Tumor cell migration in complex microenvironments

Cellular and Molecular Life Sciences

Volumn 70, Issue 8, 2013, Pages 1335-1356

  Polacheck, William J ^a   Zervantonakis, Ioannis K ^a   Kamm, Roger D ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cell migration; Chemotaxis; Interstitial flow; Mechanotransduction; Microfluidics; Tumor microenvironment

Indexed keywords

CADHERIN; FOCAL ADHESION KINASE; GROWTH FACTOR; INTEGRIN; MATRIX METALLOPROTEINASE; PROTEIN TYROSINE KINASE;

CANCER GROWTH; CANCER INVASION; CELL ASSAY; CELL DENSITY; CELL INTERACTION; CELL MIGRATION; CELL STIMULATION; CELL STRUCTURE; CELL TYPE; CELLULAR STRESS RESPONSE; CHEMOTAXIS; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; INTERSTITIAL FLUID; MACROPHAGE; MATHEMATICAL MODEL; MECHANOTRANSDUCTION; MICROFLUIDICS; MICROTECHNOLOGY; NONHUMAN; REVIEW; STROMA CELL; TRANSPORT KINETICS; TUMOR CELL MIGRATION; TUMOR MICROENVIRONMENT;

ANIMALS; CELL MOVEMENT; HUMANS; MECHANOTRANSDUCTION, CELLULAR; NEOPLASM INVASIVENESS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84876678070     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1115-1     Document Type: Review

References (223)

1. Chambers AF, Groom AC, MacDonald IC (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2(8):563-572 (Pubitemid 37328923)
2. Weigelt B, Peterse JL, van 't Veer LJ (2005) Breast cancer metastasis: markers and models. Nat Rev Cancer 5(8):591-602 (Pubitemid 41081385)
3. Mueller MM, Fusenig NE (2004) Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4(11):839-849 (Pubitemid 39472951)
4. Friedl P, Alexander S (2011) Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 147(5):992-1009
5. Bristow RG, Hill RP (2008) Hypoxia and metabolism: hypoxia, DNA repair and genetic instability. Nat Rev Cancer 8(3):180-192 (Pubitemid 351301853)
6. Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant tumor. Science 197(4306):893-895 (Pubitemid 8168759)
7. Weigelt B et al (2005) Molecular portraits and 70-gene prognosis signature are preserved throughout the metastatic process of breast cancer. Cancer Res 65(20):9155-9158 (Pubitemid 41507977)
8. Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369(9574):1742-1757 (Pubitemid 46755391)
9. Almog N (2010) Molecular mechanisms underlying tumor dormancy. Cancer Lett 294(2):139-146
10. Paez D et al (2011) Cancer dormancy: a model of early dissemination and late cancer recurrence. Clin Cancer Res 18(3):645-653
11. Rhim AD et al (2012) EMT and dissemination precede pancreatic tumor formation. Cell 148(1-2):349-361
12. Paszek MJ et al (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241-254 (Pubitemid 41317594)
13. Moore SW, Roca-Cusachs P, Sheetz MP (2010) Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev Cell 19(2):194-206
14. Roussos ET, Condeelis JS, Patsialou A (2011) Chemotaxis in cancer. Nat Rev Cancer 11(8):573-587
15. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326(5957):1216-1219
16. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9(4):239-252
17. Boyden S (1962) The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leucocytes. J Exp Med 115:453-466
18. Zigmond SH (1988) Orientation chamber in chemotaxis. Methods Enzymol 162:65-72 (Pubitemid 19019496)
19. Zicha D, Dunn GA, Brown AF (1991) A new direct-viewing chemotaxis chamber. J Cell Sci 99(Pt 4):769-775
20. Gundersen RW, Barrett JN (1979) Neuronal chemotaxis: chick dorsal-root axons turn toward high concentrations of nerve growth factor. Science 206(4422):1079-1080 (Pubitemid 10208880)
21. Soon L et al (2005) Description and characterization of a chamber for viewing and quantifying cancer cell chemotaxis. Cell Motil Cytoskelet 62(1):27-34 (Pubitemid 41254608)
22. Yarrow JC et al (2004) A high-throughput cell migration assay using scratch wound healing, a comparison of image-based readout methods. BMC Biotechnol 4:21 (Pubitemid 40195466)
23. Wong MK, Gotlieb AI (1988) The reorganization of microfilaments, centrosomes, and microtubules during in vitro small wound reendothelialization. J Cell Biol 107(5):1777-1783 (Pubitemid 18263547)
