The Effect of Physical Cues on the Stem Cell Differentiation

Author(s): Mehrdad M. Moghaddam, Shahin Bonakdar, Mona R. Shariatpanahi, Mohammad A. Shokrgozar*, Shahab Faghihi*.

Journal Name: Current Stem Cell Research & Therapy

Volume 14 , Issue 3 , 2019

Become EABM
Become Reviewer

Abstract:

Development of multicellular organisms is a very complex and organized process during which cells respond to various factors and features in extracellular environments. It has been demonstrated that during embryonic evolvement, under certain physiological or experimental conditions, unspecialized cells or stem cells can be induced to become tissue or organ-specific cells with special functions. Considering the importance of physical cues in stem cell fate, the present study reviews the role of physical factors in stem cells differentiation and discusses the molecular mechanisms associated with these factors.

Keywords: Stem cell, differentiation, physical cues, molecular mechanisms, growth, differentiation, apoptosis.

[1]
Hosseinirad H, Rashidi M, Moghaddam MM, et al. Stem cell therapy for lung diseases: From fundamental aspects to clinical applications. Cell Mol Biol (Noisy-le-Grand, France) 2018; 64(10): 92-101.
[2]
Elbuluk A, Einhorn TA, Iorio R. A comprehensive review of stem-cell therapy. JBJS Rev 2017; 5(8): e15.
[3]
Poulos J. The limited application of stem cells in medicine: A review. Stem Cell Res Ther 2018; 9(1): 1.
[4]
Chen X, He Y, Lu F. Autophagy in stem cell biology: A perspective on stem cell self-renewal and differentiation. Stem Cells Int 2018; 2018: 1-12.
[5]
Mizuno H, Tobita M, Orbay H, Uysal AC, Lu F. Adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells Cancer Stem Cells 2014; 12: 165-74.
[6]
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126(4): 663-76.
[7]
Han YL, Wang S, Zhang X, Li Y, Huang G, Qi H. Engineering physical microenvironment for stem cell based regenerative medicine. Drug Discov Today 2014; 19(6): 763-73.
[8]
Sobacchi C, Palagano E, Villa A, Menale C. Soluble factors on stage to direct mesenchymal stem cells fate. Front Bioeng Biotechnol 2017; 5(32): 1-9.
[9]
Brafman DA. Constructing stem cell microenvironments using bioengineering approaches. Physiol Genomics 2013; 45(23): 1123-35.
[10]
Lee JH, Park HK, Kim KS. Intrinsic and extrinsic mechanical properties related to the differentiation of mesenchymal stem cells. Biochem Biophys Res Commun 2016; 473(3): 752-7.
[11]
Wu Y, Yang Z, Law JBK, He AY, Abbas AA, Denslin V. The combined effect of substrate stiffness and surface topography on chondrogenic differentiation of mesenchymal stem cells. Tissue Eng Part A 2017; 23(1-2): 43-54.
[12]
Sun M, Chi G, Li P, et al. Effects of matrix stiffness on the morphology, adhesion, proliferation and osteogenic differentiation of mesenchymal stem cells. Int J Med Sci 2018; 15(3): 257-68.
[13]
Kumari S, Vermeulen S, van der Veer B, Carlier A, de Boer J, Subramanyam D. Shaping cell fate: Influence of topographical substratum properties on embryonic stem cells. Tissue Eng Part B Rev 2018; 24(4): 255-66.
[14]
Park JS, Chu JS, Tsou AD, et al. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-β. Biomaterials 2011; 32(16): 3921-30.
[15]
Xu J, Sun M, Tan Y, et al. Effect of matrix stiffness on the proliferation and differentiation of umbilical cord mesenchymal stem cells. Differentiation 2017; 96: 30-9.
[16]
McKee C, Chaudhry GR. Advances and challenges in stem cell culture. Colloids Surf B Biointerfaces 2017; 159: 62-77.
[17]
Steward AJ, Kelly DJ. Mechanical regulation of mesenchymal stem cell differentiation. J Anat 2015; 227(6): 717-31.
[18]
Andalib MN, Dzenis Y, Donahue HJ, Lim JY. Biomimetic substrate control of cellular mechanotransduction. Biomater Res 2016; 20(1): 11.
[19]
Yim EK, Pang SW, Leong KW. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 2007; 313(9): 1820-9.
[20]
Sharfeddin AS. Mechanotransduction of matrix stiffness regulates cell adhesion strength: An analysis using biomaterial surfaces with tunable mechanical and chemical properties. 2016. Graduate Theses and Dissertations. http://scholarcommons.usf.edu/etd/6387
[21]
