Directed stem cell differentiation: The role of physical forces

Cell Communication and Adhesion

Volumn 17, Issue 2, 2010, Pages 48-54

  Clause, Kelly C ^a,b   Liu, Li J ^a,b   Tobita, Kimimasa ^a,b,c  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b University of Pittsburgh   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cell shape; Cell cell contacts; Differentiation; ECM properties; Geometric controls; Mechanical force; Morphogenic factors

Indexed keywords

CELL CONTACT; CELL DIFFERENTIATION; CELL FATE; CELL SHAPE; EXTRACELLULAR MATRIX; GEOMETRY; MORPHOMETRICS; PRIORITY JOURNAL; REVIEW; STEM CELL; ANIMAL; CYTOLOGY; HUMAN; MECHANICAL STRESS; METABOLISM; MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL SHAPE; EXTRACELLULAR MATRIX; HUMANS; MICE; STEM CELLS; STRESS, MECHANICAL;

EID: 77954114677     PISSN: 15419061     EISSN: 15435180     Source Type: Journal    
DOI: 10.3109/15419061.2010.492535     Document Type: Review

References (114)

1. Abbott A (2003). Cell culture: Biology ' s new dimension. Nature. 424: 870-872.
2. Adams D, Keller R, Koehl M (1990). The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus laevis. Development. 110: 115-130.
3. Altman G, Horan RL, Martin I, Farhadi Jm, Stark PRH, Volloch V, Richmond JC, Vunjak-Novakovic G, Kaplan DL (2002). Cell differentiation by mechanical stress. FASEB J. 16: 270-272.
4. Angele P, Yoom JU, Smith C, Mansour J, Jepsen KJ, Nerlich M, Johnstone B (2003). Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res. 21: 451-457
5. Arai A, Yamamoto K, Toyama J. (1997). Murine cardiac progenitor cells require visceral embryonic endoderm and primitive streak for terminal differentiation. Dev Dyn. 210: 344-353.
6. Awad H, Wickham M, Leddy HA, Gimble J, Guilak F (2004). Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials. 25: 3211-3222.
7. Balaban N, Schwartz U, Riveling D, Goichberg P (2001). Force and focal adhesion assembly: A close relationship studied using elastic micropatterned substrates. Nat Cell Biol. 3: 466-472.
8. Beningo K, Dembo M, Kaverina I, Small J, Wang Y (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J Cell Biol. 153: 881-888.
9. Bennett KP, Bergeron C, Acar E, Klees RF, Vandenberg SL, Yenner B, Plopper GE (2007). Proteomics reveals multiple routes to the osteogenic phenotype in mesenchymal stem cells. BMC Genomics. 8: 380.
10. Benoit D, Schwartz M, Durney A, Anseth K (2008). Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater. 7: 816-823.
11. Burger E, Klein-Nulend J (1999). Mechanotranduction in bone-role of the lacuno-canalicular network. FASEB J. 13: S101-S112.
12. Chachisvilis M, Zhang Y, Frangos J (2006). G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci U S A. 103: 15463-15468.
13. Chen C, Alonso J, Ostuni E, Whitesides G, Ingber D (2003). Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Commun. 307: 355-361.
14. Chen C, Mirksich M, Huang S, Whitesides G, Ingber D (1998). Micropatterned surfaces for control of cell shape, position, and function. Biotechnol Prog. 14: 356-363.
15. Chicurel M, Chen C, Ingber D (1998). Cellular control lies in the balance of forces. Curr Opin Cell Biol. 10: 232-239.
16. Christopherson G, Song H, Mao H (2009). The influence of fi ber diameter of electrospun substrates on neural stem cell differentiation and proliferation. Biomaterials. 30: 556-564.
17. Chrzanowska-Wodnicka M, Burridge K (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol. 133: 1403-1415.
18. Chun T, Hotary K, Sabeh F, Saltiel A, Allen E, Weiss S (2006). A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell. 125: 577-591.
19. Clause K, Tinney JP, Liu L, Keller BB, Tobita K (2009). Engineered early embryonic cardiac tissue increases cardiomyocyte proliferation by cyclic mechanical stretch via p38-MAP kinase phosphorylation. Tissue Eng. 15: 1373-1380.
