Engineering microscale topographies to control the cell-substrate interface

Biomaterials

Volumn 33, Issue 21, 2012, Pages 5230-5246

  Nikkhah, Mehdi ^a,b,d   Edalat, Faramarz ^a,b,d   Manoucheri, Sam ^a,b,d   Khademhosseini, Ali ^a,b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD UNIVERSITY   (United States)

^d NONE   (United States)

Author keywords

Adhesion; Mechanobiology; Microfabrication; Migration; Surface topography; Tissue engineering

Indexed keywords

ADHESION; BIOPHYSICS; CELL ADHESION; CELLS; MICROANALYSIS; MICROFABRICATION; STIFFNESS MATRIX; SURFACE TOPOGRAPHY; TISSUE; TISSUE ENGINEERING; TOPOGRAPHY;

EXTRACELLULAR MATRICES; MECHANICAL STIFFNESS; MECHANO-BIOLOGY; MECHANOTRANSDUCTION; MICRO-FABRICATION TECHNOLOGY; MICROSCALE TOPOGRAPHY; MIGRATION; TISSUE ENGINEERING APPLICATIONS;

CELL ENGINEERING;

ALKENE; DIMETICONE; HYDROXYAPATITE; POLY(METHYL METHACRYLATE); POLYCARBONATE; POLYLACTIC ACID; POLYSTYRENE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SILICON; SILICON DIOXIDE; TITANIUM;

CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL STRUCTURE; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; MEMBRANE STRUCTURE; MESENCHYMAL STEM CELL; MICROTECHNOLOGY; NEURAL STEM CELL; NONHUMAN; PHOTOLITHOGRAPHY; PRIORITY JOURNAL; PROCEDURES; REVIEW; SOFT LITHOGRAPHY; STEREOLITHOGRAPHY; TISSUE ENGINEERING; TWO PHOTON ABSORPTION LITHOGRAPHY;

EID: 84860917121     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2012.03.079     Document Type: Review

References (233)

