Integrated regulation of motor-driven organelle transport by scaffolding proteins

Trends in Cell Biology

Volumn 24, Issue 10, 2014, Pages 564-574

  Fu, Meng meng ^a,b   Holzbaur, Erika L F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axonal transport; Dynactin; Dynein; Intracellular trafficking; Kinesin; Organelle transport

Indexed keywords

ADAPTOR PROTEIN; BINDING PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE; HOOK1 PROTEIN; HUNTINGTIN; JIP1 PROTEIN; JIP3 PROTEIN; KINESIN; MOLECULAR MOTOR; PHOSPHOTRANSFERASE; REGULATOR PROTEIN; RETROGRADE SCAFFOLDING PROTEIN; RNA; SCAFFOLD PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRAFFICKING KINESIN BINDING PROTEIN; UNCLASSIFIED DRUG; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BINDING;

CELL ORGANELLE; HUMAN; INTRACELLULAR TRANSPORT; MICROTUBULE; MOTOR ACTIVITY; NERVE CELL; NONHUMAN; PROTEIN BINDING; REGULATORY MECHANISM; REVIEW; RNA TRANSPORT; ANIMAL; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; DYNEINS; HUMANS; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; ORGANELLES; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84908488959     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2014.05.002     Document Type: Review

References (120)

