Matrix mechanics and fluid shear stress control stem cells fate in three dimensional microenvironment

Current Stem Cell Research and Therapy

Volumn 8, Issue 4, 2013, Pages 313-323

  Chen, Guobao ^a   Lv, Yonggang ^a   Guo, Pan ^a   Lin, Chongwen ^a   Zhang, Xiaomei ^a   Yang, Li ^a   Xu, Zhiling ^a  

^a CHONGQING UNIVERSITY   (China)

Author keywords

Fluid shear stress (FSS); Matrix stiffness; Mechanotransduction; Mesenchymal stem cells (MSCs); Stem cells fate; Three dimensions (3D)

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; COLLAGEN GEL; FOCAL ADHESION KINASE; INTEGRIN; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; NITRIC OXIDE SYNTHASE; OSTEOPONTIN; OXYGEN; POLYSACCHARIDE; PROTEIN TYROSINE KINASE; TITANIUM; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BONE MARROW CELL; BONE TISSUE; CALCIUM CELL LEVEL; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL GROWTH; CELL INTERACTION; CELL MIGRATION; CELL MOTION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURFACE; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; FOCAL ADHESION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTERMETHOD COMPARISON; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NONHUMAN; NUTRIENT; OSTEOBLAST; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; RIGIDITY; SHEAR STRESS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STEM CELL; STEM CELL FATE; STRESS FIBER; TISSUE ENGINEERING; YOUNG MODULUS;

ANIMALS; BIOMECHANICAL PHENOMENA; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; ELASTICITY; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STROMAL CELLS; STRESS, PHYSIOLOGICAL;

EID: 84888098643     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/1574888X11308040007     Document Type: Article

References (100)

