Mesenchymal stem cell fate: Applying biomaterials for control of stem cell behavior

Frontiers in Bioengineering and Biotechnology

Volumn 4, Issue MAY, 2016, Pages

  Anderson, Hilary J ^a   Sahoo, Jugal Kishore ^b   Ulijn, Rein V ^b,c   Dalby, Matthew J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Bioengineering; Materials synthesis; Mesenchymal stem cells; Nanotopography; Stimuli responsive material

Indexed keywords

BIOMATERIALS; CELL CULTURE; SYSTEMS SCIENCE; TISSUE; TISSUE ENGINEERING;

CONTINUOUS DEVELOPMENT; IN-VITRO; KEY OBJECTIVE; MATERIALS SYNTHESIS; MESENCHYMAL STEM CELL; NANOTOPOGRAPHIES; STIMULI-RESPONSIVE MATERIALS; TISSUE ENGINEERING APPLICATIONS;

STEM CELLS;

EID: 85001780972     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2016.00038     Document Type: Review

References (131)

1. Affrossman, S., Jerome, R., O'Neill, S. A., Schmitt, T., and Stamm, M. (2000). Surface structure of thin film blends of polystyrene and poly(n-butyl methacrylate). Colloid Polym. Sci. 278, 993-999. doi:10.1007/s003960000358
2. Albelda, S. M., and Buck, C. A. (1990). Integrins and other cell adhesion molecules. FASEB J. 4, 2868-2880.
3. Anderson, H. J. (2015). An Interview with Adam Curtis | Centre for Cell Engineering Glasgow. Available at: http://www.cceuog.co.uk/#!An-Interview-with-Adam-Curtis/cmbz/5617e0ec0cf2c3576e558247
4. Arnold, M., Hirschfeld-Warneken, V. C., Lohmüller, T., Heil, P., Blümmel, J., Cavalcanti-Adam, E. A., et al. (2008). Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. Nano Lett. 8, 2063-2069. doi:10.1021/nl801483w
5. Atala, A., Bauer, S. B., Soker, S., Yoo, J. J., and Retik, A. B. (2006). Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367, 1241-1246. doi:10.1016/S0140-6736(06)68438-9
6. Balaban, N. Q., Schwarz, U. S., Riveline, D., Goichberg, P., Tzur, G., Sabanay, I., et al. (2001). Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3, 466-472. doi:10.1038/35074532
7. Benoit, D. S. W., Schwartz, M. P., Durney, A. R., and Anseth, K. S. (2008). Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat. Mater. 7, 816-823. doi:10.1038/nmat2269
8. Bershadsky, A. D., Tint, I. S., Neyfakh, A. A., and Vasiliev, J. M. (1985). Focal contacts of normal and RSV-transformed quail cells. Hypothesis of the transformation-induced deficient maturation of focal contacts. Exp. Cell Res. 158, 433-444. doi:10.1016/0014-4827(85)90467-7
9. Biggs, M. J., Richards, R. G., Gadegaard, N., Wilkinson, C. D., Oreffo, R. O., and Dalby, M. J. (2009). The use of nanoscale topography to modulate the dynamics of adhesion formation in primary osteoblasts and ERK/MAPK signalling in STRO-1+ enriched skeletal stem cells. Biomaterials 30, 5094-5103. doi:10.1016/j.biomaterials.2009.05.049
10. Biggs, M. J., Richards, R. G., McFarlane, S., Wilkinson, C. D., Oreffo, R. O., and Dalby, M. J. (2008). Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330nm deep microgrooves. J. R. Soc. Interface 5, 1231-1242. doi:10.1098/rsif.2008.0035
11. Buensuceso, C. S., Woodside, D., Huff, J. L., Plopper, G. E., and O'Toole, T. E. (2001). The WD protein Rack1 mediates protein kinase C and integrin-dependent cell migration. J. Cell Sci. 114, 1691-1698.
