Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast

EMBO Journal

Volumn 17, Issue 18, 1998, Pages 5374-5387

  Isakoff, Steven J ^c   Cardozo, Tim ^c   Andreev, Julian ^c   Li, Zhai ^c   Ferguson, Kathryn M ^a   Abagyan, Ruben ^c   Lemmon, Mark A ^a   Aronheim, Ami ^b   Skolnik, Edward Y ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CDC25; Phosphatidylinositol 3 kinase; Phosphoinositide; Pleckstrin homology domain; Signal transduction

Indexed keywords

BINDING PROTEIN; COMPLEMENTARY DNA; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL; PLECKSTRIN; RAS PROTEIN; TRIPHOSPHOINOSITIDE;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONSENSUS SEQUENCE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE; SECOND MESSENGER; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; YEAST;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACID SEQUENCE; BLOOD PROTEINS; CELL MEMBRANE; CONSENSUS SEQUENCE; CONSERVED SEQUENCE; FUNGAL PROTEINS; MODELS, MOLECULAR; MUTATION; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOPROTEINS; PROTEIN BINDING; RAS PROTEINS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SECOND MESSENGER SYSTEMS; SEQUENCE HOMOLOGY, AMINO ACID;

SACCHAROMYCES CEREVISIAE;

EID: 0032530384     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.18.5374     Document Type: Article

References (89)