1. Weissman IL. Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000; 100(1): 157-68.
2. Zajac AL, Discher DE. Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling. Curr Opin Cell Biol 2008; 20(6): 609-15.
3. Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE. Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci USA 2007; 104(40): 15619-24.
4. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeleton tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004; 6(4): 483-95.
5. Potier E, Noailly J, Ito K. Directing bone marrow-derived stromal cell function with mechanics. J Biomech 2010; 43(5): 807-17.
6. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science 2005; 310(5751): 1139-43.
7. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126(4): 677-89.
8. Even-Ram S, Artym V, Yamada KM. Matrix control of stem cell fate. Cell 2006; 126(4): 645-7.
9. Holst J, Watson S, Lord MS, et al. Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Nat Biotechnol 2010; 28(10): 1123-8.
10. Evans ND, Minelli C, Gentleman E, et al. Substrate stiffness affects early differentiation events in embryonic stem cells. Eur Cell Mater 2009; 18: 1-13.
11. Abbott A. Cell culture: biology's new dimension. Nature 2003; 424(6951): 870-2.
12. Pampaloni F, Reynaud EG, Stelzer EH. The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol 2007; 8(10): 839-45.
13. Naito H, Dohi Y, Zimmermann WH, et al. The effect of mesenchymal stem cell osteoblastic differentiation on the mechanical properties of engineered bone-like tissue. Tissue Eng Part A 2011; 17(17-18): 2321-9.
14. Chen CS. Mechanotransduction-a field pulling together? J Cell Sci 2008; 121(pt 20): 3285-92.
15. Plant AL, Bhadriraju K, Spurlin TA, Elliott JT. Cell response to matrix mechanics: focus on collagen. Biochim Biophys Acta 2009; 1793(5): 893-902.
16. Khang D, Choi J, Im YM, et al. Role of subnano-, nanoand submicron-surface features on osteoblast differentiation of bone marrow mesenchymal stem cells. Biomaterials 2012; 33(26): 5997-6007.
17. Vogel V, Sheetz M. Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 2006; 7(4): 265-75.
18. Guo WH, Frey MT, Burnham NA, Wang YL. Substrate rigidity regulates the formation and maintenance of tissues. Biophys J 2006; 90(6): 2213-20.
19. Chowdhury F, Na S, Li D, et al. Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat Mater 2010; 9(1): 82-8.
20. Yeung T, Georges PC, Flanagan LA, et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 2005; 60(1): 24-34.
21. Wells RG. The role of matrix stiffness in regulating cell behavior. Hepatology 2008; 47(4): 1394-400.
22. Park JS, Chu JS, Tsou AD, et al. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF. Biomaterials 2011; 32(16): 3921-30.
23. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA. Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 2010; 6(6): 468-73.
24. Shih YR, Tseng KF, Lai HY, Lin CH, Lee OK. Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells. J Bone Miner Res 2011; 26(4): 730-8.
25. Leong WS, Tay CY, Yu H, et al. Thickness sensing of hMSCs on collagen gel directs stem cell fate. Biochem Biophys Res Commun 2010; 401(2): 287-92.
26. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cellmatrix adhesions to the third dimension. Science 2001; 294(5547): 1708-12.
27. Lutolf MP, Gilbert PM, Blau HM. Designing materials to direct stem-cell fate. Nature 2009; 462(7272): 433-41.
28. Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 2006; 7(3): 211-24.
29. Tee SY, Fu J, Chen CS, Janmey PA. Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 2011; 100(5): L25-7.
30. Wang LS, Boulaire J, Chan PP, Chung JE, Kurisawa M. The role of stiffness of gelatin-hydroxyphenylpropionic acid hydrogels formed by enzyme-mediated crosslinking on the differentiation of human mesenchymal stem cell. Biomaterials 2010; 31(33): 8608-16.
31. Tse JR, Engler AJ. Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS One 2011; 6(1): e15978.
32. Huebsch N, Arany PR, Mao AS, et al. Harnessing tractionmediated manipulation of cell/matrix interface to control stem-cell fate. Nat Mater 2010; 9(6): 518-26.
33. Pek YS, Wan AC, Ying JY. The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 2010; 31(3): 385-91.
34. Fu J, Wang YK, Yang MT, et al. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat Methods 2010; 7(9): 733-6.
35. Dikovsky D, Bianco-Peled H, Seliktar D. Defining the role of matrix compliance and proteolysis in three-dimensional cell spreading and remodeling. Biophys J 2008; 94(7): 2914-25.
36. Zhang YH, Zhao CQ, Jiang LS, Dai LY. Substrate stiffness regulates apoptosis and the mRNA expression of extracellular matrix regulatory genes in the rat annular cells. Matrix Biol 2011; 30(2): 135-44.
37. Levy-Mishali M, Zoldan J, Levenberg S. Effect of scaffold stiffness on myoblast differentiation. Tissue Eng Part A 2009; 15(4): 935-44.
