The UV (Ribotoxic) Stress Response of Human Keratinocytes Involves the Unexpected Uncoupling of the Ras-Extracellular Signal-Regulated Kinase Signaling Cascade from the Activated Epidermal Growth Factor Receptor

REFERENCES

• Albanell, J., J. Codony-Servat, F. Rojo, J. M. Del Campo, S. Sauleda, J. Anido, G. Raspall, J. Giralt, J. Rosello, R. I. Nicholson, J. Mendelsohn, and J. Baselga. 2001. Activated extracellular signal-regulated kinases: association with epidermal growth factor receptor/transforming growth factor alpha expression in head and neck squamous carcinoma and inhibition by anti-epidermal growth factor receptor treatments. Cancer Res. 61: 6500–6510.
   PubMed Web of Science ®Google Scholar
• Assoian, R. K., and M. A. Schwartz. 2001. Coordinate signaling by integrins and receptor tyrosine kinases in the regulation of G1 phase cell-cycle progression. Curr. Opin. Genet. Dev. 11: 48–53.
   PubMed Web of Science ®Google Scholar
• Balmanno, K., and S. J. Cook. 1999. Sustained MAP kinase activation is required for the expression of cyclin D1, p21Cip1 and a subset of AP-1 proteins in CCL39 cells. Oncogene 18: 3085–3097.
   PubMed Web of Science ®Google Scholar
• Batzer, A. G., P. Blaikie, K. Nelson, J. Schlessinger, and B. Margolis. 1995. The phosphotyrosine interaction domain of Shc binds an LXNPXY motif on the epidermal growth factor receptor. Mol. Cell. Biol. 15: 4403–4409.
   PubMedGoogle Scholar
• Batzer, A. G., D. Rotin, J. M. Urena, E. Y. Skolnik, and J. Schlessinger. 1994. Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol. Cell. Biol. 14: 5192–5201.
   PubMed Web of Science ®Google Scholar
• Bender, K., C. Blattner, A. Knebel, M. Iordanov, P. Herrlich, and H. J. Rahmsdorf. 1997. UV-induced signal transduction. J. Photochem. Photobiol. B 37: 1–17.
   PubMed Web of Science ®Google Scholar
• Bogdan, S., and C. Klambt. 2001. Epidermal growth factor receptor signaling. Curr. Biol. 11: R292–R295.
   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
• Chardin, P., J. H. Camonis, N. W. Gale, L. van Aelst, J. Schlessinger, M. H. Wigler, and D. Bar-Sagi. 1993. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260: 1338–1343.
   PubMed Web of Science ®Google Scholar
• Cobb, M. H. 1999. MAP kinase pathways. Prog. Biophys. Mol. Biol. 71: 479–500.
   PubMed Web of Science ®Google Scholar
• Coffey, R. J., Jr., R. Derynck, J. N. Wilcox, T. S. Bringman, A. S. Goustin, H. L. Moses, and M. R. Pittelkow. 1987. Production and auto-induction of transforming growth factor-alpha in human keratinocytes. Nature 328: 817–820.
   PubMed Web of Science ®Google Scholar
• Coleman, M. L., and C. J. Marshall. 2001. A family outing: small GTPases cyclin' through G1. Nat. Cell Biol. 3: E250–E251.
   PubMedGoogle Scholar
• Cook, P. W., P. A. Mattox, W. W. Keeble, M. R. Pittelkow, G. D. Plowman, M. Shoyab, J. P. Adelman, and G. D. Shipley. 1991. A heparin sulfate-regulated human keratinocyte autocrine factor is similar or identical to amphiregulin. Mol. Cell. Biol. 11: 2547–2557.
   PubMed Web of Science ®Google Scholar
• Datta, S. R., A. Brunet, and M. E. Greenberg. 1999. Cellular survival: a play in three Akts. Genes Dev. 13: 2905–2927.
   PubMed Web of Science ®Google Scholar
• Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103: 239–252.
   PubMed Web of Science ®Google Scholar
• Dong, C., R. J. Davis, and R. A. Flavell. 2001. Signaling by the JNK group of MAP kinases. c-jun N-terminal kinase. J. Clin. Immunol. 21: 253–257.
