Creating biomolecular motors based on dynein and actin-binding proteins

Nature Nanotechnology

Volumn 12, Issue 3, 2017, Pages 233-237

  Furuta, Akane ^a   Amino, Misako ^a   Yoshio, Maki ^a   Oiwa, Kazuhiro ^a,b,c   Kojima, Hiroaki ^a   Furuta, Ken'Ya ^a  

^a NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF HYOGO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NANOSTRUCTURED MATERIALS; NANOTECHNOLOGY;

ACTIN-BINDING PROTEINS; BIOMOLECULAR MACHINES; BIOMOLECULAR MOTOR; DESIGN AND CONSTRUCTION; DIRECTIONAL MOVEMENTS; NANOSCALE DIMENSIONS; NATURALLY OCCURRING; SYNTHETIC STRATEGIES;

PROTEINS;

ACTIN BINDING PROTEIN; ADENOSINE TRIPHOSPHATE; ALPHA ACTININ; DYNEIN ADENOSINE TRIPHOSPHATASE; GELSOLIN; KINESIN; MOLECULAR MOTOR; MYOSIN; VINCULIN;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HYDROLYSIS; MICROTUBULE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; CHEMISTRY; GENETICS;

CYTOSKELETON; DYNEINS; HUMANS; MICROFILAMENT PROTEINS;

EID: 85008716293     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2016.238     Document Type: Article

References (43)

