Mechanisms of stress-dependent neuroinflammation and their implications for understanding consequences of alcohol exposure

Neural-Immune Interactions in Brain Function and Alcohol Related Disorders

Volumn , Issue , 2013, Pages 133-166

  Deak, Terrence ^a   Okrainets, Anny ^a   Doremus Fitzwater, Tamara L ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84906335610     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-4729-0_5     Document Type: Chapter

References (171)

1. Dhabhar FS, McEwen BS (1997) Acute stress enhances while chronic stress suppresses cell mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behav Immun 11: 286-306
2. Deak T et al (1997) Evidence that brief stress may induce the acute phase response in rats. Am J Physiol 273: R1998-R2004
3. Deak T, Nguyen KT, Fleshner M, Watkins LR, Maier SF (1999) Acute stress may facilitate recovery from a subcutaneous bacterial challenge. Neuroimmunomodulation 6: 344-354
4. Fleshner M, Nguyen KT, Cotter CS, Watkins LR, Maier SF (1998) Acute stressor exposure both suppresses acquired immunity and potentiates innate immunity. Am J Physiol 275: R870-R878
5. Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF (2007) Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 21: 47-59
6. Frank MG, Miguel ZD, Watkins LR, Maier SF (2010) Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav Immun 24: 19-30
7. Johnson JD et al (2002) Prior stressor exposure primes the HPA axis. Psychoneuroendocrinology 27: 353-365
8. Johnson JD, O'Connor KA, Hansen MK, Watkins LR, Maier SF (2003) Effects of prior stress on LPS-induced cytokine and sickness responses. Am J Physiol 284: R422-R432
9. Johnson JD, O'Connor KA, Watkins LR, Maier SF (2004) The role of IL-1b in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 127: 569-577
10. Sawchenko PE, Li HY, Ericsson A (2000) Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Prog Brain Res 122: 61-78
11. Turnbull AV, Rivier C (1995) Regulation of the HPA axis by cytokines. Brain Behav Immun 9: 253-275
12. Turnbull AV, Rivier CL (1999) Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 79: 1-71
13. Smagin GN, Swiergiel AH, Dunn AJ (1996) Peripheral administration of interleukin-1 increases extracellular concentrations of norepinephrine in rat hypothalamus: comparison with plasma corticosterone. Psychoneuroendocrinology 21: 83-93
14. van Dam AM, Brouns M, Louisse S, Berkenbosch F (1992) Appearance of interleukin-1 in macrophages and in ramified microglia in the brain of endotoxin-treated rats: a pathway for the induction of non-specific symptoms of sickness. Brain Res 588: 291-296
15. Martinez F, Abril ER, Earnest DL, Watson RR (1992) Ethanol and cytokine secretion. Alcohol 9: 455-458
16. Tringali G et al (1996) Evidence for the neuronal origin of immunoreactive interleukin-1 beta released by rat hypothalamic explants. Neurosci Lett 219: 143-146
17. Vitkovic L, Bockaert J, Jacque C (2000) "Inflammatory" cytokines: neuromodulators in normal brain. J Neurochem 74: 457-471
18. Avitsur R, Cohen E, Yirmiya R (1997) Effects of interleukin-1 on sexual attractivity in a model of sickness behavior. Physiol Behav 63: 25-30
19. Avitsur R, Yirmiya R (1999) The immunobiology of sexual behavior: gender differences in the suppression of sexual activity during illness. Pharmacol Biochem Behav 64: 787-796
20. Bluthe RM et al (1999) Central injection of IL-10 antagonizes the behavioural effects of lipopolysaccharide in rats. Psychoneuroendocrinology 24: 301-311
21. Dantzer R (2001) Cytokine-induced sickness behavior: mechanisms and implications. Ann N Y Acad Sci 933: 222-234
22. Deak T, Bellamy C, Bordner KA (2005) Protracted increases in core body temperature and interleukin-1 following acute administration of lipopolysaccharide: implications for the stress response. Physiol Behav 85: 296-307
23. Deak T et al (2005) Behavioral responses during the forced swim test are not affected by anti-inflammatory agents or acute illness induced by lipopolysaccharide. Behav Brain Res 160: 125-134
