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Building the cell: design principles of cellular architecture

Nature Reviews Molecular Cell Biology volume 9, pages 593–602 (2008)Cite this article

Key Points

  • Cell architecture is dictated by the systems that control the size, number, position and shape of individual organelles.

  • Organelle size can be controlled by molecular rulers, quantal synthesis of precursors or dynamic balance-point mechanisms.

  • Organelle number is controlled by placing the rate of organelle production or loss under control of organelle number.

  • Organelle position is controlled by self-organizing cell polarity systems that orientate the cytoskeleton, which in turn move organelles to defined positions.

  • Organelle shape, for membrane-bound organelles, is determined in part by curvature changes driven by lipid composition and lipid-binding proteins, along with active forces exerted on the organelle surface by the cytoskeleton.

  • Cells are dynamic systems whose current organization reflects previous organization to an extent that structural variations can be propagated through cell division.

Abstract

The astounding structural complexity of a cell arises from the action of a relatively small number of genes, raising the question of how this complexity is achieved. Self-organizing processes combined with simple physical constraints seem to have key roles in controlling organelle size, number, shape and position, and these factors then combine to produce the overall cell architecture. By examining how these parameters are controlled in specific cell biological examples we can identify a handful of simple design principles that seem to underlie cellular architecture and assembly.

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Figure 1: Design principles of organelle size control.
Figure 2: The dynamic balance mechanism to control size and number.
Figure 3: Design principles of polarity and organelle positioning.
Figure 4: The regulation of organelle shape by changing the vesicle size.
Figure 5: Design principles of dynamic shape specification.

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References

  1. Marsh, B. J., Mastronarde, D. N., Buttle, K. F., Howell, K. E. & McIntosh, J. R. Organellar relationships in the Golgi region of the pancreatic β cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Natl Acad. Sci. USA 98, 2399–2406 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Minton, A. P. How can biochemical reactions within cells differ from those in test tubes? J. Cell Sci. 119, 2863–2869 (2006).

    CAS  PubMed  Google Scholar 

  3. Karsenti, E. Self-organization in cell biology: a brief history. Nature Rev. Mol. Cell Biol. 9, 255–262 (2008).

    CAS  Google Scholar 

  4. West, G. B., Brown, J. H. & Enquist, B. J. in Scaling in Biology (eds J. H. Brown & G. B. West) (Oxford University Press, New York, 2000).

    Google Scholar 

  5. Wheatley, D. N. & Bowser, S. S. Length control of primary cilia: analysis of monociliate and multiciliate PtK1 cells. Biol. Cell 92, 573–582 (2000).

    CAS  PubMed  Google Scholar 

  6. Tam, L. W., Wilson, N. F. & Lefebvre, P. A. A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J. Cell Biol. 176, 819–829 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Yan, M., Rayapuram, N. & Subramani, S. The control of peroxisome number and size during division and proliferation. Curr. Opin. Cell Biol. 17, 376–383 (2005).

    CAS  PubMed  Google Scholar 

  8. Guo, Y. et al. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453, 657–661 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Katsura, I. Determination of bacteriophage λ tail length by a protein ruler. Nature 327, 73–75 (1987). Demonstrates that the length of a biological structure can be determined by the length of a single protein, which apparently acts as a ruler during assembly.

    CAS  PubMed  Google Scholar 

  10. Shibata, S. et al. FliK regulates flagellar hook length as an internal ruler. Mol. Microbiol. 64, 1404–1415 (2007).

    CAS  PubMed  Google Scholar 

  11. Journet, L., Agrain, C., Broz, P. & Cornelis, G. R. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302, 1757–1760 (2003).

    CAS  PubMed  Google Scholar 

  12. Fowler, V. M., McKeown, C. R. & Fischer, R. S. Nebulin: does it measure up as a ruler? Curr. Biol. 16, R18–R20 (2006).