1. Vale, R. D. The molecular motor toolbox for intracellular transport. Cell 112, 467-480 (2003).
2. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton 1st edn (Sinauer Associates, 2001).
3. van den Heuvel, M. G. & Dekker, C. Motor proteins at work for nanotechnology. Science 317, 333-336 (2007).
4. Diez, S., Helenius, J. H. & Howard, J. in Protein Science Encyclopedia 185-199 (Wiley, 2008).
5. Tsiavaliaris, G., Fujita-Becker, S. & Manstein, D. J. Molecular engineering of a backwards-moving myosin motor. Nature 427, 558-561 (2004).
6. Liu, H. et al. Control of a biomolecular motor-powered nanodevice with an engineered chemical switch. Nat. Mater. 1, 173-177 (2002).
7. Nomura, A., Uyeda, T. Q., Yumoto, N. & Tatsu, Y. Photo-control of kinesinmicrotubule motility using caged peptides derived from the kinesin C-terminus domain. Chem. Commun. 3588-3590 (2006).
8. Chen, L., Nakamura, M., Schindler, T. D., Parker, D. & Bryant, Z. Engineering controllable bidirectional molecular motors based on myosin. Nat. Nanotech. 7, 252-256 (2012).
9. Hackney, D. D. The kinetic cycles of myosin, kinesin, and dynein. Annu. Rev. Physiol. 58, 731-750 (1996).
10. Howard, J. Protein power strokes. Curr. Biol. 16, R517-R519 (2006).
11. Kon, T., Mogami, T., Ohkura, R., Nishiura, M. & Sutoh, K. ATP hydrolysis cycledependent tail motions in cytoplasmic dynein. Nat. Struct. Mol. Biol. 12, 513-519 (2005).
12. Roberts, A. J., Kon, T., Knight, P. J., Sutoh, K. & Burgess, S. A. Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol. 14, 713-726 (2013).
13. Vallee, R. B., Williams, J. C., Varma, D. & Barnhart, L. E. Dynein: an ancient motor protein involved in multiple modes of transport. J. Neurobiol. 58, 189-200 (2004).
14. Gibbons, I. R. Cilia and flagella of eukaryotes. J. Cell Biol. 91, 107s-124s (1981).
15. Burgess, S. A., Walker, M. L., Sakakibara, H., Knight, P. J. & Oiwa, K. Dynein structure and power stroke. Nature 421, 715-718 (2003).
16. Roberts, A. J. et al. AAA+ Ring and linker swing mechanism in the dynein motor. Cell 136, 485-495 (2009).
17. Kon, T. et al. The 2.8 Å crystal structure of the dynein motor domain. Nature 484, 345-350 (2012).
18. Schmidt, H., Zalyte, R., Urnavicius, L. & Carter, A. P. Structure of human cytoplasmic dynein-2 primed for its power stroke. Nature 518, 435-438 (2015).
19. Carter, A. P. et al. Structure and functional role of dynein's microtubule-binding domain. Science 322, 1691-1695 (2008).
20. Redwine, W. B. et al. Structural basis for microtubule binding and release by dynein. Science 337, 1532-1536 (2012).
21. Shima, T., Kon, T., Imamula, K., Ohkura, R. & Sutoh, K. Two modes of microtubule sliding driven by cytoplasmic dynein. Proc. Natl Acad. Sci. USA 103, 17736-17740 (2006).
22. Gibbons, I. R. et al. The affinity of the dynein microtubule-binding domain is modulated by the conformation of its coiled-coil stalk. J. Biol. Chem. 280, 23960-23965 (2005).
23. Kon, T. et al. Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nat. Struct. Mol. Biol. 16, 325-333 (2009).
24. Nishikawa, Y., Inatomi, M., Iwasaki, H. & Kurisu, G. Structural change in the dynein stalk region associated with two different affinities for the microtubule. J. Mol. Biol. 428, 1886-1896 (2015).
25. Burgess, S. A. & Knight, P. J. Is the dynein motor a winch? Curr. Opin. Struct. Biol. 14, 138-146 (2004).
26. Kim, L. Y. et al. The structural basis of actin organization by vinculin and metavinculin. J. Mol. Biol. 428, 10-25 (2015).
27. Vale, R. D. & Oosawa, F. Protein motors and Maxwell's demons: does mechanochemical transduction involve a thermal ratchet? Adv. Biophys. 26, 97-134 (1990).
28. Cleary, F. B. et al. Tension on the linker gates the ATP-dependent release of dynein from microtubules. Nat. Commun. 5, 4587 (2014).
29. Bissell, R. A., Córdova, E., Kaifer, A. E. & Stoddart, J. F. A chemically and electrochemically switchable molecular shuttle. Nature 369, 133-137 (1994).
30. Bath, J. & Turberfield, A. J.DNA nanomachines. Nat. Nanotech. 2, 275-284 (2007).
31. Reck-Peterson, S. L. et al. Single-molecule analysis of dynein processivity and stepping behavior. Cell 126, 335-348 (2006).
32. Jacob, F. Evolution and tinkering. Science 196, 1161-1166 (1977).
33. Uchimura, S. et al. A flipped ion pair at the dynein-microtubule interface is critical for dynein motility and ATPase activation. J. Cell Biol. 208, 211-222 (2015).
34. Baird, G. S., Zacharias, D. A. & Tsien, R. Y. Circular permutation and receptor insertion within Green fluorescent proteins. Proc. Natl Acad. Sci. USA 96, 11241-11246 (1999).
35. Martin, A., Baker, T. A. & Sauer, R. T. Rebuilt AAA + motors reveal operating principles for ATP-fuelled machines. Nature 437, 1115-1120 (2005).
36. Torisawa, T. et al. Autoinhibition and cooperative activation mechanisms of cytoplasmic dynein. Nat. Cell Biol. 16, 1118-1124 (2014).
37. Spudich, J. A. & Watt, S. The regulation of rabbit skeletal muscle contraction. I: biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871 (1971).
38. Herm-Gotz, A. et al. Toxoplasma gondii myosin A and its light chain: a fast, single-headed, plus-end-directed motor. EMBO J. 21, 2149-2158 (2002).
39. Perry, S. V. Myosin adenosine triphosphatase. Meth. Enzymol. 2, 582-588 (1955).
40. Hyman, A. A. Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence. J. Cell Sci. Suppl. 14, 125-127 (1991).
41. Suzuki, N., Miyata, H., Ishiwata, S. & Kinosita, K. Jr. Preparation of bead-tailed actin filaments: estimation of the torque produced by the sliding force in an in vitro motility assay. Biophys. J. 70, 401-408 (1996).
42. Furuta, K. et al. Measuring collective transport by defined numbers of processive and nonprocessive kinesin motors. Proc. Natl Acad. Sci. USA 110, 501-506 (2013).
43. Edelstein, A., Amodaj, N., Hoover, K., Vale, R. & Stuurman, N. Computer control of microscopes using ?Manager. Curr. Protoc. Mol. Biol. 92, 14.20.1-14.20.17 (2010).