Context clues: The importance of stem cell-material interactions

ACS Chemical Biology

Volumn 9, Issue 1, 2014, Pages 45-56

  Khalil, Andrew S ^a   Xie, Angela W ^a   Murphy, William L ^a,b  

^a Wisconsin Electric Machines and Power Electronics Consortium   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Biologically driven assembly; Cell material adhesion; Embryoid body; Growth factor sequestering; Mechanotransduction; Stem cell biology; Stem cell microenvironment; Tissue morphogenesis

Indexed keywords

GROWTH FACTOR;

BIOENGINEERING; CELL ADHESION; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL MATERIAL INTERACTION; IN VITRO STUDY; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL ADHESION; CELL DIFFERENTIATION; HUMANS; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELLS; TISSUE ENGINEERING;

EID: 84900447541     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400801m     Document Type: Review

References (111)

1. Thomson, J. A., Itskovitz-Eldor, J., and Shapiro, S. (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
2. Zhang, J., Klos, M., Wilson, G. F., and Herman., A. M., Lian, X., Raval, K. K., and Barron., M. R., Hou, L., Soerens, A. G., Yu, J., and Palecek., S. P., Lyons, G. E., Thomson, J. A., and Herron., T. J., Jalife, J., and Kamp, T. J. (2012) Extracellular matrix promotes highly efficient cardiac differentiation of human pluripotent stem cells: the matrix sandwich method. Circ. Res. 111, 1125-1136.
3. Lian, X., Zhang, J., Azarin, S. M., Zhu, K., and Hazeltine., L. B., Bao, X., Hsiao, C., Kamp, T. J., and Palecek, S. P. (2013) Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat. Protoc. 8, 162-175.
4. Lian, X., Hsiao, C., Wilson, G., Zhu, K., and Hazeltine., L. B., Azarin, S. M., Raval, K. K., Zhang, J., and Kamp., T. J., and Palecek, S. P. (2012) Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. U.S.A. 109, E1848-1857.
5. Van Hoof, D., D'Amour, K. A., and German, M. S. (2009) Derivation of insulin-producing cells from human embryonic stem cells. Stem Cell Res. 3, 73-87.
6. Nelson, C. M., and Bissell, M. J. (2005) Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin. Cancer Biol. 15, 342-352.
7. Weaver, V. M., Lelievre, S., Lakins, J. N., and Chrenek., M. A., Jones, J. C. R., Giancotti, F., Werb, Z., and Bissell, M. J. (2002) Beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2, 205-216.
8. Weaver, V. M., and Howlett., A. R., Langton-Webster, B., Petersen, O. W., and Bissell, M. J. (1995) The development of a functionally relevant cell culture model of progressive human breast cancer. Semin. Cancer Biol. 6, 175-184.
9. Barcellos-Hoff, M. H., Aggeler, J., Ram, T. G., and Bissell, M. J. (1989) Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105, 223-235.
10. Bissell, M. J., and Hall., H. G., and Parry, G. (1982) How does the extracellular matrix direct gene expression? J. Theor. Biol. 99, 31-68.
11. Petersen, O. W., Rønnov-Jessen, L., Howlett, A. R., and Bissell, M. J. (1992) Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 89, 9064-9068.
12. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., and Sasai, Y. (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532.
13. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., and Sasai, Y. (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56.
14. Ng, E. S., and Davis., R. P., Azzola, L., Stanley, E. G., and Elefanty, A. G. (2005) Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106, 1601-1603.
15. Mohr, J. C., Zhang, J., Azarin, S. M., and Soerens., A. G., de Pablo, J. J., Thomson, J. A, Lyons, G. E., Palecek, S. P., and Kamp, T. J. (2010) The microwell control of embryoid body size in order to regulate cardiac differentiation of human embryonic stem cells. Biomaterials 31, 1885-1893.
16. Hwang, Y.-S., Chung, B. G., Ortmann, D., Hattori, N., Moeller, H.-C., and Khademhosseini, A. (2009) 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. 106, 16978-16983.
