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Self-organization in cell biology: a brief history

Abstract

Over the past two decades, molecular and cell biologists have made important progress in characterizing the components and compartments of the cell. New visualization methods have also revealed cellular dynamics. This has raised complex issues about the organization principles that underlie the emergence of coherent dynamical cell shapes and functions. Self-organization concepts that were first developed in chemistry and physics and then applied to various morphogenetic problems in biology over the past century are now beginning to be applied to the organization of the living cell.

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Figure 1: Bénard rolls.
Figure 2: Examples of self-organized microtubule patterns and cell shapes.
Figure 3: Examples of self-organized cell-cycle processes.
Figure 4: Self-organized versus templated pattern transmission.

References

  1. Babloyantz, A. Molecules, Dynamics, and Life: An Introduction to Self-Organization of Matter (Wiley, New York, 1986).

    Google Scholar 

  2. Murray, J. Discussion: Turing's theory of morphogenesis — its influence on modelling biological patterns and form. Bull. Math. Biol. 52, 119–152 (1990).

    Google Scholar 

  3. Bastiaens, P., Caudron, M., Niethammer, P. & Karsenti, E. Gradients in the self-organization of the mitotic spindle. Trends Cell Biol. 16, 125–134 (2006).

    CAS  PubMed  Google Scholar 

  4. Kholodenko, B. N. Cell-signalling dynamics in time and space. Nature Rev. Mol. Cell Biol. 7, 165–176 (2006).

    Article  CAS  Google Scholar 

  5. Thompson, D. W. On Growth and Form (Cambridge Univ. Press, 1942).

    Google Scholar 

  6. Kirschner, M., Gerhart, J. & Mitchison, T. Molecular “vitalism”. Cell 100, 79–88 (2000).

    CAS  PubMed  Google Scholar 

  7. Kurakin, A. Self-organization versus watchmaker: ambiguity of molecular recognition and design charts of cellular circuitry. J. Mol. Recognit. 20, 205–214 (2007).

    CAS  PubMed  Google Scholar 

  8. Kant, E. Critique de la Faculté de Juger (Gallimard, Paris, 1985) (in French).

    Google Scholar 

  9. Van de Vijver, G. Self-Organization and Emergence in Life Sciences (Springer, Dordrecht, 2006).

    Google Scholar 

  10. Fox Keller, E. Contenders for life at the dawn of the twenty-first century: approaches from physics, biology and engineering. Interdiscip. Sci. Rev. 32, 113–122 (2007).

    Google Scholar 

  11. Haken, H. Nonequilibrium phase transitions and self-organisation in physics, chemistry, and biology. In Synergetics: An Introduction (Springer, Berlin, 1977).

    Google Scholar 

  12. Prigogine, I. & Stengers, I. Order Out of Chaos (Bantam, Toronto, 1984).

    Google Scholar 

  13. Lotka, A. J. Contributions to the theory of periodic reactions. J. Phys. Chem. 14, 271–274 (1910).

    CAS  Google Scholar 

  14. Lotka, A. Elements of Physical Biology (Williams and Wilkins, Baltimore, 1925).

    Google Scholar 

  15. Bray, W. A periodic reaction in homogeneous solution and its relation to catalysis. J. Am. Chem. Soc. 43, 1262–1267 (1921).

    CAS  Google Scholar 

  16. Belousov, B. [A periodic reaction and its mechanism]. Compilation of Abstracts on Radiation Medicine 147, 145 (1959) (in Russian).

    Google Scholar 

  17. Zhabotinsky, A. [Periodic processes of malonic acid oxidation in a liquid phase.]. Biofizika 9, 306–311 (1964) (in Russian).

    Google Scholar 

  18. Zhabotinsky, A. M. & Zaikin, A. N. Autowave processes in a distributed chemical system. J. Theor. Biol. 40, 45–61 (1973).

    CAS  PubMed  Google Scholar 

  19. Tabony, J. Historical and conceptual background of self-organization by reactive processes. Biol. Cell 98, 589–602 (2006).

    CAS  PubMed  Google Scholar 

  20. Kolmogorov, A., Petrovsky, L. & Piskunov, N. An investigation of the diffusion equation combined with an increase in mass and its application to a biological problem. Bull. Uni. Moscow Ser. Int. A1 6, 1–26 (1937).

