PI4KIIα phosphorylation by GSK3 directs vesicular trafficking to lysosomes

Biochemical Journal

Volumn 464, Issue , 2014, Pages 145-156

  Robinson, James W ^a   Leshchyns'ka, Iryna ^b   Farghaian, Hovik ^a   Hughes, William E ^a   Sytnyk, Vladimir ^b   Neely, Graham G ^a   Cole, Adam R ^a  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Adaptin; Adaptor protein 3 (AP 3) complex; Glycogen synthase kinase 3 (GSK3); Lysosome; Phosphatidylinositol 4 kinase II (PI4KII ); Phosphorylation; Trafficking

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN 3 COMPLEX; AMPA RECEPTOR; GLYCOGEN SYNTHASE KINASE 3; PHOSPHATIDYLINOSITOL 4 KINASE II ALPHA; PHOSPHATIDYLINOSITOL KINASE; UNCLASSIFIED DRUG; PHOSPHATIDYLINOSITOL PHOSPHATE 4-KINASE; PHOSPHOTRANSFERASE;

ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONSENSUS SEQUENCE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; LYSOSOME; NEUROTRANSMISSION; PREDICTION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; ANIMAL; C57BL MOUSE; CELL CULTURE; ENZYMOLOGY; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE;

ANIMALS; BIOLOGICAL TRANSPORT; CELLS, CULTURED; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HELA CELLS; HUMANS; LYSOSOMES; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RATS; RATS, SPRAGUE-DAWLEY; TRANSPORT VESICLES;

EID: 84908376560     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140497     Document Type: Article

References (56)

