Intravital microscopy: New insights into metastasis of tumors

Journal of Cell Science

Volumn 124, Issue 3, 2011, Pages 299-310

  Beerling, Evelyne ^a   Ritsma, Laila ^a   Vrisekoop, Nienke ^b   Derksen, Patrick W B ^a   Van Rheenen, Jacco ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Cancer; Intravital imaging; Intravital microscopy; Invasion; Metastasis

Indexed keywords

CONTRAST MEDIUM; FLUORESCENT DYE; IODINATED CONTRAST MEDIUM; LUCIFERIN; PROTEINASE; RADIOACTIVE MATERIAL;

BIOLUMINESCENCE; BLOOD VESSEL; CANCER INVASION; CELL INVASION; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCEMENT; EXTRACELLULAR MATRIX; INTRAVITAL MICROSCOPY; LYMPH VESSEL; METASTASIS; MICROBUBBLE; MICROSCOPY; MULTIPHOTON MICROSCOPY; NONHUMAN; NOTE; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTICAL FREQUENCY DOMAIN IMAGING; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SPINNING DISK CONFOCAL MICROSCOPY; TUMOR CELL; ULTRASOUND; WHOLE BODY IMAGING;

BASEMENT MEMBRANE; CELL MOVEMENT; EXTRACELLULAR MATRIX; HUMANS; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MICROSCOPY, VIDEO; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 79551514043     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.072728     Document Type: Note

References (138)

1. Abdul-Karim, M.-A., Al-Kofahi, K., Brown, E. B., Jain, R. K. and Roysam, B. (2003). Automated tracing and change analysis of angiogenic vasculature from in vivo multiphoton confocal image time series. Microvasc. Res. 66, 113-125. (Pubitemid 36962873)
2. Alexander, S., Koehl, G., Hirschberg, M., Geissler, E. and Friedl, P. (2008). Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model. Histochem. Cell Biol. 130, 1147-1154.
3. Ando, R., Hama, H., Yamamoto-Hino, M., Mizuno, H. and Miyawaki, A. (2002). An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein. Proc. Natl. Acad. Sci. USA 99, 12651-12656.
4. Bajénoff, M., Egen, J. G., Koo, L. Y., Laugier Jean, P., Brau, F., Glaichenhaus, N. and Germain, R. N. (2006). Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25, 989-1001.
5. Baluk, P., Morikawa, S., Haskell, A., Mancuso, M. and McDonald, D. M. (2003). Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 163, 1801-1815.
6. Bastiaens, P. I. H. and Squire, A. (1999). Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell. Trends Cell Biol. 9, 48-52.
7. Bins, A., van Rheenen, J., Jalink, K., Halstead, J., Divecha, N., Spencer, D., Haanen, J. and Schumacher, T. (2007). Intravital imaging of fluorescent markers and FRET probes by DNA tattooing. BMC Biotechnol. 7, 2.
8. Boissonnas, A., Fetler, L., Zeelenberg, I. S., Hugues, S. and Amigorena, S. (2007). In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 204, 345-356.
9. Breart, B., Lemaître, F., Celli, S. and Bousso, P. (2008). Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J. Clin. Invest. 118, 1390-1397.
10. Brown, E. B., Campbell, R. B., Tsuzuki, Y., Xu, L., Carmeliet, P., Fukumura, D. and Jain, R. K. (2001). In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat. Med. 7, 864-868.
11. Campagnola, P. J., Millard, A. C., Terasaki, M., Hoppe, P. E., Malone, C. J. and Mohler, W. A. (2002). Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. Biophys. J. 82, 493-508.
12. Cardiff, R., Anver, M., Gusterson, B., Hennighausen, L., Jensen, R., Merino, M., Rehm, S., Russo, J., Tavassoli, F., Wakefield, L. et al. (2000). The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 19, 968-988.
13. Castellino, F., Huang, A. Y., Altan-Bonnet, G., Stoll, S., Scheinecker, C. and Germain, R. N. (2006). Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 440, 890-895.
14. Centonze, V. E. and White, J. G. (1998). Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging. Biophys. J. 75, 2015-2024.
15. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
16. Chambers, A. F., MacDonald, I. C., Schmidt, E. E., Koop, S., Morris, V. L., Khokha, R. and Groom, A. C. (1995). Steps in tumor metastasis: new concepts from intravital videomicroscopy. Cancer Metastasis Rev. 14, 279-301.
