Visualizing extravasation dynamics of metastatic tumor cells

Journal of Cell Science

Volumn 123, Issue 13, 2010, Pages 2332-2341

  Stoletov, Konstantin ^a   Kato, Hisashi ^b   Zardouzian, Erin ^a   Kelber, Jonathan ^a   Yang, Jing ^c   Shattil, Sanford ^b   Klemke, Richard ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer metastasis; Extravasation; Zebrafish

Indexed keywords

BETA1 INTEGRIN; RHO KINASE; TRANSCRIPTION FACTOR TWIST; VASCULOTROPIN A;

ARTICLE; BLOOD VESSEL WALL; CANCER CELL; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRAVASATION; HUMAN; HUMAN CELL; LOCOMOTION; METASTASIS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ZEBRA FISH; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL EMBRYO; CELL MOTION; CELL SURFACE; CYTOLOGY; ENDOTHELIUM; GENE SILENCING; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHYSIOLOGY; TRANSGENIC ANIMAL; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD29; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; EMBRYO, NONMAMMALIAN; ENDOTHELIUM; GENE KNOCKDOWN TECHNIQUES; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; RHO-ASSOCIATED KINASES; TWIST TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; ZEBRAFISH;

DANIO RERIO;

EID: 77954352788     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.069443     Document Type: Article

References (47)