12. Burridge, K., and Chrzanowska-Wodnicka, M. (1996). Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518. doi:10.1146/annurev.cellbio.12.1.463
13. Cavalcanti-Adam, E. A., Aydin, D., Hirschfeld-Warneken, V. C., and Spatz, J. P. (2008). Cell adhesion and response to synthetic nanopatterned environments by steering receptor clustering and spatial location. HFSP J. 2, 276-285. doi:10.2976/1.2976662
14. Cavalcanti-Adam, E. A., Volberg, T., Micoulet, A., Kessler, H., Geiger, B., and Spatz, J. P. (2007). Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 92, 2964-2974. doi:10.1529/biophysj.106.089730
15. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M., and Ingber, D. E. (1997). Geometric control of cell life and death. Science 276, 1425-1428. doi:10.1126/science.276.5317.1425
16. Chen, W., Villa-Diaz, L. G., Sun, Y., Weng, S., Kim, J. K., Lam, R. H., et al. (2012). Nanotopography influences adhesion, spreading, and self-renewal of human embryonic stem cells. ACS Nano 6, 4094-4103. doi:10.1021/nn3004923
17. Clark, P., Connolly, P., Curtis, A. S., Dow, J. A., and Wilkinson, C. D. (1987). Topographical control of cell behaviour. I. Simple step cues. Development 99, 439-448.
18. Clark, P., Connolly, P., Curtis, A. S., Dow, J. A., and Wilkinson, C. D. (1990). Topographical control of cell behaviour: II. Multiple grooved substrata. Development 108, 635-644.
19. Curran, J. M., Chen, R., and Hunt, J. A. (2005). Controlling the phenotype and function of mesenchymal stem cells in vitro by adhesion to silane-modified clean glass surfaces. Biomaterials 26, 7057-7067. doi:10.1016/j.biomaterials.2005.05.008
20. Curran, J. M., Chen, R., and Hunt, J. A. (2006). The guidance of human mesenchymal stem cell differentiation in vitro by controlled modifications to the cell substrate. Biomaterials 27, 4783-4793. doi:10.1016/j.biomaterials.2006.05.001
21. Curran, J. M., Stokes, R., Irvine, E., Graham, D., Amro, N. A., Sanedrin, R. G., et al. (2010). Introducing dip pen nanolithography as a tool for controlling stem cell behaviour: unlocking the potential of the next generation of smart materials in regenerative medicine. Lab. Chip 10, 1662-1670. doi:10.1039/c004149a
22. Curtis, A. S., Casey, B., Gallagher, J. O., Pasqui, D., Wood, M. A., and Wilkinson, C. D. (2001). Substratum nanotopography and the adhesion of biological cells. Are symmetry or regularity of nanotopography important? Biophys. Chem. 94, 275-283. doi:10.1016/S0301-4622(01)00247-2
23. Dalby, M., Gadegaard, N., Tare, R., Andar, A., Riehle, M. O., Herzyk, P., et al. (2007). The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 6, 997-1003. doi:10.1038/nmat2013
