Regulation of the activity of the tumor suppressor PTEN by thioredoxin in Drosophila melanogaster

Experimental Cell Research

Volumn 313, Issue 6, 2007, Pages 1161-1171

  Song, Zuohe ^a,b   Saghafi, Negin ^a   Gokhale, Vijay ^a   Brabant, Marc ^a   Meuillet, Emmanuelle J ^a,b,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c University of Arizona   (United States)

Author keywords

Akt; Drosophila; Eye development; PTEN; Thioredoxin

Indexed keywords

CYSTEINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; THIOREDOXIN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DISULFIDE BOND; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EYE DEVELOPMENT; GENE OVEREXPRESSION; NONHUMAN; OXIDATION REDUCTION REACTION; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM;

DROSOPHILA MELANOGASTER; MAMMALIA;

EID: 33947277986     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.01.004     Document Type: Article

References (42)

1. Alessi D.R., and Cohen P. Mechanism of activation and function of protein kinase B. Curr. Opin. Genet. Dev. 8 (1998) 55-62
2. Meuillet E.J., Mahadevan D., Berggren M., Coon A., and Powis G. Thioredoxin-1 binds to the C2 domain of PTEN inhibiting PTEN's lipid phosphatase activity and membrane binding: a mechanism for the functional loss of PTEN's tumor suppressor activity. Arch. Biochem. Biophys. 429 (2004) 123-133
3. Leevers S.J., Weinkove D., MacDougall L.K., Hafen E., and Waterfield M.D. The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J. 15 (1996) 6584-6594
4. Verdu J., Buratovich M.A., Wilder E.L., and Birnbaum M.J. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. (see comment). Nat. Cell Biol. 1 (1999) 500-506
5. Weinkove D., Neufeld T.P., Twardzik T., Waterfield M.D., and Leevers S.J. Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor. (erratum appears in Curr Biol 1999 Nov 18;9(22):R867). Curr. Biol. 9 (1999) 1019-1029
6. Huang H., Potter C.J., Tao W., Li D.M., Brogiolo W., Hafen E., Sun H., and Xu T. PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126 (1999) 5365-5372
7. Oldham S., Stocker H., Laffargue M., Wittwer F., Wymann M., and Hafen E. The Drosophila insulin/IGF receptor controls growth and size by modulating PtdInsP(3) levels. Development 129 (2002) 4103-4109
8. Stocker H., Andjelkovic M., Oldham S., Laffargue M., Wymann M.P., Hemmings B.A., and Hafen E. Living with lethal PIP3 levels: viability of flies lacking PTEN restored by a PH domain mutation in Akt/PKB. Science 295 (2002) 2088-2091
9. Goberdhan D.C., Paricio N., Goodman E.C., Mlodzik M., and Wilson C. Drosophila tumor suppressor PTEN controls cell size and number by antagonizing the Chico/PI3-kinase signaling pathway. Genes Dev. 13 (1999) 3244-3258
10. Gao X., Neufeld T.P., and Pan D. Drosophila PTEN regulates cell growth and proliferation through PI3K-dependent and -independent pathways. Dev. Biol. 221 (2000) 404-418
11. Tagaya Y., Wakasugi H., Masutani H., Nakamura H., Iwata S., Mitsui A., Fujii S., Wakasugi N., Tursz T., and Yodoi J. Role of ATL-derived factor (ADF) in the normal and abnormal cellular activation: involvement of dithiol related reduction. Mol. Immunol. 27 (1990) 1279-1289
12. Holmgren N. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264 (1989) 13963-13966
13. Hirota K., Murata M., Sachi Y., Nakamura H., Takeuchi J., Mori K., and Yodoi J. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J. Biol. Chem. 274 (1999) 27891-27897
14. Schenk H., Klein M., Erdbrugger W., Droge W., and Schulze-Osthoff K. Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 1672-1676
15. Watson J.A., Rumsby M.G., and Wolowacz R.G. Phage display identifies thioredoxin and superoxide dismutase as novel protein kinase C-interacting proteins: thioredoxin inhibits protein kinase C-mediated phosphorylation of histone. Biochem. J. 343 Pt. 2 (1999) 301-305
16. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., and Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17 (1998) 2596-2606
17. Kakolyris S., Giatromanolaki A., Koukourakis M., Powis G., Souglakos J., Sivridis E., Georgoulias V., Gatter K.C., and Harris A.L. Thioredoxin expression is associated with lymph node status and prognosis in early operable non-small cell lung cancer. Clin. Cancer Res. 7 (2001) 3087-3091
18. Fujii S., Nanbu Y., Nonogaki H., Konishi I., Mori T., Masutani H., and Yodoi J. Coexpression of adult T-cell leukemia-derived factor, a human thioredoxin homologue, and human papillomavirus DNA in neoplastic cervical squamous epithelium. Cancer 68 (1991) 1583-1591
