1932

Abstract

Microtubules are core components of the cytoskeleton and serve as tracks for motor protein–based intracellular transport. Microtubule networks are highly diverse across different cell types and are believed to adapt to cell type–specific transport demands. Here we review how the spatial organization of different subsets of microtubules into higher-order networks determines the traffic rules for motor-based transport in different animal cell types. We describe the interplay between microtubule network organization and motor-based transport within epithelial cells, oocytes, neurons, cilia, and the spindle apparatus.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100818-125149
2019-10-06
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/35/1/annurev-cellbio-100818-125149.html?itemId=/content/journals/10.1146/annurev-cellbio-100818-125149&mimeType=html&fmt=ahah

Literature Cited

  1. Absalon S, Blisnick T, Kohl L, Toutirais G, Doré G et al. 2008. Intraflagellar transport and functional analysis of genes required for flagellum formation in trypanosomes. Mol. Biol. Cell 19:3929–44
    [Google Scholar]
  2. Akera T, Chmátal L, Trimm E, Yang K, Aonbangkhen C et al. 2017. Spindle asymmetry drives non-Mendelian chromosome segregation. Science 358:Nov.668–72
    [Google Scholar]
  3. Akhmanova A, Hoogenraad CC. 2015. Microtubule minus-end-targeting proteins. Curr. Biol. 25:4R162–71
    [Google Scholar]
  4. Akhmanova A, Steinmetz MO. 2015. Control of microtubule organization and dynamics: two ends in the limelight. Nat. Rev. Mol. Cell Biol. 16:12711–26
    [Google Scholar]
  5. Al-Bassam J, Roger B, Halpain S, Milligan RA 2007. Analysis of the weak interactions of ADP-Unc104 and ADP-kinesin with microtubules and their inhibition by MAP2c. Cell Motil. Cytoskelet. 64:5377–89
    [Google Scholar]
  6. Anvarian Z, Mykytyn K, Mukhopadhyay S, Pedersen LB, Christensen ST 2019. Cellular signalling by primary cilia in development, organ function and disease. Nat. Rev. Nephrol. 15:4199–219
    [Google Scholar]
  7. Auckland P, McAinsh AD. 2015. Building an integrated model of chromosome congression. J. Cell Sci. 128:183363–74
    [Google Scholar]
  8. Aw WY, Devenport D. 2017. Planar cell polarity: global inputs establishing cellular asymmetry. Curr. Opin. Cell Biol. 44:110–16
    [Google Scholar]
  9. Ayloo S, Guedes-Dias P, Ghiretti AE, Holzbaur ELF 2017. Dynein efficiently navigates the dendritic cytoskeleton to drive the retrograde trafficking of BDNF/TrkB signaling endosomes. Mol. Biol. Cell 28:192543–54
    [Google Scholar]
  10. Baas PW, Deitch JS, Black MM, Banker GA 1988. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. PNAS 85:218335–39
    [Google Scholar]
  11. Baas PW, Lin S. 2011. Hooks and comets: the story of microtubule polarity orientation in the neuron. Dev. Neurobiol. 71:6403–18
    [Google Scholar]
  12. Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EH, Simons K 1989. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J. Cell Biol. 109:6 Pt 12817–32
    [Google Scholar]
  13. Barisic M, Aguiar P, Geley S, Maiato H 2014. Kinetochore motors drive congression of peripheral polar chromosomes by overcoming random arm-ejection forces. Nat. Cell Biol. 16:121249–56
    [Google Scholar]
  14. Barisic M, Silva e Sousa R, Tripathy SK, Magiera MM, Zaytsev AV et al. 2015. Microtubule detyrosination guides chromosomes during mitosis. Science 348:6236799–803
    [Google Scholar]
  15. Barlan K, Gelfand VI. 2017. Microtubule-based transport and the distribution, tethering, and organization of organelles. Cold Spring Harb. Perspect. Biol. 9:5a025817
    [Google Scholar]
  16. Bentley M, Banker G. 2016. The cellular mechanisms that maintain neuronal polarity. Nat. Rev. Neurosci. 17:10611–22
    [Google Scholar]
  17. Bertiaux E, Mallet A, Fort C, Blisnick T, Bonnefoy S et al. 2018. Bidirectional intraflagellar transport is restricted to two sets of microtubule doublets in the trypanosome flagellum. J. Cell Biol. 217:124284–97
    [Google Scholar]
  18. Blasky AJ, Mangan A, Prekeris R 2015. Polarized protein transport and lumen formation during epithelial tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 31:575–91
