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Stem Cells International
Volume 2015, Article ID 167025, 35 pages
http://dx.doi.org/10.1155/2015/167025
Review Article

Physical, Spatial, and Molecular Aspects of Extracellular Matrix of In Vivo Niches and Artificial Scaffolds Relevant to Stem Cells Research

1Imtek Limited, 3 Cherepkovskaya 15, Moscow 21552, Russia
2Gamaleya Research Institute of Epidemiology and Microbiology Federal State Budgetary Institution, Ministry of Health of the Russian Federation, Gamalei 18, Moscow 123098, Russia
3Russian Cardiology Research and Production Center Federal State Budgetary Institution, Ministry of Health of the Russian Federation, 3 Cherepkovskaya 15, Moscow 21552, Russia
4Division of Matrix Biology, Department of Medical Biochemistry and Biophysics, Karolinska Institute, 171 77 Stockholm, Sweden

Received 2 April 2015; Revised 7 June 2015; Accepted 24 June 2015

Academic Editor: Hai-Quan Mao

Copyright © 2015 Maria Akhmanova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. M. Watt and W. T. S. Huck, “Role of the extracellular matrix in regulating stem cell fate,” Nature Reviews Molecular Cell Biology, vol. 14, no. 8, pp. 467–473, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. M. J. Dalby, N. Gadegaard, and R. O. C. Oreffo, “Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate,” Nature Materials, vol. 13, no. 6, pp. 558–569, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. R. J. Klebe, “Isolation of a collagen-dependent cell attachment factor,” Nature, vol. 250, no. 463, pp. 248–251, 1974. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Timpl, H. Rohde, P. G. Robey, S. I. Rennard, J. M. Foidart, and G. R. Martin, “Laminin—a glycoprotein from basement membranes,” The Journal of Biological Chemistry, vol. 254, no. 19, pp. 9933–9937, 1979. View at Google Scholar · View at Scopus
  5. S. M. Frisch and H. Francis, “Disruption of epithelial cell-matrix interactions induces apoptosis,” Journal of Cell Biology, vol. 124, no. 4, pp. 619–626, 1994. View at Publisher · View at Google Scholar · View at Scopus
  6. J. H. Miner and P. D. Yurchenco, “Laminin functions in tissue morphogenesis,” Annual Review of Cell and Developmental Biology, vol. 20, pp. 255–284, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Domogatskaya, S. Rodin, and K. Tryggvason, “Functional diversity of laminins,” Annual Review of Cell and Developmental Biology, vol. 28, pp. 523–553, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Chiarugi and E. Giannoni, “Anoikis: a necessary death program for anchorage-dependent cells,” Biochemical Pharmacology, vol. 76, no. 11, pp. 1352–1364, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Marastoni, G. Ligresti, E. Lorenzon, A. Colombatti, and M. Mongiat, “Extracellular matrix: a matter of life and death,” Connective Tissue Research, vol. 49, no. 3-4, pp. 203–206, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, “Matrix elasticity directs stem cell lineage specification,” Cell, vol. 126, no. 4, pp. 677–689, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. D. E. Discher, D. J. Mooney, and P. W. Zandstra, “Growth factors, matrices, and forces combine and control stem cells,” Science, vol. 324, no. 5935, pp. 1673–1677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. A. R. Cameron, J. E. Frith, and J. J. Cooper-White, “The influence of substrate creep on mesenchymal stem cell behaviour and phenotype,” Biomaterials, vol. 32, no. 26, pp. 5979–5993, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. G. C. Reilly and A. J. Engler, “Intrinsic extracellular matrix properties regulate stem cell differentiation,” Journal of Biomechanics, vol. 43, no. 1, pp. 55–62, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. D. A. Lee, M. M. Knight, J. J. Campbell, and D. L. Bader, “Stem cell mechanobiology,” Journal of Cellular Biochemistry, vol. 112, no. 1, pp. 1–9, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. A. L. Zajac and D. E. Discher, “Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling,” Current Opinion in Cell Biology, vol. 20, no. 6, pp. 609–615, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. B. M. Baker and C. S. Chen, “Deconstructing the third dimension—how 3D culture microenvironments alter cellular cues,” Journal of Cell Science, vol. 125, no. 13, pp. 3015–3024, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Théry, “Micropatterning as a tool to decipher cell morphogenesis and functions,” Journal of Cell Science, vol. 123, no. 24, pp. 4201–4213, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Guilak, D. M. Cohen, B. T. Estes, J. M. Gimble, W. Liedtke, and C. S. Chen, “Control of stem cell fate by physical interactions with the extracellular matrix,” Cell Stem Cell, vol. 5, no. 1, pp. 17–26, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. R. O. Hynes, “The extracellular matrix: not just pretty fibrils,” Science, vol. 326, no. 5957, pp. 1216–1219, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Nishimune, J. R. Sanes, and S. S. Carlson, “A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals,” Nature, vol. 432, no. 7017, pp. 580–587, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Saha, A. J. Keung, E. F. Irwin et al., “Substrate modulus directs neural stem cell behavior,” Biophysical Journal, vol. 95, no. 9, pp. 4426–4438, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. A. S. Rowlands, P. A. George, and J. J. Cooper-White, “Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation,” The American Journal of Physiology—Cell Physiology, vol. 295, no. 4, pp. C1037–C1044, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Fratzl, Collagen Structure and Mechanics, Springer, 2008.
  24. A. R. Khokhlov and A. Y. Grosberg, Statistical Physics of Macromolecules, Polymers and Complex Materials, American Institute of Physics, College Park, Md, USA, 1997.
