Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein

Biochemistry

Volumn 43, Issue 35, 2004, Pages 11266-11274

  Kon, Takahide ^a   Nishiura, Masaya ^a   Ohkura, Reiko ^a   Toyoshima, Yoko Y ^a   Sutoh, Kazuo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITY; MICROTUBULES;

ADENOSINETRIPHOSPHATE; HYDROLYSIS; MUTAGENESIS; PURIFICATION;

BIOCHEMISTRY;

DYNEIN ADENOSINE TRIPHOSPHATASE; NUCLEOTIDE BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; BIOCHEMISTRY; CYTOPLASM; DICTYOSTELIUM; GENE MUTATION; HYDROLYSIS; INTRACELLULAR TRANSPORT; MICROTUBULE ASSEMBLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION;

ADENOSINE TRIPHOSPHATE; AMINO ACID MOTIFS; ANIMALS; CYTOPLASM; DICTYOSTELIUM; DYNEIN ATPASE; ENZYME ACTIVATION; GREEN FLUORESCENT PROTEINS; HISTIDINE; HYDROLYSIS; LUMINESCENT PROTEINS; MICROFILAMENTS; MICROTUBULES; PEPTIDE FRAGMENTS; PEPTIDES; PHOTOCHEMISTRY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SUBCELLULAR FRACTIONS; ULTRAVIOLET RAYS; VANADATES;

DICTYOSTELIUM;

EID: 4444330119     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048985a     Document Type: Article

References (38)

