1932

Abstract

The cell represents a highly organized state of living matter in which numerous geometrical parameters are under dynamic regulation in order to match the form of a cell with its function. Cells appear capable of regulating not only the total quantity of their internal organelles, but also the size and number of those organelles. The regulation of three parameters, size, number, and total quantity, can in principle be accomplished by regulating the production or growth of organelles, their degradation or disassembly, and their partitioning among daughter cells during division. Any or all of these steps could in principle be under regulation. But if organelle assembly or disassembly is regulated by number or size, how would the cell know how many copies of an organelle it has, or how big they are?

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/content/journals/10.1146/annurev-biophys-062215-010905
2016-07-05
2024-04-19
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Literature Cited

  1. Abuladze NK, Gingery M, Tsai J, Eiserling FA. 1.  1994. Tail length determination in bacteriophage T4. Virology 199:301–10 [Google Scholar]
  2. Avasthi P, Marshall WF. 2.  2013. Ciliary regulation: Disassembly takes the spotlight. Curr. Biol. 23:R1001–3 [Google Scholar]
  3. Bernales S, McDonald KL, Walter P. 3.  2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLOS Biol. 4:e423 [Google Scholar]
  4. Brewer JW, Jackowski S. 4.  2012. UPR-mediated membrane biogenesis in B cells. Biochem. Res. Int. 2012:739471 [Google Scholar]
  5. Castillo A, Nowak R, Littlefield KP, Fowler VM, Littlefield RS. 5.  2009. A nebulin ruler does not dictate thin filament lengths. Biophys. J. 96:1856–65 [Google Scholar]
  6. Chan YH, Marshall WF. 6.  2010. Scaling properties of cell and organelle size. Organogenesis 6:88–96 [Google Scholar]
  7. Chan YH, Marshall WF. 7.  2014. Organelle size scaling of the budding yeast vacuole is turned by membrane trafficking rates. Biophys. J. 106:1986–96 [Google Scholar]
  8. Coffman VC, Lee IJ, Wu JQ. 8.  2014. Counting Molecules within Cells Santa Rosa, CA: Morgan & Claypool Life Sci.
  9. Cox JS, Chapman RE, Walter P. 9.  1997. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8:1805–14 [Google Scholar]
  10. Decker M, Jaensch S, Pozniakovsky A, Zinke A, O'Connell KF. 10.  et al. 2011. Limiting amounts of centrosome material set centrosome size in C. elegans embryos. Curr. Biol. 21:1259–67 [Google Scholar]
  11. Dingle AD.11.  1970. Control of flagellum number in Naegleria. J. Cell Sci. 7:463–82 [Google Scholar]
  12. Ellis EL, Delbrück M. 12.  1939. The growth of bacteriophage. J. Gen. Physiol. 22:365–84 [Google Scholar]
  13. Frankel J.13.  1973. Dimensions of control of cortical patterns in Euplotes: the role of pre-existing structure, the clonal life cycle, and the genotype. J. Exp. Zool. 183:71–94 [Google Scholar]
  14. Goehring NW, Hyman AA. 14.  2012. Organelle growth control through limiting pools of cytoplasmic components. Curr. Biol. 22:R330–39 [Google Scholar]
  15. Goldenfeld N, Woese C. 15.  2011. Life is physics: evolution as a collective phenomenon far from equilibrium. Annu. Rev. Condens. Matter Phys. 2:375–99 [Google Scholar]
  16. Good MC, Vahey MD, Skandarajah A, Fletcher DA, Heald R. 16.  2013. Cytoplasmic volume modulates spindle size during embryogenesis. Science 342:856–60 [Google Scholar]
  17. Hazel J, Krutkramelis K, Mooney P, Tomschik M, Gerow K. 17.  et al. 2013. Changes in cytoplasmic volume are sufficient to drive spindle scaling. Science 342:853–56 [Google Scholar]
  18. Hennis AS, Birky CW. 18.  1984. Stochastic partitioning of chloroplasts at cell division in the alga Olisthodiscus, and compensating control of chloroplast replication. J. Cell Sci. 70:1–15 [Google Scholar]
  19. Hilton LK, Gunawardane K, Kim JW, Schwarz MC, Quarmby LM. 19.  2013. The kinases LF4 and CNK2 control ciliary length by feedback regulation of assembly and disassembly. Curr. Biol. 23:2208–14 [Google Scholar]
  20. Hiraki M, Nakazawa Y, Kamiya R, Hirono M. 20.  2007. Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr. Biol. 17:1778–83 [Google Scholar]
  21. Huh D, Paulsson J. 21.  2011. Random partitioning of molecules at cell division. PNAS 108:15004–9 [Google Scholar]
  22. Huxley J.22.  1972. Problems of Relative Growth Mineola, NY: Dover
