The role of neuroimmune signaling in alcoholism

Neuropharmacology

Volumn 122, Issue , 2017, Pages 56-73

  Crews, Fulton T ^a   Lawrimore, Colleen J ^a   Walter, T Jordan ^a   Coleman, Leon G ^a  

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

Author keywords

Addiction; Alcohol; Cytokines; HMGB1; miRNA let 7; TLR

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; IBUDILAST; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MINOCYCLINE; PIOGLITAZONE; TOLL LIKE RECEPTOR;

ALCOHOLISM; ANXIETY; AUTOCRINE EFFECT; BEHAVIORAL ADDICTION; DRUG MECHANISM; GENE AMPLIFICATION; GENE EXPRESSION; HUMAN; IMPULSIVENESS; INFLAMMATION; INNATE IMMUNITY; MICROGLIA; MOOD DISORDER; NEUROIMMUNOLOGY; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STRESS; SUBSTANCE ABUSE; ADDICTION; ANIMAL; BRAIN; COMPLICATION; ENCEPHALITIS; IMMUNOLOGY; IMMUNOMODULATION; MENTAL STRESS; METABOLISM; NERVE CELL;

ALCOHOLISM; ANIMALS; BEHAVIOR, ADDICTIVE; BRAIN; ENCEPHALITIS; HMGB1 PROTEIN; HUMANS; MICROGLIA; NEUROIMMUNOMODULATION; NEURONS; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; TOLL-LIKE RECEPTORS;

EID: 85011850238     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2017.01.031     Document Type: Review

References (234)

1. Adachi, Y., Moore, L.E., Bradford, B.U., Gao, W., Thurman, R.G., Antibiotics prevent liver injury in rats following long-term exposure to ethanol. Gastroenterology 108 (1995), 218–224.
2. Agrawal, R.G., Hewetson, A., George, C.M., Syapin, P.J., Bergeson, S.E., Minocycline reduces ethanol drinking. Brain Behav. Immun. 25:Suppl. 1 (2011), S165–S169.
3. Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., Theodorou, V., Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37 (2012), 1885–1895.
4. 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. J. Neurosci. 30 (2010), 8285–8295.
5. 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. J. Neurosci. official J. Soc. Neurosci. 30 (2010), 8285–8295.
6. Aloe, L., Properzi, F., Probert, L., Akassoglou, K., Kassiotis, G., Micera, A., Fiore, M., Learning abilities, NGF and BDNF brain levels in two lines of TNF-alpha transgenic mice, one characterized by neurological disorders, the other phenotypically normal. Brain Res. 840 (1999), 125–137.
7. Ambros, V., The functions of animal microRNAs. Nature 431 (2004), 350–355.
8. Ang, E., Chen, J., Zagouras, P., Magna, H., Holland, J., Schaeffer, E., Nestler, E.J., Induction of nuclear factor-kappaB in nucleus accumbens by chronic cocaine administration. J. Neurochem. 79 (2001), 221–224.
9. Arancio, O., Zhang, H.P., Chen, X., Lin, C., Trinchese, F., Puzzo, D., Liu, S., Hegde, A., Yan, S.F., Stern, A., Luddy, J.S., Lue, L.F., Walker, D.G., Roher, A., Buttini, M., Mucke, L., Li, W., Schmidt, A.M., Kindy, M., Hyslop, P.A., Stern, D.M., Du Yan, S.S., RAGE potentiates Abeta-induced perturbation of neuronal function in transgenic mice. EMBO J. 23 (2004), 4096–4105.
10. Arezoomandan, R., Haghparast, A., Administration of the glial cell modulator, minocycline, in the nucleus accumbens attenuated the maintenance and reinstatement of morphine-seeking behavior. Can. J. Physiol. Pharmacol. 94 (2016), 257–264.
11. Attarzadeh-Yazdi, G., Arezoomandan, R., Haghparast, A., Minocycline, an antibiotic with inhibitory effect on microglial activation, attenuates the maintenance and reinstatement of methamphetamine-seeking behavior in rat. Prog. Neuropsychopharmacol. Biol. Psychiatry 53 (2014), 142–148.
12. Badanich, K.A., Becker, H.C., Woodward, J.J., Effects of chronic intermittent ethanol exposure on orbitofrontal and medial prefrontal cortex-dependent behaviors in mice. Behav. Neurosci. 125 (2011), 879–891.
13. Bai, L., Zhai, C., Han, K., Li, Z., Qian, J., Jing, Y., Zhang, W., Xu, J.T., Toll-like receptor 4-mediated nuclear factor-kappaB activation in spinal cord contributes to chronic morphine-induced analgesic tolerance and hyperalgesia in rats. Neurosci. Bull. 30 (2014), 936–948.
14. Bajo, M., Varodayan, F.P., Madamba, S.G., Robert, A.J., Casal, L.M., Oleata, C.S., Siggins, G.R., Roberto, M., IL-1 interacts with ethanol effects on GABAergic transmission in the mouse central amygdala. Front. Pharmacol., 6, 2015, 49.
15. Bala, S., Marcos, M., Gattu, A., Catalano, D., Szabo, G., Acute binge drinking increases serum endotoxin and bacterial DNA levels in healthy individuals. PLoS One, 9, 2014, e96864.
16. Bala, S., Marcos, M., Kodys, K., Csak, T., Catalano, D., Mandrekar, P., Szabo, G., Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor {alpha} (TNF{alpha}) production via increased mRNA half-life in alcoholic liver disease. J. Biol. Chem. 286 (2011), 1436–1444.
17. Banks, W.A., Kastin, A.J., Broadwell, R.D., Passage of cytokines across the blood-brain barrier. Neuroimmunomodulation 2 (1995), 241–248.
18. Banks, W.A., Kastin, A.J., Gutierrez, E.G., Penetration of interleukin-6 across the murine blood-brain barrier. Neurosci. Lett. 179 (1994), 53–56.
19. Bartel, D.P., MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2004), 281–297.
20. Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M., Beattie, M.S., Malenka, R.C., Control of synaptic strength by glial TNFalpha. Science 295 (2002), 2282–2285.
21. Bell, R.L., Lopez, M.F., Cui, C., Egli, M., Johnson, K.W., Franklin, K.M., Becker, H.C., Ibudilast reduces alcohol drinking in multiple animal models of alcohol dependence. Addict. Biol. 20 (2015), 38–42.
22. Beynon, S.B., Walker, F.R., Microglial activation in the injured and healthy brain: what are we really talking about? Practical and theoretical issues associated with the measurement of changes in microglial morphology. Neuroscience 225 (2012), 162–171.
23. Bhattacharya, A., Derecki, N.C., Lovenberg, T.W., Drevets, W.C., Role of neuro-immunological factors in the pathophysiology of mood disorders. Psychopharmacol. Berl. 233 (2016), 1623–1636.
24. Bhattacharya, A., Drevets, W.C., Role of neuro-immunological factors in the pathophysiology of mood disorders: implications for novel therapeutics for treatment resistant depression. Curr. Top. Behav. Neurosci. 31 (2017), 339–356.
25. Bi, W., Zhu, L., Wang, C., Liang, Y., Liu, J., Shi, Q., Tao, E., Rifampicin inhibits microglial inflammation and improves neuron survival against inflammation. Brain Res. 1395 (2011), 12–20.
