The role of the glucocorticoids in developing resilience to stress and addiction

Frontiers in Psychiatry

Volumn 4, Issue AUG, 2013, Pages

  Srinivasan, Subhashini ^a   Shariff, Masroor ^b   Bartlett, Selena E ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Addiction; Cholinergic; Glucocorticoid; Mifepristone; Nicotinic acetylcholine receptors; Orexin; Resilience; Stress

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; MIFEPRISTONE; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; OREXIN A; OREXIN B;

ADDICTION; ALCOHOLISM; AMYGDALOID NUCLEUS; ARTICLE; BRAIN REGION; CHOLINERGIC SYSTEM; CHRONIC STRESS; COCAINE DEPENDENCE; COPING BEHAVIOR; CUSHING SYNDROME; DRUG EFFECT; DRUG POTENCY; GENE DELETION; GENE EXPRESSION REGULATION; GLUCOCORTICOID RECEPTOR GENE; HORMONE ACTION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALADJUSTMENT; MENTAL DISEASE; MOLECULAR INTERACTION; MORPHINE ADDICTION; NERVE CELL PLASTICITY; NEUROBIOLOGY; NEUROFEEDBACK; NEUROLOGIC DISEASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; WITHDRAWAL SYNDROME;

EID: 84884493998     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2013.00068     Document Type: Article

References (183)

1. McEwen BS. Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann N Y Acad Sci (2004) 1032:1-7. doi:10.1196/annals.1314.001
2. Russo SJ, Murrough JW, Han MH, Charney DS, Nestler EJ. Neurobiology of resilience. Nat Neurosci (2012) 15:1475-84. doi:10.1038/nn.3234
3. Nechvatal JM, Lyons DM. Coping changes the brain. Front Behav Neurosci (2013) 7:13. doi:10.3389/fnbeh.2013.00013
4. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev (1998) 19:269-301. doi:10.1210/er.19.3.269
5. Kino T. Tissue glucocorticoid sensitivity: beyond stochastic regulation on the diverse actions of glucocorticoids. Horm Metab Res (2007) 39:420-4. doi:10.1055/s-2007-980193
6. McEwen BS, De Kloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev (1986) 66:1121-88.
7. Liebal UW, Millat T, Marles-Wright J, Lewis RJ, Wolkenhauer O. Simulations of stressosome activation emphasize allosteric interactions between RsbR and RsbT. BMC Syst Biol (2013) 7:3. doi:10.1186/1752-0509-7-3
8. Marles-Wright J, Grant T, Delumeau O, van Duinen G, Firbank SJ, Lewis PJ, et al. Molecular architecture of the "stressosome," a signal integration and transduction hub. Science (2008) 322:92-6. doi:10.1126/science.1159572
9. Selye H. The significance of the adrenals for adaptation. Science (1937) 85:247-8. doi:10.1126/science.85.2201.247
10. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol (2003) 24:151-80. doi:10.1016/j.yfrne.2003.07.001
11. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci (2009) 10:397-409. doi:10.1038/nrn2647
12. Arriza JL, Simerly RB, Swanson LW, Evans RM. The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron (1988) 1:887-900. doi:10.1016/0896-6273(88)90136-5
13. Arriza JL, Weinberger C, Cerelli G, Glaser TM, Handelin BL, Housman DE, et al. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science (1987) 237:268-75. doi:10.1126/science.3037703
14. Reul JM, de Kloet ER. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology (1985) 117:2505-11. doi:10.1210/endo-117-6-2505
15. Aronsson M, Fuxe K, Dong Y, Agnati LF, Okret S, Gustafsson JA. Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. Proc Natl Acad Sci U S A (1988) 85:9331-5. doi:10.1073/pnas.85.23.9331
16. Gustafsson JA, Carlstedt-Duke J, Poellinger L, Okret S, Wikstrom AC, Bronnegard M, et al. Biochemistry, molecular biology, physiology of the glucocorticoid receptor. Endocr Rev (1987) 8:185-234. doi:10.1210/edrv-8-2-185
17. Spencer RL, Young EA, Choo PH, McEwen BS. Adrenal steroid type I and type II receptor binding: estimates of in vivo receptor number, occupancy, and activation with varying level of steroid. Brain Res (1990) 514:37-48. doi:10.1016/0006-8993(90)90433-C
18. Groeneweg FL, Karst H, de Kloet ER, Joels M. Rapid non-genomic effects of corticosteroids and their role in the central stress response. J Endocrinol (2011) 209:153-67. doi:10.1530/JOE-10-0472
19. de Kloet ER, Karst H, Joels M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol (2008) 29:268-72. doi:10.1016/j.yfrne.2007.10.002
20. Hinz B, Hirschelmann R. Rapid non-genomic feedback effects of glucocorticoids on CRF-induced ACTH secretion in rats. Pharm Res (2000) 17:1273-7. doi:10.1023/A:1007652908104
21. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev (2000) 21:55-89. doi:10.1210/er.21.1.55
22. Grino M, Burgunder JM, Eskay RL, Eiden LE. Onset of glucocorticoid responsiveness of anterior pituitary corticotrophs during development is scheduled by corticotropin-releasing factor. Endocrinology (1989) 124:2686-92. doi:10.1210/endo-124-6-2686
23. Keller-Wood ME, Dallman MF. Corticosteroid inhibition of ACTH secretion. Endocr Rev (1984) 5:1-24. doi:10.1210/edrv-5-1-1
24. Tasker JG, Di S, Malcher-Lopes R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology (2006) 147:5549-56. doi:10.1210/en.2006-0981
25. Di S, Malcher-Lopes R, Halmos KC, Tasker JG. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci (2003) 23:4850-7.