  25. J. E. Wagenseil and R. P. Mecham, “Vascular extracellular matrix and arterial mechanics,” Physiological Reviews, vol. 89, no. 3, pp. 957–989, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Wilson, C. C. van Donkelaar, R. van Rietbergen, and R. Huiskes, “The role of computational models in the search for the mechanical behavior and damage mechanisms of articular cartilage,” Medical Engineering and Physics, vol. 27, no. 10, pp. 810–826, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. I. Levental, P. C. Georges, and P. A. Janmey, “Soft biological materials and their impact on cell function,” Soft Matter, vol. 3, no. 3, pp. 299–306, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Peloquin, J. Huynh, R. M. Williams, and C. A. Reinhart-King, “Indentation measurements of the subendothelial matrix in bovine carotid arteries,” Journal of Biomechanics, vol. 44, no. 5, pp. 815–821, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Pailler-Mattei, S. Bec, and H. Zahouani, “In vivo measurements of the elastic mechanical properties of human skin by indentation tests,” Medical Engineering and Physics, vol. 30, no. 5, pp. 599–606, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. J. T. Iivarinen, R. K. Korhonen, P. Julkunen, and J. S. Jurvelin, “Experimental and computational analysis of soft tissue stiffness in forearm using a manual indentation device,” Medical Engineering and Physics, vol. 33, no. 10, pp. 1245–1253, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. X. Liang and S. A. Boppart, “Biomechanical properties of in vivo human skin from dynamic optical coherence elastography,” IEEE Transactions on Biomedical Engineering, vol. 57, no. 4, pp. 953–959, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. C. T. McKee, J. A. Last, P. Russell, and C. J. Murphy, “Indentation versus tensile measurements of young's modulus for soft biological tissues,” Tissue Engineering—Part B: Reviews, vol. 17, no. 3, pp. 155–164, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Gefen and S. S. Margulies, “Are in vivo and in situ brain tissues mechanically similar?” Journal of Biomechanics, vol. 37, no. 9, pp. 1339–1352, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. Taylor and K. Miller, “Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus,” Journal of Biomechanics, vol. 37, no. 8, pp. 1263–1269, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Y. Rho, R. B. Ashman, and C. H. Turner, “Young's modulus of trabecular and cortical bone material: ultrasonic and microtensile measurements,” Journal of Biomechanics, vol. 26, no. 2, pp. 111–119, 1993. View at Publisher · View at Google Scholar · View at Scopus
  36. F. H. Silver, Mechanosensing and Mechanochemical Transduction in Extracellular Matrix: Biological, Chemical, Engineering, and Physiological Aspects, Springer Science, 2006.
  37. F. Guilak, L. G. Alexopoulos, M. A. Haider, H. P. Ting-Beall, and L. A. Setton, “Zonal uniformity in mechanical properties of the chondrocyte pericellular matrix: micropipette aspiration of canine chondrons isolated by cartilage homogenization,” Annals of Biomedical Engineering, vol. 33, no. 10, pp. 1312–1318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. K. A. Athanasiou, M. P. Rosenwasser, J. A. Buckwalter, T. I. Malinin, and V. C. Mow, “Interspecies comparisons of in situ intrinsic mechanical properties of distal femoral cartilage,” Journal of Orthopaedic Research, vol. 9, no. 3, pp. 330–340, 1991. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Stolz, R. Gottardi, R. Raiteri et al., “Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy,” Nature Nanotechnology, vol. 4, no. 3, pp. 186–192, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. J. P. Winer, P. A. Janmey, M. E. McCormick, and M. Funaki, “Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli,” Tissue Engineering—Part A, vol. 15, no. 1, pp. 147–154, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. J.-W. Shin, J. Swift, I. Ivanovska, K. R. Spinler, A. Buxboim, and D. E. Discher, “Mechanobiology of bone marrow stem cells: from myosin-II forces to compliance of matrix and nucleus in cell forms and fates,” Differentiation, vol. 86, no. 3, pp. 77–86, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. M. F. Berry, A. J. Engler, Y. J. Woo et al., “Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 290, no. 6, pp. H2196–H2203, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. A. J. Engler, L. Richert, J. Y. Wong, C. Picart, and D. E. Discher, “Surface probe measurements of the elasticity of sectioned tissue, thin gels and polyelectrolyte multilayer films: correlations between substrate stiffness and cell adhesion,” Surface Science, vol. 570, no. 1-2, pp. 142–154, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Mueller and L. Sandrin, “Liver stiffness: a novel parameter for the diagnosis of liver disease,” Hepatic Medicine: Evidence and Research, vol. 2010, no. 2, pp. 49–67, 2010. View at Publisher · View at Google Scholar
  45. A. Urciuolo, M. Quarta, V. Morbidoni et al., “Collagen VI regulates satellite cell self-renewal and muscle regeneration,” Nature communications, vol. 4, article 1964, 2013. View at Google Scholar · View at Scopus