1. Curtis A., Wilkinson C. Topographical control of cells. Biomaterials 1997, 18:1573-1583.
2. Guck J., Lautenschlager F., Paschke S., Beil M. Critical review: cellular mechanobiology and amoeboid migration. Integr Biol (Camb) 2010, 2:575-583.
3. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219.
4. Goodman S.L., Sims P.A., Albrecht R.M. Three-dimensional extracellular matrix textured biomaterials. Biomaterials 1996, 17:2087-2095.
5. Abrams G.A., Goodman S.L., Nealey P.F., Franco M., Murphy C.J. Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque. Cell Tissue Res 2000, 299:39-46.
6. Pamula E., De Cupere V., Dufrene Y.F., Rouxhet P.G. Nanoscale organization of adsorbed collagen: influence of substrate hydrophobicity and adsorption time. J Colloid Interface Sci 2004, 271:80-91.
7. Stevens M.M., George J.H. Exploring and engineering the cell surface interface. Science 2005, 310:1135-1138.
8. Wang L., Carrier R.L. Advances in biomimetics 2011, InTech, Rijeka. A. George (Ed.).
9. Takahashi-Iwanaga H., Iwanaga T., Isayama H. Porosity of the epithelial basement membrane as an indicator of macrophage-enterocyte interaction in the intestinal mucosa. Arch Histol Cytol 1999, 62:471-481.
10. Takeuchi T., Gonda T. Distribution of the pores of epithelial basement membrane in the rat small intestine. J Vet Med Sci 2004, 66:695-700.
11. Rorth P. Whence directionality: guidance mechanisms in solitary and collective cell migration. Dev Cell 2011, 20:9-18.
12. Dent E.W., Gertler F.B. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 2003, 40:209-227.
13. Wolf K., Muller R., Borgmann S., Brocker E.B., Friedl P. Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 2003, 102:3262-3269.
14. Haga H., Irahara C., Kobayashi R., Nakagaki T., Kawabata K. Collective movement of epithelial cells on a collagen gel substrate. Biophys J 2005, 88:2250-2256.
15. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol 2004, 16:14-23.
16. Campbell R.D., Marcum B.A. Nematocyte migation in hydra - evidence for contact guidance in vivo. J Cell Sci 1980, 41:33-51.
17. Eyckmans J., Boudou T., Yu X., Chen C. A hitchhiker's guide to mechanobiology. Dev Cell 2011, 21:35-47.
18. DuFort C.C., Paszek M.J., Weaver V.M. Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 2011, 12:308-319.
19. Fletcher D.A., Mullins R.D. Cell mechanics and the cytoskeleton. Nature 2010, 463:485-492.
20. Vogel V., Sheetz M. Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 2006, 7:265-275.
21. Petrie R.J., Doyle A.D., Yamada K.M. Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 2009, 10:538-549.
22. Huang J., Grater S.V., Corbellini F., Rinck S., Bock E., Kemkemer R., et al. Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett 2009, 9:1111-1116.
23. Park T.H., Shuler M.L. Integration of cell culture and microfabrication technology. Biotechnol Prog 2003, 19:243-253.
24. Moraes C., Sun Y., Simmons C.A. (Micro)managing the mechanical microenvironment. Integr Biol (Camb) 2011, 3:959-971.
25. Bettinger C.J., Langer R., Borenstein J.T. Engineering substrate topography at the micro- and nanoscale to control cell function. Angew Chem Int Ed Engl 2009, 48:5406-5415.
26. Kim D.H., Wong P.K., Park J., Levchenko A., Sun Y. Microengineered platforms for cell mechanobiology. Annu Rev Biomed Eng 2009, 11:203-233.
27. Hoffman-Kim D., Mitchel J.A., Bellamkonda R.V. Topography, cell response, and nerve regeneration. Ann Rev Biomed Eng 2010, 12:203-231.
28. le Digabel J., Ghibaudo M., Trichet L., Richert A., Ladoux B. Microfabricated substrates as a tool to study cell mechanotransduction. Med Biol Eng Comput 2010, 48:965-976.
29. Flemming R.G., Murphy C.J., Abrams G.A., Goodman S.L., Nealey P.F. Effects of synthetic micro- and nano-structured surfaces on cell behavior. Biomaterials 1999, 20:573-588.
30. Takebe J., Champagne C.M., Offenbacher S., Ishibashi K., Cooper L.F. Titanium surface topography alters cell shape and modulates bone morphogenetic protein 2 expression in the J774A.1 macrophage cell line. J Biomed Mater Res A 2003, 64A:207-216.
31. Kunzler T.P., Drobek T., Schuler M., Spencer N.D. Systematic study of osteoblast and fibroblast response to roughness by means of surface-morphology gradients. Biomaterials 2007, 28:2175-2182.
32. Tan K.S., Qian L., Rosado R., Flood P.M., Cooper L.F. The role of titanium surface topography on J774A.1 macrophage inflammatory cytokines and nitric oxide production. Biomaterials 2006, 27:5170-5177.
33. Lauer G., Wiedmann-Al-Ahmad M., Otten J.E., Hubner U., Schmelzeisen R., Schilli W. The titanium surface texture effects adherence and growth of human gingival keratinocytes and human maxillar osteoblast-like cells in vitro. Biomaterials 2001, 22:2799-2809.
34. Eisenbarth E., Meyle J., Nachtigall W., Breme J. Influence of the surface structure of titanium materials on the adhesion of fibroblasts. Biomaterials 1996, 17:1399-1403.
35. Au H.T., Cheng I., Chowdhury M.F., Radisic M. Interactive effects of surface topography and pulsatile electrical field stimulation on orientation and elongation of fibroblasts and cardiomyocytes. Biomaterials 2007, 28:4277-4293.
36. Anselme K., Bigerelle M., Noel B., Iost A., Hardouin P. Effect of grooved titanium substratum on human osteoblastic cell growth. J Biomed Mater Res 2002, 60:529-540.
37. Castellani R., de Ruijter A., Renggli H., Jansen J. Response of rat bone marrow cells to differently roughened titanium discs. Clin Oral Implan Res 1999, 10:369-378.