Yeh YC, Ling JY, Chen WC, Lin HH, Tang MJ. Mechanotransduction of matrix stiffness in regulation of focal adhesion size and number: reciprocal regulation of caveolin-1 and β1 integrin. Sci Rep 2017; 7(1): 15008.
[22]
Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126(4): 677-89.
[23]
Smith LR, Cho S, Discher DE. Stem cell differentiation is regulated by extracellular matrix mechanics. Physiol 2017; 33(1): 16-25.
[24]
Leach JK, Whitehead J. Materials-directed differentiation of mesenchymal stem cells for tissue engineering and regeneration. ACS Biomater Sci Eng 2017; 4(4): 1115-27.
[25]
Vining KH, Mooney DJ. Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol 2017; 18(12): 728-42.
[26]
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.
[27]
Clause KC, Liu LJ, Tobita K. Directed stem cell differentiation: The role of physical forces. Cell Commun Adhes 2010; 17(2): 48-54.
[28]
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.
[29]
Sun Y, Chen CS, Fu J. Forcing stem cells to behave: A biophysical perspective of the cellular microenvironment. Annu Rev Biophys 2012; 41: 519-42.
[30]
Kurpinski K, Chu J, Hashi C, Li S. Anisotropic mechanosensing by mesenchymal stem cells. Proc Natl Acad Sci USA 2006; 103(44): 16095-100.
[31]
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 2005; 288(4): 1915-24.
[32]
Sevcik EN, Szymanski JM, Jallerat Q, Feinberg AW. Patterning on Topography for generation of cell culture substrates with independent nanoscale control of chemical and topographical extracellular matrix cues. Curr Protoc Cell Biol 2017; 75(1): 10-23.
[33]
Dalby MJ, McCloy D, Robertson M, Wilkinson CD, Oreffo RO. Osteoprogenitor response to defined topographies with nanoscale depths. Biomaterials 2006; 27(8): 1306-15.
[34]
Yim EK, Sheetz MP. Force-dependent cell signaling in stem cell differentiation. Stem Cell Res Ther 2012; 3(5): 41-6.
[35]
Bettinger CJ, Langer R, Borenstein JT. Engineering substrate topography at the micro‐and nanoscale to control cell function. Angew Chem Int Ed 2009; 48(30): 5406-15.
[36]
Chai C, Leong KW. Biomaterials approach to expand and direct differentiation of stem cells. Mol Ther 2007; 15(3): 467-80.
[37]
Christopherson GT, Song H, Mao H-Q. The influence of fiber diameter of electrospun substrates on neural stem cell differentiation and proliferation. Biomaterials 2009; 30(4): 556-64.
[38]
Turner L-A, Dalby MJ. Nanotopography-potential relevance in the stem cell niche. Biomater Sci 2014; 2(11): 1574-94.
[39]
Bonakdar S, Mahmoudi M, Montazeri L, et al. Cell-imprinted substrates modulate differentiation, redifferentiation, and transdifferentiation. ACS Appl Mater Interfaces 2016; 8(22): 13777-84.
[40]
Mashinchian O, Bonakdar S, Taghinejad H, et al. Cell-imprinted substrates act as an artificial niche for skin regeneration. ACS Appl Mater Interfaces 2014; 6(15): 13280-92.
[41]
Song W, Lu H, Kawazoe N, Chen G. Adipogenic differentiation of individual mesenchymal stem cell on different geometric micropatterns. Langmuir 2011; 27(10): 6155-62.
[42]
Abagnale G, Sechi A, Steger M, et al. Surface topography guides morphology and spatial patterning of induced pluripotent stem cell colonies. Stem Cell Reports 2017; 9(2): 654-66.
[43]
Dike LE, Chen CS, Mrksich M, Tien J, Whitesides GM, Ingber DE. Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cell Dev Biol Anim 1999; 35(8): 441-18.
[44]
Nelson CM, Jean RP, Tan JL, et al. Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci USA 2005; 102(33): 11594-9.
[45]
Folkman J, Moscona A. Role of cell shape in growth control. Nature 1978; 273: 345.
[46]
Ingber D. Extracellular matrix and cell shape: Potential control points for inhibition of angiogenesis. J Cell Biochem 1991; 47(3): 236-41.
[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]
Mahmoudi M, Bonakdar S, Shokrgozar MA, et al. Cell-imprinted substrates direct the fate of stem cells. ACS Nano 2013; 7(10): 8379-84.
[49]
Targosz‐Korecka M, Malek‐Zietek KE, Brzezinka GD, Jaglarz M. Morphological and nanomechanical changes in mechanosensitive endothelial cells induced by colloidal AFM probes. Scanning 2016; 38(6): 654-64.
[50]
