The role of the cytoskeleton and molecular motors in endosomal dynamics

Seminars in Cell and Developmental Biology

Volumn 31, Issue , 2014, Pages 20-29

  Granger, Elizabeth ^a   McNee, Gavin ^a   Allan, Victoria ^a   Woodman, Philip ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Dynein; Endosome; Kinesin; Lysosome; Myosin; Recycling

Indexed keywords

ACTIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; KINESIN 1; KINESIN 14; KINESIN 3; MOLECULAR MOTOR; MYOSIN; MYOSIN IB; MYOSIN IE; MYOSIN VA; MYOSIN VB; MYOSIN VI; PROTEIN KIF5; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CELL ADHESION; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; HUMAN; LYSOSOME; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; NUTRIENT UPTAKE; PHAGOCYTOSIS; PINOCYTOSIS; REVIEW; ANIMAL; METABOLISM;

ACTINS; ANIMALS; CELL MEMBRANE; CYTOSKELETON; ENDOSOMES; HUMANS; MOLECULAR MOTOR PROTEINS;

EID: 84901986407     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.04.011     Document Type: Review

References (166)

1. Miaczynska M., Christoforidis S., Giner A., Shevchenko A., Uttenweiler-Joseph S., Habermann B., et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004, 116:445-456.
2. Danson C., Brown E., Hemmings O.J., McGough I.J., Yarwood S., Heesom K.J., et al. SNX15 links clathrin endocytosis to the PtdIns3P early endosome independently of the APPL1 endosome. J Cell Sci 2013, 126:4885-4899.
3. Burd C., Cullen P.J. Retromer A master conductor of endosome sorting. Cold Spring Harb Perspect Biol 2014, 6:a016774.
4. Kouranti I., Sachse M., Arouche N., Goud B., Echard A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 2006, 16:1719-1725.
5. van der Sluijs P., Hull M., Webster P., Mâle P., Goud B., Mellman I. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 1992, 70:729-740.
6. Ullrich O., Reinsch S., Urbé S., Zerial M., Parton R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 1996, 135:913-924.
7. Kelly E.E., Horgan C.P., McCaffrey M.W. Rab11 proteins in health and disease. Biochem Soc Trans 2012, 40:1360-1367.
8. Yamashiro D.J., Tycko B., Fluss S.R., Maxfield F.R. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 1984, 37:789-800.
9. Kull F.J., Endow S.A. Force generation by kinesin and myosin cytoskeletal motor proteins. J Cell Sci 2013, 126:9-19.
10. Allan V. Cytoplasmic dynein. Biochem Soc Trans 2011, 39:1169.
11. Kardon J.R., Vale R.D. Regulators of the cytoplasmic dynein motor. Nat Rev Mol Cell Biol 2009, 10:854-865.
12. Hirokawa N., Noda Y., Tanaka Y., Niwa S. Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 2009, 10:682-696.
13. Hartman M.A., Spudich J.A. The myosin superfamily at a glance. J Cell Sci 2012, 125:1627-1632.
14. Wozniak M.J., Milner R., Allan V. N-terminal kinesins: many and various. Traffic 2004, 5:400-410.
15. Kull F.J., Sablin E.P., Lau R., Fletterick R.J., Vale R.D. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 1996, 380:550-555.
16. Taunton J., Rowning B.A., Coughlin M.L., Wu M., Moon R.T., Mitchison T.J., et al. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol 2000, 148:519-530.
17. Doherty G.J., McMahon H.T. Mechanisms of endocytosis. Annu Rev Biochem 2009, 78:857-902.
18. Humphries A.C., Way M. The non-canonical roles of clathrin and actin in pathogen internalization, egress and spread. Nat Rev Mol Microbiol 2013, 11:551-560.
19. Mooren O.L., Galletta B.J., Cooper J.A. Roles for actin assembly in endocytosis. Ann Rev Biochem 2012, 81:661-686.
20. Aghamohammadzadeh S., Ayscough K.R. Differential requirements for actin during yeast and mammalian endocytosis. Nat Cell Biol 2009, 11:1039-U283.
