Cytoplasmic dynein and microtubule transport in the axon: The action connection

Molecular Neurobiology

Volumn 20, Issue 2-3, 1999, Pages 81-91

  Pfister, K Kevin ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Actin; Axonal transport; Dynactin; Dynein; Microtubule; Motor protein

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; FODRIN; MESSENGER RNA; SPECTRIN;

ARTICLE; CYTOPLASM; IMMUNOCYTOCHEMISTRY; MICROTUBULE; NERVE FIBER; NERVE FIBER TRANSPORT; NONHUMAN;

EID: 0033343738     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02742435     Document Type: Article

References (93)

1. 1. Vale, R., Banker, G., and Hall, Z. W. (1992) The neuronal cytoskeleton, in An Introduction to Molecular Neurobiology (Hall, Z. W., ed.), Sineuer Associates Inc., Sunderland, MA pp. 247-279.
2. 2. Heidemann, S. R., Kanders, J. M., and Hamborg, M. A. (1981) Polarity orientation of axonal microtubules. J. Cell Biol. 91, 661-665.
3. 3. Baas, P. W., Deitch, J. S., Black, M. M., and Banker G. A. (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA 85, 8335-8339.
4. 4. Weiss, P. and Hiscoe, H. (1948) Experiments on the mechanism of nerve growth. J. Exp. Zool. 107, 315-395.
5. 5. Tytell, M., Black, M. M., Garner, J. A., and Lasek, R. J. (1981) Axonal transport: each major rate component reflects the movement of distinct macromolecular complexes. Science 214, 179-181.
6. 6. Grafstein, B. and Forman, D. S. (1980) Intracellular transport in neurons. Physiol. Rev. 60, 1167-1283.
7. 7. Hammerschlag, R. and Brady, S. T. (1989) Axonal Transport and the Neuronal Cytoskeleton, in Basic Neurochemistry (Siegel, G. J., Agranoff, B. W., Albers, R. W., and Molinoff, P. B., eds.), Raven Press, NY, pp. 457.
8. 8. Lasek, R. J., Garner, J. A., and Brady, S. T. (1984) Axonal transport of the cytoplasmic matrix. J. Cell Biol. 99, 212s-221s.
9. 9. Hirokawa, N. (1996) Organelle transport along microtubules: the role of KIFs. Trends Cell Biol 6, 135-141.
10. 10. Brady, S. T. (1991) Molecular motors in the nervous system. Neuron 7, 521-533.
11. 11. Vallee, R. B. and Bloom, G. S. (1991) Mechanisms of fast and slow axonal transport. Ann. Rev. Neurosci. 14, 59-92.
12. 12. Bloom, G. S., and Endow, S. A. (1995) Motor proteins 1: kinesins. Protein Profiles 2, 1109-1111.
13. 13. Hirokawa, N. (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279, 519-526.
14. 14. Holzbaur, E. L. and Vallee, R. B. (1994) Dyneins: molecular structure and cellular function. Ann. Rev. Cell Biol. 10, 339-372.
15. 15. Paschal, B. M., Shpetner, H. S., and Vallee, R. B. (1987a) MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol. 105, 1273-1282.
16. 16. King, S. M., Barbarese, E., Dillman, J. F., Patel-King, R. S., Carson, J. H., and Pfister, K. K. (1996) Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain. J. Biol. Chem. 271, 19358-19366.
17. 17. King, S. M., Patel-King, R. S., Wilkerson, C. G., and Witman, B. (1995) The 78,000-Mr intermediate chain of Chlamydomonas outer arm dynein is a microtubule-binding protein. J. Cell Biol. 131, 399-409.
18. 18. Steffen, W., Karki, S., Vaughan, K. T., Vallee, R. B., Holzbaur, E. L. F., Weiss, D. G., and Kuznetsov, S. A. (1998) The involvement of the intermediate chain of cytoplasmic dynein in binding the motor complex to membranous orgaelles of Xenopus oocytes. Mol. Biol. Cell 8, 2077-2088.
19. 19. Steffen, W., Hodgkinson, J. L., and Wiche, G. (1996) Immunogold localization of the intermediate chain within the protein complex of cytoplasmic dynein. J. Struct. Biol. 117, 227-235.
20. 20. Niclas, J., Allan, V. J., and Vale, R. D. (1996) Cell-cycle regulation of dynein association with membranes modulates microtubule-based organelle transport. J. Cell Biol. 133, 585-593.
21. 21. King, S. M., Barbarese, E., Dillman, J. F., Benashski, S. E., Do, K. T., Patel-King, R. S. and Pfister, K. K. (1998) Cytoplasmic dynein contains a family of differentially expressed light chains. Biochemistry 37, 15033-15041.
22. 22. Gill, S. R., Cleveland, D. W., and Schroer, T. A. (1994) Characterization of DLC-A and DLC-B, two families of cytoplasmic dynein light chain subunits. Mol. Biol. Cell 5, 645-654.