24. Van Horssen R, ten Hagen TL (2011) Crossing barriers: the new dimension of 2D cell migration assays. J Cell Physiol 226(1):288-290
25. Toley BJ et al (2012) Micrometer-scale oxygen delivery rearranges cells and prevents necrosis in tumor tissue in vitro. Biotechnol Prog 28(2):515-525
26. Simpson KJ et al (2008) Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat Cell Biol 10(9):1027-1038
27. Murrell M, Kamm R, Matsudaira P (2011) Tension, free space, and cell damage in a microfluidic wound healing assay. PLoS One 6(9):e24283
28. Chung S et al (2009) Cell migration into scaffolds under co-culture conditions in a microfluidic platform. Lab Chip 9(2):269-275
29. von Philipsborn AC et al (2006) Growth cone navigation in substrate-bound ephrin gradients. Development 133(13):2487-2495 (Pubitemid 44123398)
30. Salieb-Beugelaar GB et al (2010) Latest developments in microfluidic cell biology and analysis systems. Anal Chem 82(12):4848-4864
31. Saadi W et al (2006) A parallel-gradient microfluidic chamber for quantitative analysis of breast cancer cell chemotaxis. Biomed Microdevices 8(2):109-118 (Pubitemid 44251364)
32. Polacheck WJ, Charest JL, Kamm RD (2011) Interstitial flow influences direction of tumor cell migration through competing mechanisms. Proc Natl Acad Sci USA 108(27):11115-11120
33. Huang CW et al (2009) Electrotaxis of lung cancer cells in a multiple-electric-field chip. Biosens Bioelectron 24(12):3510-3516
34. Hsu TH et al (2012) The migration speed of cancer cells influenced by macrophages and myofibroblasts co-cultured in a microfluidic chip. Integr Biol (Camb) 4:177-182
35. Zervantonakis IK et al (2011) Microfluidic devices for studying heterotypic cell-cell interactions and tissue specimen cultures under controlled microenvironments. Biomicrofluidics 5(1):13406
36. Pathak A, Kumar S (2011) Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integr Biol (Camb) 3(4):267-278
37. Kim HD, Peyton SR (2012) Bio-inspired materials for parsing matrix physicochemical control of cell migration: a review. Integr Biol (Camb) 4(1):37-52
38. Levental KR et al (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139(5):891-906
39. 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(1):11-19
40. Lo CM et al (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79(1):144-152
41. Kaji H et al (2011) Engineering systems for the generation of patterned co-cultures for controlling cell-cell interactions. Biochim Biophys Acta 1810(3):239-250
42. Polio SR et al (2012) A micropatterning and image processing approach to simplify measurement of cellular traction forces. Acta Biomater 8(1):82-88
43. Doyle AD et al (2009) One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol 184(4):481-490
44. Jiang X et al (2005) Directing cell migration with asymmetric micropatterns. Proc Natl Acad Sci USA 102(4):975-978 (Pubitemid 40170710)
45. Irimia D, Toner M (2009) Spontaneous migration of cancer cells under conditions of mechanical confinement. Integr Biol (Camb) 1(8-9):506-512
46. Kaji H et al (2009) Controlled cocultures of HeLa cells and human umbilical vein endothelial cells on detachable substrates. Lab Chip 9(3):427-432
47. Liu L et al (2011) Probing the invasiveness of prostate cancer cells in a 3D microfabricated landscape. Proc Natl Acad Sci USA 108(17):6853-6856
48. Condeelis J, Segall JE (2003) Intravital imaging of cell movement in tumours. Nat Rev Cancer 3(12):921-930 (Pubitemid 37500177)
49. Pittet MJ, Weissleder R (2011) Intravital imaging. Cell 147(5):983-991
50. Alexander S et al (2008) Dynamic imaging of cancer growth and invasion: a modified skin-fold chamber model. Histochem Cell Biol 130(6):1147-1154
51. Stoletov K et al (2007) High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc Natl Acad Sci USA 104(44):17406-17411 (Pubitemid 350219851)
52. Zijlstra A et al (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(3):221-234 (Pubitemid 351318371)
53. Wyckoff J et al (2011) High-resolution multiphoton imaging of tumors in vivo. Cold Spring Harb Protoc 2011(10):1167-1184