  46. Z. Li, X. Guo, A. F. Palmer, H. Das, and J. Guan, “High-efficiency matrix modulus-induced cardiac differentiation of human mesenchymal stem cells inside a thermosensitive hydrogel,” Acta Biomaterialia, vol. 8, no. 10, pp. 3586–3595, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Breitbach, T. Bostani, W. Roell et al., “Potential risks of bone marrow cell transplantation into infarcted hearts,” Blood, vol. 110, no. 4, pp. 1362–1369, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. G. M. Harris, M. E. Piroli, and E. Jabbarzadeh, “Deconstructing the effects of matrix elasticity and geometry in mesenchymal stem cell lineage commitment,” Advanced Functional Materials, vol. 24, no. 16, pp. 2396–2403, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. J. H. Wen, L. G. Vincent, A. Fuhrmann et al., “Interplay of matrix stiffness and protein tethering in stem cell differentiation,” Nature Materials, vol. 13, no. 10, pp. 979–987, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. P. M. Gilbert, K. L. Havenstrite, K. E. G. Magnusson et al., “Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture,” Science, vol. 329, no. 5995, pp. 1078–1081, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. S. R. Peyton, Z. I. Kalcioglu, J. C. Cohen et al., “Marrow-Derived stem cell motility in 3D synthetic scaffold is governed by geometry along with adhesivity and stiffness,” Biotechnology and Bioengineering, vol. 108, no. 5, pp. 1181–1193, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. F. Rehfeldt, A. E. X. Brown, M. Raab et al., “Hyaluronic acid matrices show matrix stiffness in 2D and 3D dictates cytoskeletal order and myosin-II phosphorylation within stem cells,” Integrative Biology, vol. 4, no. 4, pp. 422–430, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. T. H. Kim, D. B. An, S. H. Oh, M. K. Kang, H. H. Song, and J. H. Lee, “Creating stiffness gradient polyvinyl alcohol hydrogel using a simple gradual freezing-thawing method to investigate stem cell differentiation behaviors,” Biomaterials, vol. 40, pp. 51–60, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. Z. Li, Y. Gong, S. Sun et al., “Differential regulation of stiffness, topography, and dimension of substrates in rat mesenchymal stem cells,” Biomaterials, vol. 34, no. 31, pp. 7616–7625, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. G. J. Her, H.-C. Wu, M.-H. Chen, M.-Y. Chen, S.-C. Chang, and T.-W. Wang, “Control of three-dimensional substrate stiffness to manipulate mesenchymal stem cell fate toward neuronal or glial lineages,” Acta Biomaterialia, vol. 9, no. 2, pp. 5170–5180, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Schellenberg, S. Joussen, K. Moser et al., “Matrix elasticity, replicative senescence and DNA methylation patterns of mesenchymal stem cells,” Biomaterials, vol. 35, no. 24, pp. 6351–6358, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. L.-S. Wang, J. Boulaire, P. P. Y. Chan, J. E. Chung, and M. Kurisawa, “The role of stiffness of gelatin-hydroxyphenylpropionic acid hydrogels formed by enzyme-mediated crosslinking on the differentiation of human mesenchymal stem cell,” Biomaterials, vol. 31, no. 33, pp. 8608–8616, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. P.-Y. Wang, W.-B. Tsai, and N. H. Voelcker, “Screening of rat mesenchymal stem cell behaviour on polydimethylsiloxane stiffness gradients,” Acta Biomaterialia, vol. 8, no. 2, pp. 519–530, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. L.-S. Wang, C. Du, J. E. Chung, and M. Kurisawa, “Enzymatically cross-linked gelatin-phenol hydrogels with a broader stiffness range for osteogenic differentiation of human mesenchymal stem cells,” Acta Biomaterialia, vol. 8, no. 5, pp. 1826–1837, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. Y.-C. Kuo, S.-C. Hung, and S.-H. Hsu, “The effect of elastic biodegradable polyurethane electrospun nanofibers on the differentiation of mesenchymal stem cells,” Colloids and Surfaces B: Biointerfaces, vol. 122, pp. 414–422, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Wingate, W. Bonani, Y. Tan, S. J. Bryant, and W. Tan, “Compressive elasticity of three-dimensional nanofiber matrix directs mesenchymal stem cell differentiation to vascular cells with endothelial or smooth muscle cell markers,” Acta Biomaterialia, vol. 8, no. 4, pp. 1440–1449, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. J. S. Park, J. S. Chu, A. D. Tsou et al., “The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β,” Biomaterials, vol. 32, no. 16, pp. 3921–3930, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. D. E. Discher, P. Janmey, and Y.-L. Wang, “Tissue cells feel and respond to the stiffness of their substrate,” Science, vol. 310, no. 5751, pp. 1139–1143, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. N. D. Evans, C. Minelli, E. Gentleman et al., “Substrate stiffness affects early differentiation events in embryonic stem cells,” European Cells and Materials, vol. 18, pp. 1–13, 2009. View at Google Scholar · View at Scopus
  65. J. Nam, J. Johnson, J. J. Lannutti, and S. Agarwal, “Modulation of embryonic mesenchymal progenitor cell differentiation via control over pure mechanical modulus in electrospun nanofibers,” Acta Biomaterialia, vol. 7, no. 4, pp. 1516–1524, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. D. A. Young, Y. S. Choi, A. J. Engler, and K. L. Christman, “Stimulation of adipogenesis of adult adipose-derived stem cells using substrates that mimic the stiffness of adipose tissue,” Biomaterials, vol. 34, no. 34, pp. 8581–8588, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Holst, S. Watson, M. S. Lord et al., “Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells,” Nature Biotechnology, vol. 28, no. 10, pp. 1123–1128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. C. Lee-Thedieck, N. Rauch, R. Fiammengo, G. Klein, and J. P. Spatz, “Impact of substrate elasticity on human hematopoietic stem and progenitor cell adhesion and motility,” Journal of Cell Science, vol. 125, part 16, pp. 3765–3775, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. J. R. Tse and A. J. Engler, “Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate,” PLoS ONE, vol. 6, no. 1, Article ID e15978, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. L. G. Vincent, Y. S. Choi, B. Alonso-Latorre, J. C. del Álamo, and A. J. Engler, “Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength,” Biotechnology Journal, vol. 8, no. 4, pp. 472–484, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. N. Wang, I. M. Toli-Nørrelykke, J. Chen et al., “Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells,” The American Journal of Physiology—Cell Physiology, vol. 282, no. 3, pp. 606–616, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Buxboim, K. Rajagopal, A. E. X. Brown, and D. E. Discher, “How deeply cells feel: methods for thin gels,” Journal of Physics Condensed Matter, vol. 22, no. 19, Article ID 194116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Mammoto, A. Mammoto, and D. E. Ingber, “Mechanobiology and developmental control,” Annual Review of Cell and Developmental Biology, vol. 29, pp. 27–61, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Swift, I. L. Ivanovska, A. Buxboim et al., “Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation,” Science, vol. 341, no. 6149, Article ID 1240104, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. Y.