Neuromedin s-producing neurons act as essential pacemakers in the suprachiasmatic nucleus to couple clock neurons and dictate circadian rhythms

Neuron

Volumn 85, Issue 5, 2015, Pages 1086-1102

  Lee, Ivan T ^a   Chang, Alexander S ^a   Manandhar, Manabu ^a   Shan, Yongli ^a   Fan, Junmei ^a   Izumo, Mariko ^a   Ikeda, Yuichi ^a,b   Motoike, Toshiyuki ^a,b   Dixon, Shelley ^a,b   Seinfeld, Jeffrey E ^a   Takahashi, Joseph S ^a,b,c   Yanagisawa, Masashi ^a,b,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROMEDIN S; NEUROPEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE; GENE LOSS; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MOLECULAR CLOCK; MOUSE; NEUROTRANSMISSION; NMS GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION; TRANSGENE; ANIMAL; BIOLOGICAL RHYTHM; BIOSYNTHESIS; C57BL MOUSE; NERVE CELL; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; NEUROPEPTIDES; SUPRACHIASMATIC NUCLEUS;

EID: 84924257556     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.02.006     Document Type: Article

References (67)

1. Abrahamson E.E., Moore R.Y. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res. 2001, 916:172-191.
2. Aida R., Moriya T., Araki M., Akiyama M., Wada K., Wada E., Shibata S. Gastrin-releasing peptide mediates photic entrainable signals to dorsal subsets of suprachiasmatic nucleus via induction of Period gene in mice. Mol. Pharmacol. 2002, 61:26-34.
3. Atkins N., Mitchell J.W., Romanova E.V., Morgan D.J., Cominski T.P., Ecker J.L., Pintar J.E., Sweedler J.V., Gillette M.U. Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits. PLoS ONE 2010, 5:e12612.
4. Aton S.J., Colwell C.S., Harmar A.J., Waschek J., Herzog E.D. Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat. Neurosci. 2005, 8:476-483.
5. Bae K., Jin X., Maywood E.S., Hastings M.H., Reppert S.M., Weaver D.R. Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron 2001, 30:525-536.
6. Brancaccio M., Maywood E.S., Chesham J.E., Loudon A.S.I., Hastings M.H. A Gq-Ca2+ axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus. Neuron 2013, 78:714-728.
7. Brown T.M., Hughes A.T., Piggins H.D. Gastrin-releasing peptide promotes suprachiasmatic nuclei cellular rhythmicity in the absence of vasoactive intestinal polypeptide-VPAC2 receptor signaling. J.Neurosci. 2005, 25:11155-11164.
8. Bunger M.K., Wilsbacher L.D., Moran S.M., Clendenin C., Radcliffe L.A., Hogenesch J.B., Simon M.C., Takahashi J.S., Bradfield C.A. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 2000, 103:1009-1017.
9. Chen R., Schirmer A., Lee Y., Lee H., Kumar V., Yoo S.H., Takahashi J.S., Lee C. Rhythmic PER abundance defines a critical nodal point for negative feedback within the circadian clock mechanism. Mol. Cell 2009, 36:417-430.
10. Colwell C.S., Michel S., Itri J., Rodriguez W., Tam J., Lelievre V., Hu Z., Liu X., Waschek J.A. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 285:R939-R949.
11. Evans J.A., Leise T.L., Castanon-Cervantes O., Davidson A.J. Dynamic interactions mediated by nonredundant signaling mechanisms couple circadian clock neurons. Neuron 2013, 80:973-983.
12. Field M.D., Maywood E.S., O'Brien J.A., Weaver D.R., Reppert S.M., Hastings M.H. Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron 2000, 25:437-447.
13. Habig W.H., Bigalke H., Bergey G.K., Neale E.A., Hardegree M.C., Nelson P.G. Tetanus toxin in dissociated spinal cord cultures: long-term characterization of form and action. J.Neurochem. 1986, 47:930-937.
14. Hanada R., Teranishi H., Pearson J.T., Kurokawa M., Hosoda H., Fukushima N., Fukue Y., Serino R., Fujihara H., Ueta Y., et al. Neuromedin U has a novel anorexigenic effect independent of the leptin signaling pathway. Nat. Med. 2004, 10:1067-1073.
15. Harmar A.J., Marston H.M., Shen S., Spratt C., West K.M., Sheward W.J., Morrison C.F., Dorin J.R., Piggins H.D., Reubi J.C., et al. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 2002, 109:497-508.
16. Harrington M.E., Rahmani T., Lee C.A. Effects of damage to SCN neurons and efferent pathways on circadian activity rhythms of hamsters. Brain Res. Bull. 1993, 30:655-669.
17. Herzog E.D. Neurons and networks in daily rhythms. Nat. Rev. Neurosci. 2007, 8:790-802.