    CAS  PubMed  Google Scholar 

  13. Stephens, R. E. Quantal tektin synthesis and ciliary length in sea-urchin embryos. J. Cell Sci. 92, 403–413 (1989).

    CAS  PubMed  Google Scholar 

  14. Rosenbaum, J. L., Moulder, J. E. & Ringo, D. L. Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J. Cell Biol. 41, 600–619 (1969).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Lefebvre, P. A. & Rosenbaum, J. L. Regulation of the synthesis and assembly of ciliary and flagellar proteins during regeneration. Ann. Rev. Cell Biol. 2, 517–546 (1986).

    CAS  PubMed  Google Scholar 

  16. Marshall, W. F., Qin, H., Rodrigo Brenni, M. & Rosenbaum, J. L. Flagellar length control system: testing a simple model based on intraflagellar transport and turnover. Mol. Biol. Cell 16, 270–278 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Sriburi, R., Jackowski, S., Mori, K. & Brewer, J. W. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167, 35–41 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Cox, J. S., Chapman, R. E. & Walter, P. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8, 1805–1814 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Bernales, S., McDonald, K. L. & Walter, P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4, e413 (2006).

    Google Scholar 

  20. Coyne, B. & Rosenbaum, J. L. Flagellar elongation and shortening in Chlamydomonas. II. Re-utilization of flagellar proteins. J. Cell Biol. 47, 777–781 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Marshall, W. F. & Rosenbaum, J. L. Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. J. Cell Biol. 155, 405–414 (2001). Presents a simple size-control mechanism in which size-dependent assembly counteracts size-independent disassembly, with the two processes balancing only at a unique value for size.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Rosenbaum, J. L. & Witman, G. B. Intraflagellar transport. Nature Rev. Mol. Cell Biol. 3, 813–825 (2002).

    CAS  Google Scholar 

  23. Tyska, M. J. & Mooseker, M. S. MYO1A (brush border myosin I) dynamics in the brush border of LLC-PK1-CL4 cells. Biophys. J. 82, 1869–1883 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Rzadzinska, A. K., Schneider, M. E., Davies, C., Riordan, G. P. & Kachar, B. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J. Cell Biol. 164, 887–897 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Keener, J. How Salmonella typhimurium measures the length of flagellar filaments. Bull. Math. Biol. 68, 1761–1778 (2006).

    CAS  PubMed  Google Scholar 

  26. Varga, V. et al. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nature Cell Biol. 8, 957–962 (2006).

    CAS  PubMed  Google Scholar 

  27. Burbank, K. S., Mitchison, T. J. & Fisher, D. S. Slide-and-cluster models for spindle assembly. Curr. Biol. 17, 1373–1383 (2007).

    CAS  PubMed  Google Scholar 

  28. Hennis, A. S. & Birky, C. W. Stochastic partitioning of chloroplasts at cell division in the alga Olisthodiscus, and compensating control of chloroplast replication. J. Cell Sci. 70, 1–15 (1984).

    CAS  PubMed  Google Scholar 

  29. Marshall, W. F. Stability and robustness of an organelle number control system: modeling and measuring homeostatic regulation of centriole abundance. Biophys. J. 93, 1818–1833 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Marshall, W. F., Vucica, Y. & Rosenbaum, J. L. Kinetics and regulation of de novo centriole assembly. Implications for the mechanism of centriole duplication. Curr. Biol. 11, 308–317 (2001).

    CAS  PubMed  Google Scholar 

  31. La Terra, S. et al. The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 168, 713–722 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Paulsson, J. & Ehrenberg, M. Noise in a minimal regulatory network: plasmid copy number control. Quart. Rev. Biophys. 34, 1–59 (2001).

    CAS  Google Scholar 

  33. Umen, J. G. The elusive sizer. Curr. Opin. Cell Biol. 17, 435–441 (2005).

    CAS  PubMed  Google Scholar 

  34. Bergeland, T., Widerberg, J., Bakke, O. & Nordeng, T. W. Mitotic partitioning of endosomes and lysosomes. Curr. Biol. 11, 644–651 (2001).