    Google Scholar 

  21. Turing, A. M. The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 237, 37–72 (1952).

    Google Scholar 

  22. Prigogine, I. & Nicolis, G. On symmetry-breaking instabilities in dissipative systems. J. Chem. Phys. 46, 3542–3550 (1967).

    CAS  Google Scholar 

  23. Prigogine, I., Nicolis, G. & Babloyantz, A. Nonequilibrium problems in biological phenomena. Ann. NY Acad. Sci. 231, 99–105 (1974).

    CAS  PubMed  Google Scholar 

  24. Nicolis, G. & Prigogine, I. Self-Organization in Nonequilibrium Systems: From Dissipative Structures to Order Through Fluctuations (Wiley, New York, 1977).

    Google Scholar 

  25. Goldbeter, A. & Lefever, R. Dissipative structures for an allosteric model. Application to glycolytic oscillations. Biophys. J. 12, 1302–1315 (1972).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Boiteux, A., Hess, B. & Plesser, T. Oscillatory phenomena in biological systems. FEBS Lett. 75, 1–4 (1977).

    CAS  PubMed  Google Scholar 

  27. Goldbeter, A. Biochemical Oscillations and Cellular Rhythms: The Molecular Bases of Periodic and Chaotic Behaviour (Cambridge Univ. Press, 1996).

    Google Scholar 

  28. Maini, P. K., Baker, R. E. & Chuong, C. M. Developmental biology. The Turing model comes of molecular age. Science 314, 1397–1398 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Murray, J. (ed.) Mathematical Biology (Springer, New York, 2007).

    Google Scholar 

  30. Kauffman, S. At Home in the Universe (Oxford Univ. Press, 1995).

    Google Scholar 

  31. Goodwin, B. C., Kauffman, S. & Murray, J. D. Is morphogenesis an intrinsically robust process? J. Theor. Biol. 163, 135–144 (1993).

    CAS  PubMed  Google Scholar 

  32. Kauffman, S. The Origins of Order: Self-Organization and Selection in Evolution (Oxford Univ. Press, 1993).

    Google Scholar 

  33. Ball, P. The Self-Made Tapestry (Oxford Univ. Press, 1999).

    Google Scholar 

  34. Camazine, S. et al. Self-Organization in Biological Systems (Princeton Univ. Press, 2001).

    Google Scholar 

  35. Karsenti, E., Newport, J., Hubble, R. & Kirschner, M. Interconversion of metaphase and interphase microtubule arrays, as studied by the injection of centrosomes and nuclei into Xenopus eggs. J. Cell Biol. 98, 1730–1745 (1984).

    CAS  PubMed  Google Scholar 

  36. Kirschner, M. & Mitchison, T. Beyond self-assembly: from microtubules to morphogenesis. Cell 45, 329–342. (1986).

    CAS  PubMed  Google Scholar 

  37. Tabony, J. & Job, D. Spatial structures in microtubular solutions requiring a sustained energy source. Nature 346, 448–451 (1990).

    CAS  PubMed  Google Scholar 

  38. Verde, F., Berrez, J. M., Antony, C. & Karsenti, E. Taxol induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein. J. Cell Biol. 112, 1177–1187 (1991).

    CAS  PubMed  Google Scholar 

  39. Karsenti, E. Mitotic spindle morphogenesis in animal cells. Semin. Cell Biol. 2, 251–260 (1991).

    CAS  PubMed  Google Scholar 

  40. Mitchison, T. J. Self-organization of polymer-motor systems in the cytoskeleton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 336, 99–106 (1992).

    CAS  PubMed  Google Scholar 

  41. Misteli, T. The concept of self-organization in cellular architecture. J. Cell Biol. 155, 181–185 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Kruse, K. & Jülicher, F. Oscillations in cell biology. Curr. Opin. Cell Biol. 17, 20–26 (2005).

    CAS  PubMed  Google Scholar 

  43. Glick, B. S. Let there be order. Nature Cell Biol. 9, 130–132 (2007).

    CAS  PubMed  Google Scholar 

  44. Bénard, H. Les tourbillons cellulaires dans une nappe liquide. Rev. Gen. Sci. Pure Appl. 11, 1261–1271 (1900) (in French).

    Google Scholar 

  45. Rayleigh, L. On convective currents in a horizontal layer of fluid when the higher temperature is on the under side. Philos. Mag. 32 (1916).