   PubMedGoogle Scholar
• Dulin, N. O., A. Sorokin, and J. G. Douglas. 1998. Arachidonate-induced tyrosine phosphorylation of epidermal growth factor receptor and Shc-Grb2-Sos association. Hypertension 32: 1089–1093.
   PubMedGoogle Scholar
• Funaki, M., H. Katagiri, K. Inukai, M. Kikuchi, and T. Asano. 2000. Structure and function of phosphatidylinositol-3,4 kinase. Cell. Signal. 12: 135–142.
   PubMedGoogle Scholar
• Gale, N. W., S. Kaplan, E. J. Lowenstein, J. Schlessinger, and D. Bar-Sagi. 1993. Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 363: 88–92.
   PubMed Web of Science ®Google Scholar
• Gazit, A., P. Yaish, C. Gilon, and A. Levitzki. 1989. Tyrphostins I: synthesis and biological activity of protein tyrosine kinase inhibitors. J. Med. Chem. 32: 2344–2352.
   PubMed Web of Science ®Google Scholar
• Gilchrest, B. A., H. Y. Park, M. S. Eller, and M. Yaar. 1996. Mechanisms of ultraviolet light-induced pigmentation. Photochem. Photobiol. 63: 1–10.
   PubMed Web of Science ®Google Scholar
• Goldfarb, M. 2001. Signaling by fibroblast growth factors: the inside story. Science's STKE 2001: PE37.
   PubMedGoogle Scholar
• Gross, I., B. Bassit, M. Benezra, and J. D. Licht. 2001. Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. J. Biol. Chem. 276: 46460–46468.
   PubMed Web of Science ®Google Scholar
• Haase, I., R. M. Hobbs, M. R. Romero, S. Broad, and F. M. Watt. 2001. A role for mitogen-activated protein kinase activation by integrins in the pathogenesis of psoriasis. J. Clin. Investig. 108: 527–536.
   PubMed Web of Science ®Google Scholar
• Hashimoto, K., S. Higashiyama, H. Asada, E. Hashimura, T. Kobayashi, K. Sudo, T. Nakagawa, D. Damm, K. Yoshikawa, and N. Taniguchi. 1994. Heparin-binding epidermal growth factor-like growth factor is an autocrine growth factor for human keratinocytes. J. Biol. Chem. 269: 20060–20066.
   PubMedGoogle Scholar
• Herrlich, P., K. Bender, A. Knebel, F. D. Bohmer, S. Gross, C. Blattner, H. J. Rahmsdorf, and M. Gottlicher. 1999. Radiation-induced signal transduction. Mechanisms and consequences. C. R. Acad. Sci. Ser. III 322: 121–125.
   PubMedGoogle Scholar
• Herrlich, P., C. Sachsenmaier, A. Radler-Pohl, S. Gebel, C. Blattner, and H. J. Rahmsdorf. 1994. The mammalian UV response: mechanism of DNA damage induced gene expression. Adv. Enzyme Regul. 34: 381–395.
   PubMedGoogle Scholar
• Herrmann, C., G. Horn, M. Spaargaren, and A. Wittinghofer. 1996. Differential interaction of the ras family GTP-binding proteins H-Ras, Rap1A, and R-Ras with the putative effector molecules Raf kinase and Ral-guanine nucleotide exchange factor. J. Biol. Chem. 271: 6794–6800.
   PubMed Web of Science ®Google Scholar
• Inohara, S., K. Kitagawa, and Y. Kitano. 1996. Coexpression of p21Waf1/Cip1 and p53 in sun-exposed normal epidermis, but not in neoplastic epidermis. Br. J. Dermatol. 135: 717–720.
   PubMedGoogle Scholar
• Iordanov, M., K. Bender, T. Ade, W. Schmid, C. Sachsenmaier, K. Engel, M. Gaestel, H. J. Rahmsdorf, and P. Herrlich. 1997. CREB is activated by UVC through a p38/HOG-1-dependent protein kinase. EMBO J. 16: 1009–1022.
