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Neuroinflammatory Pathways in Binge Alcohol-Induced Neuronal Degeneration: Oxidative Stress Cascade Involving Aquaporin, Brain Edema, and Phospholipase A2 Activation

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Abstract

Chronic binge alcohol exposure in adult rat models causes neuronal degeneration in the cortex and hippocampus that is not reduced by excitotoxic receptor antagonists, but is prevented by antioxidants. Neuroinflammatory (glial–neuronal) signaling pathways are believed to underlie the oxidative stress and brain damage. Based on our experimental results as well as increased knowledge about the pro-neuroinflammatory potential of glial water channels, we propose that induction of aquaporin-4 can be a critical initiating factor in alcohol’s neurotoxic effects, through the instigation of cellular edema-based neuroinflammatory cascades involving increased phospholipase A2 activities, polyunsaturated fatty acid release/membrane depletion, decreased prosurvival signaling, and oxidative stress. A testable scheme for this pathway is presented that incorporates recent findings in the alcohol–brain literature indicating a role for neuroimmune activation (upregulation of NF-kappaB, proinflammatory cytokines, and toll-like receptors). We present the argument that such neuroimmune activation could be associated with or even dependent on increased aquaporin-4 and glial swelling as well.

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Abbreviations

AA:

Arachidonic acid

AQP4:

Aquaporin-4

AZA:

Acetazolamide

DHA:

Docosahexaenoic acid

HEC:

Hippocampal-entorhinal cortical

IL:

Interleukin

LPS:

Lipopolysaccharide

MCP-1:

Monocyte chemoattractant protein-1

MP:

Mepacrine

NMDA:

N-methyl d-aspartate

NOX:

NADPH oxidase

PLA2:

Phospholipase A2

PS:

Phosphatidylserine

ROS:

Reactive oxygen species

TLR:

Toll-like receptor(s)

TNF:

Tumor necrosis factor

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Acknowledgments

The laboratory contributions of Dr. Jian Zou, Dr. Kumar Sripathirathan, and Dr. James Brown III and research assistants Mr. Nick Achille and Ms. Nuzhath Tajuddin are gratefully recognized. Financial support from the NIH (AA011543, AA014436 and AA018279), Loyola University Alcohol Research Program (T32 AA013527), and Loyola University Research Stimulation Fund (LUMC Neuroscience Institute) is responsible for our laboratories’ research funding.

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  1. Department of Molecular Pharmacology & Therapeutics, Stritch School of Medicine, Loyola University Chicago, 2160 South First Avenue, Maywood, IL, 60153, USA

    Michael A. Collins & Edward J. Neafsey

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  1. Michael A. Collins
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  2. Edward J. Neafsey
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Correspondence to Michael A. Collins.

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Collins, M.A., Neafsey, E.J. Neuroinflammatory Pathways in Binge Alcohol-Induced Neuronal Degeneration: Oxidative Stress Cascade Involving Aquaporin, Brain Edema, and Phospholipase A2 Activation. Neurotox Res 21, 70–78 (2012). https://doi.org/10.1007/s12640-011-9276-5

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  • DOI: https://doi.org/10.1007/s12640-011-9276-5

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