24. Plata-Salaman CR (1994) Meal patterns in response to the intracerebroventricular administration of interleukin-1 beta in rats. Physiol Behav 55: 727-733
25. Plata-Salaman CR, Ffrench-Mullen JM (1992) Intracerebroventricular administration of a specific IL-1 receptor antagonist blocks food and water intake suppression induced by interleukin-1 beta. Physiol Behav 51: 1277-1279
26. Hart BL (1988) Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12: 123-137
27. Johnson DR, O'Connor JC, Hartman ME, Tapping RI, Freund GG (2007) Acute hypoxia activates the neuroimmune system, which diabetes exacerbates. J Neurosci 27: 1161-1166
28. Plata-Salaman CR, Oomura Y, Kai Y (1988) Tumor necrosis factor and interleukin-1 beta: suppression of food intake by direct action in the central nervous system. Brain Res 448: 106-114
29. Maier SF, Watkins LR (1998) Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychol Rev 105: 83-107
30. Breder CD, Dinarello CA, Saper CB (1988) Interleukin-1 immunoreactive innervation of the human hypothalamus. Science 240: 321-324
31. Cadet P et al (2003) Cyclic exercise induces anti-inflammatory signal molecule increases in the plasma of Parkinson's patients. Int J Mol Med 12: 485-492
32. Wandinger KP et al (1999) Effects of amantadine treatment on in vitro production of interleukin-2 in de-novo patients with idiopathic Parkinson's disease. J Neuroimmunol 98: 214-220
33. Tringali G, Dello Russo C, Preziosi P, Navarra P (1998) Hypothalamic interleukin-1 in physiology and pathology. Toxicol Lett 102-103: 295-299
34. Opal SM, DePalo VA (2000) Anti-inflammatory cytokines. Chest 117: 1162-1172
35. Anisman H (2004) Considering cytokine panels. Brain Behav Immun 18: 221-222
36. Dantzer R (2004) Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500: 399-411
37. Barak O et al (2002) Involvement of brain cytokines in the neurobehavioral disturbances induced by HIV-1 glycoprotein120. Brain Res 933: 98-108
38. Arimoto T et al (2007) Interleukin-10 protects against inflammation-mediated degeneration of dopaminergic neurons in substantia nigra. Neurobiol Aging 28: 894-906
39. Milligan ED et al (2005) Controlling pathological pain by adenovirally driven spinal production of the anti-inflammatory cytokine, interleukin-10. Eur J Neurosci 21: 2136-2148
40. Milligan ED et al (2005) Controlling neuropathic pain by adeno-associated virus driven production of the anti-inflammatory cytokine, interleukin-10. Mol Pain 1: 9
41. Soderquist RG et al (2010) Release of plasmid DNA-encoding IL-10 from PLGA microparticles facilitates long-term reversal of neuropathic pain following a single intrathecal administration. Pharm Res 27: 841-854
42. Milligan ED et al (1998) The long term acute phase-like responses that follow acute stressor exposure are blocked by alpha-melanocyte stimulating hormone. Brain Res 810: 48-58
43. Lasaga M, Debeljuk L, Durand D, Scimonelli TN, Caruso C (2008) Role of alpha-melanocyte stimulating hormone and melanocortin 4 receptor in brain inflammation. Peptides 29: 1825-1835
44. Maslanik T, Bernstein-Hanley I, Helwig B, Fleshner M (2012) The impact of acute-stressor exposure on splenic innate immunity: a gene expression analysis. Brain Behav Immun 26: 142-149
45. Nguyen KT et al (2000) Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1b protein response to acute stress. Brain Res 859: 193-201
46. Hansen M, Krueger J (1997) Subdiaphragmatic vagotomy blocks the sleep and fever-promoting effects of interleukin-1B. Am J Physiol 273: R1246-R1253
47. Krueger JM, Walter J, Dinarello CA, Wolff SM, Chedid L (1984) Sleep promoting effects of endogenous pyrogen (interleukin-1). Am J Physiol 246: 994-999
48. Opp MR, Krueger JM (1991) Interleukin-1 receptor antagonist blocks interleukin-1-induced sleep and fever. Am J Physiol 260: 453-457
49. Taishi P, Bredow S, Guha-Thakurta N, Obal F, Krueger J (1997) Diurnal variations of interleukin-1b mRNA and b-actin mRNA in rat brain. J Neuroimmunol 75: 69-74
