EGFR and EGFRvIII undergo stress- and EGFR kinase inhibitor-induced mitochondrial translocalization: A potential mechanism of EGFR-driven antagonism of apoptosis

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Cao, Xinyu ^a   Zhu, Hu ^a,c   Ali Osman, Francis ^a,b   Lo, Hui Wen ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE CANCER INSTITUTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOMYCIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; STAUROSPORINE; EPIDERMAL GROWTH FACTOR RECEPTOR VIII; GEFITINIB; MUTANT PROTEIN; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; MITOCHONDRION; PROTEIN LOCALIZATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; PROTEIN TRANSPORT; TUMOR CELL LINE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; APOPTOSIS; CELL LINE, TUMOR; CONSERVED SEQUENCE; DRUG RESISTANCE, NEOPLASM; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 79952347920     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-26     Document Type: Article

References (50)

1. Cohen S, Fava RA, Sawyer ST. Purification and characterization of epidermal growth factor receptor/protein kinase from normal mouse liver. Proc Natl Acad Sci USA 1982, 79:6237-6241. 10.1073/pnas.79.20.6237, 347095, 6983068.
2. Sato JD, Kawamoto T, Le AD, Mendelsohn J, Polikoff J, Sato GH. Biological effects in vitro of monoclonal antibodies to human epidermal growth factor receptors. Mol Biol Med 1983, 1:511-529.
3. Lo HW. EGFR-targeted therapy in malignant glioma: novel aspects and mechanisms of drug resistance. Curr Mol Pharmacol 2010, 3:37-52.
4. Lo HW. Nuclear mode of the EGFR signaling network: biology, prognostic value, and therapeutic implications. Discov Med 2010, 10:44-51.
5. Lo HW, Hung MC. Nuclear EGFR signalling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway and patient survival. Br J Cancer 2006, 94:184-188. 10.1038/sj.bjc.6602941, 2361115, 16434982.
6. Yamazaki H, Ohba Y, Tamaoki N, Shibuya M. A deletion mutation within the ligand binding domain is responsible for activation of epidermal growth factor receptor gene in human brain tumors. Jpn J Cancer Res 1990, 81:773-779.
7. Ekstrand AJ, Sugawa N, James CD, Collins VP. Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc Natl Acad Sci USA 1992, 89:4309-4313. 10.1073/pnas.89.10.4309, 49071, 1584765.
8. Wong AJ, Ruppert JM, Bigner SH, Grzeschik CH, Humphrey PA, Bigner DS, Vogelstein B. Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci USA 1992, 89:2965-2969. 10.1073/pnas.89.7.2965, 48784, 1557402.
9. Sugawa N, Ekstrand AJ, James CD, Collins VP. Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas. Proc Natl Acad Sci USA 1990, 87:8602-8606. 10.1073/pnas.87.21.8602, 55005, 2236070.
10. Wong AJ, Bigner SH, Bigner DD, Kinzler KW, Hamilton SR, Vogelstein B. Increased expression of the epidermal growth factor receptor gene in malignant gliomas is invariably associated with gene amplification. Proc Natl Acad Sci USA 1987, 84:6899-6903. 10.1073/pnas.84.19.6899, 299192, 3477813.
11. Lo HW, Hsu SC, Hung MC. EGFR signaling pathway in breast cancers: from traditional signal transduction to direct nuclear translocalization. Breast Cancer Research and Treatment 2006, 95:211-218. 10.1007/s10549-005-9011-0, 16261406.
12. Lo HW, Cao X, Zhu H, Ali-Osman F. Constitutively activated STAT3 frequently coexpresses with epidermal growth factor receptor in high-grade gliomas and targeting STAT3 sensitizes them to Iressa and alkylators. Clin Cancer Res 2008, 14:6042-6054. 10.1158/1078-0432.CCR-07-4923, 2707832, 18829483.
13. Omuro AMP, Faivre S, Raymond E. Lessons learned in the development of targeted therapy for malignant gliomas. Mol Cancer Ther 2007, 6:1909-1919. 10.1158/1535-7163.MCT-07-0047, 17620423.
14. Reardon DA, Quinn JA, Vredenburgh JJ, Gururangan S, Friedman AH, Desjardins A, Sathornsumetee S, Herndon JE, Dowell JM, McLendon RE, et al. Phase 1 trial of gefitinib plus sirolimus in adults with recurrent malignant glioma. Clin Cancer Res 2006, 12:860-868. 10.1158/1078-0432.CCR-05-2215, 16467100.
15. Friedman HS, Bigner DD. Glioblastoma multiforme and the epidermal growth factor receptor. N Engl J Med 2005, 353:1997-1999. 10.1056/NEJMp058186, 16282174.
16. van den Bent MJ, Brandes AA, Rampling R, Kouwenhoven MC, Kros JM, Carpentier AF, Clement PM, Frenay M, Campone M, Baurain JF, et al. Randomized phase II trial of erlotinib versus temozolomide or carmustine in recurrent glioblastoma: EORTC brain tumor group study 26034. J Clin Oncol 2009, 27:1268-1274. 10.1200/JCO.2008.17.5984, 2667826, 19204207.
