Hypothalamic orexin neurons regulate arousal according to energy balance in mice

Neuron

Volumn 38, Issue 5, 2003, Pages 701-713

  Yamanaka, Akihiro ^a,b,c   Beuckmann, Carsten T ^d   Willie, Jon T ^d   Hara, Junko ^a,b,c   Tsujino, Natsuko ^a,b,c   Mieda, Michihiro ^d   Tominaga, Makoto ^a,b   Yagami, Ken Ichi ^a,b   Sugiyama, Fumihiro ^a,b   Goto, Katsutoshi ^a,b   Yanagisawa, Masashi ^a,c,d   Sakurai, Takeshi ^a,b,c  

^a Institute of Basic Medical Sciences   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GHRELIN; GLUCOSE; LEPTIN; OREXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; BRAIN NERVE CELL; CELL FUNCTION; CONTROLLED STUDY; DIET RESTRICTION; ENERGY BALANCE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HYPOTHALAMUS; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; TRANSGENIC MOUSE; WAKEFULNESS;

EID: 0038521277     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00331-3     Document Type: Article

References (66)

1. Abrahamson E.E., Leak R.K., Moore R.Y. The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport. 12:2001;435-440.
2. Banarer S., Cryer P.E. Sleep-related hypoglycemia-associated autonomic failure in type 1 diabetes. reduced awakening from sleep during hypoglycemia Diabetes. 52:2003;1195-1203.
3. Borbely A.A. Sleep in the rat during food deprivation and subsequent restitution of food. Brain Res. 124:1977;457-471.
4. Cai X.J., Widdowson P.S., Harrold J., Wilson S., Buckingham R.E., Arch J.R., Tadayyon M., Clapham J.C., Wilding J., Williams G. Hypothalamic orexin expression. modulation by blood glucose and feeding Diabetes. 48:1999;2132-2137.
5. Challet E., Pevet P., Malan A. Effect of prolonged fasting and subsequent refeeding on free-running rhythms of temperature and locomotor activity in rats. Behav. Brain Res. 84:1997;275-284.
6. Chemelli R.M., Willie J.T., Sinton C.M., Elmquist J.K., Scammell T., Lee C., Richardson J.A., Williams S.C., Xiong Y., Kisanuki Y.et al. Narcolepsy in orexin knockout mice. molecular genetics of sleep regulation Cell. 98:1999;437-451.
7. Cowley M.A., Smith R.G., Diano S., Tschop M., Pronchuk N., Grove K.L., Strasburger C.J., Bidlingmaier M., Esterman M., Heiman M.L.et al. The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron. 37:2003;649-661.
8. Crisp A.H., Stonehill E., Fenton G.W. The relationship between sleep, nutrition and mood. a study of patients with anorexia nervosa Postgrad. Med. J. 47:1971;207-213.
9. Cummings D.E., Weigle D.S., Frayo R.S., Breen P.A., Ma M.K., Dellinger E.P., Purnell J.Q. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N. Engl. J. Med. 346:2002;1623-1630.
10. Danguir J., Nicolaidis S. Dependence of sleep on nutrients' availability. Physiol. Behav. 22:1979;735-740.
11. Date Y., Ueta Y., Yamashita H., Yamaguchi H., Matsukura S., Kangawa K., Sakurai T., Yanagisawa M., Nakazato M. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc. Natl. Acad. Sci. USA. 96:1999;748-753.
12. de Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., Fukuhara C., Battenberg E.L., Gautvik V.T., Bartlett F.S. 2nd et al. The hypocretins. hypothalamus-specific peptides with neuroexcitatory activity Proc. Natl. Acad. Sci. USA. 95:1998;322-327.
13. Dewasmes G., Duchamp C., Minaire Y. Sleep changes in fasting rats. Physiol. Behav. 46:1989;179-184.
