The influence of substrate creep on mesenchymal stem cell behaviour and phenotype

Biomaterials

Volumn 32, Issue 26, 2011, Pages 5979-5993

  Cameron, Andrew R ^a   Frith, Jessica E ^a   Cooper White, Justin J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Creep; Mechanical properties; Mesenchymal stem cell; Tension; Viscoelasticity

Indexed keywords

CELL TYPES; COMPRESSIVE MODULI; CYTOSKELETAL; GEL SYSTEMS; HUMAN MESENCHYMAL STEM CELLS (HMSCS); LOSS MODULI; MESENCHYMAL STEM CELL; RELATIVE CONTRIBUTION; SUBSTRATE LOSS; TENSION; VISCO-ELASTIC MATERIAL;

BIOLOGICAL MATERIALS; BIOMECHANICS; CELL CULTURE; CREEP; STEM CELLS; VISCOELASTICITY;

SUBSTRATES;

BIOMATERIAL; POLYACRYLAMIDE GEL;

ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; COMPRESSIVE MODULUS; ELASTICITY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MUSCLE ISOMETRIC CONTRACTION; PHENOTYPE; PRIORITY JOURNAL; SUBSTRATE CREEP; VISCOELASTICITY; VISCOSITY;

BIOCOMPATIBLE MATERIALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ELASTIC MODULUS; ELASTICITY; HUMANS; MESENCHYMAL STEM CELLS; POLYMERASE CHAIN REACTION; VISCOSITY;

EID: 79959910559     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.04.003     Document Type: Article

References (65)

