Cells as liquid motors: Mechanosensitivity emerges from collective dynamics of actomyosin cortex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 9, 2015, Pages 2740-2745

  Étienne, Jocelyn ^a,b   Fouchard, Jonathan ^c   Mitrossilis, Démosthène ^c   Bufi, Nathalie ^c   Durand Smet, Pauline ^c   Asnacios, Atef ^c  

^a UNIV GRENOBLE ALPES   (France)

^b LIPHY   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cell spreading; Cytoskeleton; Retrograde flow; Rigidity sensing; Smart material

Indexed keywords

ACTIN; ALPHA ACTININ; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ADULT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SHAPE; CONTROLLED STUDY; CYTOSKELETON; DYNAMICS; EMBRYO; ENERGY; LAMELLIPODIUM; MECHANICAL STRESS; MECHANOTRANSDUCTION; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE RIGIDITY; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; TURNOVER TIME; YOUNG MODULUS; ANIMAL; BIOLOGICAL MODEL; CELL LINE; METABOLISM; MOUSE; MUSCLE STRENGTH; PHYSIOLOGY;

ACTIN CYTOSKELETON; ACTOMYOSIN; ANIMALS; CELL LINE; MECHANOTRANSDUCTION, CELLULAR; MICE; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE STRENGTH; MYOSINS; RATS;

EID: 84924352126     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417113112     Document Type: Article

References (44)

