Nrf transcription factors in keratinocytes are essential for skin tumor prevention but not for wound healing

Molecular and Cellular Biology

Volumn 26, Issue 10, 2006, Pages 3773-3784

  Auf Dem Keller, Ulrich ^a   Huber, Marcel ^b   Beyer, Tobias A ^a   Kümin, Angelika ^a   Siemes, Christina ^a   Braun, Susanne ^a   Bugnon, Philippe ^a   Mitropoulos, Varvara ^a   Johnson, Delinda A ^c   Johnson, Jeffrey A ^c   Hohl, Daniel ^b   Werner, Sabine ^a  

^a ETH ZURICH   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYCLOOXYGENASE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; RNA; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR NRF3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EPIDERMIS; FEMALE; HISTOLOGY; KERATINOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKIN CARCINOGENESIS; SKIN TUMOR; TRANSGENIC MOUSE; WESTERN BLOTTING; WOUND HEALING;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ALKALINE PHOSPHATASE; ANIMALS; BLOTTING, WESTERN; CARCINOGENICITY TESTS; CARCINOGENS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; EOSINE YELLOWISH-(YS); FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMATOXYLIN; HISTOCYTOCHEMISTRY; HYDROQUINONES; KERATINOCYTES; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; NF-E2-RELATED FACTOR 2; SKIN NEOPLASMS; TETRADECANOYLPHORBOL ACETATE; WOUND HEALING;

MUS MUSCULUS;

EID: 33646561819     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.10.3773-3784.2006     Document Type: Article

References (58)

