Synergistic activation of p21-activated kinase 1 by phosphatidylinositol 4,5-bisphosphate and Rho GTPases

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 8887-8897

  Malecka, Kimberly A ^a   Szentpetery, Zsofia ^b   Peterson, Jeffrey R ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; ENZYMES; LIPOSOMES; NICKEL COMPOUNDS; PHOSPHOLIPIDS;

5-BISPHOSPHATE; BINDING MOTIF; GTPASES; IN-VIVO; MEMBRANE BINDING; P-21 ACTIVATED KINASE; PHOSPHATIDYLINOSITOL 4; PHOSPHOINOSITIDE BINDING; PHOSPHOINOSITIDES; RHO GTPASES;

CHEMICAL ACTIVATION;

ACTIVATED CDC42 ASSOCIATED KINASE; P21 ACTIVATED KINASE 1; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PROTEIN CDC42; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME REGULATION; GOLGI COMPLEX; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84876002236     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.428904     Document Type: Article

References (62)

1. Carlton, J. G., and Cullen, P. J. (2005) Coincidence detection in phosphoinositide signaling. Trends Cell Biol. 15, 540-547
2. Di Paolo, G., and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657
3. Groves, J. T., and Kuriyan, J. (2010) Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17, 659-665
4. Balla, T., Szentpetery, Z., and Kim, Y. J. (2009) Phosphoinositide signaling. New tools and insights. Physiology 24, 231-244
5. Heo, W. D, Inoue, T., Park, W. S., Kim, M. L., Park, B. O., Wandless, T. J., and Meyer, T. (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461
6. van den Bout, I., and Divecha, N. (2009) PIP5K-driven PtdIns(4,5)P2 synthesis. Regulation and cellular functions. J. Cell Sci. 122, 3837-3850
7. McLaughlin, S., and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611
8. Strochlic, T. I., Viaud, J., Rennefahrt, U. E., Anastassiadis, T., and Peterson, J. R. (2010) Phosphoinositides are essential coactivators for p21-activated kinase 1. Mol. Cell 40, 493-500
9. Papayannopoulos, V., Co, C., Prehoda, K. E., Snapper, S., Taunton, J., and Lim, W. A. (2005) A polybasic motif allows N-WASP to act as a sensor of PIP2 density. Mol. Cell. 17, 181-191
10. Wang, J., Arbuzova, A., Hangyás-Mihályné, G., and McLaughlin, S. (2001) The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 276, 5012-5019
11. McLaughlin, S., Wang, J., Gambhir, A., and Murray, D. (2002) PIP(2) and proteins. Interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 31, 151-175
12. Prehoda, K. E., Scott, J. A., Mullins, R. D., and Lim, W. A. (2000) Integration of multiple signals through cooperative regulation of the N-WASPArp2/ 3 complex. Science 290, 801-806
13. Wild, A. C., Yu, J. W., Lemmon, M. A., and Blumer, K. J. (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
14. Koronakis, V., Hume, P. J., Humphreys, D., Liu, T., Hørning, O., Jensen, O. N., and McGhie, E. J. (2011) WAVE rgulatory complex activation by cooperating GTPases Arf and Rac1. Proc. Natl. Acad. Sci. U. S. A. 108, 14449-14454
15. Godi, A., Di Campli, A., Konstantakopoulos, A., Di Tullio, G., Alessi, D. R., Kular, G. S., Daniele, T., Marra, P., Lucocq, J. M., and De Matteis, M. A. (2004) FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 6, 393-404
16. Hemsath, L., Dvorsky, R., Fiegen, D., Carlier, M. F., and Ahmadian, M. R. (2005) An electrostatic steering mechanism of Cdc42 recognition by Wiskott-Aldrich syndrome protein. Mol. Cell 20, 313-324
17. Cory, G. O., Cramer, R., Blanchoin, L., and Ridley, A. J. (2003) Phosphorylation of the WASP-VCA domain increases its affinity for the Arp2/3 complex and enhances actin polymerization by WASP. Mol. Cell 11, 1229-1239
18. Rohatgi, R., Ho, H. Y., and Kirschner, M. W. (2000) Mechanism of NWASP activation by CDC42 and phosphatidylinositol 4,5-bisphosphate. J. Cell Biol. 150, 1299-1310
19. Prehoda, K. E., and Lim, W. A. (2002) How signaling proteins integrate multiple inputs. A comparison of N-WASP and Cdk2. Curr. Opin. Cell Biol. 14, 149-154
