Endosomal sorting of VAMP3 is regulated by PI4K2A

Journal of Cell Science

Volumn 127, Issue 17, 2014, Pages 3745-3756

  Jović, Marko ^a   Kean, Michelle J ^b,c,f   Dubankova, Anna ^d   Boura, Evzen ^d   Gingras, Anne Claude ^b,c   Brill, Julie A ^c,e   Balla, Tamas ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^e HOSPITAL FOR SICK CHILDREN   (Canada)

^f ROCKEFELLER UNIVERSITY   (United States)

Author keywords

PI4K2A; Ptdins4p; SNARE; Sorting; VAMP3; Vesicle fusion

Indexed keywords

CELLUBREVIN; PHOSPHATIDYLINOSITOL PHOSPHATE 4-KINASE; PHOSPHOTRANSFERASE; SNARE PROTEIN; TRANSFERRIN RECEPTOR; VESICULAR TRANSPORT PROTEIN;

ANIMAL; CELL MEMBRANE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; ENDOSOME; HUMAN; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOSOMES; HUMANS; MEMBRANE FUSION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN TRANSPORT; RECEPTORS, TRANSFERRIN; SNARE PROTEINS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 3; VESICULAR TRANSPORT PROTEINS;

EID: 84906861424     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.148809     Document Type: Article

References (51)