38. Khademhosseini A., Langer R., Borenstein J., Vacanti J.P. Microscale technologies for tissue engineering and biology. Proc Natl Acad Sci U S A 2006, 103:2480-2487.
39. Madou M.J. Fundamentals of microfabrication: the science of miniaturization 2002, CRC Press, Boca Raton.
40. Franssila S. Introduction to microfabrication 2004, Wiley Online Library, West Sussex.
41. Song W., Lu H., Kawazoe N., Chen G. Adipogenic differentiation of individual mesenchymal stem cell on different geometric micropatterns. Langmuir 2011, 27:6155-6162.
42. Bae H., Ahari A.F., Shin H., Nichol J.W., Hutson C.B., Masaeli M., et al. Cell-laden microengineered pullulan methacrylate hydrogels promote cell proliferation and 3D cluster formation. Soft Matter 2011, 7:1903-1911.
43. Qi H., Du Y., Wang L., Kaji H., Bae H., Khademhosseini A. Patterned differentiation of individual embryoid bodies in spatially organized 3D hybrid microgels. Adv Mater 2010, 22:5276-5281.
44. Rothschild M. Projection optical lithography. Mater Today 2005, 8:18-24.
45. Yang S.-P., Yang C.-Y., Lee T.-M., Lui T.-S. Effects of calcium-phosphate topography on osteoblast mechanobiology determined using a cytodetacher. Mater Sci Eng C 2012, 32:254-262.
46. Revzin A., Tompkins R.G., Toner M. Surface engineering with poly(ethylene glycol) photolithography to create high-density cell arrays on glass. Langmuir 2003, 19:9855-9862.
47. Kovacs G.T.A., Maluf N.I., Petersen K.E. Bulk micromachining of silicon. Proc IEEE 1998, 86:1536-1551.
48. Rangelow I.W. Critical tasks in high aspect ratio silicon dry etching for microelectromechanical systems. J Vac Sci Technol A 2003, 21:1550-1562.
49. Gantz K., Renaghan L., Agah M. Development of a comprehensive model for RIE-lag-based three-dimensional microchannel fabrication. J Micromech Microeng 2008, 18:025003.
50. Zellner P., Renaghan L., Hasnain Z., Agah M. A fabrication technology for three-dimensional micro total analysis systems. J Micromech Microeng 2010, 20:1-8.
51. Hahn M.S., Miller J.S., West J.L. Three dimensional biochemical and biomechanical patterning of hydrogels for guiding cell behavior. Adv Mater 2006, 18:2679-2684.
52. Mapili G., Lu Y., Chen S., Roy K. Laser-layered microfabrication of spatially patterned functionalized tissue-engineering scaffolds. J Biomed Mater Res B Appl Biomater 2005, 75:414-424.
53. Lan P.X., Lee J.W., Seol Y.-J., Cho D.-W. Development of 3D PPF/DEF scaffolds using micro-stereolithography and surface modification. J Mater Sci Mater Med 2009, 20:271-279.
54. Sun C., Fang N., Wu D.M., Zhang X. Projection micro-stereolithography using digital micro-mirror dynamic mask. Sens Actuators A Phys 2005, 121:113-120.
55. Lee K.-S., Kim R.H., Yang D.-Y., Park S.H. Advances in 3D nano/microfabrication using two-photon initiated polymerization. Prog Polym Sci 2008, 33:631-681.
56. Seidlits S.K., Schmidt C.E., Shear J.B. High-resolution patterning of hydrogels in three dimensions using direct-write photofabrication for cell guidance. Adv Funct Mater 2009, 19:3543-3551.
57. Weibel D.B., DiLuzio W.R., Whitesides G.M. Microfabrication meets microbiology. Nat Rev Micro 2007, 5:209-218.
58. Xia Y.N., Whitesides G.M. Soft lithography. Angew Chem Int Ed Engl 1998, 37:551-575.
59. Whitesides G.M., Ostuni E., Takayama S., Jiang X., Ingber D.E. Soft lithography in biology and biochemistry. Annu Rev Biomed Eng 2001, 3:335-373.
60. Zhong C., Kapetanovic A., Deng Y., Rolandi M. A chitin nanofiber ink for airbrushing, replica molding, and microcontact printing of self-assembled macro-, micro-, and nanostructures. Adv Mater 2011, 23:4776-4781.
61. Xia Y.N., McClelland J.J., Gupta R., Qin D., Zhao X.M., Sohn L.L., et al. Replica molding using polymeric materials: a practical step toward nanomanufacturing. Adv Mater 1997, 9:147-149.
62. Whitesides G.M. The origins and the future of microfluidics. Nature 2006, 442:368-373.
63. Perl A., Reinhoudt D.N., Huskens J. Microcontact printing: limitations and achievements. Adv Mater 2009, 21:2257-2268.
64. Schwarz U.S., Bischofs I.B. Physical determinants of cell organization in soft media. Med Eng Phys 2005, 27:763-772.
65. van der Flier A., Sonnenberg A. Function and interactions of integrins. Cell Tissue Res 2001, 305:285-298.
66. Tzima E., Irani-Tehrani M., Kiosses W.B., Dejana E., Schultz D.A., Engelhardt B., et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005, 437:426-431.
67. Hayakawa K., Tatsumi H., Sokabe M. Actin stress fibers transmit and focus force to activate mechanosensitive channels. J Cell Sci 2008, 121:496-503.
68. Giannone G., Sheetz M.P. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 2006, 16:213-223.
69. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005, 6:56-68.
70. Jaalouk D.E., Lammerding J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol 2009, 10:63-73.
71. Schwartz M.A., Ginsberg M.H. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol 2002, 4:E65-E68.
72. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
73. Riveline D., Zamir E., Balaban N.Q., Schwarz U.S., Ishizaki T., Narumiya S., et al. 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 2001, 153:1175-1185.
74. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
75. Ingber D.E. Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 1997, 59:575-599.
76. Rajnicek A., Britland S., McCaig C. Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. J Cell Sci 1997, 110:2905-2913.
