Ultraviolet irradiation-induces epidermal growth factor receptor (EGFR) nuclear translocation in human keratinocytes

Journal of Cellular Biochemistry

Volumn 107, Issue 5, 2009, Pages 873-880

  Xu, Yiru ^a   Shao, Yuan ^a   Zhou, Jin ^a   Voorhees, John J ^a   Fisher, Gary J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

EGFR; Nuclear translocation; Signal transduction; Ultraviolet

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; LEPTOMYCIN B; PROTEIN TYROSINE KINASE INHIBITOR; PROTEIN TYROSINE PHOSPHATASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELL TRANSPORT; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CHO CELLS; CRICETINAE; CRICETULUS; DOSE-RESPONSE RELATIONSHIP, RADIATION; EPIDERMAL GROWTH FACTOR; HUMANS; HYDROGEN PEROXIDE; KERATINOCYTES; MUTANT PROTEINS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 2; TIME FACTORS; ULTRAVIOLET RAYS;

EID: 67749093100     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22195     Document Type: Article

References (54)

1. Ananthaswamy H, Pierceall W. 1990. Molecular mechanisms of ultraviolet radiation carcinogenesis. Photochem Photobiol 52:1119-1136.
2. Boerner J, Demory M, Silva C, Parsons S. 2004. Phosphorylation of Y845 on the epidermal growth factor receptor mediates binding to the mitochondrial protein cytochrome c oxidase subunit II. Mol Cell Biol 24:7059-7071.
3. Carlotti F, Dower S, Qwarnstrom E. 2000. Dynamic shutting of nuclear factor kappa B between the nucleus and cytoplasm as a consequence of inhibitor dissociation. J Biol Chem 275:41028-41034.
4. Coffer L, Burgering B, Peppelenbosch M, Bos J, Kruijer W. 1995. UV activation of receptor tyrosine kinase activity. Oncogene 11:561-569.
5. Defize L, Boonstra J, Meisenhelder J, Kruijer W, Tertoolen L, Tilly B, Hunter T, van Bergen en Henegouwen P, Moolenaar W, de Laat S. 1989. Signal transduction by epidermal growth factor occurs through the subclass of high affinity receptors. J Cell Biol 109:2495-2507.
6. Ditterman K, Matyer C, Fehrenbacher B, Schaller M, Raju U, Milas L, Chen D, Kehlbach R, Rodemann H. 2005. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 280:31182-31189.
7. Fry D. 1999. Inhibition of the epidermal growth factor receptor family of tyrosine kinases as an approach to cancer chemotherapy: Progression from reversible to irreversible inhibitors. Pharmacol Ther 82:207-218.
8. 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. 1998. Specific, irreversible inactivation of the epidermal growth factor receptor and erbB2, by a new class of tyrosine kinase inhibitor. Proc Natl Acad Sci USA 95:12022-12027.
9. Gusterson B, Cowley G, McIlhinney J, Ozanne B, Fisher C, Reeves B. 1985. Evidence for increased epidermal growth factor receptors in human sarcomas. Int J Cancer 36:689-693.
10. Holt S, Alexander P, Inman C, Davies D. 1994. Epidermal growth factor induced tyrosine phosphorylation of nuclear proteins associated with translocation of epidermal growth factor receptor into the nucleus. Biochem Pharmacol 47:117-126.
11. Huang RP, Wu JX, Fan Y, Adamson ED. 1996. UV activates growth factor receptors via reactive oxygen intermediates. J Cell Biol 133:211-220.
12. Huang T, Kudo N, Yoshida M, Miyamoto S. 2000. A nuclear export signal in the N-terminal regulatory domain of IkBa controls cytoplasmic localization of inactive NF-kB/IkBa complexes. Proc Nat Acad Sci USA 97:1014-1019.
13. Huang R-P, Peng A, Golard A, Haossain M, Hunang R, Liu Y-G, Boynton A. 2001. Hydrogen peroxide promotes transformation of rat liver non-neoplastic epithelial cells through activation of epidermal growth factor receptor. Mol Carcinogenesis 30:209-217.