26. Bianchi, M.E., HMGB1 loves company. J. Leukoc. Biol. 86 (2009), 573–576.
27. Bierhaus, A., Wolf, J., Andrassy, M., Rohleder, N., Humpert, P.M., Petrov, D., Ferstl, R., von Eynatten, M., Wendt, T., Rudofsky, G., Joswig, M., Morcos, M., Schwaninger, M., McEwen, B., Kirschbaum, C., Nawroth, P.P., A mechanism converting psychosocial stress into mononuclear cell activation. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 1920–1925.
28. Blanc, L., Castanier, R., Mishra, A.K., Ray, A., Besra, G.S., Sutcliffe, I., Vercellone, A., Nigou, J., Gram-positive bacterial lipoglycans based on a glycosylated diacylglycerol lipid anchor are microbe-associated molecular patterns recognized by TLR2. PLoS One, 8, 2013, e81593.
29. Blanco, A.M., Valles, 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 ethanol in cultured astrocytes. J. Immunol. 175 (2005), 6893–6899.
30. Blednov, Y.A., Benavidez, J.M., Black, M., Harris, R.A., Inhibition of phosphodiesterase 4 reduces ethanol intake and preference in C57BL/6J mice. Front. Neurosci., 8, 2014, 129.
31. Blednov, Y.A., Benavidez, J.M., Geil, C., Perra, S., Morikawa, H., Harris, R.A., Activation of inflammatory signaling by lipopolysaccharide produces a prolonged increase of voluntary alcohol intake in mice. Brain, Behav. Immun. 25:Suppl. 1 (2011), S92–S105.
32. 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 ethanol. Behav. Brain Res. 165 (2005), 110–125.
33. 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. Addict. Biol. 17 (2012), 108–120.
34. Bluthe, R.M., Walter, V., Parnet, P., Laye, S., Lestage, J., Verrier, D., Poole, S., Stenning, B.E., Kelley, K.W., Dantzer, R., Lipopolysaccharide induces sickness behaviour in rats by a vagal mediated mechanism. C R. Acad. Sci. III 317 (1994), 499–503.
35. Bonaccorso, S., Marino, V., Biondi, M., Grimaldi, F., Ippoliti, F., Maes, M., Depression induced by treatment with interferon-alpha in patients affected by hepatitis C virus. J. Affect. Disord. 72 (2002), 237–241.
36. Borner, C., Hollt, V., Kraus, J., Mechanisms of the inhibition of nuclear factor-kappaB by morphine in neuronal cells. Mol. Pharmacol. 81 (2012), 587–597.
37. 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. Neuropsychopharmacol. official Publ. Am. Coll. Neuropsychopharmacol. 33 (2008), 867–876.
38. Brubaker, S.W., Bonham, K.S., Zanoni, I., Kagan, J.C., Innate immune pattern recognition: a cell biological perspective. Annu. Rev. Immunol. 33 (2015), 257–290.
39. Bsibsi, M., Bajramovic, J.J., Vogt, M.H., van Duijvenvoorden, E., Baghat, A., Persoon-Deen, C., Tielen, F., Verbeek, R., Huitinga, I., Ryffel, B., Kros, A., Gerritsen, W.H., Amor, S., van Noort, J.M., The microtubule regulator stathmin is an endogenous protein agonist for TLR3. J. Immunol. 184 (2010), 6929–6937.
40. Buwitt-Beckmann, U., Heine, H., Wiesmuller, K.H., Jung, G., Brock, R., Akira, S., Ulmer, A.J., TLR1- and TLR6-independent recognition of bacterial lipopeptides. J. Biol. Chem. 281 (2006), 9049–9057.
41. Calu, D.J., Roesch, M.R., Stalnaker, T.A., Schoenbaum, G., Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb. cortex 17 (2007), 1342–1349.
42. Chen, G., Ke, Z., Xu, M., Liao, M., Wang, X., Qi, Y., Zhang, T., Frank, J.A., Bower, K.A., Shi, X., Luo, J., Autophagy is a protective response to ethanol neurotoxicity. Autophagy 8 (2012), 1577–1589.
43. Chen, Y., Li, G., Liu, Y., Werth, V.P., Williams, K.J., Liu, M.L., Translocation of endogenous danger signal HMGB1 from nucleus to membrane microvesicles in macrophages. J. Cell Physiol. 231 (2016), 2319–2326.
44. Cherry, J.D., Olschowka, J.A., O'Banion, M.K., Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J. neuroinflammation, 11, 2014, 98.
45. Coleman, L.G. Jr., He, J., Lee, J., Styner, M., Crews, F.T., Adolescent binge drinking alters adult brain neurotransmitter gene expression, behavior, brain regional volumes, and neurochemistry in mice. Alcohol. Clin. Exp. Res. 35 (2011), 671–688.
46. Coleman, L.G. Jr., Zou, J., Crews, F.T., Microglial-derived miRNA Let-7 and HMGB1 contribute to ethanol-induced neurotoxicity via TLR7. J. Neuroinflammation, 14, 2017, 22.
47. Costello, E.J., Copeland, W.E., Shanahan, L., Worthman, C.M., Angold, A., C-reactive protein and substance use disorders in adolescence and early adulthood: a prospective analysis. Drug Alcohol Depend. 133 (2013), 712–717.
48. Cozzoli, D.K., Kaufman, M.N., Nipper, M.A., Hashimoto, J.G., Wiren, K.M., Finn, D.A., Functional regulation of PI3K-associated signaling in the accumbens by binge alcohol drinking in male but not female mice. Neuropharmacology 105 (2016), 164–174.
49. Crews, F., Nixon, K., Kim, D., Joseph, J., Shukitt-Hale, B., Qin, L., Zou, J., BHT blocks NF-kappaB activation and ethanol-induced brain damage. Alcohol. Clin. Exp. Res. 30 (2006), 1938–1949.
50. Crews, F.T., Boettiger, C.A., Impulsivity, frontal lobes and risk for addiction. Pharmacol. Biochem. Behav. 93 (2009), 237–247.
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. Biol. Psychiatry 73 (2013), 602–612.
52. Crews, F.T., Vetreno, R.P., Neuroimmune basis of alcoholic brain damage. Int. Rev. Neurobiol. 118 (2014), 315–357.
53. Crews, F.T., Vetreno, R.P., Mechanisms of neuroimmune gene induction in alcoholism. Psychopharmacol. Berl. 233 (2016), 1543–1557.
54. Crews, F.T., Zou, J., Qin, L., Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav. Immun. 25:Suppl. 1 (2011), S4–S12.
55. Cui, C., Noronha, A., Warren, K.R., Koob, G.F., Sinha, R., Thakkar, M., Matochik, J., Crews, F.T., Chandler, L.J., Pfefferbaum, A., Becker, H.C., Lovinger, D., Everitt, B.J., Egli, M., Mandyam, C.D., Fein, G., Potenza, M.N., Harris, R.A., Grant, K.A., Roberto, M., Meyerhoff, D.J., Sullivan, E.V., Brain pathways to recovery from alcohol dependence. Alcohol 49 (2015), 435–452.
56. Czech, B., Hannon, G.J., Small RNA sorting: matchmaking for argonautes. Nat. Rev. Genet. 12 (2011), 19–31.
57. D'Mello, C., Le, T., Swain, M.G., Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation. J. Neurosci. official J. Soc. Neurosci. 29 (2009), 2089–2102.
