Acute inhalation of combustion smoke triggers neuroinflammation and persistent anxiety-like behavior in the mouse

References

• Alarie Y. (2002). Toxicity of fire smoke. Crit Rev Toxicol 32:259–89.
   PubMed Web of Science ®Google Scholar
• Bailey KR, Crawley JN. (2009). Anxiety-related behaviors in mice. In: Buccafusco JJ, editor. Methods of behavior analysis in neuroscience. 2nd ed. Boca Raton, FL: CRC Press/Taylor & Francis.
   Google Scholar
• Baud F, Boukobza M, Borron SW. (2011). Cyanide: an unreported cause of neurological complications following smoke inhalation. BMJ Case Rep 2011. DOI:10.1136/bcr.1109.2011.4881
   PubMedGoogle Scholar
• Becher B, Spath S, Goverman J. (2017). Cytokine networks in neuroinflammation. Nat Rev Immunol 17:49–59.
   PubMed Web of Science ®Google Scholar
• Betterman K, Patel S. (2014). Neurologic complications of carbon monoxide intoxication. Handb Clin Neurol 120:971–9.
   PubMedGoogle Scholar
• Burman MA, Simmons CA, Hughes M, Lei L. (2014). Developing and validating trace fear conditioning protocols in C57BL/6 mice. J Neurosci Methods 222:111–7.
   PubMed Web of Science ®Google Scholar
• Chen H, Desai A, Kim HY. (2017). Repetitive Closed-Head Impact Model of Engineered Rotational Acceleration Induces Long-Term Cognitive Impairments with Persistent Astrogliosis and Microgliosis in Mice. J Neurotrauma 34:2291–302.
   PubMed Web of Science ®Google Scholar
• Chen L, Lee HM, Greeley GH, Jr, Englander EW. (2007). Accumulation of oxidatively generated DNA damage in the brain: a mechanism of neurotoxicity. Free Radic Biol Med 42:385–93.
   PubMed Web of Science ®Google Scholar
• Cohen JL, Ata AE, Jackson NL, et al. (2017). Differential stress induced c-Fos expression and identification of region-specific miRNA-mRNA networks in the dorsal raphe and amygdala of high-responder/low-responder rats. Behav Brain Res 319:110–23.
   PubMed Web of Science ®Google Scholar
• Cortez I, Bulavin DV, Wu P, et al. (2017). Aged dominant negative p38α MAPK mice are resistant to age-dependent decline in adult-neurogenesis and context discrimination fear conditioning. Behav Brain Res 322:212–22.
   PubMed Web of Science ®Google Scholar
• Crawley JN, Paylor R. (1997). A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm Behav 31:197–211.
   PubMed Web of Science ®Google Scholar
• di Penta A, Moreno B, Reix S, et al. (2013). Oxidative stress and proinflammatory cytokines contribute to demyelination and axonal damage in a cerebellar culture model of neuroinflammation. PLoS One 8:e54722.
   PubMed Web of Science ®Google Scholar
• Dineley KT, Hogan D, Zhang WR, Taglialatela G. (2007). Acute inhibition of calcineurin restores associative learning and memory in Tg2576 APP transgenic mice. Neurobiol Learn Mem 88:217–24.
   PubMed Web of Science ®Google Scholar
• Dineley KT, Xia X, Bui D, et al. (2002). Accelerated plaque accumulation, associative learning deficits, and up-regulation of alpha 7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J Biol Chem 277:22768–80.
   PubMed Web of Science ®Google Scholar
• Dries DJ, Endorf FW. (2013). Inhalation injury: epidemiology, pathology, treatment strategies. Scand J Trauma Resusc Emerg Med 21:31.
   PubMed Web of Science ®Google Scholar
• Fadok JP, Krabbe S, Markovic M, et al. (2017). A competitive inhibitory circuit for selection of active and passive fear responses. Nature 542:96–100.
   PubMed Web of Science ®Google Scholar
• Frugier T, Morganti-Kossmann MC, O'Reilly D, McLean CA. (2010). In situ detection of inflammatory mediators in post mortem human brain tissue after traumatic injury. J Neurotrauma 27:497–507.
   PubMed Web of Science ®Google Scholar
• Geldner G, Koch EM, Gottwald-Hostalek U, et al. (2013). Report on a study of fires with smoke gas development : determination of blood cyanide levels, clinical signs and laboratory values in victims. Anaesthesist 62:609–16.
