Inhibition of cell migration and invasion mediated by the TAT-RasGAP317-326 peptide requires the DLC1 tumor suppressor

Oncogene

Volumn 33, Issue 44, 2014, Pages 5163-5172

  Barras, D ^a   Lorusso, G ^b   Ruegg C ^b   Widmann, C ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Adhesion; DLC1; Invasion; Migration; Peptide; RasGAP

Indexed keywords

ANTINEOPLASTIC AGENT; DELETED IN LIVER CANCER 1 PROTEIN; HERMES ANTIGEN; INTEGRIN; PROTEIN INHIBITOR; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TAT RASGAP 317 326 PEPTIDE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ACTIN; DLC-1 (DELETED IN LIVER CANCER) PROTEIN, MOUSE; DLC1 PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PEPTIDE FRAGMENT; RHO KINASE; TAT-RASGAP(317-326);

ACTIN FILAMENT; ARTICLE; CANCER CELL; CELL ADHESION; CELL DEATH; CELL INVASION; CONTROLLED STUDY; FOCAL ADHESION; GENE PRODUCT; HUMAN; HUMAN CELL; MIGRATION INHIBITION; OSTEOSARCOMA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL; ANIMAL; CELL MOTION; DRUG EFFECTS; FIBROBLAST; GENETICS; METABOLISM; MOUSE; PROTEIN PROCESSING; TUMOR CELL LINE;

ACTINS; ANIMALS; ANTIGENS, CD44; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; FIBROBLASTS; GTPASE-ACTIVATING PROTEINS; HUMANS; INTEGRINS; MICE; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RHO-ASSOCIATED KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84928495354     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.465     Document Type: Article

