A Murine Toolbox for Imaging the Neurovascular Unit

The neurovascular unit (NVU) coordinates many essential functions in the brain including blood flow control, nutrient delivery, and maintenance of BBB integrity. These functions are the result of a cellular and molecular interplay that we are just beginning to understand. Cells of the NVU can now be investigated in the intact brain through the combined use of high‐resolution in vivo imaging and non‐invasive molecular tools to observe and manipulate cell function. Mouse lines that target transgene expression to cells of the NVU will be of great value in future work. However, a detailed evaluation of target cell specificity and expression pattern within the brain is required for many existing lines. The purpose of this review was to catalog mouse lines available to cerebrovascular biologists and to discuss their utility and limitations in future imaging studies.

[1]  Xiaoqin Zhu,et al.  NG2 cells generate both oligodendrocytes and gray matter astrocytes , 2007, Development.

[2]  J. Rossier,et al.  Cortical GABA Interneurons in Neurovascular Coupling: Relays for Subcortical Vasoactive Pathways , 2004, The Journal of Neuroscience.

[3]  N. Honkura,et al.  Two-photon voltage imaging using a genetically encoded voltage indicator , 2013, Scientific Reports.

[4]  P. Chambon,et al.  Efficient temporally‐controlled targeted mutagenesis in smooth muscle cells of the adult mouse , 2009, Genesis.

[5]  A. Nishiyama,et al.  Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity , 2009, Nature Reviews Neuroscience.

[6]  Karl Deisseroth,et al.  Next-generation transgenic mice for optogenetic analysis of neural circuits , 2013, Front. Neural Circuits.

[7]  Magdalena Götz,et al.  In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. , 2010, Cell stem cell.

[8]  J. Rossier,et al.  Activation of cortical 5-HT3 receptor-expressing interneurons induces NO mediated vasodilatations and NPY mediated vasoconstrictions , 2012, Front. Neural Circuits.

[9]  G. Fishell,et al.  The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors , 2010, The Journal of Neuroscience.

[10]  D. Kleinfeld,et al.  Two-Photon Microscopy as a Tool to Study Blood Flow and Neurovascular Coupling in the Rodent Brain , 2013 .

[11]  K. Jin,et al.  Notch4 is activated in endothelial and smooth muscle cells in human brain arteriovenous malformations , 2013, Journal of cellular and molecular medicine.

[12]  David Kleinfeld,et al.  A Guide to Delineate the Logic of Neurovascular Signaling in the Brain , 2010, Front. Neuroenerg..

[13]  S. Whittemore,et al.  CD47 knockout mice exhibit improved recovery from spinal cord injury , 2011, Neurobiology of Disease.

[14]  Stefan Offermanns,et al.  G12-G13–LARG–mediated signaling in vascular smooth muscle is required for salt-induced hypertension , 2008, Nature Medicine.

[15]  J. Grutzendler,et al.  Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period , 2013, Nature.

[16]  N. Mochizuki,et al.  Tie2 is tied at the cell-cell contacts and to extracellular matrix by Angiopoietin-1 , 2009, Experimental & Molecular Medicine.

[17]  T. Lemberger,et al.  Alpha complementation in the Cre recombinase enzyme. , 2003, Genesis.

[18]  D. Attwell,et al.  Capillary pericytes regulate cerebral blood flow in health and disease , 2014, Nature.

[19]  I. Kanno,et al.  Microvascular Sprouting, Extension, and Creation of New Capillary Connections with Adaptation of the Neighboring Astrocytes in Adult Mouse Cortex under Chronic Hypoxia , 2014, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[20]  Edith Hamel,et al.  Specific Subtypes of Cortical GABA Interneurons Contribute to the Neurovascular Coupling Response to Basal Forebrain Stimulation , 2008, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  Hongkui Zeng,et al.  A Cre-Dependent GCaMP3 Reporter Mouse for Neuronal Imaging In Vivo , 2012, The Journal of Neuroscience.

[22]  Rainer Constien,et al.  Temporal Cre‐mediated recombination exclusively in endothelial cells using Tie2 regulatory elements , 2002, Genesis.

[23]  Jeremy Nathans,et al.  Genetically-Directed, Cell Type-Specific Sparse Labeling for the Analysis of Neuronal Morphology , 2008, PloS one.

[24]  W. Wurst,et al.  Inducible gene deletion in astroglia and radial glia—A valuable tool for functional and lineage analysis , 2006, Glia.