24. Dalby, M. J. (2007). Cellular response to low adhesion nanotopographies. Int. J. Nanomedicine 2, 373-381.
25. Dalby, M. J., Gadegaard, N., and Oreffo, R. O. (2014). Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nat. Mater. 13, 558-569. doi:10.1038/nmat3980
26. Dalby, M. J., Hart, A., and Yarwood, S. J. (2008). The effect of the RACK1 signalling protein on the regulation of cell adhesion and cell contact guidance on nanometric grooves. Biomaterials 29, 282-289. doi:10.1016/j.biomaterials.2007.09.030
27. Dalby, M. J., Riehle, M. O., Johnstone, H., Affrossman, S., and Curtis, A. S. (2002a). In vitro reaction of endothelial cells to polymer demixed nanotopography. Biomaterials 23, 2945-2954. doi:10.1016/S0142-9612(01)00424-0
28. Dalby, M. J., Yarwood, S. J., Riehle, M. O., Johnstone, H. J., Affrossman, S., and Curtis, A. S. (2002b). Increasing fibroblast response to materials using nanotopography: morphological and genetic measurements of cell response to 13-nm-high polymer demixed islands. Exp. Cell Res. 276, 1-9. doi:10.1006/excr.2002.5498
29. Dalby, M. J., Riehle, M. O., Johnstone, H., Affrossman, S., and Curtis, A. S. G. (2004). Investigating the limits of filopodial sensing: a brief report using SEM to image the interaction between 10 nm high nano-topography and fibroblast filopodia. Cell Biol. Int. 28, 229-236. doi:10.1016/j.cellbi.2003.12.004
30. Das, R. K., Zouani, O. F., Labrugere, C., Oda, R., and Durrieu, M. C. (2013). Influence of nanohelical shape and periodicity on stem cell fate. ACS Nano 7, 3351-3361. doi:10.1021/nn4001325
31. DeForest, C. A., Polizzotti, B. D., and Anseth, K. S. (2009). Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments. Nat. Mater. 8, 659-664. doi:10.1038/nmat2473
32. Denis, F. A., Hanarp, P., Sutherland, D. S., and Dufrene, Y. F. (2002). Fabrication of nanostructured polymer surfaces using colloidal lithography and spin-coating. Nano Lett. 2, 1419-1425. doi:10.1021/nl025750g
33. Discher, D. E., Janmey, P., and Wang, Y.-L. (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143. doi:10.1126/science.1116995
34. Discher, D. E., Mooney, D. J., and Zandstra, P. W. (2009). Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673-1677. doi:10.1126/science.1171643
35. DuFort, C. C., Paszek, M. J., and Weaver, V. M. (2011). Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 12, 308-319. doi:10.1038/nrm3112
36. Ehninger, A., and Trumpp, A. (2011). The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J. Exp. Med. 208, 421-428. doi:10.1084/jem.20110132
37. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. doi:10.1016/j.cell.2006.06.044
38. Frith, J. E., Mills, R. J., and Cooper-White, J. J. (2012). Lateral spacing of adhesion peptides influences human mesenchymal stem cell behaviour. J. Cell Sci. 125, 317-327. doi:10.1242/jcs.087916
39. Gadegaard, N., Thoms, S., Macintyre, D. S., McGhee, K., Gallagher, J., Casey, B., et al. (2003a). Arrays of nano-dots for cellular engineering. Microelectron. Eng. 67, 162-168. doi:10.1016/S0167-9317(03)00067-4
40. Gadegaard, N., Mosler, S., and Larsen, N. B. (2003b). Biomimetic polymer nanostructures by injection molding. Macromol. Mater. Eng. 288, 76-83. doi:10.1002/mame.200290037
41. Gallagher, J. O., McGhee, K. F., Wilkinson, C. D., and Riehle, M. O. (2002). Interaction of animal cells with ordered nanotopography. IEEE Trans. Nanobioscience 1, 24-28. doi:10.1109/TNB.2002.806918
42. Gates, B. D., Xu, Q., Stewart, M., Ryan, D., Willson, C. G., and Whitesides, G. M. (2005). New approaches to nanofabrication: molding, printing, and other techniques. Chem. Rev. 105, 1171-1196. doi:10.1021/cr030076o
43. Geiger, B., Bershadsky, A., Pankov, R., and Yamada, K. M., (2001). Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2, 793-805. doi:10.1038/35099066
44. Giam, L. R., Massich, M. D., Hao, L., Shin Wong, L., Mader, C. C., and Mirkin, C. A. (2012). Scanning probe-enabled nanocombinatorics define the relationship between fibronectin feature size and stem cell fate. Proc. Natl. Acad. Sci. U.S.A. 109, 4377-4382. doi:10.1073/pnas.1201086109
45. Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E., Sacco, A., Leonardi, N. A., Kraft, P., et al. (2010). Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081. doi:10.1126/science.1191035
46. Ginger, D. S., Zhang, H., and Mirkin, C. A. (2004). The evolution of dip-pen nanolithography. Angew. Chem. Int. Ed. Engl. 43, 30-45. doi:10.1002/ange.200300608
47. Gobaa, S., Hoehnel, S., Roccio, M., Negro, A., Kobel, S., and Lutolf, M. P. (2011). Artificial niche microarrays for probing single stem cell fate in high throughput. Nat. Methods 8, 949-955. doi:10.1038/nmeth.1732
48. Harrison, R. G. (1911). On the stereotropism of embryonic cells. Science 34, 279-281. doi:10.1126/science.34.870.279
49. Hartmann, C. A. (2006). Wnt canon orchestrating osteoblastogenesis. Trends Cell Biol. 16, 151-158. doi:10.1016/j.tcb.2006.01.001
