Migration speed and directionality switch of normal epithelial cells after TGF-β1-induced EMT (tEMT) on micro-structured polydimethylsiloxane (PDMS) substrates with variations in stiffness and topographic patterning

Cell Communication and Adhesion

Volumn 20, Issue 5, 2013, Pages 115-126

  Wu, Tsung Hsien ^a   Li, Chia Hui ^a   Tang, Ming Jer ^a   Liang, Jen I ^a   Chen, Chia Hsin ^b   Yeh, Ming Long ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b KAOHSIUNG MUNICIPAL TA TUNG HOSPITAL   (Taiwan)

Author keywords

smooth muscle actin; cell migration speed; epithelial to mesenchymal transition; polydimethylsiloxane; substrate stiffness; substrate topography; time lapse microscopy; vinculin

Indexed keywords

DIMETICONE; TRANSFORMING GROWTH FACTOR BETA1; VINCULIN;

ARTICLE; CELL MIGRATION; CELL MOTILITY; EPITHELIAL MESENCHYMAL TRANSITION; FOCAL ADHESION; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ACTINS; ANIMALS; CELL LINE; CELL MOVEMENT; CELL SHAPE; DIMETHYLPOLYSILOXANES; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MICROSCOPY; MICROSPHERES; SURFACE PROPERTIES; TIME-LAPSE IMAGING; TRANSFORMING GROWTH FACTOR BETA1; VINCULIN;

EID: 84885209219     PISSN: 15419061     EISSN: 15435180     Source Type: Journal    
DOI: 10.3109/15419061.2013.833194     Document Type: Article

References (79)

