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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References
Babloyantz, A. Molecules, Dynamics, and Life: An Introduction to Self-Organization of Matter (Wiley, New York, 1986).
Murray, J. Discussion: Turing's theory of morphogenesis — its influence on modelling biological patterns and form. Bull. Math. Biol. 52, 119–152 (1990).
Bastiaens, P., Caudron, M., Niethammer, P. & Karsenti, E. Gradients in the self-organization of the mitotic spindle. Trends Cell Biol. 16, 125–134 (2006).
Kholodenko, B. N. Cell-signalling dynamics in time and space. Nature Rev. Mol. Cell Biol. 7, 165–176 (2006).
Thompson, D. W. On Growth and Form (Cambridge Univ. Press, 1942).
Kirschner, M., Gerhart, J. & Mitchison, T. Molecular “vitalism”. Cell 100, 79–88 (2000).
Kurakin, A. Self-organization versus watchmaker: ambiguity of molecular recognition and design charts of cellular circuitry. J. Mol. Recognit. 20, 205–214 (2007).
Kant, E. Critique de la Faculté de Juger (Gallimard, Paris, 1985) (in French).
Van de Vijver, G. Self-Organization and Emergence in Life Sciences (Springer, Dordrecht, 2006).
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).
Haken, H. Nonequilibrium phase transitions and self-organisation in physics, chemistry, and biology. In Synergetics: An Introduction (Springer, Berlin, 1977).
Prigogine, I. & Stengers, I. Order Out of Chaos (Bantam, Toronto, 1984).
Lotka, A. J. Contributions to the theory of periodic reactions. J. Phys. Chem. 14, 271–274 (1910).
Lotka, A. Elements of Physical Biology (Williams and Wilkins, Baltimore, 1925).
Bray, W. A periodic reaction in homogeneous solution and its relation to catalysis. J. Am. Chem. Soc. 43, 1262–1267 (1921).
Belousov, B. [A periodic reaction and its mechanism]. Compilation of Abstracts on Radiation Medicine 147, 145 (1959) (in Russian).
Zhabotinsky, A. [Periodic processes of malonic acid oxidation in a liquid phase.]. Biofizika 9, 306–311 (1964) (in Russian).
Zhabotinsky, A. M. & Zaikin, A. N. Autowave processes in a distributed chemical system. J. Theor. Biol. 40, 45–61 (1973).
Tabony, J. Historical and conceptual background of self-organization by reactive processes. Biol. Cell 98, 589–602 (2006).
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).
Turing, A. M. The chemical basis of morphogenesis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 237, 37–72 (1952).
Prigogine, I. & Nicolis, G. On symmetry-breaking instabilities in dissipative systems. J. Chem. Phys. 46, 3542–3550 (1967).
Prigogine, I., Nicolis, G. & Babloyantz, A. Nonequilibrium problems in biological phenomena. Ann. NY Acad. Sci. 231, 99–105 (1974).
Nicolis, G. & Prigogine, I. Self-Organization in Nonequilibrium Systems: From Dissipative Structures to Order Through Fluctuations (Wiley, New York, 1977).
Goldbeter, A. & Lefever, R. Dissipative structures for an allosteric model. Application to glycolytic oscillations. Biophys. J. 12, 1302–1315 (1972).
Boiteux, A., Hess, B. & Plesser, T. Oscillatory phenomena in biological systems. FEBS Lett. 75, 1–4 (1977).
Goldbeter, A. Biochemical Oscillations and Cellular Rhythms: The Molecular Bases of Periodic and Chaotic Behaviour (Cambridge Univ. Press, 1996).
Maini, P. K., Baker, R. E. & Chuong, C. M. Developmental biology. The Turing model comes of molecular age. Science 314, 1397–1398 (2006).
Murray, J. (ed.) Mathematical Biology (Springer, New York, 2007).
Kauffman, S. At Home in the Universe (Oxford Univ. Press, 1995).
Goodwin, B. C., Kauffman, S. & Murray, J. D. Is morphogenesis an intrinsically robust process? J. Theor. Biol. 163, 135–144 (1993).
