The DOI matches its Crossref record; 16 of the 16 references it cites were found in a registry or an index.
Cognitive deficits develop 1 month after diffuse brain injury and are exaggerated by microglia-associated reactivity to peripheral immune challenge
Open accessAbstract
Traumatic brain injury (TBI) elicits immediate neuroinflammatory events that contribute to acute cognitive, motor, and affective disturbance. Despite resolution of these acute complications, significant neuropsychiatric and cognitive issues can develop and progress after TBI. We and others have provided novel evidence that these complications are potentiated by repeated injuries, immune challenges and stressors. A key component to this may be increased sensitization or priming of glia after TBI. Therefore, our objectives were to determine the degree to which cognitive deterioration occurred after diffuse TBI (moderate midline fluid percussion injury) and ascertain if glial reactivity induced by an acute immune challenge potentiated cognitive decline 30 days post injury (dpi). In post-recovery assessments, hippocampal-dependent learning and memory recall were normal 7 dpi, but anterograde learning was impaired by 30 dpi. Examination of mRNA and morphological profiles of glia 30 dpi indicated a low but persistent level of inflammation with elevated expression of GFAP and IL-1β in astrocytes and MHCII and IL-1β in microglia. Moreover, an acute immune challenge 30 dpi robustly interrupted memory consolidation specifically in TBI mice. These deficits were associated with exaggerated microglia-mediated inflammation with amplified (IL-1β, CCL2, TNFα) and prolonged (TNFα) cytokine/chemokine expression, and a marked reactive morphological profile of microglia in the CA3 of the hippocampus. Collectively, these data indicate that microglia remain sensitized 30 dpi after moderate TBI and a secondary inflammatory challenge elicits robust microglial reactivity that augments cognitive decline. Statement of significance Traumatic brain injury (TBI) is a major risk factor in development of neuropsychiatric problems long after injury, negatively affecting quality of life. Mounting evidence indicates that inflammatory processes worsen with time after a brain injury and are likely mediated by glia. Here, we show that primed microglia and astrocytes developed in mice 1 month following moderate diffuse TBI, coinciding with cognitive deficits that were not initially evident after injury. Additionally, TBI-induced glial priming may adversely affect the ability of glia to appropriately respond to immune challenges, which occur regularly across the lifespan. Indeed, we show that an acute immune challenge augmented microglial reactivity and cognitive deficits. This idea may provide new avenues of clinical assessments and treatments following TBI.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Recent data demonstrate that TBI induces a primed microglial phenotype, defined by altered morphology and increased expression of MHC-II and CD68 (204, 208).”
From The Inflammatory Continuum of Traumatic Brain Injury and Alzheimer’s Disease (2018) · cites this paper as [208]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011) · Nature · doi:10.1038/nature09817 · Cited by 1,567
Inflammation after trauma: Microglial activation and traumatic brain injury
Ramlackhansingh, A. F., Brooks, D. J., Greenwood, R. J., Bose, S. K., Turkheimer, F. E., Kinnunen, K. M., Gentleman, S., Heckemann, R. A., Gunanayagam, K., Gelosa, G., et al. (2011) · Annals of Neurology · doi:10.1002/ana.22455 · Cited by 999
Godbout, J. P., Chen, J., Abraham, J., Richwine, A. F., Berg, B. M., Kelley, K. W., & Johnson, R. W. (2005) · The FASEB Journal · doi:10.1096/fj.05-3776fje · Cited by 813
Self-citationHenry, C. J., Huang, Y., Wynne, A. M., & Godbout, J. P. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.09.002 · Cited by 565
Self-citationLoane, D. J., Kumar, A., Stoica, B. A., Cabatbat, R., & Faden, A. I. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000021 · Cited by 498
Cunningham, A. J., Murray, C. A., O'Neill, L. A. J., Lynch, M. A., & O'Connor, J. J. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(95)12252-4 · Cited by 433
Norden, D. M., Muccigrosso, M. M., & Godbout, J. P. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.10.028 · Cited by 413
Self-citationSemple, B. D., Bye, N., Rancan, M., Ziebell, J. M., & Morganti-Kossmann, M. C. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.262 · Cited by 358
Experimental models of traumatic brain injury: do we really need to build a better mousetrap?
Morales, D. M., Marklund, N., Lebold, D., Thompson, H. J., Pitkanen, A., Maxwell, W. L., Longhi, L., Laurer, H., Maegele, M., Neugebauer, E., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.030 · Cited by 339
TGFβ produced by IL‐10 redirected astrocytes attenuates microglial activation
Norden, D. M., Fenn, A. M., Dugan, A., & Godbout, J. P. (2014) · Glia · doi:10.1002/glia.22647 · Cited by 332
Self-citation
Research works printed but not linked: 52
- Almeida, 2015, Prevalence, associated factors, mood and cognitive outcomes of traumatic brain injury in later life: the health in men study (HIMS), Int. J. Geriatr. Psychiatry, 10.1002/gps.4276 · DOI
- Bach, 1995, Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency, Cell, 81, 905, 10.1016/0092-8674(95)90010-1 · DOI
- Bachstetter, 2013, The p38alpha MAPK regulates microglial responsiveness to diffuse traumatic brain injury, J. Neurosci., 33, 6143, 10.1523/JNEUROSCI.5399-12.2013 · DOI
- Bao, 2012, A CD11d monoclonal antibody treatment reduces tissue injury and improves neurological outcome after fluid percussion brain injury in rats, J. Neurotrauma, 29, 2375, 10.1089/neu.2012.2408 · DOI
- Barrientos, 2010, Memory impairments in healthy aging: role of aging-induced microglial sensitization, Aging Dis., 1, 212