20. Arias-Romero, L. E., and Chernoff, J. (2008) A tale of two Paks. Biol. Cell 100, 97-108
21. Sells, M., Knaus, U. G., Bagrodia, S., Ambrose, D., Bokoch, G. M., and Chernoff, J. (1997) Human p21-activated kinase (Pak1) regulates actin organization in mammlian cells. Curr. Biol. 7, 202-210
22. Manser, E., Huang, H. Y., Loo, T. H., Chen, X. Q., Dong, J. M., Leung, T., and Lim, L. (1997) Expression of constitutively active α -PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143
23. Bokoch, G. M. (2003) Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781
24. Manser, E., Leung, T., Salihuddin, H., Zhao, Z. S., and Lim, L. (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46
25. Jung, I. D., Lee, J., Lee, K. B., Park, C. G., Kim, Y. K., Seo, D. W., Park, D., Lee, H. W., Han, J. W., and Lee, H. Y. (2004) Activation of p21-activated kinase 1 is required for lysophosphatidic acid-induced focal adhesion kinase phosphorylation and cell motility in human melanoma A2058 cells. Eur. J. Biochem. 271, 1557-1565
26. Pavey, S., Zuidervaart, W., van Nieuwpoort, F., Packer, L., Jager, M., Gruis, N., and Hayward, N. (2006) Increased p21-activated kinase-1 expression is associated with invasive potential in uveal melanoma. Melanoma Res. 16, 285-296
27. Yi, C., Maksimoska, J., Marmorstein, R., and Kissil, J. L. (2010) Development of small-molecule inhibitors of the group I p21-activated kinases, emerging therapeutic targets in cancer. Biochem. Pharmacol. 80, 683-689
28. Arias-Romero, L. E., and Chernoff, J. (2010) p21-activated kinases in ErbB2-positive breast cancer. Small GTPases 1, 124-128
29. Arias-Romero, L. E., Villamar-Cruz, O., Pacheco, A., Kosoff, R., Huang, M., Muthuswamy, S. K., and Chernoff, J. (2010) A Rac-Pak signaling pathway is essential for ErbB2-mediated transformation of human breast epithelial cancer cells. Oncogene 29, 5839-5849
30. Knaus, U. G., Wang, Y., Reilly, A. M., Warnock, D., and Jackson, J. H. (1998) Structural requirements for PAK activation by Rac GTPases. J. Biol. Chem. 273, 21512-21518
31. Pirruccello, M., Sondermann, H., Pelton, J. G., Pellicena, P., Hoelz, A., Chernoff, J., Wemmer, D. E., and Kuriyan, J. (2006) A dimeric kinase assembly underlying autophosphorylation in the p21 activated kinases. J. Mol. Biol. 361, 312-326
32. Parrini, M. C., Lei, M., Harrison, S. C., and Mayer, B. J. (2002) Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Mol. Cell 9, 73-83
33. Lei, M., Lu, W., Meng, W., Parrini, M. C., Eck, M. J., Mayer, B. J., and Harrison, S. C. (2000) Structure of PAK1 in an autoinhibited conformation reveals a multistage activation Switch. Cell 102, 387-397
34. Yokoyama, N., and Miller, W. T. (2003) Biochemical properties of the Cdc42-associated tyrosine kinase ACK1. Substrate specficity, autophosphorylation, and interaction with Hck. J. Biol. Chem. 278, 47713-47723
35. Ferguson, K. M., Kavran, J. M., Sankaran, V. G., Fournier, E., Isakoff, S. J., Skolnik, E. Y., and Lemmon, M. A. (2000) Structural basis for discrimination of 3-phosphoinositides by pleckstrin homology domains. Mol. Cell 6, 373-384
36. Braun, V., Wong, A., Landekic, M., Hong, W. J., Grinstein, S., and Brumell, J. H. (2010) Sorting nexin 3 (SNX3) is a component of a tublar endosomal network induced by Salmonella and involved in maturation of the Salmonella-containing vacuole. Cell. Microbiol. 12, 1352-1367
37. Ziman, M., O'Brien, J. M., Ouellette, L. A., Church, W. R., and Johnson, D. I. (1991) Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Mol. Cell. Biol. 11, 3537-3544
38. Takahashi, S., and Pryciak, P. (2007) Identification of novel membranebinding domains in multiple yeast Cdc42 effectors. Mol. Biol. Cell 18, 4945-4956
39. Halstead, J. R., Savaskan, N. E., van den Bout, I., Van Horck, F., Hajdo- Milasinovic, A., Snell, M., Keune, W. J., Ten Klooster, J. P., Hordijk, P. L., and Divecha, N. (2010) Rac controls PIP5K localisation and PtdIns(4,5)P synthesis, which modulates vinculin localisation and neurite dynamics. J. Cell Sci. 123, 3535-3546