23. 23. Dick, T., Ray, K., Salz, H. K., and Chia, W. (1996) Cytoplasmic dynein (ddlc1) mutations cause morphogenetic defects and apoptotic cell death in Drosophila melanogaster. Mol. Cell Biol. 16, 1966-1977.
24. 24. Phillis, R., Statton, D., Caruccio P., and Murphey, R. K. (1996) Mutations in the 8 kDa dynein light chain gene disrput sensory axon projections in the Drosophila imaginal disk CNS. Development 122, 2955-2963.
25. 25. Reddy, S., Jin, P., Trimarchi, J., Caruccio, P., Phillis, R., and Murphey, R. K. (1997) Mutant molecular motors disrupt neural circuits in Drosophila. J. Neurobiol. 33, 711-723.
26. 26. Hirokawa, N., Sato-Yoshitake, R., Yoshida, T., and Kawashima, T. (1990) Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J. Cell Biol. 111, 1027-1037.
27. 27. Dahlstrom, A. B. and Booj, S. (1988) Rapid axonal transport as a chromatographic process: the use of immunocytochemistry of ligated nerves to investigate the biochemistry of anterogradely versus retrogradely transported organelles. Cell Motil. Cytoskel. 10, 309-320.
28. 27a. Brady, S. T. and Lasek, R. J. (1982) Axonal transport: a cell-biological method for studying proteins that associate with the cytoskeleton. Method Cell Biol. 25 Pt B, 365-398.
29. 28. Brimijoin, S. (1975) Stop-flow: a new technique for measuring axonal transport, and its application to the transport of dopamine-beta-hydroxylase. J. Neurobiol. 6, 379-394.
30. 28a. Dillman, J. F., Dabney, L. P., and Pfister, K. K. (1996) Cytoplasmic dynein is associated with slow axonal transport. Proc. Natl. Acad. Sci. USA 93, 141-144.
31. 29. Dillman, J. F., Dabney, L. P., Karki, S., Paschal, B. M., Holzbaur, E. L. F., and Pfister, K. K. (1996) Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J. Neurosci. 16, 6742-6752.
32. 30. Allan, V. (1994) Organelle movement. Dynactin: portrait of a dynein regulator. Cur. Biol. 4, 1000-1002.
33. 31. Schafer, D. A., Gill, S. R., Cooper, J. A., Heuser, J. E., and Schroer, T. A. (1994) Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin J. Cell Biol. 126, 403-412.
34. 32. Holleran, E. A., Karki, S., and Holzbaur, E. L. (1998) The role of the dynactin complex in intracellular motility. Int. Rev. Cytol. 182, 69-109.
35. 33. Holleran, E. A., Tokito, M. K., Karki, S., and Holzbaur, E. L. (1996) Centractin (ARP1) associates with spectrin revealing a potential mechanism to link dynactin to intracellular organelles. J. Cell Biol 135, 1815-1829.
36. 34. Mullins, R. D., Kelleher, J. F., and Pollard, T. D. (1996) Actin' like actin. Trends Cell Biol. 6, 208-212.
37. 35. Schafer, D. A. and Cooper, J. A. (1995) Control of actin assembly at filament ends. Ann. Rev. Cell Dev. Biol. 11, 497-518.
38. 36. Holzbaur, E. L., Hammarback, J. A., Paschal, B. M., Kravit, N. G., Pfister, K. K., and Vallee, R. B. (1992) Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature 360, 695-695.
39. 37. Echeverri, C. J., Paschal, B. M., Vaughan, K. T., and Vallee, R. B. (1996) 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, 617-633.
40. 38. Karki, S., LaMonte, B., and Holzbaur, E. L. (1998) Characterization of the p22 subunit of dynactin reveals the localization of cytoplasmic dynein and dynactin to the midbody of dividing cells. J. Cell Biol. 142, 1023-1034.
41. 39. Pfister, K. K., Benashski, S. E., Dillman, J. F., Patel-King, R. S., and King, S. M. (1998) Identification and molecular characterization of the p24 dynactin light chain. Cell Motil. Cytoskel 41, 154-167.
42. 40. Gill, S. R., Schroer, T. A., Szilak, I., Steuer, E. R., Sheetz, M. P., and Cleveland, D. W. (1991) Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115, 1639-1650.
43. 41. Vallee, R. B. and Sheetz, M. P. (1996) Targeting of Motor Proteins. Science 271, 1539-1544.
44. Glued J. Cell Biol. 131, 1507-1516.
45. 43. Karki, S. and Holzbaur, E. L. F. (1995) Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270, 28806-28811.
46. 44. Tokito, M. K., Howland D. S., Lee, V. M., and Holzbaur, E. L. F. (1996) Functionally distinct isoforms of dynactin are expressed in human neurons. Mol. Biol. Cell 7, 1167-1180.
