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Perspective

In vivo imaging of the neurovascular unit in CNS disease

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Pages 87-94 | Received 16 Aug 2012, Accepted 12 Sep 2012, Published online: 01 Oct 2012

References

  • Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 1990; 248:73 - 6; http://dx.doi.org/10.1126/science.2321027; PMID: 2321027
  • Gan WB, Grutzendler J, Wong WT, Wong RO, Lichtman JW. Multicolor “DiOlistic” labeling of the nervous system using lipophilic dye combinations. Neuron 2000; 27:219 - 25; http://dx.doi.org/10.1016/S0896-6273(00)00031-3; PMID: 10985343
  • Helmchen F, Svoboda K, Denk W, Tank DW. In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci 1999; 2:989 - 96; http://dx.doi.org/10.1038/14788; PMID: 10526338
  • Lendvai B, Stern EA, Chen B, Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 2000; 404:876 - 81; http://dx.doi.org/10.1038/35009107; PMID: 10786794
  • Svoboda K, Helmchen F, Denk W, Tank DW. Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat Neurosci 1999; 2:65 - 73; http://dx.doi.org/10.1038/4569; PMID: 10195182
  • Misgeld T, Kerschensteiner M. In vivo imaging of the diseased nervous system. Nat Rev Neurosci 2006; 7:449 - 63; http://dx.doi.org/10.1038/nrn1905; PMID: 16715054
  • Hillman EM. Optical brain imaging in vivo: techniques and applications from animal to man. J Biomed Opt 2007; 12:051402; http://dx.doi.org/10.1117/1.2789693; PMID: 17994863
  • Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 2004; 1:31 - 7; http://dx.doi.org/10.1038/nmeth706; PMID: 15782150
  • Yoder EJ. In Vivo Microscopy of the Mouse Brain Using Multiphoton Laser Scanning Techniques. Proc Soc Photo Opt Instrum Eng 2002; 4620:14 - 29; PMID: 20975841
  • Zlokovic BV. Neurodegeneration and the neurovascular unit. Nat Med 2010; 16:1370 - 1; http://dx.doi.org/10.1038/nm1210-1370; PMID: 21135839
  • Baeten KM, Akassoglou K. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev Neurobiol 2011; 71:1018 - 39; http://dx.doi.org/10.1002/dneu.20954; PMID: 21780303
  • Barker AJ, Ullian EM. Astrocytes and synaptic plasticity. Neuroscientist 2010; 16:40 - 50; http://dx.doi.org/10.1177/1073858409339215; PMID: 20236948
  • Takano T, Han X, Deane R, Zlokovic B, Nedergaard M. Two-photon imaging of astrocytic Ca2+ signaling and the microvasculature in experimental mice models of Alzheimer’s disease. Ann N Y Acad Sci 2007; 1097:40 - 50; http://dx.doi.org/10.1196/annals.1379.004; PMID: 17413008
  • Andriezen WL. The neuroglia elements in the human brain. Br Med J 1893; 2:227 - 30; http://dx.doi.org/10.1136/bmj.2.1700.227; PMID: 20754383
  • Grutzendler J, Kasthuri N, Gan WB. Long-term dendritic spine stability in the adult cortex. Nature 2002; 420:812 - 6; http://dx.doi.org/10.1038/nature01276; PMID: 12490949
  • Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002; 420:788 - 94; http://dx.doi.org/10.1038/nature01273; PMID: 12490942
  • Bhatt DH, Zhang S, Gan WB. Dendritic spine dynamics. Annu Rev Physiol 2009; 71:261 - 82; http://dx.doi.org/10.1146/annurev.physiol.010908.163140; PMID: 19575680
  • Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 2005; 8:752 - 8; http://dx.doi.org/10.1038/nn1472; PMID: 15895084
  • Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005; 308:1314 - 8; http://dx.doi.org/10.1126/science.1110647; PMID: 15831717
  • Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 2012; 74:691 - 705; http://dx.doi.org/10.1016/j.neuron.2012.03.026; PMID: 22632727
  • Tremblay ME, Lowery RL, Majewska AK. Microglial interactions with synapses are modulated by visual experience. PLoS Biol 2010; 8:e1000527; http://dx.doi.org/10.1371/journal.pbio.1000527; PMID: 21072242
  • Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 2009; 29:3974 - 80; http://dx.doi.org/10.1523/JNEUROSCI.4363-08.2009; PMID: 19339593
  • Merlini M, Meyer EP, Ulmann-Schuler A, Nitsch RM. Vascular β-amyloid and early astrocyte alterations impair cerebrovascular function and cerebral metabolism in transgenic arcAβ mice. Acta Neuropathol 2011; 122:293 - 311; http://dx.doi.org/10.1007/s00401-011-0834-y; PMID: 21688176
  • Stanimirovic DB, Friedman A. Pathophysiology of the neurovascular unit: disease cause or consequence?. J Cereb Blood Flow Metab 2012; 32:1207 - 21; http://dx.doi.org/10.1038/jcbfm.2012.25; PMID: 22395208
  • Helmchen F, Kleinfeld D. Chapter 10. In vivo measurements of blood flow and glial cell function with two-photon laser-scanning microscopy. Methods Enzymol 2008; 444:231 - 54; http://dx.doi.org/10.1016/S0076-6879(08)02810-3; PMID: 19007667
  • Masamoto K, Tomita Y, Toriumi H, Aoki I, Unekawa M, Takuwa H, et al. Repeated longitudinal in vivo imaging of neuro-glio-vascular unit at the peripheral boundary of ischemia in mouse cerebral cortex. Neuroscience 2012; 212:190 - 200; http://dx.doi.org/10.1016/j.neuroscience.2012.03.034; PMID: 22516017
  • Zhang ZG, Zhang L, Ding G, Jiang Q, Zhang RL, Zhang X, et al. A model of mini-embolic stroke offers measurements of the neurovascular unit response in the living mouse. Stroke 2005; 36:2701 - 4; http://dx.doi.org/10.1161/01.STR.0000190007.18897.e3; PMID: 16269633
  • Lam CK, Yoo T, Hiner B, Liu Z, Grutzendler J. Embolus extravasation is an alternative mechanism for cerebral microvascular recanalization. Nature 2010; 465:478 - 82; http://dx.doi.org/10.1038/nature09001; PMID: 20505729
  • Tagami M, Nara Y, Kubota A, Fujino H, Yamori Y. Ultrastructural changes in cerebral pericytes and astrocytes of stroke-prone spontaneously hypertensive rats. Stroke 1990; 21:1064 - 71; http://dx.doi.org/10.1161/01.STR.21.7.1064; PMID: 2368108
  • Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010; 68:409 - 27; http://dx.doi.org/10.1016/j.neuron.2010.09.043; PMID: 21040844
  • Fumagalli S, Coles JA, Ejlerskov P, Ortolano F, Bushell TJ, Brewer JM, et al. In vivo real-time multiphoton imaging of T lymphocytes in the mouse brain after experimental stroke. Stroke 2011; 42:1429 - 36; http://dx.doi.org/10.1161/STROKEAHA.110.603704; PMID: 21441145
  • Fernández-Klett F, Offenhauser N, Dirnagl U, Priller J, Lindauer U. Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci U S A 2010; 107:22290 - 5; http://dx.doi.org/10.1073/pnas.1011321108; PMID: 21135230
  • Masuda T, Croom D, Hida H, Kirov SA. Capillary blood flow around microglial somata determines dynamics of microglial processes in ischemic conditions. Glia 2011; 59:1744 - 53; http://dx.doi.org/10.1002/glia.21220; PMID: 21800362
  • Chuquet J, Hollender L, Nimchinsky EA. High-resolution in vivo imaging of the neurovascular unit during spreading depression. J Neurosci 2007; 27:4036 - 44; http://dx.doi.org/10.1523/JNEUROSCI.0721-07.2007; PMID: 17428981
