Implication of nuclear EGFR in the development of resistance to anticancer therapies

BioMedicine (Netherlands)

Volumn 1, Issue 1, 2011, Pages 2-10

  Huang, Wei Chien ^a,b,c   Chen, Yun Ju ^a,d,e   Hung, Mien Chie ^a,b,f  

^a CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c ASIA UNIVERSITY   (Taiwan)

^d E DA HOSPITAL   (Taiwan)

^e I SHOU UNIVERSITY   (Taiwan)

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

Author keywords

Anticancer therapies; Drug resistance; Nuclear EGFR

Indexed keywords

CETUXIMAB; DNA DEPENDENT PROTEIN KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; IRINOTECAN; KARYOPHERIN ALPHA; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PROTEIN TYROSINE KINASE;

CANCER CHEMOTHERAPY; CANCER RESISTANCE; CARCINOGENESIS; CELL MIGRATION; COLORECTAL CANCER; DNA REPAIR; DRUG RESPONSE; DRUG TRANSPORT; DRUG TREATMENT FAILURE; ENZYME ACTIVATION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; IONIZING RADIATION; LUNG NON SMALL CELL CANCER; METASTASIS; NONHUMAN; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; OUTCOME ASSESSMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RADIOSENSITIVITY; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 84861184230     PISSN: 22118020     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomed.2011.10.001     Document Type: Review

References (87)

