Extracellular generation of hydrogen peroxide is responsible for activation of EGF receptor by ultraviolet A radiation

Free Radical Biology and Medicine

Volumn 41, Issue 9, 2006, Pages 1478-1487

  von Montfort, Claudia ^a   Fernau, Niklas S ^a   Beier, Juliane I ^a   Sies, Helmut ^a   Klotz, Lars Oliver ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Epidermal growth factor receptor; Free radicals; Hydrogen peroxide; Protein tyrosine phosphatase; Reactive oxygen species; Singlet oxygen; Stress signaling; Ultraviolet radiation

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FREE RADICAL; HYDROGEN PEROXIDE; PHOTOSENSITIZING AGENT; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE; SINGLET OXYGEN; VANADIC ACID;

ARTICLE; CELL LINE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; KERATINOCYTE; PHOTOCHEMISTRY; PRIORITY JOURNAL; RADIATION EXPOSURE; ULTRAVIOLET A RADIATION;

CELLS, CULTURED; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; KERATINOCYTES; OXIDANTS; PHOSPHORYLATION; PHOTOSENSITIVITY DISORDERS; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; SINGLET OXYGEN; ULTRAVIOLET RAYS;

EID: 33749181110     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2006.08.005     Document Type: Article

References (39)

1. Nutt J.E., Mellon J.K., Qureshi K., and Lunec J. Matrix metalloproteinase-1 is induced by epidermal growth factor in human bladder tumour cell lines and is detectable in urine of patients with bladder tumours. Br. J. Cancer 78 (1998) 215-220
2. Kim H., and Muller W.J. The role of the epidermal growth factor receptor family in mammary tumorigenesis and metastasis. Exp. Cell Res. 253 (1999) 78-87
3. Olayioye M.A., Neve R.M., Lane H.A., and Hynes N.E. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 19 (2000) 3159-3167
4. Hynes N.E., and Lane H.A. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev., Cancer 5 (2005) 341-354
5. Giaccone G. Epidermal growth factor receptor inhibitors in the treatment of non-small-cell lung cancer. J. Clin. Oncol. 23 (2005) 3235-3242
6. Wang X., McCullough K.D., Franke T.F., and Holbrook N.J. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275 (2000) 14624-14631
7. Klotz L.O., Schieke S.M., Sies H., and Holbrook N.J. Peroxynitrite activates the phosphoinositide 3-kinase/Akt pathway in human skin primary fibroblasts. Biochem. J. 352 (2000) 219-225
8. Klotz L.O., Patak P., Ale-Agha N., Buchczyk D.P., Abdelmohsen K., Gerber P.A., von Montfort C., and Sies H. 2-Methyl-1,4-naphthoquinone, vitamin K3, decreases gap-junctional intercellular communication via activation of the epidermal growth factor receptor/extracellular signal-regulated kinase cascade. Cancer Res. 62 (2002) 4922-4928
9. Abdelmohsen K., Gerber P.A., von Montfort C., Sies H., and Klotz L.O. Epidermal growth factor receptor is a common mediator of quinone-induced signaling leading to phosphorylation of connexin-43: role of glutathione and tyrosine phosphatases. J. Biol. Chem. 278 (2003) 38360-38367
10. Beier J.I., von Montfort C., Sies H., and Klotz L.O. Activation of ErbB2 by 2-methyl-1,4-naphthoquinone (menadione) in human keratinocytes: role of EGFR and protein tyrosine phosphatases. FEBS Lett. 580 (2006) 1859-1864
11. Abdelmohsen K., von Montfort C., Stuhlmann D., Gerber P.A., Decking U.K., Sies H., and Klotz L.O. Doxorubicin induces EGF receptor-dependent downregulation of gap junctional intercellular communication in rat liver epithelial cells. Biol. Chem. 386 (2005) 217-223
12. Klotz L.O., Holbrook N.J., and Sies H. UVA and singlet oxygen as inducers of cutaneous signaling events. Curr. Probl. Dermatol. 29 (2001) 95-113
13. Rosette C., and Karin M. Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274 (1996) 1194-1197
14. Knebel A., Rahmsdorf H.J., Ullrich A., and Herrlich P. Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J. 15 (1996) 5314-5325
15. El-Abaseri T.B., Fuhrman J., Trempus C., Shendrik I., Tennant R.W., and Hansen L.A. Chemoprevention of UV light-induced skin tumorigenesis by inhibition of the epidermal growth factor receptor. Cancer Res. 65 (2005) 3958-3965
16. El-Abaseri T.B., Putta S., and Hansen L.A. Ultraviolet irradiation induces keratinocyte proliferation and epidermal hyperplasia through the activation of the epidermal growth factor receptor. Carcinogenesis 27 (2006) 225-231
17. Gulati P., Markova B., Göttlicher M., Böhmer F.D., and Herrlich P.A. UVA inactivates protein tyrosine phosphatases by calpain-mediated degradation. EMBO Rep. 5 (2004) 812-817