  23. Jennings HS.23.  1937. Formation, inheritance, and variation of the teeth in Difflugia corona. A study of the morphogenetic activities of rhizopod protoplasm. J. Exp. Zool. 77:287–336 [Google Scholar]
  24. Jorgensen P, Edgington NP, Schneider BL, Rupes I, Tyers M, Futcher B. 24.  2007. The size of the nucleus increases as yeast cells grow. Mol. Biol. Cell 18:3523–32 [Google Scholar]
  25. Kalab P, Weiss K, Heald R. 25.  2002. Visualization of Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 295:2452–56 [Google Scholar]
  26. Kannegaard E, Rego EH, Schuck S, Feldman JL, Marshall WF. 26.  2014. Quantitative analysis and modeling of katanin function in flagellar length control. Mol. Biol. Cell 25:3686–98 [Google Scholar]
  27. Katsura I. 27.  1987. Determination of bacteriophage λ tail length by a protein ruler. Nature 327:73–75 [Google Scholar]
  28. Katsura I.28.  1990. Mechanism of length determination in bacteriophage lambda tails. Adv. Biophys. 26:1–18 [Google Scholar]
  29. Katsura I, Hendrix RW. 29.  1984. Length determination in bacteriophage lambda tails. Cell 39:691–98 [Google Scholar]
  30. Khodjakov A, Rieder CL, Sluder G, Cassels G, Sibon O, Wang CL. 30.  2002. De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol. 158:1171–81 [Google Scholar]
  31. Kirschner M, Gerhart J, Mitchison T. 31.  2000. Molecular “vitalism.”. Cell 100:79–88 [Google Scholar]
  32. Kuchka MR, Jarvik JW. 32.  1982. Analysis of flagellar size control using a mutant of Chlamydomonas reinhardtii with a variable number of flagella. J. Cell Biol. 92:170–75 [Google Scholar]
  33. Labeit S, Gibson T, Lakey A, Leonard K, Zeviani M. 33.  et al. 1991. Evidence that nebulin is a protein ruler in muscle thin filaments. FEBS Lett. 282:313–16 [Google Scholar]
  34. Labeit S, Kolmerer B. 34.  1995. The primary structure of human nebulin and its correlation to muscle structure. J. Mol. Biol. 248:308–15 [Google Scholar]
  35. Levy EM.35.  1974. Flagellar elongation as a moving boundary problem. Bull. Math. Biol. 36:265–73 [Google Scholar]
  36. Littlefield R, Almenar-Queralt A, Fowler VM. 36.  2001. Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat. Cell Biol. 3:544–51 [Google Scholar]
  37. Loughlin R, Wilbur JD, McNally FJ, Nedelec FJ, Heald R. 37.  2011. Katanin contributes to interspecies spindle length scaling in Xenopus. Cell 147:1397–407 [Google Scholar]
  38. Ludington WB, Ishikawa H, Serebrenik YV, Ritter A, Hernandez-Lopez RA. 38.  et al. 2015. A systematic comparison of mathematical models for inherent measurement of ciliary length: how a cell can measure length and volume. Biophys. J. 108:1361–79 [Google Scholar]
  39. Ludington WB, Shi LZ, Zhu Q, Berns MW, Marshall WF. 39.  2012. Organelle size equalization by a constitutive process. Curr. Biol. 22:2173–79 [Google Scholar]
  40. Ludington WB, Wemmer KA, Lechtreck KF, Witman GB, Marshall WF. 40.  2013. Avalanche-like behavior in ciliary import. PNAS 110:3925–30 [Google Scholar]
  41. Marshall WF. 41.  2007. Stability and robustness of an organelle number control system: modeling and measuring homeostatic regulation of centriole abundance. Biophys. J. 93:1818–33 [Google Scholar]
  42. Marshall WF, Vucica Y, Rosenbaum JL. 42.  2001. Kinetics and regulation of de novo centriole assembly. Implications for the mechanism of centriole duplication. Curr. Biol. 11:308–17 [Google Scholar]
  43. McElhinney AS, Kolmerer B, Fowler VM. 43.  2001. The N-terminal end of nebulin interacts with tropomodulin at the pointed ends of the thin filaments. J. Biol. Chem. 276:583–92 [Google Scholar]
  44. Monastryka I, Klionsky DJ. 44.  2006. Autophagy in organelle homeostasis: peroxisome turnover. Mol. Aspects Med. 27:483–94 [Google Scholar]
  45. Morgan TH.45.  1901. Regeneration of proportionate structures in Stentor. Biol. Bull. 2:311–28 [Google Scholar]
  46. Mukherji S, O'Shea EK. 46.  2014. Mechanisms of organelle biogenesis govern stochastic fluctuations in organelle abundance. eLife 3:e02678 [Google Scholar]
  47. Nanney DL.47.  1966. Corticotype transmission in Tetrahymena. Genetics 54:955–68 [Google Scholar]
  48. Neumann FR, Nurse P. 48.  2007. Nuclear size control in fission yeast. J. Cell Biol. 179:593–600 [Google Scholar]