[25]  S. Baker,et al.  Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells , 2008, Transgenic Research.

[26]  J. Tsai,et al.  Bone Marrow Lacks a Transplantable Progenitor for Smooth Muscle Type α‐Actin–Expressing Cells , 2006 .

[27]  D. Kleinfeld,et al.  Suppressed Neuronal Activity and Concurrent Arteriolar Vasoconstriction May Explain Negative Blood Oxygenation Level-Dependent Signal , 2007, The Journal of Neuroscience.

[28]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[29]  Volkhard Lindner,et al.  Characterization of Pdgfrb‐Cre transgenic mice reveals reduction of ROSA26 reporter activity in remodeling arteries , 2011, Genesis.

[30]  Benjamin F. Grewe,et al.  Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation , 2012, Nature Methods.

[31]  R. Buckner,et al.  Mapping brain networks in awake mice using combined optical neural control and fMRI. , 2011, Journal of neurophysiology.

[32]  N. Nakatsuji,et al.  Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. , 2001, Developmental biology.

[33]  Berislav V. Zlokovic,et al.  Pericytes Control Key Neurovascular Functions and Neuronal Phenotype in the Adult Brain and during Brain Aging , 2010, Neuron.

[34]  S. Dymecki,et al.  Sonic hedgehog is required for vascular outgrowth in the hindbrain choroid plexus. , 2010, Developmental biology.

[35]  G. Miyoshi,et al.  Cerebral Cortex doi:10.1093/cercor/bhp038 Characterization of Nkx6-2-Derived , 2009 .

[36]  T. Abe,et al.  Reporter Mouse Lines for Fluorescence Imaging , 2013, Development, growth & differentiation.

[37]  K. Svoboda,et al.  Genetic Dissection of Neural Circuits , 2008, Neuron.

[38]  R. Tsien,et al.  Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein , 2004, Nature Biotechnology.

[39]  K. McCarthy,et al.  Astrocytic Gq-GPCR-Linked IP3R-Dependent Ca2+ Signaling Does Not Mediate Neurovascular Coupling in Mouse Visual Cortex In Vivo , 2014, The Journal of Neuroscience.

[40]  O. Shupliakov,et al.  A Pericyte Origin of Spinal Cord Scar Tissue , 2011, Science.

[41]  E. Morrisey,et al.  High‐efficiency somatic mutagenesis in smooth muscle cells and cardiac myocytes in SM22α‐Cre transgenic mice , 2005, Genesis.

[42]  Min Zhang,et al.  Detection of epithelial to mesenchymal transition in airways of a bleomycin induced pulmonary fibrosis model derived from an α-smooth muscle actin-Cre transgenic mouse , 2007, Respiratory research.

[43]  Young Jae Lee,et al.  TGF-β signaling in endothelial cells, but not neuroepithelial cells, is essential for cerebral vascular development , 2011, Laboratory Investigation.

[44]  Martin D. Haustein,et al.  Conditions and Constraints for Astrocyte Calcium Signaling in the Hippocampal Mossy Fiber Pathway , 2014, Neuron.

[45]  W. Zipfel,et al.  BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. , 2006, Physiological genomics.

[46]  S. Kirov,et al.  Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging. , 2013, Brain : a journal of neurology.

[47]  P. Carmeliet,et al.  VE‐Cadherin‐Cre‐recombinase transgenic mouse: A tool for lineage analysis and gene deletion in endothelial cells , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[48]  S. Carmichael,et al.  Pten Deletion in Adult Neural Stem/Progenitor Cells Enhances Constitutive Neurogenesis , 2009, The Journal of Neuroscience.

[49]  Vishnu B. Sridhar,et al.  In vivo Stimulus-Induced Vasodilation Occurs without IP3 Receptor Activation and May Precede Astrocytic Calcium Increase , 2013, The Journal of Neuroscience.

[50]  G. Feng,et al.  Cell type–specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function , 2011, Nature Methods.

[51]  Matthew Grist,et al.  An Fgfr3‐iCreERT2 transgenic mouse line for studies of neural stem cells and astrocytes , 2010, Glia.

[52]  E. Hamel,et al.  Cholinergic basal forebrain neurons project to cortical microvessels in the rat: electron microscopic study with anterogradely transported Phaseolus vulgaris leucoagglutinin and choline acetyltransferase immunocytochemistry , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  Xiaoqin Zhu,et al.  Age-dependent fate and lineage restriction of single NG2 cells , 2011, Development.