Carrel A, Burrows MT. On the physicochemical regulation of the growth of tissues: The effects of the dilution of the medium on the growth of the spleen. J Exp Med 1911; 13(5): 562-70.
[51]
Weiss P, Garber B. Shape and movement of mesenchyme cells as functions of the physical structure of the medium: Contributions to a quantitative morphology. Proc Natl Acad Sci USA 1952; 38(3): 264-80.
[52]
Monici M, Cialdai F. The role of physical factors in cell differentiation, tissue repair and regeneration. Tissue Regeneration-From Basic Biology to Clinical Application: InTech; 2012.
[53]
Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 2009; 10(11): 778-84.
[54]
Worley K, Certo A, Wan LQ. Geometry–force control of stem cell fate. BioNanoSci 2013; 3(1): 43-51.
[55]
McKee CT, Raghunathan VK, Nealey PF, Russell P, Murphy CJ. Topographic modulation of the orientation and shape of cell nuclei and their influence on the measured elastic modulus of epithelial cells. Biophys J 2011; 101(9): 2139-46.
[56]
Nathan AS, Baker BM, Nerurkar NL, Mauck RL. Mechano-topographic modulation of stem cell nuclear shape on nanofibrous scaffolds. Acta Biomater 2011; 7(1): 57-66.
[57]
Ingber DE. Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 2003; 50(2-3): 255-66.
[58]
Mammoto T, Ingber DE. Mechanical control of tissue and organ development. Development 2010; 137(9): 1407-20.
[59]
Hall A. Rho GTPases and the actin cytoskeleton. Science 1998; 279(5350): 509-14.
[60]
Ohashi K, Fujiwara S, Mizuno K. Roles of the cytoskeleton, cell adhesion and rho signalling in mechanosensing and mechanotransduction. J Biochem 2017; 161(3): 245-54.
[61]
Roskelley C, Desprez P, Bissell M. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc Natl Acad Sci USA 1994; 91(26): 12378-82.
[62]
McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004; 6(4): 483-95.
[63]
Kilian KA, Bugarija B, Lahn BT, Mrksich M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 2010; 107(11): 4872-7.
[64]
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.
[65]
Zebda N, Dubrovskyi O, Birukov KG. Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvasc Res 2012; 83(1): 71-81.
[66]
Yu H, Lui YS, Xiong S, et al. Insights into the role of focal adhesion modulation in myogenic differentiation of human mesenchymal stem cells. Stem Cells Dev 2012; 22(1): 136-47.
[67]
Kuo JC. Mechanotransduction at focal adhesions: Integrating cytoskeletal mechanics in migrating cells. J Cell Mol Med 2013; 17(6): 704-12.
[68]
Ambriz X, de Lanerolle P, Ambrosio J. The mechanobiology of the actin cytoskeleton in stem cells during differentiation and interaction with biomaterials. Stem Cells Int 2018; 2018: 1-11.
[69]
Engler AJ, Kumar S. Mechanotransduction. Elsevier Science 2014.
[70]
Harris AR, Jreij P, Fletcher DA. Mechanotransduction by the actin Cytoskeleton: Converting mechanical stimuli into biochemical signals. Annu Rev Biophys 2018; 47: 617-31.
[71]
Kräter M, Sapudom J, Bilz N, Pompe T, Guck J, Claus C. Alterations in cell mechanics by actin cytoskeletal changes correlate with strain-specific rubella virus phenotypes for cell migration and induction of apoptosis. Cells 2018; 7(9): e136.
[72]
Geiger B, Spatz JP, Bershadsky AD. Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 2009; 10(1): 21-33.
[73]
Rajakylä EK, Vartiainen MK. Rho, nuclear actin, and actin-binding proteins in the regulation of transcription and gene expression. Small GTPases 2014; 5(1): e27539.
[74]
Huang C, Dai J, Zhang XA. Environmental physical cues determine the lineage specification of mesenchymal stem cells. Biochim Biophys Acta, Gen Subj 2015; 1850(6): 1261-6.
[75]
Amano M, Nakayama M, Kaibuchi K. Rho‐kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton 2010; 67(9): 545-54.
[76]
Li H, Wen F, Wang X, Tan LP. Role of RhoA/Rho kinase signaling pathway in microgroove induced stem cell myogenic differentiation. Biointerphases 2015; 10(2): 021003.
[77]
Gao L, McBeath R, Chen CS. Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N‐Cadherin. Stem Cells 2010; 28(3): 564-72.
[78]
Nalluri SM, Krishnan GR, Cheah C, et al. Hydrophilic polyurethane matrix promotes chondrogenesis of mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl 2015; 54: 182-95.
[79]
