Home LiteratureArticle Details
PMID: 16611747 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Members of the NIMA-related kinase family promote disassembly of cilia by multiple mechanisms.

Molecular biology of the cell ·Vol. 17 ·No. 6 ·2006-06-00 ·Pages 2799-810

Wloga D, Camba A, Rogowski K, Manning G, Jerka-Dziadosz M, Gaertig J

Abstract

The genome of Tetrahymena thermophila contains 39 loci encoding NIMA-related kinases (NRKs), an extraordinarily large number for a unicellular organism. Evolutionary analyses grouped these sequences into several subfamilies, some of which have orthologues in animals, whereas others are protist specific. When overproduced, NRKs of three subfamilies caused rapid shortening of cilia. Ultrastructural studies revealed that each NRK triggered ciliary resorption by a distinct mechanism that involved preferential depolymerization of a subset of axonemal microtubules, at either the distal or proximal end. Overexpression of a kinase-inactive variant caused lengthening of cilia, indicating that constitutive NRK-mediated resorption regulates the length of cilia. Each NRK preferentially resorbed a distinct subset of cilia, depending on the location along the anteroposterior axis. We also show that normal Tetrahymena cells maintain unequal length cilia. We propose that ciliates used a large number of NRK paralogues to differentially regulate the length of specific subsets of cilia in the same cell.