    [Google Scholar]
  19. Bonifacino JS, Neefjes J. 2017. Moving and positioning the endolysosomal system. Curr. Opin. Cell Biol. 47:1–8
    [Google Scholar]
  20. Bouchet BP, Gough RE, Ammon Y-C, van de Willige D, Post H et al. 2016. Talin-KANK1 interaction controls the recruitment of cortical microtubule stabilizing complexes to focal adhesions. eLife 5:e18124
    [Google Scholar]
  21. Brouhard GJ, Rice LM. 2018. Microtubule dynamics: an interplay of biochemistry and mechanics. Nat. Rev. Mol. Cell Biol. 19:7451–63
    [Google Scholar]
  22. Burton PR. 1988. Dendrites of mitral cell neurons contain microtubules of opposite polarity. Brain Res 473:1107–15
    [Google Scholar]
  23. Burton PR, Paige JL. 1981. Polarity of axoplasmic microtubules in the olfactory nerve of the frog. PNAS 78:53269–73
    [Google Scholar]
  24. Burute M, Prioux M, Blin G, Truchet S, Letort G et al. 2017. Polarity reversal by centrosome repositioning primes cell scattering during epithelial-to-mesenchymal transition. Dev. Cell 40:2168–84
    [Google Scholar]
  25. Butler MT, Wallingford JB. 2017. Planar cell polarity in development and disease. Nat. Rev. Mol. Cell Biol. 18:6375–88
    [Google Scholar]
  26. Cai D, McEwen DP, Martens JR, Meyhofer E, Verhey KJ 2009. Single molecule imaging reveals differences in microtubule track selection between kinesin motors. PLOS Biol 7:10e1000216
    [Google Scholar]
  27. Cha BJ, Koppetsch BS, Theurkauf WE 2001. In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106:135–46
    [Google Scholar]
  28. Chaaban S, Brouhard GJ. 2017. A microtubule bestiary: structural diversity in tubulin polymers. Mol. Biol. Cell 28:222924–31
    [Google Scholar]
  29. Chaudhary AR, Berger F, Berger CL, Hendricks AG 2018. Tau directs intracellular trafficking by regulating the forces exerted by kinesin and dynein teams. Traffic 19:2111–21
    [Google Scholar]
  30. Ciocanel M-V, Sandstede B, Jeschonek SP, Mowry KL 2018. Modeling microtubule-based transport and anchoring of mRNA. SIAM J. Appl. Dyn. Syst. 17:42855–81
    [Google Scholar]
  31. Coumailleau F, Fürthauer M, Knoblich JA, González-Gaitán M 2009. Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458:72411051–55
    [Google Scholar]
  32. Cunha-Ferreira I, Chazeau A, Buijs RR, Stucchi R, Will L et al. 2018. The HAUS complex is a key regulator of non-centrosomal microtubule organization during neuronal development. Cell Rep 24:4791–800
    [Google Scholar]
  33. Derivery E, Seum C, Daeden A, Loubéry S, Holtzer L et al. 2015. Polarized endosome dynamics by spindle asymmetry during asymmetric cell division. Nature 528:7581280–85
    [Google Scholar]
  34. Dixit R, Ross JL, Goldman YE, Holzbaur ELF 2008. Differential regulation of dynein and kinesin motor proteins by tau. Science 319:58661086–89
    [Google Scholar]
  35. Duan L, Che D, Zhang K, Ong Q, Guo S, Cui B 2015. Optogenetic control of molecular motors and organelle distributions in cells. Chem. Biol. 22:5671–82
    [Google Scholar]
  36. Dunn S, Morrison EE, Liverpool TB, Molina-París C, Cross RA et al. 2008. Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells. J. Cell Sci. 121:1085–95
    [Google Scholar]
  37. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM et al. 2007. Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12:6917–30
    [Google Scholar]
  38. Farías GG, Guardia CM, Britt DJ, Guo X, Bonifacino JS 2015. Sorting of dendritic and axonal vesicles at the pre-axonal exclusion zone. Cell Rep 13:61221–32
    [Google Scholar]
  39. Fink G, Hajdo L, Skowronek KJ, Reuther C, Kasprzak AA, Diez S 2009. The mitotic kinesin-14 Ncd drives directional microtubule-microtubule sliding. Nat. Cell Biol. 11:6717–23
    [Google Scholar]
  40. Fojo A 2009. The Role of Microtubules in Cell Biology, Neurobiology, and Oncology Totowa, NJ: Humana Press
  41. Foley EA, Kapoor TM. 2013. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14:125–37
    [Google Scholar]
  42. Friedman JR, Webster BM, Mastronarde DN, Verhey KJ, Voeltz GK 2010. ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules. J. Cell Biol. 190:3363–75
    [Google Scholar]
  43. Gaillard J, Neumann E, Van Damme D, Stoppin-Mellet V, Ebel C et al. 2008. Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol. Biol. Cell 19:104534–44
