Environment matters: microglia function and dysfunction in a changing world

Hanamsagar, Richa; Bilbo, Staci D

doi:10.1016/j.conb.2017.10.007

Cited by 122Neuroinflammation and Neurodegeneration MechanismsNeurogenesis and neuroplasticity mechanismsTryptophan and brain disorders

Environment matters: microglia function and dysfunction in a changing world

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Hanamsagar, Richa, Bilbo, Staci D·2017·Current Opinion in Neurobiology

DOI 10.1016/j.conb.2017.10.007PMC PMC5732848

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Abstract

The immune system is our interface with the environment, and immune molecules such as cytokines and chemokines and the cells that produce them within the brain, notably microglia, are critical for normal brain development. This recognition has in recent years led to the working hypothesis that inflammatory events during pregnancy or the early postnatal period, for example, in response to infection, may disrupt the normal developmental trajectory of microglia and consequently their interactions with neurons, thereby contributing to the risk for neurological disorders. The current article outlines recent findings on the impact of diverse, pervasive environmental challenges, beyond infection, including air pollution and maternal stress; and their impact on microglial development and its broad implications for neural pathologies.

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Microglia are macrophage-like cells that comprise 10-15% of the CNS and mediate diverse functions ranging from innate immunity and phagocytosis to synaptic pruning and the regulation of synaptic activity.
“Microglia are macrophage-like cells that comprise 10–15% of the CNS, and mediate diverse functions ranging from innate immunity and phagocytosis to synaptic pruning and the regulation of synaptic activity [416,417].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [416]

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Bilbo, S. D., Barrientos, R. M., Eads, A. S., Northcutt, A. L., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.10.003 · Cited by 104 · see citing works
Self-citation
Phenotypic dysregulation of microglial activation in young offspring rats with maternal sleep deprivation-induced cognitive impairment
Zhao, Q., Xie, X., Fan, Y., Zhang, J., Jiang, W. I., Wu, X., Yan, S., Chen, Y., Peng, C. Y., & You, Z. (2015) · Scientific Reports · doi:10.1038/srep09513 · Cited by 92 · see citing works
Neuropathological Consequences of Gestational Exposure to Concentrated Ambient Fine and Ultrafine Particles in the Mouse
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Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection
Williamson, L. L., McKenney, E. A., Holzknecht, Z. E., Belliveau, C., Rawls, J. F., Poulton, S., Parker, W., & Bilbo, S. D. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.07.006 · Cited by 84 · see citing works
Self-citation
Maternal infection during pregnancy and schizophrenia
Boksa, P. (2008) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0818 · Cited by 83 · see citing works
The Risk for Schizophrenia From Childhood and Adult Infections
Brown, A. S. (2008) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07101637 · Cited by 80 · see citing works
Suppression of glial activation is involved in the protection of IL-10 on maternal E. coli induced neonatal white matter injury
Pang, Y., Rodts‐Palenik, S., Cai, Z., Bennett, W. A., & Rhodes, P. G. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.03.015 · Cited by 75 · see citing works
Rapid and sensitive detection of bisphenol a from serum matrix
Lin, X., Cheng, C., Terry, P., Chen, J., Cui, H., & Wu, J. J. (2016) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2016.12.024 · Cited by 65 · see citing works
NeonatalE. ColiInfection Causes Neuro-Behavioral Deficits Associated with Hypomyelination and Neuronal Sequestration of Iron
Lieblein‐Boff, J. C., McKim, D. B., Shea, D. T., Wei, P. Y., Deng, Z., Sawicki, C. M., Quan, N., Bilbo, S. D., Bailey, M. T., McTigue, D. M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0708-13.2013 · Cited by 57 · see citing works
Self-citation
Early Postnatal Lipopolysaccharide Exposure Leads to Enhanced Neurogenesis and Impaired Communicative Functions in Rats
Pang, Y., Dai, X., Roller, A., Carter, K., Paul, I. A., Bhatt, A., Lin, R. C. S., & Fan, L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164403 · Cited by 57 · see citing works
Associations between maternal cytokine levels during gestation and measures of child cognitive abilities and executive functioning
Dozmorov, M. G., Bilbo, S. D., Kollins, S. H., Zucker, N. L., Do, E. K., Schechter, J. C., Zhang, J. J., Murphy, S. K., Hoyo, C., & Fuemmeler, B. F. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.03.029 · Cited by 49 · see citing works
Self-citation
Maternal viral infection during pregnancy elicits anti-social behavior in neonatal piglet offspring independent of postnatal microglial cell activation
Antonson, A. M., Radlowski, E. C., Lawson, M. A., Rytych, J. L., & Johnson, R. W. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.09.019 · Cited by 44 · see citing works
Neonatal lipopolysaccharide treatment alters hippocampal neuroinflammation, microglia morphology and anxiety-like behavior in rats selectively bred for an infantile trait
Claypoole, L. D., Zimmerberg, B., & Williamson, L. L. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.08.017 · Cited by 41 · see citing works
Peripheral viral infection induced microglial sensome genes and enhanced microglial cell activity in the hippocampus of neonatal piglets
Ji, P., Schachtschneider, K. M., Schook, L. B., Walker, F. R., & Johnson, R. W. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.02.010 · Cited by 38 · see citing works
Altered white matter integrity in adults with autism spectrum disorder and an IQ >100: a diffusion tensor imaging study
Nickel, K., van Elst, L. T., Perlov, E., Endres, D., Müller, G. T., Riedel, A., Fangmeier, T., & Maier, S. J. (2017) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12731 · Cited by 32 · see citing works