17. Chambers, A. F., Groom, A. C. and MacDonald, I. C. (2002). Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2, 563-572.
18. Chang, Y. S., di Tomaso, E., McDonald, D. M., Jones, R., Jain, R. K. and Munn, L. L. (2000). Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. USA 97, 14608-14613.
19. Chiang, A. C. and Massague, J. (2008). Molecular basis of metastasis. N. Eng. J. Med. 359, 2814-2823.
20. Chishima, T., Miyagi, Y., Wang, X., Yamaoka, H., Shimada, H., Moossa, A. R. and Hoffman, R. M. (1997). Cancer invasion and micrometastasis visualized in live tissue by green fluorescent protein expression. Cancer Res. 57, 2042-2047.
21. Christofori, G. (2006). New signals from the invasive front. Nature 441, 444-450.
22. Condeelis, J. and Pollard, J. W. (2006). Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124, 263-266.
23. Das, S. and Skobe, M. (2008). Lymphatic vessel activation in cancer. Ann. N. Y. Acad. Sci. 1131, 235-241.
24. de Visser, K. and Coussens, L. (2006). The inflammatory tumor microenvironment and Its impact on cancer development. Contrib. Microbiol. 13, 118-137.
25. DeNardo, D. G., Barreto, J. B., Andreu, P., Vasquez, L., Tawfik, D., Kolhatkar, N. and Coussens, L. M. (2009). CD4+ T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 16, 91-102.
26. Dennis, M. S., Jin, H., Dugger, D., Yang, R., McFarland, L., Ogasawara, A., Williams, S., Cole, M. J., Ross, S. and Schwall, R. (2007). Imaging tumors with an albumin-binding Fab, a novel tumor-targeting agent. Cancer Res. 67, 254-261.
27. Derksen, P. W. B., Liu, X., Saridin, F., van der Gulden, H., Zevenhoven, J., Evers, B., van Beijnum, J. R., Griffioen, A. W., Vink, J., Krimpenfort, P. et al. (2006). Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10, 437-449.
28. Dingemans, K. (1988). What's new in the ultrastructure of tumor invasion in vivo? Pathol. Res. Pract. 183, 792-808.
29. Dunn, K. W. and Young, P. A. (2006). Principles of multiphoton microscopy. Nephron Exp. Nephrol. 103, e33-e40.
30. Egeblad, M. and Werb, Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer 2, 161-174.
31. Egeblad, M., Ewald, A. J., Askautrud, H. A., Truitt, M. L., Welm, B. E., Bainbridge, E., Peeters, G., Krummel, M. F. and Werb, Z. (2008). Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis. Model. Mech. 1, 155-167.
32. Egen, J. G., Rothfuchs, A. G., Feng, C. G., Winter, N., Sher, A. and Germain, R. N. (2008). Macrophage and T cell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 28, 271-284.
33. Eggeling, C., Volkmer, A. and Seidel, C. A. M. (2005). Molecular photobleaching kinetics of rhodamine 6G by one- and two-photon induced confocal fluorescence microscopy. ChemPhysChem 6, 791-804.
34. Farhadi, M. R., Capelle, H. H., Erber, R., Ullrich, A. and Vajkoczy, P. (2005). Combined inhibition of vascular endothelial growth factor and platelet-derived growth factor signaling: effects on the angiogenesis, microcirculation, and growth of orthotopic malignant gliomas. J. Neurosurg. 102, 363-370.
35. Farina, K. L., Wyckoff, J. B., Rivera, J., Lee, H., Segall, J. E., Condeelis, J. S. and Jones, J. G. (1998). Cell motility of tumor cells visualized in living intact primary tumors using green fluorescent protein. Cancer Res. 58, 2528-2532.
36. Fouquet, W., Owald, D., Wichmann, C., Mertel, S., Depner, H., Dyba, M., Hallermann, S., Kittel, R. J., Eimer, S. and Sigrist, S. J. (2009). Maturation of active zone assembly by Drosophila Bruchpilot. J. Cell Biol. 186, 129-145.
37. Friedl, P. and Gilmour, D. (2009). Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457.
38. Fukumura, D., Duda, D. G., Munn, L. L. and Jain, R. K. (2010). Tumor microvasculature and microenvironment: novel insights through intravital imaging in pre-clinical models. Microcirculation 17, 206-225.
