A murine toolbox for imaging the neurovascular unit

Microcirculation

Volumn 22, Issue 3, 2015, Pages 168-182

  Hartmann, David A ^a   Underly, Robert G ^a   Watson, Ashley N ^a   Shih, Andy Y ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Arteriole; Astrocyte; Capillary; Cerebral blood flow; Cre recombinase; Endothelium; Pericyte; Two photon microscopy; Vascular smooth muscle; Vasculature

Indexed keywords

ASTROCYTE; BLOOD VESSEL; BRAIN BLOOD FLOW; BRAIN CIRCULATION; ENDOTHELIUM CELL; IMAGING; MICROSCOPY; NERVE CELL; NEUROVASCULAR UNIT; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SMOOTH MUSCLE FIBER; TRANSGENIC MOUSE; ANIMAL; BLOOD BRAIN BARRIER; CYTOLOGY; HUMAN; MOLECULAR IMAGING; MOUSE; NEUROVASCULAR COUPLING; PROCEDURES;

MURINAE;

ANIMALS; BLOOD-BRAIN BARRIER; HUMANS; MICE; MICE, TRANSGENIC; MOLECULAR IMAGING; NEUROVASCULAR COUPLING;

EID: 84926461872     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12176     Document Type: Review

References (145)

1. Abe T, Fujimori T. Reporter mouse lines for fluorescence imaging. Dev Growth Differ 55: 390-405, 2013.
2. Akemann W, Sasaki M, Mutoh H, Imamura T, Honkura N, Knöpfel T. Two-photon voltage imaging using a genetically encoded voltage indicator. Sci Rep 3: 2231, 2013.
3. Alva JA, Zovein AC, Monvoisin A, Murphy T, Salazar A, Harvey NL, Carmeliet P, Iruela-Arispe ML. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn 235: 759-767, 2006.
4. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ, Ehlers MD, Feng G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54: 205-218, 2007.
5. Armulik A, Genové G, Mäe M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. Pericytes regulate the blood-brain barrier. Nature 468: 557-561, 2010.
6. Asrican B, Augustine GJ, Berglund K, Chen S, Chow N, Deisseroth K, Feng G, Gloss B, Hira R, Hoffmann C, Kasai H, Katarya M, Kim J, Kudolo J, Lee LM, Lo SQ, Mancuso J, Matsuzaki M, Nakajima R, Qiu L, Tan G, Tang Y, Ting JT, Tsuda S, Wen L, Zhang X, Zhao S. Next-generation transgenic mice for optogenetic analysis of neural circuits. Front Neural Circuits 7: 160, 2013.
7. Attwell D, Buchan AM, Charpak S, Lauritzen M, MacVicar BA, Newman EA. Glial and neuronal control of brain blood flow. Nature 468: 232-243, 2010.
8. Bardehle S, Krüger M, Buggenthin F, Schwausch J, Ninkovic J, Clevers H, Snippert HJ, Theis FJ, Meyer-Luehmann M, Bechmann I, Dimou L, Götz M. Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat Neurosci 16: 580-586, 2013.
9. Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie DC, Beckers J, Yoder B, Irmler M, Götz M. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7: 744-758, 2010.
10. Bell RD, Deane R, Chow N, Long X, Sagare A, Singh I, Streb JW, Guo H, Rubio A, Van Nostrand W, Miano JM, Zlokovic BV. SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat Cell Biol 11: 143-153, 2009.
11. Bell RD, Winkler EA, Sagare AP, Singh I, LaRue B, Deane R, Zlokovic BV. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68: 409-427, 2010.
12. Bi B, Salmaso N, Komitova M, Simonini MV, Silbereis J, Cheng E, Kim J, Luft S, Ment LR, Horvath TL, Schwartz ML, Vaccarino FM. Cortical glial fibrillary acidic protein-positive cells generate neurons after perinatal hypoxic injury. J Neurosci 31: 9205-9221, 2011.
13. Bonder DE, McCarthy KD. Astrocytic Gq-GPCR-linked IP3R-dependent Ca2+ signaling does not mediate neurovascular coupling in mouse visual cortex in vivo. J Neurosci 34: 13139-13150, 2014.