    [Google Scholar]
  44. Gilbert T, Le Bivic A, Quaroni A, Rodriguez-Boulan E 1991. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells. J. Cell Biol. 113:2275–88
    [Google Scholar]
  45. Goodrich LV, Strutt D. 2011. Principles of planar polarity in animal development. Development 138:101877–92
    [Google Scholar]
  46. Goodson HV, Jonasson EM. 2018. Microtubules and microtubule-associated proteins. Cold Spring Harb. Perspect. Biol. 10:6a022608
    [Google Scholar]
  47. Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD 2008. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 181:3421–29
    [Google Scholar]
  48. Guardia CM, Farías GG, Jia R, Pu J, Bonifacino JS 2016. BORC functions upstream of kinesins 1 and 3 to coordinate regional movement of lysosomes along different microtubule tracks. Cell Rep 17:81950–61
    [Google Scholar]
  49. Gumy LF, Hoogenraad CC. 2018. Local mechanisms regulating selective cargo entry and long-range trafficking in axons. Curr. Opin. Neurobiol. 51:23–28
    [Google Scholar]
  50. Gumy LF, Katrukha EA, Grigoriev I, Jaarsma D, Kapitein LC et al. 2017. MAP2 defines a pre-axonal filtering zone to regulate KIF1- versus KIF5-dependent cargo transport in sensory neurons. Neuron 94:2347–62.e7
    [Google Scholar]
  51. Gundersen GG, Bulinski JC. 1988. Selective stabilization of microtubules oriented toward the direction of cell migration. PNAS 85:165946–50
    [Google Scholar]
  52. Hancock WO. 2014. Bidirectional cargo transport: moving beyond tug of war. Nat. Rev. Mol. Cell Biol. 15:9615–28
    [Google Scholar]
  53. Harterink M, van Bergeijk P, Allier C, de Haan B, van den Heuvel S et al. 2016. Light-controlled intracellular transport in Caenorhabditis elegans. Curr. Biol 26:4R153–54
    [Google Scholar]
  54. Harumoto T, Ito M, Shimada Y, Kobayashi TJ, Ueda HR et al. 2010. Atypical cadherins Dachsous and Fat control dynamics of noncentrosomal microtubules in planar cell polarity. Dev. Cell 19:3389–401
    [Google Scholar]
  55. Heidemann SR, Landers JM, Hamborg MA 1981. Polarity orientation of axonal microtubules. J. Cell Biol. 91:3 Pt 1661–65
    [Google Scholar]
  56. Heidemann SR, McIntosh JR. 1980. Visualization of the structural polarity of microtubules. Nature 286:5772517–19
    [Google Scholar]
  57. Henderson DJ, Long DA, Dean CH 2018. Planar cell polarity in organ formation. Curr. Opin. Cell Biol. 55:96–103
    [Google Scholar]
  58. Hirokawa N, Noda Y. 2008. Intracellular transport and kinesin superfamily proteins, KIFs: structure, function, and dynamics. Physiol. Rev. 88:31089–118
    [Google Scholar]
  59. Hooikaas PJ, Martin M, Mühlethaler T, Kuijntjes G-J, Peeters CAE et al. 2019. MAP7 family proteins regulate kinesin-1 recruitment and activation. J. Cell Biol. 218:41298–318
    [Google Scholar]
  60. Horne-Badovinac S, Bilder D. 2008. Dynein regulates epithelial polarity and the apical localization of stardustA mRNA. PLOS Genet 4:1e8
    [Google Scholar]
  61. Huang C, Banker G. 2012. The translocation selectivity of the kinesins that mediate neuronal organelle transport. Traffic 13:4549–64
    [Google Scholar]
  62. Jacobson C, Schnapp B, Banker GA 2006. A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49:6797–804
    [Google Scholar]
  63. Janke C. 2014. The tubulin code: molecular components, readout mechanisms, and functions. J. Cell Biol. 206:4461–72
    [Google Scholar]
  64. Johnson KA. 1998. The axonemal microtubules of the Chlamydomonas flagellum differ in tubulin isoform content. J. Cell Sci. 111:3313–20
    [Google Scholar]
  65. Jolly AL, Kim H, Srinivasan D, Lakonishok M, Larson AG, Gelfand VI 2010. Kinesin-1 heavy chain mediates microtubule sliding to drive changes in cell shape. PNAS 107:2712151–56
    [Google Scholar]
  66. Jordan MA, Diener DR, Stepanek L, Pigino G 2018. The cryo-EM structure of intraflagellar transport trains reveals how dynein is inactivated to ensure unidirectional anterograde movement in cilia. Nat. Cell Biol. 20:111250–55
    [Google Scholar]
  67. Kaan HY, Hackney DD, Kozielski F 2011. The structure of the kinesin-1 motor-tail complex reveals the mechanism of autoinhibition. Science 333:6044883–85
