Temporal changes in innate immune signals in a rat model of alcohol withdrawal in emotional and cardiorespiratory homeostatic nuclei

Journal of Neuroinflammation

James S Schwaber³  D Craig Hooper¹  Jan B Hoek³  Gregory E Gonye³  Melanie M Brureau³  Mary M Staehle²  Rajanikanth Vadigepalli³  Anthony Brureau³  Kate Freeman³ 

[1] Department of Cancer Biology and Neurosurgery, Thomas Jefferson University, 111 South 11th Street, Philadelphia, PA, 19107, USA;Department of Chemical Engineering, Rowan University, 201 Mullica Hill Road, Glassboro, NJ, 08028, USA;Daniel Baugh Institute for Functional Genomics and Computational Biology, Department of Pathology, Anatomy and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA, 19107, USA

关键词: IHC;    Gene expression;    MCP-1;    TNF-alpha;    Inflammation;    Withdrawal;    Alcohol;   

Others  :  1212601
DOI  :  10.1186/1742-2094-9-97

 received in 2012-02-08, accepted in 2012-05-24,  发布年份 2012

【 授权许可】

   
2012 Freeman et al; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Kelley KW, Dantzer R: Alcoholism and inflammation: neuroimmunology of behavioral and mood disorders. Brain Behav Immun 2011, 25(Suppl 1):S13-S20.
• [2]Crews FT, Zou J, Qin L: Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 2011, 25(Suppl 1):S4-S12.
• [3]Valles SL, Blanco AM, Pascual M, Guerri C: Chronic ethanol treatment enhances inflammatory mediators and cell death in the brain and in astrocytes. Brain Pathol 2004, 4:365-371.
• [4]Qin L, He J, Hanes RN, Pluzarev O, Hong JS, Crews FT: Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment. J Neuroinflammation 2008, 5:10. BioMed Central Full Text
• [5]Fernandez-Lizarbe S, Pascual M, Guerri C: Critical role of TLR4 response in the activation of microglia induced by ethanol. J Immunol 2009, 7:4733-4744.
• [6]He J, Crews FT: Increased MCP-1 and microglia in various regions of the human alcoholic brain. Exp Neurol 2008, 2:349-358.
• [7]Yakovleva T, Bazov I, Watanabe H, Hauser KF, Bakalkin G: Transcriptional control of maladaptive and protective responses in alcoholics: a role of the NF-κB system. Brain Behav Immun 2011, 25(Suppl 1):S29-S38.
• [8]Gorina R, Font-Nieves M, Marquez-Kisinousky L, Santalucia T, Planas AM: Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling, MAPK, and Jak1/Stat1 pathways. Glia 2011, 2:242-255.
• [9]Okun E, Griffioen KJ, Mattson MP: Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci 2011, 5:269-281.
• [10]Barber GN: Cytoplasmic DNA innate immune pathways. Immunol Rev 2011, 1:99-108.
• [11]Veroni C, Gabriele L, Canini I, Castiello L, Coccia E, Remoli ME, Columba-Cabezas S, Arico E, Aloisi F, Agresti C: Activation of TNF receptor 2 in microglia promotes induction of anti-inflammatory pathways. Mol Cell Neurosci 2010, 3:234-244.
• [12]Kofler J, Wiley CA: Microglia: key innate immune cells of the brain. Toxicol Pathol 2011, 1:103-114.
• [13]Sosa RA, Forsthuber TG: The critical role of antigen-presentation-induced cytokine crosstalk in the central nervous system in multiple sclerosis and experimental autoimmune encephalomyelitis. J Interferon Cytokine Res 2011, 31:753-768.
• [14]Floreani NA, Rump TJ, Muneer PM, Alikunju S, Morsey BM, Brodie MR, Persidsky Y, Haorah J: Alcohol-induced interactive phosphorylation of src and toll-like receptor regulates the secretion of inflammatory mediators by human astrocytes. J Neuroimmune Pharmacol 2010, 4:533-545.
• [15]Haorah J, Knipe B, Leibhart J, Ghorpade A, Persidsky Y: Alcohol-induced oxidative stress in brain endothelial cells causes blood–brain barrier dysfunction. J Leukoc Biol 2005, 6:1223-1232.
