Sulfiredoxin is an AP-1 target gene that is required for transformation and shows elevated expression in human skin malignancies

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 50, 2008, Pages 19738-19743

  Wei, Qiou ^a   Jiang, Hong ^a   Matthews, Connie P ^a   Colburn, Nancy H ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Peroxiredoxin; Skin tumor; Tumor promotion

Indexed keywords

OXIDOREDUCTASE; PEROXIREDOXIN; PROTEIN C JUN; SHORT HAIRPIN RNA; SULFIREDOXIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; CYSTEINE; PEPTIDE FRAGMENT; PEROXIDE; SMALL INTERFERING RNA; SRXN1 PROTEIN, HUMAN; TAM67 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; BASAL CELL CARCINOMA; CONTROLLED STUDY; FEEDBACK SYSTEM; HOMEOSTASIS; HUMAN; HUMAN TISSUE; MELANOMA; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SQUAMOUS CELL CARCINOMA; SWEAT GLAND CARCINOMA; TISSUE MICROARRAY; ANIMAL; APOPTOSIS; CELL TRANSFORMATION; DNA MICROARRAY; EPIDERMIS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROMOTER REGION; SKIN TUMOR;

ANIMALS; APOPTOSIS; CELL TRANSFORMATION, NEOPLASTIC; CYSTEINE; EPIDERMIS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; OXIDOREDUCTASES; PEPTIDE FRAGMENTS; PEROXIDES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-JUN; RNA, SMALL INTERFERING; SKIN NEOPLASMS; TRANSCRIPTION FACTOR AP-1;

EID: 58149393166     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0810676105     Document Type: Article

References (42)