1. Mallik R., et al. Teamwork in microtubule motors. Trends Cell Biol. 2013, 23:575-582.
2. Encalada S.E., et al. Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles. Cell 2011, 144:551-565.
3. Hendricks A.G., et al. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr. Biol. 2010, 20:697-702.
4. Maday S., et al. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J. Cell Biol. 2012, 196:407-417.
5. Soppina V., et al. 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.
6. Hendricks A.G., et al. Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18447-18452.
7. Szpankowski L., et al. Subpixel colocalization reveals amyloid precursor protein-dependent kinesin-1 and dynein association with axonal vesicles. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:8582-8587.
8. Muller M.J., et al. 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.
9. Fu M.-M., et al. LC3 binding to the scaffolding protein JIP1 regulates processive dynein-driven transport of autophagosomes. Dev. Cell 2014, 29:577-590.
10. Dixit R., et al. Differential regulation of dynein and kinesin motor proteins by tau. Science 2008, 319:1086-1089.
11. Blehm B.H., et al. In vivo optical trapping indicates kinesin's stall force is reduced by dynein during intracellular transport. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:3381-3386.
12. Hammond J.W., et al. Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 2008, 20:71-76.
13. Hammond J.W., et al. Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons. Mol. Biol. Cell 2010, 21:572-583.
14. Janke C., Bulinski J.C. Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 2011, 12:773-786.
15. Nakata T., et al. Preferential binding of a kinesin-1 motor to GTP-tubulin-rich microtubules underlies polarized vesicle transport. J. Cell Biol. 2011, 194:245-255.
16. Vershinin M., et al. Multiple-motor based transport and its regulation by Tau. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:87-92.
17. McVicker D.P., et al. The nucleotide-binding state of microtubules modulates kinesin processivity and the ability of Tau to inhibit kinesin-mediated transport. J. Biol. Chem. 2011, 286:42873-42880.
18. Barlan K., et al. The microtubule-binding protein ensconsin is an essential cofactor of kinesin-1. Curr. Biol. 2013, 23:317-322.
19. Balint S., et al. Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:3375-3380.
20. Ross J.L., et al. Cargo transport: molecular motors navigate a complex cytoskeleton. Curr. Opin. Cell Biol. 2008, 20:41-47.
21. Zajac A.L., et al. Local cytoskeletal and organelle interactions impact molecular-motor-driven early endosomal trafficking. Curr. Biol. 2013, 23:1173-1180.
22. Friedman J.R., et al. Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol. Biol. Cell 2013, 24:1030-1040.
23. Jordens I., et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 2001, 11:1680-1685.
24. Johansson M., et al. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol. 2007, 176:459-471.
25. Holleran E.A., et al. beta III spectrin binds to the Arp1 subunit of dynactin. J. Biol. Chem. 2001, 276:36598-36605.
26. Rai A.K., et al. Molecular adaptations allow dynein to generate large collective forces inside cells. Cell 2013, 152:172-182.
27. Rocha N., et al. Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning. J. Cell Biol. 2009, 185:1209-1225.
28. Hong Z., et al. The retromer component SNX6 interacts with dynactin p150(Glued) and mediates endosome-to-TGN transport. Cell Res. 2009, 19:1334-1349.
29. Wassmer T., 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.
30. Niu Y., et al. PtdIns(4)P regulates retromer-motor interaction to facilitate dynein-cargo dissociation at the trans-Golgi network. Nat. Cell Biol. 2013, 15:417-429.
31. MacAskill A.F., et al. Mitochondrial trafficking and the provision of energy and calcium buffering at excitatory synapses. Eur. J. Neurosci. 2010, 32:231-240.
32. Misgeld T., et al. Imaging axonal transport of mitochondria in vivo. Nat. Methods 2007, 4:559-561.
33. Bilsland L.G., et al. Deficits in axonal transport precede ALS symptoms in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20523-20528.
34. Glater E.E., et al. Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol. 2006, 173:545-557.
35. 2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009, 136:163-174.
36. Macaskill A.F., et al. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 2009, 61:541-555.
37. Wang X., et al. PINK1 and Parkin target Miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 2011, 147:893-906.
38. van Spronsen M., et al. TRAK/Milton motor-adaptor proteins steer mitochondrial trafficking to axons and dendrites. Neuron 2013, 77:485-502.
39. Kang J.S., et al. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 2008, 132:137-148.
40. Courchet J., et al. Terminal axon branching is regulated by the LKB1-NUAK1 kinase pathway via presynaptic mitochondrial capture. Cell 2013, 153:1510-1525.
41. Chen Y., Sheng Z.H. Kinesin-1-syntaphilin coupling mediates activity-dependent regulation of axonal mitochondrial transport. J. Cell Biol. 2013, 202:351-364.
42. Caviston J.P., et al. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10045-10050.