50. Hedstrom, L. (2010). Enzyme Specificity and Selectivity. Massachusetts: John Wiley & Sons, Ltd.
51. Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., et al. (2002). Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109, 625-637. doi:10.1016/S0092-8674(02)00754-7
52. Hench, L. L., and Polak, J. M. (2002). Third-generation biomedical materials. Science 295, 1014-1017. doi:10.1126/science.1067404
53. Hersel, U., Dahmen, C., and Kessler, H. (2003). RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24, 4385-4415. doi:10.1016/S0142-9612(03)00343-0
54. Hoerstrup, S. P., Sodian, R., Daebritz, S., Wang, J., Bacha, E. A., Martin, D. P., et al. (2000). Functional living trileaflet heart valves grown in vitro. Circulation 102, III44-III49. doi:10.1161/01.CIR.102.suppl_3.III-44
55. Huang, J., Grater, S. V., Corbellini, F., Rinck, S., Bock, E., Kemkemer, R., et al. (2009). Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett. 9, 1111-1116. doi:10.1021/nl803548b
56. Huebsch, N., Arany, P. R., Mao, A. S., Shvartsman, D., Ali, O. A., Bencherif, S. A., et al. (2010). Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9, 518-526. doi:10.1038/nmat2732
57. Humphries, J. D., Byron, A., and Humphries, M. J. (2006). Integrin ligands at a glance. J. Cell Sci. 119, 3901-3903. doi:10.1242/jcs.03098
58. Hur, E. M., and Kim, K. T. (2002). G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity. Cell. Signal. 14, 397-405. doi:10.1016/S0898-6568(01)00258-3
59. Ingber, D. (1993). Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 104, 613-627.
60. Ingber, D. E. (2005). Mechanical control of tissue growth: function follows form. Proc. Natl. Acad. Sci. U.S.A. 102, 11571-11572. doi:10.1073/pnas.0505939102
61. Ji, L., LaPointe, V. L. S., Evans, N. D., and Stevens, M. M. (2012). Changes in embryonic stem cell colony morphology and early differentiation markers driven by colloidal crystal topographical cues. Eur. Cell. Mater. 23, 135-146.
62. Jiang, G., Giannone, G., Critchley, D. R., Fukumoto, E., and Sheetz, M. P. (2003). Two-piconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424, 334-337. doi:10.1038/nature01805
63. Kane, R. S., Takayama, S., Ostuni, E., Ingber, D. E., and Whitesides, G. M. (1999). Patterning proteins and cells using soft lithography. Biomaterials 20, 2363-2376. doi:10.1016/S0142-9612(99)00165-9
64. Khetan, S., Guvendiren, M., Legant, W. R., Cohen, D. M., Chen, C. S., and Burdick, J. A. (2013). Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat. Mater. 12, 458-465. doi:10.1038/nmat3586
65. Kilian, K. A., Bugarija, B., Lahn, B. T., and Mrksich, M. (2010). Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. U.S.A. 107, 4872-4877. doi:10.1073/pnas.0903269107
66. Kilian, K. A., and Mrksich, M. (2012). Directing stem cell fate by controlling the affinity and density of ligand-receptor interactions at the biomaterials interface. Angew. Chem. Int. Ed. Engl. 124, 4975-4979. doi:10.1002/anie.201108746
67. Kim, J., Kim, I. S., Cho, T. H., Lee, K. B., Hwang, S. J., Tae, G., et al. (2007). Bone regeneration using hyaluronic acid-based hydrogel with bone morphogenic protein-2 and human mesenchymal stem cells. Biomaterials 28, 1830-1837. doi:10.1016/j.biomaterials.2006.11.050