- Barrientos, 2009, Characterization of the sickness response in young and aging rats following E. coli infection, Brain Behav. Immun., 23, 450, 10.1016/j.bbi.2009.01.016 · DOI
- Battista, 2006, Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus, Eur. J. Neurosci., 23, 83, 10.1111/j.1460-9568.2005.04539.x · DOI · Paper page
- Ben Menachem-Zidon, 2011, Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling, Brain Behav. Immun., 25, 1008, 10.1016/j.bbi.2010.11.007 · DOI
- Berg, 2004, Alpha-tocopherol attenuates lipopolysaccharide-induced sickness behavior in mice, Brain Behav. Immun., 18, 149, 10.1016/S0889-1591(03)00113-2 · DOI
- Briones, 2013, Decreased neuroinflammation and increased brain energy homeostasis following environmental enrichment after mild traumatic brain injury is associated with improvement in cognitive function, Acta Neuropathol. Commun., 1, 57, 10.1186/2051-5960-1-57 · DOI
- Brooks, 2000, Metabolic and cognitive response to human traumatic brain injury: a quantitative proton magnetic resonance study, J. Neurotrauma, 17, 629, 10.1089/089771500415382 · DOI
- Cavaglia, 2001, Regional variation in brain capillary density and vascular response to ischemia, Brain Res., 910, 81, 10.1016/S0006-8993(01)02637-3 · DOI
- Chen, 2008, Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system, Brain Behav. Immun., 22, 301, 10.1016/j.bbi.2007.08.014 · DOI
- Donnelly, 2009, An efficient and reproducible method for quantifying macrophages in different experimental models of central nervous system pathology, J. Neurosci. Methods, 181, 36, 10.1016/j.jneumeth.2009.04.010 · DOI
- Fenn, 2014, Immune activation promotes depression 1month after diffuse brain injury: a role for primed microglia, Biol. Psychiatry, 76, 575, 10.1016/j.biopsych.2013.10.014 · DOI · Paper page
- Fenn, 2015, Methylene blue attenuates traumatic brain injury-associated neuroinflammation and acute depressive-like behavior in mice, J. Neurotrauma, 32, 127, 10.1089/neu.2014.3514 · DOI
- Hart, 2012, A longitudinal study of major and minor depression following traumatic brain injury, Arch. Phys. Med. Rehabil., 93, 1343, 10.1016/j.apmr.2012.03.036 · DOI
- Hazra, 2014, Delayed thalamic astrocytosis and disrupted sleep-wake patterns in a preclinical model of traumatic brain injury, J. Neurosci. Res., 92, 1434, 10.1002/jnr.23430 · DOI · Paper page
- Himanen, 2006, Longitudinal cognitive changes in traumatic brain injury: a 30-year follow-up study, Neurology, 66, 187, 10.1212/01.wnl.0000194264.60150.d3 · DOI
- Hsieh, 2014, CCR2 deficiency impairs macrophage infiltration and improves cognitive function after traumatic brain injury, J. Neurotrauma, 31, 1677, 10.1089/neu.2013.3252 · DOI · Paper page
- Hylin, 2013, Behavioral and histopathological alterations resulting from mild fluid percussion injury, J. Neurotrauma, 30, 702, 10.1089/neu.2012.2630 · DOI
- Jo, 2014, GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease, Nat. Med., 20, 886, 10.1038/nm.3639 · DOI · Paper page
- Johnson, 2015, Strategies to improve quantitative assessment of immunohistochemical and immunofluorescence labelling, Sci. Rep., 10.1038/srep10607 · DOI
- Kabadi, 2014, CR8, a novel inhibitor of CDK, limits microglial activation, astrocytosis, neuronal loss, and neurologic dysfunction after experimental traumatic brain injury, J. Cereb. Blood Flow Metab., 34, 502, 10.1038/jcbfm.2013.228 · DOI
- Kelley, 2006, Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration, Exp. Neurol., 198, 350, 10.1016/j.expneurol.2005.12.017 · DOI
- Kelley, 2007, Neuroinflammatory responses after experimental diffuse traumatic brain injury, J. Neuropathol. Exp. Neurol., 66, 989, 10.1097/NEN.0b013e3181588245 · DOI
- Kongsui, 2014, Chronic stress induces prolonged suppression of the P2X7 receptor within multiple regions of the hippocampus: a cumulative threshold spectra analysis, Brain Behav. Immun., 42, 69, 10.1016/j.bbi.2014.05.017 · DOI · Paper page
- Kongsui, 2014, Quantitative assessment of microglial morphology and density reveals remarkable consistency in the distribution and morphology of cells within the healthy prefrontal cortex of the rat, J. Neuroinflammation, 11, 182, 10.1186/s12974-014-0182-7 · DOI
- Lifshitz, J., 2009 Fluid percussion injury model. In: Chen, J., Xu, Z.C., Xu, X.-M., Zhang, J.H. (Eds.), Animal Models of Acute Neurological Injuries, p. 369. · DOI
- Lifshitz, 2007, Acute cognitive impairment after lateral fluid percussion brain injury recovers by 1month: evaluation by conditioned fear response, Behav. Brain Res., 177, 347, 10.1016/j.bbr.2006.11.014 · DOI
- Millis, 2001, Long-term neuropsychological outcome after traumatic brain injury, J. Head Trauma Rehabil., 16, 343, 10.1097/00001199-200108000-00005 · DOI
- Molofsky, 2012, Astrocytes and disease: a neurodevelopmental perspective, Genes Dev., 26, 891, 10.1101/gad.188326.112 · DOI · Paper page
- Mouzon, 2014, Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model, Ann. Neurol., 75, 241, 10.1002/ana.24064 · DOI
- Norden, 2015, Sequential activation of microglia and astrocyte cytokine expression precedes increased iba-1 or GFAP immunoreactivity following systemic immune challenge, Glia
- O’Connor, 2003, Effects of daily versus weekly testing and pre-training on the assessment of neurologic impairment following diffuse traumatic brain injury in rats, J. Neurotrauma, 20, 985, 10.1089/089771503770195830 · DOI
- Rosenthal, 1998, Depression following traumatic brain injury, Arch. Phys. Med. Rehabil., 79, 90, 10.1016/S0003-9993(98)90215-5 · DOI
- Ruff, 1991, Verbal-learning deficits following severe head-injury – heterogeneity in recovery over 1year, J. Neurosurg., 75, S50, 10.3171/sup.1991.75.1s.0s50 · DOI
- Sahinkaya, 2014, Changes in NG2 cells and oligodendrocytes in a new model of intraspinal hemorrhage, Exp. Neurol., 255, 113, 10.1016/j.expneurol.2014.02.025 · DOI
- Salmond, 2006, Changes over time in cognitive and structural profiles of head injury survivors, Neuropsychologia, 44, 1995, 10.1016/j.neuropsychologia.2006.03.013 · DOI
