Local Cues Establish and Maintain Region-Specific Phenotypes of Basal Ganglia Microglia

Microglia play critical roles in tissue homeostasis and can also modulate neuronal function and synaptic connectivity. In contrast to astrocytes and oligodendrocytes, which arise from multiple progenitor pools, microglia arise from yolk sac progenitors and are widely considered to be equivalent throughout the CNS. However, little is known about basic properties of deep brain microglia, such as those within the basal ganglia (BG). Here, we show that microglial anatomical features, lysosome content, membrane properties, and transcriptomes differ significantly across BG nuclei. Region-specific phenotypes of BG microglia emerged during the second postnatal week and were re-established following genetic or pharmacological microglial ablation and repopulation in the adult, indicating that local cues play an ongoing role in shaping microglial diversity. These findings demonstrate that microglia in the healthy brain exhibit a spectrum of distinct functional states and provide a critical foundation for defining microglial contributions to BG circuit function.

[1]  F. Ginhoux,et al.  Origin and differentiation of microglia , 2013, Front. Cell. Neurosci..

[2]  R. Malenka,et al.  Synaptic plasticity and addiction , 2007, Nature Reviews Neuroscience.

[3]  H. Kettenmann,et al.  Distinct Physiologic Properties of Microglia and Blood-Borne Cells in Rat Brain Slices After Permanent Middle Cerebral Artery Occlusion , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[4]  W. Gan,et al.  ATP mediates rapid microglial response to local brain injury in vivo , 2005, Nature Neuroscience.

[5]  E. Audinat,et al.  Status Epilepticus Induces a Particular Microglial Activation State Characterized by Enhanced Purinergic Signaling , 2008, The Journal of Neuroscience.

[6]  E. Audinat,et al.  Adaptive phenotype of microglial cells during the normal postnatal development of the somatosensory “Barrel” cortex , 2013, Glia.

[7]  Thomas J. Wills,et al.  The development of spatial behaviour and the hippocampal neural representation of space , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  O. Pascual,et al.  Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission , 2011, Proceedings of the National Academy of Sciences.

[9]  Antoine G. Godin,et al.  Morphine hyperalgesia gated through microglia-mediated disruption of neuronal Cl− homeostasis , 2013, Nature Neuroscience.

[10]  Amir A Mufaddel,et al.  Familial idiopathic basal ganglia calcification (Fahr’s disease) , 2014, Neurosciences.

[11]  G. Arendt,et al.  HIV dementia: the role of the basal ganglia and dopaminergic systems , 2000, Journal of psychopharmacology.

[12]  Paul J. Lucassen,et al.  The Indispensable Roles of Microglia and Astrocytes during Brain Development , 2016, Front. Hum. Neurosci..

[13]  C. Long-Smith,et al.  The influence of microglia on the pathogenesis of Parkinson's disease , 2009, Progress in Neurobiology.

[14]  F. Zhou,et al.  Intrinsic and integrative properties of substantia nigra pars reticulata neurons , 2011, Neuroscience.

[15]  F. Ginhoux,et al.  Origin of microglia: current concepts and past controversies. , 2015, Cold Spring Harbor perspectives in biology.

[16]  Ting-ting Yang,et al.  Differential distribution and activation of microglia in the brain of male C57BL/6J mice , 2012, Brain Structure and Function.

[17]  F. Helmchen,et al.  Resting Microglial Cells Are Highly Dynamic Surveillants of Brain Parenchyma in Vivo , 2005, Science.

[18]  Ania K. Majewska,et al.  Microglial Interactions with Synapses Are Modulated by Visual Experience , 2010, PLoS biology.

[19]  D. Stellwagen,et al.  Microglial TNF-α Suppresses Cocaine-Induced Plasticity and Behavioral Sensitization , 2016, Neuron.

[20]  Toshiro K. Ohsumi,et al.  The Microglial Sensome Revealed by Direct RNA Sequencing , 2013, Nature Neuroscience.

[21]  K. Brix Lysosomal Proteases: Revival of the Sleeping Beauty , 2013 .

[22]  I. Amit,et al.  Microglia development follows a stepwise program to regulate brain homeostasis , 2016, Science.

[23]  M. Tansey,et al.  Microglial phenotypes in Parkinson’s disease and animal models of the disease , 2017, Progress in Neurobiology.

[24]  Brian L. West,et al.  Colony-Stimulating Factor 1 Receptor Signaling Is Necessary for Microglia Viability, Unmasking a Microglia Progenitor Cell in the Adult Brain , 2014, Neuron.

[25]  T. González-Hernández,et al.  Vulnerability of Mesostriatal Dopaminergic Neurons in Parkinson's Disease , 2010, Front. Neuroanat..

[26]  D. Stellwagen,et al.  Neuroimmune regulation of homeostatic synaptic plasticity , 2014, Neuropharmacology.

[27]  J. Yates,et al.  Microglia Promote Learning-Dependent Synapse Formation through Brain-Derived Neurotrophic Factor , 2013, Cell.

[28]  A. Graybiel Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

[29]  R. Albin Basal ganglia neurotoxins. , 2000, Neurologic clinics.