21. Boulant S., Kural C., Zeeh J.-C., Ubelmann F., Kirchhausen T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 2011, 13:1124-1131.
22. Cureton D.K., Massol R.H., Saffarian S., Kirchhausen T.L., Whelan S.P. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 2009, 5:e1000394.
23. Collins A., Warrington A., Taylor K.A., Svitkina T. Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr Biol 2011, 21:1167-1175.
24. Sun Y.D., Martin A.C., Drubin D.G. Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Dev Cell 2006, 11:33-46.
25. Cheng J., Grassart A., Drubin D.G. Myosin 1E coordinates actin assembly and cargo trafficking during clathrin-mediated endocytosis. Mol Biol Cell 2012, 23:2891-2904.
26. Krendel M., Osterweil E.K., Mooseker M.S. Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 2007, 581:644-650.
27. Tang N., Lin T., Ostap E.M. Dynamics of myo1c (myosin-ibeta) lipid binding and dissociation. J Biol Chem 2002, 277:42763-42768.
28. Nambiar R., McConnell R.E., Tyska M.J. Control of cell membrane tension by myosin-I. Proc Natl Acad Sci U S A 2009, 106:11972-11977.
29. Merrifield C.J., Moss S.E., Ballestrem C., Imhof B.A., Giese G., Wunderlich I., et al. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol 1999, 1:72-74.
30. Taylor M.J., Perrais D., Merrifield C.J. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 2011, 9:e1000604.
31. Buss F., Arden S.D., Lindsay M., Luzio J.P., Kendrick-Jones J. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J 2001, 20:3676-3684.
32. Inoue A., Sato O., Homma K., Ikebe M. DOC-2/DAB2 is the binding partner of myosin VI. Biochem Biophys Res Commun 2002, 292:300-307.
33. Morris S.M., Arden S.D., Roberts R.C., Kendrick-Jones J., Cooper J.A., Luzio J.P., et al. Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 2002, 3:331-341.
34. Aschenbrenner L., Lee T., Hasson T. Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol Biol Cell 2003, 14:2728-2743.
35. Naccache S.N., Hasson T., Horowitz A. Binding of internalized receptors to the PDZ domain of GIPC/synectin recruits myosin VI to endocytic vesicles. Proc Natl Acad Sci U S A 2006, 103:12735-12740.
36. Zoncu R., Perera R.M., Balkin D.M., Pirruccello M., Toomre D., De Camilli P. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 2009, 136:1110-1121.
37. Varsano T., Dong M.-Q., Niesman I., Gacula H., Lou X., Ma T., et al. GIPC is recruited by APPL to peripheral TrkA endosomes and regulates TrkA trafficking and signaling. Mol Cell Biol 2006, 26:8942-8952.
38. Lin D.C., Quevedo C., Brewer N.E., Bell A., Testa J.R., Grimes M.L., et al. APPL1 associates with TrkA and GIPC1 and is required for nerve growth factor-mediated signal transduction. Mol Cell Biol 2006, 26:8928-8941.
39. Tumbarello D.A., Waxse B.J., Arden S.D., Bright N.A., Kendrick-Jones J., Buss F. Autophagy receptors link myosin VI to autophagosomes to mediate Tom1-dependent autophagosome maturation and fusion with the lysosome. Nat Cell Biol 2012, 14:1024-1035.
40. Ross C.A., Tabrizi S.J. Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol 2011, 10:83-98.
41. Velier J., Kim M., Schwarz C., Kim T.W., Sapp E., Chase K., et al. Wild-type and mutant huntingtins function in vesicle trafficking in the secretory and endocytic pathways. Exp Neurol 1998, 152:34-40.
42. Caviston J.P., Ross J.L., Antony S.M., Tokito M., Holzbaur E.L. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc Natl Acad Sci U S A 2007, 104:10045-10050.
43. McGuire J.R., Rong J., Li S.-H., Li X.-J. Interaction of huntingtin-associated protein-1 with kinesin light chain: implications in intracellular trafficking in neurons. J Biol Chem 2006, 281:3552-3559.