    [Google Scholar]
  68. Kapitein LC, Hoogenraad CC. 2015. Building the neuronal microtubule cytoskeleton. Neuron 87:3492–506
    [Google Scholar]
  69. Kapitein LC, Peterman EJG, Kwok BH, Kim JH, Kapoor TM, Schmidt CF 2005. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 435:7038114–18
    [Google Scholar]
  70. Kapitein LC, Schlager MA, Kuijpers M, Wulf PS, van Spronsen M et al. 2010a. Mixed microtubules steer dynein-driven cargo transport into dendrites. Curr. Biol. 20:4290–99
    [Google Scholar]
  71. Kapitein LC, Schlager MA, Van Der Zwan WA, Wulf PS, Keijzer N, Hoogenraad CC 2010b. Probing intracellular motor protein activity using an inducible cargo trafficking assay. Biophys. J. 99:72143–52
    [Google Scholar]
  72. Kapoor TM, Lampson MA, Hergert P, Cameron L, Cimini D et al. 2006. Chromosomes can congress to the metaphase plate before biorientation. Science 311:5759388–91
    [Google Scholar]
  73. Karasmanis EP, Phan C-T, Angelis D, Kesisova IA, Hoogenraad CC et al. 2018. Polarity of neuronal membrane traffic requires sorting of kinesin motor cargo during entry into dendrites by a microtubule-associated septin. Dev. Cell 46:2204–18.e7
    [Google Scholar]
  74. Kaul N, Soppina V, Verhey KJ 2014. Effects of α-tubulin K40 acetylation and detyrosination on kinesin-1 motility in a purified system. Biophys. J. 106:122636–43
    [Google Scholar]
  75. Kaverina I, Straube A. 2011. Regulation of cell migration by dynamic microtubules. Semin. Cell Dev. Biol. 22:9968–74
    [Google Scholar]
  76. Kellogg EH, Hejab NMA, Poepsel S, Downing KH, DiMaio F, Nogales E 2018. Near-atomic model of microtubule-tau interactions. Science 360:63941242–46
    [Google Scholar]
  77. Khan S, Scholey JM. 2018. Assembly, functions and evolution of archaella, flagella and cilia. Curr. Biol. 28:6R278–92
    [Google Scholar]
  78. Khanal I, Elbediwy A, del Carmen Diaz de la, Loza M, Fletcher GC, Thompson BJ 2016. Shot and Patronin polarise microtubules to direct membrane traffic and biogenesis of microvilli in epithelia. J. Cell Sci. 129:132651–59
    [Google Scholar]
  79. Khuc Trong P, Doerflinger H, Dunkel J, St. Johnston D, Goldstein RE 2015. Cortical microtubule nucleation can organise the cytoskeleton of Drosophila oocytes to define the anteroposterior axis. eLife 4:e06088
    [Google Scholar]
  80. Kirschner M, Mitchison T. 1986. Beyond self-assembly: from microtubules to morphogenesis. Cell 45:3329–42
    [Google Scholar]
  81. Kleele T, Marinković P, Williams PR, Stern S, Weigand EE et al. 2014. An assay to image neuronal microtubule dynamics in mice. Nat. Commun. 5:14827
    [Google Scholar]
  82. Kollman JM, Merdes A, Mourey L, Agard DA 2011. Microtubule nucleation by γ-tubulin complexes. Nat. Rev. Mol. Cell Biol. 12:11709–21
    [Google Scholar]
  83. Korolchuk VI, Saiki S, Lichtenberg M, Siddiqi FH, Roberts EA et al. 2011. Lysosomal positioning coordinates cellular nutrient responses. Nat. Cell Biol. 13:4453–60
    [Google Scholar]
  84. Kressmann S, Campos C, Castanon I, Fürthauer M, González-Gaitán M 2015. Directional Notch trafficking in Sara endosomes during asymmetric cell division in the spinal cord. Nat. Cell Biol. 17:3333–39
    [Google Scholar]
  85. Kubo T, Yanagisawa H, Yagi T, Hirono M, Kamiya R 2010. Tubulin polyglutamylation regulates axonemal motility by modulating activities of inner-arm dyneins. Curr. Biol. 20:5441–45
    [Google Scholar]
  86. Lampson MA, Black BE. 2017. Cellular and molecular mechanisms of centromere drive. Cold Spring Harb. Symp. Quant. Biol. 82:249–57
    [Google Scholar]
  87. Lansbergen G, Grigoriev I, Mimori-Kiyosue Y, Ohtsuka T, Higa S et al. 2006. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5β. Dev. Cell 11:121–32
    [Google Scholar]
  88. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC et al. 2004. A standardized kinesin nomenclature. J. Cell Biol. 167:119–22
    [Google Scholar]
  89. Li R. 2013. The art of choreographing asymmetric cell division. Dev. Cell 25:5439–50
    [Google Scholar]
  90. Liao G, Gundersen GG. 1998. Kinesin is a candidate for cross-bridging microtubules and intermediate filaments: selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273:169797–803
