Attenuated orexinergic signaling underlies depression-like responses induced by daytime light deficiency

Neuroscience

Volumn 272, Issue , 2014, Pages 252-260

  Deats, S P ^a   Adidharma, W ^a   Lonstein, J S ^a   Yan, L ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Diurnal grass rats; Orexin; SB 334867; Seasonal affective disorder

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; OREXIN A; 1-(2-METHYLBENZOXAZOL-6-YL)-3-(1,5)NAPHTHYRIDIN-4-YL UREA; BENZOXAZOLE DERIVATIVE; NEUROPEPTIDE; OREXINS; SIGNAL PEPTIDE; UREA;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATION; BRAIN OREXINERGIC SYSTEM; CIRCADIAN RHYTHM; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; FORCED SWIM TEST; HYPOTHALAMUS; IMMUNOREACTIVITY; MALE; MOOD; NERVOUS SYSTEM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; SEASONAL AFFECTIVE DISORDER; SIGNAL TRANSDUCTION; SUNLIGHT; ANALOGS AND DERIVATIVES; ANIMAL; ANXIETY; DEPRESSION; DISEASE MODEL; LIGHT; METABOLISM; MOTOR ACTIVITY; PHOTOPERIODICITY; PHOTOTHERAPY; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BENZOXAZOLES; CIRCADIAN RHYTHM; DEPRESSION; DISEASE MODELS, ANIMAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGHT; MALE; MOTOR ACTIVITY; NEUROPEPTIDES; PHOTOPERIOD; PHOTOTHERAPY; RATS; SEASONAL AFFECTIVE DISORDER; SIGNAL TRANSDUCTION; UREA;

EID: 84901312352     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.04.069     Document Type: Article

References (83)