1. Abercrombie M, Dunn GA (1975). Adhesions of fibroblasts to substratum during contact inhibition observed by interference reflection microscopy. Exp Cell Res. 92: 57-62.
2. Baac H, Lee JH, Seo JM, Park TH, Chung H, Lee SD, Kim SJ (2004). Submicron-scale topographical control of cell growth using holographic surface relief grating. Matr Sci Eng C. 24: 209-212.
3. Barnhart EL, Lee KC, Keren K, Mogilner A, Theriot JA (2011). An adhesion-dependent switch between mechanisms that determine motile cell shape. Plos Biol. 9: e1001059.
4. Beach JR, 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.
5. Berry CC, Campbell G, Spadiccino A, Robertson M, Curtis AS (2004). The influence of microscale topography on fibroblast attachment and motility. Biomaterials. 25: 5781-5788.
6. Bhattacharya S, Datta A, Berg JM, Gangopadhyay S (2005). Studies on Surface Wettability of Poly(Dimethyl) Siloxane (PDMS) and Glass Under Oxygen Plasma under oxygenplasma treatment and correlation with bond strength. J Microelectromech Syst. 14: 590-597.
7. Bhowmick NA, et al. (2001). Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell. 12: 27-36.
8. Biela SA, Su Y, Spatz JP, Kemkemer R (2009). Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater. 5: 2460-2466.
9. Birchmeier W (2005). Cell adhesion and signal transduction in cancer. Conference on cadherins, catenins and cancer. EMBO Rep. 6: 413-417.
10. Boukhalfa G, Desmouliere A, Rondeau E, Gabbiani G, Sraer JD (1996). Relationship between alpha-smooth muscle actin expression and fibrotic changes in human kidney. Exp Nephrol. 4: 241-247.
11. Brunette DM (1986). Spreading and orientation of epithelial cells on grooved substrata. Exp Cell Res. 167: 203-217.
12. Buergy D, Wenz F, Groden C, Brockmann MA (2012). Tumor-platelet interaction in solid tumors. Int J Cancer. 130: 2747-2760.
13. Butcher DT, Alliston T, Weaver VM (2009). A tense situation: forcing tumour progression. Nature Reviews Cancer. 9: 108-122.
14. Chen C-C, Hsieh PC-H, Wang G-M, Chen W-C, Yeh M-L (2009). The influence of surface morphology and rigidity of the substrata on cell motility. Materials Letters. 63: 1872-1875.
15. Choi CH, Hagvall SH, Wu BM, Dunn JC, Beygui RE, CJ CJK (2007). Cell interaction with three-dimensional sharp-tip nanotopography. Biomaterials. 28: 1672-1679.
16. Chrzanowska-Wodnicka M, Burridge K (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol. 133: 1403-1415.
17. Clark P, Connolly P, Curtis AS, Dow JA, Wilkinson CD (1990). Topographical control of cell behaviour: II. Multiple grooved substrata. [Research Support, Non-U.S. Gov't]. Development. 108: 635-644.
18. Coleman RE, Rubens RD (1987). The clinical course of bone metastases from breast cancer. Br J Cancer. 55: 61-66.
19. Cox TR, Erler JT (2011). Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech. 4: 165-178.
20. Dalby MJ, Riehle MO, Sutherland DS, Agheli H, Curtis ASG (2004). Changes in fibroblast morphology in response to nanocolumns produced by colloidal lithography. Biomaterials. 25: 5415-5422.
21. 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. [Research Support, Non-U.S. Gov't]. J Cell Biol. 122: 103-111.
22. Doyle AD, Kutys ML, Conti MA, Matsumoto K, Adelstein RS, Yamada KM (2012). Micro-environmental control of cell migration-myosin IIA is required for efficient migration in fibrillar environments through control of cell adhesion dynamics. J Cell Sci. 125: 2244-2256.
23. Engler AJ, Griffin MA, Sen S, Bönnemann CG, Sweeney HL, Discher DE (2004). Myotubes Differentiate Optimally on Substrates with Tissue-Like Stiffness: Pathological Implications for Soft or Stiff Microenvironments. J Cell Biol. 166: 877-887.
24. Frey MT, Tsai IY, Russell TP, Hanks SK, Wang YL (2006). Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. Biophys J. 90: 3774-3782.
25. Friedl P, Wolf K (2010). Plasticity of cell migration: a multiscale tuning model. J Cell Biol. 188: 11-19.
26. Gallant ND, Michael KE, Garcia AJ (2005). Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol Biol Cell. 16: 4329-4340.
27. Grashoff C, et al. (2010). Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature. 466: 263-266.
28. Gupton SL, Waterman-Storer CM (2006). Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell. 125: 1361-1374.
29. Huttenlocher A, Ginsberg MH, Horwitz AF (1996). Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity. J Cell Biol. 134: 1551-1562.
30. Kalluri R, Neilson EG (2003). Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest. 112: 1776-1784.
31. Kass L, Erler JT, Dembo M, Weaver VM (2007). Mammary epithelial cell: Influence of extracellular matrix composition and organization during development and tumorigenesis. Int J Bio Cell Bio. 39: 1987-1994.
32. Kim DH, Wirtz D (2013). Focal adhesion size uniquely predicts cell migration. FASEB J. 27: 1351-1361.
33. Klominek J, Robert KH, Sundqvist KG (1993). Chemotaxis and Haptotaxis of Human-Malignant Mesothelioma Cells- Effects of Fibronectin, Laminin, Type-Iv Collagen, and an Autocrine Motility Factor-Like Substance. Cancer Res. 53: 4376-4382.
34. Labelle M, Begum S, Hynes RO (2011). Direct signaling between platelets and cancer cells induces an epithelial-mesenchymallike transition and promotes metastasis. Cancer Cell. 20: 576-590.
35. LaGamba D, Nawshad A, Hay ED (2005). Microarray analysis of gene expression during epithelial-mesenchymal transformation. Dev Dyn. 234: 132-142.
36. Lam WA, Rosenbluth MJ, Fletcher DA (2008). Increased leukaemia cell stiffness is associated with symptoms of leucostasis in paediatric acute lymphoblastic leukaemia. Br J Haematol. 142: 497-501.
37. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS (2012). Matrix rigidity regulates a switch between TGF-beta 1-induced apoptosis and epithelial- mesenchymal transition. Mol Biol Cell. 23: 781-791.
38. Levental KR, et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 139: 891-906.
39. Lim JY, Donahue HJ (2007). Cell sensing and response to microand nanostructured surfaces produced by chemical and topographic patterning. Tissue Eng. 13: 1879-1891.