    [Google Scholar]
  91. Lipka J, Kapitein LC, Jaworski J, Hoogenraad CC 2016. Microtubule-binding protein doublecortin-like kinase 1 (DCLK1) guides kinesin-3-mediated cargo transport to dendrites. EMBO J 35:3302–18
    [Google Scholar]
  92. Liu JS, Schubert CR, Fu X, Fourniol FJ, Jaiswal JK et al. 2012. Molecular basis for specific regulation of neuronal kinesin-3 motors by doublecortin family proteins. Mol. Cell 47:5707–21
    [Google Scholar]
  93. Luxton GW, Gundersen GG. 2011. Orientation and function of the nuclear-centrosomal axis during cell migration. Curr. Opin. Cell Biol. 23:5579–88
    [Google Scholar]
  94. Maheshwari A, Obbineni JM, Bui KH, Shibata K, Toyoshima YY, Ishikawa T 2015. α- and β-Tubulin lattice of the axonemal microtubule doublet and binding proteins revealed by single particle cryo-electron microscopy and tomography. Structure 23:91584–95
    [Google Scholar]
  95. Maniar TA, Kaplan M, Wang GJ, Shen K, Wei L et al. 2012. UNC-33 (CRMP) and ankyrin organize microtubules and localize kinesin to polarize axon-dendrite sorting. Nat. Neurosci. 15:148–56
    [Google Scholar]
  96. Manka SW, Moores CA. 2018. Microtubule structure by cryo-EM: snapshots of dynamic instability. Essays Biochem 62:6737–51
    [Google Scholar]
  97. Matis M, Russler-Germain DA, Hu Q, Tomlin CJ, Axelrod JD 2014. Microtubules provide directional information for core PCP function. eLife 3:e02893
    [Google Scholar]
  98. Mattie FJ, Stackpole MM, Stone MC, Clippard JR, Rudnick DA et al. 2010. Directed microtubule growth, +TIPs, and kinesin-2 are required for uniform microtubule polarity in dendrites. Curr. Biol. 20:242169–77
    [Google Scholar]
  99. McKenney RJ, Huynh W, Tanenbaum ME, Bhabha G, Vale RD 2014. Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science 345:6194337–41
    [Google Scholar]
  100. McKenney RJ, Huynh W, Vale RD, Sirajuddin M 2016. Tyrosination of α‐tubulin controls the initiation of processive dynein-dynactin motility. EMBO J 35:111175–85
    [Google Scholar]
  101. McNally FJ, Roll-Mecak A. 2018. Microtubule-severing enzymes: from cellular functions to molecular mechanism. J. Cell Biol. 217:124057–69
    [Google Scholar]
  102. McVicker DP, Chrin LR, Berger CL 2011. The nucleotide-binding state of microtubules modulates kinesin processivity and the ability of tau to inhibit kinesin-mediated transport. J. Biol. Chem. 286:5042873–80
    [Google Scholar]
  103. Meng W, Mushika Y, Ichii T, Takeichi M 2008. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135:5948–59
    [Google Scholar]
  104. Miller PM, Folkmann AW, Maia ARR, Efimova N, Efimov A, Kaverina I 2009. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat. Cell Biol. 11:91069–80
    [Google Scholar]
  105. Mimori-Kiyosue Y. 2011. Shaping microtubules into diverse patterns: molecular connections for setting up both ends. Cytoskeleton 68:11603–18
    [Google Scholar]
  106. Mitchison HM, Valente EM. 2017. Motile and non-motile cilia in human pathology: from function to phenotypes. J. Pathol. 241:2294–309
    [Google Scholar]
  107. Mitchison T, Kirschner M. 1984. Dynamic instability of microtubule growth. Nature 312:5991237–42
    [Google Scholar]
  108. Mogensen MM, Tucker JB, Stebbings H 1989. Microtubule polarities indicate that nucleation and capture of microtubules occurs at cell surfaces in Drosophila. J. Cell Biol 108:41445–52
    [Google Scholar]
  109. Mohan N, Sorokina EM, Verdeny IV, Alvarez AS, Lakadamyali M 2018. Detyrosinated microtubules spatially constrain lysosomes facilitating lysosome-autophagosome fusion. J. Cell Biol. 218:2632–43
    [Google Scholar]
  110. Monroy BY, Sawyer DL, Ackermann BE, Borden MM, Tan TC, Ori-McKenney KM 2018. Competition between microtubule-associated proteins directs motor transport. Nat. Commun. 9:11487
    [Google Scholar]
  111. Muto E, Sakai H, Kaseda K 2005. Long-range cooperative binding of kinesin to a microtubule in the presence of ATP. J. Cell Biol. 168:5691–96
    [Google Scholar]
  112. Nakata T, Hirokawa N. 2003. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J. Cell Biol. 162:61045–55
    [Google Scholar]