• [16]Yu CH, Yhee JY, Kim JH, Im KS, Kim NH, Jung DI, Lee HC, Chon SK, Sur JH: Pro- and anti-inflammatory cytokine expression and histopathological characteristics in canine brain with traumatic brain injury. J Vet Sci 2011, 3:299-301.
• [17]Lisak RP, Nedelkoska L, Studzinski D, Bealmear B, Xu W, Benjamins JA: Cytokines regulate neuronal gene expression: differential effects of Th1, Th2 and monocyte/macrophage cytokines. J Neuroimmunol 2011, 1–2:19-33.
• [18]Kassner SS, Kollmar R, Bonaterra GA, Hildebrandt W, Schwab S, Kinscherf R: The early immunological response to acute ischemic stroke: differential gene expression in subpopulations of mononuclear cells. Neuroscience 2009, 2:394-401.
• [19]Thibeault I, Laflamme N, Rivest S: Regulation of the gene encoding the monocyte chemoattractant protein 1 (MCP-1) in the mouse and rat brain in response to circulating LPS and proinflammatory cytokines. J Comp Neurol 2001, 4:461-477.
• [20]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, 5:777-789.
• [21]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, 4–6:385-405.
• [22]Breese GR, Knapp DJ, Overstreet DH, Navarro M, Wills TA, Angel RA: Repeated lipopolysaccharide (LPS) or cytokine treatments sensitize ethanol withdrawal-induced anxiety-like behavior. Neuropsychopharmacology 2008, 4:867-876.
• [23]McKeon A, Frye M, Delanty N: The alcohol withdrawal syndrome. J Neurol Neurosurg Psychiatry 2008, 8:854-862.
• [24]Eyer F, Schuster T, Felgenhauer N, Pfab R, Strubel T, Saugel B, Zilker T: Risk assessment of moderate to severe alcohol withdrawal-predictors for seizures and delirium tremens in the course of withdrawal. Alcohol Alcohol 2011, 4:427-433.
• [25]Jochum T, Reinhard M, Boettger MK, Piater M, Bar KJ: Impaired cerebral autoregulation during acute alcohol withdrawal. Drug Alcohol Depend 2010, 3:240-246.
• [26]Monte R, Rabunal R, Casariego E, Lopez-Agreda H, Mateos A, Pertega S: Analysis of the factors determining survival of alcoholic withdrawal syndrome patients in a general hospital. Alcohol Alcohol 2010, 2:151-158.
• [27]Shirafuji S, Liu J, Okamura N, Hamada K, Fujimiya T: QT interval dispersion and cardiac sympathovagal balance shift in rats with acute ethanol withdrawal. Alcohol Clin Exp Res 2010, 2:223-230.
• [28]McBride WJ: Central nucleus of the amygdala and the effects of alcohol and alcohol-drinking behavior in rodents. Pharmacol Biochem Behav 2002, 3:509-515.
• [29]Rodd ZA, Kimpel MW, Edenberg HJ, Bell RL, Strother WN, McClintick JN, Carr LG, Liang T, McBride WJ: Differential gene expression in the nucleus accumbens with ethanol self-administration in inbred alcohol-preferring rats. Pharmacol Biochem Behav 2008, 4:481-498.
• [30]McBride K, WJ KMW, Schultz J, McMlintick J, Edenberg H, Bell R: Changes in gene expression in regions of the extended amygdala of alcohol-preferring rats after binge-like alcohol drinking. Alcohol 2010, 2:171183.
• [31]Freeman K, Staehle M, Gümüş Z, Vadigepalli R, Gonye G, Nichols CN, Ogunnaike B, Hoek J, Schwaber J: Rapid temporal changes in the expression of a set of neuromodulatory genes during alcohol withdrawal in the dorsal vagal complex: molecular evidence of homeostatic disturbance. Alcohol Clin Exp Res 2012. [Epub ahead of print
• [32]Schwaber JS, Kapp BS, Higgins G: The origin and extent of direct amygdala projections to the region of the dorsal motor nucleus of the vagus and the nucleus of the solitary tract. Neurosci Lett 1980, 1:15-20.
• [33]Schwaber J, Kapp B, Higgins G, Rapp P: Amygdaloid and basal forebrain direct connections with the nucleus of the solitary tract and the dorsal motor nucleus. J Neurosci 1982, 10:1424-1438.
• [34]Collins MA, Neafsey EJ: Neuroinflammatory pathways in binge alcohol-induced neuronal degeneration: oxidative stress cascade involving aquaporin, brain edema, and phospholipase A2 activation. Neurotox Res 2012, 1:70-78.