18. Hong H.K., Chong J.L., Song W., Song E.J., Jyawook A.A., Schook A.C., Ko C.H., Takahashi J.S. Inducible and reversible Clock gene expression in brain using the tTA system for the study of circadian behavior. PLoS Genet. 2007, 3:e33.
19. Hughes A.T., Fahey B., Cutler D.J., Coogan A.N., Piggins H.D. Aberrant gating of photic input to the suprachiasmatic circadian pacemaker of mice lacking the VPAC2 receptor. J.Neurosci. 2004, 24:3522-3526.
20. Husse J., Zhou X., Shostak A., Oster H., Eichele G. Synaptotagmin10-Cre, a driver to disrupt clock genes in the SCN. J.Biol. Rhythms 2011, 26:379-389.
21. Karatsoreos I.N., Yan L., LeSauter J., Silver R. Phenotype matters: identification of light-responsive cells in the mouse suprachiasmatic nucleus. J.Neurosci. 2004, 24:68-75.
22. Karatsoreos I.N., Romeo R.D., McEwen B.S., Silver R. Diurnal regulation of the gastrin-releasing peptide receptor in the mouse circadian clock. Eur. J. Neurosci. 2006, 23:1047-1053.
23. King D.P., Zhao Y., Sangoram A.M., Wilsbacher L.D., Tanaka M., Antoch M.P., Steeves T.D., Vitaterna M.H., Kornhauser J.M., Lowrey P.L., et al. Positional cloning of the mouse circadian Clock gene. Cell 1997, 89:641-653.
24. Kondratov R.V., Kondratova A.A., Gorbacheva V.Y., Vykhovanets O.V., Antoch M.P. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 2006, 20:1868-1873.
25. Kriegsfeld L.J., LeSauter J., Silver R. Targeted microlesions reveal novel organization of the hamster suprachiasmatic nucleus. J.Neurosci. 2004, 24:2449-2457.
26. Lee J.E., Atkins N., Hatcher N.G., Zamdborg L., Gillette M.U., Sweedler J.V., Kelleher N.L. Endogenous peptide discovery of the rat circadian clock: a focused study of the suprachiasmatic nucleus by ultrahigh performance tandem mass spectrometry. Mol. Cell. Proteomics 2010, 9:285-297.
27. Li L., Tasic B., Micheva K.D., Ivanov V.M., Spletter M.L., Smith S.J., Luo L. Visualizing the distribution of synapses from individual neurons in the mouse brain. PLoS ONE 2010, 5:e11503.
28. Liu A.C., Welsh D.K., Ko C.H., Tran H.G., Zhang E.E., Priest A.A., Buhr E.D., Singer O., Meeker K., Verma I.M., et al. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 2007, 129:605-616.
29. Low-Zeddies S.S., Takahashi J.S. Chimera analysis of the Clock mutation in mice shows that complex cellular integration determines circadian behavior. Cell 2001, 105:25-42.
30. Lowrey P.L., Takahashi J.S. Genetics of circadian rhythms in mammalian model organisms. Adv. Genet. 2011, 74:175-230.
31. Maywood E.S., Chesham J.E., O'Brien J.A., Hastings M.H. A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc. Natl. Acad. Sci. USA 2011, 108:14306-14311.
32. McDearmon E.L., Patel K.N., Ko C.H., Walisser J.A., Schook A.C., Chong J.L., Wilsbacher L.D., Song E.J., Hong H.K., Bradfield C.A., Takahashi J.S. Dissecting the functions of the mammalian clock protein BMAL1 by tissue-specific rescue in mice. Science 2006, 314:1304-1308.
33. Meijer J.H., Rietveld W.J. Neurophysiology of the suprachiasmatic circadian pacemaker in rodents. Physiol. Rev. 1989, 69:671-707.
34. Mieda M., Sakurai T. Bmal1 in the nervous system is essential for normal adaptation of circadian locomotor activity and food intake to periodic feeding. J.Neurosci. 2011, 31:15391-15396.
35. Mohawk J.A., Takahashi J.S. Cell autonomy and synchrony of suprachiasmatic nucleus circadian oscillators. Trends Neurosci. 2011, 34:349-358.
36. Mori K., Miyazato M., Ida T., Murakami N., Serino R., Ueta Y., Kojima M., Kangawa K. Identification of neuromedin S and its possible role in the mammalian circadian oscillator system. EMBO J. 2005, 24:325-335.
37. Morin L.P., Shivers K.Y., Blanchard J.H., Muscat L. Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience 2006, 137:1285-1297.
38. Nakashiba T., Young J.Z., McHugh T.J., Buhl D.L., Tonegawa S. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008, 319:1260-1264.
39. Pendergast J.S., Friday R.C., Yamazaki S. Endogenous rhythms in Period1 mutant suprachiasmatic nuclei invitro do not represent circadian behavior. J.Neurosci. 2009, 29:14681-14686.
40. Ralph M.R., Foster R.G., Davis F.C., Menaker M. Transplanted suprachiasmatic nucleus determines circadian period. Science 1990, 247:975-978.
41. Rogan S.C., Roth B.L. Remote control of neuronal signaling. Pharmacol. Rev. 2011, 63:291-315.