39. Gaggioli, C., Hooper, S., Hidalgo-Carcedo, C., Grosse, R., Marshall, J. F., Harrington, K. and Sahai, E. (2007). Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9, 1392-1400.
40. Galletly, N., McGinty, J., Dunsby, C., Teixeira, F., Requejo-Isidro, J., Munro, I., Elson, D., Neil, M., Chu, A., French, P. et al. (2008). Fluorescence lifetime imaging distinguishes basal cell carcinoma from surrounding uninvolved skin. Br. J. Dermatol. 159, 152-161.
41. Gerritsen, H., Agronskaia, A., Bader, A. and Esposito, A. (2009). Time Domain FLIM; Theory, Instrumentation. In FRET and FLIM Techniques, vol. 33 (ed. T. W. J. Gadella), pp. 95-132. Amsterdam: Elsevier Science.
42. Ghosh, S. R. and Hope, I. A. (2010). Determination of the mobility of novel and established Caenorhabditis elegans sarcomeric proteins in vivo. Eur. J. Cell Biol. 89, 437-448.
43. Giampieri, S., Manning, C., Hooper, S., Jones, L., Hill, C. S. and Sahai, E. (2009). Localized and reversible TGF-beta signalling switches breast cancer cells from cohesive to single cell motility. Nat. Cell Biol. 11, 1287-1296.
44. Giampieri, S., Pinner, S. and Sahai, E. (2010). Intravital imaging illuminates transforming growth factor {beta} signaling switches during metastasis. Cancer Res. 70, 3435-3439.
45. Giepmans, B. N. G., Adams, S. R., Ellisman, M. H. and Tsien, R. Y. (2006). The fluorescent toolbox for assessing protein location and function. Science 312, 217-224.
46. Gligorijevic, B., Kedrin, D., Segall, J., Condeelis, J. and van Rheenen, J. (2009). Dendra2 photoswitching through the mammary imaging window. J. Vis. Exp. 28, 1278.
47. Goswami, S., Sahai, E., Wyckoff, J. B., Cammer, M., Cox, D., Pixley, F. J., Stanley, E. R., Segall, J. E. and Condeelis, J. S. (2005). Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 65, 5278-5283.
48. Grayson, M. H., Chaplin, D. D., Karl, I. E. and Hotchkiss, R. S. (2001). Confocal fluorescent intravital microscopy of the murine spleen. J. Immunol. Methods 256, 55-63.
49. Gurskaya, N. G., Verkhusha, V. V., Shcheglov, A. S., Staroverov, D. B., Chepurnykh, T. V., Fradkov, A. F., Lukyanov, S. and Lukyanov, K. A. (2006). Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461-465.
50. Guzy, R. D., Hoyos, B., Robin, E., Chen, H., Liu, L., Mansfield, K. D., Simon, M. C., Hammerling, U. and Schumacker, P. T. (2005). Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 1, 401-408.
51. Hagendoorn, J., Tong, R., Fukumura, D., Lin, Q., Lobo, J., Padera, T. P., Xu, L., Kucherlapati, R. and Jain, R. K. (2006). Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res. 66, 3360-3364.
52. Hartveit, F. (1979). Paranodal vascular spread in breast cancer with axillary node involvement. J. Pathol. 127, 111-114.
53. Hartveit, F. (1984). Paranodal tumour in breast cancer: extranodal extension versus vascular spread. J. Pathol. 144, 253-256.
54. Hayashi, K., Jiang, P., Yamauchi, K., Yamamoto, N., Tsuchiya, H., Tomita, K., Moossa, A. R., Bouvet, M. and Hoffman, R. M. (2007). Real-time imaging of tumor-cell shedding and trafficking in lymphatic channels. Cancer Res. 67, 8223-8228.
55. Heim, R. C., Cubitt, A. B. and Tsien, R. Y. (1995). Improved green fluorescence. Nature 373, 663-664.
56. Helmchen, F. and Denk, W. (2005). Deep tissue two-photon microscopy. Nat. Methods 2, 932-940.
57. Hingorani, S. R., Petricoin, E. F., Maitra, A., Rajapakse, V., King, C., Jacobetz, M. A., Ross, S., Conrads, T. P., Veenstra, T. D., Hitt, B. A. et al. (2003). Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4, 437-450.
58. Hoffman, R. (2009). Imaging cancer dynamics in vivo at the tumor and cellular level with fluorescent proteins. Clin. Exp. Metastasis 26, 345-355.