    CAS  PubMed  Google Scholar 

  35. Ludford, R. J. & Gatenby, J. B. Dictyokinesis in germ cells. Proc. R. Soc. Lond., B, Biol. Sci. 92, 235–244 (1921).

    Google Scholar 

  36. Lucocq, J. M. & Warren, G. Fragmentation and partitioning of the Golgi apparatus during mitosis in HeLA cells. EMBO J. 6, 3239–3246 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Warren, G. Membrane partitioning during cell division. Annu. Rev. Biochem. 62, 323–348 (1993).

    CAS  PubMed  Google Scholar 

  38. Farré, J. C. & Subramani, S. Peroxisome turnover by micropexophagy: an autophagy-related process. Trends Cell Biol. 14, 515–523 (2004).

    PubMed  Google Scholar 

  39. Morgan, T. H. Regeneration of proportionate structures in Stentor. Biol. Bull. 2, 311–328 (1901).

    Google Scholar 

  40. Bakowska, J. & Jerka-Dziadosz, M. Ultrastructural aspect of size dependent regulation of surface pattern of complex ciliary organelle in a protozoan ciliate. J. Embryol. Exp. Morph. 59, 355–375 (1980).

    CAS  PubMed  Google Scholar 

  41. Malawista, S. E. & Van Blaricom, G. Cytoplasts made from human blood polymorphonuclear leukocytes with or without heat: preservation of both motile function and respiratory burst oxidase activity. Proc. Natl Acad. Sci. USA 84, 454–458 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Verkhkovsky, A. B., Svitkina, T. M. & Borisy, G. G. Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11–20 (1999).

    Google Scholar 

  43. Wedlich-Soldner, R., Altschuler, S., Wu, L. & Li, R. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299, 1231–1235 (2003). Demonstrates a simple self-organizing polarity system by combining modelling and experimental measurements.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  45. Yam, P. T. et al. Actin–myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J. Cell Biol. 178, 1207–1221 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Ozbudak, E. M., Becskei, A. & van Oudenaarden, A. A system of counteracting feedback loops regulates Cdc42p activity during spontaneous cell polarization. Dev. Cell 9, 565–571 (2005).

    CAS  PubMed  Google Scholar 

  47. Jones, C. et al. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nature Genet. 40, 69–77 (2008).

    CAS  PubMed  Google Scholar 

  48. Montcouquiol, M. et al. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173–177 (2003).

    CAS  PubMed  Google Scholar 

  49. Kupfer, A., Dennert, G. & Singer, S. J. Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc. Natl Acad. Sci. USA 80, 7224–7228 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Sanchez-Madrid, F. & Serrador, J. M. Mitochondrial redistribution: adding new players to the chemotaxis game. Trends Immunol. 38, 193–196 (2007).

    Google Scholar 

  51. Kupfer, A., Louvard, D. & Singer, S. J. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc. Natl Acad. Sci. USA 79, 2603–2607 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Zmuda, J. F. & Rivas, R. J. The Golgi apparatus and the centrosome are localized to the sites of newly emerging axons in cerebellar granule neurons in vitro. Cell. Motil. Cytoskel. 41, 18–38 (1998).

    CAS  Google Scholar 

  53. Agutter, P. S. & Wheatley, D. N. Random walks and cell size. Bioessays 22, 1018–1023 (2000).

    CAS  PubMed  Google Scholar 

  54. Verkman, A. S. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 27, 27–33 (2002).

    CAS  PubMed  Google Scholar 

  55. Sun, J. & Weinstein, H. Toward realistic modeling of dynamic processes in cell signaling: quantification of macromolecular crowding effects. J. Chem. Phys. 127, 155105 (2007).

    PubMed  Google Scholar 

  56. Ridgway, D. et al. Coarse-grained molecular simulation of diffusion and reaction kinetics in a crowded virtual cytoplasm. Biophys. J. 94, 3748–3759 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Prodon, F., Sardet, C. & Nishida, H. Cortical and cytoplasmic flows driven by actin microfilaments polarize the cortical ER–mRNA domain along the a–v axis in ascidian oocytes. Dev. Biol. 313, 682–699 (2008).