[54]  N. Ropert,et al.  New tools for investigating astrocyte-to-neuron communication , 2013, Front. Cell. Neurosci..

[55]  Tomoko Nakanishi,et al.  ‘Green mice’ as a source of ubiquitous green cells , 1997, FEBS letters.

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

[57]  J. C. Kim,et al.  Genetic fate-mapping approaches: new means to explore the embryonic origins of the cochlear nucleus. , 2009, Methods in molecular biology.

[58]  Fabian J Theis,et al.  Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation , 2013, Nature Neuroscience.

[59]  Jackelyn A. Alva,et al.  VE‐cadherin‐CreERT2 transgenic mouse: A model for inducible recombination in the endothelium , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[60]  Benjamin R. Arenkiel,et al.  Imaging Neural Activity Using Thy1-GCaMP Transgenic Mice , 2012, Neuron.

[61]  Jack Waters,et al.  Selective optogenetic stimulation of cholinergic axons in neocortex. , 2012, Journal of neurophysiology.

[62]  M. Slezak,et al.  Genetic approaches to study glial cells in the rodent brain , 2012, Glia.

[63]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[64]  B. Barres,et al.  Pericytes are required for blood–brain barrier integrity during embryogenesis , 2010, Nature.

[65]  P. Chambon,et al.  Efficient, inducible Cre‐recombinase activation in vascular endothelium , 2008, Genesis.

[66]  E. Fox,et al.  Mechanism of hyperphagia contributing to obesity in brain-derived neurotrophic factor knockout mice , 2013, Neuroscience.

[67]  Hongkui Zeng,et al.  Genetic approaches to neural circuits in the mouse. , 2013, Annual review of neuroscience.

[68]  Thomas N. Sato,et al.  Universal GFP reporter for the study of vascular development , 2000, Genesis.

[69]  G. Miyoshi,et al.  Genetic Fate Mapping Reveals That the Caudal Ganglionic Eminence Produces a Large and Diverse Population of Superficial Cortical Interneurons , 2010, The Journal of Neuroscience.

[70]  Philippe Soriano,et al.  Ephrin-B2 forward signaling regulates somite patterning and neural crest cell development. , 2007, Developmental biology.

[71]  F. Kirchhoff,et al.  Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen‐inducible DNA recombinase variant CreERT2 , 2006, Glia.

[72]  K. Willecke,et al.  hGFAP‐cre transgenic mice for manipulation of glial and neuronal function in vivo , 2001, Genesis.

[73]  J. Rothstein,et al.  Variations in Promoter Activity Reveal a Differential Expression and Physiology of Glutamate Transporters by Glia in the Developing and Mature CNS , 2007, The Journal of Neuroscience.

[74]  A. Fine,et al.  Live astrocytes visualized by green fluorescent protein in transgenic mice. , 1997, Developmental biology.

[75]  G. Owens,et al.  Development of a Smooth Muscle–Targeted Cre Recombinase Mouse Reveals Novel Insights Regarding Smooth Muscle Myosin Heavy Chain Promoter Regulation , 2000, Circulation research.

[76]  T. Lemberger,et al.  α Complementation in the Cre recombinase enzyme , 2003 .

[77]  Junichi Nakai,et al.  Ca2+-sensing Transgenic Mice , 2004, Journal of Biological Chemistry.

[78]  D. Kleinfeld,et al.  Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[79]  D. Attwell,et al.  Glial and neuronal control of brain blood flow , 2022 .

[80]  Carson K. Lam,et al.  Embolus extravasation is an alternative mechanism for cerebral microvascular recanalization , 2010, Nature.

[81]  J B Patlak,et al.  Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. , 1990, The American journal of physiology.

[82]  S. Nelson,et al.  A Resource of Cre Driver Lines for Genetic Targeting of GABAergic Neurons in Cerebral Cortex , 2011, Neuron.

[83]  Allan R. Jones,et al.  A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing , 2012, Nature Neuroscience.

[84]  L. Ment,et al.  Cortical Glial Fibrillary Acidic Protein-Positive Cells Generate Neurons after Perinatal Hypoxic Injury , 2011, The Journal of Neuroscience.

[85]  Murtaza Z Mogri,et al.  Optical Deconstruction of Parkinsonian Neural Circuitry , 2009, Science.

[86]  B. Cauli,et al.  Revisiting the Role of Neurons in Neurovascular Coupling , 2010, Front. Neuroenerg..

