Orexin/hypocretin plays a role in the response to physiological disequilibrium

Sleep Medicine Reviews

Volumn 15, Issue 3, 2011, Pages 197-207

  Sinton, Christopher M ^a  

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

Author keywords

Cataplexy; Dopamine; Energy balance; GABA; Histamine; Metabolism; Orexin antagonist; Reticular formation

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; GALANIN; HISTAMINE H1 RECEPTOR; NEUROPEPTIDE; OREXIN; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; OREXIN A; OREXIN B;

ACETYLCHOLINE RELEASE; ALERTNESS; AROUSAL; CATAPLEXY; CENTRAL NERVOUS SYSTEM; FOOD DEPRIVATION; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MUSCLE WEAKNESS; NARCOLEPSY; NERVE CELL EXCITABILITY; NEUROENDOCRINE SYSTEM; NONHUMAN; PONS RETICULAR FORMATION; REVIEW; SLEEP WAKING CYCLE; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AROUSAL; BRAIN; CATAPLEXY; DOPAMINE; ENERGY METABOLISM; GAMMA-AMINOBUTYRIC ACID; HISTAMINE; HOMEOSTASIS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NARCOLEPSY; NEUROPEPTIDES; RETICULAR FORMATION; SIGNAL TRANSDUCTION; SLEEP; WAKEFULNESS;

EID: 79955021431     PISSN: 10870792     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smrv.2010.12.003     Document Type: Review

References (96)