14. Eggermann E., Bayer L., Serafin M., Saint-Mleux B., Bernheim L., Machard D., Jones B.E., Muhlethaler M. The wake-promoting hypocretin-orexin neurons are in an intrinsic state of membrane depolarization. J. Neurosci. 23:2003;1557-1562.
15. Estabrooke I.V., McCarthy M.T., Ko E., Chou T.C., Chemelli R.M., Yanagisawa M., Saper C.B., Scammell T.E. Fos expression in orexin neurons varies with behavioral state. J. Neurosci. 21:2001;1656-1662.
16. Elias C.F., Saper C.B., Maratos-Flier E., Tritos N.A., Lee C., Kelly J., Tatro J.B., Hoffman G.E., Ollmann M.M., Barsh G.S.et al. Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J. Comp. Neurol. 402:1998;442-459.
17. Elias C.F., Aschkenasi C., Lee C., Kelly J., Ahima R.S., Bjorbaek C., Flier J.S., Saper C.B., Elmquist J.K. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron. 23:1999;775-786.
18. Elmquist J.K., Bjorbaek C., Ahima R.S., Flier J.S., Saper C.B. Distributions of leptin receptor mRNA isoforms in the rat brain. J. Comp. Neurol. 395:1998;535-547.
19. Friedman J.M. Obesity in the new millennium. Nature. 404:2000;632-634.
20. Fujiki N., Yoshida Y., Ripley B., Honda K., Mignot E., Nishino S. Changes in CSF hypocretin-1 (orexin A) levels in rats across 24 hours and in response to food deprivation. Neuroreport. 12:2001;993-997.
21. Gais M.A., Born J., Peters A., Schultes B., Heindl B., Fehm H.L., Kern W. Hypoglycemia counterregulation during sleep. Sleep. 26:2003;55-59.
22. Griffond B., Risold P.Y., Jacquemard C., Colard C., Fellmann D. Insulin-induced hypoglycemia increases preprohypocretin (orexin) mRNA in the rat lateral hypothalamic area. Neurosci. Lett. 262:1999;77-80.
23. Guan X.-M., Hong Y., Palyha O.C., McKee K.K., Feighner S.D., Sirinathsinghji D.J.S., Smith R.G., Van der Ploeg L.H.T., Howard A.D. Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Mol. Brain Res. 48:1997;23-29.
24. Hagan J.J., Leslie R.A., Patel S., Evans M.L., Wattam T.A., Holmes S., Benham C.D., Taylor S.G., Routledge C., Hemmati P.et al. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc. Natl. Acad. Sci. USA. 96:1999;10911-10916.
25. Hakansson M., de Lecea L., Sutcliffe J.G., Yanagisawa M., Meister B. Leptin receptor- and STAT3-immunoreactivities in hypocretin/orexin neurons of the lateral hypothalamus. J. Neuroendocrinol. 11:1999;653-663.
26. Hara J., Beuckmann C.T., Nambu T., Willie J.T., Chemelli R.M., Sinton C.M., Sugiyama F., Yagami K., Goto K., Yanagisawa M., Sakurai T. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron. 30:2001;345-354.
27. Harnish M.J., Greenleaf S.R., Orr W.C. A comparison of feeding to cephalic stimulation on postprandial sleepiness. Physiol. Behav. 64:1998;93-96.
28. Honda Y., Doi Y., Ninomiya R., Ninomiya C. Increased frequency of non-insulin-dependent diabetes mellitus among narcoleptic patients. Sleep. 9:1986;254-259.
29. Itoh T., Murai S., Nagahama H., Miyate H., Abe E., Fujiwara H., Saito Y. Effects of 24-hr fasting on methamphetamine- and apomorphine-induced locomotor activities, and on monoamine metabolism in mouse corpus striatum and nucleus accumbens. Pharmacol. Biochem. Behav. 35:1990;391-396.
30. Jones T.W., Porter P., Sherwin R.S., Davis E.A., O'Leary P., Frazer F., Byrne G., Stick S., Tamborlane W.V. Decreased epinephrine responses to hypoglycemia during sleep. N. Engl. J. Med. 338:1998;1657-1662.
31. Karklin A., Driver H.S., Buffenstein R. Restricted energy intake affects nocturnal body temperature and sleep patterns. Am. J. Clin. Nutr. 59:1994;346-349.
32. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 402:1999;656-660.
33. Lawrence C.B., Snape A.C., Baudin F.M., Luckman S.M. Acute central ghrelin and GH secretagogues induce feeding and activate brain appetite centers. Endocrinology. 143:2002;155-162.
34. Lee H.M., Wang G., Englander E.W., Kojima M., Greeley G.H. Jr. Ghrelin, a new gastrointestinal endocrine peptide that stimulates insulin secretion. enteric distribution, ontogeny, influence of endocrine, and dietary manipulations Endocrinology. 143:2002;185-190.
35. Li Y., Gao X.B., Sakurai T., van den Pol A.N. Hypocretin/orexin excites hypocretin neurons via a local glutamate neuron - a potential mechanism for orchestrating the hypothalamic arousal system. Neuron. 36:2002;1169-1181.
36. Lin L., Faraco J., Li R., Kadotani H., Rogers W., Lin X., Qiu X., de Jong P.J., Nishino S., Mignot E. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell. 98:1999;365-376.
37. Lopez M., Seoane L., Garcia M.C., Lago F., Casanueva F.F., Senaris R., Dieguez C. Leptin regulation of prepro-orexin and orexin receptor mRNA levels in the hypothalamus. Biochem. Biophys. Res. Commun. 269:2000;41-45.
38. Lubkin M., Stricker-Krongrad A. Independent feeding and metabolic actions of orexins in mice. Biochem. Biophys. Res. Commun. 253:1998;241-245.
39. Moriguchi T., Sakurai T., Nambu T., Yanagisawa M., Goto K. Neurons containing orexin in the lateral hypothalamic area of the adult rat brain are activated by insulin-induced acute hypoglycemia. Neurosci. Lett. 264:1999;101-104.
40. Nakamura T., Uramura K., Nambu T., Yada T., Goto K., Yanagisawa M., Sakurai T. Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res. 873:2000;181-187.
41. Nakazato M., Murakami N., Date Y., Kojima M., Matsuo H., Kangawa K., Matsukura S. A role for ghrelin in the central regulation of feeding. Nature. 409:2001;194-198.
42. Nambu T., Sakurai T., Mizukami K., Hosoya Y., Yanagisawa M., Goto K. Distribution of orexin neurons in the adult rat brain. Brain Res. 827:1999;243-260.
43. Nishino S., Ripley B., Overeem S., Nevsimalova S., Lammers G.J., Vankova J., Okun M., Rogers W., Brooks S., Mignot E. Low cerebrospinal fluid hypocretin (orexin) and altered energy homeostasis in human narcolepsy. Ann. Neurol. 50:2001;381-388.
44. Oomura Y., Yoshimatsu H. Neural network of glucose monitoring system. J. Auton. Nerv. Syst. 10:1984;359-372.
45. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., Kilduff T.S. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18:1998;9996-10015.
46. Peyron C., Faraco J., Rogers W., Ripley B., Overeem S., Charnay Y., Nevsimalova S., Aldrich M., Reynolds D., Albin R.et al. A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat. Med. 9:2000;991-997.
47. Rivest S. Does circulating leptin have the ability to cross the blood-brain barrier and target neurons directly? Endocrinology. 143:2002;3211-3213.
48. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., Williams S.C., Richardson J.A., Kozlowski G.P., Wilson S.et al. Orexins and orexin receptors. a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior Cell. 92:1998;573-585.
49. Sakurai T., Moriguchi T., Furuya K., Kajiwara N., Nakamura T., Yanagisawa M., Goto K. Structure and function of human prepro-orexin gene. J. Biol. Chem. 274:1999;17771-17776.
50. Schuld A., Hebebrand J., Geller F., Pollmacher T. Increased body-mass index in patients with narcolepsy. Lancet. 355:2000;1274-1275.