58. Dantzer, R., O'Connor, J.C., Freund, G.G., Johnson, R.W., Kelley, K.W., From inflammation to sickness and depression: when the immune system subjugates the brain. Nature reviews. Neuroscience 9 (2008), 46–56.
59. Davis, R.L., Syapin, P.J., Ethanol increases nuclear factor-kappa B activity in human astroglial cells. Neurosci. Lett. 371 (2004), 128–132.
60. de Jesus, A.A., Canna, S.W., Liu, Y., Goldbach-Mansky, R., Molecular mechanisms in genetically defined autoinflammatory diseases: disorders of amplified danger signaling. Annu. Rev. Immunol. 33 (2015), 823–874.
61. Dennis, C.V., Sheahan, P.J., Graeber, M.B., Sheedy, D.L., Kril, J.J., Sutherland, G.T., Microglial proliferation in the brain of chronic alcoholics with hepatic encephalopathy. Metab. Brain Dis. 29 (2014), 1027–1039.
62. Drew, P.D., Johnson, J.W., Douglas, J.C., Phelan, K.D., Kane, C.J., Pioglitazone blocks ethanol induction of microglial activation and immune responses in the hippocampus, cerebellum, and cerebral cortex in a mouse model of fetal alcohol spectrum disorders. Alcohol Clin. Exp. Res. 39 (2015), 445–454.
63. Ek, M., Kurosawa, M., Lundeberg, T., Ericsson, A., Activation of vagal afferents after intravenous injection of interleukin-1beta: role of endogenous prostaglandins. J. Neurosci. official J. Soc. Neurosci. 18 (1998), 9471–9479.
64. Ellis, F.W., Effect of ethanol on plasma corticosterone levels. J. Pharmacol. Exp. Ther. 153 (1966), 121–127.
65. Fang, F., Lue, L.F., Yan, S., Xu, H., Luddy, J.S., Chen, D., Walker, D.G., Stern, D.M., Schmidt, A.M., Chen, J.X., Yan, S.S., RAGE-dependent signaling in microglia contributes to neuroinflammation, Abeta accumulation, and impaired learning/memory in a mouse model of Alzheimer's disease. FASEB J. official Publ. Fed. Am. Soc. Exp. Biol. 24 (2010), 1043–1055.
66. Farina, C., Aloisi, F., Meinl, E., Astrocytes are active players in cerebral innate immunity. Trends Immunol. 28 (2007), 138–145.
67. Fernandez-Lizarbe, S., Montesinos, J., Guerri, C., Ethanol induces TLR4/TLR2 association, triggering an inflammatory response in microglial cells. J. Neurochem. 126 (2013), 261–273.
68. Fernandez-Lizarbe, S., Pascual, M., Guerri, C., Critical role of TLR4 response in the activation of microglia induced by ethanol. J. Immunol. 183 (2009), 4733–4744.
69. Ferrier, L., Mazelin, L., Cenac, N., Desreumaux, P., Janin, A., Emilie, D., Colombel, J.F., Garcia-Villar, R., Fioramonti, J., Bueno, L., Stress-induced disruption of colonic epithelial barrier: role of interferon-gamma and myosin light chain kinase in mice. Gastroenterology 125 (2003), 795–804.
70. Fortier, C.B., Steffen, E.M., Lafleche, G., Venne, J.R., Disterhoft, J.F., McGlinchey, R.E., Delay discrimination and reversal eyeblink classical conditioning in abstinent chronic alcoholics. Neuropsychology 22 (2008), 196–208.
71. Frank, M.G., Baratta, M.V., Sprunger, D.B., Watkins, L.R., Maier, S.F., Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain, Behav. Immun. 21 (2007), 47–59.
72. Frank, M.G., Miguel, Z.D., Watkins, L.R., Maier, S.F., Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain, Behav. Immun. 24 (2010), 19–30.
73. Franke, H., Influence of chronic alcohol treatment on the GFAP-immunoreactivity in astrocytes of the hippocampus in rats. Acta histochem. 97 (1995), 263–271.
74. Freeman, K., Brureau, A., Vadigepalli, R., Staehle, M.M., Brureau, M.M., Gonye, G.E., Hoek, J.B., Hooper, D.C., Schwaber, J.S., Temporal changes in innate immune signals in a rat model of alcohol withdrawal in emotional and cardiorespiratory homeostatic nuclei. J. neuroinflammation, 9, 2012, 97.
75. Garate, I., Garcia-Bueno, B., Madrigal, J.L., Caso, J.R., Alou, L., Gomez-Lus, M.L., Mico, J.A., Leza, J.C., Stress-induced neuroinflammation: role of the Toll-like receptor-4 pathway. Biol. psychiatry 73 (2013), 32–43.
76. George, F.R., The role of arachidonic acid metabolites in mediating ethanol self-administration and intoxication. Ann. N. Y. Acad. Sci. 559 (1989), 382–391.
77. Giraldo, E., Multhoff, G., Ortega, E., Noradrenaline increases the expression and release of Hsp72 by human neutrophils. Brain, Behav. Immun. 24 (2010), 672–677.
78. Goshen, I., Kreisel, T., Ounallah-Saad, H., Renbaum, P., Zalzstein, Y., Ben-Hur, T., Levy-Lahad, E., Yirmiya, R., A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 32 (2007), 1106–1115.
79. Hanke, M.L., Kielian, T., Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin. Sci. 121 (2011), 367–387.
80. Harrison, N.A., Brydon, L., Walker, C., Gray, M.A., Steptoe, A., Critchley, H.D., Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biol. psychiatry 66 (2009), 407–414.
81. Harrison, N.A., Doeller, C.F., Voon, V., Burgess, N., Critchley, H.D., Peripheral inflammation acutely impairs human spatial memory via actions on medial temporal lobe glucose metabolism. Biol. psychiatry 76 (2014), 585–593.
82. He, J., Crews, F.T., Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp. Neurol. 210 (2008), 349–358.
83. Heberlein, A., Kaser, M., Lichtinghagen, R., Rhein, M., Lenz, B., Kornhuber, J., Bleich, S., Hillemacher, T., TNF-alpha and IL-6 serum levels: neurobiological markers of alcohol consumption in alcohol-dependent patients?. Alcohol 48 (2014), 671–676.
84. Hill, A.S., Sahay, A., Hen, R., Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors. Neuropsychopharmacol.: official Publ. Am. Coll. Neuropsychopharmacol. 40 (2015), 2368–2378.
85. Hori, O., Brett, J., Slattery, T., Cao, R., Zhang, J., Chen, J.X., Nagashima, M., Lundh, E.R., Vijay, S., Nitecki, D., et al. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J. Biol. Chem. 270 (1995), 25752–25761.
86. Hreggvidsdottir, H.S., Ostberg, T., Wahamaa, H., Schierbeck, H., Aveberger, A.C., Klevenvall, L., Palmblad, K., Ottosson, L., Andersson, U., Harris, H.E., The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J. Leukoc. Biol. 86 (2009), 655–662.
87. Hu, W., Lu, T., Chen, A., Huang, Y., Hansen, R., Chandler, L.J., Zhang, H.T., Inhibition of phosphodiesterase-4 decreases ethanol intake in mice. Psychopharmacol. Berl. 218 (2011), 331–339.