14. Boulday G, Rudini N, Maddaluno L, Blécon A, Arnould M, Gaudric A, Chapon F, Adams RH, Dejana E, Tournier-Lasserve E. Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J Exp Med 208: 1835-1847, 2011.
15. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268, 2005.
16. Casanova E, Lemberger T, Fehsenfeld S, Mantamadiotis T, Schütz G. Alpha complementation in the Cre recombinase enzyme. Genesis 37: 25-29, 2003.
17. Cauli B, Hamel E. Revisiting the role of neurons in neurovascular coupling. Front Neuroenergetics 2: 9, 2010.
18. Cauli B, Tong XK, Rancillac A, Serluca N, Lambolez B, Rossier J, Hamel E. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J Neurosci 24: 8940-8949, 2004.
19. Cearley CN, Vandenberghe LH, Parente MK, Carnish ER, Wilson JM, Wolfe JH. Expanded repertoire of AAV vector serotypes mediate unique patterns of transduction in mouse brain. Mol Ther 16: 1710-1718, 2008.
20. Cearley CN, Wolfe JH. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol Ther 13: 528-537, 2006.
21. Chan AC, Drakos SG, Ruiz OE, Smith AC, Gibson CC, Ling J, Passi SF, Stratman AN, Sacharidou A, Revelo MP, Grossmann AH, Diakos NA, Davis GE, Metzstein MM, Whitehead KJ, Li DY. Mutations in 2 distinct genetic pathways result in cerebral cavernous malformations in mice. J Clin Invest 121: 1871-1881, 2011.
22. Chen Q, Cichon J, Wang W, Qiu L, Lee SJ, Campbell NR, Destefino N, Goard MJ, Fu Z, Yasuda R, Looger LL, Arenkiel BR, Gan WB, Feng G. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76: 297-308, 2012.
23. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499: 295-300, 2013.
24. Chow LM, Zhang J, Baker SJ. Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells. Transgenic Res 17: 919-928, 2008.
25. Claxton S, Kostourou V, Jadeja S, Chambon P, Hodivala-Dilke K, Fruttiger M. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis 46: 74-80, 2008.
26. Crouthamel MH, Kelly EJ, Ho RJ. Development and characterization of transgenic mouse models for conditional gene knockout in the blood-brain and blood-CSF barriers. Transgenic Res 21: 113-130, 2011.
27. Cuttler AS, LeClair RJ, Stohn JP, Wang Q, Sorenson CM, Liaw L, Lindner V. Characterization of Pdgfrb-Cre transgenic mice reveals reduction of ROSA26 reporter activity in remodeling arteries. Genesis 49: 673-680, 2011.
28. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468: 562-566, 2010.
29. Davidson BL, Breakefield XO. Viral vectors for gene delivery to the nervous system. Nat Rev Neurosci 4: 353-364, 2003.
30. Davy A, Soriano P. Ephrin-B2 forward signaling regulates somite patterning and neural crest cell development. Dev Biol 304: 182-193, 2007.
31. Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science 248: 73-76, 1990.
32. Desai M, Kahn I, Knoblich U, Bernstein J, Atallah H, Yang A, Kopell N, Buckner RL, Graybiel AM, Moore CI, Boyden ES. Mapping brain networks in awake mice using combined optical neural control and fMRI. J Neurophysiol 105: 1393-1405, 2011.
33. Devor A, Tian P, Nishimura N, Teng IC, Hillman EM, Narayanan SN, Ulbert I, Boas DA, Kleinfeld D, Dale AM. Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signaling. J Neurosci 27: 4452-4459, 2007.
34. Drew PJ, Shih AY, Kleinfeld D. Fluctuating and sensory-induced vasodynamics in rodent cortex extends arteriole capacity. Proc Natl Acad Sci USA 108: 8473-8478, 2011.
35. Feil R, Wagner J, Metzger D, Chambon P. Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 237: 752-757, 1997.
36. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes Jr. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51, 2000.
37. 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 107: 22290-22295, 2010.
