Epidermal growth factor receptor is a critical mediator of ultraviolet B irradiation-induced signal transduction in immortalized human keratinocyte HaCaT cells

American Journal of Pathology

Volumn 169, Issue 3, 2006, Pages 823-830

  Xu, Yiru ^a   Voorhees, John J ^a   Fisher, Gary J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PD 169540; PROTEIN C FOS; PROTEIN C JUN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; HUMAN; HUMAN CELL; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ULTRAVIOLET B RADIATION;

EID: 33748789866     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2006.050449     Document Type: Article

References (65)

1. Egeblad M, Werb Z: New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002, 2:161-174
2. Itoh Y, Nagase H: Matrix metalloproteinases in cancer. Essays Biochem 2002, 38:21-36
3. Pupa S, Menard S, Forti S, Tagliabue E: New insights into the role of extracellular matrix during tumor onset and progression. J Cell Physiol 2002, 192:259-267
4. Zheng Z, Chen R, Prystowsky J: UVB radiation induces phosphorylation of the epidermal growth factor receptor decreases EGF binding and blocks EGF induction of ornithine decarboxylase gene expression in SV-40-transfomed human keratinocytes. Exp Dermatol 1993, 2:257-265
5. Sachsenmaier C, Radler-Pohl A, Zinck R, Nordheim A, Herrlich P, Rahmsdorf H: Involvement of growth factor receptors in the mammalian UVC response. Cell 1994, 78:963-972
6. 2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes. J Invest Dermatol 1998, 110:966-971
7. Peus D, Vasa RA, Beyerle A, Meves A, Krautmacher C, Pittelkow MR: UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J Invest Dermatol 1999, 112:751-756
8. Huang RP, Wu JX, Fan Y, Adamson ED: UV activates growth factor receptors via reactive oxygen intermediates. J Cell Biol 1996, 133:211-220
9. Zhuang S, Kochevar I: Ultraviolet A radiation induces rapid apoptosis of human leukemia cells by Fas ligand-independent activation of the Fas death pathways. Photochem Photobiol 2003, 78:61-67
10. Rosette C, Karin M: Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factors and cytokine receptors. Science 1996, 274:1194-1197
11. Bang B, Gniadecki R, Larsen J, Baadsgaard O, Skov L: In vivo UVB irradiation induces clustering of Fas (CD95) on human epidermal cells. Exp Dermatol 2003, 12:791-798
12. Klotz L, Briviba K, Sies H: Singlet oxygen mediates the activation of JNK by UVA radiation in human skin fibroblasts. FEBS Lett 1997, 408:289-291
13. Huang C, Ma WY, Dong ZG: Signal transduction through atypical PKCs, but not the EGF receptor, is necessary for UVC-induced AP-1 activation in immortal murine cells. Oncogene 1997, 14:1945-1954
14. Aragane Y, Kulms D, Luger T, Schwarz T: Down-regulation of Interferon gamma-activated STAT1 by UV light. Proc Natl Acad Sci USA 1997, 94:11490-11495
15. Zhang W, Chen S: EGF-1, a UV-inductible gene in p53 (-/-) mouse cells. Exp Cell Res 2001, 266:21-30
16. Karin M, Takahashi T, Kapahi P, Delhase M, Chen Y, Makris C, Rothwarf D, Baud V, Natoli G, Guido F, Li N: Oxidative stress and gene expression: the AP-1 and NF-κB connections. Biofactors 2001, 15:87-89
17. Legrand-Poels S, Schoonbroodt S, Matroule J, Piette J: NF-κB: an important transcription factor in photobiology. J Photochem Photobiol B 1998, 45:1-8
18. Huang R, Fan Y, Boynton A: UV irradiation upregulates EgM expression at transcription level. J Cell Biochem 1999, 73:227-236
19. Fisher G, Wang Z, Datta S, Li X, Kang S, Voorhees J: UV irradiation inhibits collagen synthesis via c-Jun mediated transcriptional repression that is reversed by all-trans retinoic acid in human skin in vivo. J Clin Invest 2000, 106:661-668
20. Sohwartz E, Cruickshank F, Christensen C, Perlish J, Lebwohl M: Collagen alterations in chronically sun-damaged human skin. Photochem Photobiol 1993, 58:841-844
21. Fisher G, Datta S, Talwar H, Wang Z, Varani J, Kang S, Voorhees J: Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature 1996, 379:335-339
22. Fisher G, Wang Z, Datta S, Varani J, Kang S, Voorhees J: Pathophysiology of premature skin aging induced by ultraviolet light. N Engl J Med 1997, 337:1419-1428