77. Karuri N.W., Nealey P.F., Murphy C.J., Albrecht R.M. Structural organization of the cytoskeleton in SV40 human corneal epithelial cells cultured on nano- and microscale grooves. Microsc Microanal 2008, 30:405-413.
78. Oakley C., Brunette D.M. The sequence of alignment of microtubules, focal contacts and actin-filaments in fibroblasts spreading on smooth and grooved titanium substrata. J Cell Sci 1993, 106:343-354.
79. Oakley C., Jaeger N.A.F., Brunette D.M. Sensitivity of fibroblasts and their cytoskeletons to substratum topographies: topographic guidance and topographic compensation by micromachined grooves of different dimensions. Exp Cell Res 1997, 234:413-424.
80. Lu X., Leng Y. Quantitative analysis of osteoblast behavior on microgrooved hydroxyapatite and titanium substrata. J Biomed Mater Res A 2003, 66A:677-687.
81. Scheideler L., Geis-Gerstorfer J., Kern D., Pfeiffer F., Rupp F., Weber H., et al. Investigation of cell reactions to microstructured implant surfaces. Mater Sci Eng C Mater Biol Appl 2003, 23:455-459.
82. Lu X., Leng Y. Comparison of the osteoblast and myoblast behavior on hydroxyapatite microgrooves. J Biomed Mater Res B Appl Biomater 2009, 90B:438-445.
83. Clark P., Connolly P., Curtis A.S.G., Dow J.A.T., Wilkinson C.D.W. Topographical control of cell behavior: II. multiple grooved substrata. Development 1990, 108:635-644.
84. Walboomers X.F., Croes H.J.E., Ginsel L.A., Jansen J.A. Contact guidance of rat fibroblasts on various implant materials. J Biomed Mater Res 1999, 47:204-212.
85. Walboomers X.F., Monaghan W., Curtis A.S.G., Jansen J.A. Attachment of fibroblasts on smooth and microgrooved polystyrene. J Biomed Mater Res 1999, 46:212-220.
86. Li J.M., McNally H., Shi R. Enhanced neurite alignment on micro-patterned poly-L-lactic acid films. J Biomed Mater Res A 2008, 87A:392-404.
87. Charest J.L., Garcia A.J., King W.P. Myoblast alignment and differentiation on cell culture substrates with microscale topography and model chemistries. Biomaterials 2007, 28:2202-2210.
88. Bettinger C.J., Orrick B., Misra A., Langer R., Borenstein J.T. Micro fabrication of poly (glycerol-sebacate) for contact guidance applications. Biomaterials 2006, 27:2558-2565.
89. Franco D., Klingauf M., Bednarzik M., Cecchini M., Kurtcuoglu V., Gobrecht J., et al. Control of initial endothelial spreading by topographic activation of focal adhesion kinase. Soft Matter 2011, 7:7313-7324.
90. Uttayarat P., Toworfe G.K., Dietrich F., Lelkes P.I., Composto R.J. Topographic guidance of endothelial cells on silicone surfaces with micro- to nanogrooves: orientation of actin filaments and focal adhesions. J Biomed Mater Res A 2005, 75A:668-680.
91. Biela S.A., Su Y., Spatz J.P., Kemkemer R. Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater 2009, 5:2460-2466.
92. den Braber E.T., de Ruijter J.E., Smits H.T.J., Ginsel L.A., von Recum A.F., Jansen J.A. Quantitative analysis of cell proliferation and orientation on substrata with uniform parallel surface micro-grooves. Biomaterials 1996, 17:1093-1099.
93. den Braber E.T., de Ruijter J.E., Ginsel L.A., von Recum A.F., Jansen J.A. Orientation of ECM protein deposition, fibroblast cytoskeleton, and attachment complex components on silicone microgrooved surfaces. J Biomed Mater Res 1998, 40:291-300.
94. Teixeira A.I., Abrams G.A., Bertics P.J., Murphy C.J., Nealey P.F. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci 2003, 116:1881-1892.
95. Turner A.M.P., Dowell N., Turner S.W.P., Kam L., Isaacson M., Turner J.N., et al. Attachment of astroglial cells to microfabricated pillar arrays of different geometries. J Biomed Mater Res 2000, 51:430-441.
96. Frey M.T., Tsai I.Y., Russell T.P., Hanks S.K., Wang Y.L. Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. Biophys J 2006, 90:3774-3782.
97. Ghibaudo M., Trichet L., Le Digabel J., Richert A., Hersen P., Ladoux B. Substrate topography induces a crossover from 2D to 3D behavior in fibroblast migration. Biophys J 2009, 97:357-368.
98. Kidambi S., Udpa N., Schroeder S.A., Findlan R., Lee I., Chan C. Cell adhesion on polyelectrolyte multilayer coated polydimethylsiloxane surfaces with varying topographies. Tissue Eng 2007, 13:2105-2117.
99. Kolind K., Dolatshahi-Pirouz A., Lovmand J., Pedersen F.S., Foss M., Besenbacher F. A combinatorial screening of human fibroblast responses on micro-structured surfaces. Biomaterials 2010, 31:9182-9191.
100. Wang L., Murthy S.K., Fowle W.H., Barabino G.A., Carrier R.L. Influence of micro-well biomimetic topography on intestinal epithelial Caco-2 cell phenotype. Biomaterials 2009, 30:6825-6834.
101. Wan Y.Q., Wang Y., Liu Z.M., Qu X., Han B.X., Bei J.Z., et al. Adhesion and proliferation of OCT-1 osteoblast-like cells on micro- and nano-scale topography structured pply(L-lactide). Biomaterials 2005, 26:4453-4459.
102. Hamilton D.W., Chehroudi B., Brunette D.M. Comparative response of epithelial cells and osteoblasts to microfabricated tapered pit topographies in vitro and in vivo. Biomaterials 2007, 28:2281-2293.
103. Le Saux G., Magenau A., Boecking T., Gaus K., Gooding J.J. The relative importance of topography and RGD ligand density for endothelial cell adhesion. Plos One 2011, 6:e21869.
104. Nikkhah M., Strobl J.S., Agah M. Attachment and response of human fibroblast and breast cancer cells to three dimensional silicon microstructures of different geometries. Biomed Microdevices 2009, 11:429-441.
