Inflammation in Traumatic Brain Injury: Roles for Toxic A1 Astrocytes and Microglial–Astrocytic Crosstalk (original) (raw)
References
Johnson VE, Stewart W, Arena JD, Smith DH (2017) Traumatic brain injury as a trigger of neurodegeneration. Adv Neurobiol 15:383–400 ArticlePubMed Google Scholar
Faden AI, Wu J, Stoica BA, Loane DJ (2016) Progressive inflammation-mediated neurodegeneration after traumatic brain or spinal cord injury. Br J Pharmacol 173:681–691 ArticleCASPubMed Google Scholar
Karve IP, Taylor JM, Crack PJ (2016) The contribution of astrocytes and microglia to traumatic brain injury. Br J Pharmacol 173:692–702 ArticleCASPubMed Google Scholar
Fehily B, Fitzgerald M (2017) Repeated mild traumatic brain injury: potential mechanisms of damage. Cell Transplant 26:1131–1155 ArticlePubMedPubMed Central Google Scholar
Sun M, McDonald SJ, Brady RD, O’Brien TJ, Shultz SR (2018) The influence of immunological stressors on traumatic brain injury. Brain Behav Immun 69:618–628 ArticleCASPubMed Google Scholar
Ziebell JM, Morganti-Kossmann MC (2010) Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury. Neurotherapeutics 7:22–30 ArticleCASPubMedPubMed Central Google Scholar
Kelso ML, Gendelman HE (2014) Bridge between neuroimmunity and traumatic brain injury. Curr Pharm Des 20:4284–4298 CASPubMedPubMed Central Google Scholar
Loane DJ, Byrnes KR (2010) Role of microglia in neurotrauma. Neurotherapeutics 7:66–77 ArticleCAS Google Scholar
Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7–35 ArticlePubMed Google Scholar
Barres BA (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60:430–440 ArticleCASPubMed Google Scholar
Verkhratsky A, Zorec R, Rodriguez JJ, Parpura V (2017) Neuroglia: functional paralysis and reactivity in Alzheimer’s disease and other neurodegenerative pathologies. Adv Neurobiol 15:427–449 ArticlePubMed Google Scholar
Bao F, Shultz SR, Hepburn JD, Omana V, Weaver LC, Cain DP, Brown A (2012) A CD11d monoclonal antibody treatment reduces tissue injury and improves neurological outcome after fluid percussion brain injury in rats. J Neurotrauma 29:2375–2392 ArticlePubMed Google Scholar
Webster KM, Wright DK, Sun M, Semple BD, Ozturk E, Stein DG, O’Brien TJ, Shultz SR (2015) Progesterone treatment reduces neuroinflammation, oxidative stress and brain damage and improves long-term outcomes in a rat model of repeated mild traumatic brain injury. J Neuroinflamm 12:238 ArticleCAS Google Scholar
Shultz SR, Sun M, Wright DK, Brady RD, Liu S, Beynon S, Schmidt SF, Kaye AH, Hamilton JA, O’Brien TJ, Grills BL, McDonald SJ (2015) Tibial fracture exacerbates traumatic brain injury outcomes and neuroinflammation in a novel mouse model of multitrauma. J Cereb Blood Flow Metab 35:1339–1347 ArticlePubMedPubMed Central Google Scholar
Webster KM, Sun M, Crack P, O’Brien TJ, Shultz SR, Semple BD (2017) Inflammation in epileptogenesis after traumatic brain injury. J Neuroinflamm 14:10 ArticleCAS Google Scholar
Cafferty WB, Yang SH, Duffy PJ, Li S, Strittmatter SM (2007) Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J Neurosci 27:2176–2185 ArticleCASPubMedPubMed Central Google Scholar
Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20:570–577 ArticleCASPubMed Google Scholar
Anderson MA, Burda JE, Ren Y, Ao Y, O’Shea TM, Kawaguchi R, Coppola G, Khakh BS, Deming TJ, Sofroniew MV (2016) Astrocyte scar formation aids central nervous system axon regeneration. Nature 532:195–200 ArticleCASPubMedPubMed Central Google Scholar