44. Engelender S., Sharp A.H., Colomer V., Tokito M.K., Lanahan A., Worley P., et al. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued bubunit of dynactin. Hum Mol Genet 1997, 6:2205-2212.
45. Caviston J.P., Zajac A.L., Tokito M., Holzbaur E.L. Huntingtin coordinates the dynein-mediated dynamic positioning of endosomes and lysosomes. Mol Biol Cell 2011, 22:478-492.
46. Pal A., Severin F., Lommer B., Shevchenko A., Zerial M. Huntingtin - HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington's disease. J Cell Biol 2006, 172:605-618.
47. Morel E., Parton R.G., Gruenberg J. Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev Cell 2009, 16:445-457.
48. Gasman S., Kalaidzidis Y., Zerial M. RhoD regulates endosome dynamics through diaphanous-related formin and Src tyrosine kinase. Nat Cell Biol 2003, 5:195-204.
49. Nielsen E., Severin F., Backer J.M., Hyman A.A., Zerial M. Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1999, 1:376-382.
50. Driskell O.J., Mironov A., Allan V.J., Woodman P.G. Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nat Cell Biol 2007, 9:113-120.
51. Rogers S.S., Flores-Rodriguez N., Allan V.J., Woodman P.G., Waigh T.A. The first passage probability of intracellular particle trafficking. Phys Chem Chem Phys 2010, 12:3753-3761.
52. Flores-Rodriguez N., Rogers S.S., Kenwright D.A., Waigh T.A., Woodman P.G., Allan V.J. Roles of dynein and dynactin in early endosome dynamics revealed using automated tracking and global analysis. PLoS ONE 2011, 6:e24479.
53. Zajac A.L., Goldman Y.E., Holzbaur E.L., Ostap E.M. Local cytoskeletal and organelle interactions impact molecular-motor-driven early endosomal trafficking. Curr Biol 2013, 23:1173-1180.
54. Rink J., Ghigo E., Kalaidzidis Y., Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122:735-749.
55. Eden E.R., White I.J., Tsapara A., Futter C.E. Membrane contacts between endosomes and ER provide sites for PTP1B - epidermal growth factor receptor interaction. Nat Cell Biol 2010, 12:267-272.
56. Foret L., Dawson J.E., Villaseñor R., Collinet C., Deutsch A., Brusch L., et al. A general theoretical framework to infer endosomal network dynamics from quantitative image analysis. Curr Biol 2012, 22:1381-1390.
57. Yi J.Y., Ori-McKenney K.M., McKenney R.J., Vershinin M., Gross S.P., Vallee R.B. High-resolution imaging reveals indirect coordination of opposite motors and a role for LIS1 in high-load axonal transport. J Cell Biol 2011, 195:193-201.
58. Hunt S.D., Townley A.K., Danson C.M., Cullen P.J., Stephens D.J. Microtubule motors mediate endosomal sorting by maintaining functional domain organization. J Cell Sci 2013, 126:2493-2501.
59. Lam C., Vergnolle M.A., Thorpe L., Woodman P.G., Allan V.J. Functional interplay between LIS1, NDE1 and NDEL1 in dynein-dependent organelle positioning. J Cell Sci 2010, 123:202-212.
60. Palmer K.J., Hughes H., Stephens D.J. Specificity of cytoplasmic dynein subunits in discrete membrane-trafficking steps. Mol Biol Cell 2009, 20:2885-2899.
61. Valetti C., Wetzel D.M., Schrader M., Hasbani M.J., Gill S.R., Kreis T.E., et al. Role of dynactin in endocytic traffic: effects of dynamitin overexpression and colocalization with CLIP-170. Mol Biol Cell 1999, 10:4107-4120.
62. Habermann A., Schroer T.A., Griffiths G., Burkhardt J.K. Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J Cell Sci 2001, 114:229-240.
63. Tan S.C., Scherer J., Vallee R.B. Recruitment of dynein to late endosomes and lysosomes through light intermediate chains. Mol Biol Cell 2011, 22:467-477.