1. Siegel J.M. Narcolepsy: a key role for hypocretins (orexins). Cell 1999, 98:409-412.
2. Lin L., Faraco J., Li R., Kadotani H., Rogers W., Lin X., et al. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 1999, 98:365-376.
3. Chemelli R.M., Willie J.T., Sinton C.M., Elmquist J.K., Scammell T., Lee C., et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 1999, 98:437-451.
4. Nishino S., Ripley B., Overeem S., Lammers G.J., Mignot E. Hypocretin (orexin) deficiency in human narcolepsy. Lancet 2000, 355:39-40.
5. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:573-585.
6. Sakurai T. Orexins and orexin receptors: implication in feeding behavior. Regul Pept 1999, 85:25-30.
7. Danguir J., Nicolaidis S. Intravenous infusions of nutrients and sleep in the rat: an ischymetric sleep regulation hypothesis. Am J Physiol 1980, 238:E307-E312.
8. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 1998, 18:9996-10015.
9. Cluderay J.E., Harrison D.C., Hervieu G.J. Protein distribution of the orexin-2 receptor in the rat central nervous system. Regul Pept 2002, 104:131-144.
10. Hervieu G.J., Cluderay J.E., Harrison D.C., Roberts J.C., Leslie R.A. Gene expression and protein distribution of the orexin-1 receptor in the rat brain and spinal cord. Neuroscience 2001, 103:777-797.
11. Hoang Q.V., Bajic D., Yanagisawa M., Nakajima S., Nakajima Y. Effects of orexin (hypocretin) on GIRK channels. J Neurophysiol 2003, 90:693-702.
12. Karteris E., Machado R.J., Chen J., Zervou S., Hillhouse E.W., Randeva H.S. Food deprivation differentially modulates orexin receptor expression and signaling in rat hypothalamus and adrenal cortex. Am J Physiol Endocrinol Metab 2005, 288:E1089-E1100.
13. Overeem S., Mignot E., van Dijk J.G., Lammers G.J. Narcolepsy: clinical features, new pathophysiologic insights, and future perspectives. J Clin Neurophysiol 2001, 18:78-105.
14. Overeem S., Black J.L., Lammers G.J. Narcolepsy: immunological aspects. Sleep Med Rev 2008, 12:95-107.
15. Kroeger D., de Lecea L. The hypocretins and their role in narcolepsy. CNS Neurol Disord Drug Targets 2009, 8:271-280.
16. Peyron C., Faraco J., Rogers W., Ripley B., Overeem S., Charnay Y., et al. A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 2000, 6:991-997.
17. Crocker A., Espana R.A., Papadopoulou M., Saper C.B., Faraco J., Sakurai T., et al. Concomitant loss of dynorphin, NARP, and orexin in narcolepsy. Neurology 2005, 65:1184-1188.
18. Bassetti C., Aldrich M.S. Narcolepsy. Neurol Clin 1996, 14:545-571.
19. McCarley R.W. Neurobiology of REM and NREM sleep. Sleep Med 2007, 8:302-330.
20. Fort P., Bassetti C.L., Luppi P.H. Alternating vigilance states: new insights regarding neuronal networks and mechanisms. Eur J Neurosci 2009, 29:1741-1753.
21. Marks G.A., Sinton C.M. The role of GABAergic nodulation of nesopontine cholinergic neurotransmission in rapid eye movement (REM) sleep. GABA and sleep: molecular, functional and clinical aspects 2010, 253-278. Springer Basel, Basel. J.M. Monti, S.R. Pandi-Perumal, H. Mohler (Eds.).
22. Nishino S., Riehl J., Hong J., Kwan M., Reid M., Mignot E. Is narcolepsy a REM sleep disorder? Analysis of sleep abnormalities in narcoleptic Dobermans. Neurosci Res 2000, 38:437-446.
23. Kisanuki Y.Y., Chemelli R.M., Tokita S., Willie J.T., Sinton C.M., Yanagisawa M. Behavioral and polysomnographic characterization of orexin-1 receptor and orexin-2 receptor double knockout mice. Sleep 2001, 24:A22.
24. Hara J., Beuckmann C.T., Nambu T., Willie J.T., Chemelli R.M., Sinton C.M., et al. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 2001, 30:345-354.
25. Willie J.T., Chemelli R.M., Sinton C.M., Tokita S., Williams S.C., Kisanuki Y.Y., et al. Distinct narcolepsy syndromes in orexin receptor-2 and orexin null mice: molecular genetic dissection of non-REM and REM sleep regulatory processes. Neuron 2003, 38:715-730.
