Alcohol-induced dysregulation of stress-related circuitry: The search for novel targets and implications for interventions across the sexes

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 65, Issue , 2016, Pages 252-259

  Retson, T A ^a   Sterling, R C ^b   Van Bockstaele, E J ^c  

^a Department of Neuroscience ^*  (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Alcohol use disorders; Central nucleus of the amygdala; Locus coeruleus; Sex differences

Indexed keywords

4 AMINOBUTYRIC ACID; ALCOHOL; BACLOFEN; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; DISULFIRAM; NALTREXONE; NORADRENALIN; PEXACERFONT; PROTEIN C FOS; TOPIRAMATE; VERUCERFONT;

ADAPTIVE BEHAVIOR; ALCOHOL ABSTINENCE; ALCOHOL CONSUMPTION; ALCOHOL USE DISORDER; ALCOHOLISM; ARTICLE; BRAIN ATROPHY; BRAIN DAMAGE; CENTRAL NUCLEUS (AMYGDALA); CLINICAL TRIAL (TOPIC); CORPUS CALLOSUM; DISEASE PREDISPOSITION; DOPAMINERGIC SYSTEM; DRUG EFFICACY; GABAERGIC TRANSMISSION; GENDER BIAS; HEALTH BEHAVIOR; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LOCUS CERULEUS; META ANALYSIS (TOPIC); NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTOXICITY; NONHUMAN; PREVALENCE; REINFORCEMENT; SEX DIFFERENCE; STRESS; WITHDRAWAL SYNDROME; ALCOHOL-RELATED DISORDERS; ANIMAL; BRAIN; MENTAL STRESS; NERVE TRACT; PATHOPHYSIOLOGY; SEXUAL DEVELOPMENT;

ALCOHOL-RELATED DISORDERS; ANIMALS; BRAIN; HUMANS; NEURAL PATHWAYS; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84949535053     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2015.05.009     Document Type: Article

References (100)

