Redox regulation of PI 3-kinase signalling via inactivation of PTEN

EMBO Journal

Volumn 22, Issue 20, 2003, Pages 5501-5510

  Leslie, Nick R ^a   Bennett, Deborah ^a   Lindsay, Yvonne E ^a   Stewart, Hazel ^a   Gray, Alex ^a   Downes, C Peter ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Oxidative stress; Phosphatase; Phosphoinositide 3 kinase; PTEN; Redox signalling

Indexed keywords

HYDROGEN PEROXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; DISULFIDE BOND; ENZYME ACTIVE SITE; ENZYME INACTIVATION; ENZYME REGULATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FAMILY; TUMOR SUPPRESSOR GENE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE; CLONING, MOLECULAR; ESCHERICHIA COLI; GENES, TUMOR SUPPRESSOR; HUMANS; MACROPHAGES; MICE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHORIC MONOESTER HYDROLASES; PTEN PHOSPHOHYDROLASE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 0142137134     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg513     Document Type: Article

References (61)

1. Ahmed, N., Kansara, M. and Berridge, M.V. (1997) Acute regulation of glucose transport in a monocyte-macrophage cell line: glut-3 affinity for glucose is enhanced during the respiratory burst. Biochem. J., 327, 369-375.
2. Alessi, D.R., Andjelkovic, M., Caudwell, B., Cron, P., Morrice, N., Cohen, P. and Hemmings, B.A. (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J., 15, 6541-6551.
3. Ali, I.U., Schriml, L.M. and Dean, M. (1999) Mutational spectra of PTEN/ MMAC1 gene: a tumor suppressor with lipid phosphatase activity. J. Natl Cancer Inst., 91, 1922-1932.
4. Babior, B.M. (1999) NADPH oxidase: an update. Blood, 93, 1464-1476.
5. Backman, S., Stambolic, V. and Mak, T. (2002) PTEN function in mammalian cell size regulation. Curr. Opin. Neurobiol., 12, 516-522.
6. Bae, Y.S., Kang, S.W., Seo, M.S., Baines, I.C., Tekle, E., Chock, P.B. and Rhee, S.G. (1997) Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem., 272, 217-221.
7. Benhar, M., Engelberg, D. and Levitzki, A. (2002) ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep., 3, 420-425.
8. Birle, D., Bottini, N., Williams, S., Huynh, H., deBelle, I., Adamson, E. and Mustelin, T. (2002) Negative feedback regulation of the tumor suppressor PTEN by phosphoinositide-induced serine phosphorylation. J. Immunol., 169, 286-291.
9. Brune, B., Gotz, C., Messmer, U.K., Sandau, K., Hirvonen, M.R. and Lapetina, E.G. (1997) Superoxide formation and macrophage resistance to nitric oxide-mediated apoptosis. J. Biol. Chem., 272, 7253-7258.
10. Burgering, B.M. and Kops, G.J. (2002) Cell cycle and death control: long live Forkheads. Trends Biochem. Sci., 27, 352-360.
11. Cadwallader, K.A., Condliffe, A.M., McGregor, A., Walker, T.R., White, J.F., Stephens, L.R. and Chilvers, E.R. (2002) Regulation of phosphatidylinositol 3-kinase activity and phosphatidylinositol 3,4,5-trisphosphate accumulation by neutrophil priming agents. J. Immunol., 169, 3336-3344.
12. Cantley, L.C. (2002) The phosphoinositide 3-kinase pathway. Science, 296, 1655-1657.
13. Cantrell, D.A. (2001) Phosphoinositide 3-kinase signalling pathways. J. Cell Sci., 114, 1439-1445.
14. Chen, Q., Olashaw, N. and Wu, J. (1995) Participation of reactive oxygen species in the lysophosphatidic acid-stimulated mitogen-activated protein kinase kinase activation pathway. J. Biol. Chem., 270, 28499-28502.
15. Das, S., Dixon, J.E. and Cho, W. (2003) Membrane-binding and activation mechanism of PTEN. Proc. Natl Acad. Sci. USA, 100, 7491-7496.
16. Davies, M.A., Kim, S.J., Parikh, N.U., Dong, Z., Bucana, C.D. and Gallick, G.E. (2002) Adenoviral-mediated expression of MMAC/ PTEN inhibits proliferation and metastasis of human prostate cancer cells. Clin. Cancer Res., 8, 1904-1914.
