A screen for novel phosphoinositide 3-kinase effector proteins

Molecular and Cellular Proteomics

Volumn 10, Issue 4, 2011, Pages

  Dixon, Miles J ^a   Gray, Alexander ^a   Boisvert, François Michel ^a   Agacan, Mark ^a   Morrice, Nicholas A ^a,b   Gourlay, Robert ^a   Leslie, Nicholas R ^a   Downes, C Peter ^a   Batty, Ian H ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; LIPID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE; PLECKSTRIN; PROTEIN KINASE B; TANDEM PLECKSTRIN HOMOLOGY DOMAIN CONTAINING PROTEIN 1; UNCLASSIFIED DRUG; WORTMANNIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HYBRID PROTEIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; PLEKHA1 PROTEIN, HUMAN; POLYPHOSPHOINOSITIDE; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ASTROCYTOMA CELL; CELL CULTURE; CELL MEMBRANE; CELL STIMULATION; CONTROLLED STUDY; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN TARGETING; BIOSYNTHESIS; FEASIBILITY STUDY; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; TUMOR CELL LINE;

CELL LINE, TUMOR; FEASIBILITY STUDIES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RAS GTPASE-ACTIVATING PROTEINS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE;

EID: 79953300492     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.003178     Document Type: Article

References (59)