64. Loubery S., Wilhelm C., Hurbain I., Neveu S., Louvard D., Coudrier E. Different microtubule motors move early and late endocytic compartments. Traffic 2008, 9:492-509.
65. Bananis E., Nath S., Gordon K., Satir P., Stockert R.J., Murray J.W., et al. Microtubule-dependent movement of late endocytic vesicles in vitro: requirements for Dynein and Kinesin. Mol Biol Cell 2004, 15:3688-3697.
66. Bananis E., Murray J.W., Stockert R.J., Satir P., Wolkoff A.W. Regulation of early endocytic vesicle motility and fission in a reconstituted system. J Cell Sci 2003, 116:2749-2761.
67. Nath S., Bananis E., Sarkar S., Stockert R.J., Sperry A.O., Murray J.W., et al. Kif5B and Kifc1 interact and are required for motility and fission of early endocytic vesicles in mouse liver. Mol Biol Cell 2007, 18:1839-1849.
68. Galjart N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr Biol 2010, 20:R528-R537.
69. Lansbergen G., Komarova Y., Modesti M., Wyman C., Hoogenraad C.C., Goodson H.V., et al. Conformational changes in CLIP-170 regulate its binding to microtubules and dynactin localization. J Cell Biol 2004, 166:1003-1014.
70. Vaughan K.T., Tynan S.H., Faulkner N.E., Echeverri C.J., Vallee R.B. Colocalization of cytoplasmic dynein with dynactin and CLIP-170 at microtubule distal ends. J Cell Sci 1999, 112(Pt 10):1437-1447.
71. Lenz J., Schuchardt I., Straube A., Steinberg G. A dynein loading zone for retrograde endosome motility at microtubule plus-ends. EMBO J 2006, 25:2275-2286.
72. Egan M.J., Tan K., Reck-Peterson S.L. Lis1 is an initiation factor for dynein-driven organelle transport. J Cell Biol 2012, 197:971-982.
73. Waterman-Storer C.M., Karki S., Holzbaur E.L. The p150Glued component of the dynactin complex binds to both microtubules and the actin-related protein centractin (Arp-1). Proc Natl Acad Sci U S A 1995, 92:1634-1638.
74. Culver-Hanlon T.L., Lex S.A., Stephens A.D., Quintyne N.J., King S.J. A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat Cell Biol 2006, 8:264-270.
75. King S.J., Schroer T.A. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat Cell Biol 2000, 2:20-24.
76. Moughamian A.J., Holzbaur E.L. Dynactin is required for transport initiation from the distal axon. Neuron 2012, 74:331-343.
77. Moughamian A.J., Osborn G.E., Lazarus J.E., Maday S., Holzbaur E.L. Ordered recruitment of dynactin to the microtubule plus-end is required for efficient initiation of retrograde axonal transport. J Neurosci 2013, 33:13190-13203.
78. Glued CAP-Gly domain regulates initiation of retrograde transport at synaptic termini. Neuron 2012, 74:344-360.
79. Lomakin A.J., Semenova I., Zaliapin I., Kraikivski P., Nadezhdina E., Slepchenko B.M., et al. CLIP-170-dependent capture of membrane organelles by microtubules initiates minus-end directed transport. Dev Cell 2009, 17:323-333.
80. Watson P., Stephens D.J. Microtubule plus-end loading of p150(Glued) is mediated by EB1 and CLIP-170 but is not required for intracellular membrane traffic in mammalian cells. J Cell Sci 2006, 119:2758-2767.
81. Dixit R., Levy J.R., Tokito M., Ligon L.A., Holzbaur E.L. Regulation of dynactin through the differential expression of p150Glued isoforms. J Biol Chem 2008, 283:33611-33619.
82. Kim H., Ling S.-C., Rogers G.C., Kural C., Selvin P.R., Rogers S.L., et al. Microtubule binding by dynactin is required for microtubule organization but not cargo transport. J Cell Biol 2007, 176:641-651.
