Persistent adaptation by chronic alcohol is facilitated by neuroimmune activation linked to stress and CRF

Alcohol

Volumn 52, Issue , 2016, Pages 9-23

  Breese, George R ^a,b   Knapp, Darin J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Adaptation; Anxiety; Chronic alcohol withdrawal; CRF; Neuroimmune; Stress

Indexed keywords

ALCOHOL; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1;

ALCOHOL ABSTINENCE; ALCOHOL ABUSE; ANXIETY; ARTICLE; BEHAVIOR ASSESSMENT; BRAIN NERVE CELL; BRAIN REGION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; SOCIAL ADAPTATION; SOCIAL INTERACTION; ALCOHOLISM; ANIMAL; IMMUNOLOGY; MENTAL STRESS; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; WITHDRAWAL SYNDROME;

ALCOHOLISM; ANIMALS; CORTICOTROPIN-RELEASING HORMONE; HUMANS; NEUROIMMUNOMODULATION; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; STRESS, PSYCHOLOGICAL; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84962584693     PISSN: 07418329     EISSN: 18736823     Source Type: Journal    
DOI: 10.1016/j.alcohol.2016.01.005     Document Type: Article

References (215)

1. al'Absi M., Hatsukami D., Davis G.L. Attenuated adrenocorticotropic responses to psychological stress are associated with early smoking relapse. Psychopharmacology 2005, 181:107-117.
2. Achur R.N., Freeman W.M., Vrana K.E. Circulating cytokines as biomarkers of alcohol abuse and alcoholism. Journal of Neuroimmune Pharmacology 2010, 5:83-91.
3. Adler M.W., Geller E.B., Chen X., Rogers T.J. Viewing chemokines as a third major system of communication in the brain. The AAPS Journal 2006, 7:E865-E870.
4. Agoglia A.E., Holstein S.E., Reid G., Hodge C.W. CaMKIIα-GluA1 activity underlies vulnerability to adolescent binge alcohol drinking. Alcoholism: Clinical and Experimental Research 2015, 39:1680-1690.
5. Akira S., Takeda K. Toll-like receptor signalling. Nature Reviews. Immunology 2004, 4:499-511.
6. Alfonso-Loeches S., Guerri C. Molecular and behavioral aspects of the actions of alcohol on the adult and developing brain. Critical Reviews in Clinical Laboratory Sciences 2011, 48:19-47.
7. Alfonso-Loeches S., Pascual-Lucas M., Blanco A.M., Sanchez-Vera I., Guerri C. Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. The Journal of Neuroscience 2010, 30:8285-8295.
8. Alfonso-Loeches S., Pascual M., Gómez-Pinedo U., Pascual-Lucas M., Renau-Piqueras J., Guerri C. Toll-like receptor 4 participates in the myelin disruptions associated with chronic alcohol abuse. Glia 2012, 60:948-964.
9. Allen mouse brain connectivity atlas 2015, Allen Institute for Brain Science, Available from. http://connectivity.brain-map.org.
10. Andersson U., Tracey K.J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annual Review of Immunology 2011, 29:139-162.
11. Anisman H., Merali Z. Cytokines, stress and depressive illness: brain-immune interactions. Annals of Medicine 2003, 35:2-11.
12. Arakawa H., Blandino P., Deak T. Central infusion of interleukin-1 receptor antagonist blocks the reduction in social behavior produced by prior stressor exposure. Physiology & Behavior 2009, 98:139-146.
13. Avery S.N., Clauss J.A., Blackford J.U. The Human BNST: functional role in anxiety and addiction. Neuropsychopharmacology 2015, 41:126-141.
14. Badrick E., Bobak M., Britton A., Kirschbaum C., Marmot M., Kumari M. The relationship between alcohol consumption and cortisol secretion in an aging cohort. The Journal of Clinical Endocrinology and Metabolism 2008, 93:750-757.
15. Bajo M., Cruz M.T., Siggins G.R., Messing R., Roberto M. Protein kinase C epsilon mediation of CRF- and ethanol-induced GABA release in central amygdala. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:8410-8415.
16. Bajo M., Herman M.A., Varodayan F.P., Oleata C.S., Madamba S.G., Harris R.A., et al. Role of the IL-1 receptor antagonist in ethanol-induced regulation of GABAergic transmission in the central amygdala. Brain, Behavior, and Immunity 2015, 45:189-197.
17. Bajo M., Madamba S.G., Roberto M., Blednov Y.A., Sagi V.N., Roberts E., et al. Innate immune factors modulate alcohol interaction with GABAergic transmission in mouse central amygdala. Brain, Behavior, and Immunity 2014, 40:191-202.
18. Bajo M., Varodayan F.P., Madamba S.G., Roberts A.J., Casal L.M., Oleata C.S., et al. IL-1 interacts with alcohol effects on GABAergic transmission in the mouse central amygdala. Frontiers in Pharmacology 2015, 6:49.
19. Baldwin H.A., Rassnick S., Rivier J., Koob G.F., Britton K.T. CRF antagonist reverses the "anxiogenic" response to ethanol withdrawal in the rat. Psychopharmacology 1991, 103:227-232.
20. Bale T.L., Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annual Review of Pharmacology and Toxicology 2004, 44:525-557.
21. Ballenger J.C., Post R.M. Kindling as a model for alcohol withdrawal syndromes. The British Journal of Psychiatry 1978, 133:1-14.
22. Banisadr G., Gosselin R.D., Mechighel P., Kitabgi P., Rostène W., Parsadaniantz S.M. Highly regionalized neuronal expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) in rat brain: evidence for its colocalization with neurotransmitters and neuropeptides. The Journal of Comparative Neurology 2005, 489:275-292.
23. Banisadr G., Gosselin R.D., Mechighel P., Rostène W., Kitabgi P., Mélik Parsadaniantz S. Constitutive neuronal expression of CCR2 chemokine receptor and its colocalization with neurotransmitters in normal rat brain: functional effect of MCP-1/CCL2 on calcium mobilization in primary cultured neurons. The Journal of Comparative Neurology 2005, 492:178-192.
