Skip to main content
SpringerLink
Log in

Morphogenesis can be driven by properly parametrised mechanical feedback

  • Regular Article
  • Published:
The European Physical Journal E Aims and scope Submit manuscript

Abstract

A fundamental problem of morphogenesis is whether it presents itself as a succession of links that are each driven by its own specific cause-effect relationship, or whether all of the links can be embraced by a common law that is possible to formulate in physical terms. We suggest that a common biophysical background for most, if not all, morphogenetic processes is based upon feedback between mechanical stresses (MS) that are imposed to a given part of a developing embryo by its other parts and MS that are actively generated within that part. The latter are directed toward hyper-restoration (restoration with an overshoot) of the initial MS values. We show that under mechanical constraints imposed by other parts, these tendencies drive forth development. To provide specificity for morphogenetic reactions, this feedback should be modulated by long-term parameters and/or initial conditions that are set up by genetic factors. The experimental and model data related to this concept are reviewed.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. R.D. Mullins, Cold Spring Hrb Persp Biol 2, a003392 (2010).

    Google Scholar 

  2. J.C Maxwell, Matter and Motion (Dover, London, 1991).

  3. A.G. Gurwitsch, Arch Entwmech Org. 51, 383 (1922).

    Google Scholar 

  4. A.G. Gurwitsch, A Theory of Biological Field (Sovetskaya Nauka, Moskva, 1944) (in Russian).

  5. D'Arcy Thompson, On Growth and Form (Cambridge University Press, Cambridge, 1961).

  6. A.I Zotin, R.S. Zotina, Phenomenological theory of development, growth and ageing (Nauka, Moskva, 1993) (in Russian).

  7. S.F. Gilbert, Developmental Biology (Sunderland, MA, Sinauer Ass., 2010).

  8. R Alberts, Molecular Biology of the Cell (Taylor & Francis Group, 2003).

  9. J.-J. Kupiec, The Origin of Individuals (Singapore, World Scientific, 2009).

  10. S. Ramaswamy, Annu. Rev. Condens. Matter Phys. 1, 323 (2010).

    Article  ADS  Google Scholar 

  11. U.S. Schwarz, M.L. Gardel, J. Cell Sci. 125, 3051 (2012).

    Article  Google Scholar 

  12. L.V. Beloussov, The Dynamic Architecture of a Developing Organism (Kluwer Academic Publishers, Dordrecht, Boston, London, 1998).