20. Cohen D, Chen C (2008). Mechanical control of stem cell differentiation. In: StemBook, Community TSCR (ed). StemBook, doi/10.3824/stembook.1.26.1, http://www.stembook.org; 2008.
21. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CDW, Oreffo ROC (2007). The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater. 6: 997-1003.
22. Davies P (1995). Flow-mediated endothelial mechanotranduction. Physiol Rev. 75: 519-560.
23. Dike L, Chen C, Mrksich M (1999). Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In VitroCell Dev Biol. 35: 441-448.
24. Discher D, Mooney D, Zandstra P (2009). Growth Factors, matrices, and forces combine and control stem cells. Science. 324: 1673-1677.
25. Engler A, Griffin M, Sen S (2004). Myotubes differentiate optimally on substrates with tissue-like stiffness: Pathological implications for soft or stiff microenvironments. J Cell Biol. 166: 877-887.
26. Engler A, Sen S, Sweeney L, Disher D (2006). Matrix elasticity directs stem cell lineage specification. Cell. 126: 677-689.
27. Erickson G, Gimble J, Franklin D, Rice H, Awad H, Guilak F (2002). Chondrogenic potential of adipose tissue-derided stromal cells in vitro and in vivo. Biochem Biophys Res Commun. 290: 763-769.
28. Folkman J, Moscona A (1978). Role of cell shape in growth control. Nature. 273: 345-349.
29. Gerecht S, Bettinger C, Zhang Z, Borenstein J, Vunjak-Novakovic G, Langer R (2007). The effect of actin disrupting agents on contact guidance of human embryonic stem cells. Biomaterials. 28: 4068-4077.
30. Gerstenfeld L, Barnes G, Shea C, Einhorn T (2003). Osteogenic differentiation is selectively promoted by morphogenetic signals from chondrocytes and synergized by a nutrient rich growth environment. Connect Tissue Res. 44: 85-91.
31. Glucksmann A (1939). Studies on bone formation in vitro. II. The role of tenstion and pressure in chondrogenesis. Anat Rec. 73: 39-55.
32. Glucksmann A (1942). The role of mechanical stress in bone formation in vitro. J Anat. 76: 231-239.
33. Gong Z, Niklason LE (2008). Small-diameter human vessel wall engineered from bone marrow-derived mesenchymal stem cells (hMSCs). FASEB J. 22: 1635-1648.
34. Griffith L, Swartz M. (2006). Capturing complex 3D tissue physiology in vitro . Nat Rev Mol Cell Biol 7: 211-224.
35. Guilak F, Cohen D, Estes B, Gimble J, Leidtke W, Chen C (2009). Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell. 5: 17-26.
36. Guo W, Frey M, Burnham N, Wang Y (2006). Susbtrate rigidity regulates the formation and maintenance of tissues. Biophys J. 90: 2213-2220.
37. Hadjipanayi E, Mudera V, Brown R (2009). Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness. J Tissue Eng Regen Med. 3: 77-84.
38. Hall B (1967). The formation of adventitious cartilage by membrane bones under the influence of mechanical stimulation applied in vitro. Life Sci. 6: 663-667.
39. Hall B (1968). In vitro studies on the mechanical evocation of advenitious cartilage in the chick. J Exp Zool. 168: 283-305.
40. Hamill O, Martinac E (2001). Molecular basis of mechanotransduction in living cells. Physiol Rev. 81: 685-740.
41. Hamilton D, Maul T, Vorp D (2004). Characterization of the response of bone marrow-derived progenitor cells to cyclic strain: Implications for vascular tissue-engineering applications. Tissue Eng. 10: 361-369.
42. Hayman M, Smith K, Cameron N, Przyborski S (2005). Growth of human stem cell-derived neurons on solid three-dimensional polymers. J Biochem Biophys Methods. 62: 231-240.
43. Helfman D, Levy E, Berthier C, Shtutman M (1999). Caldesmon inhibits nonmuscle cell contractility and interferes with the formation of focal adhesions. Mol Biol Cell. 10: 3097-4112.
44. Hoben G, Koay E, Athanasiou K (2008). Fibrochondrogenesis in two embryonic stem cell lines: Effects of differentiation timelines. Stem Cells. 26: 422-430.
