The interaction of neurofilaments with the microtubule motor cytoplasmic dynein

Molecular Biology of the Cell

Volumn 15, Issue 11, 2004, Pages 5092-5100

  Wagner, Oliver I ^a   Ascaño, Jennifer ^a   Tokito, Mariko ^a   Leterrier, Jean Francois ^b   Janmey, Paul A ^a   Holzbaur, Erika L F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITÉ DE POITIERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

AFFINITY CHROMATOGRAPHY; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOSYNTHESIS; MICROTUBULE; NERVE CELL; NERVE FIBER TRANSPORT; NEUROFILAMENT; NEUROFILAMENT MEDIUM CHAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; RETROGRADE NERVE FIBER TRANSPORT; TWO HYBRID SYSTEM;

ANIMALS; BRAIN; CATTLE; CHROMATOGRAPHY, AFFINITY; CYTOPLASM; DYNEIN ATPASE; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEUROFILAMENT PROTEINS; NEURONS; PHOSPHORYLATION; PROTEIN BINDING; RATS; SPINAL CORD; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 6344272746     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-05-0401     Document Type: Article

References (36)

1. Al-chalabi, A., and Miller, C.C. J. (2003) Neurofilaments and neurological disease. BioEssays 24, 346-355.
2. Aranda-Espinoza, H., Carl, P., Leterrier, J.F., Janmey, P., and Discher, D.E. (2002). Domain unfolding in neurofilament sidearms: effects of phosphorylation and ATP. FEBS Lett. 531, 397-401.
3. Burgess, S.A., Walker, M.L., Sakaibara, H., Knight, P.J., and Oiwa, K. (2003). Dynein structure and power stroke. Nature 421, 715-718.
4. Dogic, Z. et al. (2004). Elongation and fluctuations of semiflexible polymers in a nematic solvent. Phys. Rev. Lett. 92, 125503-125504.
5. Gee, M.A., Heuser, J.E., and Vallee, R.B. (1997). An extended microtubule-binding structure within the dynein motor domain. Nature 390, 636-639.
6. Gross, S.P., Tuma, M.C., Deacon, S.W., Serpinskaya, A.S., Reilein, A.R., and Gelfand, V.I. (2002). Interactions and regulation of molecular motors in Xenopus melanophores. J. Cell Biol. 156, 855-865.
7. Heimann, R., Shelanski, M.L., and Liem, R.K. (1985). Microtubule- associated proteins bind specifically to the 70-kDa neurofilament protein. J. Biol. Chem. 260, 12160-12166.
8. Heins, S., Wong, P.C., Muller, S., Goldie, K., Cleveland, D.W., and Aebi, U. (1993). The rod domain of NF-L determines neurofilament architecture, whereas the end domains specify filament assembly and network formation. J. Cell Biol. 123, 1517-1533.
9. Helfand, B.T., Mikami, A., Vallee, R.B., and Goldman, R.D. (2002). A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J. Cell Biol. 157, 795-806.
10. Hirokawa, N., Hisanaga, S., and Shiomura, Y. (1988). 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. 8, 2769-2779.
11. Hisanaga, S., and Hirokawa, N. (1990). Dephosphorylation-induced interactions of neurofilaments with microtubules. J. Biol. Chem. 265, 21852-21858.
12. Holleran, E.A., Tokito, M.K., LaMonte, B.H., Stankewich, M., Morrow, J., and Holzbaur, E.L.F. (2001). βIII spectrin binds to the Arp1 subunit of dynactin. J. Biol. Chem. 276, 36598-36605.
13. Hyman, A., Drechsel, D., Kellogg, D., Salser, S., Sawin, K., Steifen, P., Wordeman, L., and Mitchison, T. (1991). Preparation of modified tubulins. Methods Enzymol. 196, 478-485.
14. 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.
15. Karki, S., and Holzbaur, E.L.F. (1999). Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr. Opin. Cell Biol. 11, 45-53.
16. Karki, S., Tokito, M.K., and Holzbaur, E.L. (1997). Casein kinase II binds to and phosphorylates cytoplasmic dynein. J. Biol. Chem. 272, 5887-5891.