    CAS  PubMed  Google Scholar 

  58. Gomes, E. R., Jani, S. & Gundersen, G. G. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451–463 (2005).

    CAS  PubMed  Google Scholar 

  59. Carvalho, P., Tirnauer, J. S. & Pellman, D. Surfing on microtubule ends. Trends Cell Biol. 13, 229–237 (2003).

    CAS  PubMed  Google Scholar 

  60. Gundersen, G. G., Gomes, E. R. & Wen, Y. Cortical control of microtubule stability and polarization. Curr. Opin. Cell Biol. 16, 106–112 (2004).

    CAS  PubMed  Google Scholar 

  61. Wu, X., Xiang, X. & Hammer, J. A. Motor proteins at the microtubule plus-end. Trends Cell Biol. 16, 135–143 (2006).

    PubMed  Google Scholar 

  62. Pearson, C. G. & Bloom, K. Dynamic microtubules lead the way for spindle positioning. Nature Rev. Mol. Cell Biol. 5, 481–492 (2004).

    CAS  Google Scholar 

  63. Grill, S. W. & Hyman, A. A. Spindle positioning by cortical pulling forces. Dev. Cell 8, 461–465 (2005).

    CAS  PubMed  Google Scholar 

  64. Watanabe, T., Noritake, J. & Kaibuchi, K. Regulation of microtubules in cell migration. Trends Cell Biol. 15, 76–83 (2005).

    CAS  PubMed  Google Scholar 

  65. Allan, V. J., Thompson, H. M. & McNiven, M. A. Motoring around the Golgi. Nature Cell Biol. 4, E236–E242 (2002).

    CAS  PubMed  Google Scholar 

  66. Rios, R. M. & Bornens, M. The Golgi apparatus at the cell centre. Curr. Opin. Cell Biol. 15, 60–66 (2003).

    CAS  PubMed  Google Scholar 

  67. Barr, F. A. & Egerer, J. Golgi positioning: are we looking at the right MAP? J. Cell Biol. 168, 993–998 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Chabin-Brion, K. et al. The Golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell 12, 2047–2060 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Efimov, A. et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12, 917–930 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Drabek, K. et al. Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr. Biol. 16, 2259–2264 (2006).

    CAS  PubMed  Google Scholar 

  71. Feldman, J. L., Geimer, S. & Marshall, W. F. The mother centriole plays an instructive role in defining cell geometry. PLoS Biol. 5, e149 (2007).

    PubMed  PubMed Central  Google Scholar 

  72. Svetina, S. & Zeks, B. Shape behavior of lipid vesicles as the basis of some cellular processes. Anat. Rec. 268, 215–225 (2002).

    CAS  PubMed  Google Scholar 

  73. Deuling, H. J. & Helfrich, W. Curvature elasticity of fluid membranes — catalog of vesicle shapes. Journal De Physique 37, 1335–1345 (1976).

    CAS  Google Scholar 

  74. Kas, J. & Sackmann, E. Shape transitions and shape stability of giant phospholipid vesicles in pure water induced by area-to-volume changes. Biophys. J. 60, 825–844 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Seifert, U. Configurations of fluid membranes and vesicles. Advances in Physics 46, 13–137 (1997).

    CAS  Google Scholar 

  76. McMahon, H. T. & Gallop, J. L. Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature 438, 590–596 (2005).

    CAS  PubMed  Google Scholar 

  77. Veatch, S. L. & Keller, S. L. Organization in lipid membranes containing cholesterol. Phys. Rev. Lett. 89, 268101 (2002).

    PubMed  Google Scholar 

  78. Baumgart, T., Hess, S. T. & Webb, W. W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821–824 (2003).

    CAS  PubMed  Google Scholar 

  79. Dobereiner, H. G., Kas, J., Noppl, D., Sprenger, I. & Sackmann, E. Budding and fission of vesicles. Biophys. J. 65, 1396–1403 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Julicher, F. & Lipowsky, R. Domain-induced budding of vesicles. Phys. Rev. Lett. 70, 2964–2967 (1993).

    CAS  PubMed  Google Scholar 

  81. Roux, A. et al. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J. 24, 1537–1545 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Zimmerberg, J. & Kozlov, M. M. How proteins produce cellular membrane curvature. Nature Rev. Mol. Cell Biol. 7, 9–19 (2006).