50. Hansen MK, Taishi P, Chen Z, Krueger JM (1998) Cafeteria feeding induces interleukin-1beta mRNA expression in rat liver and brain. Am J Physiol 274: 793-798
51. Allan SM et al (2000) Cortical cell death induced by IL-1 is mediated via actions in the hypothalamus of the rat. Proc Natl Acad Sci USA 97: 5580-5585
52. Grundy R, Rothwell N, Allan S (2002) Site-specific actions of interleukin-1 on excitotoxic cell death in the rat striatum. Brain Res 926: 142-148
53. Proescholdt M et al (2002) Intracerebroventricular but not intravenous interleukin-1b induces widespread vascular-mediated leukocyte infiltration and immune signal mRNA expression followed by brain-wide glial activation. Neuroscience 112: 731-749
54. Nguyen KT et al (1998) Exposure to acute stress induces brain interleukin-1b protein in the rat. J Neurosci 18: 2239-2246
55. Deak T, Bellamy C, D'Agostine L (2003) Exposure to forced swim stress does not alter central production of IL-1. Brain Res 972: 53-63
56. O'Connor K et al (2003) Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 991: 123-132
57. Blandino P Jr, Barnum CJ, Deak T (2006) The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. J Neuroimmunol 173: 87-95
58. Blandino P Jr et al (2009) Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav Immun 23: 958-968
59. Arakawa H, Blandino P Jr, Deak T (2009) Central infusion of interleukin-1 receptor antagonist blocks the reduction in social behavior produced by prior stressor exposure. Physiol Behav 98: 139-146
60. Johnson JD et al (2005) Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 135: 1295-1307
61. Hueston CM et al (2011) Stress-dependent changes in neuroinflammatory markers observed after common laboratory stressors are not seen following acute social defeat of the Sprague Dawley rat. Physiol Behav 104: 187-198
62. Plata-Salaman CR et al (2000) Neither acute nor chronic exposure to a naturalistic (predator) stressor influences the interleukin-1beta system, tumor necrosis factor-alpha, transforming growth factor-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res Bull 51: 187-193
63. Deak T et al (2005) Stress-induced increases in hypothalamic IL-1: a systematic analysis of multiple stressor paradigms. Brain Res Bull 64: 541-556
64. Hennessy MB et al (2004) Responses of guinea pig pups during isolation in a novel environment may represent stress-induced sickness behaviors. Physiol Behav 81: 5-13
65. Barnum CJ, Blandino P Jr, Deak T (2008) Social status modulates basal IL-1 concentrations in the hypothalamus of pair-housed rats and influences certain features of stress reactivity. Brain Behav Immun 22: 517-527
66. Nair A, Bonneau RH (2006) Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol 171: 72-85
67. Kwon M et al (2008) The repeated immobilization stress increases IL-1beta immunoreactivities in only neuron, but not astrocyte or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neurosci Lett 430: 258-263
68. Jankord R et al (2010) Stress activation of IL-6 neurons in the hypothalamus. Am J Physiol Regul Integr Comp Physiol 299: R343-R351
69. Licinio J, Frost P (2000) The neuroimmune-endocrine axis: pathophysiological implications for the central nervous system cytokines and hypothalamus-pituitary-adrenal hormone dynamics. Braz J Med Biol Res 33: 1141-1148
70. Yamaguchi T, Kuraishi Y, Minami M, Yabuuchi K, Satoh M (1991) Involvement of central b-adrenoceptors in the induction of hypothalamic interleukin-1b mRNA by methamphetamine. Neurosci Res 12: 432-439
71. Maruta E et al (1997) Beta2-adrenoceptors on the glial cells mediate the induction of interleukin-1beta mRNA in the rat brain. Brain Res Mol Brain Res 49: 291-294
72. Yabuuchi K et al (1997) Intracerebroventricular injection of isoproterenol produces its analgesic effect through interleukin-1b production. Eur J Pharmacol 334: 133-140
73. Porterfield VM et al (2011) Rat strain differences in restraint stress-induced brain cytokines. Neuroscience 188: 48-54