Woods A, Wang G, Beier F. RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J Biol Chem 2005; 280(12): 11626-34.
[80]
Keung AJ, de Juan‐Pardo EM, Schaffer DV, Kumar S. Rho GTPases mediate the mechanosensitive lineage commitment of neural stem cells. Stem Cells 2011; 29(11): 1886-97.
[81]
Eberlein M, Heusinger‐Ribeiro J, Goppelt‐Struebe M. Rho‐dependent inhibition of the induction of connective tissue growth factor (CTGF) by HMG CoA reductase inhibitors (statins). Br J Pharmacol 2001; 133(7): 1172-80.
[82]
Ravi A, Kaushik S, Ravichandran A, Pan CQ, Low BC. Epidermal growth factor activates the Rho GTPase-activating protein (GAP) Deleted in Liver Cancer 1 via focal adhesion kinase and protein phosphatase 2A. J Biol Chem 2015; 290(7): 4149-62.
[83]
Konstantinidis G, Moustakas A, Stournaras C. Regulation of myosin light chain function by BMP signaling controls actin cytoskeleton remodeling. Cell Physiol Biochem 2011; 28(5): 1031-44.
[84]
Dehmelt L, Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol 2005; 6(1): 204.
[85]
Holle AW, Engler AJ. More than a feeling: Discovering, understanding, and influencing mechanosensing pathways. Curr Opin Biotechnol 2011; 22(5): 648-54.
[86]
Kaneko-Kawano T, Suzuki K. Mechanical stress regulates gene expression via Rho/Rho-kinase signaling pathway. J Phys Fitness Sports Med 2015; 4(1): 53-61.
[87]
Suzuki M, Morita H, Ueno N. Molecular mechanisms of cell shape changes that contribute to vertebrate neural tube closure. Dev Growth Differ 2012; 54(3): 266-76.
[88]
Chen B, Co C, Ho C-C. Cell shape dependent regulation of nuclear morphology. Biomaterials 2015; 67: 129-36.
[89]
Heo S-J, Cosgrove BD, Dai EN, Mauck RL. Mechano-adaptation of the stem cell nucleus. Nucleus 2018; 9(1): 9-19.
[90]
Tapley EC, Starr DA. Connecting the nucleus to the cytoskeleton by SUN–KASH bridges across the nuclear envelope. Curr Opin Cell Biol 2013; 25(1): 57-62.
[91]
Uzer G, Thompson WR, Sen B, et al. Cell mechanosensitivity to extremely low‐magnitude signals is enabled by a LINCed nucleus. Stem Cells 2015; 33(6): 2063-76.
[92]
Uzer G, Rubin CT, Rubin J. Cell mechanosensitivity is enabled by the LINC nuclear complex. Curr Mol Biol Rep 2016; 2(1): 36-47.
[93]
Yang Y, Qu R, Fan T, et al. Cross-talk between microtubules and the linker of nucleoskeleton complex plays a critical role in the adipogenesis of human adipose-derived stem cells. Stem Cell Res Ther 2018; 9(1): 125.
[94]
Lozoya OA, Gilchrist CL, Guilak F. Universally conserved relationships between nuclear shape and cytoplasmic mechanical properties in human stem cells. Sci Rep 2016; 6: 23047.
[95]
Mazumder A, Shivashankar GV. Emergence of a prestressed eukaryotic nucleus during cellular differentiation and development. J Royal Soc Interface 2010; 7(Suppl. 3): 321-30.
[96]
Li Y, Chu JS, Kurpinski K, et al. Biophysical regulation of histone acetylation in mesenchymal stem cells. Biophys J 2011; 100(8): 1902-9.
[97]
Sun M, Spill F, Zaman MH. A computational model of YAP/TAZ mechanosensing. Biophys J 2016; 110(11): 2540-50.
[98]
Mohri Z, Hernandez ADR, Krams R. The emerging role of YAP/TAZ in mechanotransduction. J Thorac Dis 2017; 9(5): e507.
[99]
Yui S, Azzolin L, Maimets M, et al. YAP/TAZ-dependent reprogramming of colonic epithelium links ecm remodeling to tissue regeneration. Cell Stem Cell 2018; 22(1): 35-49.
[100]
Totaro A, Castellan M, Battilana G, et al. YAP/TAZ link cell mechanics to Notch signalling to control epidermal stem cell fate. Nat Commun 2017; 8: 15206.
[101]
Kumari S, Vermeulen S, van der Veer B, Carlier A, de Boer J, Subramanyam D. Shaping Cell Fate: Influence of Topographical Substratum Properties on Embryonic Stem Cells. Tissue Eng Part B Rev 2018; 24(4): 255-66.
[102]
Piccolo S, Dupont S, Cordenonsi M. The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev 2014; 94(4): 1287-312.
[103]
Kamguyan K, Katbab AA, Mahmoudi M, et al. An engineered cell-imprinted substrate directs osteogenic differentiation in stem cells. Biomater Sci 2018; 6(1): 189-99.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 14
ISSUE: 3
Year: 2019
Page: [268 - 277]
Pages: 10
DOI: 10.2174/1574888X14666181227120706
Price: $58

Article Metrics

PDF: 16
HTML: 2
EPUB: 1