Aging Exacerbates Neuroinflammatory Outcomes Induced by Acute Ozone Exposure

Tyler, Christina R.; Noor, Shahani; Young, Tamara; Rivero, Valeria; Sanchez, Bethany; Lucas, Selita; Caldwell, Kevin K.; Milligan, Erin D.; Campen, Matthew J.

doi:10.1093/toxsci/kfy014

Title: Aging Exacerbates Neuroinflammatory Outcomes Induced by Acute Ozone Exposure

Journal Article · 27 January 2018 · Toxicological Sciences

DOI: https://doi.org/10.1093/toxsci/kfy014 · OSTI ID:1419764

Tyler, Christina R. ^[1]; Noor, Shahani ^[2]; Young, Tamara ^[3]; Rivero, Valeria ^[3]; Sanchez, Bethany ^[3]; Lucas, Selita ^[3]; Caldwell, Kevin K. ^[2]; Milligan, Erin D. ^[2]; Campen, Matthew J. ^[3]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States); Univ. of New Mexico, Albuquerque, NM (United States)
Univ. of New Mexico Health Sciences Center, Albuquerque, NM (United States)
Univ. of New Mexico, Albuquerque, NM (United States)

The role of environmental stressors, particularly exposure to air pollution, in the development of neurodegenerative disease remains underappreciated. We examined the neurological effects of acute ozone (O₃) exposure in aged mice, where increased blood brain barrier (BBB) permeability may confer vulnerability to neuroinflammatory outcomes. C₅₇BL/6 male mice, aged 8-10 weeks or 12–18 months were exposed to either filtered air (FA) or 1.0 ppm O₃ for 4 hours; animals received a single IP injection of sodium fluorescein (FSCN) 20 hours post-exposure. One-hour post-FSCN injection, animals were transcardially perfused for immunohistochemical analysis of BBB permeability. β-amyloid protein expression was assessed via ELISA. Flow cytometric characterization of infiltrating immune cells, including neutrophils, macrophages, and microglia populations was performed 20 hours post-O₃ exposure. Flow cytometry analysis of brains revealed increased microglia “activation” and presentation of CD11b, F4/80 and MHCII in aged animals relative to younger ones; these age-induced differences were potentiated by acute O₃ exposure. Cortical and limbic regions in aged brains had increased reactive microgliosis and β-amyloid protein expression after O₃ insult. The aged cerebellum was particularly vulnerable to acute O₃ exposure with increased populations of infiltrating neutrophils, peripheral macrophages/monocytes, and Ly6C⁺ inflammatory monocytes after insult, which were not significantly increased in the young cerebellum. O₃ exposure increased the penetration of FSCN beyond the BBB, the infiltration of peripheral immune cells, and reactive gliosis of microglia. Furthermore, the aged BBB is vulnerable to insult and becomes highly penetrable in response to O₃ exposure, leading to greater neuroinflammatory outcomes.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC52-06NA25396

OSTI ID:: 1419764

Report Number(s):: LA-UR-18-20155

Journal Information:: Toxicological Sciences, Vol. 163, Issue 1; ISSN 1096-6080

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 32 works

Citation information provided by
Web of Science

References (71)

