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PMID: 11684707 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control.

The Journal of cell biology ·Vol. 155 ·No. 3 ·2001-10-29 ·Pages 405-14

Marshall WF, Rosenbaum JL

Abstract

A central question in cell biology is how cells determine the size of their organelles. Flagellar length control is a convenient system for studying organelle size regulation. Mechanistic models proposed for flagellar length regulation have been constrained by the assumption that flagella are static structures once they are assembled. However, recent work has shown that flagella are dynamic and are constantly turning over. We have determined that this turnover occurs at the flagellar tips, and that the assembly portion of the turnover is mediated by intraflagellar transport (IFT). Blocking IFT inhibits the incorporation of tubulin at the flagellar tips and causes the flagella to resorb. These results lead to a simple steady-state model for flagellar length regulation by which a balance of assembly and disassembly can effectively regulate flagellar length.

MeSH Terms
Animals Biological Transport Chlamydomonas/drug effects,genetics,metabolism Colchicine/pharmacology Flagella/drug effects,metabolism,physiology Microtubules/drug effects,metabolism Mutagenesis Tubulin/metabolism
Chemicals
Tubulin Colchicine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Marshall W F
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06520, USA. [email protected]
Rosenbaum J L
References (31)
31 references, click to expand
  1. Genetic analysis of flagellar length control in Chlamydomonas reinhardtii: a new long-flagella locus and extragenic suppressor mutations.
    Genetics. 1998 Feb;148(2):693-702 PMID: 9504917
  2. A novel WD40 protein, CHE-2, acts cell-autonomously in the formation of C. elegans sensory cilia.
    Development. 1999 Nov;126(21):4839-48 PMID: 10518500
  3. Flagellar regeneration in protozoan flagellates.
    J Cell Biol. 1967 Jul;34(1):345-64 PMID: 6033540
  4. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons.
    J Cell Biol. 1998 May 18;141(4):993-1008 PMID: 9585417
  5. Genetic analysis of long-flagella mutants of Chlamydomonas reinhardtii.
    Genetics. 1988 Apr;118(4):637-48 PMID: 3366366
  6. Inner dynein arms but not outer dynein arms require the activity of kinesin homologue protein KHP1(FLA10) to reach the distal part of flagella in Chlamydomonas.
    J Cell Biol. 1996 Apr;133(2):371-9 PMID: 8609169
  7. The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane.
    J Cell Biol. 1995 Dec;131(6 Pt 1):1517-27 PMID: 8522608
  8. The axonemal microtubules of the Chlamydomonas flagellum differ in tubulin isoform content.
    J Cell Sci. 1998 Feb;111 ( Pt 3):313-20 PMID: 9427680
  9. Flagellar protein dynamics in Chlamydomonas.
    J Biol Chem. 2001 Aug 10;276(32):29754-63 PMID: 11384985
  10. Flagellum mutants of Chlamydomonas reinhardii.
    J Gen Microbiol. 1972 Aug;71(3):525-40 PMID: 4647471
  11. Differential effects of antimitotic agents on the stability and behavior of cytoplasmic and ciliary microtubules.
    Protoplasma. 1968;65(1):167-79 PMID: 5667676
  12. Temperature-sensitive mutations affecting flagellar assembly and function in Chlamydomonas reinhardtii.
    J Cell Biol. 1977 Jan;72(1):67-85 PMID: 830657
  13. Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins.
    J Cell Biol. 1969 May;41(2):600-19 PMID: 5783876
  14. Simple method for quantitive densitometry of polyacrylamide gels using fast green.
    Anal Biochem. 1970 Jun;35(2):359-70 PMID: 4194859
  15. Kinetic stabilization of microtubule dynamics at steady state in vitro by substoichiometric concentrations of tubulin-colchicine complex.
    Biochemistry. 1995 Aug 8;34(31):9921-9 PMID: 7632691
  16. Synthesis and turnover of embryonic sea urchin ciliary proteins during selective inhibition of tubulin synthesis and assembly.
    Mol Biol Cell. 1997 Nov;8(11):2187-98 PMID: 9362062
  17. Dynein, dynactin, and kinesin II's interaction with microtubules is regulated during bidirectional organelle transport.
    J Cell Biol. 2000 Oct 2;151(1):155-66 PMID: 11018061
  18. Heterotrimeric kinesin-II is required for the assembly of motile 9+2 ciliary axonemes on sea urchin embryos.
    J Cell Biol. 1997 Sep 8;138(5):1009-22 PMID: 9281580
  19. Short-Flagella Mutants of Chlamydomonas reinhardtii.
    Genetics. 1987 Apr;115(4):685-91 PMID: 17246376
  20. Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases.
    J Cell Biol. 2001 Apr 2;153(1):13-24 PMID: 11285270
  21. Actin filaments and microtubules play different roles during bristle elongation in Drosophila.
    J Cell Sci. 2000 Apr;113 ( Pt 7):1255-65 PMID: 10704376
  22. High level expression of nonacetylatable alpha-tubulin in Chlamydomonas reinhardtii.
    Cell Motil Cytoskeleton. 1993;25(2):158-70 PMID: 7686822
  23. Evidence for four classes of microtubules in individual cells.
    J Cell Sci. 1967 Jun;2(2):169-92 PMID: 4104123
  24. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles.
    Curr Biol. 2001 Oct 16;11(20):1586-90 PMID: 11676918
  25. Polarity of flagellar assembly in Chlamydomonas.
    J Cell Biol. 1992 Dec;119(6):1605-11 PMID: 1281816
  26. Tubulin in sea urchin embryonic cilia: characterization of the membrane-periaxonemal matrix.
    J Cell Sci. 1991 Nov;100 ( Pt 3):521-31 PMID: 1808204
  27. Intraflagellar transport: the eyes have it.
    J Cell Biol. 1999 Feb 8;144(3):385-8 PMID: 9971734
  28. A motility in the eukaryotic flagellum unrelated to flagellar beating.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5519-23 PMID: 8516294
  29. Preferential incorporation of tubulin into the junctional region of ciliary outer doublet microtubules: a model for treadmilling by lattice dislocation.
    Cell Motil Cytoskeleton. 2000 Oct;47(2):130-40 PMID: 11013393
  30. Flagellar elongation and shortening in chlamydomonas. II. Re-utilization of flagellar proteins.
    J Cell Biol. 1970 Dec;47(3):777-81 PMID: 5497553
  31. Primary cilia cycle in PtK1 cells: effects of colcemid and taxol on cilia formation and resorption.
    Cell Motil Cytoskeleton. 1987;7(3):187-97 PMID: 2885096
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.200106141
Email
[email protected]
Published
2001-10-29
Epub
2001-00-29
Pages
405-14
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2150833
Subset
IM
Grants
NIGMS NIH HHS · R01 GM014642 · United States
NIGMS NIH HHS · R37 GM014642 · United States
NIGMS NIH HHS · GM14642 · United States
External Links
PubMed source DOI: 10.1083/jcb.200106141 PMC Full Text View journal details
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