59. Hüsemann, Y., Geigl, J. B., Schubert, F., Musiani, P., Meyer, M., Burghart, E., Forni, G., Eils, R., Fehm, T., Riethmüller, G. et al. (2008). Systemic spread is an early step in breast cancer. Cancer Cell 13, 58-68.
60. Jain, R. K. (1988). Determinants of tumor blood flow: a review. Cancer Res. 48, 2641-2658.
61. Jain, R. K. (2003). Molecular regulation of vessel maturation. Nat. Med. 9, 685-693.
62. Jalink, K. and van Rheenen, J. (2009). Filter FRET: quantitative imaging of sensitized emission. In FRET and FLIM Techniques, vol. 33 (ed. T. W. J. Gadella), pp. 289-349. Amsterdam: Elsevier Science.
63. Jongsma, J., van Montfort, E., Vooijs, M., Zevenhoven, J., Krimpenfort, P., van der Valk, M., van de Vijver, M. and Berns, A. (2008). A conditional mouse model for malignant mesothelioma. Cancer Cell 13, 261-271.
64. Jonkers, J., Meuwissen, R., van der Gulden, H., Peterse, H., van der Valk, M. and Berns, A. (2001). Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29, 418-425.
65. Kalluri, R. (2003). Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3, 422-433.
66. Kedrin, D., Gligorijevic, B., Wyckoff, J., Verkhusha, V. V., Condeelis, J., Segall, J. E. and van Rheenen, J. (2008). Intravital imaging of metastatic behavior through a mammary imaging window. Nat. Methods 5, 1019-1021.
67. Keese, M., Offterdinger, M., Tischer, C., Girod, A., Lommerse, P. H., Yagublu, V., Magdeburg, R. and Bastiaens, P. I. (2007). Quantitative imaging of apoptosis commitment in colorectal tumor cells. Differentiation 75, 809-818.
68. Keese, M., Yagublu, V., Schwenke, K., Post, S. and Bastiaens, P. (2010). Fluorescence lifetime imaging microscopy of chemotherapy-induced apoptosis resistance in a syngenic mouse tumor model. Int. J. Cancer 126, 104-113.
69. Kessenbrock, K., Plaks, V. and Werb, Z. (2010). Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141, 52-67.
70. Kienast, Y., von Baumgarten, L., Fuhrmann, M., Klinkert, W. E. F., Goldbrunner, R., Herms, J. and Winkler, F. (2010). Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 16, 116-122.
71. Kimura, H., Hayashi, K., Yamauchi, K., Yamamoto, N., Tsuchiya, H., Tomita, K., Kishimoto, H., Bouvet, M. and Hoffman, R. M. (2010). Real-time imaging of single cancer-cell dynamics of lung metastasis. J. Cell. Biochem. 109, 58-64.
72. Klein, C. A. (2009). Parallel progression of primary tumours and metastases. Nat. Rev. Cancer 9, 302-312.
73. Le Dévédec, S., Lalai, R., Pont, C., de Bont, H. and van de Water, B. (2010). Two-photon intravital multicolor imaging combined with inducible gene expression to distinguish metastatic behavior of breast cancer cells in vivo. Mol. Imaging Biol. doi:10.1007/s11307-010-0307-z
74. LeBleu, V. S., MacDonald, B. and Kalluri, R. (2007). Structure and function of basement membranes. Exp. Biol. Med. 232, 1121-1129.
75. Lehr, H., Leunig, M., Menger, M., Nolte, D. and Messmer, K. (1993). Dorsal skinfold chamber technique for intravital microscopy in nude mice. Am. J. Pathol. 143, 1055-1062.
76. Leivonen, S.-K. and Kähäri, V.-M. (2007). Transforming growth factor-beta signaling in cancer invasion and metastasis. Int. J. Cancer 121, 2119-2124.
77. Llaguno, S. A., Chen, J., Kwon, C.-H. and Parada, L. F. (2008). Neural and cancer stem cells in tumor suppressor mouse models of malignant astrocytoma. Cold Spring Harb. Symp. Quant. Biol. 73, 421-426.
78. Lohela, M. and Werb, Z. (2010). Intravital imaging of stromal cell dynamics in tumors. Curr. Opin. Genet. Dev. 20, 72-78.
79. MacDonald, I. C., Schmidt, E. E., Morris, V. L., Chambers, A. F. and Groom, A. C. (1992). Intravital videomicroscopy of the chorioallantoic microcirculation: A model system for studying metastasis. Microvasc. Res. 44, 185-199.