45. Hove J, Koster R, Forouhar A, Acevedo-Bolton G, Fraser S, Gharib M (2003). Intracardiac fluid florces are an essential epigenetic factor for embryonic cardiogenesis. Nature. 421: 172-177.
46. Huang C, Hagar K, Frost L, Sun Y, Cheung H (2004). Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells. 22: 313-323.
47. Hwang N, Varghese S, Elisseeff J (2008). Controlled differentiation of stem cells. Adv Drug Deliv Rev. 60: 199-214.
48. Hwang N, Varghese S, Puleo C, Zhang Z, Elisseeff J (2007). Morphogenic signals from chondrocytes promote chondrogenic and osteogenic differentiation of mesenchymal stem cells. J Cell Physiol. 212: 281-284.
49. Hwang N, Varghese S, Zhang Z, Elisseeff J (2006). Chrondrogenic differentiation of human embryonic stem cell-derived cells in arginine-glycine-aspartate-modified hydrogels. Tissue Eng. 12: 2695-2706. (Pubitemid 46141292)
50. Iijima Y, Nagai T, Mizukami M, Matsuura K, Ogura T, Wada H, Toko H, Akazawa H, Takano H, Nakaya H, Komuro I (2003). Beating is necessary for transdifferentiation of skeletal muscle-derived cells into cardiomyocytes. FASEB J. 17: 1361-1363.
51. Ingber D (1991). Extracellular matrix and cell shape: Potential control points for inhibition of angiogenesis. J Cell Biochem. 47: 236-241.
52. Ingber D (2006). Cellular mechanotransduction: Putting all the pieces together again. FASEB J. 20: 811-827.
53. Janes K, Lauffenburger D (2006). A biological approach to computational models of proteomic networks. Curr Opin Chem Biol. 10: 73-80.
54. Johnson C, Tang H, Carag C, Speicher D, Discher D (2007). Forced unfolding of proteins within cells. Science. 317: 663-666.
55. Johnstone B, Hering T, Caplan A, Goldberg V, Yoo J (1998). In vitro cohondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res. 238: 265-272.
56. Kiger A, Jones D, Shultz C, Rogers M, Fuller M (2001). Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science. 294: 2542-2545.
57. Kirouac D, Zandstra P (2006). Understanding cellular networks to improve hematopoietic stem cell expansion cultures. Curr Opin Biotechnol. 17: 538-547.
58. Kloxin A, Kasko A, Salinas C, Anseth K (2009). Photodegradable hydrogels dor dynamic tuning of physical and chemical properties. Science. 2009;324: 59-63.
59. Kluger Y, Tuck D, Chang J, Nakayama Y, Poddar R (2004). Lineage specificity of gene expression patterns. Proc Natl Acad Sci U S A. 101: 6508-6513.
60. Lammerding J, Hsiao J, Schulze P, Kozlov S, Stewart C, Lee R (2005). Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J Cell Biol. 170: 781-791.
61. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT (2004). Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest. 113: 370-378.
62. Liu M, Post N (2000). Invited review: Mechanochemical signal tranduction in the fetal lung. J Appl Physiol. 89: 2078-2084.
63. Long F, Linsenmayer T (1998). Regulation fo growth region cartilage proliferation and differentiation by perichondrium. Development. 125: 1067-1073.
64. Lough J, Sugi Y (2000). Endoderm and heart development. Dev Dyn. 217: 327-342.
65. Manasek F, Burnside M, Waterman R (1972). Myocardial cell shape change as a mechanism of embryonic heart looping. Dev Biol. 29: 349-371.
66. Mauck R, Byers B, Yuan X, Tuan R (2007). Regulation of cartilaginous ECM gene transcription by conondrocytes and MSCs in 3D culture in response to dynamic loading. Biomech Model Mechanobiol. 6: 113-125.
67. Mauck R, Yuan X, Tuan R (2006). Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteo Cartilage. 14: 179-189.
68. McBeath R, Pirone D, Nelson CM (2004). Cell Shape, cytoskeletal tension, and rhoa regulate stem cell lineage commitment. Dev Cell. 6: 483-495.
69. McBride S, Knothe Tate M (2008). Modulation of stem cell shape and fate A: The role of density and seeding protocol on nucleus shape and gene expression. Tissue Eng Part A. 14: 1561-1572.