54. Moshitch-Moshkovitz S et al (2006) In vivo direct molecular imaging of early tumorigenesis and malignant progression induced by transgenic expression of GFP-Met. Neoplasia 8(5):353-363 (Pubitemid 43830742)
55. Wyckoff J et al (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64(19):7022-7029 (Pubitemid 39331012)
56. Byrne HM (2010) Dissecting cancer through mathematics: from the cell to the animal model. Nat Rev Cancer 10(3):221-230
57. Baxter LT, Jain RK (1989) Transport of fluid and macromolecules in tumors. 1. Role of interstitial pressure and convection. Microvasc Res 37(1):77-104 (Pubitemid 19045527)
58. Chauhan VP et al (2011) Delivery of molecular and nanoscale medicine to tumors: transport barriers and strategies. Annu Rev Chem Biomol Eng 2(1):281-298
59. Jeon J, Quaranta V, Cummings PT (2010) An off-lattice hybrid discrete-continuum model of tumor growth and invasion. Biophys J 98(1):37-47
60. Zaman MH et al (2006) Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci USA 103(29):10889-10894 (Pubitemid 44148391)
61. Zaman MH et al (2005) Computational model for cell migration in three-dimensional matrices. Biophys J 89(2):1389-1397 (Pubitemid 41099020)
62. Anderson AR et al (2006) Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127(5):905-915 (Pubitemid 44792251)
63. Sandersius SA, Weijer CJ, Newman TJ (2011) Emergent cell and tissue dynamics from subcellular modeling of active biomechanical processes. Phys Biol 8(4):045007
64. Schoeberl B et al (2002) Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat Biotechnol 20(4):370-375 (Pubitemid 34286330)
65. Painter KJ (2009) Modelling cell migration strategies in the extracellular matrix. J Math Biol 58(4-5):511-543
66. Ramis-Conde I et al (2009) Multi-scale modelling of cancer cell intravasation: the role of cadherins in metastasis. Phys Biol 6(1):016008
67. Irimia D et al (2009) Adaptive-control model for neutrophil orientation in the direction of chemical gradients. Biophys J 96(10):3897-3916
68. Thompson EW et al (1994) Oncogene-induced basement membrane invasiveness in human mammary epithelial cells. Clin Exp Metastasis 12(3):181-194 (Pubitemid 24196027)
69. Sommers CL et al (1992) Loss of epithelial markers and acquisition of vimentin expression in adriamycin- and vinblastine-resistant human breast cancer cell lines. Cancer Res 52(19):5190-5197
70. Nieman MT et al (1999) N-cadherin promotes motility in human breast cancer cells regardless of their E-cadherin expression. J Cell Biol 147(3):631-644 (Pubitemid 29523468)
71. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2(6):442-454
72. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84(3):359-369 (Pubitemid 26058561)
73. Ridley AJ et al (2003) Cell migration: integrating signals from front to back. Science 302(5651):1704-1709 (Pubitemid 37505725)
74. Weaver AM (2006) Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 23(2):97-105 (Pubitemid 44440169)
75. Tranquillo RT, Lauffenburger DA, Zigmond SH (1988) A stochastic model for leukocyte random motility and chemotaxis based on receptor binding fluctuations. J Cell Biol 106(2):303-309 (Pubitemid 18052180)
76. Stoker M, Gherardi E (1991) Regulation of cell movement: the motogenic cytokines. Biochim Biophys Acta 1072(1):81-102 (Pubitemid 121007531)
77. Petrie RJ, Doyle AD, Yamada KM (2009) Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10(8):538-549
78. Dickinson RB, Tranquillo RT (1993) Optimal estimation of cell-movement indexes from the statistical-Analysis of cell tracking data. AIChE J 39(12):1995-2010
79. Ware MF, Wells A, Lauffenburger DA (1998) Epidermal growth factor alters fibroblast migration speed and directional persistence reciprocally and in a matrix-dependent manner. J Cell Sci 111(Pt 16):2423-2432 (Pubitemid 28434928)
80. Haessler U et al (2012) Migration dynamics of breast cancer cells in a tunable 3D interstitial flow chamber. Integr Biol (Camb) 4(4):401-409
81. Bissell MJ et al (2002) The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 70(9-10):537-546 (Pubitemid 36194318)
82. Boyd NF et al (1998) Mammographic densities and breast cancer risk. Cancer Epidemiol Biomarkers Prev 7(12):1133-1144 (Pubitemid 29001671)