  113. Nashchekin D, Fernandes AR, St. Johnston D 2016. Patronin/Shot cortical foci assemble the noncentrosomal microtubule array that specifies the Drosophila anterior-posterior axis. Dev. Cell 38:161–72
    [Google Scholar]
  114. Nirschl JJ, Ghiretti AE, Holzbaur ELF 2017. The impact of cytoskeletal organization on the local regulation of neuronal transport. Nat. Rev. Neurosci. 18:10585–97
    [Google Scholar]
  115. Nirschl JJ, Magiera MM, Lazarus JE, Janke C, Holzbaur ELF 2016. α-Tubulin tyrosination and CLIP-170 phosphorylation regulate the initiation of dynein-driven transport in neurons. Cell Rep 14:112637–52
    [Google Scholar]
  116. Nogales E, Zhang R. 2016. Visualizing microtubule structural transitions and interactions with associated proteins. Curr. Opin. Struct. Biol. 37:90–96
    [Google Scholar]
  117. Noordstra I, Liu Q, Nijenhuis W, Hua S, Jiang K et al. 2016. Control of apico-basal epithelial polarity by the microtubule minus-end-binding protein CAMSAP3 and spectraplakin ACF7. J. Cell Sci. 129:224278–88
    [Google Scholar]
  118. Oladipo A, Cowan A, Rodionov V 2007. Microtubule motor Ncd induces sliding of microtubules in vivo. Mol. Biol. Cell 18:93601–6
    [Google Scholar]
  119. Olofsson J, Sharp KA, Matis M, Cho B, Axelrod JD 2014. Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity. Development 141:142866–74
    [Google Scholar]
  120. Parton RM, Hamilton RS, Ball G, Yang L, Cullen CF et al. 2011. A PAR-1-dependent orientation gradient of dynamic microtubules directs posterior cargo transport in the Drosophila oocyte. J. Cell Biol. 194:1121–35
    [Google Scholar]
  121. Peet DR, Burroughs NJ, Cross RA 2018. Kinesin expands and stabilizes the GDP-microtubule lattice. Nat. Nanotechnol. 13:5386–91
    [Google Scholar]
  122. Peris L, Wagenbach M, Lafanechère L, Brocard J, Moore AT et al. 2009. Motor-dependent microtubule disassembly driven by tubulin tyrosination. J. Cell Biol. 185:71159–66
    [Google Scholar]
  123. Petry S, Groen AC, Ishihara K, Mitchison TJ, Vale RD 2013. Branching microtubule nucleation in Xenopus egg extracts mediated by Augmin and TPX2. Cell 152:4768–77
    [Google Scholar]
  124. Prevo B, Mangeol P, Oswald F, Scholey JM, Peterman EJG 2015. Functional differentiation of cooperating kinesin-2 motors orchestrates cargo import and transport in C. elegans cilia. Nat. Cell Biol. 17:121536–45
    [Google Scholar]
  125. Prevo B, Scholey JM, Peterman EJG 2017. Intraflagellar transport: mechanisms of motor action, cooperation, and cargo delivery. FEBS J 284:182905–31
    [Google Scholar]
  126. Prosser SL, Pelletier L. 2017. Mitotic spindle assembly in animal cells: a fine balancing act. Nat. Rev. Mol. Cell Biol. 18:3187–201
    [Google Scholar]
  127. Pu J, Guardia CM, Keren-Kaplan T, Bonifacino JS 2016. Mechanisms and functions of lysosome positioning. J. Cell Sci. 129:234329–39
    [Google Scholar]
  128. Qiang L, Yu W, Andreadis A, Luo M, Baas PW 2006. Tau protects microtubules in the axon from severing by katanin. J. Neurosci. 26:123120–29
    [Google Scholar]
  129. Quinlan ME. 2016. Cytoplasmic streaming in the Drosophila oocyte. Annu. Rev. Cell Dev. Biol. 32:1173–95
    [Google Scholar]
  130. Quintin S, Wang S, Pontabry J, Bender A, Robin F et al. 2016. Non-centrosomal epidermal microtubules act in parallel to LET-502/ROCK to promote C. elegans elongation. Development 143:1160–73
    [Google Scholar]
  131. Reck-Peterson SL, Redwine WB, Vale RD, Carter AP 2018. The cytoplasmic dynein transport machinery and its many cargoes. Nat. Rev. Mol. Cell Biol. 19:6382–98
    [Google Scholar]
  132. Redwine WB, DeSantis ME, Hollyer I, Htet ZM, Tran PT et al. 2017. The human cytoplasmic dynein interactome reveals novel activators of motility. eLife 6:e28257
    [Google Scholar]
  133. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E et al. 2006. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16:212166–72
    [Google Scholar]
  134. Roll-Mecak A. 2019. How cells exploit tubulin diversity to build functional cellular microtubule mosaics. Curr. Opin. Cell Biol. 56:102–8
    [Google Scholar]
  135. Rolls MM. 2011. Neuronal polarity in Drosophila: sorting out axons and dendrites. Dev. Neurobiol. 71:6419–29
    [Google Scholar]
