Journal of Biological Physics

, Volume 30, Issue 4, pp 345–364 | Cite as

Cell Movements and Mechanical Force Distribution During the Migration of Dictyostelium Slugs

  • Jean-Paul Rieu
  • Catherine Barentin
  • Satoshi Sawai
  • Yasuo Maeda
  • Yasuji Sawada
Article

Abstract

Migration of Dictyostelium discoideum slugs results from coordinated movement of their constituent cells. It is generally assumed that each cell contributes to the total motive force of the slug. However, the basic mechanisms by which mechanical forces (traction and resistive forces) are transmitted to the substrate, their magnitude and their location, are largely unknown. In this work, we performed detailed observations of cell movements by fluorescence microscopy using two-dimensional (2D) slugs. We show that 2D slugs share most of the properties of 3D ones. In particular, waves of movement propagate in long 2D slugs, and slug speed correlates with slug length as found in 3D slugs. We also present the first measurements of the distribution of forces exerted by 2D and 3D slugs using the elastic substrate method. Traction forces are mainly exerted in the central region of the slug. The large perpendicular forces around slug boundary and the existence of parallel resistive forces in the tip and/or the tail suggest an important role of the sheath in the transmission of forces to the substrate.

Key words

Dictyostelium slug elastic substrate wave of movement traction force slime sheath 

