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PMID: 15371535 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A NIMA-related kinase, Fa2p, localizes to a novel site in the proximal cilia of Chlamydomonas and mouse kidney cells.

Molecular biology of the cell ·Vol. 15 ·No. 11 ·2004-11-00 ·Pages 5172-86

Mahjoub MR, Qasim Rasi M, Quarmby LM

Abstract

Polycystic kidney disease and related syndromes involve dysregulation of cell proliferation in conjunction with ciliary defects. The relationship between cilia and cell cycle is enigmatic, but it may involve regulation by the NIMA-family of kinases (Neks). We previously showed that the Nek Fa2p is important for ciliary function and cell cycle in Chlamydomonas. We now show that Fa2p localizes to an important regulatory site at the proximal end of cilia in both Chlamydomonas and a mouse kidney cell line. Fa2p also is associated with the proximal end of centrioles. Its localization is dynamic during the cell cycle, following a similar pattern in both cell types. The cell cycle function of Fa2p is kinase independent, whereas its ciliary function is kinase dependent. Mice with mutations in Nek1 or Nek8 have cystic kidneys; therefore, our discovery that a member of this phylogenetic group of Nek proteins is localized to the same sites in Chlamydomonas and kidney epithelial cells suggests that Neks play conserved roles in the coordination of cilia and cell cycle progression.

