The PI 3-kinase isoforms p110a and p110b have differential roles in PDGF- and insulin-mediated signaling

Journal of Cell Science

Volumn 113, Issue 2, 2000, Pages 207-214

  Hooshmand Rad, Roya ^a,e   Hájková, Lucie ^b   Klint, Peter ^d   Karlsson, Roger ^b   Vanhaesebroeck, Bart ^c   Claesson Welsh, Lena ^d   Heldin, Carl Henrik ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^d UPPSALA UNIVERSITY   (Sweden)

^e BURNHAM INSTITUTE   (United States)

Author keywords

Cytoskeleton; Insulin; PDGF; PI3 kinase

Indexed keywords

ACTIN; ANTIBODY; G PROTEIN COUPLED RECEPTOR; INSULIN; ISOENZYME; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; SYNTHETIC PEPTIDE; TYROSINE KINASE RECEPTOR;

ACTIN FILAMENT; ANIMAL CELL; AORTA; ARTICLE; ENDOTHELIUM CELL; ENZYME SUBUNIT; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SWINE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; AMINO ACID SEQUENCE; ANIMALS; ANTIBODY SPECIFICITY; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; INSULIN; ISOENZYMES; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PLATELET-DERIVED GROWTH FACTOR; PROTEIN STRUCTURE, QUATERNARY; SIGNAL TRANSDUCTION; SWINE;