88. Hulsmans, M., Holvoet, P., MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc Res. 100 (2013), 7–18.
89. Hutchinson, M.R., Zhang, Y., Shridhar, M., Evans, J.H., Buchanan, M.M., Zhao, T.X., Slivka, P.F., Coats, B.D., Rezvani, N., Wieseler, J., Hughes, T.S., Landgraf, K.E., Chan, S., Fong, S., Phipps, S., Falke, J.J., Leinwand, L.A., Maier, S.F., Yin, H., Rice, K.C., Watkins, L.R., Evidence that opioids may have toll-like receptor 4 and MD-2 effects. Brain, Behav. Immun. 24 (2010), 83–95.
90. Izquierdo, A., Brigman, J.L., Radke, A.K., Rudebeck, P.H., Holmes, A., The neural basis of reversal learning: an updated perspective. Neuroscience, 2016, 10.1016/j.neuroscience.2016.03.021 [Epub ahead of print].
91. Jackson, A.C., Rossiter, J.P., Lafon, M., Expression of Toll-like receptor 3 in the human cerebellar cortex in rabies, herpes simplex encephalitis, and other neurological diseases. J. Neurovirol 12 (2006), 229–234.
92. Jang, E., Kim, J.H., Lee, S., Seo, J.W., Jin, M., Lee, M.G., Jang, I.S., Lee, W.H., Suk, K., Phenotypic polarization of activated astrocytes: the critical role of lipocalin-2 in the classical inflammatory activation of astrocytes. J. Immunol. 191 (2013), 5204–5219.
93. Janko, C., Filipovic, M., Munoz, L.E., Schorn, C., Schett, G., Ivanovic-Burmazovic, I., Herrmann, M., Redox modulation of HMGB1-related signaling. Antioxid. Redox Signal 20 (2014), 1075–1085.
94. Jensen, C.J., Massie, A., De Keyser, J., Immune players in the CNS: the astrocyte. J. neuroimmune Pharmacol. official J. Soc. NeuroImmune Pharmacol. 8 (2013), 824–839.
95. Jimenez, J.L., Punzon, C., Navarro, J., Munoz-Fernandez, M.A., Fresno, M., Phosphodiesterase 4 inhibitors prevent cytokine secretion by T lymphocytes by inhibiting nuclear factor-kappaB and nuclear factor of activated T cells activation. J. Pharmacol. Exp. Ther. 299 (2001), 753–759.
96. Jokisch, D., Roser, P., Juckel, G., Daum, I., Bellebaum, C., Impairments in learning by monetary rewards and alcohol-associated rewards in detoxified alcoholic patients. Alcohol Clin. Exp. Res. 38 (2014), 1947–1954.
97. June, H.L., Liu, J., Warnock, K.T., Bell, K.A., Balan, I., Bollino, D., Puche, A., Aurelian, L., CRF-amplified neuronal TLR4/MCP-1 signaling regulates alcohol self-administration. Neuropsychopharmacology 40 (2015), 1549–1559.
98. Kaltschmidt, B., Kaltschmidt, C., NF-KappaB in long-term memory and structural plasticity in the adult mammalian brain. Front. Mol. Neurosci., 8, 2015, 69.
99. Kane, C.J., Phelan, K.D., Han, L., Smith, R.R., Xie, J., Douglas, J.C., Drew, P.D., Protection of neurons and microglia against ethanol in a mouse model of fetal alcohol spectrum disorders by peroxisome proliferator-activated receptor-gamma agonists. Brain Behav. Immun. 25:Suppl. 1 (2011), S137–S145.
100. Keshavarzian, A., Farhadi, A., Forsyth, C.B., Rangan, J., Jakate, S., Shaikh, M., Banan, A., Fields, J.Z., Evidence that chronic alcohol exposure promotes intestinal oxidative stress, intestinal hyperpermeability and endotoxemia prior to development of alcoholic steatohepatitis in rats. J. Hepatol. 50 (2009), 538–547.
101. Kettenmann, H., Hanisch, U.K., Noda, M., Verkhratsky, A., Physiology of microglia. Physiol. Rev. 91 (2011), 461–553.
102. Kettenmann, H., Kirchhoff, F., Verkhratsky, A., Microglia: new roles for the synaptic stripper. Neuron 77 (2013), 10–18.
103. Khairova, R.A., Machado-Vieira, R., Du, J., Manji, H.K., A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder. Int. J. Neuropsychopharmacol./official Sci. J. Coll. Int. Neuropsychopharmacol. 12 (2009), 561–578.
104. Khakh, B.S., Sofroniew, M.V., Diversity of astrocyte functions and phenotypes in neural circuits. Nat. Neurosci. 18 (2015), 942–952.
105. Kim, C., Ho, D.H., Suk, J.E., You, S., Michael, S., Kang, J., Joong Lee, S., Masliah, E., Hwang, D., Lee, H.J., Lee, S.J., Neuron-released oligomeric alpha-synuclein is an endogenous agonist of TLR2 for paracrine activation of microglia. Nat. Commun., 4, 2013, 1562.
106. Knapp, D.J., Crews, F.T., Induction of cyclooxygenase-2 in brain during acute and chronic ethanol treatment and ethanol withdrawal. Alcohol. Clin. Exp. Res. 23 (1999), 633–643.
107. Koo, J.W., Duman, R.S., IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 751–756.
108. Koob, G.F., Le Moal, M., Plasticity of reward neurocircuitry and the ‘dark side’ of drug addiction. Nat. Neurosci. 8 (2005), 1442–1444.
109. Koob, G.F., Volkow, N.D., Neurocircuitry of addiction. Neuropsychopharmacol. official Publ. Am. Coll. Neuropsychopharmacol. 35 (2010), 217–238.
110. Kreisel, T., Frank, M.G., Licht, T., Reshef, R., Ben-Menachem-Zidon, O., Baratta, M.V., Maier, S.F., Yirmiya, R., Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis. Mol. Psychiatry 19 (2014), 699–709.
111. Lacagnina, M.J., Rivera, P.D., Bilbo, S.D., Glial and neuroimmune mechanisms as critical modulators of drug use and abuse. Neuropsychopharmacology 42 (2017), 156–177.
112. Lambert, K.G., Gerecke, K.M., Quadros, P.S., Doudera, E., Jasnow, A.M., Kinsley, C.H., Activity-stress increases density of GFAP-immunoreactive astrocytes in the rat hippocampus. Stress 3 (2000), 275–284.
113. Lawrimore, C. Crews, F., 2016. Neuron-like cell line SH-SY5Y displays different ethanol-induced immune signal molecule response and NFkB activation compared to microglia-like BV2. Research Society on Alcoholism Annual Meeting Poster Abstract.
114. Leclercq, S., De Saeger, C., Delzenne, N., de Timary, P., Starkel, P., Role of inflammatory pathways, blood mononuclear cells, and gut-derived bacterial products in alcohol dependence. Biol. Psychiatry 76 (2014), 725–733.
115. Lehmann, S.M., Kruger, C., Park, B., Derkow, K., Rosenberger, K., Baumgart, J., Trimbuch, T., Eom, G., Hinz, M., Kaul, D., Habbel, P., Kalin, R., Franzoni, E., Rybak, A., Nguyen, D., Veh, R., Ninnemann, O., Peters, O., Nitsch, R., Heppner, F.L., Golenbock, D., Schott, E., Ploegh, H.L., Wulczyn, F.G., Lehnardt, S., An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci. 15 (2012), 827–835.
