Nrf2 Transcription Factor, a Novel Target of Keratinocyte Growth Factor Action Which Regulates Gene Expression and Inflammation in the Healing Skin Wound

REFERENCES

• Beer, H. D., C. Florence, J. Dammeier, L. McGuire, S. Werner, and D. R. Duan. 1997. Mouse fibroblast growth factor 10: cDNA cloning, protein characterization, and regulation of mRNA expression. Oncogene 15: 2211–2218.
   PubMedGoogle Scholar
• Bloch, W., K. Huggel, R. Sasaki, R. Grose, P. Bugnon, K. Addicks, R. Timpl, and S. Werner. 2000. The angiogenesis inhibitor endostatin impairs blood vessel maturation during wound healing. FASEB J. 14: 2373–2376.
   PubMed Web of Science ®Google Scholar
• Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106: 761–771.
   PubMed Web of Science ®Google Scholar
• Caldelari, R., M. M. Suter, D. Baumann, A. De Bruin, and E. Müller. 2000. Long-term culture of murine epidermal keratinocytes. J. Investig. Dermatol. 114: 1064–1065.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Chan, K., and Y. W. Kan. 1999. Nrf2 is essential for protection against acute pulmonary injury in mice. Proc. Natl. Acad. Sci. USA 96: 12731–12736.
   PubMed Web of Science ®Google Scholar
• Chan, K., X. D. Han, and Y. W. Kan. 2001. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc. Natl. Acad. Sci. USA 98: 4611–4616.
   PubMed Web of Science ®Google Scholar
• Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156–159.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• Danilenko, D. M. 1999. Preclinical and early clinical development of keratinocyte growth factor, an epithelial-specific tissue growth factor. Toxicol. Pathol. 27: 64–71.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Foresti, R., and R. Motterlini. 1999. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic. Res. 31: 459–475.
   PubMed Web of Science ®Google Scholar
• Frank, S., G. Hübner, G. Breier, M. T. Longaker, D. G. Greenhalgh, and S. Werner. 1995. Regulation of vascular endothelial growth factor expression in cultured keratinocytes: implications for normal and impaired wound healing. J. Biol. Chem. 270: 12607–12613.
   PubMed Web of Science ®Google Scholar
• Frank, S., M. Madlener, and S. Werner. 1996. Transforming growth factors β1, β2, and β3 and their receptors are differentially regulated during normal and impaired wound healing. J. Biol. Chem. 271: 10188–10193.
   PubMed Web of Science ®Google Scholar
• Friling, R. S., A. Bensimon, Y. Tichauer, and V. Daniel. 1990. Xenobiotic-inducible expression of murine glutathione S-transferase Ya subunit gene is controlled by an electrophile-responsive element. Proc. Natl. Acad. Sci. USA 87: 6258–6262.
   PubMed Web of Science ®Google Scholar
• Gassmann, M. G., and S. Werner. 2000. Caveolin-1 and -2 expression is differentially regulated in cultured keratinocytes and within the regenerating epidermis of cutaneous wounds. Exp. Cell Res. 258: 23–32.
   PubMedGoogle Scholar
• Guo, L., L. Degenstein, and E. Fuchs. 1996. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev. 15: 165–175.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hertel, M., S. Braun, S. Durka, C. Alzheimer, and S. Werner. Upregulation and activation of the Nrf-1 transcription factor in the lesioned hippocampus as a novel neuroprotective mechanism against reactive oxygen species. Eur. J. Neurosci., in press.
   Google Scholar
• Hübner, G., M. Brauchle, H. Smola, M. Madlener, R. Fässler, and S. Werner. 1996. Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine 8: 548–556.
   PubMed Web of Science ®Google Scholar
• Igarashi, M., P. W. Finch, and S. A. Aaronson. 1998. Characterization of recombinant human fibroblast growth factor (FGF)-10 reveals functional similarities with keratinocyte growth factor (FGF-7). J. Biol. Chem. 273: 13230–13235.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Itoh, K., T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236: 313–322.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Jimenez, P. A., D. Greenwalt, D. L. Mendrick, M. A. Rampy, J. Su, K. H. Leung, and K. M. Connolly. 2000. Keratinocyte growth factor-2, p. 101–119. In S. Narula and R. Coffman (ed.), New cytokines as potential drugs. Birkhäuser Verlag, Basel, Switzerland.
   Google Scholar
• Johnsen, O., R. Murphy, H. Prydz, and A. B. Kolsto. 1998. Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res. 26: 512–520.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lee, P. J., B. H. Jiang, B. Y. Chin, N. V. Iyer, J. Alam, G. L. Semenza, and A. M. Choi. 1997. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J. Biol. Chem. 272: 5375–5381.