1. Abramson J.L., Williams S.A., Krumholz H.M., Vaccarino V. Moderate alcohol consumption and risk of heart failure among older persons. JAMA 2001, 285:1971-1977.
2. Acevedo M.B., Nizhnikov M.E., Molina J.C., Pautassi R.M. Relationship between ethanol-induced activity and anxiolysis in the open field, elevated plus maze, light-dark box, and ethanol intake in adolescent rats. Behav. Brain Res. 2014, 265:203-215.
3. Adinoff B., Martin P.R., Bone G.H., Eckardt M.J., Roehrich L., George D.T., et al. Hypothalamic-pituitary-adrenal axis functioning and cerebrospinal fluid corticotropin releasing hormone and corticotropin levels in alcoholics after recent and long-term abstinence. Arch. Gen. Psychiatry 1990, 47:325-330.
4. Administration SAaMHS Results from the 2012 National Survey on Drug Use and Health: summary of national findings 2013, [Rockville, MD]. Admnistration SAaMHS (Ed.).
5. Alcoholism NIoAAa Alcoholic brain damage. alcohol research & health. October 2004 2003, National Institutes of Health, Department of Health and Human Services (Eds.).
6. Alcoholism NIoAAa Epidemiology of alcohol problems in the United States 2005, NIAAA publications, [Module 1 ed: NIAAA]. Disorders NSWEftPaToAU (Ed.).
7. Alcoholism NIoAAa Alcohol use disorder: a comparison between DSM-IV and DSM-5 2013, [NIAAANIHGOV].
8. Alcoholism NIoAAa, Alcohol a women's health issue 2008, [NIAAANIHGOV].
9. Alcoholism NIoAAa, Alcohol alert: the link between stress and alcohol. Alcohol Res. Curr. Rev. 2012, 34.
10. Alfonso-Loeches S., Pascual M., Guerri C. Gender differences in alcohol-induced neurotoxicity and brain damage. Toxicology 2013, 311:27-34.
11. Anton R.F., O'Malley S.S., Ciraulo D.A., Cisler R.A., Couper D., Donovan D.M., et al. Combined pharmacotherapies and behavioral interventions for alcohol dependence: the COMBINE study: a randomized controlled trial. JAMA 2006, 295:2003-2017.
12. Bangasser D.A., Curtis A., Reyes B.A., Bethea T.T., Parastatidis I., Ischiropoulos H., et al. Sex differences in corticotropin-releasing factor receptor signaling and trafficking: potential role in female vulnerability to stress-related psychopathology. Mol. Psychiatry 2010, 15(877):96-904.
13. Breese G.R., Overstreet D.H., Knapp D.J. Conceptual framework for the etiology of alcoholism: a "kindling"/stress hypothesis. Psychopharmacology (Berlin) 2005, 178:367-380.
14. Brenner S. AAAS - paleogenetics and the history of alcohol in primates 2013, [AAAS].
15. Butler T.R., Smith K.J., Berry J.N., Sharrett-Field L.J., Prendergast M.A. Sex differences in caffeine neurotoxicity following chronic ethanol exposure and withdrawal. Alcohol Alcohol. 2009, 44:567-574.
16. Carrigan M.A., Uryasev O., Davis R.P., Zhai L., Hurley T.D., Benner S.A. The natural history of class I primate alcohol dehydrogenases includes gene duplication, gene loss, and gene conversion. PLoS One 2012, 7:e41175.
17. Ceylan-Isik A.F., McBride S.M., Ren J. Sex difference in alcoholism: who is at a greater risk for development of alcoholic complication?. Life Sci. 2010, 87:133-138.
18. Clapp P., Bhave S.V., Hoffman P.L. How adaptation of the brain to alcohol leads to dependence: a pharmacological perspective. Alcohol Res Health 2008, 31:310-339.
19. Clinicaltrials.gov. Effects of corticotropin-releasing hormone receptor 1 (CRH1) antagonism on stress-induced craving in alcoholic women with high anxiety 2013, Alcoholism NIoAAa (Ed.).
20. Clinicaltrials.gov. Corticotropin-releasing hormone receptor 1 (CRH1) antagonism in anxious alcoholics 2014, National Institute on Alcohol Abuse and Alcoholism (NIAAA), Bethesda, [NCT01227980]. M.A. Heilig (Ed.).
21. Cohen S., Janicki-Deverts D., Miller G.E. Psychological stress and disease. JAMA 2007, 298:1685-1687.
22. Cui C., Noronha A., Morikawa H., Alvarez V.A., Stuber G.D., Szumlinski K.K., et al. New insights on neurobiological mechanisms underlying alcohol addiction. Neuropharmacology 2013, 67:223-232.
23. Dai X., Thavundayil J., Santella S., Gianoulakis C. Response of the HPA-axis to alcohol and stress as a function of alcohol dependence and family history of alcoholism. Psychoneuroendocrinology 2007, 32:293-305.
24. Dasgupta A. The science of drinking: how alcohol affects your body and mind 2011, Rowman & Littlefield Publishers.
25. Dudley R. Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integr. Comp. Biol. 2004, 44:315-323.