1. Abagyan, R.A. and Batalov, S. (1997) Do aligned sequences share the same fold? J. Mol. Biol., 273, 355-368.
2. Abagyan, R., Totrov, M. and Kuznetsov, D. (1993) ICM - A new method for protein modeling and design: applications to docking and structure prediction from the distorted native conformation. J. Comp. Chem., 15, 488-506.
3. Alessi, D.R. et al. (1997) 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr. Biol., 7, 776-789.
4. Aronheim, A. (1997) Improved efficiency sos recruitment system: expression of the mammalian GAP reduces isolation of Ras GTPase false positives. Nucleic Acids Res., 25, 3373-3374.
5. Aronheim, A., Engelberg, D., Li, N., al-Alawi, N., Schlessinger, J. and Karin, M. (1994) Membrane targeting of the nucleotide exchange factor Sos is sufficient for activating the Ras signaling pathway. Cell, 78, 949-961.
6. Aronheim, A., Zandi, E., Hennemann, H., Elledge, S.J. and Karin, M. (1997) Isolation of an AP-1 repressor by a novel method for detecting protein-protein interactions. Mol. Cell. Biol., 17, 3094-3102.
7. August, A., Sadra, A., Dupont, B. and Hanafusa, H. (1997) Src-induced activation of inducible T cell kinase (ITK) requires phosphatidylinositol 3-kinase activity and the Pleckstrin homology domain of inducible T cell kinase. Proc. Natl Acad. Sci. USA, 94, 11227-11232.
8. Bae, Y.S., Cantley, L.G., Chen, C.S., Kim, S.R., Kwon, K.S. and Rhee, S.G. (1998) Activation of phospholipase C-gamma by phosphatidylinositol, 3,4,5-trisphosphate. J. Biol. Chem., 273, 4465-4469.
9. Bairoch, A., Bucher, P. and Hofmann, K. (1997) The PROSITE database, its status in 1997. Nucleic Acids Res., 25, 217-221.
10. Barylko, B., Binns, D., Lin, K.M., Atkinson, M.A., Jameson, D.M., Yin, H.L. and Albanesi, J.P. (1998) Synergistic activation of dynamin GTPase by Grb2 and phosphoinositides. J. Biol. Chem., 273, 3791-3797.
11. Burgering, B.M. and Coffer, P.J. (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature, 376, 599-602.
12. Cardozo, T., Totrov, M. and Abagyan, R. (1995) Homology modeling by the ICM method. Proteins, 23, 403-414.
13. Carpenter, C.L. and Cantley, L.C. (1990) Phosphoinositide kinase. Biochemistry, 51, 11147-11156.
14. Carpenter, C.L. and Cantley, L.C. (1996) Phosphoinositide kinases. Curr. Opin. Cell Biol., 8, 153-158.
15. Chen, R.H., Corbalan-Garcia, S. and Bar-Sagi, D. (1997) The role of the PH domain in the signal-dependent membrane targeting of Sos. EMBO J., 16, 1351-1359.
16. Colicelli, J., Birchmeier, C., Michaeli, T., O'Neill, K., Riggs, M. and Wigler, M. (1989) Isolation and characterization of a mammalian gene encoding a high-affinity cAMP phosphodiesterase. Proc. Natl Acad. Sci. USA, 86, 3599-3603.
17. Cui, X., De Vivo, I., Slany, R., Miyamoto, A., Firestein, R., Cleary, M.L. (1998) Association of SET domain and myotubularin-related proteins modulates growth control. Nature Med., 18, 331-337.
18. De Camilli, P., Emr, S.D., McPherson, P.S. and Novick, P. (1996) Phosphoinositides as regulators in membrane traffic. Science, 271, 1533-1539.
19. Downward, J. (1998) Lipid-regulated kinases: Some common themes at last. Science, 279, 673-674.
20. Dudek, H., Datta, S., Franke, T., Birnbaum, M., Yao, R., Cooper, G., Segal, R., Kaplan, D. and Greenberg, M. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science, 275, 661-665.
21. Escobedo, J.A., Navankasattusas, S., Kavanaugh, W.M., Milfray, D., Fried, V.A. and Williams, L.T. (1991) cDNA cloning of a novel 85 kd protein that has SH2 domains and regulates binding of PI3-kinase to the PDGF receptor. Cell, 65, 75-82.
22. Falasca, M., Logan, S.K., Lehto, V.P., Baccante, G., Lemmon, M.A. and Schlessinger, J. (1998) Activation of phospholipase C gamma by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J., 17, 414-422.
23. Ferguson, K.M., Lemmon, M.A., Schlessinger, J. and Sigler, P.B. (1995) Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell, 83, 1037-1046.
