Distinct cytoplasmic dynein complexes are transported by different mechanisms in axons

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1496, Issue 1, 2000, Pages 76-88

  Susalka, S J ^a   Hancock, W O ^b   Pfister, K K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Axonal transport; Cytoplasmic dynein; Cytoskeleton; Microtubule; Motor protein

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

COMPLEX FORMATION; CYTOPLASM; CYTOSKELETON; MICROTUBULE; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW;

ANIMALS; AXONAL TRANSPORT; AXONS; CYTOPLASM; DYNEIN ATPASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICROTUBULES; MOLECULAR MOTOR PROTEINS; ORGAN SPECIFICITY; PROTEIN BINDING;

EID: 0034678043     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4889(00)00010-0     Document Type: Review

References (70)

1. Brady S.T. Molecular motors in the nervous system. Neuron. 7:1991;521-533.
2. Aniento F., Emans N., Griffiths G., Gruenberg J. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123:1993;1373-1387.
3. Bloom G.S., Goldstein L.S. Cruising along microtubule highways: how membranes move through the secretory pathway. J. Cell Biol. 140:1998;1277-1280.
4. Vallee R.B., Bloom G.S. Mechanisms of fast and slow axonal transport. Annu. Rev. Neurosci. 14:1991;59-92.
5. Hirokawa N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science. 279:1998;519-526.
6. Moore J.D., Endow S.A. Kinesin proteins: a phylum of motors for microtubule-based motility. Bioessays. 18:1996;207-219.
7. Bloom G.S., Wagner M.C., Pfister K.K., Brady S.T. Native structure and physical properties of bovine brain kinesin and identification of the ATP-binding subunit polypeptide. Biochemistry. 27:1988;3409-3416.
8. Holzbaur E.L., Vallee R.B. Dyneins: molecular structure and cellular function. Annu. Rev. Cell Biol. 10:1994;339-372.
9. Witman G.B. Axonemal dyneins. Curr. Opin. Cell Biol. 4:1992;74-79.
10. Gibbons B.H., Asai D.J., Tang W.J., Hays T.S., Gibbons I.R. Phylogeny and expression of axonemal and cytoplasmic dynein genes in sea urchins. Mol. Biol. Cell. 5:1994;57-70.
11. Porter M.E., Knott J.A., Myster S.H., Farlow S.J. The dynein gene family in Chlamydomonas reinhardtii. Genetics. 144:1996;569-585.
12. Porter M.E., Bower R., Knott J.A., Byrd P., Dentler W. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol. Biol. Cell. 10:1999;693-712.
13. Pazour G.J., Dickert B.L., Witman G.B. The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 144:1999;473-481.
14. Steuer E.R., Wordeman L., Schroer T.A., Sheetz M.P. Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature. 345:1990;266-268.
15. Pfarr C.M., Coue M., Grissom P.M., Hays T.S., Porter M.E., McIntosh J.R. Cytoplasmic dynein is localized to kinetochores during mitosis. Nature. 345:1997;263-265.
16. Sodeik B., Ebersold M.W., Helenius A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136:1997;1007-1021.
17. Harada A., Takei Y., Kanai Y., Tanaka Y., Nonaka S., Hirokawa N. Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J. Cell Biol. 141:1998;51-59.
18. Heald R., Tournebize R., Blank T., Sandaltzopoulos R., Becker P., Hyman A., Karsenti E. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature. 382:1996;420-425.
19. Gaglio T., Dionne M.A., Compton D.A. Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes. J. Cell Biol. 138:1997;1055-1066.
20. Dillman J.F., Dabney L.P., Pfister K.K. Cytoplasmic dynein is associated with slow axonal transport. Proc. Natl. Acad. Sci. USA. 93:1996;141-144.
21. Ahmad F.J., Echeverri C.J., Vallee R.B., Baas P.W. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J. Cell Biol. 140:1998;391-401.
22. Gee M.A., Heuser J.E., Vallee R.B. An extended microtubule-binding structure within the dynein motor domain. Nature. 390:1997;636-639.
23. glued. J. Cell Biol. 131:1995;1507-1516.