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References

  1. 1.
    Dormann, D., Siegert, F. and Weijer, C.J.: Becoming Multicellular by Aggregation; The Morphogenesis of the Social Amoebae Dicyostelium Discoideum, J. Biol. Phys. 28 (2002), 765–780.Google Scholar
  2. 2.
    Maeda, Y.:Role of Cyclic AMP in the Polarized Movement of the Migrating Pseudoplasmodium of Dictyostelium discoideum, Dev. Growth Differ. 19(1977), 201–205.Google Scholar
  3. 3.
    Siegert, F. and Weijer, C.J.: Three-Dimensional Scroll Waves Organize Dictyostelium Slugs, Proc. Natl. Acad. Sci. USA. 89(1992), 6433–6437.Google Scholar
  4. 4.
    Breen, E.J. and Williams, K.L.: Optical Flow Analysis of the Ventral Cellular Layer of the Migrating Dictyostelium discoideum Slug, Microbiology 140(1994), 1241–1252.Google Scholar
  5. 5.
    Dormann, D., Siegert, F. and Weijer, C.J.: Analysis of Cell Movement During the Culmination Phase of Dictyostelium Development, Development 122(1996), 761–769.Google Scholar
  6. 6.
    Dormann, D. and Weijer, C.J.: Propagating Chemoattractant Waves Coordinate Cell Movement in Dictyostelium Slugs, Development 128(2001), 4535–4543.Google Scholar
  7. 7.
    Inouye, K. and Takeuchi, I.: Motive Force of the Migrating Pseudoplasmodium of the Cellular Slime Mould Dictyostelium discoideum. J. Cell Sci. 41(1980), 53–64; Inouye, K.: Measurement of the Motive Force of the Migrating Slug of Dictyostelium Discoideum by a Centrifuge Method, Protoplasma 121(1984), 171–177.Google Scholar
  8. 8.
    Eliott, S., Vardy, P.H. and Williams, K.L.: The Distribution of Myosin II in Dictyostelium Discoideum Slug Cells, J. Cell Biol. 115(1991), 1267–1274.Google Scholar
  9. 9.
    Early, A., Abe, T. and Williams, K.L.: Evidence for Positional Differentiation of Prestalk Cells and for a Morphogenetic Gradient in Dictyostelium, Cell 83(1995), 91–99.Google Scholar
  10. 10.
    Dembo, M. and Wang, Y.-L.: Stresses at the Cell-to-Substrate Interface During Locomotion of Fibroblasts, Biophys. J. 76(1999), 2307–2316.Google Scholar
  11. 11.
    Schwarz, U.S., Balaban, N.Q., Riveline, D., Bershadsky, A., Geiger, B. and Safran, S. A.: Calculation of Forces at Focal Adhesions from Elastic Substrate Data: The Effect of Localized Force and the Need for Regularization, Biophys. J. 205(2002), 2583–2590.Google Scholar
  12. 12.
    Beningo, K.A. and Wang,Y.–L.: Flexible Substrata for the Detection of Cellular Traction Forces, Trends Cell Bio. 12(2002), 72–84.Google Scholar
  13. 13.
    Uchida, K.S., Kitanishi-Yumura, T. and Yumura, S.: Myosin II Contributes to the Posterior Contraction and the Anterior Extension During the Retraction Phase in Migrating Dictyostelium Cells, J. Cell Sci. 116(2003), 51–60.Google Scholar
  14. 14.
    Bonner, J.T.: A Way of Following Individual Cells in the Migrating Slugs of Dictyostelium Discoideum, Proc. Natl. Acad. Sci. USA. 95(1998), 9355–9359.Google Scholar
  15. 15.
    Rieu, J.-P., Tsuchiya, K., Sawai, S., Maeda, Y. and Sawada. Y.: Cell Movements and Traction Forces on Elastic Substrates During the Migration of 2-Dimensional Dictyostelium Slugs, J. Biol. Phys. 29(2003), SN1–SN4.Google Scholar
  16. 16.
    Umeda, T. and Inouye, K.: Theoretical Model for Morphgenesis and Cell Sorting in Dictyostelium Discoideum, Physica D. 126(1999), 189–200.Google Scholar
  17. 17.
    Palsson, E. and Othmer, H.G.: A Model for Individual and Collective Cell Movement in Dictyostelium Discoideum, Proc. Natl. Acad. Sci. USA. 97(2000), 10448–10453.Google Scholar
  18. 18.
    Vasiev, B. and Weijer, C.J.: Modelling of Dictyostelium Discoideum Slug migration, J. Theor. Biol. 223(2002), 347–59.Google Scholar
  19. 19.
    Marée, A.F., Panfilov, A.V. and Hogeweg, P.: Migration and Thermotaxis of Dictyostelium Discoideum Slugs: A Model Study, J Theor Biol. 199(1999), 297–309.Google Scholar
  20. 20.
    Bonner, J.T.: Evidence for the Formation of Cell Aggregates by Chemotaxis in the Development of the Slime Mold Dictyostelium Discoideum, J. Exp. Zool. 106(1947), 1–26.Google Scholar
  21. 21.
    Sawai, S., Hirano, T., Maeda, Y. and Sawada, Y.: Rapid Patterning and Zonal Differentiation in a Two-Dimensional Dictyostelium Cell Mass: The Role of pH and Ammonia, J. Exp. Biol. 205(2002), 2583–2590.Google Scholar
  22. 22.
    Rieu, J.-P., Upadhyaya, A., Glazier, J.A., Ouchi, N.B. and Sawada, Y.: Diffusion and Deformations of Single Hydra Cells in Cellular Aggregates, Biophys. J. 79(2000), 1903–1914.Google Scholar
  23. 23.
    Pelham, R.J. and Wang, Y-L.: High Resolution Detection of Mechanical Forces Exerted by Locomoting Fibroblasts on the Substrate, Mol. Biol. Cell. 10(1999), 935—945.Google Scholar
  24. 24.
    Landau, L.D. and Lifshitz, E.M.: Theory of Elasticity, (3rd edn.), J.B. Sykes and W.H. Reid (translators), Pergamon Press, Oxford, UK, 1986.Google Scholar
  25. 25.
    Dembo, M., Oliver, T., Ishihara, A. and Jacobson, K.: Imaging the Traction Stresses Exerted by Locomoting Cells with the Elastic Substratum Method, Biophys J. 4(1996), 2008–2022.Google Scholar
  26. 26.
    Butler, J.P., Tolic-Norrelykke, I.M., Fabry, B. and Fredberg, J.J.:Traction Fields, Moments, and Strain Energy that Cells Exert on their Surroundings, Am. J. Physiol. Cell Physiol. 282(2002), C595–C605.Google Scholar
  27. 27.
    Press, W.H., Teukolsky, S.A., Vetterling, W.T. and Flannery, B.P.: Numerical Recipes in FORTRAN: The Art of Scientific Computing(2nd edn.), Cambridge University Press, Cambridge, 1992, pp. 63–78.Google Scholar
  28. 28.
    Bonner, J.T., Fey, P. and Cox, E.C.: Expression of Prestalk and Prespore Proteins in Minute, Two-Dimensional Dictyostelium Slugs, Mech. Dev. 88(1999), 253–254.Google Scholar
  29. 29.
    Loomis, W.F. (1972)Role of the Surface Sheath in the Control of Morphogenesis in Dictyostelium DiscoideumNaure New Bio2406S9Google Scholar
  30. 30.
    Loomis, W.F.: Role of the Surface Sheath in the Control of Morphogenesis in Dictyostelium Discoideum, Naure New Bio. 240(1972), 6–S9.Google Scholar
  31. 31.
    Durston, A.J. and Vork, F.: A Cinematographical Study of the Development of Vitally Stained Dictyostelium Discoideum, J. Cell Sci. 36(1979), 261–279.Google Scholar
  32. 32.
    Shaffer, B.M.: Cell Movement Within Aggregates of the Slime Mould Dictyostelium Discoideum Revealed by Surface Markers, J. Embryol. Exp. Morphol. 13(1965), 97–117.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • Jean-Paul Rieu
    • 1
  • Catherine Barentin
    • 1
  • Satoshi Sawai
    • 2
  • Yasuo Maeda
    • 3
  • Yasuji Sawada
    • 4
  1. 1.Laboratoire de Physique de la Matière Condensée et des NanostructuresUniversité Claude Bernard Lyon I and CNRSVilleurbanne CedexFrance
  2. 2.Graduate School of Information SciencesTohoku UniversitySendaiJapan
  3. 3.Department of Developmental Biology and Neurosciences, Graduate School of Life SciencesTohoku UniversitySendaiJapan
  4. 4.Tohoku Institute of TechnologyTaihakuJapan

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