A Novel 3D Fibril Force Assay Implicates Src in Tumor Cell Force Generation in Collagen Networks

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Polackwich, Robert J ^a   Koch, Daniel ^a   Arevalo, Richard ^a   Miermont, Anne M ^b,c   Jee, Kathleen J ^b   Lazar, John ^b   Urbach, Jeffrey ^a   Mueller, Susette C ^b   McAllister, Ryan G ^a,b  

^a GEORGETOWN UNIVERSITY   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN TYROSINE KINASE;

ARTICLE; ASSAY; BREAST CANCER; CANCER CELL; CELL INTERACTION; CELL INVASION; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURFACE; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MECHANOTRANSDUCTION; METASTASIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; THREE DIMENSIONAL FIBRIL FORCE ASSAY;

BIOMECHANICAL PHENOMENA; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURFACE EXTENSIONS; COLLAGEN; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FEMALE; FOCAL ADHESIONS; GENE EXPRESSION; HUMANS; MATRIX METALLOPROTEINASE 14; NEOPLASMS; PROTEIN TRANSPORT; SRC-FAMILY KINASES; TRANSFECTION;

EID: 84874878845     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058138     Document Type: Article

References (78)

1. Hoffman BD, Crocker JC, (2009) Cell mechanics: dissecting the physical responses of cells to force. Annu Rev Biomed Eng 11 259-88: 259-288.
2. Wang JH, Lin JS, (2007) Cell traction force and measurement methods. Biomech Model Mechanobiol 6: 361-371.
3. Harris AK, Wild P, Stopak D, (1980) Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208: 177-179.
4. Kandow CE, Georges PC, Janmey PA, Beningo KA, (2007) Polyacrylamide hydrogels for cell mechanics: steps toward optimization and alternative uses. Methods Cell Biol 83: 29-46.
5. Sabass B, Gardel ML, Waterman CM, Schwarz US, (2008) High resolution traction force microscopy based on experimental and computational advances. Biophys J 94: 207-220.
6. Franck C, Maskarinec SA, Tirrell DA, Ravichandran G, (2011) Three-dimensional traction force microscopy: a new tool for quantifying cell-matrix interactions. PLoS ONE 6: e17833.
7. Legant WR, Miller JS, Blakely BL, Cohen DM, Genin GM, et al. (2010) Measurement of mechanical tractions exerted by cells in three-dimensional matrices. Nat Methods 7: 969-971.
8. Thomas SM, Brugge JS, (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13: 513-609.
9. Brown MT, Cooper JA, (1996) Regulation, substrates and functions of src. Biochim Biophys Acta 1287: 121-149.
10. Parsons SJ, Parsons JT, (2004) Src family kinases, key regulators of signal transduction. Oncogene 23: 7906-7909.
11. Puls LN, Eadens M, Messersmith W, (2011) Current status of SRC inhibitors in solid tumor malignancies. Oncologist 16: 566-578.
12. Gnoni A, Marech I, Silvestris N, Vacca A, Lorusso V, (2011) Dasatinib: an anti-tumour agent via Src inhibition. Curr Drug Targets 12: 563-578.
13. Summy JM, Gallick GE, (2003) Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 22: 337-358.
14. Mayer EL, Krop IE, (2010) Advances in targeting SRC in the treatment of breast cancer and other solid malignancies. Clin Cancer Res 16: 3526-3532.
15. Krndija D, Schmid H, Eismann JL, Lother U, Adler G, et al. (2010) Substrate stiffness and the receptor-type tyrosine-protein phosphatase alpha regulate spreading of colon cancer cells through cytoskeletal contractility. Oncogene 29: 2724-2738.
16. Jiang G, Huang AH, Cai Y, Tanase M, Sheetz MP, (2005) Rigidity Sensing at the Leading Edge Through {alpha}v{beta}3 Integrins and RPTP{alpha}. Biophys J 90: 1804-1809.
17. von Wichert G, Jiang G, Kostic A, De Vos K, Sap J, et al. (2003) RPTP-alpha acts as a transducer of mechanical force on alphav/beta3-integrin-cytoskeleton linkages. J Cell Biol 161: 143-153.
18. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, et al. (2006) Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127: 1015-1026.
19. Holle AW, Engler AJ, (2011) More than a feeling: discovering, understanding, and influencing mechanosensing pathways. Curr Opin Biotechnol 22: 648-654.
20. Kostic A, Sheetz MP, (2006) Fibronectin rigidity response through Fyn and p130Cas recruitment to the leading edge. Mol Biol Cell 17: 2684-2695.
21. Galbraith CG, Yamada KM, Sheetz MP, (2002) The relationship between force and focal complex development. J Cell Biol 159: 695-705.