38. Collins JM, Ayala P, Desai TA, Russell B. Three-dimensional culture with stiff microstructures increases proliferation and slows osteogenic differentiation of human mesenchymal stem cells. Small 2010; 6(3): 355-60.
39. Deans TL, Elisseeff JH. The life of a cell: probing the complex relationships with the world. Cell Stem Cell 2010; 6(6): 499-501.
40. Hadjipanayi E, Mudera V, Brown RA. Brown. Guiding cell migration in 3D: a collagen matrix with graded directional stiffness. Cell Motil Cytoskeleton 2009; 66(3): 121-8.
41. Wang PY, Tsai WB, Voelcker NH. Screening of rat mesenchymal stem cell behaviour on polydimethylsiloxane stiffness gradients. Acta Biomater 2012; 8(2): 519-30.
42. Lo Iacono M, Anzalone R, Corrao S, et al. Perinatal and Wharton's Jelly-derived mesenchymal stem cells in cartilage regenerative medicine and tissue engineering strategies. Open Tissue Eng Regen Med J 2011; 4: 72-81.
43. Murphy CM, Haugh MG, O'Brien FJ. The effect of mean pore size on cell attachment, proliferation and migration in collagenglycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010; 31(3): 461-6.
44. Grayson WL, Marolt D, Bhumiratana S, Fröhlich M, Guo XE, Vunjak-Novakovic G. Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol Bioeng 2011; 108(5): 1159-70.
45. Daley WP, Peters SB, Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci 2008; 121(pt 3): 255-64.
46. Hynes RO. The extracellular matrix: not just pretty fibrils. Science 2009; 326(5957): 1216-9.
47. Guilak F, Cohen DM, Estes BT, Gimble JM, Liedtke W, Chen CS. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009; 5(1): 17-26.
48. Discher DE, Mooney DJ, Zandstra PW. Growth factors, matrices, and forces combine and control stem cells. Science 2009; 324(5935): 1673-7.
49. Gilbert PM, Havenstrite KL, Magnusson KE, et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 2010; 329(5995): 1078-81.
50. Weng S, Fu J. Synergistic regulation of cell function by matrix rigidity and adhesive pattern. Biomaterials 2011; 32(36): 9584-93.
51. Du J, Chen X, Liang X, et al. Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc Natl Acad Sci USA 2011; 108(23): 9466-71.
52. Datta N, Pham QP, Sharma U, Sikavitsas VI, Jansen JA, Mikos AG. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci USA 2006; 103(8): 2488-93.
53. Pham QP, Kasper FK, Scott Baggett L, Raphael RM, Jansen JA, Mikos AG. The influence of an in vitro generated bone-like extracellular matrix on osteoblastic gene expression of marrow stromal cells. Biomaterials 2008; 29(18): 2729-39.
54. Liao J, Guo X, Grande-Allen KJ, Kasper FK, Mikos AG. Bioactive polymer/extracellular matrix scaffolds fabricated with a flow perfusion bioreactor for cartilage tissue engineering. Biomaterials 2010a; 31(34): 8911-20.
55. Liao J, Guo X, Nelson D, Kasper FK, Mikos AG. Modulation of osteogenic properties of biodegradable polymer/extracellular matrix scaffolds generated with a flow perfusion bioreactor. Acta Biomater 2010b; 6(7): 2386-93.
56. Thibault RA, Scott Baggett L, Mikos AG, Kasper FK. Osteogenic differentiation of mesenchymal stem cells on pregenerated extracellular matrix scaffolds in the absence of osteogenic cell culture supplements. Tissue Eng Part A 2010; 16(2): 431-40.
57. Chandler EM, Berglund CM, Lee JS, et al. Stiffness of photocrosslinked RGD-alginate gels regulates adipose progenitor cell behavior. Biotechnol Bioeng 2011; 108(7): 1683-92.
58. Hahn C, Schwartz MA. Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 2009; 10: 53-62.
59. Kapur S, Baylink DJ, Lau KH. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways Bone. 2003; 32(3): 241-51.
60. Adamo L, García-Cardeña G. Directed stem cell differentiation by fluid mechanical forces. Antioxid Redox Signal 2011; 15(5): 1463-73.
61. Yourek G, McCormick SM, Mao JJ, Reilly GC. Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen Med 2010; 5(5): 713-24.
62. Huang Y, Jia X, Bai K, Gong X, Fan Y. Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells. Arch Med Res. 2010; 41(7): 497-505.
63. Jagodzinski M, Breitbart A, Wehmeier M, et al. Influence of perfusion and cyclic compression on proliferation and differentiation of bone marrow stromal cells in 3-dimensional culture. J Biomech 2008; 41(9): 1885-91.
64. Owan I, Burr DB, Turner CH, et al. Mechanotransduction in bone: osteoblasts are more responsive to fluid forces than mechanical strain. Am J Physiol Cell Physiol 1997; 273(3): c810-5.
65. Bjerre L, Bünger C, Baatrup A, Kassem M, Mygind T. Flow perfusion culture of human mesenchymal stem cells on coralline hydroxyapatite scaffolds with various pore sizes. J Biomed Mater Res A 2011; 97(3): 251-63.
66. Stiehler M, Bünger C, Baatrup A, Lind M, Kassem M, Mygind T. Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. J Biomed Mater Res A 2009; 89(1): 96-107.
