Role of mechanical factors in fate decisions of stem cells

Regenerative Medicine

Volumn 6, Issue 2, 2011, Pages 229-240

  Li, Dong ^a   Zhou, Jiaxi ^a,b   Chowdhury, Farhan ^c   Cheng, Jianjun ^d   Wang, Ning ^c   Wang, Fei ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b PEKING UNION MEDICAL COLLEGE   (China)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

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

Author keywords

cell mechanics; embryonic stem cells; mechanical factors; mechanical forces; mesenchymal stem cells; stem cell fate

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; CYTOKINE; FIBROBLAST GROWTH FACTOR; INTEGRIN; LEUKEMIA INHIBITORY FACTOR; MYOSIN II; PROTEIN NODAL; TRANSCRIPTION FACTOR NANOG; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL SHAPE; CELL SIZE; CELL SURFACE; CYTOKINE RELEASE; EMBRYONIC STEM CELL; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; HUMAN; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL;

ADULT; ANIMALS; BIOMECHANICS; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; HUMANS; MECHANICAL PHENOMENA; MODELS, BIOLOGICAL; PHYSICAL STIMULATION; STEM CELLS;

EID: 79952580022     PISSN: 17460751     EISSN: None     Source Type: Journal    
DOI: 10.2217/rme.11.2     Document Type: Article

References (85)

