Quantitative analysis of APP axonal transport in neurons: Role of JIP1 in enhanced APP anterograde transport

Molecular Biology of the Cell

Volumn 25, Issue 22, 2014, Pages 3569-3580

  Chiba, Kyoko ^a   Araseki, Masahiko ^a   Nozawa, Keisuke ^a   Furukori, Keiko ^a,b   Araki, Yoichi ^a   Matsushima, Takahide ^a   Nakaya, Tadashi ^a   Hata, Saori ^a   Saito, Yuhki ^a   Uchida, Seiichi ^c   Okada, Yasushi ^d   Nairn, Angus C ^b   Davis, Roger J ^e   Yamamoto, Tohru ^f   Kinjo, Masataka ^a   Taru, Hidenori ^a   Suzuki, Toshiharu ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KYUSHU UNIVERSITY   (Japan)

^d RIKEN   (Japan)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; KINESIN 1; KINESIN LIGHT CHAIN 1; UNCLASSIFIED DRUG; AMYLOID PRECURSOR PROTEIN; KIF5B PROTEIN, MOUSE; KINESIN; KINESIN LIGHT-CHAIN PROTEINS; MAPK8IP PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ALZHEIMER DISEASE; ARTICLE; HUMAN; LIGHT CHAIN; NERVE FIBER TRANSPORT; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; TETRATRICOPEPTIDE REPEAT; VELOCITY; ANIMAL; BRAIN CORTEX; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; CYTOLOGY; DEFICIENCY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HIPPOCAMPUS; METABOLISM; MOUSE; NERVE CELL; PHOSPHORYLATION; PLASMID; PRIMARY CELL CULTURE; PROTEIN DOMAIN; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONAL TRANSPORT; CERCOPITHECUS AETHIOPS; CEREBRAL CORTEX; COS CELLS; GENE EXPRESSION REGULATION; HIPPOCAMPUS; KINESIN; MAP KINASE KINASE 4; MICE; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PHOSPHORYLATION; PLASMIDS; PRIMARY CELL CULTURE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84908565117     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-06-1111     Document Type: Article

References (40)

