1932

Abstract

Until recently, dynein was the least understood of the cytoskeletal motors. However, a wealth of new structural, mechanistic, and cell biological data is shedding light on how this complicated minus-end-directed, microtubule-based motor works. Cytoplasmic dynein-1 performs a wide array of functions in most eukaryotes, both in interphase, in which it transports organelles, proteins, mRNAs, and viruses, and in mitosis and meiosis. Mutations in dynein or its regulators are linked to neurodevelopmental and neurodegenerative diseases. Here, we begin by providing a synthesis of recent data to describe the current model of dynein's mechanochemical cycle. Next, we discuss regulators of dynein, with particular focus on those that directly interact with the motor to modulate its recruitment to microtubules, initiate cargo transport, or activate minus-end-directed motility.

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2015-11-13
2024-06-18
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Literature Cited

  1. Allan VJ. 2011. Cytoplasmic dynein. Biochem. Soc. Trans. 39:1169–78 [Google Scholar]
  2. Ananthanarayanan V, Schattat M, Vogel SK, Krull A, Pavin N, Tolic-Norrelykke IM. 2013. Dynein motion switches from diffusive to directed upon cortical anchoring. Cell 153:1526–36 [Google Scholar]
  3. Ayloo S, Lazarus JE, Dodda A, Tokito M, Ostap EM, Holzbaur EL. 2014. Dynactin functions as both a dynamic tether and brake during dynein-driven motility. Nat. Commun. 5:4807 [Google Scholar]
  4. Bader JR, Vaughan KT. 2010. Dynein at the kinetochore: timing, interactions, and functions. Semin. Cell Dev. Biol. 21:269–75 [Google Scholar]
  5. Baetz NW, Goldenring JR. 2013. Rab11-family interacting proteins define spatially and temporally distinct regions within the dynamic Rab11a-dependent recycling system. Mol. Biol. Cell 24:643–58 [Google Scholar]
  6. Barisic M, Geley S. 2011. Spindly switch controls anaphase: Spindly and RZZ functions in chromosome attachment and mitotic checkpoint control. Cell Cycle 10:449–56 [Google Scholar]
  7. Baron Gaillard CL, Pallesi-Pocachard E, Massey-Harroche D, Richard F, Arsanto JP. et al. 2011. Hook2 is involved in the morphogenesis of the primary cilium. Mol. Biol. Cell 22:4549–62 [Google Scholar]
  8. Bhabha G, Cheng HC, Zhang N, Moeller A, Liao M. et al. 2014. Allosteric communication in the Dynein motor domain. Cell 159:857–68 [Google Scholar]
  9. Bianco A, Dienstbier M, Salter HK, Gatto G, Bullock SL. 2010. Bicaudal-D regulates fragile X mental retardation protein levels, motility, and function during neuronal morphogenesis. Curr. Biol. 20:1487–92 [Google Scholar]
  10. Bielska E, Schuster M, Roger Y, Berepiki A, Soanes DM. et al. 2014. Hook is an adapter that coordinates kinesin-3 and dynein cargo attachment on early endosomes. J. Cell Biol. 204:989–1007 [Google Scholar]
  11. Bradshaw NJ, Hennah W, Soares DC. 2013. NDE1 and NDEL1: twin neurodevelopmental proteins with similar ‘nature’ but different ‘nurture.’. Biomol. Concepts 4:447–64 [Google Scholar]
  12. Bullock SL, Nicol A, Gross SP, Zicha D. 2006. Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity. Curr. Biol. 16:1447–52 [Google Scholar]
  13. Burgess SA, Walker ML, Sakakibara H, Knight PJ, Oiwa K. 2003. Dynein structure and power stroke. Nature 421:715–8 [Google Scholar]
  14. Carter AP, Cho C, Jin L, Vale RD. 2011. Crystal structure of the dynein motor domain. Science 331:1159–65 [Google Scholar]
  15. Carter AP, Garbarino JE, Wilson-Kubalek EM, Shipley WE, Cho C. et al. 2008. Structure and functional role of dynein's microtubule-binding domain. Science 322:1691–5 [Google Scholar]
  16. Carvalho P, Gupta ML Jr, Hoyt MA, Pellman D. 2004. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev. Cell 6:815–29 [Google Scholar]
  17. Caudron F, Andrieux A, Job D, Boscheron C. 2008. A new role for kinesin-directed transport of Bik1p (CLIP-170) in Saccharomyces cerevisiae. J. Cell Sci. 121:1506–13 [Google Scholar]
  18. Chan YW, Fava LL, Uldschmid A, Schmitz MH, Gerlich DW. et al. 2009. Mitotic control of kinetochore-associated dynein and spindle orientation by human Spindly. J. Cell Biol. 185:859–74 [Google Scholar]
  19. Cho C, Reck-Peterson SL, Vale RD. 2008. Regulatory ATPase sites of cytoplasmic dynein affect processivity and force generation. J. Biol. Chem. 283:25839–45 [Google Scholar]
