Controlling cell geometry on substrates of variable stiffness can tune the degree of osteogenesis in human mesenchymal stem cells

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 38, Issue , 2014, Pages 209-218

  Lee, Junmin ^a   Abdeen, Amr A ^a   Huang, Tiffany H ^a   Kilian, Kristopher A ^a  

^a University of Illinois at Urbana Champaign   (United States)

Author keywords

Microcontact printing; Microenvironment; Polyacrylamide hydrogels; Stem cell differentiation; Substrate stiffness

Indexed keywords

ELECTRON DEVICE MANUFACTURE; FLOWCHARTING; GELS; GENE EXPRESSION; GEOMETRY; HYDROGELS; STEM CELLS; STIFFNESS; SUBSTRATES;

MICRO CONTACT PRINTING; MICROENVIRONMENTS; POLYACRYLAMIDE HYDROGELS; STEM CELL DIFFERENTIATION; SUBSTRATE STIFFNESS;

CELL CULTURE;

FIBRONECTIN; MATRIX PROTEIN; POLYACRYLAMIDE; POLYACRYLAMIDE GEL; ACRYLIC ACID RESIN; HYDROGEL; SCLEROPROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BONE DEVELOPMENT; CELL ADHESION; CELL DIFFERENTIATION; CELL SHAPE; CONTROLLED STUDY; COVALENT BOND; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; RIGIDITY; YOUNG MODULUS; BIOMECHANICS; CELL LINEAGE; CHEMISTRY; CYTOLOGY; CYTOSKELETON; DRUG EFFECTS; GENE EXPRESSION REGULATION; INTRACELLULAR SPACE; MECHANICS; MESENCHYMAL STROMA CELL; METABOLISM;

ACRYLIC RESINS; BIOMECHANICAL PHENOMENA; CELL LINEAGE; CELL SHAPE; CYTOSKELETON; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; HUMANS; HYDROGELS; INTRACELLULAR SPACE; MECHANICAL PROCESSES; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS;

EID: 84905569470     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2014.01.009     Document Type: Article

References (39)