26. Errico A.L., King A.C., Lovallo W.R., Parsons O.A. Cortisol dysregulation and cognitive impairment in abstinent male alcoholics. Alcohol. Clin. Exp. Res. 2002, 26:1198-1204.
27. Fernandez-Sola J., Estruch R., Nicolas J.M., Pare J.C., Sacanella E., Antunez E., et al. Comparison of alcoholic cardiomyopathy in women versus men. Am. J. Cardiol. 1997, 80:481-485.
28. File S.E., Seth P. A review of 25years of the social interaction test. Eur. J. Pharmacol. 2003, 463:35-53.
29. Fortuna S., Pintor A., Michalek H. Adaptive processes of the central and autonomic cholinergic neurotransmitter system: age-related differences. Life Sci. 1991, 48:831-842.
30. Franck J., Jayaram-Lindstrom N. Pharmacotherapy for alcohol dependence: status of current treatments. Curr. Opin. Neurobiol. 2013, 23:692-699.
31. Fukushiro D.F., Josino F.S., Saito L.P., Berro L.F., Morgado F., Frussa-Filho R. Acute and chronic ethanol differentially modify the emotional significance of a novel environment: implications for addiction. Int. J. Neuropsychopharmacol. 2012, 15:1109-1120.
32. Fuller R.K., Branchey L., Brightwell D.R., Derman R.M., Emrick C.D., Iber F.L., et al. Disulfiram treatment of alcoholism. A Veterans Administration cooperative study. JAMA 1986, 256:1449-1455.
33. Gianoulakis C., Dai X., Thavundayil J., Brown T. Levels and circadian rhythmicity of plasma ACTH, cortisol, and beta-endorphin as a function of family history of alcoholism. Psychopharmacology (Berlin) 2005, 181:437-444.
34. Hanson G.R. New insights into relapse. NIDA Notes 2002, 17.
35. Hommer D.W. Male and female sensitivity to alcohol-induced brain damage. Alcohol Res. Health 2003, 27:181-185.
36. Hommer D.W. Male and female sensitivity to alcohol-induced brain damage 2004, [NIAAAgov].
37. Itoi K., Sugimoto N. The brainstem noradrenergic systems in stress, anxiety and depression. J. Neuroendocrinol. 2010, 22:355-361.
38. Jacobson L., Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 1991, 12:118-134.
39. Junghanns K., Backhaus J., Tietz U., Lange W., Bernzen J., Wetterling T., et al. Impaired serum cortisol stress response is a predictor of early relapse. Alcohol Alcohol. 2003, 38:189-193.
40. Junghanns K., Tietz U., Dibbelt L., Kuether M., Jurth R., Ehrenthal D., et al. Attenuated salivary cortisol secretion under cue exposure is associated with early relapse. Alcohol Alcohol. 2005, 40:80-85.
41. Kessler R.C., McGonagle K.A., Zhao S., Nelson C.B., Hughes M., Eshleman S., et al. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch. Gen. Psychiatry 1994, 51:8-19.
42. Keyes K.M., Hatzenbuehler M.L., Hasin D.S. Stressful life experiences, alcohol consumption, and alcohol use disorders: the epidemiologic evidence for four main types of stressors. Psychopharmacology (Berlin) 2011, 218:1-17.
43. Khan A., Brodhead A.E., Schwartz K.A., Kolts R.L., Brown W.A. Sex differences in antidepressant response in recent antidepressant clinical trials. J. Clin. Psychopharmacol. 2005, 25:318-324.
44. King A., Munisamy G., de Wit H., Lin S. Attenuated cortisol response to alcohol in heavy social drinkers. Int. J. Psychophysiol. 2006, 59:203-209.
45. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2001, 24:97-129.
46. Koob G.F., Le Moal M. Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat. Neurosci. 2005, 8:1442-1444.
47. Koppaka V., Thompson D.C., Chen Y., Ellermann M., Nicolaou K.C., Juvonen R.O., et al. Aldehyde dehydrogenase inhibitors: a comprehensive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol. Rev. 2012, 64:520-539.
48. Kulkarni S.K., Singh K., Bishnoi M. Elevated zero maze: a paradigm to evaluate antianxiety effects of drugs. Methods Find. Exp. Clin. Pharmacol. 2007, 29:343-348.
49. Laaksonen E., Vuoristo-Myllys S., Koski-Jannes A., Alho H. Combining medical treatment and CBT in treating alcohol-dependent patients: effects on life quality and general well-being. Alcohol Alcohol. 2013, 48:687-693.
50. Le A.D., Harding S., Juzytsch W., Watchus J., Shalev U., Shaham Y. The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology (Berlin) 2000, 150:317-324.
51. Leshner A.I., Koob G.F. Drugs of abuse and the brain. Proc. Assoc. Am. Physicians 1999, 111:99-108.
52. Longabaugh R.M.J. Cognitive-behavioral coping-skills therapy for alcohol dependence. Alcohol Res. Health 1999, 23:78-85.
53. Lovinger D.M., White G., Weight F.F. Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 1989, 243:1721-1724.