24. Banisadr G., Quéraud-Lesaux F., Boutterin M.C., Pélaprat D., Zalc B., Rostène W., et al. Distribution, cellular localization and functional role of CCR2 chemokine receptors in adult rat brain. Journal of Neurochemistry 2002, 81:257-269.
25. Bauer S., Kerr B.J., Patterson P.H. The neuropoietic cytokine family in development, plasticity, disease and injury. Nature Reviews. Neuroscience 2007, 8:221-232.
26. Belkouch M., Dansereau M.A., Réaux-Le Goazigo A., Van Steenwinckel J., Beaudet N., Chraibi A., et al. The chemokine CCL2 increases Nav1.8 sodium channel activity in primary sensory neurons through a GBγ-dependent mechanism. The Journal of Neuroscience 2011, 31:18381-18390.
27. Bi L.L., Sun X.D., Zhang J., Lu Y.S., Chen Y.H., Wang J., et al. Amygdala NRG1-ErbB4 is critical for the modulation of anxiety-like behaviors. Neuropsychopharmacology 2015, 40:974-986.
28. Blanco A.M., Vallés S.L., Pascual M., Guerri C. Involvement of TLR4/type I IL-1 receptor signaling in the induction of inflammatory mediators and cell death induced by alcohol in cultured astrocytes. Journal of Immunology 2005, 175:6893-6899.
29. Blandino P., Barnum C.J., Deak T. The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. Journal of Neuroimmunology 2006, 173:87-95.
30. Blandino P., Barnum C.J., Solomon L.G., Larish Y., Lankow B.S., Deak T. Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain, Behavior, and Immunity 2009, 23:958-968.
31. Blednov Y.A., Bergeson S.E., Walker D., Ferreira V.M., Kuziel W.A., Harris R.A. Perturbation of chemokine networks by gene deletion alters the reinforcing actions of alcohol. Behavioural Brain Research 2005, 165:110-125.
32. Blednov Y.A., Ponomarev I., Geil C., Bergeson S., Koob G.F., Harris R.A. Neuroimmune regulation of alcohol consumption: behavioral validation of genes obtained from genomic studies. Addiction Biology 2012, 17:108-120.
33. Breese G.R., Chu K., Dayas C.V., Funk D., Knapp D.J., Koob G.F., et al. Stress enhancement of craving during sobriety: a risk for relapse. Alcoholism: Clinical and Experimental Research 2005, 29:185-195.
34. Breese G.R., Knapp D.J., Overstreet D.H. Stress sensitization of ethanol withdrawal-induced reduction in social interaction: inhibition by CRF-1 and benzodiazepine receptor antagonists and a 5-HT1A-receptor agonist. Neuropsychopharmacology 2004, 29:470-482.
35. Breese G.R., Knapp D.J., Overstreet D.H., Navarro M., Wills T.A., Angel R.A. Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 2008, 33:867-876.
36. Breese G.R., Overstreet D.H., Knapp D.J. Conceptual framework for the etiology of alcoholism: a "kindling"/stress hypothesis. Psychopharmacology 2005, 178:367-380.
37. Breese G.R., Overstreet D.H., Knapp D.J., Navarro M. Prior multiple ethanol withdrawals enhance stress-induced anxiety-like behavior: inhibition by CRF1- and benzodiazepine-receptor antagonists and a 5-HT1a-receptor agonist. Neuropsychopharmacology 2005, 30:1662-1669.
38. Breese G.R., Sinha R., Heilig M. Chronic alcohol neuroadaptation and stress contribute to susceptibility for alcohol craving and relapse. Pharmacology & Therapeutics 2011, 129:149-171.
39. Brower K.J. Alcohol's effects on sleep in alcoholics. Alcohol Research & Health 2001, 25:110-125.
40. Brown S.A., Vik P.W., McQuaid J.R., Patterson T.L., Irwin M.R., Grant I. Severity of psychosocial stress and outcome of alcoholism treatment. Journal of Abnormal Psychology 1990, 99:344-348.
41. Brown S.A., Vik P.W., Patterson T.L., Grant I., Schuckit M.A. Stress, vulnerability and adult alcohol relapse. Journal of Studies on Alcohol 1995, 56:538-545.
42. Buck H.M., Hueston C.M., Bishop C., Deak T. Enhancement of the hypothalamic-pituitary-adrenal axis but not cytokine responses to stress challenges imposed during withdrawal from acute alcohol exposure in Sprague-Dawley rats. Psychopharmacology 2011, 218:203-215.
43. Cappell H., Herman C.P. Alcohol and tension reduction: a review. Quarterly Journal of Studies on Alcohol 1972, 33:33-64.
44. del Cerro S., Borrell J. Interleukin-1 affects the behavioral despair response in rats by an indirect mechanism which requires endogenous CRF. Brain Research 1990, 528:162-164.
45. Cheng Z., Taylor B., Ourthiague D.R., Hoffman A. Distinct single-cell signaling characteristics are conferred by the MyD88 and TRIF pathways during TLR4 activation. Science Signaling 2015, 8:ra69.
46. Cho J., Gruol D.L. The chemokine CCL2 activates p38 mitogen-activated protein kinase pathway in cultured rat hippocampal cells. Journal of Neuroimmunology 2008, 199:94-103.
47. Conger J.J. The effects of alcohol on conflict behavior in the albino rat. Quarterly Journal of Studies on Alcohol 1951, 12:1-29.
48. Conger J.J. Alcoholism: theory, problem and challenge. II. Reinforcement theory and the dynamics of alcoholism. Quarterly Journal of Studies on Alcohol 1956, 17:296-305.
49. Cook C.J. Stress induces CRF release in the paraventricular nucleus, and both CRF and GABA release in the amygdala. Physiology & Behavior 2004, 82:751-762.
50. Cooney N.L., Litt M.D., Morse P.A., Bauer L.O., Gaupp L. Alcohol cue reactivity, negative-mood reactivity, and relapse in treated alcoholic men. Journal of Abnormal Psychology 1997, 106:243-250.
