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

Crews, F.T.; Zou, Jian; Qin, Liya

doi:10.1016/j.bbi.2011.03.003

Cited by 313Neuroinflammation and Neurodegeneration MechanismsTryptophan and brain disordersNeurotransmitter Receptor Influence on Behavior

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

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Crews, F.T., Zou, Jian, Qin, Liya·2011·Brain, Behavior, and Immunity

DOI 10.1016/j.bbi.2011.03.003PMC PMC3552373

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Abstract

Addiction occurs through repeated abuse of drugs that progressively reduce behavioral control and cognitive flexibility while increasing limbic negative emotion. Recent discoveries indicate neuroimmune signaling underlies addiction and co-morbid depression. Low threshold microglia undergo progressive stages of innate immune activation involving astrocytes and neurons with repeated drug abuse, stress, and/or cell damage signals. Increased brain NF-κB transcription of proinflammatory chemokines, cytokines, oxidases, proteases, TLR and other genes create loops amplifying NF-κB transcription and innate immune target gene expression. Human post-mortem alcoholic brain has increased NF-κB and NF-κB target gene message, increased microglial markers and chemokine-MCP1. Polymorphisms of human NF-κB1 and other innate immune genes contribute to genetic risk for alcoholism. Animal transgenic and genetic studies link NF-κB innate immune gene expression to alcohol drinking. Human drug addicts show deficits in behavioral flexibility modeled pre-clinically using reversal learning. Binge alcohol, chronic cocaine, and lesions link addiction neurobiology to frontal cortex, neuroimmune signaling and loss of behavioral flexibility. Addiction also involves increasing limbic negative emotion and depression-like behavior that is reflected in hippocampal neurogenesis. Innate immune activation parallels loss of neurogenesis and increased depression-like behavior. Protection against loss of neurogenesis and negative affect by anti-oxidant, anti-inflammatory, anti-depressant, opiate antagonist and abstinence from ethanol dependence link limbic affect to changes in innate immune signaling. The hypothesis that innate immune gene induction underlies addiction and affective disorders creates new targets for therapy.

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The paper's pathway analysis results are consistent with earlier findings showing induction of innate immune genes by stress and drug abuse.
“Our pathway analysis results are consistent with earlier findings showing induction of innate immune genes by stress and drug abuse35.”
From Analysis of whole genome-transcriptomic organization in brain to identify genes associated with alcoholism (2019) · cites this paper as [35]
There is a close link between drug abuse and neuroinflammation.
“Accumulating evidence suggests a close link between drug abuse and neuroinflammation (Crews et al., 2011; Clark et al., 2013).”
From Engineered Extracellular Vesicles Loaded With miR-124 Attenuate Cocaine-Mediated Activation of Microglia (2020) · cites this paper as Crews et al., 2011

