Regulation of the p85/p110 phosphatidylinositol 3'-kinase: Stabilization and inhibition of the p110α catalytic subunit by the p85 regulatory subunit

Molecular and Cellular Biology

Volumn 18, Issue 3, 1998, Pages 1379-1387

  Yu, Jinghua ^a   Zhang, Yitao ^a   Mcilroy, James ^a   Rordorf Nikolic, Tamara ^a   Orr, George A ^a   Backer, Jonathan M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL; PHOSPHOPROTEIN;

ARTICLE; CATALYSIS; DATA ANALYSIS; ENZYME REGULATION; INSECT; MAMMAL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STABILITY;

EID: 0031887249     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.3.1379     Document Type: Article

References (49)

1. Antonetti, D. A., P. Algenstaedt, and C. R. Kahn. 1996. Insulin receptor substrate 1 binds two novel splice variants of the regulatory subunit of phosphatidylinositol 3-kinase in muscle and brain. Mol. Cell. Biol 16:2195-2203.
2. Backer, J. M., Jr., M. G. Myers, S. E. Shoelson, D. J. Chin, X. J. Sun, M. Miralpeix, P. Hu, B. Margolis, E. Y. Skolnik, J. Schlessinger, and M. F. White. 1992. The phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:3469-3479.
3. Booker, G. W., I. Gout, A. K. Downing, P. C. Driscoll, J. Boyd, M. D. Waterfield, and I. D. Campbell. 1993. Solution structure and ligand-binding site of the SH3 domain of the p85α subunit of phosphatidylinositol 3-kinase. Cell 73:813-822.
4. Cantley, L. C., K. R. Auger, C. Carpenter, B. Duckworth, A. Graziani, R. Kapeller, and S. Soltoff. 1991. Oncogenes and signal transduction. Cell 64:231-302.
5. Carpenter, C. L., K. R. Auger, M. Chanudhuri, M. Yoakim, B. Schaffhausen, S. Shoelson, and L. C. Cantley. 1993. Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268:9478-9483.
6. Cheatham, B., C. J. Vlahos, L. Cheatham, L. Wang, J. Blenis, and C. R. Kahn. 1994. Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase. DNA synthesis, and glucose transporter translocation. Mol. Cell. Biol. 14:4902-4911.
7. Dhand, R., K. Hara, I. Hiles, B. Bax, I. Gout, G. Panayotou, M. J. Fry, K. Yonezawa, M. Kasuga, and M. D. Waterfield. 1994. PI 3-kinase: structural and functional analysis of intersubunit interactions. EMBO J. 13:511-521.
8. Dhand, R., I. Hiles, G. Panayotou, S. Roche, M. J. Fry, I. Gout, N. F. Totty, O. Truong, P. Vicendo, K. Yonezawa, M. Kasuga, S. A. Courtneidge, and M. D. Waterfield. 1994. PI 3-kinase is a dual specificity enzyme: autoregulation by an intrinsic protein-serine kinase activity. EMBO J. 13:522-533.
9. Escobedo, J. A., S. Navankasattusas, W. M. Kavanaugh, D. Milfay, V. A. Fried, and L. T. Williams. 1991. cDNA cloning of a novel 85 kD protein that has SH2 domains and regulates binding of PI3-kinase to the PDGF β-receptor. Cell 65:75-82.
10. Guinebault, C., B. Payrastre, C. Racaud-Sultan, H. Mazarguil, M. Breton, G. Mauco, M. Plantavid, and H. Chap. 1995. Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85-α with actin filaments and focal adhesion kinase. J. Cell Biol. 129:831-842.
11. Hiles, I. D., M. Otsu, S. Volinia, M. J. Fry, I. Gout, R. Dhand, G. Panayotou, F. Ruiz-Larrea, A. Thompson, N. F. Totty, J. J. Hsuan, S. A. Courtneidge, P. J. Parker, and M. D. Waterfield. 1992. Phosphatidylinositol 3-kinase: structure and expression of the 110 kd catalytic subunit. Cell 70:419-429.
12. Holt, K. H., A. L. Olson, W. S. Moye-Rowley, and J. E. Pessin. 1994 Phosphatidylinositol 3-kinase activation is mediated by high-affinity interactions between distinct domains within the p110 and p85 subunits. Mol. Cell. Biol. 14:42-49.