51. Crews F.T., Qin L., Sheedy D., Vetreno R.P., Zou J. High mobility group box 1/Toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biological Psychiatry 2013, 73:602-612.
52. Crews F.T., Vetreno R.P. Addiction, adolescence, and innate immune gene induction. Frontiers in Psychiatry 2011, 2:19.
53. Crews F.T., Zou J., Qin L. Induction of innate immune genes in brain create the neurobiology of addiction. Brain, Behavior, and Immunity 2011, 25(SUPPL. 1):S4-S12.
54. Cruz M.T., Herman M.A., Kallupi M., Roberto M. Nociceptin/orphanin FQ blockade of corticotropin-releasing factor-induced gamma-aminobutyric acid release in central amygdala is enhanced after chronic alcohol exposure. Biological Psychiatry 2012, 71:666-676.
55. Cui C., Noronha A., Warren K.R., Koob G.F., Sinha R., Thakkar M., et al. Brain pathways to recovery from alcohol dependence. Alcohol 2015, 49:435-452.
56. Daniel S.E., Rainnie D.G. Stress modulation of opposing circuits in the bed nucleus of the stria terminalis. Neuropsychopharmacology 2015, 41:103-125.
57. Davé S.H., Tilstra J.S., Matsuoka K., Li F., DeMarco R.A., Beer-Stolz D., et al. Ethyl pyruvate decreases HMGB1 release and ameliorates murine colitis. Journal of Leukocyte Biology 2009, 86:633-643.
58. Davis M. Neurocircuitry of anxiety and stress disorders. Neuropsychopharmacology: Fifth generation of progress 2002, 931-951. Lippincott, Williams, & Wilkins, Philadelphia, PA. K.L. Davis, D. Charney, J.T. Coyle, C. Nemeroff (Eds.).
59. Deak T., Bordner K.A., McElderry N.K., Barnum C.J., Blandino P., Deak M.M., et al. Stress-induced increases in hypothalamic IL-1: a systematic analysis of multiple stressor paradigms. Brain Research Bulletin 2005, 64:541-556.
60. Deussing J.M., Breu J., Kühne C., Kallnik M., Bunck M., Glasl L., et al. Urocortin 3 modulates social discrimination abilities via corticotropin-releasing hormone receptor type 2. The Journal of Neuroscience 2010, 30:9103-9116.
61. Doremus-Fitzwater T.L., Buck H.M., Bordner K., Richey L., Jones M.E., Deak T. Intoxication- and withdrawal-dependent expression of central and peripheral cytokines following initial alcohol exposure. Alcoholism: Clinical and Experimental Research 2014, 38:2186-2198.
62. Drummond S.P., Gillin J.C., Smith T.L., DeModena A. The sleep of abstinent pure primary alcoholic patients: natural course and relationship to relapse. Alcoholism: Clinical and Experimental Research 1998, 22:1796-1802.
63. Dunn A.J., Berridge C.W. Is corticotropin-releasing factor a mediator of stress responses?. Annals of the New York Academy of Sciences 1990, 579:183-191.
64. Dunn A.J., Berridge C.W. Physiological and behavioral responses to corticotropin-releasing factor administration: is CRF a mediator of anxiety or stress responses?. Brain Research. Brain Research Reviews 1990, 15:71-100.
65. Dunn A.J., Swiergiel A.H., de Beaurepaire R. Cytokines as mediators of depression: what can we learn from animal studies?. Neuroscience and Biobehavioral Reviews 2005, 29:891-909.
66. Ehlert U., Gaab J., Heinrichs M. Psychoneuroendocrinological contributions to the etiology of depression, posttraumatic stress disorder, and stress-related bodily disorders: the role of the hypothalamus-pituitary-adrenal axis. Biological Psychiatry 2001, 57:141-152.
67. Eisenhardt M., Hansson A.C., Spanagel R., Bilbao A. Chronic intermittent ethanol exposure in mice leads to an up-regulation of CRH/CRHR1 signaling. Alcoholism: Clinical and Experimental Research 2014, 39:752-762.
68. Fernandez-Lizarbe S., Pascual M., Gascon M.S., Blanco A., Guerri C. Lipid rafts regulate ethanol-induced activation of TLR4 signaling in murine macrophages. Molecular Immunology 2008, 45:2007-2016.
69. Fernandez-Lizarbe S., Pascual M., Guerri C. Critical role of TLR4 response in the activation of microglia induced by alcohol. Journal of Immunology 2009, 183:4733-4744.
70. Fleshner M. Stress-evoked sterile inflammation, danger associated molecular patterns (DAMPs), microbial associated molecular patterns (MAMPs) and the inflammasome. Brain, Behavior, and Immunity 2013, 27:1-7.
71. Fox H.C., Bergquist K.L., Hong K.I., Sinha R. Stress-induced and alcohol cue-induced craving in recently abstinent alcohol-dependent individuals. Alcoholism: Clinical and Experimental Research 2007, 31:395-403.
72. Fox H.C., Bergquist K.L., Peihua G., Rajita S. Interactive effects of cumulative stress and impulsivity on alcohol consumption. Alcoholism: Clinical and Experimental Research 2010, 34:1376-1385.
73. Fox H.C., Hong K.I., Siedlarz K., Sinha R. Enhanced sensitivity to stress and drug/alcohol craving in abstinent cocaine-dependent individuals compared to social drinkers. Neuropsychopharmacology 2008, 33:796-805.
74. Fox H.C., Hong K.A., Sinha R. Difficulties in emotion regulation and impulse control in recently abstinent alcoholics compared with social drinkers. Addictive Behaviors 2008, 33:388-394.
75. Francesconi W., Berton F., Repunte-Canonigo V., Hagihara K., Thurbon D., Lekic D., et al. Protracted withdrawal from alcohol and drugs of abuse impairs long-term potentiation of intrinsic excitability in the juxtacapsular bed nucleus of the stria terminalis. The Journal of Neuroscience 2009, 29:5389-5401.