Fine Particulate Matter Air Pollution and Cognitive Function Among Older US Adults Ailshire, J. A.; Crimmins, E. M. American Journal of Epidemiology, Vol. 180, Issue 4 https://doi.org/10.1093/aje/kwu155	journal	June 2014
Cyclic Ozone Exposure Induces Gender-Dependent Neuropathology and Memory Decline in an Animal Model of Alzheimer’s Disease Akhter, Hasina; Ballinger, Carol; Liu, Nianjun Toxicological Sciences, Vol. 147, Issue 1 https://doi.org/10.1093/toxsci/kfv124	journal	June 2015
Serum-borne bioactivity caused by pulmonary multiwalled carbon nanotubes induces neuroinflammation via blood–brain barrier impairment Aragon, Mario J.; Topper, Lauren; Tyler, Christina R. Proceedings of the National Academy of Sciences, Vol. 114, Issue 10 https://doi.org/10.1073/pnas.1616070114	journal	February 2017
A Pilot Study to Assess Effects of Long-Term Inhalation of Airborne Particulate Matter on Early Alzheimer-Like Changes in the Mouse Brain Bhatt, Dhaval P.; Puig, Kendra L.; Gorr, Matthew W. PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0127102	journal	May 2015
The age-related deficit in LTP is associated with changes in perfusion and blood-brain barrier permeability Blau, Christoph W.; Cowley, Thelma R.; O'Sullivan, Joan Neurobiology of Aging, Vol. 33, Issue 5 https://doi.org/10.1016/j.neurobiolaging.2011.09.035	journal	May 2012
Air pollution: mechanisms of neuroinflammation and CNS disease Block, Michelle L.; Calderón-Garcidueñas, Lilian Trends in Neurosciences, Vol. 32, Issue 9 https://doi.org/10.1016/j.tins.2009.05.009	journal	September 2009
Protective Effect of Amyloid-β Peptides Against Herpes Simplex Virus-1 Infection in a Neuronal Cell Culture Model Bourgade, Karine; Le Page, Aurélie; Bocti, Christian Journal of Alzheimer's Disease, Vol. 50, Issue 4 https://doi.org/10.3233/JAD-150652	journal	February 2016
Reactive Gliosis and the Multicellular Response to CNS Damage and Disease Burda, Joshua E.; Sofroniew, Michael V. Neuron, Vol. 81, Issue 2 https://doi.org/10.1016/j.neuron.2013.12.034	journal	January 2014
The posterior parahippocampal gyrus is preferentially affected in age-related memory decline Burgmans, S.; van Boxtel, M. P. J.; van den Berg, K. E. M. Neurobiology of Aging, Vol. 32, Issue 9 https://doi.org/10.1016/j.neurobiolaging.2009.09.008	journal	September 2011
Apolipoprotein E4, Gender, Body Mass Index, Inflammation, Insulin Resistance, and Air Pollution Interactions: Recipe for Alzheimer’s Disease Development in Mexico City Young Females Calderón-Garcidueñas, Lilian; de la Monte, Suzanne M. Journal of Alzheimer's Disease, Vol. 58, Issue 3 https://doi.org/10.3233/JAD-161299	journal	June 2017
Neuroinflammation, Hyperphosphorylated Tau, Diffuse Amyloid Plaques, and Down-Regulation of the Cellular Prion Protein in Air Pollution Exposed Children and Young Adults Calderón-Garcidueñas, Lilian; Kavanaugh, Michael; Block, Michelle Journal of Alzheimer's Disease, Vol. 28, Issue 1 https://doi.org/10.3233/JAD-2011-110722	journal	January 2012
Air pollution, a rising environmental risk factor for cognition, neuroinflammation and neurodegeneration: The clinical impact on children and beyond Calderón-Garcidueñas, L.; Leray, E.; Heydarpour, P. Revue Neurologique, Vol. 172, Issue 1 https://doi.org/10.1016/j.neurol.2015.10.008	journal	January 2016
Long-term Air Pollution Exposure Is Associated with Neuroinflammation, an Altered Innate Immune Response, Disruption of the Blood-Brain Barrier, Ultrafine Particulate Deposition, and Accumulation of Amyloid β-42 and α-Synuclein in Children and Young Adults Calderón-Garcidueñas, Lilian; Solt, Anna C.; Henríquez-Roldán, Carlos Toxicologic Pathology, Vol. 36, Issue 2 https://doi.org/10.1177/0192623307313011	journal	February 2008