17. Schukur, L., Zorlutuna, P., Cha, J. M., Bae, H., and Khademhosseini, A. (2013) Directed differentiation of size-controlled embryoid bodies towards endothelial and cardiac lineages in RGD-modified poly(ethylene glycol) hydrogels. Adv. Healthcare Mater. 2, 195-205.
18. Azarin, S. M., and Larson., E. A., Almodovar-Cruz, J. M., de Pablo, J. J., and Palecek, S. P. (2012) Effects of 3D microwell culture on growth kinetics and metabolism of human embryonic stem cells. Biotechnol. Appl. Biochem. 59, 88-96.
19. Azarin, S. M., Lian, X., Larson, E. A., and Popelka., H. M., de Pablo, J. J., and Palecek, S. P. (2012) Modulation of Wnt/β-catenin signaling in human embryonic stem cells using a 3-D microwell array. Biomaterials 33, 2041-2049.
20. Park, J., and Cho., C. H., Parashurama, N., Li, Y., Berthiaume, F., Toner, M., Tilles, A. W., and Yarmush, M. L. (2007) Microfabrication-based modulation of embryonic stem cell differentiation. Lab Chip 7, 1018-1028.
21. Choi, Y. Y., and Chung., B. G., Lee, D. H., Khademhosseini, A., Kim, J.-H., and Lee, S.-H. (2010) Controlled-size embryoid body formation in concave microwell arrays. Biomaterials 31, 4296-4303.
22. Khetan, S., Guvendiren, M., Legant, W. R., and 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.
23. Anderson, S. B., Lin, C.-C., Kuntzler, D. V, and Anseth, K. S. (2011) The performance of human mesenchymal stem cells encapsulated in cell-degradable polymer-peptide hydrogels. Biomaterials 32, 3564-3574.
24. Kharkar, P. M., and Kiick., K. L., and Kloxin, A. M. (2013) Designing degradable hydrogels for orthogonal control of cell microenvironments. Chem. Soc. Rev. 42, 7335-7372.
25. Bratt-Leal, A. M., Carpenedo, R. L., and Ungrin., M. D., Zandstra, P. W., and McDevitt, T. C. (2011) Incorporation of biomaterials in multicellular aggregates modulates pluripotent stem cell differentiation. Biomaterials 32, 48-56.
26. Carpenedo, R. L., Bratt-Leal, A. M., Marklein, R. A., Seaman, S. A., Bowen, N. J., McDonald, J. F., and McDevitt, T. C. (2009) Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules. Biomaterials 30, 2507-2515.
27. Trappmann, B., and Gautrot., J. E., Connelly, J. T., Strange, D. G. T., Li, Y., Oyen, M. L., Cohen Stuart, M. A., Boehm, H., Li, B., Vogel, V., Spatz, J. P., Watt, F. M., and Huck, W. T. S. (2012) Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11, 642-649.
28. 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. 51, 4891-4895.
29. Dalby, M. J., Gadegaard, N., Tare, R., Andar, A., and Riehle., M. O., Herzyk, P., Wilkinson, C. D. W., and Oreffo, R. O. C. (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 6, 997-1003.
30. Frith, J., Mills, R., and Cooper-White, J. (2012) Lateral spacing of adhesion peptides influences human mesenchymal stem cell behaviour. J. Cell Sci., 317-327.
31. 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.
32. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
33. Humphries, M. J. (1990) The molecular basis and specificity of integrin-ligand interactions. J. Cell Sci. 97, 585-592.
34. Ivaska, J., and Heino, J. (2011) Cooperation between integrins and growth factor receptors in signaling and endocytosis. Annu. Rev. Cell Dev. Biol. 27, 291-320.
35. Yamada, K. M., and Even-Ram, S. (2002) Integrin regulation of growth factor signalling and adhesion. Nat. Cell Biol. 4, 75-76.
36. Caswell, P. T., Vadrevu, S., and Norman, J. C. (2009) Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10, 843-853.
37. Liang, C. C., and Chen, H. C. (2001) Sustained activation of extracellular signal-regulated kinase stimulated by hepatocyte growth factor leads to integrin alpha 2 expression that is involved in cell scattering. J. Biol. Chem. 276, 21146-21152.