83. Provenzano PP et al (2009) Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28(49):4326-4343
84. van der Slot AJ et al (2005) Elevated formation of pyridinoline cross-links by profibrotic cytokines is associated with enhanced lysyl hydroxylase 2b levels. Biochim Biophys Acta 1741(1-2):95-102 (Pubitemid 40824994)
85. Akiri G et al (2003) Lysyl oxidase-related protein-1 promotes tumor fibrosis and tumor progression in vivo. Cancer Res 63(7):1657-1666 (Pubitemid 36373659)
86. Paszek MJ, Weaver VM (2004) The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 9(4):325-342 (Pubitemid 41149140)
87. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673-687 (Pubitemid 35283958)
88. Alenghat FJ, DE Ingber (2002) Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci STKE 2002(119):pe6
89. Jalali S et al (2001) Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc Natl Acad Sci USA 98(3):1042-1046 (Pubitemid 32121183)
90. Kanchanawong P et al (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468(7323):580-584
91. Friedland JC, Lee MH, Boettiger D (2009) Mechanically activated integrin switch controls alpha5beta1 function. Science 323(5914):642-644
92. Galbraith CG, Yamada KM, Sheetz MP (2002) The relationship between force and focal complex development. J Cell Biol 159(4):695-705
93. Balaban NQ et al (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 3(5):466-472 (Pubitemid 32422082)
94. Burke PA et al (2002) Cilengitide targeting of alpha(v)beta(3) integrin receptor synergizes with radioimmunotherapy to increase efficacy and apoptosis in breast cancer xenografts. Cancer Res 62(15):4263-4272 (Pubitemid 34827281)
95. Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751):1139-1143 (Pubitemid 41681732)
96. Baker EL, Bonnecaze RT, Zaman MH (2009) Extracellular matrix stiffness and architecture govern intracellular rheology in cancer. Biophys J 97(4):1013-1021
97. Baker EL et al (2010) Cancer cell stiffness: integrated roles of three-dimensional matrix stiffness and transforming potential. Biophys J 99(7):2048-2057
98. Moissoglu K, Schwartz MA (2006) Integrin signalling in directed cell migration. Biol Cell 98(9):547-555 (Pubitemid 44383371)
99. Moschos SJ et al (2007) Integrins and cancer. Oncology (Williston Park) 21(9 Suppl 3):13-20
100. Alexander NR et al (2008) Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 18(17):1295-1299
101. Ulrich TA, de Juan Pardo EM, Kumar S (2009) The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 69(10):4167-4174
102. Gupta GP et al (2005) Identifying site-specific metastasis genes and functions. Cold Spring Harb Symp Quant Biol 70:149-158 (Pubitemid 44124866)
103. Kostic A, Lynch CD, Sheetz MP (2009) Differential matrix rigidity response in breast cancer cell lines correlates with the tissue tropism. PLoS One 4(7):e6361
104. Hadjipanayi E, Mudera V, Brown RA (2009) Guiding cell migration in 3D: a collagen matrix with graded directional stiffness. Cell Motil Cytoskelet 66(3):121-128
105. Ehrbar M et al (2011) Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophys J 100(2):284-293
106. Gray DS, Tien J, Chen CS (2003) Repositioning of cells by mechanotaxis on surfaces with micropatterned Young's modulus. J Biomed Mater Res A 66(3):605-614 (Pubitemid 37517206)
107. Even-Ram S, Yamada KM (2005) Cell migration in 3D matrix. Curr Opin Cell Biol 17(5):524-532 (Pubitemid 41267167)
108. Ulrich TA et al (2010) Probing cellular mechanobiology in three-dimensional culture with collagen-Agarose matrices. Biomaterials 31(7):1875-1884
109. Sasaki N, Odajima S (1996) Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. J Biomech 29(5):655-658 (Pubitemid 26093293)
110. Yang YL, Motte S, Kaufman LJ (2010) Pore size variable type I collagen gels and their interaction with glioma cells. Biomaterials 31(21):5678-5688
111. Wolf K et al (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9(8):893-904 (Pubitemid 47190444)
112. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161-174 (Pubitemid 37328786)