14. Jorissen R, Walker F, Pouliot N, Garrett T, Ward C, Burgress A. 2003. Epidermal growth factor receptor: Mechanisms of activation and signalling. Exp Cell Res 284:31-53.
15. Kamio T, Shigematsu K, Sou H, Kawai K, Tsuchiyama H. 1990. Immunohistochemical expression of epidermal growth factor receptors in human adrenocortical carcinoma. Human Pathol 21:277-282.
16. Keilhack H, Tenev T, Nyakatura E, Godovac-Zimmermann J, Nielson L, Seedorf K, Bohmer F. 1998. Phosphotyrosine 1173 mediates binding of the proteintyrosine phosphatase SHP-1 to the epidermal growth factor receptor and attenuation of receptor signaling. J Biol Chem 273:24839-24846.
17. Kelloff G, Fay J, Steele V, Lubet R, Boone C, Crowell J, Sigman C. 1996. Epidermal growth factor receptor tyrosine kinase inhibitors as potential cancer chemopreventives. Cancer Epidemiol Biomarkers Prev 5:657-666.
18. Knebel A, Rahmsdorf H, Ullrich A, Herrlich P. 1996. Dephosphorylation of receptor tyrosine kinase as target of regulation by radiation, oxidants or alkylating agents. EMBO J 15:5314-5325.
19. Koh H. 1995. Preventive strategies and research for ultraviolet- associated cancer. Environ Health Perspect 103(Suppl):255-257.
20. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner E, Wolffe B, Yoshida M, Horinouchi S. 1999. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci USA 96:9112-9117.
21. Liao H, Carpenter G. 2007. Role of the Sec61 translocon in EGF receptor trafficking to the nucleus and gene expression. Mol Biol Cell 18:1064-1072.
22. Lin S, Makino K, Xia W, Matin A, Wen Y, Kwong K, Bourguignon L, Hung M. 2001. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3:802-808.
23. Lipponen P, Eskelinen M. 1994. 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 69:1120-1125.
24. Lo H, Xia W, Wei U, Ali-Seyed M, Huang S, Hung M. 2005. Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Res 65:338-348.
25. Lo H, Ali-Seyed M, Wu Y, Bartholomeusz G, Hsu S, Hung M. 2006. Nuclear-Cytoplasmic transport of EGFR involves receptor endocytosis, importin b1 and CRM1. J Cell Biochem 98:1570-1583.
26. Lobie P, Wood T, Chen C, Waters M, Norstedt G. 1994. Nuclear translocationand anchorage of the growth hormone receptor. J Biol Chem 269:31735-31746.
27. Maher P. 1996. Nuclear translocation of fibroblast growth factor (FGF) receptors in response to FGF-2. J Cell Biol 134:529-536.
28. Ni C, Murphy M, Golde T, Carpenter G. 2001. g-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294:2179-2181.
29. Obermeier A, Tinhofer I, Grunicke H, Ullrich A. 1996. Transforming potentials of epidermal growth factor and nerve growth factor receptors inversely correlate with their phospholipase Cg affinity and signal activation. EMBO J 15:73-82.
30. Offterdinger M, Schofer C, Weipoltshammer K, Grunt T. 2002. c-erbB-3: A nuclear protein in mammary epithelial cells. J Cell Biol 157:929-939.
31. Psyrri A, Yu Z, Weinberger P, Sasaki C, Haffty B, Camp R, Rimm D, Burtness B. 2005. Quantitative determination of nuclear and cytoplasmic epidermal growth factor receptor expression in oropharyngeal squamous cell cancer by using automated quantitative analysis. Clin Cancer Res 11:5856-5862.
32. Rakowicz-Szulczynska E, Rodeck U, Herlyn M, Koprowski H. 1986. Chromatin binding of epidermal growth factor, nerve growth factor, and platelet-derived growth factor in cells bearing the appropriate surface receptors. Proc Natl Acad Sci USA 83:3728-3732.
33. Rao G. 1996. Hydrogen peroxide induces complex formation of SCH-Grb2-SOS with receptor tyrosine kinase and activates Ras and extracellular signalregulated protein kinases group of mitogen-activated protein kinases. Oncogene 13:713-719.
34. Raymond E, Faivre S, Armand J. 2000. Epidermal growth factor receptor tyrosine kinase as a target for anticancer therapy. Drugs 60(Suppl):15-23.
