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A Zebrafish Embryo Behaves both as a “Cortical Shell – Liquid Core” Structure and a Homogeneous Solid when Experiencing Mechanical Forces

Published online by Cambridge University Press:  26 September 2014

Fei Liu ,
Dan Wu  and
Ken Chen
Fei Liu*
Affiliation:
State Key Laboratory of Mechanical Transmission, College of Mechanical Engineering, Chongqing University, Chongqing 400044, China Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
Dan Wu
Affiliation:
Department of Mechanical Engineering, Tsinghua University, Beijing 100084, China, 100084
Ken Chen
Affiliation:
Department of Mechanical Engineering, Tsinghua University, Beijing 100084, China, 100084
*
*Corresponding author. [email protected]
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Abstract

Mechanical properties are vital for living cells, and various models have been developed to study the mechanical behavior of cells. However, there is debate regarding whether a cell behaves more similarly to a “cortical shell – liquid core” structure (membrane-like) or a homogeneous solid (cytoskeleton-like) when experiencing stress by mechanical forces. Unlike most experimental methods, which concern the small-strain deformation of a cell, we focused on the mechanical behavior of a cell undergoing small to large strain by conducting microinjection experiments on zebrafish embryo cells. The power law with order of 1.5 between the injection force and the injection distance indicates that the cell behaves as a homogenous solid at small-strain deformation. The linear relation between the rupture force and the microinjector radius suggests that the embryo behaves as membrane-like when subjected to large-strain deformation. We also discuss the possible reasons causing the debate by analyzing the mechanical properties of F-actin filaments.

Keywords

mechanical behaviorcell mechanical modelmicroinjection
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 20 , Issue 6 , December 2014 , pp. 1841 - 1847
Copyright
© Microscopy Society of America 2014 