1. Kaidanovich-Beilin, O. and Woodgett, J. R. (2011) GSK-3: functional insights from cell biology and animal models. Front. Mol. Neurosci. 4, 40
2. Cole, A. R. (2012) GSK3 as a sensor determining cell fate in the brain. Front. Mol. Neurosci. 5, 4
3. Hur, E. M. and Zhou, F. Q. (2010) GSK3 signalling in neural development. Nat. Rev. Neurosci. 11, 539-551
4. Mines, M. A., Beurel, E. and Jope, R. S. (2011) Regulation of cell survival mechanisms in Alzheimer's disease by glycogen synthase kinase-3. Int. J. Alzheimers Dis. 2011, 861072
5. Kim, W. Y. and Snider, W. D. (2011) Functions of GSK-3 signaling in development of the nervous system. Front. Mol. Neurosci. 4, 44
6. Cole, A. R. (2013) Regulation of cell fate in the brain by GSK3. In Trends in Cell Signalling Pathways in Neuronal Fate Decision (Wislet-Gendebien, S., ed.), pp. 153-177, InTech Publishing, Rijeka
7. Emamian, E. S., Hall, D., Birnbaum, M. J., Karayiorgou, M. and Gogos, J. A. (2004) Convergent evidence for impaired AKT1-GSK3β signaling in schizophrenia. Nat. Genet. 36, 131-137
8. Polter, A., Beurel, E., Yang, S., Garner, R., Song, L., Miller, C. A., Sweatt, J. D., McMahon, L., Bartolucci, A. A., Li, X. and Jope, R. S. (2010) Deficiency in the inhibitory serine-phosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology 35, 1761-1774
9. Klein, P. S. and Melton, D. A. (1996) A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 93, 8455-8459
10. Stambolic, V., Ruel, L. and Woodgett, J. R. (1996) Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6, 1664-1668
11. Hedgepeth, C. M., Conrad, L. J., Zhang, J., Huang, H. C., Lee, V. M. and Klein, P. S. (1997) Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev. Biol. 185, 82-91
12. De Sarno, P., Li, X. and Jope, R. S. (2002) Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 43, 1158-1164
13. Li, X. and Jope, R. S. (2010) Is glycogen synthase kinase-3 a central modulator in mood regulation? Neuropsychopharmacology 35, 2143-2154
14. Chiu, C. T. and Chuang, D. M. (2010) Molecular actions and therapeutic potential of lithium in preclinical and clinical studies of CNS disorders. Pharmacol. Ther. 128, 281-304
15. Peineau, S., Nicolas, C. S., Bortolotto, Z. A., Bhat, R. V., Ryves, W. J., Harwood, A. J., Dournaud, P., Fitzjohn, S. M. and Collingridge, G. L. (2009) A systematic investigation of the protein kinases involved in NMDA receptor-dependent LTD: evidence for a role of GSK-3 but not other serine/threonine kinases. Mol. Brain 2, 22
16. Peineau, S., Taghibiglou, C., Bradley, C., Wong, T. P., Liu, L., Lu, J., Lo, E., Wu, D., Saule, E., Bouschet, T. et al. (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53, 703-717
17. Hooper, C., Markevich, V., Plattner, F., Killick, R., Schofield, E., Engel, T., Hernandez, F., Anderton, B., Rosenblum, K., Bliss, T. et al. (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur. J. Neurosci. 25, 81-86
18. Zhu, L. Q., Wang, S. H., Liu, D., Yin, Y. Y., Tian, Q., Wang, X. C., Wang, Q., Chen, J. G. and Wang, J. Z. (2007) Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments. J. Neurosci. 27, 12211-12220
19. Zhu, L. Q., Liu, D., Hu, J., Cheng, J., Wang, S. H., Wang, Q., Wang, F., Chen, J. G. and Wang, J. Z. (2010) GSK-3 beta inhibits presynaptic vesicle exocytosis by phosphorylating P/Q-type calcium channel and interrupting SNARE complex formation. J. Neurosci. 30, 3624-3633
20. Chen, P., Gu, Z., Liu, W. and Yan, Z. (2007) Glycogen synthase kinase 3 regulates N-methyl-D-aspartate receptor channel trafficking and function in cortical neurons. Mol. Pharmacol. 72, 40-51
21. Nishimoto, T., Kihara, T., Akaike, A., Niidome, T. and Sugimoto, H. (2009) AMPA reduces surface expression of NR1 through regulation of GSK3beta. Neuroreport 20, 161-165
22. Wei, J., Liu, W. and Yan, Z. (2010) Regulation of AMPA receptor trafficking and function by glycogen synthase kinase 3. J. Biol. Chem. 285, 26369-26376
23. 2+ influx and catecholamine secretion after lithium withdrawal. Neuropharmacology 57, 311-321
24. Chen, L., Salinas, G. D. and Li, X. (2009) Regulation of serotonin 1B receptor by glycogen synthase kinase-3. Mol. Pharmacol. 76, 1150-1161
25. Chen, L., Zhou, W., Chen, P. C., Gaisina, I., Yang, S. and Li, X. (2011) Glycogen synthase kinase-3beta is a functional modulator of serotonin-1B receptors. Mol. Pharmacol. 79, 974-986
26. Sutherland, C. (2011) What are the bona fide GSK3 substrates? Int. J. Alzheimers. Dis. 2011, 505607
27. Frame, S. and Cohen, P. (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359, 1-16
28. Kennelly, P. J. and Krebs, E. G. (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266, 15555-15558
29. Farghaian, H., Turnley, A. M., Sutherland, C. and Cole, A. R. (2011) Bioinformatic prediction and confirmation of beta-adducin as a novel substrate of glycogen synthase kinase 3. J. Biol. Chem. 286, 25274-25283
30. Sytnyk, V., Leshchyns'ka, I., Delling, M., Dityateva, G., Dityatev, A. and Schachner, M. (2002) Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts. J. Cell Biol. 159, 649-661
31. Balla, A., Tuymetova, G., Barshishat, M., Geiszt, M. and Balla, T. (2002) Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 277, 20041-20050
