Activation of keap1/nrf2 signaling pathway by nuclear epidermal growth factor receptor in cancer cells

American Journal of Translational Research

Volumn 6, Issue 6, 2014, Pages 649-663

  Huo, Longfei ^a   Li, Chia Wei ^a   Huang, Tzu Hsuan ^a   Lam, Yung Carmen ^a   Xia, Weiya ^a   Tu, Chun ^a   Chang, Wei Chao ^c   Hsu, Jennifer L ^a,c,e   Lee, Dung Fang ^a   Nie, Lei ^a   Yamaguchi, Hirohito ^a   Wang, Yan ^a   Lang, Jingyu ^a   Li, Long Yuan ^c   Chen, Chung Hsuan ^d   Mishra, Lopa ^b   Hung, Mien Chie ^a,c,e  

^a Departments of Molecular and Cellular Oncology   (Taiwan)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d GENOMICS RESEARCH CENTER   (Taiwan)

^e ASIA UNIVERSITY   (Taiwan)

Author keywords

Cancer; EGFR; Keap1; Nrf2; Ubiquitination

Indexed keywords

CISPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; KELCH LIKE ECH ASSOCIATED PROTEIN 1; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CANCER CELL; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNOPRECIPITATION; MASS SPECTROMETRY; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TUMOR GROWTH; UBIQUITINATION; WESTERN BLOTTING;

EID: 84912126287     PISSN: None     EISSN: 19438141     Source Type: Journal    
DOI: None     Document Type: Article

References (34)