   PubMedGoogle Scholar
• Iordanov, M. S., and B. E. Magun. 1999. Different mechanisms of c-Jun NH(2)-terminal kinase-1 (JNK1) activation by ultraviolet-B radiation and by oxidative stressors. J. Biol. Chem. 274: 25801–25806.
   PubMed Web of Science ®Google Scholar
• Iordanov, M. S., and B. E. Magun. 1998. Loss of cellular K+ mimics ribotoxic stress. Inhibition of protein synthesis and activation of the stress kinases SEK1/MKK4, stress-activated protein kinase/c-Jun NH2-terminal kinase 1, and p38/HOG1 by palytoxin. J. Biol. Chem. 273: 3528–3534.
   PubMed Web of Science ®Google Scholar
• Iordanov, M. S., D. Pribnow, J. L. Magun, T. H. Dinh, J. A. Pearson, S. L. Chen, and B. E. Magun. 1997. Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol. Cell. Biol. 17: 3373–3381.
   PubMed Web of Science ®Google Scholar
• Iordanov, M. S., D. Pribnow, J. L. Magun, T. H. Dinh, J. A. Pearson, and B. E. Magun. 1998. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J. Biol. Chem. 273: 15794–15803.
   PubMed Web of Science ®Google Scholar
• Iordanov, M. S., J. Wong, D. L. Newton, S. M. Rybak, R. K. Bright, R. A. Flavell, R. J. Davis, and B. E. Magun. 2000. Differential requirement for the stress-activated protein kinase/c-Jun NH(2)-terminal kinase in RNA damage-induced apoptosis in primary and in immortalized fibroblasts. Mol. Cell Biol. Res. Commun. 4: 122–128.
   PubMedGoogle Scholar
• Knebel, A., H. J. Rahmsdorf, A. Ullrich, and P. Herrlich. 1996. Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J. 15: 5314–5325.
   PubMed Web of Science ®Google Scholar
• Kolch, W. 2000. Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem. J. 351: 289–305.
   PubMed Web of Science ®Google Scholar
• Kulms, D., and T. Schwarz. 2000. Molecular mechanisms of UV-induced apoptosis. Photodermatol. Photoimmunol. Photomed. 16: 195–201.
   PubMed Web of Science ®Google Scholar
• Levkowitz, G., H. Waterman, S. A. Ettenberg, M. Katz, A. Y. Tsygankov, I. Alroy, S. Lavi, K. Iwai, Y. Reiss, A. Ciechanover, S. Lipkowitz, and Y. Yarden. 1999. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4: 1029–1040.
   PubMed Web of Science ®Google Scholar
• Lewis, T. S., P. S. Shapiro, and N. G. Ahn. 1998. Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74: 49–139.
   PubMed Web of Science ®Google Scholar
• Liefer, K. M., M. I. Koster, X. J. Wang, A. Yang, F. McKeon, and D. R. Roop. 2000. Down-regulation of p63 is required for epidermal UVB-induced apoptosis. Cancer Res. 60: 4016–4020.
   PubMed Web of Science ®Google Scholar
• Lowenstein, E. J., R. J. Daly, A. G. Batzer, W. Li, B. Margolis, R. Lammers, A. Ullrich, E. Y. Skolnik, D. Bar-Sagi, and J. Schlessinger. 1992. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70: 431–442.
   PubMed Web of Science ®Google Scholar
• Matsui, M. S., and V. A. DeLeo. 1991. Longwave ultraviolet radiation and promotion of skin cancer. Cancer Cells 3: 8–12.
   PubMed Web of Science ®Google Scholar
• Migliaccio, E., S. Mele, A. E. Salcini, G. Pelicci, K. M. Lai, G. Superti-Furga, T. Pawson, P. P. Di Fiore, L. Lanfrancone, and P. G. Pelicci. 1997. Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J. 16: 706–716.
   PubMed Web of Science ®Google Scholar
• Miller, D. L., and M. A. Weinstock. 1994. Nonmelanoma skin cancer in the United States: incidence. J. Am. Acad. Dermatol. 30: 774–778.
   PubMed Web of Science ®Google Scholar
• Minden, A., and M. Karin. 1997. Regulation and function of the JNK subgroup of MAP kinases. Biochim. Biophys. Acta 1333: F85–F104.
