Interplay of Matrix Stiffness and Cell-Cell Contact in Regulating Differentiation of Stem Cells

ACS Applied Materials and Interfaces

Volumn 8, Issue 34, 2016, Pages 21903-21913

  Ye, Kai ^a   Cao, Luping ^a   Li, Shiyu ^a   Yu, Lin ^a   Ding, Jiandong ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

cell density; cell cell contact; matrix stiffness; PEG hydrogel; RGD nanopattern; stem cell differentiation

Indexed keywords

AMINO ACIDS; CELL ADHESION; CELL CULTURE; CELLS; CYTOLOGY; HYDROGELS; POLYETHYLENE GLYCOLS; STEM CELLS; STIFFNESS; STIFFNESS MATRIX;

CELL DENSITY; CELL-CELL CONTACT; NANO PATTERN; PEG HYDROGEL; STEM CELL DIFFERENTIATION;

BIOMECHANICS;

BONE DEVELOPMENT; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; MESENCHYMAL STROMA CELL;

CELL ADHESION; CELL DIFFERENTIATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; HUMANS; HYDROGELS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS;

EID: 84985955322     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b09746     Document Type: Review

References (73)

1. Takahashi, K.; Yamanaka, S. Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors Cell 2006, 126, 663-676 10.1016/j.cell.2006.07.024
2. Daley, G. Q.; Scadden, D. T. Prospects for Stem Cell-Based Therapy Cell 2008, 132, 544-548 10.1016/j.cell.2008.02.009
3. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage Potential of Adult Human Mesenchymal Stem Cells Science 1999, 284, 143-147 10.1126/science.284.5411.143
4. Lutolf, M. P.; Gilbert, P. M.; Blau, H. M. Designing Materials to Direct Stem-Cell Fate Nature 2009, 462, 433-441 10.1038/nature08602
5. Jones, D. L.; Wagers, A. J. No Place Like Home: Anatomy and Function of the Stem Cell Niche Nat. Rev. Mol. Cell Biol. 2008, 9, 11-21 10.1038/nrm2319
6. Pan, Z.; Yan, C.; Peng, R.; Zhao, Y. C.; He, Y.; Ding, J. D. Control of Cell Nucleus Shapes via Micropillar Patterns Biomaterials 2012, 33, 1730-1735 10.1016/j.biomaterials.2011.11.023
7. Yao, X.; Peng, R.; Ding, J. D. Cell-Material Interactions Revealed via Material Techniques of Surface Patterning Adv. Mater. 2013, 25, 5257-5286 10.1002/adma.201301762
8. Bain, L. E.; Collazo, R.; Hsu, S. H.; Latham, N. P.; Manfra, M. J.; Ivanisevic, A. Surface Topography and Chemistry Shape Cellular Behavior on Wide Band-Gap Semiconductors Acta Biomater. 2014, 10, 2455-2462 10.1016/j.actbio.2014.02.038
9. Bellas, E.; Chen, C. S. Forms, Forces, and Stem Cell Fate Curr. Opin. Cell Biol. 2014, 31, 92-97 10.1016/j.ceb.2014.09.006
10. Benoit, D. S.; Schwartz, M. P.; Durney, A. R.; Anseth, K. S. Small Functional Groups for Controlled Differentiation of Hydrogel-Encapsulated Human Mesenchymal Stem Cells Nat. Mater. 2008, 7, 816-823 10.1038/nmat2269
11. Lee, J.; Abdeen, A. A.; Zhang, D.; Kilian, K. A. Directing Stem Cell Fate on Hydrogel Substrates by Controlling Cell Geometry, Matrix Mechanics and Adhesion Ligand Composition Biomaterials 2013, 34, 8140-8148 10.1016/j.biomaterials.2013.07.074