- Till, 2008, Postrecovery cognitive decline in adults with traumatic brain injury, Arch. Phys. Med. Rehabil., 89, S25, 10.1016/j.apmr.2008.07.004 · DOI
- Tobinick, 2012, Selective TNF inhibition for chronic stroke and traumatic brain injury: an observational study involving 629 consecutive patients treated with perispinal etanercept, CNS Drugs, 26, 1051, 10.1007/s40263-012-0013-2 · DOI
- Valero, 2014, Long-term effects of an acute and systemic administration of LPS on adult neurogenesis and spatial memory, Front. Neurosci., 8, 83, 10.3389/fnins.2014.00083 · DOI
- Walker, 2014, Dynamic structural remodelling of microglia in health and disease: a review of the models, the signals and the mechanisms, Brain Behav. Immun., 37, 1, 10.1016/j.bbi.2013.12.010 · DOI
- Wang, 2011, Fluoxetine increases hippocampal neurogenesis and induces epigenetic factors but does not improve functional recovery after traumatic brain injury, J. Neurotrauma, 28, 259, 10.1089/neu.2010.1648 · DOI
- Weil, 2014, Injury timing alters metabolic, inflammatory and functional outcomes following repeated mild traumatic brain injury, Neurobiol. Dis., 70, 108, 10.1016/j.nbd.2014.06.016 · DOI
- Whiting, 2008, Mechanisms of anterograde and retrograde memory impairment following experimental traumatic brain injury, Brain Res., 1213, 69, 10.1016/j.brainres.2008.01.107 · DOI
- Witcher, 2015, Priming the inflammatory pump of the CNS after traumatic brain injury, Trends Neurosci., 38, 609, 10.1016/j.tins.2015.08.002 · DOI
- Witgen, 2006, Inbred mouse strains as a tool to analyze hippocampal neuronal loss after brain injury: a stereological study, J. Neurotrauma, 23, 1320, 10.1089/neu.2006.23.1320 · DOI
- Wohleb, 2012, Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice, Psychoneuroendocrinology, 37, 1491, 10.1016/j.psyneuen.2012.02.003 · DOI · Paper page
- Wohleb, 2014, Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain, Biol. Psychiatry, 75, 970, 10.1016/j.biopsych.2013.11.029 · DOI · Paper page
- Wohleb, 2013, Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior, J. Neurosci., 33, 13820, 10.1523/JNEUROSCI.1671-13.2013 · DOI · Paper page
- Ziebell, 2012, Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury, J. Neuroinflammation, 9, 247, 10.1186/1742-2094-9-247 · DOI
Cited by
Sorted by citations
Neuroinflammation: The Devil Is in the Details
DiSabato, D. J., Quan, N., & Godbout, J. P. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13607 · Cited by 1,640
“Antagonism of the IL-1 receptor at early time points following SCI, and sequestration of TNFa via administration of soluble tumor necrosis factor receptor superfamily member 1A (TNFR1), reduced apoptosis (Nesic et al. 2001; Ferguson et al. 2008).”
Self-citationWitcher, K. G., Bray, C. E., Chunchai, T., Zhao, F., O'Neil, S. M., Gordillo, A. J., Campbell, W. A., McKim, D. B., Liu, X., Dziabis, J. E., et al. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2469-20.2020 · Cited by 387
“…homeostatic processes including synaptic pruning (Schafer et al., 2012), immune surveillance (Nimmerjahn et al., 2005), and debris clearance (Neumann et al., 2009); therefore, chronic disruption of microglial homeostasis may underlie neuropsychiatric complications and neurodegenerative…”
BackgroundSelf-citationEmerging Roles for the Immune System in Traumatic Brain Injury
McKee, C. A., & Lukens, J. R. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00556 · Cited by 277
“org December 2016 | Volume 7 | Article 556 deficits that could be linked to TBI-mediated microglia priming (54).”
BackgroundBrain-gut axis dysfunction in the pathogenesis of traumatic brain injury
Hanscom, M., Loane, D. J., & Shea‐Donohue, T. (2021) · Journal of Clinical Investigation · doi:10.1172/jci143777 · Cited by 245
“Indeed, neuroinflammation is exacerbated by systemic administration of LPS following experimental TBI (74), contributing to a more pronounced TBI-induced cognitive decline (75).”
BackgroundCoughlin, J. M., Wang, Y., Minn, I., Bienko, N., Ambinder, E. B., Xu, X., Peters, M. E., Dougherty, J. W., Vranešić, M., Koo, S. M., et al. (2016) · JAMA Neurology · doi:10.1001/jamaneurol.2016.3764 · Cited by 168
Witcher, K. G., Bray, C. E., Dziabis, J. E., McKim, D. B., Benner, B. N., Rowe, R. K., Kokiko‐Cochran, O. N., Popovich, P. G., Lifshitz, J., Eiferman, D. S., et al. (2018) · Glia · doi:10.1002/glia.23523 · Cited by 153
“Persistent immune-reactivity in the cortex has been previously reported to occur months after TBI in the cortex (Fenn et al., 2014; Muccigrosso et al., 2016).”
BackgroundSelf-citationLannes, N., Eppler, E., Etemad, S., Yotovski, P., & Filgueira, L. (2017) · Oncotarget · doi:10.18632/oncotarget.23106 · Cited by 155
“), or injury in a distal CNS region, may also activate microglia in otherwise healthy tissue and result on a longer term in substantial mental disease or chronic pain [246, 247].”
BackgroundThe Inflammatory Continuum of Traumatic Brain Injury and Alzheimer’s Disease
Kokiko-Cochran, O. N., & Godbout, J. P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00672 · Cited by 128
“This supports other studies showing increased CD68+ microglia in the brains of American football players, which partially mediated coincident tau pathology (231).”
BackgroundInfluentialSelf-citationMicroglia: Key players in neurodevelopment and neuronal plasticity
Sominsky, L., Luca, S. N. D., & Spencer, S. J. (2017) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2017.11.012 · Cited by 155
O’Neil, S. M., Witcher, K. G., McKim, D. B., & Godbout, J. P. (2018) · Acta Neuropathologica Communications · doi:10.1186/s40478-018-0636-8 · Cited by 138
“We and others have reported that primed microglia in models of aging, traumatic brain injury, and stress, exhibit an exaggerated immune-reactive profile after secondary immune challenge [23, 43, 72].”