  20. Chowdhury S, Ketcham SA, Schroer TA, Lander GC. 2015. Structural organization of the dynein-dynactin complex bound to microtubules. Nat. Struct. Mol. Biol. 22:345–47 [Google Scholar]
  21. Cockell MM, Baumer K, Gonczy P. 2004. lis-1 is required for dynein-dependent cell division processes in C. elegans embryos. J. Cell Sci. 117:4571–82 [Google Scholar]
  22. Coutelis JB, Ephrussi A. 2007. Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 134:1419–30 [Google Scholar]
  23. Culver-Hanlon TL, Lex SA, Stephens AD, Quintyne NJ, King SJ. 2006. A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat. Cell Biol. 8:264–70 [Google Scholar]
  24. Deacon SW, Serpinskaya AS, Vaughan PS, Lopez Fanarraga M, Vernos I. et al. 2003. Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160:297–301 [Google Scholar]
  25. DeWitt MA, Chang AY, Combs PA, Yildiz A. 2012. Cytoplasmic dynein moves through uncoordinated stepping of the AAA+ ring domains. Science 335:221–25 [Google Scholar]
  26. DeWitt MA, Cypranowska CA, Cleary FB, Belyy V, Yildiz A. 2015. The AAA3 domain of cytoplasmic dynein acts as a switch to facilitate microtubule release. Nat. Struct. Mol. Biol. 22:73–80 [Google Scholar]
  27. Dix CI, Soundararajan HC, Dzhindzhev NS, Begum F, Suter B. et al. 2013. Lissencephaly-1 promotes the recruitment of dynein and dynactin to transported mRNAs. J. Cell Biol. 202:479–94 [Google Scholar]
  28. Dodding MP, Way M. 2011. Coupling viruses to dynein and kinesin-1. EMBO J. 30:3527–39 [Google Scholar]
  29. Duellberg C, Trokter M, Jha R, Sen I, Steinmetz MO, Surrey T. 2014. Reconstitution of a hierarchical +TIP interaction network controlling microtubule end tracking of dynein. Nat. Cell Biol. 16:804–11 [Google Scholar]
  30. Eckley DM, Melkonian KA, Bingham JB, Goodson HV, Heuser JE, Schroer TA. 1999. Analysis of dynactin subcomplexes reveals a novel actin-related protein associated with the Arp1 minifilament pointed end. J. Cell Biol. 147:307–20 [Google Scholar]
  31. Efimov VP. 2003. Roles of NUDE and NUDF proteins of Aspergillus nidulans: insights from intracellular localization and overexpression effects. Mol. Biol. Cell 14:871–88 [Google Scholar]
  32. Efimov VP, Morris NR. 2000. The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J. Cell Biol. 150:681–8 [Google Scholar]
  33. Egan MJ, McClintock MA, Hollyer IHL, Elliot HL, Reck-Peterson SL. 2015. Cytoplasmic dynein is required for the spatial organization of protein aggregates in filamentous fungi. Cell Rep. 11:201–9 [Google Scholar]
  34. Egan MJ, Tan K, Reck-Peterson SL. 2012. Lis1 is an initiation factor for dynein-driven organelle transport. J. Cell Biol. 197:971–82 [Google Scholar]
  35. Farrer MJ, Hulihan MM, Kachergus JM, Dachsel JC, Stoessl AJ. et al. 2009. DCTN1 mutations in Perry syndrome. Nat. Genet. 41:163–5 [Google Scholar]
  36. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O'Connell CB. et al. 2000. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2:784–91 [Google Scholar]
  37. Feng Y, Walsh CA. 2004. Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44:279–93 [Google Scholar]
  38. Fu MM, Holzbaur EL. 2014a. Integrated regulation of motor-driven organelle transport by scaffolding proteins. Trends Cell Biol. 24:564–74 [Google Scholar]
  39. Fu MM, Holzbaur EL. 2014b. MAPK8IP1/JIP1 regulates the trafficking of autophagosomes in neurons. Autophagy 10:2079–81 [Google Scholar]
  40. Gassmann R, Essex A, Hu JS, Maddox PS, Motegi F. et al. 2008. A new mechanism controlling kinetochore-microtubule interactions revealed by comparison of two dynein-targeting components: SPDL-1 and the Rod/Zwilch/Zw10 complex. Genes Dev. 22:2385–99 [Google Scholar]
  41. Gassmann R, Holland AJ, Varma D, Wan X, Civril F. et al. 2010. Removal of Spindly from microtubule-attached kinetochores controls spindle checkpoint silencing in human cells. Genes Dev. 24:957–71 [Google Scholar]
  42. Gee MA, Heuser JE, Vallee RB. 1997. An extended microtubule-binding structure within the dynein motor domain. Nature 390:636–9 [Google Scholar]
  43. Gennerich A, Carter AP, Reck-Peterson SL, Vale RD. 2007. Force-induced bidirectional stepping of cytoplasmic dynein. Cell 131:952–65 [Google Scholar]
  44. Gibbons IR, Garbarino JE, Tan CE, Reck-Peterson SL, Vale RD, Carter AP. 2005. The affinity of the dynein microtubule-binding domain is modulated by the conformation of its coiled-coil stalk. J. Biol. Chem. 280:23960–5 [Google Scholar]