Reexamining Alzheimer's Disease: Evidence for a Protective Role for Amyloid-β Protein Precursor and Amyloid-β Castellani, Rudy J.; Lee, Hyoung-gon; Siedlak, Sandra L. Journal of Alzheimer's Disease, Vol. 18, Issue 2 https://doi.org/10.3233/JAD-2009-1151	journal	August 2009
A statistical modeling framework for projecting future ambient ozone and its health impact due to climate change Chang, Howard H.; Hao, Hua; Sarnat, Stefanie Ebelt Atmospheric Environment, Vol. 89 https://doi.org/10.1016/j.atmosenv.2014.02.037	journal	June 2014
Circulating Factors Induce Coronary Endothelial Cell Activation Following Exposure to Inhaled Diesel Exhaust and Nitrogen Dioxide in Humans: Evidence From a Novel Translational In Vitro Model Channell, Meghan M.; Paffett, Michael L.; Devlin, Robert B. Toxicological Sciences, Vol. 127, Issue 1 https://doi.org/10.1093/toxsci/kfs084	journal	February 2012
Atrophy in the parahippocampal gyrus as an early biomarker of Alzheimer’s disease Echávarri, C.; Aalten, P.; Uylings, H. B. M. Brain Structure and Function, Vol. 215, Issue 3-4 https://doi.org/10.1007/s00429-010-0283-8	journal	October 2010
Blood–brain barrier dysfunction developed during normal aging is associated with inflammation and loss of tight junctions but not with leukocyte recruitment Elahy, Mina; Jackaman, Connie; Mamo, John Immunity & Ageing, Vol. 12, Issue 1 https://doi.org/10.1186/s12979-015-0029-9	journal	January 2015
The movers and shapers in immune privilege of the CNS Engelhardt, Britta; Vajkoczy, Peter; Weller, Roy O. Nature Immunology, Vol. 18, Issue 2 https://doi.org/10.1038/ni.3666	journal	January 2017
Blood–brain barrier changes and cell invasion differ between therapeutic immune clearance of neurotrophic virus and CNS autoimmunity Fabis, Marzena J.; Phares, Timothy W.; Kean, Rhonda B. Proceedings of the National Academy of Sciences, Vol. 105, Issue 40 https://doi.org/10.1073/pnas.0807656105	journal	September 2008
Early pulmonary response is critical for extra-pulmonary carbon nanoparticle mediated effects: comparison of inhalation versus intra-arterial infusion exposures in mice Ganguly, Koustav; Ettehadieh, Dariusch; Upadhyay, Swapna Particle and Fibre Toxicology, Vol. 14, Issue 1 https://doi.org/10.1186/s12989-017-0200-x	journal	June 2017
T Cell Recruitment in the Brain during Normal Aging Gemechu, Jickssa M.; Bentivoglio, Marina Frontiers in Cellular Neuroscience, Vol. 6 https://doi.org/10.3389/fncel.2012.00038	journal	January 2012
Oxidative Stress Activates the Transcription Factors FoxO 1a and FoxO 3a in the Hippocampus of Rats Exposed to Low Doses of Ozone Gómez-Crisóstomo, Nancy P.; Rodríguez Martínez, Erika; Rivas-Arancibia, Selva Oxidative Medicine and Cellular Longevity, Vol. 2014 https://doi.org/10.1155/2014/805764	journal	January 2014
Inhalation of environmental stressors & chronic inflammation: Autoimmunity and neurodegeneration Gomez-Mejiba, Sandra E.; Zhai, Zili; Akram, Hammad Mutation Research/Genetic Toxicology and Environmental Mutagenesis, Vol. 674, Issue 1-2 https://doi.org/10.1016/j.mrgentox.2008.09.016	journal	March 2009
Microglia Versus Myeloid Cell Nomenclature during Brain Inflammation Greter, Melanie; Lelios, Iva; Croxford, Andrew Lewis Frontiers in Immunology, Vol. 6 https://doi.org/10.3389/fimmu.2015.00249	journal	May 2015
Development and Function of the Blood-Brain Barrier in the Context of Metabolic Control Haddad-Tóvolli, Roberta; Dragano, Nathalia R. V.; Ramalho, Albina F. S. Frontiers in Neuroscience, Vol. 11 https://doi.org/10.3389/fnins.2017.00224	journal	April 2017