   PubMed Web of Science ®Google Scholar
• Marchese, C., M. Chedid, O. R. Dirsch, K. G. Csaky, F. Santanelli, C. Latini, W. J. LaRochelle, M. R. Torrisi, and S. A. Aaronson. 1995. Modulation of keratinocyte growth factor and its receptor in reepithelializing human skin. J. Exp. Med. 182: 1369–1376.
   PubMed Web of Science ®Google Scholar
• Marikovsky, M., K. Breuing, P. Y. Liu, E. Eriksson, S. Higashiyama, P. Farber, J. Abraham, and M. Klagsbrun. 1993. Appearance of heparin-binding EGF-like growth factor in wound fluid as a response to injury. Proc. Natl. Acad. Sci. USA 90: 3889–3893.
   PubMed Web of Science ®Google Scholar
• Marini, M. G., K. Chan, L. Casula, Y. W. Kan, A. Cao, and P. Moi. 1997. hMAF, a small human transcription factor that heterodimerizes specifically with Nrf1 and Nrf2. J. Biol. Chem. 272: 16490–16497.
   PubMedGoogle Scholar
• Martin, P. 1997. Wound healing—aiming for perfect skin regeneration. Science 276: 75–81.
   PubMed Web of Science ®Google Scholar
• 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 β-globin locus control region. Proc. Natl. Acad. Sci. USA 91: 9926–9930.
   PubMed Web of Science ®Google Scholar
• Mulcahy, R. T., M. A. Wartman, H. H. Bailey, and J. J. Gipp. 1997. Constitutive and β-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence. J. Biol. Chem. 272: 7445–7454.
   PubMed Web of Science ®Google Scholar
• Novotny, V., E. E. Prieschl, R. Csonga, G. Fabjani, and T. Baumruker. 1998. Nrf1 in a complex with fosB, c-jun, junD and ATF2 forms the AP1 component at the TNFα promoter in stimulated mast cells. Nucleic Acids Res. 26: 5480–5485.
   PubMedGoogle Scholar
• Oyake, T., K. Itoh, H. Motohashi, N. Hayashi, H. Hoshino, M. Nishizawa, M. Yamamoto, and K. Igarashi. 1996. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol. Cell. Biol. 16: 6083–6095.
   PubMed Web of Science ®Google Scholar
• Prestera, T., P. Talalay, J. Alam, Y. I. Ahn, P. J. Lee, and A. M. Choi. 1995. Parallel induction of heme oxygenase-1 and chemoprotective phase 2 enzymes by electrophiles and antioxidants: regulation by upstream antioxidant-responsive elements (ARE). Mol. Med. 1: 827–837.
   PubMed Web of Science ®Google Scholar
• Rubin, J. S., D. P. Bottaro, M. Chedid, T. Miki, D. Ron, H.-G. Cheon, W. G. Taylor, E. Fortney, H. Sakata, P. W. Finch, and W. J. LaRochelle. 1995. Keratinocyte growth factor. Cell Biol. Int. 19: 399–411.
   PubMed Web of Science ®Google Scholar
• Rushmore, T. H., R. G. King, K. E. Paulson, and C. B. Pickett. 1990. Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc. Natl. Acad. Sci. USA 87: 3826–3830.
   PubMed Web of Science ®Google Scholar
• Rushmore, T. H., M. R. Morton, and C. B. Pickett. 1991. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J. Biol. Chem. 266: 11632–11639.
   PubMed Web of Science ®Google Scholar
• Venugopal, R., and A. K. Jaiswal. 1996. Nrf1 and Nrf2 positively and c-fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. USA 93: 14960–14965.
   PubMed Web of Science ®Google Scholar
• Venugopal, R., and A. K. Jaiswal. 1998. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17: 3145–3156.
   PubMed Web of Science ®Google Scholar
• Wasserman, W. W., and W. E. Fahl. 1997. Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA 94: 5361–5366.
   PubMed Web of Science ®Google Scholar
• Werner, S., K. G. Peters, M. T. Longaker, F. Fuller-Pace, M. J. Banda, and L. T. Williams. 1992. Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc. Natl. Acad. Sci. USA 89: 6896–6900.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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 re-epithelialization of wounds. Science 266: 819–822.
   PubMed Web of Science ®Google Scholar
• Werner, S. 1998. Keratinocyte growth factor: a unique player in epithelial repair processes. Cytokine Growth Factor Rev. 9: 153–165.
   PubMed Web of Science ®Google Scholar
• Wilkinson, D. G., J. A. Bailes, J. E. Champion, and A. P. McMahon. 1987. A molecular analysis of mouse development from 8 to 10 days post coitum detects changes only in embryonic globin expression. Development 99: 493–500.
   PubMed Web of Science ®Google Scholar