  45. Gibbons IR, Lee-Eiford A, Mocz G, Phillipson CA, Tang WJ, Gibbons BH. 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. 262:2780–6 [Google Scholar]
  46. Gill SR, Schroer TA, Szilak I, Steuer ER, Sheetz MP, Cleveland DW. 1991. Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol. 115:1639–50 [Google Scholar]
  47. Goodenough U, Heuser J. 1984. Structural comparison of purified dynein proteins with in situ dynein arms. J. Mol. Biol. 180:1083–118 [Google Scholar]
  48. Greber UF, Way M. 2006. A superhighway to virus infection. Cell 124:741–54 [Google Scholar]
  49. Griffis ER, Stuurman N, Vale RD. 2007. Spindly, a novel protein essential for silencing the spindle assembly checkpoint, recruits dynein to the kinetochore. J. Cell Biol. 177:1005–15 [Google Scholar]
  50. Gumy LF, Katrukha EA, Kapitein LC, Hoogenraad CC. 2014. New insights into mRNA trafficking in axons. Dev. Neurobiol. 74:233–44 [Google Scholar]
  51. Harada A, Takei Y, Kanai Y, Tanaka Y, Nonaka S, Hirokawa N. 1998. Golgi vesiculation and lysosome dispersion in cells lacking cytoplasmic dynein. J. Cell Biol. 141:51–9 [Google Scholar]
  52. Harms MB, Ori-McKenney KM, Scoto M, Tuck EP, Bell S. et al. 2012. Mutations in the tail domain of DYNC1H1 cause dominant spinal muscular atrophy. Neurology 78:1714–20 [Google Scholar]
  53. Hebbar S, Mesngon MT, Guillotte AM, Desai B, Ayala R, Smith DS. 2008. Lis1 and Ndel1 influence the timing of nuclear envelope breakdown in neural stem cells. J. Cell Biol. 182:1063–71 [Google Scholar]
  54. Holt CE, Bullock SL. 2009. Subcellular mRNA localization in animal cells and why it matters. Science 326:1212–6 [Google Scholar]
  55. Hoogenraad CC, Akhmanova A, Howell SA, Dortland BR, De Zeeuw CI. et al. 2001. Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J. 20:4041–54 [Google Scholar]
  56. Hoogenraad CC, Wulf P, Schiefermeier N, Stepanova T, Galjart N. et al. 2003. Bicaudal D induces selective dynein-mediated microtubule minus end–directed transport. EMBO J. 22:6004–15 [Google Scholar]
  57. Horgan CP, Hanscom SR, Jolly RS, Futter CE, McCaffrey MW. 2010. Rab11-FIP3 binds dynein light intermediate chain 2 and its overexpression fragments the Golgi complex. Biochem. Biophys. Res. Commun. 394:387–92 [Google Scholar]
  58. Huang J, Roberts AJ, Leschziner AE, Reck-Peterson SL. 2012. Lis1 acts as a “clutch” between the ATPase and microtubule-binding domains of the dynein motor. Cell 150:975–86 [Google Scholar]
  59. Imai H, Narita A, Schroer TA, Maeda Y. 2006. Two-dimensional averaged images of the dynactin complex revealed by single particle analysis. J. Mol. Biol. 359:833–9 [Google Scholar]
  60. Imai H, Narita A, Maeda Y, Schroer TA. 2014. Dynactin 3D structure: implications for assembly and dynein binding. J. Mol. Biol. 426:3262–71 [Google Scholar]
  61. Januschke J, Nicolas E, Compagnon J, Formstecher E, Goud B, Guichet A. 2007. Rab6 and the secretory pathway affect oocyte polarity in Drosophila. Development 134:3419–25 [Google Scholar]
  62. Jha R, Surrey T. 2015. Regulation of processive motion and microtubule localization of cytoplasmic dynein. Biochem. Soc. Trans. 43:48–57 [Google Scholar]
  63. Johnston JA, Illing ME, Kopito RR. 2002. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskelet. 53:26–38 [Google Scholar]
  64. Kardon JR, Reck-Peterson SL, Vale RD. 2009. Regulation of the processivity and intracellular localization of Saccharomyces cerevisiae dynein by dynactin. PNAS 106:5669–74 [Google Scholar]
  65. Karki S, Holzbaur EL. 1995. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:28806–11 [Google Scholar]
  66. Kelly EE, Horgan CP, McCaffrey MW. 2012. Rab11 proteins in health and disease. Biochem. Soc. Trans. 40:1360–7 [Google Scholar]
  67. Kim MH, Cooper DR, Oleksy A, Devedjiev Y, Derewenda U. et al. 2004. The structure of the N-terminal domain of the product of the lissencephaly gene Lis1 and its functional implications. Structure 12:987–98 [Google Scholar]
  68. King SJ, Brown CL, Maier KC, Quintyne NJ, Schroer TA. 2003. Analysis of the dynein-dynactin interaction in vitro and in vivo. Mol. Biol. Cell 14:5089–97 [Google Scholar]
  69. King SJ, Schroer TA. 2000. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2:20–24 [Google Scholar]