74. Sawchenko PE, Swanson LW (1981) Central noradrenergic pathways for the integration of hypothalamic neuroendocrine and autonomic responses. Science 214: 685-687
75. Sawchenko PE, Swanson LW (1982) The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res 257: 275-325
76. Swanson LW, Hartman BK (1975) The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 163: 467-505
77. Swanson LW, Sawchenko PE (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6: 269-324
78. Morrow LE, McClellan JL, Conn CA, Kluger MJ (1993) Glucocorticoids alter fever and IL-6 responses to psychological stress and to lipopolysaccharide. Am J Physiol 264: R1010-R1016
79. Frank MG, Thompson BM, Watkins LR, Maier SF (2012) Glucocorticoids mediate stressinduced priming of microglial pro-inflammatory responses. Brain Behav Immun 26: 337-345
80. Sorrells SF, Sapolsky RM (2007) An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21: 259-272
81. Necela BM, Cidlowski JA (2004) Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. Proc Am Thorac Soc 1: 239-246
82. Watkins LR, Hansen MK, Nguyen KT, Lee JE, Maier SF (1999) Dynamic regulation of the proinflammatory cytokine interleukin-1b: molecular biology for non-molecular biologists. Life Sci 65: 449-481
83. Quan N, He L, Lai W, Shen T, Herkenham M (2000) Induction of IkappaBalpha mRNA expression in the brain by glucocorticoids: a negative feedback mechanism for immune-tobrain signaling. J Neurosci 20: 6473-6477
84. Deak T (2007) From hippocampus to dorsal horn: the pervasive impact of IL-1 on learning and memory spans the length of the neuroaxis. Brain Behav Immun 21: 746-747
85. Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron 11: 371-386
86. Garcia-Bueno B, Madrigal JL, Perez-Nievas BG, Leza JC (2008) Stress mediators regulate brain prostaglandin synthesis and peroxisome proliferator-activated receptor-gamma activation after stress in rats. Endocrinology 149: 1969-1978
87. Garcia-Bueno B, Caso JR, Leza JC (2008) Stress as a neuroinflammatory condition in brain: damaging and protective mechanisms. Neurosci Biobehav Rev 32: 1136-1151
88. Ziegler DR, Cullinan WE, Herman JP (2005) Organization and regulation of paraventricular nucleus glutamate signaling systems: N -methyl-d -aspartate receptors. J Comp Neurol 484: 43-56
89. Yirmiya R, Goshen I (2011) Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25: 181-213
90. Zhang XM, Zhu J (2011) Kainic acid-induced neurotoxicity: targeting glial responses and glia-derived cytokines. Curr Neuropharmacol 9: 388-398
91. Tringali G et al (1997) The release of immunoreactive interleukin-1 beta from rat hypothalamic explants is modulated by neurotransmitters and corticotropin-releasing hormone. Pharmacol Res 36: 269-273
92. Holguin A et al (2007) Characterization of the temporo-spatial effects of chronic bilateral intrahippocampal cannulae on interleukin-1beta. J Neurosci Methods 161: 265-272
93. Crews FT et al (2006) Cytokines and alcohol. Alcohol Clin Exp Res 30: 720-730
94. Achur RN, Freeman WM, Vrana KE (2010) Circulating cytokines as biomarkers of alcohol abuse and alcoholism. J Neuroimmune Pharmacol 5: 83-91
95. Sarc L, Wraber B, Lipnik-Stangelj M (2011) Ethanol and acetaldehyde disturb TNF-alpha and IL-6 production in cultured astrocytes. Hum Exp Toxicol 30: 1256-1265
96. Fernandez-Lizarbe S, Pascual M, Guerri C (2009) Critical role of TLR4 response in the activation of microglia induced by ethanol. J Immunol 183: 4733-4744
97. Tiwari V, Chopra K (2011) Resveratrol prevents alcohol-induced cognitive deficits and brain damage by blocking inflammatory signaling and cell death cascade in neonatal rat brain. J Neurochem 117: 678-690
98. Tiwari V, Kuhad A, Chopra K (2009) Suppression of neuro-inflammatory signaling cascade by tocotrienol can prevent chronic alcohol-induced cognitive dysfunction in rats. Behav Brain Res 203: 296-303
99. Emanuele N, LaPaglia N, Kovacs EJ, Emanuele MA (2005) Effects of chronic ethanol (EtOH) administration on pro-inflammatory cytokines of the hypothalamic-pituitary-gonadal (HPG) axis in female rats. Endocr Res 31: 9-16