Age related changes in microglial phenotype vary between CNS regions: Grey versus white matter differences Hart, Adam D.; Wyttenbach, Andreas; Hugh Perry, V. Brain, Behavior, and Immunity, Vol. 26, Issue 5 https://doi.org/10.1016/j.bbi.2011.11.006	journal	July 2012
Neuroinflammation, Neurodegeneration, and Depression Hurley, Laura L.; Tizabi, Yousef Neurotoxicity Research, Vol. 23, Issue 2 https://doi.org/10.1007/s12640-012-9348-1	journal	August 2012
Glio-vascular changes during ageing in wild-type and Alzheimer׳s disease-like APP/PS1 mice Janota, C. S.; Brites, D.; Lemere, C. A. Brain Research, Vol. 1620 https://doi.org/10.1016/j.brainres.2015.04.056	journal	September 2015
Outdoor Ambient Air Pollution and Neurodegenerative Diseases: the Neuroinflammation Hypothesis Jayaraj, Richard L.; Rodriguez, Eric A.; Wang, Yi Current Environmental Health Reports, Vol. 4, Issue 2 https://doi.org/10.1007/s40572-017-0142-3	journal	April 2017
Effects of aging on blood brain barrier and matrix metalloproteases following controlled cortical impact in mice Lee, Phil; Kim, Jieun; Williams, Rachel Experimental Neurology, Vol. 234, Issue 1 https://doi.org/10.1016/j.expneurol.2011.12.016	journal	March 2012
Air pollution & the brain: Subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease Levesque, Shannon; Surace, Michael J.; McDonald, Jacob Journal of Neuroinflammation, Vol. 8, Issue 1 https://doi.org/10.1186/1742-2094-8-105	journal	January 2011
Diesel Exhaust Activates and Primes Microglia: Air Pollution, Neuroinflammation, and Regulation of Dopaminergic Neurotoxicity Levesque, Shannon; Taetzsch, Thomas; Lull, Melinda E. Environmental Health Perspectives, Vol. 119, Issue 8 https://doi.org/10.1289/ehp.1002986	journal	August 2011
Magnetite pollution nanoparticles in the human brain Maher, Barbara A.; Ahmed, Imad A. M.; Karloukovski, Vassil Proceedings of the National Academy of Sciences, Vol. 113, Issue 39 https://doi.org/10.1073/pnas.1605941113	journal	September 2016
Extrapulmonary transport of MWCNT following inhalation exposure Mercer, Robert R.; Scabilloni, James F.; Hubbs, Ann F. Particle and Fibre Toxicology, Vol. 10, Issue 1 https://doi.org/10.1186/1743-8977-10-38	journal	January 2013
Inhaled Nanoparticles Accumulate at Sites of Vascular Disease Miller, Mark R.; Raftis, Jennifer B.; Langrish, Jeremy P. ACS Nano, Vol. 11, Issue 5 https://doi.org/10.1021/acsnano.6b08551	journal	April 2017
Blood-Brain Barrier Breakdown in the Aging Human Hippocampus Montagne, Axel; Barnes, Samuel R.; Sweeney, Melanie D. Neuron, Vol. 85, Issue 2 https://doi.org/10.1016/j.neuron.2014.12.032	journal	January 2015
Effect of aging on the blood-brain barrier Mooradian, Arshag D. Neurobiology of Aging, Vol. 9 https://doi.org/10.1016/S0197-4580(88)80013-7	journal	January 1988
Microglial priming through the lung–brain axis: the role of air pollution–induced circulating factors Mumaw, Christen L.; Levesque, Shannon; McGraw, Constance The FASEB Journal, Vol. 30, Issue 5 https://doi.org/10.1096/fj.201500047	journal	May 2016
Ageing as a Risk Factor for Disease Niccoli, Teresa; Partridge, Linda Current Biology, Vol. 22, Issue 17 https://doi.org/10.1016/j.cub.2012.07.024	journal	September 2012
Age-dependent differences in microglial responses to systemic inflammation are evident as early as middle age Nikodemova, Maria; Small, Alissa L.; Kimyon, Rebecca S. Physiological Genomics, Vol. 48, Issue 5 https://doi.org/10.1152/physiolgenomics.00129.2015	journal	May 2016
Prenatal alcohol exposure potentiates chronic neuropathic pain, spinal glial and immune cell activation and alters sciatic nerve and DRG cytokine levels Noor, Shahani; Sanchez, Joshua J.; Vanderwall, Arden G. Brain, Behavior, and Immunity, Vol. 61 https://doi.org/10.1016/j.bbi.2016.12.016	journal	March 2017