105. Nikkhah M., Strobl J.S., Peddi B., Agah M. Cytoskeletal role in differential adhesion patterns of normal fibroblasts and breast cancer cells inside silicon microenvironments. Biomed Microdevices 2009, 11:585-595.
106. Nikkhah M., Strobl J.S., De Vita R., Agah M. The cytoskeletal organization of breast carcinoma and fibroblast cells inside three dimensional (3-D) isotropic silicon microstructures. Biomaterials 2010, 31:4552-4561.
107. Strobl J.S., Nikkhah M., Agah M. Actions of the anti-cancer drug suberoylanilide hydroxamic acid (SAHA) on human breast cancer cytoarchitecture in silicon microstructures. Biomaterials 2010, 31:7043-7050.
108. Nikkhah M., Strobl J.S., Schmelz E.M., Roberts P.C., Zhou H., Agah M. MCF10A and MDA-MB-231 human breast basal epithelial cell co-culture in silicon micro-arrays. Biomaterials 2011, 32:7625-7632.
109. Van Haastert P.J.M., Devreotes P.N. Chemotaxis: signalling the way forward. Nat Rev Mol Cell Biol 2004, 5:626-634.
110. 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, 302:1704-1709.
111. Sidani M., Wyckoff J., Xue C., Segall J., Condeelis J. Probing the microenvironment of mammary tumors using multiphoton microscopy. J Mammary Gland Biol Neoplasia 2006, 11:151-163.
112. Provenzano P.P., Inman D.R., Eliceiri K.W., Knittel J.G., Yan L., Rueden C.T., et al. Collagen density promotes mammary tumor initiation and progression. BMC Med 2008, 6:11.
113. Provenzano P.P., Inman D.R., Eliceiri K.W., Trier S.M., Keely P.J. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 2008, 95:5374-5384.
114. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005, 21:247-269.
115. Hotulainen P., Lappalainen P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 2006, 173:383-394.
116. Huang S., Brangwynne C.P., Parker K.K., Ingber D.E. Symmetry-breaking in mammalian cell cohort migration during tissue pattern formation: role of random-walk persistence. Cell Motil Cytoskel 2005, 61:201-213.
117. Helle T., Deiss S., Schwarz U., Schlosshauer B. Glial and neuronal regulation of the lipid carrier R-FABP. Exp Cell Res 2003, 287:88-97.
118. Maheshwari G., Wells A., Griffith L.G., Lauffenburger D.A. Biophysical integration of effects of epidermal growth factor and fibronectin on fibroblast migration. Biophys J 1999, 76:2814-2823.
119. Bashyam M.D. Understanding cancer metastasis. Cancer 2002, 94:1821-1829.
120. Wells A. Tumor invasion: role of growth factor-induced cell motility. Adv Cancer Res 2000, 78:31-101.
121. Tzvetkova-Chevolleau T., Stephanou A., Fuard D., Ohayon J., Schiavone P., Tracqui P. The motility of normal and cancer cells in response to the combined influence of the substrate rigidity and anisotropic microstructure. Biomaterials 2008, 29:1541-1551.
122. Kaiser J.P., Bruinink A. Investigating cell-material interactions by monitoring and analysing cell migration. J Mater Sci Mater Med 2004, 15:429-435.
123. Kaiser J.-P., Reinmann A., Bruinink A. The effect of topographic characteristics on cell migration velocity. Biomaterials 2006, 27:5230-5241.
124. Kim D.-H., Han K., Gupta K., Kwon K.W., Suh K.-Y., Levchenko A. Mechanosensitivity of fibroblast cell shape and movement to anisotropic substratum topography gradients. Biomaterials 2009, 30:5433-5444.
125. Thampatty B.P., Wang J.H.C. A new approach to study fibroblast migration. Cell Motil Cytoskel 2007, 64:1-5.
126. Webb A., Clark P., Skepper J., Compston A., Wood A. Guidance of oligodendrocytes and their progenitors by substratum topography. J Cell Sci 1995, 108:2747-2760.
127. Gomez N., Chen S., Schmidt C.E. Polarization of hippocampal neurons with competitive surface stimuli: contact guidance cues are preferred over chemical ligands. J R Soc Interface 2007, 4:223-233.
128. Dalton B.A., Walboomers X.F., Dziegielewski M., Evans M.D.M., Taylor S., Jansen J.A., et al. Modulation of epithelial tissue and cell migration by microgrooves. J Biomed Mater Res 2001, 56:195-207.
129. Li S., Bhatia S., Hu Y.L., Shin Y.T., Li Y.S., Usami S., et al. Effects of morphological patterning on endothelial cell migration. Biorheology 2001, 38:101-108.
130. Doyle A.D., Wang F.W., Matsumoto K., Yamada K.M. One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol 2009, 184:481-490.
131. Mai J.Y., Sun C., Li S., Zhang X. A microfabricated platform probing cytoskeleton dynamics using multidirectional topographical cues. Biomed Microdevices 2007, 9:523-531.
132. Jeon H., Hidai H., Hwang D.J., Healy K.E., Grigoropoulos C.P. The effect of micronscale anisotropic cross patterns on fibroblast migration. Biomaterials 2010, 31:4286-4295.
133. Kim D.-H., Seo C.-H., Han K., Kwon K.W., Levchenko A., Suh K.-Y. Guided cell migration on microtextured substrates with variable local density and anisotropy. Adv Funct Mater 2009, 19:1579-1586.
134. Isenberg B.C., Tsuda Y., Williams C., Shimizu T., Yamato M., Okano T., et al. A thermoresponsive, microtextured substrate for cell sheet engineering with defined structural organization. Biomaterials 2008, 29:2565-2572.
135. Miyoshi H., Ju J., Lee S.M., Cho D.J., Ko J.S., Yamagata Y., et al. Control of highly migratory cells by microstructured surface based on transient change in cell behavior. Biomaterials 2010, 31:8539-8545.
136. Miyoshi H., Adachi T., Ju J., Lee S.M., Cho D.J., Ko J.S., et al. Characteristics of motility-based filtering of adherent cells on microgrooved surfaces. Biomaterials 2012, 33:395-401.