MeSH Terms
Animals Cell Cycle Cell Cycle Proteins/chemistry,physiology Cell Line Centrioles/metabolism,ultrastructure Chlamydomonas/metabolism Cilia/metabolism DNA, Complementary/metabolism Epitopes/chemistry Fluorescent Antibody Technique, Indirect Green Fluorescent Proteins/metabolism Immunoblotting Kidney/metabolism,pathology Mice Mitosis Mutation NIMA-Related Kinase 1 NIMA-Related Kinases Protein Kinases/metabolism Protein Serine-Threonine Kinases/biosynthesis,chemistry,metabolism,physiology Protein Structure, Tertiary Protein-Tyrosine Kinases/metabolism Signal Transduction Subcellular Fractions/metabolism Time Factors
Chemicals
Cell Cycle Proteins DNA, Complementary Epitopes Green Fluorescent Proteins Protein Kinases Protein-Tyrosine Kinases NIMA-Related Kinase 1 NIMA-Related Kinases Nek1 protein, mouse Nek8 protein, mouse Protein Serine-Threonine Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Mahjoub Moe R
Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada.
Qasim Rasi M
Quarmby Lynne M
References (54)
54 references, click to expand
  1. Control of cell division by a retinoblastoma protein homolog in Chlamydomonas.
    Genes Dev. 2001 Jul 1;15(13):1652-61 PMID: 11445540
  2. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney.
    Development. 2004 Aug;131(16):4085-93 PMID: 15269167
  3. 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
  4. Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells.
    Mol Biol Cell. 2002 Jun;13(6):1832-45 PMID: 12058052
  5. Nek11, a new member of the NIMA family of kinases, involved in DNA replication and genotoxic stress responses.
    J Biol Chem. 2002 Oct 18;277(42):39655-65 PMID: 12154088
  6. Fine structure of cell division in Chlamydomonas reinhardi. Basal bodies and microtubules.
    J Cell Biol. 1968 Aug;38(2):403-25 PMID: 5664210
  7. 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
  8. Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells.
    Cell. 1979 Jul;17(3):527-35 PMID: 476831
  9. Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes.
    J Cell Biol. 1980 Mar;84(3):599-617 PMID: 7358792
  10. Isolation of Chlamydomonas flagella and flagellar axonemes.
    Methods Enzymol. 1986;134:280-90 PMID: 3821567
  11. The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells.
    J Cell Biol. 1988 Aug;107(2):635-41 PMID: 3047144
  12. Centrin-mediated microtubule severing during flagellar excision in Chlamydomonas reinhardtii.
    J Cell Biol. 1989 May;108(5):1751-60 PMID: 2654141
  13. Isolation and characterization of Chlamydomonas temperature-sensitive mutants affecting gametic differentiation under nitrogen-starved conditions.
    Curr Genet. 1991 Feb;19(2):65-71 PMID: 2065364
  14. Cloning and genetic analysis of the gene encoding a new protein kinase in Saccharomyces cerevisiae.
    Yeast. 1993 Feb;9(2):141-50 PMID: 8465601
  15. Mitotic gold in a mold: Aspergillus genetics and the biology of mitosis.
    Trends Genet. 1992 Jan;8(1):32-7 PMID: 1369734
  16. Isolation of a functional homolog of the cell cycle-specific NIMA protein kinase of Aspergillus nidulans and functional analysis of conserved residues.
    J Biol Chem. 1995 Jul 28;270(30):18110-6 PMID: 7629122
  17. Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies.
    Genetics. 1995 Nov;141(3):945-60 PMID: 8582639
  18. Expression of primary cilia in mammalian cells.
    Cell Biol Int. 1996 Jan;20(1):73-81 PMID: 8936410
  19. 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
  20. A NIMA homologue promotes chromatin condensation in fission yeast.
    J Cell Sci. 1998 Apr;111 ( Pt 7):967-76 PMID: 9490640
  21. A role for katanin-mediated axonemal severing during Chlamydomonas deflagellation.
    Mol Biol Cell. 1998 May;9(5):1195-207 PMID: 9571249
  22. Genetics of the deflagellation pathway in Chlamydomonas.
    Genetics. 1998 Jun;149(2):927-36 PMID: 9611203
  23. Pharmacological and genetic evidence for a role of rootlet and phycoplast microtubules in the positioning and assembly of cleavage furrows in Chlamydomonas reinhardtii.
    Cell Motil Cytoskeleton. 1998;40(2):193-207 PMID: 9634216
  24. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas.
    Mol Biol Cell. 1999 Mar;10(3):693-712 PMID: 10069812
  25. The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly.
    J Cell Biol. 1999 Feb 8;144(3):473-81 PMID: 9971742
  26. 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
  27. Fa1p is a 171 kDa protein essential for axonemal microtubule severing in Chlamydomonas.
    J Cell Sci. 2000 Jun;113 ( Pt 11):1963-71 PMID: 10806107
  28. Intraflagellar transport.
    Nat Rev Mol Cell Biol. 2002 Nov;3(11):813-25 PMID: 12415299
  29. 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
  30. Epsilon-tubulin is an essential component of the centriole.
    Mol Biol Cell. 2002 Nov;13(11):3859-69 PMID: 12429830
  31. The vertebrate primary cilium is a sensory organelle.
    Curr Opin Cell Biol. 2003 Feb;15(1):105-10 PMID: 12517711
  32. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells.
    Nat Genet. 2003 Feb;33(2):129-37 PMID: 12514735
  33. Bending the primary cilium opens Ca2+-sensitive intermediate-conductance K+ channels in MDCK cells.
    J Membr Biol. 2003 Feb 1;191(3):193-200 PMID: 12571753
  34. Polycystic kidney disease--the ciliary connection.
    Lancet. 2003 Mar 1;361(9359):774-6 PMID: 12620752
  35. Never say never. The NIMA-related protein kinases in mitotic control.
    Trends Cell Biol. 2003 May;13(5):221-8 PMID: 12742165
  36. A novel MAP kinase regulates flagellar length in Chlamydomonas.
    Curr Biol. 2003 Jul 1;13(13):1145-9 PMID: 12842015
  37. 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
  38. Two populations of node monocilia initiate left-right asymmetry in the mouse.
    Cell. 2003 Jul 11;114(1):61-73 PMID: 12859898
  39. Systematic trans-genomic comparison of protein kinases between Arabidopsis and Saccharomyces cerevisiae.
    Plant Physiol. 2003 Aug;132(4):2152-65 PMID: 12913170
  40. Hedgehog signalling in the mouse requires intraflagellar transport proteins.
    Nature. 2003 Nov 6;426(6962):83-7 PMID: 14603322
  41. 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
  42. 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
  43. Identification of proteins that interact with the central coiled-coil region of the human protein kinase NEK1.
    Biochemistry. 2003 Dec 30;42(51):15369-76 PMID: 14690447
  44. Polycystic kidney disease.
    N Engl J Med. 2004 Jan 8;350(2):151-64 PMID: 14711914
  45. Nek2B stimulates zygotic centrosome assembly in Xenopus laevis in a kinase-independent manner.
    Dev Biol. 2004 Jan 15;265(2):384-98 PMID: 14732400
  46. Primary cilia of human endothelial cells disassemble under laminar shear stress.
    J Cell Biol. 2004 Mar 15;164(6):811-7 PMID: 15024030
  47. An aurora kinase is essential for flagellar disassembly in Chlamydomonas.
    Dev Cell. 2004 Mar;6(3):445-51 PMID: 15030766
  48. Cellular deflagellation.
    Int Rev Cytol. 2004;233:47-91 PMID: 15037362
  49. 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
  50. Establishing a connection between cilia and Bardet-Biedl Syndrome.
    Trends Mol Med. 2004 Mar;10(3):106-9 PMID: 15106604
  51. Chlamydomonas fla mutants reveal a link between deflagellation and intraflagellar transport.
    BMC Cell Biol. 2003 Aug 20;4:11 PMID: 12930563
  52. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene.
    Cell. 2004 May 14;117(4):541-52 PMID: 15137946
  53. Annexin 11 is required for midbody formation and completion of the terminal phase of cytokinesis.
    J Cell Biol. 2004 Jun 21;165(6):813-22 PMID: 15197175
  54. Assembly and motility of eukaryotic cilia and flagella. Lessons from Chlamydomonas reinhardtii.
    Plant Physiol. 2001 Dec;127(4):1500-7 PMID: 11743094
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2004-11-00
Epub
2004-00-15
Pages
5172-86
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC524795
Subset
IM
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