12. Dalby, M. J.; Gadegaard, N.; Tare, R.; Andar, A.; Riehle, M. O.; Herzyk, P.; Wilkinson, C. D.; Oreffo, R. O. The Control of Human Mesenchymal Cell Differentiation Using Nanoscale Symmetry and Disorder Nat. Mater. 2007, 6, 997-1003 10.1038/nmat2013
13. McMurray, R. J.; Gadegaard, N.; Tsimbouri, P. M.; Burgess, K. V.; McNamara, L. E.; Tare, R.; Murawski, K.; Kingham, E.; Oreffo, R. O. C.; Dalby, M. J. Nanoscale Surfaces for the Long-Term Maintenance of Mesenchymal Stem Cell Phenotype and Multipotency Nat. Mater. 2011, 10, 637-644 10.1038/nmat3058
14. Pan, Z.; Qu, Z. H.; Zhang, Z.; Peng, R.; Yan, C.; Ding, J. D. Particle-Collision and Porogen-Leaching Technique to Fabricate Polymeric Porous Scaffolds with Microscale Roughness of Interior Surfaces Chin. J. Polym. Sci. 2013, 31, 737-747 10.1007/s10118-013-1264-1
15. Wang, P. Y.; Bennetsen, D. T.; Foss, M.; Ameringer, T.; Thissen, H.; Kingshott, P. Modulation of Human Mesenchymal Stem Cell Behavior on Ordered Tantalum Nanotopographies Fabricated Using Colloidal Lithography and Glancing Angle Deposition ACS Appl. Mater. Interfaces 2015, 7, 4979-4989 10.1021/acsami.5b00107
16. Yao, X.; Hu, Y. W.; Cao, B.; Peng, R.; Ding, J. D. Effects of Surface Molecular Chirality on Adhesion and Differentiation of Stem Cells Biomaterials 2013, 34, 9001-9009 10.1016/j.biomaterials.2013.08.013
17. Chen, C. S.; Mrksich, M.; Huang, S.; Whitesides, G. M.; Ingber, D. E. Geometric Control of Cell Life and Death Science 1997, 276, 1425-1428 10.1126/science.276.5317.1425
18. Wang, X.; Li, S. Y.; Yan, C.; Liu, P.; Ding, J. D. Fabrication of RGD Micro/Nanopattern and Corresponding Study of Stem Cell Differentiation Nano Lett. 2015, 15, 1457-1467 10.1021/nl5049862
19. Peng, R.; Yao, X.; Ding, J. D. Effect of Cell Anisotropy on Differentiation of Stem Cells on Micropatterned Surfaces through the Controlled Single Cell Adhesion Biomaterials 2011, 32, 8048-8057 10.1016/j.biomaterials.2011.07.035
20. Yao, X.; Peng, R.; Ding, J. D. Effects of Aspect Ratios of Stem Cells on Lineage Commitments with and without Induction Media Biomaterials 2013, 34, 930-939 10.1016/j.biomaterials.2012.10.052
21. Tang, J.; Peng, R.; Ding, J. D. The Regulation of Stem Cell Differentiation by Cell-Cell Contact on Micropatterned Material Surfaces Biomaterials 2010, 31, 2470-2476 10.1016/j.biomaterials.2009.12.006
22. Peng, R.; Yao, X.; Cao, B.; Tang, J.; Ding, J. D. The Effect of Culture Conditions on the Adipogenic and Osteogenic Inductions of Mesenchymal Stem Cells on Micropatterned Surfaces Biomaterials 2012, 33, 6008-6019 10.1016/j.biomaterials.2012.05.010
23. Cao, B.; Li, Z. H.; Peng, R.; Ding, J. D. Effects of Cell-Cell Contact and Oxygen Tension on Chondrogenic Differentiation of Stem Cells Biomaterials 2015, 64, 21-32 10.1016/j.biomaterials.2015.06.018