  49. Norrander JM, Linck RW, Stephens RE. 49.  1995. Transcriptional control of tektin A mRNA correlates with cilia development and length determination during sea urchin embryogenesis. Development 121:1615–23 [Google Scholar]
  50. Oda T, Yanigasawa H, Kamiya R, Kikkawa M. 50.  2014. A molecular ruler determines the repeat length in eukaryotic cilia and flagella. Science 346:857–60 [Google Scholar]
  51. Pappas CT, Krieg PA, Gregorio CC. 51.  2010. Nebulin regulates actin filament lengths by a stabilization mechanism. J. Cell Biol. 189:859–70 [Google Scholar]
  52. Pedersen M, Østergaard S, Bresciani J, Vogensen FK. 52.  2000. Mutational analysis of two structural genes of the temperate lactococcal bacteriophage TP901-1 involved in tail length determination and baseplate assembly. Virology 276:315–28 [Google Scholar]
  53. Politou AS, Spadaccini R, Joseph C, Brannetti B, Guerini R. 53.  et al. 2002. The SH3 domain of nebulin binds selectively to type II peptides: theoretical prediction and experimental validation. J. Mol. Biol. 316:305–15 [Google Scholar]
  54. Rafelski SM.54.  2013. Mitochondrial network morphology: building an integrative, geometrical view. BMC Biol. 11:71 [Google Scholar]
  55. Rafelski SM, Marshall WF. 55.  2008. Building the cell: design principles of cellular architecture. Nat. Rev. Mol. Cell Biol. 9:593–602 [Google Scholar]
  56. Rafelski SM, Viana MP, Zhang Y, Chan YH, Thorn KS. 56.  et al. 2012. Mitochondrial network size scaling in budding yeast. Science 338:822–24 [Google Scholar]
  57. Rosenbaum JL, Moulder JE, Ringo DL. 57.  1969. Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J. Cell Biol. 41:600–19 [Google Scholar]
  58. Savage DF, Afonso B, Chen AH, Silver PA. 58.  2010. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327:1258–61 [Google Scholar]
  59. Schmoller KM, Turner JJ, Kõivomägi M, Skotheim JM. 59.  2015. Dilution of the cell cycle inhibitor Whi5 controls budding yeast cell size. Nature 526:268–72 [Google Scholar]
  60. Sheahan MB, Rose RJ, McCurdy DW. 60.  2004. Organelle inheritance in plant cell division: the actin cytoskeleton is required for unbiased inheritance of chloroplasts, mitochondria, and endoplasmic reticulum in dividing protoplasts. Plant J. 37:379–90 [Google Scholar]
  61. Shibata S, Takahashi N, Chevance FF, Karlinsky JE, Hughes KT, Aizawa S. 61.  2007. FliK regulates flagellar hook length as an internal ruler. Mol. Microbiol. 64:1404–15 [Google Scholar]
  62. Stephens RE.62.  1989. Quantal tektin synthesis and ciliary length in sea-urchin embryos. J. Cell Sci. 92:403–13 [Google Scholar]
  63. Uchida M, Sun Y, McDermott G, Knoechel C, LeGros MA. 63.  et al. 2011. Quantitative analysis of yeast internal architecture using soft X-ray tomography. Yeast 28:227–36 [Google Scholar]
  64. Varga V, Helenius J, Tanaka K, Hyman AA, Tanaka TU, Howard J. 64.  2006. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat. Cell Biol. 8:957–62 [Google Scholar]
  65. Wagenknecht T, Bloomfield VA. 65.  1975. Equilibrium mechanisms of length regulation in linear protein aggregates. Biopolymers 14:2297–309 [Google Scholar]
  66. Wagner S, Sorg I, Degiacomi M, Journet L, Dai Peraro M, Cornelis GR. 66.  2009. The helical content of the YscP molecular ruler determines the length of the Yersinia injectisome. Mol. Microbiol. 71:692–701 [Google Scholar]
  67. Wang L, Piao T, Cao M, Qin T, Huang L. 67.  et al. 2013. Flagellar regeneration requires cytoplasmic microtubule depolymerization and kinesin-13. J. Cell Sci. 126:1531–40 [Google Scholar]
  68. Wee DH, Hughes KT. 68.  2015. Molecular ruler determines needle length for the Salmonella Spi-1 injectisome. PNAS 112:4098–103 [Google Scholar]
  69. Wemmer KA, Marshall WF. 69.  2007. Flagellar length control in Chlamydomonas—a paradigm for organelle size regulation. Int. Rev. Cytol. 260:175–212 [Google Scholar]
  70. Wuehr M, Chen Y, Dumont S, Groen AC, Needleman DJ. 70.  et al. 2008. Evidence for an upper limit to mitotic spindle length. Curr. Biol. 18:1256–61 [Google Scholar]
  71. Xu J, Hendrix RW, Duda RL. 71.  2014. Chaperone-protein interactions that mediate assembly of the bacteriophage lambda tail to the correct length. J. Mol. Biol. 426:1004–18 [Google Scholar]
  72. Yan M, Rayapuram N, Subramani S. 72.  2005. The control of peroxisome number and size during division and proliferation. Curr. Opin. Cell Biol. 17:376–83 [Google Scholar]
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