How cells sense extracellular matrix stiffness: A material's perspective

Current Opinion in Biotechnology

Volumn 24, Issue 5, 2013, Pages 948-953

  Trappmann, Britta ^a   Chen, Christopher S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIVE PROPERTIES; CELL FATE DECISION; EXTRACELLULAR MATRICES; INDEPENDENT CONTROL; STRUCTURAL HIERARCHIES; STRUCTURAL PARAMETER; SUBSTRATE STIFFNESS; SYNTHETIC MATERIALS;

CELLS; CYTOLOGY; STIFFNESS;

BIOMECHANICS;

MOLECULAR SCAFFOLD;

CELL ENCAPSULATION; CELL ENGINEERING; CELL FUNCTION; CELLULAR PARAMETERS; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX STIFFNESS; HUMAN; HYDROGEL; MATERIALS TESTING; MOLECULAR MECHANICS; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; SYNTHETIC BIOLOGY;

EID: 84884418572     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2013.03.020     Document Type: Review

References (50)

1. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
2. Wozniak M.A., Chen C.S. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 2009, 10:34-43.
3. Paszek M.J., Weaver V.M. The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 2004, 9:325-342.
4. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
5. Georges P.C., Hui J.J., Gombos Z., McCormick M.E., Wang A.Y., Uemura M., Mick R., Janmey P.A., Furth E.E., Wells R.G. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 2007, 293:G1147-G1154.
6. Levental K.R., Yu H., Kass L., Lakins J.N., Egeblad M., Erler J.T., Fong S.F., Csiszar K., Giaccia A., Weninger W., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 2009, 139:891-906.
7. Samuel M.S., Lopez J.I., McGhee E.J., Croft D.R., Strachan D., Timpson P., Munro J., Schroder E., Zhou J., Brunton V.G., et al. Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 2011, 19:776-791.
8. Liu J., Tan Y., Zhang H., Zhang Y., Xu P., Chen J., Poh Y.C., Tang K., Wang N., Huang B. Soft fibrin gels promote selection and growth of tumorigenic cells. Nat Mater 2012, 11:734-741.
9. Alcaraz J., Xu R., Mori H., Nelson C.M., Mroue R., Spencer V.A., Brownfield D., Radisky D.C., Bustamante C., Bissell M.J. Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J 2008, 27:2829-2838.
10. Ingber D.E. Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc Natl Acad Sci USA 1990, 87:3579-3583.
11. Mason B.N., Starchenko A., Williams R.M., Bonassar L.J., Reinhart-King C.A. Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior. Acta Biomater 2013, 9:4635-4644.
12. Rault I., Frei V., Herbage D., AbdulMalak N., Huc A. Evaluation of different chemical methods for cross-linking collagen gel, films and sponges. J Mater Sci Mater Med 1996, 7:215-221.
13. Syedain Z.H., Bjork J., Sando L., Tranquillo R.T. Controlled compaction with ruthenium-catalyzed photochemical cross-linking of fibrin-based engineered connective tissue. Biomaterials 2009, 30:6695-6701.
14. Pelham R.J., Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 1997, 94:13661-13665.
15. 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.
16. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
17. Mann B.K., West J.L. Cell adhesion peptides alter smooth muscle cell adhesion, proliferation, migration, and matrix protein synthesis on modified surfaces and in polymer scaffolds. J Biomed Mater Res 2002, 60:86-93.
18. Hern D.L., Hubbell J.A. Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. J Biomed Mater Res 1998, 39:266-276.
19. Burdick J.A., Anseth K.S. Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials 2002, 23:4315-4323.
20. Mann B.K., Gobin A.S., Tsai A.T., Schmedlen R.H., West J.L. Smooth muscle cell growth in photopolymerized hydrogels with cell adhesive and proteolytically degradable domains: synthetic ECM analogs for tissue engineering. Biomaterials 2001, 22:3045-3051.
21. Burdick J.A., Prestwich G.D. Hyaluronic acid hydrogels for biomedical applications. Adv Mater 2011, 23:H41-H56.
22. Levesque S.G., Shoichet M.S. Synthesis of enzyme-degradable, peptide-cross-linked dextran hydrogels. Bioconjug Chem 2007, 18:874-885.
23. 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.
24. Lu S., Ramirez W.F., Anseth K.S. Photopolymerized, multilaminated matrix devices with optimized nonuniform initial concentration profiles to control drug release. J Pharm Sci 2000, 89:45-51.