   PubMed Web of Science ®Google Scholar
• Murphy, G., A. R. Young, H. C. Wulf, D. Kulms, and T. Schwarz. 2001. The molecular determinants of sunburn cell formation. Exp. Dermatol. 10: 155–160.
   PubMed Web of Science ®Google Scholar
• Norris, D. A., K. Whang, K. David-Bajar, and S. D. Bennion. 1997. The influence of ultraviolet light on immunological cytotoxicity in the skin. Photochem. Photobiol. 65: 636–646.
   PubMedGoogle Scholar
• Okabayashi, Y., Y. Kido, T. Okutani, Y. Sugimoto, K. Sakaguchi, and M. Kasuga. 1994. Tyrosines 1148 and 1173 of activated human epidermal growth factor receptors are binding sites of Shc in intact cells. J. Biol. Chem. 269: 18674–18678.
   PubMed Web of Science ®Google Scholar
• Okutani, T., Y. Okabayashi, Y. Kido, Y. Sugimoto, K. Sakaguchi, K. Matuoka, T. Takenawa, and M. Kasuga. 1994. Grb2/Ash binds directly to tyrosines 1068 and 1086 and indirectly to tyrosine 1148 of activated human epidermal growth factor receptors in intact cells. J. Biol. Chem. 269: 31310–31314.
   PubMedGoogle Scholar
• Osherov, N., and A. Levitzki. 1994. Epidermal-growth-factor-dependent activation of the src-family kinases. Eur. J. Biochem. 225: 1047–1053.
   PubMedGoogle Scholar
• Pawson, T., and J. D. Scott. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278: 2075–2080.
   PubMed Web of Science ®Google Scholar
• Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, T. Pawson, and P. G. Pelicci. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70: 93–104.
   PubMed Web of Science ®Google Scholar
• Pellegrini, G., E. Dellambra, O. Golisano, E. Martinelli, I. Fantozzi, S. Bondanza, D. Ponzin, F. McKeon, and M. De Luca. 2001. p63 identifies keratinocyte stem cells. Proc. Natl. Acad. Sci. USA 98: 3156–3161.
   PubMed Web of Science ®Google Scholar
• Radler-Pohl, A., C. Sachsenmaier, S. Gebel, H. P. Auer, J. T. Bruder, U. Rapp, P. Angel, H. J. Rahmsdorf, and P. Herrlich. 1993. UV-induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase. EMBO J. 12: 1005–1012.
   PubMedGoogle Scholar
• Rena, G., S. Guo, S. C. Cichy, T. G. Unterman, and P. Cohen. 1999. Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274: 17179–17183.
   PubMed Web of Science ®Google Scholar
• Rincon, M., R. A. Flavell, and R. J. Davis. 2001. Signal transduction by MAP kinases in T lymphocytes. Oncogene 20: 2490–2497.
   PubMed Web of Science ®Google Scholar
• Rodrigues, G. A., M. Falasca, Z. Zhang, S. H. Ong, and J. Schlessinger. 2000. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol. Cell. Biol. 20: 1448–1459.
   PubMedGoogle Scholar
• Romerdahl, C. A., L. C. Stephens, C. Bucana, and M. L. Kripke. 1989. The role of ultraviolet radiation in the induction of melanocytic skin tumors in inbred mice. Cancer Commun. 1: 209–216.
   PubMedGoogle Scholar
• Roovers, K., and R. K. Assoian. 2000. Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays 22: 818–826.
   PubMed Web of Science ®Google Scholar
• Rotin, D., B. Margolis, M. Mohammadi, R. J. Daly, G. Daum, N. Li, E. H. Fischer, W. H. Burgess, A. Ullrich, and J. Schlessinger. 1992. SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma. EMBO J. 11: 559–567.
   PubMedGoogle Scholar
• Rozakis-Adcock, M., J. McGlade, G. Mbamalu, G. Pelicci, R. Daly, W. Li, A. Batzer, S. Thomas, J. Brugge, P. G. Pelicci, et al. 1992. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360: 689–692.
