Sunday Driver/JIP3 binds kinesin heavy chain directly and enhances its motility

EMBO Journal

Volumn 30, Issue 16, 2011, Pages 3416-3429

  Sun, Faneng ^a   Zhu, Chuanmei ^b   Dixit, Ram ^b   Cavalli, Valeria ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

axonal transport; JIP3; kinesin; motility; syd

Indexed keywords

ADAPTOR PROTEIN; KINESIN 1; MUTANT PROTEIN; PROTEIN SUNDAY DRIVER; UNCLASSIFIED DRUG; CARRIER PROTEIN; HYBRID PROTEIN; KIFC5 PROTEIN, MOUSE; KINESIN LIGHT CHAIN PROTEINS; KINESIN LIGHT-CHAIN PROTEINS; MAPK8IP3 PROTEIN, MOUSE; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; PEPTIDE FRAGMENT; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SUNDAY DRIVER PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; IN VITRO STUDY; MOUSE; NERVE CELL; NERVE FIBER; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; WILD TYPE; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; METABOLISM; MICROTUBULE; NERVE FIBER TRANSPORT; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AXONAL TRANSPORT; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NERVE TISSUE PROTEINS; NEURONS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 80155174991     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.229     Document Type: Article

References (77)

1. Abe N, Almenar-Queralt A, Lillo C, Shen Z, Lozach J, Briggs SP, Williams DS, Goldstein LS, Cavalli V (2009) Sunday driver interacts with two distinct classes of axonal organelles. J Biol Chem 284: 34628-34639
2. Akechi M, Ito M, Uemura K, Takamatsu N, Yamashita S, Uchiyama K, Yoshioka K, Shiba T (2001) Expression of JNK cascade scaffold protein JSAP1 in the mouse nervous system. Neurosci Res 39: 391-400
3. Aoyama T, Hata S, Nakao T, Tanigawa Y, Oka C, Kawaichi M (2009) Cayman ataxia protein caytaxin is transported by kinesin along neurites through binding to kinesin light chains. J Cell Sci 122: 4177-4185
4. Araki Y, Kawano T, Taru H, Saito Y,Wada S, Miyamoto K, Kobayashi H, Ishikawa HO, Ohsugi Y, Yamamoto T, Matsuno K, Kinjo M, Suzuki T (2007) The novel cargo Alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. EMBO J 26: 1475-1486
5. Blasius TL, Cai D, Jih GT, Toret CP, Verhey KJ (2007) Two binding partners cooperate to activate the molecular motor Kinesin-1. J Cell Biol 176: 11-17
6. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, Gindhart JG, Goldstein LS (2000) Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103: 583-594
7. Bracale A, Cesca F, Neubrand VE, Newsome TP, Way M, Schiavo G (2007) Kidins220/ARMS is transported by a kinesin-1-based mechanism likely to be involved in neuronal differentiation. Mol Biol Cell 18: 142-152
8. Brown HM, Van Epps HA, Goncharov A, Grant BD, Jin Y (2009) The JIP3 scaffold protein UNC-16 regulates RAB-5 dependent membrane trafficking at C. elegans synapses. Dev Neurobiol 69: 174-190
9. Byrd DT, Kawasaki M, Walcoff M, Hisamoto N, Matsumoto K, Jin Y (2001) UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 32: 787-800
10. Cai D, Hoppe AD, Swanson JA, Verhey KJ (2007) Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells. J Cell Biol 176: 51-63
11. Cai Q, Gerwin C, Sheng ZH (2005) Syntabulin-mediated anterograde transport of mitochondria along neuronal processes. J Cell Biol 170: 959-969
12. Cai Y, Singh BB, Aslanukov A, Zhao H, Ferreira PA (2001) The docking of kinesins, KIF5B and KIF5C, to Ran-binding protein 2 (RanBP2) is mediated via a novel RanBP2 domain. J Biol Chem 276: 41594-41602