Review: Microglia of the aged brain: primed to be activated and resistant to regulation: Increased microglial reactivity with age Norden, D. M.; Godbout, J. P. Neuropathology and Applied Neurobiology, Vol. 39, Issue 1 https://doi.org/10.1111/j.1365-2990.2012.01306.x	journal	January 2013
Translocation of Inhaled Ultrafine Particles to the Brain Oberdörster, G.; Sharp, Z.; Atudorei, V. Inhalation Toxicology, Vol. 16, Issue 6-7 https://doi.org/10.1080/08958370490439597	journal	January 2004
Exposure to vehicle emissions results in altered blood brain barrier permeability and expression of matrix metalloproteinases and tight junction proteins in mice Oppenheim, Hannah A.; Lucero, JoAnn; Guyot, Anne-Cécile Particle and Fibre Toxicology, Vol. 10, Issue 1 https://doi.org/10.1186/1743-8977-10-62	journal	January 2013
Regional Differences in Blood-Brain Barrier Permeability Changes and Inflammation in the Apathogenic Clearance of Virus from the Central Nervous System Phares, Timothy W.; Kean, Rhonda B.; Mikheeva, Tatiana The Journal of Immunology, Vol. 176, Issue 12 https://doi.org/10.4049/jimmunol.176.12.7666	journal	June 2006
Variation in Estimated Ozone-Related Health Impacts of Climate Change due to Modeling Choices and Assumptions Post, Ellen S.; Grambsch, Anne; Weaver, Chris Environmental Health Perspectives, Vol. 120, Issue 11 https://doi.org/10.1289/ehp.1104271	journal	November 2012
Determinants of Inhaled Ozone Absorption in Isolated Rat Lungs Postlethwait, E. M.; Langford, S. D.; Bidani, A. Toxicology and Applied Pharmacology, Vol. 125, Issue 1 https://doi.org/10.1006/taap.1994.1051	journal	March 1994
Exposure to air pollution as a potential contributor to cognitive function, cognitive decline, brain imaging, and dementia: A systematic review of epidemiologic research Power, Melinda C.; Adar, Sara D.; Yanosky, Jeff D. NeuroToxicology, Vol. 56 https://doi.org/10.1016/j.neuro.2016.06.004	journal	September 2016
The role of peripheral immune cells in the CNS in steady state and disease Prinz, Marco; Priller, Josef Nature Neuroscience, Vol. 20, Issue 2 https://doi.org/10.1038/nn.4475	journal	January 2017
A polarizing question: do M1 and M2 microglia exist? Ransohoff, Richard M. Nature Neuroscience, Vol. 19, Issue 8 https://doi.org/10.1038/nn.4338	journal	July 2016
How neuroinflammation contributes to neurodegeneration Ransohoff, R. M. Science, Vol. 353, Issue 6301 https://doi.org/10.1126/science.aag2590	journal	August 2016
CNS Infiltration of Peripheral Immune Cells: D-Day for Neurodegenerative Disease? Rezai-Zadeh, Kavon; Gate, David; Town, Terrence Journal of Neuroimmune Pharmacology, Vol. 4, Issue 4 https://doi.org/10.1007/s11481-009-9166-2	journal	August 2009
Effects of Taurine on Ozone-Induced Memory Deficits and Lipid Peroxidation Levels in Brains of Young, Mature, and Old Rats Rivas-Arancibia, Selva; Dorado-Martı́nez, Claudia; Borgonio-Pérez, Gabino Environmental Research, Vol. 82, Issue 1 https://doi.org/10.1006/enrs.1999.3996	journal	January 2000
CD36 Mediates Endothelial Dysfunction Downstream of Circulating Factors Induced by O3 Exposure Robertson, Sarah; Colombo, Elizabeth S.; Lucas, Selita N. Toxicological Sciences, Vol. 134, Issue 2 https://doi.org/10.1093/toxsci/kft107	journal	May 2013
Neurovascular Defects and Faulty Amyloid-β Vascular Clearance in Alzheimer's Disease Sagare, Abhay P.; Bell, Robert D.; Zlokovic, Berislav V. Journal of Alzheimer's Disease, Vol. 33, Issue s1 https://doi.org/10.3233/JAD-2012-129037	journal	December 2012