17. Thiessen B, Stewart C, Tsao M, Kamel-Reid S, Schaiquevich P, Mason W, Easaw J, Belanger K, Forsyth P, McIntosh L, Eisenhauer E. A phase I/II trial of GW572016 (lapatinib) in recurrent glioblastoma multiforme: clinical outcomes, pharmacokinetics and molecular correlation. Cancer Chemother Pharmacol 2009, 65:353-361.
18. Reardon DA, Desjardins A, Vredenburgh JJ, Gururangan S, Friedman AH, Herndon JE, Marcello J, Norfleet JA, McLendon RE, Sampson JH, Friedman HS. Phase 2 trial of erlotinib plus sirolimus in adults with recurrent glioblastoma. J Neurooncol 2010, 96:219-230. 10.1007/s11060-009-9950-0, 2844073, 19562254.
19. Lo HW, Hsu SC, Ali-Seyed M, Gunduz M, Xia W, Wei Y, Bartholomeusz G, Shih JY, Hung MC. Nuclear Interaction of EGFR and STAT3 in the Activation of iNOS/NO Pathway. Cancer Cell 2005, 7:575-589. 10.1016/j.ccr.2005.05.007, 15950906.
20. Zhu H, Cao X, Ali-Osman F, Keir S, Lo HW. EGFR and EGFRvIII interact with PUMA to inhibit mitochondrial translocalization of PUMA and PUMA-mediated apoptosis independent of EGFR kinase activity. Cancer Lett 2010, 294:101-110. 10.1016/j.canlet.2010.01.028, 20153921.
21. Guillamo JS, de Bouard S, Valable S, Marteau L, Leuraud P, Marie Y, Poupon MF, Parienti JJ, Raymond E, Peschanski M. Molecular mechanisms underlying effects of epidermal growth factor receptor inhibition on invasion, proliferation, and angiogenesis in experimental glioma. Clin Cancer Res 2009, 15:3697-3704. 10.1158/1078-0432.CCR-08-2042, 19435839.
22. Mellinghoff IK, Cloughesy TF, Mischel PS. PTEN-Mediated Resistance to Epidermal Growth Factor Receptor Kinase Inhibitors. Clin Cancer Res 2007, 13:378-381. 10.1158/1078-0432.CCR-06-1992, 17255257.
23. 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. 10.1038/ncb0901-802, 11533659.
24. Lo HW, Cao X, Zhu H, Ali-Osman F. Cyclooxygenase-2 is a novel transcriptional target of the nuclear EGFR-STAT3 and EGFRvIII-STAT3 signaling axes. Mol Cancer Res 2010, 8:232-245. 10.1158/1541-7786.MCR-09-0391, 2824777, 20145033.
25. Lo HW, Xia W, Wei Y, Ali-Seyed M, Huang SF, Hung MC. Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Res 2005, 65:338-348.
26. Boerner JL, Demory ML, Silva C, Parsons SJ. Phosphorylation of Y845 on the epidermal growth factor receptor mediates binding to the mitochondrial protein cytochrome c oxidase subunit II. Mol Cell Biol 2004, 24:7059-7071. 10.1128/MCB.24.16.7059-7071.2004, 479738, 15282306.
27. Demory ML, Boerner JL, Davidson R, Faust W, Miyake T, Lee I, Hüttemann M, Douglas R, Haddad G, Parsons SJ. Epidermal Growth Factor Receptor Translocation to the Mitochondria. Journal of Biological Chemistry 2009, 284:36592-36604. 10.1074/jbc.M109.000760, 2794774, 19840943.
28. Bigner SH, Humphrey PA, Wong AJ, Vogelstein B, Mark J, Friedman HS, Bigner DD. Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res 1990, 50:8017-8022.
29. Wang Y, Lyu YL, Wang JC. Dual localization of human DNA topoisomerase IIIalpha to mitochondria and nucleus. Proc Natl Acad Sci USA 2002, 99:12114-12119. 10.1073/pnas.192449499, 129407, 12209014.
30. Kutay U, Guttinger S. Leucine-rich nuclear-export signals: born to be weak. Trends Cell Biol 2005, 15:121-124. 10.1016/j.tcb.2005.01.005, 15752974.
31. la Cour T, Gupta R, Rapacki K, Skriver K, Poulsen FM, Brunak S. NESbase version 1.0: a database of nuclear export signals. Nucleic Acids Res 2003, 31:393-396. 10.1093/nar/gkg101, 165548, 12520031.
32. Cordero JB, Cozzolino M, Lu Y, Vidal M, Slatopolsky E, Stahl PD, Barbieri MA, Dusso A. 1,25-Dihydroxyvitamin D down-regulates cell membrane growth- and nuclear growth-promoting signals by the epidermal growth factor receptor. J Biol Chem 2002, 277:38965-38971. 10.1074/jbc.M203736200, 12181310.
