POPX2 phosphatase regulates the KIF3 kinesin motor complex

Journal of Cell Science

Volumn 127, Issue 4, 2014, Pages 727-739

  Phang, Hui Qun ^a   Hoon, Jing Ling ^a   Lai, Soak Kuan ^a   Zeng, Yukai ^b   Chiam, Keng Hwee ^b,c   Li, Hoi Yeung ^a   Koh, Cheng Gee ^a,c  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b BIOINFORMATICS INSTITUTE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Calcium calmodulin kinase; Kinesin 2 motor N cadherin; POPX2 phosphatase

Indexed keywords

CALCIUM-CALMODULIN KINASE; KINESIN-2 MOTOR; N-CADHERIN; POPX2 PHOSPHATASE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; BETA CATENIN; CADHERINS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL ADHESION; CERCOPITHECUS AETHIOPS; CONSERVED SEQUENCE; COS CELLS; HELA CELLS; HUMANS; KINESIN; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT;

EID: 84894103447     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.126482     Document Type: Article

References (41)

1. Ballif, B. A., Villé n, J., Beausoleil, S. A., Schwartz, D. and Gygi, S. P. (2004). Phosphoproteomic analysis of the developing mouse brain. Mol. Cell. Proteomics 3, 1093-1101.
2. Cahu, J., Olichon, A., Hentrich, C., Schek, H., Drinjakovic, J., Zhang, C., Doherty-Kirby, A., Lajoie, G. and Surrey, T. (2008). Phosphorylation by Cdk1 increases the binding of Eg5 to microtubules in vitro and in Xenopus egg extract spindles. PLoS ONE 3, e3936.
3. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J. and Gygi, S. P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762-10767.
4. Endow, S. A., Kull, F. J. and Liu, H. (2010). Kinesins at a glance. J. Cell Sci. 123, 3420-3424.
5. Espeut, J., Gaussen, A., Bieling, P., Morin, V., Prieto, S., Fesquet, D., Surrey, T. and Abrieu, A. (2008). Phosphorylation relieves autoinhibition of the kinetochore motor Cenp-E. Mol. Cell 29, 637-643.
6. Friedman, D. S. and Vale, R. D. (1999). Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat. Cell Biol. 1, 293-297.
7. Guillaud, L., Wong, R. and Hirokawa, N. (2008). Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 10, 19-29.
8. Hammond, J. W., Blasius, T. L., Soppina, V., Cai, D. and Verhey, K. J. (2010). Autoinhibition of the kinesin-2 motor KIF17 via dual intramolecular mechanisms. J. Cell Biol. 189, 1013-1025.
9. Hirokawa, N. (2000). Stirring up development with the heterotrimeric kinesin KIF3. Traffic 1, 29-34.
10. Hirokawa, N., Nitta, R. and Okada, Y. (2009). The mechanisms of kinesin motor motility: lessons from the monomeric motor KIF1A. Nat. Rev. Mol. Cell Biol. 10, 877-884.
11. Huttlin, E. L., Jedrychowski, M. P., Elias, J. E., Goswami, T., Rad, R., Beausoleil, S. A., Villé n, J., Haas, W., Sowa, M. E. and Gygi, S. P. (2010). A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189.
12. Ichimura, T., Wakamiya-Tsuruta, A., Itagaki, C., Taoka, M., Hayano, T., Natsume, T. and Isobe, T. (2002). Phosphorylation-dependent interaction of kinesin light chain 2 and the 14-3-3 protein. Biochemistry 41, 5566-5572.
13. Ishida, A., Kameshita, I. and Fujisawa, H. (1998). A novel protein phosphatase that dephosphorylates and regulates Ca2+/calmodulin-dependent protein kinase II. J. Biol. Chem. 273, 1904-1910.
14. Jang, Y. N., Jung, Y. S., Lee, S. H., Moon, C. H., Kim, C. H. and Baik, E. J. (2009). Calpain-mediated N-cadherin proteolytic processing in brain injury. J. Neurosci. 29, 5974-5984.
15. Jaqaman, K., Loerke, D., Mettlen, M., Kuwata, H., Grinstein, S., Schmid, S. L. and Danuser, G. (2008). Robust single-particle tracking in live-cell time-lapse sequences. Nat. Methods 5, 695-702.
16. Jimbo, T., Kawasaki, Y., Koyama, R., Sato, R., Takada, S., Haraguchi, K. and Akiyama, T. (2002). Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat. Cell Biol. 4, 323-327.
17. Kanemaru, K., Kubota, J., Sekiya, H., Hirose, K., Okubo, Y. and Iino, M. (2013). Calcium-dependent N-cadherin up-regulation mediates reactive astrogliosis and neuroprotection after brain injury. Proc. Natl. Acad. Sci. USA 110, 11612-11617.
18. Koh, C. G., Tan, E. J., Manser, E. and Lim, L. (2002). The p21-activated kinase PAK is negatively regulated by POPX1 and POPX2, a pair of serine/threonine phosphatases of the PP2C family. Curr. Biol. 12, 317-321.
