Induction of innate immune genes in brain create the neurobiology of addiction

Brain, Behavior, and Immunity

Volumn 25, Issue SUPPL. 1, 2011, Pages

  Crews, F T ^a   Zou, Jian ^a   Qin, Liya ^a  

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

Author keywords

Addiction; Alcoholism; Chemokines; Cytokines; Depression; Drug abuse; Frontal cortex; Microglia; Neurogenesis; Reversal learning

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; NALTREXONE; OXIDOREDUCTASE; PROTEINASE; TOLL LIKE RECEPTOR;

AFFECT; ALCOHOL ABSTINENCE; ALCOHOLISM; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ASTROCYTE; AUTOCRINE EFFECT; BEHAVIOR; CELL DAMAGE; COCAINE DEPENDENCE; DEPRESSION; DRUG ABUSE; DRUG DEPENDENCE; EMOTION; FRONTAL CORTEX; GENE EXPRESSION; GENE INDUCTION; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; INNATE IMMUNITY; LEARNING; MICROGLIA; MONOCYTE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; REVIEW; STRESS;

BEHAVIOR, ADDICTIVE; BRAIN; HUMANS; NEUROIMMUNOMODULATION; SUBSTANCE-RELATED DISORDERS;

EID: 79955729616     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2011.03.003     Document Type: Review

References (104)

