Met-induced membrane blebbing leads to amoeboid cell motility and invasion

Oncogene

Volumn 33, Issue 14, 2014, Pages 1788-1798

  Laser Azogui, A ^a   Diamant Levi, T ^a   Israeli, S ^a   Roytman, Y ^a   Tsarfaty, I ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Amoeboid cell motility; Blebbing; Invasion; Met; Metastasis

Indexed keywords

RHO FACTOR; RHO KINASE; SCATTER FACTOR RECEPTOR;

ACTIN FILAMENT; ACTIN MYOSIN INTERACTION; ACTIN POLYMERIZATION; AMOEBOID CELL; ARTICLE; BLEB MEMBRANE; BREAST CANCER; CANCER CELL; CELL MOTILITY; CELL STRAIN HEK293; CELL TYPE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; DEPOLYMERIZATION; EMBRYO; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; METASTASIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACTIN CYTOSKELETON; ACTINS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MEMBRANE MICRODOMAINS; MYOSINS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION;

EID: 84898010113     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.138     Document Type: Article

References (43)

1. Zeng Q, Chen S, You Z, Yang F, Carey TE, Saims D, et al. Hepatocyte growth factor inhibits anoikis in head and neck squamous cell carcinoma cells by activation of ERK and Akt signaling independent of NFkappa B. J Biol Chem 2002; 277: 25203-25208
2. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: Rationale and progress. Nat Rev Cancer 2012; 12: 89-103
3. Bottaro DP, Rubin JS, Faletto DL, Chan AM, Kmiecik TE, Vande WG, et al. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991; 251: 802-804
4. Danilkovitch-Miagkova A, Zbar B. Dysregulation of Met receptor tyrosine kinase activity in invasive tumors. J Clin Invest 2002; 109: 863-867
5. Peters S, Adjei AA. MET: A promising anticancer therapeutic target. Nat Rev Clin Oncol 2012; 9: 314-326
6. Jung KH, Park BH, Hong SS. Progress in cancer therapy targeting c-Met signaling pathway. Arch Pharmacal Res. (Research Support, Non-US Gov-t Review) 2012; 35: 595-604
7. Friedl P, Wolf K. Tumour-cell invasion and migration: Diversity and escape mechanisms. Nat Rev Cancer 2003; 3: 362-374
8. Sahai E, Marshall CJ. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 2003; 5: 711-719
9. Keller HU, Bebie H. Protrusive activity quantitatively determines the rate and direction of cell locomotion. Cell Motil Cytoskeleton 1996; 33: 241-251
10. Yoshida K, Soldati T. Dissection of amoeboid movement into two mechanically distinct modes. J Cell Sci 2006; 119(Pt 18): 3833-3844
11. Tournaviti S, Hannemann S, Terjung S, Kitzing TM, Stegmayer C, Ritzerfeld J, et al. SH4-domain-induced plasma membrane dynamization promotes bleb-Associated cell motility. J Cell Sci 2007; 120(Pt 21): 3820-3829
12. Charras GT, Hu CK, Coughlin M, Mitchison TJ. Reassembly of contractile actin cortex in cell blebs. J Cell Biol 2006; 175: 477-490
13. Gadea G, De Toledo M, Anguille C, Roux P. Loss of p53 promotes RhoA-ROCKdependent cell migration and invasion in 3D matrices. J Cell Biol 2007; 178: 23-30
14. Kitzing TM, Sahadevan AS, Brandt DT, Knieling H, Hannemann S, Fackler OT, et al. Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes Dev 2007; 21: 1478-1483
15. Pinner S, Sahai E. PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 2008; 10: 127-137
16. Vasiliev JM, Omelchenko T, Gelfand IM, Feder HH, Bonder EM. Rho overexpression leads to mitosis-Associated detachment of cells from epithelial sheets: A link to the mechanism of cancer dissemination. Proc Natl Acad Sci USA 2004; 101: 12526-12530
17. Corso S, Migliore C, Ghiso E, De Rosa G, Comoglio PM, Giordano S. Silencing the MET oncogene leads to regression of experimental tumors and metastases. Oncogene 2008; 27: 684-693
18. Ma PC, Tretiakova MS, Nallasura V, Jagadeeswaran R, Husain AN, Salgia R. Downstream signalling and specific inhibition of c-MET/HGF pathway in small cell lung cancer: Implications for tumour invasion. Br J Cancer 2007; 97: 368-377
19. Nguyen TN, Wang HJ, Zalzal S, Nanci A, Nabi IR. Purification and characterization of beta-Actin-rich tumor cell pseudopodia: Role of glycolysis. Exp Cell Res 2000; 258: 171-183
20. Vadnais J, Nault G, Daher Z, AmraeiM, Dodier Y, Nabi IR, et al. Autocrine activation of the hepatocyte growth factor receptor/met tyrosine kinase induces tumor cell motility by regulating pseudopodial protrusion. J Biol Chem 2002; 277: 48342-48350