13. Cho KI, Cai Y, Yi H, Yeh A, Aslanukov A, Ferreira PA (2007) Association of the kinesin-binding domain of RanBP2 to KIF5B and KIF5C determines mitochondria localization and function. Traffic 8: 1722-1735
14. Cho KI, Yi H, Desai R, Hand AR, Haas AL, Ferreira PA (2009) RANBP2 is an allosteric activator of the conventional kinesin-1 motor protein, KIF5B, in a minimal cell-free system. EMBO Rep 10: 480-486
15. Coy DL, Hancock WO, Wagenbach M, Howard J (1999a) Kinesin's tail domain is an inhibitory regulator of the motor domain. Nat Cell Biol 1: 288-292
16. DeLuca JG, Newton CN, Himes RH, Jordan MA, Wilson L (2001) Purification and characterization of native conventional kinesin, HSET, and CENP-E from mitotic hela cells. J Biol Chem 276: 28014-28021
17. Dictenberg JB, Swanger SA, Antar LN, Singer RH, Bassell GJ (2008) A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev Cell 14: 926-939
18. Diefenbach RJ, Diefenbach E, Douglas MW, Cunningham AL (2002) The heavy chain of conventional kinesin interacts with the SNARE proteins SNAP25 and SNAP23. Biochemistry 41: 14906-14915
19. Dietrich KA, Sindelar CV, Brewer PD, Downing KH, Cremo CR, Rice SE (2008) The kinesin-1 motor protein is regulated by a direct interaction of its head and tail. Proc Natl Acad Sci USA 105: 8938-8943
20. Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319: 1086-1089
21. Friedman DS, Vale RD (1999) Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat Cell Biol 1: 293-297
22. Gindhart JG, Chen J, Faulkner M, Gandhi R, Doerner K, Wisniewski T, Nandlestadt A (2003) The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol Biol Cell 14: 3356-3365
23. Gindhart Jr JG, Desai CJ, Beushausen S, Zinn K, Goldstein LS (1998) Kinesin light chains are essential for axonal transport in Drosophila. J Cell Biol 141: 443-454
24. Glater EE, Megeath LJ, Stowers RS, Schwarz TL (2006) Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol 173: 545-557
25. Goldstein AY, Wang X, Schwarz TL (2008) Axonal transport and the delivery of pre-synaptic components. Curr Opin Neurobiol 18: 495-503
26. Grigoriev I, Splinter D, Keijzer N, Wulf PS, Demmers J, Ohtsuka T, Modesti M, Maly IV, Grosveld F, Hoogenraad CC, Akhmanova A (2007) Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13: 305-314
27. Guzik BW, Goldstein LS (2004) Microtubule-dependent transport in neurons: steps towards an understanding of regulation, function and dysfunction. Curr Opin Cell Biol 16: 443-450
28. Gyoeva FK, Bybikova EM, Minin AA (2000) An isoform of kinesin light chain specific for the Golgi complex. J Cell Sci 113 (Pt 11): 2047-2054
29. Gyoeva FK, Sarkisov DV, Khodjakov AL, Minin AA (2004) The tetrameric molecule of conventional kinesin contains identical light chains. Biochemistry 43: 13525-13531
30. Hackney DD, Levitt JD, Wagner DD (1991) Characterization of alpha 2 beta 2 and alpha 2 forms of kinesin. Biochem Biophys Res Commun 174: 810-815
31. Hackney DD, Stock MF (2000) Kinesin's IAK tail domain inhibits initial microtubule-stimulated ADP release. Nat Cell Biol 2: 257-260
32. Hackney DD, Stock MF (2008) Kinesin tail domains and Mg2+ directly inhibit release of ADP from head domains in the absence of microtubules. Biochemistry 47: 7770-7778
33. Hackney DD, Stock MF, Moore J, Patterson RA (2003) Modulation of kinesin half-site ADP release and kinetic processivity by a spacer between the head groups. Biochemistry 42: 12011-12018