23. Fisher G, Esmann J, Griffiths C, Talwar H, Duell E, Hammerberg C, Elder J, Finkel L, Karabin G, Nickoloff B, Voorhees J: Cellular, immunologic and biochemical characterization of topical retinoic-acid treated human skin. J Invest Dermatol 1991, 96:699-707
24. Gilchrest B, Yaar M: Ageing and photoageing of the skin: observations and the cellular and molecular level. Br J Dermatol 1992, 127:25-30
25. Coussens L, Tinkle C, Hanahan D, Werb Z: MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000, 103:481-490
26. Hackel P, Zwick E, Prenzel N, Ullrich A: Epidermal growth factor receptors: critical mediators of multiple receptor pathways. Curr Opin Cell Biol 1999, 11:184-189
27. Zwick E, Hackel P, Prenzel N, Ullrich A: The EGF receptor as central transducer of heterologous signalling systems. Trends Pharmacol Sci 1999, 20:408-412
28. Prenzel N, Fischer O, Streit S, Hart S, Ullrich A: The epidermal growth factor receptor family as a central element for cellular signal transduction and diversification. Endocr Relat Cancer 2001, 8:11-31
29. Yarden Y, Sliwkowski MX: Untangling the ErbB signaling network. Mol Cell Biol 2001, 2:127-137
30. Turkeri L, Erton M, Cevik I, Akdas A: Impact of the expression of epidermal growth factor, transforming growth factor alpha and epidermal growth factor receptor in the prognosis of superficial bladder cancer. Urology 1998, 51:645-649
31. Scambia G, Benedetti-Panici P, Ferrandina G, Distefano M, Salerno G, Romanini M, Fagotti A, Mancuso S: Epidermal growth factor, oestrogen and progesterone receptor expression in primary ovarian cancer: correlation with clinical outcome and response to chemotherapy. Br J Cancer 1995, 72:361-366
32. Mukaida H, Toi M, Hirai T, Yamashita Y, Toge T: Clinical significance of the expression of epidermal growth factor and its receptor in esophageal cancer. Cancer 1991, 68:142-148
33. Garcia I, Vizoso F, Martin A, Sanz L, Abdel-Lah O, Raigoso P, Garcia-Muniz J: Clinical significance of the epidermal growth factor receptor and HER2 receptor in resectable gastric cancer. Ann Surg Oncol 2003, 10:237-241
34. Reinartz J, George E, Lindgren B, Niehans G: Expression of p53, transforming growth factor alpha, epidermal growth factor, and c-erbB-2 in endometrial carcinoma and correlation with survival and known predictors of survival. Hum Pathol 1994, 25:1075-1083
35. Skirnisdottir I, Sorbe B, Seidal T: The growth factor receptors HER-2/neu and EGFR, their relationship, and their effect on the prognosis in early stage (FIGO I-II) epithelial ovarian carcinoma. Int J Gynecol Cancer 2001, 11:119-129
36. Lipponen P, Eskelinen M: Expression of epidermal growth factor receptor in bladder cancer as related to established prognostic factors, oncoprotein (c-erbB-2, p53) expression and long-term prognosis. Br J Cancer 1994, 69:1120-1125
37. Carpenter G, Zendegui J: Epidermal growth factor, its receptor, and related proteins. Exp Cell Res 1986, 164:1-10
38. Carpenter G: Employment of the epidermal growth factor receptor in growth factor-independent signaling pathways. J Cell Biol 1999, 146:697-702
39. Obata T, Yaffe M, Leparc G, Piro E, Maegawa H, Kashiwag A, Kikkawa R, Cantley L: Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J Biol Chem 2000, 275:36108-36115
40. Alessi D, Cudwell B, Andjelkovic M, Hemmings B, Cohen P: Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett 1996, 399:333-338
41. Pearson R, Kemp B: Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol 1991, 200:62-81
42. Nishikawa K, Toker A, Johannes F-J, Songyang Z, Cantley L: Determination of the specific substrate sequence motifs of protein kinase C isozymes. J Biol Chem 1997, 272:952-960
43. Fry D, Bridges A, Denny W, Doherty A, Greis K, Hicks J, Hook K, Keller P, Leopold W, Loo J, McNamara D, Nelson J, Sherwood V, Smaill J, Trump-Kallmeyer S, Dobrusin E: Specific, irreversible inactivation of the epidermal growth factor receptor and erbB2, by a new class of tyrosine kinase inhibitor. Proc Natl Acad Sci USA 1998, 95:12022-12027