1. Alam, J., D. Stewart, C. Touchard, S. Boinapally, A. M. Choi, and J. L. Cook. 1999. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274:26071-26078.
2. Baulig, A., M. Garlatti, V. Bonvallot, A. Marchand, R. Barouki, F. Marano, and A. Baeza-Squiban. 2003. Involvement of reactive oxygen species in the metabolic pathways triggered by diesel exhaust particles in human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 285:L671-L679.
3. Braun, S., C. Hanselmann, M. G. Gassmann, U. auf dem Keller, C. Born-Berclaz, K. Chan, Y. W. Kan, and S. Werner. 2002. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol. Cell. Biol. 22:5492-5505.
4. Cerutti, P. A., and B. F. Trump. 1991. Inflammation and oxidative stress in carcinogenesis. Cancer Cells 3:1-7.
5. Chan, J. Y., X. L. Han, and Y. W. Kan. 1993. Cloning of Nrf1, an NF-E2-related transcription factor, by genetic selection in yeast. Proc. Natl. Acad. Sci. USA 90:11371-11375.
6. Chan, J. Y., X. L. Han, and Y. W. Kan. 1993. Isolation of cDNA encoding the human NF-E2 protein. Proc. Natl. Acad. Sci. USA 90:11366-11370.
7. Chan, K., R. Lu, J. C. Chang, and Y. W. Kan. 1996. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. USA 93:13943-13948.
8. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
9. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
10. Clark, R. A. F. 1996. Wound repair. Overview and general considerations, p. 3-50. In R. A. F. Clark (ed.), The molecular and cellular biology of wound repair, 2nd ed. Plenum Press, New York, N.Y.
11. Coussens, L. M., and Z. Werb. 2002. Inflammation and cancer. Nature 420:860-867.
12. Cullinan, S. B., J. D. Gordan, J. Jin, J. W. Harper, and J. A. Diehl. 2004. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol. Cell. Biol. 24:8477-8486.
13. Dajee, M., M. Lazarov, J. Y. Zhang, T. Cai, C. L. Green, A. J. Russell, M. P. Marinkovich, S. Tao, Q. Lin, Y. Kubo, and P. A. Khavari. 2003. NF-κB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 421:639-643.
14. DiGiovanni, J. 1992. Multistage carcinogenesis in mouse skin. Pharmacol. Ther. 54:63-128.
15. Enomoto, A., K. Itoh, E. Nagayoshi, J. Haruta, T. Kimura, T. O'Connor, T. Harada, and M. Yamamoto. 2001. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol. Sci. 59:169-177.
16. Fridovich, I. 1978. The biology of oxygen radicals. Science 201:875-880.
17. Hager, B., J. R. Bickenbach, and P. Fleckman. 1999. Long-term culture of murine epidermal keratinocytes. J. Investig. Dermatol. 112:971-976.
18. Hanausek, M., P. Ganesh, Z. Walaszek, C. J. Arntzen, T. J. Slaga, and J. U. Gutterman. 2001. Avicins, a family of triterpenoid saponins from Acacia victoriae (Bentham), suppress H-ras mutations and aneuploidy in a murine skin carcinogenesis model, Proc. Natl. Acad. Sci. USA 98:11551-11556.
19. Hanselmann, C., C. Mauch, and S. Werner. 2001. Haem oxygenase-1: a novel player in cutaneous wound repair and psoriasis? Biochem. J. 353:459-466.
20. Hayakawa, M., H. Miyashita, I. Sakamoto, M. Kitagawa, H. Tanaka, H. Yasuda, M. Karin, and K. Kikugawa. 2003. Evidence that reactive oxygen species do not mediate NF-κB activation. EMBO J. 22:3356-3366.
21. Henderson, C. J., A. G. Smith, J. Ure, K. Brown, E. J. Bacon, and C. R. Wolf. 1998. Increased skin tumorigenesis in mice lacking pi class glutathione S-transferases. Proc. Natl. Acad. Sci. USA 95:5275-5280.
22. Hyer, M. L., R. Croxton, M. Krajewska, S. Krajewski, C. L. Kress, M. Lu, N. Suh, M. B. Sporn, V. L. Cryns, J. M. Zapata, and J. C. Reed. 2005. Synthetic triterpenoids cooperate with tumor necrosis factor-related apoptosis-inducing ligand to induce apoptosis of breast cancer cells. Cancer Res. 65:4799-4808.
23. Ishii, T., K. Itoh, S. Takahashi, H. Sato, T. Yanagawa, Y. Katoh, S. Bannai, and M. Yamamoto. 2000. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275:16023-16029.
24. 2. Mol. Cell. Biol. 24:36-45.
25. Itoh, K., K. I. Tong, and M. Yamamoto. 2004. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 36:1208-1213.
26. Itoh, K., N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J. D. Engel, and M. Yamamoto. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13:76-86.
27. Johnson, D. A., G. K. Andrews, W. Xu, and J. A. Johnson. 2002. Activation of the antioxidant response element in primary cortical neuronal cultures derived from transgenic reporter mice. J. Neurochem. 81:1233-1241.
28. Kang, K. W., S. H. Choi, and S. G. Kim. 2002. Peroxynitrite activates NF-E2-related factor 2/antioxidant response element through the pathway of phosphatidylinositol 3-kinase: the role of nitric oxide synthase in rat glutathione S-transferase A2 induction. Nitric Oxide 7:244-253.
29. Karin, M. 2005. Inflammation and cancer: the long reach of Ras. Nat. Med. 11:20-21.
30. Kemp, C. J. 2005. Multistep skin cancer in mice as a model to study the evolution of cancer cells. Semin. Cancer Biol. 15:460-473.
31. Kobayashi, A., E. Ito, T. Toki, K. Kogame, S. Takahashi, K. Igarashi, N. Hayashi, and M. Yamamoto. 1999. Molecular cloning and functional characterization of a new Cap 'n' collar family transcription factor Nrf3. J. Biol. Chem. 274:6443-6452.
32. Kobayashi, A., M. I. Kang, H. Okawa, M. Ohtsuji, Y. Zenke, T. Chiba, K. Igarashi, and M. Yamamoto. 2004. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24:7130-7139.