BackgroundSelf-citationBeyond the Brain: Peripheral Interactions after Traumatic Brain Injury
McDonald, S. J., Sharkey, J. M., Sun, M., Kaukas, L., Shultz, S. R., Turner, R. J., Leonard, A. V., Brady, R. D., & Corrigan, F. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2019.6885 · Cited by 152
“…alter TBI outcome, with LPS injection at 1 month post-TBI found to exacerbate production of inflammatory cytokines and worsen neurological function in mice, 167,168 and administration of LPS at 8 weeks post-TBI found to enhance neuronal excitability and seizure susceptibility at 24 weeks post-TBI.”
Sharma, R., Shultz, S. R., Robinson, M. J., Belli, A., Hibbs, M. L., O'Brien, T. J., & Semple, B. D. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.04.034 · Cited by 140
Time-Dependent Changes in Microglia Transcriptional Networks Following Traumatic Brain Injury
Izzy, S., Liu, Q., Fang, Z., Lule, S., Wu, L., Chung, J. Y., Sarro-Schwartz, A., Brown-Whalen, A., Perner, C., Hickman, S. E., et al. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00307 · Cited by 110
“They are among the first responders to brain injury and their persistent activation in TBI animal models and in humans with TBI may contribute to long-term functional deficits (Gentleman et al., 2004; Coughlin et al., 2015; Witcher et al., 2015; Muccigrosso et al., 2016; Jassam et al., 2017).”
BackgroundThe Role of Iron, Its Metabolism and Ferroptosis in Traumatic Brain Injury
Tang, S., Gao, P., Chen, H., Zhou, X., Ou, Y., & He, Y. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.590789 · Cited by 120
“It is thus necessary to diagnose and treat PTE in a timely manner, which can help patients to improve their quality of life (Castriotta et al., 2007; Muccigrosso et al., 2016).”
BackgroundInflammation in Traumatic Brain Injury
Postolache, T. T., Wadhawan, A., Can, A., Lowry, C. A., Woodbury, M., Makkar, H., Hoisington, A. J., Scott, A. J., Potocki, E., Benros, M. E., et al. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-191150 · Cited by 154
“A primed microglial phenotype, defined by increased expression of MHC-II and CD68 and altered morphology is consistently induced by experimental models of TBI [231, 236].”
Collins-Praino, L. E., & Corrigan, F. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.09.027 · Cited by 95
“TBI animals showed hyper-reactive microglial morphological profiles with an associated increased expression of pro-inflammatory cytokines, including IL-1b, CCL2, and TNFa, which led to an exacerbation of depressive-like behavior and impaired cognition (Fenn et al., 2014; Muccigrosso et al., 2016).”
BackgroundAlzarea, S., & Rahman, S. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.019 · Cited by 75
Savi, F. F., de Oliveira, A. L. R., de Medeiros, G. F., Bozza, F. A., Michels, M., Sharshar, T., Dal‐Pizzol, F., & Ritter, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.005 · Cited by 83
Bao, Z., Fan, L., Zhao, L., Xu, X., Liu, Y., Chao, H., Liu, N., You, Y., Liu, Y., Wang, X., et al. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00222 · Cited by 71
“Frontiers in Molecular Neuroscience | www.frontiersin.org 1 September 2019 | Volume 12 | Article 222 models of experimentally controlled cortical impact (CCI) injury (Li et al., 2013; Muccigrosso et al., 2016).”
BackgroundIn search of antiepileptogenic treatments for post-traumatic epilepsy
Saletti, P. G., Ali, I. Y., Casillas-Espinosa, P. M., Semple, B. D., Lisgaras, C. P., Moshé, S. L., & Galanopoulou, A. S. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.06.017 · Cited by 75
Huuskonen, M., Tuo, Q.-Z., Loppi, S., Dhungana, H., Korhonen, P., McInnes, L. E., Donnelly, P., Grubman, A., Wojciechowski, S., Lejavová, K., et al. (2017) · Neurotherapeutics · doi:10.1007/s13311-016-0504-9 · Cited by 66
Self-citationRisbrough, V. B., Vaughn, M. N., & Friend, S. F. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.11.012 · Cited by 79
Guan, F., Zhou, X., Li, P., Wang, Y., Liu, M., Li, F., Cui, Y., Huang, T., Yao, M., Zhang, Y.-T. Y., et al. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109684 · Cited by 69
Wangler, L. M., & Godbout, J. P. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.08.008 · Cited by 61
Self-citationParaiso, H. C., Kuo, P., Curfman, E. T., Moon, H. J., Sweazey, R. D., Yen, J.-H. J., Chang, F., & Yu, I.-C. I. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1125-5 · Cited by 72
“Systemic inflammation is reported to exacerbate preexisting conditions and accelerate cognitive decline in several models of neurodegeneration including traumatic brain injury and prion disease [52, 53].”
Bidirectional Brain-Systemic Interactions and Outcomes After TBI
Faden, A. I., Barrett, J. P., Stoica, B. A., & Henry, R. J. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.12.004 · Cited by 57
Green, T. R. F., Ortiz, J. B., Wonnacott, S., Williams, R. J., & Rowe, R. K. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00894 · Cited by 68
“Mice that had received a TBI and LPS appeared to have a poorer cognitive outcome, suggesting that microglial priming worsens cognition (Muccigrosso et al., 2016).”
BackgroundLoss of NLRX1 exacerbates neural tissue damage and NF-κB Signaling following brain injury
Theus, M., Brickler, T., Meza, A. L., Coutermarsh-Ott, S. L., Házy, A., Gris, D., & Allen, I. (2017) · Journal of Immunology · doi:10.4049/jimmunol.1700251 · Cited by 54
“Following TBI, microglia in the lesion area undergo proliferation in response to injury and play vital roles in the modulation of secondary injury and recovery (27, 28).”