68. Kingham, E., White, K., Gadegaard, N., Dalby, M. J., and Oreffo, R. O. C. (2013). Nanotopographical cues augment mesenchymal differentiation of human embryonic stem cells. Small 9, 2140-2151. doi:10.1002/smll.201202340
69. Ko, E. K., Jeong, S. I., Rim, N. G., Lee, Y. M., Shin, H., and Lee, B. K. (2008). In vitro osteogenic differentiation of human mesenchymal stem cells and in vivo bone formation in composite nanofiber meshes. Tissue Eng. Part A 14, 2105-2119. doi:10.1089/ten.tea.2008.0057
70. Kode, J. A., Mukherjee, S., Joglekar, M. V., and Hardikar, A. A. (2009). Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 11, 377-391. doi:10.1080/14653240903080367
71. Koh, C. J., and Atala, A. (2004). Tissue engineering, stem cells, and cloning: opportunities for regenerative medicine. J. Am. Soc. Nephrol. 15, 1113-1125. doi:10.1097/01.ASN.0000119683.59068.F0
72. Kong, Y. P., Tu, C. H., Donovan, P. J., and Yee, A. F. (2013). Expression of Oct4 in human embryonic stem cells is dependent on nanotopographical configuration. Acta Biomater. 9, 6369-6380. doi:10.1016/j.actbio.2013.01.036
73. Krishnamoorthy, S., Pugin, R., Brugger, J., Heinzelmann, H., Hoogerwerf, A. C., and Hinderling, C. (2006). Block copolymer micelles as switchable templates for nanofabrication. Langmuir 22, 3450-3452. doi:10.1021/la052299a
74. Lee, J. H., Rim, N. G., Jung, H. S., and Shin, H. (2010). Control of osteogenic differentiation and mineralization of human mesenchymal stem cells on composite nanofibers containing poly[lactic-co-(glycolic acid)] and hydroxyapatite. Macromol. Biosci. 10, 173-182. doi:10.1002/mabi.200900169
75. Leven, R. M., Virdi, A. S., and Sumner, D. R. (2004). Patterns of gene expression in rat bone marrow stromal cells cultured on titanium alloy discs of different roughness. J. Biomed. Mater. Res. A 70, 391-401. doi:10.1002/jbm.a.30082
76. Liu, D., Xie, Y., Shao, H., and Jiang, X. (2009). Using azobenzene-embedded self-assembled monolayers to photochemically control cell adhesion reversibly. Angew. Chem. Int. Ed. Engl. 48, 4406-4408. doi:10.1002/anie.200901130
77. Lutolf, M. P., and Blau, H. M. (2009). Artificial stem cell niches. Adv. Mater. 21, 3255-3268. doi:10.1002/adma.200802582
78. Lutolf, M. P., Gilbert, P. M., and Blau, H. M. (2009). Designing materials to direct stem-cell fate. Nature 462, 433-441. doi:10.1038/nature08602
79. Macchiarini, P., Walles, T., Biancosino, C., and Mertsching, H. (2004). First human transplantation of a bioengineered airway tissue. J. Thorac. Cardiovasc. Surg. 128, 638-641. doi:10.1016/j.jtcvs.2004.02.042
80. Maclaine, S. E., Gadhari, N., Pugin, R., Meek, R. M., Liley, M., and Dalby, M. J. (2012). Optimizing the osteogenicity of nanotopography using block co-polymer phase separation fabrication techniques. J. Orthop. Res. 30, 1190-1197. doi:10.1002/jor.22076
81. Matsuoka, F., Takeuchi, I., Agata, H., Kagami, H., Shiono, H., Kiyota, Y., et al. (2013). Morphology-based prediction of osteogenic differentiation potential of human mesenchymal stem cells. PLoS ONE 8:e55082. doi:10.1371/journal.pone.0055082
82. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., and Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495. doi:10.1016/S1534-5807(04)00075-9
