A WASp-binding type II phosphatidylinositol 4-kinase required for actin polymerization-driven endosome motility

Journal of Cell Biology

Volumn 171, Issue 1, 2005, Pages 133-142

  Chang, Fanny S ^a   Han, Gil Soo ^b   Carman, George M ^b   Blumer, Kendall J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; CARRIER PROTEIN; HYBRID PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; WISKOTT ALDRICH SYNDROME PROTEIN; WISKOTT ALDRICH SYNDROME PROTEIN BINDING PROTEIN TYPE II PHOSPHATIDYLINOSITOL 4 KINASE;

ACTIN POLYMERIZATION; ARTICLE; ENDOCYTOSIS; ENDOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SYNTHESIS;

1-PHOSPHATIDYLINOSITOL 4-KINASE; ACTINS; BIOLOGICAL TRANSPORT; ENDOSOMES; GENE DELETION; MOVEMENT; MUTATION; RECEPTORS, MATING FACTOR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; WISKOTT-ALDRICH SYNDROME PROTEIN;

MAMMALIA;

EID: 26444528971     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200501086     Document Type: Article

References (69)

1. Amatruda, J.F., D.J. Gattermeir, T.S. Karpova, and J.A. Cooper. 1992. Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution and polarized secretion in yeast. J. Cell Biol. 119:1151-1162.
2. Aniento, F., N. Emans, G. Griffiths, and J. Gruenberg. 1993. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J. Cell Biol. 123:1373-1387.
3. Apodaca, G. 2001. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic. 2:149-159.
4. Aschenbrenner, L., T. Lee, and T. Hasson. 2003. Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol. Biol. Cell. 14:2728-2743.
5. Audhya, A., M. Foti, and S.D. Emr. 2000. Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol. Biol. Cell. 11:2673-2689.
6. Balla, A., G. Tuymetova, M. Barshishat, M. Geiszt, and T. Balla. 2002. Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 277:20041-20050.
7. Bananis, E., J.W. Murray, R.J. Stockert, P. Satir, and A.W. Wolkoff. 2003. Regulation of early endocytic vesicle motility and fission in a reconstituted system. J. Cell Sci. 116:2749-2761.
8. Barylko, B., P. Wlodarski, D.D. Binns, S.H. Gerber, S. Earnest, T.C. Sudhof, N. Grichine, and J.P. Albanesi. 2002. Analysis of the catalytic domain of phosphatidylinositol 4-kinase type II. J. Biol. Chem. 277:44366-44375.
9. Benesch, S., S. Lommel, A. Steffen, T.E. Stradal, N. Scaplehorn, M. Way, J. Wehland, and K. Rottner. 2002. Phosphatidylinositol 4,5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J. Biol. Chem. 277:37771-37776.
10. Carloni, V., A. Mazzocca, and K.S. Ravichandran. 2004. Tetraspanin CD81 is linked to ERK/MAPKinase signaling by Shc in liver tumor cells. Oncogene. 23:1566-1574.
11. Carlsson, A.E., A.D. Shah, D. Elking, T.S. Karpova, and J.A. Cooper. 2002. Quantitative analysis of actin patch movement in yeast. Biophys. J. 82:2333-2343.
12. Chang, F.S., C.J. Stefan, and K.J. Blumer. 2003. A WASp homolog powers actin polymerization-dependent motility of endosomes in vivo. Curr. Biol. 13:455-463.
13. Davis, N.G., J.L. Horecka, and G.F. Sprague Jr. 1993. Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol. 122:53-65.
14. de Graaf, P., E.E. Klapisz, T.K. Schulz, A.F. Cremers, A.J. Verkleij, and P.M. van Bergen en Henegouwen. 2002. Nuclear localization of phosphatidylinositol 4-kinase beta. J Cell Sci. 115:1769-75.
15. Duncan, M.C., M.J. Cope, B.L. Goode, B. Wendland, and D.G. Drubin. 2001. Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat. Cell Biol. 3:687-690.
16. Eden, S., R. Rohatgi, A.V. Podtelejnikov, M. Mann, and M.W. Kirschner. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature. 418:790-793.
17. Eitzen, G., L. Wang, N. Thorngren, and W. Wickner. 2002. Remodeling of organelle-bound actin is required for yeast vacuole fusion. J. Cell Biol. 158:669-679.
18. Engqvist-Goldstein, A.E., and D.G. Drubin. 2003. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19:287-332.
19. Evangelista, M., B.M. Klebl, A.H. Tong, B.A. Webb, T. Leeuw, E. Leberer, M. Whiteway, D.Y. Thomas, and C. Boone. 2000. A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex. J. Cell Biol. 148:353-362.
