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PMID: 2143999 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo.

The Journal of cell biology ·Vol. 111 ·No. 3 ·1990-09-00 ·Pages 1027-37

Hirokawa N, Sato-Yoshitake R, Yoshida T, Kawashima T

Abstract

Brain dynein is a microtubule-activated ATPase considered to be a candidate to function as a molecular motor to transport membranous organelles retrogradely in the axon. To determine whether brain dynein really binds to retrogradely transported organelles in vivo and how it is transported to the nerve terminals, we studied the localization of brain dynein in axons after the ligation of peripheral nerves by light and electron microscopic immunocytochemistry using affinity-purified anti-brain dynein antibodies. Different classes of organelles preferentially accumulated at the regions proximal and distal to the ligated part. Interestingly, brain dynein accumulated both at the regions proximal and distal to the ligation sites and localized not only on retrogradely transported membranous organelles but also on anterogradely transported ones. This is the first evidence to show that brain dynein associates with retrogradely transported organelles in vivo and that brain dynein is transported to the nerve terminal by fast flow. This also suggests that there may be some mechanism that activates brain dynein only for retrograde transport.

MeSH Terms
Adenosine Triphosphatases/metabolism Animals Axons/metabolism,ultrastructure Biological Transport/physiology Brain/ultrastructure Cattle Dyneins/metabolism Female Ligation Mice Neurons/metabolism,ultrastructure Organelles/metabolism,ultrastructure Peripheral Nerves/physiology
Chemicals
Adenosine Triphosphatases Dyneins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hirokawa N
Department of Anatomy and Cell Biology, School of Medicine, University of Tokyo, Japan.
Sato-Yoshitake R
Yoshida T
Kawashima T
References (51)
51 references, click to expand
  1. Microtubule-associated protein 1B: molecular structure, localization, and phosphorylation-dependent expression in developing neurons.
    Neuron. 1989 Aug;3(2):229-38 PMID: 2562784
  2. Cytoskeletal architecture and immunocytochemical localization of microtubule-associated proteins in regions of axons associated with rapid axonal transport: the beta,beta'-iminodipropionitrile-intoxicated axon as a model system.
    J Cell Biol. 1985 Jul;101(1):227-39 PMID: 2409096
  3. Association of a cytoplasmic dynein-like protein recognizable by anti-MAP 1C with the mammalian mitotic spindle.
    Cell Biol Int Rep. 1990 Mar;14(3):189-98 PMID: 2140535
  4. Dissociated dorsal root ganglia in tissue culture.
    Am J Anat. 1956 Jul;99(1):81-129 PMID: 13362126
  5. Intracellular transport in neurons.
    Physiol Rev. 1980 Oct;60(4):1167-283 PMID: 6159657
  6. Immunochemistry on ultrathin frozen sections.
    Histochem J. 1980 Jul;12(4):381-403 PMID: 7440248
  7. The short term accumulation of axonally transported organelles in the region of localized lesions of single myelinated axons.
    J Neurocytol. 1980 Feb;9(1):39-65 PMID: 6162922
  8. Axonal transport: each major rate component reflects the movement of distinct macromolecular complexes.
    Science. 1981 Oct 9;214(4517):179-81 PMID: 6169148
  9. Polarity orientation of axonal microtubules.
    J Cell Biol. 1981 Dec;91(3 Pt 1):661-5 PMID: 6173385
  10. A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs).
    J Cell Biol. 1982 Feb;92(2):435-42 PMID: 6120944
  11. Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method.
    J Cell Biol. 1982 Jul;94(1):129-42 PMID: 6181077
  12. Fast axonal transport in squid giant axon.
    Science. 1982 Dec 10;218(4577):1127-9 PMID: 6183744
  13. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  14. Velocity and intensity of bidirectional migration of acetylcholinesterase in transected nerves.
    Brain Res. 1971 Apr 2;27(2):329-42 PMID: 4101562
  15. The association of a class of saltatory movements with microtubules in cultured cells.
    J Cell Biol. 1970 May;45(2):334-54 PMID: 5513607
  16. On the significance of cross-bridges between microtubules and synaptic vesicles.
    Philos Trans R Soc Lond B Biol Sci. 1971 Jun 17;261(839):395-405 PMID: 4399631
  17. Computer analysis of organelle translocation in primary neuronal cultures and continuous cell lines.
    J Cell Biol. 1975 Jun;65(3):562-76 PMID: 48515
  18. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  19. The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles.
    J Cell Biol. 1980 Mar;84(3):513-30 PMID: 6153657
  20. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility.
    Cell. 1985 Aug;42(1):39-50 PMID: 3926325