137. Saez A., Ghibaudo M., Buguin A., Silberzan P., Ladoux B. Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc Natl Acad Sci U S A 2007, 104:8281-8286.
138. Sochol R.D., Higa A.T., Janairo R.R.R., Li S., Lin L. Unidirectional mechanical cellular stimuli via micropost array gradients. Soft Matter 2011, 7:4606-4609.
139. Lo C.-M., Wang H.-B., Dembo M., Wang Y.-l. Cell movement is guided by the rigidity of the substrate. Biophys J 2000, 79:144-152.
140. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
141. Béduer A., Vieu C., Arnauduc F., Sol J.-C., Loubinoux I., Vaysse L. Engineering of adult human neural stem cells differentiation through surface micropatterning. Biomaterials 2012, 33:504-514.
142. Buxboim A., Discher D.E. Stem cells feel the difference. Nat Methods 2010, 7:695-697.
143. Zemel A., Rehfeldt F., Brown A.E., Discher D.E., Safran S.A. Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 2010, 6:468-473.
144. Discher D.E., Mooney D.J., Zandstra P.W. Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324:1673-1677.
145. Peerani R., Zandstra P.W. Enabling stem cell therapies through synthetic stem cell-niche engineering. J Clin Invest 2010, 120:60-70.
146. Dellatore S.M., Garcia A.S., Miller W.M. Mimicking stem cell niches to increase stem cell expansion. Curr Opin Biotechnol 2008, 19:534-540.
147. Edalat F., Bae H., Manoucheri S., Cha J.M., Khademhosseini A. Engineering approaches toward deconstructing and controlling the stem cell environment. Ann Biomed Eng 2011, 10.1007/s10439-011-0452-9.
148. Chai C., Leong K.W. Biomaterials approach to expand and direct differentiation of stem cells. Mol Ther 2007, 15:467-480.
149. Tsuruma A., Tanaka M., Yamamoto S., Shimomura M. Control of neural stem cell differentiation on honeycomb films. Colloids Surf A Physicochem Eng Asp 2008, 313-314:536-540.
150. Myllymaa S., Kaivosoja E., Myllymaa K., Sillat T., Korhonen H., Lappalainen R., et al. Adhesion, spreading and osteogenic differentiation of mesenchymal stem cells cultured on micropatterned amorphous diamond, titanium, tantalum and chromium coatings on silicon. J Mater Sci Mater Med 2010, 21:329-341.
151. Fu J., Wang Y.K., Yang M.T., Desai R.A., Yu X., Liu Z., et al. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 2010, 7:733-736.
152. Lim J.Y., Donahue H.J. Cell sensing and response to micro- and nanostructured surfaces produced by chemical and topographic patterning. Tissue Eng 2007, 13:1879-1891.
153. Dickinson L.E., Kusuma S., Gerecht S. Reconstructing the differentiation niche of embryonic stem cells using biomaterials. Macromol Biosci 2011, 11:36-49.
154. Moeller H.C., Mian M.K., Shrivastava S., Chung B.G., Khademhosseini A. A microwell array system for stem cell culture. Biomaterials 2008, 29:752-763.
155. Markert L.D., Lovmand J., Foss M., Lauridsen R.H., Lovmand M., Fuchtbauer E.M., et al. Identification of distinct topographical surface microstructures favoring either undifferentiated expansion or differentiation of murine embryonic stem cells. Stem Cells Dev 2009, 18:1331-1342.
156. Yang M.T., Fu J., Wang Y.K., Desai R.A., Chen C.S. Assaying stem cell mechanobiology on microfabricated elastomeric substrates with geometrically modulated rigidity. Nat Protoc 2011, 6:187-213.
157. Guvendiren M., Burdick J.A. The control of stem cell morphology and differentiation by hydrogel surface wrinkles. Biomaterials 2010, 31:6511-6518.
158. Seo C.H., Furukawa K., Suzuki Y., Kasagi N., Ichiki T., Ushida T. A topographically optimized substrate with well-ordered lattice micropatterns for enhancing the osteogenic differentiation of murine mesenchymal stem cells. Macromol Biosci 2011, 11:938-945.
159. Seo C.H., Furukawa K., Montagne K., Jeong H., Ushida T. The effect of substrate microtopography on focal adhesion maturation and actin organization via the RhoA/ROCK pathway. Biomaterials 2011, 32:9568-9575.
160. Wang G., Ao Q., Gong K., Wang A., Zheng L., Gong Y., et al. The effect of topology of chitosan biomaterials on the differentiation and proliferation of neural stem cells. Acta Biomater 2010, 6:3630-3639.
161. Kim S.J., Lee J.K., Kim J.W., Jung J.W., Seo K., Park S.B., et al. Surface modification of polydimethylsiloxane (PDMS) induced proliferation and neural-like cells differentiation of umbilical cord blood-derived mesenchymal stem cells. J Mater Sci Mater Med 2008, 19:2953-2962.
162. Hwang Y.S., Chung B.G., Ortmann D., Hattori N., Moeller H.C., Khademhosseini A. Microwell-mediated control of embryoid body size regulates embryonic stem cell fate via differential expression of WNT5a and WNT11. Proc Natl Acad Sci U S A 2009, 106:16978-16983.
163. Karp J.M., Yeh J., Eng G., Fukuda J., Blumling J., Suh K.Y., et al. Controlling size, shape and homogeneity of embryoid bodies using poly(ethylene glycol) microwells. Lab Chip 2007, 7:786-794.
164. Khademhosseini A., Ferreira L., Blumling, Yeh J., Karp J.M., Fukuda J., et al. Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates. Biomaterials 2006, 27:5968-5977.
165. Selimovic S., Piraino F., Bae H., Rasponi M., Redaelli A., Khademhosseini A. Microfabricated polyester conical microwells for cell culture applications. Lab Chip 2011, 11:2325-2332.
166. Tekin H., Anaya M., Brigham M.D., Nauman C., Langer R., Khademhosseini A. Stimuli-responsive microwells for formation and retrieval of cell aggregates. Lab Chip 2010, 10:2411-2418.