  136. Roman W, Gomes ER. 2018. Nuclear positioning in skeletal muscle. Semin. Cell Dev. Biol. 82:51–56
    [Google Scholar]
  137. Sanchez AD, Feldman JL. 2017. Microtubule-organizing centers: from the centrosome to non-centrosomal sites. Curr. Opin. Cell Biol. 44:93–101
    [Google Scholar]
  138. Sánchez-Huertas C, Freixo F, Viais R, Lacasa C, Soriano E, Lüders J 2016. Non-centrosomal nucleation mediated by augmin organizes microtubules in post-mitotic neurons and controls axonal microtubule polarity. Nat. Commun. 7:112187
    [Google Scholar]
  139. Schlager MA, Hoang HT, Urnavicius L, Bullock SL, Carter AP 2014. In vitro reconstitution of a highly processive recombinant human dynein complex. EMBO J 33:171855–68
    [Google Scholar]
  140. Schlager MA, Kapitein LC, Grigoriev I, Burzynski GM, Wulf PS et al. 2010. Pericentrosomal targeting of Rab6 secretory vesicles by Bicaudal-D-related protein 1 (BICDR-1) regulates neuritogenesis. EMBO J 29:101637–51
    [Google Scholar]
  141. Schmidt-Cernohorska M, Zhernov I, Steib E, Le Guennec M, Achek R et al. 2019. Flagellar microtubule doublet assembly in vitro reveals a regulatory role of tubulin C-terminal tails. Science 363:6424285–88
    [Google Scholar]
  142. Schmoranzer J, Kreitzer G, Simon SM, Migala A, Almers W, Gerdes HH 2003. Migrating fibroblasts perform polarized, microtubule-dependent exocytosis towards the leading edge. J. Cell Sci. 116:Pt 224513–19
    [Google Scholar]
  143. Shigematsu H, Imasaki T, Doki C, Sumi T, Aoki M et al. 2018. Structural insight into microtubule stabilization and kinesin inhibition by Tau family MAPs. J. Cell Biol. 217:124155–63
    [Google Scholar]
  144. Shima T, Morikawa M, Kaneshiro J, Kambara T, Kamimura S et al. 2018. Kinesin-binding-triggered conformation switching of microtubules contributes to polarized transport. J. Cell Biol. 217:124164–83
    [Google Scholar]
  145. Shimada Y, Yonemura S, Ohkura H, Strutt D, Uemura T 2006. Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev. Cell 10:2209–22
    [Google Scholar]
  146. Silva M, Morsci N, Nguyen KCQ, Rizvi A, Rongo C et al. 2017. Cell-specific α-tubulin isotype regulates ciliary microtubule ultrastructure, intraflagellar transport, and extracellular vesicle biology. Curr. Biol. 27:7968–80
    [Google Scholar]
  147. Singh A, Saha T, Begemann I, Ricker A, Nüsse H et al. 2018. Polarized microtubule dynamics directs cell mechanics and coordinates forces during epithelial morphogenesis. Nat. Cell Biol. 20:101126–33
    [Google Scholar]
  148. Sirajuddin M, Rice LM, Vale RD 2014. Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat. Cell Biol. 16:4335–44
    [Google Scholar]
  149. Snow JJ, Ou G, Gunnarson AL, Walker MRS, Zhou HM et al. 2004. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6:111109–13
    [Google Scholar]
  150. Song Y, Brady ST. 2015. Post-translational modifications of tubulin: pathways to functional diversity of microtubules. Trends Cell Biol 25:3125–36
    [Google Scholar]
  151. 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 23:214226–41
    [Google Scholar]
  152. 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 8:4e1000350
    [Google Scholar]
  153. St. Johnston D 2005. Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 6:5363–75
    [Google Scholar]
  154. Stehbens S, Wittmann T. 2012. Targeting and transport: how microtubules control focal adhesion dynamics. J. Cell Biol. 198:4481–89
    [Google Scholar]
  155. Stehbens SJ, Paszek M, Pemble H, Ettinger A, Gierke S, Wittmann T 2014. CLASPs link focal-adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover. Nat. Cell Biol. 16:6561–73
    [Google Scholar]
  156. Stepanek L, Pigino G. 2016. Microtubule doublets are double-track railways for intraflagellar transport trains. Science 352:6286721–24
    [Google Scholar]
  157. Stepanova T, Slemmer J, Hoogenraad CC, Lansbergen G, Dortland B et al. 2003. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23:72655–64
    [Google Scholar]
  158. Stinchcombe JC, Majorovits E, Bossi G, Fuller S, Griffiths GM 2006. Centrosome polarization delivers secretory granules to the immunological synapse. Nature 443:7110462–65
    [Google Scholar]