Liddelow SA, Guttenplan KA, Clarke LE, Bennett FC, Bohlen CJ, Schirmer L, Bennett ML, Münch AE, Chung WS, Peterson TC, Wilton DK, Frouin A, Napier BA, Panicker N, Kumar M, Buckwalter MS, Rowitch DH, Dawson VL, Dawson TM, Stevens B, Barres BA (2017) Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541:481–487 ArticleCASPubMedPubMed Central Google Scholar
Sewell DL, Nacewicz B, Liu F, Macvilay S, Erdei A, Lambris JD, Sandor M, Fabry Z (2004) Complement C3 and C5 play critical roles in traumatic brain cryoinjury: blocking effects on neutrophil extravasation by C5a receptor antagonist. J Neuroimmunol 155:55–63 ArticleCASPubMedPubMed Central Google Scholar
Loane DJ, Kumar A (2016) Microglia in the TBI brain: the good, the bad, and the dysregulated. Exp Neurol 275:316–327 ArticleCASPubMed Google Scholar
Kumar A, Alvarez-Croda DM, Stoica BA, Faden AI, Loane DJ (2016) Microglial/macrophage polarization dynamics following traumatic brain injury. J Neurotrauma 33:1732–1750 ArticlePubMedPubMed Central Google Scholar
Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312–318 ArticleCASPubMed Google Scholar
Hanisch UK, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387–1394 ArticleCASPubMed Google Scholar
Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, Barres BA (2012) Genomic analysis of reactive astrogliosis. J Neurosci 32:6391–6410 ArticleCASPubMedPubMed Central Google Scholar
Natale JE, Ahmed F, Cernak I, Stoica B, Faden AI (2003) Gene expression profile changes are commonly modulated across models and species after traumatic brain injury. J Neurotrauma 20:907–927 ArticlePubMed Google Scholar
Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, Yefanov A, Lee H, Zhang N, Robertson CL, Serova N, Davis S, Soboleva A (2013) NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res 41:D991–D995 ArticleCASPubMed Google Scholar
Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics 19:185–193 ArticleCASPubMed Google Scholar
RStudio Team (2015) RStudio: integrated development for R. RStudio, Inc., Boston Google Scholar
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York Book Google Scholar
Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12:996–1006 ArticleCASPubMedPubMed Central Google Scholar
Shultz SR, Cardamone L, Liu YR, Hogan RE, Maccotta L, Wright DK, Zheng P, Koe A, Gregoire MC, Williams JP, Hicks RJ, Jones NC, Myers DE, O’Brien TJ, Bouilleret V (2013) Can structural or functional changes following traumatic brain injury in the rat predict epileptic outcome? Epilepsia 54:1240–1250 ArticlePubMedPubMed Central Google Scholar
Johnstone VP, Wright DK, Wong KK, O’Brien TJ, Rajan R, Shultz S (2015) Experimental traumatic brain injury results in long-term recovery of functional responsiveness in sensory cortex but persisting structural changes and sensorimotor, cognitive, and emotional deficits. J Neurotrauma 32:1333–1346 ArticlePubMed Google Scholar
Wright DK, Liu S, van der Poel C, McDonald SJ, Brady RD, Taylor L, Yang L, Gardner AJ, Ordidge R, O’Brien TJ, Johnston LA, Shultz SR (2017) Traumatic brain injury results in cellular, structural and functional changes resembling motor neuron disease. Cereb Cortex 27:4503–4515 PubMed Google Scholar
Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press, San Diego Google Scholar