167. Purpura K.A., Bratt-Leal A.M., Hammersmith K.A., McDevitt T.C., Zandstra P.W. Systematic engineering of 3D pluripotent stem cell niches to guide blood development. Biomaterials 2012, 33:1271-1280.
168. Wolff Y. Das gesetz der transformation der knochen 1892, Verlag von August Hirschwald, Berlin.
169. Yashiro K., Shiratori H., Hamada H. Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 2007, 450:285-288.
170. Hahn C., Schwartz M.A. Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 2009, 10:53-62.
171. Jacobs C.R., Temiyasathit S., Castillo A.B. Osteocyte mechanobiology and pericellular mechanics. Annu Rev Biomed Eng 2010, 12:369-400.
172. Chandrasekharan K., Martin P.T. Genetic defects in muscular dystrophy. Methods Enzymol 2010, 291-322.
173. Yu H., Mouw J.K., Weaver V.M. Forcing form and function: biomechanical regulation of tumor evolution. Trends Cell Biol 2011, 21:47-56.
174. Nelson C.M., Jean R.P., Tan J.L., Liu W.F., Sniadecki N.J., Spector A.A., et al. Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci U S A 2005, 102:11594-11599.
175. Kilian K.A., Bugarija B., Lahn B.T., Mrksich M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A 2010, 107:4872-4877.
176. Gilbert P.M., Havenstrite K.L., Magnusson K.E.G., Sacco A., Leonardi N.A., Kraft P., et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 2010, 329:1078-1081.
177. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci U S A 2003, 100:1484-1489.
178. Crandall S.H. An introduction to the mechanics of solids 1978, McGraw-Hill, New York.
179. Balaban N.Q., Schwarz U.S., Riveline D., Goichberg P., Tzur G., Sabanay I., et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 2001, 3:466-472.
180. Ghibaudo M., Di Meglio J.-M., Hersen P., Ladoux B. Mechanics of cell spreading within 3D-micropatterned environments. Lab Chip 2011, 11:805-812.
181. Mège R.-M., Gavard J., Lambert M. Regulation of cell-cell junctions by the cytoskeleton. Curr Opin Cell Biol 2006, 18:541-548.
182. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457:495-499.
183. Dawes-Hoang R.E., Parmar K.M., Christiansen A.E., Phelps C.B., Brand A.H., Wieschaus E.F. Folded gastrulation, cell shape change and the control of myosin localization. Development 2005, 132:4165-4178.
184. Ganz A., Lambert M., Saez A., Silberzan P., Buguin A., Mège R.-M., et al. Traction forces exerted through N-cadherin contacts. Biol Cell 2006, 98:721-730.
185. Liu Z., Tan J.L., Cohen D.M., Yang M.T., Sniadecki N.J., Ruiz S.A., et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A 2010, 107:9944-9949.
186. Sniadecki N.J., Lamb C.M., Liu Y., Chen C.S., Reich D.H. Magnetic microposts for mechanical stimulation of biological cells: fabrication, characterization, and analysis. Rev Sci Instrum 2008, 79:44302-44308.
187. le Digabel J., Biais N., Fresnais J., Berret J.-F., Hersen P., Ladoux B. Magnetic micropillars as a tool to govern substrate deformations. Lab Chip 2011, 11:2630-2636.
188. Sniadecki N.J., Anguelouch A., Yang M.T., Lamb C.M., Liu Z., Kirschner S.B., et al. Magnetic microposts as an approach to apply forces to living cells. Proc Natl Acad Sci U S A 2007, 104:14553-14558.
189. Liang X.M., Han S.J., Reems J.-A., Gao D., Sniadecki N.J. Platelet retraction force measurements using flexible post force sensors. Lab Chip 2010, 10:991-998.
190. Liu Z., Sniadecki N., Chen C. Mechanical forces in endothelial cells during firm adhesion and early transmigration of human monocytes. Cell Mol Bioeng 2010, 3:50-59.
191. Saez A., Anon E., Ghibaudo M., du Roure O., Di Meglio J.-M., Hersen P., et al. Traction forces exerted by epithelial cell sheets. J Phys Condens Matter 2010, 22:194119.
192. Nadarajah B., Alifragis P., Wong R.O.L., Parnavelas J.G. Ventricle-directed migration in the developing cerebral cortex. Nat Neurosci 2002, 5:218-224.
193. Malatesta P., Appolloni I., Calzolari F. Radial glia and neural stem cells. Cell Tissue Res 2008, 331:165-178.
194. Gumera C., Rauck B., Wang Y. Materials for central nervous system regeneration: bioactive cues. J Mater Chem 2011, 21:7033-7051.
195. Yao L., Wang S., Cui W., Sherlock R., O'Connell C., Damodaran G., et al. Effect of functionalized micropatterned PLGA on guided neurite growth. Acta Biomater 2009, 5:580-588.
196. Miller C., Jeftinija S., Mallapragada S. Synergistic effects of physical and chemical guidance cues on neurite alignment and outgrowth on biodegradable polymer substrates. Tissue Eng 2002, 8:367-378.
197. Li N., Folch A. Integration of topographical and biochemical cues by axons during growth on microfabricated 3-D substrates. Exp Cell Res 2005, 311:307-316.
198. Mahoney M.J., Chen R.R., Tan J., Mark Saltzman W. The influence of microchannels on neurite growth and architecture. Biomaterials 2005, 26:771-778.
199. Gomez N., Lu Y., Chen S., Schmidt C.E. Immobilized nerve growth factor and microtopography have distinct effects on polarization versus axon elongation in hippocampal cells in culture. Biomaterials 2007, 28:271-284.
200. Kang E., Jeong G.S., Choi Y.Y., Lee K.H., Khademhosseini A., Lee S.-H. Digitally tunable physicochemical coding of material composition and topography in continuous microfibres. Nat Mater 2011, 10:877-883.
201. Houchin-Ray T., Swift L.A., Jang J.-H., Shea L.D. Patterned PLG substrates for localized DNA delivery and directed neurite extension. Biomaterials 2007, 28:2603-2611.
202. Recknor J.B., Sakaguchi D.S., Mallapragada S.K. Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials 2006, 27:4098-4108.