38. Foo LC, Dougherty JD. Aldh1L1 is expressed by postnatal neural stem cells in vivo. Glia 61: 1533-1541, 2013.
39. Forde A, Constien R, Gröne HJ, Hämmerling G, Arnold B. Temporal Cre-mediated recombination exclusively in endothelial cells using Tie2 regulatory elements. Genesis 33: 191-197, 2002.
40. Fox EA, Biddinger JE, Jones KR, McAdams J, Worman A. Mechanism of hyperphagia contributing to obesity in brain-derived neurotrophic factor knockout mice. Neuroscience 229: 176-199, 2013.
41. Fukuhara S, Sako K, Noda K, Nagao K, Miura K, Mochizuki N. Tie2 is tied at the cell-cell contacts and to extracellular matrix by angiopoietin-1. Exp Mol Med 41: 133-139, 2009.
42. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26: 8609-8621, 2006.
43. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7: 1233-1241, 2004.
44. Gong S, Zheng1 C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925, 2003.
45. Göritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Frisén J. A pericyte origin of spinal cord scar tissue. Science 333: 238-242, 2011.
46. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of Parkinsonian neural circuitry. Science 324: 354-359, 2009.
47. Gregorian C, Nakashima J, Le Belle J, Ohab J, Kim R, Liu A, Smith KB, Groszer M, Garcia AD, Sofroniew MV, Carmichael ST, Kornblum HI, Liu X, Wu H. Pten deletion in adult neural stem/progenitor cells enhances constitutive neurogenesis. J Neurosci 29: 1874-1886, 2009.
48. Hall CN, Reynell C, Gesslein B, Hamilton NB, Mishra A, Sutherland BA, O'Farrell FM, Buchan AM, Lauritzen M, Attwell D. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 508: 55-60, 2014.
49. Harris JA, Hirokawa KE, Sorensen SA, Gu H, Mills M, Ng LL, Bohn P, Mortrud M, Ouellette B, Kidney J, Smith KA, Dang C, Sunkin S, Bernard A, Oh SW, Madisen L, Zeng H. Anatomical characterization of Cre driver mice for neural circuit mapping and manipulation. Front Neural Circuits 8: 76, 2014.
50. Haustein MD, Kracun S, Lu XH, Shih T, Jackson-Weaver O, Tong X, Xu J, Yang XW, O'Dell TJ, Marvin JS, Ellisman MH, Bushong EA, Looger LL, Khakh BS. Conditions and constraints for astrocyte calcium signaling in the hippocampal mossy fiber pathway. Neuron 82: 413-429, 2014.
51. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmcol Rev 57: 173-185, 2005.
52. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3: e159, 2005.
53. Hirrlinger PG, Scheller A, Braun C, Hirrlinger J, Kirchhoff F. Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen-inducible DNA recombinase variant CreERT2. Glia 54: 11-20, 2006.
54. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, Zetsche B, Hammer RE, Herz J, Kuhn M. Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci 99: 7142-7147, 2002.
55. Huang ZJ, Taniguchi H, He M, Kuhlman S. Cre-dependent adeno-associated virus preparation and delivery for labeling neurons in the mouse brain. Cold Spring Harb Protoc 2014: 190-194, 2014.
56. Huang ZJ, Zeng H. Genetic approaches to neural circuits in the mouse. Annu Rev Neurosci 16: 668-676, 2013.
57. Hughes EG, Kang SH, Fukaya M, Bergles DE. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 16: 668-676, 2013.
58. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid ß. Sci Transl Med 4: 147ra111, 2012.
59. Isotani E, Zhi G, Lau KS, Huang J, Mizuno Y, Persechini A, Geguchadze R, Kamm KE, Stull JT. Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc Natl Acad Sci 101: 6279-6284, 2004.
60. Ji G, Feldman ME, Deng KY, Greene KS, Wilson J, Lee JC, Johnston RC, Rishniw M, Tallini Y, Zhang J, Wier WG, Blaustein MP, Xin HB, Nakai J, Kotlikoff MI. Ca2+-sensing transgenic mice: postsynaptic signaling in smooth muscle. J Biol Chem 279: 21461-21468, 2004.