MethodHanscom, M., Loane, D. J., Aubretch, T., Leser, J. M., Molesworth, K., Hedgekar, N., Ritzel, R. M., Abulwerdi, G. A., Shea‐Donohue, T., & Faden, A. I. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02067-x · Cited by 61
STAT6 mediates the effect of ethanol on neuroinflammatory response in TBI
Heuvel, F. O., Holl, S., Chandrasekar, A., Li, Z., Wang, Y., Rehman, R., Förstner, P., Sinske, D., Palmer, A., Wiesner, D., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.06.019 · Cited by 56
Mollayeva, T., Mollayeva, S., Pacheco, N., D’Souza, A., & Colantonio, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.01.011 · Cited by 56
Microglia dynamics in adolescent traumatic brain injury
Eyolfson, E., Khan, A. C., Mychasiuk, R., & Lohman, A. W. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01994-z · Cited by 68
Sleep Disruption Exacerbates and Prolongs the Inflammatory Response to Traumatic Brain Injury
Tapp, Z. M., Kumar, J. E., Witcher, K. G., Atluri, R. R., Velasquez, J., O’Neil, S. M., Dziabis, J. E., Bray, C. E., Sheridan, J. F., Godbout, J. P., et al. (2020) · Journal of Neurotrauma · doi:10.1089/neu.2020.7010 · Cited by 55
Self-citationIncretin Mimetics as Rational Candidates for the Treatment of Traumatic Brain Injury
Glotfelty, E. J., Delgado, T., Tovar‐y‐Romo, L. B., Luo, Y., Hoffer, B. J., Olson, L., Karlsson, T. E., Mattson, M. P., Harvey, B. K., Tweedie, D., et al. (2019) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.9b00003 · Cited by 48
Doran, S. J., Henry, R. J., Shirey, K. A., Barrett, J. P., Ritzel, R. M., Lai, W., Blanco, J. C. G., Faden, A. I., Vogel, S. N., & Loane, D. J. (2020) · Critical Care Medicine · doi:10.1097/ccm.0000000000004273 · Cited by 61
“In fact, systemic injection of lipopolysaccharide following diffuse TBI in mice exaggerates glial activation and worsens cognitive outcomes (53, 54).”
BackgroundZiebell, J. M., Rowe, R. K., Muccigrosso, M. M., Reddaway, J., Adelson, P. D., Godbout, J. P., & Lifshitz, J. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.03.008 · Cited by 55
Self-citationNeuroimmune Activation Drives Multiple Brain States
Tchessalova, D., Posillico, C. K., & Tronson, N. C. (2018) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00039 · Cited by 52
“…3 August 2018 | Volume 12 | Article 39 priming effects after immune challenge in adults, with changes in microglial and astrocytic function and behavior (Fenn et al., 2014; Norden et al., 2015; Muccigrosso et al., 2016; Liddelow and Barres, 2017; Olivieri et al., 2018; Wendeln et al., 2018).”
BackgroundCollins‐Praino, L. E., Arulsamy, A., Katharesan, V., & Corrigan, F. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.08.035 · Cited by 44
Packer, J. M., Bray, C. E., Beckman, N. B., Wangler, L. M., Davis, A. C., Goodman, E. J., Klingele, N. E., & Godbout, J. P. (2023) · Glia · doi:10.1002/glia.24475 · Cited by 48
“This matches well with previous work that reported astro-gliosis remains 30 dpi following diffuse TBI (mFPI), (Fenn et al., 2014; Muccigrosso et al., 2016) and is dependent on STING (Abdullah et al., 2018).”
BackgroundResultInfluentialSelf-citationAntimicrobial immunity impedes CNS vascular repair following brain injury
Mastorakos, P., Russo, M. V., Zhou, T., Johnson, K. R., & McGavern, D. B. (2021) · Nature Immunology · doi:10.1038/s41590-021-01012-1 · Cited by 44
Glial Fibrillary Acidic Protein: A Biomarker and Drug Target for Alzheimer’s Disease
Ganne, A., Balasubramaniam, M., Griffin, W., Reis, R. S., & Ayyadevara, S. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14071354 · Cited by 40
The influence of immunological stressors on traumatic brain injury
Sun, M., McDonald, S. J., Brady, R. D., O'Brien, T. J., & Shultz, S. R. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.01.007 · Cited by 41
“Mice given a systemic LPS challenge at 1 month post-TBI also had worse cognitive deficits compared to their saline-treated counterparts (Muccigrosso et al., 2016).”
León‐Rodríguez, A., Fernández‐Arjona, M. D. M., Grondona, J. M., Pedraza, C., & López-Ávalos, M. D. (2022) · Scientific Reports · doi:10.1038/s41598-022-15617-5 · Cited by 41
Salmani, H., Hosseini, M., Beheshti, F., Baghcheghi, Y., Sadeghnia, H., Soukhtanloo, M., Shafei, M., & Khazaei, M. (2018) · Life Science · doi:10.1016/j.lfs.2018.04.033 · Cited by 36
Modulation of Neural Networks by Interleukin-1
Nemeth, D. P., & Quan, N. (2020) · Brain Plasticity · doi:10.3233/bpl-200109 · Cited by 46
“In contrast, in models of severe stress [14, 82], brain injury [83, 84], or IL-1 overexpression [85], IL-1 was found to impair memory.”
BackgroundXie, S.-T., Chen, A.-X., Song, B., Fan, J., Li, W., Xing, Z., Peng, S.-Y., Zhang, Q.-P., Dong, L., Yan, C., et al. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.07.027 · Cited by 33
Neuroimmune and neuroinflammation response for traumatic brain injury
Wu, J., Ren, R., Chen, T., Su, L., & Tang, T. (2024) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2024.111066 · Cited by 32
“Also, they found that secondary immune challenge leads to memory and learning impairments (Muccigrosso et al., 2016).”
Sharma, R., Zamani, A., Dill, L. K., Sun, M., Chu, E., Robinson, M. J., O'Brien, T. J., Shultz, S. R., & Semple, B. D. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02114-1 · Cited by 40
“Here, we hypothesized that pediatric TBI and LPS would separately initiate a broad range of immune responses, while in combination, this dual-insult would have additive effects, as has been previously reported in the few studies performed to date in adult animals [17, 24, 59].”