1. Al-Mehdi, A. B., Tozawa, K., Fisher, A. B., Shientag, L., Lee, A. and Muschel, R. J. (2000). Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis. Nat. Med. 6, 100-102.
2. Blum, Y., Belting, H. G., Ellertsdottir, E., Herwig, L., Lüders, F. and Affolter, M. (2008). Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322.
3. Bos, P. D., Zhang, X. H., Nadal, C., Shu, W., Gomis, R. R., Nguyen, D. X., Minn, A. J., van de Vijver, M. J., Gerald, W. L., Foeken, J. A. et al. (2009). Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005-1012.
4. Colmone, A., Amorim, M., Andrea, L., Pontier, A. L., Wang, S., Jablonski, E. and Sipkins, D. A. (2008). Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 322, 1861-1865.
5. Crawford, Y. and Ferrara, N. (2008). VEGF inhibition: insights from preclinical and clinical studies. Cell Tissue Res. 335, 261-269.
6. Engelhardt, B. and Wolburg, H. (2004). Transendothelial migration of leukocytes: through the front door or around the side of the house? Eur. J. Immunol. 34, 2955-2963.
7. Fischer, R. S., Gardel, M., Ma, X., Adelstein, R. S. and Waterman, C. M. (2009). Local cortical tension by myosin II guides 3D endothelial cell branching. Curr. Biol. 19, 260-265.
8. Friedl, P. (2004). Prespecification and plasticity: shifting mechanisms of cell migration. Curr. Opin. Cell Biol. 16, 14-23.
9. Gupta, G. P., Nguyen, D. X., Chiang, A. C., Bos, P. D., Kim, J. Y., Nadal, C., Gomis, R. R., Manova-Todorova, K. and Massagué, J. (2007). Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446, 765-771.
10. Haddad, O., Chotard-Ghodsnia, R., Verdier, C. and Duperray, A. (2010). Tumor cell/endothelial cell tight contact upregulates endothelial adhesion molecule expression mediated by NFkappaB: differential role of the shear stress. Exp. Cell. Res. 316, 615-626.
11. Haldi, M., Ton, C., Seng, W. L. and McGrath, P. (2005). Human melanoma cells transplanted into zebrafish proliferate, migrate, produce melanin, form masses and stimulate angiogenesis in zebrafish. Angiogenesis 9, 139-151.
12. Hewitt, R. E., McMarlin, A., Kleiner, D., Wersto, R., Martin, P., Tsokos, M., Stamp, G. W. and Stetler-Stevenson, W. G. (2000). Validation of a model of colon cancer progression. J. Pathol. 192, 446-454.
13. Heyder, C., Gloria-Maercker, E., Hatzmann, W., Zaenker, K. S. and Dittmar, T. (2006). Visualization of tumor cell extravasation. Contrib. Microbiol. 13, 200-208.
14. Isogai, S., Lawson, N. D., Torrealday, S., Horiguchi, M. and Weinstein, B. M. (2003). Angiogenic network formation in the developing vertebrate trunk. Development 130, 5281-5290.
15. Kienast, Y., von Baumgarten, L., Fuhrmann, M., Klinkert, W. E., Goldbrunner, R., Herms, J. and Winkler, F. (2010). Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med. 16, 116-122.
16. Koop, S., Schmidt, E. E., MacDonald, I. C., Morris, V. L., Khokha, R., Grattan, M., Leone, J., Chambers, A. F. and Groom, A. C. (1996). Independence of metastatic ability and extravasation: metastatic ras-transformed and control fibroblasts extravasate equally well. Proc. Natl. Acad. Sci. USA 93, 11080-11084.
17. Kubens, B. S. and Zänker, K. S. (1998). Differences in the migration capacity of primary human colon carcinoma cells (SW480) and their lymph node metastatic derivatives (SW620). Cancer Lett. 131, 55-64.
18. Lee, S. L., Rouhi, P., Dahl Jensen, L., Zhang, D., Ji, H., Hauptmann, G., Ingham, P. and Cao, Y. (2009). Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model. Proc. Natl. Acad. Sci. USA 106, 19485-19490.
19. Luzzi, K. J., MacDonald, I. C., Schmidt, E. E., Kerkvliet, N., Morris, V. L., Chambers, A. F. and Groom, A. C. (1998). Multistep nature of metastatic inefficiency. Am. J. Pathol. 153, 865-873.
20. Ma, L., Teruya-Feldstein, J. and Weinberg, R. A. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682-688.
21. Matsumoto, T. and Claesson-Welsh, L. (2001). VEGF receptor signal transduction. Sci. STKE 112, 1-17.
22. Montero-Balaguer, M., Swirsding, K., Orsenigo, F., Cotelli, F., Mione, M. and Dejana, E. (2009). Stable vascular connections and remodeling require full expression of VE-cadherin in zebrafish embryos. PLoS ONE 4, 1-14.
23. Morozevich, G., Kozlova, N., Cheglakov, I., Ushakova, N. and Berman, A. (2009). Integrin alpha5beta1 controls invasion of human breast carcinoma cells by direct and indirect modulation of MMP-2 collagenase activity. Cell Cycle 8, 2219-2225.
24. Narumiya, S., Tanji, M. and Ishizaki, T. (2009). Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 28, 65-76.
25. Nguyen, D. X., Bos, P. D. and Massague, J. (2009). Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer 9, 274-284.
26. Nicoli, S., Ribatti, D., Cotelli, F. and Presta, M. (2007). Mammalian tumor xenografts induce neovascularization in zebrafish embryos. Cancer Res. 67, 2927-2931.
27. Nusslein-Volhard, C. and Dahm, R. (2002). Zebrafish: A Practical Approach, 1st edn. Oxford: Oxford University Press.
28. Pinner, S. and Sahai, E. (2008). Imaging amoeboid cancer cell motility in vivo. J. Microsc. 231, 441-445.
29. Podsypanina, K., Du, Y. C., Jechlinger, M., Beverly, L. J., Hambardzumyan, D. and Varmus, H. (2008). Seeding and propagation of untransformed mouse mammary cells in the lung. Science 321, 1841-1844.
30. Qin, X. F., An, D. S., Chen, I. S. and Baltimore, D. (2003). Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc. Natl. Acad. Sci. USA 100, 183-188.
31. Sahai, E. (2007). Illuminating the metastatic process. Nat. Rev. Cancer 7, 737-749.
32. Schluter, K., Gassmann, P., Enns, A., Korb, T., Hemping-Bovenkerk, A., Holzen, J. and Haier, J. (2006). Organ-specific metastatic tumor cell adhesion and extravasation of colon carcinoma cells with different metastatic potential. Am. J. Pathol. 169, 1064-1073.
33. Shibue, T. and Weinberg, R. A. (2009). Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proc. Natl. Acad. Sci. USA 106, 10290-10295.
34. Siekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
35. Sipkins, D. A., Wei, X., Wu, J. W., Runnels, J. M., Côté, 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.
36. Stoletov, K. and Klemke, R. (2008). Catch of the day: zebrafish as a human cancer model. Oncogene 27, 4509-4520.
37. Stoletov, K., Montel, V., Lester, R. D., Gonias, S. L. and Klemke. R. (2007). High-resolution imaging of the dynamic tumor cell-vascular interface in transparent zebrafish. Proc. Natl. Acad. Sci. USA 104, 17406-17411.
38. Townson, J. L. and Chambers, A. F. (2006). Dormancy of solitary metastatic cells. Cell Cycle 5, 1744-1750.
39. Voura, E. B., Jaiswal, J. K., Mattoussi, H. and Simon, S. M. (2004). Tracking metastatic tumor cell extravasation with quantum dot nanocrystals and fluorescence emission-scanning microscopy. Nat. Med. 10, 993-998.
40. 1 integrin and vascular laminin-5 mediate pulmonary arrest and metastasis. J. Cell Biol. 164, 935-941.
41. 3. J. Cell Biol. 30, 1211-1222.
42. Weis, S., Cui, J., Barnes, L. and Cheresh, D. (2004). Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J. Cell Biol. 167, 223-229.
43. 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: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160, 267-277. (Pubitemid 36254960)
44. Wyckoff, J. B., Pinner, S. E., Gschmeissner, S., Condeelis, J. S. and Sahai, E. (2006). ROCK-and myosin-dependent matrix deformation enables protease-independent tumor cell invasion in vivo. Curr. Biol. 16, 1515-1523.
45. 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.
46. Yang, J., Mani, S. A., Donaher, J. L., Ramaswamy, S., Itzykson, R. A., Come, C., Savagner, P., Gitelman, I., Richardson, A. and Weinberg, R. A. (2004). Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939.
47. Zijlstra, A., Mellor, R., Panzarella, G., Aimes, R. T., Hooper, J. D., Marchenko, N. D. and Quigley, J. P. (2002). A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res. 62, 7083-7092.