1. Balla, A. and Balla, T. (2006). Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 16, 351-361.
2. 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.
3. Balla, A., Tuymetova, G., Tsiomenko, A., Várnai, P. and Balla, T. (2005). A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol. Biol. Cell 16, 1282-1295.
4. Balla, A., Kim, Y. J., Varnai, P., Szentpetery, Z., Knight, Z., Shokat, K. M. and Balla, T. (2008). Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIalpha. Mol. Biol. Cell 19, 711-721.
5. Barylko, B., Gerber, S. H., Binns, D. D., Grichine, N., Khvotchev, M., Südhof, T. C. and Albanesi, J. P. (2001). A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans. J. Biol. Chem. 276, 7705-7708.
6. Bethani, I., Lang, T., Geumann, U., Sieber, J. J., Jahn, R. and Rizzoli, S. O. (2007). The specificity of SNARE pairing in biological membranes is mediated by both proof-reading and spatial segregation. EMBO J. 26, 3981-3992.
7. Brandhorst, D., Zwilling, D., Rizzoli, S. O., Lippert, U., Lang, T. and Jahn, R. (2006). Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity. Proc. Natl. Acad. Sci. USA 103, 2701-2706.
8. Burgess, J., Del Bel, L. M., Ma, C. I., Barylko, B., Polevoy, G., Rollins, J., Albanesi, J. P., Krämer, H. and Brill, J. A. (2012). Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. Development 139, 3040-3050.
9. Craige, B., Salazar, G. and Faundez, V. (2008). Phosphatidylinositol-4-kinase type II alpha contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic. Mol. Biol. Cell 19, 1415-1426.
10. Ellena, J. F., Liang, B., Wiktor, M., Stein, A., Cafiso, D. S., Jahn, R. and Tamm, L. K. (2009). Dynamic structure of lipid-bound synaptobrevin suggests a nucleation-propagation mechanism for trans-SNARE complex formation. Proc. Natl. Acad. Sci. USA 106, 20306-20311.
11. Fasshauer, D., Sutton, R. B., Brunger, A. T. and Jahn, R. (1998). Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. USA 95, 15781-15786.
12. Fasshauer, D., Antonin, W., Margittai, M., Pabst, S. and Jahn, R. (1999). Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties. J. Biol. Chem. 274, 15440-15446.
13. Feng, D., Crane, K., Rozenvayn, N., Dvorak, A. M. and Flaumenhaft, R. (2002). Subcellular distribution of 3 functional platelet SNARE proteins: human cellubrevin, SNAP-23, and syntaxin 2. Blood 99, 4006-4014.
14. Galli, T., Chilcote, T., Mundigl, O., Binz, T., Niemann, H. and De Camilli, P. (1994). Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J. Cell Biol. 125, 1015-1024.
15. Ganley, I. G., Espinosa, E. and Pfeffer, S. R. (2008). A syntaxin 10-SNARE complex distinguishes two distinct transport routes from endosomes to the trans-Golgi in human cells. J. Cell Biol. 180, 159-172.
16. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G. and Stenmark, H. (2000). Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
17. Gillooly, D. J., Raiborg, C. and Stenmark, H. (2003). Phosphatidylinositol 3-phosphate is found in microdomains of early endosomes. Histochem. Cell Biol. 120, 445-453.
18. Gordon, D. E., Mirza, M., Sahlender, D. A., Jakovleska, J. and Peden, A. A. (2009). Coiled-coil interactions are required for post-Golgi R-SNARE trafficking. EMBO Rep. 10, 851-856.
19. Goudreault, M., D'Ambrosio, L. M., Kean, M. J., Mullin, M. J., Larsen, B. G., Sanchez, A., Chaudhry, S., Chen, G. I., Sicheri, F., Nesvizhskii, A. I. et al. (2009). A PP2A phosphatase high density interaction network identifies a novel striatin-interacting phosphatase and kinase complex linked to the cerebral cavernous malformation 3 (CCM3) protein. Mol. Cell. Proteomics 8, 157-171.
20. Guo, J., Wenk, M. R., Pellegrini, L., Onofri, F., Benfenati, F. and De Camilli, P. (2003). Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. USA 100, 3995-4000.
21. Hsu, V. W., Bai, M. and Li, J. (2012). Getting active: protein sorting in endocytic recycling. Nat. Rev. Mol. Cell Biol. 13, 323-328.
22. Inoue, T., Heo, W. D., Grimley, J. S., Wandless, T. J. and Meyer, T. (2005). An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat. Methods 2, 415-418.
23. 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, b-glucocerebrosidase. Mol. Biol. Cell 23, 1533-1545.
24. Knight, Z. A., Gonzalez, B., Feldman, M. E., Zunder, E. R., Goldenberg, D. D., Williams, O., Loewith, R., Stokoe, D., Balla, A., Toth, B. et al. (2006). A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling. Cell 125, 733-747.
25. Komatsu, T., Kukelyansky, I., McCaffery, J. M., Ueno, T., Varela, L. C. and Inoue, T. (2010). Organelle-specific, rapid induction of molecular activities and membrane tethering. Nat. Methods 7, 206-208.