47. 45. Plamann, M, Minke, P. F., Tinsley, J. H., and Bruno, K. S. (1994) Cytoplasmic dynein and actin-related protein Arp1 are required for normal nuclear distribution in filamentous fungi. J. Cell Biol. 127, 139-149.
48. 46. McGrail, M., Gepner, J., Silvanovich, A., Ludman, S., Serr, M., and Hays, T. S. (1995) Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued complex. J. Cell Biol. 131, 411-425.
49. 47. Muhua, L., Karpova, T. S., and Cooper, J. A. (1994) A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration. Cell 78, 669-679.
50. 48. Bruno, K. S., Tinsley, J. H., Minke, P. F., and Plamann, M. (1996) Genetic interactions among cytoplasmic dynein, dynactin, and nuclear distribution mutants of Neurospora crassa. Proc. Natl. Acad. Sci. USA 93, 4775-4780.
51. 49. Burkhardt, J. K., Echeverri, C. J., Nilsson, T., and Vallee, R. B. (1997) Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenence of membrane organelle distribution. J. Cell Biol. 139, 469-484.
52. 50. Presley, J. F., Cole, N. B., Schroer, T. A., Hirschberg, K., Zaal, K. J., and Lippincott-Schwartz, J. (1997) ER-Golgi transport visualized in living cells. Nature 389, 81-85.
53. 51. Ahmad, F. J., Echeverri, C. J., Vallee, R. B., and Baas P. W. (1998) Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J. Cell Biol. 140, 391-401.
54. 52. Holleran, E. A. and Holzbaur, E. L. (1998) Speculating about spectrin: new insights into the Golgi-associated cytoskeleton. Trends Cell Biol. 8, 26-29.
55. 53. Fath, K. R., Trimbur, G. M., and Burgess, D. R. (1997) Molecular motors and a spectrin matrix associate with Golgi membranes in vitro. J. Cell Biol. 139, 1169-1181.
56. 54. Lippincott-Schwartz, J. (1998) Cytoskeletal proteins and Golgi dynamics. Curr. Opin. Cell Biol. 10, 52-59.
57. 55. Beck, K. A. and Nelson, W. J. (1998) A spectrin membrane skeleton of the Golgi complex. Biochim. Biophys. Acta 1404, 153-160.
58. 56. Levine, J. and Willard, M. (1981) Fodrin: axonally transported polypeptides associated with the internal periphery of many cells. J. Cell Biol. 90, 631-643.
59. 57. Garner, J. A. and Lasek, R. J. (1982) Cohesive axonal transport of the slow component b complex of polypeptides. J. Neurosci. 2, 1824-1835.
60. 58. Xiang, X., Roghi C., and Morris, N. R. (1995) Characterization and localization of the cytoplasmic dynein heavy chain in Aspergillus nidulans. Proc. Natl. Acad. Sci. U.S.A. 92, 9890-9894.
61. 59. Busson, S., Dujardin, D., Moreau, A., Dompierre, J., and De, M. J. (1998) Dynein and dynactin are localized to astral microtubules and at cortical sites in mitotic epithelial cells. Curr. Biol. 8, 541-544.
62. 60. Carminati, J. L. and Stearns, T. (1997) Microtubules orient the mitotic spindle in yeast through dynein dependent interactions with the cell cortex. J. Cell Biol. 138, 629-641.
63. 61. Skop, A. R. and White, J. G. (1998) The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos. Curr. Biol. 8, 1110-1116.
64. 62. Kahana, J. A., Schlenstedt, G., Evanchuk, D. M., Geiser, J. R., Hoyt, M. A., and Silver, P. A. (1998) The yeast dynactin complex is involved in partitioning the mitotic spindle between mother and daughter cells during anaphase B. Mol Biol. Cell 9, 1741-1756.
65. 63. Pfister, K. K., Salata, M. W., Dillman, J. F., Vaughan, K. T., Vallee, R. B., Torre E., and Lye, R. J. (1996) Differential expression and phosphorylation of IC74 subunits of cytoplasmic dynein in cultured neurons and glia. J. Biol. Chem. 271, 1687-1694.
66. 64. Pfister, K. K., Salata, M. W., Dillman, J. F., Torre, E., and Lye, R. J. (1996) Identification and developmental regulation of a neuron specific subunit of cytoplasmic dynein. Mol. Cell Biol. 7, 331-343.
67. 64a. Salata, M. W., Dillman, J. F., III, Lye, R. J., and Pfister, K. K. (2000) Changes in the expression of cyloptasmic dynein intermediate chain isoforms precede neurite extension. Submitted.
68. 65. Black, M. M. (1994) Microtubule transport and assembly cooperate to generate the microtubule array of growing axons. Prog. Brain. Res. 102, 61-77.
