Stress and alcohol interactions: Animal studies and clinical significance

Trends in Neurosciences

Volumn 37, Issue 4, 2014, Pages 219-227

  Spanagel, Rainer ^a   Noori, Hamid R ^a   Heilig, Markus ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Alcohol; Glucocorticoids; HPA axis; Organ cation transporter (OCT); Stress

Indexed keywords

ALCOHOL; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; DOPAMINE; GLUCOCORTICOID;

ALCOHOL CONSUMPTION; ALCOHOL USE DISORDER; AMYGDALOID NUCLEUS; DOPAMINE UPTAKE; DRINKING BEHAVIOR; GENETIC ASSOCIATION; GENETIC LOAD; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MESOLIMBIC DOPAMINERGIC SYSTEM; META ANALYSIS (TOPIC); NEUROBIOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REVIEW; RODENT; STRESS; AGE; ALCOHOL ABUSE; ALCOHOLISM; DISEASE MODEL; DRUG SEEKING BEHAVIOR; GENE INTERACTION; LIMBIC SYSTEM; MENTAL STRESS; RELAPSE; REWARD; ANIMAL; BRAIN; COMPLICATION; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOPHYSIOLOGY;

ALCOHOL DRINKING; ALCOHOLISM; ANIMALS; BRAIN; GLUCOCORTICOIDS; HUMANS; REWARD; STRESS, PSYCHOLOGICAL;

EID: 84897374019     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2014.02.006     Document Type: Review

References (93)