24. McBeath, R.; Pirone, D. M.; Nelson, C. M.; Bhadriraju, K.; Chen, C. S. Cell Shape, Cytoskeletal Tension, and RhoA Regulate Stem Cell Lineage Commitment Dev. Cell 2004, 6, 483-495 10.1016/S1534-5807(04)00075-9
25. Pelham, R. J.; Wang, Y.-L. Cell Locomotion and Focal Adhesions Are Regulated by Substrate Flexibility Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 13661-13665 10.1073/pnas.94.25.13661
26. Liao, Y. C.; Ma, Y. T.; Huang, C. H.; Yu, J.; Hsiao, H. M. Rigidity Guided Cell Attachment on Inkjet-Printed Patterns ACS Appl. Mater. Interfaces 2012, 4, 3335-3339 10.1021/am300918s
27. Missirlis, D.; Spatz, J. P. Combined Effects of PEG Hydrogel Elasticity and Cell-Adhesive Coating on Fibroblast Adhesion and Persistent Migration Biomacromolecules 2014, 15, 195-205 10.1021/bm4014827
28. Engler, A.; Bacakova, L.; Newman, C.; Hategan, A.; Griffin, M.; Discher, D. Substrate Compliance versus Ligand Density in Cell on Gel Responses Biophys. J. 2004, 86, 617-628 10.1016/S0006-3495(04)74140-5
29. Chen, C.; Xie, J.; Deng, L. H.; Yang, L. Substrate Stiffness Together with Soluble Factors Affects Chondrocyte Mechanoresponses ACS Appl. Mater. Interfaces 2014, 6, 16106-16116 10.1021/am504135b
30. Chaudhuri, O.; Gu, L.; Darnell, M.; Klumpers, D.; Bencherif, S. A.; Weaver, J. C.; Huebsch, N.; Mooney, D. J. Substrate Stress Relaxation Regulates Cell Spreading Nat. Commun. 2015, 6, 6365 10.1038/ncomms7365
31. Lo, C. M.; Wang, H. B.; Dembo, M.; Wang, Y.-L. Cell Movement Is Guided by the Rigidity of the Substrate Biophys. J. 2000, 79, 144-152 10.1016/S0006-3495(00)76279-5
32. Tse, J. R.; Engler, A. J. Stiffness Gradients Mimicking In Vivo Tissue Variation Regulate Mesenchymal Stem Cell Fate PLoS One 2011, 6, e15978 10.1371/journal.pone.0015978
33. Banerjee, A.; Arha, M.; Choudhary, S.; Ashton, R. S.; Bhatia, S. R.; Schaffer, D. V.; Kane, R. S. The Influence of Hydrogel Modulus on the Proliferation and Differentiation of Encapsulated Neural Stem Cells Biomaterials 2009, 30, 4695-4699 10.1016/j.biomaterials.2009.05.050
34. Gilbert, P. M.; Havenstrite, K. L.; Magnusson, K. E.; Sacco, A.; Leonardi, N. A.; Kraft, P.; Nguyen, N. K.; Thrun, S.; Lutolf, M. P.; Blau, H. M. Substrate Elasticity Regulates Skeletal Muscle Stem Cell Self-Renewal in Culture Science 2010, 329, 1078-1081 10.1126/science.1191035
35. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix Elasticity Directs Stem Cell Lineage Specification Cell 2006, 126, 677-689 10.1016/j.cell.2006.06.044
36. Fu, J. P.; Wang, Y. K.; Yang, M. T.; Desai, R. A.; Yu, X. A.; Liu, Z. J.; Chen, C. S. Mechanical Regulation of Cell Function with Geometrically Modulated Elastomeric Substrates Nat. Methods 2010, 7, 733-736 10.1038/nmeth.1487
37. Huebsch, N.; Lippens, E.; Lee, K.; Mehta, M.; Koshy, S. T.; Darnell, M. C.; Desai, R. M.; Madl, C. M.; Xu, M.; Zhao, X. H.; Chaudhuri, O.; Verbeke, C.; Kim, W. S.; Alim, K.; Mammoto, A.; Ingber, D. E.; Duda, G. N.; Mooney, D. J. Matrix Elasticity of Void-Forming Hydrogels Controls Transplanted-Stem-Cell-Mediated Bone Formation Nat. Mater. 2015, 10.1038/nmat4407