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Research works printed but not linked: 2

[86]Diz-Chaves Y Pernía O Carrero P Garcia-Segura L Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice Journal of Neuroinflammation 2012 9 71 22520439 PMC3409032
[87]Zhao Q Xie X Fan Y Zhang J Jiang W Wu X Yan S Chen Y Peng C You Z Phenotypic dysregulation of microglial activation in young offspring rats with maternal sleep deprivation-induced cognitive impairment Sci Rep 2015 5 9513 25830666 PMC5381687

Sorted by citations

Microglia in Neurological Diseases: A Road Map to Brain-Disease Dependent-Inflammatory Response
Bachiller, S., Jiménez-Ferrer, I., Paulus, A., Yang, Y., Swanberg, M., Deierborg, T., & Boza‐Serrano, A. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00488 · Cited by 706 · see citing works
Delivering transformative action in paediatric pain: a Lancet Child & Adolescent Health Commission
Eccleston, C., Fisher, E., Howard, R. F., Slater, R., Forgeron, P. A., Palermo, T. M., Birnie, K. A., Anderson, B. J., Chambers, C. T., Crombez, G., et al. (2020) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(20)30277-7 · Cited by 338 · see citing works
Autophagy and ALS: mechanistic insights and therapeutic implications
Chua, J. P., De Calbiac, H., Kabashi, E., & Barmada, S. J. (2022) · Autophagy · doi:10.1080/15548627.2021.1926656 · Cited by 189 · see citing works
“pruning and the regulation of synaptic activity [416,417].”
Background
Maternal immune activation in neurodevelopmental disorders
Solek, C. M., Farooqi, N., Verly, M., Lim, T. K., & Ruthazer, E. S. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24612 · Cited by 168 · see citing works
AD-linked R47H- <i>TREM2</i> mutation induces disease-enhancing microglial states via AKT hyperactivation
Sayed, F. A., Kodama, L., Fan, L., Carling, G. K., Udeochu, J. C., Le, D., Li, Q., Zhou, L., Wong, M. Y., Horowitz, R., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abe3947 · Cited by 155 · see citing works
A Developmental Analysis of Juxtavascular Microglia Dynamics and Interactions with the Vasculature
Mondo, E., Becker, S. C., Kautzman, A. G., Schifferer, M., Baer, C. E., Chen, J., Huang, E. J., Simons, M., & Schafer, D. P. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.3006-19.2020 · Cited by 146 · see citing works
Prenatal paracetamol exposure and child neurodevelopment: A review
Bauer, A. Z., Kriebel, D., Herbert, M. R., Bornehag, C.-G., & Swan, S. H. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.01.003 · Cited by 127 · see citing works
“This inflammatory event may disrupt normal microglia development and their interaction with neurons contributing to the risk of neurological disorders (Hanamsagar and Bilbo, 2017; Bilbo et al., 2015).”
Microglia: Brain cells on the move
Smolders, S., Kessels, S., Vangansewinkel, T., Rigo, J., Legendre, P., & Brône, B. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.04.001 · Cited by 114 · see citing works
Enforced microglial depletion and repopulation as a promising strategy for the treatment of neurological disorders
Han, J., Zhu, K., Zhang, X., & Harris, R. A. (2018) · Glia · doi:10.1002/glia.23529 · Cited by 114 · see citing works
“We are beginning to recognize that activated microglia are also quite plastic cells that may differentiate into a plethora of subsets and perform various functions in response to different stimuli and environmental changes such as obesity, diet, alcohol, and even the host microbiota (Chunchai, Chattipakorn, & Chattipa…”
Background
Neurons, Glia, Extracellular Matrix and Neurovascular Unit: A Systems Biology Approach to the Complexity of Synaptic Plasticity in Health and Disease
Luca, C. D., Colangelo, A. M., Virtuoso, A., Alberghina, L., & Papa, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041539 · Cited by 104 · see citing works
“This specialized function is based on high‐density surface receptors (called sensome) to detect both physiological (cognitive stimulation, diet, physical exercise) or pathological stressors [108,120].”
Background
Early Life Exposure to Air Pollution and Autism Spectrum Disorder: Findings from a Multisite Case–Control Study
McGuinn, L. A., Windham, G., Kalkbrenner, A., Bradley, C. B., Di, Q., Croen, L., Fallin, M. D., Hoffman, K., Ladd-Acosta, C., Schwartz, J., et al. (2020) · Epidemiology · doi:10.1097/ede.0000000000001109 · Cited by 72 · see citing works
Controversies and prospects about microglia in maternal immune activation models for neurodevelopmental disorders
Smolders, S., Notter, T., Smolders, S., Rigo, J., & Brône, B. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.06.001 · Cited by 93 · see citing works
Outdoor Air Pollution and Brain Structure and Function From Across Childhood to Young Adulthood: A Methodological Review of Brain MRI Studies
Herting, M. M., Younan, D., Campbell, C. E., & Chen, J. (2019) · Frontiers in Public Health · doi:10.3389/fpubh.2019.00332 · Cited by 94 · see citing works