EID: 0033952239     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Antonetti, D. A., Algenstaedt, P. and Kahn, C. R. (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. Ayscough, K. R. (1998). In vivo functions of actin-binding proteins. Curr. Opin. Cell Biol. 10, 102-111.
3. Cantrell, D. (1998). Lymphocyte signalling: a coordinating role for Vav? Curr. Biol. 8, R535-538.
4. Carpenter, C. L., Auger, K. R., Chanudhuri, M., Yoakim, M., Schaffhausen, B., Shoelson, S. and Cantley, L. C. (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.
5. Cheatham, B., Vlahos, C. J., Cheatham, L., Wang, L., Blenis, J. and Kahn, C. R. (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.
6. Chinkers, M., McKanna, J. A. and Cohen, S. (1979). Rapid induction of morphological changes in human carcinoma cells A-431 by epidermal growth factors. J. Cell Biol. 83, 260-265.
7. Christoforidis, S., Miaczynska, M., Ashman, K., Wilm, M., Zhao, L., Yip, S., Waterfield, M. D., Backer, J. M. and Zerial, M. (1999). Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nature Cell Biol. 1, 249-252.
8. Claesson-Welsh, L. (1994). Platelet-derived growth factor receptor signals. J. Biol. Chem. 269, 32023-6.
9. Cohen, G. B., Ren, R. and Baltimore, D. (1995). Modular binding domains in signal transduction proteins. Cell 80, 237-248.
10. Corvera, S. and Czech, M. P. (1998). Direct targets of phosphoinositide 3-kinase products in membrane traffic and signal transduction. Trends Cell Biol. 8, 442-446.
11. Deora, A. A., Win, T., Vanhaesebroeck, B. and Lander, H. M. (1998). A Redox-triggered Ras-Effector Interaction. Recruitment of phosphatidylinositol 3′-kinase to ras by redox stress. J. Biol. Chem. 273, 29923-29928.
12. Fantl, W. J., Escobedo, J. A., Martin, G. A., Turck, C. W., del Rosario, M., McCormick, F. and Williams, L. T. (1992). Distinct phosphotyrosines on a growth factor receptor bind to specific molecules that mediate different signaling pathways. Cell 69, 413-423.
13. Frevert, E. U. and Kahn, B. B. (1997). Differential effects of constitutively active phosphatidylinositol 3-kinase on glucose transport, glycogen synthase activity, and DNA synthesis in 3T3-L1 adipocytes. Mol. Cell Biol. 17, 190-198.
14. Fry, M. J. (1994). Structure, regulation and function of phosphoinositide 3-kinases. Biochim. Biophys. Acta 1226, 237-268.
15. Goldschmidt-Clermont, P. J., Machesky, L. M., Baldassare, J. J. and Pollard, T. D. (1990). The actin-binding protein prufilin binds to PIP2 and inhibits its hydrolysis by phospholipase C. Science 247, 1575-1578.
16. Goldschmidt-Clermont, P. J., Kim, J. W., Machesky, L. M., Rhee, S. G. and Pollard, T. D. (1991). Regulation of phospholipase C-gamma 1 by profilin and tyrosine phosphorylation. Science 251, 1231-1233.
17. Guinebault, C., Payrastre, B., Racaud-Sultan, C., Mazarguil, H., Breton, M., Mauco, G., Plantavid, M. and Chap, H. (1995). Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85α with actin filaments and focal adhesion kinase. J. Cell Biol. 129, 831-842.
18. Hartwig, J. H., Bokoch, G. M., Carpenter, C. L., Janmey, P. A., Taylor, L. A., Toker, A. and Stossel, T. P. (1995). Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82, 643-653.
19. Heldin, C. H., Östman, A. and Rönnstrand, L. (1998). Signal transduction via platelet-derived growth factor receptors. Biochim. Biophys. Acta 1378, F79-113.
20. Hiles, I. D., Otsu, M., Volinia, S., Fry, M. J., Gout, I., Dhand, R., Panayotou, G., Ruiz-Larrea, F., Thompson, A., Totty, N. F., Hsuan, J. J., Courtneidge, S. A., Parker, P. J. and Waterfield, M. D. (1992). Phosphatidylinositol 3-kinase: structure and expression of the 110 kd catalytic subunit. Cell 70, 419-429.
21. Höglund, A. S., Karlsson, R., Arro, E., Fredriksson, B. A. and Lindberg, U. (1980). Visualization of the peripheral weave of microfilaments in glia cells. J. Muscle Res. Cell Motil. 1, 127-146.
22. Hooshmand-Rad, R., Claesson-Welsh, L., Wennström, S., Yokote, K., Siegbahn, A. and Heldin, C. H. (1997). Involvement of phosphatidylinositide 3′-kinase and Rac in platelet-derived growth factor-induced actin reorganization and chemotaxis. Exp. Cell Res. 234, 434-441.
23. Hu, P., Mondino, A., Skolnik, E. Y. and Schlessinger, J. (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.
24. Hunter, S., Koch, B. L. and Anderson, S. M. (1997). Phosphorylation of cb1 after stimulation of Nb2 cells with prolactin and its association with phosphatidylinositol 3-kinase. Mol. Endocrinol. 11, 1213-1222.