69. 66. Baas, P. W. (1997) Microtubules and axonal growth. Cur. Opin. Cell Biol. 9, 29-36.
70. 67. Baas, P. W. and Brown A. (1997) Slow axonal transport: the polymer transport model. Trends Cell Biol. 7, 380-384.
71. 68. Hirokawa, N., Terada, S., Funakoshi, T., and Takeda, S. (1997) Slow axonal transport: the subunit transport model. Trends Cell Biol. 7, 384-388.
72. 69. Campenot, B., Lund, K., and Senger, D. L. (1996) Delivery of newly synthesized tubulin to rapidly growing distal axons of sympathetic neurons in compartmented cultures. J. Cell Biol. 135, 701-709.
73. 70. Nixon, R. A. (1998) The slow axonal transport debate. Trends Cell Biol. 8, 100
74. 71. Keating, T. J., Peloquin, J. G., Rodionov, V. I., Momcilovic, D., and Borisy, G. G. (1997) Microtubule release from the centrosome. Proc. Natl. Acad. Sci. USA 94, 5078-5083.
75. 72. Gibbons, I. R. (1981) Cilia and flagella of eukaryotes. J. Cell Biol. 91, 107s-124s.
76. 73. Witman, G. B. (1992) Axonemal dyneins. Curr. Opin. Cell Biol. 4, 74-79.
77. 74. King, S. M., Wilkerson, C. G., and Witman, G. B. (1991) The Mr 78,000 intermediate chain of Chlamydomonas outer arm dynein interacts with alpha-tubulin in situ. J. Biol. Chem. 266, 8401-8407.
78. 75. Gibbons, I. R. (1988) Dynein ATPases as microtubule motors. J. Biol. Chem. 263, 15837-15840.
79. 76. Porter, M. E. (1996) Axonemal dyneins: assembly, organization, and regulation. Cur. Opin. Cell Biol. 8, 10-17.
80. 77. McQuarrie, I. G., Brady, S. T., and Lasek, R. J. (1986) Diversity in the axonal transport of structural proteins: major differences between optic and spinal axons in the rat. J. Neurosci. 6, 1593-1605.
81. 78. Hoffman, P. N. and Lasek, R. J. (1975a) The slow component of axonal transport. Identification of major structural polypeptides of the axon and their generality among mammalian neurons. J. Cell Biol. 66, 351-366.
82. 79. Black, M. M., and Lasek, R. J. (1978) A difference between the proteins conveyed in the fast component of axonal transport in guinea pig hypoglossal and vagus motor neurons. J. Neurobiol. 9, 433-443.
83. 80. Hoffman, P. N. and Lasek, R. J. (1980b) Axonal transport of the cytoskeleton in regenerating motor neurons: constancy and change. Brain Res. 202, 317-333.
84. 81. McQuarrie, I. G., Brady, S. T., and Lasek, R. J. (1989) Retardation in the slow axonal transport of cytoskeletal elements during maturation and aging. Neurobiol. Aging 10, 359-365.
85. 82. Hoffman, P. N., Lasek, R. J., Griffin, J. W., and Price, D. L. (1983) Slowing of the axonal transport of neurofilament proteins during development. J. Neurosci. 3, 1694-1700.
86. 83. Cleveland, D. W. and Hoffman, P. N. (1991) Slow axonal transport models come full circle: evidence that microtubule sliding mediates axon elongation and tubulin transport. Cell 67, 453-456.
87. 84. Nixon, R. A. and Logvinenko, K. B. (1986) Multiple fates of newly synthesized neurofilament proteins: evidence for a stationary neurofilament network distributed nonuniformly along axons of retinal ganglion cell neurons. J. Cell Biol. 102, 647-659.
88. 85. Paschal, B. M. and Vallee R. B. (1987) Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330, 181-183.
89. 86. Paschal, B. M., King, S. M., Moss, A. G., Collins, C. A., Vallee, R. B., and Witman, G. B. (1987b) Isolated flagellar outer arm dynein translocates brain microtubules in vitro. Nature 330, 672-674.
90. 87. Mitchison, T. and Kirschner, M. (1984) Dynamic instability of microtubule growth. Nature 312, 237-242.
91. 88. Stewart, R. J., Semerjian, J., and Schmidt, C. F. (1998) Highly processive motility is not a general feature of the kinesins. Eur. Biophys. J. 27, 353-360.
92. 89. Muresan, V., Godek, C. P., Reese, T. S., and Schnapp, B. J. (1996) Plus-end motors override minus-end motors during transport of squid axon vesicles on microtubules. J. Cell Biol 135, 383-397.
93. 90. Ainger, K., Avossa, D., Morgan, F., Hill, S. J., Barry, C., Barbarese, E., and Carson, J. H. (1993) Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. J. Cell Biol 123, 431-441.