1. Holzbaur, E. L., and Vallee, R. B. (1994) DYNEINS: molecular structure and cellular function, Annu. Rev. Cell Biol. 10, 339-372.
2. Vallee, R. B., and Sheetz, M. P. (1996) Targeting of motor proteins, Science 271, 1539-1544.
3. Vale, R. D. (2003) The molecular motor toolbox for intracellular transport, Cell 112, 467-480.
4. Habura, A., Tikhonenko, I., Chisholm, R. L., and Koonce, M. P. (1999) Interaction mapping of a dynein heavy chain. Identification of dimerization and intermediate-chain binding domains, J. Biol. Chem. 274, 15447-15453.
5. Tynan, S. H., Gee, M. A., and Vallee, R. B. (2000) Distinct but overlapping sites within the cytoplasmic dynein heavy chain for dimerization and for intermediate chain and light intermediate chain binding, J. Biol. Chem. 275, 32769-32774.
6. Paschal, B. M., Shpetner, H. S., and Vallee, R. B. (1987) MAP IC is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol. 105, 1273-1282.
7. Koonce, M. P., and Samso, M. (1996) Overexpression of cytoplasmic dynein's globular head causes a collapse of the interphase microtubule network in Dictyostelium, Mol. Biol. Cell 7, 935-948.
8. Nishiura, M., Kon, T., Shiroguchi, K., Ohkura, R., Shima, T., Toyoshima, Y., and Sutoh, K. (2004) A single-headed recombinant fragment of Dictyostelium cytoplasmic dynein can drive the robust sliding of microtubules, J. Biol. Chem. 279, 22799-22902.
9. Samso, M., Radermacher, M., Frank, J., and Koonce, M. P. (1998) Structural characterization of a dynein motor domain, J. Mol. Biol. 276, 927-937.
10. +: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes, Genome Res. 9, 27-43.
11. Goodenough, U., and Heuser, J. (1984) Structural comparison of purified dynein proteins with in situ dynein arms, J. Mol. Biol. 180, 1083-1118.
12. 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.
13. Koonce, M. P. (1997) Identification of a microtubule-binding domain in a cytoplasmic dynein heavy chain, J. Biol. Chem. 272, 19714-19718.
14. Koonce, M. P., and Tikhonenko, I. (2000) Functional elements within the dynein microtubule-binding domain, Mol. Biol. Cell 11, 523-529.
15. King, S. M. (2000) AAA domains and organization of the dynein motor unit, J. Cell Sci. 113, 2521-2526.
16. Vale, R. D. (2000) AAA proteins. Lords of the ring, J. Cell Biol. 150, F13-F19.
17. Asai, D. J., and Koonce, M. P. (2001) The dynein heavy chain: structure, mechanics and evolution, Trends Cell Biol. 11, 196-202.
18. Burgess, S. A., Walker, M. L., Sakakibara, H., Knight, P. J., and Oiwa, K. (2003) Dynein structure and power stroke, Nature 421, 715-718.
19. Vale, R. D., and Milligan, R. A. (2000) The way things move: looking under the hood of molecular motor proteins, Science 288, 88-95.
20. Gibbons, I. R., Gibbons, B. H., Mocz, G., and Asai, D. J. (1991) Multiple nucleotide-binding sites in the sequence of dynein β heavy chain, Nature 352, 640-643.
21. Ogawa, K. (1991) Four ATP-binding sites in the midregion of the β heavy chain of dynein, Nature 352, 643-645.
22. Koonce, M. P., Grissom, P. M., and McIntosh, J. R. (1992) Dynein from Dictyostelium: primary structure comparisons between a cytoplasmic motor enzyme and flagellar dynein, J. Cell Biol. 119, 1597-1604.
23. Mikami, A., Paschal, B. M., Mazumdar, M., and Vallee, R. B. (1993) Molecular cloning of the retrograde transport motor cytoplasmic dynein (MAP IC), Neuron 10, 787-796.
24. Mocz, G., and Gibbons, I. R. (1996) Phase partition analysis of nucleotide binding to axonemal dynein, Biochemistry 35, 9204-9211.
25. Shimizu, T., and Johnson, K. A. (1983) Kinetic evidence for multiple dynein ATPase sites, J. Biol. Chem. 258, 13841-13846.
26. Gibbons, I. R., Lee-Eiford, A., Mocz, G., Phillipson, C. A., Tang, W. J., and Gibbons, B. H. (1987) Photosensitized cleavage of dynein heavy chains. Cleavage at the "V1 site" by irradiation at 365 nm in the presence of ATP and vanadate, J. Biol. Chem. 262, 2780-2786.
27. Silvanovich, A., Li, M. G., Serr, M., Mische, S., and Hays, T. S. (2003) The third P-loop domain in cytoplasmic dynein heavy chain is essential for dynein motor function and ATP-sensitive microtubule binding, Mol. Biol. Cell 14, 1355-1365.
28. Reck-Peterson, S. L., and Vale, R. D. (2004) Molecular dissection of the roles of nucleotide binding and hydrolysis in dynein's AAA domains in Saccharomyces cerevisiae, Proc. Natl. Acad. Sci. U.S.A. 101, 1491-1495.
29. Blaauw, M., Linskens, M. H., and van Haastert, P. J. (2000) Efficient control of gene expression by a tetracycline-dependent transactivator in single Dictyostelium discoideum cells, Gene 252, 71-82.
30. Sloboda, R. D., and Rosenbaum, J. L. (1982) Purification and assay of microtubule-associated proteins (MAPs), Methods Enzymol. 85, 409-416.
31. Vale, R. D., and Toyoshima, Y. Y. (1988) Rotation and translocation of microtubules in vitro induced by dyneins from Tetrahymena cilia, Cell 52, 459-469.
32. Schirmer, E. C., Queitsch, C., Kowal, A. S., Parsell, D. A., and Lindquist, S. (1998) The ATPase activity of Hsp104, effects of environmental conditions and mutations, J. Biol. Chem. 273, 15546-15552.
33. Krzewska, J., Konopa, G., and Liberek, K. (2001) Importance of two ATP-binding sites for oligomerization, ATPase activity and chaperone function of mitochondrial Hsp78 protein, J. Mol. Biol. 314, 901-910.
34. + superfamily ATPases: common structure-diverse function, Genes Cells 6, 575-597.
35. Wang, Q., Song, C., Yang, X., and Li, C. C. (2003) D1 ring is stable and nucleotide-independent, whereas D2 ring undergoes major conformational changes during the ATPase cycle of p97-VCP, J. Biol. Chem. 278, 32784-32793.
36. Gibbons, I. R. (1995) Dynein family of motor proteins: present status and future questions, Cell Motil. Cytoskeleton 32, 136-144.
37. Howard, J. (2001) Speeds of Motors, in Mechanics of Motor Proteins and the Cytoskeleton, pp 213-227, Sinauer Associates, Sunderland, MA.
38. Mallik, R., Carter, B. C., Lex, S. A., King, S. J., and Gross, S. P. (2004) Cytoplasmic dynein functions as a gear in response to load, Nature 427, 649-652.