26. Evanson NK, Tasker JG, Hill MN, Hillard CJ, Herman JP. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology (2010) 151:4811-9. doi:10.1210/en.2010-0285
27. Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A (2005) 102:19204-7. doi:10.1073/pnas.0507572102
28. Qiu S, Champagne DL, Peters M, Catania EH, Weeber EJ, Levitt P, et al. Loss of limbic system-associated membrane protein leads to reduced hippocampal mineralocorticoid receptor expression, impaired synaptic plasticity, and spatial memory deficit. Biol Psychiatry (2010) 68:197-204. doi:10.1016/j.biopsych.2010.02.013
29. Barik J, Marti F, Morel C, Fernandez SP, Lanteri C, Godeheu G, et al. Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science (2013) 339:332-5. doi:10.1126/science.1226767
30. De Kloet ER, Reul JM. Feedback action and tonic influence of corticosteroids on brain function: a concept arising from the heterogeneity of brain receptor systems. Psychoneuroendocrinology (1987) 12:83-105. doi:10.1016/0306-4530(87)90040-0
31. Diorio D, Viau V, Meaney MJ. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci (1993) 13:3839-47.
32. Magarinos AM, Somoza G, De Nicola AF. Glucocorticoid negative feedback and glucocorticoid receptors after hippocampectomy in rats. Horm Metab Res (1987) 19:105-9. doi:10.1055/s-2007-1011753
33. McEwen BS, Stellar E. Stress and the individual. Mechanisms leading to disease. Arch Intern Med (1993) 153:2093-101. doi:10.1001/archinte.153.18.2093
34. Koob GF. A role for brain stress systems in addiction. Neuron (2008) 59:11-34. doi:10.1016/j.neuron.2008.06.012
35. Holsboer F, von Bardeleben U, Wiedemann K, Muller OA, Stalla GK. Serial assessment of corticotropin-releasing hormone response after dexamethasone in depression. Implications for pathophysiology of DST nonsuppression. Biol Psychiatry (1987) 22:228-34. doi:10.1016/0006-3223(87)90237-X
36. Nemeroff CB, Widerlov E, Bissette G, Walleus H, Karlsson I, Eklund K, et al. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science (1984) 226:1342-4. doi:10.1126/science.6334362
37. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci (2002) 22:6810-8.
38. Lakshminarasimhan H, Chattarji S. Stress leads to contrasting effects on the levels of brain derived neurotrophic factor in the hippocampus and amygdala. PLoS ONE (2012) 7:e30481. doi:10.1371/journal.pone.0030481
39. Arendt DH, Smith JP, Bastida CC, Prasad MS, Oliver KD, Eyster KM, et al. Contrasting hippocampal and amygdalar expression of genes related to neural plasticity during escape from social aggression. Physiol Behav (2012) 107:670-9. doi:10.1016/j.physbeh.2012.03.005
40. Kolber BJ, Roberts MS, Howell MP, Wozniak DF, Sands MS, Muglia LJ. Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning. Proc Natl Acad Sci U S A (2008) 105:12004-9. doi:10.1073/pnas.0803216105
41. Schwabe L, Tegenthoff M, Hoffken O, Wolf OT. Simultaneous glucocorticoid and noradrenergic activity disrupts the neural basis of goal-directed action in the human brain. J Neurosci (2012) 32:10146-55. doi:10.1523/JNEUROSCI.1304-12.2012
42. Sarabdjitsingh RA, Kofink D, Karst H, de Kloet ER, Joels M. Stress-induced enhancement of mouse amygdalar synaptic plasticity depends on glucocorticoid and β-adrenergic activity. PLoS ONE (2012) 7:e42143. doi:10.1371/journal.pone.0042143
43. Gourley SL, Swanson AM, Koleske AJ. Corticosteroid-induced neural remodeling predicts behavioral vulnerability and resilience. J Neurosci (2013) 33:3107-12. doi:10.1523/JNEUROSCI.2138-12.2013
44. Lehmann ML, Brachman RA, Martinowich K, Schloesser RJ, Herkenham M. Glucocorticoids orchestrate divergent effects on mood through adult neurogenesis. J Neurosci (2013) 33:2961-72. doi:10.1523/JNEUROSCI.3878-12.2013
45. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, et al. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci (1996) 18:49-72. doi:10.1159/000111395
46. Chen DY, Bambah-Mukku D, Pollonini G, Alberini CM. Glucocorticoid receptors recruit the CaMKIIalpha-BDNF-CREB pathways to mediate memory consolidation. Nat Neurosci (2012) 15:1707-14. doi:10.1038/nn.3266
47. Gourley SL, Swanson AM, Jacobs AM, Howell JL, Mo M, Dileone RJ, et al. Action control is mediated by prefrontal BDNF and glucocorticoid receptor binding. Proc Natl Acad Sci U S A (2012) 109:20714-9. doi:10.1073/pnas.1208342109
48. Schwabe L, Oitzl MS, Philippsen C, Richter S, Bohringer A, Wippich W, et al. Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learn Mem (2007) 14:109-16. doi:10.1101/lm.435807
49. Schwabe L, Schachinger H, de Kloet ER, Oitzl MS. Stress impairs spatial but not early stimulus-response learning. Behav Brain Res (2010) 213:50-5. doi:10.1016/j.bbr
50. ter Horst JP, van der Mark MH, Arp M, Berger S, de Kloet ER, Oitzl MS. Stress or no stress: mineralocorticoid receptors in the forebrain regulate behavioral adaptation. Neurobiol Learn Mem (2012) 98:33-40. doi:10.1016/j.nlm
51. Yuen EY, Liu W, Karatsoreos IN, Ren Y, Feng J, McEwen BS, et al. Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Mol Psychiatry (2011) 16:156-70. doi:10.1038/mp.2010.50