  • Tymianski M. Emerging mechanisms of disrupted cellular signaling in brain ischemia. Nat Neurosci 2011; 14:1369 - 73; http://dx.doi.org/10.1038/nn.2951; PMID: 22030547
  • Brown CE, Li P, Boyd JD, Delaney KR, Murphy TH. Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci 2007; 27:4101 - 9; http://dx.doi.org/10.1523/JNEUROSCI.4295-06.2007; PMID: 17428988
  • Johnston DG, Denizet M, Mostany R, Portera-Cailliau C. Chronic In Vivo Imaging Shows No Evidence of Dendritic Plasticity or Functional Remapping in the Contralesional Cortex after Stroke. Cereb Cortex 2012; In press http://dx.doi.org/10.1093/cercor/bhs092; PMID: 22499800
  • Murphy TH, Li P, Betts K, Liu R. Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J Neurosci 2008; 28:1756 - 72; http://dx.doi.org/10.1523/JNEUROSCI.5128-07.2008; PMID: 18272696
  • Lassmann H. Axonal and neuronal pathology in multiple sclerosis: what have we learnt from animal models. Exp Neurol 2010; 225:2 - 8; http://dx.doi.org/10.1016/j.expneurol.2009.10.009; PMID: 19840788
  • Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hövelmeyer N, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 2005; 11:146 - 52; http://dx.doi.org/10.1038/nm1177; PMID: 15665833
  • Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 2011; 14:1142 - 9; http://dx.doi.org/10.1038/nn.2887; PMID: 21804537
  • Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, et al. The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 2007; 204:571 - 82; http://dx.doi.org/10.1084/jem.20061931; PMID: 17339406
  • Adams RA, Schachtrup C, Davalos D, Tsigelny I, Akassoglou K. Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis. Curr Med Chem 2007; 14:2925 - 36; http://dx.doi.org/10.2174/092986707782360015; PMID: 18045138
  • Siffrin V, Radbruch H, Glumm R, Niesner R, Paterka M, Herz J, et al. In vivo imaging of partially reversible th17 cell-induced neuronal dysfunction in the course of encephalomyelitis. Immunity 2010; 33:424 - 36; http://dx.doi.org/10.1016/j.immuni.2010.08.018; PMID: 20870176
  • Bartholomäus I, Kawakami N, Odoardi F, Schläger C, Miljkovic D, Ellwart JW, et al. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 2009; 462:94 - 8; http://dx.doi.org/10.1038/nature08478; PMID: 19829296
  • Nikić I, Merkler D, Sorbara C, Brinkoetter M, Kreutzfeldt M, Bareyre FM, et al. A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 2011; 17:495 - 9; http://dx.doi.org/10.1038/nm.2324; PMID: 21441916
  • Davalos D, Lee JK, Smith WB, Brinkman B, Ellisman MH, Zheng B, et al. Stable in vivo imaging of densely populated glia, axons and blood vessels in the mouse spinal cord using two-photon microscopy. J Neurosci Methods 2008; 169:1 - 7; http://dx.doi.org/10.1016/j.jneumeth.2007.11.011; PMID: 18192022
  • Davalos D, Akassoglou K. In vivo imaging of the mouse spinal cord using two-photon microscopy. J Vis Exp 2012; 59:e2760; PMID: 22258623
  • Kim JV, Jiang N, Tadokoro CE, Liu L, Ransohoff RM, Lafaille JJ, et al. Two-photon laser scanning microscopy imaging of intact spinal cord and cerebral cortex reveals requirement for CXCR6 and neuroinflammation in immune cell infiltration of cortical injury sites. J Immunol Methods 2010; 352:89 - 100; http://dx.doi.org/10.1016/j.jim.2009.09.007; PMID: 19800886
  • Pimplikar SW. Reassessing the amyloid cascade hypothesis of Alzheimer’s disease. Int J Biochem Cell Biol 2009; 41:1261 - 8; http://dx.doi.org/10.1016/j.biocel.2008.12.015; PMID: 19124085
