Role of the innate immune system in the neuropathological consequences induced by adolescent binge drinking

María Pascual; Jorge Montesinos; Consuelo Guerri

doi:10.1002/jnr.24203

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Publisher: Wiley Subscription Services, Inc., A Wiley Company
Copyright: © 2018 Wiley Periodicals, Inc.
ISSN: 0360-4012
eISSN: 1097-4547
D.O.I.: 10.1002/jnr.24203
Publisher site: See Article on Publisher Site

Abstract

Adolescence is a critical stage of brain maturation in which important plastic and dynamic processes take place in different brain regions, leading to development of the adult brain. Ethanol drinking in adolescence disrupts brain plasticity and causes structural and functional changes in immature brain areas (prefrontal cortex, limbic system) that result in cognitive and behavioral deficits. These changes, along with secretion of sexual and stress‐related hormones in adolescence, may impact self‐control, decision making, and risk‐taking behaviors that contribute to anxiety and initiation of alcohol consumption. New data support the participation of the neuroimmune system in the effects of ethanol on the developing and adult brain. This article reviews the potential pathological bases that underlie the effects of alcohol on the adolescent brain, such as the contribution of genetic background, the perturbation of epigenetic programming, and the influence of the neuroimmune response. Special emphasis is given to the actions of ethanol in the innate immune receptor toll‐like receptor 4 (TLR4), since recent studies have demonstrated that by activating the inflammatory TLR4/NFκB signaling response in glial cells, binge drinking of ethanol triggers the release of cytokines/chemokines and free radicals, which exacerbate the immune response that causes neuroinflammation/neural damage as well as short‐ and long‐term neurophysiological, cognitive, and behavioral dysfunction. Finally, potential treatments that target the neuroimmune response to treat the neuropathological and behavioral consequences of adolescent alcohol abuse are discussed.

Journal

Journal of Neuroscience Research – Wiley

Published: Jan 1, 2018

Keywords: ; ; ; ; ;

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Gender differences in nitric oxide production by alveolar macrophages in ethanol plus lipopolysaccharide‐treated rats

Spitzer, J. A.
Microglia modulate wiring of the embryonic forebrain

Squarzoni, P.; Oller, G.; Hoeffel, G.; Pont‐Lezica, L.; Rostaing, P.; Low, D.; Garel, S.
Neural predictors of initiating alcohol use during adolescence

Squeglia, L. M.; Ball, T. M.; Jacobus, J.; Brumback, T.; McKenna, B. S.; Nguyen‐Louie, T. T.; Tapert, S. F.
Adolescent binge drinking linked to abnormal spatial working memory brain activation: Differential gender effects

Squeglia, L. M.; Schweinsburg, A. D.; Pulido, C.; Tapert, S. F.
Structural connectivity of neural reward networks in youth at risk for substance use disorders

Squeglia, L. M.; Sorg, S. F.; Jacobus, J.; Brumback, T.; Taylor, C. T.; Tapert, S. F.
Binge drinking differentially affects adolescent male and female brain morphometry

Squeglia, L. M.; Sorg, S. F.; Schweinsburg, A. D.; Wetherill, R. R.; Pulido, C.; Tapert, S. F.
Initiating moderate to heavy alcohol use predicts changes in neuropsychological functioning for adolescent girls and boys

Squeglia, L. M.; Spadoni, A. D.; Infante, M. A.; Myers, M. G.; Tapert, S. F.
Ethane‐β‐sultam modifies the activation of the innate immune system induced by intermittent ethanol administration in female adolescent rats

Stefanini, C.; Colivicchi, M. A.; Della Corte, L.; Ward, R. J.; Witte, P.; Lallemand, F.; Dexter, D. T.
Around the world, adolescence is a time of heightened sensation seeking and immature self‐regulation

Steinberg, L.; Icenogle, G.; Shulman, E. P.; Breiner, K.; Chein, J.; Bacchini, D.; Takash, H. M.
Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor‐alpha

Stellwagen, D.; Beattie, E. C.; Seo, J. Y.; Malenka, R. C.
The classical complement cascade mediates CNS synapse elimination

Stevens, B.; Allen, N. J.; Vazquez, L. E.; Howell, G. R.; Christopherson, K. S.; Nouri, N.; Barres, B. A.
Activation of nuclear PPARgamma receptors by the antidiabetic agent pioglitazone suppresses alcohol drinking and relapse to alcohol seeking

Stopponi, S.; Somaini, L.; Cippitelli, A.; Cannella, N.; Braconi, S.; Kallupi, M.; Ciccocioppo, R.
"Binge" drinking experience in adolescent mice shows sex differences and elevated ethanol intake in adulthood

Strong, M. N.; Yoneyama, N.; Fretwell, A. M.; Snelling, C.; Tanchuck, M. A.; Finn, D. A.
Cognitive, emotion control, and motor performance of adolescents in the NCANDA study: Contributions from alcohol consumption, age, sex, ethnicity, and family history of addiction

Sullivan, E. V.; Brumback, T.; Tapert, S. F.; Fama, R.; Prouty, D.; Brown, S. A.; Pfefferbaum, A.
Age‐dependent inhibition of long‐term potentiation by ethanol in immature versus mature hippocampus

Swartzwelder, H. S.; Wilson, W. A.; Tayyeb, M. I.
Alcohol's effect on host defense

Szabo, G.; Saha, B.
Accumbens neurochemical adaptations produced by binge‐like alcohol consumption