20. Evangelista, M., D. Pruyne, D.C. Amberg, C. Boone, and A. Bretscher. 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4:32-41.
21. Gaborik, Z., and L. Hunyady. 2004. Intracellular trafficking of hormone receptors. Trends Endocrinol. Metab. 15:286-293.
22. Geli, M.I., R. Lombardi, B. Schmelzl, and H. Riezman. 2000. An intact SH3 domain is required for myosin I-induced actin polymerization. EMBO J. 19:4281-4291.
23. Guo, J., M.R. Wenk, L. Pellegrini, F. Onofri, F. Benfenati, and P. De Camilli. 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.
24. Han, G.S., A. Audhya, D.J. Markley, S.D. Emr, and G.M. Carman. 2002. The Saccharomyces cerevisiae LSB6 gene encodes phosphatidylinositol 4-kinase activity. J. Biol. Chem. 277:47709-47718.
25. Hasson, T. 2003. Myosin VI: two distinct roles in endocytosis. J. Cell Sci. 116:3453-3461.
26. Higgs, H.N., and T.D. Pollard. 2001. Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70:649-676.
27. Ho, H.Y., R. Rohatgi, A.M. Lebensohn, M. Le, J. Li, S.P. Gygi, and M.W. Kirschner. 2004. Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell. 118:203-216.
28. Huckaba, T.M., A.C. Gay, L.F. Pantalena, H.C. Yang, and L.A. Pon. 2004. Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 167:519-530.
29. Innocenti, M., A. Zucconi, A. Disanza, E. Frittoli, L.B. Areces, A. Steffen, T.E. Stradal, P.P. Di Fiore, M.F. Carlier, and G. Scita. 2004. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat. Cell Biol. 6:319-327.
30. James, P., J. Halladay, and E.A. Craig. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 144:1425-1436.
31. Kaksonen, M., H.B. Peng, and H. Rauvala. 2000. Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. J. Cell Sci. 113:4421-4426.
32. Kaksonen, M., Y. Sun, and D.G. Drubin. 2003. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell. 115:475-487.
33. Kanzaki, M., R.T. Watson, A.H. Khan, and J.E. Pessin. 2001. Insulin stimulates actin comet tails on intracellular GLUT4-containing compartments in differentiated 3T3L1 adipocytes. J. Biol. Chem. 276:49331-49336.
34. Lechler, T., A. Shevchenko, and R. Li. 2000. Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. J. Cell Biol. 148:363-373.
35. Loisel, T.P., R. Boujemaa, D. Pantaloni, and M.F. Carlier. 1999. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature. 401:613-616.
36. Luo, W., and A. Chang. 2000. An endosome-to-plasma membrane pathway involved in trafficking of a mutant plasma membrane ATPase in yeast. Mol. Biol. Cell. 11:579-592.
37. Madania, A., P. Dumoulin, S. Grava, H. Kitamoto, C. Scharer-Brodbeck, A. Soulard, V. Moreau, and B. Winsor. 1999. The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol. Biol. Cell. 10:3521-3538.
38. Merrifield, C.J., U. Rescher, W. Almers, J. Proust, V. Gerke, A.S. Sechi, and S.E. Moss. 2001. Annexin 2 has an essential role in actin-based macropinocytic rocketing. Curr. Biol. 11:1136-1141.
39. Minogue, S., J.S. Anderson, M.G. Waugh, M. dos Santos, S. Corless, R. Cramer, and J.J. Hsuan. 2001. Cloning of a human type II phosphatidylinositol 4-kinase reveals a novel lipid kinase family. J. Biol. Chem. 276:16635-16640.
40. Moreau, V., F. Frischknecht, I. Reckmann, R. Vincentelli, G. Rabut, D. Stewart, and M. Way. 2000. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat. Cell Biol. 2:441-448.
41. Mulholland, J., J. Konopka, B. Singer-Kruger, M. Zerial, and D. Botstein. 1999. Visualization of receptor-mediated endocytosis in yeast. Mol. Biol. Cell. 10:799-817.
42. Munn, A.L. 2000. The yeast endocytic membrane transport system. Microsc. Res. Tech. 51:547-562.
43. Overton, M.C., and K.J. Blumer. 2000. G-protein-coupled receptors function as oligomers in vivo. Curr. Biol. 10:341-344.
44. Pollard, T.D., and G.G. Borisy. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 112:453-465.
45. Pruyne, D., M. Evangelista, C. Yang, E. Bi, S. Zigmond, A. Bretscher, and C. Boone. 2002. Role of formins in actin assembly: nucleation and barbedend association. Science. 297:612-615.
46. Pruyne, D.W., D.H. Schott, and A. Bretscher. 1998. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143:1931-1945.