24. Steffen W., Karki S., Vaughan K.T., Vallee R.B., Holzbaur E.L.F., Weiss D.G., Kuznetsov S.A. The involvement of the intermediate chain of cytoplasmic dynein in binding the motor complex to membranous organelles of Xenopus oocytes. Mol. Biol. Cell. 8:1998;2077-2088.
25. Karki S., Holzbaur E.L.F. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:1995;28806-28811.
26. Hughes S.M., Vaughan K.T., Herskovits J.S., Vallee R.B. Molecular analysis of a cytoplasmic dynein light intermediate chain reveals homology to a family of ATPases. J. Cell Sci. 108:1995;17-24.
27. Gill S.R., Cleveland D.W., Schroer T.A. Characterization of DLC-A and DLC-B, two families of cytoplasmic dynein light chain subunits. Mol. Biol. Cell. 5:1994;645-654.
28. King S.M., Barbarese E., Dillman J.F., Patel-King R.S., Carson J.H., Pfister K.K. Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8000 light chain. J. Biol. Chem. 271:1996;19358-19366.
29. Benashski S.E., Harrison A., Patel-King R.S., King S.M. Dimerization of the highly conserved light chain shared by dynein and myosin V. J. Biol. Chem. 272:1997;20929-20935.
30. Samso M., Radermacher M., Frank J., Koonce M.P. Structural characterization of a dynein motor domain. J. Mol. Biol. 276:1998;927-937.
31. Jaffrey S.R., Snyder S.H. PIN: An associated protein inhibitor of neuronal nitric oxide synthase. Science. 274:1996;774-777.
32. Crepieux P., Kwon H., Leclerc N., Spencer W., Richard S., Lin R., Hiscott J. I kappaB alpha physically interacts with a cytoskeleton-associated protein through its signal response domain. Mol. Cell. Biol. 17:1997;7375-7385.
33. Jeffery C.J. Moonlighting proteins. Trends Biochem. Sci. 24:1999;8-11.
34. Bowman A.B., Patel-King R.S., Benashski S.E., McCaffery J.M., Goldstein L.S., King S.M. Drosophila roadblock and Chlamydomonas LC7. A conserved family of dynein-associated proteins involved in axonal transport, flagellar motility, and mitosis. J. Cell Biol. 146:1999;165-180.
35. King S.M., Barbarese E., Dillman J.F., Benashski S.E., Do K.T., Patel-King R.S., Pfister K.K. Cytoplasmic dynein contains a family of differentially expressed light chains. Biochemistry. 37:1998;15033-15041.
36. Dillman J.F., Dabney L.P., Karki S., Paschal B.M., Holzbaur E.L.F., Pfister K.K. Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J. Neurosci. 16:1996;6742-6752.
37. Paschal B.M., Mikami A., Pfister K.K., Vallee R.B. Homology of the 74-kD cytoplasmic dynein subunit with a flagellar dynein polypeptide suggests an intracellular targeting function. J. Cell Biol. 118:1992;1133-1143.
38. Wilkerson C.G., King S.M., Koutoulis A., Pazour G.J., Witman G.B. The 78,000 M(r) intermediate chain of Chlamydomonas outer arm dynein is a WD-repeat protein required for arm assembly. J. Cell Biol. 129:1995;169-178.
39. Nurminsky D.I., Nurminskaya M.V., Benevolenskaya E.V., Shevelyov Y.Y., Hartl D.L., Gvozdev V.A. Cytoplasmic dynein intermediate-chain isoforms with different targeting properties created by tissue-specific alternative splicing. Mol. Cell. Biol. 18:1998;6816-6825.
40. Pfister K.K., Salata M.W., Dillman J.F., Vaughan K.T., Vallee R.B., Torre E., Lye R.J. Differential expression and phosphorylation of IC74 subunits of cytoplasmic dynein in cultured neurons and glia. J. Biol. Chem. 271:1996;1687-1694.
41. Dillman J.F., Pfister K.K. Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles. J. Cell Biol. 127:1994;1671-1681.
42. Pfister K.K., Salata M.W., Dillman J.F., Torre E., Lye R.J. Identification and developmental regulation of a neuron specific subunit of cytoplasmic dynein. Mol. Cell. Biol. 7:1996;331-343.
43. Neer E.J., Schmidt C.J., Nambudripad R., Smith T.F. The ancient regulatory-protein family of WD-repeat proteins. Nature. 371:1994;297-300.
44. Smith T.F., Gaitatzes C., Saxena K., Neer E.J. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24:1999;181-185.
45. R. Hammerschlag S.T. Brady, in: G.J. Siegel, B.W. Agranoff, R.W. Albers, P.B. Molinoff (Eds.), Basic Neurochemistry, Raven Press, New York, 1989, pp. 457-478.