100. Valles SL, Blanco AM, Pascual M, Guerri C (2004) Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes. Brain Pathol 14: 365-371
101. Breese GR et al (2008) Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 33: 867-876
102. Qin L et al (2008) Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 5: 10
103. Emanuele NV, LaPaglia N, Kovacs EJ, Emanuele MA (2005) The impact of burn injury and ethanol on the cytokine network of the mouse hypothalamus: reproductive implications. Cytokine 30: 109-115
104. Lee H et al (2004) Ethanol selectively modulates inflammatory activation signaling of brain microglia. J Neuroimmunol 156: 88-95
105. Alfonso-Loeches S, Pascual-Lucas M, Blanco AM, Sanchez-Vera I, Guerri C (2011) Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. J Neurosci 30: 8285-8295
106. D'Souza NB, Nelson S, Summer WR, Deaciuc IV (1996) Alcohol modulates alveolar macrophage tumor necrosis factor-alpha, superoxide anion, and nitric oxide secretion in the rat. Alcohol Clin Exp Res 20: 156-163
107. Honchel R et al (1992) Tumor necrosis factor in alcohol enhanced endotoxin liver injury. Alcohol Clin Exp Res 16: 665-669
108. D'Souza NB, Bagby GJ, Nelson S, Lang CH, Spitzer JJ (1989) Acute alcohol infusion suppresses endotoxin-induced serum tumor necrosis factor. Alcohol Clin Exp Res 13: 295-298
109. Nelson S, Bagby G, Summer WR (1989) Alcohol suppresses lipopolysaccharide-induced tumor necrosis factor activity in serum and lung. Life Sci 44: 673-676
110. Tiwari V, Kuhad A, Chopra K (2011) Amelioration of functional, biochemical and molecular deficits by epigallocatechin gallate in experimental model of alcoholic neuropathy. Eur J Pain 15: 286-292
111. Enomoto N et al (2003) Prevention of ethanol-induced liver injury in rats by an agonist of peroxisome proliferator-activated receptor-gamma, pioglitazone. J Pharmacol Exp Ther 306: 846-854
112. Valles SL et al (2003) Chronic ethanol consumption enhances interleukin-1-mediated signal transduction in rat liver and in cultured hepatocytes. Alcohol Clin Exp Res 27: 1979-1986
113. Kishore R, Hill JR, McMullen MR, Frenkel J, Nagy LE (2002) ERK1/2 and Egr-1 contribute to increased TNF-alpha production in rat Kupffer cells after chronic ethanol feeding. Am J Physiol Gastrointest Liver Physiol 282: G6-G15
114. Kishore R, McMullen MR, Nagy LE (2001) Stabilization of tumor necrosis factor alpha mRNA by chronic ethanol: role of A + U-rich elements and p38 mitogen-activated protein kinase signaling pathway. J Biol Chem 276: 41930-41937
115. Bhatty M, Jan BL, Tan W, Pruett SB, Nanduri B (2011) Role of acute ethanol exposure and TLR4 in early events of sepsis in a mouse model. Alcohol 45: 795-803
116. Pruett SB et al (2010) Innate immunity and inflammation in sepsis: mechanisms of suppressed host resistance in mice treated with ethanol in a binge-drinking model. Toxicol Sci 117: 314-324
117. Glover M, Cheng B, Fan R, Pruett S (2009) The role of stress mediators in modulation of cytokine production by ethanol. Toxicol Appl Pharmacol 239: 98-105
118. Pruett SB, Fan R (2009) Ethanol inhibits LPS-induced signaling and modulates cytokine production in peritoneal macrophages in vivo in a model for binge drinking. BMC Immunol 10: 49
119. Fernandez-Lizarbe S, Pascual M, Gascon MS, Blanco A, Guerri C (2008) Lipid rafts regulate ethanol-induced activation of TLR4 signaling in murine macrophages. Mol Immunol 45: 2007-2016
120. Dai Q, Pruett SB (2006) Different effects of acute and chronic ethanol on LPS-induced cytokine production and TLR4 receptor behavior in mouse peritoneal macrophages. J Immunotoxicol 3: 217-225
121. Pruett BS, Pruett SB (2006) An explanation for the paradoxical induction and suppression of an acute phase response by ethanol. Alcohol 39: 105-110
122. Dai Q, Zhang J, Pruett SB (2005) Ethanol alters cellular activation and CD14 partitioning in lipid rafts. Biochem Biophys Res Commun 332: 37-42
123. Goral J, Kovacs EJ (2005) In vivo ethanol exposure down-regulates TLR2-, TLR4-, and TLR9-mediated macrophage inflammatory response by limiting p38 and ERK1/2 activation. J Immunol 174: 456-463