  70. Kon T, Imamula K, Roberts AJ, Ohkura R, Knight PJ. et al. 2009. Helix sliding in the stalk coiled coil of dynein couples ATPase and microtubule binding. Nat. Struct. Mol. Biol. 16:325–33 [Google Scholar]
  71. Kon T, Mogami T, Ohkura R, Nishiura M, Sutoh K. 2005. ATP hydrolysis cycle–dependent tail motions in cytoplasmic dynein. Nat. Struct. Mol. Biol. 12:513–19 [Google Scholar]
  72. Kon T, Nishiura M, Ohkura R, Toyoshima YY, Sutoh K. 2004. Distinct functions of nucleotide-binding/hydrolysis sites in the four AAA modules of cytoplasmic dynein. Biochemistry 43:11266–74 [Google Scholar]
  73. Kon T, Oyama T, Shimo-Kon R, Imamula K, Shima T. et al. 2012. The 2.8 Å crystal structure of the dynein motor domain. Nature 484:345–50 [Google Scholar]
  74. Kon T, Sutoh K, Kurisu G. 2011. X-ray structure of a functional full-length dynein motor domain. Nat. Struct. Mol. Biol. 18:638–42 [Google Scholar]
  75. Koonce MP, Samso M. 1996. Overexpression of cytoplasmic dynein's globular head causes a collapse of the interphase microtubule network in Dictyostelium. Mol. Biol. Cell 7:935–48 [Google Scholar]
  76. Kramer H, Phistry M. 1996. Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies. J. Cell Biol. 133:1205–15 [Google Scholar]
  77. Kull FJ, Endow SA. 2013. Force generation by kinesin and myosin cytoskeletal motor proteins. J. Cell Sci. 126:9–19 [Google Scholar]
  78. Lam C, Vergnolle MA, Thorpe L, Woodman PG, Allan VJ. 2010. Functional interplay between LIS1, NDE1 and NDEL1 in dynein-dependent organelle positioning. J. Cell Sci. 123:202–12 [Google Scholar]
  79. Lazarus JE, Moughamian AJ, Tokito MK, Holzbaur EL. 2013. Dynactin subunit p150Glued is a neuron-specific anti-catastrophe factor. PLOS Biol. 11:e1001611 [Google Scholar]
  80. Lee WL, Oberle JR, Cooper JA. 2003. The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J. Cell Biol. 160:355–64 [Google Scholar]
  81. Lenz JH, Schuchardt I, Straube A, Steinberg G. 2006. A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J. 25:2275–86 [Google Scholar]
  82. Li J, Lee WL, Cooper JA. 2005. NudEL targets dynein to microtubule ends through LIS1. Nat. Cell Biol. 7:686–90 [Google Scholar]
  83. Li X, Kuromi H, Briggs L, Green DB, Rocha JJ. et al. 2010. Bicaudal-D binds clathrin heavy chain to promote its transport and augments synaptic vesicle recycling. EMBO J. 29:992–1006 [Google Scholar]
  84. Ligon LA, Tokito M, Finklestein JM, Grossman FE, Holzbaur EL. 2004. A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J. Biol. Chem. 279:19201–8 [Google Scholar]
  85. Lipka J, Kuijpers M, Jaworski J, Hoogenraad CC. 2013. Mutations in cytoplasmic dynein and its regulators cause malformations of cortical development and neurodegenerative diseases. Biochem. Soc. Trans. 41:1605–12 [Google Scholar]
  86. Liu Y, Salter HK, Holding AN, Johnson CM, Stephens E. et al. 2013. Bicaudal-D uses a parallel, homodimeric coiled coil with heterotypic registry to coordinate recruitment of cargos to dynein. Genes Dev. 27:1233–46 [Google Scholar]
  87. Liu Z, Steward R, Luo L. 2000. Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat. Cell Biol. 2:776–83 [Google Scholar]
  88. Liu Z, Xie T, Steward R. 1999. Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation. Development 126:4477–88 [Google Scholar]
  89. Lloyd TE, Machamer J, O'Hara K, Kim JH, Collins SE. et al. 2012. The p150Glued CAP-Gly domain regulates initiation of retrograde transport at synaptic termini. Neuron 74:344–60 [Google Scholar]
  90. Lockrow JP, Holden KR, Dwivedi A, Matheus MG, Lyons MJ. 2012. LIS1 duplication: expanding the phenotype. J. Child Neurol. 27:791–95 [Google Scholar]
  91. Lomakin AJ, Semenova I, Zaliapin I, Kraikivski P, Nadezhdina E. et al. 2009. CLIP-170–dependent capture of membrane organelles by microtubules initiates minus-end directed transport. Dev. Cell 17:323–33 [Google Scholar]
  92. Loschi M, Leishman CC, Berardone N, Boccaccio GL. 2009. Dynein and kinesin regulate stress-granule and P-body dynamics. J. Cell Sci. 122:3973–82 [Google Scholar]
  93. Maday S, Twelvetrees AE, Moughamian AJ, Holzbaur EL. 2014. Axonal transport: cargo-specific mechanisms of motility and regulation. Neuron 84:292–309 [Google Scholar]
  94. Maday S, Wallace KE, Holzbaur EL. 2012. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J. Cell Biol. 196:407–17 [Google Scholar]
  95. Maldonado-Baez L, Cole NB, Kramer H, Donaldson JG. 2013. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J. Cell Biol. 201:233–47 [Google Scholar]