1. Evans MJ, Kaufman MH: Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154-156 (1981). (Pubitemid 11050741)
2. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al.: Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998). (Pubitemid 28516247)
3. Jiang Y, Jahagirdar BN, Reinhardt RL et al.: Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41-49 (2002). (Pubitemid 34742565)
4. Pittenger MF, Mackay AM, Beck SC et al.: Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147 (1999). (Pubitemid 29282067)
5. Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED: Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24, 1054-1064 (2006). (Pubitemid 44464738)
6. Hofstetter CP, Schwarz EJ, Hess D et al.: Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl Acad. Sci. USA 99, 2199-2204 (2002). (Pubitemid 34169038)
7. Kondo T, Johnson SA, Yoder MC, Romand R, Hashino E: Sonic hedgehog and retinoic acid synergistically promote sensory fate specifcation from bone marrow-derived pluripotent stem cells. Proc. Natl Acad. Sci. USA 102, 4789-4794 (2005). (Pubitemid 40471532)
8. Engler AJ, Sen S, Sweeney HL, Discher DE: Matrix elasticity directs stem cell lineage specifcation. Cell 126, 677-689 (2006). (Pubitemid 44233625)
9. O'Neill C, Jordan P, Ireland G: Evidence for two distinct mechanisms of anchorage stimulation in freshly explanted and 3T3 Swiss mouse fbroblasts. Cell 44, 489-496 (1986). (Pubitemid 16043339)
10. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE: Geometric control of cell life and death. Science 276, 1425-1428 (1997). (Pubitemid 27235413)
11. Engler AJ, Griffn MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE: Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell. Biol. 166, 877-887 (2004). (Pubitemid 39249838)
12. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS: Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004). (Pubitemid 38456178)
13. Georges PC, Miller WJ, Meaney DF, Sawyer ES, Janmey PA: Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys. J. 90, 3012-3018 (2006).
14. Discher DE, Janmey P, Wang YL: Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143 (2005). (Pubitemid 41681732)
15. Wang N, Tytell JD, Ingber DE: Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mo l. Cell. Biol. 10, 75-82 (2009).
16. Yeung T, Georges PC, Flanagan LA et al.: Effects of substrate stiffness on cell morphology cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34 (2005). (Pubitemid 40066224)
17. Pouille PA, Ahmadi P, Brunet AC, Farge E: Mechanical signals trigger Myosin II redistribution and mesoderm invagination in Drosophila embryos. Sci. Signal 2, ra16 (2009).
18. Martin AC, Kaschube M, Wieschaus EF: Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495-499 (2009).
19. Krieg M, Arboleda-Estudillo Y, Puech PH et al.: Tensile forces govern germ-layer organization in zebrafsh. Nat. Cell Biol. 10, 429-436 (2008).
20. Rauzi M, Verant P, Lecuit T, Lenne PF: Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell Biol. 10, 1401-1410 (2008).
21. Desprat N, Supatto W, Pouille PA, Beaurepaire E, Farge E: Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev. Cell 15, 470-477 (2008).
22. Levenstein ME, Ludwig TE, Xu RH et al.: Basic fbroblast growth factor support of human embryonic stem cell self-renewal. Stem Cells 24, 568-574 (2006). (Pubitemid 44464760)
23. Vallier L, Alexander M, Pedersen RA: Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J. Cell Sci. 118, 4495-4509 (2005). (Pubitemid 41556347)
24. Xu RH, Sampsell-Barron TL, Gu F et al.: NANOG is a direct target of TGF-β/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3, 196-206 (2008).
25. Chadwick K, Wang L, Li L et al.: Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 102, 906-915 (2003). (Pubitemid 36917782)
26. Xu RH, Chen X, Li DS et al.: BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat. Biotechnol. 20, 1261-1264 (2002). (Pubitemid 35462493)
27. Zhang P, Li J, Tan Z et al.: Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood 111, 1933-1941 (2008). (Pubitemid 351451502)
28. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE: Effcient differentiation of human embryonic stem cells to defnitive endoderm. Nat. Biotechnol. 23, 1534-1541 (2005). (Pubitemid 41752931)
29. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L: Highly effcient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280 (2009).
30. Pera MF, Andrade J, Houssami S et al.: Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J. Cell Sci. 117, 1269-1280 (2004). (Pubitemid 38456107)
31. Smith JR, Vallier L, Lupo G, Alexander M, Harris WA, Pedersen RA: Inhibition of Activin/Nodal signaling promotes specifcation of human embryonic stem cells into neuroectoderm. Dev. Biol. 313, 107-117 (2008). (Pubitemid 350298306)
32. Zhou J, Su P, Li D, Tsang S, Duan E, Wang F: High-effciency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor-β superfamily receptors. Stem Cells 28, 1741-1750 (2010).
33. Daheron L, Opitz SL, Zaehres H et al.: LIF/STAT3 signaling fails to maintain self-renewal of human embryonic stem cells. Stem Cells 22, 770-778 (2004). (Pubitemid 39166934)
34. Ying QL, Nichols J, Chambers I, Smith A: BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292 (2003). (Pubitemid 37487702)
35. Brons IG, Smithers LE, Trotter MW et al.: Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195 (2007). (Pubitemid 47067373)
36. Barry F, Boynton RE, Liu B, Murphy JM: Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp. Cell Res. 268, 189-200 (2001). (Pubitemid 32744650)
37. Ng F, Boucher S, Koh S et al.: PDGF, TGF-β, and FGF signaling is important for differentiation and growth of mesenchymal stem cells (MSCs): transcriptional profling can identify markers and signaling pathways important in differentiation of MSCs into adipogenic, chondrogenic, and osteogenic lineages. Blood 112, 295-307 (2008).
38. Discher D, Dong C, Fredberg JJ et al.: Biomechanics: cell research and applications for the next decade. Ann. Biomed. Eng. 37, 847-859 (2009).
39. Janmey PA, McCulloch CA: Cell mechanics: integrating cell responses to mechanical stimuli. Ann. Rev. Biomed. Eng. 9, 1-34 (2007). (Pubitemid 350252899)
40. Hahn C, Schwartz MA: Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell. Biol. 10, 53-62 (2009).
41. Paszek MJ, Zahir N, Johnson KR et al.: Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 (2005). (Pubitemid 41317594)