124. Pruett SB, Fan R, Zheng Q, Schwab C (2005) Differences in IL-10 and IL-12 production patterns and differences in the effects of acute ethanol treatment on macrophages in vivo and in vitro. Alcohol 37: 1-8
125. Goral J, Choudhry MA, Kovacs EJ (2004) Acute ethanol exposure inhibits macrophage IL-6 production: role of p38 and ERK1/2 MAPK. J Leukoc Biol 75: 553-559
126. Pruett SB, Schwab C, Zheng Q, Fan R (2004) Suppression of innate immunity by acute ethanol administration: a global perspective and a new mechanism beginning with inhibition of signaling through TLR3. J Immunol 173: 2715-2724
127. Pruett SB, Zheng Q, Fan R, Matthews K, Schwab C (2004) Ethanol suppresses cytokine responses induced through Toll-like receptors as well as innate resistance to Escherichia coli in a mouse model for binge drinking. Alcohol 33: 147-155
128. Pruett SB, Fan R, Zheng Q (2003) Acute ethanol administration profoundly alters poly I: Cinduced cytokine expression in mice by a mechanism that is not dependent on corticosterone. Life Sci 72: 1825-1839
129. Mason CM, Dobard E, Kolls JK, Nelson S (2000) Ethanol and murine interleukin (IL)-12 production. Alcohol Clin Exp Res 24: 553-559
130. Vinson RB, Carroll JL, Pruett SB (1998) Mechanism of suppressed neutrophil mobilization in a mouse model for binge drinking: role of glucocorticoids. Am J Physiol 275: R1049-R1057
131. Han YC, Pruett SB (1995) Mechanisms of ethanol-induced suppression of a primary antibody response in a mouse model for binge drinking. J Pharmacol Exp Ther 275: 950-957
132. Hill DB et al (2002) A role for interleukin-10 in alcohol-induced liver sensitization to bacterial lipopolysaccharide. Alcohol Clin Exp Res 26: 74-82
133. Wang Y, Huang DS, Giger PT, Watson RR (1994) Influence of chronic dietary ethanol on cytokine production by murine splenocytes and thymocytes. Alcohol Clin Exp Res 18: 64-70
134. Crews FT, Vetreno RP (2011) Addiction, adolescence, and innate immune gene induction. Front Psychiatry 2: 19
135. Crews FT, Zou J, Qin L (2011) Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 25(Suppl 1): S4-S12
136. Kutscher S et al (2002) Concomitant endocrine and immune alterations during alcohol intoxication and acute withdrawal in alcohol-dependent subjects. Neuropsychobiology 45: 144-149
137. Laso FJ et al (1996) Long lasting immunological effects of ethanol after withdrawal. Cytometry 26: 275-280
138. Riikonen J et al (2002) Intermittent ethanol exposure increases the number of cerebellar microglia. Alcohol Alcohol 37: 421-426
139. Kim DJ et al (2003) Effects of alcohol hangover on cytokine production in healthy subjects. Alcohol 31: 167-170
140. Gonzalez-Quintela A et al (2000) Influence of acute ethanol intake and alcohol withdrawal on circulating levels of IL-6, IL-8, IL-10 and IL-12. Cytokine 12: 1437-1440
141. Qin L et al (2007) Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55: 453-462
142. Polazzi E, Contestabile A (2002) Reciprocal interactions between microglia and neurons: from survival to neuropathology. Rev Neurosci 13: 221-242
143. Colton CA, Snell-Callahan J, Chernyshev ON (1998) Ethanol induced changes in superoxide anion and nitric oxide in cultured microglia. Alcohol Clin Exp Res 22: 710-716
144. Vezzani A, Moneta D, Richichi C, Perego C, De Simoni MG (2004) Functional role of proin flammatory and anti-inflammatory cytokines in seizures. Adv Exp Med Biol 548: 123-133
145. Trevisan LA, Boutros N, Petrakis IL, Krystal JH (1998) Complications of alcohol withdrawal: pathophysiological insights. Alcohol Health Res World 22: 61-66
146. Goehler LE et al (2000) Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton Neurosci 85: 49-59
147. Hosoi T, Okuma Y, Nomura Y (2000) Electrical stimulation of afferent vagus nerve induces IL-1b expression in the brain and activates HPA axis. Am J Physiol 279: R141-R147
148. Hansen MK et al (2000) Effects of vagotomy on serum endotoxin, cytokines, and corticosterone after intraperitoneal lipopolysaccharide. Am J Physiol 278: R331-R336