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The Intestinal Microbiota Affect Central Levels of Brain-Derived Neurotropic Factor and Behavior in Mice
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Gene Coexpression Networks in Human Brain Identify Epigenetic Modifications in Alcohol Dependence
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Common cellular and molecular mechanisms in obesity and drug addiction
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Alcohol dependence as a chronic pain disorder
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Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior
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The role of neuroimmune signaling in alcoholism
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High Mobility Group Box 1/Toll-like Receptor Danger Signaling Increases Brain Neuroimmune Activation in Alcohol Dependence
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Cessation and reduction in alcohol consumption and misuse after psychedelic use
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NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration
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Microglial activation is not equivalent to neuroinflammation in alcohol-induced neurodegeneration: The importance of microglia phenotype
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Mechanisms of neuroimmune gene induction in alcoholism
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Neuroimmune signaling in alcohol use disorder
Erickson, E. K., Grantham, E. K., Warden, A. S., & Harris, R. A. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2018.12.007 · Cited by 224 · see citing works
The Role of NFkB in Drug Addiction: Beyond Inflammation
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Neuroimmune Function and the Consequences of Alcohol Exposure
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Neuroimmune signaling: a key component of alcohol abuse
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Chronic ethanol increases systemic TLR3 agonist-induced neuroinflammation and neurodegeneration
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Psychostimulant abuse and neuroinflammation: emerging evidence of their interconnection.
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Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and toll-like receptors in the adult prefrontal cortex
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Chronic traumatic encephalopathy in contact sports: A systematic review of all reported pathological cases
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The Role of Transposable Elements in Health and Diseases of the Central Nervous System
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The link between inflammation, bugs, the intestine and the brain in alcohol dependence
Leclercq, S., de Timary, P., Delzenne, N. M., & Stärkel, P. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.15 · Cited by 174 · see citing works
Release of Neuronal HMGB1 by Ethanol through Decreased HDAC Activity Activates Brain Neuroimmune Signaling
Zou, J., & Crews, F. T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087915 · Cited by 169 · see citing works
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Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning
Vetreno, R. P., & Crews, F. T. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00035 · Cited by 166 · see citing works
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Neuroimmune Basis of Alcoholic Brain Damage
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Toll-like receptor signaling and stages of addiction
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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
Drew, P. D., Johnson, J. W., Douglas, J. C., Phelan, K. D., & Kane, C. J. M. (2015) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12639 · Cited by 150 · see citing works
Short term changes in the proteome of human cerebral organoids induced by 5-MeO-DMT
Dakic, V., Minardi Nascimento, J., Costa Sartore, R., Maciel, R. D. M., de Araujo, D. B., Ribeiro, S., Martins-de-Souza, D., & Rehen, S. K. (2017) · Scientific Reports · doi:10.1038/s41598-017-12779-5 · Cited by 134 · see citing works
Ibudilast reduces alcohol drinking in multiple animal models of alcohol dependence: Ibudilast and alcohol
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microRNA-206 in Rat Medial Prefrontal Cortex Regulates BDNF Expression and Alcohol Drinking
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Increased receptor for advanced glycation end product expression in the human alcoholic prefrontal cortex is linked to adolescent drinking
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Inflammasome-IL-1β Signaling Mediates Ethanol Inhibition of Hippocampal Neurogenesis
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Intestinal dysbiosis and permeability: the yin and yang in alcohol dependence and alcoholic liver disease
