Orexins/hypocretins act in the posterior paraventricular thalamic nucleus during repeated stress to regulate facilitation to novel stress

Endocrinology

Volumn 152, Issue 12, 2011, Pages 4738-4752

  Heydendael, Willem ^a   Sharma, Kanika ^a   Iyer, Vikram ^a   Luz, Sandra ^a   Piel, David ^a   Beck, Sheryl ^a   Bhatnagar, Seema ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; ARGIPRESSIN; CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; OREXIN A; OREXIN B; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; CORTICOTROPIN RELEASE; CYTOSOLIC FRACTION; ENZYME PHOSPHORYLATION; FORCED SWIMMING TEST; HORMONE RESPONSE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; IMMUNOCOMPETENT CELL; MALE; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR BLOCKING; STRESS;

ACTION POTENTIALS; ADRENOCORTICOTROPIC HORMONE; ANIMALS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MIDLINE THALAMIC NUCLEI; NEUROPEPTIDES; PITUITARY-ADRENAL SYSTEM; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; STRESS, PHYSIOLOGICAL; SWIMMING; SYMPATHOMIMETICS;

EID: 82355165090     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1652     Document Type: Article

References (52)

1. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett 2nd FS, Frankel WN,van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG 1998 The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95:322-327 (Pubitemid 28103952)
2. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, LiuWS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M 1998 Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573-585 (Pubitemid 28101119)
3. Adamantidis A, de Lecea L 2008 Physiological arousal: a role for hypothalamic systems. Cell Mol Life Sci 65:1475-1488
4. Peyron C, Petit JM, Rampon C, Jouvet M, Luppi PH 1998 Forebrain afferents to the rat dorsal raphe nucleus demontrated by retrograde and anterograde tracing methods. Neuroscience 82:443-468 (Pubitemid 27461632)
5. Johnson PL, Truitt W, Fitz SD, Minick PE, Dietrich A, Sanghani S, Träskman-Bendz L, Goddard AW, Brundin L, Shekhar A 2010 A key role for orexin in panic anxiety. Nat Med 16:111-115
6. Suzuki M, Beuckmann CT, Shikata K, Ogura H, Sawai T 2005 Orexin-A (hypocretin-1) is possibly involved in generation of anxiety- like behavior. Brain Res 1044:116-121 (Pubitemid 40616058)
7. Date Y, Ueta Y, Yamashita H, Yamaguchi H, Matsukura S, Kangawa K, Sakurai T, Yanagisawa M, Nakazato M 1999 Orexins, orexinergic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci USA 96:748-753 (Pubitemid 29061280)
8. Samson WK, Taylor MM, Follwell M, Ferguson AV 2002 Orexin actions in hypothalamic paraventricular nucleus: physiological consequences and cellular correlates. Regul Peptides 104:97-103 (Pubitemid 34119379)
9. Chang H, Saito T, Ohiwa N, Tateoka M, Deocaris CC, Fujikawa T, Soya H 2007 Inhibitory effects of an orexin-2 receptor antagonist on orexin A- and stress-induced ACTH responses in conscious rats. Neurosci Res 57:462-466 (Pubitemid 46283070)
10. Kuru M, Ueta Y, Serino R, Nakazato M, Yamamoto Y, Shibuya I, Yamashita H 2000 Centrally administered orexin/hypocretin activates HPA axis in rats. Neuroreport 11:1977-1980 (Pubitemid 30429147)
11. Berendse HW, Groenewegen HJ 1991 Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:73-102
12. Kirouac GJ, Parsons MP, Li S 2005 Orexin (hypocretin) innervation of the paraventricular nucleus of the thalamus. Brain Res 1059: 179-188 (Pubitemid 41457316)
13. Moga MM, Weis RP, Moore RY 1995 Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359: 221-238
14. Su HS, BentivoglioM1990 Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J Comp Neurol 297:582-593 (Pubitemid 20217221)
15. Turner BH, Herkenham M 1991 Thalamoamygdaloid projections in the rat: a test of the amygdalaís role in sensory processing. J Comp Neurol 313:295-325
