IQGAP proteins reveal an atypical phosphoinositide (aPI) binding domain with a pseudo C2 domain fold

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22483-22496

  Dixon, Miles J ^a   Gray, Alexander ^a   Schenning, Martijn ^a   Agacan, Mark ^a   Tempel, Wolfram ^b   Tong, Yufeng ^b   Nedyalkova, Lyudmila ^b   Park, Hee Won ^b,c   Leslie, Nicholas R ^a   Van Aalten, Daan M F ^a   Downes, C Peter ^a   Batty, Ian H ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACID REGION; BINDING AFFINITIES; BINDING DOMAIN; CELL PERIPHERY; CELLULAR SIGNALING; CLASS I; CYTOSKELETAL DYNAMICS; CYTOSOLS; ENHANCED GREEN FLUORESCENT PROTEIN; GTPASE-ACTIVATING PROTEIN; PHOSPHATIDYLINOSITOL; PHOSPHOINOSITIDE BINDING; PHOSPHOINOSITIDES; PLECKSTRIN HOMOLOGY DOMAINS; SELECTIVE RECOGNITION; TERMINAL DOMAIN; TOPOLOGICAL SIMILARITY;

AMINO ACIDS; BINDING ENERGY; CELL CULTURE; ENZYMES; PHOSPHOLIPIDS;

PROTEINS;

BINDING PROTEIN; CYTOHESIN 3; ENHANCED GREEN FLUORESCENT PROTEIN; ENZYME ACTIVATOR; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 2; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 3; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PLECKSTRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN 3T3; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOSKELETON; CYTOSOL; ENZYME ACTIVATION; INTRACELLULAR SIGNALING; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; STRUCTURAL HOMOLOGY;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY; GTPASE-ACTIVATING PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RAS GTPASE-ACTIVATING PROTEINS; SIGNAL TRANSDUCTION;

EID: 84863307218     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.352773     Document Type: Article

References (51)