24. Franke, T.F., Yang, S.I., Chan, T.O., Datta, K., Kazlauskas, A., Morrison, D.K., Kaplan, D.R. and Tsichlis, P.N. (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell, 81, 727-736.
25. Franke, T.F., Kaplan, D.R. and Cantley, L.C. (1997a) PI3K: downstream AKTion blocks apoptosis. Cell, 88, 435-437.
26. Franke, T.F., Kaplan, D.R., Cantley, L.C. and Toker, A. (1997b) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science, 275, 665-668.
27. Frech, M., Andjelkovic, M., Ingley, E., Reddy, K.K., Falck, J.R. and Hemmings, B.A. (1997) High affinity binding of inositol phosphates and phosphoinositides to the pleckstrin homology domain of RAC/ protein kinase B and their influence on kinase activity. J. Biol. Chem., 272, 8474-8481.
28. Fukuda, M. and Mikoshiba, K. (1996) Structure-function relationships of the mouse Gap1m. Determination of the inositol, 1,3,4,5-tetrakisphosphate-binding domain. J. Biol. Chem., 271, 18838-18842.
29. Fukuda, M. and Mikoshiba, K. (1997) The function of inositol high polyphosphate binding proteins. Bioessays, 19, 593-603.
30. Fukuda, M., Kojima, T., Kabayama, H. and Mikoshiba, K. (1996) Mutation of the pleckstrin homology domain of Bruton's tyrosine kinase in immunodeficiency impaired inositol, 1,3,4,5-tetrakisphosphate binding capacity. J. Biol. Chem., 271, 30303-30306.
31. Gibson, T.J., Hyvonen, M., Musacchio, A., Saraste, M. and Birney, E. (1994) PH domain: the first anniversary. Trends Biochem. Sci., 19, 349-353.
32. Gietz, R.D. and Schiestl, R.H. (1995) Transforming Yeast with DNA. In Methods Mol. Cell., pp. 255-269.
33. Hammonds-Odie, L.P., Jackson, T.R., Profit, A.A., Blader, I.J., Turck, C.W., Prestwich, G.D. and Theibert, A.B. (1996) Identification and cloning of centaurin-alpha. A novel phosphatidylinositol, 3,4,5-trisphosphate-binding protein from rat brain. J. Biol. Chem., 271, 18859-18868.
34. Han, J., Luby-Phelps, K., Das, B., Shu, X., Xia, Y., Mosteller, R.D., Krishna, U.M., Falck, J.R., White, M.A. and Broek, D. (1998) Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science, 279, 558-560.
35. 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.
36. Harlan, J.E., Yoon, H.S., Hajduk, P.J. and Fesik, S.W. (1995) Structural characterization of the interaction between a pleckstrin homology domain and phosphatidylinositol, 4,5-bisphosphate. Biochemistry, 34, 9859-9864.
37. Herbst, R., Carroll, P.M., Allard, J.D., Schilling, J., Raabe, T. and Simon, M.A. (1996) Daughter of sevenless is a substrate of the phosphotyrosine phosphatase Corkscrew and functions during sevenless signaling. Cell, 85, 899-909.
38. Hiles, I. et al. (1992) P13-kinase: structure and expression of the 110 kd catalytic subunit. Cell, 70, 419-429.
39. Holgado-Madruga, M., Emlet, D.R., Moscatello, D.K., Godwin, A.K. and Wong, A.J. (1996) A Grb2-associated docking protein in EGF- and insulin-receptor signalling. Nature, 379, 560-564.
40. Hu, P. and Schlessinger, J. (1994) Direct association of p110-beta phosphatidylinositol 3-kinase with p85 is mediated by an N-terminal fragment of p110-beta. Mol. Cell. Biol., 14, 2577-2583.
41. Hu, P., Modino, A., Skolnik, E.Y. and Schlessinger, J. (1993) Identification and cloning of a novel PI-3 kinase. Mol. Cell. Biol., 13, 7677-7688.
42. Hyvonen, M. and Saraste, M. (1997) Structure of the PH domain and Btk motif from Bruton's tyrosine kinase: molecular explanations for X-linked agammaglobulinaemia. EMBO J., 16, 3396-3404.
43. Hyvonen, M., Macias, M.J., Nilges, M., Oschkinat, H., Saraste, M. and Wilmanns, M. (1995) Structure of the binding site for inositol phosphates in a PH domain. EMBO J., 14, 4676-4685.
44. Irvine, R. and Cullen, P. (1996) Inositol phosphates - whither bound? Intracellular signalling. Curr. Biol., 6, 537-540.
45. Isakoff, S.J., Yu, Y., Su, Y.-C., Blaikie, P., Yajnik, V., Rose, E., Weidner, K.M., Sachs, M., Margolis, B. and Skolnik, E.Y. (1996) Interaction between the phosphotyrosine binding domain of Shc and the Insulin Receptor is required for Shc phosphorylation by insulin in vivo. J. Biol. Chem., 271, 3959-3962.