116. Lehmann, S.M., Rosenberger, K., Kruger, C., Habbel, P., Derkow, K., Kaul, D., Rybak, A., Brandt, C., Schott, E., Wulczyn, F.G., Lehnardt, S., Extracellularly delivered single-stranded viral RNA causes neurodegeneration dependent on TLR7. J. Immunol. 189 (2012), 1448–1458.
117. Lewohl, J.M., Nunez, Y.O., Dodd, P.R., Tiwari, G.R., Harris, R.A., Mayfield, R.D., Up-regulation of microRNAs in brain of human alcoholics. Alcohol Clin. Exp. Res. 35 (2011), 1928–1937.
118. Lim, S.W., Shiue, Y.L., Liao, J.C., Wee, H.Y., Wang, C.C., Chio, C.C., Chang, C.H., Hu, C.Y., Kuo, J.R., Simvastatin therapy in the acute stage of traumatic brain injury attenuates brain trauma-induced depression-like behavior in rats by reducing neuroinflammation in the hippocampus. Neurocrit Care 26 (2017), 122–132.
119. Lippai, D., Bala, S., Csak, T., Kurt-Jones, E.A., Szabo, G., Chronic alcohol-induced microRNA-155 contributes to neuroinflammation in a TLR4-dependent manner in mice. PLoS One, 8, 2013, e70945.
120. Lippai, D., Bala, S., Petrasek, J., Csak, T., Levin, I., Kurt-Jones, E.A., Szabo, G., Alcohol-induced IL-1beta in the brain is mediated by NLRP3/ASC inflammasome activation that amplifies neuroinflammation. J. Leukoc. Biol. 94 (2013), 171–182.
121. Liu, A., Fang, H., Dirsch, O., Jin, H., Dahmen, U., Oxidation of HMGB1 causes attenuation of its pro-inflammatory activity and occurs during liver ischemia and reperfusion. PLoS One, 7, 2012, e35379.
122. Liu, B., Du, L., Hong, J.S., Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J. Pharmacol. Exp. Ther. 293 (2000), 607–617.
123. Liu, B., Du, L., Kong, L.Y., Hudson, P.M., Wilson, B.C., Chang, R.C., Abel, H.H., Hong, J.S., Reduction by naloxone of lipopolysaccharide-induced neurotoxicity in mouse cortical neuron-glia co-cultures. Neuroscience 97 (2000), 749–756.
124. Liu, J., Yang, A.R., Kelly, T., Puche, A., Esoga, C., June, H.L. Jr., Elnabawi, A., Merchenthaler, I., Sieghart, W., June, H.L. Sr., Aurelian, L., Binge alcohol drinking is associated with GABAA alpha2-regulated Toll-like receptor 4 (TLR4) expression in the central amygdala. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4465–4470.
125. Liu, W., Crews, F.T., Adolescent intermittent ethanol exposure enhances ethanol activation of the nucleus accumbens while blunting the prefrontal cortex responses in adult rat. Neuroscience 293 (2015), 92–108.
126. Maczurek, A., Shanmugam, K., Munch, G., Inflammation and the redox-sensitive AGE-RAGE pathway as a therapeutic target in Alzheimer's disease. Ann. N. Y. Acad. Sci. 1126 (2008), 147–151.
127. Madrigal, J.L., Garcia-Bueno, B., Moro, M.A., Lizasoain, I., Lorenzo, P., Leza, J.C., Relationship between cyclooxygenase-2 and nitric oxide synthase-2 in rat cortex after stress. Eur. J. Neurosci. 18 (2003), 1701–1705.
128. Madrigal, J.L., Moro, M.A., Lizasoain, I., Lorenzo, P., Leza, J.C., Stress-induced increase in extracellular sucrose space in rats is mediated by nitric oxide. Brain Res. 938 (2002), 87–91.
129. Maes, M., Berk, M., Goehler, L., Song, C., Anderson, G., Galecki, P., Leonard, B., Depression and sickness behavior are Janus-faced responses to shared inflammatory pathways. BMC Med., 10, 2012, 66.
130. Malberg, J.E., Eisch, A.J., Nestler, E.J., Duman, R.S., Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. official J. Soc. Neurosci. 20 (2000), 9104–9110.
131. Mao, X.R., Moerman-Herzog, A.M., Chen, Y., Barger, S.W., Unique aspects of transcriptional regulation in neurons–nuances in NFkappaB and Sp1-related factors. J. neuroinflammation, 6, 2009, 16.
132. Maroso, M., Balosso, S., Ravizza, T., Liu, J., Bianchi, M.E., Vezzani, A., Interleukin-1 type 1 receptor/Toll-like receptor signalling in epilepsy: the importance of IL-1beta and high-mobility group box 1. J. Intern Med. 270 (2011), 319–326.
133. Marshall, S.A., Casachahua, J.D., Rinker, J.A., Blose, A.K., Lysle, D.T., Thiele, T.E., IL-1 receptor signaling in the basolateral amygdala modulates binge-like ethanol consumption in male C57BL/6J mice. Brain Behav. Immun. 51 (2016), 258–267.
134. Marshall, S.A., Geil, C.R., Nixon, K., Prior binge ethanol exposure potentiates the microglial response in a model of alcohol-induced neurodegeneration. Brain Sci., 6, 2016.
135. Marshall, S.A., McClain, J.A., Kelso, M.L., Hopkins, D.M., Pauly, J.R., Nixon, K., Microglial activation is not equivalent to neuroinflammation in alcohol-induced neurodegeneration: the importance of microglia phenotype. Neurobiol. Dis. 54 (2013), 239–251.
136. Marshall, S.A., McKnight, K.H., Blose, A.K., Lysle, D.T., Thiele, T.E., Modulation of binge-like ethanol consumption by IL-10 signaling in the basolateral amygdala. J. Neuroimmune Pharmacol., 2016, 1–11.
137. Maslanik, T., Mahaffey, L., Tannura, K., Beninson, L., Greenwood, B.N., Fleshner, M., The inflammasome and danger associated molecular patterns (DAMPs) are implicated in cytokine and chemokine responses following stressor exposure. Brain, Behav. Immun. 28 (2013), 54–62.
138. Mayfield, J., Ferguson, L., Harris, R.A., Neuroimmune signaling: a key component of alcohol abuse. Curr. Opin. Neurobiol. 23 (2013), 513–520.
139. Merlot, E., Moze, E., Dantzer, R., Neveu, P.J., Suppression of restraint-induced plasma cytokines in mice pretreated with LPS. Stress 5 (2002), 131–135.
140. Miller, A.H., Raison, C.L., The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nat. Rev. Immunol. 16 (2016), 22–34.
141. Muller, S., Ronfani, L., Bianchi, M.E., Regulated expression and subcellular localization of HMGB1, a chromatin protein with a cytokine function. J. Intern Med. 255 (2004), 332–343.
142. Mulligan, M.K., Ponomarev, I., Hitzemann, R.J., Belknap, J.K., Tabakoff, B., Harris, R.A., Crabbe, J.C., Blednov, Y.A., Grahame, N.J., Phillips, T.J., Finn, D.A., Hoffman, P.L., Iyer, V.R., Koob, G.F., Bergeson, S.E., Toward understanding the genetics of alcohol drinking through transcriptome meta-analysis. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 6368–6373.