83. Steinberg G. Motors in fungal morphogenesis: cooperation versus competition. Curr Opin Microbiol 2011, 14:660-667.
84. Peñalva M.Á. Endocytosis in filamentous fungi: cinderella gets her reward. Curr Opin Microbiol 2010, 13:684-692.
85. Zhang J., Li S., Fischer R., Xiang X. Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol Biol Cell 2003, 14:1479-1488.
86. Schuster M., Kilaru S., Ashwin P., Lin C., Severs N.J., Steinberg G. Controlled and stochastic retention concentrates dynein at microtubule ends to keep endosomes on track. EMBO J 2011, 30:652-664.
87. Zhang J., Zhuang L., Lee Y., Abenza J.F., Peñalva M.A., Xiang X. The microtubule plus-end localization of Aspergillus dynein is important for dynein - early-endosome interaction but not for dynein ATPase activation. J Cell Sci 2010, 123:3596-3604.
88. Schuster M., Lipowsky R., Assmann M.-A., Lenz P., Steinberg G. Transient binding of dynein controls bidirectional long-range motility of early endosomes. Proc Natl Acad Sci U S A 2011, 108:3618-3623.
89. Satoh D., Sato D., Tsuyama T., Saito M., Ohkura H., Rolls M.M., et al. Spatial control of branching within dendritic arbors by dynein-dependent transport of Rab5-endosomes. Nat Cell Biol 2008, 10:1164-1171.
90. Bielli A., Thörnqvist P.-O., Hendrick A.G., Finn R., Fitzgerald K., McCaffrey M.W. The small GTPase Rab4A interacts with the central region of cytoplasmic dynein light intermediate chain-1. Biochem Biophys Res Commun 2001, 281:1141-1153.
91. Ha J., Lo K.W.-H., Myers K.R., Carr T.M., Humsi M.K., Rasoul B.A., et al. A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. J Cell Biol 2008, 181:1027-1039.
92. Zhang J., Yao X., Fischer L., Abenza J.F., Peñalva M.A., Xiang X. The p25 subunit of the dynactin complex is required for dynein - early endosome interaction. J Cell Biol 2011, 193:1245-1255.
93. Yeh T.-Y., Quintyne N.J., Scipioni B.R., Eckley D.M., Schroer T.A. Dynactin's pointed-end complex is a cargo-targeting module. Mol Biol Cell 2012, 23:3827-3837.
94. Zhang J., Qiu R., Arst H.N., Penalva M.A., Xiang X. HookA is a novel dynein-early endosome linker critical for cargo movement in vivo. J Cell Biol 2014, 204:1009-1026.
95. Bielska E., Schuster M., Roger Y., Berepiki A., Soanes D.M., Talbot N.J., et al. Hook is an adapter that coordinates kinesin-3 and dynein cargo attachment on early endosomes. J Cell Biol 2014, 204:989-1007.
96. Johansson M., Rocha N., Zwart W., Jordens I., Janssen L., Kuijl C., et al. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150(Glued), ORP1L, and the receptor beta III spectrin. J Cell Biol 2007, 176:459-471.
97. Jordens I., Fernandez-Borja M., Marsman M., Dusseljee S., Janssen L., Calafat J., et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol 2001, 11:1680-1685.
98. Balderhaar H.J.k., Ungermann C. Corvet and HOPS tethering complexes - coordinators of endosome and lysosome fusion. J Cell Sci 2013, 126:1307-1316.
99. van der Kant R., Fish A., Janssen L., Janssen H., Krom S., Ho N., et al. Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J Cell Sci 2013, 126:3462-3474.
100. Drerup C.M., Nechiporuk A.V. JNK-interacting protein 3 mediates the retrograde transport of activated c-Jun N-terminal kinase and lysosomes. PLoS Genet 2013, 9:e1003303.
101. Lee H.H., Nemecek D., Schindler C., Smith W.J., Ghirlando R., Steven A.C., et al. Assembly and architecture of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J Biol Chem 2012, 287:5882-5890.