-C. Poh, F. Chowdhury, T. S. Tanaka, and N. Wangt, “Embryonic stem cells do not stiffen on rigid substrates,” Biophysical Journal, vol. 99, no. 2, pp. L19–L21, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. E. T. Curtis, S. Zhang, V. Khalilzad-Sharghi, T. Boulet, and S. F. Othman, “Magnetic resonance elastography methodology for the evaluation of tissue engineered construct growth,” Journal of Visualized Experiments, no. 60, Article ID e3618, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. J. Du, X. Chen, X. Liang et al., “Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 23, pp. 9466–9471, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. Y.-R. V. Shih, K.-F. Tseng, H.-Y. Lai, C.-H. Lin, and O. K. Lee, “Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells,” Journal of Bone and Mineral Research, vol. 26, no. 4, pp. 730–738, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. M. P. Lutolf and H. M. Blau, “Artificial stem cell niches,” Advanced Materials, vol. 21, no. 32-33, pp. 3255–3268, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Kim, Y. H. Kim, and G. Tae, “Human mesenchymal stem cell culture on heparin-based hydrogels and the modulation of interactions by gel elasticity and heparin amount,” Acta Biomaterialia, vol. 9, no. 8, pp. 7833–7844, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. M. A. Conti, S. Even-Ram, C. Liu, K. M. Yamada, and R. S. Adelstein, “Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice,” The Journal of Biological Chemistry, vol. 279, no. 40, pp. 41263–41266, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. R. McBeath, D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen, “Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment,” Developmental Cell, vol. 6, no. 4, pp. 483–495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. T.-J. Kim, J. Seong, M. Ouyang et al., “Substrate rigidity regulates Ca2+ oscillation via RhoA pathway in stem cells,” Journal of Cellular Physiology, vol. 218, no. 2, pp. 285–293, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. B. Holt, A. Tripathi, and J. Morgan, “Viscoelastic response of human skin to low magnitude physiologically relevant shear,” Journal of Biomechanics, vol. 41, no. 12, pp. 2689–2695, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Ikoma, M. Kido, M. Nagae et al., “Effects of stress-shielding on the dynamic viscoelasticity and ordering of the collagen fibers in rabbit Achilles tendon,” Journal of Orthopaedic Research, vol. 31, no. 11, pp. 1708–1712, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. A. R. Cameron, J. E. Frith, G. A. Gomez, A. S. Yap, and J. J. Cooper-White, “The effect of time-dependent deformation of viscoelastic hydrogels on myogenic induction and Rac1 activity in mesenchymal stem cells,” Biomaterials, vol. 35, no. 6, pp. 1857–1868, 2014. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. S. Pek, A. C. A. Wan, and J. Y. Ying, “The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel,” Biomaterials, vol. 31, no. 3, pp. 385–391, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. Y. Sun, K. M. A. Yong, L. G. Villa-Diaz et al., “Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells,” Nature Materials, vol. 13, no. 6, pp. 599–604, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. B. Trappmann, J. E. Gautrot, J. T. Connelly et al., “Extracellular-matrix tethering regulates stem-cell fate,” Nature Materials, vol. 11, no. 7, pp. 642–649, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. S. Ramanujan, A. Pluen, T. D. McKee, E. B. Brown, Y. Boucher, and R. K. Jain, “Diffusion and convection in collagen gels: implications for transport in the tumor interstitium,” Biophysical Journal, vol. 83, no. 3, pp. 1650–1660, 2002. View at Publisher · View at Google Scholar · View at Scopus
  91. M. B. Albro, N. O. Chahine, R. Li, K. Yeager, C. T. Hung, and G. A. Ateshian, “Dynamic loading of deformable porous media can induce active solute transport,” Journal of Biomechanics, vol. 41, no. 15, pp. 3152–3157, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. M. M. Stevens and J. H. George, “Exploring and engineering the cell surface interface,” Science, vol. 310, no. 5751, pp. 1135–1138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. N. D. Evans, R. O. C. Oreffo, E. Healy, P. J. Thurner, and Y. H. Man, “Epithelial mechanobiology, skin wound healing, and the stem cell niche,” Journal of the Mechanical Behavior of Biomedical Materials, vol. 28, pp. 397–409, 2013. View at Publisher · View at Google Scholar · View at Scopus
  94. K. Yamamoto, T. Sokabe, T. Watabe et al., “Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro,” The American Journal of Physiology—Heart and Circulatory Physiology, vol. 288, no. 4, pp. H1915–H1924, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. M. S. Osidak, E. Osidak, M. Akhmanova, S. Domogatsky, and A. Domogatskaya, “Fibrillar, fibril-associated and basement membrane collagens of the arterial wall: architecture, elasticity and remodeling under stress,” Current Pharmaceutical Design, vol. 21, no. 9, pp. 1124–1133, 2015. View at Publisher · View at Google Scholar