    CAS  Google Scholar 

  83. Farsad, K. & De Camilli, P. Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372–381 (2003).

    CAS  PubMed  Google Scholar 

  84. Antonny, B. Membrane deformation by protein coats. Curr. Opin. Cell Biol. 18, 386–394 (2006).

    CAS  PubMed  Google Scholar 

  85. Frost, A. et al. Structural basis of membrane invagination by F-BAR domains. Cell 132, 807–817 (2008). Describes how a class of membrane curvature-inducing proteins operates at a structural level.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Shnyrova, A. V. et al. Vesicle formation by self-assembly of membrane-bound matrix proteins into a fluidlike budding domain. J. Cell Biol. 179, 627–633 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Shibata, Y., Voeltz, G. K. & Rapoport, T. A. Rough sheets and smooth tubules. Cell 126, 435–439 (2006).

    CAS  PubMed  Google Scholar 

  88. Dabora, S. L. & Sheetz, M. P. The microtubule-dependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts. Cell 54, 27–35 (1988).

    CAS  PubMed  Google Scholar 

  89. Vale, R. D. & Hotani, H. Formation of membrane networks in vitro by kinesin-driven microtubule movement. J. Cell Biol. 107, 2233–2241 (1988).

    CAS  PubMed  Google Scholar 

  90. Leduc, C. et al. Cooperative extraction of membrane nanotubes by molecular motors. Proc. Natl Acad. Sci. USA 101, 17096–17101 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Dreier, L. & Rapoport, T. A. In vitro formation of the endoplasmic reticulum occurs independently of microtubules by a controlled fusion reaction. J. Cell Biol. 148, 883–898 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Waterman-Storer, C. M. & Salmon, E. D. Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 8, 798–806 (1998).

    CAS  PubMed  Google Scholar 

  93. Vedrenne, C. & Hauri, H. P. Morphogenesis of the endoplasmic reticulum: beyond active membrane expansion. Traffic 7, 639–646 (2006).

    CAS  PubMed  Google Scholar 

  94. Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M. & Rapoport, T. A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573–586 (2006). Shows how proteins can induce specific changes in membrane shape.

    CAS  PubMed  Google Scholar 

  95. De Craene, J. O. et al. Rtn1p is involved in structuring the cortical endoplasmic reticulum. Mol. Biol. Cell 17, 3009–3020 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Hu, J. et al. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319, 1247–1250 (2008).

    CAS  PubMed  Google Scholar 

  97. Bereiter-Hahn, J. Behavior of mitochondria in the living cell. Int. Rev. Cytol. 122, 1–63 (1990).

    CAS  PubMed  Google Scholar 

  98. Okamoto, K. & Shaw, J. M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39, 503–536 (2005).

    CAS  PubMed  Google Scholar 

  99. Boldogh, I. R. & Pon, L. A. Mitochondria on the move. Trends Cell Biol. 17, 502–510 (2007).

    CAS  PubMed  Google Scholar 

  100. Hoppins, S., Lackner, L. & Nunnari, J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751–780 (2007).

    CAS  PubMed  Google Scholar 

  101. Merz, S., Hammermeister, M., Altmann, K., Durr, M. & Westermann, B. Molecular machinery of mitochondrial dynamics in yeast. Biol. Chem. 388, 917–926 (2007).

    CAS  PubMed  Google Scholar 

  102. Nunnari, J. et al. Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell 8, 1233–1242 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Arakaki, N. et al. Dynamics of mitochondria during the cell cycle. Biol. Pharm. Bull. 29, 1962–1965 (2006).

    CAS  PubMed  Google Scholar 

  104. Taguchi, N., Ishihara, N., Jofuku, A., Oka, T. & Mihara, K. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282, 11521–11529 (2007).