ResultMechanisms of tertiary neurodegeneration after neonatal hypoxic-ischemic brain damage
Levison, S. W., Rocha‐Ferreira, E., Kim, B. H., Hagberg, H., Fleiss, B., Gressèns, P., & Dobrowolski, R. (2021) · Pediatric Medicine · doi:10.21037/pm-20-104 · Cited by 37
“The majority of experimental descriptions of tertiary phase microglial reactivity comes from models of maternal (101-103) or early postnatal life immune activation (104) and from studies of adult traumatic brain injury (91,105,106).”
BackgroundBromberg, C. E., Condon, A. M., Ridgway, S. W., Krishna, G., Garcia-Filion, P. C., Adelson, P. D., Rowe, R. K., & Thomas, T. C. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00946 · Cited by 36
Altered Blood Biomarker Profiles in Athletes with a History of Repetitive Head Impacts
Battista, A. P. D., Rhind, S. G., Richards, D. W., Churchill, N. W., BAKER, A. J., & Hutchison, M. G. (2016) · PLoS ONE · doi:10.1371/journal.pone.0159929 · Cited by 62
“Nevertheless, peripheral blood samples have the potential to provide meaningful information regarding inflammatory processes both in the CNS and periphery in response to brain injury, in a relatively cost-effective, non-invasive manner [18,30,31].”
BackgroundResultPerispinal Delivery of CNS Drugs
Tobinick, E. L. (2016) · CNS Drugs · doi:10.1007/s40263-016-0339-2 · Cited by 31
“These new findings and accumulating evidence of the central involvement of neuroinflammatory mechanisms in brain disorders challenge existing dogma regarding brain physiology, support the rapid neurological effects seen following PSE administration, and underscore the importance of further research exploring CNS deliv…”
BackgroundDeplete and repeat: microglial CSF1R inhibition and traumatic brain injury
Boland, R., & Kokiko‐Cochran, O. N. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1352790 · Cited by 32
Lu, X., Xue, Z.-Y., Yu, Q., Wei, S., Qiao, Y., Zhang, W., & Lü, H. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.945851 · Cited by 29
“The model of preterm rats with cognitive impairment was established as described previously (Muccigrosso et al., 2016).”
MethodZhang, L., Zhang, D., Zheng, W., Hu, J.-S., Fu, L., Li, Y., Xin, Y., & Wang, X. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113683 · Cited by 32
Packer, J. M., Giammo, S. G., Wangler, L. M., Davis, A. C., Bray, C. E., & Godbout, J. P. (2025) · Journal of Neuroinflammation · doi:10.1186/s12974-025-03451-1 · Cited by 31
“C. influence microglial proliferation [11, 39].”
Self-citationAbd‐El‐Basset, E. M., Rao, M. S. R., & Alsaqobi, A. K. (2020) · Neuroscience Insights · doi:10.1177/2633105520947081 · Cited by 30
Traumatic Brain Injury and Suicidal Behavior: A Review
Wadhawan, A., Stiller, J. W., Potocki, E., Okusaga, O. O., Dagdag, A., Lowry, C. A., Benros, M. E., & Postolache, T. T. (2019) · Journal of Alzheimer s Disease · doi:10.3233/jad-181055 · Cited by 40
A negative allosteric modulator of PDE4D enhances learning after traumatic brain injury
Titus, D. J., Wilson, N. M., Alcazar, O., Calixte, D. A., Dietrich, W. D., Gurney, M. E., & Atkins, C. M. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.12.008 · Cited by 29
The Role of Microglia in the Etiology and Evolution of Chronic Traumatic Encephalopathy
Makinde, H. M., Just, T. B., Cuda, C. M., Perlman, H., & Schwulst, S. J. (2017) · Shock · doi:10.1097/shk.0000000000000859 · Cited by 24
“That is, primed microglia from an initial injury may respond in an amplified manner to subsequent insults, even if milder in nature (70, 71).”
de la Tremblaye, P. B., O’Neil, D. A., LaPorte, M. J., B, J. P. C. A., Beitchman, J. A., Thomas, T. C., Bondi, C. O., & Kline, A. E. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.05.022 · Cited by 25
“Muccigrosso et al. (2016) measured cognitive deficits at one month following midline FP injury in adult male BALB/C mice using the Barnes maze.”
Ovariectomy in mice primes hippocampal microglia to exacerbate behavioral sickness responses
Sanchez, K. G., Wu, S. L., Kakkar, R., Darling, J. S., Harper, C., & Fonken, L. K. (2023) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2023.100638 · Cited by 16
“For example, traumatic brain injury can modulate the neuroimmune system and cause marked behavioral changes reminiscent of the aforementioned sickness behaviors (Muccigrosso et al., 2016; Niraula et al., 2017; Tapp et al., 2019).”
BackgroundFernández‐Arjona, M. D. M., León‐Rodríguez, A., Grondona, J. M., & López-Ávalos, M. D. (2022) · Glia · doi:10.1002/glia.24217 · Cited by 28
“MHC II has been reported as a marker of primed microglia (Ling et al., 2004; Muccigrosso et al., 2016) which, in non-injured rats, is expressed by an increasing proportion of hippocampal microglial cells during aging progression (VanGuilder et al., 2011).”
BackgroundInfluentialYamakawa, G. R., Brady, R. D., Sun, M., McDonald, S. J., Shultz, S. R., & Mychasiuk, R. (2020) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2020.100058 · Cited by 27
“The P55 or TNFR1 receptor is ubiquitously expressed at low levels in ependymal walls, the arcuate, supraoptic nucleus, and cerebellum (Nadeau and Rivest, 1999).”
BackgroundWang, Y., Wei, Y., Oguntayo, S., Wilder, D. M., Tong, L. C., Su, Y., Gist, I. D., Arun, P., & Long, J. B. (2016) · Journal of Neurotrauma · doi:10.1089/neu.2016.4465 · Cited by 20
Wang, H., Huang, Q., Zhang, Z., Ji, J., Sun, T., & Wang, D. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02535-6 · Cited by 20
“Previous studies have found that LPS stimulation promotes the inflammatory response of microglia in TBI mice and increases the risk of depression-like behavior and cognitive impairment [24, 25], and therefore drove the important effects of subsequent systemic immune activation, induced by post-injury infection, on the…”
BackgroundGreen, T. R. F., Murphy, S. M., Ortiz, J. B., & Rowe, R. K. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.804139 · Cited by 26
Long COVID in Children: A Multidisciplinary Review
Sansone, F., Pellegrino, G. M., Caronni, A., Bonazza, F., Vegni, E. A. M., Luè, A., Bocci, T., Pipolo, C., Giusti, G., Filippo, P. D., et al. (2023) · Diagnostics · doi:10.3390/diagnostics13121990 · Cited by 24
Huo, X., Xu, X., Li, M., Xiao, L., Wang, Y., Li, W., Wang, C., & Sun, T. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1001363 · Cited by 22
“PTE following TBI may further exacerbate the effects of TBI on memory and cognition, damage the cerebrovascular system or blood-brain barrier, and lead to depression or post-traumatic stress disorder (Castriotta et al., 2007; Luo et al., 2014; Muccigrosso et al., 2016; Vos et al., 2018).”
