Home LiteratureArticle Details
PMID: 15496456 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Flagellar length control system: testing a simple model based on intraflagellar transport and turnover.

Molecular biology of the cell ·Vol. 16 ·No. 1 ·2005-01-00 ·Pages 270-8

Marshall WF, Qin H, Rodrigo Brenni M, Rosenbaum JL

Abstract

Flagellar length regulation provides a simple model system for addressing the general problem of organelle size control. Based on a systems-level analysis of flagellar dynamics, we have proposed a mechanism for flagellar length control in which length is set by the balance of continuous flagellar assembly and disassembly. The model proposes that the assembly rate is length dependent due to the inherent length dependence of intraflagellar transport, whereas disassembly is length independent, such that the two rates can only reach a balance point at a single length. In this report, we test this theoretical model by using three different measurements: 1) the quantity of intraflagellar transport machinery as a function of length, 2) the variation of flagellar length as a function of flagellar number, and 3) the rate of flagellar growth as a function of length. We find that the quantity of intraflagellar transport machinery is independent of length, that flagellar length is a decreasing function of flagellar number, and that flagellar growth rate in regenerating flagella depends on length and not on the time since regeneration began. These results are consistent with the balance-point model for length control. The three strategies used here are not limited to flagella and can in principle be adapted to probe size control systems for any organelle.

MeSH Terms
Animals Biological Transport Chlamydomonas/metabolism,physiology Flagella/metabolism,physiology Hydrogen-Ion Concentration Macromolecular Substances/metabolism Microscopy, Electron Models, Biological Models, Theoretical Mutation Organelles/metabolism Time Factors
Chemicals
Macromolecular Substances
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Marshall Wallace F
Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94143, USA. wmarshall@biochem.ucsf.edu
Qin Hongmin
Rodrigo Brenni Mónica
Rosenbaum Joel L
References (36)
36 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. The UNI3 gene is required for assembly of basal bodies of Chlamydomonas and encodes delta-tubulin, a new member of the tubulin superfamily.
    Mol Biol Cell. 1998 Jun;9(6):1293-308 PMID: 9614175
  3. Resorption of organelles containing microtubules.
    Cytobios. 1974 Mar-Apr;9(35):142-61 PMID: 4603233
  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. Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control.
    J Cell Biol. 2001 Oct 29;155(3):405-14 PMID: 11684707
  6. Genetic analysis of long-flagella mutants of Chlamydomonas reinhardtii.
    Genetics. 1988 Apr;118(4):637-48 PMID: 3366366
  7. Abnormal basal-body number, location, and orientation in a striated fiber-defective mutant of Chlamydomonas reinhardtii.
    J Cell Biol. 1983 Jun;96(6):1697-707 PMID: 6853600
  8. Cellular deflagellation.
    Int Rev Cytol. 2004;233:47-91 PMID: 15037362
  9. Conditional mutants in Chlamydomonas reinhardtii blocked in the vegetative cell cycle. I. An analysis of cell cycle block points.
    J Cell Biol. 1973 Jun;57(3):760-72 PMID: 4698905
  10. 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
  11. Flagellar protein dynamics in Chlamydomonas.
    J Biol Chem. 2001 Aug 10;276(32):29754-63 PMID: 11384985
  12. Flagellum mutants of Chlamydomonas reinhardii.
    J Gen Microbiol. 1972 Aug;71(3):525-40 PMID: 4647471
  13. Organelle size regulation: length matters.
    Curr Biol. 2003 Jul 1;13(13):R506-7 PMID: 12842024
  14. A case of an infertile man with short-tailed spermatozoa.
    Andrologia. 1996 Mar-Apr;28(2):81-7 PMID: 8849049
  15. Extreme asthenozoospermia and chronic respiratory disease: a new variant of the immotile cilia syndrome.
    Int J Androl. 1990 Jun;13(3):216-22 PMID: 2387641
  16. 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
  17. Size control in dynamic organelles.
    Trends Cell Biol. 2002 Sep;12(9):414-9 PMID: 12220861
  18. The intraflagellar transport machinery of Chlamydomonas reinhardtii.
    Traffic. 2003 Jul;4(7):435-42 PMID: 12795688
  19. Analysis of flagellar size control using a mutant of Chlamydomonas reinhardtii with a variable number of flagella.
    J Cell Biol. 1982 Jan;92(1):170-5 PMID: 7056798
  20. Intraflagellar transport.
    Nat Rev Mol Cell Biol. 2002 Nov;3(11):813-25 PMID: 12415299
  21. 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
  22. Short-Flagella Mutants of Chlamydomonas reinhardtii.
    Genetics. 1987 Apr;115(4):685-91 PMID: 17246376
  23. 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
  24. The Vfl1 Protein in Chlamydomonas localizes in a rotationally asymmetric pattern at the distal ends of the basal bodies.
    J Cell Biol. 2001 Apr 2;153(1):63-74 PMID: 11285274
  25. Mutational analysis of centrin: an EF-hand protein associated with three distinct contractile fibers in the basal body apparatus of Chlamydomonas.
    J Cell Biol. 1992 Dec;119(6):1613-24 PMID: 1361488
  26. A novel MAP kinase regulates flagellar length in Chlamydomonas.
    Curr Biol. 2003 Jul 1;13(13):1145-9 PMID: 12842015
  27. Defective temporal and spatial control of flagellar assembly in a mutant of Chlamydomonas reinhardtii with variable flagellar number.
    J Cell Biol. 1985 Mar;100(3):955-64 PMID: 3972905
  28. Defects in cholangiocyte fibrocystin expression and ciliary structure in the PCK rat.
    Gastroenterology. 2003 Nov;125(5):1303-10 PMID: 14598246
  29. Kinetics and regulation of de novo centriole assembly. Implications for the mechanism of centriole duplication.
    Curr Biol. 2001 Mar 6;11(5):308-17 PMID: 11267867
  30. Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis.
    J Cell Biol. 1978 Jul;78(1):8-27 PMID: 149796
  31. 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
  32. Polarity of flagellar assembly in Chlamydomonas.
    J Cell Biol. 1992 Dec;119(6):1605-11 PMID: 1281816
  33. Chlamydomonas fla mutants reveal a link between deflagellation and intraflagellar transport.
    BMC Cell Biol. 2003 Aug 20;4:11 PMID: 12930563
  34. 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
  35. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body.
    J Cell Biol. 2004 Jan 19;164(2):255-66 PMID: 14718520
  36. Flagellar elongation and shortening in chlamydomonas. II. Re-utilization of flagellar proteins.
    J Cell Biol. 1970 Dec;47(3):777-81 PMID: 5497553
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2005-01-00
Epub
2004-00-20
Pages
270-8
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC539171
Subset
IM
Grants
NIGMS NIH HHS · R01 GM014642 · United States
NIGMS NIH HHS · R37 GM014642 · United States
NIGMS NIH HHS · GM-14642 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com