Glutathione Depletion and Parkinsonian Neurotoxin MPP+-Induced TRPM2 Channel Activation Play Central Roles in Oxidative Cytotoxicity and Inflammation in Microglia
Yıldızhan, K., & Nazıroğlu, M. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01974-7 · Cited by 94 · see citing works
LPS versus Poly I:C model: comparison of long-term effects of bacterial and viral maternal immune activation on the offspring
Bao, M., Hofsink, N., & Plösch, T. (2021) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00087.2021 · Cited by 91 · see citing works
The emerging tale of microglia in psychiatric disorders
Rahimian, R., Wakid, M., O’Leary, L. A., & Mechawar, N. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.023 · Cited by 91 · see citing works
Early life stress by repeated maternal separation induces long-term neuroinflammatory response in glial cells of male rats
Banqueri, M., Méndez, M., Gómez-Lázaro, E., & Arias, J. L. (2019) · Stress · doi:10.1080/10253890.2019.1604666 · Cited by 89 · see citing works
“Microglia display many functions; they phagocytose apoptotic cells, and support neurogenesis and neuronal wiring (Hanamsagar & Bilbo, 2017; Lenz & Nelson, 2018; Tay et al., 2018).”
Background
Role of microgliosis, oxidative stress and associated neuroinflammation in the pathogenesis of Parkinson's disease: The therapeutic role of Nrf2 activators
Saravanan, J., & Krishnamurthy, P. T. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.105014 · Cited by 89 · see citing works
APOE4 confers transcriptomic and functional alterations to primary mouse microglia
Machlovi, S. I., Neuner, S. M., Hemmer, B. M., Khan, R., Liu, Y., Huang, M., Zhu, J. D., Castellano, J. M., Cai, D., Marcora, E., et al. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105615 · Cited by 73 · see citing works
“However, as microglia are exquisitely primed to respond to their environment (Hanamsagar and Bilbo, 2017), studies conducted outside the brain should be interpreted with caution as isolation procedures (Ayata et al.”
Background
Priming of Adult Incision Response by Early-Life Injury: Neonatal Microglial Inhibition Has Persistent But Sexually Dimorphic Effects in Adult Rats
Moriarty, O., Tu, Y., Sengar, A. S., Salter, M. W., Beggs, S., & Walker, S. M. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1786-18.2019 · Cited by 75 · see citing works
“Early-life stress and tissue injury can disrupt microglial sex-dependent maturation or trigger long-term changes in microglial phenotype, altering reactivity to future immune or environmental challenges and influencing responses to physical and psychological stressors and susceptibility to neurological disorders (Perr…”
Background
Rewiring of Memory Circuits: Connecting Adult Newborn Neurons With the Help of Microglia
Rodríguez-Iglesias, N., Sierra, A., & Valero, J. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00024 · Cited by 74 · see citing works
“Importantly, during the first 2–3 weeks after cell birth a moderated GABA input is able to induce action potentials in young GCs when paired to the weak glutamatergic input (Heigele et al., 2016).”
Background
Microglial replacement therapy: a potential therapeutic strategy for incurable CSF1R-related leukoencephalopathy
Han, J., Sarlus, H., Wszolek, Z. K., Karrenbauer, V. D., & Harris, R. A. (2020) · Acta Neuropathologica Communications · doi:10.1186/s40478-020-01093-3 · Cited by 65 · see citing works
Developmental exposure to environmental levels of cadmium induces neurotoxicity and activates microglia in zebrafish larvae: From the perspectives of neurobehavior and neuroimaging
Xu, Y., Zhao, H., Wang, Z., Gao, H., Liu, J., Li, K., Song, Z., Yuan, C., Lan, X., Pan, C., et al. (2021) · Chemosphere · doi:10.1016/j.chemosphere.2021.132802 · Cited by 64 · see citing works
Microglial and Astrocytic Function in Physiological and Pathological Conditions: Estrogenic Modulation
Crespo‐Castrillo, A., & Arévalo, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093219 · Cited by 62 · see citing works
α– Linolenic acid modulates phagocytosis and endosomal pathways of extracellular Tau in microglia
Desale, S. E., & Chinnathambi, S. (2021) · Cell Adhesion & Migration · doi:10.1080/19336918.2021.1898727 · Cited by 63 · see citing works
“Phagocytic ability of microglia is under the influence of various environmental factors such as lipids, lipopolysaccharides (LPS), and cytokines [14,15].”
Background
Toxicity effects of pesticides based on zebrafish (Danio rerio) models: Advances and perspectives
Cui, J., Tian, S., Gu, Y., Wu, X., Wang, L., Wang, J., Chen, X., & Meng, Z. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.139825 · Cited by 63 · see citing works
Biphasic Impact of Prenatal Inflammation and Macrophage Depletion on the Wiring of Neocortical Inhibitory Circuits
Thion, M. S., Mosser, C., Férézou, I., Grisel, P., Baptista, S., Low, D., Ginhoux, F., Garel, S., & Audinat, É. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.086 · Cited by 62 · see citing works
Physiology of Microglia
Tay, T. L., Carrier, M., & Tremblay, M. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-9913-8_6 · Cited by 61 · see citing works
