Cancer cell invasion is enhanced by applied mechanical stimulation

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Menon, Shalini ^a   Beningo, Karen A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COFILIN; CYTOCHALASIN B; FIBRONECTIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER INVASION; CELL MIGRATION; CONTROLLED STUDY; DEPOLYMERIZATION; GENE SILENCING; HUMAN; HUMAN CELL; MECHANICAL STIMULATION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; RIGIDITY; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; WESTERN BLOTTING; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CELL CULTURE; CELL MOTION; EVALUATION; EXTRACELLULAR MATRIX; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; METASTASIS; NEOPLASM; PATHOLOGY; PHYSIOLOGY; STIMULATION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; EMBRYO, MAMMALIAN; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICE; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; PHYSICAL STIMULATION; STRESS, MECHANICAL;

EID: 79951909900     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017277     Document Type: Article

References (72)

1. Alexander NR, Branch KM, Parekh A, Clark ES, Iwueke IC, et al. (2008) Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 18: 1295-1299.
2. Poincloux R, Lizarraga F, Chavrier P, (2009) Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 122: 3015-3024.
3. Busco G, Cardone RA, Greco MR, Bellizzi A, Colella M, et al. (2010) NHE1 promotes invadopodial ECM proteolysis through acidification of the peri-invadopodial space. FASEB J.
4. Chambers AF, Groom AC, MacDonald IC, (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2: 563-572.
5. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, et al. (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709.
6. Desmouliere A, Guyot C, Gabbiani G, (2004) The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 48: 509-517.
7. Tlsty TD, Coussens LM, (2006) Tumor stroma and regulation of cancer development. Annu Rev Pathol 1: 119-150.
8. Bissell MJ, Radisky D, (2001) Putting tumours in context. Nat Rev Cancer 1: 46-54.
9. Amatangelo MD, Bassi DE, Klein-Szanto AJ, Cukierman E, (2005) Stroma-derived three-dimensional matrices are necessary and sufficient to promote desmoplastic differentiation of normal fibroblasts. Am J Pathol 167: 475-488.
10. Condeelis J, Pollard JW, (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266.
11. Pollard JW, (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4: 71-78.
12. Mueller MM, Fusenig NE, (2004) Friends or foes- bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4: 839-849.
13. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
14. Kostic A, Lynch CD, Sheetz MP, (2009) Differential matrix rigidity response in breast cancer cell lines correlates with the tissue tropism. PLoS One 4: e6361.
15. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139: 891-906.
16. Kostic A, Sheetz MP, (2006) Fibronectin rigidity response through Fyn and p130Cas recruitment to the leading edge. Mol Biol Cell 17: 2684-2695.
17. Kostic A, Sap J, Sheetz MP, (2007) RPTPalpha is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J Cell Sci 120: 3895-3904.
18. Friedland JC, Lee MH, Boettiger D, (2009) Mechanically activated integrin switch controls alpha5beta1 function. Science 323: 642-644.
19. Bhowmick NA, Neilson EG, Moses HL, (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337.
20. Follonier L, Schaub S, Meister JJ, Hinz B, (2008) Myofibroblast communication is controlled by intercellular mechanical coupling. J Cell Sci 121: 3305-3316.
21. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C, (2001) Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12: 2730-2741.
22. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G, (1993) Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122: 103-111.
23. Singer II, Kawka DW, Kazazis DM, Clark RA, (1984) In vivo co-distribution of fibronectin and actin fibers in granulation tissue: immunofluorescence and electron microscope studies of the fibronexus at the myofibroblast surface. J Cell Biol 98: 2091-2106.
24. Dugina V, Fontao L, Chaponnier C, Vasiliev J, Gabbiani G, (2001) Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. J Cell Sci 114: 3285-3296.
25. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA, (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-363.
26. Goffin JM, Pittet P, Csucs G, Lussi JW, Meister JJ, et al. (2006) Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J Cell Biol 172: 259-268.
27. Beningo KA, Lo CM, Wang YL, (2002) Flexible polyacrylamide substrata for the analysis of mechanical interactions at cell-substratum adhesions. Methods Cell Biol 69: 325-339.
28. Wrobel LK, Fray TR, Molloy JE, Adams JJ, Armitage MP, et al. (2002) Contractility of single human dermal myofibroblasts and fibroblasts. Cell Motil Cytoskeleton 52: 82-90.
29. Meshel AS, Wei Q, Adelstein RS, Sheetz MP, (2005) Basic mechanism of three-dimensional collagen fibre transport by fibroblasts. Nat Cell Biol 7: 157-164.
30. Gimona M, Buccione R, Courtneidge SA, Linder S, (2008) Assembly and biological role of podosomes and invadopodia. Curr Opin Cell Biol 20: 235-241.
31. Ingham KC, Brew SA, Migliorini M, (2002) Type I collagen contains at least 14 cryptic fibronectin binding sites of similar affinity. Arch Biochem Biophys 407: 217-223.
32. Friedl P, Brocker EB, (2000) The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol Life Sci 57: 41-64.
33. Yu J, Ustach C, Kim HR, (2003) Platelet-derived growth factor signaling and human cancer. J Biochem Mol Biol 36: 49-59.
34. Pietras K, Sjoblom T, Rubin K, Heldin CH, Ostman A, (2003) PDGF receptors as cancer drug targets. Cancer Cell 3: 439-443.