42. Romijn H.J., Sluiter A.A., Wortel J., Van Uum J.F., Buijs R.M. Immunocytochemical evidence for a diurnal rhythm of neurons showing colocalization of VIP with GRP in the rat suprachiasmatic nucleus. J.Comp. Neurol. 1998, 391:397-405.
43. Saper C.B. The central circadian timing system. Curr. Opin. Neurobiol. 2013, 23:747-751.
44. Schoch S., Deák F., Königstorfer A., Mozhayeva M., Sara Y., Südhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001, 294:1117-1122.
45. Schwartz W.J., Gross R.A., Morton M.T. The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker. Proc. Natl. Acad. Sci. USA 1987, 84:1694-1698.
46. Shigeyoshi Y., Taguchi K., Yamamoto S., Takekida S., Yan L., Tei H., Moriya T., Shibata S., Loros J.J., Dunlap J.C., Okamura H. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 1997, 91:1043-1053.
47. Siepka S.M., Takahashi J.S. Forward genetic screens to identify circadian rhythm mutants in mice. Methods Enzymol. 2005, 393:219-229.
48. Silver R., Lehman M.N., Gibson M., Gladstone W.R., Bittman E.L. Dispersed cell suspensions of fetal SCN restore circadian rhythmicity in SCN-lesioned adult hamsters. Brain Res. 1990, 525:45-58.
49. Silver R., LeSauter J., Tresco P.A., Lehman M.N. A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 1996, 382:810-813.
50. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
51. Storch K.F., Paz C., Signorovitch J., Raviola E., Pawlyk B., Li T., Weitz C.J. Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 2007, 130:730-741.
52. Sun Y., Yang Z., Niu Z., Wang W., Peng J., Li Q., Ma M.Y., Zhao Y. The mortality of MOP3 deficient mice with a systemic functional failure. J.Biomed. Sci. 2006, 13:845-851.
53. Taniguchi H., He M., Wu P., Kim S., Paik R., Sugino K., Kvitsiani D., Fu Y., Lu J., Lin Y., et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011, 71:995-1013.
54. Van den Pol A.N., Powley T. A fine-grained anatomical analysis of the role of the rat suprachiasmatic nucleus in circadian rhythms of feeding and drinking. Brain Res. 1979, 160:307-326.
55. Vitaterna M.H., King D.P., Chang A.M., Kornhauser J.M., Lowrey P.L., McDonald J.D., Dove W.F., Pinto L.H., Turek F.W., Takahashi J.S. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 1994, 264:719-725.
56. Vitaterna M.H., Ko C.H., Chang A.M., Buhr E.D., Fruechte E.M., Schook A., Antoch M.P., Turek F.W., Takahashi J.S. The mouse Clock mutation reduces circadian pacemaker amplitude and enhances efficacy of resetting stimuli and phase-response curve amplitude. Proc. Natl. Acad. Sci. USA 2006, 103:9327-9332.
57. Wang L., Sharma K., Deng H.X., Siddique T., Grisotti G., Liu E., Roos R.P. Restricted expression of mutant SOD1 in spinal motor neurons and interneurons induces motor neuron pathology. Neurobiol. Dis. 2008, 29:400-408.
58. Webb A.B., Angelo N., Huettner J.E., Herzog E.D. Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc. Natl. Acad. Sci. USA 2009, 106:16493-16498.
59. Welsh D.K., Logothetis D.E., Meister M., Reppert S.M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995, 14:697-706.
60. Welsh D.K., Takahashi J.S., Kay S.A. Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 2010, 72:551-577.
61. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 1991, 231:482-497.
62. Xu Y., Toh K.L., Jones C.R., Shin J.Y., Fu Y.H., Ptácek L.J. Modeling of a human circadian mutation yields insights into clock regulation by PER2. Cell 2007, 128:59-70.
63. Yamaguchi S., Isejima H., Matsuo T., Okura R., Yagita K., Kobayashi M., Okamura H. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science 2003, 302:1408-1412.
64. Yamamoto M., Wada N., Kitabatake Y., Watanabe D., Anzai M., Yokoyama M., Teranishi Y., Nakanishi S. Reversible suppression of glutamatergic neurotransmission of cerebellar granule cells invivo by genetically manipulated expression of tetanus neurotoxin light chain. J.Neurosci. 2003, 23:6759-6767.
65. Yan L., Okamura H. Gradients in the circadian expression of Per1 and Per2 genes in the rat suprachiasmatic nucleus. Eur. J. Neurosci. 2002, 15:1153-1162.
66. Yoo S.H., Yamazaki S., Lowrey P.L., Shimomura K., Ko C.H., Buhr E.D., Siepka S.M., Hong H.K., Oh W.J., Yoo O.J., et al. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 2004, 101:5339-5346.
67. Zheng B., Larkin D.W., Albrecht U., Sun Z.S., Sage M., Eichele G., Lee C.C., Bradley A. The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 1999, 400:169-173.