40. Varnai, P., Thyagarajan, B., Rohacs, T., and Balla, T. (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J. Cell Biol. 175, 377-382
41. Sells, M. A., Barratt, J. T., Caviston, J., Ottilie, S., Leberer, E., and Chernoff, J. (1998) Characterization of Pak2p, a pleckstrin homology domain-containing, p21-activated protein kinase from fission yeast. J. Biol. Chem. 273, 18490-18498
42. Banting, G., and Ponnambalam, S. (1997) TGN38 and its orthologues. Roles in post-TGN vesicle formation and maintenance of TGN morphology. Biochim. Biophys. Acta 1355, 209-217
43. Adamson, P., Marshall, C. J., Hall, A., and Tilbrook, P. A. (1992) Posttranslational modifications of p21rho proteins. J. Biol. Chem. 267, 20033-20038
44. Armstrong, S. A., Hannah, V. C., Goldstein, J. L., and Brown, M. S. (1995) CAAX geranylgeranyl transferase tranfers farnesyl as efficiently as geranylgeranyl to RhoB. J. Biol. Chem. 270, 7864-7868
45. Cox, A. D., and Der, C. J. (1992) Protein prenylation. More than just glue? Curr. Opin. Cell Biol. 4, 1008-1016
46. Zhang, H., Shen, W., Rempel, D., Monsey, J., Vidavsky, I., Gross, M., and Bose, R. (2011) Carboxyl-group footprinting maps the dimerization interface and phosphorylation-induced conformational changes of a membrane-associated tyrosine kinase. Mol. Cell. Proteomics 10, doi: 10.1074/mcpM110.005678
47. Merrill, S. A., and Hanson, P. I. (2010) Activation of human VPS4A by ESCRT-III proteins reveals ability of substrates to relieve enzyme inhibition. J. Biol. Chem. 285, 35428-35438
48. Monsey, J., Shen, W., Schlesinger, P., and Bose, R. (2010) Her4 and Her2/neu tyrosine kinase domains dimerize and activate in a reconstituted in vitro system. J. Biol. Chem. 285, 7035-7044
49. Montefusco, D. J., Asinas, A. E., and Weis, R. M. (2007) Liposome-mediated assembly of receptor signaling complexes. Methods Enzymol. 423, 267-298
50. Zhang, X., Gureasko, J., Shen, K., Cole, P. A., and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149
51. Shrout, A. L., Montefusco, D. J., and Weis, R. M. (2003) Template-directed assembly of receptor signaling complexes. Biochemistry 42, 13379-13385
52. Lemmon, M. A. (2003) Phosphoinositide recognition domains. Traffic 4, 201-213
53. Nalbant, P., Hodgson, L., Kraynov, V., Toutchkine, A., and Hahn, K. M. (2004) Activation of endogenous Cdc42 visualized in living cells. Science 305, 1615-1619
54. Kodani, A., Kristensen, I., Huang, L., and Sütterlin, C. (2009) GM130-dependent control of Cdc42 activity at the Golgi regulates centrosome organization. Mol. Biol. Cell 20, 1192-1200
55. Dubois, T., Paléotti, O., Mironov, A. A., Fraisier, V., Stradal, T. E., De Matteis, M. A., Franco, M., and Chavrier, P. (2005) Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics. Nat. Cell Biol. 7, 353-364
56. Müsch, A., Cohen, D., Kreitzer, G., and Rodriguez-Boulan, E. (2001) cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J. 20, 2171-2179
57. Osmani, N., Peglion, F., Chavrier, P., and Etienne-Manneville, S. (2010) Cdc42 localization and cell polarity depend on membrane traffic. J. Cell Biol. 191, 1261-1269
58. Matas, O. B., Martínez-Menárguez, J. A., and Egea, G. (2004) Association of Cdc42/N-WASP/Arp2/3 signaling pathway with Golgi membranes. Traffic 5, 838-846
59. Estrada, L., Caron, E., and Gorski, J. (2001) Fgd1, the Cdc42 guanine nucleotide exchange factor responsible for faciogenital dysplasia, is localized to the subcortical actin cytoskeleton and Golgi membrane. Hum. Mol. Genet. 10, 485-495
60. Sells, M. A., Pfaff, A., and Chernoff, J. (2000) Temporal and spatial distribution of activated Pak1 in fibroblasts. J. Cell Biol. 151, 1449-1458
61. Dharmawardhane, S., Sanders, L. C., Martin, S. S., Daniels, R. H., and Bokoch, G. M. (1997) Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138, 1265-1278
62. Szentpetery, Z., Várnai, P., and Balla, T. (2010) Acute manipulations of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 8225-8230