Selective cellular effects of overexpressed pleckstrin-homology domains that recognize Ptdlns(3,4,5)P3 suggest their interaction with protein binding partners

Journal of Cell Science

Volumn 118, Issue 20, 2005, Pages 4879-4888

  Várni, Péter ^a,b   Bondeva, Tzvetanka ^a   Tamás, Péter ^b   Tóth, Balázs ^a   Buday, László ^b   Hunyady, László ^b   Balla, Tamas ^a  

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

^b SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Akt kinase; Cell adhesion; GFP; PH domain; PI 3 kinase; PIP3; PtdIns(3,4,5)P3

Indexed keywords

BRUTON TYROSINE KINASE; EPIDERMAL GROWTH FACTOR; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PLECKSTRIN; PROTEIN KINASE B; WORTMANNIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CELL CULTURE; CELL MEMBRANE; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENZYME INHIBITION; GENE MUTATION; GENE OVEREXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANDROSTADIENES; ANIMALS; BLOOD PROTEINS; CELL ADHESION; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; EPIDERMAL GROWTH FACTOR; FIBROBLASTS; GENE EXPRESSION; HUMANS; MICE; MUTAGENESIS; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSFECTION;

ANIMALIA;

EID: 27844469655     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02606     Document Type: Article

References (48)