BackgroundInfluentialXue, W.-K., Zhao, W.-J., Meng, X.-F., Shen, H.-F., & Huang, P.-Z. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.12.002 · Cited by 18
Bai, R., Gao, H., Han, Z., Ge, X.-T., Huang, S., Chen, F.-L., & Lei, P. (2017) · Medical Science Monitor · doi:10.12659/msm.901124 · Cited by 17
“We carried out FCM to show that microglia strongly infiltrated the brain in the entire phase, with an initial peak of CD206+/CD11b+ M2-like microglia at 1 week and a secondary peak of CD86+/CD11b+ M1like microglia at 4 weeks, which is consistent with results of a previous study [27].”
ResultTargeting Kv1.3 channels to reduce white matter pathology after traumatic brain injury
Reeves, T. M., Trimmer, P., Colley, B. S., & Phillips, L. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.06.011 · Cited by 17
“…become apoptotic following CFZ administration (Fukutomi et al., 2011), which, with TBI, could reduce the number of activated inflammatory macrophages available to infiltrate injured white matter (Hsieh et al., 2014; Muccigrosso et al., 2016; Semple et al., 2010; Szmydynger-Chodobska et al., 2011).”
Epigenetic and 3D genome reprogramming during the aging of human hippocampus
Zemke, N. R., Lee, S., Mamde, S., Yang, B., Berchtold, N. C., Garduño, B. M., Indralingam, H. S., Bartosik, W. M., Lau, P., Dong, K., et al. (2024) · bioRxiv · doi:10.1101/2024.10.14.618338 · Cited by 16
Traumatic Brain Injury and Immunological Outcomes: the double-edged Killer
Datta, S., Lin, F., Jones, L., Pingle, S. C., Kesari, S., & Ashili, S. (2023) · Future Science OA · doi:10.2144/fsoa-2023-0037 · Cited by 15
Hosseini, M., Salmani, H., & Baghcheghi, Y. (2021) · Physiological Reports · doi:10.14814/phy2.14874 · Cited by 16
“This time point (72 h after the LPS injection) was chosen since the acute effects of LPS have been shown to diminish at this time point (Godbout et al., 2008; Muccigrosso et al., 2016),”
MethodInfluentialClausen, F., Hansson, H., Raud, J., & Marklund, N. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00039 · Cited by 15
“(51-2700) Axonal deposits Life technologies 1:200”
Taylor, M. A., & Kokiko‐Cochran, O. N. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1351685 · Cited by 15
Brett, B. L., Savitz, J. B., Nitta, M. E., España, L. Y., Teague, T. K., Nelson, L. D., McCrea, M., & Meier, T. B. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.07.024 · Cited by 21
“There is also evidence that chronic inflammation can change the reactive state of immune cells, sensitizing or “priming” the immune system to react more strongly to additional inflammatory triggers (Dilger and Johnson, 2008; Muccigrosso et al., 2016).”
BackgroundMollayeva, T., Pacheco, N., D’Souza, A., & Colantonio, A. (2017) · BMJ Open · doi:10.1136/bmjopen-2017-017165 · Cited by 14
“The abstracted data will include the following: (1) study characteristics (author names, publication year, country of study, study setting, study design, sample size, method of measuring cognition and cognitive domains covered, number of participants assessed for at each time point, time between assessments and time s…”
BackgroundHoule, S., Tapp, Z. M., Dobres, S., Ahsan, S., Reyes, Y., Cotter, C., Mitsch, J., Zimomra, Z., Peng, J., Rowe, R. K., et al. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100797 · Cited by 9
“6D), a key region in spatial learning and memory, which is also vulnerable to TBI induced inflammation (Muccigrosso et al., 2016; Tapp et al., 2022).”
BackgroundSelf-citationBi-directional neuro-immune dysfunction after chronic experimental brain injury
Ritzel, R., Li, Y., Jiao, Y., Doran, S. J., Khan, N. Z., Henry, R., Brunner, K., Loane, D., Faden, A. I., Szeto, G. L., et al. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03082-y · Cited by 12
“Impor-tantly, we found that bone marrow-derived macrophage cultures harvested from chronic (90d) TBI mice exhibited significantly higher sensitivity to LPS stimulation compared to macrophages cultured from sham mice [54, 55].”
BackgroundMollayeva, T., Hurst, M., Chan, V., Escobar, M., Sutton, M., & Colantonio, A. (2020) · Preventive Medicine · doi:10.1016/j.ypmed.2020.106213 · Cited by 12
Long‐term reprogramming of primed microglia after moderate inhibition of CSF1R signaling
León‐Rodríguez, A., Grondona, J. M., Marín‐Wong, S., López‐Aranda, M. F., & López-Ávalos, M. D. (2024) · Glia · doi:10.1002/glia.24627 · Cited by 13
Shi, S., Zhang, S., & Kong, L. (2023) · Life · doi:10.3390/life13091829 · Cited by 10
Beitchman, J. A., Lifshitz, J., Harris, N., Thomas, T. C., Lafrenaye, A. D., Hånell, A., Dixon, C. E., Povlishock, J., & Rowe, R. K. (2020) · bioRxiv · doi:10.1089/neur.2020.0046 · Cited by 10
Self-citationSrinivasan, G. R., & Brafman, D. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.813544 · Cited by 10
“…dpi ↑ at 120 dpi Kokiko-Cochran et al., 2015 Non-transgenic (BALB/c) mFPI 3 months 7, 30 days LPS challenge 30 dpi ↑inflammation and cognitive deficits Muccigrosso et al., 2016 Non-transgenic (C57BL/6) CCI 3 months ↑Microglial mGluR5 expression which when inhibited ↓neuronal loss Byrnes et al.,…”
BackgroundShi, R., Liu, H., Tan, P., Hu, Z., Ma, Y., Ye, M., Gu, Y., Wang, Y., Ye, T., Gu, Y., et al. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.108950 · Cited by 9
Wang, Y., Andrade, P., & Pitkänen, A. (2021) · Biomedicines · doi:10.3390/biomedicines9121946 · Cited by 9
“For example, LPS administration at 30 days post-TBI exacerbated cognitive impairment and induced depression-like behavior, both of which were associated with microglial reactivation and an exaggerated production of pro-inflammatory cytokines IL1-β and TNFα [45,46].”