102. Cai Q., Lu L., Tian J.-H., Zhu Y.-B., Qiao H., Sheng Z.-H. Snapin-regulated late endosomal transport is critical for efficient autophagy-lysosomal function in neurons. Neuron 2010, 68:73-86.
103. Ye X., Cai Q. Snapin-mediated BACE1 retrograde transport is essential for its degradation in lysosomes and regulation of APP processing in neurons. Cell Rep 2014, 6:24-31.
104. Ivan V., Martinez-Sanchez E., Sima L.E., Oorschot V., Klumperman J., Petrescu S.M., et al. AP-3 and Rabip4' coordinately regulate spatial distribution of lysosomes. PLoS ONE 2012, 7:e48142.
105. Bananis E., Murray J.W., Stockert R.J., Satir P., Wolkoff A.W. Microtubule and motor-dependent endocytic vesicle sorting in vitro. J Cell Biol 2000, 151:179-186.
106. Huckaba T.M., Gennerich A., Wilhelm J.E., Chishti A.H., Vale R.D. Kinesin-73 is a processive motor that localizes to Rab5-containing organelles. J Biol Chem 2011, 286:7457-7467.
107. Hoepfner S., Severin F., Cabezas A., Habermann B., Runge A., Gillooly D., et al. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 2005, 121:437-450.
108. Perez Bay A.E., Schreiner R., Mazzoni F., Carvajal-Gonzalez J.M., Gravotta D., Perret E., et al. The kinesin KIF16B mediates apical transcytosis of transferrin receptor in AP-1B-deficient epithelia. EMBO J 2013, 32:2125-2139.
109. Brown C.L., Maier K.C., Stauber T., Ginkel L.M., Wordeman L., Vernos I., et al. Kinesin-2 is a motor for late endosomes and lysosomes. Traffic 2005, 6:1114-1124.
110. Heuser J. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J Cell Biol 1989, 108:855-864.
111. Nakata T., Hirokawa N. Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J Cell Biol 1995, 131:1039-1053.
112. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., et al. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998, 93:1147-1158.
113. Rosa-Ferreira C., Munro S. Arl8 and SKIP act together to link lysosomes to kinesin-1. Dev Cell 2011, 21:1171-1178.
114. Dumont A., Boucrot E., Drevensek S., Daire V., Gorvel J.P., Pous C., et al. SKIP, the host target of the Salmonella virulence factor SifA, promotes kinesin-1-dependent vacuolar membrane exchanges. Traffic 2010, 11:899-911.
115. Matsushita M., Tanaka S., Nakamura N., Inoue H., Kanazawa H. A novel kinesin-like protein, KIF1Bβ3 is involved in the movement of lysosomes to the cell periphery in non-neuronal cells. Traffic 2004, 5:140-151.
116. Santama N., Krijnse-Locker J., Griffiths G., Noda Y., Hirokawa N., Dotti C.G. KIF2beta, a new kinesin superfamily protein in non-neuronal cells, is associated with lysosomes and may be implicated in their centrifugal translocation. EMBO J 1998, 17:5855-5867.
117. Welte M.A. Bidirectional transport along microtubules. Curr Biol 2004, 14:R525-R537.
118. Hendricks A.G., Perlson E., Ross J.L., Schroeder H.W., Tokito M., Holzbaur E.L. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr Biol 2010, 20:697-702.
119. Muller M.J., Klumpp S., Lipowsky R. Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc Natl Acad Sci U S A 2008, 105:4609-4614.
120. Soppina V., Rai A.K., Ramaiya A.J., Barak P., Mallik R. Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc Natl Acad Sci U S A 2009, 106:19381-19386.
121. Ally S., Larson A.G., Barlan K., Rice S.E., Gelfand V.I. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J Cell Biol 2009, 187:1071-1082.
122. Colin E., Zala D., Liot G., Rangone H., Borrell-Pages M., Li X.J., et al. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J 2008, 27:2124-2134.
123. Bowman A.B., Kamal A., Ritchings B.W., Philp A.V., McGrail M., Gindhart J.G., et al. Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 2000, 103:583-594.