17. Denu, J.M. and Tanner, K.G. (1998) Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry, 37, 5633-5642.
18. Droge, W. (2002) Free radicals in the physiological control of cell function. Physiol. Rev., 82, 47-95.
19. Finkel, T. (1998) Oxygen radicals and signaling. Curr. Opin. Cell Biol., 10, 248-253.
20. Finkel, T. (2000) Redox-dependent signal transduction. FEBS Lett., 476, 52-54.
21. Furnari, F.B., Huang, H.J. and Cavenee, W.K. (1998) The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res., 58, 5002-5008.
22. Gems, D. and Partridge, L. (2001) Insulin/IGF signalling and ageing: seeing the bigger picture. Curr. Opin. Genet. Dev., 11, 287-292.
23. 2 and nitric oxide in inducible nitric oxide synthase expression in macrophages. Nitric Oxide, 5, 504-513.
24. Holzenberger, M., Dupont, J., Ducos, B., Leneuve, P., Geloen, A., Even, P.C., Cervera, P. and Le Bouc, Y. (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature, 421, 182-187.
25. Katso, R., Okkenhaug, K., Ahmadi, K., White, S., Timms, J. and Waterfield, M.D. (2001) Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis and cancer. Annu. Rev. Cell. Dev. Biol., 17, 615-675.
26. Lee, S.R., Kwon, K.S., Kim, S.R. and Rhee, S.G. (1998) Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem., 273, 15366-15372.
27. 2. J. Biol. Chem., 277, 20336-20342.
28. Leslie, N.R. and Downes, C.P. (2002) PTEN: the down side of PI 3-kinase signalling. Cell Signal, 14, 285-295.
29. Leslie, N.R., Bennett, D., Gray, A., Pass, I., Hoang-Xuan, K. and Downes, C.P. (2001) Targeting mutants of PTEN reveal distinct subsets of tumour suppressor functions. Biochem. J., 357, 427-435.
30. Liu, H., Perlman, H., Pagliari, L.J. and Pope, R.M. (2001) Constitutively activated Akt-1 is vital for the survival of human monocyte-differentiated macrophages. Role of Mcl-1, independent of nuclear factor (NF)-κB, Bad, or caspase activation. J. Exp. Med., 194, 113-126.
31. Maehama, T. and Dixon, J.E. (1998) The tumor suppressor, PTEN/ MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem., 273, 13375-13378.
32. Maehama, T., Taylor, G.S. and Dixon, J.E. (2001) PTEN and myotubularin: novel phosphoinositide phosphatases. Annu. Rev. Biochem., 70, 247-279.
33. McConnachie, G., Pass, I., Walker, S.M. and Downes, C.P. (2003) Interfacial kinetic analysis of the tumour suppressor phosphatase, PTEN: evidence for activation by anionic phospholipids. Biochem. J., 371, 947-955.
34. Meng, T.C., Fukada, T. and Tonks, N.K. (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell, 9, 387-399.
35. Migliaccio, E., Giorgio, M., Mele, S., Pelicci, G., Reboldi, P., Pandolfi, P.P., Lanfrancone, L. and Pelicci, P.G. (1999) The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature, 402, 309-313.
36. Monick, M.M., Carter, A.B., Robeff, P.K., Flaherty, D.M., Peterson, M.W. and Hunninghake, G.W. (2001) Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumulation and transcriptional activity of β-catenin. J. Immunol., 166, 4713-4720.
37. Myers, M.P., Pass, I., Batty, I.H., Van der Kaay, J., Stolarov, J.P., Hemmings, B.A., Wigler, M.H., Downes, C.P. and Tonks, N.K. (1998) The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc. Natl Acad. Sci. USA, 95, 13513-13518.
38. Nemoto, S. and Finkel, T. (2002) Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science, 295, 2450-2452.
39. Patel, L., Pass, I., Coxon, P., Downes, C.P., Smith, S.A. and Macphee, C.H. (2001) Tumor suppressor and anti-inflammatory actions of PPARγ agonists are mediated via upregulation of PTEN. Curr. Biol., 11, 764-768.