  46. Castets, V. V., Dulos, E., Boissonade, J. & De Kepper, P. Experimental evidence of a sustained standing Turing-type nonequilibrium chemical pattern. Phys. Rev. Lett. 64, 2953–2956 (1990).

    CAS  PubMed  Google Scholar 

  47. Ouyang, Q. & Swinney, H. Transition from a uniform state to hexagonal and striped Turing patterns. Nature 352, 610–612 (1991).

    Google Scholar 

  48. Shoji, H., Yamada, K., Ueyama, D. & Ohta, T. Turing patterns in three dimensions. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75, 046212 (2007).

    PubMed  Google Scholar 

  49. Yang, L. & Epstein, I. Oscillatory Turing patterns in reaction–diffusion systems with two coupled layers. Physic. Rev. Lett. 90, 178303 (2003).

    Google Scholar 

  50. Gierer, A. & Meinhardt, H. A theory of biological pattern formation. Kybernetik 12, 30–39 (1972).

    CAS  PubMed  Google Scholar 

  51. Meinhardt, H. & Gierer, A. Pattern formation by local self-activation and lateral inhibition. Bioessays 22, 753–760 (2000).

    CAS  PubMed  Google Scholar 

  52. Tyson, J. J., Chen, K. C. & Novak, B. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 15, 221–231 (2003).

    CAS  PubMed  Google Scholar 

  53. Glade, N., Demongeot, J. & Tabony, J. Comparison of reaction–diffusion simulations with experiment in self-organized microtubule solutions. CR Biol. 325, 283–294 (2002).

    CAS  Google Scholar 

  54. Guo, Y., Liu, Y., Tang, J. X. & Valles, J. M. Polymerization force driven buckling of microtubule bundles determines the wavelength of patterns formed in tubulin solutions. Phys. Rev. Lett. 98, 198103-1-4 (2007).

    PubMed  Google Scholar 

  55. Cortes, S., Glade, N., Chartier, I. & Tabony, J. Microtubule self-organisation by reaction–diffusion processes in miniature cell-sized containers and phospholipid vesicles. Biophys. Chem. 120, 168–177 (2006).

    CAS  PubMed  Google Scholar 

  56. Maly, I. V. & Borisy, G. G. Self-organization of treadmilling microtubules into a polar array. Trends Cell Biol. 12, 462–465 (2002).

    CAS  PubMed  Google Scholar 

  57. Nédélec, F. J., Surrey, T., Maggs, A. C. & Leibler, S. Self-organization of microtubules and motors. Nature 389, 305–308 (1997).

    PubMed  Google Scholar 

  58. Surrey, T., Nédélec, F., Leibler, S. & Karsenti, E. Physical properties determining self-organization of motors and microtubules. Science 292, 1167–1171 (2001).

    CAS  PubMed  Google Scholar 

  59. Nédélec, F. Computer simulations reveal motor properties generating stable antiparallel microtubule interactions. J. Cell Biol. 158, 1005–1015 (2002).

    PubMed  PubMed Central  Google Scholar 

  60. Nogales, E., Whittaker, M., Milligan, R. A. & Downing, K. H. High-resolution model of the microtubule. Cell 96, 79–88 (1999).

    CAS  PubMed  Google Scholar 

  61. Vallee, R. B. & Stehman, S. A. How dynein helps the cell find its center: a servomechanical model. Trends Cell Biol. 15, 288–294 (2005).

    CAS  PubMed  Google Scholar 

  62. Backouche, F., Haviv, L., Groswasser, D. & Bernheim-Groswasser, A. Active gels: dynamics of patterning and self-organization. Phys. Biol. 3, 264–273 (2006).

    CAS  PubMed  Google Scholar 

  63. Kruse, K., Joanny, J., Julicher, F., Prost, J. & Sekimoto, K. Asters, vortices, and rotating spirals in active gels of polar filaments. Phys. Rev. Lett. 92, 078101–078104 (2004).

    CAS  PubMed  Google Scholar 

  64. Haviv, L. et al. Reconstitution of the transition from lamellipodium to filopodium in a membrane-free system. Proc. Natl Acad. Sci. USA 103, 4906–4911 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Jülicher, F. & Prost, J. Spontaneous oscillations of collective molecular motors. Phys. Rev. Lett. 78, 4510–4513 (1997).

    Google Scholar 

  66. Goldbeter, A. Oscillations and waves of cyclic AMP in Dictyostelium: a prototype for spatio-temporal organization and pulsatile intercellular communication. Bull. Math. Biol. 68, 1095–1109 (2006).