38. Ye, K.; Wang, X.; Cao, L. P.; Li, S. Y.; Li, Z. H.; Yu, L.; Ding, J. D. Matrix Stiffness and Nanoscale Spatial Organization of Cell-Adhesive Ligands Direct Stem Cell Fate Nano Lett. 2015, 15, 4720-4729 10.1021/acs.nanolett.5b01619
39. Discher, D. E.; Janmey, P.; Wang, Y.-L. Tissue Cells Feel and Respond to the Stiffness of Their Substrate Science 2005, 310, 1139-1143 10.1126/science.1116995
40. Huebsch, N.; Arany, P. R.; Mao, A. S.; Shvartsman, D.; Ali, O. A.; Bencherif, S. A.; Rivera-Feliciano, J.; Mooney, D. J. Harnessing Traction-Mediated Manipulation of the Cell/Matrix Interface to Control Stem-Cell Fate Nat. Mater. 2010, 9, 518-526 10.1038/nmat2732
41. Wen, J. H.; Vincent, L. G.; Fuhrmann, A.; Choi, Y. S.; Hribar, K. C.; Taylor-Weiner, H.; Chen, S. C.; Engler, A. J. Interplay of Matrix Stiffness and Protein Tethering in Stem Cell Differentiation Nat. Mater. 2014, 13, 979-987 10.1038/nmat4051
42. Zhang, Z.; Ni, J.; Chen, L.; Yu, L.; Xu, J. W.; Ding, J. D. Biodegradable and Thermoreversible PCLA-PEG-PCLA Hydrogel as a Barrier for Prevention of Post-Operative Adhesion Biomaterials 2011, 32, 4725-4736 10.1016/j.biomaterials.2011.03.046
43. Wang, X.; Ye, K.; Li, Z. H.; Yan, C.; Ding, J. D. Adhesion, Proliferation, and Differentiation of Mesenchymal Stem Cells on RGD Nanopatterns of Varied Nanospacings Organogenesis 2013, 9, 280-286 10.4161/org.26080
44. Cao, B.; Peng, R.; Li, Z. H.; Ding, J. D. Effects of Spreading Areas and Aspect Ratios of Single Cells on Dedifferentiation of Chondrocytes Biomaterials 2014, 35, 6871-6881 10.1016/j.biomaterials.2014.04.107
45. Li, Z. H.; Cao, B.; Wang, X.; Ye, K.; Li, S. Y.; Ding, J. D. Effects of RGD Nanospacing on Chondrogenic Differentiation of Mesenchymal Stem Cells J. Mater. Chem. B 2015, 3, 5197-5209 10.1039/C5TB00455A
46. Lai, Y. X.; Xie, C.; Zhang, Z.; Lu, W. Y.; Ding, J. D. Design and Synthesis of a Potent Peptide Containing Both Specific and Non-Specific Cell-Adhesion Motifs Biomaterials 2010, 31, 4809-4817 10.1016/j.biomaterials.2010.02.064
47. Zhang, Z.; Lai, Y. X.; Yu, L.; Ding, J. D. Effects of Immobilizing Sites of RGD Peptides in Amphiphilic Block Copolymers on Efficacy of Cell Adhesion Biomaterials 2010, 31, 7873-7882 10.1016/j.biomaterials.2010.07.014
48. Cao, F. Y.; Yin, W. N.; Fan, J. X.; Tao, L.; Qin, S. Y.; Zhuo, R. X.; Zhang, X. Z. Evaluating the Effects of Charged Oligopeptide Motifs Coupled with RGD on Osteogenic Differentiation of Mesenchymal Stem Cells ACS Appl. Mater. Interfaces 2015, 7, 6698-6705 10.1021/acsami.5b00064
49. Xiong, J. P.; Stehle, T.; Zhang, R. G.; Joachimiak, A.; Frech, M.; Goodman, S. L.; Arnaout, M. A. Crystal Structure of the Extracellular Segment of Integrin αVβ3 in Complex with an Arg-Gly-Asp Ligand Science 2002, 296, 151-155 10.1126/science.1069040