22. Matthews BD, Overby DR, Mannix R, Ingber DE, (2006) Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119: 508-518.
23. Giannone G, Sheetz MP, (2006) Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 16: 213-223.
24. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC, (2006) Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 66: 3034-3043.
25. Murphy DA, Courtneidge SA, (2011) The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12: 413-426.
26. Kelley LC, Ammer AG, Hayes KE, Martin KH, Machida K, Jia L, Mayer BJ, Weed SA, (2010) Oncogenic Src requires a wild-type counterpart to regulate invadopodia maturation. J Cell Sci 123: 3923-3932.
27. Hoffman BD, Grashoff C, Schwartz MA, (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475: 316-323.
28. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A, et al. (2011) Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol 13: 1457-1465.
29. Wang Y, Botvinick EL, Zhao Y, Berns MW, Usami S, et al. (2005) Visualizing the mechanical activation of Src. Nature 434: 1040-1045.
30. Na S, Collin O, Chowdhury F, Tay B, Ouyang M, et al. (2008) Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc Natl Acad Sci U S A 105: 6626-6631.
31. Yu CH, Law JB, Suryana M, Low HY, Sheetz MP, (2011) Early integrin binding to Arg-Gly-Asp peptide activates actin polymerization and contractile movement that stimulates outward translocation. Proc Natl Acad Sci U S A 108: 20585-20590.
32. Wang N, Butler JP, Ingber DE, (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124-1127.
33. Machesky LM, Li A, (2010) Fascin: Invasive filopodia promoting metastasis. Commun Integr Biol 3: 263-270.
34. Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, et al. (2009) Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol 186: 571-587.
35. Pelham RJ Jr, Wang Y, (1999) High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol Biol Cell 10: 935-945.
36. Pelham RJ Jr, Wang YL, (1998) Cell locomotion and focal adhesions are regulated by the mechanical properties of the substrate. Biol Bull 194: 348-349.
37. Giannone G, Dubin-Thaler BJ, Dobereiner HG, Kieffer N, Bresnick AR, et al, (2004) Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116: 431-443.
38. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, et al. (2001) Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol 153: 1175-1186.
39. Kirmse R, Otto H, Ludwig T, (2011) Interdependency of cell adhesion, force generation and extracellular proteolysis in matrix remodeling. J Cell Sci 124: 1857-1866.
40. Beach JR, Hussey GS, Miller TE, Chaudhury A, Patel P, et al. (2011) Myosin II isoform switching mediates invasiveness after TGF-beta-induced epithelial-mesenchymal transition. Proc Natl Acad Sci U S A 108: 17991-17996.
41. Cukierman E, Bassi DE, (2010) Physico-mechanical aspects of extracellular matrix influences on tumorigenic behaviors. Semin Cancer Biol 20: 139-145.
42. Yu H, Mouw JK, Weaver VM, (2011) Forcing form and function: biomechanical regulation of tumor evolution. Trends Cell Biol 21: 47-56.
43. Artym VV, Matsumoto K, Mueller SC, Yamada KM, (2011) Dynamic membrane remodeling at invadopodia differentiates invadopodia from podosomes. Eur J Cell Biol 90: 172-180.
44. Bowden ET, Onikoyi E, Slack R, Myoui A, Yoneda T, et al. (2006) Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp Cell Res 312: 1240-1253.
45. Artym VV, Matsumoto K, (2010) Imaging cells in three-dimensional collagen matrix. Curr Protoc Cell Biol Chapter 10: 1-20.
46. Sabeh F, Shimizu-Hirota R, Weiss SJ, (2009) Protease-dependent versus-independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 185: 11-19.
47. Mueller SC, Artym VV, Kelly T (2008) Invadopodia: Interface for Invasion. In: Dylan E, Hoyer-Hansen G, Blasi F, Sloane BF, editors. The Cancer Degradome - Proteases in Cancer Biology. New York: Springer. 403-432.
48. Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, et al. (2004) Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 167: 769-781.
49. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ, (2006) A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 20: 2673-2686.