61. Kalmbach A, Hedrick T, Waters J. Selective optogenetic stimulation of cholinergic axons in neocortex. J Neurophysiol 107: 2008-2019, 2012.
62. Karram K, Goebbels S, Schwab M, Jennissen K, Seifert G, Steinhäuser C, Nave KA, Trotter J. NG2-expressing cells in the nervous system revealed by the NG2-EYFP-knockin mouse. Genesis 46: 743-757, 2008.
63. Kim JC, Dymecki SM. Genetic fate-mapping approaches: new means to explore the embryonic origins of the cochlear nucleus. Methods Mol Biol 493: 65-85, 2009.
64. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 230: 230-242, 2001.
65. Kleinfeld D, Blinder P, Drew PJ, Driscoll JD, Muller A, Tsai PS, Shih AY. A guide to delineate the logic of neurovascular signaling in the brain. Front Neuroenergetics 1: 1-9, 2011.
66. Kleinfeld D, Mitra PP, Helmchen F, Denk W. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc Natl Acad Sci USA 95: 15741-15746, 1998.
67. Knowland D, Arac A, Sekiguchi KJ, Hsu M, Lutz SE, Perrino J, Steinberg GK, Barres BA, Nimmerjahn A, Agalliu D. Stepwise recruitment of transcellular and paracellular pathways underlies blood-brain barrier breakdown in stroke. Neuron 82: 603-617, 2014.
68. Kocharyan A, Fernandes P, Tong XK, Vaucher E, Hamel E. Specific subtypes of cortical GABA interneurons contribute to the neurovascular coupling response to basal forebrain stimulation. J Cereb Blood Flow Metab 28: 221-231, 2008.
69. Kühbandner S, Brummer S, Metzger D, Chambon P, Hofmann F, Feil R. Temporally controlled somatic mutagenesis in smooth muscle. Genesis 28: 15-22, 2000.
70. Lam CK, Yoo T, Hiner B, Liu Z, Grutzendler J. Embolus extravasation is an alternative mechanism for cerebral microvascular recanalization. Nature 465: 478-482, 2010.
71. Lee JH, Durand R, Gradinaru V, Zhang F, Goshen I, Kim DS, Fenno LE, Ramakrishnan C, Deisseroth K. Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465: 788-792, 2010.
72. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 30: 16796-16808, 2010.
73. Lepore JJ, Cheng L, Min Lu M, Mericko PA, Morrisey EE, Parmacek MS. High-efficiency somatic mutagenesis in smooth muscle cells and cardiac myocytes in SM22alpha-Cre transgenic mice. Genesis 41: 179-184, 2005.
74. Li D, Agulhon C, Schmidt E, Oheim M, Ropert N. New tools for investigating astrocyte-to-neuron communication. Front Cell Neurosci 7: 193, 2013.
75. Luo L, Callaway EM, Svoboda K. Genetic dissection of neural circuits. Neuron 57: 635-660, 2008.
76. Lush ME, Li Y, Kwon CH, Chen J, Parada LF. Neurofibromin is required for barrel formation in the mouse somatosensory cortex. J Neurosci 28: 1580-1587, 2008.
77. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, Fujisawa S, Hsu YW, Garcia AJ, Gu X, Zanella S, Kidney J, Gu H, Mao Y, Hooks BM, Boyden ES, Buzsáki G, Ramirez JM, Jones AR, Svoboda K, Han X, Turner EE, Zeng H. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 15: 793-802, 2012.
78. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140, 2010.
79. Masamoto K, Takuwa H, Seki C, Taniguchi J, Itoh Y, Tomita Y, Toriumi H, Unekawa M, Kawaguchi H, Ito H, Suzuki N, Kanno I. Microvascular sprouting, extension, and creation of new capillary connections with adaptation of the neighboring astrocytes in adult mouse cortex under chronic hypoxia. J Cereb Blood Flow Metab 34: 325-331, 2014.
80. Mauban JR, Fairfax ST, Rizzo MA, Zhang J, Wier WG. A method for noninvasive longitudinal measurements of [Ca2+] in arterioles of hypertensive optical biosensor mice. Am J Physiol 307: H173-H181, 2014.