Ziebell JM, Taylor SE, Cao T, Harrison JL, Lifshitz J (2012) Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury. J Neuroinflamm 9:247 Article Google Scholar
Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263 ArticleCASPubMed Google Scholar
Lenz KM, Nelson LH (2018) Microglia and beyond: innate immune cells as regulators of brain development and behavioral function. Front Immunol 9:698 ArticleCASPubMedPubMed Central Google Scholar
Colton CA (2009) Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4:399–418 ArticlePubMedPubMed Central Google Scholar
Ransohoff RM (2016) A polarizing question: do M1 and M2 microglia exist? Nat Neurosci 19:987–991 ArticleCASPubMed Google Scholar
Keren-Shaul H, Spinrad A, Weiner A, Matcovitch-Natan O, Dvir-Szternfeld R, Ulland TK, David E, Baruch K, Lara-Astaiso D, Toth B, Itzkovitz S, Colonna M, Schwartz M, Amit I (2017) A unique microglia type associated with restricting development of Alzheimer’s disease. Cell 169:1276–1290 ArticleCASPubMed Google Scholar
Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16:1896–1905 ArticleCASPubMedPubMed Central Google Scholar
Deczkowska A, Keren-Shaul H, Weiner A, Colonna M, Schwartz M, Amit I (2018) Disease-associated microglia: a universal immune sensor of neurodegeneration. Cell 173:1073–1081 ArticleCASPubMed Google Scholar
Grabert K, Michoel T, Karavolos MH, Clohisey S, Baillie JK, Stevens MP, Freeman TC, Summers KM, McColl BW (2016) Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat Neurosci 19:504–516 ArticleCASPubMedPubMed Central Google Scholar
Jassam YN, Izzy S, Whalen M, McGavern DB, El Khoury J (2017) Neuroimmunology of traumatic brain injury: time for a paradigm shift. Neuron 95:1246–1265 ArticleCASPubMedPubMed Central Google Scholar
Ramlackhansingh AF, Brooks DJ, Greenwood RJ, Bose SK, Turkheimer FE, Kinnunen KM, Gentleman S, Heckemann RA, Gunanayagam K, Gelosa G, Sharp DJ (2011) Inflammation after trauma: microglial activation and traumatic brain injury. Ann Neurol 70:374–383 ArticlePubMed Google Scholar
Fourgeaud L, Través PG, Tufail Y, Leal-Bailey H, Lew ED, Burrola PG, Callaway P, Zagórska A, Rothlin CV, Nimmerjahn A, Lemke G (2016) TAM receptors regulate multiple features of microglial physiology. Nature 532:240–244 ArticleCASPubMedPubMed Central Google Scholar
Roth TL, Nayak D, Atanasijevic T, Koretsky AP, Latour LL, McGavern DB (2014) Transcranial amelioration of inflammation and cell death after brain injury. Nature 505:223–228 ArticleCASPubMed Google Scholar
Shitaka Y, Tran HT, Bennett RE, Sanchez L, Levy MA, Dikranian K, Brody DL (2011) Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J Neuropathol Exp Neurol 70:551–567 ArticlePubMed Google Scholar
Mannix R, Meehan WP, Mandeville J, Grant PE, Gray T, Berglass J, Zhang J, Bryant J, Rezaie S, Chung JY, Peters NV, Lee C, Tien LW, Kaplan DL, Feany M, Whalen M (2013) Clinical correlates in an experimental model of repetitive mild brain injury. Ann Neurol 74:65–75 ArticlePubMedPubMed Central Google Scholar
Meng Q, Zhuang Y, Ying Z, Agrawal R, Yang X, Gomez-Pinilla F (2017) Traumatic brain injury induces genome-wide transcriptomic, methylomic, and network perturbations in brain and blood predicting neurological disorders. EBioMedicine 16:184–194 ArticlePubMedPubMed Central Google Scholar
Chiu CC, Liao YE, Yang LY, Wang JY, Tweedie D, Karnati HK, Greig NH, Wang JY (2016) Neuroinflammation in animal models of traumatic brain injury. J Neurosci Methods 272:49 Article Google Scholar