83. McMurray, R. J., Gadegaard, N., Tsimbouri, P. M., Burgess, K. V., McNamara, L. E., Tare, R., et al. (2011). Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat. Mater. 10, 637-644. doi:10.1038/nmat3058
84. McNamara, L. E., Sjöström, T., Burgess, K. E., Kim, J. J., Liu, E., Gordonov, S., et al. (2011). Skeletal stem cell physiology on functionally distinct titania nanotopographies. Biomaterials 32, 7403-7410. doi:10.1016/j.biomaterials.2011.06.063
85. Mei, Y., Saha, K., Bogatyrev, S. R., Yang, J., Hook, A. L., Kalcioglu, Z. I., et al. (2010). Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells. Nat. Mater. 9, 768-778. doi:10.1038/nmat2812
86. Mosiewicz, K. A., Kolb, L., van der Vlies, A. J., Martino, M. M., Lienemann, P. S., Hubbell, J. A., et al. (2013). In situ cell manipulation through enzymatic hydrogel photopatterning. Nat. Mater. 12, 1072-1078. doi:10.1038/nmat3766
87. Murphy, S. V., and Atala, A. (2013). Organ engineering combining stem cells, biomaterials, and bioreactors to produce bioengineered organs for transplantation. Bioessays 35, 163-172. doi:10.1002/bies.201200062
88. Nuttelman, C. R., Tripodi, M. C., and Anseth, K. S. (2006). Dexamethasone-functionalized gels induce osteogenic differentiation of encapsulated hMSCs. J. Biomed. Mater. Res. A 76, 183-195. doi:10.1002/jbm.a.30537
89. Ohmuro-Matsuyama, Y., and Tatsu, Y. (2008). Photocontrolled cell adhesion on a surface functionalized with a caged arginine-glycine-aspartate peptide. Angew. Chem. Int. Ed. Engl. 47, 7527-7529. doi:10.1002/anie.200802731
90. Oreffo, R. O. C., Cooper, C., Mason, C., and Clements, M. (2005). Mesenchymal stem cells: lineage, plasticity, and skeletal therapeutic potential. Stem Cell. Rev. 1, 169-178. doi:10.1385/SCR:1:2:169
91. Ott, H. C., Matthiesen, T. S., Goh, S. K., Black, L. D., Kren, S. M., Netoff, T. I., et al. (2008). Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14, 213-221. doi:10.1038/nm1684
92. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254. doi:10.1016/j.ccr.2005.08.010
93. Petersen, S., Alonso, J. M., Specht, A., Duodu, P., Goeldner, M., and del Campo, A. (2008). Phototriggering of cell adhesion by caged cyclic RGD peptides. Angew. Chem. Int. Ed. Engl. 47, 3192-3195. doi:10.1002/anie.200704857
94. Pittenger, M. F. (2008). Mesenchymal stem cells from adult bone marrow. Methods Mol. Biol. 449, 27-44. doi:10.1007/978-1-60327-169-1_2
95. Pouille, P. A., Ahmadi, P., Brunet, A. C., and Farge, E. (2009). Mechanical signals trigger myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci. Signal. 2, ra16. doi:10.1126/scisignal.2000098
96. Prusty, D., Park, B.-H., Davis, K. E., and Farmer, S. R. (2002). Activation of MEK/ERK signaling promotes adipogenesis by enhancing peroxisome proliferator-activated receptor gamma (PPARgamma) and C/EBPalpha gene expression during the differentiation of 3T3-L1 preadipocytes. J. Biol. Chem. 277, 46226-46232. doi:10.1074/jbc.M207776200
97. Putnam, A. J., Schultz, K., and Mooney, D. J. (2001). Control of microtubule assembly by extracellular matrix and externally applied strain. Am. J. Physiol. Cell Physiol. 280, C556-C564.