Glial smog: Interplay between air pollution and astrocyte-microglia interactions
Gómez‐Budia, M., Konttinen, H., Saveleva, L., Korhonen, P., Jalava, P., Kanninen, K. M., & Malm, T. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104715 · Cited by 59 · see citing works
Region-Specific Phenotypes of Microglia: The Role of Local Regulatory Cues
Biase, L. M. D., & Bonci, A. (2018) · The Neuroscientist · doi:10.1177/1073858418800996 · Cited by 55 · see citing works
Glia-specific autophagy dysfunction in ALS
Strohm, L., & Behrends, C. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.05.024 · Cited by 53 · see citing works
Chronic exposure to IL-6 induces a desensitized phenotype of the microglia
Recasens, M., Almolda, B., Pérez‐Clausell, J., Campbell, I. L., González, B., & Castellano, B. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02063-1 · Cited by 55 · see citing works
“This activation is totally dependent on the type, location, and duration of damage as well as the specific environment in which microglial cell activation takes place [45, 61].”
Background
Microglia exit the CNS in spinal root avulsion
Green, L. A., Nebiolo, J. C., & Smith, C. J. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000159 · Cited by 51 · see citing works
Direct and indirect effects of lipids on microglia function
Leyrolle, Q., Layé, S., & Nadjar, A. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134348 · Cited by 50 · see citing works
Long-term bisphenol A exposure exacerbates diet-induced prediabetes via TLR4-dependent hypothalamic inflammation
Ma, Q., Deng, P., Lin, M., Yang, L., Li, L., Guo, L., Zhang, L., He, M., Lu, Y., Pi, H., et al. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123926 · Cited by 50 · see citing works
Differential impact of dose-range glyphosate on locomotor behavior, neuronal activity, glio-cerebrovascular structures, and transcript regulations in zebrafish larvae
Forner-Piquer, I., Faucherre, A., Byram, J., Blaquière, M., de Bock, F., Gamet‐Payrastre, L., Ellero‐Simatos, S., Audinat, É., Jopling, C., & Marchi, N. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.128986 · Cited by 49 · see citing works
Microglia: The Brain's First Responders.
Bilbo, S. D., & Stevens, B. (2017) · Europe PMC (PubMed Central) · Cited by 47 · see citing works
Self-citation
Microglial functional alteration and increased diversity in the challenged brain: Insights into novel targets for intervention
Tremblay, M.-È. (2021) · Brain, Behavior, & Immunity - Health · doi:10.1016/j.bbih.2021.100301 · Cited by 42 · see citing works
Microglia Drive Pockets of Neuroinflammation in Middle Age
Moca, E. N., Lecca, D., Hope, K. T., Etienne, F., Schaler, A. W., Espinoza, K., Chappell, M. S., Gray, D. T., Tweedie, D., Sidhu, S., et al. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.1922-21.2022 · Cited by 42 · see citing works
Bundling the haystack to find the needle: Challenges and opportunities in modeling risk and resilience following early life stress
Brenhouse, H. C., & Bath, K. G. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100768 · Cited by 40 · see citing works
Psychological Stress as a Risk Factor for Accelerated Cellular Aging and Cognitive Decline: The Involvement of Microglia-Neuron Crosstalk
Carrier, M., Šimončičová, E., St‐Pierre, M., McKee, C., & Tremblay, M. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.749737 · Cited by 37 · see citing works
Hofbauer cells and fetal brain microglia share transcriptional profiles and responses to maternal diet-induced obesity
Batorsky, R., Ceasrine, A. M., Shook, L. L., Kışlal, S., Bordt, E. A., Devlin, B. A., Perlis, R. H., Slonim, D. K., Bilbo, S. D., & Edlow, A. G. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114326 · Cited by 38 · see citing works
Self-citation
Early life pain—effects in the adult
Walker, S. M. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.04.011 · Cited by 36 · see citing works
Immune-Related Comorbidities in Childhood-Onset Obsessive Compulsive Disorder: Lifetime Prevalence in the Obsessive Compulsive Disorder Collaborative Genetics Association Study
Westwell-Roper, C. Y., Williams, K. B., SAMUELS, J. F., Bienvenu, O. J., Cullen, B., Goes, F. S., Grados, M. A., GELLER, D. A., Greenberg, B. D., Knowles, J. A., et al. (2019) · Journal of Child and Adolescent Psychopharmacology · doi:10.1089/cap.2018.0140 · Cited by 39 · see citing works
“For example, the putative associations described herein may represent shared genetic and/or environmental risks predisposing individuals to both peripheral and central inflammation with neurodevelopmental consequences, including OCD (Hanamsagar and Bilbo 2017).”
Background
Indirect mediators of systemic health outcomes following nanoparticle inhalation exposure
Mostovenko, E., Canal, C. G., Cho, M. J., Sharma, K., Erdely, A., Campen, M. J., & Ottens, A. K. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108120 · Cited by 34 · see citing works