43. Twelvetrees A.E., et al. Delivery of GABAARs to synapses is mediated by HAP1-KIF5 and disrupted by mutant huntingtin. Neuron 2010, 65:53-65.
44. McGuire J.R., et al. Interaction of Huntingtin-associated protein-1 with kinesin light chain: implications in intracellular trafficking in neurons. J. Biol. Chem. 2006, 281:3552-3559.
45. Engelender S., et al. Huntingtin-associated protein 1 (HAP1) interacts with the p150Glued subunit of dynactin. Hum. Mol. Genet. 1997, 6:2205-2212.
46. Li S.H., et al. Interaction of huntingtin-associated protein with dynactin P150Glued. J. Neurosci. 1998, 18:1261-1269.
47. Caviston J.P., et al. Huntingtin coordinates the dynein-mediated dynamic positioning of endosomes and lysosomes. Mol. Biol. Cell 2011, 22:478-492.
48. Gunawardena S., et al. Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 2003, 40:25-40.
49. Her L.S., Goldstein L.S. Enhanced sensitivity of striatal neurons to axonal transport defects induced by mutant huntingtin. J. Neurosci. 2008, 28:13662-13672.
50. Colin E., et al. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J. 2008, 27:2124-2134.
51. Wong Y.C., Holzbaur E.L. The regulation of autophagosome dynamics by huntingtin and HAP1 is disrupted by expression of mutant huntingtin, leading to defective cargo degradation. J. Neurosci. 2014, 34:1293-1305.
52. Ma B., et al. Huntingtin mediates dendritic transport of beta-actin mRNA in rat neurons. Sci. Rep. 2011, 1:140.
53. Liot G., et al. Mutant Huntingtin alters retrograde transport of TrkB receptors in striatal dendrites. J. Neurosci. 2013, 33:6298-6309.
54. Sahlender D.A., et al. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J. Cell Biol. 2005, 169:285-295.
55. Caviston J.P., Holzbaur E.L. Huntingtin as an essential integrator of intracellular vesicular trafficking. Trends Cell Biol. 2009, 19:147-155.
56. Zala D., et al. Phosphorylation of mutant huntingtin at S421 restores anterograde and retrograde transport in neurons. Hum. Mol. Genet. 2008, 17:3837-3846.
57. Morfini G., et al. JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat. Neurosci. 2006, 9:907-916.
58. Morfini G.A., et al. Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat. Neurosci. 2009, 12:864-871.
59. Deberg H.A., et al. Motor domain phosphorylation modulates Kinesin-1 transport. J. Biol. Chem. 2013, 288:32612-32621.
60. van Niekerk E.A., et al. Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12913-12918.
61. Whitmarsh A.J. The JIP family of MAPK scaffold proteins. Biochem. Soc. Trans. 2006, 34:828-832.
62. Cavalli V., et al. Sunday Driver links axonal transport to damage signaling. J. Cell Biol. 2005, 168:775-787.
63. Abe N., et al. Sunday driver interacts with two distinct classes of axonal organelles. J. Biol. Chem. 2009, 284:34628-34639.
64. Sun F., et al. Sunday Driver/JIP3 binds kinesin heavy chain directly and enhances its motility. EMBO J. 2011, 30:3416-3429.
65. Arimoto M., et al. The Caenorhabditis elegans JIP3 protein UNC-16 functions as an adaptor to link kinesin-1 with cytoplasmic dynein. J. Neurosci. 2011, 31:2216-2224.
66. Deinhardt K., et al. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 2006, 52:293-305.
67. Mitchell D.J., et al. Trk activation of the ERK1/2 kinase pathway stimulates intermediate chain phosphorylation and recruits cytoplasmic dynein to signaling endosomes for retrograde axonal transport. J. Neurosci. 2012, 32:15495-15510.
68. Huang S.H., et al. JIP3 mediates TrkB axonal anterograde transport and enhances BDNF signaling by directly bridging TrkB with kinesin-1. J. Neurosci. 2011, 31:10602-10614.
69. Montagnac G., et al. ARF6 Interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Curr. Biol. 2009, 19:184-195.
70. Horiuchi D., et al. APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr. Biol. 2005, 15:2137-2141.
71. 2-terminal kinase-interacting protein-3 facilitates phosphorylation and controls localization of amyloid-beta precursor protein. J. Neurosci. 2005, 25:3741-3751.
72. Fu M.M., Holzbaur E.L. JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J. Cell Biol. 2013, 202:495-508.
73. Verhey K.J., et al. Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 2001, 152:959-970.
74. Matsuda S., et al. c-Jun N-terminal kinase (JNK)-interacting protein-1b/islet-brain-1 scaffolds Alzheimer's amyloid precursor protein with JNK. J. Neurosci. 2001, 21:6597-6607.
75. 2-terminal kinase (JNK) interacting protein 1 (JIP1) binds the cytoplasmic domain of the Alzheimer's beta-amyloid precursor protein (APP). J. Biol. Chem. 2002, 277:3767-3775.
76. Nihalani D., et al. Recruitment of JNK to JIP1 and JNK-dependent JIP1 phosphorylation regulates JNK module dynamics and activation. J. Biol. Chem. 2003, 278:28694-28702.
77. Willoughby E.A., et al. The JNK-interacting protein-1 scaffold protein targets MAPK phosphatase-7 to dephosphorylate JNK. J. Biol. Chem. 2003, 278:10731-10736.
78. Blasius T.L., et al. Two binding partners cooperate to activate the molecular motor Kinesin-1. J. Cell Biol. 2007, 176:11-17.
79. Kristensen O., et al. A unique set of SH3-SH3 interactions controls IB1 homodimerization. EMBO J. 2006, 25:785-797.
80. Hammond J.W., et al. Co-operative versus independent transport of different cargoes by Kinesin-1. Traffic 2008, 9:725-741.