    CAS  PubMed  Google Scholar 

  67. Novak, B. & Tyson, J. J. Modelling the controls of the eukaryotic cell cycle. Biochem. Soc. Trans. 31, 1526–1529 (2003).

    CAS  PubMed  Google Scholar 

  68. Sha, W. et al. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc. Natl Acad. Sci. USA 100, 975–980 (2003).

    CAS  PubMed  Google Scholar 

  69. Murray, A. W., Solomon, M. J. & Kirschner, M. W. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280–286 (1989).

    CAS  PubMed  Google Scholar 

  70. Murray, A. W. & Kirschner, M. W. Dominoes and clocks: the union of two views of cell cycle regulation. Science 246, 614–621 (1989).

    CAS  PubMed  Google Scholar 

  71. Félix, M.-A., Pines, J., Hunt, T. & Karsenti, E. Temporal regulation of Cdc2 mitotic kinase activity and cyclin degradation in cell-free extracts of Xenopus eggs. J. Cell Sci. 246, 614–621 (1989).

    Google Scholar 

  72. Félix, M. A., Labbé, J. C., Dorée, M., Hunt, T. & Karsenti, E. Triggering of cyclin degradation in interphase extracts of amphibian eggs by Cdc2 kinase. Nature 346, 379–382 (1990).

    PubMed  Google Scholar 

  73. Yang, L., MacLellan, W. R., Han, Z., Weiss, J. N. & Qu, Z. Multisite phosphorylation and network dynamics of cyclin-dependent kinase signaling in the eukaryotic cell cycle. Biophys. J. 86, 3432–3443 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Zwolak, J. W., Tyson, J. J. & Watson, L. T. Parameter estimation for a mathematical model of the cell cycle in frog eggs. J. Comput. Biol. 12, 48–63 (2005).

    CAS  PubMed  Google Scholar 

  75. Hetzer, M., Gruss, O. J. & Mattaj, I. W. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nature Cell Biol. 4, E177–E184 (2002).

    CAS  PubMed  Google Scholar 

  76. Karsenti, E. & Vernos, I. The mitotic spindle: a self-made machine. Science 294, 543–547 (2001).

    CAS  PubMed  Google Scholar 

  77. Cook, P. R. Predicting three-dimensional genome structure from transcriptional activity. Nature Genet. 32, 347–352 (2002).

    CAS  PubMed  Google Scholar 

  78. Iborra, F. J. & Cook, P. R. The interdependence of nuclear structure and function. Curr. Opin. Cell Biol. 14, 780–785 (2002).

    CAS  PubMed  Google Scholar 

  79. Meaburn, K. J., Misteli, T. & Soutoglou, E. Spatial genome organization in the formation of chromosomal translocations. Semin. Cancer Biol. 17, 80–90 (2007).

    CAS  PubMed  Google Scholar 

  80. Misteli, T. Beyond the sequence: cellular organization of genome function. Cell 128, 787–800 (2007).

    CAS  PubMed  Google Scholar 

  81. Piekny, A., Werner, M. & Glotzer, M. Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 15, 651–658 (2005).

    CAS  PubMed  Google Scholar 

  82. Camalet, S. & Jülicher, F. Generic aspects of axonemal beating. New J. Phys. 2, 24.1–24.23 (2000).

    Google Scholar 

  83. Verde, F., Mata, J. & Nurse, P. Fission yeast cell morphogenesis: identification of new genes and analysis of their role during the cell cycle. J. Cell Biol. 131, 1529–1538 (1995).

    CAS  PubMed  Google Scholar 

  84. Brunner, D. & Nurse, P. New concepts in fission yeast morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 873–877 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Carazo-Salas, R. E. & Nurse, P. Self-organization of interphase microtubule arrays in fission yeast. Nature Cell Biol. 8, 1102–1107 (2006).

    CAS  PubMed  Google Scholar 

  86. Daga, R. R., Lee, K. G., Bratman, S., Salas-Pino, S. & Chang, F. Self-organization of microtubule bundles in anucleate fission yeast cells. Nature Cell Biol. 8, 1108–1113 (2006).