1. Cantley, L. C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657
2. Di Paolo, G., and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (Pubitemid 44564702)
3. Kok, K., Geering, B., and Vanhaesebroeck, B. (2009) Regulation of phosphoinositide 3-kinase expression in health and disease. Trends Biochem. Sci. 34, 115-127
4. Marone, R., Cmiljanovic, V., Giese, B., and Wymann, M. P. (2008) Targeting phosphoinositide 3-kinase: moving towards therapy. Biochim. Biophys. Acta 1784, 159-185
5. Hawkins, P. T., Anderson, K. E., Davidson, K., and Stephens, L. R. (2006) Signalling through Class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34, 647-662
6. Lemmon, M. A. (2003) Phosphoinositide recognition domains. Traffic 4, 201-213
7. Leslie, N. R., and Downes, C. P. (2002) PTEN: The down side of PI 3-kinase signalling. Cell. Signal. 14, 285-295
8. Backers, K., Blero, D., Paternotte, N., Zhang, J., and Erneux, C. (2003) The termination of PI3K signalling by SHIP1 and SHIP2 inositol 5-phosphatases. Adv. Enzyme Regul. 43, 15-28
9. Lazar, D. F., and Saltiel, A. R. (2006) Lipid phosphatases as drug discovery targets for type 2 diabetes. Nat. Rev. Drug Discov. 5, 333-342
10. Simonsen, A., Wurmser, A. E., Emr, S. D., and Stenmark, H. (2001) The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485-492
11. Batty, I. H., van der Kaay, J., Gray, A., Telfer, J. F., Dixon, M. J., and Downes, C. P. (2007) The control of phosphatidylinositol 3,4-bisphosphate concentrations by activation of the Src homology 2 domain containing inositol polyphosphate 5-phosphatase 2, SHIP2. Biochem. J. 407, 255-266 (Pubitemid 47556990)
12. Sleeman, M. W., Wortley, K. E., Lai, K. M., Gowen, L. C., Kintner, J., Kline, W. O., Garcia, K., Stitt, T. N., Yancopoulos, G. D., Wiegand, S. J., and Glass, D. J. (2005) Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat. Med. 11, 199-205
13. Majerus, P. W., Kisseleva, M. V., and Norris, F. A. (1999) The role of phosphatases in inositol signaling reactions. J. Biol. Chem. 274, 10669-10672
14. Vyas, P., Norris, F. A., Joseph, R., Majerus, P. W., and Orkin, S. H. (2000) Inositol polyphosphate 4-phosphatase type I regulates cell growth downstream of transcription factor GATA-1. Proc. Natl. Acad. Sci. U.S.A. 97, 13696-13701
15. Nystuen, A., Legare, M. E., Shultz, L. D., and Frankel, W. N. (2001) A null mutation in inositol polyphosphate 4-phosphatase type I causes selective neuronal loss in weeble mutant mice. Neuron 32, 203-212
16. Sasaki, J., Kofuji, S., Itoh, R., Momiyama, T., Takayama, K., Murakami, H., Chida, S., Tsuya, Y., Takasuga, S., Eguchi, S., Asanuma, K., Horie, Y., Miura, K., Davies, E. M., Mitchell, C., Yamazaki, M., Hirai, H., Takenawa, T., Suzuki, A., and Sasaki, T. (2010) The PtdIns(3,4)P(2) phosphatase INPP4A is a suppressor of excitotoxic neuronal death. Nature 465, 497-501
17. Gewinner, C., Wang, Z. C., Richardson, A., Teruya-Feldstein, J., Etemadmoghadam, D., Bowtell, D., Barretina, J., Lin, W. M., Rameh, L., Salmena, L., Pandolfi, P. P., and Cantley, L. C. (2009) Evidence that inositol polyphosphate 4-phosphatase type II is a tumor suppressor that inhibits PI3K signaling. Cancer Cell. 16, 115-125
18. Banfić, H., Tang, X., Batty, I. H., Downes, C. P., Chen, C., and Rittenhouse, S. E. (1998) A novel integrin-activated pathway forms PKB/Akt-stimulatory phosphatidylinositol 3,4-bisphosphate via phosphatidylinositol 3-phosphate in platelets. J. Biol. Chem. 273, 13-16
19. Franke, T. F., Kaplan, D. R., Cantley, L. C., and Toker, A. (1997) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4- bisphosphate. Science 275, 665-668 (Pubitemid 27061333)
20. Gray, A., Van Der Kaay, J., and Downes, C. P. (1999) The pleckstrin homology domains of protein kinase B and GRP1 (general receptor for phosphoinositides-1) are sensitive and selective probes for the cellular detection of phosphatidylinositol 3,4-bisphosphate and/or phosphatidyl-inositol 3,4,5-trisphosphate in vivo. Biochem. J. 344, 929-936 (Pubitemid 30032544)