[87]  Allan R. Jones,et al.  A robust and high-throughput Cre reporting and characterization system for the whole mouse brain , 2009, Nature Neuroscience.

[88]  Amber N. Stratman,et al.  Mutations in 2 distinct genetic pathways result in cerebral cavernous malformations in mice. , 2011, The Journal of clinical investigation.

[89]  G. Feng,et al.  Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP , 2000, Neuron.

[90]  Alan Urban,et al.  Deciphering the Neuronal Circuitry Controlling Local Blood Flow in the Cerebral Cortex with Optogenetics in PV::Cre Transgenic Mice , 2012, Front. Pharmacol..

[91]  M. Sofroniew,et al.  GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain , 2004, Nature Neuroscience.

[92]  Ulrich Dirnagl,et al.  Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain , 2010, Proceedings of the National Academy of Sciences.

[93]  M. Kotlikoff,et al.  Smooth muscle expression of Cre recombinase and eGFP in transgenic mice. , 2002, Physiological genomics.

[94]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[95]  L. Parada,et al.  Neurofibromin Is Required for Barrel Formation in the Mouse Somatosensory Cortex , 2008, The Journal of Neuroscience.

[96]  James M. Wilson,et al.  Expanded repertoire of AAV vector serotypes mediate unique patterns of transduction in mouse brain. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[97]  K. Nave,et al.  NG2‐expressing cells in the nervous system revealed by the NG2‐EYFP‐knockin mouse , 2008, Genesis.

[98]  Yuko Sato,et al.  Regulation of regional cerebral blood flow by cholinergic fibers originating in the basal forebrain , 1992, Neuroscience Research.

[99]  J. Stull,et al.  Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[100]  L. Luo,et al.  A global double‐fluorescent Cre reporter mouse , 2007, Genesis.

[101]  Timothy H. Murphy,et al.  Hemodynamic Responses Evoked by Neuronal Stimulation via Channelrhodopsin-2 Can Be Independent of Intracortical Glutamatergic Synaptic Transmission , 2012, PloS one.

[102]  Y. Nagai,et al.  Bone marrow lacks a transplantable progenitor for smooth muscle type alpha-actin-expressing cells. , 2006, Stem Cells.

[103]  Guoping Feng,et al.  Development of transgenic animals for optogenetic manipulation of mammalian nervous system function: Progress and prospects for behavioral neuroscience , 2013, Behavioural Brain Research.

[104]  Andras Nagy,et al.  Cre recombinase: The universal reagent for genome tailoring , 2000, Genesis.

[105]  E. Dejana,et al.  Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice , 2011, The Journal of experimental medicine.

[106]  V. Murthy,et al.  Coupling of Neural Activity to Blood Flow in Olfactory Glomeruli Is Mediated by Astrocytic Pathways , 2008, Neuron.

[107]  P Chambon,et al.  Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. , 1997, Biochemical and biophysical research communications.

[108]  D. Metzger,et al.  Temporally controlled somatic mutagenesis in smooth muscle , 2000, Genesis.

[109]  D. Kleinfeld,et al.  Fluctuating and sensory-induced vasodynamics in rodent cortex extend arteriole capacity , 2011, Proceedings of the National Academy of Sciences.

[110]  Staci A. Sorensen,et al.  Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation , 2014, Front. Neural Circuits.

[111]  J. Dougherty,et al.  Aldh1L1 is expressed by postnatal neural stem cells in vivo , 2013, Glia.

[112]  Shiaoching Gong,et al.  A gene expression atlas of the central nervous system based on bacterial artificial chromosomes , 2003, Nature.

[113]  Fan Wang,et al.  Intersectional Cre Driver Lines Generated Using Split-Intein Mediated Split-Cre Reconstitution , 2012, Scientific Reports.

[114]  R. Deane,et al.  SRF and myocardin regulate LRP-mediated amyloid-β clearance in brain vascular cells , 2009, Nature Cell Biology.

[115]  E. Englund,et al.  Brain pericytes acquire a microglial phenotype after stroke , 2014, Acta Neuropathologica.

[116]  G. E. Vates,et al.  A Paravascular Pathway Facilitates CSF Flow Through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid β , 2012, Science Translational Medicine.

[117]  S. Arber,et al.  A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling , 2005, PLoS biology.