Kauffman, S. The Origins of Order: Self-Organization and Selection in Evolution (Oxford Univ. Press, 1993).
Ball, P. The Self-Made Tapestry (Oxford Univ. Press, 1999).
Camazine, S. et al. Self-Organization in Biological Systems (Princeton Univ. Press, 2001).
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).
Kirschner, M. & Mitchison, T. Beyond self-assembly: from microtubules to morphogenesis. Cell 45, 329–342. (1986).
Tabony, J. & Job, D. Spatial structures in microtubular solutions requiring a sustained energy source. Nature 346, 448–451 (1990).
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).
Karsenti, E. Mitotic spindle morphogenesis in animal cells. Semin. Cell Biol. 2, 251–260 (1991).
Mitchison, T. J. Self-organization of polymer-motor systems in the cytoskeleton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 336, 99–106 (1992).
Misteli, T. The concept of self-organization in cellular architecture. J. Cell Biol. 155, 181–185 (2001).
Kruse, K. & Jülicher, F. Oscillations in cell biology. Curr. Opin. Cell Biol. 17, 20–26 (2005).
Glick, B. S. Let there be order. Nature Cell Biol. 9, 130–132 (2007).
Bénard, H. Les tourbillons cellulaires dans une nappe liquide. Rev. Gen. Sci. Pure Appl. 11, 1261–1271 (1900) (in French).
Rayleigh, L. On convective currents in a horizontal layer of fluid when the higher temperature is on the under side. Philos. Mag. 32 (1916).
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).
Ouyang, Q. & Swinney, H. Transition from a uniform state to hexagonal and striped Turing patterns. Nature 352, 610–612 (1991).
Shoji, H., Yamada, K., Ueyama, D. & Ohta, T. Turing patterns in three dimensions. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 75, 046212 (2007).
Yang, L. & Epstein, I. Oscillatory Turing patterns in reaction–diffusion systems with two coupled layers. Physic. Rev. Lett. 90, 178303 (2003).
Gierer, A. & Meinhardt, H. A theory of biological pattern formation. Kybernetik 12, 30–39 (1972).
Meinhardt, H. & Gierer, A. Pattern formation by local self-activation and lateral inhibition. Bioessays 22, 753–760 (2000).
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).
Glade, N., Demongeot, J. & Tabony, J. Comparison of reaction–diffusion simulations with experiment in self-organized microtubule solutions. CR Biol. 325, 283–294 (2002).
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).
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).
Maly, I. V. & Borisy, G. G. Self-organization of treadmilling microtubules into a polar array. Trends Cell Biol. 12, 462–465 (2002).
Nédélec, F. J., Surrey, T., Maggs, A. C. & Leibler, S. Self-organization of microtubules and motors. Nature 389, 305–308 (1997).
Surrey, T., Nédélec, F., Leibler, S. & Karsenti, E. Physical properties determining self-organization of motors and microtubules. Science 292, 1167–1171 (2001).
Nédélec, F. Computer simulations reveal motor properties generating stable antiparallel microtubule interactions. J. Cell Biol. 158, 1005–1015 (2002).
Nogales, E., Whittaker, M., Milligan, R. A. & Downing, K. H. High-resolution model of the microtubule. Cell 96, 79–88 (1999).
Vallee, R. B. & Stehman, S. A. How dynein helps the cell find its center: a servomechanical model. Trends Cell Biol. 15, 288–294 (2005).
Backouche, F., Haviv, L., Groswasser, D. & Bernheim-Groswasser, A. Active gels: dynamics of patterning and self-organization. Phys. Biol. 3, 264–273 (2006).
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).
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).
Jülicher, F. & Prost, J. Spontaneous oscillations of collective molecular motors. Phys. Rev. Lett. 78, 4510–4513 (1997).
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).
Novak, B. & Tyson, J. J. Modelling the controls of the eukaryotic cell cycle. Biochem. Soc. Trans. 31, 1526–1529 (2003).