  21. A novel brain ATPase with properties expected for the fast axonal transport motor.
    Nature. 1985 Sep 5-11;317(6032):73-5 PMID: 2412134
  22. Association of anti-dynein-1 cross-reactive antigen with the mitotic spindle of mammalian cells.
    Cell Struct Funct. 1985 Sep;10(3):245-58 PMID: 2931187
  23. Cross-bridges mediate anterograde and retrograde vesicle transport along microtubules in squid axoplasm.
    J Cell Biol. 1985 Dec;101(6):2181-93 PMID: 2415536
  24. Specific cleavage of dynein heavy chains by ultraviolet irradiation in the presence of ATP and vanadate.
    J Biol Chem. 1986 Feb 15;261(5):2337-42 PMID: 2935534
  25. Reactivation of organelle movements along the cytoskeletal framework of a giant freshwater ameba.
    J Cell Biol. 1986 Aug;103(2):605-12 PMID: 3733883
  26. Identification of a MAP 2-like ATP-binding protein associated with axoplasmic vesicles that translocate on isolated microtubules.
    J Cell Biol. 1986 Sep;103(3):947-56 PMID: 3091608
  27. Stable complexes of axoplasmic vesicles and microtubules: protein composition and ATPase activity.
    J Cell Biol. 1986 Sep;103(3):957-68 PMID: 2943747
  28. Characterization of the microtubule movement produced by sea urchin egg kinesin.
    J Biol Chem. 1987 Feb 25;262(6):2794-802 PMID: 3102475
  29. The molecular structure of microtubule-associated protein 1A (MAP1A) in vivo and in vitro. An immunoelectron microscopy and quick-freeze, deep-etch study.
    J Neurosci. 1987 May;7(5):1461-9 PMID: 3553448
  30. Organelle dynamics in lobster axons: anterograde, retrograde and stationary mitochondria.
    Brain Res. 1987 May 26;412(1):96-106 PMID: 3607465
  31. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties.
    J Cell Biol. 1987 Sep;105(3):1273-82 PMID: 2958482
  32. Identification of a microtubule-based cytoplasmic motor in the nematode C. elegans.
    Cell. 1987 Oct 23;51(2):309-18 PMID: 2959372
  33. Retrograde transport by the microtubule-associated protein MAP 1C.
    Nature. 1987 Nov 12-18;330(6144):181-3 PMID: 3670402
  34. Drosophila kinesin: characterization of microtubule motility and ATPase.
    Proc Natl Acad Sci U S A. 1988 Feb;85(4):1109-13 PMID: 2963338
  35. An ATPase with properties expected for the organelle motor of the giant amoeba, Reticulomyxa.
    Nature. 1988 Mar 10;332(6160):176-8 PMID: 2964563
  36. Microtubule-associated protein 1C from brain is a two-headed cytosolic dynein.
    Nature. 1988 Apr 7;332(6164):561-3 PMID: 2965791
  37. MAP2 is a component of crossbridges between microtubules and neurofilaments in the neuronal cytoskeleton: quick-freeze, deep-etch immunoelectron microscopy and reconstitution studies.
    J Neurosci. 1988 Aug;8(8):2769-79 PMID: 3045269
  38. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1.
    J Cell Biol. 1989 Jan;108(1):111-26 PMID: 2536030
  39. 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
  40. Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration.
    Cell. 1989 Mar 10;56(5):867-78 PMID: 2522351
  41. Cytoplasmic dynein is a minus end-directed motor for membranous organelles.
    Cell. 1989 Mar 24;56(6):937-46 PMID: 2522353
  42. Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells.
    J Cell Biol. 1989 Apr;108(4):1453-63 PMID: 2522455
  43. A novel 58-kDa protein associates with the Golgi apparatus and microtubules.
    J Biol Chem. 1989 Sep 25;264(27):16083-92 PMID: 2777777
  44. A squid dynein isoform promotes axoplasmic vesicle translocation.
    J Cell Biol. 1989 Nov;109(5):2379-94 PMID: 2478567
  45. Fast axonal transport in permeabilized lobster giant axons is inhibited by vanadate.
    J Neurosci. 1983 Jun;3(6):1279-88 PMID: 6189982
  46. Mechanisms of intracellular organelle transport.
    Cell Muscle Motil. 1984;5:1-82,403-6 PMID: 6200203
  47. Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton.
    J Cell Biol. 1984 Apr;98(4):1523-36 PMID: 6425303
  48. Movement of organelles along filaments dissociated from the axoplasm of the squid giant axon.
    Cell. 1985 Feb;40(2):449-54 PMID: 2578324
  49. Single microtubules from squid axoplasm support bidirectional movement of organelles.
    Cell. 1985 Feb;40(2):455-62 PMID: 2578325
  50. Video microscopy of fast axonal transport in extruded axoplasm: a new model for study of molecular mechanisms.
    Cell Motil. 1985;5(2):81-101 PMID: 2580632
  51. Preparation of microtubules from rat liver and testis: cytoplasmic dynein is a major microtubule associated protein.
    Cell Motil Cytoskeleton. 1989;14(4):491-500 PMID: 2560414
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1990-09-00
Pages
1027-37
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2116262
Subset
IM
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