50. Wang, X.; Yan, C.; Ye, K.; He, Y.; Li, Z. H.; Ding, J. D. Effect of RGD Nanospacing on Differentiation of Stem Cells Biomaterials 2013, 34, 2865-2874 10.1016/j.biomaterials.2013.01.021
51. Sun, J. G.; Graeter, S. V.; Yu, L.; Duan, S. F.; Spatz, J. P.; Ding, J. D. Technique of Surface Modification of a Cell-Adhesion-Resistant Hydrogel by a Cell-Adhesion-Available Inorganic Microarray Biomacromolecules 2008, 9, 2569-2572 10.1021/bm800477s
52. Aydin, D.; Louban, I.; Perschmann, N.; Blummel, J.; Lohmuller, T.; Cavalcanti-Adam, E. A.; Haas, T. L.; Walczak, H.; Kessler, H.; Fiammengo, R.; Spatz, J. P. Polymeric Substrates with Tunable Elasticity and Nanoscopically Controlled Biomolecule Presentation Langmuir 2010, 26, 15472-15480 10.1021/la103065x
53. Sun, J. G.; Graeter, S. V.; Tang, J.; Huang, J. H.; Liu, P.; Lai, Y. X.; Yu, L.; Majer, G.; Spatz, J. P.; Ding, J. D. Preparation of Stable Micropatterns of Gold on Cell-Adhesion-Resistant Hydrogels Assisted by a Hetero-Bifunctional Macromonomer Linker Sci. China: Chem. 2014, 57, 645-653 10.1007/s11426-013-5057-8
54. Humphries, J. D.; Wang, P.; Streuli, C.; Geiger, B.; Humphries, M. J.; Ballestrem, C. Vinculin Controls Focal Adhesion Formation by Direct Interactions with Talin and Actin J. Cell Biol. 2007, 179, 1043-1057 10.1083/jcb.200703036
55. Lee, J.; Abdeen, A. A.; Huang, T. H.; Kilian, K. A. Controlling Cell Geometry on Substrates of Variable Stiffness can Tune the Degree of Osteogenesis in Human Mesenchymal Stem Cells J. Mech. Behav. Biomed. Mater. 2014, 38, 209-218 10.1016/j.jmbbm.2014.01.009
56. Lee, J.; Abdeen, A. A.; Tang, X.; Saif, T. A.; Kilian, K. A. Geometric Guidance of Integrin Mediated Traction Stress during Stem Cell Differentiation Biomaterials 2015, 69, 174-183 10.1016/j.biomaterials.2015.08.005
57. Vogel, V.; Sheetz, M. Local Force and Geometry Sensing Regulate Cell Functions Nat. Rev. Mol. Cell Biol. 2006, 7, 265-275 10.1038/nrm1890
58. Swift, J.; Ivanovska, I. L.; Buxboim, A.; Harada, T.; Dingal, P. C. D. P.; Pinter, J.; Pajerowski, J. D.; Spinler, K. R.; Shin, J. W.; Tewari, M.; Rehfeldt, F.; Speicher, D. W.; Discher, D. E. Nuclear Lamin-A Scales with Tissue Stiffness and Enhances Matrix-Directed Differentiation Science 2013, 341, 1240104 10.1126/science.1240104
59. Arnold, M.; Cavalcanti-Adam, E. A.; Glass, R.; Blummel, J.; Eck, W.; Kantlehner, M.; Kessler, H.; Spatz, J. P. Activation of Integrin Function by Nanopatterned Adhesive Interfaces ChemPhysChem 2004, 5, 383-388 10.1002/cphc.200301014
60. Graeter, S. V.; Huang, J. H.; Perschmann, N.; Lopez-Garcia, M.; Kessler, H.; Ding, J. D.; Spatz, J. P. Mimicking Cellular Environments by Nanostructured Soft Interfaces Nano Lett. 2007, 7, 1413-1418 10.1021/nl070098g
61. Huang, J. H.; Graeter, S. V.; Corbellini, F.; Rinck, S.; Bock, E.; Kemkemer, R.; Kessler, H.; Ding, J. D.; Spatz, J. P. Impact of Order and Disorder in RGD Nanopatterns on Cell Adhesion Nano Lett. 2009, 9, 1111-1116 10.1021/nl803548b