203. Lietz M., Dreesmann L., Hoss M., Oberhoffner S., Schlosshauer B. Neuro tissue engineering of glial nerve guides and the impact of different cell types. Biomaterials 2006, 27:1425-1436.
204. Wang M., Zhai P., Chen X., Schreyer D.J., Sun X., Cui F. Bioengineered scaffolds for spinal cord repair. Tissue Eng Part B Rev 2011, 17:177-194.
205. Orive G., Anitua E., Pedraz J.L., Emerich D.F. Biomaterials for promoting brain protection, repair and regeneration. Nat Rev Neurosci 2009, 10:682-692.
206. Thuret S., Moon L.D.F., Gage F.H. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006, 7:628-643.
207. Wong D.Y., Leveque J.-C., Brumblay H., Krebsbach P.H., Hollister S.J., LaMarca F. Macro-architectures in spinal cord scaffold implants influence regeneration. J Neurotrauma 2008, 25:1027-1037.
208. He L., Zhang Y., Zeng C., Ngiam M., Liao S., Quan D., et al. Manufacture of PLGA multiple-channel conduits with precise hierarchical pore architectures and in vitro/vivo evaluation for spinal cord injury. Tissue Eng Part C Methods 2009, 15:243-255.
209. Krych A.J., Rooney G.E., Chen B., Schermerhorn T.C., Ameenuddin S., Gross L., et al. Relationship between scaffold channel diameter and number of regenerating axons in the transected rat spinal cord. Acta Biomater 2009, 5:2551-2559.
210. Rutkowski G.E., Miller C.A., Jeftinija S., Mallapragada S.K. Synergistic effects of micropatterned biodegradable conduits and Schwann cells on sciatic nerve regeneration. J Neural Eng 2004, 1:151-157.
211. Feinberg A.W., Feigel A., Shevkoplyas S.S., Sheehy S., Whitesides G.M., Parker K.K. Muscular thin films for building actuators and powering devices. Science 2007, 317:1366-1370.
212. Bursac N., Parker K.K., Iravanian S., Tung L. Cardiomyocyte cultures with controlled macroscopic anisotropy: a model for functional electrophysiological studies of cardiac muscle. Circ Res 2002, 91:e45-e54.
213. Kajzar A., Cesa C.M., Kirchgessner N., Hoffmann B., Merkel R. Toward physiological conditions for cell analyses: forces of heart muscle cells suspended between elastic micropillars. Biophys J 2008, 94:1854-1866.
214. Zhang T., Wan L.Q., Xiong Z., Marsano A., Maidhof R., Park M., et al. Channelled scaffolds for engineering myocardium with mechanical stimulation. J Tissue Eng Regen Med 2011, 10.1002/term.481.
215. Heidi Au H.T., Cui B., Chu Z.E., Veres T., Radisic M. Cell culture chips for simultaneous application of topographical and electrical cues enhance phenotype of cardiomyocytes. Lab Chip 2009, 9:564-575.
216. Yin L., Bien H., Entcheva E. Scaffold topography alters intracellular calcium dynamics in cultured cardiomyocyte networks. Am J Physiol Heart Circ Physiol 2004, 287:H1276-H1285.
217. Kim J., Park J., Na K., Yang S., Baek J., Yoon E., et al. Quantitative evaluation of cardiomyocyte contractility in a 3D microenvironment. J Biomech 2008, 41:2396-2401.
218. Patel A.A., Desai T.A., Kumar S. Microtopographical assembly of cardiomyocytes. Integr Biol (Camb) 2011, 3:1011-1019.
219. Engelmayr G.C., Cheng M., Bettinger C.J., Borenstein J.T., Langer R., Freed L.E. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 2008, 7:1003-1010.
220. Kneser U., Schaefer D.J., Polykandriotis E., Horch R.E. Tissue engineering of bone: the reconstructive surgeon's point of view. J Cell Mol Med 2006, 10:7-19.
221. Freed L.E., Engelmayr G.C., Borenstein J.T., Moutos F.T., Guilak F. Advanced material strategies for tissue engineering scaffolds. Adv Mater 2009, 21:3410-3418.
222. Kenar H., Kocabas A., Aydinli A., Hasirci V. Chemical and topographical modification of PHBV surface to promote osteoblast alignment and confinement. J Biomed Mater Res A 2008, 85:1001-1010.
223. Holthaus M.G., Stolle J., Treccani L., Rezwan K. Orientation of human osteoblasts on hydroxyapatite-based microchannels. Acta Biomater 2012, 8:394-403.
224. Kirmizidis G., Birch M.A. Microfabricated grooved substrates influence cell-cell communication and osteoblast differentiation in vitro. Tissue Eng Part A 2009, 15:1427-1436.
225. Kim I.L., Mauck R.L., Burdick J.A. Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 2011, 32:8771-8782.
226. Hutmacher D.W. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000, 21:2529-2543.
227. Hamilton D.W., Riehle M.O., Monaghan W., Curtis A.S. Chondrocyte aggregation on micrometric surface topography: a time-lapse study. Tissue Eng 2006, 12:189-199.
228. Moutos F.T., Freed L.E., Guilak F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 2007, 6:162-167.
229. Narang D., Sood S., Thomas M.K., Dinda A.K., Maulik S.K. Effect of dietary palm olein oil on oxidative stress associated with ischemic-reperfusion injury in isolated rat heart. BMC Pharmacol 2004, 4:29.
230. Hakem R., de la Pompa J.L., Sirard C., Mo R., Woo M., Hakem A., et al. The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 1996, 85:1009-1023.
231. Choi Y.Y., Chung B.G., Lee D.H., Khademhosseini A., Kim J.H., Lee S.H. Controlled-size embryoid body formation in concave microwell arrays. Biomaterials 2010, 31:4296-4303.
232. Marty R., Fuentes C. Aspects tridimensionnels du cortex cérébral: étude par la méthode de Golgi-Cox souséclairage incident. Brain Res 1968, 11:124-133.
233. Gros T., Sakamoto J.S., Blesch A., Havton L.A., Tuszynski M.H. Regeneration of long-tract axons through sites of spinal cord injury using templated agarose scaffolds. Biomaterials 2010, 31:6719-6729.