143. Northcutt, A.L., Hutchinson, M.R., Wang, X., Baratta, M.V., Hiranita, T., Cochran, T.A., Pomrenze, M.B., Galer, E.L., Kopajtic, T.A., Li, C.M., Amat, J., Larson, G., Cooper, D.C., Huang, Y., O'Neill, C.E., Yin, H., Zahniser, N.R., Katz, J.L., Rice, K.C., Maier, S.F., Bachtell, R.K., Watkins, L.R., DAT isn't all that: cocaine reward and reinforcement require Toll-like receptor 4 signaling. Mol. Psychiatry 20 (2015), 1525–1537.
144. Nunez, Y.O., Mayfield, R.D., Understanding alcoholism through microRNA signatures in brains of human alcoholics. Front. Genet., 3, 2012, 43.
145. Nunez, Y.O., Truitt, J.M., Gorini, G., Ponomareva, O.N., Blednov, Y.A., Harris, R.A., Mayfield, R.D., Positively correlated miRNA-mRNA regulatory networks in mouse frontal cortex during early stages of alcohol dependence. BMC Genomics, 14, 2013, 725.
146. O'Connor, J.C., Lawson, M.A., Andre, C., Moreau, M., Lestage, J., Castanon, N., Kelley, K.W., Dantzer, R., Lipopolysaccharide-induced depressive-like behavior is mediated by indoleamine 2,3-dioxygenase activation in mice. Mol. Psychiatry 14 (2009), 511–522.
147. Obernier, J.A., White, A.M., Swartzwelder, H.S., Crews, F.T., Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats. Pharmacol. Biochem. Behav. 72 (2002), 521–532.
148. Ohshima, K., Inoue, K., Fujiwara, A., Hatakeyama, K., Kanto, K., Watanabe, Y., Muramatsu, K., Fukuda, Y., Ogura, S., Yamaguchi, K., Mochizuki, T., Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One, 5, 2010, e13247.
149. Okuma, Y., Liu, K., Wake, H., Liu, R., Nishimura, Y., Hui, Z., Teshigawara, K., Haruma, J., Yamamoto, Y., Yamamoto, H., Date, I., Takahashi, H.K., Mori, S., Nishibori, M., Glycyrrhizin inhibits traumatic brain injury by reducing HMGB1-RAGE interaction. Neuropharmacology 85 (2014), 18–26.
150. Okun, E., Griffioen, K., Barak, B., Roberts, N.J., Castro, K., Pita, M.A., Cheng, A., Mughal, M.R., Wan, R., Ashery, U., Mattson, M.P., Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 15625–15630.
151. Okvist, A., Johansson, S., Kuzmin, A., Bazov, I., Merino-Martinez, R., Ponomarev, I., Mayfield, R.D., Harris, R.A., Sheedy, D., Garrick, T., Harper, C., Hurd, Y.L., Terenius, L., Ekstrom, T.J., Bakalkin, G., Yakovleva, T., Neuroadaptations in human chronic alcoholics: dysregulation of the NF-kappaB system. PLoS One, 2, 2007, e930.
152. Overman, E.L., Rivier, J.E., Moeser, A.J., CRF induces intestinal epithelial barrier injury via the release of mast cell proteases and TNF-alpha. PLoS One, 7, 2012, e39935.
153. Pahl, H.L., Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18 (1999), 6853–6866.
154. Park, A., Ghezzi, A., Thilini, P., Wijesekera, Atkinson, N., Genetics and genomics of alcohol responses in drosophila. Neuropharmacology, 2017.
155. Park, C.K., Xu, Z.Z., Berta, T., Han, Q., Chen, G., Liu, X.J., Ji, R.R., Extracellular microRNAs activate nociceptor neurons to elicit pain via TLR7 and TRPA1. Neuron 82 (2014), 47–54.
156. Pascual, M., Balino, P., Alfonso-Loeches, S., Aragon, C.M., Guerri, C., Impact of TLR4 on behavioral and cognitive dysfunctions associated with alcohol-induced neuroinflammatory damage. Brain, Behav. Immun. 25:Suppl. 1 (2011), S80–S91.
157. Pascual, M., Blanco, A.M., Cauli, O., Minarro, J., Guerri, C., Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur. J. Neurosci. 25 (2007), 541–550.
158. Pekny, M., Pekna, M., Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol. Rev. 94 (2014), 1077–1098.
159. Perry, V.H., Holmes, C., Microglial priming in neurodegenerative disease. Nature reviews. Neurology 10 (2014), 217–224.
160. Pietri, M., Schneider, B., Mouillet-Richard, S., Ermonval, M., Mutel, V., Launay, J.M., Kellermann, O., Reactive oxygen species-dependent TNF-alpha converting enzyme activation through stimulation of 5-HT2B and alpha1D autoreceptors in neuronal cells. FASEB J. 19 (2005), 1078–1087.
161. Pla, A., Pascual, M., Guerri, C., Autophagy constitutes a protective mechanism against ethanol toxicity in mouse astrocytes and neurons. PLoS One, 11, 2016, e0153097.
162. Plane, J.M., Shen, Y., Pleasure, D.E., Deng, W., Prospects for minocycline neuroprotection. Archives neurol. 67 (2010), 1442–1448.
163. Qiang, M., Ticku, M.K., Role of AP-1 in ethanol-induced N-methyl-D-aspartate receptor 2B subunit gene up-regulation in mouse cortical neurons. J. Neurochem. 95 (2005), 1332–1341.
164. Qin, L., Crews, F.T., Chronic ethanol increases systemic TLR3 agonist-induced neuroinflammation and neurodegeneration. J. Neuroinflammation, 9, 2012, 130.
165. Qin, L., Crews, F.T., NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration. J. Neuroinflammation, 9, 2012, 5.
166. 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. J. Neuroinflammation, 5, 2008, 10.
167. Qin, L., Liu, Y., Hong, J.S., Crews, F.T., NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration. Glia 61 (2013), 855–868.
168. Qin, L., Wu, X., Block, M.L., Liu, Y., Breese, G.R., Hong, J.S., Knapp, D.J., Crews, F.T., Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55 (2007), 453–462.
169. Rajkowska, G., Stockmeier, C.A., Astrocyte pathology in major depressive disorder: insights from human postmortem brain tissue. Curr. drug targets 14 (2013), 1225–1236.
170. Reissner, K.J., Kalivas, P.W., Using glutamate homeostasis as a target for treating addictive disorders. Behav. Pharmacol. 21 (2010), 514–522.
171. Rocha, N.P., de Miranda, A.S., Teixeira, A.L., Insights into neuroinflammation in Parkinson's disease: from biomarkers to anti-inflammatory based therapies. Biomed. Res. Int., 2015, 2015, 628192.
172. Rubio-Araiz, A., Porcu, F., Perez-Hernandez, M., Garcia-Gutierrez, M.S., Aracil-Fernandez, M.A., Gutierrez-Lopez, M.D., Guerri, C., Manzanares, J., O'Shea, E., Colado, M.I., Disruption of blood-brain barrier integrity in postmortem alcoholic brain: preclinical evidence of TLR4 involvement from a binge-like drinking model. Addict. Biol., 2016, 10.1111/adb.12376 [Epub ahead of print], n/a–n/a.
173. Russo, S.J., Wilkinson, M.B., Mazei-Robison, M.S., Dietz, D.M., Maze, I., Krishnan, V., Renthal, W., Graham, A., Birnbaum, S.G., Green, T.A., Robison, B., Lesselyong, A., Perrotti, L.I., Bolanos, C.A., Kumar, A., Clark, M.S., Neumaier, J.F., Neve, R.L., Bhakar, A.L., Barker, P.A., Nestler, E.J., Nuclear factor kappa B signaling regulates neuronal morphology and cocaine reward. J. Neurosci. 29 (2009), 3529–3537.
