Functions and mechanics of dynein motor proteins (original) (raw)

• Moughamian, A. J. & Holzbaur, E. in Dyneins: Structure, Biology and Disease (ed. King, S. M) 584–601 (Elsevier Inc., 2011).
• Fliegauf, M., Benzing, T. & Omran, H. When cilia go bad: cilia defects and ciliopathies. Nature Rev. Mol. Cell Biol. 8, 880–893 (2007).
  Article CAS Google Scholar
• Gibbons, I. R. Studies on the protein components of cilia from Tetrahymena pyriformis. Proc. Natl Acad. Sci. USA 50, 1002–1010 (1963).
  Article CAS PubMed PubMed Central Google Scholar
• Gibbons, I. & Rowe, A. Dynein: a protein with adenosine triphosphatase activity from cilia. Science 149, 424–426 (1965). References 3 and 4 mark the discovery of dynein motor proteins.
  Article CAS PubMed Google Scholar
• Paschal, B. M., Shpetner, H. S. & Vallee, R. B. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol. 105, 1273–1282 (1987). Describes the isolation and characterization of cytoplasmic dynein.
  Article CAS PubMed Google Scholar
• Paschal, B. M. & Vallee, R. B. Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330, 181–183 (1987).
  Article CAS PubMed Google Scholar
• Schroer, T. A., Steuer, E. R. & Sheetz, M. P. Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell 56, 937–946 (1989).
  Article CAS PubMed Google Scholar
• Vale, R. D., Reese, T. S. & Sheetz, M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39–50 (1985).
  Article PubMed PubMed Central CAS Google Scholar
• Vale, R. D. & Milligan, R. A. The way things move: looking under the hood of molecular motor proteins. Science 288, 88–95 (2000).
  Article CAS PubMed Google Scholar
• Billington, N. & Sellers, J. R. Dynein struts its stuff. Nature Struct. Mol. Biol. 18, 635–636 (2011).
  Article CAS Google Scholar
• Neuwald, A. F., Aravind, L., Spouge, J. L. & Koonin, E. V. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27–43 (1999).
  CAS PubMed Google Scholar
• Vallee, R. B., McKenney, R. J. & Ori-McKenney, K. M. Multiple modes of cytoplasmic dynein regulation. Nature Cell Biol. 14, 224–230 (2012).
  Article CAS PubMed Google Scholar
• Kardon, J. & Vale, R. Regulators of the cytoplasmic dynein motor. Nature Rev. Mol. Cell Biol. 10, 854–865 (2009).
  Article CAS Google Scholar
• Allan, V. J. Cytoplasmic dynein. Biochem. Soc. Trans. 39, 1169–1178 (2011).
  Article CAS PubMed Google Scholar
• Akhmanova, A. & Hammer, J. A. 3rd. Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 22, 479–487 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Riedel-Kruse, I. H., Hilfinger, A., Howard, J. & Jülicher, F. How molecular motors shape the flagellar beat. HFSP J. 1, 192–208 (2007).
  Article PubMed PubMed Central Google Scholar
• Brokaw, C. Thinking about flagellar oscillation. Cell. Motil. Cytoskeleton 66, 425–436 (2009).
  Article CAS PubMed Google Scholar
• Lindemann, C. B. & Lesich, K. A. Flagellar and ciliary beating: the proven and the possible. J. Cell Sci. 123, 519–528 (2010).
  Article CAS PubMed Google Scholar
• King, S. M. Integrated control of axonemal dynein AAA+ motors. J. Struct. Biol. 179, 222–228 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Wickstead, B. & Gull, K. Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8, 1708–1721 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Vale, R. D. The molecular motor toolbox for intracellular transport. Cell 112, 467–480 (2003).
  Article CAS PubMed Google Scholar
• Yagi, T. Bioinformatic approaches to dynein heavy chain classification. Methods Cell Biol. 92, 1–9 (2009).
  Article CAS PubMed Google Scholar
• Moore, J., Stuchell-Brereton, M. & Cooper, J. Function of dynein in budding yeast: mitotic spindle positioning in a polarized cell. Cell. Motil. Cytoskeleton 66, 546–555 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Egan, M. J., McClintock, M. A. & Reck-Peterson, S. L. Microtubule-based transport in filamentous fungi. Curr. Opin. Microbiol. 15, 637–645 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Koonce, M. P. Dictyostelium, a model organism for microtubule-based transport. Protist 151, 17–25 (2000).