MeSH Terms
Animals Cell Cycle Proteins/classification,genetics,metabolism Cilia/physiology Genes, Protozoan Genes, Reporter Genome Green Fluorescent Proteins/genetics NIMA-Related Kinase 1 Phylogeny Protein Serine-Threonine Kinases/classification,genetics,metabolism Protozoan Proteins/chemistry,metabolism Tetrahymena thermophila/physiology,ultrastructure
Chemicals
Cell Cycle Proteins Protozoan Proteins Green Fluorescent Proteins NIMA-Related Kinase 1 Protein Serine-Threonine Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wloga Dorota
Department of Cellular Biology, University of Georgia, Athens, GA 30602-2607, USA.
Camba Amy
Rogowski Krzysztof
Manning Gerard
Jerka-Dziadosz Maria
Gaertig Jacek
References (57)
57 references, click to expand
  1. An alternating least squares approach to inferring phylogenies from pairwise distances.
    Syst Biol. 1997 Mar;46(1):101-11 PMID: 11975348
  2. 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
  3. Insulin receptor-like proteins in Tetrahymena thermophila ciliary membranes.
    Curr Biol. 2003 Jan 21;13(2):R50-2 PMID: 12546802
  4. Cytoskeletal reorganization and plasma membrane fusion in conjugating Tetrahymena.
    J Cell Sci. 1985 Feb;73:69-85 PMID: 3894390
  5. Kinesin-II is preferentially targeted to assembling cilia and is required for ciliogenesis and normal cytokinesis in Tetrahymena.
    Mol Biol Cell. 1999 Oct;10(10):3081-96 PMID: 10512852
  6. Preparation of cytoskeletal fractions from Tetrahymena thermophila.
    Methods Cell Biol. 2000;62:441-7 PMID: 10503209
  7. An aurora kinase is essential for flagellar disassembly in Chlamydomonas.
    Dev Cell. 2004 Mar;6(3):445-51 PMID: 15030766
  8. Transformation in Tetrahymena thermophila. Development of an inducible phenotype.
    Dev Biol. 1978 Sep;66(1):17-31 PMID: 109331
  9. A NIMA-related kinase, Cnk2p, regulates both flagellar length and cell size in Chlamydomonas.
    J Cell Sci. 2005 Aug 1;118(Pt 15):3317-26 PMID: 16030138
  10. Surface display of a parasite antigen in the ciliate Tetrahymena thermophila.
    Nat Biotechnol. 1999 May;17(5):462-5 PMID: 10331805
  11. Chlamydomonas fla mutants reveal a link between deflagellation and intraflagellar transport.
    BMC Cell Biol. 2003 Aug 20;4:11 PMID: 12930563
  12. Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans.
    J Cell Biol. 1999 Nov 1;147(3):519-30 PMID: 10545497
  13. Effects of various agents on flagellar activity, flagellar autotomy and cell viability in four species of Chlamydomonas (chlorophyta: volvocales).
    Symp Soc Exp Biol. 1982;35:421-37 PMID: 6764045
  14. Transformation in Tetrahymena pyriformis: description of an inducible phenotype.
    J Protozool. 1978 Feb;25(1):113-9 PMID: 96253
  15. A novel MAP kinase regulates flagellar length in Chlamydomonas.
    Curr Biol. 2003 Jul 1;13(13):1145-9 PMID: 12842015
  16. A NIMA-related kinase, Fa2p, localizes to a novel site in the proximal cilia of Chlamydomonas and mouse kidney cells.
    Mol Biol Cell. 2004 Nov;15(11):5172-86 PMID: 15371535
  17. The serine/threonine kinase Nek6 is required for cell cycle progression through mitosis.
    J Biol Chem. 2003 Dec 26;278(52):52454-60 PMID: 14563848
  18. The resorption of primary cilia during mitosis in a vertebrate (PtK1) cell line.
    J Ultrastruct Res. 1979 Aug;68(2):173-85 PMID: 480410
  19. 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
  20. Structural interaction of cytoskeletal components.
    J Cell Biol. 1981 Jul;90(1):222-35 PMID: 7019221
  21. The Nek2 protein kinase: a novel regulator of centrosome structure.
    Oncogene. 2002 Sep 9;21(40):6184-94 PMID: 12214248
  22. The dynamics of filamentous structures in the apical band, oral crescent, fission line and the postoral meridional filament in Tetrahymena thermophila revealed by monoclonal antibody 12G9.
    Protist. 2001 May;152(1):53-67 PMID: 11401037
  23. Cell context-specific effects of the beta-tubulin glycylation domain on assembly and size of microtubular organelles.
    Mol Biol Cell. 2004 Sep;15(9):4136-47 PMID: 15254268
  24. Intraflagellar transport.
    Nat Rev Mol Cell Biol. 2002 Nov;3(11):813-25 PMID: 12415299
  25. Polyglycylation domain of beta-tubulin maintains axonemal architecture and affects cytokinesis in Tetrahymena.
    Nat Cell Biol. 2002 Mar;4(3):256-9 PMID: 11862218
  26. Intraflagellar transport.
    Annu Rev Cell Dev Biol. 2003;19:423-43 PMID: 14570576
  27. A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3734-9 PMID: 11891286
  28. The FA2 gene of Chlamydomonas encodes a NIMA family kinase with roles in cell cycle progression and microtubule severing during deflagellation.
    J Cell Sci. 2002 Apr 15;115(Pt 8):1759-68 PMID: 11950892
  29. A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators.
    EMBO J. 1998 Jan 15;17(2):470-81 PMID: 9430639
  30. Flagellar protein dynamics in Chlamydomonas.
    J Biol Chem. 2001 Aug 10;276(32):29754-63 PMID: 11384985
  31. 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
  32. Hypoxia regulates assembly of cilia in suppressors of Tetrahymena lacking an intraflagellar transport subunit gene.
    Mol Biol Cell. 2003 Aug;14(8):3192-207 PMID: 12925756
  33. Development of the ciliature of Tetrahymena thermophila. I. Temporal coordination with oral development.
    Dev Biol. 1981 Nov;88(1):27-38 PMID: 7286446
  34. Mutations in a NIMA-related kinase gene, Nek1, cause pleiotropic effects including a progressive polycystic kidney disease in mice.
    Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):217-21 PMID: 10618398
  35. Genetic analysis of long-flagella mutants of Chlamydomonas reinhardtii.
    Genetics. 1988 Apr;118(4):637-48 PMID: 3366366
  36. Caught Nek-ing: cilia and centrioles.
    J Cell Sci. 2005 Nov 15;118(Pt 22):5161-9 PMID: 16280549
  37. Flagellar elongation and shortening in chlamydomonas. II. Re-utilization of flagellar proteins.
    J Cell Biol. 1970 Dec;47(3):777-81 PMID: 5497553
  38. Flagellar length control system: testing a simple model based on intraflagellar transport and turnover.
    Mol Biol Cell. 2005 Jan;16(1):270-8 PMID: 15496456
  39. The Kin I kinesins are microtubule end-stimulated ATPases.
    Mol Cell. 2003 Feb;11(2):286-8 PMID: 12620216
  40. Substrate specificity and cell cycle regulation of the Nek2 protein kinase, a potential human homolog of the mitotic regulator NIMA of Aspergillus nidulans.
    J Biol Chem. 1995 May 26;270(21):12899-905 PMID: 7759549
  41. The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends.
    Mol Cell. 2003 Feb;11(2):445-57 PMID: 12620232
  42. Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane.
    Curr Biol. 2005 Sep 20;15(18):1695-9 PMID: 16169494
  43. Cellular deflagellation.
    Int Rev Cytol. 2004;233:47-91 PMID: 15037362
  44. Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii.
    J Cell Sci. 1974 Dec;16(3):529-56 PMID: 4615103
  45. Spindle formation and chromatin condensation in cells blocked at interphase by mutation of a negative cell cycle control gene.
    Cell. 1988 Jan 29;52(2):241-51 PMID: 3277718
  46. The Microtubule plus end-tracking protein EB1 is localized to the flagellar tip and basal bodies in Chlamydomonas reinhardtii.
    Curr Biol. 2003 Nov 11;13(22):1969-74 PMID: 14614822
  47. Identification and sequence analysis of six new members of the NIMA-related kinase family in Chlamydomonas.
    J Eukaryot Microbiol. 2004 Jan-Feb;51(1):66-72 PMID: 15068267
  48. 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
  49. Nek2A kinase stimulates centrosome disjunction and is required for formation of bipolar mitotic spindles.
    Mol Biol Cell. 2003 Jul;14(7):2876-89 PMID: 12857871
  50. Molecular cloning and cell-cycle-dependent expression of a novel NIMA (never-in-mitosis in Aspergillus nidulans)-related protein kinase (TpNrk) in Tetrahymena cells.
    Biochem J. 1998 Aug 15;334 ( Pt 1):197-203 PMID: 9693120
  51. Inhibition of oral morphogenesis during conjugation of Tetrahymena thermophila and its resumption after cell separation.
    Eur J Protistol. 1993 Nov 12;29(4):359-69 PMID: 23195734
  52. A defect in a novel Nek-family kinase causes cystic kidney disease in the mouse and in zebrafish.
    Development. 2002 Dec;129(24):5839-46 PMID: 12421721
  53. 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
  54. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny.
    Comput Appl Biosci. 1996 Dec;12(6):543-8 PMID: 9021275
  55. 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
  56. Chlamydomonas shortens its flagella by activating axonemal disassembly, stimulating IFT particle trafficking, and blocking anterograde cargo loading.
    Dev Cell. 2005 Sep;9(3):431-8 PMID: 16139231
  57. Size control in dynamic organelles.
    Trends Cell Biol. 2002 Sep;12(9):414-9 PMID: 12220861
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2006-06-00
Epub
2006-00-12
Pages
2799-810
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1474788
Subset
IM
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