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. Stephens, L. R., Jackson, T. R., and Hawkins, P. T. (1993) Agonist-stimulated synthesis of phosphatidylinositol(3,4,5)-trisphosphate. A new intracellular signalling system? Biochim. Biophys. Acta 1179, 27-75
4. Vanhaesebroeck, B., Leevers, S. J., Ahmadi, K., Timms, J., Katso, R., Driscoll, P. C., Woscholski, R., Parker, P. J., and Waterfield, M. D. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70, 535-602 (Pubitemid 32662219)
5. Hawkins, P. T., Anderson, K. E., Davidson, K., and Stephens, L. R. (2006) Signaling through class I PI3Ks in mammalian cells. Biochem. Soc. Trans. 34, 647-662 (Pubitemid 44796393)
6. Leslie, N. R., and Downes, C. P. (2002) PTEN. The down side of PI 3-kinase signaling. Cell Signal. 14, 285-295 (Pubitemid 34164684)
7. Majerus, P. W., Kisseleva, M. V., and Norris, F. A. (1999) The role ofphosphatases in inositol signaling reactions. J. Biol. Chem. 274, 10669-10672
8. 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 (Pubitemid 46596465)
9. Stenmark, H., and Aasland, R. (1999) FYVE-finger proteins. Effectors of an inositol lipid. J. Cell Sci. 112, 4175-4183 (Pubitemid 30122010)
10. Marone, R., Cmiljanovic, V., Giese, B., and Wymann, M. P. (2008) Targeting phosphoinositide 3-kinase. Moving towards therapy. Biochim. Biophys. Acta 1784, 159-185
11. Kok, K., Geering, B., and Vanhaesebroeck, B. (2009) Regulation of phosphoinositide 3-kinase expression in health and disease. Trends Biochem. Sci. 34, 115-127
12. Lemmon, M. A. (2003) Phosphoinositide recognition domains. Traffic 4, 201-213
13. Narayan, K., and Lemmon, M. A. (2006) Determining selectivity of phosphoinositide-binding domains. Methods 39, 122-133 (Pubitemid 44107710)
14. Lemmon, M. A. (2008) Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99-111
15. Dixon, M. J., Gray, A., Boisvert, F. M., Agacan, M., Morrice, N. A., Gourlay, R., Leslie, N. R., Downes, C. P., and Batty, I. H. (2011) A screen for novel phospho-inositide 3-kinase effector proteins. Mol. Cell Proteomics 10, M110.003178
16. Brown, M. D., and Sacks, D. B. (2006) IQGAP1 in cellular signaling. Bridging the GAP. Trends Cell Biol. 16, 242-249 (Pubitemid 43744436)
17. 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
18. 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)
19. Brandt, D. T., and Grosse, R. (2007) Get to grips. Steering local actin dynamics with IQGAPs. EMBO Rep. 8, 1019-1023 (Pubitemid 350042336)
20. Tirnauer, J. S. (2004) A new cytoskeletal connection for APC. Linked to actin through IQGAP. Dev. Cell 7, 778-780
21. Cain, R. J., and Ridley, A. J. (2009) Phosphoinositide 3-kinases in cell migration. Biol. Cell 101, 13-29
22. Stephens, L., Milne, L., and Hawkins, P. (2008) Moving towards a better understanding of chemotaxis. Curr. Biol. 18, R485-494 (Pubitemid 351734644)
23. + as secondary, selective, consequences of inositol depletion in 1321N1 cells. Biochem. J. 297, 529-537
24. Gray, A., Olsson, H., Batty, I. H., Priganica, L., and Peter Downes, C. (2003) Nonradioactive methods for the assay of phosphoinositide 3-kinases and phosphoinositide phosphatases and selective detection of signaling lipids in cell and tissue extracts. Anal. Biochem. 313, 234-245 (Pubitemid 36259947)
25. Dong, A., Xu, X., Edwards, A. M., Midwest Center for Structural Genomics, Structural Genomics Consortium,Chang, C., Chruszcz, M., Cuff, M., Cymborowski, M., Di Leo, R., Egorova, O., Evdokimova, E., Filippova, E., Gu, J., Guthrie, J., Ignatchenko, A., Joachimiak, A., Klostermann, N., Kim, Y., Korniyenko, Y., Minor, W., Que, Q., Savchenko, A., Skarina, T., Tan, K., Yakunin, A., Yee, A., Yim, V., Zhang, R., Zheng, H., Akutsu, M., Arrowsmith, C., Avvakumov, G. V., Bochkarev, A., Dahlgren, L. G., Dhe-Paganon, S., Dimov, S., Dombrovski, L., Finerty, P., Jr., Flodin, S., Flores, A., Gräslund, S., Hammerström, M., Herman, M. D., Hong, B. S., Hui, R., Johansson, I., Liu, Y., Nilsson, M., Nedyalkova, L., Nordlund, P., Nyman, T., Min, J., Ouyang, H., Park, H. W., Qi, C., Rabeh, W., Shen, L., Shen, Y., Sukumard, D., Tempel, W., Tong, Y., Tresagues, L., Vedadi, M., Walker, J. R., Weigelt, J., Welin, M., Wu, H., Xiao, T., Zeng, H., and Zhu, H. (2007) In situ proteolysis for protein crystallization and structure determination. Nat. Methods 4, 1019-1021 (Pubitemid 350201773)
26. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
27. Pape, T., and Schneider, T. R. (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844
28. Perrakis, A., Morris, R., and Lamzin, V. S. (1999) Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6, 458-463 (Pubitemid 29218016)
29. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
30. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
31. White, C. D., Erdemir, H. H., and Sacks, D. B. (2012) IQGAP1 and its binding proteins control diverse biological functions. Cell Signal. 24, 826-834
32. Brandt, D. T., Marion, S., Griffiths, G., Watanabe, T., Kaibuchi, K., and Grosse, R. (2007) Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J. Cell Biol. 178, 193-200 (Pubitemid 47076456)
33. Klarlund, J. K., Guilherme, A., Holik, J. J., Virbasius, J. V., Chawla, A., and Czech, M. P. (1997) Signaling by phosphoinositide 3,4,5-trisphosphate through proteins containing pleckstrin and Sec7 homology domains. Science 275, 1927-1930 (Pubitemid 27148813)
34. Garcia, P., Gupta, R., Shah, S., Morris, A. J., Rudge, S. A., Scarlata, S., Petrova, V., McLaughlin, S., and Rebecchi, M. J. (1995) The pleckstrin homology domain of phospholipase C-delta 1 binds with high affinity to phosphatidylinositol 4,5-bisphosphate in bilayer membranes. Biochemistry 34, 16228-16234
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. Irvine, R. F., and Schell, M. J. (2001) Back in the water. The return of the inositol phosphates. Nat. Rev. Mol. Cell Biol. 2, 327-338 (Pubitemid 33674045)
37. Van der Kaay, J., Beck, M., Gray, A., and Downes, C. P. (1999) Distinct phosphatidylinositol 3-kinase lipid products accumulate upon oxidative and osmotic stress and lead to different cellular responses. J. Biol. Chem. 274, 35963-35968 (Pubitemid 129512906)
38. 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 phosphatidylinositol 3,4,5-trisphosphate in vivo. Biochem. J. 344, 929-936 (Pubitemid 30032544)
39. Li, Z., Kim, S. H., Higgins, J. M., Brenner, M. B., and Sacks, D. B. (1999) IQGAP1 and calmodulin modulate E-cadherin function. J. Biol. Chem. 274, 37885-37892 (Pubitemid 30026855)
40. 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)
41. DiNitto, J. P., Cronin, T. C., and Lambright, D. G. (2003) Membrane recognition and targeting by lipid-binding domains. Sci. STKE 2003, re16
42. Kutateladze, T. G. (2010) Translation of the phosphoinositide code by PI effectors. Nat. Chem. Biol. 6, 507-513
43. Moravcevic, K., Oxley, C. L., and Lemmon, M. A. (2012) Conditional peripheral membrane proteins. Facing up to limited specificity. Structure 20, 15-27
44. Holm, L., and Sander, C. (1995) Dali, a network tool for protein structure comparison. Trends Biochem. Sci. 20, 478-480
45. Krissinel, E., and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268 (Pubitemid 41742778)
46. 2. Proc. Natl. Acad. Sci. U.S.A. 106, 6603-6607
47. 2+/phospholipid-binding fold. Cell 80, 929-938
48. 2+ bridges the C2 membrane-binding domain ofprotein kinase Cα directly to phosphatidylserine.EMBOJ. 18, 6329-6338
49. Corbalán-García, S., García-García, J., Rodríguez-Alfaro, J. A., and Gómez-Fernández, J. C. (2003) A new phosphatidylinositol 4,5-bisphosphate-binding site located in the C2 domain of protein kinase Cα. J. Biol. Chem. 278, 4972-4980
50. Batty, I. R., Nahorski, S. R., and Irvine, R. F. (1985) Rapid formation of inositol 1,3,4,5-tetrakisphosphate following muscarinic receptor stimulation of rat cerebral cortical slices. Biochem. J. 232, 211-215 (Pubitemid 16199003)
51. 2-sensing domains. Biochem. Soc. Trans. 35, 1046-1048