34. Hammond JW, Griffin K, Jih GT, Stuckey J, Verhey KJ (2008) Co-operative versus independent transport of different cargoes by Kinesin-1. Traffic 9: 725-741
35. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10: 682-696
36. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6: 201-214
37. Ito M, Yoshioka K, Akechi M, Yamashita S, Takamatsu N, Sugiyama K, Hibi M, Nakabeppu Y, Shiba T, Yamamoto KI (1999) JSAP1, a novel jun N-terminal protein kinase (JNK)-binding protein that functions as a Scaffold factor in the JNK signaling pathway. Mol Cell Biol 19: 7539-7548
38. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28: 449-459
39. Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43: 513-525
40. Kelkar N, Delmotte MH, Weston CR, Barrett T, Sheppard BJ, Flavell RA, Davis RJ (2003) Morphogenesis of the telencephalic commissure requires scaffold protein JNK-interacting protein 3 (JIP3). Proc Natl Acad Sci USA 100: 9843-9848
41. Kelkar N, Gupta S, Dickens M, Davis RJ (2000) Interaction of a mitogen-activated protein kinase signaling module with the neuronal protein JIP3. Mol Cell Biol 20: 1030-1043
42. Kelkar N, Standen CL, Davis RJ (2005) Role of the JIP4 scaffold protein in the regulation of mitogen-activated protein kinase signaling pathways. Mol Cell Biol 25: 2733-2743
43. Khodjakov A, Lizunova EM, Minin AA, Koonce MP, Gyoeva FK (1998) A specific light chain of kinesin associates with mitochondria in cultured cells. Mol Biol Cell 9: 333-343
44. Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K (2005) Tubulin and CRMP-2 complex is transported via Kinesin-1. J Neurochem 93: 1371-1382
45. Konecna A, Frischknecht R, Kinter J, Ludwig A, Steuble M, Meskenaite V, Indermuhle M, Engel M, Cen C, Mateos JM, Streit P, Sonderegger P (2006) Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol Biol Cell 17: 3651-3663
46. Koushika SP (2008) 'JIP'ing along the axon: the complex roles of JIPs in axonal transport. Bioessays 30: 10-14
47. Kristensen O, Guenat S, Dar I, Allaman-Pillet N, Abderrahmani A, Ferdaoussi M, Roduit R, Maurer F, Beckmann JS, Kastrup JS, Gajhede M, Bonny C (2006) A unique set of SH3-SH3 interactions controls IB1 homodimerization. EMBO J 25: 785-797
48. Ling SC, Fahrner PS, Greenough WT, Gelfand VI (2004) Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc Natl Acad Sci USA 101: 17428-17433
49. Loiseau P, Davies T, Williams LS, Mishima M, Palacios IM (2010) Drosophila PAT1 is required for Kinesin-1 to transport cargo and to maximize its motility. Development 137: 2763-2772
50. Mavlyutov TA, Cai Y, Ferreira PA (2002) Identification of RanBP2-and kinesin-mediated transport pathways with restricted neuronal and subcellular localization. Traffic 3: 630-640
51. Morfini G, Szebenyi G, Richards B, Brady ST (2001) Regulation of kinesin: implications for neuronal development. Dev Neurosci 23: 364-376
52. Nguyen Q, Lee CM, Le A, Reddy EP (2005) JLP associates with kinesin light chain 1 through a novel leucine zipper-like domain. J Biol Chem 280: 30185-30191
53. Palacios IM, St Johnston D (2002) Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129: 5473-5485
54. Pérez-Pinera P (2006) Deletion of DNA sequences of using a polymerase chain reaction based. Electronic J Biotechnol 9: 604-609
55. Rahman A, Friedman DS, Goldstein LS (1998) Two kinesin light chain genes in mice. Identification and characterization of the encoded proteins. J Biol Chem 273: 15395-15403