33. Lee, J. M., M. J. Calkins, K. Chan, Y. W. Kan, and J. A. Johnson. 2003. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J. Biol. Chem. 278:12029-12038.
34. Leung, L., M. Kwong, S. Hou, C. Lee, and J. Y. Chan. 2003. Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278:48021-48029.
35. Li, G., C. Gustafson-Brown, S. K. Hanks, K. Nason, J. M. Arbeit, K. Pogliano, R. M. Wisdom, and R. S. Johnson. 2003. c-Jun is essential for organization of the epidermal leading edge. Dev. Cell 4:865-877.
36. Li, J., T. D. Stein, and J. A. Johnson. 2004. Genetic dissection of systemic autoimmune disease in Nrf2-deficient mice. Physiol. Genomics 18:261-272.
37. Liby, K., T. Hock, M. M. Yore, N. Suh, A. E. Place, R. Risingsong, C. R. Williams, D. B. Royce, T. Honda, Y. Honda, G. W. Gribble, N. Hill-Kapturczak, A. Agarwal, and M. B. Sporn. 2005. The synthetic triterpenoids, CDDO and CDDO-imidazolide, are potent inducers of heme oxygenase-1 and Nrf2/ARE signaling. Cancer Res. 65:4789-4798.
38. Lind, M. H., B. Rozell, R. P. Wallin, M. van Hogerlinden, H. G. Ljunggren, R. Toftgard, and I. Sur. 2004. Tumor necrosis factor receptor 1-mediated signaling is required for skin cancer development induced by NF-κB inhibition. Proc. Natl. Acad. Sci. USA 101:4972-4977.
39. Long, D. J., II, R. L. Waikel, X. J. Wang, D. R. Roop, and A. K. Jaiswal. 2001. NAD(P)H:quinone oxidoreductase 1 deficiency and increased susceptibility to 7,12-dimethylbenz[a]-anthracene-induced carcinogenesis in mouse skin. J. Natl. Cancer Inst. 93:1166-1170.
40. Moi, P., K. Chan, I. Asunis, A. Cao, and Y. W. Kan. 1994. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc. Natl. Acad. Sci. USA 91:9926-9930.
41. Munz, B., H. Smola, F. Engelhardt, K. Bleuel, M. Brauchle, I. Lein, L. W. Evans, D. Huylebroeck, R. Balling, and S. Werner. 1999. Overexpression of activin A in the skin of transgenic mice reveals new activities of activin in epidermal morphogenesis, dermal fibrosis and wound repair. EMBO J. 18:5205-5215.
42. Nguyen, T., P. J. Sherratt, and C. B. Pickett. 2003. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43:233-260.
43. Nguyen, T., C. S. Yang, and C. B. Pickett. 2004. The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic. Biol. Med. 37:433-441.
44. Nioi, P., and J. D. Hayes. 2004. Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat. Res. 555:149-171.
45. Park, J. H., S. Gopishetty, L. M. Szewczuk, A. B. Troxel, R. G. Harvey, and T. M. Penning. 2005. Formation of 8-oxo-7,8-dihydro-2′-deoxyguanosine (8-oxo-dGuo) by PAH o-quinones: involvement of reactive oxygen species and copper(II)/copper(I) redox cycling. Chem. Res. Toxicol. 18:1026-1037.
46. Pedersen, T. X., C. Leethanakul, V. Patel, D. Mitola, L. R. Lund, K. Dano, M. Johnsen, J. S. Gutkind, and T. H. Bugge. 2003. Laser capture microdissection-based in vivo genomic profiling of wound keratinocytes identifies similarities and differences to squamous cell carcinoma. Oncogene 22:3964-3976.
47. Ramos-Gomez, M., M. K. Kwak, P. M. Dolan, K. Itoh, M. Yamamoto, P. Talalay, and T. W. Kensler. 2001. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. USA 98:3410-3415.
48. Sander, C. S., H. Chang, F. Hamm, P. Elsner, and J. J. Thiele. 2004. Role of oxidative stress and the antioxidant network in cutaneous carcinogenesis. Int. J. Dermatol. 43:326-335.
49. Schor, N. A., K. Morgan, N. Epstein, and R. Knight. 1983. The influence of polycyclic hydrocarbons on the activity of NAD(P)H-dehydrogenating enzymes 7in rat thymus. A biochemical and histochemical study. Enzyme 29:167-174.
50. Vassar, R., M. Rosenberg, S. Ross, A. Tyner, and E. Fuchs. 1989. Tissue-specific and differentiation-specific expression of a human K14 keratin gene in transgenic mice. Proc. Natl. Acad. Sci. USA 86:1563-1567.
51. Wankell, M., B. Munz, G. Hubner, W. Hans, E. Wolf, A. Goppelt, and S. Werner. 2001. Impaired wound healing in transgenic mice overexpressing the activin antagonist follistatin in the epidermis. EMBO J. 20:5361-5372.
52. Werner, S., H. Smola, X. Liao, M. T. Longaker, T. Krieg, P. H. Hofschneider, and L. T. Williams. 1994. The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science 266:819-822.
53. Werner, S., W. Weinberg, X. Liao, K. G. Peters, M. Blessing, S. H. Yuspa, R. L. Weiner, and L. T. Williams. 1993. Targeted expression of a dominant-negative FGF receptor mutant in the epidermis of transgenic mice reveals a role of FGF in keratinocyte organization and differentiation. EMBO J. 12:2635-2643.
54. Yuspa, S. H., A. A. Dlugosz, M. F. Denning, and A. B. Glick. 1996. Multistage carcinogenesis in the skin. J. Investig. Dermatol. Symp. Proc. 1:147-150.
55. Zenz, R., R. Eferl, L. Kenner, L. Florin, L. Hummerich, D. Mehic, H. Scheuch, P. Angel, E. Tschachler, and E. F. Wagner. 2005. Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 437:369-375.
56. Zenz, R., H. Scheuch, P. Martin, C. Frank, R. Eferl, L. Kenner, M. Sibilia, and E. F. Wagner. 2003. c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev. Cell 4:879-889.
57. Zhang, J. Y., C. L. Green, S. Tao, and P. A. Khavari. 2004. NF-κB RelA opposes epidermal proliferation driven by TNFR1 and JNK. Genes Dev. 18:17-22.
58. Zhang, J. Y., S. Tao, R. Kimmel, and P. A. Khavari. 2005. CDK4 regulation by TNFR1 and JNK is required for NF-κB-mediated epidermal growth control. J. Cell Biol. 168:561-566.