  Article CAS PubMed Google Scholar
• Pfister, K. K. et al. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet. 2, e1 (2006).
  Article PubMed PubMed Central CAS Google Scholar
• Trokter, M., Mücke, N. & Surrey, T. Reconstitution of the human cytoplasmic dynein complex. Proc. Natl Acad. Sci. USA 109, 20895–20900 (2012). Describes the reconstitution of the human cytoplasmic dynein complex from recombinant subunits. Surprisingly, despite driving robust microtubule gliding, the complexes do not show processive motility, suggesting that additional factors might be required for this behaviour.
  Article CAS PubMed PubMed Central Google Scholar
• Schroer, T. A. Dynactin. Annu. Rev. Cell Dev. Biol. 20, 759–779 (2004).
  Article CAS PubMed Google Scholar
• Driskell, O. J., Mironov, A., Allan, V. J. & Woodman, P. G. Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nature Cell Biol. 9, 113–120 (2007).
  Article CAS PubMed Google Scholar
• Jordens, I. et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680–1685 (2001).
  Article CAS PubMed Google Scholar
• Blocker, A. et al. Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137, 113–129 (1997).
  Article PubMed PubMed Central CAS Google Scholar
• Gross, S. P. et al. Interactions and regulation of molecular motors in Xenopus melanophores. J. Cell Biol. 156, 855–865 (2002).
  Article PubMed PubMed Central CAS Google Scholar
• Kural, C. et al. Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308, 1469–1472 (2005).
  Article CAS PubMed Google Scholar
• Gross, S. P., Welte, M. A., Block, S. M. & Wieschaus, E. F. Dynein-mediated cargo transport in vivo. A switch controls travel distance. J. Cell Biol. 148, 945–956 (2000).
  Article PubMed PubMed Central CAS Google Scholar
• Pilling, A. D., Horiuchi, D., Lively, C. M. & Saxton, W. M. Kinesin-1 and dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell 17, 2057–2068 (2006).
  Article PubMed PubMed Central CAS Google Scholar
• Presley, J. F. et al. ER-to-Golgi transport visualized in living cells. Nature 389, 81–85 (1997).
  Article CAS PubMed Google Scholar
• Heerssen, H. M., Pazyra, M. F. & Segal, R. A. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nature Neurosci. 7, 596–604 (2004).
  Article CAS PubMed Google Scholar
• Young, A., Dictenberg, J. B., Purohit, A., Tuft, R. & Doxsey, S. J. Cytoplasmic dynein-mediated assembly of pericentrin and gamma tubulin onto centrosomes. Mol. Biol. Cell 11, 2047–2056 (2000).
  Article PubMed PubMed Central CAS Google Scholar
• Harrell, J. M. et al. Evidence for glucocorticoid receptor transport on microtubules by dynein. J. Biol. Chem. 279, 54647–54654 (2004).
  Article CAS PubMed Google Scholar
• Shah, J. V., Flanagan, L. A., Janmey, P. A. & Leterrier, J. F. Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol. Biol. Cell 11, 3495–3508 (2000).
  Article PubMed PubMed Central CAS Google Scholar
• Wilkie, G. S. & Davis, I. Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell 105, 209–219 (2001).
  Article CAS PubMed Google Scholar
• Johnston, J. A., Illing, M. E. & Kopito, R. R. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell. Motil. Cytoskeleton 53, 26–38 (2002).
  Article CAS PubMed Google Scholar
• Maday, S., Wallace, K. E. & Holzbaur, E. L. F. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J. Cell Biol. 196, 407–417 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Dodding, M. P. & Way, M. Coupling viruses to dynein and kinesin-1. EMBO J. 30, 3527–3539 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Sato, A. et al. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139, 907–919 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Steinberg, G. et al. Motor-driven motility of fungal nuclear pores organizes chromosomes and fosters nucleocytoplasmic transport. J. Cell Biol. 198, 343–355 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Schnyder, T. et al. B cell receptor-mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok-3 to recruit dynein to the signaling microcluster. Immunity 34, 905–918 (2011).
  Article CAS PubMed Google Scholar
• Hashimoto-Tane, A. et al. Dynein-driven transport of T cell receptor microclusters regulates immune synapse formation and T cell activation. Immunity 34, 919–931 (2011).