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Glial cell diversity and methamphetamine-induced neuroinflammation in human cerebral organoids
Dang, J. W., Tiwari, S. K., Agrawal, K., Hui, H., Qin, Y., & Rana, T. M. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0676-x · Cited by 123 · see citing works
Endogenous Neurosteroid (3α,5α)3-Hydroxypregnan-20-one Inhibits Toll-like-4 Receptor Activation and Pro-inflammatory Signaling in Macrophages and Brain
Balan, I. S., Beattie, M. C., O’Buckley, T. K., Aurelian, L., & Morrow, A. L. (2019) · Scientific Reports · doi:10.1038/s41598-018-37409-6 · Cited by 118 · see citing works
Prior Binge Ethanol Exposure Potentiates the Microglial Response in a Model of Alcohol-Induced Neurodegeneration
Marshall, S. A., Geil, C., & Nixon, K. (2016) · Brain Sciences · doi:10.3390/brainsci6020016 · Cited by 115 · see citing works
Animal models of post-traumatic stress disorder and recent neurobiological insights
Whitaker, A. M., Gilpin, N. W., & Edwards, S. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000069 · Cited by 110 · see citing works
CRF-Amplified Neuronal TLR4/MCP-1 Signaling Regulates Alcohol Self-Administration
June, H. L., Liu, J., Warnock, K. T., Bell, K., Balan, I. S., Bollino, D. R., Puché, A. C., & Aurelian, L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.4 · Cited by 108 · see citing works
Plasma profile of pro‐inflammatory cytokines and chemokines in cocaine users under outpatient treatment: influence of cocaine symptom severity and psychiatric co‐morbidity
Araos, P. F., Pedraz, M., Serrano, A., Lucena, M. A., Barrios, V., García‐Marchena, N., Campos‐Cloute, R., Ruiz, J. J., Romero‐Sanchiz, P., Suárez, J., et al. (2014) · Addiction Biology · doi:10.1111/adb.12156 · Cited by 107 · see citing works
Stress–response pathways are altered in the hippocampus of chronic alcoholics
McClintick, J. N., Xuei, X., Tischfield, J. A., Goate, A., Foroud, T., Wetherill, L., Ehringer, M. A., & Edenberg, H. J. (2013) · Alcohol · doi:10.1016/j.alcohol.2013.07.002 · Cited by 105 · see citing works
Alcohol and adult hippocampal neurogenesis: Promiscuous drug, wanton effects
Geil, C., Hayes, D. M., McClain, J. A., Liput, D. J., Marshall, S. A., Chen, K. Y., & Nixon, K. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.05.003 · Cited by 104 · see citing works
The Epigenetic Landscape of Alcoholism
Krishnan, H. R., Sakharkar, A. J., Teppen, T. L., Berkel, T. D. M., & Pandey, S. C. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801311-3.00003-2 · Cited by 98 · see citing works
Neuroimmune Interface in the Comorbidity between Alcohol Use Disorder and Major Depression
Neupane, S. P. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00655 · Cited by 97 · see citing works
Increased expression of M1 and M2 phenotypic markers in isolated microglia after four-day binge alcohol exposure in male rats
Peng, H., Geil, C., Chen, K. Y., McClain, J. A., & Nixon, K. (2017) · Alcohol · doi:10.1016/j.alcohol.2017.02.175 · Cited by 95 · see citing works
The Challenge by Multiple Environmental and Biological Factors Induce Inflammation in Aging: Their Role in the Promotion of Chronic Disease
Bachmann, M. C., Bellalta, S., Basoalto, R., Gómez‐Valenzuela, F., Jalil, Y., Lépez, M., Matamoros, A., & Rommy von Bernhardi, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.570083 · Cited by 96 · see citing works
Analysis of whole genome-transcriptomic organization in brain to identify genes associated with alcoholism
Kapoor, M., Wang, J.-C., Farris, S. P., Liu, Y., McClintick, J., Gupta, I., Meyers, J. L., Bertelsen, S., Chao, M., Nurnberger, J., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0384-y · Cited by 92 · see citing works
Epigenetic control of gene expression in the alcoholic brain
Ponomarev, I. (2013) · Alcohol research · doi:10.35946/arcr.v35.1.08 · Cited by 92 · see citing works
Innate Immune Signaling and Alcohol Use Disorders
Coleman, L. G., & Crews, F. T. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_92 · Cited by 90 · see citing works
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Role of Microglia in Regulation of Ethanol Neurotoxic Action
Chastain, L. G., & Sarkar, D. K. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801284-0.00004-x · Cited by 84 · see citing works
Gene Expression in Brain and Liver Produced by Three Different Regimens of Alcohol Consumption in Mice: Comparison with Immune Activation
Osterndorff-Kahanek, E. A., Ponomarev, I., Blednov, Y. A., & Harris, R. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059870 · Cited by 82 · see citing works
Glial Modulators as Potential Treatments of Psychostimulant Abuse
Beardsley, P. M., & Hauser, K. F. (2014) · Advances in pharmacology · doi:10.1016/b978-0-12-420118-7.00001-9 · Cited by 82 · see citing works
HMGB1/IL-1β complexes regulate neuroimmune responses in alcoholism