  • Bacskai BJ, Kajdasz ST, Christie RH, Carter C, Games D, Seubert P, et al. Imaging of amyloid-beta deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy. Nat Med 2001; 7:369 - 72; http://dx.doi.org/10.1038/85525; PMID: 11231639
  • Burgold S, Bittner T, Dorostkar MM, Kieser D, Fuhrmann M, Mitteregger G, et al. In vivo multiphoton imaging reveals gradual growth of newborn amyloid plaques over weeks. Acta Neuropathol 2011; 121:327 - 35; http://dx.doi.org/10.1007/s00401-010-0787-6; PMID: 21136067
  • Skoch J, Hickey GA, Kajdasz ST, Hyman BT, Bacskai BJ. In vivo imaging of amyloid-beta deposits in mouse brain with multiphoton microscopy. Methods Mol Biol 2005; 299:349 - 63; PMID: 15980616
  • Dong J, Revilla-Sanchez R, Moss S, Haydon PG. Multiphoton in vivo imaging of amyloid in animal models of Alzheimer’s disease. Neuropharmacology 2010; 59:268 - 75; http://dx.doi.org/10.1016/j.neuropharm.2010.04.007; PMID: 20398680
  • Yan P, Bero AW, Cirrito JR, Xiao Q, Hu X, Wang Y, et al. Characterizing the appearance and growth of amyloid plaques in APP/PS1 mice. J Neurosci 2009; 29:10706 - 14; http://dx.doi.org/10.1523/JNEUROSCI.2637-09.2009; PMID: 19710322
  • Hefendehl JK, Wegenast-Braun BM, Liebig C, Eicke D, Milford D, Calhoun ME, et al. Long-term in vivo imaging of β-amyloid plaque appearance and growth in a mouse model of cerebral β-amyloidosis. J Neurosci 2011; 31:624 - 9; http://dx.doi.org/10.1523/JNEUROSCI.5147-10.2011; PMID: 21228171
  • Cortes-Canteli M, Paul J, Norris EH, Bronstein R, Ahn HJ, Zamolodchikov D, et al. Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer’s disease. Neuron 2010; 66:695 - 709; http://dx.doi.org/10.1016/j.neuron.2010.05.014; PMID: 20547128
  • Condello C, Schain A, Grutzendler J. Multicolor time-stamp reveals the dynamics and toxicity of amyloid deposition. Sci Rep 2011; 1:19; http://dx.doi.org/10.1038/srep00019; PMID: 22355538
  • Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G, et al. Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease. Nat Neurosci 2010; 13:411 - 3; http://dx.doi.org/10.1038/nn.2511; PMID: 20305648
  • Liu Z, Condello C, Schain A, Harb R, Grutzendler J. CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-β phagocytosis. J Neurosci 2010; 30:17091 - 101; http://dx.doi.org/10.1523/JNEUROSCI.4403-10.2010; PMID: 21159979
  • Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, et al. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 2003; 9:453 - 7; http://dx.doi.org/10.1038/nm838; PMID: 12612547
  • Spires-Jones TL, Mielke ML, Rozkalne A, Meyer-Luehmann M, de Calignon A, Bacskai BJ, et al. Passive immunotherapy rapidly increases structural plasticity in a mouse model of Alzheimer disease. Neurobiol Dis 2009; 33:213 - 20; http://dx.doi.org/10.1016/j.nbd.2008.10.011; PMID: 19028582
  • Tsai J, Grutzendler J, Duff K, Gan WB. Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat Neurosci 2004; 7:1181 - 3; http://dx.doi.org/10.1038/nn1335; PMID: 15475950
  • Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, et al. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 2005; 25:7278 - 87; http://dx.doi.org/10.1523/JNEUROSCI.1879-05.2005; PMID: 16079410