113. Friedl P, Wolf K (2008) Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Res 68(18):7247-7249
114. Sabeh F et al (2004) Tumor cell traffic through the extracellular matrix is controlled by the membrane-Anchored collagenase MT1-MMP. J Cell Biol 167(4):769-781 (Pubitemid 39565156)
115. Mu D et al (2002) The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol 157(3):493-507 (Pubitemid 34839812)
116. Lee S et al (2005) Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 169(4):681-691 (Pubitemid 41002860)
117. Fleury ME, Boardman KC, Swartz MA (2006) Autologous morphogen gradients by subtle interstitial flow and matrix interactions. Biophys J 91(1):113-121 (Pubitemid 44015312)
118. Tomasek JJ et al (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5):349-363 (Pubitemid 34619269)
119. Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315(26):1650-1659 (Pubitemid 17052899)
120. Sappino AP et al (1988) Smooth-muscle differentiation in stromal cells of malignant and non-malignant breast tissues. Int J Cancer 41(5):707-712
121. De Wever O et al (2008) Stromal myofibroblasts are drivers of invasive cancer growth. Int J Cancer 123(10):2229-2238
122. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6(5):392-401
123. Sadlonova A et al (2009) Identification of molecular distinctions between normal breast-Associated fibroblasts and breast cancer-Associated fibroblasts. Cancer Microenviron 2(1):9-21
124. Beacham DA, Cukierman E (2005) Stromagenesis: the changing face of fibroblastic microenvironments during tumor progression. Semin Cancer Biol 15(5):329-341 (Pubitemid 41140303)
125. Ronnov-Jessen L, Petersen OW, Bissell MJ (1996) Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev 76(1):69-125 (Pubitemid 26048279)
126. Dimanche-Boitrel MT et al (1994) In vivo and in vitro invasiveness of a rat colon-cancer cell line maintaining E-cadherin expression: an enhancing role of tumor-Associated myofibroblasts. Int J Cancer 56(4):512-521 (Pubitemid 24094402)
127. Huang D et al (1993) Mechanisms and dynamics of mechanical strengthening in ligament-equivalent fibroblast-populated collagen matrices. Ann Biomed Eng 21(3):289-305 (Pubitemid 23177289)
128. Grinnell F, Ho CH (2002) Transforming growth factor beta stimulates fibroblast-collagen matrix contraction by different mechanisms in mechanically loaded and unloaded matrices. Exp Cell Res 273(2):248-255 (Pubitemid 34920675)
129. Gaggioli C et al (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9(12):1392-1400 (Pubitemid 350201752)
130. Stevenson MD et al (2010) Pericellular conditions regulate extent of cell-mediated compaction of collagen gels. Biophys J 99(1):19-28
131. Provenzano PP et al (2006) Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 4(1):38 (Pubitemid 46210997)
132. Wang W et al (2002) Single cell behavior in metastatic primary mammary tumors correlated with gene expression patterns revealed by molecular profiling. Cancer Res 62(21):6278-6288 (Pubitemid 35244482)
133. Wyckoff JB et al (2006) ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr Biol 16(15):1515-1523 (Pubitemid 44142977)
134. Provenzano PP et al (2008) Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 95(11):5374-5384
135. Dickinson RB, Guido S, Tranquillo RT (1994) Biased cell migration of fibroblasts exhibiting contact guidance in oriented collagen gels. Ann Biomed Eng 22(4):342-356 (Pubitemid 24264082)
136. Ilina O et al (2011) Two-photon laser-generated microtracks in 3D collagen lattices: principles of MMP-dependent and -independent collective cancer cell invasion. Physical Biol 8:015010 8(2)
137. Boucher Y, Jain RK (1992) Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse. Cancer Res 52(18):5110-5114
138. Sarntinoranont M, Rooney F, Ferrari M (2003) Interstitial stress and fluid pressure within a growing tumor. Ann Biomed Eng 31(3):327-335
139. Helmlinger G et al (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 15(8):778-783 (Pubitemid 27329482)
140. Roose T et al (2003) Solid stress generated by spheroid growth estimated using a linear poroelasticity modelẫ†. Microvasc Res 66(3):204-212 (Pubitemid 37373595)