81. Muresan Z., Muresan V. Coordinated transport of phosphorylated amyloid-beta precursor protein and c-Jun NH2-terminal kinase-interacting protein-1. J. Cell Biol. 2005, 171:615-625.
82. Hammond J.W., et al. Autoinhibition of the kinesin-2 motor KIF17 via dual intramolecular mechanisms. J. Cell Biol. 2010, 189:1013-1025.
83. Hammond J.W., et al. Mammalian Kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol. 2009, 7:e72.
84. Setou M., et al. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 2000, 288:1796-1802.
85. Guillaud L., et al. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 2008, 10:19-29.
86. Yin X., et al. Regulation of NMDA receptor transport: a KIF17-cargo binding/releasing underlies synaptic plasticity and memory in vivo. J. Neurosci. 2012, 32:5486-5499.
87. Deacon S.W., et al. Dynactin is required for bidirectional organelle transport. J. Cell Biol. 2003, 160:297-301.
88. Berezuk M.A., Schroer T.A. Dynactin enhances the processivity of kinesin-2. Traffic 2007, 8:124-129.
89. Niwa S., et al. KIF1Bbeta- and KIF1A-mediated axonal transport of presynaptic regulator Rab3 occurs in a GTP-dependent manner through DENN/MADD. Nat. Cell Biol. 2008, 10:1269-1279.
90. Zhang J., et al. HookA is a novel dynein-early endosome linker critical for cargo movement in vivo. J. Cell Biol. 2014, 204:1009-1026.
91. Bielska E., et al. Hook is an adapter that coordinates kinesin-3 and dynein cargo attachment on early endosomes. J. Cell Biol. 2014, 204:989-1007.
92. Walenta J.H., et al. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 2001, 152:923-934.
93. Maldonado-Baez L., et al. Microtubule-dependent endosomal sorting of clathrin-independent cargo by Hook1. J. Cell Biol. 2013, 201:233-247.
94. Xu L., et al. An FTS/Hook/p107(FHIP) complex interacts with and promotes endosomal clustering by the homotypic vacuolar protein sorting complex. Mol. Biol. Cell 2008, 19:5059-5071.
95. Hirokawa N., et al. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 2009, 10:682-696.
96. Kanai Y., et al. KIF5C, a novel neuronal kinesin enriched in motor neurons. J. Neurosci. 2000, 20:6374-6384.
97. Nakajima K., et al. Molecular motor KIF5A is essential for GABA(A) receptor transport, and KIF5A deletion causes epilepsy. Neuron 2012, 76:945-961.
98. Verhey K.J., Hammond J.W. Traffic control: regulation of kinesin motors. Nat. Rev. Mol. Cell Biol. 2009, 10:765-777.
99. Stock M.F., et al. Formation of the compact confomer of kinesin requires a COOH-terminal heavy chain domain and inhibits microtubule-stimulated ATPase activity. J. Biol. Chem. 1999, 274:14617-14623.
100. Friedman D.S., Vale R.D. Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat. Cell Biol. 1999, 1:293-297.
101. Hirokawa N., et al. Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration. Cell 1989, 56:867-878.
102. Hackney D.D., et al. Half-site inhibition of dimeric kinesin head domains by monomeric tail domains. Biochemistry 2009, 48:3448-3456.
103. Kaan H.Y., et al. The structure of the kinesin-1 motor-tail complex reveals the mechanism of autoinhibition. Science 2011, 333:883-885.
104. Roberts A.J., et al. Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol. 2013, 14:713-726.
105. Ross J.L., et al. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat. Cell Biol. 2006, 8:562-570.
106. Kardon J.R., Vale R.D. Regulators of the cytoplasmic dynein motor. Nat. Rev. Mol. Cell Biol. 2009, 10:854-865.
107. Holzbaur E.L., et al. Homology of a 150K cytoplasmic dynein-associated polypeptide with the Drosophila gene Glued. Nature 1991, 351:579-583.
108. Waterman-Storer C.M., et al. 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.
109. Culver-Hanlon T.L., et al. A microtubule-binding domain in dynactin increases dynein processivity by skating along microtubules. Nat. Cell Biol. 2006, 8:264-270.
110. Karki S., Holzbaur E.L. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 1995, 270:28806-28811.
111. Vaughan K.T., Vallee R.B. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 1995, 131:1507-1516.
112. Siglin A.E., et al. Dynein and dynactin leverage their bivalent character to form a high-affinity interaction. PLoS ONE 2013, 8:e59453.
113. Schroer T.A. Dynactin. Annu. Rev. Cell Dev. Biol. 2004, 20:759-779.
114. Verhey K.J., et al. Light chain-dependent regulation of Kinesin's interaction with microtubules. J. Cell Biol. 1998, 143:1053-1066.
115. Diefenbach R.J., et al. The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. Biochemistry 1998, 37:16663-16670.
116. Hackney D.D., et al. Kinesin undergoes a 9S to 6S conformational transition. J. Biol. Chem. 1992, 267:8696-8701.
117. Palacios I.M., St Johnston D. Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 2002, 129:5473-5485.
118. Pernigo S., et al. Structural basis for kinesin-1:cargo recognition. Science 2013, 340:356-359.
119. Williams L.S., et al. The auto-inhibitory domain and ATP-independent microtubule-binding region of Kinesin heavy chain are major functional domains for transport in the Drosophila germline. Development 2014, 141:176-186.
120. Vagnoni A., et al. Phosphorylation of kinesin light chain 1 at serine 460 modulates binding and trafficking of calsyntenin-1. J. Cell Sci. 2011, 124:1032-1042.