1. Ando K, Iijima K, Elliott JI, Kirino Y, Suzuki T (2001). Phosphorylation-dependent regulation of the interaction of amyloid precursor protein with Fe65 affects the production of β-amyloid. J Biol Chem 276, 40353-40361.
2. Araki Y, Kawano T, Taru H, Saito Y, Wada S, Miyamoto K, Kobayashi H, Ishikawa HO, Ohsugi Y, Yamamoto T, et al. (2007). The novel cargo Alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. EMBO J 26, 1475-1486.
3. Bartlett WP, Banker GA (1984). An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. I. Cells which develop without intercellular contacts. J Neurosci 4, 1944-1953.
4. 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.
5. Chiba K, Shimada Y, Kinjo M, Suzuki T, Uchida S (2014). Simple and direct assembly of kymographs from movies using KYMOMAKER. Traffic 15, 1-11.
6. Dickens M, Rogers JS, Cavanagh J, Raitano A, Xia Z, Halpern JR, Greenberg ME, Sawyers CL, Davis RJ (1997). A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277, 693-696.
7. 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.
8. Fu MM, Holzbaur EL (2013). JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors. J Cell Biol 202, 495-508.
9. Gandy S (2005). The role of cerebral amyloid beta accumulation in common forms of Alzheimer disease. J Clin Invest 115, 1121-1129.
10. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009). Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10, 682-696.
11. Horiuchi D, Barkus RV, Pilling AD, Gassman A, Saxton WM (2005). APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr Biol 15, 2137-2141.
12. Huang Y, Mucke L (2012). Alzheimer mechanisms and therapeutic strategies. Cell 148, 1204-1222.
13. Iijima K, Ando K, Takeda S, Satoh Y, Seki T, Itohara S, Greengard P, Kirino Y, Nairn AC, Suzuki T (2000). Neuron-specific phosphorylation of Alzheimer's β-amyloid precursor protein by cyclin-dependent kinase 5. J Neurochem 75, 1085-1091.
14. Inomata H, Nakamura Y, Hayakawa A, Takata H, Suzuki T, Miyazawa K, Kitamura N (2003). A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1. J Biol Chem 278, 22946-22955.
15. 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.
16. Kawano T, Araseki M, Araki Y, Kinjo M, Yamamoto T, Suzuki T (2012). A small peptide sequence is sufficient for initiating kinesin-1 activation through part of TPR region of KLC1. Traffic 13, 834-848.
17. Konecna A, Frischknecht R, Kinter J, Ludwig A, Steuble M, Meskenaite V, Indermuhle M, Engel M, Cen C, Mateos JM, et al. (2006). Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol Biol Cell 17, 3651-3663.
18. Matsuda S, Matsuda Y, D'Adamio L (2003). Amyloid beta protein precursor (AbetaPP), but not AbetaPP-like protein 2, is bridged to the kinesin light chain by the scaffold protein JNK-interacting protein 1. J Biol Chem 278, 38601-38606.
19. Matsushima T, Saito Y, Elliott JI, Iijima-Ando K, Nishimura M, Kimura N, Hata S, Yamamoto T, Nakaya T, Suzuki T (2012). Membrane-microdomain localization of amyloid beta-precursor protein (APP) C-terminal fragments is regulated by phosphorylation of the cytoplasmic Thr668 residue. J Biol Chem 287, 19715-19724.
20. Morel M, Heraud C, Nicaise C, Suain V, Brion JP (2012). Levels of kinesin light chain and dynein intermediate chain are reduced in the frontal cortex in Alzheimer's disease: implications for axoplasmic transport. Acta Neuropathol 123, 71-84.
21. Morihara T, Hayashi N, Yokokoji M, Akatsu H, Silverman MA, Kimura N, Sato M, Saito Y, Suzuki T, Yanagida K, et al. (2013). Transcriptome analysis of distinct mouse strains reveals kinesin light chain-1 splicing as an amyloid β accumulation modifier. Proc Natl Acad Sci USA 111, 2638-2643.
22. Niclas J, Navone F, Hom-Booher N, Vale RD (1994). Cloning and localization of a conventional kinesin motor expressed exclusively in neurons. Neuron 12, 1059-1072.
23. Nihalani D, Wong HN, Holzman LB (2003). Recruitment of JNK to JIP1 and JNK-dependent JIP1 phosphorylation regulates JNK module dynamics and activation. J Biol Chem 278, 28694-28702.
24. Ramelot TA, Nicholson LK (2001). Phosphorylation-induced structural changes in the amyloid precursor protein cytoplasmic tail detected by NMR. J Mol Biol 307, 871-884.
25. Sano Y, Nakaya T, Pedrini S, Takeda S, Iijima-Ando K, Iijima K, Mathews PM, Itohara S, Gandy S, Suzuki T (2006). Physiological mouse brain Abeta levels are not related to the phosphorylation state of threonine-668 of Alzheimer's APP. PLoS One 1, e51.
26. Scheinfeld MH, Roncarati R, Vito P, Lopez PA, Abdallah M, D'Adamio L (2002). Jun NH2-terminal kinase (JNK) interacting protein 1 (JIP1) binds the cytoplasmic domain of the Alzheimer's beta-amyloid precursor protein (APP). J Biol Chem 277, 3767-3775.
27. Steuble M, Diep TM, Schatzle P, Ludwig A, Tagaya M, Kunz B, Sonderegger P (2012). Calsyntenin-1 shelters APP from proteolytic processing during anterograde axonal transport. Biol Open 1, 761-774.
28. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, Raman R, Davies P, Masliah E, Williams DS, et al. (2005). Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307, 1282-1288.
29. Suzuki T, Nakaya T (2008). Regulation of amyloid beta-protein precursor by phosphorylation and protein interactions. J Biol Chem 283, 29633-29637.
30. Taru H, Iijima K, Hase M, Kirino Y, Yagi Y, Suzuki T (2002). Interaction of Alzheimer's beta-amyloid precursor family proteins with scaffold proteins of the JNK signaling cascade. J Biol Chem 277, 20070-20078.
31. Taru H, Suzuki T (2004). Facilitation of stress-induced phosphorylation of beta-amyloid precursor protein family members by X11-like/Mint2 protein. J Biol Chem 279, 21628-21636.
32. Thinakaran G, Koo EH (2008). Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283, 29615-29619.
33. Toprak E, Yildiz A, Hoffman MT, Rosenfeld SS, Selvin PR (2009). Why kinesin is so processive. Proc Natl Acad Sci USA 106, 12717-12722.
34. Vagnoni A, Glennon EB, Perkinton MS, Gray EH, Noble W, Miller CC (2013). Loss of c-Jun N-terminal kinase-interacting protein-1 does not affect axonal transport of the amyloid precursor protein or Abeta production. Hum Mol Genet 22, 4646-4652.
35. Vagnoni A, Perkinton MS, Gray EH, Francis PT, Noble W, Miller CC (2012). Calsyntenin-1 mediates axonal transport of the amyloid precursor protein and regulates Abeta production. Hum Mol Genet 21, 2845-2854.
36. Verhey KJ, Hammond JW (2009). Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10, 765-777.
37. 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.
38. 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.
39. Weston CR, Davis RJ (2007). The JNK signal transduction pathway. Curr Opin Cell Biol 19, 142-149.
40. Whitmarsh AJ, Kuan CY, Kennedy NJ, Kelkar N, Haydar TF, Mordes JP, Appel M, Rossini AA, Jones SN, Flavell RA, et al. (2001). Requirement of the JIP1 scaffold protein for stress-induced JNK activation. Genes Dev 15, 2421-2432.