PM2.5 exposure upregulates pro-inflammatory protein expression in human microglial cells via oxidant stress and TLR4/NF-κB pathway
Zhang, L., Xu, F., Yang, Y., Yang, L., Wu, Q., Sun, H., An, Z., Li, J., Wu, H., Song, J., et al. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.116386 · Cited by 31 · see citing works
α-Tocopherol Protects Lipopolysaccharide-Activated BV2 Microglia
Torre, M. E. L., Cianciulli, A., Monda, V., Monda, M., Filannino, F. M., Antonucci, L., Valenzano, A. A., Cibelli, G., Porro, C., Messina, G., et al. (2023) · Molecules · doi:10.3390/molecules28083340 · Cited by 30 · see citing works
“When, due to genetic, external, or environmental factors, there is an imbalance in the regulatory systems of these functions, the presence of a persistent response could lead to inflammation in the brain [47], with consequent long-time neuronal damage and the subsequent appearance of neurodegenerative diseases [48].”
Background
Sex differences in effects of gestational polychlorinated biphenyl exposure on hypothalamic neuroimmune and neuromodulator systems in neonatal rats
Bell, M. R., Dryden, A., Will, R. G., & Gore, A. C. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.06.002 · Cited by 29 · see citing works
“They mediate basic processes like synaptic pruning and formation, neuronal survival, differentiation, and programmed cell death (Hanamsagar and Bilbo, 2017).”
Background
Diesel exhaust impairs TREM2 to dysregulate neuroinflammation
Greve, H. J., Mumaw, C. L., Messenger, E. J., Kodavanti, P. R. S., Royland, J. L., Kodavanti, U. P., & Block, M. L. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-02017-7 · Cited by 28 · see citing works
“Microglia, the myeloid cell of the brain parenchyma, function as immune sentinels and are a prominent source of neuroinflammation in the CNS during disease [13, 14], which is implicated as a central mechanism of many neurodegenerative diseases, including AD [15].”
Background
Microglia isolation from aging mice for cell culture: A beginner’s guide
Vijaya, A. K., Iešmantaitė, M., Mela, V., Baltriukienė, D., & Burokas, A. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1082180 · Cited by 23 · see citing works
“Even in a healthy brain, microglia are highly active, pulling in and out motile processes through which they monitor their microenvironment and dynamically interact with surrounding cells (Parkhurst and Gan, 2010; Hanamsagar and Bilbo, 2017).”
Background
The link between microglia and the severity of COVID‐19: The “two‐hit” hypothesis
Bouayed, J., & Bohn, T. (2021) · Journal of Medical Virology · doi:10.1002/jmv.26984 · Cited by 23 · see citing works
“These cells are derived from macrophages and constitute the most prominent immune and cytokine‐producing cells in the brain.(9) The”
Background
Microglia as a Hub for Suicide Neuropathology: Future Investigation and Prevention Targets
de Andrade, E. G., Ibáñez, F. G., & Tremblay, M. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.839396 · Cited by 19 · see citing works
“Microglial diversity is drawn by cues from their microenvironment, which differ according to the species, age, sex, CNS region, particular context of health or disease, as well as lifestyle habits of the organism (Hanamsagar and Bilbo, 2017; Bordeleau et al., 2019; Masuda et al., 2020).”
Background
Microglia/macrophage diversities in central nervous system physiology and pathology
Xie, D., He, M., & Hu, X. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13257 · Cited by 20 · see citing works
A Diversity of Cell Types, Subtypes and Phenotypes in the Central Nervous System: The Importance of Studying Their Complex Relationships
Tremblay, M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.628347 · Cited by 21 · see citing works
“, exposure to nature, social support), thus tremendously increasing the variability (Hanamsagar and Bilbo, 2017; Tay et al., 2017a; Savage and Tremblay, 2019; Madore et al., 2020).”
Background
Antenatal Hypoxia Accelerates the Onset of Alzheimer’s Disease Pathology in 5xFAD Mouse Model
Shen, G., Hu, S. X., Zhao, Z., Zhang, L., & Ma, Q. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00251 · Cited by 20 · see citing works
Microglia involvement in sex-dependent behaviors and schizophrenia occurrence in offspring with maternal dexamethasone exposure
Rim, C., Park, H., You, M., Yang, B., Kim, H.-J., Sung, S., & Kwon, M. (2022) · Schizophrenia · doi:10.1038/s41537-022-00280-6 · Cited by 19 · see citing works
Cognitive Development and Prenatal Air Pollution Exposure in the CHAMACOS Cohort
Holm, S. M., Balmes, J. R., Gunier, R. B., Kogut, K. R., Harley, K. G., & Eskenazi, B. (2023) · Environmental Health Perspectives · doi:10.1289/ehp10812 · Cited by 20 · see citing works
Sex- and Development-Dependent Responses of Rat Microglia to Pro- and Anti-inflammatory Stimulation
Lively, S. S., Wong, R., Lam, D., & Schlichter, L. C. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00433 · Cited by 20 · see citing works
