Acetylcholine receptor (AChR) clustering is regulated both by glycogen synthase kinase 3β (GSK3β)-dependent Phosphorylation and the level of CLIP-associated protein 2 (CLASP2) mediating the capture of microtubule plus-ends

Journal of Biological Chemistry

Volumn 289, Issue 44, 2014, Pages 30857-30867

  Basu, Sreya ^a,c   Sladecek, Stefan ^a   Pemble, Hayley ^c   Wittmann, Torsten ^c   Slotman, Johan A ^d   Van Cappellen, Wiggert ^d   Brenner, Hans Rudolf ^a   Galjart, Niels ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d GENERAL ELECTRIC COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; CLASP2 PROTEIN, HUMAN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MICROTUBULE ASSOCIATED PROTEIN;

ANIMAL; C57BL MOUSE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; MICROTUBULE; PHOSPHORYLATION; PHYSIOLOGY; PRIMARY CELL CULTURE; PROTEIN PROCESSING; PROTEIN TRANSPORT; SKELETAL MUSCLE; ULTRASTRUCTURE;

AGRIN; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HUMANS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUSCLE FIBERS, SKELETAL; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECEPTORS, CHOLINERGIC;

EID: 84908701461     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.589457     Document Type: Article

References (33)

1. McMahan, U. J., Horton, S. E., Werle, M. J., Honig, L. S., Kröger, S., Ruegg, M. A., and Escher, G. (1992) Agrin isoforms and their role in synaptogenesis. Curr. Opin. Cell Biol. 4, 869-874
2. Sanes, J. R., and Lichtman, J. W. (1999) Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22, 389-442
3. Wu, H., Xiong, W. C., and Mei, L. (2010) To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137, 1017-1033
4. Kim, N., Stiegler, A. L., Cameron, T. O., Hallock, P. T., Gomez, A. M., Huang, J. H., Hubbard, S. R., Dustin, M. L., and Burden, S. J. (2008) Lrp4 is a receptor for agrin and forms a complex with MuSK. Cell 135, 334-342
5. Zhang, B., Luo, S., Wang, Q., Suzuki, T., Xiong, W. C., and Mei, L. (2008) LRP4 serves as a coreceptor of agrin. Neuron 60, 285-297
6. Cohen, I., Rimer, M., Lømo, T., and McMahan, U. J. (1997) Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol. Cell. Neurosci. 9, 237-253
7. Jones, G., Meier, T., Lichtsteiner, M., Witzemann, V., Sakmann, B., and Brenner, H. R. (1997) Induction by agrin of ectopic and functional postsynapticlike membrane in innervated muscle. Proc. Natl. Acad. Sci. U. S. A. 94, 2654-2659
8. Meier, T., Hauser, D. M., Chiquet, M., Landmann, L., Ruegg, M. A., and Brenner, H. R. (1997) Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers. J. Neurosci. 17, 6534-6544
9. Chen, Y., Ip, F. C., Shi, L., Zhang, Z., Tang, H., Ng, Y. P., Ye, W. C., Fu, A. K., and Ip, N. Y. (2014) Coronin 6 regulates acetylcholine receptor clustering through modulating receptor anchorage to actin cytoskeleton. J. Neurosci. 34, 2413-2421
10. Dai, Z., Luo, X., Xie, H., and Peng, H. B. (2000) The actin-driven movement and formation of acetylcholine receptor clusters. J. Cell Biol. 150, 1321-1334
11. Geng, L., Qian, Y. K., Madhavan, R., and Peng, H. B. (2008) Transmembrane mechanisms in the assembly of the postsynaptic apparatus at the neuromuscular junction. Chem. Biol. Interact. 175, 108-112
12. Hall, Z. W., Lubit, B. W., and Schwartz, J. H. (1981) Cytoplasmic actin in postsynaptic structures at the neuromuscular junction. J. Cell Biol. 90, 789-792
13. Schmidt, N., Basu, S., Sladecek, S., Gatti, S., van Haren, J., Treves, S., Pielage, J., Galjart, N., and Brenner, H. R. (2012) Agrin regulates CLASP2-mediated capture of microtubules at the neuromuscular junction synaptic membrane. J. Cell Biol. 198, 421-437
14. Akhmanova, A., Hoogenraad, C. C., Drabek, K., Stepanova, T., Dortland, B., Verkerk, T., Vermeulen, W., Burgering, B. M., De Zeeuw, C. I., Grosveld, F., and Galjart, N. (2001) CLASPs are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104, 923-935