[30]  V. Perry,et al.  Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain , 1990, Neuroscience.

[31]  Manoj Kumar,et al.  INGE GRUNDKE-IQBAL AWARD FOR ALZHEIMER’S RESEARCH: NEUROTOXIC REACTIVE ASTROCYTES ARE INDUCED BY ACTIVATED MICROGLIA , 2019, Alzheimer's & Dementia.

[32]  S. Gygi,et al.  Identification of a Unique TGF-β Dependent Molecular and Functional Signature in Microglia , 2013, Nature Neuroscience.

[33]  K. Biber,et al.  Region‐specific expression of immunoregulatory proteins on microglia in the healthy CNS , 2008, Glia.

[34]  G. Garden Epigenetics and the Modulation of Neuroinflammation , 2013, Neurotherapeutics.

[35]  C. Boucsein,et al.  Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro , 2003, The European journal of neuroscience.

[36]  Katarina Kågedal,et al.  The lysosome: from waste bag to potential therapeutic target. , 2013, Journal of molecular cell biology.

[37]  Oscar Marín,et al.  Developmental timing and critical windows for the treatment of psychiatric disorders , 2016, Nature Medicine.

[38]  V. Perry,et al.  Microglial physiology: unique stimuli, specialized responses. , 2009, Annual review of immunology.

[39]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[40]  Tom Michoel,et al.  Microglial brain region-dependent diversity and selective regional sensitivities to ageing , 2015, Nature Neuroscience.

[41]  J. Zuchero,et al.  Glia in mammalian development and disease , 2015, Development.

[42]  Valentin Jaumouillé,et al.  The position of lysosomes within the cell determines their luminal pH , 2016, The Journal of cell biology.

[43]  S. Mohan,et al.  Differential diagnosis for bilateral abnormalities of the basal ganglia and thalamus. , 2011, Radiographics : a review publication of the Radiological Society of North America, Inc.

[44]  W. Richardson,et al.  Oligodendrocyte Development and Plasticity. , 2016, Cold Spring Harbor perspectives in biology.

[45]  H. Kettenmann,et al.  Physiology of microglia. , 2011, Physiological reviews.

[46]  Ben A. Barres,et al.  Complement and microglia mediate early synapse loss in Alzheimer mouse models , 2016, Science.

[47]  H. Kettenmann,et al.  Microglia: active sensor and versatile effector cells in the normal and pathologic brain , 2007, Nature Neuroscience.

[48]  Grayson O. Sipe,et al.  Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex , 2016, Nature Communications.

[49]  Ben A. Barres,et al.  Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner , 2012, Neuron.

[50]  K. Green,et al.  Characterizing Newly Repopulated Microglia in the Adult Mouse: Impacts on Animal Behavior, Cell Morphology, and Neuroinflammation , 2015, PloS one.

[51]  Y. Shaham,et al.  Detection of molecular alterations in methamphetamine‐activated Fos‐expressing neurons from a single rat dorsal striatum using fluorescence‐activated cell sorting (FACS) , 2014, Journal of neurochemistry.

[52]  P. De Camilli,et al.  Massive accumulation of luminal protease-deficient axonal lysosomes at Alzheimer’s disease amyloid plaques , 2015, Proceedings of the National Academy of Sciences.

[53]  C. Boucsein,et al.  Electrophysiological properties of microglial cells in normal and pathologic rat brain slices , 2000, The European journal of neuroscience.

[54]  T. Maniatis,et al.  An RNA-Sequencing Transcriptome and Splicing Database of Glia, Neurons, and Vascular Cells of the Cerebral Cortex , 2014, The Journal of Neuroscience.

[55]  A. Björklund,et al.  Dopamine neuron systems in the brain: an update , 2007, Trends in Neurosciences.

[56]  S. Ferguson Beyond indigestion: emerging roles for lysosome-based signaling in human disease. , 2015, Current opinion in cell biology.

[57]  B. Williams,et al.  From single-cell to cell-pool transcriptomes: Stochasticity in gene expression and RNA splicing , 2014, Genome research.

[58]  R. Myers,et al.  A neurodegeneration-specific gene-expression signature of acutely isolated microglia from an amyotrophic lateral sclerosis mouse model. , 2013, Cell reports.

[59]  Omer Ali Bayraktar,et al.  Astrocyte development and heterogeneity. , 2014, Cold Spring Harbor perspectives in biology.

[60]  K. Krieglstein,et al.  Distribution of microglia in the postnatal murine nigrostriatal system , 2012, Cell and Tissue Research.

[61]  Hui Zhao,et al.  The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. , 2012, Investigative ophthalmology & visual science.

[62]  M. Fukaya,et al.  Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain , 2013, Nature Neuroscience.

[63]  W. Richardson,et al.  Developmental Origin of Oligodendrocyte Lineage Cells Determines Response to Demyelination and Susceptibility to Age-Associated Functional Decline , 2016, Cell reports.

[64]  Anatol C. Kreitzer,et al.  Reassessing models of basal ganglia function and dysfunction. , 2014, Annual review of neuroscience.