   PubMed Web of Science ®Google Scholar
• Sachsenmaier, C., A. Radler-Pohl, R. Zinck, A. Nordheim, P. Herrlich, and H. J. Rahmsdorf. 1994. Involvement of growth factor receptors in the mammalian UVC response. Cell 78: 963–972.
   PubMed Web of Science ®Google Scholar
• Schaeffer, H. J., and M. J. Weber. 1999. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol. 19: 2435–2444.
   PubMed Web of Science ®Google Scholar
• Schlessinger, J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103: 211–225.
   PubMed Web of Science ®Google Scholar
• Schwartz, M. A., and R. K. Assoian. 2001. Integrins and cell proliferation: regulation of cyclin-dependent kinases via cytoplasmic signaling pathways. J. Cell Sci. 114: 2553–2560.
   PubMed Web of Science ®Google Scholar
• Shirakata, Y., T. Komurasaki, H. Toyoda, Y. Hanakawa, K. Yamasaki, S. Tokumaru, K. Sayama, and K. Hashimoto. 2000. Epiregulin, a novel member of the epidermal growth factor family, is an autocrine growth factor in normal human keratinocytes. J. Biol. Chem. 275: 5748–5753.
   PubMed Web of Science ®Google Scholar
• Sibilia, M., A. Fleischmann, A. Behrens, L. Stingl, J. Carroll, F. M. Watt, J. Schlessinger, and E. F. Wagner. 2000. The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 102: 211–220.
   PubMed Web of Science ®Google Scholar
• Sorkin, A., M. Mazzotti, T. Sorkina, L. Scotto, and L. Beguinot. 1996. Epidermal growth factor receptor interaction with clathrin adaptors is mediated by the Tyr974-containing internalization motif. J. Biol. Chem. 271: 13377–13384.
   PubMedGoogle Scholar
• Takahashi, H., M. Honma, A. Ishida-Yamamoto, K. Namikawa, H. Kiyama, and H. Iizuka. 2001. Expression of human cystatin A by keratinocytes is positively regulated via the Ras/MEKK1/MKK7/JNK signal transduction pathway but negatively regulated via the Ras/Raf-1/MEK1/ERK pathway. J. Biol. Chem. 276: 36632–36638.
   PubMedGoogle Scholar
• Takai, Y., T. Sasaki, and T. Matozaki. 2001. Small GTP-binding proteins. Physiol. Rev. 81: 153–208.
   PubMed Web of Science ®Google Scholar
• Taylor, C. R., R. S. Stern, J. J. Leyden, and B. A. Gilchrest. 1990. Photoaging/photodamage and photoprotection. J. Am. Acad. Dermatol. 22: 1–15.
   PubMed Web of Science ®Google Scholar
• Tibbles, L. A., and J. R. Woodgett. 1999. The stress-activated protein kinase pathways. Cell. Mol. Life Sci. 55: 1230–1254.
   PubMed Web of Science ®Google Scholar
• Ward, C. W., K. H. Gough, M. Rashke, S. S. Wan, G. Tribbick, and J. Wang. 1996. Systematic mapping of potential binding sites for Shc and Grb2 SH2 domains on insulin receptor substrate-1 and the receptors for insulin, epidermal growth factor, platelet-derived growth factor, and fibroblast growth factor. J. Biol. Chem. 271: 5603–5609.
   PubMedGoogle Scholar
• Watt, F. M. 2001. Stem cell fate and patterning in mammalian epidermis. Curr. Opin. Genet. Dev. 11: 410–417.
   PubMed Web of Science ®Google Scholar
• Weber, J. D., D. M. Raben, P. J. Phillips, and J. J. Baldassare. 1997. Sustained activation of extracellular-signal-regulated kinase 1 (ERK1) is required for the continued expression of cyclin D1 in G1 phase. Biochem. J. 326: 61–68.
   PubMed Web of Science ®Google Scholar
• Yang, A., M. Kaghad, Y. Wang, E. Gillett, M. D. Fleming, V. Dotsch, N. C. Andrews, D. Caput, and F. McKeon. 1998. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2: 305–316.
   PubMed Web of Science ®Google Scholar