76. Frank M.G., Weber M.D., Watkins L.R., Maier S.F. Stress sounds the alarmin: the role of the danger-associated molecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain, Behavior, and Immunity 2015, 48:1-7.
77. Gárate I., Garcia-Bueno B., Madrigal J.L., Caso J.R., Alou L., Gomez-Lus M.L., et al. Stress-induced neuroinflammation: role of the Toll-like receptor-4 pathway. Biological Psychiatry 2013, 73:32-43.
78. 2+ dynamics and electrophysiological properties of cultured cerebellar Purkinje neurons. The European Journal of Neuroscience 2005, 21:2949-2957.
79. Gilman J.M., Hommer D.W. Modulation of brain response to emotional images by alcohol cues in alcohol-dependent patients. Addiction Biology 2008, 13:423-434.
80. Gilman J.M., Ramchandani V.A., Davis M.B., Bjork J.M., Hommer D.W. Why we like to drink: a functional magnetic resonance imaging study of the rewarding and anxiolytic effects of alcohol. The Journal of Neuroscience 2008, 28:4583-4591.
81. Gilpin N.W., Herman M.A., Roberto M. The central amygdala as an integrative hub for anxiety and alcohol use disorders. Biological Psychiatry 2015, 77:859-869.
82. Girotti M., Donegan J.J., Morilak D.A. Chronic intermittent cold stress sensitizes neuro-immune reactivity in the rat brain. Psychoneuroendocrinology 2011, 36:1164-1174.
83. Giuliani F., Hader W., Yong V.W. Minocycline attenuates T cell and microglia activity to impair cytokine production in T cell-microglia interaction. Journal of Leukocyte Biology 2005, 78:135-143.
84. Gong K., Zou X., Fuchs P.N., Lin Q. Minocycline inhibits neurogenic inflammation by blocking the effects of tumor necrosis factor-α. Clinical and Experimental Pharmacology & Physiology 2015, (Epub ahead of print), http://dx.doi.org/10.1111/1440-1681.12444.
85. Gosselin R.D., Varela C., Banisadr G., Mechighel P., Rostene W., Kitabgi P., et al. Constitutive expression of CCR2 chemokine receptor and inhibition by MCP-1/CCL2 of GABA-induced currents in spinal cord neurones. Journal of Neurochemistry 2005, 95:1023-1034.
86. Gray J.M., Vecchiarelli H.A., Morena M., Lee T.T., Hermanson D.J., Kim A.B., et al. Corticotropin-releasing hormone drives anandamide hydrolysis in the amygdala to promote anxiety. The Journal of Neuroscience 2015, 35:3879-3892.
87. Guyon A., Skrzydelski D., De Giry I., Rovère C., Conductier G., Trocello J.M., et al. Long term exposure to the chemokine CCL2 activates the nigrostriatal dopamine system: a novel mechanism for the control of dopamine release. Neuroscience 2009, 162:1072-1080.
88. Hammen C. Stress and depression. Annual Review of Clinical Psychology 2005, 1:293-319.
89. Hanoune J., Defer N. Regulation and role of adenylyl cyclase isoforms. Annual Review of Pharmacology and Toxicology 2001, 41:145-174.
90. Harper K.M., Knapp D.J., Breese G.R. Withdrawal from chronic alcohol induces a unique CCL2 mRNA increase in adolescent but not adult brain - relationship to blood alcohol levels and seizures. Alcoholism: Clinical and Experimental Research 2015, 39:2375-2385.
91. Hayley S., Anisman H. Multiple mechanisms of cytokine action in neurodegenerative and psychiatric states: neurochemical and molecular substrates. Current Pharmaceutical Design 2005, 11:947-962.
92. He J., Crews F.T. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Experimental Neurology 2008, 210:349-358.
93. Heilig M., Koob G.F. A key role for corticotropin-releasing factor in alcohol dependence. Trends in Neurosciences 2007, 30:399-406.
94. Herman M.A., Roberto M. Cell-type-specific tonic GABA signaling in the rat central amygdala is selectively altered by acute and chronic alcohol. Addiction Biology 2014, 21:72-86.
95. Herman M.A., Roberto M. The addicted brain: understanding the neurophysiological mechanisms of addictive disorders. Frontiers in Integrative Neuroscience 2015, 9:18.
96. Herman M.A., Varodayan F.P., Oleata C.S., Luu G., Kirson D., Heilig M., et al. Glutamatergic transmission in the central nucleus of the amygdala is selectively altered in Marchigian Sardinian alcohol-preferring rats: alcohol and CRF effects. Neuropharmacology 2015, 102:21-31.
97. Higgins R.L., Marlatt G.A. Effects of anxiety arousal on the consumption of alcohol by alcoholics and social drinkers. Journal of Consulting and Clinical Psychology 1973, 41:426-433.
98. Higgins R.L., Marlatt G.A. Fear of interpersonal evaluation as a determinant of alcohol consumption in male social drinkers. Journal of Abnormal Psychology 1975, 84:644-651.
99. Hingson R.W., Heeren T., Winter M.R. Age at drinking onset and alcohol dependence: age at onset, duration, and severity. Archives of Pediatrics & Adolescent Medicine 2006, 160:739-746.
100. Huang M.M., Overstreet D.H., Knapp D.J., Angel R., Wills T.A., Navarro M., et al. Corticotropin-releasing factor (CRF) sensitization of ethanol withdrawal-induced anxiety-like behavior is site specific and mediated by CRF-1 receptors: relation to stress-induced sensitization. The Journal of Pharmacology and Experimental Therapeutics 2010, 332:298-307.
101. Hueston C.M., Barnum C.J., Eberle J.A., Ferraioli F.J., Buck H.M., Deak T. Stress-dependent changes in neuroinflammatory markers observed after common laboratory stressors are not seen following acute social defeat of the Sprague Dawley rat. Physiology & Behavior 2011, 104:187-198.
102. Imaki T., Shibasaki T., Hotta M., Demura H. Intracerebroventricular administration of corticotropin-releasing factor induces c-fos mRNA expression in brain regions related to stress responses: comparison with pattern of c-fos mRNA induction after stress. Brain Research 1993, 616:114-125.