141. Cheng G et al (2009) Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 4(2):e4632
142. Padera TP et al (2004) Pathology: cancer cells compress intratumour vessels. Nature 427(6976):695 (Pubitemid 38294577)
143. Khalil AA, Friedl P (2010) Determinants of leader cells in collective cell migration. Integr Biol (Camb) 2(11-12):568-574
144. Tse JM et al (2012) Mechanical compression drives cancer cells toward invasive phenotype. Proc Natl Acad Sci USA 109:911-916
145. Muller A et al (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50-56 (Pubitemid 32225831)
146. Ben-Baruch A (2006) The multifaceted roles of chemokines in malignancy. Cancer Metastasis Rev 25(3):357-371 (Pubitemid 44922355)
147. Wang SJ et al (2004) Differential effects of EGF gradient profiles on MDA-MB-231 breast cancer cell chemotaxis. Exp Cell Res 300(1):180-189 (Pubitemid 39286227)
148. Scherber C et al (2012) Epithelial cell guidance by self-generated EGF gradients. Integr Biol (Camb) 4:259-269
149. Raja WK et al (2010) A new chemotaxis device for cell migration studies. Integr Biol (Camb) 2(11-12):696-706
150. Calvo F, Sahai E (2011) Cell communication networks in cancer invasion. Curr Opin Cell Biol 23:621-629
151. Li H, Fan X, Houghton J (2007) Tumor microenvironment: the role of the tumor stroma in cancer. J Cell Biochem 101(4):805-815 (Pubitemid 47040863)
152. Schor SL, Schor AM (2001) Phenotypic and genetic alterations in mammary stroma: implications for tumour progression. Breast Cancer Res 3(6):373-379 (Pubitemid 34196363)
153. Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4(1):71-78 (Pubitemid 38082155)
154. Sung KE et al (2011) Transition to invasion in breast cancer: a microfluidic in vitro model enables examination of spatial and temporal effects. Integr Biol (Camb) 3(4):439-450
155. Green CE et al (2009) Chemoattractant signaling between tumor cells and macrophages regulates cancer cell migration, metastasis and neovascularization. PLoS One 4(8):e6713
156. De Wever O et al (2004) Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J 18(9):1016-1018 (Pubitemid 39561510)
157. Liu T, Lin B, Qin J (2010) Carcinoma-Associated fibroblasts promoted tumor spheroid invasion on a microfluidic 3D co-culture device. Lab Chip 10(13):1671-1677
158. Franses JW et al (2011) Stromal endothelial cells directly influence cancer progression. Sci Transl Med 3(66):66ra5
159. Issa A et al (2009) Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumor cell-lymphatic cross-talk promote invasive phenotype. Cancer Res 69(1):349-357
160. Walter-Yohrling J et al (2003) Identification of genes expressed in malignant cells that promote invasion. Cancer Res 63(24):8939-8947 (Pubitemid 38064074)
161. Swartz MA, Fleury ME (2007) Interstitial flow and its effects in soft tissues. Annu Rev Biomed Eng 9:229-256 (Pubitemid 350246657)
162. Jain RK (1987) Transport of molecules in the tumor interstitium: a review. Cancer Res 47(12):3039-3051 (Pubitemid 17082621)
163. Jain RK, Baxter LT (1988) Mechanisms of heterogeneous distribution of monoclonal-Antibodies and other macromolecules in tumors - significance of elevated interstitial pressure. Cancer Res 48(24):7022-7032 (Pubitemid 19013976)
164. Stohrer M et al (2000) Oncotic pressure in solid tumors is elevated. Cancer Res 60(15):4251-4255 (Pubitemid 30636613)
165. Curti BD et al (1993) Interstitial pressure of subcutaneous nodules in melanoma and lymphoma patients: changes during treatment. Cancer Res 53(10 Suppl):2204-2207 (Pubitemid 23156799)
166. Jain RK, Tong RT, Munn LL (2007) Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model. Cancer Res 67(6):2729-2735 (Pubitemid 46548961)
167. Chary SR, Jain RK (1989) Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc Natl Acad Sci USA 86(14):5385-5389 (Pubitemid 19185554)
168. Dafni H et al (2002) Overexpression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin. Cancer Res 62(22):6731-6739 (Pubitemid 35364145)
169. Shieh AC, Swartz MA (2011) Regulation of tumor invasion by interstitial fluid flow. Phys Biol 8(1):015012