19. Nakamura H., Bai J., Nishinaka Y., Ueda S., Sasada T., Ohshio G., Imamura M., Takabayashi A., Yamaoka Y., and Yodoi J. Expression of thioredoxin and glutaredoxin, redox-regulating proteins, in pancreatic cancer. Cancer Detect. Prev. 24 (2000) 53-60
20. Nakamura H., Masutani H., Tagaya Y., Yamauchi A., Inamoto T., Nanbu Y., Fujii S., Ozawa K., and Yodoi J. Expression and growth-promoting effect of adult T-cell leukemia-derived factor. A human thioredoxin homologue in hepatocellular carcinoma. Cancer 69 (1992) 2091-2097
21. Grogan T.M., Fenoglio-Prieser C., Zeheb R., Bellamy W., Frutiger Y., Vela E., Stemmerman G., Macdonald J., Richter L., Gallegos A., and Powis G. Thioredoxin, a putative oncogene product, is overexpressed in gastric carcinoma and associated with increased proliferation and increased cell survival. Hum. Pathol. 31 (2000) 475-481
22. Raffel J., Bhattacharyya A.K., Gallegos A., Cui H., Einspahr J.G., Alberts D.S., and Powis G. Increased expression of thioredoxin-1 in human colorectal cancer is associated with decreased patient survival. (see comment). J. Lab. Clin. Med. 142 (2003) 46-51
23. Svensson M.J., Chen J.D., Pirrotta V., and Larsson J. The ThioredoxinT and deadhead gene pair encode testis- and ovary-specific thioredoxins in Drosophila melanogaster. Chromosoma 112 (2003) 133-143
24. Bauer H., Kanzok S.M., and Schirmer R.H. Thioredoxin-2 but not thioredoxin-1 is a substrate of thioredoxin peroxidase-1 from Drosophila melanogaster: isolation and characterization of a second thioredoxin in D. melanogaster and evidence for distinct biological functions of Trx-1 and Trx-2. J. Biol. Chem. 277 (2002) 17457-17463
25. Wahl M.C., Irmler A., Hecker B., Schirmer R.H., and Becker K. Comparative structural analysis of oxidized and reduced thioredoxin from Drosophila melanogaster. J. Mol. Biol. 345 (2005) 1119-1130
26. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
27. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87 (1996) 651-660
28. Quiring R., Walldorf U., Kloter U., and Gehring W.J. Homology of the eyeless gene of Drosophila to the small eye gene in mice and Aniridia in humans. (see comment). Science 265 (1994) 785-789
29. Halder G., Callaerts P., Flister S., Walldorf U., Kloter U., and Gehring W.J. Eyeless initiates the expression of both sine oculis and eyes absent during Drosophila compound eye development. Development 125 (1998) 2181-2191
30. Hay B.A., Maile R., and Rubin G.M. P element insertion-dependent gene activation in the Drosophila eye. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 5195-5200
31. Raftopoulou M., Etienne-Manneville S., Self A., Nicholls S., and Hall A. Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science 303 (2004) 1179-1181
32. Lee J.O., Yang H., Georgescu M.M., Di Cristofano A., Maehama T., Shi Y., Dixon J.E., Pandolfi P., and Pavletich N.P. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 99 (1999) 323-334
33. Weichsel A., Gasdaska J.R., Powis G., and Montfort W.R. Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer. Structure 4 (1996) 735-751
34. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
35. Reynolds R.A., Yem A.W., Wolfe C.L., Deibel Jr. M.R., Chidester C.G., and Watenpaugh K.D. Crystal structure of the catalytic subunit of Cdc25B required for G2/M phase transition of the cell cycle. J. Mol. Biol. 293 (1999) 559-568
36. Jorgensen W.L.C., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
37. Gasdaska J.R., Kirkpatrick D.L., Montfort W., Kuperus M., Hill S.R., Berggren M., and Powis G. Oxidative inactivation of thioredoxin as a cellular growth factor and protection by a Cys73->Ser mutation. Biochem. Pharmacol. 52 (1996) 1741-1747
38. Powis G., Kirkpatrick D.L., Angulo M., and Baker A. Thioredoxin redox control of cell growth and death and the effects of inhibitors. Chem.-Biol. Interact. 111-112 (1998) 23-34
39. Powis G., Mustacich D., and Coon A. The role of the redox protein thioredoxin in cell growth and cancer. Free Rad. Biol. Med. 29 (2000) 312-322
40. Smith A., Smith A., Alrubaie S., Coehlo C., Leevers S.J., and Ashworth A. Alternative splicing of the Drosophila PTEN gene. Biochim. Biophys. Acta 1447 (1999) 313-317
41. Maehama T., Kosaka N., Okahara F., Takeuchi K., Umeda M., Dixon J.E., and Kanaho Y. Suppression of a phosphatidylinositol 3-kinase signal by a specific spliced variant of Drosophila PTEN. FEBS Lett. 565 (2004) 43-47
42. Seong K.H., Ogashiwa T., Matsuo T., Fuyama Y., and Aigaki T. Application of the gene search system to screen for longevity genes in Drosophila. Biogerontology 2 3 (2001) 209-217