Pericyte structure and distribution in the cerebral cortex revealed by high-resolution imaging of transgenic mice

Neurophotonics

Volumn 2, Issue 4, 2015, Pages

  Hartmann, David A ^a   Underly, Robert G ^a   Grant, Roger I ^a   Watson, Ashley N ^a   Lindner, Volkhard ^b   Shih, Andy Y ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b Maine Medical Center Research Institute   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

capillary; cerebral blood blow; microcirculation; pericyte; smooth muscle; two photon microscopy

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; IMAGE RECONSTRUCTION; MAMMALS; MICROCIRCULATION;

CAPILLARY; CEREBRAL BLOOD BLOW; PERICYTE; SMOOTH MUSCLES; TWO PHOTON MICROSCOPY;

BRAIN;

ANTIGEN; CRE RECOMBINASE; NEURAL GLIAL ANTIGEN 2; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN CORTEX; BRAIN PERICYTE; CELL LABELING; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NEUROIMAGING; NONHUMAN; SENSORY CORTEX; TRANSGENIC MOUSE;

EID: 84956522491     PISSN: 2329423X     EISSN: 23294248     Source Type: Journal    
DOI: 10.1117/1.NPh.2.4.041402     Document Type: Article

References (40)

1. C. Rouget, "Memoire sur le developpement la structure et les proprietes physiologiques des capillaires sanguins et lymphatiques," Arch. Physiol. Norm. Path. 5, 603-663 (1873).
2. A. Armulik et al., "Pericytes regulate the blood-brain barrier," Nature 468(7323), 557-561 (2010).
3. R. Daneman et al., "Pericytes are required for blood-brain barrier integrity during embryogenesis," Nature 468(7323), 562-566 (2010).
4. H. Gerhardt and C. Betsholtz, "Endothelial-pericyte interactions in angiogenesis," Cell Tissue Res. 314(1), 15-23 (2003).
5. C. N. Hall et al., "Capillary pericytes regulate cerebral blood flow in health and disease," Nature 508(7494), 55-60 (2014).
6. R. D. Bell et al., "Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging," Neuron 68, 409-427 (2010).
7. B. V. Zlokovic, "The blood-brain barrier in health and chronic neurodegenerative disorders," Neuron 57, 178-201 (2008).
8. P. Dore-Duffy, "Pericytes: pluripotent cells of the blood brain barrier," Curr. Pharm. Des. 14, 1581-1593 (2008).
9. M. Yemisci et al., "Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery," Nat. Med. 15, 1031-1037 (2009).
10. S. Lui et al., "The role of pericytes in blood-brain barrier function and stroke," Curr. Pharm. Des. 18, 3653-3662 (2012).
11. A. Armulik, G. Genove, and C. Betsholtz, "Pericytes: developmental, physiological, and pathological perspectives, problems and promises," Dev. Cell 21(2), 193-215 (2011).
12. H. A. Zariwala et al., "A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo," J. Neurosci. 32(9), 3131-3141 (2012).
13. L. Madisen et al., "A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing," Nat. Neurosci. 15(5), 793-802 (2012).
14. F. Fernández-Klett et al., "Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain," Proc. Natl. Acad. Sci. U. S. A. 107(51), 22290-22295 (2010).
15. A. Nagy, "Cre recombinase: the universal reagent for genome tailoring," Genesis 26(2), 99-109 (2000).
16. L. Madisen et al., "A robust and high-throughput Cre reporting and characterization system for the whole mouse brain," Nat. Neurosci. 13, 133-140 (2010).
17. D. A. Hartmann et al., "Murine toolbox for imaging the neurovascular unit," Microcirculation 22(3), 168-182 (2015).
18. U. Ozerdem et al., "NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis," Dev. Dyn. 222(2), 218-227 (2001).
19. A. S. Cuttler et al., "Characterization of Pdgfrb-Cre transgenic mice reveals reduction of ROSA26 reporter activity in remodeling arteries," Genesis 49(8), 673-680 (2011).
20. X. Zhu et al., "Age-dependent fate and lineage restriction of single NG2 cells," Development 138(4), 745-753 (2011).
21. N. C. Shaner et al., "Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein," Nat. Biotechnol. 22, 1567-1572 (2004).
22. K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron 50, 823-839 (2006).
23. J. Kunz et al., "The 140-kDa protein of blood-brain barrier-associated pericytes is identical to aminopeptidase N," J. Neurochem. 62(6), 2375-2786 (1994).
24. P. Lindahl et al., "Pericyte loss and microaneurysm formation in PDGFB- deficient mice," Science 277, 242-245 (1997).
25. F. Alliot et al., "Pericytes and periendothelial cells of brain parenchyma vessels co-express aminopeptidase N, aminopeptidase A, and nestin," J. Neurosci. Res. 58(3), 367-378 (1999).
26. A. Y. Shih et al., "Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain," J. Cereb. Blood Flow Metab. 32(7), 1277-1309 (2012).
27. M. Drobizhev et al., "Two-photon absorption properties of fluorescent proteins," Nat. Methods 8(5), 393-399 (2011).
28. I. Ushiwata and T. Ushiki, "Cytoarchitecture of the smooth muscles and pericytes of rat cerebral blood vessels," J. Neurosurg. 73, 82-90 (1990).
29. I. M. Herman and P. A. D'Amore, "Microvascular pericytes contain muscle and nonmuscle actins," J. Cell Biol. 101, 43-52 (1985).
30. P. S. Tsai et al., "Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of cell nuclei and microvessels," J. Neurosci. 29, 14553-14570 (2009).
31. V. Nehls and D. Drenckhahn, "Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin," J. Cell Biol. 113, 147-154 (1991).
32. P. Blinder and P et al., "The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow," Nat. Neurosci. 16, 889-897 (2013).
33. E. A.Winkler et al., "Blood-spinal cord barrier pericyte reductions contribute to increased capillary permeability," J. Cereb. Blood Flow Metab. 32(10), 1841-1852 (2012).
34. N. Makihara et al., "Involvement of platelet-derived growth factor receptor β in fibrosis through extracellular matrix protein production after ischemic stroke," Exp. Neurol. 264, 127-134 (2014).
35. E. A. Winkler, R. D. Bell, and B. Zlokovic, "Central nervous system pericytes in health and disease," Nat. Neurosci. 14(11), 1398-1405 (2011).
36. A. Mishra et al., "Imaging pericytes and capillary diameter in brain slices and isolated retinae," Nat. Protoc. 9(2), 323-326 (2014).
37. P. Osten and T.W. Margrie, "Mapping brain circuitry with a light microscope," Nat. Methods 10(6), 515-523 (2013).
38. R. Mostany and C. Portera-Cailliau, "A craniotomy surgery procedure for chronic brain imaging," J. Vis. Exp. 12, e680 (2008).
39. M. T. Ke, S. Fujimoto, and T. Imai, "SeeDB: a simple and morphologypreserving optical clearing agent for neuronal circuit reconstruction," Nat. Neurosci. 16(8), 1154-1161 (2013).
40. J. DeFelipe, L. Alonso-Nanclares, and J. I. Arellano, "Microstructure of the neocortex: comparative aspects," J. Neurocytol. 31(3-5), 299-316 (2002).