Alcohol and Stress Activation of Microglia and Neurons: Brain Regional Effects

Alcoholism: Clinical and Experimental Research

Volumn 41, Issue 12, 2017, Pages 2066-2081

  Walter, Thomas Jordan ^a   Vetreno, Ryan P ^a   Crews, Fulton T ^a  

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

Author keywords

Alcohol; Endotoxin; Microglia; Neurons; Stress

Indexed keywords

ALCOHOL; CD11B ANTIGEN; CORTICOSTERONE; ENDOTOXIN; PROTEIN C FOS;

ACUTE STRESS; ALCOHOL ABSTINENCE; ALCOHOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN REGION; CELL ACTIVATION; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FEMALE; IMMOBILIZATION STRESS; IMMUNOHISTOCHEMISTRY; INFRALIMBIC CORTEX; MALE; MICROGLIA; NERVE CELL; NONHUMAN; NUCLEUS ACCUMBENS CORE; NUCLEUS ACCUMBENS SHELL; PARAVENTRICULAR THALAMIC NUCLEUS; PREFRONTAL CORTEX; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; WATER IMMERSION; ANIMAL; BLOOD; BRAIN; CENTRAL NERVOUS SYSTEM SENSITIZATION; CYTOLOGY; DRUG EFFECT; MENTAL STRESS; METABOLISM;

ANIMALS; BRAIN; CD11B ANTIGEN; CENTRAL NERVOUS SYSTEM SENSITIZATION; CORTICOSTERONE; ENDOTOXINS; ETHANOL; MALE; MICROGLIA; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; STRESS, PSYCHOLOGICAL;

EID: 85034059009     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.13511     Document Type: Article

References (54)

