A dominant-negative c-jun mutant inhibits lung carcinogenesis in mice

Cancer Prevention Research

Volumn 3, Issue 9, 2010, Pages 1148-1156

  Tichelaar, Jay W ^a   Yan, Ying ^a   Tan, Qing ^a   Wang, Yian ^a   Estensen, Richard D ^b   Young, Matthew R ^c   Colburn, Nancy H ^c   Yin, Hulian ^d   Goodin, Colleen ^e   Anderson, Marshall W ^e   You, Ming ^a  

^a USA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CINCINNATI   (United States)

^e UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; MUTANT PROTEIN; PROTEIN C JUN; PROTEIN TAM67; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; GENE INDUCTION; LUNG ALVEOLUS EPITHELIUM; LUNG CANCER; LUNG CARCINOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; BENZO(A)PYRENE; CARCINOGENS; CARCINOMA; CELL TRANSFORMATION, NEOPLASTIC; CYTOPROTECTION; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, DOMINANT; GENES, JUN; GENES, TUMOR SUPPRESSOR; LUNG NEOPLASMS; MICE; MICE, TRANSGENIC; MUTANT PROTEINS; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS C-JUN; TRANSCRIPTION FACTOR AP-1;

EID: 77956408222     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-10-0023     Document Type: Article

References (55)