40. Pfeiffer, S., Lass, A., Schmidt, K. and Mayer, B. (2001) Protein tyrosine nitration in cytokine-activated murine macrophages. Involvement of a peroxidase/nitrite pathway rather than peroxynitrite. J. Biol. Chem., 276, 34051-34058.
41. Salh, B., Wagey, R., Marotta, A., Tao, J.S. and Pelech, S. (1998) Activation of phosphatidylinositol 3-kinase, protein kinase B and p70 S6 kinases in lipopolysaccharide-stimulated Raw 264.7 cells: differential effects of rapamycin, Ly294002 and wortmannin on nitric oxide production. J. Immunol., 161, 6947-6954.
42. Seo, Y.R., Kelley, M.R. and Smith, M.L. (2002) Selenomethionine regulation of p53 by a ref1-dependent redox mechanism. Proc. Natl Acad. Sci. USA, 99, 14548-14553.
43. Simpson, L. and Parsons, R. (2001) PTEN: life as a tumor suppressor. Exp. Cell Res., 264, 29-41.
44. Splettstoesser, W.D. and Schuff-Werner, P. (2002) Oxidative stress in phagocytes-'the enemy within'. Microsc. Res. Tech., 57, 441-455.
45. Stambolic, V. et al. (1998) Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell, 95, 29-39.
46. Sun, H. et al. (1999) PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/ protein kinase B signaling pathway. Proc. Natl Acad. Sci. USA, 96, 6199-6204.
47. 2 for platelet-derived growth factor signal transduction. Science, 270, 296-299.
48. Tamura, M., Gu, J., Matsumoto, K., Aota, S., Parsons, R. and Yamada, K.M. (1998) Inhibition of cell migration, spreading and focal adhesions by tumor suppressor PTEN. Science, 280, 1614-1617.
49. Tonks, N.K. and Neel, B.G. (2001) Combinatorial control of the specificity of protein tyrosine phosphatases. Curr. Opin. Cell Biol., 13, 182-195.
50. Torres, J. and Pulido, R. (2001) The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J. Biol. Chem., 276, 993-998.
51. Trinei, M. et al. (2002) A p53-p66Shc signalling pathway controls intracellular redox status, levels of oxidation-damaged DNA and oxidative stress-induced apoptosis. Oncogene, 21, 3872-3878.
52. 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.
53. 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
54. Vazquez, F., Ramaswamy, S., Nakamura, N. and Sellers, W.R. (2000) Phosphorylation of the PTEN tail regulates protein stability and function. Mol. Cell. Biol., 20, 5010-5018.
55. Virolle, T., Adamson, E.D., Baron, V., Birle, D., Mercola, D., Mustelin, T. and de Belle, I. (2001) The Egr-1 transcription factor directly activates PTEN during irradiation-induced signalling. Nat. Cell Biol., 3, 1124-1128.
56. Walker, K.S., Deak, M., Paterson, A., Hudson, K., Cohen, P. and Alessi, D.R. (1998) Activation of protein kinase B β and γ isoforms by insulin in vivo and by 3-phosphoinositide-dependent protein kinase-1 in vitro: comparison with protein kinase Bα. Biochem. J., 331, 299-308.
57. Walker, S.M., Downes, C.P. and Leslie, N. R. (2001) TPIP: a novel phosphoinositide 3-phosphatase. Biochem. J., 360, 277-283.
58. Welch, H.C., Coadwell, W.J., Ellson, C.D., Ferguson, G.J., Andrews, S.R., Erdjument-Bromage, H., Tempst, P., Hawkins, P.T. and Stephens, L.R. (2002) P-Rex1, a PtdIns(3,4,5)P3- and Gβγ-regulated guanine-nucleotide exchange factor for Rac. Cell, 108, 809-821.
59. Wu, H.H. and Momand, J. (1998) Pyrrolidine dithiocarbamate prevents p53 activation and promotes p53 cysteine residue oxidation. J. Biol. Chem., 273, 18898-18905.
60. Wu, X. et al. (2000) Evidence for regulation of the PTEN tumor suppressor by a membrane- localized multi-PDZ domain containing scaffold protein MAGI-2. Proc. Natl Acad. Sci. USA, 97, 4233-4238.
61. Wu, Y., Dowbenko, D., Spencer, S., Laura, R., Lee, J., Gu, Q. and Lasky, L.A. (2000) Interaction of the tumor suppressor PTEN/ MMAC with a PDZ domain of MAGI3, a novel membrane-associated guanylate kinase. J. Biol. Chem., 275, 21477-21485.