1. Adidharma W., Leach G., Yan L. Orexinergic signaling mediates light-induced neuronal activation in the dorsal raphe nucleus. Neuroscience 2012, 220:201-207.
2. Allard J.S., Tizabi Y., Shaffery J.P., Trouth C.O., Manaye K. Stereological analysis of the hypothalamic hypocretin/orexin neurons in an animal model of depression. Neuropeptides 2004, 38:311-315.
3. Arendt D.H., Ronan P.J., Oliver K.D., Callahan L.B., Summers T.R., Summers C.H. Depressive behavior and activation of the orexin/hypocretin system. Behav Neurosci 2013, 127:86-94.
4. Ashkenazy-Frolinger T., Kronfeld-Schor N., Juetten J., Einat H. It is darkness and not light: depression-like behaviors of diurnal unstriped Nile grass rats maintained under a short photoperiod schedule. J Neurosci Methods 2009, 186:165-170.
5. Beiko J., Lander R., Hampson E., Boon F., Cain D.P. Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat. Behav Brain Res 2004, 151:239-253.
6. Blanchong J.A., McElhinny T.L., Mahoney M.M., Smale L. Nocturnal and diurnal rhythms in the unstriped Nile rat, Arvicanthis niloticus. J Biol Rhythms 1999, 14:364-377.
7. Blouin A.M., Fried I., Wilson C.L., Staba R.J., Behnke E.J., Lam H.A., Maidment N.T., Karlsson K.A.E., Lapierre J.L., Siegel J.M. Human hypocretin and melanin-concentrating hormone levels are linked to emotion and social interaction. Nat Commun 2013, 4:1547.
8. Borgland S.L., Labouebe G. Orexin/hypocretin in psychiatric disorders: present state of knowledge and future potential. Neuropsychopharmacology 2010, 35:353-354.
9. Brundin L., Bjorkqvist M., Petersen A., Traskman-Bendz L. Reduced orexin levels in the cerebrospinal fluid of suicidal patients with major depressive disorder. Eur Neuropsychopharmacol 2007, 17:573-579.
10. Brundin L., Bjorkqvist M., Traskman-Bendz L., Petersen A. Increased orexin levels in the cerebrospinal fluid the first year after a suicide attempt. J Affect Disord 2009, 113:179-182.
11. Brundin L., Petersen A., Bjorkqvist M., Traskman-Bendz L. Orexin and psychiatric symptoms in suicide attempters. J Affect Disord 2007, 100:259-263.
12. Chen C.T., Dun S.L., Kwok E.H., Dun N.J., Chang J.K. Orexin A-like immunoreactivity in the rat brain. Neurosci Lett 1999, 260:161-164.
13. Cutler D.J., Morris R., Sheridhar V., Wattam T.A., Holmes S., Patel S., Arch J.R., Wilson S., Buckingham R.E., Evans M.L., Leslie R.A., Williams G. Differential distribution of orexin-A and orexin-B immunoreactivity in the rat brain and spinal cord. Peptides 1999, 20:1455-1470.
14. 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 1999, 96:748-753.
15. Deurveilher S., Semba K. Indirect projections from the suprachiasmatic nucleus to major arousal-promoting cell groups in rat: implications for the circadian control of behavioural state. Neuroscience 2005, 130:165-183.
16. 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 2001, 21:1656-1662.
17. Feng P., Vurbic D., Wu Z., Hu Y., Strohl K.P. Changes in brain orexin levels in a rat model of depression induced by neonatal administration of clomipramine. J Psychopharmacol 2008, 22:784-791.
18. Feng P., Vurbic D., Wu Z., Strohl K.P. Brain orexins and wake regulation in rats exposed to maternal deprivation. Brain Res 2007, 1154:163-172.
19. Fortuyn H.A., Lappenschaar M.A., Furer J.W., Hodiamont P.P., Rijnders C.A., Renier W.O., Buitelaar J.K., Overeem S. Anxiety and mood disorders in narcolepsy: a case-control study. Gen Hosp Psychiatry 2010, 32:49-56.
20. Fujiki N., Yoshida Y., Ripley B., Honda K., Mignot E., Nishino S. Changes in CSF hypocretin-1 (orexin A) levels in rats across 24h and in response to food deprivation. Neuroreport 2001, 12:993-997.
21. Gaillard F., Karten H.J., Sauve Y. Retinorecipient areas in the diurnal murine rodent Arvicanthis niloticus: a disproportionally large superior colliculus. J Comp Neurol 2013, 521:1699-1726.
22. Gotter A.L., Webber A.L., Coleman P.J., Renger J.J., Winrow C.J. International Union of Basic and Clinical Pharmacology. LXXXVI. Orexin receptor function, nomenclature and pharmacology. Pharmacol Rev 2012, 64:389-420.
23. Hale M.W., Lowry C.A. Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology (Berl) 2011, 213:243-264.
24. Harris G.C., Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci 2006, 29:571-577.
25. Harris G.C., Wimmer M., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005, 437:556-559.
26. Hebert M., Dumont M., Paquet J. Seasonal and diurnal patterns of human illumination under natural conditions. Chronobiol Int 1998, 15:59-70.
27. Herrero A.I., Sandi C., Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol Learn Mem 2006, 86:150-159.
28. 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.
29. Huang Y., Zhou W., Zhang Y. Bright lighting conditions during testing increase thigmotaxis and impair water maze performance in BALB/c mice. Behav Brain Res 2012, 226:26-31.
30. Ito N., Yabe T., Gamo Y., Nagai T., Oikawa T., Yamada H., Hanawa T. I.c.v. administration of orexin-A induces an antidepressive-like effect through hippocampal cell proliferation. Neuroscience 2008, 157:720-732.