  96. A. S. Adhikari, J. Chai, and A. R. Dunn, “Mechanical load induces a 100-fold increase in the rate of collagen proteolysis by MMP-1,” Journal of the American Chemical Society, vol. 133, no. 6, pp. 1686–1689, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. N. Gjorevski and M. Lutolf, “Biomaterials approaches in stem cell mechanobiology,” Progress in Molecular Biology and Translational Science, vol. 126, pp. 257–278, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. D. Lacroix, P. J. Prendergast, G. Li, and D. Marsh, “Biomechanical model to simulate tissue differentiation and bone regeneration: application to fracture healing,” Medical and Biological Engineering and Computing, vol. 40, no. 1, pp. 14–21, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. J. L. Chen, W. Zhang, Z. Y. Liu, B. C. Heng, H. W. Ouyang, and X. S. Dai, “Physical regulation of stem cells differentiation into teno-lineage: current strategies and future direction,” Cell and Tissue Research, vol. 360, no. 2, pp. 195–207, 2015. View at Publisher · View at Google Scholar
  100. P. J. Prendergast, R. Huiskes, and K. Søballe, “Biophysical stimuli on cells during tissue differentiation at implant interfaces,” Journal of Biomechanics, vol. 30, no. 6, pp. 539–548, 1997. View at Publisher · View at Google Scholar · View at Scopus
  101. H. Isaksson, W. Wilson, C. C. van Donkelaar, R. Huiskes, and K. Ito, “Comparison of biophysical stimuli for mechano-regulation of tissue differentiation during fracture healing,” Journal of Biomechanics, vol. 39, no. 8, pp. 1507–1516, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. I. Takahashi, G. H. Nuckolls, K. Takahashi et al., “Compressive force promotes Sox9, type II collagen and aggrecan and inhibits IL-1β expression resulting in chondrogenesis in mouse embryonic limb bud mesenchymal cells,” Journal of Cell Science, vol. 111, no. 14, pp. 2067–2076, 1998. View at Google Scholar · View at Scopus
  103. A. J. Steward and D. J. Kelly, “Mechanical regulation of mesenchymal stem cell differentiation,” Journal of Anatomy, 2014. View at Publisher · View at Google Scholar
  104. J. K. Mouw, J. T. Connelly, C. G. Wilson, K. E. Michael, and M. E. Levenston, “Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells,” Stem Cells, vol. 25, no. 3, pp. 655–663, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. Z. Li, S.-J. Yao, M. Alini, and M. J. Stoddart, “Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites is modulated by frequency and amplitude of dynamic compression and shear stress,” Tissue Engineering Part A, vol. 16, no. 2, pp. 575–584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. D. F. Ward Jr., R. M. Salasznyk, R. F. Klees et al., “Mechanical strain enhances extracellular matrix-induced gene focusing and promotes osteogenic differentiation of human mesenchymal stem cells through an extracellular-related kinase-dependent pathway,” Stem Cells and Development, vol. 16, no. 3, pp. 467–480, 2007. View at Publisher · View at Google Scholar · View at Scopus
  107. Y. J. Chen, C. H. Huang, I. C. Lee, Y. T. Lee, M. H. Chen, and T. H. Young, “Effects of cyclic mechanical stretching on the mRNA expression of tendon/ligament-related and osteoblast-specific genes in human mesenchymal stem cells,” Connective Tissue Research, vol. 49, no. 1, pp. 7–14, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. K. Kurpinski, J. Chu, C. Hashi, and S. Li, “Anisotropic mechanosensing by mesenchymal stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 44, pp. 16095–16100, 2006. View at Publisher · View at Google Scholar · View at Scopus
  109. J. S. Harunaga and K. M. Yamada, “Cell-matrix adhesions in 3D,” Matrix Biology, vol. 30, no. 7-8, pp. 363–368, 2011. View at Publisher · View at Google Scholar · View at Scopus
  110. E. Cukierman, R. Pankov, D. R. Stevens, and K. M. Yamada, “Taking cell-matrix adhesions to the third dimension,” Science, vol. 294, no. 5547, pp. 1708–1712, 2001. View at Publisher · View at Google Scholar · View at Scopus
  111. M. P. Lutolf, P. M. Gilbert, and H. M. Blau, “Designing materials to direct stem-cell fate,” Nature, vol. 462, no. 7272, pp. 433–441, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. M. Häger, K. Gawlik, A. Nyström, T. Sasaki, and M. Durbeej, “Laminin α1 chain corrects male infertility caused by absence of laminin α2 chain,” The American Journal of Pathology, vol. 167, no. 3, pp. 823–833, 2005. View at Publisher · View at Google Scholar · View at Scopus
  113. P. D. Yurchenco, “Basement membranes: cell scaffoldings and signaling platforms,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 2, Article ID a004911, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. K. A. Beningo, M. Dembo, and Y.-L. Wang, “Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 52, pp. 18024–18029, 2004. View at Publisher · View at Google Scholar · View at Scopus
  115. L. Khorsandi, F. Nejad-Dehbashi, A. Ahangarpour, and M. Hashemitabar, “Three-dimensional differentiation of bone marrow-derived mesenchymal stem cells into insulin-producing cells,” Tissue and Cell, vol. 47, no. 1, pp. 66–72, 2015. View at Publisher · View at Google Scholar
  116. C. R. Kothapalli and R. D. Kamm, “3D matrix microenvironment for targeted differentiation of embryonic stem cells into neural and glial lineages,” Biomaterials, vol. 34, no. 25, pp. 5995–6007, 2013. View at Publisher · View at Google Scholar · View at Scopus
  117. I. Smith, V. Silveirinha, J. L. Stein et al., “Human neural stem cell-derived cultures in three-dimensional substrates form spontaneously functional neuronal networks,” Journal of Tissue Engineering and Regenerative Medicine, 2015. View at Publisher · View at Google Scholar
  118. J. Kim, P. Sachdev, and K. Sidhu, “Alginate microcapsule as a 3D platform for the efficient differentiation of human embryonic stem cells to dopamine neurons,” Stem Cell Research, vol. 11, no. 3, pp. 978–989, 2013. View at Publisher · View at Google Scholar · View at Scopus
  119. A. M. Kloxin, A. M. Kasko, C. N. Salinas, and K. S. Anseth, “Photodegradable hydrogels for dynamic tuning of physical and chemical properties,” Science, vol. 324, no. 5923, pp. 59–63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. T. Mseka, J. R. Bamburg, and L. P. Cramer, “ADF/cofilin family proteins control formation of oriented actin-filament bundles in the cell body to trigger fibroblast polarization,” Journal of Cell Science, vol. 120, no. 24, pp. 4332–4344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  121. R. Xu, C. M. Nelson, J. L. Muschler, M. Veiseh, B. K. Vonderhaar, and M. J. Bissell, “Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function,” Journal of Cell Biology, vol. 184, no. 1, pp. 57–66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. J. T. Connelly, J. E. Gautrot, B. Trappmann et al., “Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions,” Nature Cell Biology, vol. 12, no. 7, pp. 711–718, 2010. View at Publisher · View at Google Scholar · View at Scopus