1. Shaulian E, Karin M. AP-1 in cell proliferation and survival. Oncogene 2001;20:2390-400.
2. Wisdom R, Johnson RS, Moore C. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. EMBO J 1999;18:188-97. (Pubitemid 29005035)
3. Sato H, Seiki M. Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene 1993;8:395-405.
4. Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 2003;3:859-68.
5. 2/M arrest in a p53-deficient human lung cancer cell. Biochem Biophys Res Commun 2002;293:1248-53.
6. Zoumpourlis V, Papassava P, Linardopoulos S, Gillespie D, Balmain A, Pintzas A. High levels of phosphorylated c-Jun, Fra-1, Fra-2 and ATF-2 proteins correlate with malignant phenotypes in the multistage mouse skin carcinogenesis model. Oncogene 2000;19:4011-21.
7. Urakami S, Tsuchiya H, Orimoto K, Kobayashi T, Igawa M, Hino O. Overexpression of members of the AP-1 transcriptional factor family from an early stage of renal carcinogenesis and inhibition of cell growth by AP-1 gene antisense oligonucleotides in the Tsc2 gene mutant (Eker) rat model. Biochem Biophys Res Commun 1997;241:24-30. (Pubitemid 28033533)
8. Ostrowski J, Woszczynski M, Kowalczyk P, et al. Increased activity of MAP, p70S6 and p90rs kinases is associated with AP-1 activation in spontaneous liver tumours, but not in adjacent tissue in mice. Br J Cancer 2000;82:1041-50.
9. Battista S, de Nigris F, Fedele M, et al. Increase in AP-1 activity is a general event in thyroid cell transformation in vitro and in vivo. Oncogene 1998;17:377-85.
10. Wong YC, Bernal SD. Expression of enhancer binding factors associated with various cell types of lung cancer. Biochem Biophys Res Commun 1991;180:1064-9.
11. Szabo E, Riffe ME, Steinberg SM, Birrer MJ, Linnoila RI. Altered cJUN expression: an early event in human lung carcinogenesis. Cancer Res 1996;56:305-15. (Pubitemid 26026359)
12. Volm M, Drings P, Wodrich W. Prognostic significance of the expression of c-fos, c-jun and c-erbB-1 oncogene products in human squamous cell lung carcinomas. J Cancer Res Clin Oncol 1993;119:507-10.
13. Volm M, Drings P, Wodrich W, van Kaick G. Expression of oncoproteins in primary human non-small cell lung cancer and incidence of metastases. Clin Exp Metastasis 1993;11:325-9. (Pubitemid 23195956)
14. Wodrich W, Volm M. Overexpression of oncoproteins in non-small cell lung carcinomas of smokers. Carcinogenesis 1993;14:1121-4.
15. Mattern J, Koomagi R, Volm M. Characteristics of long-term survivors of untreated lung cancer. Lung Cancer 2002;36:277-82.
16. Volm M, Koomagi R, Mattern J, Efferth T. Expression profile of genes in non-small cell lung carcinomas from long-term surviving patients. Clin Cancer Res 2002;8:1843-8. (Pubitemid 34633744)
17. Wattenberg LW, Wiedmann TS, Estensen RD, et al. Chemoprevention of pulmonary carcinogenesis by brief exposures to aerosolized budesonide or beclomethasone dipropionate and by the combination of aerosolized budesonide and dietary myo-inositol. Carcinogenesis 2000;21:179-82.
18. Wattenberg LW, Wiedmann TS, Estensen RD, Zimmerman CL, Steele VE, Kelloff GJ. Chemoprevention of pulmonary carcinogenesis by aerosolized budesonide in female A/J mice. Cancer Res 1997;57:5489-92.
19. Park AM, Dong Z. Signal transduction pathways: targets for green and black tea polyphenols. J Biochem Mol Biol 2003;36:66-77.
20. Zhang Z, Liu Q, Lantry LE, et al. A germ-line p53 mutation accelerates pulmonary tumorigenesis: p53-independent efficacy of chemopreventive agents green tea or dexamethasone/myo-inositol and chemotherapeutic agents taxol or adriamycin. Cancer Res 2000;60:901-7.
21. Yu R, Hebbar V, Kim DW, Mandlekar S, Pezzuto JM, Kong AN. Resveratrol inhibits phorbol ester and UV-induced activator protein 1 activation by interfering with mitogen-activated protein kinase pathways. Mol Pharmacol 2001;60:217-24. (Pubitemid 32595249)
22. Revel A, Raanani H, Younglai E, et al. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects lung from DNA damage and apoptosis caused by benzo[a]pyrene. J Appl Toxicol 2003;23:255-61.
23. Kimura Y, Okuda H. Resveratrol isolated from Polygonum cuspidatum root prevents tumor growth and metastasis to lung and tumorinduced neovascularization in Lewis lung carcinoma-bearing mice. J Nutr 2001;131:1844-9. (Pubitemid 32520456)
24. Huang C, Ma WY, Dawson MI, Rincon M, Flavell RA, Dong Z. Blocking activator protein-1 activity, but not activating retinoic acid response element, is required for the antitumor promotion effect of retinoic acid. Proc Natl Acad Sci U S A 1997;94:5826-30.
25. Huang C, Huang Y, Li J, et al. Inhibition of benzo(a)pyrene diolepoxide-induced transactivation of activated protein 1 and nuclear factor κB by black raspberry extracts. Cancer Res 2002;62:6857-63.
26. Kresty LA, Morse MA, Morgan C, et al. Chemoprevention of esophageal tumorigenesis by dietary administration of lyophilized black raspberries. Cancer Res 2001;61:6112-9. (Pubitemid 32762547)
27. Brown PH, Alani R, Preis LH, Szabo E, Birrer MJ. Suppression of oncogene-induced transformation by a deletion mutant of c-jun. Oncogene 1993;8:877-86.