54. Lowery E.G., Sparrow A.M., Breese G.R., Knapp D.J., Thiele T.E. The CRF-1 receptor antagonist, CP-154,526, attenuates stress-induced increases in ethanol consumption by BALB/cJ mice. Alcohol. Clin. Exp. Res. 2008, 32:240-248.
55. Martin-Fardon R., Zorrilla E.P., Ciccocioppo R., Weiss F. Role of innate and drug-induced dysregulation of brain stress and arousal systems in addiction: focus on corticotropin-releasing factor, nociceptin/orphanin FQ, and orexin/hypocretin. Brain Res. 2010, 1314:145-161.
56. Mather M., Lighthall N.R., Nga L., Gorlick M.A. Sex differences in how stress affects brain activity during face viewing. Neuroreport. 2010, 21:933-937.
57. McClung C.A., Ulery P.G., Perrotti L.I., Zachariou V., Berton O., Nestler E.J. DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res. Mol. Brain Res. 2004, 132:146-154.
58. McEwen B.S., Stellar E. Stress and the individual. Mechanisms leading to disease. Arch. Intern. Med. 1993, 153:2093-2101.
59. McEwen B.S., Eiland L., Hunter R.G., Miller M.M. Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 2012, 62:3-12.
60. McGovern P.E. Ancient wine: the search for the origins of viniculture 2007, Princeton University Press.
61. McGovern P.E., Zhang J., Tang J., Zhang Z., Hall G.R., Moreau R.A., et al. Fermented beverages of pre- and proto-historic China. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:17593-17598.
62. Micallef M., Lexis L., Lewandowski P. Red wine consumption increases antioxidant status and decreases oxidative stress in the circulation of both young and old humans. Nutr. J. 2007, 6:27.
63. Moos R.H., Moos B.S. Rates and predictors of relapse after natural and treated remission from alcohol use disorders. Addiction 2006, 101:212-222.
64. Moyer A., Finney J.W. Outcomes for untreated individuals involved in randomized trials of alcohol treatment. J. Subst. Abuse Treat. 2002, 23:247-252.
65. Muzyk A.J., Rivelli S.K., Gagliardi J.P. Defining the role of baclofen for the treatment of alcohol dependence: a systematic review of the evidence. CNS Drugs 2012, 26:69-78.
66. Nixon S.J., Tivis R., Ceballos N., Varner J.L., Rohrbaugh J. Neurophysiological efficiency in male and female alcoholics. Prog. Neuropsychopharmacol. Biol. Psychiatry 2002, 26:919-927.
67. Obara I., Bell R.L., Goulding S.P., Reyes C.M., Larson L.A., Ary A.W., et al. Differential effects of chronic ethanol consumption and withdrawal on homer/glutamate receptor expression in subregions of the accumbens and amygdala of P rats. Alcohol. Clin. Exp. Res. 2009, 33:1924-1934.
68. O'Brien C.P., Volpicelli L.A., Volpicelli J.R. Naltrexone in the treatment of alcoholism: a clinical review. Alcohol 1996, 13:35-39.
69. Pastor R., Reed C., Burkhart-Kasch S., Li N., Sharpe A.L., Coste S.C., et al. Ethanol concentration-dependent effects and the role of stress on ethanol drinking in corticotropin-releasing factor type 1 and double type 1 and 2 receptor knockout mice. Psychopharmacology (Berlin) 2011, 218:169-177.
70. Pfefferbaum A., Rosenbloom M., Deshmukh A., Sullivan E. Sex differences in the effects of alcohol on brain structure. Am. J. Psychiatry 2001, 158:188-197.
71. Ponomarev I. Epigenetic control of gene expression in the alcoholic brain. Alcohol Res. 2013, 35:69-76.
72. Prickett C.D., Lister E., Collins M., Trevithick-Sutton C.C., Hirst M., Vinson J.A., et al. Alcohol: friend or foe? Alcoholic beverage hormesis for cataract and atherosclerosis is related to plasma antioxidant activity. Nonlinearity Biol. Toxicol. Med. 2004, 2:353-370.
73. Rehm J., Mathers C., Popova S., Thavorncharoensap M., Teerawattananon Y., Patra J. Global burden of disease and injury and economic cost attributable to alcohol use and alcohol-use disorders. Lancet 2009, 373:2223-2233.
74. Retson T.A. Hoek JB 2014, Sterling RC, Van Bockstaele EJ. Amygdalar neuronal plasticity and the interactions of alcohol, sex, and stress. Brain Struct Funct.
75. Retson T.A., Reyes B.A., Van Bockstaele E.J. Chronic alcohol exposure differentially affects activation of female locus coeruleus neurons and the subcellular distribution of corticotropin releasing factor receptors. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2014, 56C:66-74.
76. Reyes B.A., Valentino R.J., Van Bockstaele E.J. Stress-induced intracellular trafficking of corticotropin-releasing factor receptors in rat locus coeruleus neurons. Endocrinology 2008, 149:122-130.
