Control of stem cell fate by physical interactions with the extracellular matrix

Guilak, Farshid<sup>1,2</sup>; Cohen, Daniel M.<sup>3</sup>; Estes, Bradley T.<sup>1,2</sup>; Gimble, Jeffrey M.<sup>4</sup>; Liedtke, Wolfgang<sup>5</sup>; Chen, Christopher S.<sup>3</sup>

Affiliations

¹Department of Surgery, Duke University Medical Center, Durham, NC 27710, USA

²Department of Biomedical Engineering, Duke University Medical Center, Durham, NC 27710, USA

³Department of Bioengineering University of Pennsylvania, Philadelphia, PA 19104, USA

⁴Stem Cell Laboratory, Pennington Biomedical Research Center, Louisiana State University System, Baton Rouge, LA 70808, USA

⁵Department of Medicine, Duke University Medical Center, Durham, NC 27710, USA

Abstract

A diverse array of environmental factors contributes to the overall control of stem cell activity. In particular, new data continue to mount on the influence of the extracellular matrix (ECM) on stem cell fate through physical interactions with cells, such as the control of cell geometry, ECM geometry/topography at the nanoscale, ECM mechanical properties, and the transmission of mechanical or other biophysical factors to the cell. Here, we review some of the physical processes by which cues from the ECM can influence stem cell fate, with particular relevance to the use of stem cells in tissue engineering and regenerative medicine.

Links

DOI: 10.1016/j.stem.2009.06.016

PubMed: 19570510

PubMedCentral: PMC2768283

WoS: 000267879200007

History

Revised: 2009-07-2

Online: 2009-07-2

Cited Works (17)

Year	Entry
1998	Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res. January 10, 1998;238(1):265-272.
2004	McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell. April 2004;6(4):483-495.
2001	Elder SH, Goldstein SA, Kimura JH, Soslowsky LJ, Spengler DM. Chondrocyte differentiation is modulated by frequency and duration of cyclic compressive loading. Ann Biomed Eng. June 2001;29(6):476-482.
2003	Angele P, Yoo JU, Smith C, Mansour J, Jepsen KJ, Nerlich M, Johnstone B. Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res. May 2003;21(3):451-457.
2005	Discher DE, Janmey P, Wang Y-l. Tissue cells feel and respond to the stiffness of their substrate. Science. November 18, 2005;310(5751):1139-1143.
1982	Benya PD, Shaffer JD. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell. August 1982;30(1):215-224.
2003	Simmons CA, Matlis S, Thornton AJ, Chen S, Wang C-Y, Mooney DJ. Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J Biomech. August 2003;36(8):1087-1096.
2002	Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun. January 18, 2002;290(2):763-769.
1997	Pelham RJ Jr, Wang Y-l. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA. December 9, 1997;94(25):13661-13665.
1995	Guilak F, Ratcliffe A, Mow VC. Chondrocyte deformation and local tissue strain in articular cartilage: a confocal microscopy study. J Orthop Res. May 1995;13(3):410-421.
2000	Elder SH, Kimura JH, Soslowsky LJ, Lavagnino M, Goldstein SA. Effect of compressive loading on chondrocyte differentiation in agarose cultures of chick limb-bud cells. J Orthop Res. January 2000;18(1):78-86.
2004	Huang CC, Hagar KL, Frost LE, Sun Y, Cheung HS. Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells. May 2004;22(3):313-323.
2004	Awad HA, Wickham MQ, Leddy HA, Gimble JM, Guilak F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials. July 2004;25(16):3211-3222.
2007	Mauck RL, Byers BA, Yuan X, Tuan RS. Regulation of cartilaginous ECM gene transcription by chondrocytes and MSCs in 3D culture in response to dynamic loading. Biomech Model Mechanobiol. January 2007;6(1-2):113-125.
2007	David V, Martin A, Lafage-Proust M-H, Malaval L, Peyroche S, Jones DB, Vico L, Guignandon A. Mechanical loading down-regulates peroxisome proliferator-activated receptor γ in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology. May 2007;148(5):2553-2562.
2006	Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. August 25, 2006;126(4):P677-P689.
2007	Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. November 2007;213(2):341-347.

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2010	Jacobs CR, Temiyasathit S, Castillo AB. Osteocyte mechanobiology and pericellular mechanics. Annu Rev Biomed Eng. 2010;12:369-400.
2010	Estes BT, Diekman BO, Gimble JM, Guilak F. Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc. July 2010;5(7):1294-1311.
2013	Miller GJ. Mechanoregulation and Mechanotransduction in Skeletal Tissue Differentiation [Master's thesis]. Boston University; 2013.
2013	Chang H. Toward Clinical Stem Cell Sourcing and Definition of Prescriptive Biophysical Protocols to Guide Stem Cell Fate During Healing [PhD thesis]. Cleveland, OH: Case Western Reserve University; August 2013.
2016	Rusin MC. Impact of Ionizing Radiation Dose and Dose Rate on Adipose Stem Cell Function [PhD thesis]. Clemson, SC: Clemson University; August 2016.
2009	Gilchrist CL. The Effects of Extracellular Matrix Mechanics and Composition on the Behaviors of Nucleus Pulposus Cells from the Intervertebral Disc [PhD thesis]. Duke University; 2009.
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2012	Allen J. Modeling Cartilage Extracellular Matrix Stiffness: A Potent Regulator of TGFbeta-Inducible Chondrocyte Differentiation [PhD thesis]. San Francisco, University of California; 2012.
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2015	Heo SC. Differentiation Induces Dynamic Alterations in Mesenchymal Stem Cell Nuclear Architecture and Mechanotransduction [PhD thesis]. Philadelphia, PA: University of Pennsylvania; 2015.