Coleman, L. G., Zou, J., Qin, L., & Crews, F. T. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.10.027 · Cited by 82 · see citing works
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The Cytokine mRNA Increase Induced by Withdrawal from Chronic Ethanol in the Sterile Environment of Brain is Mediated by CRF and HMGB1 Release
Whitman, B. A., Knapp, D. J., Werner, D. F., Crews, F. T., & Breese, G. R. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12189 · Cited by 79 · see citing works
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Alcohol abuse after traumatic brain injury: Experimental and clinical evidence
Weil, Z. M., Corrigan, J. D., & Karelina, K. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.005 · Cited by 79 · see citing works
Neuroimmune Mechanisms as Novel Treatment Targets for Substance Use Disorders and Associated Comorbidities
Namba, M. D., Leyrer-Jackson, J. M., Nagy, E. K., Olive, M. F., & Neisewander, J. L. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.650785 · Cited by 76 · see citing works
Impact of neuroimmune activation induced by alcohol or drug abuse on adolescent brain development
Guerri, C., & Pascual, M. (2019) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2018.11.006 · Cited by 78 · see citing works
Cannabidiol Treatment Might Promote Resilience to Cocaine and Methamphetamine Use Disorders: A Review of Possible Mechanisms
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Integrating mRNA and miRNA Weighted Gene Co-Expression Networks with eQTLs in the Nucleus Accumbens of Subjects with Alcohol Dependence
Mamdani, M., Williamson, V., McMichael, G. O., Blevins, T., Aliev, F., Adkins, A., Hack, L., Bigdeli, T., D. van der Vaart, A., Web, B. T., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0137671 · Cited by 73 · see citing works
IL-1 receptor signaling in the basolateral amygdala modulates binge-like ethanol consumption in male C57BL/6J mice
Marshall, S. A., Casachahua, J., Rinker, J. A., Blose, A. K., Lysle, D. T., & Thiele, T. E. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.006 · Cited by 73 · see citing works
Molecular basis of alcoholism
Most, D., Ferguson, L. B., & Harris, R. A. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-62619-6.00006-9 · Cited by 70 · see citing works
IL-1β expression is increased and regulates GABA transmission following chronic ethanol in mouse central amygdala
Patel, R. R., Khom, S., Steinman, M. Q., Varodayan, F. P., Kiosses, W. B., Hedges, D. M., Vlkolinský, R., Nadav, T., Polis, I. Y., Bajo, M., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.10.009 · Cited by 70 · see citing works
Role of microglia in ethanol-induced neurodegenerative disease: Pathological and behavioral dysfunction at different developmental stages
Yang, J., Xue, X., Tian, H., Wang, X., Dong, Y., Wang, F., Zhao, Y., Yao, X., Cui, W., & Wu, C. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.07.002 · Cited by 72 · see citing works
Current hypotheses on the mechanisms of alcoholism
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Reviewed by:
Crews, F. T., Vetreno, R. P., Kane, C. J. M., & Crews, F. T. (2011)
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S07 * COMBINED DEPENDENCE FROM ALCOHOL AND TOBACCO: INTERACTIONS AND CLINICAL IMPLICATIONS * S07.1 * THE IMPACT OF SMOKING AND ALCOHOL ON ACUTE AND CHRONIC PANCREATITIS IN THE WESTERN WORLD
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Authors: Crews, F. T., Zou, J., & Qin, L.
Affiliations: University of North Carolina at Chapel Hill (US)
Corresponding author: Crews, F.T.
ORCID: Crews, F.T.
Zou, Jian
Qin, Liya
Venue: Brain, Behavior, and Immunity
Publisher: Elsevier BV
Published: 2011-06
Volume: 25
Pages: S4-S12
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2011.03.003
PMC: PMC3552373
OpenAlex: W2018062658
Cited by: 313
References: 105
Citations by year: 2026: 7 · 2025: 14 · 2024: 21 · 2023: 13 · 2022: 17 · 2021: 25 · 2020: 21 · 2019: 18 · 2018: 15 · 2017: 25 · 2016: 23 · 2015: 28 · 2014: 33 · 2013: 18 · 2012: 28
FWCI: 2.41
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
UNC Libraries
Funders: Center for Alcohol Studies
National Institutes of Health (AA-11605, AA019767)
National Institute on Alcohol Abuse and Alcoholism (P50AA011605, AA 11605, U24AA020022, U01AA020023, AA020023, AA020022, AA020024, U24AA020024, U54AA019767, AA019767, P60AA011605)
Bowles Center for Alcohol Studies, University of North Carolina at Chapel Hill
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: addiction, neuroimmune signaling, innate immunity, NF-κB, microglia, astrocytes, alcoholism, cocaine dependence, behavioral flexibility, reversal learning, depression-like behavior, hippocampal neurogenesis, MCP-1, chemokines, cytokines, genetic polymorphism, frontal cortex, anti-inflammatory therapy
MeSH terms: Brain, Humans, Neuroimmunomodulation, Behavior, Addictive, Substance-Related Disorders

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

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