38. Hermanto, U., and Zong., C. S., Li, W., and Wang, L. (2002) RACK1, an insulin-like growth factor I, modulates IGF-I-dependent integrin signaling and promotes cell spreading and contact with extracellular matrix. Mol. Cell. Biol. 22, 2345-2365.
39. Dalton, S. L. (1999) Transforming growth factor-beta overrides the adhesion requirement for surface expression of alpha5beta1 integrin in normal rat kidney fibroblasts. A necessary effect for induction of anchorage-independent growth. J. Biol. Chem. 274, 30139-30145.
40. Lynch, L., and Vodyanik., P. I., Boettiger, D., and Guvakova, M. A. (2005) Insulin-like growth factor I controls adhesion strength mediated by alpha5beta1integrins in motile carcinoma cells. Mol. Cell. Biol. 16, 51-63.
41. Tamura, Y., Takeuchi, Y., Suzawa, M., Fukumoto, S., Kato, M., Miyazono, K., and Fujita, T. (2001) Focal adhesion kinase activity is required for bone morphogenetic protein-Smad1 signaling and osteoblastic differentiation in murine MC3T3-E1 cells. J. Bone Miner. Res. 16, 1772-1779.
42. Suzawa, M., Tamura, Y., Fukumoto, S., Miyazono, K., Fujita, T., Kato, S., and Takeuchi, Y. (2002) Stimulation of Smad1 transcriptional activity by Ras-extracellular signal-regulated kinase pathway: a possible mechanism for collagen-dependent osteoblastic differentiation. J. Bone Miner. Res. 17, 240-248.
43. Mu, D., Cambier, S., Fjellbirkeland, L., Baron, J. L., and Munger., J. S., Kawakatsu, H., Sheppard, D., Broaddus, V. C., and Nishimura, S. L. (2002) The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 157, 493-507.
44. Munger, J. S., Huang, X., Kawakatsu, H., Griffiths, M. J., and Dalton., S. L., Wu, J., Pittet, J. F., Kaminski, N., Garat, C., Matthay, M. A., and Rifkin., D. B., and Sheppard, D. (1999) The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96, 319-328.
45. Soldi, R., Mitola, S., Strasly, M., and Defilippi, P. (1999) Role of αvβ3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 18, 882-892.
46. Borges, E., Jan, Y., and Ruoslahti, E. (2000) Platelet-derived growth factor receptor beta and vascular endothelial growth factor receptor 2 bind to the beta 3 integrin through its extracellular domain. J. Biol. Chem. 275, 39867-39873.
47. Koepsel, J. T., and Brown., P. T., Loveland, S. G., Li, W., and Murphy, W. L. (2012) Combinatorial screening of chemically defined human mesenchymal stem cell culture substrates. J. Mater. Chem., 19474-19481.
48. Koepsel, J. T., and Nguyen., E. H., and Murphy, W. L. (2012) Differential effects of a soluble or immobilized VEGFR-binding peptide. Integr. Biol. 4, 914-924.
49. Mahabeleshwar, G. H., Feng, W., Reddy, K., Plow, E. F., and Byzova, T. V. (2007) Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res. 101, 570-580.
50. Byzova, T. V., and Goldman., C. K., Pampori, N., Thomas, K. A., Bett, A., and Shattil., S. J., and Plow, E. F. (2000) A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol. Cell 6, 851-860.
51. Provenzano, P. P., and Keely, P. J. (2011) Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J. Cell Sci. 124, 1195-1205.
52. Pathak, A., and Kumar, S. (2011) Biophysical regulation of tumor cell invasion: moving beyond matrix stiffness. Integr. Biol. 3, 267-278.
53. Ulrich, T. A., Jain, A., Tanner, K., MacKay, J. L., and Kumar, S. (2010) Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices. Biomaterials 31, 1875-1884.
54. Provenzano, P. P., and Inman., D. R., Eliceiri, K. W., and Keely, P. J. (2009) Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28, 4326-4343.