26. Kisanuki Y.Y., Chemelli R.M., Sinton C.M., Williams S.C., Richardson J.A., Hammer R.E., et al. The role of orexin receptor type-1 (OX1R) in the regulation of sleep. Sleep 2000, 23:A91.
27. Dugovic C., Shelton J.E., Aluisio L.E., Fraser I.C., Jiang X., Sutton S.W., et al. Blockade of orexin-1 receptors attenuates orexin-2 receptor antagonism-induced sleep promotion in the rat. J Pharmacol Exp Ther 2009, 330:142-151.
28. Okura M., Fujiki N., Kita I., Honda K., Yoshida Y., Mignot E., et al. The roles of midbrain and diencephalic dopamine cell groups in the regulation of cataplexy in narcoleptic Dobermans. Neurobiol Dis 2004, 16:274-282.
29. Burgess C., Tse G., Peever J. Dopaminergic modulation of cataplexy in hypocretin-null mice. Sleep 2008, 31:A5.
30. Dahan L., Astier B., Vautrelle N., Urbain N., Kocsis B., Chouvet G. Prominent burst firing of dopaminergic neurons in the ventral tegmental area during paradoxical sleep. Neuropsychopharmacology 2007, 32:1232-1241.
31. Saper C.B., Chou T.C., Scammell T.E. The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci 2001, 24:726-731.
32. Szymusiak R., Alam N., Steininger T.L., McGinty D. Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res 1998, 803:178-188.
33. Chou T.C., Bjorkum A.A., Gaus S.E., Lu J., Scammell T.E., Saper C.B. Afferents to the ventrolateral preoptic nucleus. J Neurosci 2002, 22:977-990.
34. Gallopin T., Fort P., Eggermann E., Cauli B., Luppi P.H., Rossier J., et al. Identification of sleep-promoting neurons in vitro. Nature 2000, 404:992-995.
35. Hagan J.J., Leslie R.A., Patel S., Evans M.L., Wattam T.A., Holmes S., et al. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci U S A 1999, 96:10911-10916.
36. Eggermann E., Serafin M., Bayer L., Machard D., Saint-Mleux B., Jones B.E., et al. Orexins/hypocretins excite basal forebrain cholinergic neurones. Neuroscience 2001, 108:177-181.
37. Eriksson K.S., Sergeeva O., Brown R.E., Haas H.L. Orexin/hypocretin excites the histaminergic neurons of the tuberomammillary nucleus. J Neurosci 2001, 21:9273-9279.
38. Brown R.E., Sergeeva O., Eriksson K.S., Haas H.L. Orexin A excites serotonergic neurons in the dorsal raphe nucleus of the rat. Neuropharmacology 2001, 40:457-459.
39. Burlet S., Tyler C.J., Leonard C.S. Direct and indirect excitation of laterodorsal tegmental neurons by hypocretin/orexin peptides: implications for wakefulness and narcolepsy. J Neurosci 2002, 22:2862-2872.
40. Kohlmeier K.A., Inoue T., Leonard C.S. Hypocretin/orexin peptide signaling in the ascending arousal system: elevation of intracellular calcium in the mouse dorsal raphe and laterodorsal tegmentum. J Neurophysiol 2004, 92:221-235.
41. Lu J., Greco M.A., Shiromani P., Saper C.B. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 2000, 20:3830-3842.
42. Lu J., Sherman D., Devor M., Saper C.B. A putative flip-flop switch for control of REM sleep. Nature 2006, 441:589-594.
43. Hishikawa Y., Shimizu T. Physiology of REM sleep, cataplexy, and sleep paralysis. Adv Neurol 1995, 67:245-271.
44. Roth B., Bruhova S., Lehovsky M. REM sleep and NREM sleep in narcolepsy and hypersomnia. Electroencephalogr Clin Neurophysiol 1969, 26:176-182.
45. Vetrugno R., D'Angelo R., Moghadam K.K., Vandi S., Franceschini C., Mignot E., et al. Behavioural and neurophysiological correlates of human cataplexy: a video-polygraphic study. Clin Neurophysiol 2010, 121:153-162.
46. Overeem S., Lammers G.J., van Dijk J.G. Cataplexy: 'tonic immobility' rather than 'REM-sleep atonia'?. Sleep Med 2002, 3:471-477.
47. Brischoux F., Mainville L., Jones B.E. Muscarinic-2 and orexin-2 receptors on GABAergic and other neurons in the rat mesopontine tegmentum and their potential role in sleep-wake state control. J Comp Neurol 2008, 510:607-630.
48. Beuckmann C.T., Sinton C.M., Williams S.C., Richardson J.A., Hammer R.E., Sakurai T., et al. Expression of a poly-glutamine-ataxin-3 transgene in orexin neurons induces narcolepsy-cataplexy in the rat. J Neurosci 2004, 24:4469-4477.