“Age-dependent differences in gene expression can influence microglial responses to CNS insults and, conversely, brain insults can affect microglia development and their subsequent responses (Hanamsagar and Bilbo, 2017).”
Background
Developmental and neurobehavioral toxicity of 2,2′-methylenebis(6-tert-butyl-4-methylphenol) (antioxidant AO2246) during the early life stage of zebrafish
Chai, Y., Sheng, D., Ji, X., Meng, Y., Shen, F., He, R., Ma, R., & Wang, Y. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.166306 · Cited by 19 · see citing works
Alterations in Chromatin Structure and Function in the Microglia
Fujita, Y., & Yamashita, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.626541 · Cited by 18 · see citing works
“5, shortly after the initiation of sex hormone production (Nelson and Lenz, 2017), exhibit low numbers of differentially expressed genes mostly present on the X and Y chromosomes, which may limit embryonic transcriptomic sexual dimorphism in adult females and males, consistent with other studies (Hanamsagar and Bilbo,…”
Result
Decoding the role of zebrafish neuroglia in CNS disease modeling
Zabegalov, K. N., Wang, D., Yang, L., Wang, J., Hu, G., Serikuly, N., Alpyshov, E. T., Khatsko, S. L., Zhdanov, A., Demin, K. A., et al. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.09.020 · Cited by 16 · see citing works
“logical changes during SCI, since activated microglia have already been linked to various CNS deficits, including autism (Hanamsagar and Bilbo, 2017; Zeidán-Chuliá et al., 2014), AD (Hansen et al.”
Background
Sex and Region-Specific Differences in Microglial Morphology and Function Across Development
Bishnoi, I. R., & Bordt, E. A. (2025) · Neuroglia · doi:10.3390/neuroglia6010002 · Cited by 17 · see citing works
“Sex differences in microglial activity have garnered significant attention in recent years, driven by growing evidence that microglia in males and females exhibit distinct morphological and functional trajectories [10,11].”
Synapse-specific roles for microglia in development: New horizons in the prefrontal cortex
Blagburn-Blanco, S. V., Chappell, M. S., Biase, L. M. D., & DeNardo, L. A. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.965756 · Cited by 16 · see citing works
“Because they are exquisitely sensitive to changes in neural activity, inflammation, and stress, microglial support for circuit development can be perturbed by numerous CNS insults (Hanamsagar and Bilbo, 2017).”
Background
Effects of Genetic Counseling on Reducing Prenatal Stress and Autism Rates in the Asia-Pacific Region
Bi, Y., & Uludağ, K. (2024) · Advances in healthcare information systems and administration book series · doi:10.4018/979-8-3693-1214-8.ch016 · Cited by 15 · see citing works
Dynamic changes in mitochondria support phenotypic flexibility of microglia
Espinoza, K., Schaler, A. W., Gray, D. T., Sass, A. R., Escobar, A., Moore, K., Yu, M. A., Chamorro, C. G., & Biase, L. M. D. (2025) · Nature Communications · doi:10.1038/s41467-025-66709-5 · Cited by 14 · see citing works
Isolation driven changes in Iba1-positive microglial morphology are associated with social recognition memory in adults and adolescents
Ferrara, N. C., Trask, S., Yan, L., Padival, M., Helmstetter, F. J., & Rosenkranz, J. A. (2022) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2022.107626 · Cited by 12 · see citing works
Examining the impact of neuroimmune dysregulation on social behavior of male and female juvenile rats
Turano, A., McAuley, E. M., Muench, M. C., & Schwarz, J. M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113449 · Cited by 11 · see citing works
Prenatal Pollutant Exposures and Hypothalamic Development: Early Life Disruption of Metabolic Programming
Koshko, L., Scofield, S., Mor, G., & Sadagurski, M. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.938094 · Cited by 14 · see citing works
The Endocannabinoid System in Glial Cells and Their Profitable Interactions to Treat Epilepsy: Evidence from Animal Models
Huguet, J. E., Gómez, E. S., & Grandes, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413231 · Cited by 13 · see citing works
Particulate matter from car exhaust alters function of human iPSC-derived microglia
Jäntti, H., Jonk, S. M., Gómez‐Budia, M., Ohtonen, S., Fagerlund, I., Fazaludeen, M. F., Aakko-Saksa, P. T., Pébay, A., Lehtonen, Š., Koıstınaho, J., et al. (2024) · Particle and Fibre Toxicology · doi:10.1186/s12989-024-00564-y · Cited by 12 · see citing works
Combined Effect of Maternal Separation and Early-Life Immune Activation on Brain and Behaviour of Rat Offspring
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“From the open-field test and object-place recognition test conducted in this study, it can be concluded that MS induced anxiety-like behaviour in male and reduced locomotor activity in both male and female offspring, and LPS administration at P3 induced subtle memory deficits in male offspring.”
Method
Neurotoxicity of air pollution: Role of neuroinflammation
Costa, L. G., Cole, T. B., Dao, K., Chang, Y. C., Coburn, J. L., & Garrick, J. M. (2018) · Advances in neurotoxicology · doi:10.1016/bs.ant.2018.10.007 · Cited by 9 · see citing works