1. Wang N., Butler J.P., Ingber D.E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260(5111):1124-1127.
2. Wang N., Naruse K., Stamenovic D., Fredberg J.J., Mijailovich S.M., Tolic-Norrelykke I.M., et al. Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci U S A 2001, 98(14):7765-7770.
3. 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(25):13661-13665.
4. 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(4):1037-1044.
5. 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(1):617-628.
6. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126(4):677-689.
7. Guo W.-h., Frey M.T., Burnham N.A., Wang Y.-l. Substrate rigidity regulates the formation and maintenance of tissues. Biophys J 2006, 90(6):2213-2220.
8. 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(1):144-152.
9. Geiger B., Spatz J.P., Bershadsky A.D. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 2009, 10(1):21-33.
10. Geiger B., Bershadsky A., Pankov R., Yamada K.M. Transmembrane crosstalk between the extracellular matrix and the cytoskeleton. Nat Rev Mol Cell Biol 2001, 2(11):793-805.
11. Evans N., Minelli C., Gentleman E., LaPointe V., Patankar S., Kallivretaki M., et al. Substrate stiffness affects early differentiation events in embryonic stem cells. Eur Cell Mater 2009, 18:1-14.
12. Saha K., Keung A.J., Irwin E.F., Li Y., Little L., Schaffer D.V., et al. Substrate modulus directs neural stem cell behavior. Biophys J 2008, 95(9):4426-4438.
13. Liu Z., Bilston L. On the viscoelastic character of liver tissue: experiments and modelling of the linear behaviour. Biorheology 2000, 37(3):191-201.
14. Geerligs M., Peters G.W.M., Ackermans P.A.J., Oomens C.W.J., Baaijens F.P.T. Linear viscoelastic behavior of subcutaneous adipose tissue. Biorheology 2008, 45(6):677-688.
15. van Dam E., Dams S., Peters G., Rutten M., Schurink G., Buth J., et al. Non-linear viscoelastic behavior of abdominal aortic aneurysm thrombus. Biomech Model Mechanobiol 2008, 7(2):127-137.
16. Hrapko M., van Dommelen J.A.W., Peters G.W.M., Wismans J.S.H.M. The mechanical behaviour of brain tissue: large strain response and constitutive modelling. Biorheology 2006, 43(5):623-636.
17. Wang Y.-l., Pelham R.J. Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods in Enzymology: Molecular Motors and the cytoskeleton Part B 1998, 489-496. Academic Press. R.B. Valee (Ed.).
18. Geissler E., Hecht A.M. The Poisson ratio in polymer gels. Macromolecules 1980, 13(5):1276-1280.
19. Mahaffy R.E., Shih C.K., MacKintosh F.C., Käs J. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys Rev Lett 2000, 85(4):880.
20. Boudou T., Ohayon J., Picart C., Tracqui P. An extended relationship for the characterization of Young's modulus and Poisson's ratio of tunable polyacrylamide gels. Biorheology 2006, 43(6):721-728.
21. Yeung T., Georges P.C., Flanagan L.A., Marg B., Ortiz M., Funaki M., et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 2005, 60(1):24-34.
22. Calvet D., Wong J.Y., Giasson S. Rheological monitoring of polyacrylamide gelation: importance of cross-link density and temperature. Macromolecules 2004, 37(20):7762-7771.
23. Grattoni C.A., Al-Sharji H.H., Yang C., Muggeridge A.H., Zimmerman R.W. Rheology and permeability of crosslinked polyacrylamide gel. J Colloid Interface Sci 2001, 240(2):601-607.
24. du Roure O., Saez A., Buguin A., Austin R.H., Chavrier P., Siberzan P., et al. Force mapping in epithelial cell migration. Proc Natl Acad Sci U S A 2005, 102(7):2390-2395.
25. 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 U S A 2003, 100(4):1484-1489.
26. Galbraith C.G., Sheetz M.P. A micromachined device provides a new bend on fibroblast tractional forces. Proc Natl Acad Sci U S A 1997, 94(17):9114-9118.
27. Dembo M., Wang Y.-l. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 1999, 76(4):2307-2316.
28. Discher D.E., Janmey P., Wang Y.-l. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310(5751):1139-1143.
29. Beningo K.A., Dembo M., Kaverina I., Small J.V., Wang Y.-l. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J Cell Biol 2001, 153(4):881-888.
30. Ingber D., Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci 2003, 116(7):1157-1173.
31. Ingber D.E. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 1993, 104(3):613-627.
32. Petroll W.M., Vishwanath M., Ma L. Corneal fibroblasts respond rapidly to changes in local mechanical stress. Invest Ophthalmol Vis Sci 2004, 45(10):3466-3474.
33. Hytönen V.P., Vogel V. How force mght activate talin's vinculin binding sites: SMD reveals a structural mechanism. PLoS Comput Biol 2008, 4(2):e24.
34. Gallant N.D., Michael K.E., Garcia A.J. Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol Biol Cell 2005, 16(9):4329-4340.
35. Klein E.A., Yin L., Kothapalli D., Castagnino P., Byfield F.J., Xu T., et al. Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr Biol 2009, 19(18):1511-1518.