49. Scammell T.E., Willie J.T., Guilleminault C., Siegel J.M. A consensus definition of cataplexy in mouse models of narcolepsy. Sleep 2009, 32:111-116.
50. Gulyani S., Wu M.F., Nienhuis R., John J., Siegel J.M. Cataplexy-related neurons in the amygdala of the narcoleptic dog. Neuroscience 2002, 112:355-365.
51. John J., Wu M.F., Boehmer L.N., Siegel J.M. Cataplexy-active neurons in the hypothalamus: implications for the role of histamine in sleep and waking behavior. Neuron 2004, 42:619-634.
52. Sutcliffe J.G., de Lecea L. The hypocretins: setting the arousal threshold. Nat Rev Neurosci 2002, 3:339-349.
53. Jones B.E. Arousal systems. Front Biosci 2003, 8:S438-S451.
54. Szymusiak R. Magnocellular nuclei of the basal forebrain: substrates of sleep and arousal regulation. Sleep 1995, 18:478-500.
55. von Economo C. Sleep as a problem of localization. J Nerv Ment Dis 1930, 71:249-259.
56. Sherin J.E., Elmquist J.K., Torrealba F., Saper C.B. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 1998, 18:4705-4721.
57. Steininger T.L., Alam M.N., Gong H., Szymusiak R., McGinty D. Sleep-waking discharge of neurons in the posterior lateral hypothalamus of the albino rat. Brain Res 1999, 840:138-147.
58. Mileykovskiy B.Y., Kiyashchenko L.I., Siegel J.M. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005, 46:787-798.
59. Lee M.G., Hassani O.K., Jones B.E. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J Neurosci 2005, 25:6716-6720.
60. Takahashi K., Lin J.S., Sakai K. Neuronal activity of orexin and non-orexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 2008, 153:860-870.
61. Vanni-Mercier G., Sakai K., Jouvet M. Specific neurons for wakefulness in the posterior hypothalamus in the cat. C R Acad Sci 1984, 298:195-200.
62. McGinty D.J., Harper R.M. Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 1976, 101:569-575.
63. Aston-Jones G., Bloom F.E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1981, 1:876-886.
64. Adamantidis A.R., Zhang F., Aravanis A.M., Deisseroth K., de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 2007, 450:420-424.
65. Carter M.E., Adamantidis A., Ohtsu H., Deisseroth K., de Lecea L. Sleep homeostasis modulates hypocretin-mediated sleep-to-wake transitions. J Neurosci 2009, 29:10939-10949.
66. Nishino S., Fujiki N., Ripley B., Sakurai E., Kato M., Watanabe T., et al. Decreased brain histamine content in hypocretin/orexin receptor-2 mutated narcoleptic dogs. Neurosci Lett 2001, 313:125-128.
67. Nishino S., Sakurai E., Nevsimalova S., Yoshida Y., Watanabe T., Yanai K., et al. Decreased CSF histamine in narcolepsy with and without low CSF hypocretin-1 in comparison to healthy controls. Sleep 2009, 32:175-180.
68. Huang Z.L., Qu W.M., Li W.D., Mochizuki T., Eguchi N., Watanabe T., et al. Arousal effect of orexin A depends on activation of the histaminergic system. Proc Natl Acad Sci U S A 2001, 98:9965-9970.
69. Yasuko S., Atanda A.M., Masato M., Kazuhiko Y., Kazuki H. Alpha-fluoromethylhistidine, a histamine synthesis inhibitor, inhibits orexin-induced wakefulness in rats. Behav Brain Res 2010, 207:151-154.
70. Hong Z.Y., Huang Z.L., Qu W.M., Eguchi N. Orexin A promotes histamine, but not norepinephrine or serotonin, release in frontal cortex of mice. Acta Pharmacol Sin 2005, 26:155-159.
71. Parmentier R., Ohtsu H., Djebbara-Hannas Z., Valatx J.L., Watanabe T., Lin J.S. Anatomical, physiological, and pharmacological characteristics of histidine decarboxylase knock-out mice: evidence for the role of brain histamine in behavioral and sleep-wake control. J Neurosci 2002, 22:7695-7711.
72. Anaclet C., Parmentier R., Ouk K., Guidon G., Buda C., Sastre J.P., et al. Orexin/hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J Neurosci 2009, 29:14423-14438.
73. Burgess C.R. Histamine and orexin in the control of arousal, locomotion, and motivation. J Neurosci 2010, 30:2810-2811.