   PubMed Web of Science ®Google Scholar
• Ghosh N, Ghosh R, Mandal SC. (2011). Antioxidant protection: a promising therapeutic intervention in neurodegenerative disease. Free Radic Res 45:888–905.
   PubMed Web of Science ®Google Scholar
• Gorgun FM, Zhuo M, Singh S, Englander EW. (2014). Neuroglobin mitigates mitochondrial impairments induced by acute inhalation of combustion smoke in the mouse brain. Inhal Toxicol 26:361–9.
   PubMed Web of Science ®Google Scholar
• Gorgun MF, Zhuo M, Englander EW. (2017). Cisplatin toxicity in dorsal root ganglion neurons is relieved by meclizine via diminution of mitochondrial compromise and improved clearance of DNA damage. Mol Neurobiol 54:7883--95.
   PubMed Web of Science ®Google Scholar
• Graham BH, David Sweatt J, Craigen WJ. (2002). Noninvasive, in vivo approaches to evaluating behavior and exercise physiology in mouse models of mitochondrial disease. Methods 26:364–70.
   PubMed Web of Science ®Google Scholar
• Hammelrath L, Skokic S, Khmelinskii A, et al. (2016). Morphological maturation of the mouse brain: An in vivo MRI and histology investigation. Neuroimage 125:144–52.
   PubMed Web of Science ®Google Scholar
• Hartzell GE. (1996). Overview of combustion toxicology. Toxicology 115:7–23.
   PubMed Web of Science ®Google Scholar
• Huang CC, Chung MH, Weng SF, et al. (2014). Long-term prognosis of patients with carbon monoxide poisoning: a nationwide cohort study. PLoS One 9:e105503
   PubMed Web of Science ®Google Scholar
• Komada M, Takao K, Miyakawa T. (2008). Elevated plus maze for mice. J Vis Exp:1088.
   PubMedGoogle Scholar
• Kumar A, Stoica BA, Loane DJ, et al. (2017). Microglial-derived microparticles mediate neuroinflammation after traumatic brain injury. J Neuroinflammation 14:47
   PubMed Web of Science ®Google Scholar
• Kuroda H, Fujihara K, Kushimoto S, Aoki M. (2015). Novel clinical grading of delayed neurologic sequelae after carbon monoxide poisoning and factors associated with outcome. Neurotoxicology 48:35–43.
   PubMed Web of Science ®Google Scholar
• LeDoux JE. (2000). Emotion circuits in the brain. Annu Rev Neurosci 23:155–84.
   PubMed Web of Science ®Google Scholar
• Lee HM, Greeley GH, Herndon DN, et al. (2005). A rat model of smoke inhalation injury: influence of combustion smoke on gene expression in the brain. Toxicol Appl Pharmacol 208:255–65.
   PubMed Web of Science ®Google Scholar
• Lee HM, Greeley GH, Jr, Englander EW. (2011). Transgenic overexpression of neuroglobin attenuates formation of smoke-inhalation-induced oxidative DNA damage, in vivo, in the mouse brain. Free Radic Biol Med 51:2281–7.
   PubMed Web of Science ®Google Scholar
• Lee HM, Hallberg LM, Greeley GH Jr, Englander EW. (2010). Differential inhibition of mitochondrial respiratory complexes by inhalation of combustion smoke and carbon monoxide, in vivo, in the rat brain. Inhal Toxicol 22:770–7.
   PubMed Web of Science ®Google Scholar
• Lee HM, Reed J, Greeley GH Jr, Englander EW. (2009). Impaired mitochondrial respiration and protein nitration in the rat hippocampus after acute inhalation of combustion smoke. Toxicol Appl Pharmacol 235:208–15.
   PubMed Web of Science ®Google Scholar
• Lei Y, Chen CJ, Yan XX, et al. (2017). Early-life lipopolysaccharide exposure potentiates forebrain expression of NLRP3 inflammasome proteins and anxiety-like behavior in adolescent rats. Brain Res 1671:43–54.
   PubMed Web of Science ®Google Scholar
• Mangold CA, Wronowski B, Du M, et al. (2017). Sexually divergent induction of microglial-associated neuroinflammation with hippocampal aging. J Neuroinflammation 14:141
   PubMed Web of Science ®Google Scholar
• Maren S. (2001). Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931.
   PubMed Web of Science ®Google Scholar
• Mayerhofer R, Frohlich EE, Reichmann F, et al. (2017). Diverse action of lipoteichoic acid and lipopolysaccharide on neuroinflammation, blood-brain barrier disruption, and anxiety in mice. Brain Behav Immun 60:174–87.