46. James, S., Downes, C., Gigg, R., Grove, S., Holmes, A. and Alessi, D. (1996) Specific binding of the Akt-1 protein kinase to phosphatidylinositol, 3,4,5-trisphosphate without subsequent activation. Biochem. J., 315, 709-713.
47. Karlin, S. and Altschul, S.F. (1990) Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc. Natl Acad. Sci. USA, 87, 2264-2268.
48. 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.
49. Klarlund, J.K., Rameh, L.E., Cantley, L.C., Buxton, J.M., Holik, J.J., Sakelis, C., Patki, V., Corvera, S. and Czech, M.P. (1998) Regulation of GRP1-catalyzed ADP ribosylation factor guanine nucleotide exchange by phosphatidylinositol, 3,4,5-trisphosphate. J. Biol. Chem., 273, 1859-1862.
50. Klippel, A., Escobedo, J.A., Hu, Q. and Williams, L.T. (1993) A region of the 85-kilodalton subunit of phosphatidylinositol 3-kinase binds the 110 kDa catalytic subunit in vivo. Mol. Cell. Biol., 13, 5560-5566.
51. Klippel, A., Kavanaugh, W.M., Pot, D. and Williams, L.T. (1997) A specific product of phosphatidylinositol 3-kinase directly activates the protein kinase Akt through its pleckstrin homology domain. Mol. Cell. Biol., 17, 338-344.
52. Kodaki, T., Woscholski, R., Emr, S., Waterfield, M., Nurse, P. and Parker, P. (1994a) Mammalian phosphatidylinoskol 3′-kinase induces a lethal phenotype on expression in Schizosaccharomyes pombe; comparison with VPS34 gene product. Eur. J. Biochem., 219, 775-780.
53. Kodaki, T., Woscholski, R., Hallberg, B., Rodriquez-Viciana, P., Downward, J. and Parker, P. (1994b) The activation of phosphatidylinositol 3-kinase by Ras. Curr. Biol., 4, 798-806.
54. Kojima, T., Fukuda, M., Watanabe, Y., Hamazato, F. and Mikoshiba, K. (1997) Characterization of the pleckstrin homology domain of Btk as an inositol polyphosphate and phosphoinositide binding domain. Biochem. Biophys. Res. Comm., 236, 333-339.
55. Koshiba, S., Kigawa, T., Kim, J.H., Shirouzu, M., Bowtell, D. and Yokoyama, S. (1997) The solution structure of the pleckstrin homology domain of mouse Son-of-sevenless 1 (mSos1). J. Mol. Biol., 269, 579-591.
56. Kubiseski, T.J., Chook, Y.M., Parris, W.E., Rozakis-Adcock, M. and Pawson, T. (1997) High affinity binding of the pleckstrin homology domain of mSos1 to phosphatidylinositol (4,5)-bisphosphate. J. Biol. Chem., 272, 1799-1804.
57. Lemmon, M.A., Ferguson, K.M., O'Brien, R., Sigler, P.B. and Schlessinger, J. (1995) Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl Acad. Sci. USA, 92, 10472-10476.
58. Lemmon, M.A., Ferguson, K.M. and Schlessinger, J. (1996) PH domains: diverse sequences with a common fold recruit signaling molecules to the cell surface. Cell, 85, 621-624.
59. Lemmon, M.A., Falasca, M., Ferguson, K.M. and Schlessinger, J. (1997) Regulatory reruitment of signalling molecules to the cell membrane by plekstrin homology domains. Trends Cell Biol., 7, 237-242.
60. Lockyer, P.J., Bottomley, J.R., Reynolds, J.S., McNulty, T.J., Venkateswarlu, K., Potter, B.V., Dempsey, C.E. and Cullen, P.J. (1997) Distinct subcellular localisations of the putative inositol, 1,3,4,5-tetrakisphosphate receptors GAP1IP4BP and GAP1m result from the GAP1IP4BP PH domain directing plasma membrane targeting. Curr. Biol., 7, 1007-1010.
61. Logan, S., Falasca, M., Hu, P. and Schlessinger, J. (1997) Phosphatidylinositol 3-kinase mediates epidermal growth factor-induced activation of the c-Jun N-terminal kinase signaling pathway. Mol. Cell. Biol., 17, 5784-5790.
62. Mattsson, P.T., Vihinen, M. and Smith, C.I. (1996) X-linked agammaglobulinemia (XLA): a genetic tyrosine kinase (Btk) disease. Bioessays, 18, 825-834.
63. Mayer, B.J., Ren, R., Clark, K.L. and Baltimore, D. (1993) A putative modular domain present in diverse signaling proteins. Cell, 73, 629-630.
64. Mermall, V., Post, P.L. and Mooseker, M.S. (1998) Unconventional myosins in cell movement, membrane traffic and signal transduction. Science, 279, 527-533.