  Article CAS PubMed Google Scholar
• Laan, L. et al. Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters. Cell 148, 502–514 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Hendricks, A. G. et al. Dynein tethers and stabilizes dynamic microtubule plus ends. Curr. Biol. 22, 632–637 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Tsai, J.-W., Bremner, K. H. & Vallee, R. B. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nature Neurosci. 10, 970–979 (2007).
  Article CAS PubMed Google Scholar
• Dujardin, D. L. et al. A role for cytoplasmic dynein and LIS1 in directed cell movement. J. Cell Biol. 163, 1205–1211 (2003).
  Article PubMed PubMed Central CAS Google Scholar
• Combs, J. et al. Recruitment of dynein to the Jurkat immunological synapse. Proc. Natl Acad. Sci. USA 103, 14883–14888 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• McNally, F. J. Mechanisms of spindle positioning. J. Cell Biol. 200, 131–140 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Kiyomitsu, T. & Cheeseman, I. M. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nature Cell Biol. 14, 311–317 (2012).
  Article CAS PubMed Google Scholar
• Collins, E. S., Balchand, S. K., Faraci, J. L., Wadsworth, P. & Lee, W.-L. Cell cycle-regulated cortical dynein/dynactin promotes symmetric cell division by differential pole motion in anaphase. Mol. Biol. Cell 23, 3380–3390 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Mitchison, T. et al. Growth, interaction, and positioning of microtubule asters in extremely large vertebrate embryo cells. Cytoskeleton (Hoboken) 69, 738–750 (2012).
  Article CAS Google Scholar
• Kimura, K. & Kimura, A. Intracellular organelles mediate cytoplasmic pulling force for centrosome centration in the Caenorhabditis elegans early embryo. Proc. Natl Acad. Sci. USA 108, 137–142 (2011).
  Article CAS PubMed Google Scholar
• Longoria, R. A. & Shubeita, G. T. Cargo transport by cytoplasmic dynein can center embryonic centrosomes. PLoS ONE 8, e67710 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Corthesy-Theulaz, I., Pauloin, A. & Pfeffer, S. R. Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol. 118, 1333–1345 (1992).
  Article CAS PubMed Google Scholar
• Levy, J. R. & Holzbaur, E. L. Dynein drives nuclear rotation during forward progression of motile fibroblasts. J. Cell Sci. 121, 3187–3195 (2008).
  Article PubMed CAS Google Scholar
• Raaijmakers, J. A. et al. Nuclear envelope-associated dynein drives prophase centrosome separation and enables Eg5-independent bipolar spindle formation. EMBO J. 31, 4179–4190 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Salina, D. et al. Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108, 97–107 (2002).
  Article CAS PubMed Google Scholar
• Heald, R. et al. Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382, 420–425 (1996).
  Article CAS PubMed Google Scholar
• Merdes, A., Ramyar, K., Vechio, J. D. & Cleveland, D. W. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87, 447–458 (1996).
  Article CAS PubMed Google Scholar
• Foley, E. A. & Kapoor, T. M. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nature Rev. Mol. Cell Biol. 14, 25–37 (2012).
  Article CAS Google Scholar
• Howell, B. J. et al. Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J. Cell Biol. 155, 1159–1172 (2001).
  Article PubMed PubMed Central CAS Google Scholar
• Wojcik, E. et al. Kinetochore dynein: its dynamics and role in the transport of the Rough deal checkpoint protein. Nature Cell Biol. 3, 1001–1007 (2001).
  Article CAS PubMed Google Scholar
• Varma, D., Monzo, P., Stehman, S. A. & Vallee, R. B. Direct role of dynein motor in stable kinetochore–microtubule attachment, orientation, and alignment. J. Cell Biol. 182, 1045–1054 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Yang, Z., Tulu, U. S., Wadsworth, P. & Rieder, C. L. Kinetochore dynein is required for chromosome motion and congression independent of the spindle checkpoint. Curr. Biol. 17, 973–980 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Ishikawa, H. & Marshall, W. F. Ciliogenesis: building the cell's antenna. Nature Rev. Mol. Cell Biol. 12, 222–234 (2011).
  Article CAS Google Scholar
• 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, 473–481 (1999).