81. McCaslin AF, Chen BR, Radosevich AJ, Cauli B, Hillman EM. In vivo 3D morphology of astrocyte-vasculature interactions in the somatosensory cortex: implications for neurovascular coupling. J Cereb Blood Flow Metab 31: 795-806, 2010.
82. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30: 1582-1594, 2010.
83. Monvoisin A, Alva JA, Hofmann JJ, Zovein AC, Lane TF, Iruela-Arispe ML. VE-cadherin-CreERT2 transgenic mouse: a model for inducible recombination in the endothelium. Dev Dyn 235: 3413-3422, 2006.
84. Mori T, Tanaka K, Buffo A, Wurst W, Kühn R, Götz M. Inducible gene deletion in astroglia and radial glia-a valuable tool for functional and lineage analysis. Glia 54: 21-34, 2006.
85. Motoike T, Loughna S, Perens E, Roman BL, Liao W, Chau TC, Richardson CD, Kawate T, Kuno J, Weinstein BM, Stainier DY, Sato TN. Universal GFP reporter for the study of vascular development. Genesis 28: 75-81, 2000.
86. Murphy PA, Lam MT, Wu X, Kim TN, Vartanian SM, Bollen AW, Carlson TR, Wang RA. Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice. Proc Natl Acad Sci 105: 10901-10906, 2008.
87. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 45: 593-605, 2007.
88. Myers SA, DeVries WH, Andres KR, Gruenthal MJ, Benton RL, Hoying JB, Hagg T, Whittemore SR. CD47 knockout mice exhibit improved recovery from spinal cord injury. Neurobiol Dis 42: 21-34, 2011.
89. Nagy A. Cre recombinase: the universal reagent for genome tailoring. Genesis 26: 99-109, 2000.
90. Nelson MT, Patlak JB, Worley JF, Standen NB. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol 259: C3-C18, 1990.
91. Nguyen HL, Lee YJ, Shin J, Lee E, Park SO, McCarty JH, Oh SP. TGF-β signaling in endothelial cells, but not neuroepithelial cells, is essential for cerebral vascular development. Lab Invest 91: 1554-1563, 2011.
92. Nielsen CM, Dymecki SM. Sonic hedgehog is required for vascular outgrowth in the hindbrain choroid plexus. Dev Biol 340: 430-437, 2010.
93. Nisancioglu MH, Mahoney WMJ, Kimmel DD, Schwartz SM, Betsholtz C, Genové G. Generation and characterization of rgs5 mutant mice. Mol Cell Biol 28: 2324-2331, 2008.
94. Nishiyama A, Komitova M, Suzuki R, Zhu X. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat Rev Neurosci 10: 9-22, 2009.
95. Nizar K, Uhlirova H, Tian P, Saisan PA, Cheng Q, Reznichenko L, Weldy KL, Steed TC, Sridhar VB, MacDonald CL, Cui J, Gratiy SL, Sakadzic S, Boas DA, Beka TI, Einevoll GT, Chen J, Masliah E, Dale AM, Silva GA, Devor A. In vivo stimulus-induced vasodilation occurs without IP3 receptor activation and may precede astrocytic calcium increase. J Neurosci 33: 8411-8422, 2013.
96. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H. GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33: 72-86, 2001.
97. Novak A, Guo C, Yang W, Nagy A, Lobe CG. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28: 147-155, 2000.
98. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 407: 313-319, 1997.
99. Ozen I, Deierborg T, Miharada K, Padel T, Englund E, Genové G, Paul G. Brain pericytes acquire a microglial phenotype after stroke. Acta Neuropathol 128: 381-396, 2014.
100. Perrenoud Q, Rossier J, Férézou I, Geoffroy H, Gallopin T, Vitalis T, Rancillac A. Activation of cortical 5-HT(3) receptor-expressing interneurons induces NO mediated vasodilatations and NPY mediated vasoconstrictions. Front Neural Circuits 6: 50, 2012.
101. Petzold GC, Albeanu DF, Sato TF, Murthy VN. Coupling of neural activity to blood flow in olfactory glomeruli is mediated by astrocytic pathways. Neuron 58: 879-910, 2008.