15. Wittmann, T., and Waterman-Storer, C. M. (2005) Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3β in migrating epithelial cells. J. Cell Biol. 169, 929-939
16. Watanabe, T., Noritake, J., Kakeno, M., Matsui, T., Harada, T., Wang, S., Itoh, N., Sato, K., Matsuzawa, K., Iwamatsu, A., Galjart, N., and Kaibuchi, K. (2009) Phosphorylation of CLASP2 by GSK-3β regulates its interaction with IQGAP1, EB1 and microtubules. J. Cell Sci. 122, 2969-2979
17. Mimori-Kiyosue, Y., Grigoriev, I., Lansbergen, G., Sasaki, H., Matsui, C., Severin, F., Galjart, N., Grosveld, F., Vorobjev, I., Tsukita, S., and Akhmanova, A. (2005) CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168, 141-153
18. Kumar, P., Chimenti, M. S., Pemble, H., Schönichen, A., Thompson, O., Jacobson, M. P., and Wittmann, T. (2012) Multisite phosphorylation disrupts arginine-glutamate salt bridge networks required for binding of cytoplasmic linker-associated protein 2 (CLASP2) to end-binding protein 1 (EB1). J. Biol. Chem. 287, 17050-17064
19. Patel, K., Nogales, E., and Heald, R. (2012) Multiple domains of human CLASP contribute to microtubule dynamics and organization in vitro and in Xenopus egg extracts. Cytoskeleton 69, 155-165
20. Kumar, P., Lyle, K. S., Gierke, S., Matov, A., Danuser, G., and Wittmann, T. (2009) GSK3β phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 184, 895-908
21. Efimov, A., Kharitonov, A., Efimova, N., Loncarek, J., Miller, P. M., Andreyeva, N., Gleeson, P., Galjart, N., Maia, A. R., McLeod, I. X., Yates, J. R., 3rd, Maiato, H., Khodjakov, A., Akhmanova, A., and Kaverina, I. (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev. Cell 12, 917-930
22. Lansbergen, G., Grigoriev, I., Mimori-Kiyosue, Y., Ohtsuka, T., Higa, S., Kitajima, I., Demmers, J., Galjart, N., Houtsmuller, A. B., Grosveld, F., and Akhmanova, A. (2006) CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5β. Dev. Cell 11, 21-32
23. Kishi, M., Kummer, T. T., Eglen, S. J., and Sanes, J. R. (2005) LL5β. J. Cell Biol. 169, 355-366
24. Blanco-Bose, W. E., Yao, C. C., Kramer, R. H., and Blau, H. M. (2001) Purification of mouse primary myoblasts based on γ7 integrin expression. Exp. Cell Res. 265, 212-220
25. Schmidt, N., Akaaboune, M., Gajendran, N., Martinez-Pena y Valenzuela, I., Wakefield, S., Thurnheer, R., and Brenner, H. R. (2011) Neuregulin/ErbB regulate neuromuscular junction development by phosphorylation of γ-dystrobrevin. J. Cell Biol. 195, 1171-1184
26. Jones, G., Herczeg, A., Ruegg, M. A., Lichtsteiner, M., Kröger, S., and Brenner, H. R. (1996) Substrate-bound agrin induces expression of acetylcholine receptor γ-subunit gene in cultured mammalian muscle cells. Proc. Natl. Acad. Sci. U. S. A. 93, 5985-5990
27. Lin, S., Landmann, L., Ruegg, M. A., and Brenner, H. R. (2008) The role of nerve versus muscle-derived factors in mammalian neuromuscular junction formation. J. Neurosci. 28, 3333-3340
28. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., and Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682
29. Sugiyama, J. E., Glass, D. J., Yancopoulos, G. D., and Hall, Z. W. (1997) Laminin-induced acetylcholine receptor clustering: an alternative pathway. J. Cell Biol. 139, 181-191
30. Drabek, K., van Ham, M., Stepanova, T., Draegestein, K., van Horssen, R., Sayas, C. L., Akhmanova, A., Ten Hagen, T., Smits, R., Fodde, R., Grosveld, F., and Galjart, N. (2006) Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr. Biol. 16, 2259-2264
31. Al-Bassam, J., and Chang, F. (2011) Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 21, 604-614
32. Maurer, S. P., Cade, N. I., Bohner, G., Gustafsson, N., Boutant, E., and Surrey, T. (2014) EB1 accelerates two conformational transitions important for microtubule maturation and dynamics. Curr. Biol. 24, 372-384
33. Slep, K. C., and Vale, R. D. (2007) Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol. Cell 27, 976-991