21. Ma, K., Cheung, S. M., Marshall, A. J., and Duronio, V. (2008) PI(3,4,5)P3 and PI(3,4)P2 levels correlate with PKB/akt phosphorylation at Thr308 and Ser473, respectively; PI(3,4)P2 levels determine PKB activity. Cell. Signal. 20, 684-694
22. Thomas, C. C., Deak, M., Alessi, D. R., and van Aalten, D. M. (2002) High-resolution structure of the pleckstrin homology domain of protein kinase b/akt bound to phosphatidylinositol (3,4,5)-trisphosphate. Curr. Biol. 12, 1256-1262
23. Dowler, S., Currie, R. A., Campbell, D. G., Deak, M., Kular, G., Downes, C. P., and Alessi, D. R. (2000) Identification of pleckstrin-homologydomain- containing proteins with novel phosphoinositide-binding specificities. Biochem. J. 351, 19-31
24. Krause, M., Leslie, J. D., Stewart, M., Lafuente, E. M., Valderrama, F., Jagannathan, R., Strasser, G. A., Rubinson, D. A., Liu, H., Way, M., Yaffe, M. B., Boussiotis, V. A., and Gertler, F. B. (2004) Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571-583
25. Dowler, S., Currie, R. A., Downes, C. P., and Alessi, D. R. (1999) DAPP1: a dual adaptor for phosphotyrosine and 3-phosphoinositides. Biochem. J. 342, 7-12
26. Tiwari, S., Choi, H. P., Matsuzawa, T., Pypaert, M., and MacMicking, J. D. (2009) Targeting of the GTPase Irgm1 to the phagosomal membrane via PtdIns(3,4)P(2) and PtdIns(3,4,5)P(3) promotes immunity to mycobacteria. Nat. Immunol. 10, 907-917
27. Smith, K., Humphreys, D., Hume, P. J., and Koronakis, V. (2010) Enteropathogenic Escherichia coli recruits the cellular inositol phosphatase SHIP2 to regulate actin-pedestal formation. Cell Host Microbe 7, 13-24
28. Downes, C. P., Leslie, N. R., Batty, I. H., and van der Kaay, J. (2007) Metabolic switching of PI3K-dependent lipid signals. Biochem. Soc. Trans. 35, 188-192
29. Catimel, B., Schieber, C., Condron, M., Patsiouras, H., Connolly, L., Catimel, J., Nice, E. C., Burgess, A. W., and Holmes, A. B. (2008) The PI(3,5)P2 and PI(4,5)P2 interactomes. J. Proteome Res. 7, 5295-5313
30. Catimel, B., Yin, M. X., Schieber, C., Condron, M., Patsiouras, H., Catimel, J., Robinson, D. E., Wong, L. S., Nice, E. C., Holmes, A. B., and Burgess, A. W. (2009) PI(3,4,5)P3 Interactome. J. Proteome Res. 8, 3712-3726
31. Krugmann, S., Anderson, K. E., Ridley, S. H., Risso, N., McGregor, A., Coadwell, J., Davidson, K., Eguinoa, A., Ellson, C. D., Lipp, P., Manifava, M., Ktistakis, N., Painter, G., Thuring, J. W., Cooper, M. A., Lim, Z. Y., Holmes, A. B., Dove, S. K., Michell, R. H., Grewal, A., Nazarian, A., Erdjument-Bromage, H., Tempst, P., Stephens, L. R., and Hawkins, P. T. (2002) Identification of ARAP3, a novel PI3K effector regulating both Arf and Rho GTPases, by selective capture on phosphoinositide affinity matrices. Mol. Cell 9, 95-108
32. Pasquali, C., Bertschy-Meier, D., Chabert, C., Curchod, M. L., Arod, C., Booth, R., Mechtler, K., Vilbois, F., Xenarios, I., Ferguson, C. G., Prestwich, G. D., Camps, M., and Rommel, C. (2007) A chemical proteomics approach to phosphatidylinositol 3-kinase signaling in macrophages. Mol. Cell. Proteomics 6, 1829-1841
33. Shinohara, M., Terada, Y., Iwamatsu, A., Shinohara, A., Mochizuki, N., Higuchi, M., Gotoh, Y., Ihara, S., Nagata, S., Itoh, H., Fukui, Y., and Jessberger, R. (2002) SWAP-70 is a guanine-nucleotide-exchange factor that mediates signalling of membrane ruffling. Nature 416, 759-763 (Pubitemid 34429154)
34. Kimber, W. A., Trinkle-Mulcahy, L., Cheung, P. C., Deak, M., Marsden, L. J., Kieloch, A., Watt, S., Javier, R. T., Gray, A., Downes, C. P., Lucocq, J. M., and Alessi, D. R. (2002) Evidence that the tandem-pleckstrin-homologydomain- containing protein TAPP1 interacts with Ptd(3,4)P2 and the multi-PDZ-domain- containing protein MUPP1 in vivo. Biochem. J. 361, 525-536