33. Wang SC, Hung MC. Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin Cancer Res 2009, 15:6484-6489. 10.1158/1078-0432.CCR-08-2813, 19861462.
34. Psyrri A, Yu Z, Weinberger PM, Sasaki C, Haffty B, Camp R, Rimm D, Burtness BA. Quantitative determination of nuclear and cytoplasmic epidermal growth factor receptor expression in oropharyngeal squamous cell cancer by using automated quantitative analysis. Clin Cancer Res 2005, 11:5856-5862. 10.1158/1078-0432.CCR-05-0420, 16115926.
35. Wang SC, Nakajima Y, Yu YL, Xia W, Chen CT, Yang CC, McIntush EW, Li LY, Hawke DH, Kobayashi R, Hung MC. Tyrosine phosphorylation controls PCNA function through protein stability. Nat Cell Biol 2006, 8:1359-1368. 10.1038/ncb1501, 17115032.
36. Xia W, Wei Y, Du Y, Liu J, Chang B, Yu YL, Huo LF, Miller S, Hung MC. Nuclear expression of epidermal growth factor receptor is a novel prognostic value in patients with ovarian cancer. Mol Carcinog 2009, 48:610-617. 10.1002/mc.20504, 2718429, 19058255.
37. Yue X, Song W, Zhang W, Chen L, Xi Z, Xin Z, Jiang X. Mitochondrially localized EGFR is subjected to autophagic regulation and implicated in cell survival. Autophagy 2008, 4:641-649.
38. De Potter CR, Quatacker J, Maertens G, Van Daele S, Pauwels C, Verhofstede C, Eechaute W, Roels H. The subcellular localization of the neu protein in human normal and neoplastic cells. Int J Cancer 1989, 44:969-974. 10.1002/ijc.2910440604, 2575084.
39. Vidal GA, Naresh A, Marrero L, Jones FE. Presenilin-dependent gamma-secretase processing regulates multiple ERBB4/HER4 activities. J Biol Chem 2005, 280:19777-19783. 10.1074/jbc.M412457200, 15746097.
40. Naresh A, Long W, Vidal GA, Wimley WC, Marrero L, Sartor CI, Tovey S, Cooke TG, Bartlett JMS, Jones FE. The ERBB4/HER4 Intracellular Domain 4ICD Is a BH3-Only Protein Promoting Apoptosis of Breast Cancer Cells. Cancer Res 2006, 66:6412-6420. 10.1158/0008-5472.CAN-05-2368, 16778220.
41. Liao HJ, Carpenter G. Role of the Sec61 translocon in EGF receptor trafficking to the nucleus and gene expression. Mol Biol Cell 2007, 18:1064-1072. 10.1091/mbc.E06-09-0802, 1805100, 17215517.
42. Lo HW, Ali-Seyed M, Wu Y, Bartholomeusz G, Hsu SC, Hung MC. Nuclear-cytoplasmic transport of EGFR involves receptor endocytosis, importin beta1 and CRM1. J Cell Biochem 2006, 98:1570-1583. 10.1002/jcb.20876, 16552725.
43. Marchenko ND, Zaika A, Moll UM. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 2000, 275:16202-16212. 10.1074/jbc.275.21.16202, 10821866.
44. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 2003, 11:577-590. 10.1016/S1097-2765(03)00050-9, 12667443.
45. Sansome C, Zaika A, Marchenko ND, Moll UM. Hypoxia death stimulus induces translocation of p53 protein to mitochondria. Detection by immunofluorescence on whole cells. FEBS Lett 2001, 488:110-115. 10.1016/S0014-5793(00)02368-1, 11163756.
46. Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, Raina D, Chen W, Kharbanda S, Kufe D. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 2004, 5:163-175. 10.1016/S1535-6108(04)00020-0, 14998492.
47. Ren J, Bharti A, Raina D, Chen W, Ahmad R, Kufe D. MUC1 oncoprotein is targeted to mitochondria by heregulin-induced activation of c-Src and the molecular chaperone HSP90. Oncogene 2006, 25:20-31.
48. Zhao Y, Chaiswing L, Velez JM, Batinic-Haberle I, Colburn NH, Oberley TD, St Clair DK. p53 translocation to mitochondria precedes its nuclear translocation and targets mitochondrial oxidative defense protein-manganese superoxide dismutase. Cancer Res 2005, 65:3745-3750. 10.1158/0008-5472.CAN-04-3835, 15867370.
49. Lo H-W, Hsu S-C, Xia W, Cao X, Shih J-Y, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung M-C. Epidermal Growth Factor Receptor Cooperates with Signal Transducer and Activator of Transcription 3 to Induce Epithelial-Mesenchymal Transition in Cancer Cells via Up-regulation of TWIST Gene Expression. Cancer Res 2007, 67:9066-9076. 10.1158/0008-5472.CAN-07-0575, 2570961, 17909010.
50. Lo HW, Zhu H, Cao X, Aldrich A, Ali-Osman F. A novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion. Cancer Res 2009, 69:6790-6798. 10.1158/0008-5472.CAN-09-0886, 2771365, 19706761.