80. Massberg, S., Schaerli, P., Knezevic-Maramica, I., Köllnberger, M., Tubo, N., Moseman, E. A., Huff, I. V., Junt, T., Wagers, A. J., Mazo, I. B. et al. (2007). Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131, 994-1008.
81. McElroy, M., Bouvet, M. and Hoffman, R. M. (2008). Color-coded fluorescent mouse models of cancer cell interactions with blood vessels and lymphatics. In Methods in Enzymology, vol. 445, pp. 27-52. New York: Academic Press.
82. McIntyre, J. O., Scherer, R. L. and Matrisian, L. M. (2010). Near-infrared optical proteolytic beacons for in vivo imaging of matrix metalloproteinase activity. Methods Mol. Biol. 622, 279-304.
83. Mempel, T. R., Scimone, M. L., Mora, J. R. and von Andrian, U. H. (2004). In vivo imaging of leukocyte trafficking in blood vessels and tissues. Curr. Opin. Immunol. 16, 406-417.
84. Meuwissen, R., Linn, S. C., Linnoila, R. I., Zevenhoven, J., Mooi, W. J. and Berns, A. (2003). Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 4, 181-189.
85. Mohler, W., Millard, A. C. and Campagnola, P. J. (2003). Second harmonic generation imaging of endogenous structural proteins. Methods 29, 97-109. (Pubitemid 36259916)
86. Monici, M. and El-Gewely, M. R. (2005). Cell and tissue autofluorescence research and diagnostic applications. Biotechnol. Annu. Rev. 11, 227-256.
87. Morris, M. (2010). Fluorescent biosensors of intracellular targets from genetically encoded reporters to modular polypeptide probes. Cell Biochem. Biophys. 56, 19-37.
88. Naumov, G., Wilson, S., MacDonald, I., Schmidt, E., Morris, V., Groom, A., Hoffman, R. and Chambers, A. (1999). Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. J. Cell Sci. 112, 1835-1842. (Pubitemid 29338809)
89. Nguyen, D. X., Bos, P. D. and Massague, J. (2009). Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 9, 274-284.
90. Ntziachristos, V. (2010). Going deeper than microscopy: the optical imaging frontier in biology. Nat. Methods 7, 603-614.
91. Olive, K. P., Tuveson, D. A., Ruhe, Z. C., Yin, B., Willis, N. A., Bronson, R. T., Crowley, D. and Jacks, T. (2004). Mutant p53 gain of function in two mouse models of Li-Fraumeni Syndrome. Cell 119, 847-860. (Pubitemid 40017690)
92. Olson, E. S., Aguilera, T. A., Jiang, T., Ellies, L. G., Nguyen, Q. T., Wong, E. H., Gross, L. A. and Tsien, R. Y. (2009). In vivo characterization of activatable cell penetrating peptides for targeting protease activity in cancer. Integr. Biol. (Camb) 1, 382-393.
93. Olson, E. S., Jiang, T., Aguilera, T. A., Nguyen, Q. T., Ellies, L. G., Scadeng, M. and Tsien, R. Y. (2010). Activatable cell penetrating peptides linked to nanoparticles as dual probes for in vivo fluorescence and MR imaging of proteases. Proc. Natl. Acad. Sci. USA 107, 4311-4316.
94. Orimo, A. and Weinberg, R. (2006). Stromal fibroblasts in cancer: a novel tumorpromoting cell type. Cell Cycle 5, 1597-1601. (Pubitemid 44285243)
95. Padera, T. P., Kadambi, A., di Tomaso, E., Carreira, C. M., Brown, E. B., Boucher, Y., Choi, N. C., Mathisen, D., Wain, J., Mark, E. J. et al. (2002). Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296, 1883-1886.
96. Perentes, J. Y., McKee, T. D., Ley, C. D., Mathiew, H., Dawson, M., Padera, T. P., Munn, L. L., Jain, R. K. and Boucher, Y. (2009). In vivo imaging of extracellular matrix remodeling by tumor-associated fibroblasts. Nat. Methods 6, 143-145.
97. Philippar, U., Roussos, E. T., Oser, M., Yamaguchi, H., Kim, H.-D., Giampieri, S., Wang, Y., Goswami, S., Wyckoff, J. B., Lauffenburger, D. A. et al. (2008). A mena invasion isoform potentiates EGF-induced carcinoma cell invasion and metastasis. Dev. Cell 15, 813-828.