13. Hu, P., A. Mondino, E. Y. Skolnik, and J. Schlessinger. 1993. Cloning of a novel, ubiquitously expressed human phosphatidylinositol 3-kinase and identification of its binding site on p85. Mol. Cell. Biol. 13:7677-7688.
14. Hu, P., and J. Schlessinger. 1994. Direct association of p110β phosphatidylinositol 3-kinase with p85 is mediated by an N-terminal fragment of p110β. Mol. Cell. Biol. 14:2577-2583.
15. Hu, Q., A. Klippel, A. J. Muslin, W. J. Fantl, and L. T. Williams. 1995. Ras-dependent induction of cellular responses by constitutively active phosphatidylinositol-3 kinase. Science 268:100-102.
16. Joly, M., A. Kazlauskas, and S. Corvera. 1995. Phosphatidylinositol 3-kinase activity is required at a postendocytic step in platelet-derived growth factor receptor trafficking. J. Biol. Chem. 270:13225-13230.
17. Kapeller, R., K. V. S. Prasad, O. Janssen, W. Hou, B. S. Schaffhausen, C. E. Rudd, and L. C. Cantley. 1994. Identification of two SH3-binding motifs in the regulatory subunit of phosphatidylinositol 3-kinase. J. Biol. Chem. 269:1927-1933.
18. Klippel, A., J. A. Escobedo, M. Hirano, and L. T. Williams. 1994. The interaction of small domains between the subunits of phosphatidylinositol 3-kinase determines enzyme activity. Mol. Cell. Biol. 14:2675-2685.
19. Klippel, A., J. A. Escobedo, Q. Hu, and L. T. Williams. 1993. A region of the 85-kilodalton (kDa) subunit of phosphatidylinositol 3-kinase binds the 110-kDa catalytic subunit in vivo. Mol. Cell. Biol. 13:5560-5566.
20. Kotani, K., K. Yonezawa, K. Hara, H. Ueda, Y. Kitamura, H. Sakaue, A. Ando, A. Chavanieu, B. Calas, F. Grigorescu, M. Nishiyama, M. D. Waterfield, and M. Kasuga. 1994. Involvement of phosphoinositide 3-kinase in insulin-or IGF-1-induced membrane ruffling. EMBO J. 13:2313-2321.
21. Kozak, M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283-292.
22. Kozak, M. 1997. Recognition of AUG and alternative initiator codons is augmented by G in position +4 but is not generally affected by the nucleotides in positions +5 and +6. EMBO J. 16:2482-2492.
23. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol 154:367-382.
24. Leevers, S. J., D. Weinkove, L. K. MacDougall, E. Hafen, and M. D. Waterfield. 1996. The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J. 15:6584-6594.
25. McIlroy, J., D. Chen, C. Wjasow, T. Michaeli, and J. M. Backer. 1997. Specific activation of p85-p110 phosphatidylinositol 3′-kinase stimulates DNA synthesis by ras-and p70 S6 kinase-dependent pathways. Mol Cell Biol. 17:248-255.
26. Molz, L., Y. W. Chen, M. Hirano, and L. T. Williams. 1996. Cpk is a novel class of Drosophila PtdIns 3-kinase containing a C2 domain. J. Biol. Chem 271:13892-13899.
27. c-src complexes and PI3-kinase. Cell 65:91-104.
28. Pleiman, C. M., W. M. Hertz, and J. C. Cambier. 1994. Activation of phosphatidylinositol-3′ kinase by Src-family kinase SH3 binding to the p85 subunit. Science 263:1609-1612.
29. PIK reveal a new regulatory subunit for phosphatidylinositol 3-kinase. Mol. Cell. Biol. 15:4453-4465.
30. Rameh, L. E., C.-S. Chen, and L. C. Cantley. 1995. Phosphatidylinositol (3,4,5)P3 interacts with SH2 domains and modulates PI3-kinase association with tyrosine-phosphorylated proteins. Cell 83:821-830.
31. Roche, S., M. Koegl, and S. A. Courtneidge. 1994. The phosphatidylinositol 3-kinase α is required for DNA synthesis induced by some, but not all, growth factors. Proc. Natl. Acad. Sci. USA 91:9185-9189.