1. Hynes N.E., Lane H.A. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 2005, 5:341-354.
2. Holbro T., Hynes N.E. ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 2004, 44:195-217.
3. Yarden Y., Sliwkowski M.X. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001, 2:127-137.
4. Schlessinger J. Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 2004, 306:1506-1507.
5. Yu H., Jove R. The STATs of cancer - new molecular targets come of age. Nat Rev Cancer 2004, 4:97-105.
6. Ishizawar R., Parsons S.J. c-Src and cooperating partners in human cancer. Cancer Cell 2004, 6:209-214.
7. Bjornsti M.A., Houghton P.J. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 2004, 4:335-348.
8. Lo H.W., Hsu S.C., Ali-Seyed M., Gunduz M., Xia W., Wei Y., et al. Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell 2005, 7:575-589.
9. Lo H.W., 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. Lin S.Y., Makino K., Xia W., Matin A., Wen Y., Kwong K.Y., et al. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 2001, 3:802-808.
11. Xie Y., Hung M.C. Nuclear localization of p185neu tyrosine kinase and its association with transcriptional transactivation. Biochem Biophys Res Commun 1994, 203:1589-1598.
12. Wang S.C., Lien H.C., Xia W., Chen I.F., Lo H.W., Wang Z., et al. Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2. Cancer Cell 2004, 6:251-261.
13. Wang S.C., Nakajima Y., Yu Y.L., Xia W., Chen C.T., Yang C.C., et al. Tyrosine phosphorylation controls PCNA function through protein stability. Nat Cell Biol 2006, 8:1359-1368.
14. Dittmann K., Mayer C., Fehrenbacher B., Schaller M., Raju U., Milas L., et al. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 2005, 280:31182-31189.
15. Chen D.J., Nirodi C.S. The epidermal growth factor receptor: a role in repair of radiation-induced DNA damage. Clin Cancer Res 2007, 13:6555-6560.
16. Dittmann K., Mayer C., Fehrenbacher B., Schaller M., Kehlbach R., Rodemann H.P. Nuclear epidermal growth factor receptor modulates cellular radio-sensitivity by regulation of chromatin access. Radiother Oncol 2011, 99:317-322.
17. Li L.Y., Chen H., Hsieh Y.H., Wang Y.N., Chu H.J., Chen Y.H., et al. Nuclear ErbB2 enhances translation and cell growth by activating transcription of ribosomal RNA genes. Cancer Res 2011, 71:4269-4279.
18. Wanner G., Mayer C., Kehlbach R., Rodemann H.P., Dittmann K. Activation of protein kinase C epsilon stimulates DNA-repair via epidermal growth factor receptor nuclear accumulation. Radiother Oncol 2008, 86:383-390.
19. Hsu S.C., Miller S.A., Wang Y., Hung M.C. Nuclear EGFR is required for cisplatin resistance and DNA repair. Am J Transl Res 2009, 1:249-258.
20. Li C., Iida M., Dunn E.F., Ghia A.J., Wheeler D.L. Nuclear EGFR contributes to acquired resistance to cetuximab. Oncogene 2009, 28:3801-3813.
21. Huang W.C., Chen Y.J., Li L.Y., Wei Y.L., Hsu S.C., Tsai S.L., et al. Nuclear translocation of EGFR by AKT-dependent phosphorylation enhances BCRP/ABCG2 expression in gefitinib-resistant cells. J Biol Chem 2011, 286:20558-20568.
22. Dittmann K., Mayer C., Kehlbach R., Rothmund M.C., Peter Rodemann H. Radiation-induced lipid peroxidation activates src kinase and triggers nuclear EGFR transport. Radiother Oncol 2009, 92:379-382.
23. Dittmann K., Mayer C., Fehrenbacher B., Schaller M., Kehlbach R., Rodemann H.P. Nuclear EGFR shuttling induced by ionizing radiation is regulated by phosphorylation at residue Thr654. FEBS Lett 2010, 584:3878-3884.
24. Marti U., Burwen S.J., Wells A., Barker M.E., Huling S., Feren A.M., et al. Localization of epidermal growth factor receptor in hepatocyte nuclei. Hepatology 1991, 13:15-20.
25. Marti U., Ruchti C., Kampf J., Thomas G.A., Williams E.D., Peter H.J., et al. Nuclear localization of epidermal growth factor and epidermal growth factor receptors in human thyroid tissues. Thyroid 2001, 11:137-145.
26. Cordero J.B., Cozzolino M., Lu Y., Vidal M., Slatopolsky E., Stahl P.D., et al. 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.
27. Hanada N., Lo H.W., Day C.P., Pan Y., Nakajima Y., Hung M.C. Co-regulation of B-Myb expression by E2F1 and EGF receptor. Mol Carcinog 2006, 45:10-17.
28. Lo H.W., Xia W., Wei Y., Ali-Seyed M., Huang S.F., Hung M.C. Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Res 2005, 65:338-348.
29. Psyrri A., Yu Z., Weinberger P.M., Sasaki C., Haffty B., Camp R., et al. 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.
30. Xia W., Wei Y., Du Y., Liu J., Chang B., Yu Y.L., et al. Nuclear expression of epidermal growth factor receptor is a novel prognostic value in patients with ovarian cancer. Mol Carcinog 2009, 48:610-617.
31. Xu Y., Shao Y., Zhou J., Voorhees J.J., Fisher G.J. Ultraviolet irradiation-induces epidermal growth factor receptor (EGFR) nuclear translocation in human keratinocytes. J Cell Biochem 2009, 107:873-880.
32. Hung L.Y., Tseng J.T., Lee Y.C., Xia W., Wang Y.N., Wu M.L., et al. Nuclear epidermal growth factor receptor (EGFR) interacts with signal transducer and activator of transcription 5 (STAT5) in activating Aurora-A gene expression. Nucleic Acids Res 2008, 36:4337-4351.
33. Huo L., Wang Y.N., Xia W., Hsu S.C., Lai C.C., Li L.Y., et al. RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc Natl Acad Sci USA 2010, 107:16125-16130.
34. Bandyopadhyay D., Mandal M., Adam L., Mendelsohn J., Kumar R. Physical interaction between epidermal growth factor receptor and DNA-dependent protein kinase in mammalian cells. J Biol Chem 1998, 273:1568-1573.
35. Um J.H., Kwon J.K., Kang C.D., Kim M.J., Ju D.S., Bae J.H., et al. Relationship between antiapoptotic molecules and metastatic potency and the involvement of DNA-dependent protein kinase in the chemosensitization of metastatic human cancer cells by epidermal growth factor receptor blockade. J Pharmacol Exp Ther 2004, 311:1062-1070.
36. Liccardi G., Hartley J.A., Hochhauser D. EGFR nuclear translocation modulates DNA repair following cisplatin and ionizing radiation treatment. Cancer Res 2011, 71:1103-1114.