Endothelial inflammatory transcriptional responses to an altered plasma exposome following inhalation of diesel emissions Schisler, Jonathan C.; Ronnebaum, Sarah M.; Madden, Michael Inhalation Toxicology, Vol. 27, Issue 5 https://doi.org/10.3109/08958378.2015.1030481	journal	March 2015
Age-related changes in the mesial temporal lobe: the parahippocampal white matter region Stoub, Travis R.; Barnes, Carol A.; Shah, Raj C. Neurobiology of Aging, Vol. 33, Issue 7 https://doi.org/10.1016/j.neurobiolaging.2011.02.010	journal	July 2012
The impact of climate change and emissions control on future ozone levels: Implications for human health Stowell, Jennifer D.; Kim, Young-min; Gao, Yang Environment International, Vol. 108 https://doi.org/10.1016/j.envint.2017.08.001	journal	November 2017
Cytokine mRNA Profiles in Contused Spinal Cord and Axotomized Facial Nucleus Suggest a Beneficial Role for Inflammation and Gliosis Streit, Wolfgang J.; Semple-Rowland, Susan L.; Hurley, Sean D. Experimental Neurology, Vol. 152, Issue 1 https://doi.org/10.1006/exnr.1998.6835	journal	July 1998
Ozone Inhalation Provokes Glucocorticoid-Dependent and -Independent Effects on Inflammatory and Metabolic Pathways Thomson, Errol M.; Pal, Shinjini; Guénette, Josée Toxicological Sciences, Vol. 152, Issue 1 https://doi.org/10.1093/toxsci/kfw061	journal	April 2016
Mapping Acute Systemic Effects of Inhaled Particulate Matter and Ozone: Multiorgan Gene Expression and Glucocorticoid Activity Thomson, Errol M.; Vladisavljevic, Djordje; Mohottalage, Susantha Toxicological Sciences, Vol. 135, Issue 1 https://doi.org/10.1093/toxsci/kft137	journal	June 2013
Surface area-dependence of gas-particle interactions influences pulmonary and neuroinflammatory outcomes Tyler, Christina R.; Zychowski, Katherine E.; Sanchez, Bethany N. Particle and Fibre Toxicology, Vol. 13, Issue 1 https://doi.org/10.1186/s12989-016-0177-x	journal	December 2016
The ageing systemic milieu negatively regulates neurogenesis and cognitive function Villeda, Saul A.; Luo, Jian; Mosher, Kira I. Nature, Vol. 477, Issue 7362 https://doi.org/10.1038/nature10357	journal	August 2011
Heterogeneity of the blood-brain barrier Wilhelm, Imola; Nyúl-Tóth, Ádám; Suciu, Maria Tissue Barriers, Vol. 4, Issue 1 https://doi.org/10.1080/21688370.2016.1143544	journal	January 2016
Reproductive hormones regulate the selective permeability of the blood-brain barrier Wilson, Andrea C.; Clemente, Luca; Liu, Tianbing Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1782, Issue 6 https://doi.org/10.1016/j.bbadis.2008.02.011	journal	June 2008
Traffic-related air pollution impact on mouse brain accelerates myelin and neuritic aging changes with specificity for CA1 neurons Woodward, Nicholas C.; Pakbin, Payam; Saffari, Arian Neurobiology of Aging, Vol. 53 https://doi.org/10.1016/j.neurobiolaging.2017.01.007	journal	May 2017
A Statistical Modeling Framework for Projecting Future Ambient Ozone and Its Health Impact Due to Climate Change Chang*, Howard H.; Hao, Hua; Sarnat, Stefanie Ebelt ISEE Conference Abstracts, Vol. 2014, Issue 1 https://doi.org/10.1289/isee.2014.o-017	journal	October 2014
Endothelial inflammatory transcriptional responses to an altered plasma exposome following inhalation of diesel emissions Meghan, Channell,; Matthew, Campen,; C., Schisler, Jonathan The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/m44s-rj65	text	January 2015
Microglia versus myeloid cell nomenclature during brain inflammation Greter, Melanie; Lelios, Iva; Croxford, Andrew Lewis Frontiers Research Foundation https://doi.org/10.5167/uzh-118485	text	January 2015
The movers and shapers in immune privilege of the CNS. Engelhardt, Britta; Vajkoczy, Peter; Weller, Roy O. Nature Publishing Group https://doi.org/10.7892/boris.111261	text	January 2017