40. Lo CM, Wang HB, Dembo M, Wang YL (2000). Cell movement is guided by the rigidity of the substrate. Biophys J. 79: 144-152.
41. Mani SA, et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 133: 704-715.
42. Martínez E, Engel E, Planell JA, Samitier J (2009). Effects of artificial micro-and nano-structured surfaces on cell behaviour. Ann Anat. 191: 126-135.
43. Masszi A, et al. (2003). Central role for Rho in TGF-b1-induced a-smooth muscle actin expression during epithelialmesenchymal transition. Am J Physiol Renal Physiol. 284: F911-F924.
44. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell. 6: 483-495.
45. McCain ML, Lee H, Aratyn-Schaus Y, Kleber AG, Parker KK (2012). Cooperative coupling of cell-matrix and cell-cell adhesions in cardiac muscle. Proc Natl Acad Sci U S A. 109: 9881-9886.
46. Mierke CT, Kollmannsberger P, Zitterbart DP, Smith J, Fabry B, Goldmann WH (2008). Mechano-coupling and regulation of contractility by the vinculin tail domain. Biophys J. 94: 661-670.
47. Miettinen PJ, Ebner R, Lopez AR, Derynck R (1994). TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol. 127(6 Pt 2): 2021-2036.
48. Miyoshi H, et al. (2012). Characteristics of motility-based filtering of adherent cells on microgrooved surfaces. [Research Support, Non-U.S. Gov't]. Biomaterials. 33: 395-401.
49. Miyoshi H, Ju J, Lee SM, Cho DJ, Ko JS, Yamagata Y, Adachi T (2010). Control of highly migratory cells by microstructured surface based on transient change in cell behavior. Biomaterials. 31: 8539-8545.
50. Mori M, et al. (2009). Zyxin mediates actin fiber reorganization in epithelial-mesenchymal transition and contributes to endocardial morphogenesis. Mol Biol Cell. 20: 3115-3124.
51. Nawshad A, Lagamba D, Polad A, Hay ED (2005). Transforming growth factor-beta signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs. 179: 11-23.
52. Ng MR, Besser A, Danuser G, Brugge JS (2012). Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J Cell Biol. 199: 545-563.
53. Oakes PW, Patel DC, Morin NA, Zitterbart DP, Fabry B, Reichner JS, Tang JX (2009). Neutrophil morphology and migration are affected by substrate elasticity. Blood. 114: 1387-1395.
54. Paszek MJ, et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell. 8: 241-254.
55. Provenzano PP, Keely PJ (2009). The role of focal adhesion kinase in tumor initiation and progression. Cell Adh Migr. 3: 347-350.
56. Ronnov-Jessen L, Petersen OW (1993). Induction of alpha-smooth muscle actin by transforming growth factor-beta 1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab Invest. 68: 696-707.
57. Ronnov-Jessen L, Petersen OW (1996). A function for filamentous alpha-smooth muscle actin: retardation of motility in fibroblasts. J Cell Biol. 134: 67-80.
58. Schober M, et al. (2007). Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J Cell Biol. 176: 667-680.
59. Schoenwaelder SM, Burridge K (1999). Bidirectional signaling between the cytoskeleton and integrins. Curr Opin Cell Biol. 11: 274-286.
60. Serini G, Bochaton-Piallat ML, Ropraz P, Geinoz A, Borsi L, Zardi L, Gabbiani G (1998). The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. Journal of Cell Biology. 142: 873-881.
61. Small JV, Rottner K, Kaverina I, Anderson KI (1998). Assembling an actin cytoskeleton for cell attachment and movement. Biochim Biophys Acta. 1404: 271-281.
62. Suva LJ, Griffin RJ, Makhoul I (2009). Mechanisms of bone metastases of breast cancer. Endocr Relat Cancer. 16: 703-713.
63. Teixeira AI, Abrams GA, Bertics PJ, Murphy CJ, Nealey PF (2003). Epithelial contact guidance on well-defined microand nanostructured substrates. J Cell Sci. 116: 1881-1892.
64. Teixeira AI, McKie GA, Foley JD, Bertics PJ, Nealey PF, Murphy CJ (2006). The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials. 27: 3945-3954.
65. Thiery JP, Sleeman JP (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 7: 131-142.
66. Wilkinson CDW, Riehle M, Wood M, Gallagher J, Curtis ASG (2002). The use of materials patterned on a nano-and micro-metric scale in cellular engineering. Mater Sci Eng C. 19: 263-269.
67. Wójciak-Stothard B, Madeja Z, Korohoda W, Curtis A, Wilkinson C (1995). Activation of macrophage-like cells by multiple grooved substrata. Topographical control of cell behaviour. Cell Biol Int. 19: 485-490.
68. Wolfenson H, Bershadsky A, Henis YI, Geiger B (2011). Actomyosin-generated tension controls the molecular kinetics of focal adhesions. J Cell Sci. 124: 1425-1432.
69. Wong GS, Rustgi AK (2013). Matricellular proteins: priming the tumour microenvironment for cancer development and metastasis. Br J Cancer. 108: 755-761.
70. Wood A (1988). Contact guidance on microfabricated substrata: the response of teleost fin mesenchyme cells to repeating topographical patterns. J Cell Sci. 90: 667-681.
71. Xie L, Law BK, Chytil AM, Brown KA, Aakre ME, Moses HL (2004). Activation of the Erk pathway is required for TGF-beta1-induced EMT in vitro. Neoplasia. 6: 603-610.
72. Yeung T, et al. (2005). Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton. 60: 24-34.
73. Yim EK, Darling EM, Kulangara K, Guilak F, Leong KW (2010). Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials. 31: 1299-1306.
74. Yoon SH, Kim YK, Han ED, Seo YH, Kim BH, Mofrad MR (2012). Passive control of cell locomotion using micropatterns: the effect of micropattern geometry on the migratory behavior of adherent cells. Lab Chip. 12: 2391-2402.
75. Zavadil J, et al. (2001). Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci U S A. 98: 6686-6691.
76. Zavadil J, Bottinger EP (2005). TGF-beta and epithelial-tomesenchymal transitions. Oncogene. 24: 5764-5774.
77. Zavadil J, Cermak L, Soto-Nieves N, Bottinger EP (2004). Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J. 23: 1155-1165.
78. Zeisberg EM, et al. (2007). Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med. 13: 952-961.
79. Zeisberg M, Neilson EG (2009). Biomarkers for epithelialmesenchymal transitions. J Clin Invest. 119: 1429-1437.