Home LiteratureArticle Details
PMID: 9342383 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport.

Waterman-Storer CM, Karki SB, Kuznetsov SA, Tabb JS, Weiss DG, Langford GM, Holzbaur EL

Abstract

Fast axonal transport is characterized by the bidirectional, microtubule-based movement of membranous organelles. Cytoplasmic dynein is necessary but not sufficient for retrograde transport directed from the synapse to the cell body. Dynactin is a heteromultimeric protein complex, enriched in neurons, that binds to both microtubules and cytoplasmic dynein. To determine whether dynactin is required for retrograde axonal transport, we examined the effects of anti-dynactin antibodies on organelle transport in extruded axoplasm. Treatment of axoplasm with antibodies to the p150(Glued) subunit of dynactin resulted in a significant decrease in the velocity of microtubule-based organelle transport, with many organelles bound along microtubules. We examined the molecular mechanism of the observed inhibition of motility, and we demonstrated that antibodies to p150(Glued) disrupted the binding of cytoplasmic dynein to dynactin and also inhibited the association of cytoplasmic dynein with organelles. In contrast, the anti-p150(Glued) antibodies had no effect on the binding of dynactin to microtubules nor on cytoplasmic dynein-driven microtubule gliding. These results indicate that the interaction between cytoplasmic dynein and the dynactin complex is required for the axonal transport of membrane-bound vesicles and support the hypothesis that dynactin may function as a link between the organelle, the microtubule, and cytoplasmic dynein during vesicle transport.

MeSH Terms
Animals Antibodies/pharmacology Axonal Transport/physiology Axons/metabolism Biological Transport/drug effects Cell-Free System Cytoplasm/metabolism Decapodiformes Dynactin Complex Dyneins/metabolism Microtubule-Associated Proteins/immunology,metabolism Microtubules/drug effects,ultrastructure Organelles/physiology Protein Binding
Chemicals
Antibodies Dynactin Complex Microtubule-Associated Proteins Dyneins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Waterman-Storer C M
Department of Animal Biology, University of Pennsylvania, Philadelphia, PA 19104, USA. waterman@email.unc.edu
Karki S B
Kuznetsov S A
Tabb J S
Weiss D G
Langford G M
Holzbaur E L
References (32)
32 references, click to expand
  1. Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles.
    J Cell Biol. 1996 Dec;135(6 Pt 2):1815-29 PMID: 8991093
  2. Opposing motor activities are required for the organization of the mammalian mitotic spindle pole.
    J Cell Biol. 1996 Oct;135(2):399-414 PMID: 8896597
  3. Movement of organelles along filaments dissociated from the axoplasm of the squid giant axon.
    Cell. 1985 Feb;40(2):449-54 PMID: 2578324
  4. Bidirectional transport of fluorescently labeled vesicles introduced into extruded axoplasm of squid Loligo pealei.
    J Cell Biol. 1984 Aug;99(2):445-52 PMID: 6204992
  5. Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: evidence for an active role of microtubules in cytoplasmic transport.
    J Cell Biol. 1985 May;100(5):1736-52 PMID: 2580845
  6. Translocation of vesicles from squid axoplasm on flagellar microtubules.
    Nature. 1985 May 16-22;315(6016):245-8 PMID: 2582264
  7. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility.
    Cell. 1985 Aug;42(1):39-50 PMID: 3926325
  8. Towards a new classification of intracellular particle movements based on quantitative analyses.
    Cell Motil Cytoskeleton. 1986;6(2):128-35 PMID: 2423255
  9. Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies.
    J Cell Biol. 1988 Oct;107(4):1437-48 PMID: 3170635
  10. Dynein is the motor for retrograde axonal transport of organelles.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1548-52 PMID: 2466291
  11. Cytoplasmic dynein is a minus end-directed motor for membranous organelles.
    Cell. 1989 Mar 24;56(6):937-46 PMID: 2522353
  12. A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm.
    Proc Natl Acad Sci U S A. 1990 Feb;87(3):1061-5 PMID: 1689058
  13. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo.
    J Cell Biol. 1990 Sep;111(3):1027-37 PMID: 2143999
  14. Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued.
    Nature. 1991 Jun 13;351(6327):579-83 PMID: 1828535
  15. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein.
    J Cell Biol. 1991 Dec;115(6):1639-50 PMID: 1836789
  16. Actin-dependent organelle movement in squid axoplasm.
    Nature. 1992 Apr 23;356(6371):722-5 PMID: 1570018
  17. Analysis of the gliding, fishtailing and circling motions of native microtubules.
    Acta Histochem Suppl. 1991;41:81-105 PMID: 1725829
  18. A vertebrate actin-related protein is a component of a multisubunit complex involved in microtubule-based vesicle motility.
    Nature. 1992 Sep 17;359(6392):244-6 PMID: 1528266
  19. Characterization of a 50-kDa polypeptide in cytoplasmic dynein preparations reveals a complex with p150GLUED and a novel actin.
    J Biol Chem. 1993 Jul 15;268(20):15318-23 PMID: 8325901
  20. Mechanism of axonal transport. Identification of new molecular motors and regulations of transports.
    Neurosci Res. 1993 Oct;18(1):1-9 PMID: 7510857
  21. Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin.
    J Cell Biol. 1994 Jul;126(2):403-12 PMID: 7518465
  22. Cytoplasmic dynein binds to phospholipid vesicles.
    Cell Motil Cytoskeleton. 1994;28(3):205-12 PMID: 7954849
  23. The p150Glued component of the dynactin complex binds to both microtubules and the actin-related protein centractin (Arp-1).
    Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1634-8 PMID: 7878030
  24. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex.
    J Biol Chem. 1995 Dec 1;270(48):28806-11 PMID: 7499404
  25. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued.
    J Cell Biol. 1995 Dec;131(6 Pt 1):1507-16 PMID: 8522607
  26. The product of the Drosophila gene, Glued, is the functional homologue of the p150Glued component of the vertebrate dynactin complex.
    J Biol Chem. 1996 Jan 12;271(2):1153-9 PMID: 8557644
  27. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis.
    J Cell Biol. 1996 Feb;132(4):617-33 PMID: 8647893
  28. Targeting of motor proteins.
    Science. 1996 Mar 15;271(5255):1539-44 PMID: 8599110
  29. Cell cycle regulation of dynein association with membranes modulates microtubule-based organelle transport.
    J Cell Biol. 1996 May;133(3):585-93 PMID: 8636233
  30. Mutational analysis of motor proteins.
    Annu Rev Physiol. 1996;58:751-92 PMID: 8815819
  31. Functionally distinct isoforms of dynactin are expressed in human neurons.
    Mol Biol Cell. 1996 Aug;7(8):1167-80 PMID: 8856662
  32. Single microtubules from squid axoplasm support bidirectional movement of organelles.
    Cell. 1985 Feb;40(2):455-62 PMID: 2578325
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-10-28
Pages
12180-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC23743
Subset
IM
Grants
NIGMS NIH HHS · R01 GM048661 · United States
NIGMS NIH HHS · GM48661 · 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