170. Shields JD et al (2007) Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 11(6):526-538 (Pubitemid 46856909)
171. Ng CP, Hinz B, Swartz MA (2005) Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118(Pt 20):4731-4739 (Pubitemid 41646383)
172. Shi ZD et al (2009) Interstitial flow promotes vascular fibroblast, myofibroblast, and smooth muscle cell motility in 3-D collagen I via upregulation of MMP-1. Am J Physiol Heart Circ Physiol 297(4):H1225-H1234
173. Shieh AC et al (2011) Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res 71(3):790-800
174. Pedersen JA, Lichter S, Swartz MA (2010) Cells in 3D matrices under interstitial flow: effects of extracellular matrix alignment on cell shear stress and drag forces. J Biomech 43(5):900-905
175. Pedersen JA, Boschetti F, Swartz MA (2007) Effects of extracellular fiber architecture on cell membrane shear stress in a 3D fibrous matrix. J Biomech 40(7):1484-1492 (Pubitemid 46628685)
176. Shi ZD, Wang H, Tarbell JM (2011) Heparan sulfate proteoglycans mediate interstitial flow mechanotransduction regulating MMP-13 expression and cell motility via FAK-ERK in 3D collagen. PLoS One 6(1):e15956
177. Beauvais DM, Rapraeger AC (2003) Syndecan-1-mediated cell spreading requires signaling by alpha(v)beta(3) integrins in human breast carcinoma cells. Exp Cell Res 286(2):219-232 (Pubitemid 36566435)
178. Qazi H, Shi ZD, Tarbell JM (2011) Fluid shear stress regulates the invasive potential of glioma cells via modulation of migratory activity and matrix metalloproteinase expression. PLoS One 6(5):e20348
179. McLean GW et al (2005) The role of focal-Adhesion kinase in cancer - a new therapeutic opportunity. Nat Rev Cancer 5(7):505-515 (Pubitemid 40942827)
180. Shi Q et al (2007) A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol Carcinog 46(6):488-496 (Pubitemid 46897053)
181. Shi Q, Boettiger D (2003) A novel mode for integrin-mediated signaling: tethering is required for phosphorylation of FAK Y397. Mol Biol Cell 14(10):4306-4315 (Pubitemid 37186330)
182. Schlaepfer DD et al (1994) Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372(6508):786-791
183. Calalb MB, Polte TR, Hanks SK (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 15(2):954-963
184. Sieg DJ et al (2000) FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2(5):249-256
185. Chan KT, Cortesio CL, Huttenlocher A (2009) FAK alters invadopodia and focal adhesion composition and dynamics to regulate breast cancer invasion. J Cell Biol 185(2):357-370
186. Hsia DA et al (2003) Differential regulation of cell motility and invasion by FAK. J Cell Biol 160(5):753-767 (Pubitemid 36298270)
187. Kim LC, Song LX, Haura EB (2009) Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 6(10):587-595
188. Frame MC (2002) Src in cancer: deregulation and consequences for cell behaviour. Biochim Biophys Acta 1602(2):114-130 (Pubitemid 34521791)
189. Giancotti FG, Tarone G (2003) Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu Rev Cell Dev Biol 19:173-206 (Pubitemid 37487347)
190. Cabodi S et al (2004) Integrin regulation of epidermal growth factor (EGF) receptor and of EGF-dependent responses. Biochem Soc Trans 32(Pt3):438-442 (Pubitemid 38813532)
191. Ivaska J, Heino J (2011) Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu Rev Cell Dev Biol 27:291-320
192. Wang F et al (1998) Reciprocal interactions between beta1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: a different perspective in epithelial biology. Proc Natl Acad Sci USA 95(25):14821-14826 (Pubitemid 29003714)
193. Trusolino L, Bertotti A, Comoglio PM (2001) A signaling adapter function for alpha 6 beta 4 integrin in the control of HGF-dependent invasive growth. Cell 107(5):643-654 (Pubitemid 34014865)
194. Kim JH, Asthagiri AR (2011) Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation. J Cell Sci 124(8):1280-1287
195. Engl T et al (2006) CXCR4 chemokine receptor mediates prostate tumor cell adhesion through alpha5 and beta3 integrins. Neoplasia 8(4):290-301