18. Zhang Y., Dong Z., Bode A.M., Ma W.Y., Chen N., and Dong Z. Induction of EGFR-dependent and EGFR-independent signaling pathways by ultraviolet A irradiation. DNA Cell Biol. 20 (2001) 769-779
19. He Y.Y., Huang J.L., Gentry J.B., and Chignell C.F. Epidermal growth factor receptor down-regulation induced by UVA in human keratinocytes does not require the receptor kinase activity. J. Biol. Chem. 278 (2003) 42457-42465
20. Maziere C., Floret S., Santus R., Morliere P., Marcheux V., and Maziere J.C. Impairment of the EGF signaling pathway by the oxidative stress generated with UVA. Free Radic. Biol. Med. 34 (2003) 629-636
21. Klotz L.O., Briviba K., and Sies H. Mitogen-activated protein kinase activation by singlet oxygen and ultraviolet A. Methods Enzymol. 319 (2000) 130-143
22. He Y.Y., Huang J.L., and Chignell C.F. Delayed and sustained activation of extracellular signal-regulated kinase in human keratinocytes by UVA: implications in carcinogenesis. J. Biol. Chem. 279 (2004) 53867-53874
23. Schieke S.M., Ruwiedel K., Gers-Barlag H., Grether-Beck S., and Krutmann J. Molecular crosstalk of the ultraviolet A and ultraviolet B signaling responses at the level of mitogen-activated protein kinases. J. Invest Dermatol. 124 (2005) 857-859
24. Klotz L.O., Pellieux C., Briviba K., Pierlot C., Aubry J.M., and Sies H. Mitogen-activated protein kinase (p38-, JNK-, ERK-) activation pattern induced by extracellular and intracellular singlet oxygen and UVA. Eur. J. Biochem. 260 (1999) 917-922
25. Pierlot C., Aubry J.M., Briviba K., Sies H., and Di Mascio P. Naphthalene endoperoxides as generators of singlet oxygen in biological media. Methods Enzymol. 319 (2000) 3-20
26. Abdelmohsen K., Patak P., von Montfort C., Melchheier I., Sies H., and Klotz L.O. Signaling effects of menadione: from tyrosine phosphatase inactivation to connexin phosphorylation. Methods Enzymol. 378 (2004) 258-272
27. Knebel A., Böhmer F.D., and Herrlich P. Radiation-induced signal transduction. Methods Enzymol. 319 (2000) 255-272
28. Mendez F., and Penner R. Near-visible ultraviolet light induces a novel ubiquitous calcium-permeable cation current in mammalian cell lines. J. Physiol. 507 (1998) 365-377
29. Zhuang S., Ouedraogo G.D., and Kochevar I.E. Downregulation of epidermal growth factor receptor signaling by singlet oxygen through activation of caspase-3 and protein phosphatases. Oncogene 22 (2003) 4413-4424
30. Schieke S.M., von Montfort C., Buchczyk D.P., Timmer A., Grether-Beck S., Krutmann J., Holbrook N.J., and Klotz L.O. Singlet oxygen-induced attenuation of growth factor signaling: possible role of ceramides. Free Radic. Res. 38 (2004) 729-737
31. Mahns A., Melchheier I., Suschek C.V., Sies H., and Klotz L.O. Irradiation of cells with ultraviolet-A (320-400(nm) in the presence of cell culture medium elicits biological effects due to extracellular generation of hydrogen peroxide. Free Radic. Res. 37 (2003) 391-397
32. Zigman S., Reddan J., Schultz J.B., and McDaniel T. Structural and functional changes in catalase induced by near-UV radiation. Photochem. Photobiol. 63 (1996) 818-824
33. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat. Rev., Mol. Cell Biol. 6 (2005) 32-43
34. Gross S., Knebel A., Tenev T., Neininger A., Gaestel M., Herrlich P., and Böhmer F.D. Inactivation of protein-tyrosine phosphatases as mechanism of UV-induced signal transduction. J. Biol. Chem. 274 (1999) 26378-26386
35. Tyrrell R.M., and Pidoux M. Singlet oxygen involvement in the inactivation of cultured human fibroblasts by UVA (334 nm, 365 nm) and near-visible (405 nm) radiations. Photochem. Photobiol. 49 (1989) 407-412
36. Grzelak A., Rychlik B., and Bartosz G. Light-dependent generation of reactive oxygen species in cell culture media. Free Radic. Biol. Med. 30 (2001) 1418-1425
37. Herrlich P., and Böhmer F.D. Redox regulation of signal transduction in mammalian cells. Biochem. Pharmacol. 59 (2000) 35-41
38. DeYulia Jr. G.J., Carcamo J.M., Borquez-Ojeda O., Shelton C.C., and Golde D.W. Hydrogen peroxide generated extracellularly by receptor-ligand interaction facilitates cell signaling. Proc. Natl. Acad. Sci. USA 102 (2005) 5044-5049
39. DeYulia Jr. G.J., and Carcamo J.M. EGF receptor-ligand interaction generates extracellular hydrogen peroxide that inhibits EGFR-associated protein tyrosine phosphatases. Biochem. Biophys. Res. Commun. 334 (2005) 38-42