  96. Mallik R, Carter BC, Lex SA, King SJ, Gross SP. 2004. Cytoplasmic dynein functions as a gear in response to load. Nature 427:649–52 [Google Scholar]
  97. Mallik R, Rai AK, Barak P, Rai A, Kunwar A. 2013. Teamwork in microtubule motors. Trends Cell Biol. 23:575–82 [Google Scholar]
  98. Markus SM, Lee WL. 2011. Microtubule-dependent path to the cell cortex for cytoplasmic dynein in mitotic spindle orientation. Bioarchitecture 1:209–15 [Google Scholar]
  99. Markus SM, Punch JJ, Lee WL. 2009. Motor- and tail-dependent targeting of dynein to microtubule plus ends and the cell cortex. Curr. Biol. 19:196–205 [Google Scholar]
  100. Matanis T, Akhmanova A, Wulf P, Del Nery E, Weide T. et al. 2002. Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat. Cell Biol. 4:986–92 [Google Scholar]
  101. McKenney RJ, Huynh W, Tanenbaum ME, Bhabha G, Vale RD. 2014. Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science 345:337–41 [Google Scholar]
  102. McKenney RJ, Vershinin M, Kunwar A, Vallee RB, Gross SP. 2010. LIS1 and NudE induce a persistent dynein force-producing state. Cell 141:304–14 [Google Scholar]
  103. McKenney RJ, Weil SJ, Scherer J, Vallee RB. 2011. Mutually exclusive cytoplasmic dynein regulation by NudE-Lis1 and dynactin. J. Biol. Chem. 286:39615–22 [Google Scholar]
  104. Millecamps S, Julien JP. 2013. Axonal transport deficits and neurodegenerative diseases. Nat. Rev. Neurosci. 14:161–76 [Google Scholar]
  105. Minke PF, Lee IH, Plamann M. 1999. Microscopic analysis of Neurospora ropy mutants defective in nuclear distribution. Fungal Genet. Biol. 28:55–67 [Google Scholar]
  106. Mizuno N, Toba S, Edamatsu M, Watai-Nishii J, Hirokawa N. et al. 2004. Dynein and kinesin share an overlapping microtubule-binding site. EMBO J. 23:2459–67 [Google Scholar]
  107. Mohler J, Wieschaus EF. 1986. Dominant maternal-effect mutations of Drosophila melanogaster causing the production of double-abdomen embryos. Genetics 112:803–22 [Google Scholar]
  108. Moon HM, Youn YH, Pemble H, Yingling J, Wittmann T, Wynshaw-Boris A. 2014. LIS1 controls mitosis and mitotic spindle organization via the LIS1-NDEL1-dynein complex. Hum. Mol. Genet. 23:449–66 [Google Scholar]
  109. Moore JK, Stuchell-Brereton MD, Cooper JA. 2009. Function of dynein in budding yeast: mitotic spindle positioning in a polarized cell. Cell Motil. Cytoskelet. 66:546–55 [Google Scholar]
  110. Moughamian AJ, Holzbaur EL. 2012. Dynactin is required for transport initiation from the distal axon. Neuron 74:331–43 [Google Scholar]
  111. Moughamian AJ, Osborn GE, Lazarus JE, Maday S, Holzbaur EL. 2013. Ordered recruitment of dynactin to the microtubule plus-end is required for efficient initiation of retrograde axonal transport. J. Neurosci. 33:13190–203 [Google Scholar]
  112. Neuwald AF, Aravind L, Spouge JL, Koonin EV. 1999. AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9:27–43 [Google Scholar]
  113. Neveling K, Martinez-Carrera LA, Holker I, Heister A, Verrips A. et al. 2013. Mutations in BICD2, which encodes a golgin and important motor adaptor, cause congenital autosomal-dominant spinal muscular atrophy. Am. J. Hum. Genet. 92:946–54 [Google Scholar]
  114. Nicholas MP, Berger F, Rao L, Brenner S, Cho C, Gennerich A. 2015a. Cytoplasmic dynein regulates its attachment to microtubules via nucleotide state-switched mechanosensing at multiple AAA domains. PNAS 112:6371–76 [Google Scholar]
  115. Nicholas MP, Hook P, Brenner S, Wynne CL, Vallee RB, Gennerich A. 2015b. Control of cytoplasmic dynein force production and processivity by its C-terminal domain. Nat. Commun. 6:6206 [Google Scholar]
  116. Nishiura M, Kon T, Shiroguchi K, Ohkura R, Shima T. et al. 2004. A single-headed recombinant fragment of Dictyostelium cytoplasmic dynein can drive the robust sliding of microtubules. J. Biol. Chem. 279:22799–802 [Google Scholar]
  117. Numata N, Shima T, Ohkura R, Kon T, Sutoh K. 2011. C-sequence of the Dictyostelium cytoplasmic dynein participates in processivity modulation. FEBS Lett. 585:1185–90 [Google Scholar]
  118. Nyarko A, Song Y, Barbar E. 2012. Intrinsic disorder in dynein intermediate chain modulates its interactions with NudE and dynactin. J. Biol. Chem. 287:24884–93 [Google Scholar]