  • Bittner T, Fuhrmann M, Burgold S, Ochs SM, Hoffmann N, Mitteregger G, et al. Multiple events lead to dendritic spine loss in triple transgenic Alzheimer’s disease mice. PLoS One 2010; 5:e15477; http://dx.doi.org/10.1371/journal.pone.0015477; PMID: 21103384
  • Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, et al. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer’s disease. Science 2008; 321:1686 - 9; http://dx.doi.org/10.1126/science.1162844; PMID: 18802001
  • de la Torre JC. Is Alzheimer’s disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 2004; 3:184 - 90; http://dx.doi.org/10.1016/S1474-4422(04)00683-0; PMID: 14980533
  • Bullen A. Microscopic imaging techniques for drug discovery. Nat Rev Drug Discov 2008; 7:54 - 67; http://dx.doi.org/10.1038/nrd2446; PMID: 18079755
  • Borsook D, Becerra L, Hargreaves R. A role for fMRI in optimizing CNS drug development. Nat Rev Drug Discov 2006; 5:411 - 24; http://dx.doi.org/10.1038/nrd2027; PMID: 16604100
  • Sashindranath M, Sales E, Daglas M, Freeman R, Samson AL, Cops EJ, et al. The tissue-type plasminogen activator-plasminogen activator inhibitor 1 complex promotes neurovascular injury in brain trauma: evidence from mice and humans. Brain 2012; In press; http://dx.doi.org/10.1093/brain/aws178; PMID: 22822039
  • Lee DK, Nahrendorf M, Schellingerhout D, Kim DE. Will molecular optical imaging have clinically important roles in stroke management, and how?. J Clin Neurol 2010; 6:10 - 8; http://dx.doi.org/10.3988/jcn.2010.6.1.10; PMID: 20386638
  • Chen B, Friedman B, Whitney MA, Winkle JA, Lei IF, Olson ES, et al. Thrombin activity associated with neuronal damage during acute focal ischemia. J Neurosci 2012; 32:7622 - 31; http://dx.doi.org/10.1523/JNEUROSCI.0369-12.2012; PMID: 22649241
  • Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, et al. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 2001; 33:72 - 86; http://dx.doi.org/10.1002/1098-1136(20010101)33:1<72::AID-GLIA1007>3.0.CO;2-A; PMID: 11169793
  • Guo F, Maeda Y, Ma J, Delgado M, Sohn J, Miers L, et al. Macroglial plasticity and the origins of reactive astroglia in experimental autoimmune encephalomyelitis. J Neurosci 2011; 31:11914 - 28; http://dx.doi.org/10.1523/JNEUROSCI.1759-11.2011; PMID: 21849552
  • Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000; 20:4106 - 14; http://dx.doi.org/10.1128/MCB.20.11.4106-4114.2000; PMID: 10805752
  • Hirase H, Creso J, Singleton M, Barthó P, Buzsáki G. Two-photon imaging of brain pericytes in vivo using dextran-conjugated dyes. Glia 2004; 46:95 - 100; http://dx.doi.org/10.1002/glia.10295; PMID: 14999817
  • Yokota T, Kawakami Y, Nagai Y, Ma JX, Tsai JY, Kincade PW, et al. Bone marrow lacks a transplantable progenitor for smooth muscle type alpha-actin-expressing cells. Stem Cells 2006; 24:13 - 22; http://dx.doi.org/10.1634/stemcells.2004-0346; PMID: 16099999
  • Proebstl D, Voisin MB, Woodfin A, Whiteford J, D’Acquisto F, Jones GE, et al. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. J Exp Med 2012; 209:1219 - 34; http://dx.doi.org/10.1084/jem.20111622; PMID: 22615129
  • Motoike T, Loughna S, Perens E, Roman BL, Liao W, Chau TC, et al. Universal GFP reporter for the study of vascular development. Genesis 2000; 28:75 - 81; http://dx.doi.org/10.1002/1526-968X(200010)28:2<75::AID-GENE50>3.0.CO;2-S; PMID: 11064424
  • Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28:41 - 51; http://dx.doi.org/10.1016/S0896-6273(00)00084-2; PMID: 11086982