Cited By (9)

Development of a large-scale computer-controlled ozone inhalation exposure system for rodents Smith, Gregory J.; Walsh, Leon; Higuchi, Mark Inhalation Toxicology, Vol. 31, Issue 2 https://doi.org/10.1080/08958378.2019.1597222	journal	January 2019
Co-exposure to ambient PM _2.5 plus gaseous pollutants increases amyloid β1–42 accumulation in the hippocampus of male and female rats Motesaddi Zarandi, Saeed; Shahsavani, Abbas; Khodagholi, Fariba Toxin Reviews https://doi.org/10.1080/15569543.2019.1611604	journal	May 2019
Ozone-Induced Dysregulation of Neuroendocrine Axes Requires Adrenal-Derived Stress Hormones Henriquez, Andres R.; House, John S.; Snow, Samantha J. Toxicological Sciences, Vol. 172, Issue 1 https://doi.org/10.1093/toxsci/kfz182	journal	August 2019
¹¹¹ In-DANBIRT In Vivo Molecular Imaging of Inflammatory Cells in Atherosclerosis Mota, Roberto; Campen, Matthew J.; Cuellar, Matthew E. Contrast Media & Molecular Imaging, Vol. 2018 https://doi.org/10.1155/2018/6508724	journal	November 2018
Serum-borne factors alter cerebrovascular endothelial microRNA expression following particulate matter exposure near an abandoned uranium mine on the Navajo Nation Sanchez, Bethany; Zhou, Xixi; Gardiner, Amy S. Particle and Fibre Toxicology, Vol. 17, Issue 1 https://doi.org/10.1186/s12989-020-00361-3	journal	July 2020
Planetary Health and the Future of Human Capacity: The Increasing Impact of Planetary Distress on the Human Brain Chen, Chong; Nakagawa, Shin Challenges, Vol. 9, Issue 2 https://doi.org/10.3390/challe9020041	journal	November 2018
Development of a large-scale computer-controlled ozone inhalation exposure system for rodents Smith, Gregory J.; Walsh, Leon; Higuchi, Mark Taylor & Francis https://doi.org/10.6084/m9.figshare.8081930	text	January 2019
Alzheimer and depressive cognitive-like behaviors in male and female rats: A new method for exposure to ambient air pollution Motesaddi Zarandi, Saeed; Shahsavani, Abbas; Khodagholi, Fariba MethodsX, Vol. 6 https://doi.org/10.1016/j.mex.2019.03.018	journal	January 2019
¹¹¹ In-DANBIRT In Vivo Molecular Imaging of Inflammatory Cells in Atherosclerosis Mota, Roberto; Campen, Matthew J.; Cuellar, Matthew E. Contrast Media & Molecular Imaging, Vol. 2018 https://doi.org/10.1155/2018/6508724	journal	November 2018

Figures / Tables (11)

Similar Records

Sub-chronic exposure to the insecticide dimethoate induces a proinflammatory status and enhances the neuroinflammatory response to bacterial lypopolysaccharide in the hippocampus and striatum of male mice

Journal Article · 2013 · Toxicology and Applied Pharmacology · OSTI ID:22285418

Astiz, Mariana; Diz-Chaves, Yolanda

Region-selective effects of neuroinflammation and antioxidant treatment on peripheral benzodiazepine receptors and NMDA receptors in the rat brain

Journal Article · 2001 · Journal of Neurochemistry · OSTI ID:808920

Biegon, A; Alvarado, M; Budinger, T F; +6 more

Anti-Neuroinflammatory Effects of Vanillin Through the Regulation of Inflammatory Factors and NF-κB Signaling in LPS-Stimulated Microglia

Journal Article · 2019 · Applied Biochemistry and Biotechnology · OSTI ID:22927818

Kim, Mi Eun; Na, Ju Yong; Park, Yong-Duk

Related Subjects

60 APPLIED LIFE SCIENCES
Biological Science
neuroinflammation
microglia
aging
reproductive & developmental toxicology
ozone
blood–brain barrier
inhalation toxicology
respiratory toxicology