1. Ahlers KE, Karacay B, Fuller L, Bonthius DJ, Dailey ME (2015) Transient activation of microglia following acute alcohol exposure in developing mouse neocortex is primarily driven by BAX-dependent neurodegeneration. Glia 63:1694–1713.
2. Ait-Belgnaoui A, Durand H, Cartier C, Chaumaz G, Eutamene H, Ferrier L, Houdeau E, Fioramonti J, Bueno L, Theodorou V (2012) Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37:1885–1895.
3. Beynon SB, Walker FR (2012) 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 225:162–171.
4. Blaine SK, Sinha R (2017) Alcohol, stress, and glucocorticoids: from risk to dependence and relapse in alcohol use disorders. Neuropharmacology 122:136–147.
5. Breese GR, Knapp DJ, Overstreet DH, Navarro M, Wills TA, Angel RA (2008) Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 33:867–876.
6. Crews FT, Lawrimore CJ, Walter TJ, Coleman LG (2017) The role of neuroimmune signaling in alcoholism. Neuropharmacology 122:56–73.
7. Crews FT, Nixon K, Wilkie ME (2004) Exercise reverses ethanol inhibition of neural stem cell proliferation. Alcohol 33:63–71.
8. Crews FT, Qin L, Sheedy D, Vetreno RP, Zou J (2013) High mobility group box 1/Toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biol Psychiatry 73:602–612.
9. Crews FT, Vetreno RP (2016) Mechanisms of neuroimmune gene induction in alcoholism. Psychopharmacology 233:1543–1557.
10. Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477–505.
11. Ellis FW (1966) Effect of ethanol on plasma corticosterone levels. J Pharmacol Exp Ther 153:121–127.
12. Ferrier L, Berard F, Debrauwer L, Chabo C, Langella P, Bueno L, Fioramonti J (2006) Impairment of the intestinal barrier by ethanol involves enteric microflora and mast cell activation in rodents. Am J Pathol 168:1148–1154.
13. 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.
14. Frank MG, Weber MD, Fonken LK, Hershman SA, Watkins LR, Maier SF (2016) The redox state of the alarmin HMGB1 is a pivotal factor in neuroinflammatory and microglial priming: a role for the NLRP3 inflammasome. Brain Behav Immun 55:215–224.
15. Frank MG, Weber MD, Watkins LR, Maier SF (2015) Stress sounds the alarmin: the role of the danger-associated molecular pattern HMGB1 in stress-induced neuroinflammatory priming. Brain Behav Immun 48:1–7.
16. He J, Crews FT (2008) Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 210:349–358.
17. Herman JP (2013) Neural control of chronic stress adaptation. Front Behav Neurosci 7:61.
18. Karlsson C, Schank JR, Rehman F, Stojakovic A, Björk K, Barbier E, Solomon M, Tapocik J, Engblom D, Thorsell A, Heilig M (2017) Proinflammatory signaling regulates voluntary alcohol intake and stress-induced consumption after exposure to social defeat stress in mice. Addict Biol 22:1279–1288.
19. Kato K, Murai I, Asai S, Matsuno Y, Komuro S, Kaneda N, Iwasaki A, Ishikawa K, Nakagawa S, Arakawa Y, Kuwayama H (1998) Protective role of melatonin and the pineal gland in modulating water immersion restraint stress ulcer in rats. J Clin Gastroenterol 27(Suppl 1):S110–S115.
20. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91:461–553.
21. Knapp DJ, Harper KM, Whitman BA, Zimomra Z, Breese GR (2016) Stress and withdrawal from chronic ethanol induce selective changes in neuroimmune mRNAs in differing brain sites. Brain Sci 6:1–19.
22. Koob GF (2013) Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr Top Behav Neurosci 13:3–30.
23. Koob GF, Ahmed SH, Boutrel B, Chen SA, Kenny PJ, Markou A, O'Dell LE, Parsons LH, Sanna PP (2004) Neurobiological mechanisms in the transition from drug use to drug dependence. Neurosci Biobehav Rev 27:739–749.
24. Lewitus GM, Konefal SC, Greenhalgh AD, Pribiag H, Augereau K, Stellwagen D (2016) Microglial TNF-alpha suppresses cocaine-induced plasticity and behavioral sensitization. Neuron 90:483–491.
25. Liu W, Crews FT (2015) Adolescent intermittent ethanol exposure enhances ethanol activation of the nucleus accumbens while blunting the prefrontal cortex responses in adult rat. Neuroscience 293:92–108.
26. Marshall SA, Casachahua JD, Rinker JA, Blose AK, Lysle DT, Thiele TE (2016) IL-1 receptor signaling in the basolateral amygdala modulates binge-like ethanol consumption in male C57BL/6J mice. Brain Behav Immun 51:258–267.
27. Marshall SA, McClain JA, Kelso ML, Hopkins DM, Pauly JR, Nixon K (2013) Microglial activation is not equivalent to neuroinflammation in alcohol-induced neurodegeneration: the importance of microglia phenotype. Neurobiol Dis 54:239–251.
28. Marshall SA, McKnight KH, Blose AK, Lysle DT, Thiele TE (2017) Modulation of binge-like ethanol consumption by IL-10 signaling in the basolateral amygdala. J Neuroimmune Pharmacol 12:249–259.
29. Mayfield J, Ferguson L, Harris RA (2013) Neuroimmune signaling: a key component of alcohol abuse. Curr Opin Neurobiol 23:513–520.
30. McClain JA, Morris SA, Deeny MA, Marshall SA, Hayes DM, Kiser ZM, Nixon K (2011) Adolescent binge alcohol exposure induces long-lasting partial activation of microglia. Brain Behav Immun 25(Suppl 1):S120–S128.
31. Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Chui DH, Tabira T (2000) Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 20:1568–1574.
32. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR 3rd, Lafaille JJ, Hempstead BL, Littman DR, Gan WB (2013) Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155:1596–1609.
33. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego, CA.
34. Perry VH, Holmes C (2014) Microglial priming in neurodegenerative disease. Nat Rev Neurol 10:217–224.
35. Qin L, Crews FT (2012) Chronic ethanol increases systemic TLR3 agonist-induced neuroinflammation and neurodegeneration. J Neuroinflammation 9:130.
36. Qin L, Wu X, Block M, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews F (2007) Systemic LPS causes chronic inflammation and progressive neurodegeneration. Glia 55:453–462.
37. Rao R (2009) Endotoxemia and gut barrier dysfunction in alcoholic liver disease. Hepatology 50:638–644.
38. Rivera CA, Bradford BU, Seabra V, Thurman RG (1998) Role of endotoxin in the hypermetabolic state after acute ethanol exposure. Am J Physiol 275:G1252–G1258.
39. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691–705.
40. Schepis TS, Rao U, Yadav H, Adinoff B (2011) The limbic-hypothalamic-pituitary-adrenal axis and the development of alcohol use disorders in youth. Alcohol Clin Exp Res 35:595–605.
41. Solovjov DA, Pluskota E, Plow EF (2005) Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. J Biol Chem 280:1336–1345.
42. Sorrells SF, Caso JR, Munhoz CD, Sapolsky RM (2009) The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 64:33–39.
43. Stephens MA, Wand G (2012) Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res 34:468–483.
44. Sugama S, Takenouchi T, Fujita M, Conti B, Hashimoto M (2009) Differential microglial activation between acute stress and lipopolysaccharide treatment. J Neuroimmunol 207:24–31.
45. de Timary P, Starkel P, Delzenne NM, Leclercq S (2017) A role for the peripheral immune system in the development of alcohol use disorders? Neuropharmacology 122:148–160.
46. Trudeau LE, Aragon CM, Amit Z (1990) Effects of ethanol on locomotor depression and corticosterone release induced by restraint-stress: support for a stress-ethanol interaction. Pharmacol Biochem Behav 36:273–278.
47. Vetreno RP, Crews FT (2012) Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and Toll-like receptors in the adult prefrontal cortex. Neuroscience 226:475–488.
48. Vetreno RP, Crews FT (2014) Current hypotheses on the mechanisms of alcoholism. Handb Clin Neurol 125:477–497.
49. Vetreno RP, Qin L, Crews FT (2013) Increased receptor for advanced glycation end product expression in the human alcoholic prefrontal cortex is linked to adolescent drinking. Neurobiol Dis 59:52–62.
50. Vilpoux C, Warnault V, Pierrefiche O, Daoust M, Naassila M (2009) Ethanol-sensitive brain regions in rat and mouse: a cartographic review, using immediate early gene expression. Alcohol Clin Exp Res 33:945–969.
51. Walter TJ, Crews FT (2017) Microglial depletion alters the brain neuroimmune response to acute binge ethanol withdrawal. J Neuroinflammation 14:86.
52. Watanabe Y, Stone E, McEwen BS (1994) Induction and habituation of c-fos and zif/268 by acute and repeated stressors. NeuroReport 5:1321–1324.
53. Weber MD, Frank MG, Tracey KJ, Watkins LR, Maier SF (2015) 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 35:316–324.
54. Whitman BA, Knapp DJ, Werner DF, Crews FT, Breese GR (2013) The cytokine mRNA increase induced by withdrawal from chronic ethanol in the sterile environment of brain is mediated by CRF and HMGB1 release. Alcohol Clin Exp Res 37:2086–2097.