Sha, W. et al. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc. Natl Acad. Sci. USA 100, 975–980 (2003).
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).
Murray, A. W. & Kirschner, M. W. Dominoes and clocks: the union of two views of cell cycle regulation. Science 246, 614–621 (1989).
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).
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).
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).
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).
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).
Karsenti, E. & Vernos, I. The mitotic spindle: a self-made machine. Science 294, 543–547 (2001).
Cook, P. R. Predicting three-dimensional genome structure from transcriptional activity. Nature Genet. 32, 347–352 (2002).
Iborra, F. J. & Cook, P. R. The interdependence of nuclear structure and function. Curr. Opin. Cell Biol. 14, 780–785 (2002).
Meaburn, K. J., Misteli, T. & Soutoglou, E. Spatial genome organization in the formation of chromosomal translocations. Semin. Cancer Biol. 17, 80–90 (2007).
Misteli, T. Beyond the sequence: cellular organization of genome function. Cell 128, 787–800 (2007).
Piekny, A., Werner, M. & Glotzer, M. Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 15, 651–658 (2005).
Camalet, S. & Jülicher, F. Generic aspects of axonemal beating. New J. Phys. 2, 24.1–24.23 (2000).
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).
Brunner, D. & Nurse, P. New concepts in fission yeast morphogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 873–877 (2000).
Carazo-Salas, R. E. & Nurse, P. Self-organization of interphase microtubule arrays in fission yeast. Nature Cell Biol. 8, 1102–1107 (2006).
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).
Janson, M. E. et al. Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128, 357–368 (2007).
Carazo-Salas, R. & Nurse, P. Sorting out interphase microtubules. Mol. Syst. Biol. 3, 95 (2007).
Castagnetti, S., Novak, B. & Nurse, P. Microtubules offset growth site from the cell centre in fission yeast. J. Cell Sci. 120, 2205–2213 (2007).
Devreotes, P. N. & Zigmond, S. H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu. Rev. Cell Biol. 4, 649–686 (1988).
Devreotes, P. & Janetopoulos, C. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem. 278, 20445–20448 (2003).
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).
Xu, J. et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201–214 (2003).
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).
Wedlich-Soldner, R. & Li, R. Spontaneous cell polarization: undermining determinism. Nature Cell Biol. 5, 267–270 (2003).
Nigg, E. A. Centrosome duplication: of rules and licenses. Trends Cell Biol. 17, 215–221 (2007).
Dutcher, S. K. Finding treasures in frozen cells: new centriole intermediates. Bioessays 29, 630–634 (2007).
Vladar, E. K. & Stearns, T. Molecular characterization of centriole assembly in ciliated epithelial cells. J. Cell Biol. 178, 31–42 (2007).
Pelletier, L. Centrioles: duplicating precariously. Curr. Biol. 17, R770–R773 (2007).
Bornens, M. & Karsenti, E. In Membrane Structure and Function (ed. Bittar, E. E.) 99–171 (Wiley, New York, 1984).
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).
Azimzadeh, J. & Bornens, M. Structure and duplication of the centrosome. J. Cell Sci. 120, 2139–2142 (2007).
Heald, R. & Weis, K. Spindles get the ran around. Trends Cell Biol. 10, 1–4 (2000).
Pelletier, L. et al. Golgi biogenesis in Toxoplasma gondii. Nature 418, 548–552 (2002).
He, C. Y., Pypaert, M. & Warren, G. Golgi duplication in Trypanosoma brucei requires Centrin2. Science 310, 1196–1198 (2005).
He, C. Y. et al. Golgi duplication in Trypanosoma brucei. J. Cell Biol. 165, 313–321 (2004).
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).
Glick, B. S. Can the Golgi form de novo? Nature Rev. Mol. Cell Biol. 3, 615–619 (2002).
Simpson, J. C., Nilsson, T. & Pepperkok, R. Biogenesis of tubular ER-to-Golgi transport intermediates. Mol. Biol. Cell 17, 723–737 (2006).
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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DOI: https://doi.org/10.1038/nrm2357
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