124. Verhey K.J., Meyer D., Deehan R., Blenis J., Schnapp B.J., Rapoport T.A., et al. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 2001, 152:959-970.
125. Byrd D.T., Kawasaki M., Walcoff M., Hisamoto N., Matsumoto K., Jin Y. UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 2001, 32:787-800.
126. Fu M.M., Holzbaur E.L.F. JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J Cell Biol 2013, 202:495-508.
127. Montagnac G., Sibarita J.B., Loubery S., Daviet L., Romao M., Raposo G., et al. ARF6 interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Curr Biol 2009, 19:184-195.
128. Wassmer T., Attar N., Harterink M., van Weering J.R.T., Traer C.J., Oakley J., et al. The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 2009, 17:110-122.
129. Traer C.J., Rutherford A.C., Palmer K.J., Wassmer T., Oakley J., Attar N., et al. SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat Cell Biol 2007, 9:1370-U55.
130. Horgan C.P., Hanscom S.R., Jolly R.S., Futter C.E., McCaffrey M.W. Rab11-FIP3 binds dynein light intermediate chain 2 and its overexpression fragments the Golgi complex. Biochem Biophys Res Commun 2010, 394:387-392.
131. Horgan C.P., Hanscom S.R., Jolly R.S., Futter C.E., McCaffrey M.W. Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J Cell Sci 2010, 123:181-191.
132. Delevoye C., Miserey-Lenkei S., Montagnac G., Gilles-Marsens F., Paul-Gilloteaux P., Giordano F., et al. Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Rep 2014, 6:445-454.
133. Schonteich E., Wilson G.M., Burden J., Hopkins C.R., Anderson K., Goldenring J.R., et al. The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J Cell Sci 2008, 121:3824-3833.
134. Schmidt M.R., Maritzen T., Kukhtina V., Higman V.A., Doglio L., Barak N.N., et al. Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc Natl Acad Sci U S A 2009, 106:15344-15349.
135. Winter J.F., Hopfner S., Korn K., Farnung B.O., Bradshaw C.R., Marsico G., et al. Caenorhabditis elegans screen reveals role of PAR-5 in RAB-11-recycling endosome positioning and apicobasal cell polarity. Nat Cell Biol 2012, 14:666-676.
136. Lin S.X., Gundersen G.G., Maxfield F.R. Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol Biol Cell 2002, 13:96-109.
137. Puthenveedu M.A., Lauffer B., Temkin P., Vistein R., Carlton P., Thorn K., et al. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 2010, 143:761-773.
138. Rotty J.D., Wu C., Bear J.E. New insights into the regulation and cellular functions of the ARP2/3 complex. Nat Rev Mol Cell Biol 2013, 14:7-12.
139. Seaman M., Gautreau A., Billadeau D.D. Retromer-mediated endosomal protein sorting: all WASHed up!. Trends Cell Biol 2013, 23:522-528.
140. Gomez T.S., Billadeau D.D. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev Cell 2009, 17:699-711.
141. Chibalina M.V., Seaman M.N., Miller C.C., Kendrick-Jones J., Buss F. Myosin VI and its interacting protein LMTK2 regulate tubule formation and transport to the endocytic recycling compartment. J Cell Sci 2007, 120:4278-4288.
142. Salas-Cortes L., Ye F., Tenza D., Wilhelm C., Theos A., Louvard D., et al. Myosin Ib modulates the morphology and the protein transport within multi-vesicular sorting endosomes. J Cell Sci 2005, 118:4823-4832.
143. Raposo G., Cordonnier M.N., Tenza D., Menichi B., Durrbach A., Louvard D., et al. Association of myosin I alpha with endosomes and lysosomes in mammalian cells. Mol Biol Cell 1999, 10:1477-1494.
144. Cordonnier M.-N., Dauzonne D., Louvard D., Coudrier E. Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol Biol Cell 2001, 12:4013-4029.