  13. L.V. Beloussov, Phys. Biol. 5, 015009 (2008).

    Article  ADS  Google Scholar 

  14. L.V. Beloussov, N.N. Luchinskaia, A.S. Ermakov, N.S. Glagoleva, Int. J. Dev Biol. 50, 113 (2006).

    Article  Google Scholar 

  15. E.S. Kornikova, E.G. Korvin-Pavlovskaya, L.V. Beloussov, Dev. Genes Evol. 219, 1 (2009).

    Article  Google Scholar 

  16. E.S. Kornikova, T.G. Troshina, S.V. Kremnyov, L.V. Beloussov, Devel Dyn. 239, 885 (2010).

    Article  Google Scholar 

  17. S.V. Kremnyov, T.G. Troshina, L.V. Beloussov, Mech. Devel. 129, 51 (2012).

    Article  Google Scholar 

  18. A.N. Mansurov, A.A. Stein, L.V. Beloussov, Biomech. Model. Mechanobiol. 11, 1123 (2012).

    Article  Google Scholar 

  19. W. His, Unsere Korpers Form (Engelmann, Leipzig, 1878).

  20. G.H. Pollack, Cells, Gels and the Engines of Life (Ebner & Sons, Seattle, 2001).

  21. H.X. Zhou, G. Rivas, A.P Minton, Annu. Rev. Biophys. 37, 375 (2008).

    Article  Google Scholar 

  22. R. Fernandez-Gonzalez, J.A. Zallen, Sci. Signal 2, 78 (2009).

    Google Scholar 

  23. G. Bao et al., Mol. Cell. Biomech. 3, 91 (2010).

    Google Scholar 

  24. B.D. Hoffman, C. Grashoff, M.A. Schwartz, Nature 475, 316 (2011).

    Article  Google Scholar 

  25. J. Howard, Annu. Rev. Biophys. 38, 217 (2009).

    Article  Google Scholar 

  26. J. Howard, S.W. Grill, J.S. Bois, Nat. Rev. Mol. Cell Biol. 12, 392 (2011).

    Article  Google Scholar 

  27. L.V. Beloussov, J.G. Dorfman, V.G. Cherdantzev, J. Embr. Exp. Morphol. 34, 559 (1975).

    Google Scholar 

  28. L.V. Beloussov, S.V. Saveliev, I.I. Naumidi, V.V. Novoselov, Int. Rev. Cytol. 150, 1 (1994).

    Google Scholar 

  29. D.P. Kiehart, C.G. Galbraith, K.A. Edwards, W.L. Rickoll, R.A. Montague, J. Cell Biol. 149, 471 (2000).

    Article  Google Scholar 

  30. E.V. Cherdantzeva, V.G. Cherdantzev, Int. J. Dev. Biol. 50, 157 (2006).

    Article  Google Scholar 

  31. Ju.A. Kraus, Int. J. Dev. Biol. 50, 267 (2006).

    Article  Google Scholar 

  32. R. Bellairs, D.R. Bromham, C.C. Wylie, J. Embryol. Exp. Morphol. 17, 197 (1967).

    Google Scholar 

  33. V.G. Cherdantzev, Int. J. Dev. Biol. 50, 169 (2006).

    Article  Google Scholar 

  34. N. Gjorevski, C.M. Nelson, Integr. Biol. 2, 424 (2010).

    Article  Google Scholar 

  35. A.Ju. Evstifeeva, S.V. Kremnyov, L.V. Beloussov, Ontogenez (Russ. J. Dev. Biol.) 41, 190 (2010).

    Google Scholar 

  36. G.F. Oster, G.M. Odell, Cell Motil. 4, 469 (1984).

    Article  Google Scholar 

  37. B.C. Goodwin, L.E.H. Trainor, J. Theor. Biol. 117, 79 (1985).

    Article  Google Scholar 

  38. S. Chr Chen, M. Mrksich, Sui Huang, G.M. Whitesides, D.E. Ingber, Science 276, 1425 (1997).

    Article  Google Scholar 

  39. L.A. Martynov, Mathematical Biology of Development edited by A.I. Zotin, E.V. Presnov (Nauka, Moskva, 1982) (in Russian).

  40. S. Svetina, B. Zeks, J. Theor. Biol. 146, 115 (1990).

    Article  Google Scholar 

  41. P.B. Green, C.S. Steele, S.C. Rennich, Ann. Bot. 77, 515 (1996).

    Article  Google Scholar 

  42. G.M. Odell, G. Oster, P. Alberch, B. Burnside, Dev. Biol. 85, 446 (1981).

    Article  Google Scholar 

  43. A.K. Harris, D. Stopak, P. Warner, J. Embryol. Exp. Morphol. 80, 1 (1984).

    Google Scholar 

  44. B.N. Belintzev, L.V. Beloussov, A.G. Zaraisky, J. Theor. Biol. 129, 369 (1987).

    Article  Google Scholar 

  45. C.H. Waddington, Organizers and genes (Cambridge University Press, Cambridge, 1940).

  46. A.M. Turing, Philos. Trans. Roy. Soc. London, Ser. B 237, 37 (1952).

    Article  ADS  Google Scholar 

  47. L. Wolpert, Trends Genet. 12, 359 (1996).

    Article  Google Scholar 

  48. M. Spiegel, E.S. Spiegel, Amer. Zool. 15, 583 (1975).

    Google Scholar 

  49. T.G. Troshina, N.S. Glagoleva, L.V. Beloussov, L.V. Ontogenez, Russ. J. Dev. Biol. 42, 346 (2011).

    Article  Google Scholar 

  50. R. Keller, P. Tibbetts P., Dev. Biol. 131, 539 (1989).

    Article  Google Scholar 

  51. R. Keller, L. Davidson, A. Edlund, T. Elul, M. Ezin, D. Shook, P. Skoglund, Philos. Trans. R. Soc. London, Ser. B 355, 897 (2000).