32. Wang, Y. J., Wang, J., Sun, H. Q., Martinez, M., Sun, Y. X., Macia, E., Kirchhausen, T., Albanesi, J. P., Roth, M. G. and Yin, H. L. (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299-310
33. Guo, J., Wenk, M. R., Pellegrini, L., Onofri, F., Benfenati, F. and De Camilli, P. (2003) Phosphatidylinositol 4-kinase type IIα is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. U. S. A. 100, 3995-4000
34. Bain, J., Plater, L., Elliott, M., Shpiro, N., Hastie, C. J., McLauchlan, H., Klevernic, I., Arthur, J. S., Alessi, D. R. and Cohen, P. (2007) The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297-315
35. Cole, A. R., Soutar, M. P., Rembutsu, M., van Aalten, L., Hastie, C. J., McLauchlan, H., Peggie, M., Balastik, M., Lu, K. P. and Sutherland, C. (2008) Relative resistance of Cdk5-phosphorylated CRMP2 to dephosphorylation. J. Biol. Chem. 283, 18227-18237
36. Craige, B., Salazar, G. and Faundez, V. (2008) Phosphatidylinositol-4-kinase type IIα contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic. Mol. Biol. Cell 19, 1415-1426
37. Mossinger, J., Wieffer, M., Krause, E., Freund, C., Gerth, F., Krauss, M. and Haucke, V. (2012) Phosphatidylinositol 4-kinase IIα function at endosomes is regulated by the ubiquitin ligase Itch. EMBO Rep. 13, 1087-1094
38. Chen, C. H., Hwang, S. L., Howng, S. L., Chou, C. K. and Hong, Y. R. (2000) Three rat brain alternative splicing dynamin-like protein variants: interaction with the glycogen synthase kinase 3β and action as a substrate. Biochem. Biophys. Res. Commun. 268, 893-898
39. Clayton, E. L., Sue, N., Smillie, K. J., O'Leary, T., Bache, N., Cheung, G., Cole, A. R., Wyllie, D. J., Sutherland, C., Robinson, P. J. and Cousin, M. A. (2010) Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat. Neurosci. 13, 845-851
40. Keune, W. J., Jones, D. R., Bultsma, Y., Sommer, L., Zhou, X. Z., Lu, K. P. and Divecha, N. (2012) Regulation of phosphatidylinositol-5-phosphate signaling by Pin1 determines sensitivity to oxidative stress. Sci. Signal. 5, ra86
41. Nishimura, T., Fukata, Y., Kato, K., Yamaguchi, T., Matsuura, Y., Kamiguchi, H. and Kaibuchi, K. (2003) CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat. Cell Biol. 5, 819-826
42. Brittain, J. M., Duarte, D. B., Wilson, S. M., Zhu, W., Ballard, C., Johnson, P. L., Liu, N., Xiong, W., Ripsch, M. S., Wang, Y. et al. (2011) Suppression of inflammatory and neuropathic pain by uncoupling CRMP-2 from the presynaptic Ca (2) channel complex. Nat. Med. 17, 822-829
43. Brittain, J. M., Piekarz, A. D., Wang, Y., Kondo, T., Cummins, T. R. and Khanna, R. (2009) An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated calcium channels. J. Biol. Chem. 284, 31375-31390
44. Chi, X. X., Schmutzler, B. S., Brittain, J. M., Wang, Y., Hingtgen, C. M., Nicol, G. D. and Khanna, R. (2009) Regulation of N-type voltage-gated calcium channels (Cav2.2) and transmitter release by collapsin response mediator protein-2 (CRMP-2) in sensory neurons. J. Cell Sci. 122, 4351-4362
45. Brittain, J. M., Wang, Y., Eruvwetere, O. and Khanna, R. (2012) Cdk5-mediated phosphorylation of CRMP-2 enhances its interaction with CaV2.2. FEBS Lett. 586, 3813-3818
46. Lu, D., Sun, H. Q., Wang, H., Barylko, B., Fukata, Y., Fukata, M., Albanesi, J. P. and Yin, H. L. (2012) Phosphatidylinositol 4-kinase IIα is palmitoylated by Golgi-localized palmitoyltransferases in cholesterol-dependent manner. J. Biol. Chem. 287, 21856-21865
47. Barylko, B., Mao, Y. S., Wlodarski, P., Jung, G., Binns, D. D., Sun, H. Q., Yin, H. L. and Albanesi, J. P. (2009) Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase IIα. J. Biol. Chem. 284, 9994-10003
48. Salazar, G., Craige, B., Wainer, B. H., Guo, J., De Camilli, P. and Faundez, V. (2005) Phosphatidylinositol-4-kinase type IIα is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 16, 3692-3704
49. Cole, A. R., Causeret, F., Yadirgi, G., Hastie, C. J., McLauchlan, H., McManus, E. J., Hernández, F., Eickholt, B. J., Nikolic, M. and Sutherland, C. (2006) Distinct priming kinases contribute to differential regulation of collapsin response mediator proteins by glycogen synthase kinase-3 in vivo. J. Biol. Chem. 281, 16591-16598
50. Minogue, S., Waugh, M. G., De Matteis, M. A., Stephens, D. J., Berditchevski, F. and Hsuan, J. J. (2006) Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J. Cell Sci. 119, 571-581
51. Jović, M., Kean, M. J., Szentpetery, Z., Polevoy, G., Gingras, A. C., Brill, J. A. and Balla, T. (2012) Two phosphatidylinositol 4-kinases control lysosomal delivery of the Gaucher disease enzyme, β-glucocerebrosidase. Mol. Biol. Cell 23, 1533-1545
52. Daboussi, L., Costaguta, G. and Payne, G. S. (2012) Phosphoinositide-mediated clathrin adaptor progression at the trans-Golgi network. Nat. Cell Biol. 14, 239-248
53. Adachi, A., Kano, F., Tsuboi, T., Fujita, M., Maeda, Y. and Murata, M. (2010) Golgi-associated GSK3beta regulates the sorting process of post-Golgi membrane trafficking. J. Cell Sci. 123, 3215-3225
54. Hanley, J. G. (2010) Endosomal sorting of AMPA receptors in hippocampal neurons. Biochem. Soc. Trans. 38, 460-465
55. Kessels, H. W. and Malinow, R. (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61, 340-350
56. Kerchner, G. A. and Nicoll, R. A. (2008) Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat. Rev. Neurosci. 9, 813-825