98. Qin, D., Xia, Y., and Whitesides, G. M. (2010). Soft lithography for micro-and nanoscale patterning. Nat. Protoc. 5, 491-502. doi:10.1038/nprot.2009.234
99. Rahman, M. S., Akhtar, N., Jamil, H. M., Banik, R. S., and Asaduzzaman, S. M. (2015). TGF-beta/BMP signaling and other molecular events: regulation of osteoblastogenesis and bone formation. Bone Res. 3, 15005. doi:10.1038/boneres.2015.5
100. Rawsterne, R. E., Todd, S. J., Gough, J. E., Farrar, D., Rutten, F. J., Alexander, M. R., et al. (2007). Cell spreading correlates with calculated logP of amino acid-modified surfaces. Acta Biomater. 3, 715-721. doi:10.1016/j.actbio.2007.02.006
101. Rim, N. G., Shin, C. S., and Shin, H. (2013). Current approaches to electrospun nanofibers for tissue engineering. Biomed. Mater. 8, 014102. doi:10.1088/1748-6041/8/1/014102
102. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., et al. (2001). 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. 153, 1175-1186. doi:10.1083/jcb.153.6.1175
103. Ruoslahti, E., and Pierschbacher, M. D. (1987). New perspectives in cell adhesion: RGD and integrins. Science 238, 491-497. doi:10.1126/science.2821619
104. Shemesh, T., Geiger, B., Bershadsky, A. D., and Kozlov, M. M. (2005). Focal adhesions as mechanosensors: a physical mechanism. Proc. Natl. Acad. Sci. U.S.A. 102, 12383-12388. doi:10.1073/pnas.0500254102
105. Sjöström, T., Dalby, M. J., Hart, A., Tare, R., Oreffo, R. O., and Su, B. (2009). Fabrication of pillar-like titania nanostructures on titanium and their interactions with human skeletal stem cells. Acta Biomater. 5, 1433-1441. doi:10.1016/j.actbio.2009.01.007
106. Sjöström, T., McNamara, L. E., Meek, R. M. D., Dalby, M. J., and Su, B. (2013). 2D and 3D nanopatterning of titanium for enhancing osteoinduction of stem cells at implant surfaces. Adv. Healthc. Mater. 2, 1285-1293. doi:10.1002/adhm.201200353
107. Sjöström, T., McNamara, L. E., Yang, L., Dalby, M. J., and Su, B. (2012). Novel anodization technique using a block copolymer template for nanopatterning of titanium implant surfaces. ACS Appl. Mater. Interfaces 4, 6354-6361. doi:10.1021/am301987e
108. Teixeira, A. I., McKie, G. A., Foley, J. D., Bertics, P. J., Nealey, P. F., and Murphy, C. J. (2006). The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials 27, 3945-3954. doi:10.1016/j.biomaterials.2006.01.044
109. Todd, S. J., Farrar, D., Gough, J. E., and Ulijn, R. V. (2007). Enzyme-triggered cell attachment to hydrogel surfaces. Soft Matter 3, 547-550. doi:10.1039/b618256a
110. Tourniaire, G., Collins, J., Campbell, S., Mizomoto, H., Ogawa, S., Thaburet, J. F., et al. (2006). Polymer microarrays for cellular adhesion. Chem. Commun. 2118-2120. doi:10.1039/b602009g
111. Trappmann, B., Gautrot, J. E., Connelly, J. T., Strange, D. G., Li, Y., Oyen, M. L., et al. (2012). Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11, 642-649. doi:10.1038/nmat3339
112. Tsimbouri, P. M., McMurray, R. J., Burgess, K. V., Alakpa, E. V., Reynolds, P. M., Murawski, K., et al. (2012). Using nanotopography and metabolomics to identify biochemical effectors of multipotency. ACS Nano 6, 10239-10249. doi:10.1021/nn304046m
113. Tsimbouri, P. M., Murawski, K., Hamilton, G., Herzyk, P., Oreffo, R. O., Gadegaard, N., et al. (2013). A genomics approach in determining nanotopographical effects on MSC phenotype. Biomaterials 34, 2177-2184. doi:10.1016/j.biomaterials.2012.12.019
114. Visse, R., and Nagase, H. (2003). Matrix metalloproteinases and tissue inhibitors of metalloproteinases-structure, function, and biochemistry. Circ. Res. 92, 827-839. doi:10.1161/01.RES.0000070112.80711.3D
115. Watt, F. M., and Hogan, B. L. M. (2000). Out of Eden: stem cells and their niches. Science 287, 1427-1430. doi:10.1126/science.287.5457.1427
116. Weber, L. M., Hayda, K. N., Haskins, K., and Anseth, K. S. (2007). The effects of cell-matrix interactions on encapsulated beta-cell function within hydrogels functionalized with matrix-derived adhesive peptides. Biomaterials 28, 3004-3011. doi:10.1016/j.biomaterials.2007.03.005
117. Wei, S. C., Fattet, L., Tsai, J. H., Guo, Y., Pai, V. H., Majeski, H. E., et al. (2015). Matrix stiffness drives epithelial-mesenchymal transition and tumour metastasis through a TWIST1-G3BP2 mechanotransduction pathway. Nat. Cell Biol. 17, 678-688. doi:10.1038/ncb3157
118. Weiss, P., and Garber, B. (1952). Shape and movement of mesenchyme cells as functions of the physical structure of the medium-contributions to a quantitative morphology. Proc. Natl. Acad. Sci. U.S.A. 38, 264-280. doi:10.1073/pnas.38.3.264
119. Wen, J. H., Vincent, L. G., Fuhrmann, A., Choi, Y. S., Hribar, K. C., Taylor-Weiner, H., et al. (2014). Interplay of matrix stiffness and protein tethering in stem cell differentiation. Nat. Mater. 13, 979-987. doi:10.1038/nmat4051