• [35]Brown J, Achille N, Neafsey EJ, Collins MA: Binge ethanol-induced neurodegeneration in rat organotypic brain slice cultures: effects of PLA2 inhibitor mepacrine and docosahexaenoic acid (DHA). Neurochem Res 2009, 2:260-267.
• [36]Lieber CS, DeCarli LM: An experimental model of alcohol feeding and liver injury in the baboon. J Med Primatol 1974, 3:153-163.
• [37]Hall Pd, Lieber CS, DeCarli LM, French SW, Lindros KO, Jarvelainen H, Bode C, Parlesak A, Bode JC: Models of alcoholic liver disease in rodents: a critical evaluation. Alcohol Clin Exp Res 2001, 25(Suppl 5):254S-261S.
• [38]Lieber CS, DeCarli LM: Animal models of chronic ethanol toxicity. Methods Enzymol 1994, 233:585-594.
• [39]Wilson JS, Korsten MA, Lieber CS: The combined effects of protein deficiency and chronic ethanol administration on rat ethanol metabolism. Hepatology 1986, 5:823-829.
• [40]Macey DJ, Schulteis G, Heinrichs SC, Koob GF: Time-dependent quantifiable withdrawal from ethanol in the rat: effect of method of dependence induction. Alcohol 1996, 2:163-170.
• [41]Walker DW, Hunter BE, Riley J: A behavioral and electrophysiological analysis of ethanol dependence in the rat. Adv Exp Med Biol 1975, 59:353-372.
• [42]Hunter BE, Riley JN, Walker DW: Ethanol dependence in the rat: a parametric analysis. Pharmacol Biochem Behav 1975, 4:619-629.
• [43]Geisler RF, Hunter BE, Walker DW: Ethanol dependence in the rat: temporal changes in neuroexcitability following withdrawal. Psychopharmacology (Berl) 1978, 3:287-292.
• [44]Macey DJ, Schulteis G, Heinrichs SC, Koob GF: Time-dependent quantifiable withdrawal from ethanol in the rat: effect of method of dependence induction. Alcohol 1996, 2:163-170.
• [45]Khan RL, Vadigepalli R, McDonald MK, Rogers RF, Gao GR, Schwaber JS: Dynamic transcriptomic response to acute hypertension in the nucleus tractus solitarius. Am J Physiol Regul Integr Comp Physiol 2008, 295:R15-R27.
• [46]Orina JN, Calcagno AM, Wu CP, Varma S, Shih J, Lin M, Eichler G, Weinstein JN, Pommier Y, Ambudkar SV, Gottesman MM, Gillet JP: Evaluation of current methods used to analyze the expression profiles of ATP-binding cassette transporters yields an improved drug-discovery database. Mol Cancer Ther 2009, 7:2057-2066.
• [47]Spurgeon SL, Jones RC, Ramakrishnan R: High throughput gene expression measurement with real time PCR in a microfluidic dynamic array. PLoS One 2008, 2:e1662.
• [48]Fujita A, Sato JR, DeRodrigues LO, Ferreira CE, Sogayar MC: Evaluating different methods of microarray data normalization. BMC Bioinformatics 2006, 7:469. BioMed Central Full Text
• [49]Bolstad BM, Irizarry RA, Astrand M, Speed TP: A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 2:185-193.
• [50]Pradervand S, Weber J, Thomas J, Bueno M, Wirapati P, Lefort K, Dotto GP, Harshman K: Impact of normalization on miRNA microarray expression profiling. RNA 2009, 3:493-501.
• [51]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 6:1101-1108.
• [52]Duijvestijn AM, van Goor H, Klatter F, Majoor GD, van Bussel E, van Breda Vriesman PJ: Antibodies defining rat endothelial cells: RECA-1, a pan-endothelial cell-specific monoclonal antibody. Lab Invest 1992, 4:459-466.
• [53]Sims MR: Blood vessel response to pan-endothelium (RECA-1) antibody in normal and tooth loaded rat periodontal ligament. Eur J Orthod 1999, 5:469-479.
• [54]Saubaméa B, Cochois-Guégan V, Cisternino S, Scherrmann JM: Heterogeneity in the rat brain vasculature revealed by quantitative confocal analysis of endothelial barrier antigen and P-glycoprotein expression. J Cereb Blood Flow Metab 2012, 1:81-92.