70. Moore KA, Polte T, Huang S, Shi B, Alsberg E, Sunday ME, Ingber DE (2005). Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn. 232: 268-281.
71. Nelson CM, Jean R, Tan J, Liu W (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Aacad Sci U S A. 102: 11594-11599.
72. Niklason LE, Gao J, Abbott W, Hirschi KK, Houser SR, Marini R, Langer R (1999). Functional arteries grown in vitro. Science. 284: 489-493.
73. O'Cearbhaill E, Punchard M, Murphy M, Barry F, McHugh P, Barron V (2008). Response of mesenchymal stem cells to the biomechanical environment of the endothelium on a flexible tubular silicone substrate. Biomaterials. 29: 1610-1619.
74. Orr A, Helmke B, Blackman B, Schwartz M (2006). Mechanisms of mechanotransduction. Dev Cell. 10: 11-20.
75. Parfitt A (1984). Age-related structural changes in trabecular and cortical bone: Cellular mechanisms and biomechanical consequences. Calcif Tissue Int. 36: S123-S128.
76. Park J, Chum JS, CHeng C, Chen F, Chen D, Li S (2004). Differential effects of equiaxial and uniaxial strain on mesenchymal stem cells. Biotechnol Bioeng. 88: 359-368.
77. Pelham R Jr, Wang Y. (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A. 94: 13661-13665.
78. Radisic M, Rpark H, Cerecht-Nir S, Cannizzaro C, Langer R, Vunjak-Novakovic G (2007). Biomimetic approach to cardiac tissue engineering. Phil Trans R Soc Lond B Biol Sci. 362: 1357-1368. (Pubitemid 47195028)
79. Recknor J, Sakaguchi D, Mallapragada S (2006). Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials. 27: 4098-4108.
80. Resnick A, Hopfer U (2007). Force-response considerations in ciliary mechanosensation. Biophys J. 93: 1380-1390.
81. Riveline D, Zamir EA, Balaban N, Schwartz U (2001). Focal contacts as mechanosensors: Externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J Cell Biol. 153: 1175-1186.
82. Rizzo V, Sung A, Oh P, Schnitzer J (1998). Rapid mechanotransduction in situ at the luminal cell surface of vascular endothelium and its caveolae. J Biol Chem. 273: 26323-26329. (Pubitemid 28471635)
83. Rooney P, Archer C (1992). The development of the perichondrium in the aivan ulna. J Anat. 181: 393-401.
84. Rudy-Reil D, Lough J (2004). Avian precardiac endoderm/ mesoderm induces cardiac myocyte differentiation in murine embryonic stem cells. Circ Res. 94: e107-e116.
85. Saha K, Keung AJ, Irwin EF, Li Y, Little L, Schaffer DV, Healy KE (2008). Substrate modulus directs neural stem cell behavior. Biophys J. 95: 4426-4438.
86. Saha S, Ji L, de Pablo J, Palecek S (2006). Inhibition of human embryonic stem cell differentiation by mechanical strain. J Cell Physiol. 206: 126-137. (Pubitemid 41740724)
87. Saitoh S, Takahashi I, Mizoguchi I, Sasano Y, Kagayama M, Mitani H (2000). Compressive force promotes chondrogenic differentiation and hypertrophy in midpalatal suture cartilage in growing rats. Anat Rec. 260: 392-401.
88. Sawada Y, Tamada M, Dubin-Thaler BJ, Cherniavskaya O, Sakai R, Tanaka S, Sheetz MP (2006). Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell. 127: 1015-1026.
89. Serluca F, Drummond I, Fishman M (2002). Endothelial signaling in kidney morphogenesis: A role for hemodynamic forces. Curr Biol. 12: 492-497.
90. Shimizu N, Yamamoto K, Obi S, Kumagaya S, Masumura T, Shumano T, Naruse K, Yamashita JK, Igarashi T, Ando J (2008). Cyclic strain induces mouse embryonic stem cell differentiation into vascular smooth muscle cells by activating PDGF receptor beta. J Appl Physiol. 104: 766-772.
91. Sniadecki N, Anguelouch A, Yang M, Lamb C (2007). Magnetic microposts as an approach to apply forces to living cells. Proc Natl Acad Sci U S A. 104: 14553-14558.