46. Hirokawa N., Sato-Yoshitake R., Yoshida T., Kawashima T. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J. Cell Biol. 111:1990;1027-1037.
47. Mercer J.A., Albanesi J.P., Brady S.T. Molecular motors and cell motility in the brain. Brain Pathol. 4:1994;167-179.
48. Lasek R.J. Polymer sliding in axons. J. Cell Sci. Suppl. 5:1986;161-179.
49. Presley J.F., Cole N.B., Schroer T.A., Hirschberg K., Zaal K.J., Lippincott-Schwartz J. ER-Golgi transport visualized in living cells. Nature. 389:1997;81-85.
50. Echeverri C.J., Paschal B.M., Vaughan K.T., Vallee R.B. 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. 132:1996;617-633.
51. Burkhardt J.K., Echeverri C.J., Nilsson T., Vallee R.B. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139:1997;469-484.
52. Allan V. Organelle movement. Dynactin: portrait of a dynein regulator. Curr. Biol. 4:1994;1000-1002.
53. Holleran E.A., Karki S., Holzbaur E.L. The role of the dynactin complex in intracellular motility. Int. Rev. Cytol. 182:1998;69-109.
54. Mullins R.D., Kelleher J.F., Pollard T.D. Actin' like actin. Trends Cell Biol. 6:1996;208-212.
55. Holleran E.A., Tokito M.K., Karki S., Holzbaur E.L. Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol. 135:1996;1815-1829.
56. Cheney R., Hirokawa N., Levine J., Willard M. Intracellular movement of fodrin. Cell Motil. 3:1983;649-655.
57. Hirokawa N., Sato-Yoshitake R., Kobayashi N., Pfister K.K., Bloom G.S., Brady S.T. Kinesin associates with anterogradely transported membranous organelles in vivo. J. Cell Biol. 114:1991;295-302.
58. Ferreira A., Niclas J., Vale R.D., Banker G., Kosik K.S. Suppression of kinesin expression in cultured hippocampal neurons using antisense oligonucleotides. J. Cell Biol. 117:1992;595-606.
59. Elluru R.G., Bloom G.S., Brady S.T. Fast axonal transport of kinesin in the rat visual system: functionality of kinesin heavy chain isoforms. Mol. Biol. Cell. 6:1995;21-40.
60. Nilsson H., Rutberg M., Wallin M. Localization of kinesin and cytoplasmic dynein in cultured melanophores from Atlantic cod, Gadus morhua. Cell Motil. Cytoskeleton. 33:1996;183-196.
61. Rogers S.L., Tint I.S., Fanapour P.C., Gelfand I.M. Regulated bidirectional motility of melanophore pigment granules along microtubules in vitro. Proc. Natl. Acad. Sci. USA. 94:1997;3720-3725.
62. Blocker A., Severin F.F., Burkhardt J.K., Bingham J.B., Yu H., Olivo J.C., Schroer T.A., Hyman A.A., Griffiths G. Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137:1997;113-129.
63. Lin S.X., Pfister K.K., Collins C.A. Comparison of the intracellular distribution of cytoplasmic dynein and kinesin in cultured cells: motor protein location does not reliably predict function. Cell Motil. Cytoskeleton. 34:1996;299-312.
64. Lippincott-Schwartz J., Cole N.B., Marotta A., Conrad P.A., Bloom G.S. Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell Biol. 128:1995;293-306.
65. Wubbolts R., Fernandez-Borja M., Jordens I., Reits E., Dusseljee S., Echeverri C., Vallee R.B., Neefjes J. Opposing motor activities of dynein and kinesin determine retention and transport of MHC class II-containing compartments. J. Cell Sci. 112:1999;785-795.
66. Keating T.J., Peloquin J.G., Rodionov V.I., Momcilovic D., Borisy G.G. Microtubule release from the centrosome. Proc. Natl. Acad. Sci. USA. 94:1997;5078-5083.
67. Gibbons I.R. Dynein ATPases as microtubule motors. J. Biol. Chem. 263:1988;15837-15840.
68. Gibbons I.R. Cilia and flagella of eukaryotes. J. Cell Biol. 91:1981;107s-124s.
69. Xiang X., Roghi C., Morris N.R. Characterization and localization of the cytoplasmic dynein heavy chain in Aspergillus nidulans. Proc. Natl. Acad. Sci. USA. 92:1995;9890-9894.
70. Leopold P.L., Kreitzer G., Miyazawa N., Rempel S., Pfister K.K., Rodriguez-Boulan E., Crystal R.G. Dynein- and microtubule-mediated translocation of adenovirus serotype 5 occurs after endosomal lysis. Hum. Gene Ther. 11:2000;151-165.