19. Loubéry, S., Wilhelm, C., Hurbain, I., Neveu, S., Louvard, D. and Coudrier, E. (2008). Different microtubule motors move early and late endocytic compartments. Traffic 9, 492-509.
20. Lowe, D. G. (2004). Distinctive image features from scale-invariant keypoints. Int. J. Comput. Vis. 60, 91-110.
21. Manser, E., Loo, T. H., Koh, C. G., Zhao, Z. S., Chen, X. Q., Tan, L., Tan, I., Leung, T. and Lim, L. (1998). PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1, 183-192.
22. Mary, S., Charrasse, S., Meriane, M., Comunale, F., Travo, P., Blangy, A. and Gauthier-Rouvière, C. (2002). Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. Mol. Biol. Cell 13, 285-301.
23. Morfini, G. A., You, Y. M., Pollema, S. L., Kaminska, A., Liu, K., Yoshioka, K., Bjö rkblom, B., Coffey, E. T., Bagnato, C., Han, D. et al. (2009). Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat. Neurosci. 12, 864-871.
24. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A. et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3.
25. Ozawa, M., Ringwald, M. and Kemler, R. (1990). Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Natl. Acad. Sci. USA 87, 4246-4250.
26. Pan, C., Gnad, F., Olsen, J. V. and Mann, M. (2008). Quantitative phosphoproteome analysis of a mouse liver cell line reveals specificity of phosphatase inhibitors. Proteomics 8, 4534-4546.
27. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
28. Schonteich, E., Wilson, G. M., Burden, J., Hopkins, C. R., Anderson, K., Goldenring, J. R. and Prekeris, R. (2008). The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J. Cell Sci. 121, 3824-3833.
29. Singh, P., Gan, C. S., Guo, T., Phang, H. Q., Sze, S. K. and Koh, C. G. (2011). Investigation of POPX2 phosphatase functions by comparative phosphoproteomic analysis. Proteomics 11, 2891-2900.
30. Stock, M. F., Guerrero, J., Cobb, B., Eggers, C. T., Huang, T. G., Li, X. and Hackney, D. D. (1999). Formation of the compact confomer of kinesin requires a COOH-terminal heavy chain domain and inhibits microtubule-stimulated ATPase activity. J. Biol. Chem. 274, 14617-14623.
31. Susila, A., Chan, H., Loh, A. X., Phang, H. Q., Wong, E. T., Tergaonkar, V. and Koh, C. G. (2010). The POPX2 phosphatase regulates cancer cell motility and invasiveness. Cell Cycle 9, 179-187.
32. Takeda, S., Yamazaki, H., Seog, D. H., Kanai, Y., Terada, S. and Hirokawa, N. (2000). Kinesin superfamily protein 3 (KIF3) motor transports fodrinassociating vesicles important for neurite building. J. Cell Biol. 148, 1255-1266.
33. Tanuma, N., Nomura, M., Ikeda, M., Kasugai, I., Tsubaki, Y., Takagaki, K., Kawamura, T., Yamashita, Y., Sato, I., Sato, M. et al. (2009). Protein phosphatase Dusp26 associates with KIF3 motor and promotes N-cadherinmediated cell-cell adhesion. Oncogene 28, 752-761.
34. Teng, J., Rai, T., Tanaka, Y., Takei, Y., Nakata, T., Hirasawa, M., Kulkarni, A. B. and Hirokawa, N. (2005). The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium. Nat. Cell Biol. 7, 474-482.
35. Tweedie-Cullen, R. Y., Reck, J. M. and Mansuy, I. M. (2009). Comprehensive mapping of post-translational modifications on synaptic, nuclear, and histone proteins in the adult mouse brain. J. Proteome Res. 8, 4966-4982.
36. Vagnoni, A., Rodriguez, L., Manser, C., De Vos, K. J. and Miller, C. C. (2011). Phosphorylation of kinesin light chain 1 at serine 460 modulates binding and trafficking of calsyntenin-1. J. Cell Sci. 124, 1032-1042.
37. Wedaman, K. P., Meyer, D. W., Rashid, D. J., Cole, D. G. and Scholey, J. M. (1996). Sequence and submolecular localization of the 115-kD accessory subunit of the heterotrimeric kinesin-II (KRP85/95) complex. J. Cell Biol. 132, 371-380.
38. Winiewski, J. R., Nagaraj, N., Zougman, A., Gnad, F. and Mann, M. (2010). Brain phosphoproteome obtained by a FASP-based method reveals plasma membrane protein topology. J. Proteome Res. 9, 3280-3289.
39. Woniak, M. J. and Allan, V. J. (2006). Cargo selection by specific kinesin light chain 1 isoforms. EMBO J. 25, 5457-5468.
40. Xie, Y., Tan, E. J., Wee, S., Manser, E., Lim, L. and Koh, C. G. (2008). Functional interactions between phosphatase POPX2 and mDia modulate RhoA pathways. J. Cell Sci. 121, 514-521.
41. Zhang, S., Guo, T., Chan, H., Sze, S. K. and Koh, C. G. (2013). Integrative transcriptome and proteome study to identify the signaling network regulated by POPX2 phosphatase. J. Proteome Res. 12, 2525-2536.