25. Inukai, K., Funaki, M., Ogihara, T., Katagiri, H., Kanda, A., Anai, M., Fukushima, Y., Hosaka, T., Suzuki, M., Shin, B. C., Takata, K., Yazaki, Y., Kikuchi, M., Oka, Y. and Asano, T. (1997). p85α gene generates three isoforms of regulatory subunit for phosphatidylinositol 3-kinase (PI 3-Kinase). p50α, p55α, and p85α, with different PI 3-kinase activity elevating responses to insulin. J. Biol. Chem. 272, 7873-7882.
26. Jhun, B. H., Rose, D. W., Seely, B. L., Rameh, L., Cantley, L., Saltiel, A. R. and Olefsky, J. M. (1994). Microinjection of the SH2 domain of the 85-kilodalton subunit of phosphatidylinositol 3-kinase inhibits insulin-induced DNA synthesis and c-fos expression. Mol. Cell Biol. 14, 7466-7475.
27. Kaliman, P., Canicio, J., Shepherd, P. R., Beeton, C. A., Testar, X., Palacin, M. and Zorzano, A. (1998). Insulin-like growth factors require phosphatidylinositol 3-kinase to signal myogenesis: dominant negative p85 expression blocks differentiation of L6E9 muscle cells. Mol. Endocrinol. 12, 66-77.
28. Kazlauskas, A., Kashishian, A., Cooper, J. A. and Valius, M. (1992). GTPase-activating protein and phosphatidylinositol 3-kinase bind to distinct regions of the platelet-derived growth factor receptor beta subunit. Mol. Cell Biol. 12, 2534-2544.
29. Kerouz, N. J., Horsch, D., Pons, S. and Kahn, C. R. (1997). Differential regulation of insulin receptor substrates-1 and -2 (IRS-1 and IRS-2) and phosphatidylinositol 3-kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. J. Clin. Invest. 100, 3164-3172.
30. Klippel, A., Escobedo, J. A., Hirano, M. and Williams, L. T. (1994). The interaction of small domains between the subunits of phosphatidylinositol 3-kinase determines enzyme activity. Mol. Cell Biol. 14, 2675-2685.
31. Kotani, K., Yonezawa, K., Hara, K., Ueda, H., Kitamura, Y., Sakaue, H., Ando, A., Chavanieu, A., Calas, B., Grigorescu, F., Nishiyama, M., Waterfield, M. D. and Kasuga, M. (1994). Involvement of phosphoinositide 3-kinase in insulin-or IGF-induced membrane ruffling. EMBO J. 13, 2313-2321.
32. Kundra, V., Escobedo, J. A., Kazlauskas, A., Kim, H. K., Rhee, S. G., Williams, L. T. and Zetter, B. R. (1994). Regulation of chemotaxis by the platelet-derived growth factor receptor-beta. Nature 367, 474-476.
33. Kurosu, H., Maehama, T., Okada, T., Yamamoto, T., Hoshino, S., Fukui, Y., Ui, M., Hazeki, O. and Katada, T. (1997). Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110β is synergistically activated by the βγ subunits of G proteins and phosphotyrosyl peptide. J. Biol. Chem. 272, 24252-24256.
34. Lassing, I. and Lindberg, U. (1985). Specific interaction between phosphatidylinositol 4, 5-bisphosphate and profilactin. Nature 314, 472-474.
35. Liu, X., Marengere, L. E., Koch, C. A. and Pawson, T. (1993). The v-Src SH3 domain binds phosphatidylinositol 3′-kinase. Mol. Cell Biol. 13, 5225-5232.
36. Lu, P. J., Shieh, W. R., Rhee, S. G., Yin, H. L. and Chen, C. S. (1996). Lipid products of phosphoinositide 3-kinase bind human profilin with high affinity. Biochemistry 35, 14027-14034.
37. McIlroy, J., Chen, D., Wjasow, C., Michaeli, T. and Backer, J. M. (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.
38. Mellström, K., Höglund, A. S., Nistér, M., Heldin, C. H., Westermark, B. and Lindberg, U. (1983). the effect of platelet-derived growth factor on morphology and motility of human glial cells. J. Muscle Res. Cell Motil. 4, 589-609.
39. Nave, B. T., Haigh, R. J., Hayward, A. C., Siddle, K. and Shepherd, P. R. (1996). Compartment-specific regulation of phosphoinositide 3-kinase by platelet-derived growth factor and insulin in 3T3-L1 adipocytes. Biochem. J. 318, 55-60.
40. Nobes, C. D., Hawkins, P., Stephens, L. and Hall, A. (1995). Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108, 225-233.
41. Pleiman, C. M., Hertz, W. M. and Cambier, J. C. (1994). Activation of phosphatidylinositol-3′ kinase by Src-family kinase SH3 binding to the p85 subunit. Science 263, 1609-1612.
42. Roche, S., Koegl, M. and Courtneidge, S. A. (1994). The phosphatidylinositol 3-kinase α is required for DNA synthesis induced by some, but not all, growth factors. Proc. Nat. Acad. Sci. USA 91, 9185-9189.
43. Roche, S., Downward, J., Raynal, P. and Courtneidge, S. A. (1998). A function for phosphatidylinositol 3-kinase beta (p85α-p110β) in fibroblasts during mitogenesis: requirement for insulin- and lysophosphatidic acid-mediated signal transduction. Mol. Cell Biol. 18, 7119-7129.