1. 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. 2010, 30(24):8285-8295.
2. Armario A. Activation of the hypothalamic-pituitary-adrenal axis by addictive drugs: different pathways, common outcome. Trends Pharmacol. Sci. 2010, 31(7):318-325.
3. Bechara A., Dolan S., Hindes A. Decision-making and addiction (part II): myopia for the future or hypersensitivity to reward?. Neuropsychologia 2002, 40(10):1690-1705.
4. Blednov, Y., Benavidez, Jillian M., Perra, Simona, Morikawa, Hitoshi, Harris, Adron R., in press-a. Activation of neuroinflammatory Signaling by Lipopolysaccharide Produces a Prolonged increase of Voluntary Alcohol Intake in Mice. Brain Behav. Immun.
5. 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. 2005, 165(1):110-125.
6. Blednov, Y.A., Ponomarev, I., Geil, C., Bergeson, S., Koob, G.F., Harris, R.A., in press-b. Neuroimmune regulation of alcohol consumption: behavioral validation of genes obtained from genomic studiesl. Addict. Biol.
7. Breese G.R., Knapp D.J., Overstreet D.H., Navarro M., Wills T.A., Angel R.A. Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 2008, 33(4):867-876.
8. Breese G.R., Overstreet D.H., Knapp D.J. Conceptual framework for the etiology of alcoholism: a " kindling" /stress hypothesis. Psychopharmacology (Berl) 2005, 178(4):367-380.
9. 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 2007, 17(6):1342-1349.
10. Cao Q., Mak K.M., Lieber C.S. Cytochrome P4502E1 primes macrophages to increase TNF-alpha production in response to lipopolysaccharide. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289(1):G95-G107.
11. Christoffel D.J., Golden S.A., Dumitriu D., Robison A.J., Janssen W.G., Ahn H.F., Krishnan V., Reyes C.M., Han M.-H., Ables J.L., Eisch A.J., Dietz D.M., Ferguson D., Neve R.L., Greengard P., Kim Y., Morrison J.H., Russo a.S.J. IkB kinase regulates social defeat stress-induced synaptic and behavioral plasticity. J. Neurosci. 2011, 31(1):314-321.
12. Chvatal A., Anderova M., Hock M., Prajerova I., Neprasova H., Chvatal V., Kirchhoff F., Sykova E. Three-dimensional confocal morphometry reveals structural changes in astrocyte morphology in situ. J. Neurosci. Res. 2007, 85(2):260-271.
13. Coleman L., Jun H., Joohwi L., 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. 2010, 35(4).
14. Colton C.A., Wilcock D.M. Assessing activation states in microglia. CNS Neurol. Disord. Drug Targets 2010, 9(2):174-191.
15. Crews F., He J., Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol. Biochem. Behav. 2007, 86(2):189-199.
16. 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. 2006, 30(11):1938-1949.
17. Crews F.T., Bechara R., Brown L.A., Guidot D.M., Mandrekar P., Oak S., Qin L., Szabo G., Wheeler M., Zou J. Cytokines and alcohol. Alcohol. Clin. Exp. Res. 2006, 30(4):720-730.
18. Crews F.T., Braun C.J., Hoplight B., Switzer R.C., Knapp D.J. Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol. Clin. Exp. Res. 2000, 24(11):1712-1723.
19. Crews F.T., Mdzinarishvili A., Kim D., He J., Nixon K. Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 2006, 137(2):437-445.
20. Crews F.T., Nixon K. Alcohol, neural stem cells, and adult neurogenesis. Alcohol. Res. Health 2003, 27(2):197-204.
21. Crews F.T., Nixon K. Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol. 2009, 44(2):115-127.
22. Dranovsky A., Hen R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol. Psychiatry 2006, 59(12):1136-1143.
23. Eisenberger N.I., Berkman E.T., Inagaki T.K., Rameson L.T., Mashal N.M., Irwin M.R. Inflammation-induced anhedonia: endotoxin reduces ventral striatum responses to reward. Biol. Psychiatry 2010, 68(8):748-754.
24. Ernst M., Romeo R.D., Andersen S.L. Neurobiology of the development of motivated behaviors in adolescence: a window into a neural systems model. Pharmacol. Biochem. Behav. 2009, 93(3):199-211.
25. Flatscher-Bader T., van der Brug M., Hwang J.W., Gochee P.A., Matsumoto I., Niwa S., Wilce P.A. Alcohol-responsive genes in the frontal cortex and nucleus accumbens of human alcoholics. J. Neurochem. 2005, 93(2):359-370.