    CAS  PubMed  Google Scholar 

  105. Youle, R. J. & Karbowski, M. Mitochondrial fission in apoptosis. Nature Rev. Mol. Cell Biol. 6, 657–663 (2005).

    CAS  Google Scholar 

  106. Egner, A., Jakobs, S. & Hell, S. W. Fast 100-nm resolution three-dimensional microscope reveals structural plasticity of mitochondria in live yeast. Proc. Natl Acad. Sci. USA 99, 3370–3375 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Keren, K. et al. Mechanism of shape determination in motile cells. Nature 453, 475–480 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Solomon, F. Specification of cell morphology by endogenous determinants. J. Cell Biol. 90, 547–553 (1981).

    CAS  PubMed  Google Scholar 

  109. Bouck, G. B. & Brown, D. L. Microtubule biogenesis and cell shape in Ochromonas: II. The role of nucleating sites in shape development. J. Cell Biol. 56, 360–378 (1987).

    Google Scholar 

  110. Albrecht-Buehler, G. Daughter 3T3 cells. Are they mirror images of each other? J. Cell Biol. 72, 595–603 (1977). Shows images of sister cells that seem to be mirror images of each other, suggesting the propagation of structural determinants to the two daughter cells in opposite directions by the mitotic spindle during division.

    CAS  PubMed  Google Scholar 

  111. Solomon, F. Detailed neurite morphologies of sister neuroblastoma cells are related. Cell 16, 165–169 (1979).

    CAS  PubMed  Google Scholar 

  112. Locke, M. Is there somatic inheritance of intracellular patterns? J. Cell Biol. 96, 563–567 (1990).

    Google Scholar 

  113. Tawk, M. et al. A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446, 797–800 (2007).

    CAS  PubMed  Google Scholar 

  114. Beisson, J. & Sonneborn, T. M. Cytoplasmic inheritance of the organization of the cell cortex in Paramecium aurelia. Proc. Natl Acad. Sci. USA 53, 275–282 (1965). A classic study showing that when part of the cortex of a ciliate is rearranged, the rearrangement can propagate for multiple cell divisions without any accompanying genetic change.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Shi, X. B. & Frankel, J. Morphology and development of mirror-image doublets of Stylonychia mytilus. J. Protozool. 37, 1–13 (1990).

    CAS  PubMed  Google Scholar 

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Acknowledgements

W.F.M. acknowledges the support of the WM Keck Foundation, the Searle Scholars Program and NIH grant R01 GM077004. S.M.R. acknowledges the support of the Sandler Postdoctoral Research Fellowship.

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  1. Department of Biochemistry and Biophysics, University of California, San Francisco, 600 16th Street, San Francisco, 94158, California, USA

    Susanne M. Rafelski & Wallace F. Marshall

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Glossary

Self-organizing process

A process by which a set of components that can, in principle, be connected in various possible patterns will spontaneously associate into a limited subset of patterns, without any external input of information. 'Self-organization' is to be contrasted with 'self-assembly', in which components can only fit together such that only one pattern is possible.

Cilium

A microtubule-based motile and sensory organelle that projects from the surface of many eukaryotic cells.

Flagellum

An alternative term for cilia when applied to eukaryotic cells.

Mitotic spindle

A highly dynamic array of microtubules that forms during mitosis and serves to move the duplicated chromosomes apart.

Centriole

A short, barrel-like array of microtubules that organizes the centrosome and contributes to cytokinesis and cell-cycle progression.

Autophagy

A pathway for the recycling of cellular contents, in which materials inside the cell are packaged into vesicles and are then targeted to the vacuole or lysosome for bulk turnover.

Binomial statistics

A statistical distribution that describes the probability distribution that is obtained by several successive decisions, each of which has two possible outcomes with constant probabilities. For example, the distribution of the numbers of heads or tails after a particular number of coin flips.

Fluctuating asymmetry

Asymmetry resulting from slight stochastic differences in the molecular concentration in two different regions of a cell.

Centrosome

An organelle that contains the centrioles and that anchors the 'minus' ends of microtubules.

Dynamic morphology

A term that considers complex organelles not as static structures, but as encompassing the effects of constant shape-altering dynamics.

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Rafelski, S., Marshall, W. Building the cell: design principles of cellular architecture. Nat Rev Mol Cell Biol 9, 593–602 (2008). https://doi.org/10.1038/nrm2460

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