Myosin light chain kinase mediates transcellular intravasation of breast cancer cells through the underlying endothelial cells: A three-dimensional FRET study

Journal of Cell Science

Volumn 123, Issue 3, 2010, Pages 431-440

  Khuon, Satya ^a   Liang, Luke ^a   Dettman, Robert W ^a   Sporn, Peter H S ^a,b   Wysolmerski, Robert B ^c   Chew, Teng Leong ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

^c WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytoskeletal signaling; Endothelium; FRET imaging; Transcellular invasion; Tumor intravasation; Vascular engineering

Indexed keywords

CALCIUM ION; COLLAGEN GEL; MYOSIN II; MYOSIN LIGHT CHAIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER CELL; CELL INVASION; CELL JUNCTION; CELL MIGRATION; CELL POLARITY; CONTROLLED STUDY; CULTURE MEDIUM; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME PHOSPHORYLATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; MUSCLE CONTRACTION; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSOR; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING; TUMOR VASCULARIZATION;

ANIMALS; BREAST NEOPLASMS; CATTLE; CELL LINE, TUMOR; CELL MOVEMENT; ENDOTHELIAL CELLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, CONFOCAL; MYOSIN-LIGHT-CHAIN KINASE; NEOPLASM INVASIVENESS; PHOSPHORYLATION;

EID: 76649119448     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.053793     Document Type: Article

References (54)

1. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y. and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 2026-2029.
2. Amano, M., Chihara, K., Kimura, K., Fukata, Y., Nakamura, N., Matsuura, Y. and Kaibuchi, K. (1997). Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275, 1308-1311.
3. Bell, S. E., Mavila, A., Salazar, R., Bayless, K. J., Kanagala, S., Maxwell, S. A. and Davis, G. E. (2001). Differential gene expression during capillary morphogenesis in 3D collagen matrices: regulated expression of genes involved in basement membrane matrix assembly, cell cycle progression, cellular differentiation and G-protein signaling. J. Cell Sci. 114, 2755-2773.
4. Bresnick, A. R. (1999). Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11, 26-33.
5. Carman, C. V. and Springer, T. A. (2004). A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J. Cell Biol. 167, 377-388.
6. Chew, T. L., Masaracchia, R. and Wysolmerski, R. (1998). Phosphorylation of nonmuscle myosin II regulatory light chain by p21-activated kinase (gamma-PAK). J. Muscle Res. Cell Motil. 19, 839-854.
7. Chew, T. L., Wolf, W. A., Gallagher, P. J., Matsumura, F. and Chisholm, R. L. (2002). A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 156, 543-553.
8. Choe, M. M., Sporn, P. H. and Swartz, M. A. (2003). An in vitro airway wall model of remodeling. Am. J. Physiol. Lung Cell Mol. Physiol. 285, L427-L433.
9. Condeelis, J. and Pollard, J. W. (2006). Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124, 263-266.
10. Coulombe, P. A. and Wong, P. (2004). Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat. Cell Biol. 6, 699-706.
11. Darland, D. C. and D'Amore, P. A. (2001). TGF beta is required for the formation of capillary-like structures in three-dimensional cocultures of 10T1/2 and endothelial cells. Angiogenesis 4, 11-20.
12. Davis, G. E. and Bayless, K. J. (2003). An integrin and Rho GTPase-dependent pinocytic vacuole mechanism controls capillary lumen formation in collagen and fibrin matrices. Microcirculation 10, 27-44.
13. Davis, G. E., Koh, W. and Stratman, A. N. (2007). Mechanisms controlling human endothelial lumen formation and tube assembly in three-dimensional extracellular matrices. Birth Defects Res. C. Embryo Today 81, 270-285.
14. Dyson, S. E., Jones, D. G. and Kendrick, W. L. (1976). Some observations on the ultrastructure of developing rat cerebral capillaries. Cell Tissue Res. 173, 529-542.
15. Folkman, J. and Haudenschild, C. (1980). Angiogenesis in vitro. Nature 288, 551-556.
16. Garcia, J. G. and Schaphorst, K. L. (1995). Regulation of endothelial cell gap formation and paracellular permeability. J. Investig. Med. 43, 117-126.
17. Garcia, J. G., Davis, H. W. and Patterson, C. E. (1995). Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J. Cell Physiol. 163, 510-522.
18. Garcia, J. G. N., Verin, A. D., Herenyiova, M. and English, D. (1998). Adherent neutrophils activate endothelial myosin light chain kinase: role in transendothelial migration. J. Appl. Physiol. 84, 1817-1821.
19. Goeckeler, Z. M. and Wysolmerski, R. B. (1995). Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation. J. Cell Biol. 130, 613-627.
20. Gonzalez, A. M., Gonzales, M., Herron, G. S., Nagavarapu, U., Hopkinson, S. B., Tsuruta, D. and Jones, J. C. (2002). Complex interactions between the laminin alpha 4 subunit and integrins regulate endothelial cell behavior in vitro and angiogenesis in vivo. Proc. Natl. Acad. Sci. USA 99, 16075-16080.
21. Hixenbaugh, E. A., Goeckeler, Z. M., Papaiya, N. N., Wysolmerski, R. B., Silverstein, S. C. and Huang, A. J. (1997). Stimulated neutrophils induce myosin light chain phosphorylation and isometric tension in endothelial cells. Am. J. Physiol. 273, H981-H988.
22. Ingber, D. E. and Folkman, J. (1989a). How does extracellular matrix control capillary morphogenesis? Cell 58, 803-805.
23. Ingber, D. E. and Folkman, J. (1989b). Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J. Cell Biol. 109, 317-330.
24. Kamei, M., Saunders, W. B., Bayless, K. J., Dye, L., Davis, G. E. and Weinstein, B. M. (2006). Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442, 453-456.
25. Kamm, K. E. and Stull, J. T. (2001). Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem. 276, 4527-4530.
26. 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.
27. Korff, T. and Augustin, H. G. (1999). Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J. Cell Sci. 112 (Pt 19), 3249-3258.
28. Li, H., Fan, X. and Houghton, J. (2007). Tumor microenvironment: the role of the tumor stroma in cancer. J. Cell Biochem. 101, 805-815.