  159. Stone MC, Roegiers F, Rolls MM 2008. Microtubules have opposite orientation in axons and dendrites of Drosophila neurons. Mol. Biol. Cell 19:104122–29
    [Google Scholar]
  160. Suryavanshi S, Eddé B, Fox LA, Guerrero S, Hard R et al. 2010. Tubulin glutamylation regulates ciliary motility by altering inner dynein arm activity. Curr. Biol. 20:5435–40
    [Google Scholar]
  161. Sweeney HL, Holzbaur ELF. 2018. Motor proteins. Cold Spring Harb. Perspect. Biol. 10:5a021931
    [Google Scholar]
  162. Tas RP, Chazeau A, Cloin BMC, Lambers MLA, Hoogenraad CC, Kapitein LC 2017. Differentiation between oppositely oriented microtubules controls polarized neuronal transport. Neuron 96:61264–71.e5
    [Google Scholar]
  163. Toya M, Kobayashi S, Kawasaki M, Shioi G, Kaneko M et al. 2016. CAMSAP3 orients the apical-to-basal polarity of microtubule arrays in epithelial cells. PNAS 113:2332–37
    [Google Scholar]
  164. Toya M, Takeichi M. 2016. Organization of non-centrosomal microtubules in epithelial cells. Cell Struct. Funct. 41:2127–35
    [Google Scholar]
  165. Troutt LL, Burnside B. 1988. The unusual microtubule polarity in teleost retinal pigment epithelial cells. J. Cell Biol. 107:41461–64
    [Google Scholar]
  166. Vale RD. 2003. The molecular motor toolbox for intracellular transport. Cell 112:4467–80
    [Google Scholar]
  167. Valenstein ML, Roll-Mecak A. 2016. Graded control of microtubule severing by tubulin glutamylation. Cell 164:5911–21
    [Google Scholar]
  168. van Bergeijk P, Adrian M, Hoogenraad CC, Kapitein LC 2015. Optogenetic control of organelle transport and positioning. Nature 518:7537111–14
    [Google Scholar]
  169. Verhey KJ, Gaertig J. 2007. The tubulin code. Cell Cycle 6:172152–60
    [Google Scholar]
  170. Vershinin M, Carter BC, Razafsky DS, King SJ, Gross SP 2007. Multiple-motor based transport and its regulation by Tau. PNAS 104:187–92
    [Google Scholar]
  171. Vershinin M, Xu J, Razafsky DS, King SJ, Gross SP 2008. Tuning microtubule-based transport through filamentous MAPs: the problem of dynein. Traffic 9:6882–92
    [Google Scholar]
  172. Winding M, Kelliher MT, Lu W, Wildonger J, Gelfand VI 2016. Role of kinesin-1-based microtubule sliding in Drosophila nervous system development. PNAS 113:34E4985–94
    [Google Scholar]
  173. Wloga D, Joachimiak E, Louka P, Gaertig J 2017. Posttranslational modifications of tubulin and cilia. Cold Spring Harb. Perspect. Biol. 9:6a028159
    [Google Scholar]
  174. Wood KW, Sakowicz R, Goldstein LS, Cleveland DW 1997. CENP-E is a plus end–directed kinetochore motor required for metaphase chromosome alignment. Cell 91:3357–66
    [Google Scholar]
  175. Wu J, Akhmanova A. 2017. Microtubule-organizing centers. Annu. Rev. Cell Dev. Biol. 33:51–75
    [Google Scholar]
  176. Xu J, King SJ, Lapierre-Landry M, Nemec B 2013. Interplay between velocity and travel distance of kinesin-based transport in the presence of tau. Biophys. J. 105:10L23–25
    [Google Scholar]
  177. Yang Z, Tulu US, Wadsworth P, Rieder CL 2007. Kinetochore dynein is required for chromosome motion and congression independent of the spindle checkpoint. Curr. Biol. 17:11973–80
    [Google Scholar]
  178. Yau KW, Schatzle P, Tortosa E, Pages S, Holtmaat A et al. 2016. Dendrites in vitro and in vivo contain microtubules of opposite polarity and axon formation correlates with uniform plus-end-out microtubule orientation. J. Neurosci. 36:41071–85
    [Google Scholar]
  179. Yogev S, Cooper R, Fetter R, Horowitz M, Shen K 2016. Microtubule organization determines axonal transport dynamics. Neuron 92:2449–60
    [Google Scholar]
  180. Yu I, Garnham CP, Roll-Mecak A 2015. Writing and reading the tubulin code. J. Biol. Chem. 290:2817163–72
    [Google Scholar]
  181. Zhang R, Alushin GM, Brown A, Nogales E 2015. Mechanistic origin of microtubule dynamic instability and its modulation by EB proteins. Cell 162:4849–59
    [Google Scholar]
  182. Zimyanin VL, Belaya K, Pecreaux J, Gilchrist MJ, Clark A et al. 2008. In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134:5843–53
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100818-125149
Loading
/content/journals/10.1146/annurev-cellbio-100818-125149
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error