103. Iwata M., Ota K.T., Duman R.S. The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain, Behavior, and Immunity 2013, 31:105-114.
104. Jiménez-Sainz M.C., Fast B., Mayor F., Aragay A.M. Signaling pathways for monocyte chemoattractant protein 1-mediated extracellular signal-regulated kinase activation. Molecular Pharmacology 2003, 64:773-782.
105. Johnson J.D., Campisi J., Sharkey C.M., Kennedy S.L., Nickerson M., Greenwood B.N., et al. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 2005, 135:1295-1307.
106. Johnson J.D., O'Connor K.A., Watkins L.R., Maier S.F. The role of IL-1beta in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 2004, 127:569-577.
107. Johnson J.D., Zimomra Z.R., Stewart L.T. Beta-adrenergic receptor activation primes microglia cytokine production. Journal of Neuroimmunology 2013, 254:161-164.
108. June H.L., Liu J., Warnock K.T., Bell K.A., Balan I., Bollino D., et al. CRF-amplified neuronal TLR4/MCP-1 signaling regulates alcohol self-administration. Neuropsychopharmacology 2015, 40:1549-1559.
109. 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 and Alcoholism 2003, 38:189-193.
110. Kane C.J., Phelan K.D., Douglas J.C., Wagoner G., Johnson J.W., Xu J., et al. Effects of alcohol on immune response in the brain: region-specific changes in adolescent versus adult mice. Alcoholism: Clinical and Experimental Research 2014, 38:384-391.
111. Kiefer F., Jahn H., Schick M., Wiedemann K. Alcohol intake, tumour necrosis factor-alpha, leptin and craving: factors of a possibly vicious circle?. Alcohol and Alcoholism 2002, 37:401-404.
112. Kim J.B., Sig Choi J., Yu Y.M., Nam K., Piao C.S., Kim S.W., et al. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. The Journal of Neuroscience 2006, 26:6413-6421.
113. Knapp D.J., Overstreet D.H., Angel R.A., Navarro M., Breese G.R. The amygdala regulates the antianxiety sensitization effect of flumazenil during repeated chronic ethanol or repeated stress. Alcoholism: Clinical and Experimental Research 2007, 31:1872-1882.
114. Knapp D.J., Overstreet D.H., Breese G.R. Modulation of ethanol withdrawal-induced anxiety-like behavior during later withdrawals by treatment of early withdrawals with benzodiazepine/gamma-aminobutyric acid ligands. Alcoholism: Clinical and Experimental Research 2005, 29:553-563.
115. Knapp D.J., Overstreet D.H., Breese G.R. Baclofen blocks expression and sensitization of anxiety-like behavior in an animal model of repeated stress and ethanol withdrawal. Alcoholism: Clinical and Experimental Research 2007, 31:582-595.
116. Knapp D.J., Overstreet D.H., Moy S.S., Breese G.R. SB242084, flumazenil, and CRA1000 block alcohol withdrawal-induced anxiety in rats. Alcohol 2004, 32:101-111.
117. Knapp D.J., Whitman B.A., Harper K., Breese G.R. Stress and chronic alcohol differentially induce neuroimmune mRNAs in subregions of the rat brain. Alcoholism: Clinical and Experimental Research 2015, 39:127a. supplement S1.
118. Knapp D.J., Whitman B.A., Wills T.A., Angel R.A., Overstreet D.H., Criswell H.E., et al. Cytokine involvement in stress may depend on corticotrophin releasing factor to sensitize ethanol withdrawal anxiety. Brain, Behavior, and Immunity 2011, 25:S146-S154.
119. Kofoed L., Friedman M.J., Peck R. Alcoholism and drug abuse in patients with PTSD. The Psychiatric Quarterly 1993, 64:151-171.
120. Koob G.F. Neuroadaptive mechanisms of addiction: studies on the extended amygdala. European Neuropsychopharmacology 2003, 13:442-452.
121. Koob G.F. Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 2008, 56(SUPPL. 1):18-31.
122. Koob G.F. Neurocircuitry of alcohol addiction: synthesis from animal models. Handbook of Clinical Neurology 2014, 125:33-54.
123. Koob G.F. The dark side of emotion: the addiction perspective. European Journal of Pharmacology 2015, 753:73-87.
124. Koob G.F., Heinrichs S.C. A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Research 1999, 848:141-152.
125. Kwako L.E., Spagnolo P.A., Schwandt M.L., Thorsell A., George D.T., Momenan R., et al. The corticotropin releasing hormone-1 (CRH1) receptor antagonist pexacerfont in alcohol dependence: a randomized controlled experimental medicine study. Neuropsychopharmacology 2015, 40:1053-1063.
126. Lin Q., Yang X.P., Fang D., Ren X., Zhou H., Fang J., et al. High-mobility group box-1 mediates toll-like receptor 4-dependent angiogenesis. Arteriosclerosis, Thrombosis, and Vascular Biology 2011, 31:1024-1032.
127. Liu L., Hutchinson M.R., White J.M., Somogyi A.A., Coller J.K. Association of IL-1B genetic polymorphisms with an increased risk of opioid and alcohol dependence. Pharmacogenetics and Genomics 2009, 19:869-876.
128. Liu J., Yang A.R., Kelly T., Puche A., Esoga C., June H.L., et al. Binge alcohol drinking is associated with GABAA alpha2-regulated Toll-like receptor 4 (TLR4) expression in the central amygdala. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:4465-4470.
129. Lovallo W.R., Dickensheets S.L., Myers D.A., Thomas T.L., Nixon S.J. Blunted stress cortisol response in abstinent alcoholic and polysubstance-abusing men. Alcoholism: Clinical and Experimental Research 2000, 24:651-658.
130. Lukáts B., Egyed R., Karádi Z. Single neuron activity changes to interleukin-1beta in the orbitofrontal cortex of the rat. Brain Research 2005, 1038:243-246.
131. Lutz B., Marsicano G., Maldonado R., Hillard C.J. The endocannabinoid system in guarding against fear, anxiety and stress. Nature Reviews. Neuroscience 2015, 16:705-718.
132. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience 2010, 13:133-140.
133. Madrigal J.L., Garcia-Bueno B., Hinojosa A.E., Polak P., Feinstein D.L., Leza J.C. Regulation of MCP-1 production in brain by stress and noradrenaline-modulating drugs. Journal of Neurochemistry 2010, 113:543-551.
134. Mantsch J.R., Baker D.A., Funk D., Lê A.D., Shaham Y. Stress-induced reinstatement of drug seeking: 20 years of progress. Neuropsychopharmacology 2015, 41:335-356.
135. Relapse prevention: Maintenance strategies in the treatment of addictive behaviors 1985, The Guilford Press, New York, NY. G.A. Marlatt, J.R. Gordon (Eds.).
136. Marshall S.A., Casachahua J.D., Rinker J.A., Blose A.K., Lyse D.T., Thiele T.E. IL-1 receptor signaling in the basolateral amygdala modulates binge-like ethanol consumption in male C57BL/6J mice. Brain, Behavior, and Immunity 2015, 51:258-267.
137. Mayfield J., Ferguson L., Harris R.A. Neuroimmune signaling: a key component of alcohol abuse. Current Opinion in Neurobiology 2013, 23:513-520.
138. McCown T.J., Breese G.R. Multiple withdrawals from chronic alcohol "kindles" inferior collicular seizure activity: evidence for kindling of seizures associated with alcoholism. Alcoholism: Clinical and Experimental Research 1990, 14:394-399.
139. McEwen B.S., Nasca C., Gray J.D. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 2015, 41:3-23.
140. Merlo Pich E., Lorang M., Yeganeh M., Rodriguez de Fonseca F., Raber J., Koob G.F., et al. Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and alcohol withdrawal as measured by microdialysis. The Journal of Neuroscience 1995, 15:5439-5447.
141. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biological Psychiatry 2009, 65:732-741.
142. Minami M., Kuraishi Y., Yamaguchi T., Nakai S., Hirai Y., Satoh M. Immobilization stress induces interleukin-1 beta mRNA in the rat hypothalamus. Neuroscience Letters 1991, 123:254-256.
143. Ming Z., Criswell H.E., Breese G.R. Evidence for TNFα action on excitatory and inhibitory neurotransmission in the central amygdala: a brain site influenced by stress. Brain, Behavior, and Immunity 2013, 33:102-111.
144. Montesinos J., Pascual M., Pla A., Maldonado C., Rodríguez-Arias M., Miñarro J., et al. TLR4 elimination prevents synaptic and myelin alterations and long-term cognitive dysfunctions in adolescent mice with intermittent alcohol treatment. Brain, Behavior, and Immunity 2015, 45:233-244.
145. Monti P.M., Binkoff J.A., Abrams D.B., Zwick W.R., Nirenberg T.D., Liepman M.R. Reactivity of alcoholics and nonalcoholics to drinking cues. Journal of Abnormal Psychology 1987, 96:122-126.
146. Munro C.A., Oswald L.M., Weerts E.M., McCaul M.E., Wand G.S. Hormone responses to social stress in abstinent alcohol-dependent subjects and social drinkers with no history of alcohol dependence. Alcoholism: Clinical and Experimental Research 2005, 29:1133-1138.
147. Muscatell K.A., Dedovic K., Slavich G.M., Jarcho M.R., Breen E.C., Bower J.E., et al. Greater amygdala activity and dorsomedial prefrontal-amygdala coupling are associated with enhanced inflammatory responses to stress. Brain, Behavior, and Immunity 2015, 43:46-53.
148. Namburi P., Beyeler A., Yorozu S., Calhoon G.G., Halbert S.A., Wichmann R., et al. A circuit mechanism for differentiating positive and negative associations. Nature 2015, 520:675-678.
149. Nguyen K.T., Deak T., Owens S.M., Kohno T., Fleshner M., Watkins L.R., et al. Exposure to acute stress induces brain interleukin-1beta protein in the rat. The Journal of Neuroscience 1998, 18:2239-2246.
150. Nguyen K.T., Deak T., Will M.J., Hansen M.K., Hunsaker B.N., Fleshner M., et al. Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1beta protein response to acute stress. Brain Research 2000, 859:193-201.
151. O'Connor K.A., Johnson J.D., Hansen M.K., Wieseler Frank J.L., Maksimova E., Watkins L.R., et al. Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Research 2003, 991:123-132.
152. Oh S.W., Harris J.A., Ng L., Winslow B., Cain N., Mihalas S., et al. A mesoscale connectome of the mouse brain. Nature 2014, 508:207-214.
153. Overstreet D.H., Knapp D.J., Breese G.R. Accentuated decrease in social interaction in rats subjected to repeated alcohol withdrawals. Alcoholism: Clinical and Experimental Research 2002, 26:1259-1268.
154. Overstreet D.H., Knapp D.J., Breese G.R. Modulation of multiple ethanol withdrawal-induced anxiety-like behavior by CRF and CRF1 receptors. Pharmacology, Biochemistry, and Behavior 2004, 77:405-413.
155. Overstreet D.H., Knapp D.J., Breese G.R. Similar anxiety-like responses in male and female rats exposed to repeated withdrawals from alcohol. Pharmacology, Biochemistry, and Behavior 2004, 78:459-464.
156. Overstreet D.H., Knapp D.J., Breese G.R. Pharmacological modulation of repeated ethanol withdrawal-induced anxiety-like behavior differs in alcohol-preferring P and Sprague-Dawley rats. Pharmacology, Biochemistry, and Behavior 2005, 81:122-130.
157. Overstreet D.H., Knapp D.J., Moy S.S., Breese G.R. A 5-HT1A agonist and a 5-HT2c antagonist reduce social interaction deficit induced by multiple ethanol withdrawals in rats. Psychopharmacology 2003, 167:344-352.
158. Pandey S.C. TLR4-MyD88 signalling: a molecular target for alcohol actions. British Journal of Pharmacology 2012, 165:1316-1318.