Single cell profiling of Hofbauer cells and fetal brain microglia reveals shared programs and functionsPreprint
Ceasrine, A. M., Batorsky, R., Shook, L. L., Kışlal, S., Bordt, E. A., Devlin, B. A., Perlis, R. H., Slonim, D. K., Bilbo, S. D., & Edlow, A. G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.03.471177 · Cited by 10 · see citing works
“This programming in turn may contribute to adverse neurodevelopmental and psychiatric outcomes in offspring ranging from autism spectrum disorder/social behavioral deficits, to attention deficit hyperactivity disorder, cognitive deficits, schizophrenia, obsessive compulsive disorder, anxiety, and depression (Bachiller…”
BackgroundSelf-citation
Prenatal benzene exposure in mice alters offspring hypothalamic development predisposing to metabolic disease in later life
Koshko, L., Scofield, S., Debarba, L. K., Stilgenbauer, L., FAKHOURY, P. I., Jayarathne, H. S. M., Pérez-Mojica, J. E., Griggs, E., Lempradl, A. M., & Sadagurski, M. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.138738 · Cited by 9 · see citing works
Exercise, microglia, and beyond – workout to communicate with microglia
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Diurnal variation in the proinflammatory activity of urban fine particulate matter (PM2.5) by in vitro assays
Lovett, C., Cacciottolo, M., Shirmohammadi, F., Haghani, A., Morgan, T. E., Sioutas, C., & Finch, C. E. (2018) · F1000Research · doi:10.12688/f1000research.14836.3 · Cited by 8 · see citing works
β-Alanine Supplementation Attenuates the Neurophysiological Response in Animals Exposed to an Acute Heat Stress
Belity, T., Hoffman, J. R., Horowitz, M., Epstein, Y., Bruchim, Y., & Cohen, H. (2021) · Journal of Dietary Supplements · doi:10.1080/19390211.2021.1889734 · Cited by 7 · see citing works
“Microglia are immune cells of the central nervous system that have an important function in the repair and protection of neuronal tissue (29, 30).”
Background
Effects of developmental exposure to FireMaster® 550 (FM 550) on microglia density, reactivity and morphology in a prosocial animal model
Marinello, W. P., Gillera, S. E. A., Fanning, M. J., Malinsky, L. B., Rhodes, C. L., Horman, B. M., & Patisaul, H. B. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.04.015 · Cited by 7 · see citing works
Early‐life IL ‐4 administration induces long‐term changes in microglia in the cerebellum and prefrontal cortex
Ferreira, P. A., Lebre, C., Costa, J., Amaral, F., Ferreira, R., Martinho, F., Paiva, V. H., Cardoso, A. L., Peça, J., & Guedes, J. R. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16266 · Cited by 6 · see citing works
Polychlorinated Biphenyls, Oxidative Stress, and Brain Health: Mechanistic Links to Neurodegenerative and Neurodevelopmental Diseases
Minuti, A., Floramo, A., Argento, V., Anchesi, I., Muscarà, C., Calabrò, M., & Silvestro, S. (2026) · Antioxidants · doi:10.3390/antiox15020242 · Cited by 6 · see citing works
“Neuroimmune signaling functions during development can be disrupted not only by inflammatory challenges but also by environmental factors such as maternal stress, a high-fat diet, or environmental pollutants, which influence microglial activity [208,209].”
Diurnal variation in the proinflammatory activity of urban fine particulate matter (PM2.5) by in vitro assays
Lovett, C., Cacciottolo, M., Shirmohammadi, F., Haghani, A., Morgan, T. E., Sioutas, C., & Finch, C. E. (2018) · F1000Research · doi:10.12688/f1000research.14836.2 · Cited by 6 · see citing works
Morphological and functional differences between hippocampal and cortical microglia and its impact on neuronal over-excitation in a germline Pten mutant mouse model.
Tan, Z.-B., Bussies, P. L., Sarn, N. B., Irfan, M., DeSilva, T. M., & Eng, C. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.02.044 · Cited by 6 · see citing works
“This gives rise to significant phenotypic heterogeneity, such as temporospatial and gender-specific differences in cellular origin, colonization, density, morphology, and gene expression (Grabert et al., 2016; Hanamsagar et al., 2017; Villa et al., 2018; Masuda et al., 2019; Tan et al., 2020).”
Microglia Activation in the Midbrain of the Human Neonate: The Effect of Perinatal Hypoxic-Ischemic Injury
Panayotacopoulou, M. T., Papageorgiou, I. E., Pagida, M. A., Katsogridaki, A. E., Chrysanthou‐Piterou, M., Valous, N. A., Halama, N., Patsouris, E., & Konstantinidou, A. E. (2022) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlab135 · Cited by 5 · see citing works
Metabolic control of microglia in health and disease
Colombo, G., Monsorno, K., & Paolicelli, R. C. (2025) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19104-6.00009-7 · Cited by 4 · see citing works
Developmental ablation of mature oligodendrocytes exacerbates adult CNS demyelination
Pajoohesh‐Ganji, A., Karl, M. T., Garrison, E. D., Osei-Bonsu, N. A., Paredes, C. C., Ahn, J. J., & Miller, R. H. (2020) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2020.100110 · Cited by 4 · see citing works