  Article PubMed PubMed Central CAS Google Scholar
• 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, 693–712 (1999).
  Article PubMed PubMed Central CAS Google Scholar
• Mikami, A. et al. Molecular structure of cytoplasmic dynein 2 and its distribution in neuronal and ciliated cells. J. Cell Sci. 115, 4801–4808 (2002).
  Article CAS PubMed Google Scholar
• Perrone, C. A. et al. A novel dynein light intermediate chain colocalizes with the retrograde motor for intraflagellar transport at sites of axoneme assembly in Chlamydomonas and mammalian cells. Mol. Biol. Cell 14, 2041–2056 (2003).
  Article PubMed PubMed Central CAS Google Scholar
• Ichikawa, M., Watanabe, Y., Murayama, T. & Toyoshima, Y. Y. Recombinant human cytoplasmic dynein heavy chain 1 and 2: observation of dynein-2 motor activity in vitro. FEBS Lett. 585, 2419–2423 (2011).
  Article CAS PubMed Google Scholar
• Pigino, G. et al. Electron-tomographic analysis of intraflagellar transport particle trains in situ. J. Cell Biol. 187, 135–148 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Laib, J. A., Marin, J. A., Bloodgood, R. A. & Guilford, W. H. The reciprocal coordination and mechanics of molecular motors in living cells. Proc. Natl Acad. Sci. USA 106, 3190–3195 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Shih, S. M. et al. Intraflagellar transport drives flagellar surface motility. Elife 2, e00744 (2013).
  Article PubMed PubMed Central Google Scholar
• Mallik, R., Rai, A. K., Barak, P., Rai, A. & Kunwar, A. Teamwork in microtubule motors. Trends Cell Biol. http://dx.doi.org/10.1016/j.tcb.2013.06.003 (2013).
• Koonce, M. P. & Samsó, M. Overexpression of cytoplasmic dynein's globular head causes a collapse of the interphase microtubule network in Dictyostelium. Mol. Biol. Cell 7, 935–948 (1996). Details a recombinant expression system for the D. discoideum cytoplasmic dynein motor domain, forming the foundation for numerous structural and functional analyses. Also demonstrates that the motor domain includes the globular head structure seen in earlier electron microscopy images.
  Article PubMed PubMed Central CAS Google Scholar
• Nishiura, M. et al. A single-headed recombinant fragment of Dictyostelium cytoplasmic dynein can drive the robust sliding of microtubules. J. Biol. Chem. 279, 22799–22802 (2004).
  Article CAS PubMed Google Scholar
• Reck-Peterson, S. L. et al. Single-molecule analysis of dynein processivity and stepping behavior. Cell 126, 335–348 (2006). Establishes S. cerevisiae as another important cytoplasmic dynein expression system and provides insight into the requirements for processive dynein motion.
  Article PubMed PubMed Central CAS Google Scholar
• Höök, P. et al. Long range allosteric control of cytoplasmic dynein ATPase activity by the stalk and C-terminal domains. J. Biol. Chem. 280, 33045–33054 (2005).
  Article CAS PubMed Google Scholar
• Imamula, K., Kon, T., Ohkura, R. & Sutoh, K. The coordination of cyclic microtubule association/dissociation and tail swing of cytoplasmic dynein. Proc. Natl Acad. Sci. USA 104, 16134–16139 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Mogami, T., Kon, T., Ito, K. & Sutoh, K. Kinetic characterization of tail swing steps in the ATPase cycle of Dictyostelium cytoplasmic dynein. J. Biol. Chem. 282, 21639–21644 (2007).
  Article CAS PubMed Google Scholar
• Johnson, K. A. Pathway of the microtubule–dynein ATPase and the structure of dynein: a comparison with actomyosin. Annu. Rev. Biophys. Biophys. Chem. 14, 161–188 (1985).
  Article CAS PubMed Google Scholar
• Samsó, M., Radermacher, M., Frank, J. & Koonce, M. P. Structural characterization of a dynein motor domain. J. Mol. Biol. 276, 927–937 (1998).
  Article PubMed Google Scholar
• Gee, M. A., Heuser, J. E. & Vallee, R. B. An extended microtubule-binding structure within the dynein motor domain. Nature 390, 636–639 (1997).