  119. Oates EC, Rossor AM, Hafezparast M, Gonzalez M, Speziani F. et al. 2013. Mutations in BICD2 cause dominant congenital spinal muscular atrophy and hereditary spastic paraplegia. Am. J. Hum. Genet. 92:965–73 [Google Scholar]
  120. Pandey JP, Smith DS. 2011. A Cdk5-dependent switch regulates Lis1/Ndel1/dynein-driven organelle transport in adult axons. J. Neurosci. 31:17207–19 [Google Scholar]
  121. Paschal BM, Shpetner HS, Vallee RB. 1987. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol. 105:1273–82 [Google Scholar]
  122. Paschal BM, Vallee RB. 1987. Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330:181–83 [Google Scholar]
  123. Peeters K, Litvinenko I, Asselbergh B, Almeida-Souza L, Chamova T. et al. 2013. Molecular defects in the motor adaptor BICD2 cause proximal spinal muscular atrophy with autosomal-dominant inheritance. Am. J. Hum. Genet. 92:955–64 [Google Scholar]
  124. Poirier K, Lebrun N, Broix L, Tian G, Saillour Y. et al. 2013. Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat. Genet. 45:639–47 [Google Scholar]
  125. Preitner N, Quan J, Nowakowski DW, Hancock ML, Shi J. et al. 2014. APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly. Cell 158:368–82 [Google Scholar]
  126. Puls I, Jonnakuty C, LaMonte BH, Holzbaur EL, Tokito M. et al. 2003. Mutant dynactin in motor neuron disease. Nat. Genet. 33:455–6 [Google Scholar]
  127. Qiu W, Derr ND, Goodman BS, Villa E, Wu D. et al. 2012. Dynein achieves processive motion using both stochastic and coordinated stepping. Nat. Struct. Mol. Biol. 19:193–200 [Google Scholar]
  128. Reck-Peterson SL, Yildiz A, Carter AP, Gennerich A, Zhang N, Vale RD. 2006. Single-molecule analysis of dynein processivity and stepping behavior. Cell 126:335–48 [Google Scholar]
  129. Redwine WB, Hernandez-Lopez R, Zou S, Huang J, Reck-Peterson SL, Leschziner AE. 2012. Structural basis for microtubule binding and release by dynein. Science 337:1532–6 [Google Scholar]
  130. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F. et al. 1993. Isolation of a Miller-Dieker lissencephaly gene containing G protein β–subunit-like repeats. Nature 364:717–21 [Google Scholar]
  131. Reiner O, Sapir T. 2013. LIS1 functions in normal development and disease. Curr. Opin. Neurobiol. 23:951–56 [Google Scholar]
  132. Roberts AJ, Goodman BS, Reck-Peterson SL. 2014. Reconstitution of dynein transport to the microtubule plus end by kinesin. eLife 3e02641 [Google Scholar]
  133. Roberts AJ, Malkova B, Walker ML, Sakakibara H, Numata N. et al. 2012. ATP-driven remodeling of the linker domain in the dynein motor. Structure 20:1670–80 [Google Scholar]
  134. Roberts AJ, Numata N, Walker ML, Kato YS, Malkova B. et al. 2009. AAA+ Ring and linker swing mechanism in the dynein motor. Cell 136:485–95 [Google Scholar]
  135. Ross JL, Wallace K, Shuman H, Goldman YE, Holzbaur EL. 2006. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat. Cell Biol. 8:562–70 [Google Scholar]
  136. Saito T, Hanai S, Takashima S, Nakagawa E, Okazaki S. et al. 2011. Neocortical layer formation of human developing brains and lissencephalies: consideration of layer-specific marker expression. Cereb. Cortex 21:588–96 [Google Scholar]
  137. Sasaki S, Mori D, Toyo-oka K, Chen A, Garrett-Beal L. et al. 2005. Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol. Cell. Biol. 25:7812–27 [Google Scholar]
  138. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J. et al. 2000. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28:681–96 [Google Scholar]
  139. Schafer DA, Gill SR, Cooper JA, Heuser JE, Schroer TA. 1994. Ultrastructural analysis of the dynactin complex: an actin-related protein is a component of a filament that resembles F-actin. J. Cell Biol. 126:403–12 [Google Scholar]
  140. Schlager MA, Hoang HT, Urnavicius L, Bullock SL, Carter AP. 2014. In vitro reconstitution of a highly processive recombinant human dynein complex. EMBO J. 33:1855–68 [Google Scholar]
  141. Schmidt H, Gleave ES, Carter AP. 2012. Insights into dynein motor domain function from a 3.3-Å crystal structure. Nat. Struct. Mol. Biol. 19:492–97 [Google Scholar]
  142. Schmidt H, Zalyte R, Urnavicius L, Carter AP. 2014. Structure of human cytoplasmic dynein-2 primed for its power stroke. Nature 518:435–38 [Google Scholar]
  143. Schroer TA. 2004. Dynactin. Annu. Rev. Cell Dev. Biol. 20:759–79 [Google Scholar]
  144. Schroer TA, Sheetz MP. 1991. Two activators of microtubule-based vesicle transport. J. Cell Biol. 115:1309–18 [Google Scholar]