1. Angel P, Hattori K, Smeal T, Karin M (1988) The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1 Cell 55:875-885.
2. Saez E, et al. (1995) c-fos is required for malignant progression of skin tumors. Cell 82:721-732.
3. Zenz R, et al. (2003). c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev Cell 4:879-889.
4. Lloyd A, Yancheva N, Wasylyk B (1991) Transformation suppressor activity of a Jun transcription factor lacking its activation domain. Nature 352:635-638.
5. Dong Z, Birrer MJ, Watts RG, Matrisian LM, Colburn NH (1994) Blocking of tumor promoter-induced AP-1 activity inhibits induced transformation in JB6 mouse epidermal cells. Proc Natl Acad Sci USA 91:609-613.
6. Young MR, et al. (1999) Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc Natl Acad Sci USA 96:9827-9832.
7. Shen Q, et al. (2008). Targeting the activator protein 1 transcription factor for the prevention of estrogen receptor-negative mammary tumors. Cancer Prev Res 1, first published on line March 31, 2008, 2010.1158/1940-6207.CAPR-2008-0034.
8. Bernstein LR, Colburn NH (1989) AP1/jun function is differentially induced in promotion-sensitive and resistant JB6 cells. Science 244:566-569.
9. Matthews CP, et al. (2007) Dominant-negative activator protein 1 (TAM67) targets cyclooxygenase-2 and osteopontin under conditions in which it specifically inhibits tumorigenesis. Cancer Res 67:2430-2438.
10. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980-984.
11. Chang TS, et al. (2004) Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J Biol Chem 279:50994-51001.
12. Colburn NH, et al. (1978) Correlation of anchorage-independent growth with tumorigenicity of chemically transformed mouse epidermal cells. Cancer Res 38:624-634.
13. Sun Y, Hegamyer G, Colburn NH (1994) Molecular cloning of five messenger RNAs differentially expressed in preneoplastic or neoplastic JB6 mouse epidermal cells: one is homologous to human tissue inhibitor of metalloproteinases-3. Cancer Res 54:1139-1144.
14. Lee SC, et al. (2000) Peroxiredoxin is ubiquitously expressed in rat skin: isotype-specific expression in the epidermis and hair follicle. J Invest Dermatol 115:1108-1114.
15. Lee W, Mitchell P, Tjian R (1987) Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell 49:741-752.
16. Woo HA, et al. (2005) Reduction of cysteine sulfinic acid by sulfiredoxin is specific to 2-cys peroxiredoxins. J Biol Chem 280:3125-3128.
17. Freedman VH, Shin SI (1974) Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 3:355-359.
18. Minden A, et al. (1994). Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719-1723.
19. Hilberg F, Aguzzi A, Howells N, Wagner EF (1993) c-jun is essential for normal mouse development and hepatogenesis. Nature 365:179-181.
20. Johnson RS, van Lingen B, Papaioannou VE, Spiegelman BM (1993) A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev 7:1309-1317.
21. Jain PT, et al. (1994) Differential cytotoxicity in mouse epidermal JB6 cells: a potential mechanism for oxidant tumor promotion. Mol Carcinog 11:164-169.
22. Tavender TJ, Sheppard AM, Bulleid NJ (2008) Peroxiredoxin IV is an endoplasmic reticulum-localized enzyme forming oligomeric complexes in human cells. Biochem J 411:191-199.
23. Choi MH, et al. (2005). Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II. Nature 435:347-353.
24. Prosperi MT, Ferbus D, Karczinski I, Goubin G (1993) A human cDNA corresponding to a gene overexpressed during cell proliferation encodes a product sharing homology with amoebic and bacterial proteins. J Biol Chem 268:11050-11056.
25. Prosperi MT, Ferbus D, Rouillard D, Goubin G (1998) The pag gene product, a physiological inhibitor of c-abl tyrosine kinase, is overexpressed in cells entering S phase and by contact with agents inducing oxidative stress. FEBS Lett 423:39-44.
26. Neumann CA, et al. (2003) Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424:561-565.
27. Egler RA, et al. (2005) Regulation of reactive oxygen species, DNA damage, and c-Myc function by peroxiredoxin 1. Oncogene 24:8038-8050.
28. Mu ZM, Yin XY, Prochownik EV (2002) Pag, a putative tumor suppressor, interacts with the Myc Box II domain of c-Myc and selectively alters its biological function and target gene expression. J Biol Chem 277:43175-43184.
29. Jang HH, et al. (2004) Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117:625-635.
30. Moon JC, et al. (2005) Oxidative stress-dependent structural and functional switching of a human 2-Cys peroxiredoxin isotype II that enhances HeLa cell resistance to H2O2-induced cell death. J Biol Chem 280:28775-28784.
31. Jeong W, Park SJ, Chang TS, Lee DY, Rhee SG (2006) Molecular mechanism of the reduction of cysteine sulfinic acid of peroxiredoxin to cysteine by mammalian sulfiredoxin. J Biol Chem 281:14400-14407.
32. Jonsson TJ, Johnson LC, Lowther WT (2008) Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451:98-101.
33. Bozonet SM, et al. (2005) Oxidation of a eukaryotic 2-Cys peroxiredoxin is a molecular switch controlling the transcriptional response to increasing levels of hydrogen peroxide. J Biol Chem 280:23319-23327.
34. Rey P, et al. (2007) The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J 49:505-514.
35. Kang SW, et al. (2004) Cytosolic peroxiredoxin attenuates the activation of Jnk and p38 but potentiates that of Erk in Hela cells stimulated with tumor necrosis factor-alpha. J Biol Chem 279:2535-2543.
36. Kim YJ, et al. (2006) Prx1 suppresses radiation-induced c-Jun NH2-terminal kinase signaling in lung cancer cells through interaction with the glutathione S-transferase Pi/c-Jun NH2-terminal kinase complex. Cancer Res 66:7136-7142.
37. Yang S, Misner BJ, Chiu RJ, Meyskens FL, Jr. (2007) Redox effector factor-1, combined with reactive oxygen species, plays an important role in the transformation of JB6 cells. Carcinogenesis 28:2382-2390.
38. Vivancos AP, et al. (2005) A cysteine-sulfinic acid in peroxiredoxin regulates H2O2-sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci USA 102:8875-8880.
39. Findlay VJ, et al. (2006) A novel role for human sulfiredoxin in the reversal of glutathionylation. Cancer Res 66:6800-6806.
40. Lei K, Townsend DM, Tew KD (2008) Protein cysteine sulfinic acid reductase (sulfiredoxin) as a regulator of cell proliferation and drug response. Oncogene 27:4877-4887.
41. Kang SW, Rhee SG, Chang TS, Jeong W, Choi MH (2005) 2-Cys peroxiredoxin function in intracellular signal transduction: therapeutic implications. Trends Mol Med 11:571-578.
42. Reynolds A, et al. (2004) Rational siRNA design for RNA interference. Nat Biotechnol 22:326-330.