1. Lim S.S., et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012, 380:2224-2260.
2. Spanagel R. Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol. Rev. 2009, 89:649-705.
3. Martin C.S., et al. Development and validation of the Biphasic Alcohol Effects Scale. Alcohol. Clin. Exp. Res. 1993, 17:140-146.
4. Conger J.J. The effect of alcohol on conflict behaviour in the albino rat. Q. J. Stud. Alcohol. 1951, 12:1-49.
5. Cappell H., Herman C.P. Alcohol and tension reduction. A review. Q. J. Stud. Alcohol 1972, 33:33-64.
6. Cooper M.L., et al. Stress and alcohol use: moderating effects of gender, coping, and alcohol expectancies. J. Abnorm. Psychol. 1992, 101:139-152.
7. Becker H.C., et al. Effect of stress on alcohol drinking: a review of animal studies. Psychopharmacology (Berl.) 2011, 218:131-156.
8. Thomas S., et al. Clinical laboratory stressors used to study alcohol-stress relationships. Alcohol Res. 2012, 34:459-467.
9. Miller P.M., et al. Effects of social stress on operant drinking of alcoholics and social drinkers. Behav. Res. Ther. 1974, 12:67-72.
10. de Wit H., et al. Effects of acute social stress on alcohol consumption in healthy subjects. Alcohol. Clin. Exp. Res. 2003, 27:1270-1277.
11. Thomas S.E., et al. An acute psychosocial stressor increases drinking in non-treatment-seeking alcoholics. Psychopharmacology 2011, 218:19-28.
12. Brandon T.H., et al. Relapse and relapse prevention. Annu. Rev. Clin. Psychol. 2007, 3:257-284.
13. Sinha R. How does stress lead to risk of alcohol relapse?. Alcohol Res. 2012, 34:432-440.
14. Sinha R., et al. Effects of adrenal sensitivity, stress- and cue-induced craving, and anxiety on subsequent alcohol relapse and treatment outcomes. Arch. Gen. Psychiatry 2011, 68:942-952.
15. Heilig M., Egli M. Pharmacological treatment of alcohol dependence: target symptoms and target mechanisms. Pharmacol. Ther. 2006, 111:855-876.
16. Litten R.Z., et al. Medications development to treat alcohol dependence: a vision for the next decade. Addict. Biol. 2012, 17:513-527.
17. Stephens M.A., Wand G. Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res. 2012, 34:468-483.
18. Heilig M., Koob G.F. A key role for corticotropin-releasing factor in alcohol dependence. Trends Neurosci. 2007, 30:399-406.
19. Noori H.R., et al. Cluster and meta-analyses on factors influencing stress-induced alcohol drinking and relapse in rodents. Addict. Biol. 2014, 19:225-232.
20. Hermens D.F., et al. Pathways to alcohol-induced brain impairment in young people: a review. Cortex 2013, 49:3-17.
21. Heilig M., et al. Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked?. Addict. Biol. 2010, 15:169-184.
22. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 2011, 62:431-445.
23. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
24. Fahlke C., Eriksson C.J. Effect of adrenalectomy and exposure to corticosterone on alcohol intake in alcohol-preferring and alcohol-avoiding rat lines. Alcohol Alcohol. 2000, 35:139-144.
25. Fahlke C., et al. Facilitation of ethanol consumption by intracerebroventricular infusions of corticosterone. Psychopharmacology (Berl.) 1996, 127:133-139.
26. Piazza P.V. Corticosterone in the range of stress-induced levels possesses reinforcing properties: implications for sensation-seeking behaviors. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:11738-11742.
27. Spanagel R., Weiss F. The dopamine hypothesis of reward: past and current status. Trends Neurosci. 1999, 22:521-527.
28. Brand I., et al. Global ethanol-induced enhancements of monoaminergic neurotransmission: a meta-analysis study. Alcohol. Clin. Exp. Res. 2013, 37:2048-2057.
29. Ambroggi F., et al. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat. Neurosci. 2009, 12:247-249.
30. Barik J., et al. Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science 2013, 339:332-335.
31. Fahlke C., et al. 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, 117:216-224.
32. Schömig E., et al. Extraneuronal monoamine transporter and organic cation transporters 1 and 2: a review of transport efficiency. Handb. Exp. Pharmacol. 2006, 175:151-180.
33. Graf E.N., et al. Corticosterone acts in the nucleus accumbens to enhance dopamine signaling and potentiate reinstatement of cocaine seeking. J. Neurosci. 2013, 17:11800-11810.
34. Gasser P.J., et al. Corticosterone-sensitive monoamine transport in the rat dorsomedial hypothalamus: potential role for organic cation transporter 3 in stress-induced modulation of monoaminergic neurotransmission. J. Neurosci. 2006, 26:8758-8766.