44. Bertios P, Chen W, Hubler L, Lazar C, Rosenfeld M, Gill G: Alteration of epidermal growth factor receptor activity by mutation of its primary carboxyl-terminal site of tyrosine self-phosphorylation. J Biol Chem 1988, 263:3610-3617
45. Davies R, Grosse V, Kucherlapati R, Bothwell M: Genetic analysis of epidermal growth factor action: assignment of human epidermal growth factor receptor gene to chromosome. Proc Natl Acad Sci USA 1980, 77:4188-4192
46. Fisher G, Kang S, Varani J, Bata-Csorgo Z, Wan Y, Datta S, Voorhees J: Mechanisms of photoaging and chronological skin aging. Arch Dermatol 2002, 138:1462-1470
47. Fisher G, Talwar H, Lin P, McPhillips F, Wang Z, Li X, Wan Y, Kang S, Voorhees J: Retinoic acid inhibits induction of c-Jun protein by ultraviolet irradiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo. J Clin Invest 1998, 101:1432-1440
48. Threadgill D, Dlugosz A, Hansen L, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris R: Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 1995, 269:230-234
49. Wang H, Quan T, He T, Franke T, Voorhees J, Fisher G: EGF receptor-dependent NF-κB independent activation of PI-3-kinase/AKT pathway inhibits ultraviolet irradiation-induced caspases 3, 8, and 9 in human keratinocytes. J Biol Chem 2003, 278:45737-45745
50. Peus D, Vasa RA, Meves A, Beyerle A, Pittelkow MR: UVB-induced epidermal growth factor receptor phosphorylation is critical for downstream signaling and keratinocyte survival. Photochem Photobiol 2000, 72:135-140
51. Bae Y, Kang S, Seo M, Baines I, Tekle E, Chock P, Rhee S: Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 1997, 272:217-221
52. Saez E, Rutberg S, Mueller E, Oppenheim H, Smoluk J, Yuspaa S, Spiegelman B: C-fos is required for malignant progression of skin tumors. Cell 1995, 82:721-732
53. Yuspa S: The pathogensis of squamous cell cancer: lessons learned from studies of skin carcinogenesis. J Dermatol Sci 1998, 17:1-7
54. Albert M, Ostheimer K: The evolution of current medical and popular attitudes toward ultraviolet light exposure: part 3. J Am Acad Dermatol 2003, 49:1096-1106
55. Autier P, Boniol M, Severi G, Dore J: Quantity of sunscreen used by European students. Br J Dermatol 2001, 144:288-291
56. Kang S, Chung J, Lee J, Fisher G, Wan Y, Duell E, Voorhees J: Topical N-acetyl cysteine and genisten prevent ultraviolet light-induced signaling that leads to photoaging in human skin in vivo. J Invest Dermatol 2003, 120:835-841
57. Wei H, Bowen R, Zhang X, Lebwohl M: Isoflavone genistein inhibits the initiation and promotion of two-stage skin carcinogenesis in mice. Carcinogenesis 1998, 19:1509-1514
58. Wei H, Saladi R, Lu Y, Wnag Y, Palep S, Moore J, Phelps R, Shyong E, Lebwohl M: Isoflavone genistein: photoprotection and clinical implications in dermatology. J Nutr 2003, 133:38113-38195
59. Lynch T, Bell D, Sordella R, Gurubhagavatula S, Okimoto R, Brannigan B, Harris P, Haserlat S, Supko J, Haluska F, Louis D, Christiani D, Settleman J, Haber D: Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004, 350:2129-2139
60. Paez J, Janne P, Lee J, Tracy S, Greulich H, Gabriel S, Herman P, Kaye F, Lindeman N, Boggon T, Naoki K, Sasaki H, Fujii Y, Eck M, Sellers W, Johnson B, Meyerson M: EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004, 304:1497-1500
61. Persson C, Sjoblom T, Groen A, Kappert K, Engstrom U, Hellman U, Heldin C, den Hertog J, Ostman A: Preferential oxidation of the second phosphatase domain of receptor-like PTP-α revealed by an antibody against oxidized protein tyrosine phosphatases. Proc Natl Acad Sci USA 2004, 101:1886-1891
62. Lee S, Kwon K, Kim S, Rhee S: Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 1998, 273:15366-15372
63. Denu J, Tanner K: Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 1998, 37:5633-5642
64. Huyer G, Lui S, Kelly J, Maffat J, Payette P, Kennedy B, Tsaprailis G, Gresser M, Ramachandran C: Mechanisms of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J Biol Chem 1997, 272:843-851
65. Gross S, Knebel A, Tenev T, Neininger A, Gaestel M, Herrlich P, Bohmer FD: Inactivation of protein tyrosine phosphatases as mechanism of UV-induced signal transduction. J Biol Chem 1999, 274:26378-26386