55. Paszek, M. J., and Weaver, V. M. (2004) The tension mounts: mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia 9, 325-342.
56. Wang, N., and Tytell., J. D., and Ingber, D. E. (2009) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82.
57. Engler, A. J., Sen, S., Sweeney, H. L., and Discher, D. E. (2006) Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689.
58. Rudnicki, M. A., and Schnegelsberg., P. N., Stead, R. H., Braun, T., Arnold, H. H., and Jaenisch, R. (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
59. Von Maltzahn, J., Chang, N. C., and Bentzinger., C. F., and Rudnicki, M. A. (2012) Wnt signaling in myogenesis. Trends Cell Biol. 22, 602-609.
60. Gaur, T., and Lengner., C. J., Hovhannisyan, H., Bhat, R. A., Bodine, P. V. N., Komm, B. S., Javed, A., van Wijnen, A. J., Stein, J. L., Stein, G. S., and Lian, J. B. (2005) Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J. Biol. Chem. 280, 33132-33140.
61. Gilbert, P. M., and Havenstrite., K. L., Magnusson, K. E. G., Sacco, A., Leonardi, N. A., Kraft, P., and Nguyen., N. K., Thrun, S., Lutolf, M. P., and Blau, H. M. (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081.
62. Park, J. S., and Chu., J. S., Tsou, A. D., Diop, R., Tang, Z., Wang, A., and Li, S. (2011) The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β. Biomaterials 32, 3921-3930.
63. Parekh, S. H., Chatterjee, K., Lin-Gibson, S., Moore, N. M., and Cicerone., M. T., Young, M. F., and Simon, C. G. (2011) Modulus-driven differentiation of marrow stromal cells in 3D scaffolds that is independent of myosin-based cytoskeletal tension. Biomaterials 32, 2256-2264.
64. Pek, Y. S., Wan, A. C. A., and Ying, J. Y. (2010) The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 31, 385-391.
65. Shih, Y.-R. V., Tseng, K.-F., Lai, H.-Y., Lin, C.-H., and Lee, O. K. (2011) Matrix stiffness regulation of integrin-mediated mechano-transduction during osteogenic differentiation of human mesenchymal stem cells. J. Bone Miner. Res. 26, 730-738.
66. Saha, K., and Keung., A. J., Irwin, E. F., Li, Y., Little, L., Schaffer, D. V, and Healy, K. E. (2008) Substrate modulus directs neural stem cell behavior. Biophys. J. 95, 4426-4438.
67. Huebsch, N., and Arany., P. R., Mao, A. S., Shvartsman, D., Ali, O. A., and Bencherif., S. A., Rivera-Feliciano, J., and Mooney, D. J. (2010) Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9, 518-526.
68. Musah, S., Morin, S., Wrighton, P., and Zwick, D. (2012) Glycosaminoglycan-binding hydrogels enable mechanical control of human pluripotent stem cell self-renewal. ACS Nano 6, 10168-10177.
69. McMurray, R. J., Gadegaard, N., Tsimbouri, P. M., Burgess, K. V, McNamara, L. E., Tare, R., Murawski, K., Kingham, E., Oreffo, R. O. C., and Dalby, M. J. (2011) Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat. Mater. 10, 637-644.
70. McBeath, R., and 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.
71. Lee, J., Abdeen, A. a, Zhang, D., and Kilian, K. A. (2013) Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition. Biomaterials 34, 8140-8148.
72. Bhatia, S. N., and Balis., U. J., Yarmush, M. L., and Toner, M. (1999) Effect of cell-cell interactions in preservation of cellular phenotype: cocultivation of hepatocytes and nonparenchymal cells. FASEB J. 13, 1883-1900.
73. Tang, J., Peng, R., and Ding, J. (2010) The regulation of stem cell differentiation by cell-cell contact on micropatterned material surfaces. Biomaterials 31, 2470-2476.