[118]  Bruno Cauli,et al.  in vivo 3D Morphology of Astrocyte—Vasculature Interactions in the Somatosensory Cortex: Implications for Neurovascular Coupling , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[119]  Maiken Nedergaard,et al.  Paravascular microcirculation facilitates rapid lipid transport and astrocyte signaling in the brain , 2013, Scientific Reports.

[120]  J. Wolfe,et al.  Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. , 2006, Molecular therapy : the journal of the American Society of Gene Therapy.

[121]  W. Denk,et al.  Two-photon laser scanning fluorescence microscopy. , 1990, Science.

[122]  X. Tong,et al.  GABA neurons provide a rich input to microvessels but not nitric oxide neurons in the rat cerebral cortex: A means for direct regulation of local cerebral blood flow , 2000, The Journal of comparative neurology.

[123]  B. Zlokovic,et al.  Pericyte loss influences Alzheimer-like neurodegeneration in mice , 2013, Nature Communications.

[124]  H. Taniguchi,et al.  Cre-dependent adeno-associated virus preparation and delivery for labeling neurons in the mouse brain. , 2014, Cold Spring Harbor protocols.

[125]  B. Lowell,et al.  Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. , 2011, Cell metabolism.

[126]  Benjamin R. Arenkiel,et al.  In Vivo Light-Induced Activation of Neural Circuitry in Transgenic Mice Expressing Channelrhodopsin-2 , 2007, Neuron.

[127]  T. Davis,et al.  The Blood-Brain Barrier/Neurovascular Unit in Health and Disease , 2005, Pharmacological Reviews.

[128]  F. D’Acquisto,et al.  Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo , 2012, The Journal of experimental medicine.

[129]  Jonas Frisén,et al.  Transgenic mice for conditional gene manipulation in astroglial cells , 2007, Glia.

[130]  Caiying Guo,et al.  Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon cre‐mediated excision , 2000, Genesis.

[131]  Turgay Dalkara,et al.  Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery , 2009, Nature Medicine.

[132]  J. Nathans,et al.  Norrin/Frizzled4 Signaling in Retinal Vascular Development and Blood Brain Barrier Plasticity , 2012, Cell.

[133]  Dae-Shik Kim,et al.  Global and local fMRI signals driven by neurons defined optogenetically by type and wiring , 2010, Nature.

[134]  L. Ment,et al.  Early Postnatal Astroglial Cells Produce Multilineage Precursors and Neural Stem Cells In Vivo , 2006, The Journal of Neuroscience.

[135]  J. Rothstein,et al.  Molecular comparison of GLT1+ and ALDH1L1+ astrocytes in vivo in astroglial reporter mice , 2011, Glia.

[136]  A. Nimmerjahn,et al.  Stepwise Recruitment of Transcellular and Paracellular Pathways Underlies Blood-Brain Barrier Breakdown in Stroke , 2014, Neuron.

[137]  R. Hammer,et al.  Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. , 2001, Developmental biology.

[138]  J. R. Mauban,et al.  A method for noninvasive longitudinal measurements of [Ca2+] in arterioles of hypertensive optical biosensor mice. , 2014, American journal of physiology. Heart and circulatory physiology.

[139]  R. Hammer,et al.  Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[140]  C. Betsholtz,et al.  Generation and Characterization of rgs5 Mutant Mice , 2008, Molecular and Cellular Biology.

[141]  R. Ho,et al.  Development and characterization of transgenic mouse models for conditional gene knockout in the blood–brain and blood-CSF barriers , 2011, Transgenic Research.

[142]  Tyson N. Kim,et al.  Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice , 2008, Proceedings of the National Academy of Sciences.

[143]  F. Kirchhoff,et al.  GFAP promoter‐controlled EGFP‐expressing transgenic mice: A tool to visualize astrocytes and astrogliosis in living brain tissue , 2001, Glia.

[144]  Guy Salama,et al.  Propagated Endothelial Ca2+ Waves and Arteriolar Dilation In Vivo: Measurements in Cx40BAC-GCaMP2 Transgenic Mice , 2007, Circulation research.

[145]  Bengt R. Johansson,et al.  Pericytes regulate the blood–brain barrier , 2010, Nature.

[146]  X. Breakefield,et al.  Viral vectors for gene delivery to the nervous system , 2003, Nature Reviews Neuroscience.

[147]  R. Dringen,et al.  Differential Effects of Iodoacetamide and Iodoacetate on Glycolysis and Glutathione Metabolism of Cultured Astrocytes , 2009, Front. Neuroenerg..