52. Lai M, Horsburgh K, Bae SE, Carter RN, Stenvers DJ, Fowler JH, et al. Forebrain mineralocorticoid receptor overexpression enhances memory, reduces anxiety and attenuates neuronal loss in cerebral ischaemia. Eur J Neurosci (2007) 25:1832-42. doi:10.1111/j.1460-9568.2007.05427.x
53. Richardson HN, Lee SY, O'Dell LE, Koob GF, Rivier CL. Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur J Neurosci (2008) 28:1641-53. doi:10.1111/j.1460-9568.2008.06455.x
54. Wei Q, Fentress HM, Hoversten MT, Zhang L, Hebda-Bauer EK, Watson SJ, et al. Early-life forebrain glucocorticoid receptor overexpression increases anxiety behavior and cocaine sensitization. Biol Psychiatry (2012) 71:224-31. doi:10.1016/j.biopsych.2011.07.009
55. de Jong IE, de Kloet ER. Glucocorticoids and vulnerability to psychostimulant drugs: toward substrate and mechanism. Ann N Y Acad Sci (2004) 1018:192-8. doi:10.1196/annals.1296.022
56. Marinelli M, Piazza PV. Interaction between glucocorticoid hormones, stress and psychostimulant drugs. Eur J Neurosci (2002) 16:387-94. doi:10.1046/j.1460-9568.2002.02089.x
57. Roberts AJ, Lessov CN, Phillips TJ. Critical role for glucocorticoid receptors in stress- and ethanol-induced locomotor sensitization. J Pharmacol Exp Ther (1995) 275:790-7.
58. Rouge-Pont F, Marinelli M, Le Moal M, Simon H, Piazza PV. Stress-induced sensitization and glucocorticoids. II. Sensitization of the increase in extracellular dopamine induced by cocaine depends on stress-induced corticosterone secretion. J Neurosci (1995) 15:7189-95.
59. Saal D, Dong Y, Bonci A, Malenka RC. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron (2003) 37:577-82. doi:10.1016/S0896-6273(03)00021-7
60. Tye SJ, Miller AD, Blaha CD. Differential corticosteroid receptor regulation of mesoaccumbens dopamine efflux during the peak and nadir of the circadian rhythm: a molecular equilibrium in the midbrain? Synapse (2009) 63:982-90. doi:10.1002/syn.20682
61. Ambroggi F, Turiault M, Milet A, Deroche-Gamonet V, Parnaudeau S, Balado E, et al. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat Neurosci (2009) 12:247-9. doi:10.1038/nn.2282
62. Costin BN, Wolen AR, Fitting S, Shelton KL, Miles MF. Role of adrenal glucocorticoid signaling in prefrontal cortex gene expression and acute behavioral responses to ethanol. Alcohol Clin Exp Res (2013) 37:57-66. doi:10.1111/j.1530-0277.2012.01841.x
63. Cippitelli A, Damadzic R, Hamelink C, Brunnquell M, Thorsell A, Heilig M, et al. Binge-like ethanol consumption increases corticosterone levels and neurodegneration whereas occupancy of type II glucocorticoid receptors with mifepristone is neuroprotective. Addict Biol (2012). doi:10.1111/j.1369-1600.2012.00451.x
64. Prendergast MA, Mulholland PJ. Glucocorticoid and polyamine interactions in the plasticity of glutamatergic synapses that contribute to ethanol-associated dependence and neuronal injury. Addict Biol (2012) 17:209-23. doi:10.1111/j.1369-1600.2011.00375.x
65. Little HJ, Croft AP, O'Callaghan MJ, Brooks SP, Wang G, Shaw SG. Selective increases in regional brain glucocorticoid: a novel effect of chronic alcohol. Neuroscience (2008) 156:1017-27. doi:10.1016/j.neuroscience.2008.08.029
66. Vendruscolo LF, Barbier E, Schlosburg JE, Misra KK, Whitfield TW Jr., Logrip ML, et al. Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci (2012) 32:7563-71. doi:10.1523/JNEUROSCI.0069-12.2012
67. Rose AK, Shaw SG, Prendergast MA, Little HJ. The importance of glucocorticoids in alcohol dependence and neurotoxicity. Alcohol Clin Exp Res (2010) 34:2011-8. doi:10.1111/j.1530-0277.2010.01298.x
68. Yin HH, Mulcare SP, Hilario MR, Clouse E, Holloway T, Davis MI, et al. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci (2009) 12:333-41. doi:10.1038/nn.2261
69. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A (1998) 95:322-7. doi:10.1073/pnas.95.1.322
70. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell (1998) 92:573-85. doi:10.1016/S0092-8674(02)09256-5
71. Anaclet C, Parmentier R, Ouk K, Guidon G, Buda C, Sastre JP, et al. Orexin/hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J Neurosci (2009) 29:14423-38. doi:10.1523/JNEUROSCI.2604-09.2009
72. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell (1999) 98:437-51. doi:10.1016/S0092-8674(00)81973-X
73. Haynes AC, Jackson B, Chapman H, Tadayyon M, Johns A, Porter RA, et al. A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul Pept (2000) 96:45-51. doi:10.1016/S0167-0115(00)00199-3
74. Yamada H, Okumura T, Motomura W, Kobayashi Y, Kohgo Y. Inhibition of food intake by central injection of anti-orexin antibody in fasted rats. Biochem Biophys Res Commun (2000) 267:527-31. doi:10.1006/bbrc.1999.1998
75. Elias CF, Saper CB, Maratos-Flier E, Tritos NA, Lee C, Kelly J, et al. Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J Comp Neurol (1998) 402:442-59. doi:10.1002/(SICI)1096-9861(19981228)402:4<442::AID-CNE2>3.3.CO;2- I
76. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci (1998) 18:9996-10015.