67. Zhao F, Grayson WL, Ma T, Irsigler A. Perfusion affects the tissue developmental patterns of human mesenchymal stem cells in 3D scaffolds. J Cell Physiol 2009; 219(2): 421-9.
68. Braccini A, Wendt D, Jaquiery C, et al. Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells 2005; 23(8): 1066-72.
69. Dong JD, Gu YQ, Li CM, et al. Response of mesenchymal stem cells to shear stress in tissue-engineered vascular grafts. Acta Pharmacol Sin 2009; 30(5): 530-6.
70. Alves da Silva ML, Martins A, Costa-Pinto AR, et al. Chondrogenic differentiation of human bone marrow mesenchymal stem cells in chitosan-based scaffolds using a flow-perfusion bioreactor. J Tissue Eng Regen Med 2011; 5(9): 722-32.
71. Buxboim A, Rajagopal K, Brown AE, Discher DE. How deeply cells feel: methods for thin gels. J Phys Condens Matter 2010; 22(19): 194116.
72. Kolahi KS, Mofrad MR. Mechanotransduction: a major regulator of homeostasis and development. Wiley Interdiscip Rev Syst Biol Med 2010; 2(6): 625-39.
73. Jaalouk DE, Lammerding J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol 2009; 10(1): 63-73.
74. Orr AW, Helmke BP, Blackman BR, Schwartz MA. Mechanisms of Mechanotransduction. Dev Cell 2006; 10(1): 11-20.
75. Geiger B, Spatz JP, Bershadsky AD. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 2009; 10(1): 21-33.
76. Chalfie M. Neurosensory mechanotransduction. Nature Rev Mol Cell Biol 2009; 10(1): 44-52.
77. Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10(1): 75-82.
78. Wozniak MA, Chen CS. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 2009; 10(1): 34-43.
79. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J 2006; 20(7): 811-27.
80. Titushkin IA, Shin J, Cho M. A new perspective for stem-cell mechanobiology: biomechanical control of stem-cell behavior and fate. Crit Rev Biomed Eng 2010; 38(5): 393-433.
81. Li D, Zhou J, Chowdhury F, Cheng J, Wang N, Wang F. Role of mechanical factors in fate decisions of stem cells. Regen Med 2011; 6(2): 229-40.
82. DuFort CC, Paszek MJ, Weaver VM. Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 2011; 12(5): 308-19.
83. Seong J, Tajik A, Wang N, Wang YX. Distinct mechanism of FAK mechanotransduction by different extracellular matrix proteins. Journal of Medical Biomechanics 2012; 27 (Suppl): 10-1.
84. Trappmann B, Gautrot JE, Connelly JT, et al. Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 2012; 11(7): 642-9.
85. Dupont S, Morsut L, Aragona M, et al. Role of YAP/TAZ in mechanotransduction. Nature 2011; 474(7350): 179-83.
86. Wrighton KH. Mechanotransduction: YAP and TAZ feel the force. Nat Rev Mol Cell Biol 2011; 12(7): 404.
87. Liu L, Yuan W, Wang J. Mechanisms for osteogenic differentiation of human mesenchymal stem cells induced by fluid shear stress. Biomech Model Mechanobiol 2010; 9(6): 659-70.
88. Li YJ, Batra NN, You L, et al. Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation. J Orthop Res 2004; 22(6): 1283-9.
89. Riddle RC, Taylor AF, Genetos DC, Donahue HJ. MAP kinase and calcium signaling mediate fluid flow-induced human mesenchymal stem cell proliferation. Am J Physiol Cell Physiol 2006; 290(3): C776-84.
90. Glossop JR, Cartmell SH. Effect of fluid flow-induced shear stress on human mesenchymal stem cells: differential gene expression of IL1B and MAP3K8 in MAPK signaling. Gene Expr Patterns 2009; 9(5): 381-8.
91. Kapur S, Baylink DJ, Lau KH. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 2003; 32(3): 241-51.
92. Huang CH, Chen MH, Young TH, Jeng JH, Chen YJ. Interactive effects of mechanical stretching and extracellular matrix proteins on initiating osteogenic differentiation of human mesenchymal stem cells. J Cell Biochem 2009; 108(6): 1263-73.
93. Salasznyk RM, Klees RF, Williams WA, Boskey A, Plopper GE. Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp Cell Res 2007; 313(1): 22-37.
94. Liu L, Yu B, Chen J, et al. Different effects of intermittent and continuous fluid shear stresses on osteogenic differentiation of human mesenchymal stem cells. Biomech Model Mechanobiol 2011; 11(3-4): 391-401.
95. Bassaneze V, Barauna VG, Lavini-Ramos C, et al. Shear stress induces nitric oxide-mediated vascular endothelial growth factor production in human adipose tissue mesenchymal stem cells. Stem Cells Dev 2010; 19(3): 371-8.
96. Kraehenbuehl TP, Langer R, Ferreira LS. Three-dimensional biomaterials for the study of human pluripotent stem cells. Nat Methods 2011; 8(9): 731-6.
97. Stolberg S, McCloskey KE. Can shear stress direct stem cell fate? Biotechnol Prog 2009; 25(1): 10-9.
98. Lee DA, Knight MM, Campbell JJ, Bader DL. Stem cell mechanobiology. J Cell Biochem 2011; 112(1): 1-9.
99. Stevens MM, George JH. Exploring and engineering the cell surface interface. Science 2005; 310(57): 1135-8.
100. Breuls RG, Jiya TU, Smit TH. Scaffold stiffness influences cell behavior: opportunities for skeletal tissue engineering. Open Orthop J 2008; 2: 103-9.