Building the cell: Design principles of cellular architecture

Nature Reviews Molecular Cell Biology

Volumn 9, Issue 8, 2008, Pages 593-602

  Rafelski, Susanne M ^a   Marshall, Wallace F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; PROTEIN CDC42;

CELL DIFFERENTIATION; CELL ORGANELLE; CELL POLARITY; CELL STRUCTURE; CELL VOLUME; GENE EXPRESSION; GOLGI COMPLEX; HUMAN; LIPID ANALYSIS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; REVIEW; SARCOMERE;

ANIMALS; CELL PHYSIOLOGY; CELL POLARITY; CELL SHAPE; CELL SIZE; CELLS; CELLULAR STRUCTURES; HUMANS; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; QUANTUM THEORY;

EID: 47749146582     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm2460     Document Type: Review

References (115)

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).
2. Minton, A. P. How can biochemical reactions within cells differ from those in test tubes? J. Cell Sci. 119, 2863-2869 (2006).
3. Karsenti, E. Self-organization in cell biology: a brief history. Nature Rev. Mol. Cell Biol. 9, 255-262 (2008).
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).
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).
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).
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).
8. Guo, Y. et al. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 453, 657-661 (2008).
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.
10. Shibata, S. et al. FliK regulates flagellar hook length as an internal ruler. Mol. Microbiol. 64, 1404-1415 (2007).
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).
12. Fowler, V. M., McKeown, C. R. & Fischer, R. S. Nebulin: does it measure up as a ruler? Curr. Biol. 16, R18-R20 (2006).
13. Stephens, R. E. Quantal tektin synthesis and ciliary length in sea-urchin embryos. J. Cell Sci. 92, 403-413 (1989).
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).
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).
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).
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).
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).
19. Bernales, S., McDonald, K. L. & Walter, P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4, e413 (2006).
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).
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.
22. Rosenbaum, J. L. & Witman, G. B. Intraflagellar transport. Nature Rev. Mol. Cell Biol. 3, 813-825 (2002).
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).
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).
25. Keener, J. How Salmonella typhimurium measures the length of flagellar filaments. Bull. Math. Biol. 68, 1761-1778 (2006).
26. Varga, V. et al. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nature Cell Biol. 8, 957-962 (2006).
27. Burbank, K. S., Mitchison, T. J. & Fisher, D. S. Slide-and-cluster models for spindle assembly. Curr. Biol. 17, 1373-1383 (2007).
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).
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).
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).
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).
32. Paulsson, J. & Ehrenberg, M. Noise in a minimal regulatory network: plasmid copy number control. Quart. Rev. Biophys. 34, 1-59 (2001).
33. Umen, J. G. The elusive sizer. Curr. Opin. Cell Biol. 17, 435-441 (2005).
34. Bergeland, T., Widerberg, J., Bakke, O. & Nordeng, T. W. Mitotic partitioning of endosomes and lysosomes. Curr. Biol. 11, 644-651 (2001).
35. Ludford, R. J. & Gatenby, J. B. Dictyokinesis in germ cells. Proc. R. Soc. Lond., B, Biol. Sci. 92, 235-244 (1921).
36. Lucocq, J. M. & Warren, G. Fragmentation and partitioning of the Golgi apparatus during mitosis in HeLA cells. EMBO J. 6, 3239-3246 (1987).
37. Warren, G. Membrane partitioning during cell division. Annu. Rev. Biochem. 62, 323-348 (1993).
38. Farré, J. C. & Subramani, S. Peroxisome turnover by micropexophagy: an autophagy-related process. Trends Cell Biol. 14, 515-523 (2004).
39. Morgan, T. H. Regeneration of proportionate structures in Stentor. Biol. Bull. 2, 311-328 (1901).
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).
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).
42. Verkhkovsky, A. B., Svitkina, T. M. & Borisy, G. G. Self-polarization and directional motility of cytoplasm. Curr. Biol. 9, 11-20 (1999).
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.
44. Xu, J. et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114, 201-214 (2003).
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).
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).
47. Jones, C. et al. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nature Genet. 40, 69-77 (2008).
48. Montcouquiol, M. et al. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177 (2003).
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).
50. Sanchez-Madrid, F. & Serrador, J. M. Mitochondrial redistribution: adding new players to the chemotaxis game. Trends Immunol. 38, 193-196 (2007).
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).
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).
53. Agutter, P. S. & Wheatley, D. N. Random walks and cell size. Bioessays 22, 1018-1023 (2000).
54. Verkman, A. S. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 27, 27-33 (2002).
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).
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).
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).
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).
59. Carvalho, P., Tirnauer, J. S. & Pellman, D. Surfing on microtubule ends. Trends Cell Biol. 13, 229-237 (2003).
