Cell Differentiation Through Tissue Elasticity-coupled, Myosin-driven Remodeling

Overview

Journal Curr Opin Cell Biol

Publisher Elsevier

Specialty Cell Biology

Date 2008 Oct 18

PMID 18926907

Citations 33

Authors

Allison L Zajac

Dennis E Discher

Affiliations

Soon will be listed here.

Abstract

Cells may lack eyes to see and ears to hear, but cells do seem to have a sense of 'touch' that allows them to feel their microenvironment. This is achieved in part through contractility coupled adhesion to physically flexible 'soft' tissue. Here we summarize some of the known variations in elasticity of solid tissue and review some of the long-term effects of cells 'feeling' this elasticity, focusing on differentiation processes of both committed cell types and stem cells. We then highlight what is known of molecular remodeling in cells under stress on short time scales. Key roles for forces generated by ubiquitous and essential myosin-II motors in feedback remodeling are emphasized throughout.

Citing Articles

Tough gelatine hydrogels reinforced with silk fibroin nanofiber.

Shibata M, Okahisa Y Heliyon. 2024; 10(20):e39101.

PMID: 39640684 PMC: 11620089. DOI: 10.1016/j.heliyon.2024.e39101.

Key role for Rac in the early transcriptional response to extracellular matrix stiffness and stiffness-dependent repression of ATF3.

Dang I, Brazzo J, Bae Y, Assoian R J Cell Sci. 2023; 136(19).

PMID: 37737020 PMC: 10617619. DOI: 10.1242/jcs.260636.

Vimentin Intermediate Filaments Mediate Cell Morphology on Viscoelastic Substrates.

Swoger M, Gupta S, Charrier E, Bates M, Hehnly H, Patteson A ACS Appl Bio Mater. 2022; 5(2):552-561.

PMID: 34995457 PMC: 8864613. DOI: 10.1021/acsabm.1c01046.

The Emerging Role of Decellularized Plant-Based Scaffolds as a New Biomaterial.

Harris A, Lacombe J, Zenhausern F Int J Mol Sci. 2021; 22(22).

PMID: 34830229 PMC: 8625747. DOI: 10.3390/ijms222212347.

A State-of-the-Art of Functional Scaffolds for 3D Nervous Tissue Regeneration.

Tupone M, dAngelo M, Castelli V, Catanesi M, Benedetti E, Cimini A Front Bioeng Biotechnol. 2021; 9:639765.

PMID: 33816451 PMC: 8012845. DOI: 10.3389/fbioe.2021.639765.

References

Schwaiger I, Sattler C, Hostetter D, Rief M . The myosin coiled-coil is a truly elastic protein structure. Nat Mater. 2003; 1(4):232-5. DOI: 10.1038/nmat776. View

Winer J, Janmey P, McCormick M, Funaki M . Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng Part A. 2008; 15(1):147-54. DOI: 10.1089/ten.tea.2007.0388. View

Engler A, Bacakova L, Newman C, Hategan A, Griffin M, Discher D . Substrate compliance versus ligand density in cell on gel responses. Biophys J. 2003; 86(1 Pt 1):617-28. PMC: 1303831. DOI: 10.1016/S0006-3495(04)74140-5. View

Law R, Harper S, Speicher D, Discher D . Influence of lateral association on forced unfolding of antiparallel spectrin heterodimers. J Biol Chem. 2004; 279(16):16410-6. DOI: 10.1074/jbc.M313107200. View

Gefen A, Margulies S . Are in vivo and in situ brain tissues mechanically similar?. J Biomech. 2004; 37(9):1339-52. DOI: 10.1016/j.jbiomech.2003.12.032. View

Engler A, Griffin M, Sen S, Bonnemann C, Sweeney H, Discher D . Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol. 2004; 166(6):877-87. PMC: 2172122. DOI: 10.1083/jcb.200405004. View

Conti M, Even-Ram S, Liu C, Yamada K, Adelstein R . Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J Biol Chem. 2004; 279(40):41263-6. DOI: 10.1074/jbc.C400352200. View

Hu S, Eberhard L, Chen J, Love J, Butler J, Fredberg J . Mechanical anisotropy of adherent cells probed by a three-dimensional magnetic twisting device. Am J Physiol Cell Physiol. 2004; 287(5):C1184-91. DOI: 10.1152/ajpcell.00224.2004. View

Bhasin N, Carl P, Harper S, Feng G, Lu H, Speicher D . Chemistry on a single protein, vascular cell adhesion molecule-1, during forced unfolding. J Biol Chem. 2004; 279(44):45865-74. DOI: 10.1074/jbc.M404103200. View

10.

CHIANCONE E, Currell D, VECCHINI P, Antonini E, Wyman J . Kinetics of the reaction of the "masked" and "free" sulfhydryl groups of human hemoglobin with p-mercuribenzoate. J Biol Chem. 1970; 245(16):4105-11. View

11.

Wang H, Dembo M, Wang Y . Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol. 2000; 279(5):C1345-50. DOI: 10.1152/ajpcell.2000.279.5.C1345. View

12.

Deroanne C, Lapiere C, Nusgens B . In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovasc Res. 2001; 49(3):647-58. DOI: 10.1016/s0008-6363(00)00233-9. View

13.

Balaban N, Schwarz U, Riveline D, Goichberg P, Tzur G, Sabanay I . Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol. 2001; 3(5):466-72. DOI: 10.1038/35074532. View

14.

Furuike S, Ito T, Yamazaki M . Mechanical unfolding of single filamin A (ABP-280) molecules detected by atomic force microscopy. FEBS Lett. 2001; 498(1):72-5. DOI: 10.1016/s0014-5793(01)02497-8. View

15.

Wang N, Naruse K, Stamenovic D, Fredberg J, Mijailovich S, Tolic-Norrelykke I . Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci U S A. 2001; 98(14):7765-70. PMC: 35416. DOI: 10.1073/pnas.141199598. View

16.

Cukierman E, Pankov R, Stevens D, Yamada K . Taking cell-matrix adhesions to the third dimension. Science. 2001; 294(5547):1708-12. DOI: 10.1126/science.1064829. View

17.

Beningo K, Wang Y . Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J Cell Sci. 2002; 115(Pt 4):849-56. DOI: 10.1242/jcs.115.4.849. View

18.

Silverman J, Harbury P . Rapid mapping of protein structure, interactions, and ligand binding by misincorporation proton-alkyl exchange. J Biol Chem. 2002; 277(34):30968-75. DOI: 10.1074/jbc.M203172200. View

19.

Collinsworth A, Zhang S, Kraus W, Truskey G . Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Physiol Cell Physiol. 2002; 283(4):C1219-27. DOI: 10.1152/ajpcell.00502.2001. View

20.

Flanagan L, Ju Y, Marg B, Osterfield M, Janmey P . Neurite branching on deformable substrates. Neuroreport. 2002; 13(18):2411-5. PMC: 2408859. DOI: 10.1097/00001756-200212200-00007. View