  Article CAS PubMed Google Scholar
• Roberts, A. J. et al. ATP-driven remodeling of the linker domain in the dynein motor. Structure 20, 1670–1680 (2012). A 2D and 3D electron microscopy study of an axonemal and cytoplasmic dynein, revealing that the linker domain is a stable structural entity that is remodelled by the AAA+ ring.
  Article PubMed PubMed Central CAS Google Scholar
• Roberts, A. et al. AAA+ ring and linker swing mechanism in the dynein motor. Cell 136, 485–495 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Burgess, S. A., Walker, M. L., Sakakibara, H., Knight, P. J. & Oiwa, K. Dynein structure and power stroke. Nature 421, 715–718 (2003).
  Article CAS PubMed Google Scholar
• Kon, T. et al. The 2.8 Å crystal structure of the dynein motor domain. Nature 484, 345–350 (2012). Reports a high-resolution crystal structure of the D. discoideum dynein motor domain in the ADP-bound state. Structure-guided mutagenesis provides insight into how the linker domain moves and the roles of the AAA+ modules, strut and C-terminal sequence in allosteric communication.
  Article CAS PubMed Google Scholar
• Kon, T., Sutoh, K. & Kurisu, G. X-ray structure of a functional full-length dynein motor domain. Nature Struct. Mol. Biol. 18, 638–642 (2011).
  Article CAS Google Scholar
• Schmidt, H., Gleave, E. S. & Carter, A. P. Insights into dynein motor domain function from a 3.3-Å crystal structure. Nature Struct. Mol. Biol. 19, 492–497 (2012). Reports a high-resolution structure of the S. cerevisiae dynein motor domain, crystallized in the absence of nucleotide. Crystal-soaking experiments reveal distinct nucleotide-binding behaviours in AAA1–AAA4, and mutagenesis suggests a functional role for linker docking at AAA5.
  Article CAS Google Scholar
• Carter, A. P., Cho, C., Jin, L. & Vale, R. D. Crystal structure of the dynein motor domain. Science 331, 1159–1165 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Glynn, S. E., Martin, A., Nager, A. R., Baker, T. A. & Sauer, R. T. Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139, 744–756 (2009).
  Article PubMed PubMed Central CAS Google Scholar
• Wang, J. et al. Nucleotide-dependent conformational changes in a protease-associated ATPase HsIU. Structure 9, 1107–1116 (2001).
  Article CAS PubMed Google Scholar
• Gibbons, I. R. et al. 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 (1987).
  CAS PubMed Google Scholar
• Kon, T., Nishiura, M., Ohkura, R., Toyoshima, Y. Y. & Sutoh, K. Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein. Biochemistry 43, 11266–11274 (2004).
  Article CAS PubMed Google Scholar
• Enemark, E. J. & Joshua-Tor, L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442, 270–275 (2006).
  Article CAS PubMed Google Scholar
• Cho, C., Reck-Peterson, S. & Vale, R. Cytoplasmic dynein's regulatory ATPase sites affect processivity and force generation. J. Biol. Chem. 283, 25839–25845 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Huang, J., Roberts, A. J., Leschziner, A. E. & Reck-Peterson, S. L. Lis1 acts as a “clutch” between the ATPase and microtubule-binding domains of the dynein motor. Cell 150, 975–986 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• McKenney, R. J., Vershinin, M., Kunwar, A., Vallee, R. B. & Gross, S. P. LIS1 and NudE induce a persistent dynein force-producing state. Cell 141, 304–314 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• Yamada, M. et al. LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J. 27, 2471–2483 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Cho, C. & Vale, R. D. The mechanism of dynein motility: insight from crystal structures of the motor domain. Biochim. Biophys. Acta 1823, 182–191 (2011).
  Article PubMed PubMed Central CAS Google Scholar
• Numata, N., Shima, T., Ohkura, R., Kon, T. & Sutoh, K. C-Sequence of the Dictyostelium cytoplasmic dynein participates in processivity modulation. FEBS Lett. 585, 1185–1190 (2011).
  Article CAS PubMed Google Scholar
• Hwang, W. & Lang, M. J. Nucleotide-dependent control of internal strains in ring-shaped AAA+ motors. Cell. Mol. Bioeng. 6, 65–73 (2013).
  Article CAS PubMed Google Scholar
• 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).