145. Lindsay A.J., Jollivet F., Horgan C.P., Khan A.R., Raposo G., McCaffrey M.W., et al. Identification and characterization of multiple novel Rab-myosin Va interactions. Mol Biol Cell 2013, 24:3420-3434.
146. Wagner W., Brenowitz S.D., Hammer J.A. Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat Cell Biol 2011, 13:40-48.
147. Wang Z., Edwards J.G., Riley N., Provance D.W., Karcher R., Li X.D., et al. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 2008, 135:535-548.
148. Schuh M. An actin-dependent mechanism for long-range vesicle transport. Nat Cell Biol 2011, 13:1431-1436.
149. Nelson S.R., Ali M.Y., Trybus K.M., Warshaw D.M. Random walk of processive, quantum dot-labeled myosin Va molecules within the actin cortex of COS-7 cells. Biophys J 2009, 97:509-518.
150. Hammer J.A., Sellers J.R. Walking to work: roles for class V myosins as cargo transporters. Nat Rev Mol Cell Biol 2012, 13:13-26.
151. Woolner S., Bement W.M. Unconventional myosins acting unconventionally. Trends Cell Biol 2009, 19:245-252.
152. Lapierre L.A., Kumar R., Hales C.M., Navarre J., Bhartur S.G., Burnette J.O., et al. Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 2001, 12:1843-1857.
153. Hales C.M., Vaerman J.P., Goldenring J.R. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 2002, 277:50415-50421.
154. Provance D.W., Gourley C.R., Silan C.M., Cameron L., Shokat K.M., Goldenring J.R., et al. Chemical-genetic inhibition of a sensitized mutant myosin Vb demonstrates a role in peripheral-pericentriolar membrane traffic. Proc Natl Acad Sci U S A 2004, 101:1868-1873.
155. Schafer J.C., Baetz N.W., Lapierre L.A., McRae R.E., Roland J.T., Goldenring J.R. Rab11-FIP2 interaction with MYO5B regulates movement of Rab11a-containing recycling vesicles. Traffic 2014, 15:292-308.
156. Provance D.W., Addison E.J., Wood P.R., Chen D.Z., Silan C.M., Mercer J.A. Myosin-Vb functions as a dynamic tether for peripheral endocytic compartments during transferrin trafficking. BMC Cell Biol 2008, 9:44.
157. Holt J.P., Bottomly K., Mooseker M.S. Assessment of myosin II, Va, VI and VIIa loss of function on endocytosis and endocytic vesicle motility in bone marrow-derived dendritic cells. Cell Motil Cytoskeleton 2007, 64:756-766.
158. Yan Q., Sun W., Kujala P., Lotfi Y., Vida T.A., Bean A.J. CART: an Hrs/actinin-4/BERP/myosin V protein complex required for efficient receptor recycling. Mol Biol Cell 2005, 16:2470-2482.
159. Heerssen H.M., Pazyra M.F., Segal R.A. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat Neurosci 2004, 7:596-604.
160. Schwenk B.M., Lang C.M., Hogl S., Tahirovic S., Orozco D., Rentzsch K., et al. The FTLD risk factor TMEM106B and MAP6 control dendritic trafficking of lysosomes. EMBO J 2014, 33:450-467.
161. Andrews R., Ahringer J. Asymmetry of early endosome distribution in C. elegans embryos. PLoS ONE 2007, 2:e493.
162. Coumailleau F., Furthauer M., Knoblich J.A., Gonzalez-Gaitan M. Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 2009, 458:1051-1055.
163. Jacquemet G., Humphries M.J., Caswell P.T. Role of adhesion receptor trafficking in 3D cell migration. Curr Opin Cell Biol 2013, 25:627-632.
164. Baumann S., Pohlmann T., Jungbluth M., Brachmann A., Feldbrugge M. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J Cell Sci 2012, 125:2740-2752.
165. Higuchi Y., Ashwin P., Roger Y., Steinberg G. Early endosome motility spatially organizes polysome distribution. J Cell Biol 2014, 204:343-357.
166. a-mediated functional coupling between Rab4 and the motor protein kinesin. Mol Cell Biol 2003, 23:4892-4900.