47. Qualmann, B., M.M. Kessels, and R.B. Kelly. 2000. Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150:F111-F116.
48. Rodal, A.A., A.L. Manning, B.L. Goode, and D.G. Drubin. 2003. Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr. Biol. 13:1000-1008.
49. Rohatgi, R., H.Y. Ho, and M.W. Kirschner. 2000. Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4, 5-bisphosphate. J. Cell Biol. 150:1299-1310.
50. Rozelle, A.L., L.M. Machesky, M. Yamamoto, M.H. Driessens, R.H. Insall, M.G. Roth, K. Luby-Phelps, G. Marriott, A. Hall, and H.L. Yin. 2000. Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10:311-320.
51. Schafer, D.A. 2002. Coupling actin dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14:76-81.
52. Schmelzle, T., T. Beck, D.E. Martin, and M.N. Hall. 2004. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 24:338-351.
53. Schott, D., J. Ho, D. Pruyne, and A. Bretscher. 1999. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147:791-808.
54. Seastone, D.J., E. Harris, L.A. Temesvari, J.E. Bear, C.L. Saxe, and J. Cardelli. 2001. The WASp-like protein scar regulates macropinocytosis, phagocytosis and endosomal membrane flow in Dictyostelium. J. Cell Sci. 114:2673-2683.
55. Shelton, S.N., B. Barylko, D.D. Binns, B.F. Horazdovsky, J.P. Albanesi, and J.M. Goodman. 2003. Saccharomyces cerevisiae contains a type II phosphoinositide 4-kinase. Biochem. J. 371:533-540.
56. Sokac, A.M., C. Co, J. Taunton, and W. Bement. 2003. Cdc42-dependent actin polymerization during compensatory endocytosis in Xenopus eggs. Nat. Cell Biol. 5:727-732.
57. Soldati, T. 2003. Unconventional myosins, actin dynamics and endocytosis: a menage a trois? Traffic. 4:358-366.
58. Sorkin, A., and M. Von Zastrow. 2002. Signal transduction and endocytosis: close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3:600-614.
59. Southwick, F.S., W. Li, F. Zhang, W.L. Zeile, and D.L. Purich. 2003. Actin-based endosome and phagosome rocketing in macrophages: activation by the secretagogue antagonists lanthanum and zinc. Cell Motil. Cytoskeleton. 54:41-55.
60. Stefan, C.J., and K.J. Blumer. 1999. A syntaxin homolog encoded by VAM3 mediates down-regulation of a yeast G protein-coupled receptor. J. Biol. Chem. 274:1835-1841.
61. Stefan, C.J., M.C. Overton, and K.J. Blumer. 1998. Mechanisms governing the activation and trafficking of yeast G protein-coupled receptors. Mol. Biol. Cell. 9:885-899.
62. Steffen, A., K. Rottner, J. Ehinger, M. Innocenti, G. Scita, J. Wehland, and T.E. Stradal. 2004. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23:749-759.
63. Taunton, J., B.A. Rowning, M.L. Coughlin, M. Wu, R.T. Moon, T.J. Mitchison, and C.A. Larabell. 2000. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148:519-530.
64. Wang, Y.J., J. Wang, H.Q. Sun, M. Martinez, Y.X. Sun, E. Macia, T. Kirchhausen, J.P. Albanesi, M.G. Roth, and H.L. Yin. 2003. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell. 114:299-310.
65. Waugh, M.G., S. Minogue, J.S. Anderson, A. Balinger, D. Blumenkrantz, D.P. Calnan, R. Cramer, and J.J. Hsuan. 2003. Localization of a highly active pool of type II phosphatidylinositol 4-kinase in a p97/valosin-containing- protein-rich fraction of the endoplasmic reticulum. Biochem. J. 373:57-63.
66. Wei, Y.J., H.Q. Sun, M. Yamamoto, P. Wlodarski, K. Kunii, M. Martinez, B. Barylko, J.P. Albanesi, and H.L. Yin. 2002. Type II phosphatidylinositol 4-kinase beta is a cytosolic and peripheral membrane protein that is recruited to the plasma membrane and activated by Rac-GTP. J. Biol. Chem. 277:46586-46593.
67. Wild, A.C., J.W. Yu, M.A. Lemmon, and K.J. Blumer. 2004. The p21-activated protein kinase-related kinase Cla4 is a coincidence detector of signaling by Cdc42 and phosphatidylinositol 4-phosphate. J. Biol. Chem. 279:17101-17110.
68. Winter, D., T. Lechler, and R. Li. 1999. Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr. Biol. 9:501-504.
69. Young, M.E., J.A. Cooper, and P.C. Bridgman. 2004. Yeast actin patches are networks of branched actin filaments. J. Cell Biol. 166:629-635.