31. Ito N., Yabe T., Nagai T., Oikawa T., Yamada H., Hanawa T. A possible mechanism underlying an antidepressive-like effect of Kososan, a Kampo medicine, via the hypothalamic orexinergic system in the stress-induced depression-like model mice. Biol Pharm Bull 2009, 32:1716-1722.
32. Janusonis S., Fite K.V. Diurnal variation of c-Fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus). J Comp Neurol 2001, 440:31-42.
33. Johnson P.L., Molosh A., Fitz S.D., Truitt W.A., Shekhar A. Orexin, stress, and anxiety/panic states. Prog Brain Res 2012, 198:133-161.
34. Johnson P.L., Samuels B.C., Fitz S.D., Federici L.M., Hammes N., Early M.C., Truitt W., Lowry C.A., Shekhar A. Orexin 1 receptors are a novel target to modulate panic responses and the panic brain network. Physiol Behav 2012, 107:733-742.
35. Johnson P.L., Truitt W., Fitz S.D., Minick P.E., Dietrich A., Sanghani S., Traskman-Bendz L., Goddard A.W., Brundin L., Shekhar A. A key role for orexin in panic anxiety. Nat Med 2010, 16:111-115.
36. Johnson R.F., Morin L.P., Moore R.Y. Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Res 1988, 462:301-312.
37. Kodama T., Usui S., Honda Y., Kimura M. High Fos expression during the active phase in orexin neurons of a diurnal rodent, Tamias sibiricus barberi. Peptides 2005, 26:631-638.
38. Leach G., Adidharma W., Yan L. Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). PLoS One 2013, 8:e57115.
39. Leach G., Ramanathan C., Langel J., Yan L. Responses of brain and behavior to changing day-length in the diurnal grass rat (Arvicanthis niloticus). Neuroscience 2013, 234C:31-39.
40. Leak R.K., Moore R.Y. Identification of retinal ganglion cells projecting to the lateral hypothalamic area of the rat. Brain Res 1997, 770:105-114.
41. LeGates T.A., Altimus C.M., Wang H., Lee H.K., Yang S., Zhao H., Kirkwood A., Weber E.T., Hattar S. Aberrant light directly impairs mood and learning through melanopsin-expressing neurons. Nature 2012, 491:594-598.
42. Levitan R.D. The chronobiology and neurobiology of winter seasonal affective disorder. Dialogues Clin Neurosci 2007, 9:315-324.
43. Lewy A.J. Circadian misalignment in mood disturbances. Curr Psychiatry Rep 2009, 11:459-465.
44. Lewy A.J., Rough J.N., Songer J.B., Mishra N., Yuhas K., Emens J.S. The phase shift hypothesis for the circadian component of winter depression. Dialogues Clin Neurosci 2007, 9:291-300.
45. Lewy A.J., Sack R.L., Miller L.S., Hoban T.M. Antidepressant and circadian phase-shifting effects of light. Science 1987, 235:352-354.
46. Lu X.Y., Bagnol D., Burke S., Akil H., Watson S.J. Differential distribution and regulation of OX1 and OX2 orexin/hypocretin receptor messenger RNA in the brain upon fasting. Horm Behav 2000, 37:335-344.
47. Lutter M., Krishnan V., Russo S.J., Jung S., McClung C.A., Nestler E.J. Orexin signaling mediates the antidepressant-like effect of calorie restriction. J Neurosci 2008, 28:3071-3075.
48. Marston O.J., Williams R.H., Canal M.M., Samuels R.E., Upton N., Piggins H.D. Circadian and dark-pulse activation of orexin/hypocretin neurons. Mol Brain 2008, 1:19.
49. Martinez G.S., Smale L., Nunez A.A. Diurnal and nocturnal rodents show rhythms in orexinergic neurons. Brain Res 2002, 955:1-7.
50. McElhinny T.L., Smale L., Holekamp K.E. Patterns of body temperature, activity, and reproductive behavior in a tropical murid rodent, Arvicanthis niloticus. Physiol Behav 1997, 62:91-96.
51. McGregor R., Wu M.F., Barber G., Ramanathan L., Siegel J.M. Highly specific role of hypocretin (orexin) neurons: differential activation as a function of diurnal phase, operant reinforcement versus operant avoidance and light level. J Neurosci 2011, 31:15455-15467.
52. Mintz E.M., van den Pol A.N., Casano A.A., Albers H.E. Distribution of hypocretin-(orexin) immunoreactivity in the central nervous system of Syrian hamsters (Mesocricetus auratus). J Chem Neuroanat 2001, 21:225-238.
53. Mosko S., Zetin M., Glen S., Garber D., DeAntonio M., Sassin J., McAnich J., Warren S. Self-reported depressive symptomatology, mood ratings, and treatment outcome in sleep disorders patients. J Clin Psychol 1989, 45:51-60.
54. Nambu T., Sakurai T., Mizukami K., Hosoya Y., Yanagisawa M., Goto K. Distribution of orexin neurons in the adult rat brain. Brain Res 1999, 827:243-260.
55. Nixon J.P., Smale L. Individual differences in wheel-running rhythms are related to temporal and spatial patterns of activation of orexin A and B cells in a diurnal rodent (Arvicanthis niloticus). Neuroscience 2004, 127:25-34.
56. Nixon J.P., Smale L. A comparative analysis of the distribution of immunoreactive orexin A and B in the brains of nocturnal and diurnal rodents. Behav Brain Funct 2007, 3:28.
57. Nocjar C., Zhang J., Feng P., Panksepp J. The social defeat animal model of depression shows diminished levels of orexin in mesocortical regions of the dopamine system, and of dynorphin and orexin in the hypothalamus. Neuroscience 2012, 218:138-153.