120. Wilkinson, C. D. (2004). Making structures for cell engineering. Eur. Cell. Mater. 8, 21-26.
121. Wirkner, M., Alonso, J. M., Maus, V., Salierno, M., Lee, T. T., García, A. J., et al. (2011a). Triggered cell release from materials using bioadhesive photocleavable linkers. Adv. Mater. Weinheim 23, 3907-3910. doi:10.1002/adma.201100925
122. Wirkner, M., Weis, S., San Miguel, V., Álvarez, M., Gropeanu, R. A., Salierno, M., et al. (2011b). Photoactivatable caged cyclic RGD peptide for triggering integrin binding and cell adhesion to surfaces. Chembiochem 12, 2623-2629. doi:10.1002/cbic.201100437
123. Xiao, G., Jiang, D., Gopalakrishnan, R., and Franceschi, R. T. (2002). Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J. Biol. Chem. 277, 36181-36187. doi:10.1074/jbc.M206057200
124. Yamada, K. M. (1991). Adhesive recognition sequences. J. Biol. Chem. 266, 12809-12812.
125. Yamato, M., Konno, C., Utsumi, M., Kikuchi, A., and Okano, T. (2002). Thermally responsive polymer-grafted surfaces facilitate patterned cell seeding and co-culture. Biomaterials 23, 561-567. doi:10.1016/S0142-9612(01)00138-7
126. Yang, C., Tibbitt, M. W., Basta, L., and Anseth, K. S. (2014). Mechanical memory and dosing influence stem cell fate. Nat. Mater. 13, 645-652. doi:10.1038/nmat3889
127. Yang, X., Harkins, L. K., Zubanova, O., Harrington, A., Kovalenko, D., Nadeau, R. J., et al. (2008). Overexpression of Spry1 in chondrocytes causes attenuated FGFR ubiquitination and sustained ERK activation resulting in chondrodysplasia. Dev. Biol. 321, 64-76. doi:10.1016/j.ydbio.2008.05.555
128. Yeo, W. S., Yousaf, M. N., and Mrksich, M. (2003). Dynamic interfaces between cells and surfaces: electroactive substrates that sequentially release and attach cells. J. Am. Chem. Soc. 125, 14994-14995. doi:10.1021/ja038265b
129. Yim, E. K. F., Pang, S. W., and Leong, K. W. (2007). Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp. Cell Res. 313, 1820-1829. doi:10.1016/j.yexcr.2007.02.031
130. Zelzer, M., Scurr, D. J., Alexander, M. R., and Ulijn, R. V. (2012). Development and validation of a fluorescence method to follow the build-up of short peptide sequences on solid 2D surfaces. ACS Appl. Mater. Interfaces 4, 53-58. doi:10.1021/am2015266
131. Zhang, Y., Ouyang, H., Chwee, T. L., Ramakrishna, S., and Huang, Z. M. (2005). Electrospinning of gelatin fibers and gelatin/PCL composite fibrous scaffolds. J. Biomed. Mater. Res. Part B Appl. Biomater. 72, 156-165. doi:10.1002/jbm.b.30128