References (45)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Hanahan D, Weinberg RA. Hallmarks of cancer:the next generation. Cell 2011; 5: 646-674.
3. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat RevCancer 2002; 6: 442-454.
4. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 2009; 1-2: 15-33.
5. Chiang AC, Massague J. Molecular basis of metastasis. N Engl J Med 2008; 26: 2814-2823.
6. Sethi N, Kang Y. Unravelling the complexity of metastasis-molecular understanding and targeted therapies. Nat Rev Cancer 2011; 10: 735-748.
7. Bravo-Cordero JJ, Hodgson L, Condeelis J. Directed cell invasion and migration during metastasis. Curr Opin Cell Biol 2012; 2: 277-283.
8. Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003; 5: 362-374.
9. Byron A, Morgan MR, Humphries MJ. Adhesion signalling complexes. Curr Biol 2010; 24: R1063-R1067.
10. Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 2004; 1: 23-32.
11. Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane crosstalk between the extracellular matrix - Cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2001; 11: 793-805.
12. McClatchey AI, Giovannini M. Membrane organization and tumorigenesis-the NF2 tumor suppressor, Merlin. Genes Dev 2005; 19: 2265-2277.
13. Aoki K, Taketo MM. Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J Cell Sci 2007; 120: 3327-3335.
14. Durkin ME, Yuan BZ, Zhou X, Zimonjic DB, Lowy DR, Thorgeirsson SS et al. DLC-1:a Rho GTPase-activating protein and tumour suppressor. J Cell Mol Med 2007; 5: 1185-1207.
15. Lahoz A, Hall A. DLC1: a significant GAP in the cancer genome. Genes Dev 2008; 13: 1724-1730.
16. Yang X, Popescu NC, Zimonjic DB. DLC1 interaction with S100A10 mediates inhibition of in vitro cell invasion and tumorigenicity of lung cancer cells through a RhoGAP-independent mechanism. Cancer Res 2011; 8: 2916-2925.
17. Pamonsinlapatham P, Hadj-Slimane R, Lepelletier Y, Allain B, Toccafondi M, Garbay C et al. P120-Ras GTPase activating protein (RasGAP): a multi-interacting protein in downstream signaling. Biochimie 2009; 3: 320-328.
18. Yang JY, Widmann C. Antiapoptotic signaling generated by caspase-induced cleavage of RasGAP. Mol Cell Biol 2001; 16: 5346-5358.
19. Michod D, Yang JY, Chen J, Bonny C, Widmann C. A RasGAP-derived cell permeable peptide potently enhances genotoxin-induced cytotoxicity in tumor cells. Oncogene 2004; 55: 8971-8978.
20. Michod D, Annibaldi A, Schaefer S, Dapples C, Rochat B, Widmann C. Effect of RasGAP N2 fragment-derived peptide on tumor growth in mice. J Natl Cancer Inst 2009; 11: 828-832.
21. Pittet O, Petermann D, Michod D, Krueger T, Cheng C, Ris HB et al. Effect of the TAT-RasGAP(317-326) peptide on apoptosis of human malignant mesothelioma cells and fibroblasts exposed to meso-tetra-hydroxyphenyl-chlorin and light. J Photochem Photobiol B 2007; 1: 29-35.
22. Barras D, Widmann C. Promises of apoptosis-inducing peptides in cancer therapeutics. Curr Pharm Biotechnol 2011; 8: 1153-1165.
23. Yang JY, Walicki J, Michod D, Dubuis G, Widmann C. Impaired Akt activity downmodulation, caspase-3 activation, and apoptosis in cells expressing a caspaseresistant mutant of RasGAP at position 157. Mol Biol Cell 2005; 8: 3511-3520.
24. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT et al. A quantitativeanalysis of kinase inhibitor selectivity. Nat Biotechnol 2008; 1: 127-132.
25. Ross B, Kristensen O, Favre D, Walicki J, Kastrup JS, Widmann C et al. High resolution crystal structures of the p120 RasGAP SH3 domain. Biochem Biophys Res Commun 2007; 2: 463-468.
26. Felding-Habermann B, Mueller BM, Romerdahl CA, Cheresh DA. Involvement of integrin alpha V gene expression in human melanoma tumorigenicity. J Clin Invest 1992; 6: 2018-2022.
27. Beck M, Schmidt A, Malmstroem J, Claassen M, Ori A, Szymborska A et al. The quantitative proteome of a human cell line. Mol Syst Biol 2011; 7: 549.
28. Sheppard D. In vivo functions of integrins: lessons from null mutations in mice. Matrix Biol 2000; 3: 203-209.
29. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003; 1: 33-45.
30. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005; 1: 56-68.
31. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995; 6549: 539-544.
32. Hamadi A, Bouali M, Dontenwill M, Stoeckel H, Takeda K, Ronde P. Regulation of focal adhesion dynamics and disassembly by phosphorylation of FAK at tyrosine 397. J Cell Sci 2005; 118: 4415-4425.
33. Leblanc V, Tocque B, Delumeau I. Ras-GAP controls Rho-mediated cytoskeletal reorganization through its SH3 domain. Mol Cell Biol 1998; 9: 5567-5578.
34. Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 1999; 3: 578-585.
35. Hu KQ, Settleman J. Tandem SH2 binding sites mediate the RasGAP-RhoGAP interaction: a conformational mechanism for SH3 domain regulation. EMBO J 1997; 3: 473-483.
36. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 1997; 6616: 537-540.
37. Yang XY, Guan M, Vigil D, Der CJ, Lowy DR, Popescu NC. p120Ras-GAP binds the DLC1 Rho-GAP tumor suppressor protein and inhibits its RhoA GTPase and growth-suppressing activities. Oncogene 2009; 11: 1401-1409.
38. Kulkarni SV, Gish G, van der Geer P, Henkemeyer M, Pawson T. Role of p120 Ras-GAP in directed cell movement. J Cell Biol 2000; 2: 457-470.
39. Mai A, Veltel S, Pellinen T, Padzik A, Coffey E, Marjomaki V et al. Competitive binding of Rab21 and p120RasGAP to integrins regulates receptor traffic and migration. J Cell Biol 2011; 2: 291-306.
40. McGlade J, Brunkhorst B, Anderson D, Mbamalu G, Settleman J, Dedhar S et al. The N-terminal region of GAP regulates cytoskeletal structure and cell adhesion. EMBO J 1993; 8: 3073-3081.
41. Kawai K, Yamaga M, Iwamae Y, Kiyota M, Kamata H, Hirata H et al. A PLCd1-binding protein, p122RhoGAP, is localized in focal adhesions. Biochem Soc Trans 2004; 32: 1107-1109.
42. Li G, Du X, Vass WC, Papageorge AG, Lowy DR, Qian X. Full activity of the deleted in liver cancer 1 (DLC1) tumor suppressor depends on an LD-like motif that binds talin and focal adhesion kinase (FAK). Proc Natl Acad Sci USA 2011; 41: 17129-17134.
43. Yin HL, Janmey PA. Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 2003; 65: 761-789.
44. Jordan M, Schallhorn A, Wurm FM. Transfecting mammalian cells: optimization of critical parameters affecting calcium-phosphate precipitate formation. Nucleic Acids Res 1996; 4: 596-601.
45. Bulat N, Waeber G, Widmann C. LDLs stimulate p38 MAPKs and wound healing through SR-BI independently of Ras and PI3 kinase. J Lipid Res 2009; 1: 81-89.