  123. L. Gao, R. McBeath, and C. S. Chen, “Stem cell shape regulates a chondrogenic versus myogenic fate through rac1 and N-cadherin,” Stem Cells, vol. 28, no. 3, pp. 564–572, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. K. A. Kilian, B. Bugarija, B. T. Lahn, and M. Mrksich, “Geometric cues for directing the differentiation of mesenchymal stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 11, pp. 4872–4877, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. M. Thé, V. Racine, M. Piel et al., “Anisotropy of cell adhesive microenvironment governs cell internal organization and orientation of polarity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 52, pp. 19771–19776, 2006. View at Publisher · View at Google Scholar · View at Scopus
  126. D. Lü, C. Luo, C. Zhang, Z. Li, and M. Long, “Differential regulation of morphology and stemness of mouse embryonic stem cells by substrate stiffness and topography,” Biomaterials, vol. 35, no. 13, pp. 3945–3955, 2014. View at Publisher · View at Google Scholar · View at Scopus
  127. H. Zhang, S. Dai, J. Bi, and K.-K. Liu, “Biomimetic three-dimensional microenvironment for controlling stem cell fate,” Interface Focus, vol. 1, no. 5, pp. 792–803, 2011. View at Publisher · View at Google Scholar · View at Scopus
  128. E. A. Cavalcanti-Adam, D. Aydin, V. C. Hirschfeld-Warneken, and J. P. Spatz, “Cell adhesion and response to synthetic nanopatterned environments by steering receptor clustering and spatial location,” HFSP Journal, vol. 2, no. 5, pp. 276–285, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. J. Huang, S. V. Gräter, F. Corbellini et al., “Impact of order and disorder in RGD nanopatterns on cell adhesion,” Nano Letters, vol. 9, no. 3, pp. 1111–1116, 2009. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Arnold, E. A. Cavalcanti-Adam, R. Glass et al., “Activation of integrin function by nanopatterned adhesive interfaces,” ChemPhysChem, vol. 5, no. 3, pp. 383–388, 2004. View at Publisher · View at Google Scholar · View at Scopus
  131. G. A. Silva, C. Czeisler, K. L. Niece et al., “Selective differentiation of neural progenitor cells by high-epitope density nanofibers,” Science, vol. 303, no. 5662, pp. 1352–1355, 2004. View at Publisher · View at Google Scholar · View at Scopus
  132. N. Huebsch, P. R. Arany, A. S. Mao et al., “Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate,” Nature Materials, vol. 9, no. 6, pp. 518–526, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. A. Shaw, V. Lundin, E. Petrova et al., “Spatial control of membrane receptor function using ligand nanocalipers,” Nature Methods, vol. 11, no. 8, pp. 841–846, 2014. View at Publisher · View at Google Scholar · View at Scopus
  134. M. Schvartzman, M. Palma, J. Sable et al., “Nanolithographic control of the spatial organization of cellular adhesion receptors at the single-molecule level,” Nano Letters, vol. 11, no. 3, pp. 1306–1312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  135. G. Maheshwari, G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith, “Cell adhesion and motility depend on nanoscale RGD clustering,” Journal of Cell Science, vol. 113, no. 10, pp. 1677–1686, 2000. View at Google Scholar · View at Scopus
  136. E. K. F. Yim, S. W. Pang, and K. W. Leong, “Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage,” Experimental Cell Research, vol. 313, no. 9, pp. 1820–1829, 2007. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Oh, K. S. Brammer, Y. S. J. Li et al., “Stem cell fate dictated solely by altered nanotube dimension,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 7, pp. 2130–2135, 2009. View at Publisher · View at Google Scholar · View at Scopus
  138. M. J. Dalby, N. Gadegaard, R. Tare et al., “The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder,” Nature Materials, vol. 6, no. 12, pp. 997–1003, 2007. View at Publisher · View at Google Scholar · View at Scopus
  139. E. Kingham, K. White, N. Gadegaard, M. J. Dalby, and R. O. C. Oreffo, “Nanotopographical cues augment mesenchymal differentiation of human embryonic stem cells,” Small, vol. 9, no. 12, pp. 2140–2151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  140. A. P. L. Kwan, C. E. Cummings, J. A. Chapman, and M. E. Grant, “Macromolecular organization of chicken type X collagen in vitro,” The Journal of Cell Biology, vol. 114, no. 3, pp. 597–604, 1991. View at Publisher · View at Google Scholar · View at Scopus
  141. R. J. McMurray, N. Gadegaard, P. M. Tsimbouri et al., “Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency,” Nature Materials, vol. 10, no. 8, pp. 637–644, 2011. View at Publisher · View at Google Scholar · View at Scopus
  142. R. K. Das, O. F. Zouani, C. Labrugère, R. Oda, and M.-C. Durrieu, “Influence of nanohelical shape and periodicity on stem cell fate,” ACS Nano, vol. 7, no. 4, pp. 3351–3361, 2013. View at Publisher · View at Google Scholar · View at Scopus
  143. R. O. Hynes, “Integrins: bidirectional, allosteric signaling machines,” Cell, vol. 110, no. 6, pp. 673–687, 2002. View at Publisher · View at Google Scholar · View at Scopus
  144. Y. Oikawa, J. Hansson, T. Sasaki et al., “Melanoma cells produce multiple laminin isoforms and strongly migrate on α5 laminin(s) via several integrin receptors,” Experimental Cell Research, vol. 317, no. 8, pp. 1119–1133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  145. M. Aumailley and B. Gayraud, “Structure and biological activity of the extracellular matrix,” Journal of Molecular Medicine, vol. 76, no. 3-4, pp. 253–265, 1998. View at Publisher · View at Google Scholar · View at Scopus