29. Lorenzon, P., Vecile, E., Nardon, E., Ferrero, E., Harlan, J. M., Tedesco, F. and Dobrina, A. (1998). Endothelial cell E- and P-selectin and vascular cell adhesion molecule-1 function as signaling receptors. J. Cell Biol. 142, 1381-1391.
30. Lunt, S. J., Chaudary, N. and Hill, R. P. (2008). The tumor microenvironment and metastatic disease. Clin. Exp. Metastasis. 26, 19-34.
31. Mierke, C. T., Rosel, D., Fabry, B. and Brabek, J. (2008a). Contractile forces in tumor cell migration. Eur. J. Cell Biol. 87, 669-676.
32. Mierke, C. T., Zitterbart, D. P., Kollmannsberger, P., Raupach, C., Schlotzer-Schrehardt, U., Goecke, T. W., Behrens, J. and Fabry, B. (2008b). Breakdown of the endothelial barrier function in tumor cell transmigration. Biophys. J. 94, 2832-2846.
33. Millan, J., Hewlett, L., Glyn, M., Toomre, D., Clark, P. and Ridley, A. J. (2006). Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat. Cell Biol. 8, 113-123.
34. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikura, M. and Tsien, R. Y. (1997). Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882-887.
35. Montesano, R. and Orci, L. (1988). Intracellular diaphragmed fenestrae in cultured capillary endothelial cells. J. Cell Sci. 89 (Pt 3), 441-447.
36. Montesano, R., Pepper, M. S., Vassalli, J. D. and Orci, L. (1987). Phorbol ester induces cultured endothelial cells to invade a fibrin matrix in the presence of fibrinolytic inhibitors. J. Cell Physiol. 132, 509-516.
37. Nakatsu, M. N., Sainson, R. C., Aoto, J. N., Taylor, K. L., Aitkenhead, M., Perezdel-Pulgar, S., Carpenter, P. M. and Hughes, C. C. (2003). Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and Angiopoietin-1. Microvasc. Res. 66, 102-112.
38. Nicosia, R. F., Tchao, R. and Leighton, J. (1982). Histotypic angiogenesis in vitro: light microscopic, ultrastructural, and radioautographic studies. In Vitro 18, 538-549.
39. Nieminen, M., Henttinen, T., Merinen, M., Marttila-Ichihara, F., Eriksson, J. E. and Jalkanen, S. (2006). Vimentin function in lymphocyte adhesion and transcellular migration. Nat. Cell Biol. 8, 156-162.
40. Parkhurst, M. R. and Saltzman, W. M. (1992). Quantification of human neutrophil motility in three-dimensional collagen gels. Effect of collagen concentration. Biophys. J. 61, 306-315.
41. Stull, J. T., Bowman, B. F., Gallagher, P. J., Herring, B. P., Hsu, L. C., Kamm, K. E., Kubota, Y., Leachman, S. A., Sweeney, H. L. and Tansey, M. G. (1990). Myosin phosphorylation in smooth and skeletal muscles: regulation and function. Prog. Clin. Biol. Res. 327, 107-126.
42. Totsukawa, G., Yamakita, Y., Yamashiro, S., Hartshorne, D. J., Sasaki, Y. and Matsumura, F. (2000). Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150, 797-806.
43. Verin, A. D., Patterson, C. E., Day, M. A. and Garcia, J. G. (1995). Regulation of endothelial cell gap formation and barrier function by myosin-associated phosphatase activities. Am. J. Physiol. 269, L99-L108.
44. Wiche, G. (1998). Role of plectin in cytoskeleton organization and dynamics. J. Cell Sci. 111 (Pt 17), 2477-2486.
45. Wittchen, E. S., van Buul, J. D., Burridge, K. and Worthylake, R. A. (2005). Trading spaces: Rap, Rac, and Rho as architects of transendothelial migration. Curr. Opin. Hematol. 12, 14-21.
46. Witz, I. P. (2006). Tumor-microenvironment interactions: the selectin-selectin ligand axis in tumor-endothelium cross talk. Cancer Treat Res. 130, 125-140.
47. Witz, I. P. (2008). Yin-yang activities and vicious cycles in the tumor microenvironment. Cancer Res. 68, 9-13.
48. Wolff, J. R. and Bar, T. (1972). 'Seamless' endothelia in brain capillaries during development of the rat's cerebral cortex. Brain Res. 41, 17-24.
49. Worthylake, R. A., Lemoine, S., Watson, J. M. and Burridge, K. (2001). RhoA is required for monocyte tail retraction during transendothelial migration. J. Cell Biol. 154, 147-160.
50. Wysolmerski, R. B. and Lagunoff, D. (1990). Involvement of myosin light-chain kinase in endothelial cell retraction. Proc. Natl. Acad. Sci. USA 87, 16-20.
51. Wysolmerski, R. B. and Lagunoff, D. (1991). Regulation of permeabilized endothelial cell retraction by myosin phosphorylation. Am J. Physiol. 261, C32-C40.
52. Youvan, D. C., Silva, C. M., Bylina, E. J., Coleman, W. J., Dilworth, M. R. and Yang, M. M. (1997). Calibration of fluorescence resonance energy transfer in microscopy using genetically engineered GFP derivatives on nickel chelating beads. Biotechnology et alia 3, 1-18.
53. Zeng, Q., Lagunoff, D., Masaracchia, R., Goeckeler, Z., Cote, G. and Wysolmerski, R. (2000). Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II. J. Cell Sci. 113, 471-482.
54. Zijlstra, A., Lewis, J., Degryse, B., Stuhlmann, H. and Quigley, J. P. (2008). The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 13, 221-234.