44. Shepherd, P. R., Nave, B. T., Rincon, J., Nolte, L. A., Bevan, A. P., Siddle, K., Zierath, J. R. and Wallberg-Henriksson, H. (1997). Differential regulation of phosphoinositide 3-kinase adapter subunit variants by insulin in human skeletal muscle. J. Biol. Chem. 272, 19000-19007.
45. Shibasaki, F., Fukami, K., Fukui, Y. and Takenawa, T. (1994). Phosphatidylinositol 3-kinase binds to α-actinin through the p85 subunit. Biochem. J. 302, 551-557.
46. Siddhanta, U., McIlroy, J., Shah, A., Zhang, Y. and Backer, J. M. (1998). Distinct roles for the p110α and hVPS34 phosphatidylinositol 3′-kinases in vesicular trafficking, regulation of the actin cytoskeleton, and mitogenesis. J. Cell Biol. 143, 1647-1659.
47. Singh, S. S., Chauhan, A., Murakami, N. and Chauhan, V. P. (1996). Profilin and gelsolin stimulate phosphatidylinositol 3-kinase activity. Biochemistry 35, 16544-16549.
48. Small, J. V. (1981). Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks. J. Cell Biol. 91, 695-705.
49. Small, J. V., Rottner, K. and Kaverina, I. (1999). Functional design in the actin cytoskeleton. Curr. Opin. Cell Biol. 11, 54-60.
50. 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.
51. Stephens, L., Smrcka, A., Cooke, F. T., Jackson, T. R., Sternweis, P. C. and Hawkins, P. T. (1994). A novel phosphoinositide 3 kinase activity in myeloid-derived cells is activated by G protein βγ subunits. Cell 77, 83-93.
52. Stoyanov, B., Volinia, S., Hanck, T., Rubio, I., Loubtchenkov, M., Malek, D., Stoyanova, S., Vanhaesebroeck, B., Dhand, R., Nurnberg, B., Gierschik, P., Seedorf, K., Hsuan, J. J., Waterfield, M. D. and Wetzker, R. (1995). Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 269, 690-693.
53. Tomiyama, K., Nakata, H., Sasa, H., Arimura, S., Nishio, E. and Watanabe, Y. (1995). Wortmannin, a specific phosphatidylinositol 3-kinase inhibitor, inhibits adipocytic differentiation of 3T3-L1 cells. Biochem. Biophys Res. Commun. 212, 263-269.
54. Vanhaesebroeck, B., Leevers, S. J., Panayotou, G. and Waterfield, M. D. (1997a). Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem. Sci. 22, 267-272.
55. Vanhaesebroeck, B., Welham, M. J., Kotani, K., Stein, R., Warne, P. H., Zvelebil, M. J., Higashi, K., Volinia, S., Downward, J. and Waterfield, M. D. (1997b). P110δ, a novel phosphoinositide 3-kinase in leukocytes. Proc. Nat. Acad. Sci. USA 94, 4330-4335.
56. Vanhaesebroeck, B., Jones, G. E., Allen, W. E., Zicha, D., Hooshmand-Rad, R., Sawyer, C., Wells, C., Waterfield, M. D. and Ridley, A. J. (1999a). Distinct PI(3)Ks mediate mitogenic signalling and cell migration in macrophages. Nature Cell Biol. 1, 69-71.
57. Vanhaesebroeck, B., Higashi, K., Raven, C., Welham, M., Anderson, S., Brennan, P., Ward, S. G. and Waterfield, M. D. (1999b). Autophosphorylation of p110δ phosphoinositide 3-kinase: a new paradigm for the regulation of lipid kinases in vitro and in vivo. EMBO J. 18, 1292-1302.
58. Wang, J., Auger, K. R., Jarvis, L., Shi, Y. and Roberts, T. M. (1995). Direct association of Grb2 with the p85 subunit of phosphatidylinositol 3-kinase. J. Biol. Chem. 270, 12774-12780.
59. Wang, Q., Bilan, P. J., Tsakiridis, T., Hinek, A. and Klip, A. (1998). Actin filaments participate in the relocalization of phosphatidylinositol 3-kinase to glucose transporter-containing compartments and in the stimulation of glucose uptake in 3T3-L1 adipocytes. Biochem. J. 331, 917-928.
60. Wennström, S., Hawkins, P., Cooke, F., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T., Claesson-Welsh, L. and Stephens, L. (1994a). Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393.
61. Wennström, S., Siegbahn, A., Yokote, K., Arvidsson, A. K., Heldin, C. H., Mori, S. and Claesson-Welsh, L. (1994b). Membrane ruffling and chemotaxis transduced by the PDGF β-receptor require the binding site for phosphatidylinositol 3′ kinase. Oncogene 9, 651-660.
62. Yao, R. and Cooper, G. M. (1995). Requirement for phosphatidylinositol-3 kinase in the prevention of apoptosis by nerve growth factor. Science 267, 2003-2006.
63. Yuan, Z. M., Utsugisawa, T., Huang, Y., Ishiko, T., Nakada, S., Kharbanda, S., Weichselbaum, R. and Kufe, D. (1997). Inhibition of phosphatidylinositol 3-kinase by c-Abl in the genotoxic stress response. J. Biol. Chem. 272, 23485-23488.