    Article  Google Scholar 

  52. L.V. Beloussov, N.N. Luchinskaia, A.A.Stein, Dev. Genes Evol. 210, 92 (2000).

    Article  Google Scholar 

  53. L.V. Beloussov, V.I. Grabovsky, Comp. Methods Biomech. Biomed. Engin. 8, 381 (2005).

    Article  Google Scholar 

  54. L.A. Taber, Biomech. Model Mechanobiol. 7, 427 (2008).

    Article  Google Scholar 

  55. O. Kaverina, O. Krylyshkina, K. Beningo, K. Anderson, Yu-Li Wang, J.V. Small J., Cell Science 115, 2283 (2002).

    Google Scholar 

  56. M.K. Gardner, C.G. Pearson, B.L. Sprague, T.R. Zarzar, K.Bloom, E.D. Salmon, D.J. Odde, Mol. Biol. Cell. 16, 3764 (2005).

    Article  Google Scholar 

  57. A. Nekouzadeh, K.M. Pryse, E.L. Elson, G.M. Genin, J. Biomech. 41, 2964 (2008).

    Article  Google Scholar 

  58. S. Deguchi, M. Sato, Biorheology 46, 93 (2009).

    Google Scholar 

  59. T. Shemesh, A.D. Bershadsky, M.M. Kozlov, Biophys. J. 102, 1746 (2012).

    Article  Google Scholar 

  60. H.R.W. Wirtz, L.G. Dobbs, Science 298, 1266 (1990).

    Article  ADS  Google Scholar 

  61. J. Dai, M.P. Sheetz, Cold Spring Hrb. Symp. Quant. Biol. 60, 567 (1995).

    Article  Google Scholar 

  62. C. Rauch, E. Farge, Biophys. J. 78, 3036 (2000).

    Article  ADS  Google Scholar 

  63. N.C. Gauthier, M.A. Fardin, P. Roca-Cusach, M.P. Sheetz, Proc. Natl. Acad. Sci. U.S.A. 108, 14467 (2011).

    Article  ADS  Google Scholar 

  64. O.J. Pletjushkina, A.M. Belkin O.J. Ivanova, T. Oliver, J.M. Vasiliev, K. Jacobson, Cell Adhes. Commun. 5, 121 (1998).

    Article  Google Scholar 

  65. D. Riveline, E. Zamir, N.Q. Balaban, U.S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, A.D. Bershadsky, J. Cell Biol. 153, 1175 (2001).

    Article  Google Scholar 

  66. L.D. Landau, L.M. Livshitz, Theory of Elasticity (Nauka, Moskva, 1976) (In Russian).

  67. L.V. Beloussov, Ju.A. Labas, N.I. Kazakova, A.G. Zaraisky, J. Exp. Zool. 249, 258 (1989).

    Article  Google Scholar 

  68. L.V. Beloussov, V.I. Grabovsky, Comp. Methods Biomech. Biomed. Engin. 6, 53 (2003).

    Article  Google Scholar 

  69. E. Munro, B. Bowerman, Cold Spring Hrb. Persp. Biol. 1, a003400 (2009).

    Google Scholar 

  70. T.E. Schroeder, Ann. N.Y. Acad. Sci. 582, 78 (1990).

    Article  ADS  Google Scholar 

  71. J.G. White, Ann. N.Y. Acad. Sci. 582, 50 (1990).

    Article  ADS  Google Scholar 

  72. B.J. Cha, D.L. Gard, Dev. Biol. 205, 275 (1999).

    Article  Google Scholar 

  73. E. Farge, Curr. Biol. 13, 1365 (2003).

    Article  Google Scholar 

  74. R. McBeath, D.M. Pirone, C.M. Nelson, K. Bhadriraju, C.S. Chen, Dev. Cell 6, 483 (2004).

    Article  Google Scholar 

  75. A.J. Engler, S. Sen, H.L. Sweeney, D.E. Discher, Cell 126, 677 (2006).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Developmental Biophysics, Faculty of Biology, Moscow State University, 119992, Moscow, Russia

    L. V. Beloussov

Authors
  1. L. V. Beloussov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. V. Beloussov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Beloussov, L.V. Morphogenesis can be driven by properly parametrised mechanical feedback. Eur. Phys. J. E 36, 132 (2013). https://doi.org/10.1140/epje/i2013-13132-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1140/epje/i2013-13132-x

Keywords

Search

Navigation