1. Turner FR, Mahowald AP (1977) Scanning electron microscopy of Drosophila melanogaster embryogenesis. II. Gastrulation and segmentation. Dev Biol 57(2):403-416
2. Engler A, et al. (2004) Substrate compliance versus ligand density in cell on gel responses. Biophys J 86(1 Pt 1):617-628
3. Yeung T, et al. (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60(1):24-34
4. Saez A, Ghibaudo M, Buguin A, Silberzan P, Ladoux B (2007) Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc Natl Acad Sci USA 104(20):8281-8286
5. Zhong J, et al. (2012) NEDD9 stabilizes focal adhesions, increases binding to the extracellular matrix and differentially effects 2D versus 3D cell migration. PLoS ONE 7(4): e35058
6. Young PE, Richman AM, Ketchum AS, Kiehart DP (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7(1):29-41
7. Pelham RJ, Jr, Wang Yl (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94(25):13661-13665
8. Chicurel ME, Chen CS, Ingber DE (1998) Cellular control lies in the balance of forces. Curr Opin Cell Biol 10(2):232-239
9. Zajac AL, Discher DE (2008) Cell differentiation through tissue elasticity-coupled, myosin-driven remodeling. Curr Opin Cell Biol 20(6):609-615
10. Cai Y, et al. (2010) Cytoskeletal coherence requires myosin-IIA contractility. J Cell Sci 123(Pt 3):413-423
11. Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310(5751):1139-1143
12. Vogel V, Sheetz M (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7(4):265-275
13. Mitrossilis D, et al. (2009) Single-cell response to stiffness exhibits muscle-like behavior. Proc Natl Acad Sci USA 106(43):18243-18248
14. Mitrossilis D, et al. (2010) Real-time single-cell response to stiffness. Proc Natl Acad Sci USA 107(38):16518-16523
15. Webster KD, Crow A, Fletcher DA (2011) An AFM-based stiffness clamp for dynamic control of rigidity. PLoS ONE 6(3):e17807
16. Crow A, et al. (2012) Contractile equilibration of single cells to step changes in extracellular stiffness. Biophys J 102(3):443-451
17. Trichet L, et al. (2012) Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness. Proc Natl Acad Sci USA 109(18):6933-6938
18. Rossier OM, et al. (2010) Force generated by actomyosin contraction builds bridges between adhesive contacts. EMBO J 29(6):1055-1068
19. Zemel A, Rehfeldt F, Brown AEX, Discher DE, Safran SA (2010) Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 6(6):468-473
20. Marcq P, Yoshinaga N, Prost J (2011) Rigidity sensing explained by active matter theory. Biophys J 101(6):L33-L35
21. Yamamoto M (1956) The visco-elastic properties of network structure: I. General formalism. J Phys Soc Jpn 11(4):413-421
22. Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Chem 7:255-318
23. Kovács M, Thirumurugan K, Knight PJ, Sellers JR (2007) Load-dependent mechanism of nonmuscle myosin 2. Proc Natl Acad Sci USA 104(24):9994-9999
24. Yao NY, et al. (2013) Stress-enhanced gelation: A dynamic nonlinearity of elasticity. Phys Rev Lett 110(1):018103
25. Borau C, Kim T, Bidone T, García-Aznar JM, Kamm RD (2012) Dynamic mechanisms of cell rigidity sensing: Insights from a computational model of actomyosin networks. PLoS ONE 7(11):e49174
26. Parameswaran H, Lutchen KR, Suki B (2014) A computational model of the response of adherent cells to stretch and changes in substrate stiffness. J Appl Physiol (1985) 116(7):825-834
27. Mukhina S, Wang YL, Murata-Hori M (2007) a-actinin is required for tightly regulated remodeling of the actin cortical network during cytokinesis. Dev Cell 13(4):554-565
28. Fritzsche M, Lewalle A, Duke T, Kruse K, Charras G (2013) Analysis of turnover dynamics of the submembranous actin cortex. Mol Biol Cell 24(6):757-767
29. Vaziri A, Gopinath A (2008) Cell and biomolecular mechanics in silico. Nat Mater 7(1): 15-23
30. Harris AK, Wild P, Stopak D (1980) Silicone rubber substrata: A new wrinkle in the study of cell locomotion. Science 208(4440):177-179
31. He X, Dembo M (1997) On the mechanics of the first cleavage division of the sea urchin egg. Exp Cell Res 233(2):252-273
32. Kruse K, Joanny JF, Jülicher F, Prost J, Sekimoto K (2005) Generic theory of active polar gels: A paradigm for cytoskeletal dynamics. Eur Phys J E Soft Matter 16(1):5-16
33. Soares e Silva M, et al. (2011) Active multistage coarsening of actin networks driven by myosin motors. Proc Natl Acad Sci USA 108(23):9408-9413.
34. Fouchard J, et al. (2014) Three-dimensional cell body shape dictates the onset of traction force generation and growth of focal adhesions. Proc Natl Acad Sci USA 111(36):13075-13080
35. Saez A, Buguin A, Silberzan P, Ladoux B (2005) Is the mechanical activity of epithelial cells controlled by deformations or forces? Biophys J 89(6):L52-L54
36. Mitchison TJ, Cramer LP (1996) Actin-based cell motility and cell locomotion. Cell 84(3):371-379
37. Fournier MF, Sauser R, Ambrosi D, Meister JJ, Verkhovsky AB (2010) Force transmission in migrating cells. J Cell Biol 188(2):287-297
38. Pollard TD, Blanchoin L, Mullins RD (2000) Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 29:545-576
39. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305(5691): 1782-1786
40. Small JV, Resch GP (2005) The comings and goings of actin: Coupling protrusion and retraction in cell motility. Curr Opin Cell Biol 17(5):517-523
41. Fällman E, Schedin S, Jass J, Uhlin BE, Axner O (2005) The unfolding of the P pili quaternary structure by stretching is reversible, not plastic. EMBO Rep 6(1):52-56
42. Federle W, Brainerd EL, McMahon TA, Hölldobler B (2001) Biomechanics of the movable pretarsal adhesive organ in ants and bees. Proc Natl Acad Sci USA 98(11): 6215-6220
43. Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci 126(843):136-195
44. Desprats N, Guiroy A, Asnacios A (2006) Microplates-based rheometer for a single living cell. Rev Sci Instrum 77:055111