35. Batty, I. H., Fleming, I. N., and Downes, C. P. (2004) Muscarinic-receptor-mediated inhibition of insulin-like growth factor-1 receptor-stimulated phosphoinositide 3-kinase signalling in 1321N1 astrocytoma cells. Biochem. J. 379, 641-651 (Pubitemid 38703648)
36. Batty, I. H., and Downes, C. P. (1994) The inhibition of phosphoinositide synthesis and muscarinic-receptor-mediated phospholipase C activity by Li+ as secondary, selective, consequences of inositol depletion in 1321N1 cells. Biochem. J. 297, 529-537 (Pubitemid 24056107)
37. Boisvert, F. M., Lam, Y. W., Lamont, D., and Lamond, A. I. (2010) A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 9, 457-470
38. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
39. Cox, J., Matic, I., Hilger, M., Nagaraj, N., Selbach, M., Olsen, J. V., and Mann, M. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4, 698-705
40. Hilpelä, P., Oberbanscheidt, P., Hahne, P., Hund, M., Kalhammer, G., Small, J. V., and Bähler, M. (2003) SWAP-70 identifies a transitional subset of actin filaments in motile cells. Mol. Biol. Cell 14, 3242-3253
41. Zhou, Y., Toth, M., Hamman, M. S., Monahan, S. J., Lodge, P. A., Boynton, A. L., and Salgaller, M. L. (2002) Serological cloning of PARIS-1: a new TBC domain-containing, immunogenic tumor antigen from a prostate cancer cell line. Biochem. Biophys. Res. Commun. 290, 830-838
42. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
43. Ong, S. E., Foster, L. J., and Mann, M. (2003) Mass spectrometric-based approaches in quantitative proteomics. Methods 29, 124-130 (Pubitemid 36269199)
44. Brown, M. D., and Sacks, D. B. (2006) IQGAP1 in cellular signaling: bridging the GAP. Trends Cell Biol. 16, 242-249
45. Noritake, J., Watanabe, T., Sato, K., Wang, S., and Kaibuchi, K. (2005) IQGAP1: a key regulator of adhesion and migration. J. Cell Sci. 118, 2085-2092 (Pubitemid 40872832)
46. Lemmon, M. A., and Ferguson, K. M. (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem. J. 350, 1-18
47. Narayan, K., and Lemmon, M. A. (2006) Determining selectivity of phosphoinositide- binding domains. Methods 39, 122-133
48. Lemmon, M. A. (2008) Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111
49. DiNitto, J. P., and Lambright, D. G. (2006) Membrane and juxtamembrane targeting by PH and PTB domains. Biochim. Biophys. Acta 1761, 850-867
50. 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
51. Isakoff, S. J., Cardozo, T., Andreev, J., Li, Z., Ferguson, K. M., Abagyan, R., Lemmon, M. A., Aronheim, A., and Skolnik, E. Y. (1998) Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17, 5374-5387
52. Wakamatsu, I., Ihara, S., and Fukui, Y. (2006) Mutational analysis on the function of the SWAP-70 PH domain. Mol. Cell. Biochem. 293, 137-145
53. Campa, F., Yoon, H. Y., Ha, V. L., Szentpetery, Z., Balla, T., and Randazzo, P. A. (2009) A PH domain in the Arf GTPase-activating protein (GAP) ARAP1 binds phosphatidylinositol 3,4,5-trisphosphate and regulates Arf GAP activity independently of recruitment to the plasma membranes. J. Biol. Chem. 284, 28069-28083
54. Miura, K., Jacques, K. M., Stauffer, S., Kubosaki, A., Zhu, K., Hirsch, D. S., Resau, J., Zheng, Y., and Randazzo, P. A. (2002) ARAP1: a point of convergence for Arf and Rho signaling. Mol. Cell 9, 109-119
55. Brandt, D. T., and Grosse, R. (2007) Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep. 8, 1019-1023 (Pubitemid 350042336)
56. White, C. D., Brown, M. D., and Sacks, D. B. (2009) IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS Lett. 583, 1817-1824
57. Tirnauer, J. S. (2004) A new cytoskeletal connection for APC: linked to actin through IQGAP. Dev. Cell 7, 778-780
58. Cain, R. J., and Ridley, A. J. (2009) Phosphoinositide 3-kinases in cell migration. Biol. Cell 101, 13-29
59. Stephens, L., Milne, L., and Hawkins, P. (2008) Moving towards a better understanding of chemotaxis. Curr. Biol. 18, R485-494