65. Musacchio, A., Gibson, T., Rice, P., Thompson, J. and Saraste, M. (1993) The PH domain: a common piece in the structural patchwork of signalling proteins. Trends Biochem. Sci., 18, 343-348.
66. Nimnual, A.S., Yatsula, B.A. and Bar-Sagi, D. (1998) Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science, 279, 560-563.
67. Otsu, M. et al. (1991) Characterization of two 85 kD proteins that associate with receptor tyrosine kinases, middle-T/pp60c-src complexes and PI3 kinase. Cell, 65, 91-104.
68. Pitcher, J.A., Touhara, K., Payne, E.S. and Lefkowitz, R.J. (1995) Pleckstrin homology domain-mediated membrane association and activation of the beta-adrenergic receptor kinase requires coordinate interaction with G beta gamma subunits and lipid. J. Biol. Chem., 270, 11707-11710.
69. Raabe, T., Riesgo-Escovar, J., Liu, X., Bausenwein, B.S., Deak, P., Maroy, P. and Hafen, E. (1996) DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and Ras1 in Drosophila. Cell, 85, 911-920.
70. Rameh, L.E., Chen, C.-S. and Cantley, L.C. (1995) Phosphatidylinositol (3,4,5)P3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell, 83, 821-830.
71. Rameh, L.E. et al. (1997) A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem., 272, 22059-22066.
72. Rawlings, D.J. et al. (1993) Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science, 261, 358-361.
73. Salim, K. et al. (1996) Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J., 15, 6241-6250.
74. Scharenberg, A.M., El-Hillal, O., Fruman, D.A., Beitz, L.O., Li, Z., Lin, S., Gout, I., Cantley, L.C., Rawlings, D.J. and Kinet, J.P. (1998) Phosphatidylinositol-3,4,5-trisphosphate (PtdIns-3,4,5-P3)/Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO J., 17, 1961-1972.
75. Shaw, G. (1996) The pleckstrin homology domain: an intriguing multifunctional protein module. Bioessays, 18, 35-46.
76. Skolnik, E.Y., Batzer, A., Li, N., Lee, C.H., Lowenstein, E., Mohammadi, M., Margolis, B. and Schlessinger, J. (1993) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science, 260, 1953-1955.
77. 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.
78. Stephens, L.R. et al. (1997) The G beta gamma sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell, 89, 105-114.
79. Stephens, L. et al. (1998) Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science, 279, 710-714.
80. Stoyanov, B. et al. (1995) Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science, 269, 690-693.
81. Superti-Furga, G., Jonsson, K. and Courtneidge, S.A. (1996) A functional screen in yeast for regulators and antagonizers of heterologous tyrosine kinases. Nature Biotech., 5, 600-605.
82. Toker, A. and Cantley, L.C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature, 387, 673-676.
83. Vanhaesebroeck, B., Leavers, S.J., Panayotou, G.P. and Waterfield, M.D. (1997) Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem. Sci., 22, 267-272.
84. Venkateswarlu, K., Oatey, P., Tavaré, J. and Cullen, P. (1998) Insulin-dependent translocation of ARNO to the plasma membrane of adipocytes requires phosphatidylinositol 3-kinase. Curr. Biol., 8, 463-466.
85. Vihinen, M., Iwata, T., Kinnon, C., Kwan, S.P., Ochs, H.D., Vorechovsky, I. and Smith, C.I. (1996) BTKbase, mutation database for X-linked agammaglobulinemia (XLA). Nucleic Acids Res., 24, 160-165.
86. Vojtek, A.B., Hollenberg, S.M. and Cooper, J.A. (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell, 74, 205-214.
87. Weidner, K.M., Di Cesare, S., Sachs, M., Brinkmann, V., Behrens, J. and Birchmeier, W. (1996) Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature, 384, 173-176.
88. Yang, W. and Desiderio, S. (1997) BAP-135, a target for Bruton's tyrosine kinase in response to B cell receptor engagement. Proc. Natl Acad. Sci. USA, 94, 604-609.
89. Zheng, J., Cahill, S.M., Lemmon, M.A., Fushman, D., Schlessinger, J. and Cowburn, D. (1996) Identification of binding site for acidic phospholipids on the PH domain of dynamin: implication for stimulation of GTPase activity. J. Mol. Biol., 255, 14-21.