   PubMed Web of Science ®Google Scholar
• McShane R, Areosa SA, Minakaran N. (2006). Memantine for dementia. Cochrane Database Syst Rev 19:CD003154.
   Google Scholar
• Micu I, Plemel JR, Caprariello AV, et al. (2018). Axo-myelinic neurotransmission: a novel mode of cell signalling in the central nervous system. Nat Rev Neurosci 19:49–58.
   PubMed Web of Science ®Google Scholar
• Mizuno Y, Sakurai Y, Sugimoto I, et al. (2014). Delayed leukoencephalopathy after carbon monoxide poisoning presenting as subacute dementia. Intern Med 53:1441–5.
   PubMed Web of Science ®Google Scholar
• Pages B, Planton M, Buys S, et al. (2014). Neuropsychological outcome after carbon monoxide exposure following a storm: a case-control study. BMC Neurol 14:153
   PubMed Web of Science ®Google Scholar
• Pang L, Wang HL, Wang ZH, et al. (2014). Plasma copeptin as a predictor of intoxication severity and delayed neurological sequelae in acute carbon monoxide poisoning. Peptides 59:89–93.
   PubMed Web of Science ®Google Scholar
• Papa L, Wang KKW. (2017). Raising the bar for traumatic brain injury biomarker research: Methods make a difference. J Neurotrauma 34:2187–9.
   PubMed Web of Science ®Google Scholar
• Peruga I, Hartwig S, Thone J, et al. (2011). Inflammation modulates anxiety in an animal model of multiple sclerosis. Behav Brain Res 220:20–9.
   PubMed Web of Science ®Google Scholar
• Phillips RG, LeDoux JE. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274–85.
   PubMed Web of Science ®Google Scholar
• Prokop S, Miller KR, Heppner FL. (2013). Microglia actions in Alzheimer’s disease. Acta Neuropathol 126:461–77.
   PubMedGoogle Scholar
• Raj D, Yin Z, Breur M, et al. (2017). Increased white matter inflammation in aging- and Alzheimer's disease brain. Front Mol Neurosci 10:206
   PubMed Web of Science ®Google Scholar
• Rodriguez-Rivera J, Denner L, Dineley KT. (2011). Rosiglitazone reversal of Tg2576 cognitive deficits is independent of peripheral gluco-regulatory status. Behav Brain Res 216:255–61.
   PubMed Web of Science ®Google Scholar
• Rossi J, 3rd, Ritchie GD, Macys DA, Still KR. (1996). An overview of the development, validation, and application of neurobehavioral and neuromolecular toxicity assessment batteries: potential applications to combustion toxicology. Toxicology 115:107–17.
   PubMed Web of Science ®Google Scholar
• Russell PA. (1973). Open-field defecation in rats: relationships with body weight and basal defecation level. Br J Psychol 64:109–14.
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Livak KJ. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–8.
   PubMed Web of Science ®Google Scholar
• Schregel K, Wuerfel E, Garteiser P, et al. (2012). Demyelination reduces brain parenchymal stiffness quantified in vivo by magnetic resonance elastography. Proc Natl Acad Sci USA 109:6650–5.
   PubMed Web of Science ®Google Scholar
• Serra-de-Oliveira N, Boilesen SN, Prado de Franca Carvalho C, et al. (2015). Behavioural changes observed in demyelination model shares similarities with white matter abnormalities in humans. Behav Brain Res 287:265–75.
   PubMed Web of Science ®Google Scholar
• Shoji H, Takao K, Hattori S, Miyakawa T. (2014). Contextual and cued fear conditioning test using a video analyzing system in mice. J Vis Exp 85:50871.
   Google Scholar
• Simon DW, McGeachy MJ, Bayir H, et al. (2017). The far-reaching scope of neuroinflammation after traumatic brain injury. Nat Rev Neurol 13:171–91.
   PubMed Web of Science ®Google Scholar
• Smith SM, Stuhmiller JH, Januszkiewicz AJ. (1996). Evaluation of lethality estimates for combustion gases in military scenarios. Toxicology 115:157–65.
   PubMed Web of Science ®Google Scholar
• Stuhmiller JH, Long DW, Stuhmiller LM. (2006). An internal dose model of incapacitation and lethality risk from inhalation of fire gases. Inhal Toxicol 18:347–64.
