Comp Physiol 287: R1071-R1079, 2004.
2. Cable NT, Drust B, Gregson WA. The impact of altered climatic conditions and altitude on circadian physiology. Physiol Behav 90: 267-273, 2007.
3. Caldelas I, Poirel VJ, Sicard B, Pevet P, Challet E. Circadian profile and photic regulation of clock genes in the suprachiasmatic nucleus of a diurnal mammal Arvicanthis ansorgei. Neuroscience 116: 583-591, 2003.
4. Challet E. Minireview: Entrainment of the Suprachiasmatic Clockwork in Diurnal and Nocturnal Mammals. Endocrinology 148: 5648-5655, 2007.
5. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417: 405-410, 2002.
6. Cordido F, Isidro ML, Nemiña R, Sangiao-Alvarellos S. Ghrelin and growth hormone secretagogues, physiological and pharmacological aspect. Curr Drug Discov Technol 6: 34-42, 2009.
7. Demers A, McNicoll N, Febbraio M, Servant M, Marleau S, Silverstein R, Ong H. Identification of the growth hormone-releasing peptide binding site in CD36: a photoaffinity cross-linking study. Biochem J 382: 417-424, 2004.
8. Ding JM, Chen D, Weber ET, Faiman LE, Rea MA, Gillette MU. Resetting the biological clock: mediation of nocturnal circadian shifts by glutamate and NO. Science 266: 1713-1717, 1994.
9. Ding JM, Faiman LE, Hurst WJ, Kuriashkina LR, Gillette MU. Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. J Neurosci 17: 667-675, 1997.
10. Fukuhara C, Brewer JM, Dirden JC, Bittman EL, Tosini G, Harrington ME. Neuropeptide Y rapidly reduces Period 1 and Period 2 mRNA levels in the hamster suprachiasmatic nucleus. Neurosci Lett 314: 119-122, 2001.
11. Ginty DD, Kornhauser JM, Thompson MA, Bading H, Mayo KE, Takahashi JS, Greenberg ME. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260: 238-241, 1993.
12. Golombek DA, Rosenstein RE. Physiology of circadian entrainment. Physiol Rev 90: 1063-1102, 2010.
13. Guo S, Gao Q, Jiao Q, Hao W, Gao X, Cao JM. Gastric mucosal damage in water immersion stress: Mechanism and prevention with GHRP-6. World J Gastroenterol 18: 3145-3155, 2012.
14. Horikawa K, Yokota S, Fuji K, Akiyama M, Moriya T, Okamura H, Shibata S. Nonphotic entrainment by 5-HT1A/7 receptor agonists accompanied by reduced Per1 and Per2 mRNA levels in the suprachiasmatic nuclei. J Neurosci 20: 5867-5873, 2000.
15. Jud C, Schmutz I, Hampp G, Oster H, Albrecht U. A guideline for analyzing circadian wheel-running behavior in rodents under different lighting conditions. Biol Proced Online 7: 101-16, 2005.
16. Kamegai J, Tamura H, Shimizu T, Ishii S, Tatsuguchi A, Sugihara H, Oikawa S, Kineman RD. The role of pituitary ghrelin in growth hormone (GH) secretion: GH-releasing hormone-dependent regulation of pituitary ghrelin gene expression and peptide content. Endocrinology 145: 3731-3738, 2004.
17. Lee Y, Lee J, Kwon I, Nakajima Y, Ohmiya Y, Son GH, Lee KH, Kim K. Coactivation of the CLOCK-BMAL1 complex by CBP mediates resetting of the circadian clock. J Cell Sci 123: 3547-3557, 2010.
18. Mayr B, Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2: 599-609, 2001.
19. Maywood ES, Mrosovsky N. A molecular explanation of interactions between photic and non-photic circadian clock-resetting stimuli. Gene Expr Patt 1: 27-31, 2001.
20. Means AR. The Year in Basic Science: calmodulin kinase cascades. Mol Endocrinol 22: 2759-2765, 2008.
21. Meijer JH, Rietveld WJ. Neurophysiology of the suprachiasmatic nucleus. Physiol Rev 69: 671-707, 1989.
22. Mendoza J. Circadian clocks: setting time by food. J Neuroendocrinol 19: 127-137, 2006.
23. 2+ channels in rat suprachiasmatic nuclei are required for circadian clock control of behavior. J Biol Rhythms 24: 203-210, 2009.
24. Mistlberger RE, Antle MC. The enigma of behavioral inputs to the circadian clock: a test of function using restraint. Physiol Behav 87: 948-954, 2006.
25. Mondal MS, Date Y, Yamaguchi H, Toshinai K, Tsuruta T, Kangawa K, Nakazato M. Identification of ghrelin and its receptor in neurons of the rat arcuate nucleus. Regul Pept 126: 55-59, 2005.
26. Moreno-Reyes R, Kerkhofs M, L’Hermite-Balériaux M, Thorner MO, Van Cauter E, Copinschi G. Evidence against a role for the growth hormone-releasing peptide axis in human slow-wave sleep regulation. Am J Physiol Endocrinol Metab 274: E779-E784, 1998.
27. Morin LP. The circadian visual system. Brain Res Rev 19: 102-127, 1994.
28. Morin LP. Neuroanatomy of the extended circadian rhythm system. Exp Neurol 243: 4-20, 2013.
29. Mrosovsky N, Reebs SG, Honrado GI, Salmon PA. Behavioural entrainment of circadian rhythms. Experientia 45: 696-702, 1989.