77. Richardson H.N., Lee S.Y., O'Dell L.E., Koob G.F., Rivier C.L. Alcohol self-administration acutely stimulates the hypothalamic-pituitary-adrenal axis, but alcohol dependence leads to a dampened neuroendocrine state. Eur. J. Neurosci. 2008, 28:1641-1653.
78. Rivier C. Alcohol stimulates ACTH secretion in the rat: mechanisms of action and interactions with other stimuli. Alcohol. Clin. Exp. Res. 1996, 20:240-254.
79. Rivier C., Lee S. Acute alcohol administration stimulates the activity of hypothalamic neurons that express corticotropin-releasing factor and vasopressin. Brain Res. 1996, 726:1-10.
80. Rivier C., Bruhn T., Vale W. Effect of ethanol on the hypothalamic-pituitary-adrenal axis in the rat: role of corticotropin-releasing factor (CRF). J. Pharmacol. Exp. Ther. 1984, 229:127-131.
81. Ruiz S.M., Oscar-Berman M., Sawyer K.S., Valmas M.M., Urban T., Harris G.J. Drinking history associations with regional white matter volumes in alcoholic men and women. Alcohol. Clin. Exp. Res. 2013, 37:110-122.
82. Sawchenko P.E. Evidence for a local site of action for glucocorticoids in inhibiting CRF and vasopressin expression in the paraventricular nucleus. Brain Res. 1987, 403:213-223.
83. Schepis T.S., Rao U., Yadav H., Adinoff B. The limbic-hypothalamic-pituitary-adrenal axis and the development of alcohol use disorders in youth. Alcohol. Clin. Exp. Res. 2011, 35:595-605.
84. Sharrett-Field L., Butler T.R., Reynolds A.R., Berry J.N., Prendergast M.A. Sex differences in neuroadaptation to alcohol and withdrawal neurotoxicity. Pflugers Arch. 2013, 465:643-654.
85. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., Dourish C.T. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berlin) 1994, 116:56-64.
86. Sher L. The role of the hypothalamic-pituitary-adrenal axis dysfunction in the pathophysiology of alcohol misuse and suicidal behavior in adolescents. Int. J. Adolesc. Med. Health 2007, 19:3-9.
87. Simpson T.L., Stappenbeck C.A., Luterek J.A., Lehavot K., Kaysen D.L. Drinking motives moderate daily relationships between PTSD symptoms and alcohol use. J. Abnorm. Psychol. 2014, 123:237-247.
88. Sinha R. Chronic stress, drug use, and vulnerability to addiction. Ann. N. Y. Acad. Sci. 2008, 1141:105-130.
89. Skaff M.M., Finney J.W., Moos R.H. Gender differences in problem drinking and depression: different "vulnerabilities?". Am. J. Community Psychol. 1999, 27:25-54.
90. Smith S.M., Vale W.W. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin. Neurosci. 2006, 8:383-395.
91. Spanagel R. Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol. Rev. 2009, 89:649-705.
92. Stephens M.A., Wand G. Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res. 2012, 34:468-483.
93. Sterling P., Allostasis J.E. a new paradigm to explain arousal pathology. Handbook of life stress, cognition, and health 1998, 629-649. John Wiley and Sons, Inc, New York. J. Fisher JR (Ed.).
94. Thiele T.E., van Dijk G., Bernstein I.L. Ethanol-induced c-Fos expression in rat lines selected for low and high alcohol consumption. Brain Res. 1997, 756:278-282.
95. Thurman R.G. Sex-related liver injury due to alcohol involves activation of Kupffer cells by endotoxin. Can. J. Gastroenterol. 2000, 14(Suppl. D):129D-135D.
96. Van Bockstaele E.J., Colago E.E., Valentino R.J. Corticotropin-releasing factor-containing axon terminals synapse onto catecholamine dendrites and may presynaptically modulate other afferents in the rostral pole of the nucleus locus coeruleus in the rat brain. J. Comp. Neurol. 1996, 364:523-534.
97. Varlinskaya E.I., Spear L.P. Differences in the social consequences of ethanol emerge during the course of adolescence in rats: social facilitation, social inhibition, and anxiolysis. Dev. Psychobiol. 2006, 48:146-161.
98. Vilpoux C., Warnault V., Pierrefiche O., Daoust M., Naassila M. Ethanol-sensitive brain regions in rat and mouse: a cartographic review, using immediate early gene expression. Alcohol. Clin. Exp. Res. 2009, 33:945-969.
99. Waselus M., Nazzaro C., Valentino R.J., Van Bockstaele E.J. Stress-induced redistribution of corticotropin-releasing factor receptor subtypes in the dorsal raphe nucleus. Biol. Psychiatry 2009, 66:76-83.
100. Weisner C., Matzger H., Kaskutas L.A. How important is treatment? One-year outcomes of treated and untreated alcohol-dependent individuals. Addiction 2003, 98:901-911.