196. Mitra AK et al (2011) Ligand-independent activation of c-Met by fibronectin and alpha(5)beta(1)-integrin regulates ovarian cancer invasion and metastasis. Oncogene 30(13):1566-1576
197. Weber GF, Bjerke MA, DeSimone DW (2011) Integrins and cadherins join forces to form adhesive networks. J Cell Sci 124(Pt 8):1183-1193
198. Avizienyte E et al (2002) Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat Cell Biol 4(8):632-638
199. Liu X, Feng R (2010) Inhibition of epithelial to mesenchymal transition in metastatic breast carcinoma cells by c-Src suppression. Acta Biochim Biophys Sin (Shanghai) 42(7):496-501
200. Martinez-Rico C et al (2010) Integrins stimulate E-cadherin-mediated intercellular adhesion by regulating Src-kinase activation and actomyosin contractility. J Cell Sci 123(5):712-722
201. Tseng Q et al (2012) Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc Natl Acad Sci USA 109(5):1506-1511
202. Borghi N et al (2010) Regulation of cell motile behavior by crosstalk between cadherin- and integrin-mediated adhesions. Proc Natl Acad Sci USA 107(30):13324-13329
203. Abercrombie M, Heaysman JEM (1953) Observations on the social behaviour of cells in tissue culture. 1. Speed of movement of chick heart fibroblasts in relation to their mutual contacts. Exp Cell Res 5(1):111-131
204. Astin JW et al (2010) Competition amongst Eph receptors regulates contact inhibition of locomotion and invasiveness in prostate cancer cells. Nat Cell Biol 12(12):1194-1204
205. Provenzano PP et al (2012) Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 21(3):418-429
206. Song JW, Munn LL (2011) Fluid forces control endothelial sprouting. Proc Natl Acad Sci USA 108(37):15342-15347
207. Netti PA et al (2000) Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60(9):2497-2503 (Pubitemid 30262444)
208. Gilbert PM et al (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329(5995):1078-1081
209. Cross SE et al (2007) Nanomechanical analysis of cells from cancer patients. Nat Nanotechnol 2(12):780-783 (Pubitemid 350223349)
210. Kalluri R (2003) Angiogenesis: basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer 3(6):422-433 (Pubitemid 37328846)
211. Pluen A (2001) Role of tumor-host interactions in interstitial diffusion of macromolecules: cranial vs. subcutaneous tumors. Proc Natl Acad Sci USA 98(8):4628-4633 (Pubitemid 32295027)
212. McKee TD (2006) Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res 66(5):2509-2513
213. Castello-Cros R et al (2009) Staged stromal extracellular 3D matrices differentially regulate breast cancer cell responses through PI3K and beta I-integrins. BMC Cancer 9:94
214. Montes GS (1996) Structural biology of the fibres of the collagenous and elastic systems. Cell Biol Int 20(1):15-27 (Pubitemid 26128875)
215. Yamamura N et al (2007) Effects of the mechanical properties of collagen gel on the in vitro formation of microvessel networks by endothelial cells. Tissue Eng 13(7):1443-1453 (Pubitemid 47105753)
216. Thorne RG, Hrabetova S, Nicholson C (2004) Diffusion of epidermal growth factor in rat brain extracellular space measured by integrative optical imaging. J Neurophysiol 92(6):3471-3481 (Pubitemid 39506324)
217. Griffith LG, Swartz MA (2006) Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 7(3):211-224
218. Tyska MJ et al (1999) Two heads of myosin are better than one for generating force and motion. Proc Natl Acad Sci USA 96(8):4402-4407 (Pubitemid 29190348)
219. Guilford WH et al (1997) Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys J 72(3):1006-1021 (Pubitemid 27113629)
220. du Roure O et al (2005) Force mapping in epithelial cell migration. Proc Natl Acad Sci USA 102(7):2390-2395 (Pubitemid 40279386)
221. Kraning-Rush CM et al (2011) The role of the cytoskeleton in cellular force generation in 2D and 3D environments. Phys Biol 8(1):015009
222. Dembo M, Wang YL (1999) Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 76(4):2307-2316 (Pubitemid 29266384)
223. Boucher Y, Baxter LT, Jain RK (1990) Interstitial pressure-gradients in tissue-isolated and subcutaneous tumors - implications for therapy. Cancer Res 50(15):4478-4484 (Pubitemid 20230379)