77. Harris GC, Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci (2006) 29:571-7. doi:10.1016/j.tins.2006.08.002
78. Ida T, Nakahara K, Murakami T, Hanada R, Nakazato M, Murakami N. Possible involvement of orexin in the stress reaction in rats. Biochem Biophys Res Commun (2000) 270:318-23. doi:10.1006/bbrc.2000.2412
79. Kagerer SM, Johren O. Interactions of orexins/hypocretins with adrenocortical functions. Acta Physiol (Oxf) (2010) 198:361-71. doi:10.1111/j.1748-1716.2009.02034.x
80. Al-Barazanji KA, Wilson S, Baker J, Jessop DS, Harbuz MS. Central orexin-A activates hypothalamic-pituitary-adrenal axis and stimulates hypothalamic corticotropin releasing factor and arginine vasopressin neurones in conscious rats. J Neuroendocrinol (2001) 13:421-4. doi:10.1046/j.1365-2826.2001.00655.x
81. Jaszberenyi M, Bujdoso E, Pataki I, Telegdy G. Effects of orexins on the hypothalamic-pituitary-adrenal system. J Neuroendocrinol (2000) 12:1174-8. doi:10.1046/j.1365-2826.2000.00572.x
82. Kuru M, Ueta Y, Serino R, Nakazato M, Yamamoto Y, Shibuya I, et al. Centrally administered orexin/hypocretin activates HPA axis in rats. Neuroreport (2000) 11:1977-80. doi:10.1097/00001756-200006260-00034
83. Kuwaki T, Zhang W. Orexin neurons and emotional stress. Vitam Horm (2012) 89:135-58. doi:10.1016/B978-0-12-394623-2.00008-1
84. Di Chiara G, Imperato A. Ethanol preferentially stimulates dopamine release in the nucleus accumbens of freely moving rats. Eur J Pharmacol (1985) 115:131-2. doi:10.1016/0014-2999(85)90598-9
85. Koob GF, Bloom FE. Cellular and molecular mechanisms of drug dependence. Science (1988) 242:715-23. doi:10.1126/science.2903550
86. Wise RA, Rompre PP. Brain dopamine and reward. Annu Rev Psychol (1989) 40:191-225. doi:10.1146/annurev.ps.40.020189.001203
87. Borgland SL, Taha SA, Sarti F, Fields HL, 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. doi:10.1016/j.neuron.2006.01.016
88. DiLeone RJ, Georgescu D, Nestler EJ. Lateral hypothalamic neuropeptides in reward and drug addiction. Life Sci (2003) 73:759-68. doi:10.1016/S0024-3205(03)00408-9
89. Harris GC, Wimmer M, Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature (2005) 437:556-9. doi:10.1038/nature04071
90. Paneda C, Winsky-Sommerer R, Boutrel B, de Lecea L. The corticotropin-releasing factor-hypocretin connection: implications in stress response and addiction. Drug News Perspect (2005) 18:250-5. doi:10.1358/dnp.2005.18.4.908659
91. Pasumarthi RK, Reznikov LR, Fadel J. Activation of orexin neurons by acute nicotine. Eur J Pharmacol (2006) 535:172-6. doi:10.1016/j.ejphar.2006.02.021
92. Dayas CV, McGranahan TM, Martin-Fardon R, Weiss F. Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse. Biol Psychiatry (2008) 63:152-7. doi:10.1016/j.biopsych.2007.02.002
93. Jupp B, Krivdic B, Krstew E, Lawrence AJ. The orexin receptor antagonist SB-334867 dissociates the motivational properties of alcohol and sucrose in rats. Brain Res (2011) 1391:54-9. doi:10.1016/j.brainres.2011.03.045
94. Lawrence AJ, Cowen MS, Yang HJ, Chen F, Oldfield B. The orexin system regulates alcohol-seeking in rats. Br J Pharmacol (2006) 148:752-9. doi:10.1038/sj.bjp.0706789
95. Moorman DE, Aston-Jones G. Orexin-1 receptor antagonism decreases ethanol consumption and preference selectively in high-ethanol - preferring Sprague - Dawley rats. Alcohol (2009) 43:379-86. doi:10.1016/j.alcohol.2009.07.002
96. Richards JK, Simms JA, Steensland P, Taha SA, Borgland SL, Bonci A, et al. Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology (Berl) (2008) 199:109-17. doi:10.1007/s00213-008-1136-5
97. Srinivasan S, Simms JA, Nielsen CK, Lieske SP, Bito-Onon JJ, Yi H, et al. The dual orexin/hypocretin receptor antagonist, almorexant, in the ventral tegmental area attenuates ethanol self-administration. PLoS ONE (2012) 7:e44726. doi:10.1371/journal.pone.0044726
98. Kim AK, Brown RM, Lawrence AJ. The role of orexins/hypocretins in alcohol use and abuse: an appetitive-reward relationship. Front Behav Neurosci (2012) 6:78. doi:10.3389/fnbeh.2012.00078
99. Shoblock JR, Welty N, Aluisio L, Fraser I, Motley ST, Morton K, et al. Selective blockade of the orexin-2 receptor attenuates ethanol self-administration, place preference, and reinstatement. Psychopharmacology (Berl) (2011) 215:191-203. doi:10.1007/s00213-010-2127-x
100. Boutrel B, Kenny PJ, Specio SE, Martin-Fardon R, Markou A, Koob GF, et al. Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci U S A (2005) 102:19168-73. doi:10.1073/pnas.0507480102
