The Caenorhabditis elegans JIP3 Protein UNC-16 functions as an adaptor to link kinesin-1 with cytoplasmic dynein

Journal of Neuroscience

Volumn 31, Issue 6, 2011, Pages 2216-2224

  Arimoto, Makoto ^a   Koushika, Sandhya P ^b   Choudhary, Bikash C ^b   Li, Chris ^c   Matsumoto, Kunihiro ^a   Hisamoto, Naoki ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^c CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN 1; UNC 16 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; MICROTUBULE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL TRANSPORT; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOPLASMIC DYNEINS; DYNEINS; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; KINESIN; LUMINESCENT PROTEINS; MECHANORECEPTORS; MEMBRANE PROTEINS; MICROINJECTIONS; PRESYNAPTIC TERMINALS; PROTEIN BINDING; PROTEIN TRANSPORT; TRANSFECTION;

EID: 79951528510     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2653-10.2011     Document Type: Article

References (39)

1. 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. (Pubitemid 46480935)
2. 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.
3. 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. (Pubitemid 34024841)
4. Cavalli V, Kujala P, Klumperman J, Goldstein LS (2005) Sunday Driver links axonal transport to damage signaling. J Cell Biol 168:775-787. (Pubitemid 40328161)
5. Caviston JP, Holzbaur EL (2006) Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol 16:530-537. (Pubitemid 44444994)
6. Chalfie M (1993) Touch receptor development and function in Caenorhabditis elegans. J Neurobiol 24:1433-1441.
7. Colin E, Zala D, Liot G, Rangone H, Borrell-Pagès M, Li XJ, Saudou F, Humbert S (2008) Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J 27:2124-2134.
8. Daigle I, Li C (1993) apl-1, a Caenorhabditis elegans gene encoding a protein related to the human β-amyloid protein precursor. Proc Natl Acad Sci U S A 90:12045-12049.
9. Duerr JS, Han HP, Fields SD, Rand JB (2008) Identification of major classes of cholinergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 506:398-408.
10. Gindhart JG Jr, 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. (Pubitemid 28237092)
11. 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. (Pubitemid 37013132)
12. 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. (Pubitemid 38903151)
13. Hall DH, Hedgecock EM (1991) Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65:837-847. (Pubitemid 121001315)
14. Hall DH, Plenefisch J, Hedgecock EM (1991) Ultrastructural abnormalities of kinesin mutant unc-116. J Cell Biol 115:389A.
15. Han G, Liu B, Zhang J, Zuo W, Morris NR, Xiang X (2001) The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr Biol 11:719-724.
16. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6:201-214. (Pubitemid 40342415)
17. Hornsten A, Lieberthal J, Fadia S, Malins R, Ha L, Xu X, Daigle I, Markowitz M, O'Connor G, Plasterk R, Li C (2007) APL-1, a Caenorhabditis elegans protein related to the human β-amyloid precursor protein, is essential for viability. Proc Natl Acad Sci U S A 104:1971-1976.
18. Hurd DD, Saxton WM (1996) Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144:1075-1085.
19. Kawasaki M, Hisamoto N, Iino Y, Yamamoto M, Ninomiya-Tsuji J, Matsumoto K (1999) A Caenorhabditis elegans JNK signal transduction pathway regulates coordinated movement via type-D GABAergic motor neurons. EMBO J 18:3604-3615.
20. 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 U S A 100:9843-9848. (Pubitemid 37087029)
21. Kimura N, Imamura O, Ono F, Terao K (2007) Aging attenuates dynactin-dynein interaction: down-regulation of dynein causes accumulation of endogenous tau and amyloid precursor protein in human neuroblastoma cells. J Neurosci Res 85:2909-2916. (Pubitemid 47523575)
22. Koushika SP, Schaefer AM, Vincent R, Willis JH, Bowerman B, Nonet ML (2004) Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J Neurosci 24:3907-3916.
23. Lee WL, Oberle JR, Cooper JA (2003) The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J Cell Biol 160:355-364. (Pubitemid 36182726)
24. Ligon LA, Tokito M, Finklestein JM, Grossman FE, Holzbaur EL (2004) A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J Biol Chem 279:19201-19208. (Pubitemid 38623351)
25. Martin M, Iyadurai SJ, Gassman A, Gindhart JG Jr, Hays TS, Saxton WM (1999) Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol Biol Cell 10:3717-3728. (Pubitemid 29534021)
26. Motegi F, Velarde NV, Piano F, Sugimoto A (2006) Two phases of astral microtubule activity during cytokinesis in C. elegans embryos. Dev Cell 10:509-520.
27. 2-terminal kinase-interacting protein-1. J Cell Biol 171:615-625.
28. Nonet ML (1999) Visualization of presynaptic terminal specializations in live C. elegans using synaptic vesicle protein-GFP fusions. J Neurosci Methods 89:33-40.
29. Otsuka AJ, Jeyaprakash A, García-Añoveros J, Tang LZ, Fisk G, Hartshorne T, Franco R, Born T (1991) The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein. Neuron 6:113-122.
30. Robin G, DeBonis S, Dornier A, Cappello G, Ebel C, Wade RH, Thierry-Mieg D, Kozielski F (2005) Essential kinesins: characterization of Caenorhabditis elegans KLP-15. Biochemistry 44:6526-6536.
31. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerrière A, Vital A, Dumanchin C, Feuillette S, Brice A, Vercelletto M, Dubas F, Frebourg T, Campion D (2006) APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 38:24-26. (Pubitemid 43011878)
32. 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.
33. Sato S, Ito M, Ito T, Yoshioka K (2004) Scaffold protein JSAP1 is transported to growth cones of neurites independent of JNK signaling pathways in PC12h cells. Gene 329:51-60. (Pubitemid 38366494)
34. Sheeman B, Carvalho P, Sagot I, Geiser J, Kho D, Hoyt MA, Pellman D (2003) Determinants of S. cerevisiae dynein localization and activation. Implications for the mechanism of spindle positioning. Curr Biol 13:364-372.
35. Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112:467-480.
36. 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. (Pubitemid 34286072)
37. Yamada M, Toba S, Yoshida Y, Haratani K, Mori D, Yano Y, Mimori-Kiyosue Y, Nakamura T, Itoh K, Fushiki S, Setou M, Wynshaw-Boris A, Torisawa T, Toyoshima YY, Hirotsune S (2008) LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J 27:2471-2483.
38. 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-end-directed transport of cytoplasmic dynein and dynactins by kinesin-1. EMBO J 29:517-531.
39. Zhang J, Li S, Fischer R, Xiang X (2003) Accumulation of cytoplasmic dynein and dynactin at microtubule plus ends in Aspergillus nidulans is kinesin dependent. Mol Biol Cell 14:1479-1488.