42. Pelham RJ Jr, Wang Y-L: High resolution detection of mechanical forces exerted by locomoting fbroblasts on the substrate. Mol. Biol. Cell 10, 935-945 (1999). (Pubitemid 29193722)
43. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA: Optimal matrix rigidity for stress fber polarization in stem cells. Nat. Phys. 6, 468-473 (2010).
44. Huebsch N, Arany PR, Mao AS et al.: Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9, 518-526 (2010).
45. Gilbert PM, Havenstrite KL, Magnusson KE et al.: Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081 (2010).
46. Roskelley CD, Desprez PY, Bissell MJ: Extracellular matrix-dependent tissue-specifc gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl Acad. Sci. USA 91, 12378-12382 (1994).
47. Watt FM, Jordan PW, O'Neill CH: Cell shape controls terminal differentiation of human epidermal keratinocytes. Proc. Natl Acad. Sci. USA 85, 5576-5580 (1988).
48. Ren XD, Kiosses WB, Schwartz MA: Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585 (1999). (Pubitemid 29057242)
49. Curtis A, Wilkinson C: Nantotechniques and approaches in biotechnology. Trends Biotechnol. 19, 97-101 (2001). (Pubitemid 32155429)
50. Flemming RG, Murphy CJ, Abrams GA, Goodman SL, Nealey PF: Effects of synthetic micro-and nano-structured surfaces on cell behavior. Biomaterials 20, 573-588 (1999). (Pubitemid 29116854)
51. Dalby MJ, Gadegaard N, Tare R et al.: The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 6, 997-1003 (2007). (Pubitemid 350210577)
52. Kurpinski K, Chu J, Hashi C, Li S: Anisotropic mechanosensing by mesenchymal stem cells. Proc. Natl Acad. Sci. USA 103, 16095-16100 (2006). (Pubitemid 44715157)
53. Kurpinski K, Chu J, Wang D, Li S: Proteomic profling of mesenchymal stem cell responses to mechanical strain and TGF-β1. Cell. Mol. Bioeng. 2, 606-614 (2009).
54. Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fbroblast cultures by defned factors. Cell 126, 663-676 (2006). (Pubitemid 44233629)
55. Takahashi K, Tanabe K, Ohnuki M et al.: Induction of pluripotent stem cells from adult human fbroblasts by defned factors. Cell 131, 861-872 (2007). (Pubitemid 350138099)
56. Yu J, Vodyanik MA, Smuga-Otto K et al.: Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
57. Park IH, Zhao R, West JA et al.: Reprogramming of human somatic cells to pluripotency with defned factors. Nature 451, 141-146 (2008).
58. Wozniak MA, Chen CS: Mechanotransduction in development: a growing role for contractility. Nat. Rev. Mol. Cell. Biol. 10, 34-43 (2009).
59. 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. 9, 82-88 (2010).
60. Poh YC, Chowdhury F, Tanaka TS, Wang N: Embryonic stem cells do not stiffen on rigid substrates. Biophys. J. 99, L19-L21 (2010).
61. Chowdhury F, Li Y, Poh YC, Yokohama-Tamaki T, Wang N, Tanaka TS: Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS One 5, e15655 (2010).
62. Shimizu N, Yamamoto K, Obi S et al.: Cyclic strain induces mouse embryonic stem cell differentiation into vascular smooth muscle cells by activating PDGF receptor-β. J. Appl. Physiol. 104, 766-772 (2008). (Pubitemid 351468806)
63. Yamamoto K, Sokabe T, Watabe T et al.: 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 (2005). (Pubitemid 40418021)
64. Garin G, Berk BC: Flow-mediated signaling modulates endothelial cell phenotype. Endothelium 13, 375-384 (2006). (Pubitemid 44941970)
65. Adamo L, Naveiras O, Wenzel PL et al.: Biomechanical forces promote embryonic haematopoiesis. Nature 459, 1131-1135 (2009).
66. Evans ND, Minelli C, Gentleman E et al.: Substrate stiffness affects early differentiation events in embryonic stem cells. Eur. Cell Mater. 18, 1-13; discussion 13-14 (2009).
67. Peerani R, Rao BM, Bauwens C et al.: Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J. 26, 4744-4755 (2007). (Pubitemid 350126801)
68. Ng ES, Davis RP, Azzola L, Stanley EG, Elefanty AG: Forced aggregation of defned numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood 106, 1601-1603 (2005). (Pubitemid 41208571)
69. Nostro MC, Cheng X, Keller GM, Gadue P: Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2, 60-71 (2008).
70. Friedland JC, Lee MH, Boettiger D: Mechanically activated integrin switch controlsα,5β1 function. Science 323, 642-644 (2009).
71. Shin ME, He Y, Li D et al.: Spatiotemporal organization, regulation, and functions of tractions during neutrophil chemotaxis. Blood 116, 3297-3310 (2010).
72. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP: Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
73. Grashoff C, Hoffman BD, Brenner MD et al.: Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266 (2010).
74. Johnson CP, Tang HY, Carag C, Speicher DW, Discher DE: Forced unfolding of proteins within cells. Science 317, 663-666 (2007). (Pubitemid 47229965)
75. Lyons RM, Gentry LE, Purchio AF, Moses HL: Mechanism of activation of latent recombinant transforming growth factor-β1 by plasmin. J. Cell. Biol. 110, 1361-1367 (1990).
76. Wipff PJ, Rifkin DB, Meister JJ, Hinz B: Myofbroblast contraction activates latent TGF-β1 from the extracellular matrix. J. Cell. Biol. 179, 1311-1323 (2007). (Pubitemid 350277747)
77. Ahamed J, Burg N, Yoshinaga K, Janczak CA, Rifkin DB, Coller BS: In vitro and in vivo evidence for shear-induced activation of latent transforming growth factor-β1. Blood 112, 3650-3660 (2008).
78. Conti MA, Even-Ram S, Liu C, Yamada KM, Adelstein RS: Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J. Biol. Chem. 279, 41263-41266 (2004). (Pubitemid 39313562)
79. Tullio AN, Accili D, Ferrans VJ et al.: Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc. Natl Acad. Sci. USA 94, 12407-12412 (1997). (Pubitemid 27492541)
80. Watanabe K, Ueno M, Kamiya D et al.: A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25, 681-686 (2007). (Pubitemid 46897207)
81. Xu Y, Zhu X, Hahm HS et al.: Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc. Natl Acad. Sci. USA 107, 8129-8134 (2010).
82. Li D, Zhou J, Wang L et al.: Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. J. Cell. Biol. 191, 631-644 (2010).
83. Chen G, Hou Z, Gulbranson DR, Thomson JA: Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell 7, 240-248 (2010).
84. Ohgushi M, Matsumura M, Eiraku M et al.: Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 7, 225-239 (2010).
85. Shewan AM, Maddugoda M, Kraemer A et al.: Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531-4542 (2005). (Pubitemid 41416439)