Bouvier DS, Murai KK (2015) Synergistic actions of microglia and astrocytes in the progression of Alzheimer’s disease. J Alzheimers Dis 45:1001–1014 ArticlePubMed Google Scholar
Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752–758 ArticleCASPubMed Google Scholar
Kim JV, Dustin ML (2006) Innate response to focal necrotic injury inside the blood-brain barrier. J Immunol 177:5269–5277 ArticleCASPubMed Google Scholar
Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143–2155 ArticleCASPubMedPubMed Central Google Scholar
Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, Korsak RA, Takeda K, Akira S, Sofroniew MV (2008) STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28:7231–7243 ArticleCASPubMedPubMed Central Google Scholar
Boisvert MM, Erikson GA, Shokhirev MN, Allen NJ (2018) The aging astrocyte transcriptome from multiple regions of the mouse brain. Cell Rep 22:269–285 ArticleCASPubMedPubMed Central Google Scholar
Clarke LE, Liddelow SA, Chakraborty C, Münch AE, Heiman M, Barres BA (2018) Normal aging induces A1-like astrocyte reactivity. Proc Natl Acad Sci USA 115:E1896–E1905 ArticleCASPubMedPubMed Central Google Scholar
Yun SP, Kam TI, Panicker N, Kim S, Oh Y, Park JS, Kwon SH, Park YJ, Karuppagounder SS, Park H, Kim S, Oh N, Kim NA, Lee S, Brahmachari S, Mao X, Lee JH, Kumar M, An D, Kang SU, Lee Y, Lee KC, Na DH, Kim D, Lee SH, Roschke VV, Liddelow SA, Mari Z, Barres BA, Dawson VL, Lee S, Dawson TM, Ko HS (2018) Block of A1 astrocyte conversion by microglia is neuroprotective in models of Parkinson’s disease. Nat Med 24:931–938 ArticleCASPubMedPubMed Central Google Scholar
Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208–215 ArticleCASPubMed Google Scholar
Beart PM, O’Shea RD (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol 150:5–17 ArticleCASPubMed Google Scholar
Martinez-Lozada Z, Guillem AM, Robinson MB (2016) Transcriptional regulation of glutamate transporters: from extracellular signals to transcription factors. Adv Pharmacol 76:103–145 ArticleCASPubMedPubMed Central Google Scholar
Panickar KS, Norenberg MD (2005) Astrocytes in cerebral ischemic injury: morphological and general considerations. Glia 50:287–298 ArticlePubMed Google Scholar
Schipke CG, Boucsein C, Ohlemeyer C, Kirchhoff F, Kettenmann H (2002) Astrocyte Ca2+ waves trigger responses in microglial cells in brain slices. FASEB J 16:255–257 ArticleCASPubMed Google Scholar
Verderio C, Matteoli M (2001) ATP mediates calcium signaling between astrocytes and microglial cells: modulation by IFN-gamma. J Immunol 166:6383–6391 ArticleCASPubMed Google Scholar
Norden DM, Fenn AM, Dugan A, Godbout JP (2014) TGFß produced by IL-10 redirected astrocytes attenuates microglial activation. Glia 62:881–895 ArticlePubMedPubMed Central Google Scholar
Li L, Lundkvist A, Andersson D, Wilhelmsson U, Nagai N, Pardo AC, Nodin C, Ståhlberg A, Aprico K, Larsson K, Yabe T, Moons L, Fotheringham A, Davies I, Carmeliet P, Schwartz JP, Pekna M, Kubista M, Blomstrand F, Maragakis N, Nilsson M, Pekny M (2008) Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab 28:468–481 ArticleCASPubMed Google Scholar
Abeysinghe HC, Phillips EL, Chin-Cheng H, Beart PM, Roulston CL (2016) Modulating astrocyte transition after stroke to promote brain rescue and functional recovery: emerging targets include rho kinase. Int J Mol Sci 17:288–305 ArticleCASPubMedPubMed Central Google Scholar