98. Piatkevich, K. D. and Verkhusha, V. V. (2009). Advances in engineering of fluorescent proteins and photoactivatable proteins with red emission. Curr. Opin. Chem. Biol. 14, 23-29.
99. Pinner, S. and Sahai, E. (2008). Imaging amoeboid cancer cell motility in vivo. J. Microsc. 231, 441-445.
100. Poincloux, R., Lizarraga, F. and Chavrier, P. (2009). Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J. Cell Sci. 122, 3015-3024.
101. Provenzano, P., Eliceiri, K. and Keely, P. (2009). Multiphoton microscopy and fluorescence lifetime imaging microscopy (FLIM) to monitor metastasis and the tumor microenvironment. Clin. Exp. Metastasis 26, 357-370.
102. Rowe, R. G. and Weiss, S. J. (2008). Breaching the basement membrane: who, when and how? Trends Cell Biol. 18, 560-574.
103. Rowe, R. G. and Weiss, S. J. (2009). Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Annu. Rev. Cell Dev. Biol. 25, 567-595.
104. Sahai, E. and Marshall, C. J. (2003). Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5, 711-719.
105. Sahai, E., Wyckoff, J., Philippar, U., Segall, J., Gertler, F. and Condeelis, J. (2005). Simultaneous imaging of GFP, CFP and collagen in tumors in vivo using multiphoton microscopy. BMC Biotechnol. 5, 14.
106. Scherer, R. L., VanSaun, M. N., McIntyre, O. and Matrisian, L. M. (2008). Optical imaging of matrix metalloproteinase-7 activity in vivo using a proteolytic nanobeacon. Mol. Imaging 7, 118-131.
107. Serrel, A., Timpson, P., Canel, M., Schwarz, J. P., Carragher, N. O., Frame, M. C., Brunton, V. G. and Anderson, K. I. (2009). Real-time study of E-cadherin and membrane dynamics in living animals: implications for disease modeling and drug development. Cancer Res. 69, 2714-2719.
108. Shan, S., Sorg, B. and Dewhirst, M. W. (2003). A novel rodent mammary window of orthotopic breast cancer for intravital microscopy. Microvasc. Res. 65, 109-117.
109. Shimomura, O., Johnson, F. H. and Saiga, Y. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J. Cell. Comp. Physiol. 59, 223-239.
110. Sipkins, D. A., Wei, X., Wu, J. W., Runnels, J. M., Cote, D., Means, T. K., Luster, A. D., Scadden, D. T. and Lin, C. P. (2005). In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 435, 969-973.
111. Sleeman, J. P. and Thiele, W. (2009). Tumor metastasis and the lymphatic vasculature. Int. J. Cancer 125, 2747-2756.
112. Stockholm, D., Bartoli, M., Sillon, G., Bourg, N., Davoust, J. and Richard, I. (2005). Imaging calpain protease activity by multiphoton FRET in living mice. J. Mol. Biol. 346, 215-222.
113. Stoletov, K., Kato, H., Zardouzian, E., Kelber, J., Yang, J., Shattil, S. and Klemke, R. (2010). Visualizing extravasation dynamics of metastatic tumor cells. J. Cell Sci. 123, 2332-2341.
114. Stylli, S. S., Kaye, A. H. and Lock, P. (2008). Invadopodia: At the cutting edge of tumour invasion. J. Clin. Neurosci. 15, 725-737.
115. Talmadge, J. E. and Fidler, I. J. (2010). AACR Centennial Series: The Biology of Cancer Metastasis: Historical Perspective. Cancer Res. 70, 5649-5669.
116. Tanis, P., Nieweg, O., Valdes Olmos, R., Th Rutgers, E. and Kroon, B. (2001). History of sentinel node and validation of the technique. Breast Cancer Res. 3, 109-112.
117. Tanjore, H. and Kalluri, R. (2006). The role of type IV collagen and basement membranes in cancer progression and metastasis. Am. J. Pathol. 168, 715-717.
118. Theer, P., Hasan, M. T. and Denk, W. (2003). Two-photon imaging to a depth of 1000 μm in living brains by use of a Ti:Al2O3 regenerative amplifier. Opt. Lett. 28, 1022-1024.
119. Ting, A. Y., Kain, K. H., Klemke, R. L. and Tsien, R. Y. (2001). Genetically encoded fluorescent reporters of protein tyrosine kinase activities in living cells. Proc. Natl. Acad. Sci. USA 98, 15003-15008.