174. Ryan, S.M., Nolan, Y.M., Neuroinflammation negatively affects adult hippocampal neurogenesis and cognition: can exercise compensate?. Neurosci. Biobehav. Rev. 61 (2016), 121–131.
175. Saha, B., Momen-Heravi, F., Kodys, K., Szabo, G., MicroRNA cargo of extracellular vesicles from alcohol-exposed monocytes signals naive monocytes to differentiate into M2 macrophages. J. Biol. Chem. 291 (2016), 149–159.
176. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., Hen, R., Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003), 805–809.
177. Saunders, P.R., Santos, J., Hanssen, N.P., Yates, D., Groot, J.A., Perdue, M.H., Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig. Dis. Sci. 47 (2002), 208–215.
178. Schoenbaum, G., Roesch, M.R., Stalnaker, T.A., Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci. 29 (2006), 116–124.
179. Schoenbaum, G., Saddoris, M.P., Ramus, S.J., Shaham, Y., Setlow, B., Cocaine-experienced rats exhibit learning deficits in a task sensitive to orbitofrontal cortex lesions. Eur. J. Neurosci. 19 (2004), 1997–2002.
180. Setiawan, E., Wilson, A.A., Mizrahi, R., Rusjan, P.M., Miler, L., Rajkowska, G., Suridjan, I., Kennedy, J.L., Rekkas, P.V., Houle, S., Meyer, J.H., Role of translocator protein density, a marker of neuroinflammation, in the brain during major depressive episodes. JAMA psychiatry 72 (2015), 268–275.
181. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., Gould, E., Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001), 372–376.
182. Sironi, L., Banfi, C., Brioschi, M., Gelosa, P., Guerrini, U., Nobili, E., Gianella, A., Paoletti, R., Tremoli, E., Cimino, M., Activation of NF-kB and ERK1/2 after permanent focal ischemia is abolished by simvastatin treatment. Neurobiol. Dis. 22 (2006), 445–451.
183. Sorrells, S.F., Caso, J.R., Munhoz, C.D., Sapolsky, R.M., The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64 (2009), 33–39.
184. Stalnaker, T.A., Takahashi, Y., Roesch, M.R., Schoenbaum, G., Neural substrates of cognitive inflexibility after chronic cocaine exposure. Neuropharmacology 56:Suppl. 1 (2009), 63–72.
185. Steptoe, A., Hamer, M., Chida, Y., The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain, Behav. Immun. 21 (2007), 901–912.
186. Stevenson, J.R., Schroeder, J.P., Nixon, K., Besheer, J., Crews, F.T., Hodge, C.W., Abstinence following alcohol drinking produces depression-like behavior and reduced hippocampal neurogenesis in mice. Neuropsychopharmacol. official Publ. Am. Coll. Neuropsychopharmacol. 34 (2009), 1209–1222.
187. Storer, P.D., Xu, J., Chavis, J., Drew, P.D., Peroxisome proliferator-activated receptor-gamma agonists inhibit the activation of microglia and astrocytes: implications for multiple sclerosis. J. Neuroimmunol. 161 (2005), 113–122.
188. Stott, K., Watson, M., Howe, F.S., Grossmann, J.G., Thomas, J.O., Tail-mediated collapse of HMGB1 is dynamic and occurs via differential binding of the acidic tail to the A and B domains. J. Mol. Biol. 403 (2010), 706–722.
189. Szabo, G., Bala, S., Petrasek, J., Gattu, A., Gut-liver axis and sensing microbes. Dig. Dis. 28 (2010), 737–744.
190. Szabo, G., Lippai, D., Converging actions of alcohol on liver and brain immune signaling. Int. Rev. Neurobiol. 118 (2014), 359–380.
191. Takeuchi, O., Akira, S., Pattern recognition receptors and inflammation. Cell 140 (2010), 805–820.
192. Tancredi, V., D'Arcangelo, G., Grassi, F., Tarroni, P., Palmieri, G., Santoni, A., Eusebi, F., Tumor necrosis factor alters synaptic transmission in rat hippocampal slices. Neurosci. Lett. 146 (1992), 176–178.
193. Teitelbaum, A.A., Gareau, M.G., Jury, J., Yang, P.C., Perdue, M.H., Chronic peripheral administration of corticotropin-releasing factor causes colonic barrier dysfunction similar to psychological stress. Am. J. Physiol. Gastrointest. Liver Physiol. 295 (2008), G452–G459.
194. Thakur, V., McMullen, M.R., Pritchard, M.T., Nagy, L.E., Regulation of macrophage activation in alcoholic liver disease. J. gastroenterol. hepatol. 22:Suppl. 1 (2007), S53–S56.
195. Thomas, J.O., Stott, K., H1 and HMGB1: modulators of chromatin structure. Biochem. Soc. Trans. 40 (2012), 341–346.
196. Thounaojam, M.C., Kaushik, D.K., Basu, A., MicroRNAs in the brain: it's regulatory role in neuroinflammation. Mol. Neurobiol. 47 (2013), 1034–1044.
197. Torres-Platas, S.G., Cruceanu, C., Chen, G.G., Turecki, G., Mechawar, N., Evidence for increased microglial priming and macrophage recruitment in the dorsal anterior cingulate white matter of depressed suicides. Brain, Behav. Immun. 42 (2014), 50–59.
198. Townshend, J.M., Duka, T., Mixed emotions: alcoholics' impairments in the recognition of specific emotional facial expressions. Neuropsychologia 41 (2003), 773–782.
199. Turchinovich, A., Samatov, T.R., Tonevitsky, A.G., Burwinkel, B., Circulating miRNAs: cell-cell communication function?. Front. Genet., 4, 2013, 119.
200. Tynan, R.J., Naicker, S., Hinwood, M., Nalivaiko, E., Buller, K.M., Pow, D.V., Day, T.A., Walker, F.R., Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain, Behav. Immun. 24 (2010), 1058–1068.
201. Vabulas, R.M., Braedel, S., Hilf, N., Singh-Jasuja, H., Herter, S., Ahmad-Nejad, P., Kirschning, C.J., Da Costa, C., Rammensee, H.G., Wagner, H., Schild, H., The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J. Biol. Chem. 277 (2002), 20847–20853.
202. Valenta, J.P., Gonzales, R.A., Chronic intracerebroventricular infusion of monocyte chemoattractant Protein-1 leads to a persistent increase in sweetened ethanol consumption during operant self-administration but does not influence sucrose consumption in long-evans rats. Alcohol. Clin. Exp. Res. 40 (2016), 187–195.
203. Valles, S.L., Blanco, A.M., Pascual, M., Guerri, C., Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes. Brain pathol. 14 (2004), 365–371.
204. Venereau, E., Casalgrandi, M., Schiraldi, M., Antoine, D.J., Cattaneo, A., De Marchis, F., Liu, J., Antonelli, A., Preti, A., Raeli, L., Shams, S.S., Yang, H., Varani, L., Andersson, U., Tracey, K.J., Bachi, A., Uguccioni, M., Bianchi, M.E., Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 209 (2012), 1519–1528.
205. Vetreno, R.P., Crews, F.T., Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and Toll-like receptors in the adult prefrontal cortex. Neuroscience 226 (2012), 475–488.
