Cancer cell migration within 3D layer-by-layer microfabricated photocrosslinked PEG scaffolds with tunable stiffness

Biomaterials

Volumn 33, Issue 29, 2012, Pages 7064-7070

  Soman, Pranav ^a   Kelber, Jonathan A ^b   Lee, Jin Woo ^a   Wright, Tracy N ^b   Vecchio, Kenneth S ^a   Klemke, Richard L ^b   Chen, Shaochen ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell migration; Mechanical stiffness; Microstructure; Normal breast epithelial cells; Oncogene transformed cells; Scaffold

Indexed keywords

3-DIMENSIONAL; 3D MIGRATION; 3D SCAFFOLDS; CANCER CELLS; CELL MIGRATION; CELL MOTILITY; EPITHELIAL CELLS; FIBROUS SCAFFOLDS; INTERNAL ARCHITECTURE; LAYER-BY-LAYERS; MATRIX PARAMETERS; MECHANICAL STIFFNESS; MICROFABRICATED; MICROSTRUCTURAL INFLUENCES; STATISTICALLY SIGNIFICANT DIFFERENCE; VARYING STIFFNESS;

CELLS; CYTOLOGY; D REGION; MICROSTRUCTURE; PILES; POLYETHYLENE GLYCOLS; SCAFFOLDS; STIFFNESS; STIFFNESS MATRIX; SUBSTRATES; THREE DIMENSIONAL; TISSUE;

SCAFFOLDS (BIOLOGY);

ACRYLIC ACID; MACROGOL; TEMPOL; TISSUE SCAFFOLD;

ARTICLE; BREAST EPITHELIUM; CANCER CELL; CELL MIGRATION; CELL TRANSFORMATION; CONTROLLED STUDY; CROSS LINKING; HUMAN; HUMAN CELL; MICROTECHNOLOGY; PRIORITY JOURNAL; RIGIDITY;

BIOPHYSICS; BREAST; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CROSS-LINKING REAGENTS; ELASTICITY; EPITHELIAL CELLS; EQUIPMENT DESIGN; FEMALE; HUMANS; MICROSCOPY, ELECTRON, SCANNING; NEOPLASM METASTASIS; NEOPLASMS; POLYETHYLENE GLYCOLS; POLYMERS; STRESS, MECHANICAL; TISSUE SCAFFOLDS;

EID: 84864311480     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.06.012     Document Type: Article

References (43)

1. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., et al. Cell migration: Integrating signals from front to back. Science 2003, 302(5651):1704-1709.
2. Pollard T.D., Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003, 112(4):453-465.
3. Lauffenburger D.A., Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 1996, 84(3):359-369.
4. Hanahan D., Weinberg Robert A. Hallmarks of cancer: the next generation. Cell 2011, 144(5):646-674.
5. Sanz-Moreno V., Marshall C.J. The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr Opin Cell Biol 2010, 22(5):690-696.
6. Stoletov K., Kato H., Zardouzian E., Kelber J., Yang J., Shattil S., et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci 2010, 123(13):2332-2341.
7. Stoletov K., Montel V., Lester R.D., Gonias S.L., Klemke R. High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc Natl Acad Sci U S A 2007, 104(44):17406-17411.
8. Indra I., Beningo K.A. An in vitro correlation of metastatic capacity, substrate rigidity, and ECM composition. J Cell Biochem 2011, 112(11):3151-3158.
9. Ho M.-H., Kuo P.-Y., Hsieh H.-J., Hsien T.-Y., Hou L.-T., Lai J.-Y., et al. Preparation of porous scaffolds by using freeze-extraction and freeze-gelation methods. Biomaterials 2004, 25(1):129-138.
10. Ovsianikov A., Deiwick A., Van Vlierberghe S., Pflaum M., Wilhelmi M., Dubruel P., et al. Laser fabrication of 3D gelatin scaffolds for the generation of bioartificial tissues. Materials 2011, 4(1):288-299.
11. Baker E.L., Srivastava J., Yu D., Bonnecaze R.T., Zaman M.H. Cancer cell migration: Integrated roles of matrix mechanics and transforming potential. PLoS ONE 2011, 6(5):20355.
12. Zaman M.H., Trapani L.M., Sieminski A.L., MacKellar D., Gong H., Kamm R.D., et al. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc Natl Acad Sci U S A 2006, 103(29):10889-10894.
13. Willerth S.M., Arendas K.J., Gottlieb D.I., Sakiyama-Elbert S.E. Optimization of fibrin scaffolds for differentiation of murine embryonic stem cells into neural lineage cells. Biomaterials 2006, 27(36):5990-6003.
14. Raeber G.P., Lutolf M.P., Hubbell J.A. Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration. Biophys J 2005, 89(2):1374-1388.
15. Ma P.X., Choi J.-W. Biodegradable polymer scaffolds with well-defined interconnected spherical pore network. Tissue Eng 2001, 7(1):23-33.
16. Kuntz R.M., Saltzman W.M. Neutrophil motility in extracellular matrix gels: mesh size and adhesion affect speed of migration. Biophys J 1997, 72(3):1472-1480.
17. Choi Y., Kang T., Lee L.P. Plasmon resonance energy transfer (PRET)-based molecular imaging of cytochrome c in living cells. Nano Lett 2008, 9(1):85-90.
18. Storm C., Pastore J.J., MacKintosh F.C., Lubensky T.C., Janmey P.A. Nonlinear elasticity in biological gels. Nature 2005, 435(7039):191-194.
19. Chandran P.L.B.V. Affine versus non-affine fibril kinematics in collagen networks: theoretical studies of network behavior. J Biomech Eng 2006, 128(2):259-270.
20. Pedersen J., Swartz M. Mechanobiology in the third dimension. Ann Biomed Eng 2005, 33(11):1469-1490.
21. Kaufman L.J., Brangwynne C.P., Kasza K.E., Filippidi E., Gordon V.D., Deisboeck T.S., et al. Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. Biophys J 2005, 89(11):635-650.
22. Gelse K., Pöschl E., Aigner T. Collagens-structure, function, and biosynthesis. Adv Drug Deliv Rev 2003, 55(12):1531-1546.
23. Winer J.P., Oake S., Janmey P.A. Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS ONE 2009, 4(7):6382.
24. Pathak A, Kumar S. Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integr Biol;3(4):267-78.
25. Hayen W., Goebeler M., Kumar S., Riessen R., Nehls V. Hyaluronan stimulates tumor cell migration by modulating the fibrin fiber architecture. J Cell Sci 1999, 112(13):2241-2251.
26. Lannutti J., Reneker D., Ma T., Tomasko D., Farson D. Electrospinning for tissue engineering scaffolds. Mater Sci Eng C Mater Biol Appl 2007, 27(3):504-509.
27. Krause B., Diekmann K., van der Vegt N.F.A., Wessling M. Open nanoporous morphologies from polymeric blends by carbon dioxide foaming. Macromolecules 2002, 35(5):1738-1745.
28. da Silva J., Lautenschlager F., Sivaniah E., Guck J.R. The cavity-to-cavity migration of leukaemic cells through 3D honey-combed hydrogels with adjustable internal dimension and stiffness. Biomaterials 2009, 31(8):2201-2208.
29. Tayalia P., Mendonca C.R., Baldacchini T., Mooney D.J., Mazur E. 3D cell-migration studies using two-photon engineered polymer scaffolds. Adv Mater 2008, 20(23):4494-4498.
30. Yung-Shin S., Shih-Wei P., Keng-Hui L., Ji-Yen C. Electrotaxis of lung cancer cells in ordered three-dimensional scaffolds. Biomicrofluidics 2012, 6(1):014102.
31. Khademhosseini A., Langer R. Microengineered hydrogels for tissue engineering. Biomaterials 2007, 28(34):5087-5092.
32. Lee K.Y., Mooney D.J. Hydrogels for tissue engineering. Chem Rev 2001, 101(7):1869-1880.
33. Fozdar D.Y., Soman P., Lee J.W., Han L.-H., Chen S. Three-dimensional polymer constructs exhibiting a tunable negative Poisson's ratio. Adv Funct Mater 2011, 21(14):2712-2720.
34. Han L.-H., Mapili G., Chen S., Roy K. Projection microfabrication of three-dimensional scaffolds for tissue engineering. J Manuf Sci Eng 2008, 130(2):021005.
35. Han L.-H., Suri S., Schmidt C.E., Chen S. Fabrication of three-dimensional scaffolds for heterogeneous tissue engineering. Biomed Microdevices 2010, 12:721-725.
36. Lu Y., Mapili G., Suhali G., Chen S.C., Roy K. A digital micro-mirror device-based system for the microfabrication of complex, spatially patterned tissue engineering scaffolds. J Biomed Mater Res A 2006, 77(2):396-405.
37. Soman P., Lee J.W., Phadke A., Varghese S., Chen S. Spatial tuning of negative and positive Poisson's ratio in a multi-layer scaffold. Acta Biomater 2012, 8(7):2587-2594.
38. Soman P., Fozdar D.Y., Lee J.W., Phadke A., Varghese S., Chen S. A three-dimensional polymer scaffolding material exhibiting a zero Poisson's ratio. Soft Matter 2012, 8(18):4946-4951.
39. Mani S.A., Guo W., Liao M.-J., Eaton E.N., Ayyanan A., Zhou A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133(4):704-715.
40. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117(7):927-939.
41. Green C.E., Liu T., Montel V., Hsiao G., Lester R.D., Subramaniam S., et al. Chemoattractant signaling between tumor cells and macrophages regulates cancer cell migration, metastasis and neovascularization. PLoS ONE 2009, 4(8):6713.
42. Friedl P., Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003, 3(5):362-374.
43. Bell C., Waizbard E. Variability of cell size in primary and metastatic human breast carcinoma. Invasion Metastasis 1986, 6(1):11-20.