Home LiteratureArticle Details
PMID: 11581287 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes.

The Journal of cell biology ·Vol. 155 ·No. 1 ·2001-10-01 ·Pages 77-88

Noda Y, Okada Y, Saito N, Setou M, Xu Y, Zhang Z, Hirokawa N

Abstract

We have identified and characterized a COOH-terminal motor domain-type kinesin superfamily protein (KIFC), KIFC3, in the kidney. KIFC3 is a minus end-directed microtubule motor protein, therefore it accumulates in regions where minus ends of microtubules assemble. In polarized epithelial cells, KIFC3 is localized on membrane organelles immediately beneath the apical plasma membrane of renal tubular epithelial cells in vivo and polarized MDCK II cells in vitro. Flotation assay, coupled with detergent extraction, demonstrated that KIFC3 is associated with Triton X-100-insoluble membrane organelles, and that it overlaps with apically transported TGN-derived vesicles. This was confirmed by immunoprecipitation and by GST pulldown experiments showing the specific colocalization of KIFC3 and annexin XIIIb, a previously characterized membrane protein for apically transported vesicles (Lafont, F., S. Lecat, P. Verkade, and K. Simons. 1998. J. Cell Biol. 142:1413-1427). Furthermore, we proved that the apical transport of both influenza hemagglutinin and annexin XIIIb was partially inhibited or accelerated by overexpression of motor-domainless (dominant negative) or full-length KIFC3, respectively. Absence of cytoplasmic dynein on these annexin XIIIb-associated vesicles and distinct distribution of the two motors on the EM level verified the existence of KIFC3-driven transport in epithelial cells.