159. Papadopoulou N., Chen J., Randeva H.S., Levine M.A., Hillhouse E.W., Grammatopoulos D.K. Protein kinase A-induced negative regulation of the corticotropin-releasing hormone R1alpha receptor-extracellularly regulated kinase signal transduction pathway: the critical role of Ser301 for signaling switch and selectivity. Molecular Endocrinology 2004, 18:624-639.
160. Park J.S., Gamboni-Robertson F., He Q., Svetkauskaite D., Kim J.Y., Strassheim D., et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. American Journal of Physiology. Cell Physiology 2006, 290:C917-C924.
161. Park J.S., Svetkauskaite D., He Q., Kim J.Y., Strassheim D., Ishizaka A., et al. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. The Journal of Biological Chemistry 2004, 279:7370-7377.
162. Pascual M., Baliño P., Alfonso-Loeches S., Aragón C.M., Guerri C. Impact of TLR4 on behavioral and cognitive dysfunctions associated with alcohol-induced neuroinflammatory damage. Brain, Behavior, and Immunity 2011, 25(SUPPL. 1):S80-S91.
163. Pascual M., Baliño P., Aragón C.M., Guerri C. Cytokines and chemokines as biomarkers of ethanol-induced neuroinflammation and anxiety-related behavior: role of TLR4 and TLR2. Neuropharmacology 2015, 89:352-359.
164. Payne T.J., Rychtarik R.G., Rappaport N.B., Smith P.O., Etscheidt M., Brown T.A., et al. Reactivity to alcohol-relevant beverage and imaginal cues in alcoholics. Addictive Behaviors 1992, 17:209-217.
165. Pla A., Pascual M., Renau-Piqueras J., Guerri C. TLR4 mediates the impairment of ubiquitin-proteasome and autophagy-lysosome pathways induced by ethanol treatment in brain. Cell Death & Disease 2014, 5:e1066.
166. Porterfield V.M., Gabella K.M., Simmons M.A., Johnson J.D. Repeated stressor exposure regionally enhances beta-adrenergic receptor-mediated brain IL-1β production. Brain, Behavior, and Immunity 2012, 26:1249-1255.
167. Porterfield V.M., Zimomra Z.R., Caldwell E.A., Camp R.M., Gabella K.M., Johnson J.D. Rat strain differences in restraint stress-induced brain cytokines. Neuroscience 2011, 188:48-54.
168. Pucak M.L., Kaplin A.I. Unkind cytokines: current evidence for the potential role of cytokines in immune-mediated depression. International Review of Psychiatry 2005, 17:477-483.
169. Qin L., He J., Hanes R.N., Pluzarev O., Hong J.S., Crews F.T. Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. Journal of Neuroinflammation 2008, 5:10.
170. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
171. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends in Immunology 2006, 27:24-31.
172. Rassnick S., Heinrichs S.C., Britton K.T., Koob G.F. Microinjection of a corticotropin-releasing factor antagonist into the central nucleus of the amygdala reverses anxiogenic-like effects of ethanol withdrawal. Brain Research 1993, 605:25-32.
173. Rau A.R., Chappell A.M., Butler T.R., Ariwodola O.J., Weiner J.L. Increased basolateral amygdala pyramidal cell excitability may contribute to the anxiogenic phenotype induced by chronic early-life stress. The Journal of Neuroscience 2015, 35:9730-9740.
174. Richiardi J., Altmann A., Milazzo A.C., Chang C., Chakravarty M.M., Banaschewski T., et al. Brain networks. Correlated gene expression supports synchronous activity in brain networks. Science 2015, 348:1241-1244.
175. Rossi S., Sacchetti L., Napolitano F., De Chiara V., Motta C., Studer V., et al. Interleukin-1β causes anxiety by interacting with the endocannabinoid system. The Journal of Neuroscience 2012, 32:13896-13905.
176. Rostène W., Kitabgi P., Parsadaniantz S.M. Chemokines: a new class of neuromodulator?. Nature Reviews. Neuroscience 2007, 8:895-903.
177. Saiz P.A., Garcia-Portilla M.P., Florez G., Corcoran P., Arango C., Morales B., et al. Polymorphisms of the IL-1 gene complex are associated with alcohol dependence in Spanish Caucasians: data from an association study. Alcoholism: Clinical and Experimental Research 2009, 33:2147-2153.
178. Seo D., Jia Z., Lacadie C.M., Tsou K.A., Bergquist K., Sinha R. Sex differences in neural responses to stress and alcohol context cues. Human Brain Mapping 2011, 32:1998-2013.
179. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
180. Shintani F., Nakaki T., Kanba S., Kato R., Asai M. Role of interleukin-1 in stress responses. A putative neurotransmitter. Molecular Neurobiology 1995, 10:47-71.
181. Shintani F., Nakaki T., Kanba S., Sato K., Yagi G., Shiozawa M., et al. Involvement of interleukin-1 in immobilization stress-induced increase in plasma adrenocorticotropic hormone and in release of hypothalamic monoamines in the rat. The Journal of Neuroscience 1995, 15:1961-1970.
182. Shizuya K., Komori T., Fujiwara R., Miyahara S., Ohmori M., Nomura J. The influence of restraint stress on the expression of mRNAs for IL-6 and the IL-6 receptor in the hypothalamus and midbrain of the rat. Life Sciences 1997, 61:PL 135-140.
183. Silberman Y., Winder D.G. Ethanol and corticotropin releasing factor receptor modulation of central amygdala neurocircuitry: an update and future directions. Alcohol 2015, 49:179-184.
184. Sillaber I., Henniger M.S. Stress and alcohol drinking. Annals of Medicine 2004, 36:596-605.
185. Sinha R. How does stress increase risk of drug abuse and relapse?. Psychopharmacology 2001, 158:343-359.
186. Sinha R. The role of stress in addiction relapse. Current Psychiatry Reports 2007, 9:388-395.
187. Sinha R., Fox H.C., Hong K.A., Bergquist K., Bhagwagar Z., Siedlarz K.M. Enhanced negative emotion and alcohol craving, and altered physiological responses following stress and cue exposure in alcohol dependent individuals. Neuropsychopharmacology 2009, 34:1198-1208.