16. Dong HW, Swanson LW 2006 Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol 494:142-178 (Pubitemid 41780619)
17. Bhatnagar S, Huber R, Nowak N, Trotter P 2002 Lesions of the posterior paraventricular thalamus block habituation of hypothalamic- pituitary-adrenal responses to repeated restraint. J Neuroendocrinol 14:403-410 (Pubitemid 34477265)
18. Jaferi A, Bhatnagar S 2006 Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 147:4917-4930 (Pubitemid 44402199)
19. Cluderay JE, Harrison DC, Hervieu GJ 2002 Protein distribution of the orexin-2 receptor in the rat central nervous system. Regul Peptides 104:131-144 (Pubitemid 34119384)
20. Lu XY, Bagnol D, Burke S, Akil H, Watson SJ 2000 Differential distribution and regulation of OX1 and OX2 orexin/hypocretin receptor messenger RNA in the brain upon fasting. Horm Behav 37: 335-344 (Pubitemid 30432352)
21. Marcus JN, Aschkenasi CJ, Lee CE, Chemelli RM, Saper CB, Yanagisawa M, Elmquist JK 2001 Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435:6-25 (Pubitemid 32448719)
22. Trivedi P, Yu H, MacNeil DJ, Van der Ploeg LH, Guan XM 1998 Distribution of orexin receptor mRNA in the rat brain. Fed Eur Biochem Soc 438:71-75 (Pubitemid 28517837)
23. Hsu DT, Price JL 2009 Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin and corticotropin- releasing hormone in macaque monkeys. J Comp Neurol 512:825-848
24. Kerman IA, Bernard R, Rosenthal D, Beals J, Akil H, Watson SJ 2007 Distinct populations of presympathetic premotor neurons express orexin or melanin-concentrating hormone in the rat lateral hypothalamus. J Comp Neurol 505:586-601
25. NambuT, Sakurai T, Mizukami K, Hosoya Y, Yanagisawa M, Goto K 1999 Distribution of orexin neurons in the adult rat brain. Brain Res 827:243-260 (Pubitemid 29222929)
26. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS 1998 Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015 (Pubitemid 28543775)
27. Baldo BA, Daniel RA, Berridge CW, Kelley AE 2003 Overlapping distributions of orexin/hypocretin- and dopamine-(-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J Comp Neurol 464:220-237 (Pubitemid 36976049)
28. Ishibashi M, Takano S, Yanagida H, Takatsuna M, Nakajima K, Oomura Y, Wayner MJ, Sasaki K 2005 Effects of orexins/hypocretins on neuronal activity in the paraventricular nucleus of the thalamus in rats in vitro. Peptides 26:471-481 (Pubitemid 40126704)
29. Kolaj M, Doroshenko P, Yan Cao X, Coderre E, Renaud LP 2007 Orexin-induced modulation of state-dependent intrinsic properties in thalamic paraventricular nucleus neurons attenuates action potential patterning and frequency. Neuroscience 147:1066-1075 (Pubitemid 47102543)
30. Li Y, Li S, Wei C, Wang H, Sui N, Kirouac GJ 2010 Orexins in the paraventricular nucleus of the thalamus mediate anxiety-like responses in rats. Psychopharmacology 212:251-265
31. Bhatnagar S, Viau V, Chu A, Soriano L, Meijer OC, Dallman MF 2000 A cholecystokinin-mediated pathway to the paraventricular thalamus is recruited in chronically stressed rats and regulates hypothalamic- pituitary-adrenal function. J Neurosci 20:5564-5573 (Pubitemid 30457753)
32. Dallman MF, Jones MT 1973 Corticosteroid feedback control of ACTH secretion on subsequent stress responses in the rat. Endocrinology 92:1367-1375
33. Grissom NM, Bhatnagar S 2011 The basolateral amygdala regulates adaptation to stress via β-adrenergic receptor-mediated reductions in phosphorylated extracellular signal-regulated kinase. Neuroscience 178:108-122
34. Paranjape S, Vavaiya K, Kale A, Briski K 2007 Role of dorsal vagal motor nucleus orexin-receptor-1 in glycemic responses to acute versus repeated insulin administration. Neuropeptides 41:111-116 (Pubitemid 46329097)