35. Wipff PJ, Rifkin DB, Meister JJ, Hinz B, (2007) Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 179: 1311-1323.
36. Pietras K, Pahler J, Bergers G, Hanahan D, (2008) Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med 5: e19.
37. Fraley SI, Feng Y, Krishnamurthy R, Kim DH, Celedon A, et al. (2010) A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat Cell Biol 12: 598-604.
38. Bijman MN, van Berkel MP, van Nieuw Amerongen GP, Boven E, (2008) Interference with actin dynamics is superior to disturbance of microtubule function in the inhibition of human ovarian cancer cell motility. Biochem Pharmacol 76: 707-716.
39. Bousquet PF, Paulsen LA, Fondy C, Lipski KM, Loucy KJ, et al. (1990) Effects of cytochalasin B in culture and in vivo on murine Madison 109 lung carcinoma and on B16 melanoma. Cancer Res 50: 1431-1439.
40. Yamaguchi H, Lorenz M, Kempiak S, Sarmiento C, Coniglio S, et al. (2005) Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J Cell Biol 168: 441-452.
41. Klemke M, Kramer E, Konstandin MH, Wabnitz GH, Samstag Y, (2010) An MEK-cofilin signalling module controls migration of human T cells in 3D but not 2D environments. EMBO J 29: 2915-2929.
42. Mouneimne G, DesMarais V, Sidani M, Scemes E, Wang W, et al. (2006) Spatial and temporal control of cofilin activity is required for directional sensing during chemotaxis. Curr Biol 16: 2193-2205.
43. Mierke CT, Rosel D, Fabry B, Brabek J, (2008) Contractile forces in tumor cell migration. Eur J Cell Biol 87: 669-676.
44. Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ, Jain RK, (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 15: 778-783.
45. Cheng G, Tse J, Jain RK, Munn LL, (2009) Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 4: e4632.
46. Craig DH, Basson MD, (2009) Biological impact of mechanical stimuli on tumor metastasis. Cell Cycle 8: 828-831.
47. Kumar S, Weaver VM, (2009) Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev 28: 113-127.
48. Lo CM, Wang HB, Dembo M, Wang YL, (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79: 144-152.
49. Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ, (2003) ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 163: 583-595.
50. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, et al. (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166: 877-887.
51. Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, et al. (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60: 24-34.
52. 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.
53. Pietras K, Ostman A, (2010) Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 316: 1324-1331.
54. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, et al. (2002) Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 160: 985-1000.
55. Lee S, et al. (2010) Pericyte actomyosin-mediated contraction at the cell-material interface can modulate the microvascular niche. Journal of Physics: Condensed Matter 22: 194115.
56. Kutcher ME, Kolyada AY, Surks HK, Herman IM, (2007) Pericyte Rho GTPase mediates both pericyte contractile phenotype and capillary endothelial growth state. Am J Pathol 171: 693-701.
57. Kopfstein L, Christofori G, (2006) Metastasis: cell-autonomous mechanisms versus contributions by the tumor microenvironment. Cell Mol Life Sci 63: 449-468.
58. Weaver AM, (2006) Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 23: 97-105.
59. Buccione R, Caldieri G, Ayala I, (2009) Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev 28: 137-149.
60. Yamazaki D, Kurisu S, Takenawa T, (2005) Regulation of cancer cell motility through actin reorganization. Cancer Sci 96: 379-386.
61. Akiyama SK, Olden K, Yamada KM, (1995) Fibronectin and integrins in invasion and metastasis. Cancer Metastasis Rev 14: 173-189.
62. Krammer A, Craig D, Thomas WE, Schulten K, Vogel V, (2002) A structural model for force regulated integrin binding to fibronectin's RGD-synergy site. Matrix Biol 21: 139-147.
63. Gee EP, Ingber DE, Stultz CM, (2008) Fibronectin unfolding revisited: modeling cell traction-mediated unfolding of the tenth type-III repeat. PLoS One 3: e2373.
64. Krammer A, Lu H, Isralewitz B, Schulten K, Vogel V, (1999) Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc Natl Acad Sci U S A 96: 1351-1356.
65. Gao M, Craig D, Vogel V, Schulten K, (2002) Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics. J Mol Biol 323: 939-950.
66. Garcia AJ, Schwarzbauer JE, Boettiger D, (2002) Distinct activation states of alpha5beta1 integrin show differential binding to RGD and synergy domains of fibronectin. Biochemistry 41: 9063-9069.
67. Li F, Redick SD, Erickson HP, Moy VT, (2003) Force measurements of the alpha5beta1 integrin-fibronectin interaction. Biophys J 84: 1252-1262.
68. Jin H, Varner J, (2004) Integrins: roles in cancer development and as treatment targets. Br J Cancer 90: 561-565.
69. Martinkova E, Maglott A, Leger DY, Bonnet D, Stiborova M, et al. (2010) alpha5beta1 integrin antagonists reduce chemotherapy-induced premature senescence and facilitate apoptosis in human glioblastoma cells. Int J Cancer 127: 1240-1248.
70. Nam JM, Onodera Y, Bissell MJ, Park CC, (2010) Breast cancer cells in three-dimensional culture display an enhanced radioresponse after coordinate targeting of integrin alpha5beta1 and fibronectin. Cancer Res 70: 5238-5248.
71. Mueller SC, Ghersi G, Akiyama SK, Sang QX, Howard L, et al. (1999) A novel protease-docking function of integrin at invadopodia. J Biol Chem 274: 24947-24952.
72. Stylli SS, Kaye AH, Lock P, (2008) Invadopodia: at the cutting edge of tumour invasion. J Clin Neurosci 15: 725-737.