  Article PubMed CAS Google Scholar
• Carter, A. P. et al. Structure and functional role of dynein's microtubule-binding domain. Science 322, 1691–1695 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Kon, T. et al. Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nature Struct. Mol. Biol. 16, 325–333 (2009).
  Article CAS Google Scholar
• Redwine, W. B. et al. Structural basis for microtubule binding and release by dynein. Science 337, 1532–1536 (2012). References 109–112 provide evidence for the helix-sliding hypothesis for allosteric communication through the stalk of dynein, which was put forward in reference 109. Reference 112 also provides insight into the structural changes within the microtubule-binding domain of dynein.
  Article PubMed PubMed Central CAS Google Scholar
• Sweeney, H. L. & Houdusse, A. The motor mechanism of myosin V: insights for muscle contraction. Philo. Trans. R. Soc. Lond. B 359, 1829–1841 (2004).
  Article CAS Google Scholar
• Xi, Z., Gao, Y., Sirinakis, G., Guo, H. & Zhang, Y. Single-molecule observation of helix staggering, sliding, and coiled coil misfolding. Proc. Natl Acad. Sci. USA 109, 5711–5716 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Burgess, S. A., Walker, M. L., Sakakibara, H., Oiwa, K. & Knight, P. J. The structure of dynein-c by negative stain electron microscopy. J. Struct. Biol. 146, 205–216 (2004).
  Article CAS PubMed Google Scholar
• Burgess, S. A. & Knight, P. J. Is the dynein motor a winch? Curr. Opin. Struct. Biol. 14, 138–146 (2004).
  Article CAS PubMed Google Scholar
• Gennerich, A., Carter, A. P., Reck-Peterson, S. L. & Vale, R. D. Force-induced bidirectional stepping of cytoplasmic dynein. Cell 131, 952–965 (2007).
  Article PubMed PubMed Central CAS Google Scholar
• Kon, T., Mogami, T., Ohkura, R., Nishiura, M. & Sutoh, K. ATP hydrolysis cycle-dependent tail motions in cytoplasmic dynein. Nature Struct. Mol. Biol. 12, 513–519 (2005).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Ueno, H., Yasunaga, T., Shingyoji, C. & Hirose, K. Dynein pulls microtubules without rotating its stalk. Proc. Natl Acad. Sci. USA 105, 19702–19707 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Movassagh, T., Bui, K. H., Sakakibara, H., Oiwa, K. & Ishikawa, T. Nucleotide-induced global conformational changes of flagellar dynein arms revealed by in situ analysis. Nature Struct. Mol. Biol. 17, 761–767 (2010).
  Article CAS Google Scholar
• Qiu, W. et al. Dynein achieves processive motion using both stochastic and coordinated stepping. Nature Struct. Mol. Biol. 19, 193–200 (2012).
  Article CAS Google Scholar
• Dewitt, M. A., Chang, A. Y., Combs, P. A. & Yildiz, A. Cytoplasmic dynein moves through uncoordinated stepping of the AAA+ ring domains. Science 335, 221–225 (2011). References 122 and 123 use two-colour single-molecule experiments to reveal that S. cerevisiae cytoplasmic dynein dimers can move processively along the microtubule without following a strict stepping pattern. Analysis of the stepping traces provides insight into the spatial configuration of the motor domains and their loose, tension-based coordination.
  Article PubMed PubMed Central CAS Google Scholar
• Veigel, C., Wang, F., Bartoo, M. L., Sellers, J. R. & Molloy, J. E. The gated gait of the processive molecular motor, myosin V. Nature Cell Biol. 4, 59–65 (2002).
  Article CAS PubMed Google Scholar
• Shima, T., Imamula, K., Kon, T., Ohkura, R. & Sutoh, K. Head-head coordination is required for the processive motion of cytoplasmic dynein, an AAA+ molecular motor. J. Struct. Biol. 156, 182–189 (2006).
  Article CAS PubMed Google Scholar
• Stinson, B. M. et al. Nucleotide binding and conformational switching in the hexameric ring of a AAA+ machine. Cell 153, 628–639 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Sakamoto, T., Webb, M. R., Forgacs, E., White, H. D. & Sellers, J. R. Direct observation of the mechanochemical coupling in myosin Va during processive movement. Nature 455, 128–132 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Firestone, A. J. et al. Small-molecule inhibitors of the AAA+ ATPase motor cytoplasmic dynein. Nature 484, 125–129 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Kamiya, R. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int. Rev. Cytol. 219, 115–155 (2002).