MeSH Terms
Amino Acid Sequence Animals Annexins/metabolism Cell Line Cell Membrane/chemistry,metabolism Cell Polarity Cholesterol/metabolism Cloning, Molecular Consensus Sequence Detergents/chemistry Dogs Epithelial Cells/drug effects,metabolism Immunohistochemistry Kidney Tubules/metabolism,ultrastructure Kinesins/chemistry,genetics,metabolism Microtubules/metabolism Molecular Motor Proteins/chemistry,genetics,metabolism Molecular Sequence Data Nocodazole/pharmacology Octoxynol/chemistry Protein Isoforms/metabolism Protein Structure, Tertiary Protein Transport Recombinant Fusion Proteins/metabolism Sequence Alignment Temperature
Chemicals
Annexins Detergents Kifc3 protein, mouse Molecular Motor Proteins Protein Isoforms Recombinant Fusion Proteins Octoxynol Cholesterol Kinesins Nocodazole
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Noda Y
Department of Cell Biology and Anatomy, Graduate School of Medicine, University of Tokyo, Hongo, Tokyo 113-0033, Japan.
Okada Y
Saito N
Setou M
Xu Y
Zhang Z
Hirokawa N
References (52)
52 references, click to expand
  1. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2817-32 PMID: 2592406
  2. KIF5C, a novel neuronal kinesin enriched in motor neurons.
    J Neurosci. 2000 Sep 1;20(17):6374-84 PMID: 10964943
  3. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant.
    Cell. 1991 Sep 6;66(5):907-20 PMID: 1909606
  4. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface.
    Cell. 1992 Feb 7;68(3):533-44 PMID: 1531449
  5. Regulation of the direction of chromosome movement.
    Cold Spring Harb Symp Quant Biol. 1991;56:745-50 PMID: 1819521
  6. Selective inhibition of protein targeting to the apical domain of MDCK cells by brefeldin A.
    J Cell Biol. 1992 Jul;118(1):51-62 PMID: 1352300
  7. Kinesin family in murine central nervous system.
    J Cell Biol. 1992 Dec;119(5):1287-96 PMID: 1447303
  8. Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking.
    Science. 1994 Feb 25;263(5150):1146-9 PMID: 8108733
  9. Polarized sorting of the polymeric immunoglobulin receptor in the exocytotic and endocytotic pathways is controlled by the same amino acids.
    EMBO J. 1994 May 15;13(10):2297-304 PMID: 8194521
  10. Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid-enriched membrane fraction.
    Mol Cell Biol. 1994 Aug;14(8):5384-91 PMID: 8035816
  11. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics.
    Curr Biol. 1994 Mar 1;4(3):220-33 PMID: 7922327
  12. Neurotransmission: harnessing fusion machinery at the synapse.
    Trends Neurosci. 1994 Aug;17(8):344-8 PMID: 7526506
  13. Mechanisms of cell polarity: sorting and transport in epithelial cells.
    Curr Opin Cell Biol. 1994 Aug;6(4):545-54 PMID: 7986532
  14. Involvement of microtubule motors in basolateral and apical transport in kidney cells.
    Nature. 1994 Dec 22-29;372(6508):801-3 PMID: 7997271
  15. KIF2 is a new microtubule-based anterograde motor that transports membranous organelles distinct from those carried by kinesin heavy chain or KIF3A/B.
    J Cell Biol. 1995 Apr;129(1):157-67 PMID: 7535303
  16. Cellular cholesterol efflux mediated by cyclodextrins.
    J Biol Chem. 1995 Jul 21;270(29):17250-6 PMID: 7615524
  17. KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport.
    J Cell Biol. 1995 Sep;130(6):1387-99 PMID: 7559760
  18. Direct observation of single kinesin molecules moving along microtubules.
    Nature. 1996 Apr 4;380(6573):451-3 PMID: 8602245
  19. Origins of cell polarity.
    Cell. 1996 Feb 9;84(3):335-44 PMID: 8608587
  20. Active transport of photoactivated tubulin molecules in growing axons revealed by a new electron microscopic analysis.
    J Cell Biol. 1996 Jun;133(6):1347-53 PMID: 8682869
  21. Visualization of slow axonal transport in vivo.
    Science. 1996 Aug 9;273(5276):784-8 PMID: 8670416
  22. Endocytosis and molecular sorting.
    Annu Rev Cell Dev Biol. 1996;12:575-625 PMID: 8970738
  23. Molecular cloning and functional analysis of mouse C-terminal kinesin motor KifC3.
    Mol Cell Biol. 2001 Feb;21(3):765-70 PMID: 11154264
  24. Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation.
    Cell. 1983 Aug;34(1):233-43 PMID: 6883510
  25. Microtubules and actin filaments are not critically involved in the biogenesis of epithelial cell surface polarity.
    J Cell Biol. 1986 May;102(5):1853-67 PMID: 2871031
  26. The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2377-87 PMID: 3198692
  27. Release of putative exocytic transport vesicles from perforated MDCK cells.
    EMBO J. 1988 Dec 20;7(13):4075-85 PMID: 3243273
  28. KIFC2 is a novel neuron-specific C-terminal type kinesin superfamily motor for dendritic transport of multivesicular body-like organelles.
    Neuron. 1997 Mar;18(3):425-38 PMID: 9115736
  29. Increased fluid secretion after adenoviral-mediated transfer of the aquaporin-1 cDNA to irradiated rat salivary glands.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3268-73 PMID: 9096382
  30. Kinesin hydrolyses one ATP per 8-nm step.
    Nature. 1997 Jul 24;388(6640):386-90 PMID: 9237757
  31. Multiple kinesin family members expressed in teleost retina and RPE include a novel C-terminal kinesin.
    Exp Eye Res. 1997 May;64(5):781-94 PMID: 9245909
  32. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains.
    Curr Opin Cell Biol. 1997 Aug;9(4):534-42 PMID: 9261060
  33. Identification and classification of 16 new kinesin superfamily (KIF) proteins in mouse genome.
    Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9654-9 PMID: 9275178
  34. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  35. Molecular motors and a spectrin matrix associate with Golgi membranes in vitro.
    J Cell Biol. 1997 Dec 1;139(5):1169-81 PMID: 9382864
  36. Kinesin and dynein superfamily proteins and the mechanism of organelle transport.
    Science. 1998 Jan 23;279(5350):519-26 PMID: 9438838
  37. Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons.
    J Cell Biol. 1998 Feb 9;140(3):659-74 PMID: 9456325
  38. Kinesin and dynein superfamily proteins in organelle transport and cell division.
    Curr Opin Cell Biol. 1998 Feb;10(1):60-73 PMID: 9484596
  39. Apiconuclear organization of microtubules does not specify protein delivery from the trans-Golgi network to different membrane domains in polarized epithelial cells.
    Mol Biol Cell. 1998 Mar;9(3):685-99 PMID: 9487135
  40. Cholesterol is required for surface transport of influenza virus hemagglutinin.
    J Cell Biol. 1998 Mar 23;140(6):1357-67 PMID: 9508769
  41. Determinants of kinesin motor polarity.
    Science. 1998 Aug 21;281(5380):1200-2 PMID: 9712586
  42. Annexin XIIIb associates with lipid microdomains to function in apical delivery.
    J Cell Biol. 1998 Sep 21;142(6):1413-27 PMID: 9744874
  43. Cloning of a novel C-terminal kinesin (KIFC3) that maps to human chromosome 16q13-q21 and thus is a candidate gene for Bardet-Biedl syndrome.
    Genomics. 1998 Sep 1;52(2):219-22 PMID: 9782090
  44. Direction determination in the minus-end-directed kinesin motor ncd.
    Nature. 1998 Oct 22;395(6704):813-6 PMID: 9796817
  45. Kinetic analysis of secretory protein traffic and characterization of golgi to plasma membrane transport intermediates in living cells.
    J Cell Biol. 1998 Dec 14;143(6):1485-503 PMID: 9852146
  46. New perspectives on mechanisms involved in generating epithelial cell polarity.
    Physiol Rev. 1999 Jan;79(1):73-98 PMID: 9922368
  47. A processive single-headed motor: kinesin superfamily protein KIF1A.
    Science. 1999 Feb 19;283(5405):1152-7 PMID: 10024239
  48. Cytoplasmic dynein and dynactin as likely candidates for microtubule-dependent apical targeting of pancreatic zymogen granules.
    Eur J Cell Biol. 1999 Apr;78(4):265-77 PMID: 10350215
  49. Mechanism of the single-headed processivity: diffusional anchoring between the K-loop of kinesin and the C terminus of tubulin.
    Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):640-5 PMID: 10639132
  50. Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein.
    Nat Cell Biol. 2000 Feb;2(2):125-7 PMID: 10655593
  51. Dissecting the role of the golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8375-80 PMID: 10890900
  52. Effect of nocodazole on vesicular traffic to the apical and basolateral surfaces of polarized MDCK cells.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2365-73 PMID: 2277063
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2001-10-01
Pages
77-88
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2150803
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