    CAS  PubMed  Google Scholar 

  87. Janson, M. E. et al. Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128, 357–368 (2007).

    CAS  PubMed  Google Scholar 

  88. Carazo-Salas, R. & Nurse, P. Sorting out interphase microtubules. Mol. Syst. Biol. 3, 95 (2007).

    PubMed  PubMed Central  Google Scholar 

  89. Castagnetti, S., Novak, B. & Nurse, P. Microtubules offset growth site from the cell centre in fission yeast. J. Cell Sci. 120, 2205–2213 (2007).

    CAS  PubMed  Google Scholar 

  90. Devreotes, P. N. & Zigmond, S. H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol. 4, 649–686 (1988).

    CAS  PubMed  Google Scholar 

  91. Devreotes, P. & Janetopoulos, C. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem. 278, 20445–20448 (2003).

    CAS  PubMed  Google Scholar 

  92. Wedlich-Soldner, R., Wai, S. C., Schmidt, T. & Li, R. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J. Cell Biol. 166, 889–900 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Xu, J. et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201–214 (2003).

    CAS  PubMed  Google Scholar 

  94. Maly, I. V., Wiley, H. S. & Lauffenburger, D. A. Self-organization of polarized cell signaling via autocrine circuits: computational model analysis. Biophys. J. 86, 10–22 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Wedlich-Soldner, R. & Li, R. Spontaneous cell polarization: undermining determinism. Nature Cell Biol. 5, 267–270 (2003).

    CAS  PubMed  Google Scholar 

  96. Nigg, E. A. Centrosome duplication: of rules and licenses. Trends Cell Biol. 17, 215–221 (2007).

    CAS  PubMed  Google Scholar 

  97. Dutcher, S. K. Finding treasures in frozen cells: new centriole intermediates. Bioessays 29, 630–634 (2007).

    CAS  PubMed  Google Scholar 

  98. Vladar, E. K. & Stearns, T. Molecular characterization of centriole assembly in ciliated epithelial cells. J. Cell Biol. 178, 31–42 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Pelletier, L. Centrioles: duplicating precariously. Curr. Biol. 17, R770–R773 (2007).

    CAS  PubMed  Google Scholar 

  100. Bornens, M. & Karsenti, E. In Membrane Structure and Function (ed. Bittar, E. E.) 99–171 (Wiley, New York, 1984).

    Google Scholar 

  101. Rodrigues-Martins, A., Riparbelli, M., Callaini, G., Glover, D. M. & Bettencourt-Dias, M. Revisiting the role of the mother centriole in centriole biogenesis. Science 316, 1046–1050 (2007).

    CAS  PubMed  Google Scholar 

  102. Azimzadeh, J. & Bornens, M. Structure and duplication of the centrosome. J. Cell Sci. 120, 2139–2142 (2007).

    CAS  PubMed  Google Scholar 

  103. Heald, R. & Weis, K. Spindles get the ran around. Trends Cell Biol. 10, 1–4 (2000).

    CAS  PubMed  Google Scholar 

  104. Pelletier, L. et al. Golgi biogenesis in Toxoplasma gondii. Nature 418, 548–552 (2002).

    CAS  PubMed  Google Scholar 

  105. He, C. Y., Pypaert, M. & Warren, G. Golgi duplication in Trypanosoma brucei requires Centrin2. Science 310, 1196–1198 (2005).

    CAS  PubMed  Google Scholar 

  106. He, C. Y. et al. Golgi duplication in Trypanosoma brucei. J. Cell Biol. 165, 313–321 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Thiele, C. & Huttner, W. B. Protein and lipid sorting from the trans-Golgi network to secretory granules — recent developments. Semin. Cell Dev. Biol. 9, 511–516 (1998).

    CAS  PubMed  Google Scholar 

  108. Glick, B. S. Can the Golgi form de novo? Nature Rev. Mol. Cell Biol. 3, 615–619 (2002).

    CAS  Google Scholar 

  109. Simpson, J. C., Nilsson, T. & Pepperkok, R. Biogenesis of tubular ER-to-Golgi transport intermediates. Mol. Biol. Cell 17, 723–737 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

I thank colleagues of the Cell Biology and Biophysics Unit at the European Molecular Biology Laboratory for all of the discussions and collective work. I also thank the three anonymous reviewers who helped bring this text to something that looks, I hope, like a balanced and coherent whole. I apologize to all those who have not been cited owing to lack of space or because of my ignorance.

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Karsenti, E. Self-organization in cell biology: a brief history. Nat Rev Mol Cell Biol 9, 255–262 (2008). https://doi.org/10.1038/nrm2357

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