17. Kumar, S., Yin, X., Trapp, B.D., Hoh, J.H., and Paulaitis, M.E. (2002a). Relating interactions between neurofilaments to the structure of axonal neurofilament distributions through polymer brush models. Biophys. J. 82, 2360-2372.
18. Kumar, S., Yin, X., Trapp, B.D., Paulairis, M.E., and Hoh, J.H. (2002b). Role of long-range repulsive forces in organizing axonal neurofilament distributions: evidence from mice deficient in myelin-associated glycoprotein. J. Neurosci. Res. 68, 681-690.
19. LaMonte, B. H., Wallace, K. E., Holloway, B. A., Shelly, S. S., Ascano, J., Tokito, M., Van Winkle, T., Howland, D. S. and Holzbaur, E. L. (2002). Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34, 715-727.
20. Leterrier, J.F., Kas, J., Hartwig, J., Vegners, R., and Janmey, P.A. (1996). Mechanical effects of neurofilament cross-bridges. Modulation by phosphorylation, lipids, and interactions with F-actin. J. Biol. Chem. 271, 15687-15694.
21. Ligon, L.A., Karki, S., Tokito, M., and Holzbaur, E.L.F. (2002). Dynein binds to β-catenin and may tether microtubules at adherens junctions. Nat. Cell Biol. 3, 913-917.
22. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951). Protein measurement using the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
23. Nguyen, M.D., Shu, T., Sanada, K., Lariviere, R.C., Tseng, H.-C, Park, S.K., Julien, J.-P., and Tsai, L.-H. (2004). A NUDEL-dependent mechanism of neurofilament assembly regulates the integrity of CNS neurons. Nat. Cell Biol. 6, 595-608.
24. Prahlad, V., Helfand, B.T., Langford, G.M., Vale, R.D., and Goldman, R.D. (2000). Fast transport of neurofilament protein along microtubules in squid axoplasm. J. Cell Sci. 113, 3939-3946.
25. Rao, M.V. et al. (2002). Myosin Va binding to neurofilaments is essential for correct myosin Va distribution and transport and neurofilament density. J. Cell Biol. 159, 279-289.
26. Rao, M.V. et al. (2003). The neuroflament middle molecular mass subunit carboxyl-terminal tail domains is essential for the radial growth and cytoskeletal architecture of axons but not for regulating neurofilament transport rate. J. Cell Biol. 163, 1021-1031.
27. Roy, S., Coffee, P., Smith, G., Liem, R.K., Brady, S.T., and Black, M.M. (2000). Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J. Neurosci. 20, 6849-6861.
28. 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.
29. Shah, J.V., Flanagan, L.A., Janmey, P.A., and Leterrier, J.F. (2000). Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol. Biol. Cell 11, 3495-3508.
30. Shea, T.B. and Flanagan, L.A. (2001) Kinesin, dynein and neurofilament transport. Trends Neurosci. 24, 644-648.
31. Toyoshima, I., Kato, K., Sugawara, M., Wada, C., and Masamune, O. (1998). Kinesin accumulation in chick spinal axonal swellings with beta, beta′-iminodipropionitrile (IDPN) intoxication. Neurosci. Lett. 249, 103-106.
32. Vallee, R.B., Wall, J.S., Paschal, B.M., and Shpetner, H.S. (1988). Microtubule-associated protein 1C from brain is a two-headed cytosolic dynein. Nature 332, 561-563.
33. Wagner, O.I., Lifshitz, J., Janmey, P.A., Linden, M., McIntosh, T.K., and Leterrier, J.F. (2003). Mechanisms of mitochondria-neurofilament interactions. J. Neurosci. 23, 9046-9058.
34. Wang, L., Ho, C.L., Sun, D., Liem, R.K., and Brown, A. (2000). Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nat. Cell Biol. 2, 137-141.
35. Xia, C-H., Roberts, E.A., her, L.-S., Liu, X., Williams, D.S., Cleveland, D.W., and Goldstein, L.S.B. (2003) Abnormal neurofilaments transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J. Cell Biol. 161, 55-66.
36. Xu, Z., and Tung, V.W. (2000). Overexpression of neurofilament subunit M accelerates axonal transport of neurofilaments. Brain Res. 866, 326-332.