28. Brown PH, Chen TK, Birrer MJ. Mechanism of action of a dominant-negative mutant of c-Jun. Oncogene 1994;9:791-9.
29. Brown PH, Kim SH, Wise SC, Sabichi AL, Birrer MJ. Dominant-negative mutants of cJun inhibit AP-1 activity through multiple mechanisms and with different potencies. Cell Growth Differ 1996;7:1013-21.
30. Young MR, Li JJ, Rincon M, et al. Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion. Proc Natl Acad Sci U S A 1999;96:9827-32.
31. Cooper SJ, MacGowan J, Ranger-Moore J, Young MR, Colburn NH, Bowden GT. Expression of dominant negative c-jun inhibits ultraviolet B-induced squamous cell carcinoma number and size in an SKH-1 hairless mouse model. Mol Cancer Res 2003;1:848-54. (Pubitemid 37174456)
32. Shen Q, Uray IP, Li Y, et al. Targeting the activator protein 1 transcription factor for the prevention of estrogen receptor-negative mammary tumors. Cancer Prev Res 2008;1:45-55.
33. Jin X, Song X, Li L, et al. Blockade of AP-1 activity by dominant-negative TAM67 can abrogate the oncogenic phenotype in latent membrane protein 1-positive human nasopharyngeal carcinoma. Mol Carcinog 2007;46:901-11.
34. Liu Y, Ludes-Meyers J, Zhang Y, et al. Inhibition of AP-1 transcription factor causes blockade of multiple signal transduction pathways and inhibits breast cancer growth. Oncogene 2002;21:7680-9.
35. Shimizu Y, Kinoshita I, Kikuchi J, et al. Growth inhibition of non-small cell lung cancer cells by AP-1 blockade using a cJun dominant-negative mutant. Br J Cancer 2008;98:915-22. (Pubitemid 351341616)
36. Suto R, Tominaga K, Mizuguchi H, et al. Dominant-negative mutant of c-Jun gene transfer: a novel therapeutic strategy for colorectal cancer. Gene Ther 2004;11:187-93.
37. Leaner VD, Chick JF, Donninger H, et al. Inhibition of AP-1 transcriptional activity blocks the migration, invasion, and experimental metastasis of murine osteosarcoma. Am J Pathol 2009;174:265-75.
38. Kikuchi J, Kinoshita I, Shimizu Y, et al. Simultaneous blockade of AP-1 and phosphatidylinositol 3-kinase pathway in non-small cell lung cancer cells. Br J Cancer 2008;99:2013-9.
39. Tichelaar JW, Lu W, Whitsett JA. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 2000;275:11858-64. (Pubitemid 30237754)
40. Shen Q, Zhang Y, Uray IP, et al. The AP-1 transcription factor regulates postnatal mammary gland development. Developmental Biology 2006;295:589-603.
41. Rincon M, Flavell RA. AP-1 transcriptional activity requires both T-cell receptor-mediated and co-stimulatory signals in primary T lymphocytes. EMBO J 1994;13:4370-81.
42. Anderson MW, Goodin C, Zhang Y, et al. Effect of dietary green tea extract and aerosolized difluoromethylornithine during lung tumor progression in A/J strain mice. Carcinogenesis 2008;29:1594-600.
43. Foley JF, Anderson MW, Stoner GD, Gaul BW, Hardisty JF, Maronpot RR. Proliferative lesions of the mouse lung: progression studies in strain A mice. Exp Lung Res 1991;17:157-68.
44. Estensen RD, Jordan MM, Wiedmann TS, Galbraith AR, Steele VE, Wattenberg LW. Effect of chemopreventive agents on separate stages of progression of benzo[α]pyrene induced lung tumors in A/J mice. Carcinogenesis 2004;25:197-201.
45. Zhong S, Quealy JA, Bode AM, et al. Organ-specific activation of activator protien-1 in transgenic mice by 12-O-tetradecanoylphorbol-13-acetate with different administration methods. Cancer Res 2001;61:4084-91.
46. Perl AK, Tichelaar JW, Whitsett JA. Conditional gene expression in the respiratory epithelium of the mouse. Transgenic Res 2002;11:21-9.
47. Jaffuel D, Demoly P, Gougat C, et al. Transcriptional potencies of inhaled glucocorticoids. Am J Respir Crit Care Med 2000;162:57-63.
48. Matthews CP, Colburn NH, Young MR. AP-1 a target for cancer prevention. Curr Cancer Drug Targets 2007;7:317-24.
49. 1 cyclin expression and reducing cyclin-dependent kinase activity. Oncogene 2004;23:8238-46.
50. Shen Q, Uray IP, Li Y, et al. The AP-1 transcription factor regulates breast cancer cell growth via cyclins and E2F factors. Oncogene 2008;27:366-77.
51. Matthews CP, Birkholz AM, Baker AR, et al. Dominant-negative activator protein 1 (TAM67) targets cyclooxygenase-2 and osteopontin under conditions in which it specifically inhibits tumorigenesis. Cancer Res 2007;67:2430-8.
52. Wei Q, Jiang H, Matthews CP, Colburn NH. Sulfiredoxin is an AP-1 target gene that is required for transformation and shows elevated expression in human skin malignancies. Proc Natl Acad Sci U S A 2008;105:19738-43.
53. Dhar A, Hu J, Reeves R, Resar LM, Colburn NH. Dominant-negative c-Jun (TAM67) target genes: HMGA1 is required for tumor promoter-induced transformation. Oncogene 2004;23:4466-76. (Pubitemid 38850425)
54. Cooper S, Ranger-Moore J, Bowden TG. Differential inhibition of UVB-induced AP-1 and NF-κB transactivation by components of the jun bZIP domain. Mol Carcinog 2005;43:108-16.
55. Li JJ, Cao Y, Young MR, Colburn NH. Induced expression of dominant-negative c-jun downregulates NFκB and AP-1 target genes and suppresses tumor phenotype in human keratinocytes. Mol Carcinog 2000;29:159-69.