35. Cui M., et al. The organic cation transporter-3 is a pivotal modulator of neurodegeneration in the nigrostriatal dopaminergic pathway. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:8043-8048.
36. Lemos J.C., et al. Severe stress switches CRF action in the nucleus accumbens from appetitive to aversive. Nature 2012, 490:402-406.
37. Bilbao A. Advanced transgenic approaches to understand alcohol-related phenotypes in animals. Curr. Top. Behav. Neurosci. 2013, 13:271-311.
38. Mayfield R.D., et al. Genetic factors influencing alcohol dependence. Br. J. Pharmacol. 2008, 154:275-287.
39. Goldman D., et al. The genetics of addictions: uncovering the genes. Nat. Rev. Genet. 2005, 6:521-532.
40. Rietschel M., Treutlein J. The genetics of alcohol dependence. Ann. N.Y. Acad. Sci. 2013, 282:39-70.
41. Spanagel R., et al. A systems medicine research approach for studying alcohol addiction. Addict. Biol. 2013, 18:883-896.
42. Frank J., et al. Genome-wide significant association between alcohol dependence and a variant in the ADH gene cluster. Addict. Biol. 2012, 17:171-180.
43. Biernacka J.M., et al. Replication of genome wide association studies of alcohol dependence: support for association with variation in ADH1C. PLoS ONE 2013, 8:e58798.
44. Sher K.J., et al. Consilient research approaches in studying gene × environment interactions in alcohol research. Addict. Biol. 2010, 15:200-216.
45. Timpl P., et al. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat. Genet. 1998, 19:162-166.
46. Sillaber I., et al. Enhanced and delayed stress-induced alcohol drinking in mice lacking functional CRH1 receptors. Science 2002, 296:931-933.
47. Molander A., et al. Brain-specific inactivation of the Crhr1 gene inhibits post-dependent and stress-induced alcohol intake, but does not affect relapse-like drinking. Neuropsychopharmacology 2012, 37:1047-1056.
48. Treutlein J. Genetic association of the human corticotropin releasing hormone receptor 1 (CRHR1) with binge drinking and alcohol intake patterns in two independent samples. Mol. Psychiatry 2006, 11:594-602.
49. Blomeyer D., et al. Interaction between CRHR1 gene and stressful life events predicts adolescent heavy alcohol use. Biol. Psychiatry 2008, 63:146-151.
50. Nelson E.C., et al. H2 haplotype at chromosome 17q21.31 protects against childhood sexual abuse-associated risk for alcohol consumption and dependence. Addict. Biol. 2010, 15:1-11.
51. Schmid B., et al. Interacting effects of CRHR1 gene and stressful life events on drinking initiation and progression among 19-year-olds. Int. J. Neuropsychopharmacol. 2010, 13:703-714.
52. Schank J.R., et al. Stress-related neuropeptides and addictive behaviors: beyond the usual suspects. Neuron 2012, 76:192-208.
53. Heilig M., et al. Corticotropin-releasing factor and neuropeptide Y: role in emotional integration. Trends Neurosci. 1994, 17:80-85.
54. Gilpin N.W. Corticotropin-releasing factor (CRF) and neuropeptide Y (NPY): effects on inhibitory transmission in central amygdala, and anxiety- & alcohol-related behaviors. Alcohol 2012, 46:329-337.
55. Roberto M., et al. Corticotropin releasing factor-induced amygdala gamma-aminobutyric acid release plays a key role in alcohol dependence. Biol. Psychiatry 2010, 67:831-839.
56. Gilpin N.W., et al. Neuropeptide Y opposes alcohol effects on gamma-aminobutyric acid release in amygdala and blocks the transition to alcohol dependence. Biol. Psychiatry 2011, 69:1091-1099.
57. Zhou Z., et al. Genetic variation in human NPY expression affects stress response and emotion. Nature 2008, 452:997-1001.
58. Sommer W.H., et al. Human NPY promoter variation rs16147:T>C as a moderator of prefrontal NPY gene expression and negative affect. Hum. Mutat. 2010, 31:E1594-E1608.
59. Thiele T.E., et al. Ethanol consumption and resistance are inversely related to neuropeptide Y levels. Nature 1998, 396:366-369.
60. Lindell S.G. Functional NPY variation as a factor in stress resilience and alcohol consumption in rhesus macaques. Arch. Gen. Psychiatry 2010, 67:423-431.
61. Sarkar D.K. Circadian genes, the stress axis, and alcoholism. Alcohol Res. 2012, 34:362-366.
62. Spanagel R., et al. The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat. Med. 2005, 11:35-42.
63. Blomeyer D., et al. Association of PER2 genotype and stressful life events with alcohol drinking in young adults. PLoS ONE 2013, 8:e59136.
64. Yamamoto T., et al. Acute physical stress elevates mouse period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element. J. Biol. Chem. 2005, 280:42036-42043.
65. Reddy T.E., et al. Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res. 2009, 19:2163-2171.