206. Vetreno, R.P., Crews, F.T., Current hypotheses on the mechanisms of alcoholism. Handb. Clin. Neurol. 125 (2014), 477–497.
207. Vetreno, R.P., Qin, L., Crews, F.T., Increased receptor for advanced glycation end product expression in the human alcoholic prefrontal cortex is linked to adolescent drinking. Neurobiol. Dis. 59 (2013), 52–62.
208. Volkow, N.D., Koob, G.F., McLellan, A.T., Neurobiologic advances from the brain disease model of addiction. N. Engl. J. Med. 374 (2016), 363–371.
209. von Bernhardi, R., Eugenin-von Bernhardi, L., Eugenin, J., Microglial cell dysregulation in brain aging and neurodegeneration. Front. Aging Neurosci., 7, 2015, 124.
210. Wagley, Y., Hwang, C.K., Lin, H.Y., Kam, A.F., Law, P.Y., Loh, H.H., Wei, L.N., Inhibition of c-Jun NH2-terminal kinase stimulates mu opioid receptor expression via p38 MAPK-mediated nuclear NF-kappaB activation in neuronal and non-neuronal cells. Biochim. Biophys. Acta 1833 (2013), 1476–1488.
211. Wang, W.Y., Tan, M.S., Yu, J.T., Tan, L., Role of pro-inflammatory cytokines released from microglia in Alzheimer's disease. Ann. Transl. Med., 3, 2015, 136.
212. Wang, X., Grace, P.M., Pham, M.N., Cheng, K., Strand, K.A., Smith, C., Li, J., Watkins, L.R., Yin, H., Rifampin inhibits Toll-like receptor 4 signaling by targeting myeloid differentiation protein 2 and attenuates neuropathic pain. FASEB J. 27 (2013), 2713–2722.
213. Wang, X., Zhang, Y., Peng, Y., Hutchinson, M.R., Rice, K.C., Yin, H., Watkins, L.R., Pharmacological characterization of the opioid inactive isomers (+)-naltrexone and (+)-naloxone as antagonists of toll-like receptor 4. Br. J. Pharmacol. 173 (2016), 856–869.
214. Ward, R.J., Colivicchi, M.A., Allen, R., Schol, F., Lallemand, F., de Witte, P., Ballini, C., Corte, L.D., Dexter, D., Neuro-inflammation induced in the hippocampus of ‘binge drinking’ rats may be mediated by elevated extracellular glutamate content. J. Neurochem. 111 (2009), 1119–1128.
215. Ward, R.J., Zhang, Y., Crichton, R.R., Piret, B., Piette, J., de Witte, P., Identification of the nuclear transcription factor NFkappaB in rat after in vivo ethanol administration. FEBS Lett. 389 (1996), 119–122.
216. Warden, A., Mayfield, R.D., Gene expression profiling in the human alcoholic brain. Neuropharmacology, 2017.
217. Weber, M.D., Frank, M.G., Tracey, K.J., Watkins, L.R., Maier, S.F., Stress induces the danger-associated molecular pattern HMGB-1 in the hippocampus of male Sprague Dawley rats: a priming stimulus of microglia and the NLRP3 inflammasome. J. Neurosci. official J. Soc. Neurosci. 35 (2015), 316–324.
218. Weissenborn, R., Duka, T., Acute alcohol effects on cognitive function in social drinkers: their relationship to drinking habits. Psychopharmacology 165 (2003), 306–312.
219. Wilson, J.S., Mruthinti, S., Buccafusco, J.J., Schade, R.F., Mitchell, M.B., Harrell, D.U., Gulati, N.K., Miller, L.S., Anti-RAGE and Abeta immunoglobulin levels are related to dementia level and cognitive performance. J. gerontol. Ser. A, Biol. Sci. Med. Sci. 64 (2009), 264–271.
220. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., Stiner, L.M., Bailey, M.T., Nelson, R.J., Godbout, J.P., Sheridan, J.F., beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. official J. Soc. Neurosci. 31 (2011), 6277–6288.
221. Wohleb, E.S., Powell, N.D., Godbout, J.P., Sheridan, J.F., Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J. Neurosci. official J. Soc. Neurosci. 33 (2013), 13820–13833.
222. Worley, M.J., Heinzerling, K.G., Roche, D.J., Shoptaw, S., Ibudilast attenuates subjective effects of methamphetamine in a placebo-controlled inpatient study. Drug Alcohol Depend. 162 (2016), 245–250.
223. Xue, J., Schmidt, S.V., Sander, J., Draffehn, A., Krebs, W., Quester, I., De Nardo, D., Gohel, T.D., Emde, M., Schmidleithner, L., Ganesan, H., Nino-Castro, A., Mallmann, M.R., Labzin, L., Theis, H., Kraut, M., Beyer, M., Latz, E., Freeman, T.C., Ulas, T., Schultze, J.L., Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40 (2014), 274–288.
224. Yanai, H., Ban, T., Wang, Z., Choi, M.K., Kawamura, T., Negishi, H., Nakasato, M., Lu, Y., Hangai, S., Koshiba, R., Savitsky, D., Ronfani, L., Akira, S., Bianchi, M.E., Honda, K., Tamura, T., Kodama, T., Taniguchi, T., HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462 (2009), 99–103.
225. Yang, H., Lundback, P., Ottosson, L., Erlandsson-Harris, H., Venereau, E., Bianchi, M.E., Al-Abed, Y., Andersson, U., Tracey, K.J., Antoine, D.J., Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol. Med. 18 (2012), 250–259.
226. Yelamanchili, S.V., Lamberty, B.G., Rennard, D.A., Morsey, B.M., Hochfelder, C.G., Meays, B.M., Levy, E., Fox, H.S., MiR-21 in extracellular vesicles leads to neurotoxicity via TLR7 signaling in SIV neurological disease. PLoS Pathog., 11, 2015, e1005032.
227. Yirmiya, R., Goshen, I., Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain, Behav. Immun. 25 (2011), 181–213.
228. Young, J.J., Bruno, D., Pomara, N., A review of the relationship between proinflammatory cytokines and major depressive disorder. J. Affect Disord. 169 (2014), 15–20.
229. Zhang, B., Bailey, W.M., Kopper, T.J., Orr, M.B., Feola, D.J., Gensel, J.C., Azithromycin drives alternative macrophage activation and improves recovery and tissue sparing in contusion spinal cord injury. J. Neuroinflammation, 12, 2015, 218.
230. Zhu, C.B., Lindler, K.M., Owens, A.W., Daws, L.C., Blakely, R.D., Hewlett, W.A., Interleukin-1 receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters. Neuropsychopharmacol. official Publ. Am. Coll. Neuropsychopharmacol. 35 (2010), 2510–2520.
231. Zou, J., Crews, F., CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell. Mol. Neurobiol. 26 (2006), 385–405.
232. Zou, J., Crews, F., Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-kappaB and proinflammatory cytokines. Alcohol. Clin. Exp. Res. 34 (2010), 777–789.
233. Zou, J.Y., Crews, F.T., TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: neuroprotection by NF kappa B inhibition. Brain Res. 1034 (2005), 11–24.
234. Zou, J.Y., Crews, F.T., Release of neuronal HMGB1 by ethanol through decreased HDAC activity activates brain neuroimmune signaling. PLoS One, 9, 2014, e87915.