Insights into cell-to-cell and cell-to-blood-vessel communications in the brain: In vivo multiphoton microscopy

Cell and Tissue Research

Volumn 352, Issue 1, 2013, Pages 149-159

  Osswald, Matthias ^a   Winkler, Frank ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Brain; Cancer; Multiphoton microscopy; Neuroscience; Two photon microscopy

Indexed keywords

CALCIUM; FLUORESCEIN ISOTHIOCYANATE; FLUORESCENT DYE;

BRAIN; BRAIN TUMOR; CALCIUM SIGNALING; CARCINOGENESIS; CELL COMMUNICATION; CELL FUNCTION; CELL LABELING; CELL METABOLISM; CELL STRUCTURE; CELL TO BLOOD VESSEL COMMUNICATION; CONFOCAL MICROSCOPY; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; HUMAN; INTRAVITAL MICROSCOPY; MICROSCOPY; MOLECULAR INTERACTION; MOLECULAR PROBE; MULTIPHOTON MICROSCOPY; NEUROIMAGING; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING; TREATMENT RESPONSE; TUMOR GROWTH;

ANIMALS; BRAIN; BRAIN NEOPLASMS; CELL COMMUNICATION; HUMANS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; STAINING AND LABELING;

EID: 84875234590     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1580-3     Document Type: Review

References (65)