  146. A. Naba, K. R. Clauser, S. Hoersch, H. Liu, S. A. Carr, and R. O. Hynes, “The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices,” Molecular & Cellular Proteomics, vol. 11, no. 4, Article ID M111.014647, 2012. View at Publisher · View at Google Scholar · View at Scopus
  147. E. Pöschl, U. Schlötzer-Schrehardt, B. Brachvogel, K. Saito, Y. Ninomiya, and U. Mayer, “Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development,” Development, vol. 131, no. 7, pp. 1619–1628, 2004. View at Publisher · View at Google Scholar · View at Scopus
  148. S. Li, P. Liquari, K. K. McKee et al., “Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts,” Journal of Cell Biology, vol. 169, no. 1, pp. 179–189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  149. S. R. Braam, L. Zeinstra, S. Litjens et al., “Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via αVβ5 integrin,” Stem Cells, vol. 26, no. 9, pp. 2257–2265, 2008. View at Publisher · View at Google Scholar · View at Scopus
  150. T. E. Ludwig, M. E. Levenstein, J. M. Jones et al., “Derivation of human embryonic stem cells in defined conditions,” Nature Biotechnology, vol. 24, no. 2, pp. 185–187, 2006. View at Publisher · View at Google Scholar · View at Scopus
  151. A. Domogatskaya, S. Rodin, A. Boutaud, and K. Tryggvason, “Laminin-511 but not -332, -111, or -411 enables mouse embryonic stem cell self-renewal in vitro,” Stem Cells, vol. 26, no. 11, pp. 2800–2809, 2008. View at Publisher · View at Google Scholar · View at Scopus
  152. S. Rodin, A. Domogatskaya, S. Ström et al., “Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511,” Nature Biotechnology, vol. 28, no. 6, pp. 611–615, 2010. View at Publisher · View at Google Scholar · View at Scopus
  153. S. Rodin, L. Antonsson, C. Niaudet et al., “Clonal culturing of human embryonic stem cells on laminin-521/E-cadherin matrix in defined and xeno-free environment,” Nature Communications, vol. 5, article 3195, 2014. View at Publisher · View at Google Scholar · View at Scopus
  154. E. Klaffky, R. Williams, C.-C. Yao, B. Ziober, R. Kramer, and A. Sutherland, “Trophoblast-specific expression and function of the integrin α7 subunit in the peri-implantation mouse embryo,” Developmental Biology, vol. 239, no. 1, pp. 161–175, 2001. View at Publisher · View at Google Scholar · View at Scopus
  155. D. Evseenko, K. Schenke-Layland, G. Dravid et al., “Identification of the critical extracellular matrix proteins that promote human embryonic stem cell assembly,” Stem Cells and Development, vol. 18, no. 6, pp. 919–927, 2009. View at Publisher · View at Google Scholar · View at Scopus
  156. D. Stenzel, C. A. Franco, S. Estrach et al., “Endothelial basement membrane limits tip cell formation by inducing Dll4/Notch signalling in vivo,” EMBO Reports, vol. 12, no. 11, pp. 1135–1143, 2011. View at Publisher · View at Google Scholar · View at Scopus
  157. G. Nikolova, N. Jabs, I. Konstantinova et al., “The vascular basement membrane: a niche for insulin gene expression and β cell proliferation,” Developmental Cell, vol. 10, no. 3, pp. 397–405, 2006. View at Publisher · View at Google Scholar · View at Scopus
  158. Z.-L. Chen, J. A. Indyk, and S. Strickland, “The hippocampal laminin matrix is dynamic and critical for neuronal survival,” Molecular Biology of the Cell, vol. 14, no. 7, pp. 2665–2676, 2003. View at Publisher · View at Google Scholar · View at Scopus
  159. W. Wallquist, S. Plantman, S. Thams et al., “Impeded interaction between Schwann cells and axons in the absence of laminin alpha4,” The Journal of Neuroscience, vol. 25, no. 14, pp. 3692–3700, 2005. View at Publisher · View at Google Scholar · View at Scopus
  160. S. Plantman, M. Patarroyo, K. Fried et al., “Integrin-laminin interactions controlling neurite outgrowth from adult DRG neurons in vitro,” Molecular and Cellular Neuroscience, vol. 39, no. 1, pp. 50–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  161. S. Li, D. Harrison, S. Carbonetto et al., “Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation,” Journal of Cell Biology, vol. 157, no. 7, pp. 1279–1290, 2002. View at Publisher · View at Google Scholar · View at Scopus
  162. S. Li, D. Edgar, R. Fässler, W. Wadsworth, and P. D. Yurchenco, “The role of laminin in embryonic cell polarization and tissue organization,” Developmental Cell, vol. 4, no. 5, pp. 613–624, 2003. View at Publisher · View at Google Scholar · View at Scopus
  163. L. Li, E. Arman, P. Ekblom, D. Edgar, P. Murray, and P. Lonai, “Distinct GATA6- and laminin-dependent mechanisms regulate endodermal and ectodermal embryonic stem cell fates,” Development, vol. 131, no. 21, pp. 5277–5286, 2004. View at Publisher · View at Google Scholar · View at Scopus
  164. K. Guan, F. Wolf, A. Becker, W. Engel, K. Nayernia, and G. Hasenfuss, “Isolation and cultivation of stem cells from adult mouse testes,” Nature Protocols, vol. 4, no. 2, pp. 143–154, 2009. View at Publisher · View at Google Scholar · View at Scopus
  165. Y. Gu, L. Sorokin, M. Durbeej, T. Hjalt, J.-I. Jönsson, and M. Ekblom, “Characterization of bone marrow laminins and identification of α5-containing laminins as adhesive proteins for multipotent hematopoietic FDCP-Mix cells,” Blood, vol. 93, no. 8, pp. 2533–2542, 1999. View at Google Scholar · View at Scopus
  166. U. Siler, M. Seiffert, S. Puch et al., “Characterization and functional analysis of laminin isoforms in human bone marrow,” Blood, vol. 96, no. 13, pp. 4194–4203, 2000. View at Google Scholar · View at Scopus
  167. Y.-C. Gu, J. Kortesmaa, K. Tryggvason et al., “Laminin isoform-specific promotion of adhesion and migration of human bone marrow progenitor cells,” Blood, vol. 101, no. 3, pp. 877–885, 2003. View at Publisher · View at Google Scholar · View at Scopus
  168. H. Qian, K. Tryggvason, S. E. Jacobsen, and M. Ekblom, “Contribution of α6 integrins to hematopoietic stem and progenitor cell homing to bone marrow and collaboration with α4 integrins,” Blood, vol. 107, no. 9, pp. 3503–3510, 2006. View at Publisher · View at Google Scholar · View at Scopus