32. Rodriguez-Viciana, P., P. H. Warne, B. Vanhaesebroeck, M. D. Waterfield, and J. Downward. 1996. Activation of phosphoinositide 3-kinase by interaction with Ras and by point mutation. EMBO J. 15:2442-2451.
33. Rordorf-Nikolic, T., D. J. Van Horn, D. Chen, M. F. White, and J. M. Backer. 1995. Regulation of phosphatidylinositol 3′-kinase by tyrosyl phosphoproteins. Full activation requires occupancy of both SH2 domains in the 85-kDa regulatory subunit. J. Biol. Chem. 270:3662-3666.
34. Ruderman, N., R. Kapeller, M. F. White, and L. C. Cantley. 1990. Activation of phosphatidylinositol-3-kinase by insulin. Proc. Natl. Acad Sci. USA 87:1411-1415.
35. Schu, P. V., K. Takegawa, M. J. Fry, J. H. Stack, M. D. Waterfield, and S. D. Emr. 1993. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260:88-91.
36. Skolnik, E. Y., B. Margolis, M. Mohammadi, E. Lowenstein, R. Fischer, A. Drepps, A. Ullrich, and J. Schlessinger. 1991. Cloning of PI3 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases. Cell 65:83-90.
37. Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
38. Stephens, L. R., A. Eguinoa, H. Erdjument-Bromage, M. Lui, F. Cooke, J. Coadwell, A. S. Smrcka, M. Thelen, K. Cadwallader, P. Tempst, and P. T. Hawkins. 1997. The Gβgamma sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 89:105-114.
39. Stoyanov, B., S. Volinia, T. Hanck, I. Rubio, M. Loubtchenkov, D. Makk, S. Stoyanova, B. Vanhaesebroeck, R. Dhand, B. Nurnberg, P. Gierschik, K. Seedorf, J. J. Hsuan, M. D. Waterfield, and R. Wetzker. 1995. Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 269:690-693.
40. Sun, X. J., P. Rothenberg, C. R. Kahn, J. M. Backer, E. Araki, P. A. Wilden, D. A. Cahill, B. J. Goldstein, and M. F. White. 1991. The structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352:73-77.
41. Tolias, K. F., L. C. Cantley, and C. L. Carpenter. 1995. Rho family GTPases bind to phosphoinositide kinases. J. Biol. Chem. 270:17656-17659.
42. Vanhaesebroeck, B., M. J. Welham, K. Kotani, R. Stein, P. H. Warne, M. J. Zvelebil, K. Higashi, S. Volinia, J. Downward, and M. D. Waterfield. 1997. p110-delta, a novel phosphoinositide 3-kinase in leukocytes. Proc. Natl. Acad. Sci. USA 94:4330-4335.
43. Virbasius, J. V., A. Guilherme, and M. P. Czech. 1996. Mouse p170 is a novel phosphatidylinosilol 3-kinase containing a C2 domain. J. Biol. Chem. 271:13304-13307.
44. Volinia S., R. Dhand, B. Vanhaesebroeck, L. K. MacDougall, R. Stein, M. J. Zvelebil, J. Domin, C. Panaretou, and M. D. Waterfleld. 1995. A human phosphatidylinositol 3-kinase complex related to the yeast Vps34p-Vps15p protein sorting system. EMBO J. 14:3339-3348.
45. Woscholski, R., R. Dhand, M. J. Fry, M. D. Waterfield, and P. J. Parker. 1994. Biochemical characterization of the free catalytic p110α and the complexed heterodimeric p110α · p85α forms of the mammalian phosphatidylinositol 3-kinase. J. Biol. Chem. 269:25067-25072.
46. Yao, R., and G. M. Cooper. 1995. Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267:2003-2006.
47. Yu, J., and J. M. Backer. Unpublished data.
48. Zheng, Y., S. Bagrodia, and R. A. Cerione. 1994. Activation of phosphoinositide 3-kinase by Cdc42Hs binding to p85. J. Biol. Chem. 269:18727-18730.
49. Zvelebil, M. J., L. MacDougall, S. Leevers, S. Volinia, B. Vanhaesebroeck, I. Gout, G. Panayotou, J. Domin, R. Stein, F. Pages, F. Hoga, K. Salim, J. Linacre, P. Das, C. Panaretou, R. Wetzker, and M. Waterfleld. 1996. Structural and functional diversity of phosphoinositide 3-kinases. Philos. Trans. R. Soc. Lond. 351:217-223.