35. Reilly J, Maher P. 2001. Importin b-mediated nuclear import of fibroblast growth factor receptor: Role in cell proliferation. J Cell Biol 152:1307-1312.
36. Rojas M, Yao S, Lin Y-Z. 1996. Controlling epidermal growth factor (EGF)-stimulated Ras activation in intact cells by a cell-permeable peptide mimicking phosphorylated EGF receptor. J Biol Chem 271:27456-27461.
37. Rosette C, Karin M. 1996. Ultraviolet light and osmotic stress: Activation of the JNK cascade through multiple growth factors and cytokine receptors. Science 274:1194-1197.
38. Sachsenmaier C, Radler-Pohl A, Zinck R, Nordheim A, Herrlich P, Rahmsdorf H. 1994. Involvement of growth factor receptors in the mammalian UVC response. Cell 78:963-972.
39. Srinivasan R, Gillet C, Barnes D, Gullick W. 2000. Nuclear expression of the cerbB-4/HER-4 growth factor receptor in invasive breast cancers. Cancer Res 60:1483-1487.
40. Staberg B, Wulf H, Klemp P, Poulsen T, Brodthagen H. 1983. The carcinogenic effect of UVA irradiation. J Invest Dermatol 81:517-519.
41. Stachowiak M, Maher PAJ, Mordechai E, Stachowiak E. 1996. Nuclear accumulation of fibroblast growth factor receptors is regulated by multiple signals in adrenal medullary cells. Mol Biol Cell 7:1299-1317.
42. Strickland P. 1986. Photocarcinogenesis by near-ultraviolet (UVA) radiation is Sencar mice. J Invest Dermatol 87:272-275.
43. Tervahauta A, Syrjanen S, Syrjanen K. 1994. Epidermal growth factor receptor c-erbB-2 proto-oncogene and estrogen receptor expression in human papillpmavirus lesions of the uterine cervix. Int J Gynecol Pathol 13:234-240.
44. Vigneri R, Goldfine I, Wong K, Smith G, Pezzino V. 1978. The nuclear envelope. The major site of insulin binding in rat liver nuclei. J Biol Chem 253:2098-2103.
45. Wakshull E, Wharton W. 1985. Stablized complexes of epidermal growth factor and its receptor on the cell surface stimulate RNA synthesis but not mitogenesis. Proc Nat Acad Sci USA 82:8513-8517.
46. Wang S-C, Knakajima Y, Yu Y-L, Xia W, Chen C-T, Yang C-C, McIntush E, Li L-Y, Hawke D, Kobayashi R, Hung M-C. 2006. Tyrosine phosphorylation controls PCNA function through protein stability. Nature Cell Biol 8:1359-1368.
47. Xie Y, Hung M. 1994. Nuclear localization of p185neu tyrosine kinase and its association with transcriptional transactivation. Biochem Biophys Res Commun 203:1589-1598.
48. Xu Y, Fisher G. 2005. Ultraviolet (UV) light irradiation induced signal transduction in skin photoaging. J Dermatol Sci Suppl 1:S1-S8.
49. Xu Y, Tan L, Grachtchouk V, Voorhees J, Fisher G. 2005. Receptor-type protein-tyrosine phosphatase-k regulates epidermal growth factor receptor function. J Biol Chem 280:42694-42700.
50. Xu Y, Shao Y, Voorhees J, Fisher G. 2006a. Oxidative inhibition of receptor-type protein-tyrosine phosphatase-k by ultraviolet irradiation activates epidermal growth factor receptor in human keratinocytes. J Biol Chem 281:27389-27397.
51. Xu Y, Voorhees J, Fisher G. 2006b. Epidermal growth factor receptor is a critical mediator of ultraviolet B irradiation-induced signal transduction in immortalized human keratinocyte HaCaT cells. Am J Pathol 169:823-830.
52. Yarden Y, Sliwkowski MX. 2001. Untangling the ErbB signalling network. Mol Cell Biol 2:127-137.
53. Zimmermann H, Ganz P, Zimmermann A, Oguey D, Marti U, Reichen J. 1995. The overexpression of proliferating cell nuclear antigen in biliary cirrhosis in the rat and its relationship with epidermal growth factor receptor. J Hepatol 23:459-464.
54. Zwick E, Hackel P, Prenzel N, Ullrich A. 1999. The EGF receptor as central transducer of heterologous signalling systems. Trends Pharmacol Sci 20:408-412.