BackgroundExacerbated immune response of the brain to peripheral immune challenge in post-septic mice
Salmani, H., Hosseini, M., Nabi, M. M., Noshahr, Z. S., Baghcheghi, Y., & Sadeghi, M. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.04.013 · Cited by 6
Hadanny, A., & Efrati, S. (2025) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2025.2515061 · Cited by 8
Law, L. M., Griffiths, D. R., & Lifshitz, J. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114355 · Cited by 5
Self-citationRichter, M., Negro‐Demontel, M. L., Blanco‐Ocampo, D., Taranto, E., Lago, N., & Peluffo, H. (2018) · Current Protocols in Immunology · doi:10.1002/cpim.42 · Cited by 5
“Accordingly, cognitive deficits develop at 1 month post-mild TBI that were not present at 7 dpl (Muccigrosso et al., 2016).”
BackgroundTapp, Z., Ren, C., Palmer, K., Kumar, J., Atluri, R., Fitzgerald, J. A., Velasquez, J., Godbout, J., Sheridan, J. F., & Kokiko-Cochran, O. (2023) · Neurotrauma Reports · doi:10.1089/neur.2023.0018 · Cited by 5
Self-citationKaukas, L., Krieg, J. L., Collins‐Praino, L. E., & Corrigan, F. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.659679 · Cited by 5
“Even remote inflammatory stimuli can drive this response, with a peripheral immune challenge at 1-month post-injury acutely worsening memory consolidation on the Barnes Maze (Muccigrosso et al., 2016) and enhancing depressive-like behavior on the tail suspension test (Fenn et al., 2014).”
BackgroundInfluentialKamal, K., Keiter, J. A., Binyamin, T., Dapula, J. N. D. L. C., Vergara, A., Hawk, C., Izadi, A., Lyeth, B. G., Gurkoff, G. G., Sharp, F., et al. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105084 · Cited by 5
Apple cider vinegar attenuates lipopolysaccharide-induced neurobehavioral deficits in mice
Asejeje, F. O., Abiola, M. A., Ben‐Azu, B., Adeosun, A., Ighodaro, O. M., & Ajayi, A. M. (2020) · Nutrire · doi:10.1186/s41110-020-00125-1 · Cited by 6
Zhang, Z., Xiao, T., Hall, M. R., Crodian, J. S., Alford, A., Kimbrough, A., & Shi, R. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.10.003 · Cited by 6
Neurodegenerative Disorders in the Context of Vascular Changes after Traumatic Brain Injury
Segherlou, Z. H., Masheghati, F., Shakeri-Darzehkanani, M., Siyanaki, M. R. H., & Lucke-Wold, B. P. (2024) · Journal of Vascular Diseases · doi:10.3390/jvd3030025 · Cited by 5
“They are one of the initial groups to react to brain injury, and their continuous activation in animal models and individuals with TBI could play a role in causing long-term functional impairments [97,108–111].”
Microbial neuraminidase induces TLR4-dependent long-term immune priming in the brain
Fernández‐Arjona, M. D. M., León‐Rodríguez, A., Grondona, J. M., & López-Ávalos, M. D. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.945229 · Cited by 4
“, 2017), some authors have reported evidences of priming in astrocytes (Hennessy et al., 2015; Muccigrosso et al., 2016).”
BackgroundDavis, A. C., Goodman, E. J., Wangler, L. M., Packer, J. M., Thammachack, R., Yildiz, V. O., Sharma, P., Pietrzak, M., Xiaokui, M., Quan, N., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106524 · Cited by 3
Self-citation
Metadata
- Authors
- Muccigrosso, M. M., Ford, J., Benner, B., Moussa, D., Burnsides, C., Fenn, A. M., Popovich, P. G., Lifshitz, J., Walker, F. R., Eiferman, D. S., & Godbout, J. P.
- Affiliations
- The Ohio State University (US)
- The Ohio State University Wexner Medical Center (US)
- Barrow Neurological Institute (US)
- University of Newcastle Australia (AU)
- Corresponding author
- Godbout, Jonathan P.
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2016-05
- Volume
- 54
- Pages
- 95-109
- ISSN
- 0889-1591 (ISSN-L)
- PMC
- PMC4828283
- OpenAlex
- W2237921172
- Cited by
- 146
- References
- 70
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 14 · 2023: 11 · 2022: 18 · 2021: 23 · 2020: 19 · 2019: 10 · 2018: 11 · 2017: 16 · 2016: 11
- FWCI
- 12.03
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- NOVA (University of Newcastle Australia) (submittedVersion)
- Funders
- NIA Grant (R01-AG-033028)
- College of Medicine Dean’s Discovery Grant
- Center for Brain and Spinal Cord Repair
- American Surgical Society Fellowship
- P30 Core Grant
- National Institute of Dental and Craniofacial Research Training Grant
- Topics
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury Research
- Keywords
- traumatic brain injury, diffuse brain injury, fluid percussion injury, microglial activation, neuroinflammation, cognitive impairment, memory consolidation, anterograde amnesia, hippocampus, CA3, astrocytes, IL-1β, TNF-α, MCP-1, MHC class II, glial fibrillary acidic protein, immune challenge
- MeSH terms
- Brain Injuries, Diffuse, Brain Injuries, Traumatic, Animals, Astrocytes, Cognition, Cognition Disorders, Disease Models, Animal, Inflammation, Male, Memory, Mice, Inbred BALB C, Quality of Life, Cytokines, Microglia, Inflammation Mediators, Chemokines, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