51. Shirasaka T., Nakazato M., Matsukura S., Takasaki M., Kannan H. Sympathetic and cardiovascular actions of orexins in conscious rats. Am. J. Physiol. 277:1999;R1780-R1785.
52. Sinton C.M., Fitch T.E., Gershenfeld H.K. The effects of leptin on REM sleep and slow wave delta in rats are reversed by food deprivation. J. Sleep Res. 8:1999;197-203.
53. Smart D., Haynes A.C., Williams G. Orexins and the treatment of obesity. Eur. J. Pharmacol. 440:2002;199-212.
54. Spanswick D., Smith M.A., Groppi V.E., Logan S.D., Ashford M.L.J. Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature. 390:1997;521-552.
55. Thannickal T.C., Moore R.Y., Nienhuis R., Ramanathan L., Gulyani S., Aldrich M., Cornford M., Siegel J.M. Reduced number of hypocretin neurons in human narcolepsy. Neuron. 27:2000;469-474.
56. Tolle V., Bassant M.-H., Zizzari P., Poindessous-Jazat F., Tomasetto C., Epelbaum J., Bluet-Pajot M.-T. Ultradian rhythmicity of ghrelin secretion in relation with GH, feeding behavior, and sleep-wake patterns in rats. Endocrinology. 143:2002;1353-1361.
57. Toshinai K., Date Y., Murakami N., Shimada M., Mondal M.S., Shimbara T., Guan J.L., Wang Q.P., Funahashi H., Sakurai T.et al. Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology. 144:2003;1506-1512.
58. Valentinuzzi V.S., Buxton O.M., Chang A.-M., Scarbrough K., Ferrari E.A.M., Takahashi J.S., Turek F.W. Locomotor response to an open field during C57BL/6J active and inactive phases. differences dependent on conditions of illumination Physiol. Behav. 69:2000;269-275.
59. Wang L., Saint-Pierre D.H., Tache Y. Peripheral ghrelin selectively increases Fos expression in neuropeptide Y-synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci. Lett. 325:2002;47-51.
60. Williams T.D., Chambers J.B., Henderson R.P., Rathotte M.E., Overton J.M. Cardiovascular responses to caloric restriction and thermoneutrality in C57BL/6J mice. Am. J. Physiol. 282:2002;R1459-R1467.
61. Willie J.T., Chemelli R.M., Sinton C.M., Yanagisawa M. To eat or sleep? Orexin in the regulation of feeding and wakefulness. Annu. Rev. Neurosci. 24:2001;429-458.
62. Willie J.T., Chemelli R.M., Sinton C.M., Tokita S., Williams S.C., Kisanuki Y.Y., Marcus J.N., Lee C., Elmquist J.K., Kohlmeier K.A.et al. Distinct narcolepsy syndromes in Orexin Receptor-2 (OX2R) and Orexin null mice. molecular genetic dissection of non-REM and REM sleep regulatory processes Neuron. 38:2003;715-730. this issue,
63. Yamamoto Y., Ueta Y., Date Y., Nakazato M., Hara Y., Serino R., Nomura M., Shibuya I., Matsukura S., Yamashita H. Down regulation of the prepro-orexin gene expression in genetically obese mice. Brain Res. Mol. Brain Res. 65:1999;14-22.
64. Yamanaka A., Kunii K., Nambu T., Tsujino N., Sakai A., Matsuzaki I., Miwa Y., Goto K., Sakurai T. Orexin-induced food intake involves neuropeptide Y pathway. Brain Res. 24:2000;404-409.
65. Yamanaka A., Muraki Y., Tsujino N., Goto K., Sakurai T. Regulation of orexin neurons by the monoaminergic and cholinergic systems. Biochem. Biophys. Res. Commun. 28:2003;120-129.
66. Yoshida Y., Fujiki N., Nakajima T., Ripley B., Matsumura H., Yoneda H., Mignot E., Nishino S. Fluctuation of extracellular hypocretin-1 (orexin A) levels in the rat in relation to the light-dark cycle and sleep-wake activities. Eur. J. Neurosci. 14:2001;1075-1081.