  145. Shao CY, Zhu J, Xie YJ, Wang Z, Wang YN. et al. 2013. Distinct functions of nuclear distribution proteins LIS1, Ndel1 and NudCL in regulating axonal mitochondrial transport. Traffic 14:785–97 [Google Scholar]
  146. Sheeman B, Carvalho P, Sagot I, Geiser J, Kho D. et al. 2003. Determinants of S. cerevisiae dynein localization and activation: implications for the mechanism of spindle positioning. Curr. Biol. 13:364–72 [Google Scholar]
  147. Shima T, Kon T, Imamula K, Ohkura R, Sutoh K. 2006. Two modes of microtubule sliding driven by cytoplasmic dynein. PNAS 103:17736–40 [Google Scholar]
  148. Siglin AE, Sun S, Moore JK, Tan S, Poenie M. et al. 2013. Dynein and dynactin leverage their bivalent character to form a high-affinity interaction. PLOS ONE 8:e59453 [Google Scholar]
  149. Silvanovich A, Li MG, Serr M, Mische S, Hays TS. 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 14:1355–65 [Google Scholar]
  150. Simpson F, Martin S, Evans TM, Kerr M, James DE. et al. 2005. A novel hook-related protein family and the characterization of hook-related protein 1. Traffic 6:442–58 [Google Scholar]
  151. Sitaram P, Anderson MA, Jodoin JN, Lee E, Lee LA. 2012. Regulation of dynein localization and centrosome positioning by Lis-1 and asunder during Drosophila spermatogenesis. Development 139:2945–54 [Google Scholar]
  152. Smith DS, Niethammer M, Ayala R, Zhou Y, Gambello MJ. et al. 2000. Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat. Cell Biol. 2:767–75 [Google Scholar]
  153. Splinter D, Razafsky DS, Schlager MA, Serra-Marques A, Grigoriev I. et al. 2012. BICD2, dynactin, and LIS1 cooperate in regulating dynein recruitment to cellular structures. Mol. Biol. Cell 23:4226–41 [Google Scholar]
  154. Splinter D, Tanenbaum ME, Lindqvist A, Jaarsma D, Flotho A. et al. 2010. Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLOS Biol. 8:e1000350 [Google Scholar]
  155. Szebenyi G, Hall B, Yu R, Hashim AI, Kramer H. 2007a. Hook2 localizes to the centrosome, binds directly to centriolin/CEP110 and contributes to centrosomal function. Traffic 8:32–46 [Google Scholar]
  156. Szebenyi G, Wigley WC, Hall B, Didier A, Yu M. et al. 2007b. Hook2 contributes to aggresome formation. BMC Cell Biol. 8:19 [Google Scholar]
  157. Tai CY, Dujardin DL, Faulkner NE, Vallee RB. 2002. Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J. Cell Biol. 156:959–68 [Google Scholar]
  158. Tarricone C, Perrina F, Monzani S, Massimiliano L, Kim MH. et al. 2004. Coupling PAF signaling to dynein regulation: structure of LIS1 in complex with PAF-acetylhydrolase. Neuron 44:809–21 [Google Scholar]
  159. Toba S, Watanabe TM, Yamaguchi-Okimoto L, Toyoshima YY, Higuchi H. 2006. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. PNAS 103:5741–45 [Google Scholar]
  160. Torisawa T, Ichikawa M, Furuta A, Saito K, Oiwa K. et al. 2014. Autoinhibition and cooperative activation mechanisms of cytoplasmic dynein. Nat. Cell Biol. 16:1118–24 [Google Scholar]
  161. Toropova K, Zou S, Roberts AJ, Redwine WB, Goodman BS. et al. 2014. Lis1 regulates dynein by sterically blocking its mechanochemical cycle. eLife 3:e03372 [Google Scholar]
  162. Tripathy SK, Weil SJ, Chen C, Anand P, Vallee RB, Gross SP. 2014. Autoregulatory mechanism for dynactin control of processive and diffusive dynein transport. Nat. Cell Biol. 16:1192–201 [Google Scholar]
  163. Tsai JW, Bremner KH, Vallee RB. 2007. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat. Neurosci. 10:970–79 [Google Scholar]
  164. Urnavicius L, Zhang K, Diamant AG, Motz C, Schlager MA. et al. 2015. The structure of the dynactin complex and its interaction with dynein. Science 347:1441–46 [Google Scholar]
  165. Vale RD. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467–80 [Google Scholar]
  166. Vale RD, Milligan RA. 2000. The way things move: looking under the hood of molecular motor proteins. Science 288:88–95 [Google Scholar]
  167. Vallee RB, Tsai JW. 2006. The cellular roles of the lissencephaly gene LIS1, and what they tell us about brain development. Genes Dev. 20:1384–93 [Google Scholar]
  168. Vaughan KT, Vallee RB. 1995. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 131:1507–16 [Google Scholar]
  169. Vaughan PS, Miura P, Henderson M, Byrne B, Vaughan KT. 2002. A role for regulated binding of p150Glued to microtubule plus ends in organelle transport. J. Cell Biol. 158:305–19 [Google Scholar]