Szumlinski, K. K.; Diab, M. E.; Friedman, R.; Henze, L. M.; Lominac, K. D.; Bowers, M. S.
Long‐lasting reduction in hippocampal neurogenesis by alcohol consumption in adolescent nonhuman primates

Taffe, M. A.; Kotzebue, R. W.; Crean, R. D.; Crawford, E. F.; Edwards, S.; Mandyam, C. D.
Substance use and withdrawal: Neuropsychological functioning over 8 years in youth

Tapert, S. F.; Granholm, E.; Leedy, N. G.; Brown, S. A.
Temporal dynamics of brain anatomy

Toga, A. W.; Thompson, P. M.
Binge drinking, cognitive performance and mood in a population of young social drinkers

Townshend, J. M.; Duka, T.
Inhibition of IKKbeta reduces ethanol consumption in C57BL/6J mice

Truitt, J. M.; Blednov, Y. A.; Benavidez, J. M.; Black, M.; Ponomareva, O.; Law, J.; Mayfield, R. D.
Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals

Uematsu, A.; Matsui, M.; Tanaka, C.; Takahashi, T.; Noguchi, K.; Suzuki, M.; Nishijo, H.
Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes

Valles, S. L.; Blanco, A. M.; Pascual, M.; Guerri, C.
Functional neurogenesis in the adult hippocampus

Praag, H.; Schinder, A. F.; Christie, B. R.; Toni, N.; Palmer, T. D.; Gage, F. H.
Chronic intermittent ethanol exposure during adolescence: Effects on stress‐induced social alterations and social drinking in adulthood

Varlinskaya, E. I.; Kim, E. U.; Spear, L. P.
Ethanol intake under social circumstances or alone in Sprague–Dawley rats: Impact of age, sex, social activity, and social anxiety‐like behavior

Varlinskaya, E. I.; Truxell, E. M.; Spear, L. P.
Adolescent, but not adult, binge ethanol exposure leads to persistent global reductions of choline acetyltransferase expressing neurons in brain

Vetreno, R. P.; Broadwater, M.; Liu, W.; Spear, L. 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

Vetreno, R. P.; Crews, F. T.
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.
Increased receptor for advanced glycation end product expression in the human alcoholic prefrontal cortex is linked to adolescent drinking

Vetreno, R. P.; Qin, L.; Crews, F. T.
Diffusion tensor imaging reveals adolescent binge ethanol‐induced brain structural integrity alterations in adult rats that correlate with behavioral dysfunction

Vetreno, R. P.; Yaxley, R.; Paniagua, B.; Crews, F. T.
Adult rat cortical thickness changes across age and following adolescent intermittent ethanol treatment

Vetreno, R. P.; Yaxley, R.; Paniagua, B.; Johnson, G. A.; Crews, F. T.
Neuromodulatory properties of inflammatory cytokines and their impact on neuronal excitability

Vezzani, A.; Viviani, B.
Interleukin‐1beta enhances NMDA receptor‐mediated intracellular calcium increase through activation of the Src family of kinases

Viviani, B.; Bartesaghi, S.; Gardoni, F.; Vezzani, A.; Behrens, M. M.; Bartfai, T.; Marinovich, M.
Neuro‐inflammation induced in the hippocampus of “binge drinking” rats may be mediated by elevated extracellular glutamate content

Ward, R. J.; Colivicchi, M. A.; Allen, R.; Schol, F.; Lallemand, F.; Witte, P.; Dexter, D.
Biochemical and neurotransmitter changes implicated in alcohol‐induced brain damage in chronic or “binge drinking” alcohol abuse

Ward, R. J.; Lallemand, F.; Witte, P.
Influence of adolescent heavy session drinking on the systemic and brain innate immune system

Ward, R. J.; Lallemand, F.; Witte, P.
A gender‐specific measure of binge drinking among college students

Wechsler, H.; Dowdall, G. W.; Davenport, A.; Rimm, E. B.
Tumor necrosis factor‐alpha‐induced neutral sphingomyelinase‐2 modulates synaptic plasticity by controlling the membrane insertion of NMDA receptors

Wheeler, D.; Knapp, E.; Bandaru, V. V.; Wang, Y.; Knorr, D.; Poirier, C.; Haughey, N. J.
Global status report on alcohol and health
A novel microglial subset plays a key role in myelinogenesis in developing brain

Wlodarczyk, A.; Holtman, I. R.; Krueger, M.; Yogev, N.; Bruttger, J.; Khorooshi, R.; Owens, T.
Astrocytes contribute to synapse elimination via type 2 inositol 1,4,5‐trisphosphate receptor‐dependent release of ATP

Yang, J.; Yang, H.; Liu, Y.; Li, X.; Qin, L.; Lou, H.; Wang, H.
Minocycline and sulforaphane inhibited lipopolysaccharide‐mediated retinal microglial activation

Yang, L. P.; Zhu, X. A.; Tso, M. O.
Effects of interleukin‐1beta on hippocampal glutamate and GABA releases associated with Ca2+‐induced Ca2 + releasing systems

Zhu, G.; Okada, M.; Yoshida, S.; Mori, F.; Ueno, S.; Wakabayashi, K.; Kaneko, S.

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Role of the innate immune system in the neuropathological consequences induced by adolescent binge drinking

Role of the innate immune system in the neuropathological consequences induced by adolescent binge drinking

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Role of the innate immune system in the neuropathological consequences induced by adolescent binge drinking

Role of the innate immune system in the neuropathological consequences induced by adolescent binge drinking

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