74. Harris G.C., Wimmer M., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005, 437:556-559.
75. Borbely A.A. Sleep in the rat during food deprivation and subsequent restitution of food. Brain Res 1977, 124:457-471.
76. Dewasmes G., Duchamp C., Minaire Y. Sleep changes in fasting rats. Physiol Behav 1989, 46:179-184.
77. Yamanaka A., Beuckmann C.T., Willie J.T., Hara J., Tsujino N., Mieda M., et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 2003, 38:701-713.
78. Williams G., Cai X.J., Elliott J.C., Harrold J.A. Anabolic neuropeptides. Physiol Behav 2004, 81:211-222.
79. Burdakov D., Gerasimenko O., Verkhratsky A. Physiological changes in glucose differentially modulate the excitability of hypothalamic melanin-concentrating hormone and orexin neurons in situ. J Neurosci 2005, 25:2429-2433.
80. Mieda M., Williams S.C., Sinton C.M., Richardson J.A., Sakurai T., Yanagisawa M. Orexin neurons function in an efferent pathway of a food-entrainable circadian oscillator in eliciting food-anticipatory activity and wakefulness. J Neurosci 2004, 24:10493-10501.
81. Williams R.H., Jensen L.T., Verkhratsky A., Fugger L., Burdakov D. Control of hypothalamic orexin neurons by acid and CO2. Proc Natl Acad Sci U S A 2007, 104:10685-10690.
82. de Lecea L., Sutcliffe J.G., Fabre V. Hypocretins/orexins as integrators of physiological information: lessons from mutant animals. Neuropeptides 2002, 36:85-95.
83. Zhang S., Zeitzer J.M., Sakurai T., Nishino S., Mignot E. Sleep/wake fragmentation disrupts metabolism in a mouse model of narcolepsy. J Physiol 2007, 581:649-663.
84. Diniz Behn C.G., Kopell N., Brown E.N., Mochizuki T., Scammell T.E. Delayed orexin signaling consolidates wakefulness and sleep: physiology and modeling. J Neurophysiol 2008, 99:3090-3103.
85. Wayner M.J., Armstrong D.L., Phelix C.F., Oomura Y. Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo. Peptides 2004, 25:991-996.
86. Aou S., Li X.L., Li A.J., Oomura Y., Shiraishi T., Sasaki K., et al. Orexin-A (hypocretin-1) impairs Morris water maze performance and CA1-Schaffer collateral long-term potentiation in rats. Neuroscience 2003, 119:1221-1228.
87. Selbach O., Bohla C., Barbara A., Doreulee N., Eriksson K.S., Sergeeva O.A., et al. Orexins/hypocretins control bistability of hippocampal long-term synaptic plasticity through co-activation of multiple kinases. Acta Physiol 2010, 198:277-285.
88. Borgland S.L., Taha S.A., Sarti F., Fields H.L., Bonci A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 2006, 49:589-601.
89. Johnson S.W., Seutin V., North R.A. Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science 1992, 258:665-667.
90. Tsai H.C., Zhang F., Adamantidis A., Stuber G.D., Bonci A., de Lecea L., et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 2009, 324:1080-1084.
91. Horvath T.L., Gao X.B. Input organization and plasticity of hypocretin neurons: possible clues to obesity's association with insomnia. Cell Metab 2005, 1:279-286.
92. Rao Y., Liu Z.W., Borok E., Rabenstein R.L., Shanabrough M., Lu M., et al. Prolonged wakefulness induces experience-dependent synaptic plasticity in mouse hypocretin/orexin neurons. J Clin Invest 2007, 117:4022-4033.
93. Samson W.K., Taylor M.M., Ferguson A.V. Non-sleep effects of hypocretin/orexin. Sleep Med Rev 2005, 9:243-252.
94. Spinazzi R., Andreis P.G., Rossi G.P., Nussdorfer G.G. Orexins in the regulation of the hypothalamic-pituitary-adrenal axis. Pharmacol Rev 2006, 58:46-57.
95. Zhang W., Sakurai T., Fukuda Y., Kuwaki T. Orexin neuron-mediated skeletal muscle vasodilation and shift of baroreflex during defense response in mice. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1654-R1663.
96. Kayaba Y., Nakamura A., Kasuya Y., Ohuchi T., Yanagisawa M., Komuro I., et al. Attenuated defense response and low basal blood pressure in orexin knockout mice. Am J Physiol Regul Integr Comp Physiol 2003, 285:R581-R593.