188. Sinha R., Fox H.C., Hong K.I., Hansen J., Tuit K., Kreek M.J. Effects of adrenal sensitivity, stress- and cue-induced craving, and anxiety on subsequent alcohol relapse and treatment outcomes. Archives of General Psychiatry 2011, 68:942-952.
189. Sinha R., O'Malley S.S. Craving for alcohol: findings from the clinic and the laboratory. Alcohol and Alcoholism 1999, 34:223-230.
190. Sternson S.M., Roth B.L. Chemogenetic tools to interrogate brain function. Annual Review of Neuroscience 2014, 37:387-407.
191. Su X., Wang H., Zhao J., Pan H., Mao L. Beneficial effects of ethyl pyruvate through inhibiting high-mobility group box 1 expression and TLR4/NF-κB pathway after traumatic brain injury in the rat. Mediators of Inflammation 2011, 286:12213-12220.
192. Suzuki E., Shintani F., Kanba S., Asai M., Nakaki T. Immobilization stress increases mRNA levels of interleukin-1 receptor antagonist in various rat brain regions. Cellular and Molecular Neurobiology 1997, 17:557-562.
193. Szczytkowski J.L., Lysle D.T. Dopamine D1 receptors within the basolateral amygdala mediate heroin-induced conditioned immunomodulation. Journal of Neuroimmunology 2010, 226:38-47.
194. Tate S.R., McQuaid J.R., Brown S.A. Characteristics of life stressors predictive of substance treatment outcomes. Journal of Substance Abuse Treatment 2005, 29:107-115.
195. Tovote P., Fadok J.P., Lüthi A. Neuronal circuits for fear and anxiety. Nature Reviews. Neuroscience 2015, 16:317-331.
196. Turnbull A.V., Rivier C. Regulation of the HPA axis by cytokines. Brain, Behavior, and Immunity 1995, 9:253-275.
197. Uddin M., Koenen K.C., Aiello A.E., Wildman D.E., de los Santos R., Galea S. Epigenetic and inflammatory marker profiles associated with depression in a community-based epidemiologic sample. Psychological Medicine 2011, 41:997-1007.
198. Uhart M., Wand G.S. Stress, alcohol and drug interaction: an update of human research. Addiction Biology 2009, 14:43-64.
199. Ulloa L., Ochani M., Yang H., Tanovic M., Halperin D., Yang R., et al. Ethyl pyruvate prevents lethality in mice with established lethal sepsis and systemic inflammation. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:12351-12356.
200. Urban D.J., Roth B.L. DREADDs (designer receptors exclusively activated by designer drugs): chemogenetic tools with therapeutic utility. Annual Review of Pharmacology and Toxicology 2015, 55:399-417.
201. Valdez G.R., Zorrilla E.P., Roberts A.J., Koob G.F. Antagonism of corticotropin-releasing factor attenuates the enhanced responsiveness to stress observed during protracted alcohol abstinence. Alcohol 2003, 29:55-60.
202. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
203. Vujanovic A.A., Bonn-Miller M.O., Marlatt G.A. Posttraumatic stress and alcohol use coping motives among a trauma-exposed community sample: the mediating role of non-judgmental acceptance. Addictive Behaviors 2011, 36:707-712.
204. Weber M.D., Frank M.G., Sobesky J.L., Watkins L.R., Maier S.F. Blocking toll-like receptor 2 and 4 signaling during a stressor prevents stress-induced priming of neuroinflammatory responses to a subsequent immune challenge. Brain, Behavior, and Immunity 2013, 32:112-121.
205. Whitman, B.. (2012). Neuroimmune consequences of chronic alcohol exposure: relationship to stress. Dissertation in partial fulfillment of the requirements for degree of Doctor of Philosophy in the Curriculum of Neurobiology, UNC at Chapel Hill.
206. Whitman B., Knapp D.J., Werner D.F., Crews F.T., Breese G.R. The cytokine mRNA increase induced by withdrawal from chronic alcohol in the sterile environment of brain is mediated by CRF and HMGB1 release. Alcoholism: Clinical and Experimental Research 2013, 37:2086-2097.
207. Wohleb E.S., Hanke M.L., Corona A.W., Powell N.D., Stiner L.M., Bailey M.T., et al. β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. The Journal of Neuroscience 2011, 31:6277-6288.
208. Wu Y., Lousberg E.L., Moldenhauer L.M., Hayball J.D., Coller J.K., Rice K.C., et al. Inhibiting the TLR4-MyD88 signalling cascade by genetic or pharmacological strategies reduces acute alcohol-induced sedation and motor impairment in mice. British Journal of Pharmacology 2012, 165:1319-1329.
209. Yamada S., Maruyama I. HMGB1, a novel inflammatory cytokine. Clinica Chimica Acta 2007, 375:36-42.
210. Yang H., Wang H., Czura C.J., Tracey K.J. The cytokine activity of HMGB1. Journal of Leukocyte Biology 2005, 78:1-8.
211. Yehuda R., Giller E.L., Southwick S.M., Lowy M.T., Mason J.W. Hypothalamic-pituitary-adrenal dysfunction in posttraumatic stress disorder. Biological Psychiatry 1991, 30:1031-1048.
212. Yu M., Wang H., Ding A., Golenbock D.T., Latz E., Czura C.J., et al. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 2006, 26:174-179.
213. Zhou Y., Tang H., Liu J., Dong J., Xiong H. Chemokine CCL2 modulation of neuronal excitability and synaptic transmission in rat hippocampal slices. Journal of Neurochemistry 2011, 116:406-414.
214. Zou J., Crews F. Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-κB and proinflammatory cytokines. Alcoholism: Clinical and Experimental Research 2010, 34:777-789.
215. Zou J., Vetreno R.P., Crews F.T. ATP-P2X7 receptor signaling controls basal and TNFα-stimulated glial cell proliferation. Glia 2012, 60:661-673.