26. Frank G.M., Maier Steven F., Watkins Linda R. Stress- and glucocorticoid-induced priming of neuroinflammatory responses: potential mechanisms of stress-induced vulnerability to drugs of abuse. Brain Behav. Immun. 2011, 10.1016/j.bbi.2011.03.003.
27. Garg A.D., Nowis D., Golab J., Vandenabeele P., Krysko D.V., Agostinis P. Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim. Biophys. Acta 2010, 1805(1):53-71.
28. Ghosh S., Hayden M.S. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 2008, 8(11):837-848.
29. Gilson A.M. The concept of addiction in law and regulatory policy related to pain management: a critical review. Clin. J. Pain 2010, 26(1):70-77.
30. Gomez-Pinedo U., Felez M.C., Sancho-Bielsa F.J., Vidueira S., Cabanes C., Soriano M., Garcia-Verdugo J.M., Barcia J.A. Improved technique for stereotactic placement of nerve grafts between two locations inside the rat brain. J. Neurosci. Methods 2008, 174(2):194-201.
31. Graeber M.B. Changing face of microglia. Science 2010, 330(6005):783-788.
32. Greenfield S.F., Weiss R.D., Muenz L.R., Vagge L.M., Kelly J.F., Bello L.R., Michael J. The effect of depression on return to drinking: a prospective study. Arch. Gen. Psychiatry 1998, 55(3):259-265.
33. Greer J.M., Capecchi M.R. Hoxb8 is required for normal grooming behavior in mice. Neuron 2002, 33(1):23-34.
34. Gregus A., Wintink A.J., Davis A.C., Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav. Brain Res. 2005, 156(1):105-114.
35. Gruber A.J., Calhoun Gwendolyn G., Shusterman Igor, Schoenbaum Geoffrey, Roesch Matthew R., O'Donnell Patricio More is less: a disinhibited prefrontal cortex impairs cognitive flexibility. J. Neurosci. 2010, 30(50):17102-17110.
36. He J., Crews F.T. Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp. Neurol. 2008, 210(2):349-358.
37. Hingson, R.W., Zha, W., Weitzman, E. R., 2009. Magnitude of and trends in alcohol-related mortality and morbidity among U.S. college students ages 18-24, 1998-2005. J. Stud. Alcohol Drugs Suppl(16), 12-20.
38. Huang W., Tang Y., Li L. HMGB1, a potent proinflammatory cytokine in sepsis. Cytokine 2010, 51(2):119-126.
39. Hutchinson, M.R., Wu, Yue, Lousberg, Erin L., Moldenhauer, Lachlan M., Hayball, John, D., Robertson, Sarah A., Coller, Janet K., Watkings, Linda R., Somogyi, Andrew A., in press. Attenuation of microglial and IL-1 signaling protects mice from acute alcohol-induced sedation and/or motor impairment. Brain Behav. Immun.
40. Jentsch J.D., Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 1999, 146(4):373-390.
41. Johnson S.A., Fournier N.M., Kalynchuk L.E. Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav. Brain Res. 2006, 168(2):280-288.
42. Kalivas P.W., O'Brien C. Drug addiction as a pathology of staged neuroplasticity. Neuropsychopharmacology 2008, 33(1):166-180.
43. Kelley, K.W., Dantzer, Robert, in press. Alcoholism and inflammation: neuroimmunology of behavioral and mood disorders. Brain Behav. Immun.
44. 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. 1999, 23(4):633-643.
45. Koo J.W., Duman R.S. IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 2008, 105(2):751-756.
46. Koo J.W., Russo S.J., Ferguson D., Nestler E.J., Duman R.S. Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc. Natl. Acad. Sci. USA 2011, 107(6):2669-2674.
47. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35(1):217-238.
48. Li T.K. Quantifying the risk for alcohol-use and alcohol-attributable health disorders: present findings and future research needs. J. Gastroenterol. Hepatol. 2008, 23(Suppl. 1):S2-S8.
49. 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. 2000, 293(2):607-617.
50. Liu B., Jiang J.W., Wilson B.C., Du L., Yang S.N., Wang J.Y., Wu G.C., Cao X.D., Hong J.S. Systemic infusion of naloxone reduces degeneration of rat substantia nigral dopaminergic neurons induced by intranigral injection of lipopolysaccharide. J. Pharmacol. Exp. Ther. 2000, 295(1):125-132.
51. Liu J., Lewohl J.M., Harris R.A., Iyer V.R., Dodd P.R., Randall P.K., Mayfield R.D. Patterns of gene expression in the frontal cortex discriminate alcoholic from nonalcoholic individuals. Neuropsychopharmacology 2006, 31(7):1574-1582.