30. Nitabach MN, Sheeba V, Vera DA, Blau J, Holmes TC. Membrane electrical excitability is necessary for the free-running larval Drosophila circadian clock. J Neurobiol 62: 1-13, 2005.
31. O’Neill JS, Reddy AB. The essential role of cAMP/Ca2+ signalling in mammalian circadian timekeeping. Biochem Soc Trans 40: 44-50, 2012.
32. Palus S, Schur R, Akashi YJ, Bockmeyer B, Datta R, Halem H, Dong J, Culler MD, Adams V, Anker SD, Springer J. Ghrelin and its analogues, BIM-28131 and BIM-28125, improve body weight and regulate the expression of MuRF-1 and MAFbx in a rat heart failure model. PLoS One 6: e26865, 2011.
33. Pang J, Xu Q, Xu X, Yin H, Xu R, Guo S, Hao W, Wang L, Chen C, Cao JM. Hexarelin suppresses high lipid diet and vitamin D3-induced atherosclerosis in the rat. Peptides 31: 630-638, 2010.
34. Pitrosky B, Kirsch R, Malan A, Mocaer E, P’evet P. Organization of rat circadian rhythms during daily infusion of melatonin or S20098, a melatonin agonist. Am J Physiol Regul Integr Comp Physiol 277: R812-R828, 1999.
35. Shearman LP, Zylka MJ, Weaver DR, Kolakowski LF Jr, Reppert SM. Two period homologs: circadian expression and photic regulation in the suprachiasmatic nuclei. Neuron 19: 1261-1269, 1997.
36. Shigeyoshi Y, Taguchi K, Yamamoto S, Takekida S, Yan L, Tei H, Moriya T, Shibata S, Loros JJ, Dunlap JC, Okamura H. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 91: 1043-1053, 1997.
37. Slotten HA, Krekling S, Pévet P. Photic and nonphotic effects on the circadian activity rhythm in the diurnal rodent Arvicanthis ansorgei. Behav Brain Res 165: 91-97, 2005.
38. Szentirmai É. Central but not systemic administration of ghrelin induces wakefulness in mice. PLoS One 7: e41172, 2012.
39. Szentirmai E, Kapás L, Krueger JM. Ghrelin microinjection into forebrain sites induces wakefulness and feeding in rats. Am J Physiol Regul Integr Comp Physiol 292: R575-R585, 2007.
40. Tischkau SA, Mitchell JW, Tyan SH, Buchanan GF, Gillette MU. Ca2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J Biol Chem 278: 718-723, 2003.
41. Tolle V, Bassant MH, Zizzari P, Poindessous-Jazat F, Tomasetto C, Epelbaum J, Bluet-Pajot MT. Ultradian rhythmicity of ghrelin secretion in relation with GH, feeding behavior, and sleep-wake patterns in rats. Endocrinology 143: 1353-1361, 2002.
42. van der Lely AJ, Tschöp M, Heiman ML, Ghigo E. Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocr Rev 25: 426-457, 2004.
43. Van Reeth O, Hinch D, Tecco JM, Turek FW. The effects of short periods of immobilization on the hamster circadian clock. Brain Res 545: 208-214, 1991.
44. Wee R, Castrucci AM, Provencio I, Gan L, Van Gelder RN. Loss of photic entrainment and altered free-running circadian rhythms in math5/ mice. J Neurosci 22: 10427-10433, 2002.
45. Weikel JC, Wichniak A, Ising M, Brunner H, Friess E, Held K, Mathias S, Schmid DA, Uhr M, Steiger A. Ghrelin promotes slow-wave sleep in humans. Am J Physiol Endocrinol Metab 284: E407-E415, 2003.
46. Xu X, Ding F, Pang J, Gao X, Xu RK, Hao W, Cao JM, Chen C. Chronic administration of hexarelin attenuates cardiac fibrosis in the spontaneously hypertensive rat. Am J Physiol Heart Circ Physiol 303: H703-H711, 2012.
47. Xu XB, Pang JJ, Cao JM, Ni C, Xu RK, Peng XZ, Yu XX, Guo S, Chen MC, Chen C. GH-releasing peptides improve cardiac dysfunction and cachexia and suppress stress-related hormones and cardiomyocyte apoptosis in rats with heart failure. Am J Physiol Heart Circ Physiol 289: H1643-H1651, 2005.
48. Yan L. Structural and functional changes in the suprachiasmatic nucleus following chronic circadian rhythm perturbation. Neuroscience 183: 99-107, 2011.
49. Yannielli PC, McKinley BJ, Harrington ME. Is novel wheel inhibition of Per1 and Per2 expression linked to phase shift occurrence? Neuroscience 112: 677-685, 2002.
50. Yannielli PC, Molyneux PC, Harrington ME, Golombek DA. Ghrelin effects on the circadian system of mice. J Neurosci 27: 2890-2895, 2007.
51. Zhang C, Ng KL, Li JD, He F, Anderson DJ, Sun YE, Zhou QY. Prokineticin 2 is a target gene of proneural basic helix-loop-helix factors for olfactory bulb neurogenesis. J Biol Chem 282: 6917-6921, 2007.
52. Zhou QY, Cheng MY. Prokineticin 2 and circadian clock output. FEBS J 272: 5703-5709, 2005.
53. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK. Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 494: 528-548, 2006.
54. Zylka MJ, Shearman LP, Weaver DR, Reppert SM. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 20: 1103-1110, 1998.