• [55]Macdonald JA, Murugesan N, Pachter JS: Endothelial cell heterogeneity of blood–brain barrier gene expression along the cerebral microvasculature. J Neurosci Res 2010, 7:1457-1474.
• [56]Seguin R, Biernacki K, Rotondo RL, Prat A, Antel JP: Regulation and functional effects of monocyte migration across human brain-derived endothelial cells. J Neuropathol Exp Neurol 2003, 4:412-419.
• [57]Turowski P, Adamson P, Greenwood J: Pharmacological targeting of ICAM-1 signaling in brain endothelial cells: potential for treating neuroinflammation. Cell Mol Neurobiol 2005, 1:153-170.
• [58]Wong D, Prameya R, Dorovini-Zis K: Adhesion and migration of polymorphonuclear leukocytes across human brain microvessel endothelial cells are differentially regulated by endothelial cell adhesion molecules and modulate monolayer permeability. J Neuroimmunol 2007, 1–2:136-148.
• [59]Bar KJ, Boettger MK, Schulz S, Neubauer R, Jochum T, Voss A, Yeragani VK: Reduced cardio-respiratory coupling in acute alcohol withdrawal. Drug Alcohol Depend 2008, 3:210-217.
• [60]Zera T, Ufnal M, Szczepanska-Sadowska E: Central TNF-alpha elevates blood pressure and sensitizes to central pressor action of angiotensin II in the infarcted rats. J Physiol Pharmacol 2008, 59(Suppl 8):S117-S121.
• [61]Knapp DJ, Whitman BA, Wills TA, Angel RA, Overstreet DH, Criswell HE, Ming Z, Breese GR: Cytokine involvement in stress may depend on corticotrophin releasing factor to sensitize ethanol withdrawal anxiety. Brain Behav Immun 2011, 25(Suppl 1):S146-S154.
• [62]Pascual M, Balino P, Alfonso-Loeches S, Aragon CM, Guerri C: Impact of TLR4 on behavioral and cognitive dysfunctions associated with alcohol-induced neuroinflammatory damage. Brain Behav Immun 2011, 25(Suppl 1):S80-S91.
• [63]Koob GF: Theoretical frameworks and mechanistic aspects of alcohol addiction: alcohol addiction as a reward deficit disorder. Curr Top Behav Neurosci 2011. Epub ahead of print
• [64]Collins MA, Corso TD, Neafsey EJ: Neuronal degeneration in rat cerebrocortical and olfactory regions during subchronic "binge" intoxication with ethanol: possible explanation for olfactory deficits in alcoholics. Alcohol Clin Exp Res 1996, 2:284-292.
• [65]Prendergast MA, Harris BR, Mullholland PJ, Blanchard JA, Gibson DA, Holley RC, Littleton JM: Hippocampal CA1 region neurodegeneration produced by ethanol withdrawal requires activation of intrinsic polysynaptic hippocampal pathways and function of N-methyl-D-aspartate receptors. Neuroscience 2004, 4:869-877.
• [66]Mechtcheriakov S, Brenneis C, Egger K, Koppelstaetter F, Schocke M, Marksteiner J: A widespread distinct pattern of cerebral atrophy in patients with alcohol addiction revealed by voxel-based morphometry. J Neurol Neurosurg Psychiatry 2007, 6:610-614.
• [67]Benjamins JA, Nedelkoska L, Lisak RP, Hannigan JH, Sokol RJ: Cytokines reduce toxic effects of ethanol on oligodendroglia. Neurochem Res 2011, 9:1677-1686.
• [68]Rump TJ, Abdul Muneer PM, Szlachetka AM, Lamb A, Haorei C, Alikunju S, Xiong H, Keblesh J, Liu J, Zimmerman MC, Jones J, Donohue TM, Persidsky Y, Haorah J: Acetyl-L-carnitine protects neuronal function from alcohol-induced oxidative damage in the brain. Free Radic Biol Med 2010, 10:1494-1504.
• [69]Zahr NM, Luong R, Sullivan EV, Pfefferbaum A: Measurement of serum, liver, and brain cytokine induction, thiamine levels, and hepatopathology in rats exposed to a 4-day alcohol binge protocol. Alcohol Clin Exp Res 2010, 34:1858-1870.
• [70]Freeman K, Staehle MM, Vadigepalli R, Gonye GE, Ogunnaike BA, Hoek JB, Schwaber JS: Measurement of serum, liver, and brain cytokine induction, thiamine levels, and hepatopathology in rats exposed to a 4-day alcohol binge protocol. Alcohol Clin Exp Res 2012, 34:1858-1870.