102. Pfrieger FW, Slezak M. Genetic approaches to study glial cells in the rodent brain. Glia 60: 681-701, 2012.
103. Prakash R, Yizhar O, Grewe B, Ramakrishnan C, Wang N, Goshen I, Packer AM, Peterka DS, Yuste R, Schnitzer MJ, Deisseroth K. Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat Methods 9: 1171-1179, 2012.
104. Proebstl D, Voisin MB, Woodfin A, Whiteford J, D'Acquisto F, Jones GE, Rowe D, Nourshargh S. Pericytes support neutrophil subendothelial cell crawling and breaching of venular walls in vivo. J Exp Med 209: 1219-1234, 2012.
105. Rangroo Thrane V, Thrane AS, Plog BA, Thiyagarajan M, Iliff JJ, Deane R, Nagelhus EA, Nedergaard M. Paravascular microcirculation facilitates rapid lipid transport and astrocyte signaling in the brain. Sci Rep 3: 2582, 2013.
106. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 27: 6607-6619, 2007.
107. Regan CP, Manabe I, Owens GK. Development of a smooth muscle-targeted cre recombinase mouse reveals novel insights regarding smooth muscle myosin heavy chain promoter regulation. Circ Res 87: 363-369, 2000.
108. Rossi J, Balthasar N, Olson D, Scott M, Berglund E, Lee CE, Choi MJ, Lauzon D, Lowell BB, Elmquist JK. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab 13: 195-204, 2011.
109. Rotolo T, Smallwood PM, Williams J, Nathans J. Genetically-directed, cell type-specific sparse labeling for the analysis of neuronal morphology. PLoS ONE 3: e4099, 2008.
110. Sagare AP, Bell RD, Zhao Z, Ma Q, Winkler EA, Ramanathan A, Zlokovic BV. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat Commun 4: 2932, 2013.
111. Saito T, Nakatsuji N. Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240: 237-246, 2001.
112. Sato A, Sato Y. Regulation of regional cerebral blood flow by cholinergic fibers originating in the basal forebrain. Neurosci Res 14: 242-272, 1992.
113. Scott NA, Murphy TH. Hemodynamic responses evoked by neuronal stimulation via channelrhodopsin-2 can be independent of intracortical glutamatergic synaptic transmission. Public Library of Science One 7: e29859, 2012.
114. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572, 2004.
115. Shigetomi E, Bushong EA, Haustein MD, Tong X, Jackson-Weaver O, Kracun S, Xu J, Sofroniew MV, Ellisman MH, Khakh BS. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J Gen Physiol 141: 633-647, 2013.
116. Shih AY, Driscoll JD, Drew PJ, Nishimura N, Schaffer CB, Kleinfeld D. Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain. J Cereb Blood Flow Metab 32: 1277-1309, 2012.
117. Slezak M, Göritz C, Niemiec A, Frisén J, Chambon P, Metzger D, Pfrieger FW. Transgenic mice for conditional gene manipulation in astroglial cells. Glia 55: 1565-1576, 2007.
118. Sousa VH, Miyoshi G, Hjerling-Leffler J, Karayannis T, Fishell G. Characterization of Nk6-2-derived neocortical interneuron lineages. Cereb Cortex 19(Suppl. 1): i1-i10, 2009.
119. Sword J, Masuda T, Croom D, Kirov SA. Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging. Brain 136: 1446-1461, 2013.
120. Tallini YN, Brekke JF, Shui B, Doran R, Hwang SM, Nakai J, Salama G, Segal SS, Kotlikoff MI. Propagated endothelial Ca2+ waves and arteriolar dilation in vivo: measurements in Cx40BAC GCaMP2 transgenic mice. Circ Res 101: 1300-1309, 2007.
121. Tallini YN, Shui B, Greene KS, Deng KY, Doran R, Fisher PJ, Zipfel W, Kotlikoff MI. BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Phyiological Genomics 27: 391-397, 2006.
122. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71: 995-1013, 2011.
123. Ting JT, Feng G. Development of transgenic animals for optogenetic manipulation of mammalian nervous system function: progress and prospects for behavioral neuroscience. Behav Brain Res 255: 3-18, 2013.
124. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420: 788-794, 2002.
125. Urban A, Rancillac A, Martinez L, Rossier J. Deciphering the neuronal circuitry controlling local blood flow in the cerebral cortex with optogenetics in PV:Cre transgenic mice. Frontiers in Pharmacology 3: 105, 2012.
126. Vaucher E, Hamel E. Cholinergic basal forebrain neurons project to cortical microvessels in the rat: electron microscopic study with anterogradely transported Phaseolus vulgaris leucoagglutinin and choline acetyltransferase immunocytochemistry. J Neurosci 15: 7427-7441, 1995.
127. Vaucher E, Tong XK, Cholet N, Lantin S, Hamel E. 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. J Comp Neurol 421: 161-171, 2000.
128. Wang P, Chen T, Sakurai K, Han BX, He Z, Feng G, Wang F. Intersectional Cre driver lines generated using split-intein mediated split-Cre reconstitution. Sci Rep 2: 497, 2012.
129. Wang Y, Rattner A, Zhou Y, Williams J, Smallwood PM, Nathans J. Norrin/Frizzled4 signaling in retinal vascular development and blood brain barrier plasticity. Cell 151: 1332-1344, 2012.
130. Wendling O, Bornert JM, Chambon P, Metzger D. Efficient temporally-controlled targeted mutagenesis in smooth muscle cells of the adult mouse. Genesis 47: 14-18, 2009.
131. Whiteus C, Freitas C, Grutzendler J. Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period. Nature 505: 407-411, 2014.
132. Wirth A, Benyó Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horváth B, Maser-Gluth C, Greiner E, Lemmer B, Schütz G, Gutkind JS. Offermanns pp. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med 14: 64-68, 2008.
133. Wu Z, Yang L, Cai L, Zhang M, Cheng X, Yang X, Xu J. Detection of epithelial to mesenchymal transition in airways of a bleomycin induced pulmonary fibrosis model derived from an alpha-smooth muscle actin-Cre transgenic mouse. Respir Res 8: 1, 2007.
134. Xin HB, Deng KY, Rishniw M, Ji G, Kotlikoff MI. Smooth muscle expression of Cre recombinase and eGFP in transgenic mice. Physiol Genomics 10: 211-219, 2002.
135. Yang Y, Vidensky S, Jin L, Jie C, Lorenzini I, Frankl M, Rothstein JD. Molecular comparison of GLT1+ and ALDH1L1+ astrocytes in vivo in astroglial reporter mice. Glia 59: 200-207, 2011.
136. Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, Dalkara T. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med 15: 1031-1037, 2009.
137. Yokota T, Kawakami Y, Nagai Y, Ma JX, Tsai JY, Kincade PW, Sato S. Bone marrow lacks a transplantable progenitor for smooth muscle type alpha-actin-expressing cells. Stem Cells 24: 13-22, 2006.
138. Young KM, Mitsumori T, Pringle N, Grist M, Kessaris N, Richardson WD. An Fgfr3-iCreER(T2) transgenic mouse line for studies of neural stem cells and astrocytes. Glia 58: 943-953, 2010.
139. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw CI, Zeng H, Looger LL, Svoboda K, Chen TW. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. The Journal of Neuroscience 32: 3131-3141, 2012.
140. Zhao S, Ting JT, Atallah HE, Qiu L, Tan J, Gloss B, Augustine GJ, Deisseroth K, Luo M, Graybiel AM, Feng G. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat Methods 8: 745-752, 2011.
141. Zhu X, Bergles DE, Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135: 145-157, 2008.
142. Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. Age-dependent fate and lineage restriction of single NG2 cells. Development 138: 745-753, 2011.
143. ZhuGe Q, Wu Z, Huang L, Zhao B, Zhong M, Zheng W, GouRong C, Mao X, Xie L, Wang X, Jin K. Notch4 is activated in endothelial and smooth muscle cells in human brain arteriovenous malformations. J Cell Mol Med 17: 1458-1464, 2013.
144. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, Messing A. Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187: 36-42, 1997.
145. Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A. hGFAP-cre transgenic mice for the manipulation of glial and neuronal function in vivo. Genesis 31: 85-94, 2001.