Single Cell Profiling of Hofbauer Cells and Fetal Brain Microglia Reveals Shared Programs and FunctionsPreprint
Caesarine, A., Batorsky, R., Shook, L. L., Kışlal, S., Bordt, E. A., Devlin, B. A., Perlis, R. H., Slonim, D. K., Bilbo, S. D., & Edlow, A. G. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3985607 · Cited by 4 · see citing works
Self-citation
Common Respiratory Viruses and Collapsing Health
Gupta, J. K. (2022) · Biomedical and Biotechnology Research Journal (BBRJ) · doi:10.4103/bbrj.bbrj_201_21 · Cited by 3 · see citing works
Neurological Complications of SARS-CoV-2 Infection and COVID-19 Vaccines: From Molecular Mechanisms to Clinical Manifestations
Yepes, M. (2022) · Current Drug Targets · doi:10.2174/1389450123666220919123029 · Cited by 4 · see citing works
Non-neuronal brain biology and its relevance to animal welfare
Lawrence, A. B., Brown, S. M., Bradford, B. M., Mabbott, N. A., Bombail, V., & Rutherford, K. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106136 · Cited by 3 · see citing works
“More generally it has been proposed that inflammatory events during pregnancy and early life can disrupt the developmental trajectory of microglia and contribute to later susceptibility to neurological disorders (Hanamsagar and Bilbo, 2017).”
Integrated network toxicology and transcriptomics reveal NF-κB signaling as a key mediator of TDCPP-induced inflammatory responses in human microglia
Zhang, C., Song, T., Zhou, J., Wang, X., Rao, X., 丁铲, Cao, H., Jiang, Z., Li, Y. X., Xu, H., et al. (2026) · Environment International · doi:10.1016/j.envint.2026.110373 · Cited by 2 · see citing works
Link Between the Immune System and Aggression
Takahashi, A., & Russo, S. J. (2022) · Springer eBooks · doi:10.1007/978-3-030-98711-4_146-1 · Cited by 2 · see citing works
Unraveling the enigma: housekeeping gene Ugt1a7c as a universal biomarker for microglia
Kim, W., Kim, M.-J., & Kim, B. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1364201 · Cited by 2 · see citing works
The Neuroimmunological Nexus of Multiple Sclerosis: Deciphering the Microglial Transcriptomic Tapestry
Jha, A., & Kumar, H. (2024) · Neuroglia · doi:10.3390/neuroglia5030017 · Cited by 3 · see citing works
“Fourth, microglias’ sensitivity to external environmental cues is noteworthy [133], especially during the enzymatic dissociation and temperature changes involved in sample processing, which can trigger microglial reactions.”
Background
Substance Use and Addiction
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Prenatal benzene exposure alters offspring hypothalamic development predisposing to metabolic disease in later lifePreprint
Koshko, L., Scofield, S., Debarba, L. K., Stilgenbauer, L., Sacla, M., FAKHOURY, P. I., Jayarathne, H. S. M., Pérez-Mojica, J. E., Griggs, E., Lempradl, A. M., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.01.05.522910 · Cited by 2 · see citing works
“Microglia, the major cell type responsible for CNS immune response, are exquisitely sensitive to stressors and are activated by inhaled components of urban air pollution through both direct and indirect pathways (15-17).”
Background
Microglial NF-κB Signaling Deficiency Protects Against Metabolic Disruptions Caused by Volatile Organic Compound via Modulating the Hypothalamic TranscriptomePreprint
Debarba, L. K., Jayarathne, H. S. M., Stilgenbauer, L., dos Santos, A. L. T., Koshko, L., Scofield, S., Sullivan, R., Mandal, A., Klueh, U., & Sadagurski, M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.08.566279 · Cited by 2 · see citing works
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Authors: Hanamsagar, R., & Bilbo, S. D.
Affiliations: Harvard University (US)
Corresponding author: Bilbo, Staci D
ORCID: Hanamsagar, Richa
Bilbo, Staci D
Venue: Current Opinion in Neurobiology
Publisher: Elsevier BV
Published: 2017-12
Volume: 47
Pages: 146-155
ISSN: 0959-4388 (ISSN-L)
DOI: 10.1016/j.conb.2017.10.007
PMC: PMC5732848
OpenAlex: W2767521151
Cited by: 122
References: 91
Citations by year: 2026: 9 · 2025: 6 · 2024: 10 · 2023: 10 · 2022: 15 · 2021: 19 · 2020: 25 · 2019: 15 · 2018: 11 · 2017: 2
FWCI: 1.39
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Current Opinion in Neurobiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH101183, R01MH083698)
National Institute of Environmental Health Sciences (R01ES025549)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: microglia, microglial development, environmental influences on brain development, neuroinflammation, prenatal infection, maternal stress, air pollution, cytokines, chemokines, microglia-neuron interaction, neurological disorders, developmental programming
MeSH terms: Animals, Brain, Environmental Exposure, Female, Humans, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Microglia

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Environment matters: microglia function and dysfunction in a changing world

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