1. Aratyn-Schaus Y., Oakes P.W., Stricker J., Winter S.P., Gardel M.L. Preparation of complaint matrices for quantifying cellular contraction. J. Vis. Exp 2010, 1-6.
2. Crisan M., Yap S., Casteilla L., Chen C.-W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., Norotte C., Teng P.-N., Traas J., Schugar R., Deasy B.M., Badylak S., Buhring H.-J., Giacobino J.-P., Lazzari L., Huard J., Péault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
3. Dalby M.J., Gadegaard N., Tare R., Andar A., Riehle M.O., Herzyk P., Wilkinson C.D.W., Oreffo R.O.C. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 2007, 6:997-1003.
4. Damljanović V., Lagerholm B.C., Jacobson K. Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. Biotechniques 2005, 39:847-851.
5. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
6. Flanagan L.A., Ju Y., Marg B., Osterfield M., Paul A. Neuroreport 2002, 13:2411-2415.
7. Frith J.E., Mills R.J., Hudson J.E., Cooper-White J.J. Tailored integrin-extracellular matrix interactions to direct human mesenchymal stem cell differentiation. Stem Cells Dev. 2012, 21:2442-2456.
8. Gao L., McBeath R., Chen C.S. Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-cadherin. Stem Cells 2010, 28:564-572.
9. Gilbert P.M., Havenstrite K.L., Magnusson K.E.G., 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, 80(329):1078-1081.
10. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
11. Guvendiren M., Burdick J.a Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics. Nat. Commun 2012, 3:792.
12. Higuchi A., Ling Q., Chang Y., Hsu S., Umezawa A. Physical cues of biomaterials guide stem cell differentiation fate. Chem. Rev 2013, 113:3297-3328.
13. Keung A.J., Asuri P., Kumar S., Schaffer D.V Soft microenvironments promote the early neurogenic differentiation but not self-renewal of human pluripotent stem cells. Integr. Biol. 2012, 4:1049-1058.
14. 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, 12:1-8.
15. Kilian K.a, Bugarija B., Lahn B.T., Mrksich M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:4872-4877.
16. Kilian K.a, Mrksich M. Directing stem cell fate by controlling the affinity and density of ligand-receptor interactions at the biomaterials interface. Angew. Chem. Int. Ed. Engl 2012, 51:4891-4895.
17. Komori T., Yagi H., Nomura S., Yamaguchi a, Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., Kishimoto T Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
18. Kurpinski K., Chu J., Hashi C., Li S. Anisotropic mechanosensing by mesenchymal stem cells. Proc. Nat. Acad. Sci. U.S.A. 2006, 103:16095-16100.
19. 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.
20. 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.
21. McGarry J.P., Fu J., Yang M.T., Chen C.S., McMeeking R.M., Evans a G., Deshpande V.S. Simulation of the contractile response of cells on an array of micro-posts. Philos. Trans. R. Soc. London, Ser. A 2009, 367:3477-3497.
22. Ni X.F., Crozatier C., Sensebé L., Langonne a., Wang L., Fan Y., He P.G., Chen Y. On-chip differentiation of human mesenchymal stem cells into adipocytes. Microelectron. Eng. 2008, 85:1330-1333.
23. Oh S., Brammer K.S., Li Y.S.J., Teng D., Engler A.J., Chien S., Jin S. Stem cell fate dictated solely by altered nanotube dimension. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:2130-2135.
24. Peng R., Yao X., Cao B., Tang J., Ding J. The effect of culture conditions on the adipogenic and osteogenic inductions of mesenchymal stem cells on micropatterned surfaces. Biomaterials 2012, 33:6008-6019.
25. Pittenger M.F. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 80(284):143-147.
26. Rape A.D., Guo W.-H., Wang Y.-L. The regulation of traction force in relation to cell shape and focal adhesions. Biomaterials 2011, 32:2043-2051.
27. Rotsch C., Jacobson K., Radmacher M. Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Nat. Acad. Sci. U.S.A. 1999, 96:921-926.
28. 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.
29. Saha K., Keung A.J., Irwin E.F., Li Y., Little L., Schaffer D.V, Healy K.E. Substrate modulus directs neural stem cell behavior. Biophys. J. 2008, 95:4426-4438.
30. Tang X., Yakut Ali M., Saif M.T.A. A novel technique for micro-patterning proteins and cells on polyacrylamide gels. Soft Matter 2012, 8:7197-7206.
31. Tee S.-Y., Fu J., Chen C.S., Janmey P.a Cell shape and substrate rigidity both regulate cell stiffness. Biophys. J. 2011, 100:L25-L27.
32. Théry M. Micropatterning as a tool to decipher cell morphogenesis and functions. J. Cell Sci 2010, 123:4201-4213.
33. 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., 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.
34. Tse J.R., Engler A.J. Preparation of hydrogel substrates with tunable mechanical properties. Curr. Protoc. Cell Biol 2010, 16. (Chapter 10, Unit 10.).
35. Tseng Q., Wang I., Duchemin-Pelletier E., Azioune A., Carpi N., Gao J., Filhol O., Piel M., Théry M., Balland M. A new micropatterning method of soft substrates reveals that different tumorigenic signals can promote or reduce cell contraction levels. Lab Chip 2011, 11:2231-2240.
36. Winer J.P., Janmey P.a, McCormick M.E., Funaki M. Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng. Part A 2009, 15:147-154.
37. Yang, Relan, N.K., Przywara, D.A., Schuger, L., 1999. Embryonic mesenchymal cells share the potential for smooth muscle differentiation: myogenesis is controlled by the cell's shape 3033, 3027-3033.
38. Yim E.K., Darling E.M., Kulangara K., Guilak F., Leong K.W. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 2010, 31:1299-1306.
39. Zhang D., Kilian K.a The effect of mesenchymal stem cell shape on the maintenance of multipotency. Biomaterials 2013, 34:3962-3969.