36. Wozniak M.A., Chen C.S. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 2009, 10(1):34-43.
37. Schwartz M.A., Ginsberg M.H. Networks and crosstalk: integrin signalling spreads. Nat Cell Biol 2002, 4(4):65-68.
38. Chen C.S., Mrksich M., Huang S., Whitesides G.M., Ingber D.E. Geometric control of cell life and death. Science 1997, 276(5317):1425-1428.
39. 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(3):564-572.
40. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279(5350):509-514.
41. Nobes C.D., Hall A. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81(1):53-62.
42. Geiger B., Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr Opin Cell Biol 2001, 13(5):584-592.
43. 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(4):483-495.
44. Arnsdorf E.J., Tummala P., Kwon R.Y., Jacobs C.R. Mechanically induced osteogenic differentiation - the role of RhoA, ROCKII and cytoskeletal dynamics. J Cell Sci 2009, 122(4):546-553.
45. Kawada N., Seki S., Kuroki T., Kaneda K. ROCK inhibitor Y-27632 attenuates stellate cell contraction and portal pressure increase induced by Endothelin-1. Biochem Biophys Res Commun 1999, 266(2):296-300.
46. Salhia B., Rutten F., Nakada M., Beaudry C., Berens M., Kwan A., et al. Inhibition of Rho-Kinase affects astrocytoma morphology, motility, and invasion through activation of Rac1. Cancer Res 2005, 65(19):8792-8800.
47. Scaife R.M., Job D., Langdon W.Y. Rapid microtubule-dependent induction of neurite-like extensions in NIH 3T3 fibroblasts by inhibition of ROCK and Cbl. Mol Biol Cell 2003, 14(11):4605-4617.
48. Ulrich T.A., de Juan Pardo E.M., Kumar S. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res 2009, 69(10):4167-4174.
49. Wakatsuki T., Wysolmerski R.B., Elson E.L. Mechanics of cell spreading: role of myosin II. J Cell Sci 2003, 116(8):1617-1625.
50. Cai Y., Biais N., Giannone G., Tanase M., Jiang G., Hofman J.M., et al. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 2006, 91(10):3907-3920.
51. Peyton S., Ghajar C., Khatiwala C., Putnam A. The emergence of ECM mechanics and cytoskeletal tension as important regulators of cell function. Cell Biochem Biophys 2007, 47(2):300-320.
52. Martin I., Jakob M., Schäfer D., Dick W., Spagnoli G., Heberer M. Quantitative analysis of gene expression in human articular cartilage from normal and osteoarthritic joints. Osteoarthritis Cartilage 2001, 9(2):112-118.
53. Au P., Tam J., Fukumura D., Jain R.K. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood 2008, 111(9):4551-4558.
54. Miano J.M., Olson E.N. Expression of the smooth muscle cell calponin gene marks the early cardiac and smooth muscle cell lineages during mouse embryogenesis. J Biol Chem 1996, 271(12):7095-7103.
55. Ball S.G., Shuttleworth A.C., Kielty C.M. Direct cell contact influences bone marrow mesenchymal stem cell fate. Int J Biochem Cell Biol 2004, 36(4):714-727.
56. Sinha S., Hoofnagle M.H., Kingston P.A., McCanna M.E., Owens G.K. Transforming growth factor-{beta}1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol 2004, 287(6):1560-1568.
57. Jeon E.S., Moon H.J., Lee M.J., Song H.Y., Kim Y.M., Bae Y.C., et al. Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-{beta}-dependent mechanism. J Cell Sci 2006, 119(23):4994-5005.
58. Lozito T.P., Taboas J.M., Kuo C.K., Tuan R.S. Mesenchymal stem cell modification of endothelial matrix regulates their vascular differentiation. J Cell Biochem 2009, 107(4):706-713.
59. Lozito T.P., Kuo C.K., Taboas J.M., Tuan R.S. Human mesenchymal stem cells express vascular cell phenotypes upon interaction with endothelial cell matrix. J Cell Biochem 2009, 107(4):714-722.
60. Kanematsu A., Yamamoto S., Iwai-Kanai E., Kanatani I., Imamura M., Adam R.M., et al. Induction of smooth muscle cell-like phenotype in marrow-derived cells among regenerating urinary bladder smooth muscle cells. Am J Pathol 2005, 166(2):565-573.
61. Simper D., Stalboerger P.G., Panetta C.J., Wang S., Caplice N.M. Smooth muscle progenitor cells in human blood. Circulation 2002, 106(10):1199-1204.
62. Narita Y., Yamawaki A., Kagami H., Ueda M., Ueda Y. Effects of transforming growth factor-{beta}1 and ascorbic acid on differentiation of human bone-marrow-derived mesenchymal stem cells into smooth muscle cell lineage. Cell Tissue Res 2008, 333(3):449-459.
63. Hudson J.E., Mills R.J., Frith J.E., Brooke G., Jaramillo-Ferrada P., Wolvetang E.J., et al. A defined media and substrate for expansion of human mesenchymal stromal cell progenitors that enriches for osteo- and chondro-genic precursors. Stem Cells Dev 2011, 20(1).
64. Frith J.E., Thomson B., Genever P. Dynamic three-dimensional culture methods enhance mesenchymal stem cell properties and increase therapeutic potential. Tissue Eng Part C Methods 2009, 16(4):735-749.
65. Sordella R., Jiang W., Chen G.-C., Curto M., Settleman J. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell 2003, 113(2):147-158.