52. Liu L., Belkadi A., Darnall L., Hu T., Drescher C., Cotleur A.C., Padovani-Claudio D., He T., Choi K., Lane T.E., Miller R.H., Ransohoff R.M. CXCR2-positive neutrophils are essential for cuprizone-induced demyelination: relevance to multiple sclerosis. Nat. Neurosci. 2010, 13(3):319-326.
53. Loftis, J. M., Choi, D., Hoffman, W., Huckans, M. S., 2010. Methamphetamine causes persistent immune dysregulation: a cross-species, Translational Report. Neurotox. Res.
54. Madrigal B., Puebla P., Caballero E., Pelaez R., Gravalos D.G., Medarde M. Synthesis of imidazo[4,5-d]oxazolo[3,4-a]pyridines. New heterocyclic analogues of lignans. Arch. Pharm. (Weinheim) 2001, 334(5):177-179.
55. 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. 2003, 18(6):1701-1705.
56. 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. 2002, 938(1-2):87-91.
57. Malberg J.E., Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003, 28(9):1562-1571.
58. 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 2009, 6:16.
59. Maroso M., Balosso S., Ravizza T., Liu J., Aronica E., Iyer A.M., Rossetti C., Molteni M., Casalgrandi M., Manfredi A.A., Bianchi M.E., Vezzani A. Toll-like receptor 4 and high-mobility group box-1 are involved in ictogenesis and can be targeted to reduce seizures. Nat. Med. 2010, 16(4):413-419.
60. Massa P.T., Aleyasin H., Park D.S., Mao X., Barger S.W. NFkappaB in neurons? The uncertainty principle in neurobiology. J. Neurochem. 2006, 97(3):607-618.
61. Mendelson J.H., Babor T.F., Mello N.K., Pratt H. Alcoholism and prevalence of medical and psychiatric disorders. J. Stud. Alcohol. 1986, 47(5):361-366.
62. Miller N.S., Klamen D., Hoffmann N.G., Flaherty J.A. Prevalence of depression and alcohol and other drug dependence in addictions treatment populations. J. Psychoactive Drugs 1996, 28(2):111-124.
63. Mueller T.I., Lavori P.W., Keller M.B., Swartz A., Warshaw M., Hasin D., Coryell W., Endicott J., Rice J., Akiskal H. Prognostic effect of the variable course of alcoholism on the 10-year course of depression. Am. J. Psychiatry 1994, 151(5):701-706.
64. 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. USA 2006, 103(16):6368-6373.
65. Munhoz C.D., Sorrells S.F., Caso J.R., Scavone C., Sapolsky R.M. Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner. J. Neurosci. 2010, 30(41):13690-13698.
66. O'Brien C.P. Review. Evidence-based treatments of addiction. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2008, 363(1507):3277-3286.
67. 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. 2002, 72(3):521-532.
68. 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 2007, 2(9):e930.
69. Pahl H.L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 1999, 18(49):6853-6866.
70. 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. 2007, 25(2):541-550.
71. Pastor I.J., Laso F.J., Avila J.J., Rodriguez R.E., Gonzalez-Sarmiento R. Polymorphism in the interleukin-1 receptor antagonist gene is associated with alcoholism in Spanish men. Alcohol. Clin. Exp. Res. 2000, 24(10):1479-1482.
72. Pastor I.J., Laso F.J., Romero A., Gonzalez-Sarmiento R. Interleukin-1 gene cluster polymorphisms and alcoholism in Spanish men. Alcohol Alcohol. 2005, 40(3):181-186.
73. Powell E.E., Edwards-Smith C.J., Hay J.L., Clouston A.D., Crawford D.H., Shorthouse C., Purdie D.M., Jonsson J.R. Host genetic factors influence disease progression in chronic hepatitis C. Hepatology 2000, 31(4):828-833.
74. Qin L., Block M.L., Liu Y., Bienstock R.J., Pei Z., Zhang W., Wu X., Wilson B., Burka T., Hong J.S. Microglial NADPH oxidase is a novel target for femtomolar neuroprotection against oxidative stress. FASEB J. 2005, 19(6):550-557.
75. 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 2008, 5:10.
76. 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 2007, 55(5):453-462.
77. Raison C.L., Borisov A.S., Majer M., Drake D.F., Pagnoni G., Woolwine B.J., Vogt G.J., Massung B., Miller A.H. Activation of central nervous system inflammatory pathways by interferon-alpha: relationship to monoamines and depression. Biol. Psychiatry 2009, 65(4):296-303.