101. Wang B, You ZB, Wise RA. Reinstatement of cocaine seeking by hypocretin (orexin) in the ventral tegmental area: independence from the local corticotropin-releasing factor network. Biol Psychiatry (2009) 65:857-62. doi:10.1016/j.biopsych.2009.01.018
102. Jupp B, Krstew E, Dezsi G, Lawrence AJ. Discrete cue-conditioned alcohol-seeking after protracted abstinence: pattern of neural activation and involvement of orexin(1) receptors. Br J Pharmacol (2011) 162:880-9. doi:10.1111/j.1476-5381.2010.01088.x
103. Moller C, Wiklund L, Sommer W, Thorsell A, Heilig M. Decreased experimental anxiety and voluntary ethanol consumption in rats following central but not basolateral amygdala lesions. Brain Res (1997) 760:94-101. doi:10.1016/S0006-8993(97)00308-9
104. McFarland K, Davidge SB, Lapish CC, Kalivas PW. Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J Neurosci (2004) 24:1551-60. doi:10.1523/JNEUROSCI.4177-03.2004
105. Schmidt FM, Arendt E, Steinmetzer A, Bruegel M, Kratzsch J, Strauss M, et al. CSF-hypocretin-1 levels in patients with major depressive disorder compared to healthy controls. Psychiatry Res (2011) 190:240-3. doi:10.1016/j.psychres.2011.06.004
106. Schmitt O, Usunoff KG, Lazarov NE, Itzev DE, Eipert P, Rolfs A, et al. Orexinergic innervation of the extended amygdala and basal ganglia in the rat. Brain Struct Funct (2012) 217:233-56. doi:10.1007/s00429-011-0343-8
107. Lungwitz EA, Molosh A, Johnson PL, Harvey BP, Dirks RC, Dietrich A, et al. Orexin-A induces anxiety-like behavior through interactions with glutamatergic receptors in the bed nucleus of the stria terminalis of rats. Physiol Behav (2012) 107:726-32. doi:10.1016/j.physbeh.2012.05.019
108. Conrad KL, Davis AR, Silberman Y, Sheffler DJ, Shields AD, Saleh SA, et al. Yohimbine depresses excitatory transmission in BNST and impairs extinction of cocaine place preference through orexin-dependent, norepinephrine-independent processes. Neuropsychopharmacology (2012) 37:2253-66. doi:10.1038/npp.2012.76
109. Winrow CJ, Gotter AL, Cox CD, Doran SM, Tannenbaum PL, Breslin MJ, et al. Promotion of sleep by suvorexant-a novel dual orexin receptor antagonist. J Neurogenet (2011) 25:52-61. doi:10.3109/01677063.2011.566953
110. Garrido P, De Blas M, Ronzoni G, Cordero I, Anton M, Gine E, et al. Differential effects of environmental enrichment and isolation housing on the hormonal and neurochemical responses to stress in the prefrontal cortex of the adult rat: relationship to working and emotional memories. J Neural Transm (2013) 120:829-43. doi:10.1007/s00702-012-0935-3
111. Herman JP, Ostrander MM, Mueller NK, Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry (2005) 29:1201-13. doi:10.1016/j.pnpbp.2005.08.006
112. Sullivan RM, Gratton A. Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology (2002) 27:99-114. doi:10.1016/S0306-4530(01)00038-5
113. Weinberg MS, Johnson DC, Bhatt AP, Spencer RL. Medial prefrontal cortex activity can disrupt the expression of stress response habituation. Neuroscience (2010) 168:744-56. doi:10.1016/j.neuroscience.2010.04.006
114. Gold PE. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol Learn Mem (2003) 80:194-210. doi:10.1016/j.nlm.2003.07.003
115. Levin HS, Rodnitzky RL. Behavioral effects of organophosphate in man. Clin Toxicol (1976) 9:391-403. doi:10.3109/15563657608988138
116. Kim JJ, Diamond DM. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci (2002) 3:453-62.
117. McEwen BS. Effects of adverse experiences for brain structure and function. Biol Psychiatry (2000) 48:721-31. doi:10.1016/S0006-3223(00)00964-1
118. McEwen BS, Weiss JM, Schwartz LS. Selective retention of corticosterone by limbic structures in rat brain. Nature (1968) 220:911-2. doi:10.1038/220911a0
119. Del Arco A, Mora F. Neurotransmitters and prefrontal cortex-limbic system interactions: implications for plasticity and psychiatric disorders. J Neural Transm (2009) 116:941-52. doi:10.1007/s00702-009-0243-8
120. Vizi ES, Kiss JP. Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and nonsynaptic interactions. Hippocampus (1998) 8:566-607. doi:10.1002/(SICI)1098-1063(1998)8:6<566::AID-HIPO2>3.0.CO;2-W
121. Imperato A, Puglisi-Allegra S, Casolini P, Angelucci L. Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis. Brain Res (1991) 538:111-7. doi:10.1016/0006-8993(91)90384-8
122. Ross SA, Wong JY, Clifford JJ, Kinsella A, Massalas JS, Horne MK, et al. Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J Neurosci (2000) 20:6431-41.