60. Gundersen, G. G., Gomes, E. R. & Wen, Y. Cortical control of microtubule stability and polarization. Curr. Opin. Cell Biol. 16, 106-112 (2004).
61. Wu, X., Xiang, X. & Hammer, J. A. Motor proteins at the microtubule plus-end. Trends Cell Biol. 16, 135-143 (2006).
62. Pearson, C. G. & Bloom, K. Dynamic microtubules lead the way for spindle positioning. Nature Rev. Mol. Cell Biol. 5, 481-492 (2004).
63. Grill, S. W. & Hyman, A. A. Spindle positioning by cortical pulling forces. Dev. Cell 8, 461-465 (2005).
64. Watanabe, T., Noritake, J. & Kaibuchi, K. Regulation of microtubules in cell migration. Trends Cell Biol. 15, 76-83 (2005).
65. Allan, V. J., Thompson, H. M. & McNiven, M. A. Motoring around the Golgi. Nature Cell Biol. 4, E236-E242 (2002).
66. Rios, R. M. & Bornens, M. The Golgi apparatus at the cell centre. Curr. Opin. Cell Biol. 15, 60-66 (2003).
67. Barr, F. A. & Egerer, J. Golgi positioning: are we looking at the right MAP? J. Cell Biol. 168, 993-998 (2005).
68. Chabin-Brion, K. et al. The Golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell 12, 2047-2060 (2001).
69. Efimov, A. et al. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12, 917-930 (2007).
70. Drabek, K. et al. Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr. Biol. 16, 2259-2264 (2006).
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).
72. Svetina, S. & Zeks, B. Shape behavior of lipid vesicles as the basis of some cellular processes. Anat. Rec. 268, 215-225 (2002).
73. Deuling, H. J. & Helfrich, W. Curvature elasticity of fluid membranes - catalog of vesicle shapes. Journal De Physique 37, 1335-1345 (1976).
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).
75. Seifert, U. Configurations of fluid membranes and vesicles. Advances in Physics 46, 13-137 (1997).
76. McMahon, H. T. & Gallop, J. L. Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature 438, 590-596 (2005).
77. Veatch, S. L. & Keller, S. L. Organization in lipid membranes containing cholesterol. Phys. Rev. Lett. 89, 268101 (2002).
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).
79. Dobereiner, H. G., Kas, J., Noppl, D., Sprenger, I. & Sackmann, E. Budding and fission of vesicles. Biophys. J. 65, 1396-1403 (1993).
80. Julicher, F. & Lipowsky, R. Domain-induced budding of vesicles. Phys. Rev. Lett. 70, 2964-2967 (1993).
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).
82. Zimmerberg, J. & Kozlov, M. M. How proteins produce cellular membrane curvature. Nature Rev. Mol. Cell Biol. 7, 9-19 (2006).
83. Farsad, K. & De Camilli, P. Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372-381 (2003).
84. Antonny, B. Membrane deformation by protein coats. Curr. Opin. Cell Biol. 18, 386-394 (2006).
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.
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).
87. Shibata, Y., Voeltz, G. K. & Rapoport, T. A. Rough sheets and smooth tubules. Cell 126, 435-439 (2006).
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).
89. Vale, R. D. & Hotani, H. Formation of membrane networks in vitro by kinesin-driven microtubule movement. J. Cell Biol. 107, 2233-2241 (1988).
90. Leduc, C. et al. Cooperative extraction of membrane nanotubes by molecular motors. Proc. Natl Acad. Sci. USA 101, 17096-17101 (2004).
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).
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).
93. Vedrenne, C. & Hauri, H. P. Morphogenesis of the endoplasmic reticulum: beyond active membrane expansion. Traffic 7, 639-646 (2006).
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.
95. De Craene, J. O. et al. Rtn1p is involved in structuring the cortical endoplasmic reticulum. Mol. Biol. Cell 17, 3009-3020 (2006).
96. Hu, J. et al. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science 319, 1247-1250 (2008).
97. Bereiter-Hahn, J. Behavior of mitochondria in the living cell. Int. Rev. Cytol. 122, 1-63 (1990).
98. Okamoto, K. & Shaw, J. M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39, 503-536 (2005).
99. Boldogh, I. R. & Pon, L. A. Mitochondria on the move. Trends Cell Biol. 17, 502-510 (2007).
100. Hoppins, S., Lackner, L. & Nunnari, J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780 (2007).
101. Merz, S., Hammermeister, M., Altmann, K., Durr, M. & Westermann, B. Molecular machinery of mitochondrial dynamics in yeast. Biol. Chem. 388, 917-926 (2007).
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).
103. Arakaki, N. et al. Dynamics of mitochondria during the cell cycle. Biol. Pharm. Bull. 29, 1962-1965 (2006).
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).
105. Youle, R. J. & Karbowski, M. Mitochondrial fission in apoptosis. Nature Rev. Mol. Cell Biol. 6, 657-663 (2005).
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).
107. Keren, K. et al. Mechanism of shape determination in motile cells. Nature 453, 475-480 (2008).
108. Solomon, F. Specification of cell morphology by endogenous determinants. J. Cell Biol. 90, 547-553 (1981).
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).
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.
111. Solomon, F. Detailed neurite morphologies of sister neuroblastoma cells are related. Cell 16, 165-169 (1979).
112. Locke, M. Is there somatic inheritance of intracellular patterns? J. Cell Biol. 96, 563-567 (1990).
113. Tawk, M. et al. A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446, 797-800 (2007).
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.
115. Shi, X. B. & Frankel, J. Morphology and development of mirror-image doublets of Stylonychia mytilus. J. Protozool. 37, 1-13 (1990).