1. Artalejo, C. R., Lemmon, M. A., Schlessinger, J. and Palfrey, H. C. (1997). Specific role for the PH domain of dynamin-1 in the regulation of rapid exocytosis in adrenal chromaffin cells. EMBO J. 16, 1565-1574.
2. Bae, Y. S., Cantley, L. G., Chen, C.-S., Kim, S.-R., Kwon, K.-S. and Rhee, S. G. (1998). Activation of phosphpolipase C-γ by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 4465-4469.
3. Balla, T. and Varnai, P. (2002). Visualizing cellular phosphoinositide pools with GFP-fused protein-modules. Sci STKE 125, 1-16.
4. Balla, T., Bondeva, T. and Varnai, P. (2000). How accurately can we image inositol lipids in live cells? Trends Pharmacol. Sci. 21, 238-241.
5. Bondeva, T., Pirola, L., Bulgarelli-Leva, G., Rubio, L, Wetzker, R. and Wymann, M. P. (1998). Bifurcation of lipid and protein kinase signals of P13Kγ to the protein kinases PKB and MAPK. Science 282, 293-296.
6. Carman, C. V., Barak, L. S., Chen, C., Liu-Chen, L.-Y., Onorato, J. J., Kennedy, S. P., Caron, M. G. and Benovic, J. L. (2000). Mutational analysis of Gβγ and phospholipid interaction with G protein-coupled receptor kinase 2. J. Biol. Chem. 275, 10443-10452.
7. Clark, A. J., Beguinot, L., Ishii, S., Ma, D. P., Roe, B. A., Merlino, G. T. and Pastan, I. (1986). Synthesis of epidermal growth factor (EGF) receptor in vitro using SP6 RNA polymerase-transcribed template mRNA. Biochim. Biophys. Acta 867, 244-251.
8. Cozier, G. E., Carlton, J., Bouyoucef, D. and Cullen, P. J. (2004). Membrane targeting by pleckstrin homology domains. Curr. Top. Microbiol. Immunol. 282, 49-88.
9. Falasca, M., Logan, S. K., Lehto, V. P., Baccante, G., Lemmon, M. A. and Schlessinger, J. (1998). Activation of phospholipase Cγ by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J. 17, 414-422.
10. Harlan, J. E., Hajduk, P. J., Yoon, H. S. and Fesik, S. W. (1994). Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371, 168-170.
11. Hawadle, M. A., Folarin, N., Martin, R. and Jackson, T. R. (2002). Cytohesins and centaurins control subcellular trafficking of macromolecular signaling complexes: regulation by phosphoinositides and ADP-ribosylation factors. Biol. Res. 35, 247-265.
12. Heraud, J. M., Racaud-Sultan, C., Gironcel, D., Albiges-Rizo, C., Giacomini, T., Roques, S., Martel, V., Breton-Douitlon, M., Perret, B. and Chap, H. (1998). Lipid products of phosphomositide 3-kinase and phosphatidylinositol 4',5'-bisphosphate are both required for ADP-dependent platelet spreading. J. Biol. Chem. 273, 17817-17823.
13. Hunyady, L., Baukal, A. J., Balla, T. and Catt, K. J. (1994). Independence of type 1 angiotensin II receptor endocytosis from G protein coupling and signal transduction. J. Biol. Chem. 269, 24798-24804.
14. Irvine, R. (2004). Inositol Lipids: To PHix or Not to PHix? Curr. Biol. 14, R308-R310.
15. Kinashi, T., Escobedo, J. A., Williams, L. T., Takatsu, K. and Springer, T. A. (1995). Receptor tyrosine kinase stimulates cell-matrix adhesion by phosphatidylinositol 3 kinase and phospholipase C-gamma 1 pathways. Blood 86, 2086-2090.
16. 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 plekstrin and Sec7 homology domains. Science 275, 1927-1930.
17. Klarlund, J. K., Tsiaras, W., Holik, J. J., Chawla, A. and Czech, M. P. (2000). Distinct polyphosphoinositide binding selectivities for pleckstrin homology domains of GRP1-like proteins based on diglycine versus triglycine motifs. J Biol. Chem. 275, 32816-32821.
18. Lemmon, M. A. (2003). Phosphoinositide recognition domains. Traffic 4,201-213.
19. Lemmon, M. A. and Ferguson, K. M. (2000). Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem. J. 350, 1-18.
20. Lemmon, M. A., Falasca, M., Ferguson, K. M. and Schlessinger, J. (1997). Regulatory recruitment of signalling molecules to the cell membrane by plekstrin-homology domains. Trends Cell Biol. 7, 237-242.
21. Lietzke, S. E., Bose, S., Cronin, T., Klarlund, J., Chawla, A., Czech, M. P. and Lambright, D. G. (2000). Structural basis of 3-phosphoinositide recognition by pleckstrin homology domains. Mol. Cell 6, 385-394.
22. Lodowski, D. T., Pitcher, J. A., Capel, W. D., Lefkowitz, R. J. and Tesmer, J. J. (2003). Keeping G proteins at bay: a complex between G protein-coupled receptor kinase 2 and Gbetagamma. Science 300, 1256-1262.
23. Lomasney, J. W., Cheng, H. F., Wang, L. P., Kuan, Y., Liu, S., Fesik, S. W. and King, K. (1996). Phosphatidylinositol 4,5-bisphosphate binding to the pleckstrin homology domain of phospholipase C-delta1 enhances enzyme activity. J. Biol. Chem. 271, 25316-25326.
24. Lu, M., Kinchen, J. M., Rossman, K. L., Grimsley, C., deBakker, C., Brugnera, E., Tosello-Trampont, A. C., Haney, L. B., Klingele, D., Sondek, J. et al. (2004). PH domain of ELMO functions in trans to regulate Rac activation via Dock180. Nat. Struct. Mol. Biol. 11, 756-762.