92. Sordella R, Jiang W, Chen G (2003). Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell. 113: 147-158.
93. Sukharev S, Corey D. Mechanosensitive channels: Multiplicity of families and gating paradigms. Sci STKE. 2004;re4.
94. Sze KS, de Kleijn DP, Lai RC, Tan EK, Zhao H, Yeo KS, Low TY, Lian Q, Lee CN, Mitchell W, El Oakley RM, Lim SK (2007). Elucidating the secretion proteome of human ESCderived mesenchymal stem cells. Mol Cell Proteomics. 10: 1680-1689.
95. Takahashi I, Onodera K, Sasano Y, Mizoguchi I, Bae JW, Mitani H, Kagayama M, Mitani H (2003). Effect of stretching on gene expression of beta1 integrin and focal adhesion kinase on chondrogenesis through cell-extracellular matrix interactions. Eur J Cell Biol. 82: 182-192.
96. Takahashi K, Mizoguchi I, Nakamura M, Sasano Y, Saitoh S, Kagayama M, Mitani H (1996). Effects of expansive force on the differentiation of midpalatal suture cartilage in rats. Bone. 18: 341-348.
97. Tan J, Tien J, Pirone D, Gray D (2003). Cells lying on a bed of microneedles: An approach to isolate mechanical force. Proc Natl Acad Sci U S A. 100: 1484-1489.
98. Tang J, Peng R, Ding J (2010). The regulation of stem cell differentiation by cell-cell contact on micropatterned material surfaces. Biomaterials. 31: 2470-2476.
99. Terraciano V, Hwang N, Moroni L, Park HB, Zhang Z, Mizrahi J, Seliktar D, Elisseeff J (2007). Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells. 25: 2730-2738.
100. Tobita K, Liu LJ, Janczewski AM, Tinney JP, Nonemaker JM, Augustine S, Stolz DB, Shroff SG, Keller BB (2006). Engineered early embryonic cardiac tissue retains proliferative and contractile properties of developing embryonic myocardium. Am J Physiol Heart Circ Physiol. 2006;291: H1829-H1837.
101. Tsai R, McKay R (2000). Cell contact regulates fate choic by cortical stem cells. J Neurosci. 20: 3725-3735.
102. Vats A, Bielby RC, Tolley N, Dickinson SC, Boccaccini AR, Hollander AP, Bishop AE, Polak JM (2006). Chondrogenic differentiation of human embryonic stem cells: The effect of the micro-environment. Tissue Eng. 12: 1687-1697.
103. Wagner W, Saffrich R, Wirkner U, Eckstein V, Blake J, Ansorge A (2005). Hematopoietic progenitor cells and cellular microenvironment: Behavioral and molecular changes upon interaction. Stem Cells. 23: 1180-1191.
104. Wang H, Dembo M, Wang YL (2000). Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol. 279: C1345-C1350.
105. Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C (2005). Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol. 25: 1817-1823.
106. Winer J, Janmey P, McCormick M, Funaki M (2009). Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A. 15: 147-154.
107. Xie T, Spradling A (2000). A niche maintaining germ line stem cells in the Drosophila ovary. Science. 290: 328-330.
108. Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J (2005). Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol. 288: H1915-H1924.
109. Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A, Ando J (2003). Proliferation, differentiation, and tube formation by endothelial progeni tor cells in response to shear stress. J Appl Physiol. 95:2081-2088.
110. Yang Y, Beqaj S, Kemp P, Ariel I, Schuger L (2000). Stretchinduced alternative splicing of serum response factor promotes bronchial myogenesis and is defectivbe in lung hypoplasia. J Clin Invest. 106: 1321-1330.
111. Yang Y, Relan N, Przywara D, Schuger L (1999). Embryonic mesenchymal cells share the potential for smooth muscle differentiation: Myogenesis is controlled by the cell's shape. Development. 126: 3027-3033.
112. Yim E, Pang S, Leong K (2007). Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res. 313: 1820-1829.
113. Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T (2002). Tissue engineering of a differentiated cardiac muscle construct. Circ Res. 90: 223-230.
114. Zimmermann WH, Fink C, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000). Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng. 68: 106-114.