56. Rahman A, Kamal A, Roberts EA, Goldstein LS (1999) Defective kinesin heavy chain behavior in mouse kinesin light chain mutants. J Cell Biol 146: 1277-1288
57. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B (2009) Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci USA 106: 2194-2199
58. Sakamoto R, Byrd DT, Brown HM, Hisamoto N, Matsumoto K, Jin Y (2005) The Caenorhabditis elegans UNC-14 RUN domain protein binds to the kinesin-1 and UNC-16 complex and regulates synaptic vesicle localization. Mol Biol Cell 16: 483-496
59. Seeger MA, Rice SE (2010) Microtubule-associated protein-like binding of the kinesin-1 tail to microtubules. J Biol Chem 285: 8155-8162
60. Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, Hirokawa N (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417: 83-87
61. Shastry S, Hancock WO (2010) Neck linker length determines the degree of processivity in kinesin-1 and kinesin-2 motors. Curr Biol 20: 939-943
62. Skoufias DA, Cole DG, Wedaman KP, Scholey JM (1994) The carboxyl-terminal domain of kinesin heavy chain is important for membrane binding. J Biol Chem 269: 1477-1485
63. Stenoien DL, Brady ST (1997) Immunochemical analysis of kinesin light chain function. Mol Biol Cell 8: 675-689
64. Su Q, Cai Q, Gerwin C, Smith CL, Sheng ZH (2004) Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat Cell Biol 6: 941-953
65. Sung HH, Telley IA, Papadaki P, Ephrussi A, Surrey T, Rorth P (2008) Drosophila ensconsin promotes productive recruitment of Kinesin-1 to microtubules. Dev Cell 15: 866-876
66. Taya S, Shinoda T, Tsuboi D, Asaki J, Nagai K, Hikita T, Kuroda S, Kuroda K, Shimizu M, Hirotsune S, Iwamatsu A, Kaibuchi K (2007) DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J Neurosci 27: 15-26
67. Terada S, Kinjo M, Aihara M, Takei Y, Hirokawa N (2010) Kinesin-1/Hsc70-dependent mechanism of slow axonal transport and its relation to fast axonal transport. EMBO J 29: 843-854
68. Verhey KJ, Hammond JW (2009) Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10: 765-777
69. Verhey KJ, Lizotte DL, Abramson T, Barenboim L, Schnapp BJ, Rapoport TA (1998) Light chain-dependent regulation of Kinesin's interaction with microtubules. J Cell Biol 143: 1053-1066
70. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, Rapoport TA, Margolis B (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152: 959-970
71. Watanabe TM, Yanagida T, Iwane AH (2010) Single molecular observation of self-regulated Kinesin motility. Biochemistry 49: 4654-4661
72. Wong YL, Dietrich KA, Naber N, Cooke R, Rice SE (2009) The Kinesin-1 tail conformationally restricts the nucleotide pocket. Biophys J 96: 2799-2807
73. Wozniak MJ, Allan VJ (2006) Cargo selection by specific kinesin light chain 1 isoforms. EMBO J 25: 5457-5468
74. Xia CH, Roberts EA, Her LS, Liu X, Williams DS, Cleveland DW, Goldstein LS (2003) Abnormal neurofilament transport caused by targeted disruption of neuronal kinesin heavy chain KIF5A. J Cell Biol 161: 55-66
75. Yamada M, Toba S, Takitoh T, Yoshida Y, Mori D, Nakamura T, Iwane AH, Yanagida T, Imai H, Yu-Lee LY, Schroer T, Wynshaw-Boris A, Hirotsune S (2010) mNUDC is required for plus-enddirected transport of cytoplasmic dynein and dynactins by kinesin-1. EMBO J 29: 517-531
76. Yasuda J, Whitmarsh AJ, Cavanagh J, Sharma M, Davis RJ (1999) The JIP group of mitogen-activated protein kinase scaffold proteins. Mol Cell Biol 19: 7245-7254
77. Yildiz A, Tomishige M, Gennerich A, Vale RD (2008) Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134: 1030-1041