1. Stepkowski TM, Kruszewski MK. Molecular cross-talk between the NRF2/KEAP1 signaling pathway, autophagy, and apoptosis. Free Radic Biol Med 2011; 50: 1186-1195.
2. Lee DF, Kuo HP, Liu M, Chou CK, Xia W, Du Y, Shen J, Chen CT, Huo L, Hsu MC, Li CW, Ding Q, Liao TL, Lai CC, Lin AC, Chang YH, Tsai SF, Li LY, Hung MC. KEAP1 E3 ligase-mediated down-regulation of NF-kappaB signaling by targeting IKKbeta. Mol Cell 2009; 36: 131-140.
3. Niture SK, Khatri R, Jaiswal AK. Regulation of Nrf2-an update. Free Radic Biol Med 2014; 66: 36-44.
4. Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 2011; 85: 241-272.
5. Copple IM, Goldring CE, Kitteringham NR, Park BK. The keap1-nrf2 cellular defense pathway: mechanisms of regulation and role in protection against drug-induced toxicity. Handb Exp Pharmacol 2010; 233-266.
6. Sun Z, Zhang S, Chan JY, Zhang DD. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol 2007; 27: 6334-6349.
7. Watai Y, Kobayashi A, Nagase H, Mizukami M, McEvoy J, Singer JD, Itoh K, Yamamoto M. Subcellular localization and cytoplasmic complex status of endogenous Keap1. Genes Cells 2007; 12: 1163-1178.
8. Niture SK, Kaspar JW, Shen J, Jaiswal AK. Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 2010; 244: 37-42.
9. Wujcik D. EGFR as a target: rationale for therapy. Semin Oncol Nurs 2006; 22: 5-9.
10. Huo L, Hsu JL, Hung MC. Receptor Tyrosine Kinases in the Nucleus: Nuclear Functions and Therapeutic Implications In Cancers. In: Kumar R, editor. Nuclear Signaling Pathways and Targeting Transcription in Cancer. New York: Springer; 2014. pp. 189-229.
11. Ciardiello F, Tortora G. EGFR antagonists in cancer treatment. N Engl J Med 2008; 358: 1160-1174.
12. Burgess AW. EGFR family: structure physiology signalling and therapeutic targets. Growth Factors 2008; 26: 263-274.
13. Huang PH, Xu AM, White FM. Oncogenic EGFR signaling networks in glioma. Sci Signal 2009; 2: re6.
14. Tebbutt N, Pedersen MW, Johns TG. Targeting the ERBB family in cancer: couples therapy. Nat Rev Cancer 2013; 13: 663-673.
15. Wang YN, Yamaguchi H, Hsu JM, Hung MC. Nuclear traffcking of the epidermal growth factor receptor family membrane proteins. Oncogene 2010; 29: 3997-4006.
16. Han W, Lo HW. Landscape of EGFR signaling network in human cancers: biology and therapeutic response in relation to receptor subcel-lular locations. Cancer Lett 2012; 318: 124-134.
17. Wang YN, Hung MC. Nuclear functions and subcellular traffcking mechanisms of the epidermal growth factor receptor family. Cell Biosci 2012; 2: 13.
18. Huang WC, Chen YJ, Li LY, Wei YL, Hsu SC, Tsai SL, Chiu PC, Huang WP, Wang YN, Chen CH, Chang WC, Chen AJ, Tsai CH, Hung MC. Nuclear translocation of epidermal growth factor receptor by Akt-dependent phosphorylation enhances breast cancer-resistant protein expression in geftinib-resistant cells. J Biol Chem 2011; 286: 20558-20568.
19. Yu YL, Chou RH, Wu CH, Wang YN, Chang WJ, Tseng YJ, Chang WC, Lai CC, Lee HJ, Huo L, Chen CH, Hung MC. Nuclear EGFR suppresses ribonuclease activity of polynucleotide phos-phorylase through DNAPK-mediated phos-phorylation at serine 776. J Biol Chem 2012; 287: 31015-31026.
20. Yamadori T, Ishii Y, Homma S, Morishima Y, Kurishima K, Itoh K, Yamamoto M, Minami Y, Noguchi M, Hizawa N. Molecular mechanisms for the regulation of Nrf2-mediated cell proliferation in non-small-cell lung cancers. Oncogene 2012; 31: 4768-77.
21. Huo L, Wang YN, Xia W, Hsu SC, Lai CC, Li LY, Chang WC, Wang Y, Hsu MC, Yu YL, Huang TH, Ding Q, Chen CH, Tsai CH, Hung MC. RNA heli-case A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc Natl Acad Sci U S A 2010; 107: 16125-16130.
22. Hsu SC, Miller SA, Wang Y, Hung MC. Nuclear EGFR is required for cisplatin resistance and DNA repair. Am J Transl Res 2009; 1: 249-258.
23. Dhakshinamoorthy S. Small Maf (MafG and MafK) Proteins Negatively Regulate Antioxidant Response Element-mediated Expression and Antioxidant Induction of the NAD(P)H:Quinone Oxidoreductase1 Gene. J Biol Chem 2000; 275: 40134-40141.
24. Huang TH, Huo L, Wang YN, Xia W, Wei Y, Chang SS, Chang WC, Fang YF, Chen CT, Lang JY, Tu C, Wang Y, Hsu MC, Kuo HP, Ko HW, Shen J, Lee HH, Lee PC, Wu Y, Chen CH, Hung MC. Epidermal Growth Factor Receptor Potentiates MCM7-Mediated DNA Replication through Tyrosine Phosphorylation of Lyn Kinase in Human Cancers. Cancer Cell 2013; 23: 796-810.
25. Jain AK, Mahajan S, Jaiswal AK. Phosphorylation and dephosphorylation of tyrosine 141 regulate stability and degradation of INrf2: a novel mechanism in Nrf2 activation. J Biol Chem 2008; 283: 17712-17720.
26. Itoh K, Mimura J, Yamamoto M. Discovery of the Negative Regulator of Nrf2, Keap1: A Historical Overview. Antioxid Redox Signal 2010; 13: 1665-1678.
27. Villeneuve NF, Lau A, Zhang DD. Regulation of the Nrf2–Keap1 Antioxidant Response by the Ubiquitin Proteasome System: An Insight into Cullin-Ring Ubiquitin Ligases. Antioxid Redox Signal 2010; 13: 1699-1712.
28. Florea AM, Büsselberg D. Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers 2011; 3: 1351-1371.
29. Cho JM, Manandhar S, Lee HR, Park HM, Kwak MK. Role of the Nrf2-antioxidant system in cy-totoxicity mediated by anticancer cisplatin: implication to cancer cell resistance. Cancer Lett 2008; 260: 96-108.
30. Homma S, Ishii Y, Morishima Y, Yamadori T, Matsuno Y, Haraguchi N, Kikuchi N, Satoh H, Sakamoto T, Hizawa N, Itoh K, Yamamoto M. Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer. Clin Cancer Res 2009; 15: 3423-3432.
31. Wang XJ, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, Chen W, Yi X, Zheng W, Wondrak GT, Wong PK, Zhang DD. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis 2008; 29: 1235-1243.
32. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 2001; 3: 802-808.
33. Kaspar JW, Niture SK, Jaiswal AK. Antioxidant-induced INrf2 (Keap1) tyrosine 85 phosphory-lation controls the nuclear export and degradation of the INrf2-Cul3-Rbx1 complex to allow normal Nrf2 activation and repression. J Cell Sci 2012; 125: 1027-1038.
34. Zhang DD. Ubiquitination of Keap1, a BTB-Kelch Substrate Adaptor Protein for Cul3, Targets Keap1 for Degradation by a Protea-some-independent Pathway. J Biol Chem 2005; 280: 30091-30099.