   PubMed Web of Science ®Google Scholar
• Taglialatela G, Hogan D, Zhang WR, Dineley KT. (2009). Intermediate- and long-term recognition memory deficits in Tg2576 mice are reversed with acute calcineurin inhibition. Behav Brain Res 200:95–9.
   PubMed Web of Science ®Google Scholar
• Tsai CF, Yip PK, Chen SY, et al. (2014). The impacts of acute carbon monoxide poisoning on the brain: Longitudinal clinical and 99mTc ethyl cysteinate brain SPECT characterization of patients with persistent and delayed neurological sequelae. Clin Neurol Neurosurg 119:21–7.
   PubMed Web of Science ®Google Scholar
• Tu TW, Kim JH, Yin FQ, et al. (2013). The impact of myelination on axon sparing and locomotor function recovery in spinal cord injury assessed using diffusion tensor imaging. NMR Biomed 26:1484–95.
   PubMed Web of Science ®Google Scholar
• Waisman A, Liblau RS, Becher B. (2015). Innate and adaptive immune responses in the CNS. Lancet Neurol 14:945–55.
   PubMed Web of Science ®Google Scholar
• Weaver LK. (2009). Clinical practice. Carbon monoxide poisoning. N Engl J Med 360:1217–25.
   PubMed Web of Science ®Google Scholar
• Xu H, Zhang SL, Tan GW, et al. (2012). Reactive gliosis and neuroinflammation in rats with communicating hydrocephalus. Neuroscience 218:317–25.
   PubMed Web of Science ®Google Scholar
• Yeh ZT, Tsai CF, Yip PK, et al. (2014). Neuropsychological performance in patients with carbon monoxide poisoning. Appl Neuropsychol Adult 21:278–87.
   PubMed Web of Science ®Google Scholar
• Yin F, Yao J, Brinton RD, Cadenas E. (2017). Editorial: The metabolic-inflammatory axis in brain aging and neurodegeneration. Front Aging Neurosci 9:209
   PubMed Web of Science ®Google Scholar
• Yin M, Chen Y, Zheng H, et al. (2017). Assessment of mouse cognitive and anxiety-like behaviors and hippocampal inflammation following a repeated and intermittent paradoxical sleep deprivation procedure. Behav Brain Res 321:69–78.
   PubMed Web of Science ®Google Scholar
• Zhang H, Yan G, Xu H, et al. (2016). The recovery trajectory of adolescent social defeat stress-induced behavioral, (1)H-MRS metabolites and myelin changes in Balb/c mice. Sci Rep 6:27906.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Mondello S, Kobeissy F, et al. (2011). Protein biomarkers for traumatic and ischemic brain injury: from bench to bedside. Transl Stroke Res 2:455–62.
   PubMed Web of Science ®Google Scholar
• Zhuo M, Gorgun MF, Englander EW. (2016). Augmentation of glycolytic metabolism by meclizine is indispensable for protection of dorsal root ganglion neurons from hypoxia-induced mitochondrial compromise. Free Radic Biol Med 99:20–31.
   PubMed Web of Science ®Google Scholar
• Zhuo M, Gorgun MF, Englander EW. (2017). Translesion synthesis DNA polymerase kappa is indispensable for DNA repair synthesis in cisplatin exposed dorsal root ganglion neurons. Mol Neurobiol. [Epub ahead of print]. DOI:10.1007/s12035-017-0507-5
   Web of Science ®Google Scholar
• Zikria BA, Budd DC, Floch F, Ferrer JM. (1975). What is clinical smoke poisoning?. Ann Surg 181:151–6.
   PubMed Web of Science ®Google Scholar
• Zimmermann J, Emrich M, Krauthausen M, et al. (2017). IL-17A promotes granulocyte infiltration, myelin loss, microglia activation, and behavioral deficits during cuprizone-induced demyelination. Mol Neurobiol. [Epub ahead of print]. DOI:10.1007/s12035-016-0368-3
   Web of Science ®Google Scholar
• Zou YY, Kan EM, Cao Q, et al. (2013). Combustion smoke-induced inflammation in the cerebellum and hippocampus of adult rats. Neuropathol Appl Neurobiol 39:531–52.
   PubMed Web of Science ®Google Scholar
• Zou YY, Yuan Y, Kan EM, et al. (2014). Combustion smoke-induced inflammation in the olfactory bulb of adult rats. J Neuroinflammation 11:176.
   PubMed Web of Science ®Google Scholar