149. Hansen MK et al (2000) Effects of vagotomy on lipopolysaccharide-induced brain interleukin-1beta protein in rats. Auton Neurosci 85: 119-126
150. Herzberg U, Sagen J (2001) Peripheral nerve exposure to HIV viral envelope protein gp120 induces neuropathic pain and spinal gliosis. J Neuroimmunol 116: 29-39
151. Romeo H, Tio D, Rahman S, Chiappelli F, Taylor A (2001) The glossopharyngeal nerve as a novel pathway in immune-to-brain communication: relevance to neuroimmune surveillance of the oral cavity. J Neuroimmunol 115: 91-100
152. Romeo H, Tio D, Taylor A (2003) Effects of glossopharyngeal nerve transection on central and peripheral cytokines and serum corticosterone induced by localized inflammation. J Neuroimmunol 136: 104-111
153. Fleming S et al (2001) Pro-and anti-inflammatory gene expression in the murine small intestine and liver after chronic exposure to alcohol. Alcohol Clin Exp Res 25: 579-589
154. Adinoff B, Iranmanesh A, Veldhuis J, Fisher L (1998) Disturbances of the stress response: the role of the HPA axis during alcohol withdrawal and abstinence. Alcohol Health Res World 22: 67-72
155. Koob GF (2003) Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27: 232-243
156. Linniola M, Mefford I, Nutt D, Adinoff B (1987) NIH conference: alcohol withdrawal and noradrenergic function. Ann Intern Med 107: 875-889
157. Benavides M, Laorden ML, Garcia-Borron JC, Milanes MV (2003) Regulation of tyrosine hydroxylase levels and activity and Fos expression during opioid withdrawal in the hypothalamic PVN and medulla oblongata catecholaminergic cell groups innervating the PVN. Eur J Neurosci 17: 103-112
158. Becker HC, Lopez MF, Doremus-Fitzwater TL (2011) Effects of stress on alcohol drinking: a review of animal studies. Psychopharmacology (Berl) 218: 131-156
159. Pohorecky LA (1981) The interaction of alcohol and stress. A review. Neurosci Biobehav Rev 5: 209-229
160. Pohorecky LA (1990) Interaction of ethanol and stress: research with experimental animals -an update. Alcohol Alcohol 25: 263-276
161. Pohorecky LA (1991) Stress and alcohol interaction: an update of human research. Alcohol Clin Exp Res 15: 438-459
162. Becker HC (2000) Animal models of alcohol withdrawal. Alcohol Res Health 24: 105-113
163. Doremus TL, Brunell SC, Varlinskaya EI, Spear LP (2003) Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats. Pharmacol Biochem Behav 75: 411-418
164. Doremus-Fitzwater TL, Spear LP (2007) Developmental differences in acute ethanol withdrawal in adolescent and adult rats. Alcohol Clin Exp Res 31: 1516-1527
165. Varlinskaya EI, Spear LP (2004) Acute ethanol withdrawal (hangover) and social behavior in adolescent and adult male and female Sprague-Dawley rats. Alcohol Clin Exp Res 28: 40-50
166. Overstreet DH, Knapp DJ, Breese GR (2002) Accentuated decrease in social interaction in rats subjected to repeated ethanol withdrawals. Alcohol Clin Exp Res 26: 1259-1268
167. Breese GR, Knapp DJ, Overstreet DH (2004) Stress sensitization of ethanol withdrawalinduced reduction in social interaction: inhibition by CRF-1 and benzodiazepine receptor antagonists and a 5-HT1A-receptor agonist. Neuropsychopharmacology 29: 470-482
168. Rylkova D, Shah HP, Small E, Bruijnzeel AW (2009) Deficit in brain reward function and acute and protracted anxiety-like behavior after discontinuation of a chronic alcohol liquid diet in rats. Psychopharmacology (Berl) 203: 629-640
169. Zhao Y, Weiss F, Zorrilla EP (2007) Remission and resurgence of anxiety-like behavior across protracted withdrawal stages in ethanol-dependent rats. Alcohol Clin Exp Res 31: 1505-1515
170. Buck HM, Hueston CM, Bishop C, Deak T (2011) 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 (Berl) 218: 203-215
171. Richey L, Doremus-Fitzwater TL, Bush HM, Deak T (2012) Acute illness-induced behavioral alterations are similar to those observed during withdrawal from acute alcohol exposure. Pharmacol Biochem Behav 103: 281-294