123. Booker TK, Butt CM, Wehner JM, Heinemann SF, Collins AC. Decreased anxiety-like behavior in beta3 nicotinic receptor subunit knockout mice. Pharmacol Biochem Behav (2007) 87:146-57. doi:10.1016/j.pbb.2007.04.011
124. Salas R, Pieri F, Fung B, Dani JA, De Biasi M. Altered anxiety-related responses in mutant mice lacking the beta4 subunit of the nicotinic receptor. J Neurosci (2003) 23:6255-63.
125. Salas R, Orr-Urtreger A, Broide RS, Beaudet A, Paylor R, De Biasi M. The nicotinic acetylcholine receptor subunit alpha 5 mediates short-term effects of nicotine in vivo. Mol Pharmacol (2003) 63:1059-66. doi:10.1124/mol.63.5.1059
126. Salas R, Pieri F, De Biasi M. Decreased signs of nicotine withdrawal in mice null for the beta4 nicotinic acetylcholine receptor subunit. J Neurosci (2004) 24:10035-9. doi:10.1523/JNEUROSCI.1939-04.2004
127. Brioni JD, O'Neill AB, Kim DJ, Decker MW. Nicotinic receptor agonists exhibit anxiolytic-like effects on the elevated plus-maze test. Eur J Pharmacol (1993) 238:1-8. doi:10.1016/0014-2999(93)90498-7
128. Cao W, Burkholder T, Wilkins L, Collins AC. A genetic comparison of behavioral actions of ethanol and nicotine in the mirrored chamber. Pharmacol Biochem Behav (1993) 45:803-9. doi:10.1016/0091-3057(93)90124-C
129. Costall B, Kelly ME, Naylor RJ, Onaivi ES. The actions of nicotine and cocaine in a mouse model of anxiety. Pharmacol Biochem Behav (1989) 33:197-203. doi:10.1016/0091-3057(89)90450-4
130. File SE, Cheeta S, Kenny PJ. Neurobiological mechanisms by which nicotine mediates different types of anxiety. Eur J Pharmacol (2000) 393:231-6. doi:10.1016/S0014-2999(99)00889-4
131. Alzoubi KH, Srivareerat M, Tran TT, Alkadhi KA. Role of alpha7- and alpha4beta2-nAChRs in the neuroprotective effect of nicotine in stress-induced impairment of hippocampus-dependent memory. Int J Neuropsychopharmacol (2013) 16:1105-13. doi:10.1017/S1461145712001046
132. Akana SF, Chu A, Soriano L, Dallman MF. Corticosterone exerts site-specific and state-dependent effects in prefrontal cortex and amygdala on regulation of adrenocorticotropic hormone, insulin and fat depots. J Neuroendocrinol (2001) 13:625-37. doi:10.1046/j.1365-2826.2001.00676.x
133. Feldman S, Conforti N, Saphier D. The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience (1990) 37:775-9. doi:10.1016/0306-4522(90)90107-F
134. Herman JP, Schafer MK, Young EA, Thompson R, Douglass J, Akil H, et al. Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J Neurosci (1989) 9:3072-82.
135. Jacobson L, Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev (1991) 12:118-34. doi:10.1210/edrv-12-2-118
136. Sapolsky RM, Krey LC, McEwen BS. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A (1984) 81:6174-7. doi:10.1073/pnas.81.19.6174
137. Matta SG, Beyer HS, McAllen KM, Sharp BM. Nicotine elevates rat plasma ACTH by a central mechanism. J Pharmacol Exp Ther (1987) 243:217-26.
138. Matta SG, McAllen KM, Sharp BM. Role of the fourth cerebroventricle in mediating rat plasma ACTH responses to intravenous nicotine. J Pharmacol Exp Ther (1990) 252:623-30.
139. Sawchenko PE, Bohn MC. Glucocorticoid receptor-immunoreactivity in C1, C2, and C3 adrenergic neurons that project to the hypothalamus or to the spinal cord in the rat. J Comp Neurol (1989) 285:107-16. doi:10.1002/cne.902850109
140. Swanson LW, Sawchenko PE, Rivier J, Vale WW. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology (1983) 36:165-86. doi:10.1159/000123454
141. Fu Y, Matta SG, Valentine JD, Sharp BM. Adrenocorticotropin response and nicotine-induced norepinephrine secretion in the rat paraventricular nucleus are mediated through brainstem receptors. Endocrinology (1997) 138:1935-43. doi:10.1210/en.138.5.1935
142. Zhao R, Chen H, Sharp BM. Nicotine-induced norepinephrine release in hypothalamic paraventricular nucleus and amygdala is mediated by N-methyl-D-aspartate receptors and nitric oxide in the nucleus tractus solitarius. J Pharmacol Exp Ther (2007) 320:837-44. doi:10.1124/jpet.106.112474