66. Dong L., et al. Effects of the circadian rhythm gene period 1 (per1) on psychosocial stress-induced alcohol drinking. Am. J. Psychiatry 2011, 168:1090-1098.
67. Wang X., et al. A promoter polymorphism in the Per3 gene is associated with alcohol and stress response. Transl. Psychiatry 2012, 2:e73.
68. Koob G.F. Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr. Top. Behav. Neurosci. 2013, 13:3-30.
69. Diana M. The dopamine hypothesis of drug addiction and its potential therapeutic value. Front. Psychiatry 2011, 2:64.
70. Volkow N.D., et al. Profound decreases in dopamine release in striatum in detoxified alcoholics: possible orbitofrontal involvement. J. Neurosci. 2007, 27:12700-12706.
71. Wanat M.J., et al. Phasic dopamine release in appetitive behaviors and drug addiction. Curr. Drug Abuse Rev. 2009, 2:195-213.
72. Shaham Y., et al. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl.) 2003, 168:3-20.
73. Sanchis-Segura C., Spanagel R. Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict. Biol. 2006, 11:2-38.
74. Gozzi A., et al. Differential effect of orexin-1 and CRF-1 antagonism on stress circuits: a fMRI study in the rat with the pharmacological stressor yohimbine. Neuropsychopharmacology 2013, 38:2120-2130.
75. Sommer W.H., et al. Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala crhr1 expression following a history of dependence. Biol. Psychiatry 2008, 63:139-145.
76. Zhao Y., et al. Activation of group II metabotropic glutamate receptors attenuates both stress and cue-induced ethanol-seeking and modulates c-fos expression in the hippocampus and amygdala. J. Neurosci. 2006, 26:9967-9974.
77. Funk D., et al. Effects of pharmacological stressors on c-fos and CRF mRNA in mouse brain: relationship to alcohol seeking. Neurosci. Lett. 2008, 444:254-258.
78. Shalev U., et al. Role of CRF and other neuropeptides in stress-induced reinstatement of drug seeking. Brain Res. 2010, 1314:15-28.
79. Schank J.R., et al. Stress-induced reinstatement of alcohol-seeking in rats is selectively suppressed by the neurokinin 1 (NK1) antagonist L822429. Psychopharmacology (Berl.) 2011, 218:111-119.
80. Schank J.R., et al. The role of the neurokinin-1 receptor in stress-induced reinstatement of alcohol and cocaine seeking. Neuropsychopharmacology 2013, 10.1038/npp.2013.309.
81. Lê A.D., et al. Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats. Psychopharmacology (Berl.) 2011, 218:89-99.
82. Cippitelli A., et al. Neuropeptide Y (NPY) suppresses yohimbine-induced reinstatement of alcohol seeking. Psychopharmacology (Berl.) 2010, 208:417-426.
83. Niwa M., et al. Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 2013, 339:335-339.
84. Logrip M.L., Zorrilla E.P. Stress history increases alcohol intake in relapse: relation to phosphodiesterase 10A. Addict. Biol. 2012, 17:920-933.
85. Gehlert D.R., et al. 3-(4-Chloro-2-morpholin-4-yl-thiazol-5-yl)-8-(1-ethylpropyl)-2,6-dimethyl-imidazo[1,2-b]pyridazine: a novel brain-penetrant, orally available corticotropin-releasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J. Neurosci. 2007, 27. 2718-2126.
86. Hansson A.C., et al. Variation at the rat Crhr1 locus and sensitivity to relapse into alcohol seeking induced by environmental stress. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15236-15241.
87. Marinelli P.W., et al. The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology (Berl.) 2007, 195:345-355.
88. Ayanwuyi L.O., et al. Role of a genetic polymorphism in the corticotropin-releasing factor receptor 1 gene in alcohol drinking and seeking behaviors of marchigian sardinian alcohol-preferring rats. Front. Psychiatry 2013, 4:23.
89. Lê A.D., et al. Effects of naltrexone and fluoxetine on alcohol self-administration and reinstatement of alcohol seeking induced by priming injections of alcohol and exposure to stress. Neuropsychopharmacology 1999, 21:435-444.
90. Liu X., Weiss F. Additive effect of stress and drug cues on reinstatement of ethanol seeking: exacerbation by history of dependence and role of concurrent activation of corticotropin-releasing factor and opioid mechanisms. J. Neurosci. 2002, 22:7856-7861.
91. Nielsen C.K., et al. The delta opioid receptor antagonist, SoRI-9409, decreases yohimbine stress-induced reinstatement of ethanol-seeking. Addict. Biol. 2012, 17:224-234.
92. Schank J.R., et al. The kappa opioid receptor antagonist JDTic attenuates alcohol seeking and withdrawal anxiety. Addict. Biol. 2012, 17:634-647.
93. Economidou D., et al. Effect of the cannabinoid CB1 receptor antagonist SR-141716A on ethanol self-administration and ethanol-seeking behaviour in rats. Psychopharmacology (Berl.) 2006, 183:394-403.