25. Alberti K., Davey R.E., Onishi K., George S., Salchert K., Seib F.P., Bornhauser M., Pompe T., Nagy A., Werner C., et al. Functional immobilization of signaling proteins enables control of stem cell fate. Nat Methods 2008, 5:645-650.
26. Fan V.H., Tamama K., Au A., Littrell R., Richardson L.B., Wright J.W., Wells A., Griffith L.G. Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 2007, 25:1241-1251.
27. Beer J.H., Springer K.T., Coller B.S. Immobilized Arg-Gly-Asp (RGD) peptides of varying lengths as structural probes of the platelet glycoprotein IIb/IIIa receptor. Blood 1992, 79:117-128.
28. Houseman B.T., Mrksich M. The microenvironment of immobilized Arg-Gly-Asp peptides is an important determinant of cell adhesion. Biomaterials 2001, 22:943-955.
29. Trappmann B., Gautrot J.E., Connelly J.T., Strange D.G., Li Y., Oyen M.L., Cohen Stuart M.A., Boehm H., Li B., Vogel V., et al. Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 2012, 11:642-649.
30. 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.
31. Selhuber-Unkel C., Lopez-Garcia M., Kessler H., Spatz J.P. Cooperativity in adhesion cluster formation during initial cell adhesion. Biophys J 2008, 95:5424-5431.
32. Aydin D., Louban I., Perschmann N., Blummel J., Lohmuller T., Cavalcanti-Adam E.A., Haas T.L., Walczak H., Kessler H., Fiammengo R., et al. Polymeric substrates with tunable elasticity and nanoscopically controlled biomolecule presentation. Langmuir 2010, 26:15472-15480.
33. Tan J.L., Tien J., Pirone D.M., Gray D.S., Bhadriraju K., Chen C.S. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci USA 2003, 100:1484-1489.
34. Fu J., Wang Y.K., Yang M.T., Desai R.A., Yu X., Liu Z., Chen C.S. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 2010, 7:733-736.
35. Nowak A.P., Breedveld V., Pakstis L., Ozbas B., Pine D.J., Pochan D., Deming T.J. Rapidly recovering hydrogel scaffolds from self-assembling diblock copolypeptide amphiphiles. Nature 2002, 417:424-428.
36. Shen W., Kornfield J.A., Tirrell D.A. Structure and mechanical properties of artificial protein hydrogels assembled through aggregation of leucine zipper peptide domains. Soft Matter 2007, 3:99-107.
37. O'Leary L.E., Fallas J.A., Bakota E.L., Kang M.K., Hartgerink J.D. Multi-hierarchical self-assembly of a collagen mimetic peptide from triple helix to nanofibre and hydrogel. Nat Chem 2011, 3:821-828.
38. Gelain F., Bottai D., Vescovi A., Zhang S.G. Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures. PLoS ONE 2006, 1:e119.
39. Pashuck E.T., Cui H.G., Stupp S.I. Tuning supramolecular rigidity of peptide fibers through molecular structure. J Am Chem Soc 2010, 132:6041-6046.
40. Stahl P.J., Romano N.H., Wirtz D., Yu S.M. PEG-based hydrogels with collagen mimetic peptide-mediated and tunable physical cross-links. Biomacromolecules 2010, 11:2336-2344.
41. Mammoto T., Ingber D.E. Mechanical control of tissue and organ development. Development 2010, 137:1407-1420.
42. Lutolf M.P., Lauer-Fields J.L., Schmoekel H.G., Metters A.T., Weber F.E., Fields G.B., Hubbell J.A. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci USA 2003, 100:5413-5418.
43. Lutolf M.P., Raeber G.P., Zisch A.H., Tirelli N., Hubbell J.A. Cell-responsive synthetic hydrogels. Adv Mater 2003, 15:888-892.
44. Miller J.S., Shen C.J., Legant W.R., Baranski J.D., Blakely B.L., Chen C.S. Bioactive hydrogels made from step-growth derived PEG-peptide macromers. Biomaterials 2010, 31:3736-3743.
45. Kloxin A.M., Kasko A.M., Salinas C.N., Anseth K.S. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 2009, 324:59-63.
46. Kloxin A.M., Benton J.A., Anseth K.S. In situ elasticity modulation with dynamic substrates to direct cell phenotype. Biomaterials 2010, 31:1-8.
47. Guvendiren M., Burdick J.A. Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics. Nat Commun 2012, 3:792.
48. 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, 10.1038/nmat3586.
49. Little W.C., Smith M.L., Ebneter U., Vogel V. Assay to mechanically tune and optically probe fibrillar fibronectin conformations from fully relaxed to breakage. Matrix Biol 2008, 27:451-461.
50. Schwartz M.A., Ginsberg M.H. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol 2002, 4:E65-E68.