21. Jia Z, Vadnais J, Lu ML, Noel J, Nabi IR. Rho/ROCK-dependent pseudopodial protrusion and cellular blebbing are regulated by p38 MAPK in tumour cells exhibiting autocrine c-Met activation. Biol Cell 2006; 98: 337-351
22. Maulik G, Kijima T, Ma PC, Ghosh SK, Lin J, Shapiro GI, et al. Modulation of the c-Met/hepatocyte growth factor pathway in small cell lung cancer. Clin Cancer Res 2002; 8: 620-627
23. Firon M, Shaharabany M, Altstock RT, Horev J, Abramovici A, Resau JH, et al. Dominant negative Met reduces tumorigenicity-metastasis and increases tubule formation in mammary cells. Oncogene 2000; 19: 2386-2397
24. Moshitch-Moshkovitz S, Tsarfaty G, Kaufman DW, Stein GY, Shichrur K, Solomon E, et al. In vivo direct molecular imaging of early tumorigenesis and malignant progression induced by transgenic expression of GFP-Met. Neoplasia 2006; 8: 353-363
25. Moffatt OD, Devitt A, Bell ED, Simmons DL, Gregory CD. Macrophage recognition of ICAM-3 on apoptotic leukocytes. J Immunol 1999; 162: 6800-6810
26. Jeffers M, Fiscella M, Webb CP, Anver M, Koochekpour S, Vande Woude GF. The mutationally activated Met receptor mediates motility and metastasis. Proc Natl Acad Sci USA. 1998; 95: 14417-14422
27. Miller M, Ginalski K, Lesyng B, Nakaigawa N, Schmidt L, Zbar B. Structural basis of oncogenic activation caused by point mutations in the kinase domain of the MET proto-oncogene: Modeling studies. Proteins 2001; 44: 32-43
28. Jiang WG, Martin TA, Parr C, Davies G, Matsumoto K, Nakamura T. Hepatocyte growth factor, its receptor, and their potential value in cancer therapies. Crit Rev Oncol Hematol 2005; 53: 35-69
29. Christensen JG, Burrows J, Salgia R. c-Met as a target for human cancer and characterization of inhibitors for therapeutic intervention. Cancer Lett 2005; 225: 1-26
30. Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, et al. Compensation mechanism in tumor cell migration: Mesenchymal-Amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 2003; 160: 267-277
31. Zeng Q, McCauley LK, Wang CY. Hepatocyte growth factor inhibits anoikis by induction of activator protein 1-dependent cyclooxygenase-2. Implication in head and neck squamous cell carcinoma progression. J Biol Chem 2002; 277: 50137-50142
32. Charras GT, Coughlin M, Mitchison TJ, Mahadevan L. Life and times of a cellular bleb. Biophys J 2008; 94: 1836-1853
33. Cunningham CC. Actin polymerization and intracellular solvent flow in cell surface blebbing. J Cell Biol 1995; 129: 1589-1599
34. Arni S, Ilangumaran S, van Echten-Deckert G, Sandhoff K, Poincelet M, Briol A, et al. Differential regulation of Src-family protein tyrosine kinases in GPI domains of T lymphocyte plasma membranes. Biochem Biophys Res Commun 1996; 225: 801-807
35. Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 2003; 100: 5813-5818
36. Douglass AD, Vale RD. Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells. Cell 2005; 121: 937-950
37. Maxfield FR. Plasma membrane microdomains. Curr Opin Cell Biol 2002; 14: 483-487
38. Abella JV, Parachoniak CA, Sangwan V, Park M. Dorsal ruffle microdomains potentiate Met receptor tyrosine kinase signaling and down-regulation. J Biol Chem 2010; 285: 24956-24967
39. Abella JV, Vaillancourt R, Frigault MM, Ponzo MG, Zuo D, Sangwan V, et al. The Gab1 scaffold regulates RTK-dependent dorsal ruffle formation through the adaptor Nck. J Cell Sci 2010; 123(Pt 8): 1306-1319
40. Holowka D, Sheets ED, Baird B. Interactions between Fc(epsilon)RI and lipid raft components are regulated by the actin cytoskeleton. J Cell Sci 2000; 113(Pt 6): 1009-1019
41. Andrews NL, Lidke KA, Pfeiffer JR, Burns AR, Wilson BS, Oliver JM, et al. Actin restricts FcepsilonRI diffusion and facilitates antigen-induced receptor immobilization. Nat Cell Biol 2008; 10: 955-963
42. Rong S, Segal S, Anver M, Resau JH, Vande Woude GF. Invasiveness and metastasis of NIH 3T3 cells induced by Met-hepatocyte growth factor/ scatter factor autocrine stimulation. Proc Natl Acad Sci USA 1994; 91: 4731-4735
43. Sambrook A, Fritsch EF, Maniatis T. Molecular Cloning. A laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory: New York, NY, USA, 1989.