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References

Boal, D. & Boal, D.H. (2012). Mechanics of the Cell. Cambridge, UK: Cambridge University Press.Google Scholar
Boudreau, N. & Bissell, M.J. (1998). Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr Opin Cell Biol 10(5), 640–646.Google Scholar
DiMilla, P., Barbee, K. & Lauffenburger, D. (1991). Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys J 60(1), 15–37.Google Scholar
Discher, D., Dong, C., Fredberg, J.J., Guilak, F., Ingber, D., Janmey, P., Kamm, R.D., Schmid-Schönbein, G.W. & Weinbaum, S. (2009). Biomechanics: cell research and applications for the next decade. Ann Biomed Eng 37(5), 847–859.CrossRefGoogle Scholar
Dong, C., Skalak, R. & Sung, K. (1991). Cytoplasmic rheology of passive neutrophils. Biorheology 28(6), 557–567.Google Scholar
Dong, C., Skalak, R., Sung, K., Schmid-Schönbein, G. & Chien, S. (1988). Passive deformation analysis of human leukocytes. J Biomech Eng 110(1), 27–36.Google Scholar
Fletcher, D.A. & Mullins, R.D. (2010). Cell mechanics and the cytoskeleton. Nature 463(7280), 485–492.CrossRefGoogle ScholarPubMed
Georges, P.C., Miller, W.J., Meaney, D.F., Sawyer, E.S. & Janmey, P.A. (2006). Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J 90(8), 3012–3018.Google Scholar
Gibson, L.J. & Ashby, M.F. (1999). Cellular Solids: Structure and Properties. Cambridge, UK: Cambridge University Press.Google Scholar
Grinnell, F. & Petroll, W.M. (2010). Cell motility and mechanics in three-dimensional collagen matrices. Annu Rev Cell Dev Biol 26, 335–361.Google Scholar
Lauffenburger, D.A. & Horwitz, A.F. (1996). Cell migration: review a physically integrated molecular process. Cell 84, 359–369.Google Scholar
Lim, C., Zhou, E., Li, A., Vedula, S. & Fu, H. (2006a). Experimental techniques for single cell and single molecule biomechanics. Mater Sci Eng C 26(8), 1278–1288.Google Scholar
Lim, C., Zhou, E. & Quek, S. (2006b). Mechanical models for living cells—a review. J Biomech 39(2), 195–216.Google Scholar
Liu, Z., Tan, J.L., Cohen, D.M., Yang, M.T., Sniadecki, N.J., Ruiz, S.A., Nelson, C.M. & Chen, C.S. (2010). Mechanical tugging force regulates the size of cell–cell junctions. Proc Natl Acad Sci USA 107(22), 9944–9949.Google Scholar
Mammoto, T. & Ingber, D.E. (2010). Mechanical control of tissue and organ development. Development 137(9), 1407–1420.Google Scholar
Matsuoka, H., Shimoda, S., Ozaki, M., Mizukami, H., Shibusawa, M., Yamada, Y. & Saito, M. (2007). Semi-quantitative expression and knockdown of a target gene in single-cell mouse embryonic stem cells by high performance microinjection. Biotechnol Lett 29(3), 341–350.Google Scholar
Mijailovich, S.M., Kojic, M., Zivkovic, M., Fabry, B. & Fredberg, J.J. (2002). A finite element model of cell deformation during magnetic bead twisting. J Appl Physiol 93(4), 1429–1436.Google Scholar
Nasevicius, A. & Ekker, S.C. (2000). Effective targeted gene ‘knockdown’ in zebrafish. Nat Genet 26(2), 216–220.CrossRefGoogle ScholarPubMed
Palmer, J.S. & Boyce, M.C. (2008). Constitutive modeling of the stress–strain behavior of F-actin filament networks. Acta Biomater 4(3), 597–612.Google Scholar
Petersen, N.O., McConnaughey, W.B. & Elson, E.L. (1982). Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B. Proc Natl Acad Sci USA 79(17), 5327–5331.Google Scholar
Reilly, G.C. & Engler, A.J. (2010). Intrinsic extracellular matrix properties regulate stem cell differentiation. J Biomech 43(1), 55–62.Google Scholar
Schmid-Schönbein, G., Sung, K., Tözeren, H., Skalak, R. & Chien, S. (1981). Passive mechanical properties of human leukocytes. Biophys J 36(1), 243–256.Google Scholar
Shin, D. & Athanasiou, K. (1999). Cytoindentation for obtaining cell biomechanical properties. J Orthopaed Res 17(6), 880–890.Google Scholar
Stamenović, D. & Ingber, D.E. (2002). Models of cytoskeletal mechanics of adherent cells. Biomech Model Mechanobiol 1(1), 95–108.Google Scholar
Stricker, J., Falzone, T. & Gardel, M.L. (2010). Mechanics of the F-actin cytoskeleton. J Biomech 43(1), 9–14.Google Scholar
Tan, Y., Sun, D., Huang, W. & Cheng, S.H. (2008). Mechanical modeling of biological cells in microinjection. IEEE Trans Nanobioscience 7(4), 257–266.Google Scholar
Theret, D.P., Levesque, M., Sato, M., Nerem, R. & Wheeler, L. (1988). The application of a homogeneous half-space model in the analysis of endothelial cell micropipette measurements. J Biomech Eng 110(3), 190–199.Google Scholar
Tomasini, M.D., Rinaldi, C. & Tomassone, M.S. (2010). Molecular dynamics simulations of rupture in lipid bilayers. Exp Biol Med 235(2), 181–188.Google Scholar
Touhami, A., Nysten, B. & Dufrêne, Y.F. (2003). Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy. Langmuir 19(11), 4539–4543.Google Scholar
Trepat, X., Wasserman, M.R., Angelini, T.E., Millet, E., Weitz, D.A., Butler, J.P. & Fredberg, J.J. (2009). Physical forces during collective cell migration. Nat Phys 5(6), 426–430.Google Scholar
Trickey, W.R., Lee, G.M. & Guilak, F. (2000). Viscoelastic properties of chondrocytes from normal and osteoarthritic human cartilage. J Orthop Res 18(6), 891–898.CrossRefGoogle ScholarPubMed
Tsai, M.A., Frank, R.S. & Waugh, R.E. (1993). Passive mechanical behavior of human neutrophils: power-law fluid. Biophys J 65(5), 2078–2088.Google Scholar
van der Merwe, P.A. & Dushek, O. (2010). Mechanisms for T cell receptor triggering. Nat Rev Immunol 11(1), 47–55.Google Scholar
Wang, K. & Sun, D. (2012). Influence of semiflexible structural features of actin cytoskeleton on cell stiffness based on actin microstructural modeling. J Biomech 45(11), 1900–1908.Google Scholar
Wang, N., Butler, J.P. & Ingber, D.E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124–1127.Google Scholar
Wang, W., Liu, X., Gelinas, D., Ciruna, B. & Sun, Y. (2007). A fully automated robotic system for microinjection of zebrafish embryos. PLoS One 2(9), e862.Google Scholar
Westerfield, M., Zon, L.I. & Detrich, H.W. III (2009). Essential Zebrafish Methods. New York, USA: Academic Press.Google Scholar
Yeung, A. & Evans, E. (1989). Cortical shell-liquid core model for passive flow of liquid-like spherical cells into micropipets. Biophys J 56(1), 139–149.CrossRefGoogle ScholarPubMed
Zhang, Y. & Yu, L.-C. (2008). Microinjection as a tool of mechanical delivery. Curr Opin Biotech 19(5), 506–510.Google Scholar
Zhelev, D.V., Needham, D. & Hochmuth, R.M. (1994). Role of the membrane cortex in neutrophil deformation in small pipets. Biophys J 67(2), 696–705.Google Scholar

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