35. Akana SF, Hanson ES, Horsley CJ, Strack AM, Bhatnagar S, Bradbury MJ, Milligan ED, Dallman MF 1996 Clamped corticosterone (B) reveals the effect of endogenousBon both facilitated responsivity to acute restraint and metabolic responses to chronic stress. Stress 1:33-49
36. Lapiz-Bluhm MD, Bondi CO, Doyen J, Rodriguez GA, Bédard-Arana T, Morilak DA 2008 Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. J Neuroendocrinol 20:1115-1137
37. Langmead CJ, Jerman JC, Brough SJ, Scott C, Porter RA, HerdonHJ 2004 Characterisation of the binding of [3H]-SB-674042, a novel nonpeptide antagonist, to the human orexin-1 receptor. Br J Pharmacol 141:340-346 (Pubitemid 38250904)
38. Smart D, Sabido-David C, Brough SJ, Jewitt F, Johns A, Porter RA, Jerman JC 2001 SB-334867-A: the first selective orexin-1 receptor antagonist. Br J Pharmacol 132:1179-1182 (Pubitemid 32234700)
39. Harris GC, Wimmer M, Randall-Thompson JF, Aston-Jones G 2007 Lateral hypothalamic orexin neurons are critically involved in learning to associate an environment with morphine reward. Behav Brain Res 183:43-51 (Pubitemid 47259526)
40. Bai YJ, Li YH, Zheng XG, Han J, Yang XY, Sui N 2009 Orexin Aattenuates unconditioned sexual motivation in male rats. Pharmacol Biochem Behav 91:581-589
41. Bhatnagar S, Vining C, Iyer V, Kinni V 2006 Changes in hypothalamic- pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J Neuroendocrinol 18:13-24
42. Wood SK, Walker HE, Valentino RJ, Bhatnagar S 2010 Individual differences in reactivity to social stress predict susceptibility and resilience to a depressive phenotype: role of corticotropin-releasing factor. Endocrinology 151:1795-1805
43. Bhatnagar S, Dallman M 1998 and Dallman, M.F Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84:1025-1039
44. Castro MG, Morrison E, Perone MJ, Brown OA, Murray CA, Ahmed I, Perkins AV, Europe-Finner G, Lowenstein PR, Linton EA 1996 Corticotropin-releasing hormone receptor type 1: generation and characterization of polyclonal antipeptide antibodies and their localization in pituitary cells and cortical neurones in vitro. J Neuroendocrinol 8:521-531 (Pubitemid 26239720)
45. Chen MH, Malbon CC 2009 G-protein-coupled receptor-associated A-kinase anchoring proteins AKAP5 and AKAP12: differential trafficking and distribution. Cell Signal 21:136-142
46. Karteris E, Randeva HS 2003 Orexin receptors and G-protein coupling: evidence for another "promiscuous" seven transmembrane domain receptor. J Pharmacol Sci 93:126-128 (Pubitemid 37254278)
47. Milasta S, Evans NA, Ormiston L, Wilson S, Lefkowitz RJ, Milligan G 2005 The sustainability of interactions between the orexin-1 receptor and β-arrestin-2 is defined by a single C-terminal cluster of hydroxy amino acids and modulates the kinetics of ERK MAPK regulation. Biochem J 387(Pt 3):573-584 (Pubitemid 40685690)
48. Ramanjaneya M, Conner AC, Chen J, Stanfield PR, Randeva HS 2008 Orexins stimulate steroidogenic acute regulatory protein expression throughmultiple signaling pathways in human adrenal H295R cells. Endocrinology 149:4106-4115
49. Gray M, Bingham B, Viau V 2010 A comparison of two repeated restraint stress paradigms on hypothalamic-pituitary-adrenal axis habituation, gonadal status and central neuropeptide expression in adult male rats. J Neuroendocrinol 22:92-101
50. Duric V, Banasr M, Licznerski P, Schmidt HD, Stockmeier CA, Simen AA, Newton SS, Duman RS 2010 A negative regulator of MAP kinase causes depressive behavior. Nat Med 16:1328-1332
51. Ward RJ, Pediani JD, Milligan G 2011 Ligand-induced internalization of the orexin OX(1) and cannabinoid CB(1) receptors assessed via N-terminal SNAP and CLIP-tagging. Br J Pharmacol 162:1439-1452
52. Paxinos G, Watson C 2005 The rat brain in stereotaxic coordinates: the new coronal set. 5th Edition, San Diego: Elsevier Academic Press.