1. Adelsberger H, Garaschuk O, Konnerth A (2005) Cortical calcium waves in resting newborn mice. Nat Neurosci 8:988-990
2. Attwell D, Buchan AM, Charpak S, Lauritzen M, Macvicar BA, Newman EA (2010) Glial and neuronal control of brain blood flow. Nature 468:232-243
3. Barretto RP, Ko TH, Jung JC, Wang TJ, Capps G, Waters AC, Ziv Y, Attardo A, Recht L, Schnitzer MJ (2011) Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Nat Med 17:223-228
4. Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, Klinkert WE, Flugel-Koch C, Issekutz TB, Wekerle H, Flugel A (2009) Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462:94-98
5. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315-325
6. Brown EB, Campbell RB, Tsuzuki Y, Xu L, Carmeliet P, Fukumura D, Jain RK (2001) In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat Med 7:864-868
7. Brown E, McKee T, di Tomaso E, Pluen A, Seed B, Boucher Y, Jain RK (2003) Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 9:796-800
8. Chae SS, Kamoun WS, Farrar CT, Kirkpatrick ND, Niemeyer E, de Graaf AM, Sorensen AG, Munn LL, Jain RK, Fukumura D (2010) Angiopoietin-2 interferes with anti-VEGFR2-induced vessel normalization and survival benefit in mice bearing gliomas. Clin Cancer Res 16:3618-3627
9. Dakin K, Li WH (2006) Infrared-LAMP: two-photon uncaging and imaging of gap junctional communication in three dimensions. Nat Methods 3:959
10. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758
11. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73-76
12. 2+ signaling in vivo. Glia 57:767-776
13. Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J, Margrie TW, Helmchen F, Denk W, Brecht M, Osten P (2004) Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc Natl Acad Sci USA 101:18206-18211
14. Drobizhev M, Makarov NS, Tillo SE, Hughes TE, Rebane A (2011) Two-photon absorption properties of fluorescent proteins. Nat Methods 8:393-399
15. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51
16. Fuhrmann M, Mitteregger G, Kretzschmar H, Herms J (2007) Dendritic pathology in prion disease starts at the synaptic spine. J Neurosci 27:6224-6233
17. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G, Haass C, LaFerla FM, Kretzschmar H, Herms J (2010) Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 13:411-413
18. Fukumura D, Xavier R, Sugiura T, Chen Y, Park EC, Lu N, Selig M, Nielsen G, Taksir T, Jain RK, Seed B (1998) Tumor induction of VEGF promoter activity in stromal cells. Cell 94:715-725
19. Gee KR, Brown KA, Chen WN, Bishop-Stewart J, Gray D, Johnson I (2000) Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes. Cell Calcium 27:97-106
20. Gobel W, Kampa BM, Helmchen F (2007) Imaging cellular network dynamics in three dimensions using fast 3D laser scanning. Nat Methods 4:73-79
21. Grewe BF, Langer D, Kasper H, Kampa BM, Helmchen F (2010) High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat Methods 7:399-405
22. Haas B, Schipke CG, Peters O, Sohl G, Willecke K, Kettenmann H (2006) Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb Cortex 16:237-246
23. Hefendehl JK, Wegenast-Braun BM, Liebig C, Eicke D, Milford D, Calhoun ME, Kohsaka S, Eichner M, Jucker M (2011) Long-term in vivo imaging of beta-amyloid plaque appearance and growth in a mouse model of cerebral beta-amyloidosis. J Neurosci 31:624-629
24. Helmchen F, Denk W (2005) Deep tissue two-photon microscopy. Nat Methods 2:932-940
25. Hirase H (2005) A multi-photon window onto neuronal-glial-vascular communication. Trends Neurosci 28:217-219
26. Hirase H, Qian L, Bartho P, Buzsaki G (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2:E96
27. Hoogland TM, Kuhn B, Gobel W, Huang W, Nakai J, Helmchen F, Flint J, Wang SS (2009) Radially expanding transglial calcium waves in the intact cerebellum. Proc Natl Acad Sci USA 106:3496-3501
28. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106-4114
29. Kamoun WS, Chae SS, Lacorre DA, Tyrrell JA, Mitre M, Gillissen MA, Fukumura D, Jain RK, Munn LL (2010) Simultaneous measurement of RBC velocity, flux, hematocrit and shear rate in vascular networks. Nat Methods 7:655-660
30. Kantevari S, Matsuzaki M, Kanemoto Y, Kasai H, Ellis-Davies GC (2010) Two-color, two-photon uncaging of glutamate and GABA. Nat Methods 7:123-125
31. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103
32. Kasischke KA, Lambert EM, Panepento B, Sun A, Gelbard HA, Burgess RW, Foster TH, Nedergaard M (2011) Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions. J Cereb Blood Flow Metab 31:68-81
33. Kawakami N, Nagerl UV, Odoardi F, Bonhoeffer T, Wekerle H, Flugel A (2005) Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion. J Exp Med 201:1805-1814
34. Kedrin D, Gligorijevic B, Wyckoff J, Verkhusha VV, Condeelis J, Segall JE, van Rheenen J (2008) Intravital imaging of metastatic behavior through a mammary imaging window. Nat Methods 5:1019-1021
35. Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, Winkler F (2010) Real-time imaging reveals the single steps of brain metastasis formation. Nat Med 16:116-122
36. Koehler RC, Roman RJ, Harder DR (2009) Astrocytes and the regulation of cerebral blood flow. Trends Neurosci 32:160-169
37. Kuchibhotla KV, Lattarulo CR, Hyman BT, Bacskai BJ (2009) Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323:1211-1215
38. Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y (2011) Large-scale calcium waves traveling through astrocytic networks in vivo. J Neurosci 31:2607-2614
39. Leybaert L, Sanderson MJ (2012) Intercellular Ca(2+) waves: mechanisms and function. Physiol Rev 92:1359-1392
40. Misgeld T, Kerschensteiner M, Bareyre FM, Burgess RW, Lichtman JW (2007) Imaging axonal transport of mitochondria in vivo. Nat Methods 4:559-561
41. Motoike T, Loughna S, Perens E, Roman BL, Liao W, Chau TC, Richardson CD, Kawate T, Kuno J, Weinstein BM et al (2000) Universal GFP reporter for the study of vascular development. Genesis 28:75-81
42. Nagayama S, Zeng S, Xiong W, Fletcher ML, Masurkar AV, Davis DJ, Pieribone VA, Chen WR (2007) In vivo simultaneous tracing and Ca(2+) imaging of local neuronal circuits. Neuron 53:789-803
43. Niesner RA, Hauser AE (2011) Recent advances in dynamic intravital multi-photon microscopy. Cytometry A 79:789-798
44. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1:31-37
45. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318
46. Nolte C, Matyash M, Pivneva T, Schipke CG, Ohlemeyer C, Hanisch UK, Kirchhoff F, Kettenmann H (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33:72-86
47. Sipkins DA, Wei X, Wu JW, Runnels JM, Cote D, Means TK, Luster AD, Scadden DT, Lin CP (2005) In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 435:969-973
48. Squirrell JM, Wokosin DL, White JG, Bavister BD (1999) Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability. Nat Biotechnol 17:763-767
49. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci USA 100:7319-7324
50. Svoboda K, Tank DW, Denk W (1996) Direct measurement of coupling between dendritic spines and shafts. Science 272:716-719
51. 2+ signaling and the microvasculature in experimental mice models of Alzheimer's disease. Ann N Y Acad Sci 1097:40-50
52. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007b) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754-762
53. Tantama M, Hung YP, Yellen G (2011) Imaging intracellular pH in live cells with a genetically encoded red fluorescent protein sensor. J Am Chem Soc 133:10034-10037
54. Tatenhorst L, Puttmann S, Senner V, Paulus W (2005) Genes associated with fast glioma cell migration in vitro and in vivo. Brain Pathol 15:46-54
55. Tong RT, Boucher Y, Kozin SV, Winkler F, Hicklin DJ, Jain RK (2004) Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res 64:3731-3736
56. von Baumgarten L, Brucker D, Tirniceru A, Kienast Y, Grau S, Burgold S, Herms J, Winkler F (2011) Bevacizumab has differential and dose-dependent effects on glioma blood vessels and tumor cells. Clin Cancer Res 17:6192-6205
57. 2+ signaling evoked by sensory stimulation in vivo. Nat Neurosci 9:816-823
58. Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, Garkavtsev I, Xu L, Hicklin DJ, Fukumura D, di Tomaso E et al (2004) Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6:553-563
59. Winkler F, Kienast Y, Fuhrmann M, von Baumgarten L, Burgold S, Mitteregger G, Kretzschmar H, Herms J (2009) Imaging glioma cell invasion in vivo reveals mechanisms of dissemination and peritumoral angiogenesis. Glia 57:1306-1315
60. Winship IR, Plaa N, Murphy TH (2007) Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo. J Neurosci 27:6268-6272
61. Wood S (1958) Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. AMA Arch Pathol 66:550-568
62. Xu HT, Pan F, Yang G, Gan WB (2007) Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat Neurosci 10:549-551
63. Yamauchi K, Yang M, Jiang P, Xu M, Yamamoto N, Tsuchiya H, Tomita K, Moossa AR, Bouvet M, Hoffman RM (2006) Development of real-time subcellular dynamic multicolor imaging of cancer-cell trafficking in live mice with a variable-magnification whole-mouse imaging system. Cancer Res 66:4208-4214
64. Yuan F, Salehi HA, Boucher Y, Vasthare US, Tuma RF, Jain RK (1994) Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res 54:4564-4568
65. Yuan F, Chen Y, Dellian M, Safabakhsh N, Ferrara N, Jain RK (1996) Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc Natl Acad Sci USA 93:14765-14770