120. Vakoc, B. J., Lanning, R. M., Tyrrell, J. A., Padera, T. P., Bartlett, L. A., Stylianopoulos, T., Munn, L. L., Tearney, G. J., Fukumura, D., Jain, R. K. et al. (2009). Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging. Nat. Med. 15, 1219-1223.
121. VanEngelenburg, S. B. and Palmer, A. E. (2008). Fluorescent biosensors of protein function. Curr. Opin. Chem. Biol. 12, 60-65.
122. Wagner, R. (1839). Erlauterungstaflen zur physiologie und entwicklungsgeschichte. Leipzig, Germany: Leopold Voss.
123. Weissleder, R., Tung, C.-H., Mahmood, U. and Bogdanov, A. (1999). In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat. Biotech. 17, 375-378.
124. Wolf, K., Mazo, I., Leung, H., Engelke, K., von Andrian, U. H., Deryugina, E. I., Strongin, A. Y., Bröcker, E.-B. and Friedl, P. (2003). Compensation mechanism in tumor cell migration. J. Cell Biol. 160, 267-277.
125. Wolf, K., Alexander, S., Schacht, V., Coussens, L. M., von Andrian, U. H., van Rheenen, J., Deryugina, E. and Friedl, P. (2009). Collagen-based cell migration models in vitro and in vivo. Semin. Cell Dev. Biol. 20, 931-941.
126. Wood, S. J. (1958). Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. AMA Arch. Pathol. 66, 550-568.
127. Wouters, F. S., Verveer, P. J. and Bastiaens, P. I. H. (2001). Imaging biochemistry inside cells. Trends Cell Biol. 11, 203-211.
128. Wyckoff, J. B., Jones, J. G., Condeelis, J. S. and Segall, J. E. (2000). A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 60, 2504-2511.
129. Wyckoff, J. B., Pinner, S. E., Gschmeissner, S., Condeelis, J. S. and Sahai, E. (2006). ROCK- and myosin-dependent matrix deformation enables protease-independent tumorcell invasion in vivo. Curr. Biol. 16, 1515-1523.
130. Wyckoff, J. B., Wang, Y., Lin, E. Y., Li, J.-f., Goswami, S., Stanley, E. R., Segall, J. E., Pollard, J. W. and Condeelis, J. (2007). Direct visualization of macrophageassisted tumor cell intravasation in mammary tumors. Cancer Res. 67, 2649-2656.
131. Xiao, A., Wu, H., Pandolfi, P. P., Louis, D. N. and Van Dyke, T. (2002). Astrocyte inactivation of the pRb pathway predisposes mice to malignant astrocytoma development that is accelerated by PTEN mutation. Cancer Cell 1, 157-168.
132. Xu, X., Qiao, W., Linke, S. P., Cao, L., Li, W.-M., Furth, P. A., Harris, C. C. and Deng, C.-X. (2001). Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Natl. Genet. 28, 266-271.
133. Yamauchi, K., Yang, M., Jiang, P., Xu, M., Yamamoto, N., Tsuchiya, H., Tomita, K., Moossa, A. R., Bouvet, M. and Hoffman, R. M. (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.
134. Yang, M., Baranov, E., Wang, J.-W., Jiang, P., Wang, X., Sun, F.-X., Bouvet, M., Moossa, A. R., Penman, S. and Hoffman, R. M. (2002). Direct external imaging of nascent cancer, tumor progression, angiogenesis, and metastasis on internal organs in the fluorescent orthotopic model. Proc. Natl. Acad. Sci. USA 99, 3824-3829.
135. Yuan, F., Salehi, H. A., Boucher, Y., Vasthare, U. S., Tuma, R. F. and Jain, R. K. (1994). Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res. 54, 4564-4568.
136. Zhang, J., Chen, L., Raina, H., Blaustein, M. P. and Wier, W. G. (2010). In vivo assessment of artery smooth muscle [Ca2+]i and MLCK activation in FRET-based biosensor mice. Am. J. Physiol. Heart Circ. Physiol. 299, H946-H956.
137. Zipfel, W. R., Williams, R. M., Christie, R., Nikitin, A. Y., Hyman, B. T. and Webb, W. W. (2003a). Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. USA 100, 7075-7080.
138. Zipfel, W. R., Williams, R. M. and Webb, W. W. (2003b). Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369-1377.