74. Mei, Y., Saha, K., Bogatyrev, S. R., Yang, J., and Hook., A. L., Kalcioglu, Z. I., Cho, S.-W., Mitalipova, M., Pyzocha, N., Rojas, F., Van Vliet, K. J., Davies, M. C., Alexander, M. R., Langer, R., Jaenisch, R., and Anderson, D. G. (2010) Combinatorial development of biomaterials for clonal growth of human pluripotent stem cells. Nat. Mater. 9, 768-778.
75. Yao, S., Liu, X., Wang, X., Merolli, A., Chen, X., and Cui, F. (2013) Directing neural stem cell fate with biomaterial parameters for injured brain regeneration. Prog. Nat. Sci. Mater. Int. 23, 103-112.
76. Nguyen, E. H., and Schwartz., M. P., and Murphy, W. L. (2011) Biomimetic approaches to control soluble concentration gradients in biomaterials. Macromol. Biosci. 11, 483-492.
77. Hudalla, G. A., and Murphy, W. L. (2011) Biomaterials that regulate growth factor activity via bioinspired interactions. Adv. Funct. Mater. 21, 1754-1768.
78. Hudalla, G., Koepsel, J., and Murphy, W. (2011) Surfaces that sequester serum borne-heparin amplify growth factor activity. Adv. Mater., 5415-5418.
79. Cai, S., Liu, Y., Zheng Shu, X., and Prestwich, G. D. (2005) Injectable glycosaminoglycan hydrogels for controlled release of human basic fibroblast growth factor. Biomaterials 26, 6054-6067.
80. Benoit, D. S. W., and Anseth, K. S. (2005) Heparin functionalized PEG gels that modulate protein adsorption for hMSC adhesion and differentiation. Acta Biomater. 1, 461-470.
81. Masters, K. S., and Shah., D. N., Walker, G., Leinwand, L. A., and Anseth, K. S. (2004) Designing scaffolds for valvular interstitial cells: cell adhesion and function on naturally derived materials. J. Biomed. Mater. Res. A 71, 172-180.
82. Halstenberg, S., Panitch, A., Rizzi, S., Hall, H., and Hubbell, J. A. (2002) Biologically engineered protein-graft-poly(ethylene glycol) hydrogels: a cell adhesive and plasmin-degradable biosynthetic material for tissue repair. Biomacromolecules 3, 710-723.
83. Shu, X. Z., Liu, Y., Luo, Y., Roberts, M. C., and Prestwich, G. D. (2002) Disulfide cross-linked hyaluronan hydrogels. Biomacromolecules 3, 1304-1311.
84. Yamamoto, M., Ikada, Y., and Tabata, Y. (2001) Controlled release of growth factors based on biodegradation of gelatin hydrogel. J. Biomater. Sci. Polym. Ed. 12, 77-88.
85. Luo, Y., and Kirker., K. R., and Prestwich, G. D. (2000) Cross-linked hyaluronic acid hydrogel films: new biomaterials for drug delivery. J. Controlled Release 69, 169-184.
86. Bulpitt, P., and Aeschlimann, D. (1999) New strategy for chemical modification of hyaluronic acid: preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J. Biomed. Mater. Res. 47, 152-169.
87. Prestwich, G. D., and Marecak., D. M., Marecek, J. F., Vercruysse, K. P., and Ziebell, M. R. (1998) Controlled chemical modification of hyaluronic acid: synthesis, applications, and biodegradation of hydrazide derivatives. J. Controlled Release 53, 93-103.
88. Roghani, M., Mansukhani, A., Dell'Era, P., Bellosta, P., Basilico, C., Rifkin, D. B., and Moscatelli, D. (1994) Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J. Biol. Chem. 269, 3976-3984.
89. Martino, M. M., and Hubbell, J. A. (2010) The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J. 24, 4711-4721.
90. Winterton, L. C., and Andrade., J. D., Feijen, J., and Kim, S. W. (1986) Heparin interaction with protein-adsorbed surfaces. J. Colloid Interface Sci. 111, 314-342.
91. Mohammed, J. S., and Murphy, W. L. (2009) Bioinspired design of dynamic materials. Adv. Mater. 21, 2361-2374.
92. Nie, T., Baldwin, A., Yamaguchi, N., and Kiick, K. L. (2007) Production of heparin-functionalized hydrogels for the development of responsive and controlled growth factor delivery systems. J. Controlled Release 122, 287-296.