58. Novak C.M., Albers H.E. Localization of hypocretin-like immunoreactivity in the brain of the diurnal rodent, Arvicanthis niloticus. J Chem Neuroanat 2002, 23:49-58.
59. Ohayon M.M. Narcolepsy is complicated by high medical and psychiatric comorbidities: a comparison with the general population. Sleep Med 2013, 14:488-492.
60. Peyron C., Faraco J., Rogers W., Ripley B., Overeem S., Charnay Y., Nevsimalova S., Aldrich M., Reynolds D., Albin R., Li R., Hungs M., Pedrazzoli M., Padigaru M., Kucherlapati M., Fan J., Maki R., Lammers G.J., Bouras C., Kucherlapati R., Nishino S., Mignot E. 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.
61. 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 1998, 18:9996-10015.
62. Pittendrigh C.S. Temporal organization: reflections of a Darwinian clock-watcher. Annu Rev Physiol 1993, 55:16-54.
63. Plaza-Zabala A., Martin-Garcia E., de Lecea L., Maldonado R., Berrendero F. Hypocretins regulate the anxiogenic-like effects of nicotine and induce reinstatement of nicotine-seeking behavior. J Neurosci 2010, 30:2300-2310.
64. Rainero I., Ostacoli L., Rubino E., Gallone S., Picci L.R., Fenoglio P., Negro E., Rosso C., De Martino P., De Marchi M., Furlan P.M., Pinessi L. Association between major mood disorders and the hypocretin receptor 1 gene. J Affect Disord 2011, 130:487-491.
65. Rosenthal N.E., Sack D.A., Gillin J.C., Lewy A.J., Goodwin F.K., Davenport Y., Mueller P.S., Newsome D.A., Wehr T.A. Seasonal affective disorder. A description of the syndrome and preliminary findings with light therapy. Arch Gen Psychiatry 1984, 41:72-80.
66. Rotter A., Asemann R., Decker A., Kornhuber J., Biermann T. Orexin expression and promoter-methylation in peripheral blood of patients suffering from major depressive disorder. J Affect Disord 2011, 131:186-192.
67. Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 2007, 8:171-181.
68. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., Williams S.C., Richarson J.A., Kozlowski G.P., Wilson S., Arch J.R., Buckingham R.E., Haynes A.C., Carr S.A., Annan R.S., McNulty D.E., Liu W.S., Terrett J.A., Elshourbagy N.A., Bergsma D.J., Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:1. page following 696.
69. Salomon R.M., Ripley B., Kennedy J.S., Johnson B., Schmidt D., Zeitzer J.M., Nishino S., Mignot E. Diurnal variation of cerebrospinal fluid hypocretin-1 (Orexin-A) levels in control and depressed subjects. Biol Psychiatry 2003, 54:96-104.
70. Scott M.M., Marcus J.N., Pettersen A., Birnbaum S.G., Mochizuki T., Scammell T.E., Nestler E.J., Elmquist J.K., Lutter M. Hcrtr1 and 2 signaling differentially regulates depression-like behaviors. Behav Brain Res 2011, 222:289-294.
71. Stephenson K.M., Schroder C.M., Bertschy G., Bourgin P. Complex interaction of circadian and non-circadian effects of light on mood: shedding new light on an old story. Sleep Med Rev 2012, 16:445-454.
72. Sunter D., Morgan I., Edwards C.M., Dakin C.L., Murphy K.G., Gardiner J., Taheri S., Rayes E., Bloom S.R. Orexins: effects on behavior and localisation of orexin receptor 2 messenger ribonucleic acid in the rat brainstem. Brain Res 2001, 907:27-34.
73. Terman J.S., Terman M., Schlager D., Rafferty B., Rosofsky M., Link M.J., Gallin P.F., Quitkin F.M. Efficacy of brief, intense light exposure for treatment of winter depression. Psychopharmacol Bull 1990, 26:3-11.
74. Terman M., Amira L., Terman J.S., Ross D.C. Predictors of response and nonresponse to light treatment for winter depression. Am J Psychiatry 1996, 153:1423-1429.
75. Terman M., Terman J.S. Light therapy for seasonal and nonseasonal depression: efficacy, protocol, safety, and side effects. CNS Spectr 2005, 10:647-663. quiz 672.
76. 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 2000, 27:469-474.
77. Treit D., Fundytus M. Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 1988, 31:959-962.
78. Trivedi P., Yu H., MacNeil D.J., Van der Ploeg L.H., Guan X.M. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett 1998, 438:71-75.
79. Tsujino N., Sakurai T. Orexin/hypocretin: a neuropeptide at the interface of sleep, energy homeostasis, and reward system. Pharmacol Rev 2009, 61:162-176.
80. Workman J.L., Nelson R.J. Potential animal models of seasonal affective disorder. Neurosci Biobehav Rev 2011, 35:669-679.
81. Wu M.F., Nienhuis R., Maidment N., Lam H.A., Siegel J.M. Cerebrospinal fluid hypocretin (orexin) levels are elevated by play but are not raised by exercise and its associated heart rate, blood pressure, respiration or body temperature changes. Arch Ital Biol 2011, 149:492-498.
82. Yan L., Silver R., Gorman M. Reorganization of suprachiasmatic nucleus networks under 24-h LDLD conditions. J Biol Rhythms 2010, 25:19-27.
83. Zeitzer J.M., Dijk D.J., Kronauer R., Brown E., Czeisler C. Sensitivity of the human circadian pacemaker to nocturnal light: melatonin phase resetting and suppression. J Physiol 2000, 526(Pt 3):695-702.