  Article CAS PubMed Google Scholar
• Kikushima, K. & Kamiya, R. Clockwise translocation of microtubules by flagellar inner-arm dyneins in vitro. Biophys. J. 94, 4014–4019 (2008).
  Article PubMed PubMed Central CAS Google Scholar
• Mallik, R., Carter, B. C., Lex, S. A., King, S. J. & Gross, S. P. Cytoplasmic dynein functions as a gear in response to load. Nature 427, 649–652 (2004).
  Article CAS PubMed Google Scholar
• Rai, A. K., Rai, A., Ramaiya, A. J., Jha, R. & Mallik, R. Molecular adaptations allow dynein to generate large collective forces inside cells. Cell 152, 172–182 (2013).
  Article CAS PubMed Google Scholar
• Schroeder, H. W., Mitchell, C., Shuman, H., Holzbaur, E. L. F. & Goldman, Y. E. Motor number controls cargo switching at actin-microtubule intersections in vitro. Curr. Biol. 20, 687–696 (2010).
  Article CAS PubMed Google Scholar
• Toba, S., Watanabe, T. M., Yamaguchi-Okimoto, L., Toyoshima, Y. Y. & Higuchi, H. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. Proc. Natl Acad. Sci. USA 103, 5741–5745 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Walter, W. J., Koonce, M. P., Brenner, B. & Steffen, W. Two independent switches regulate cytoplasmic dynein's processivity and directionality. Proc. Natl Acad. Sci. USA 109, 5289–5293 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Ross, J. L., Wallace, K., Shuman, H., Goldman, Y. E. & Holzbaur, E. L. F. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nature Cell Biol. 8, 562–570 (2006).
  Article CAS PubMed Google Scholar
• Ananthanarayanan, V. et al. Dynein motion switches from diffusive to directed upon cortical anchoring. Cell 153, 1526–1536 (2013).
  Article CAS PubMed Google Scholar
• Nicastro, D. et al. Cryo-electron tomography reveals conserved features of doublet microtubules in flagella. Proc. Natl Acad. Sci. USA 108, E845–E853 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Summers, K. E. & Gibbons, I. R. Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc. Natl Acad. Sci. USA 68, 3092–3096 (1971).
  Article CAS PubMed PubMed Central Google Scholar
• Nicastro, D. Cryo-electron microscope tomography to study axonemal organization. Methods Cell Biol. 91, 1–39 (2009).
  Article CAS PubMed Google Scholar
• Hom, E. F. et al. A unified taxonomy for ciliary dyneins. Cytoskeleton (Hoboken) 68, 555–565 (2011).
  Article CAS Google Scholar
• Bui, K. H., Yagi, T., Yamamoto, R., Kamiya, R. & Ishikawa, T. Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. J. Cell Biol. 198, 913–925 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Kagami, O. & Kamiya, R. Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J. Cell Sci. 103, 653–664 (1992).
  CAS Google Scholar
• Yagi, T., Uematsu, K., Liu, Z. & Kamiya, R. Identification of dyneins that localize exclusively to the proximal portion of Chlamydomonas flagella. J. Cell Sci. 122, 1306–1314 (2009).
  Article CAS PubMed Google Scholar
• Woolley, D. M. Studies on the eel sperm flagellum. I. The structure of the inner dynein arm complex. J. Cell Sci. 110, 85–94 (1997).
  CAS PubMed Google Scholar
• Zhang, X. & Wigley, D. The 'glutamate switch' provides a link between ATPase activity and ligand binding in AAA+ proteins. Nature Struct. Mol. Biol. 15, 1223–1227 (2008).
  Article CAS Google Scholar
• Hanson, P. I. & Whiteheart, S. W. AAA+ proteins: have engine, will work. Nature Rev. Mol. Cell Biol. 6, 519–529 (2005).
  Article CAS Google Scholar
• Pfister, K. K. et al. Cytoplasmic dynein nomenclature. J. Cell Biol. 171, 411–413 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Mizuno, N. et al. Dynein and kinesin share an overlapping microtubule-binding site. EMBO J. 23, 2459–2467 (2004).
  Article PubMed PubMed Central CAS Google Scholar