143. Sawchenko PE, Swanson LW. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res (1982) 257:275-325.
144. Swanson LW, Sawchenko PE, Berod A, Hartman BK, Helle KB, Vanorden DE. An immunohistochemical study of the organization of catecholaminergic cells and terminal fields in the paraventricular and supraoptic nuclei of the hypothalamus. J Comp Neurol (1981) 196:271-85. doi:10.1002/cne.901960207
145. Kalappa BI, Feng L, Kem WR, Gusev AG, Uteshev VV. Mechanisms of facilitation of synaptic glutamate release by nicotinic agonists in the nucleus of the solitary tract. Am J Physiol Cell Physiol (2011) 301:C347-61. doi:10.1152/ajpcell.00473.2010
146. Smith DV, Uteshev VV. Heterogeneity of nicotinic acetylcholine receptor expression in the caudal nucleus of the solitary tract. Neuropharmacology (2008) 54:445-53. doi:10.1016/j.neuropharm.2007.10.018
147. Bullock AE, Clark AL, Grady SR, Robinson SF, Slobe BS, Marks MJ, et al. Neurosteroids modulate nicotinic receptor function in mouse striatal and thalamic synaptosomes. J Neurochem (1997) 68:2412-23. doi:10.1046/j.1471-4159.1997.68062412.x
148. Ke L, Lukas RJ. Effects of steroid exposure on ligand binding and functional activities of diverse nicotinic acetylcholine receptor subtypes. J Neurochem (1996) 67:1100-12. doi:10.1046/j.1471-4159.1996.67031100.x
149. Shi LJ, He HY, Liu LA, Wang CA. Rapid nongenomic effect of corticosterone on neuronal nicotinic acetylcholine receptor in PC12 cells. Arch Biochem Biophys (2001) 394:145-50. doi:10.1006/abbi.2001.2519
150. Takita M, Muramatsu I. Alteration of brain nicotinic receptors induced by immobilization stress and nicotine in rats. Brain Res (1995) 681:190-2. doi:10.1016/0006-8993(95)00265-R
151. Almeida LE, Pereira EF, Alkondon M, Fawcett WP, Randall WR, Albuquerque EX. The opioid antagonist naltrexone inhibits activity and alters expression of alpha7 and alpha4beta2 nicotinic receptors in hippocampal neurons: implications for smoking cessation programs. Neuropharmacology (2000) 39:2740-55. doi:10.1016/S0028-3908(00)00157-X
152. Leonard S, Gault J, Hopkins J, Logel J, Vianzon R, Short M, et al. Association of promoter variants in the alpha7 nicotinic acetylcholine receptor subunit gene with an inhibitory deficit found in schizophrenia. Arch Gen Psychiatry (2002) 59:1085-96. doi:10.1001/archpsyc.59.12.1085
153. Berse B, Blusztajn JK. Modulation of cholinergic locus expression by glucocorticoids and retinoic acid is cell-type specific. FEBS Lett (1997) 410:175-9. doi:10.1016/S0014-5793(97)00568-1
154. Battaglia M, Ogliari A. Anxiety and panic: from human studies to animal research and back. Neurosci Biobehav Rev (2005) 29:169-79. doi:10.1016/j.neubiorev.2004.06.013
155. Meshorer E, Soreq H. Virtues and woes of AChE alternative splicing in stress-related neuropathologies. Trends Neurosci (2006) 29:216-24. doi:10.1016/j.tins.2006.02.005
156. Meerson A, Cacheaux L, Goosens KA, Sapolsky RM, Soreq H, Kaufer D. Changes in brain MicroRNAs contribute to cholinergic stress reactions. J Mol Neurosci (2010) 40:47-55. doi:10.1007/s12031-009-9252-1
157. Shaltiel G, Hanan M, Wolf Y, Barbash S, Kovalev E, Shoham S, et al. Hippocampal microRNA-132 mediates stress-inducible cognitive deficits through its acetylcholinesterase target. Brain Struct Funct (2013) 218:59-72. doi:10.1007/s00429-011-0376-z
158. Zhao T, Huang GB, Muna SS, Bagalkot TR, Jin HM, Chae HJ, et al. Effects of chronic social defeat stress on behavior and choline acetyltransferase, 78-kDa glucose-regulated protein, and CCAAT/enhancer-binding protein (C/EBP) homologous protein in adult mice. Psychopharmacology (Berl) (2013) 228:217-30. doi:10.1007/s00213-013-3028-6
159. Sailaja BS, Cohen-Carmon D, Zimmerman G, Soreq H, Meshorer E. Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4. Proc Natl Acad Sci U S A (2012) 109:E3687-95. doi:10.1073/pnas.1209990110
160. Kaufer D, Friedman A, Seidman S, Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature (1998) 393:373-7. doi:10.1038/30741
161. Pavlovsky L, Bitan Y, Shalev H, Serlin Y, Friedman A. Stress-induced altered cholinergic-glutamatergic interactions in the mouse hippocampus. Brain Res (2012) 1472:99-106. doi:10.1016/j.brainres.2012.05.057
162. Fahlke C, Hard E, Eriksson CJ, Engel JA, Hansen S. Consequence of long-term exposure to corticosterone or dexamethasone on ethanol consumption in the adrenalectomized rat, and the effect of type I and type II corticosteroid receptor antagonists. Psychopharmacology (Berl) (1995) 117:216-24. doi:10.1007/BF02245190
163. Uhart M, Wand GS. Stress, alcohol and drug interaction: an update of human research. Addict Biol (2009) 14:43-64. doi:10.1111/j.1369-1600.2008.00131.x
164. Sinha R. The role of stress in addiction relapse. Curr Psychiatry Rep (2007) 9:388-95. doi:10.1007/s11920-007-0050-6
165. Sinha R, Catapano D, O'Malley S. Stress-induced craving and stress response in cocaine dependent individuals. Psychopharmacology (Berl) (1999) 142:343-51. doi:10.1007/s002130050898
166. Simms JA, Haass-Koffler CL, Bito-Onon J, Li R, Bartlett SE. Mifepristone in the central nucleus of the amygdala reduces yohimbine stress-induced reinstatement of ethanol-seeking. Neuropsychopharmacology (2012) 37:906-18. doi:10.1038/npp.2011.268
167. De Vries TJ, Schoffelmeer AN, Tjon GH, Nestby P, Mulder AH, Vanderschuren LJ. Mifepristone prevents the expression of long-term behavioural sensitization to amphetamine. Eur J Pharmacol (1996) 307:R3-4. doi:10.1016/0014-2999(96)00308-1
168. Deroche-Gamonet V, Sillaber I, Aouizerate B, Izawa R, Jaber M, Ghozland S, et al. The glucocorticoid receptor as a potential target to reduce cocaine abuse. J Neurosci (2003) 23:4785-90.