93. Hudalla, G. A., and Kouris., N. A., Koepsel, J. T., Ogle, B. M., and Murphy, W. L. (2011) Harnessing endogenous growth factor activity modulates stem cell behavior. Integr. Biol. 3, 832-842.
94. Klim, J. R., Li, L., Wrighton, P. J., and Piekarczyk., M. S., and Kiessling, L. L. (2010) A defined glycosaminoglycan-binding substratum for human pluripotent stem cells. Nat. Methods 7, 989-994.
95. Belair, D. G., and Murphy, W. L. (2013) Specific VEGF sequestering to biomaterials: Influence of serum stability. Acta Biomater. 9, 8823-8831.
96. Impellitteri, N. A., and Toepke., M. W., Lan Levengood, S. K., and Murphy, W. L. (2012) Specific VEGF sequestering and release using peptide-functionalized hydrogel microspheres. Biomaterials 33, 3475-3484.
97. Toepke, M. W., and Impellitteri., N. A., Lan Levengood, S. K., Boeldt, D. S., Bird, I. M., and Murphy, W. L. (2012) Regulating specific growth factor signaling using immobilized branched ligands. Adv. Healthcare Mater. 1, 457-460.
98. Gandavarapu, N. R., and Mariner P. D., Schwartz, M. P., and Anseth, K. S. (2013) Extracellular matrix protein adsorption to phosphate-functionalized gels from serum promotes osteogenic differentiation of human mesenchymal stem cells. Acta Biomater. 9, 4525-4534.
99. Benoit, D. S. W., and 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.
100. Zhang, Y. S., Sevilla, A., Wan, L. Q., and Lemischka., I. R., and Vunjak-Novakovic, G. (2013) Patterning pluripotency in embryonic stem cells. Stem Cells 31, 1806-1815.
101. Van Winkle, A. P., Gates, I. D., and Kallos, M. S. (2012) Mass transfer limitations in embryoid bodies during human embryonic stem cell differentiation. Cells Tissues Organs 196, 34-47.
102. Ferreira, L., Squier, T., Park, H., Choe, H., and Kohane., D. S., and Langer, R. (2008) Human embryoid bodies containing nano- and microparticulate delivery vehicles. Adv. Mater. 20, 2285-2291.
103. Carpenedo, R. L., and Seaman., S. A., and McDevitt, T. C. (2010) Microsphere size effects on embryoid body incorporation and embryonic stem cell differentiation. J. Biomed. Mater. Res. A. 94, 466-475.
104. Purpura, K. A., Bratt-Leal, A. M., Hammersmith, K. A., McDevitt, T. C., and Zandstra, P. W. (2012) Systematic engineering of 3D pluripotent stem cell niches to guide blood development. Biomaterials 33, 1271-1280.
105. Burdick, J., and Murphy, W. (2012) Moving from static to dynamic complexity in hydrogel design. Nat. Commun. 3, 1-8.
106. Tibbitt, M. W., and Anseth, K. S. (2012) Dynamic microenvironments: the fourth dimension. Sci. Transl. Med. 4, 160ps24.
107. Mrksich, M., and Dike., L. E., Tien, J., Ingber, D. E., and Whitesides, G. M. (1997) Using microcontact printing to pattern the attachment of mammalian cells to self-assembled monolayers of alkanethiolates on transparent films of gold and silver. Exp. Cell Res. 235, 305-313.
108. 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.
109. Alom Ruiz, S., and Chen, C. S. (2007) Microcontact printing: A tool to pattern. Soft Matter 3, 168-177.
110. Bauwens, C. L., Peerani, R., Niebruegge, S., Woodhouse, K. A., Kumacheva, E., Husain, M., and Zandstra, P. W. (2008) Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26, 2300-2310.
111. Kong, H. J., and Polte., T. R., Alsberg, E., and Mooney, D. J. (2005) FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc. Natl. Acad. Sci. U.S.A. 102, 4300-4305.