62. Huang, J. H.; Ding, J. D. Nanostructured Interfaces with RGD Arrays to Control Cell-Matrix Interaction Soft Matter 2010, 6, 3395-3401 10.1039/b927168f
63. Yan, C.; Sun, J. G.; Ding, J. D. Critical Areas of Cell Adhesion on Micropatterned Surfaces Biomaterials 2011, 32, 3931-3938 10.1016/j.biomaterials.2011.01.078
64. Yang, F.; Williams, C. G.; Wang, D. A.; Lee, H.; Manson, P. N.; Elisseeff, J. The Effect of Incorporating RGD Adhesive Peptide in Polyethylene Glycol Diacrylate Hydrogel on Osteogenesis of Bone Marrow Stromal Cells Biomaterials 2005, 26, 5991-5998 10.1016/j.biomaterials.2005.03.018
65. Hosseinkhani, H.; Hosseinkhani, M.; Tian, F.; Kobayashi, H.; Tabata, Y. Osteogenic Differentiation of Mesenchymal Stem Cells in Self-Assembled Peptide-Amphiphile Nanofibers Biomaterials 2006, 27, 4079-4086 10.1016/j.biomaterials.2006.03.030
66. Park, J. S.; Yang, H. N.; Jeon, S. Y.; Woo, D. G.; Na, K.; Park, K. H. Osteogenic Differentiation of Human Mesenchymal Stem Cells Using RGD-Modified BMP-2 Coated Microspheres Biomaterials 2010, 31, 6239-6248 10.1016/j.biomaterials.2010.05.002
67. Yeung, T.; Georges, P. C.; Flanagan, L. A.; Marg, B.; Ortiz, M.; Funaki, M.; Zahir, N.; Ming, W.; Weaver, V.; Janmey, P. A. Effects of Substrate Stiffness on Cell Morphology, Cytoskeletal Structure, and Adhesion Cell Motil. Cytoskeleton 2005, 60, 24-34 10.1002/cm.20041
68. Rowlands, A. S.; George, P. A.; Cooper-White, J. J. Directing Osteogenic and Myogenic Differentiation of MSCs: Interplay of Stiffness and Adhesive Ligand Presentation Am. J. Physiol. Cell Physiol. 2008, 295, C1037-C1044 10.1152/ajpcell.67.2008
69. Trappmann, B.; Gautrot, J. E.; Connelly, J. T.; Strange, D. G. T.; Li, Y.; Oyen, M. L.; Cohen Stuart, M. A.; Boehm, H.; Li, B. J.; Vogel, V.; Spatz, J. P.; Watt, F. M.; Huck, W. T. S. Extracellular-Matrix Tethering Regulates Stem-Cell Fate Nat. Mater. 2012, 11, 642-649 10.1038/nmat3339
70. Yang, C.; Tibbitt, M. W.; Basta, L.; Anseth, K. S. Mechanical Memory and Dosing Influence Stem Cell Fate Nat. Mater. 2014, 13, 645-652 10.1038/nmat3889
71. Discher, D. E.; Mooney, D. J.; Zandstra, P. W. Growth Factors, Matrices, and Forces Combine and Control Stem Cells Science 2009, 324, 1673-1677 10.1126/science.1171643
72. Rao, N.; Grover, G. N.; Vincent, L. G.; Evans, S. C.; Choi, Y. S.; Spencer, K. H.; Hui, E. E.; Engler, A. J.; Christman, K. L. A Co-Culture Device with a Tunable Stiffness to Understand Combinatorial Cell-Cell and Cell-Matrix Interactions Integr. Biol. 2013, 5, 1344-1354 10.1039/c3ib40078f
73. Khetan, S.; Guvendiren, M.; Legant, W. R.; Cohen, D. M.; Chen, C. S.; Burdick, J. A. Degradation-Mediated Cellular Traction Directs Stem Cell Fate in Covalently Crosslinked Three-Dimensional Hydrogels Nat. Mater. 2013, 12, 458-465 10.1038/nmat3586