169. Fiancette JF, Balado E, Piazza PV, Deroche-Gamonet V. Mifepristone and spironolactone differently alter cocaine intravenous self-administration and cocaine-induced locomotion in C57BL/6J mice. Addict Biol (2010) 15:81-7. doi:10.1111/j.1369-1600.2009.00178.x
170. Mesripour A, Hajhashemi V, Rabbani M. Metyrapone and mifepristone reverse recognition memory loss induced by spontaneous morphine withdrawal in mice. Basic Clin Pharmacol Toxicol (2008) 102:377-81. doi:10.1111/j.1742-7843.2007.00183.x
171. Jacquot C, Croft AP, Prendergast MA, Mulholland P, Shaw SG, Little HJ. Effects of the glucocorticoid antagonist, mifepristone, on the consequences of withdrawal from long term alcohol consumption. Alcohol Clin Exp Res (2008) 32:2107-16. doi:10.1111/j.1530-0277.2008.00799.x
172. Koenig HN, Olive MF. The glucocorticoid receptor antagonist mifepristone reduces ethanol intake in rats under limited access conditions. Psychoneuroendocrinology (2004) 29:999-1003. doi:10.1016/j.psyneuen.2003.09.004
173. Lowery EG, Spanos M, Navarro M, Lyons AM, Hodge CW, Thiele TE. CRF-1 antagonist and CRF-2 agonist decrease binge-like ethanol drinking in C57BL/6J mice independent of the HPA axis. Neuropsychopharmacology (2010) 35:1241-52. doi:10.1038/npp.2009.209
174. O'Callaghan MJ, Croft AP, Jacquot C, Little HJ. The hypothalamopituitary-adrenal axis and alcohol preference. Brain Res Bull (2005) 68:171-8. doi:10.1016/j.brainresbull.2005.08.006
175. Yang X, Wang S, Rice KC, Munro CA, Wand GS. Restraint stress and ethanol consumption in two mouse strains. Alcohol Clin Exp Res (2008) 32:840-52. doi:10.1111/j.1530-0277.2008.00632.x
176. Sharrett-Field L, Butler TR, Berry JN, Reynolds AR, Prendergast MA. Mifepristone pretreatment reduces ethanol withdrawal severity in vivo. Alcohol Clin Exp Res (2013): doi:10.1111/acer.12093
177. Johanssen S, Allolio B. Mifepristone (RU 486) in Cushing's syndrome. Eur J Endocrinol (2007) 157:561-9. doi:10.1530/EJE-07-0458
178. DeBattista C, Belanoff J. The use of mifepristone in the treatment of neuropsychiatric disorders. Trends Endocrinol Metab (2006) 17:117-21. doi:10.1016/j.tem.2006.02.006
179. Gallagher P, Watson S, Elizabeth Dye C, Young AH, Nicol Ferrier I. Persistent effects of mifepristone (RU-486) on cortisol levels in bipolar disorder and schizophrenia. J Psychiatr Res (2008) 42:1037-41. doi:10.1016/j.jpsychires.2007.12.005
180. Gallagher P, Watson S, Smith MS, Ferrier IN, Young AH. Effects of adjunctive mifepristone (RU-486) administration on neurocognitive function and symptoms in schizophrenia. Biol Psychiatry (2005) 57:155-61. doi:10.1016/j.biopsych.2004.10.017
181. Gallagher P, Young AH. Mifepristone (RU-486) treatment for depression and psychosis: a review of the therapeutic implications. Neuropsychiatr Dis Treat (2006) 2:33-42.
182. Wulsin AC, Herman JP, Solomon MB. Mifepristone decreases depression-like behavior and modulates neuroendocrine and central hypothalamic-pituitary-adrenocortical axis responsiveness to stress. Psychoneuroendocrinology (2010) 35:1100-12. doi:10.1016/j.psyneuen.2010.01.011
183. Young AM. Antiglucocorticoid treatments for depression. Aust N Z J Psychiatry (2006) 40:402-5. doi:10.1080/j.1440-1614.2006.01813.x