78. Ransohoff R.M., Cardona A.E. The myeloid cells of the central nervous system parenchyma. Nature 2010, 468(7321):253-262.
79. Reissner K.J., Kalivas P.W. Using glutamate homeostasis as a target for treating addictive disorders. Behav. Pharmacol. 2010, 21(5-6):514-522.
80. Ries, R.K., Miller, S.C., Fiellin, D.A., Saltz, R., 2009. Principles of addiction medicine. Am. Soc. Addict. Med.
81. Robinson T.E., Berridge K.C. Addiction. Annu. Rev. Psychol. 2003, 54:25-53.
82. Russo S.J., Mazei-Robison M.S., Ables J.L., Nestler E.J. Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 2009, 56(Suppl. 1):73-82.
83. Saiz P.A., Garcia-Portilla M.P., Florez G., Corcoran P., Arango C., Morales B., Leza J.C., Alvarez S., Diaz E.M., Alvarez V., Coto E., Nogueiras L., Bobes J. Polymorphisms of the IL-1 gene complex are associated with alcohol dependence in Spanish Caucasians: data from an association study. Alcohol. Clin. Exp. Res. 2009, 33(12):2147-2153.
84. 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 2003, 301(5634):805-809.
85. Schoenbaum G., Roesch M.R., Stalnaker T.A. Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci. 2006, 29(2):116-124.
86. 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. 2004, 19(7):1997-2002.
87. Schoenbaum G., Shaham Y. The role of orbitofrontal cortex in drug addiction: a review of preclinical studies. Biol. Psychiatry 2008, 63(3):256-262.
88. Schuckit M.A. An overview of genetic influences in alcoholism. J. Subst. Abuse Treat. 2009, 36(1):S5-S14.
89. Schuckit M.A., Tipp J.E., Bucholz K.K., Nurnberger J.I., Hesselbrock V.M., Crowe R.R., Kramer J. The life-time rates of three major mood disorders and four major anxiety disorders in alcoholics and controls. Addiction 1997, 92(10):1289-1304.
90. Shpargel K.B., Jalabi W., Jin Y., Dadabayev A., Penn M.S., Trapp B.D. Preconditioning paradigms and pathways in the brain. Cleve. Clin. J. Med. 2008, 75(Suppl. 2):S77-S82.
91. Stalnaker T.A., Takahashi Y., Roesch M.R., Schoenbaum G. Neural substrates of cognitive inflexibility after chronic cocaine exposure. Neuropharmacology 2009, 56(Suppl. 1):63-72.
92. 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. Neuropsychopharmacology 2009, 34(5):1209-1222.
93. Tanapat P., Hastings N.B., Rydel T.A., Galea L.A., Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 2001, 437(4):496-504.
94. Taylor M.W., Tsukahara T., McClintick J.N., Edenberg H.J., Kwo P. Cyclic changes in gene expression induced by Peg-interferon alfa-2b plus ribavirin in peripheral blood monocytes (PBMC) of hepatitis C patients during the first 10 weeks of treatment. J. Transl. Med. 2008, 6:66.
95. Videbech P., Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am. J. Psychiatry 2004, 161(11):1957-1966.
96. Volkow N.D., Baler R.D., Goldstein R.Z. Addiction: pulling at the neural threads of social behaviors. Neuron 2011, 69(4):599-602.
97. 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. 2009, 111(5):1119-1128.
98. 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. 1996, 389(2):119-122.
99. Webb A., Lind P.A., Kalmijn J., Feiler H.S., Smith T.L., Schuckit M.A., Wilhelmsen K. The investigation into CYP2E1 in relation to the level of response to alcohol through a combination of linkage and association analysis. Alcohol. Clin. Exp. Res. 2010, 35(1):10-18.
100. Wilhelmsson U., Bushong E.A., Price D.L., Smarr B.L., Phung V., Terada M., Ellisman M.H., Pekny M. Redefining the concept of reactive astrocytes as cells that remain within their unique domains upon reaction to injury. Proc. Natl. Acad. Sci. USA 2006, 103(46):17513-17518.
101. Yang L., Seifert A., Wu D., Wang X., Rankovic V., Schroder H., Brandenburg L.O., Hollt V., Koch T. Role of phospholipase D2/phosphatidic acid signal transduction in micro- and delta-opioid receptor endocytosis. Mol. Pharmacol. 2010, 78(1):105-113.
102. Zou J., Crews F. CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell. Mol. Neurobiol. 2006, 26(4-6):385-405.
103. 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. 2010, 34(5):777-789.
104. 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. 2005, 1034(1-2):11-24.