50. Mierke CT, Bretz N, Altevogt P, (2011) Contractile forces contribute to increased glycosylphosphatidylinositol-anchored receptor CD24-facilitated cancer cell invasion. J Biol Chem 286: 34858-34871.
51. Schoumacher M, Goldman RD, Louvard D, Vignjevic DM, (2010) Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol 189: 541-556.
52. Chen W-T, (1989) Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool 251: 167-185.
53. Weaver AM, (2006) Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 23: 97-105.
54. Petroll WM, Cavanagh HD, Jester JV, (2004) Dynamic three-dimensional visualization of collagen matrix remodeling and cytoskeletal organization in living corneal fibroblasts. Scanning 26: 1-10.
55. Grinnell F, Petroll WM, (2010) Cell motility and mechanics in three-dimensional collagen matrices. Annu Rev Cell Dev Biol 26: 335-361.
56. Parekh A, Ruppender NS, Branch KM, Sewell-Loftin MK, Lin J, et al. (2011) Sensing and Modulation of Invadopodia across a Wide Range of Rigidities. Biophys J 100: 573-582.
57. Albiges-Rizo C, Destaing O, Fourcade B, Planus E, Block MR, (2009) Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J Cell Sci 122: 3037-3049.
58. Collin O, Na S, Chowdhury F, Hong M, Shin ME, et al. (2008) Self-organized podosomes are dynamic mechanosensors. Curr Biol 18: 1288-1294.
59. Destaing O, Block MR, Planus E, Albiges-Rizo C, (2011) Invadosome regulation by adhesion signaling. Curr Opin Cell Biol 23: 597-606.
60. Gulyani A, Vitriol E, Allen R, Wu J, Gremyachinskiy D, et al. (2011) A biosensor generated via high-throughput screening quantifies cell edge Src dynamics. Nat Chem Biol 7: 437-444.
61. Li A, Dawson JC, Forero-Vargas M, Spence HJ, Yu X, et al. (2010) The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr Biol 20: 339-345.
62. Kikuchi K, Takahashi K, (2008) WAVE2- and microtubule-dependent formation of long protrusions and invasion of cancer cells cultured on three-dimensional extracellular matrices. Cancer Sci 99: 2252-2259.
63. Schoumacher M, Louvard D, Vignjevic D, (2011) Cytoskeleton networks in basement membrane transmigration. Eur J Cell Biol 90: 93-99.
64. Hotary K, Allen E, Punturieri A, Yana I, Weiss SJ, (2000) Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J Cell Biol 149: 1309-1323.
65. Tilghman RW, Cowan CR, Mih JD, Koryakina Y, Gioeli D, et al. (2010) Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS ONE 5: e12905.
66. Verollet C, Charriere GM, Labrousse A, Cougoule C, Le C, et al. (2011) Extracellular proteolysis in macrophage migration: losing grip for a breakthrough. Eur J Immunol 41: 2805-2813.
67. Van Goethem E, Guiet R, Balor S, Charriere GM, Poincloux R, et al. (2011) Macrophage podosomes go 3D. Eur J Cell Biol 90: 224-236.
68. Monsky WL, Lin C-Y, Aoyama A, Kelly T, Mueller SC, et al. (1994) A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells. Cancer Res 54: 5702-5710.
69. Linder S, (2009) Invadosomes at a glance. J Cell Sci 122: 3009-3013.
70. Linder S, Wiesner C, Himmel M, (2011) Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 27: 185-211.
71. Sung BH, Weaver A, (2011) Cell-cell fusion: a new function for invadosomes. Curr Biol 21: R121-R123.
72. Sens KL, Zhang S, Jin P, Duan R, Zhang G, et al. (2010) An invasive podosome-like structure promotes fusion pore formation during myoblast fusion. J Cell Biol 191: 1013-1027.
73. Carman CV, Sage PT, Sciuto TE, de la Fuente MA, Geha RS, et al. (2007) Transcellular diapedesis is initiated by invasive podosomes. Immunity 26: 784-797.
74. Artym VV, Yamada KM, Mueller SC, (2009) ECM Degradation Assays for Analyzing Local Cell Invasion. Methods Mol Biol 522: 1-9.
75. Bowden ET, Coopman PJ, Mueller SC, (2001) Invadopodia: unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol 63: 613-627.
76. Kaufman LJ, Brangwynne CP, Kasza KE, Filippidi E, Gordon VD, et al. (2005) Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. Biophys J 89: 635-650.
77. Frey MT, Engler A, Discher DE, Lee J, Wang YL, (2007) Microscopic methods for measuring the elasticity of gel substrates for cell culture: microspheres, microindenters, and atomic force microscopy. Methods Cell Biol 83: 47-65.
78. Xu Y, Engl WC, Jerison ER, Wallenstein KJ, Hyland C, et al. (2010) Imaging in-plane and normal stresses near an interface crack using traction force microscopy. Proc Natl Acad Sci U S A 107: 14964-14967.