  170. Vilarino-Guell C, Wider C, Soto-Ortolaza AI, Cobb SA, Kachergus JM. et al. 2009. Characterization of DCTN1 genetic variability in neurodegeneration. Neurology 72:2024–28 [Google Scholar]
  171. Walenta JH, Didier AJ, Liu X, Kramer H. 2001. The Golgi-associated Hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152:923–34 [Google Scholar]
  172. Wang S, Ketcham SA, Schon A, Goodman B, Wang Y. et al. 2013. Nudel/NudE and Lis1 promote dynein and dynactin interaction in the context of spindle morphogenesis. Mol. Biol. Cell 24:3522–33 [Google Scholar]
  173. Wang S, Zheng Y. 2011. Identification of a novel dynein binding domain in Nudel essential for spindle pole organization in Xenopus egg extract. J. Biol. Chem. 286:587–93 [Google Scholar]
  174. Wang Y, Jin F, Higgins R, McKnight K. 2014. The current view for the silencing of the spindle assembly checkpoint. Cell Cycle 13:1694–701 [Google Scholar]
  175. Wang Z, Khan S, Sheetz MP. 1995. Single cytoplasmic dynein molecule movements: characterization and comparison with kinesin. Biophys. J. 69:2011–23 [Google Scholar]
  176. Weedon MN, Hastings R, Caswell R, Xie W, Paszkiewicz K. et al. 2011. Exome sequencing identifies a DYNC1H1 mutation in a large pedigree with dominant axonal Charcot-Marie-Tooth disease. Am. J. Hum. Genet. 89:308–12 [Google Scholar]
  177. Wickstead B, Gull K. 2007. Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8:1708–21 [Google Scholar]
  178. Wynshaw-Boris A. 2007. Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development. Clin. Genet. 72:296–304 [Google Scholar]
  179. Xiang X, Osmani AH, Osmani SA, Xin M, Morris NR. 1995. NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell 6:297–310 [Google Scholar]
  180. Yagi T. 2009. Bioinformatic approaches to dynein heavy chain classification. Methods Cell Biol. 92:1–9 [Google Scholar]
  181. Yamada M, Hirotsune S, Wynshaw-Boris A. 2010. The essential role of LIS1, NDEL1 and Aurora-A in polarity formation and microtubule organization during neurogensis. Cell Adhes. Migr. 4:180–84 [Google Scholar]
  182. Yamada M, Toba S, Yoshida Y, Haratani K, Mori D. et al. 2008. LIS1 and NDEL1 coordinate the plus-end–directed transport of cytoplasmic dynein. EMBO J. 27:2471–83 [Google Scholar]
  183. Yeh TY, Kowalska AK, Scipioni BR, Cheong FK, Zheng M. et al. 2013. Dynactin helps target Polo-like kinase 1 to kinetochores via its left-handed β-helical p27 subunit. EMBO J. 32:1023–35 [Google Scholar]
  184. Yeh TY, Quintyne NJ, Scipioni BR, Eckley DM, Schroer TA. 2012. Dynactin's pointed-end complex is a cargo-targeting module. Mol. Biol. Cell 23:3827–37 [Google Scholar]
  185. Yi JY, Ori-McKenney KM, McKenney RJ, Vershinin M, Gross SP, Vallee RB. 2011. High-resolution imaging reveals indirect coordination of opposite motors and a role for LIS1 in high-load axonal transport. J. Cell Biol. 195:193–201 [Google Scholar]
  186. Yingling J, Youn YH, Darling D, Toyo-Oka K, Pramparo T. et al. 2008. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132:474–86 [Google Scholar]
  187. Youn YH, Pramparo T, Hirotsune S, Wynshaw-Boris A. 2009. Distinct dose-dependent cortical neuronal migration and neurite extension defects in Lis1 and Ndel1 mutant mice. J. Neurosci. 29:15520–30 [Google Scholar]
  188. Zhang J, Li S, Fischer R, Xiang X. 2003. Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol. Biol. Cell 14:1479–88 [Google Scholar]
  189. Zhang J, Qiu R, Arst HN Jr, Penalva MA, Xiang X. 2014. HookA is a novel dynein–early endosome linker critical for cargo movement in vivo. J. Cell Biol. 204:1009–26 [Google Scholar]
  190. Zhang J, Yao X, Fischer L, Abenza JF, Peñalva MA, Xiang X. 2011. The p25 subunit of the dynactin complex is required for dynein–early endosome interaction. J. Cell Biol. 193:1245–55 [Google Scholar]
  191. Zhang J, Zhuang L, Lee Y, Abenza JF, Penalva MA, Xiang X. 2010. The microtubule plus-end localization of Aspergillus dynein is important for dynein–early-endosome interaction but not for dynein ATPase activation. J. Cell Sci. 123:3596–604 [Google Scholar]
  192. Zylkiewicz E, Kijanska M, Choi WC, Derewenda U, Derewenda ZS, Stukenberg PT. 2011. The N-terminal coiled-coil of Ndel1 is a regulated scaffold that recruits LIS1 to dynein. J. Cell Biol. 192:433–45 [Google Scholar]
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