25. Milburn, C. C., Deak, M., Kelly, S. M., Price, N. C., Alessi, D. R. and Van Aalten, D. M. (2003). Binding of phosphatidylinositol 3,4,5-trisphosphate to the pleckstrin homology domain of protein kinase B induces a conformational change. Biochem. J. 375, 531-538.
26. Oatey, P. B., Venkateswarlu, K., Williams, A. G., Fletcher, L. M., Foulstone, E., Cullen, P. J. and Tavare, J. M. (1999). Confocal imaging of the subcellular distribution of phosphatidylinositol 3,4,5-trisphosphate in insulin-and PDGF-stimulated 3T3-L1 adipocytes. Biochem. J 344, 511-518.
27. Odorizzi, G., Babst, M. and Emr, S. D. (2000). Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci. 25, 229-235.
28. Powell, D. J., Hajduch, E., Kular, G. and Hundal, H. S. (2003). Ceramide disables 3-phosphoinositide binding to the pleckstrin homology domain of protein kinase B (PKB)/Akt by a PKCζ-dependent mechanism. Mol. Cell. Biol. 23, 7794-7808.
29. Rossman, K. L., Worthylake, D. K., Snyder, J. T., Siderowski, D. P., Campbell, S. L. and Sondek, J. (2002). A crystallographic view of interactions between Dbs and Cdc42: PH domain-assisted guanine nucleotide exchange. EMBO J. 21, 1315-1326.
30. Saito, K., Scharenberg, A. M. and Kinet, J. P. (2001). Interaction between the Btk PH domain and phosphatidylinositol-3,4,5-trisphosphate directly regulates Btk. J. Biol. Chem. 276, 16201-16206.
31. 2 synthesis: importance for calcium signaling and P13K activity. Immunity 19, 669-678.
32. Servant, G., Weiner, O. D., Herzmark, P., Balla, T., Sedat, J. W. and Bourne, H. R. (2000). Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287, 1037-1040.
33. Skowronek, K. R., Guo, E, Zheng, Y. and Nassar, N. (2004). The C-terminal basic tail of RhoG assists the guanine nucleotide exchange factor Trio in binding to phospholipids. J. Biol. Chem. 279, 37895-37907.
34. Snyder, J. T., Rossman, K. L., Baumesister, M. A., Pruitt, W. M., Siderowski, D. P., Der, C. J., Lemmon, M. A. and Sondek, J. (2001). Quantitative analysis of the effect of phosphoinositide interactions on the function of Db1 family proteins. J. Biol. Chem. 276, 45865-45868.
35. Soisson, S. M., Nimnual, A. S., Uly, M., Bar-Sagi, D. and Kuriyan, J. (1998). Crystal structure of the Db1 and pleckstrin homology domains from the human son of sevenless protein. Cell 95, 259-268.
36. Stratford, S., DeWald, D. B. and Summers, S. A. (2001). Ceramide dissociates 3′-phosphoinositide production from pleckstrin homology domain translocation. Biochem. J. 354, 359-368.
37. Szaszak, M., Gaborik, Z., Turu, G., McPherson, P. S., Clark, A. J., Catt, K. J. and Hunyady, L. (2002). Role of the proline-rich domain of dynamin-2 and its interactions with Src homology 3 domains during endocytosis of the AT1 angiotensin receptor. J. Biol. Chem. 277, 21650-21656.
38. Tanaka, M., Konishi, H., Touhara, K., Sakane, F., Hirata, M., Ono, Y. and Kikkawa, U. (1999). Identification of myosin II as a binding protein to the PH domain of protein kinase B. Biochem. Biophys. Res. Commun. 255, 169-174.
39. Tsukada, S., Simon, M., Witte, O. and Katz, A. (1994). Binding of the βγ subunits of heterotrimeric G-proteins to the PH domain of Bruton's tyrosine kinase. Proc. Natl. Acad. Sci. USA 91, 11256-11260.
40. Varnai, P., Rother, K. I. and Balla, T. (1999). Phosphatidylinositol 3-kinase-dependent membrane association of the Bruton's tyrosine kinase pleckstrin homology domain visualized in single living cells. J. Biol. Chem. 274, 10983-10989.
41. Varnai, P., Lin, X., Lee, S. B., Tuymetova, G., Bondeva, T., Spat, A., Rhee, S. G., Hajnoczky, G. and Balla, T. (2002). Inositol lipid binding and membrane localization of isolated pleckstrin homology (PH) domains. Studies on the PH domains of phospholipase C delta 1 and p130. J. Biol. Chem. 277, 27412-27422.
42. Venkateswarlu, K., Oatey, P. B., Tavare, J. M. and Cullen, P. J. (1998). Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol. 8, 463-466.
43. Watton, J. and Downward, J. (1999). Akt/PKB localisation and 3′ phosphoinositide generation at sites of epithetial cell-matrix and cell-cell interaction. Curr. Biol. 9, 433-436.
44. 3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 108, 809-821.
45. Worthylake, D. K., Rossman, K. L. and Sondek, J. (2004). Crystal structure of the DH/PH fragment of Dbs without bound GTPase. Structure 12, 1079-1086.
46. Yamboliev, I. A., Chen, J. and Gerthoffer, W. T. (2001). PI 3-kinases and Src kinases regulate spreading and migration of cultured VSMCs. Am. J. Physiol. Cell Physiol. 281, C709-C718.
47. Yao, L., Kawakami, Y. and Kawakami, T. (1994). The pleckstrin homology domain of Bruton's tyrosine kinase interacts with protein kinase C. Proc. Natl. Acad. Sci. USA 91, 9175-9179.
48. Yu, J. W., Mendrola, J. M., Audhya, A., Singh, S., Keleti, D., DeWald, D. B., Murray, D., Emr, S. D. and Lemmon, M. A. (2004). Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol. Cell 13, 677-688.