  169. N. S. Astrof, A. Salas, M. Shimaoka, J. Chen, and T. A. Springer, “Importance of force linkage in mechanochemistry of adhesion receptors,” Biochemistry, vol. 45, no. 50, pp. 15020–15028, 2006. View at Publisher · View at Google Scholar · View at Scopus
  170. D. Telci, Z. Wang, X. Li et al., “Fibronectin-tissue transglutaminase matrix rescues RGD-impaired cell adhesion through syndecan-4 and beta1 integrin co-signaling,” The Journal of Biological Chemistry, vol. 283, no. 30, pp. 20937–20947, 2008. View at Publisher · View at Google Scholar · View at Scopus
  171. P. R. Somanath, N. L. Malinin, and T. V. Byzova, “Cooperation between integrin αvβ3 and VEGFR2 in angiogenesis,” Angiogenesis, vol. 12, no. 2, pp. 177–185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  172. J. Heino and J. Käpylä, “Cellular receptors of extracellular matrix molecules,” Current Pharmaceutical Design, vol. 15, no. 12, pp. 1309–1317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  173. T. Miyazaki, S. Futaki, H. Suemori et al., “Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells,” Nature Communications, vol. 3, article 1236, 2012. View at Publisher · View at Google Scholar · View at Scopus
  174. K. Watanabe, M. Ueno, D. Kamiya et al., “A ROCK inhibitor permits survival of dissociated human embryonic stem cells,” Nature Biotechnology, vol. 25, no. 6, pp. 681–686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  175. M. P. Marinkovich, “Tumour microenvironment: laminin 332 in squamous-cell carcinoma,” Nature Reviews Cancer, vol. 7, no. 5, pp. 370–380, 2007. View at Publisher · View at Google Scholar · View at Scopus
  176. S. Schéele, M. Falk, A. Franzén et al., “Laminin alpha1 globular domains 4-5 induce fetal development but are not vital for embryonic basement membrane assembly,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 5, pp. 1502–1506, 2005. View at Publisher · View at Google Scholar · View at Scopus
  177. K. M. Malinda, M. Nomizu, M. Chung et al., “Identification of laminin α1 and β1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting,” The FASEB Journal, vol. 13, no. 1, pp. 53–62, 1999. View at Google Scholar · View at Scopus
  178. S. Rodin, L. Antonsson, O. Hovatta, and K. Tryggvason, “Monolayer culturing and cloning of human pluripotent stem cells on laminin-521–based matrices under xeno-free and chemically defined conditions,” Nature Protocols, vol. 9, no. 10, pp. 2354–2368, 2014. View at Publisher · View at Google Scholar
  179. Z. Wondimu, G. Gorfu, T. Kawataki et al., “Characterization of commercial laminin preparations from human placenta in comparison to recombinant laminins 2 (alpha2beta1gamma1), 8 (alpha4beta1gamma1), 10 (alpha5beta1gamma1),” Matrix Biology, vol. 25, no. 2, pp. 89–93, 2006. View at Google Scholar
  180. Y. Feng and M. Mrksich, “The synergy peptide PHSRN and the adhesion peptide RGD mediate cell adhesion through a common mechanism,” Biochemistry, vol. 43, no. 50, pp. 15811–15821, 2004. View at Publisher · View at Google Scholar · View at Scopus
  181. J. Wang, L. Wang, X. Li, and C. Mao, “Virus activated artificial ECM induces the osteoblastic differentiation of mesenchymal stem cells without osteogenic supplements,” Scientific Reports, vol. 3, article 1242, 2013. View at Publisher · View at Google Scholar · View at Scopus
  182. J. Ivaska and J. Heino, “Cooperation between integrins and growth factor receptors in signaling and endocytosis,” Annual Review of Cell and Developmental Biology, vol. 27, pp. 291–320, 2011. View at Publisher · View at Google Scholar · View at Scopus
  183. G. Chen, Z. Hou, D. R. Gulbranson, and J. A. Thomson, “Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells,” Cell Stem Cell, vol. 7, no. 2, pp. 240–248, 2010. View at Publisher · View at Google Scholar · View at Scopus
  184. P. G. Noakes, M. Gautam, J. Mudd, J. R. Sanes, and J. P. Merlie, “Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2,” Nature, vol. 374, no. 6519, pp. 258–262, 1995. View at Publisher · View at Google Scholar · View at Scopus
  185. B. L. Patton, A. Y. Chiu, and J. R. Sanes, “Synaptic laminin prevents glial entry into the synaptic cleft,” Nature, vol. 393, no. 6686, pp. 698–701, 1998. View at Publisher · View at Google Scholar · View at Scopus
  186. M. F. Brizzi, G. Tarone, and P. Defilippi, “Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche,” Current Opinion in Cell Biology, vol. 24, no. 5, pp. 645–651, 2012. View at Publisher · View at Google Scholar · View at Scopus
  187. P. D. Yurchenco and Y.-S. Cheng, “Self-assembly and calcium-binding sites in laminin. A three-arm interaction model,” Journal of Biological Chemistry, vol. 268, no. 23, pp. 17286–17299, 1993. View at Google Scholar · View at Scopus
  188. U. Odenthal, S. Haehn, P. Tunggal et al., “Molecular analysis of laminin N-terminal domains mediating self-interactions,” The Journal of Biological Chemistry, vol. 279, no. 43, pp. 44504–44512, 2004. View at Publisher · View at Google Scholar · View at Scopus
  189. C. J. Flaim, S. Chien, and S. N. Bhatia, “An extracellular matrix microarray for probing cellular differentiation,” Nature Methods, vol. 2, no. 2, pp. 119–125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  190. S. Ding and P. G. Schultz, “A role for chemistry in stem cell biology,” Nature Biotechnology, vol. 22, no. 7, pp. 833–840, 2004. View at Publisher · View at Google Scholar · View at Scopus
  191. S. Gobaa, S. Hoehnel, M. Roccio, A. Negro, S. Kobel, and M. P. Lutolf, “Artificial niche microarrays for probing single stem cell fate in high throughput,” Nature Methods, vol. 8, no. 11, pp. 949–955, 2011. View at Publisher · View at Google Scholar · View at Scopus
  192. J. Lee, A. A. Abdeen, D. Zhang, and K. A. Kilian, “Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition,” Biomaterials, vol. 34, no. 33, pp. 8140–8148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  193. Y. Soen, A. Mori, T. D. Palmer, and P. O. Brown, “Exploring the regulation of human neural precursor cell differentiation using arrays of signaling microenvironments,” Molecular Systems Biology, vol. 2, article 37, 2006. View at Publisher · View at Google Scholar · View at Scopus