26. Liu, G., Zhang, J., Larsen, B., Stark, C., Breitkreutz, A., Lin, Z. Y., Breitkreutz, B. J., Ding, Y., Colwill, K., Pasculescu, A. et al. (2010). ProHits: integrated software for mass spectrometry-based interaction proteomics. Nat. Biotechnol. 28, 1015-1017.
27. Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B. and Johannes, L. (2002). Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156, 653-664.
28. Martinez-Arca, S., Rudge, R., Vacca, M., Raposo, G., Camonis, J., Proux-Gillardeaux, V., Daviet, L., Formstecher, E., Hamburger, A., Filippini, F. et al. (2003). A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. USA 100, 9011-9016.
29. Maxfield, F. R. and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132.
30. Mayer, A., Wickner, W. and Haas, A. (1996). Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85, 83-94.
31. McMahon, H. T., Ushkaryov, Y. A., Edelmann, L., Link, E., Binz, T., Niemann, H., Jahn, R. and Südhof, T. C. (1993). Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 364, 346-349.
32. McNew, J. A., Parlati, F., Fukuda, R., Johnston, R. J., Paz, K., Paumet, F., Söllner, T. H. and Rothman, J. E. (2000). Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407, 153-159.
33. Miller, S. E., Sahlender, D. A., Graham, S. C., Höning, S., Robinson, M. S., Peden, A. A. and Owen, D. J. (2011). The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147, 1118-1131.
34. 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.
35. Naughtin, M. J., Sheffield, D. A., Rahman, P., Hughes, W. E., Gurung, R., Stow, J. L., Nandurkar, H. H., Dyson, J. M. and Mitchell, C. A. (2010). The myotubularin phosphatase MTMR4 regulates sorting from early endosomes. J. Cell Sci. 123, 3071-3083.
36. Pan, W., Choi, S. C., Wang, H., Qin, Y., Volpicelli-Daley, L., Swan, L., Lucast, L., Khoo, C., Zhang, X., Li, L. et al. (2008). Wnt3a-mediated formation of phosphatidylinositol 4,5-bisphosphate regulates LRP6 phosphorylation. Science 321, 1350-1353.
37. Parlati, F., Varlamov, O., Paz, K., McNew, J. A., Hurtado, D., Söllner, T. H. and Rothman, J. E. (2002). Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity. Proc. Natl. Acad. Sci. USA 99, 5424-5429.
38. Poirier, M. A., Xiao, W., Macosko, J. C., Chan, C., Shin, Y. K. and Bennett, M. K. (1998). The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5, 765-769.
39. Polgár, J., Chung, S. H. and Reed, G. L. (2002). Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood 100, 1081-1083.
40. Regazzi, R., Sadoul, K., Meda, P., Kelly, R. B., Halban, P. A. and Wollheim, C. B. (1996). Mutational analysis of VAMP domains implicated in Ca2+-induced insulin exocytosis. EMBO J. 15, 6951-6959.
41. Rothenberger, F., Velic, A., Stehberger, P. A., Kovacikova, J. and Wagner, C. A. (2007). Angiotensin II stimulates vacuolar H+ -ATPase activity in renal acid-secretory intercalated cells from the outer medullary collecting duct. J. Am. Soc. Nephrol. 18, 2085-2093.
42. Ryder, P. V., Vistein, R., Gokhale, A., Seaman, M. N., Puthenveedu, M. A. and Faundez, V. (2013). The WASH complex, an endosomal Arp2/3 activator, interacts with the Hermansky-Pudlak syndrome complex BLOC-1 and its cargo phosphatidylinositol-4-kinase type IIa. Mol. Biol. Cell 24, 2269-2284.
43. Salazar, G., Zlatic, S., Craige, B., Peden, A. A., Pohl, J. and Faundez, V. (2009). Hermansky-Pudlak syndrome protein complexes associate with phosphatidylinositol 4-kinase type II alpha in neuronal and non-neuronal cells. J. Biol. Chem. 284, 1790-1802.
44. Simons, J. P., Al-Shawi, R., Minogue, S., Waugh, M. G., Wiedemann, C., Evangelou, S., Loesch, A., Sihra, T. S., King, R., Warner, T. T. et al. (2009). Loss of phosphatidylinositol 4-kinase 2alpha activity causes late onset degeneration of spinal cord axons. Proc. Natl. Acad. Sci. USA 106, 11535-11539.
45. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. and Rothman, J. E. (1993). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418.
46. Sutton, R. B., Fasshauer, D., Jahn, R. and Brunger, A. T. (1998). Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353.
47. Szentpetery, Z., Várnai, P. and Balla, T. (2010). Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc. Natl. Acad. Sci. USA 107, 8225-8230.
48. Vicogne, J., Vollenweider, D., Smith, J. R., Huang, P., Frohman, M. A. and Pessin, J. E. (2006). Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc. Natl. Acad. Sci. USA 103, 14761-14766.
49. Volchuk, A., Sargeant, R., Sumitani, S., Liu, Z., He, L. and Klip, A. (1995). Cellubrevin is a resident protein of insulin-sensitive GLUT4 glucose transporter vesicles in 3T3-L1 adipocytes. J. Biol. Chem. 270, 8233-8240.
50. 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.
51. Xu, H. and Wickner, W. (2010). Phosphoinositides function asymmetrically for membrane fusion, promoting tethering and 3Q-SNARE subcomplex assembly. J. Biol. Chem. 285, 39359-39365.