37. Hadzisejdic I., Mustac E., Jonjic N., Petkovic M., Grahovac B. Nuclear EGFR in ductal invasive breast cancer: correlation with cyclin-D1 and prognosis. Mod Pathol 2010, 23:392-403.
38. Hoshino M., Fukui H., Ono Y., Sekikawa A., Ichikawa K., Tomita S., et al. Nuclear expression of phosphorylated EGFR is associated with poor prognosis of patients with esophageal squamous cell carcinoma. Pathobiology 2007, 74:15-21.
39. Hsu S.C., Hung M.C. Characterization of a novel tripartite nuclear localization sequence in the EGFR family. J Biol Chem 2007, 282:10432-10440.
40. Wang Y.N., Wang H., Yamaguchi H., Lee H.J., Lee H.H., Hung M.C. COPI-mediated retrograde trafficking from the Golgi to the ER regulates EGFR nuclear transport. Biochem Biophys Res Commun 2010, 399:498-504.
41. Li C., Iida M., Dunn E.F., Wheeler D.L. Dasatinib blocks cetuximab- and radiation-induced nuclear translocation of the epidermal growth factor receptor in head and neck squamous cell carcinoma. Radiother Oncol 2010, 97:330-337.
42. Li F., Yang W., Guo D., Hu Z., Xu H., Ye Z. LRIG1 combined with cisplatin enhances bladder cancer lesions via a novel pathway. Oncol Rep 2011, 25:1629-1637.
43. Lynch T.J., Bell D.W., Sordella R., Gurubhagavatula S., Okimoto R.A., Brannigan B.W., et al. 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.
44. Chen Y.J., Huang W.C., Wei Y.L., Hsu S.C., Yuan P., Lin H.Y., et al. Elevated BCRP/ABCG2 expression confers acquired resistance to gefitinib in wild-type EGFR-expressing cells. PLoS One 2011, 6:e21428.
45. Wang Y.N., Yamaguchi H., Huo L., Du Y., Lee H.J., Lee H.H., et al. The translocon Sec61beta localized in the inner nuclear membrane transports membrane-embedded EGF receptor to the nucleus. J Biol Chem 2010, 285:38720-38729.
46. Batra S.K., Castelino-Prabhu S., Wikstrand C.J., Zhu X., Humphrey P.A., Friedman H.S., et al. Epidermal growth factor ligand-independent, unregulated, cell-transforming potential of a naturally occurring human mutant EGFRvIII gene. Cell Growth Differ 1995, 6:1251-1259.
47. Lo H.W., 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.
48. de la Iglesia N., Konopka G., Puram S.V., Chan J.A., Bachoo R.M., You M.J., et al. Identification of a PTEN-regulated STAT3 brain tumor suppressor pathway. Genes Dev 2008, 22:449-462.
49. Lo H.W. EGFR-targeted therapy in malignant glioma: novel aspects and mechanisms of drug resistance. Curr Mol Pharmacol 2010, 3:37-52.
50. Huang S.M., Harari P.M. Modulation of radiation response after epidermal growth factor receptor blockade in squamous cell carcinomas: inhibition of damage repair, cell cycle kinetics, and tumor angiogenesis. Clin Cancer Res 2000, 6:2166-2174.
51. Harari P.M., Huang S.M. Modulation of molecular targets to enhance radiation. Clin Cancer Res 2000, 6:323-325.
52. Wang Y.N., Yamaguchi H., Hsu J.M., Hung M.C. Nuclear trafficking of the epidermal growth factor receptor family membrane proteins. Oncogene 2010, 29:3997-4006.
53. Xu D., Farmer A., Chook Y.M. Recognition of nuclear targeting signals by karyopherin-beta proteins. Curr Opin Struct Biol 2010, 20:782-790.
54. Lo H.W., Ali-Seyed M., Wu Y., Bartholomeusz G., Hsu S.C., Hung M.C. Nuclear-cytoplasmic transport of EGFR involves receptor endocytosis, importin beta1 and CRM1. J Cell Biochem 2006, 98:1570-1583.
55. Giri D.K., Ali-Seyed M., Li L.Y., Lee D.F., Ling P., Bartholomeusz G., et al. Endosomal transport of ErbB-2: mechanism for nuclear entry of the cell surface receptor. Mol Cell Biol 2005, 25:11005-11018.
56. Gluz O., Wild P., Meiler R., Diallo-Danebrock R., Ting E., Mohrmann S., et al. Nuclear karyopherin alpha2 expression predicts poor survival in patients with advanced breast cancer irrespective of treatment intensity. Int J Cancer 2008, 123:1433-1438.
57. Bao J., Alroy I., Waterman H., Schejter E.D., Brodie C., Gruenberg J., et al. Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J Biol Chem 2000, 275:26178-26186.
58. Wheeler D.L., Huang S., Kruser T.J., Nechrebecki M.M., Armstrong E.A., Benavente S., et al. Mechanisms of acquired resistance to cetuximab: role of HER (ErbB) family members. Oncogene 2008, 27:3944-3956.
59. Paez J.G., Janne P.A., Lee J.C., Tracy S., Greulich H., Gabriel S., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004, 304:1497-1500.
60. Engelman J.A., Zejnullahu K., Mitsudomi T., Song Y., Hyland C., Park J.O., et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
61. Engelman J.A., Janne P.A. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2008, 14:2895-2899.
62. Guillamo J.S., de Bouard S., Valable S., Marteau L., Leuraud P., Marie Y., et al. 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.
63. Mellinghoff I.K., Cloughesy T.F., Mischel P.S. PTEN-mediated resistance to epidermal growth factor receptor kinase inhibitors. Clin Cancer Res 2007, 13:378-381.
64. Guix M., Faber A.C., Wang S.E., Olivares M.G., Song Y., Qu S., et al. Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 2008, 118:2609-2619.
65. Cappuzzo F., Toschi L., Tallini G., Ceresoli G.L., Domenichini I., Bartolini S., et al. Insulin-like growth factor receptor 1 (IGFR-1) is significantly associated with longer survival in non-small-cell lung cancer patients treated with gefitinib. Ann Oncol 2006, 17:1120-1127.
66. Das A.K., Chen B.P., Story M.D., Sato M., Minna J.D., Chen D.J., et al. Somatic mutations in the tyrosine kinase domain of epidermal growth factor receptor (EGFR) abrogate EGFR-mediated radioprotection in non-small cell lung carcinoma. Cancer Res 2007, 67:5267-5274.
67. Huang W.C., Chen W.S., Chen Y.J., Wang L.Y., Hsu S.C. Hepatitis B virus X protein induces IKKalpha nuclear translocation via Akt-dependent phosphorylation to promote the motility of hepatocarcinoma cells. J Cell Physiol 2011, 10.1002/jcp.22860.
68. Geetha T., Kenchappa R.S., Wooten M.W., Carter B.D. TRAF6-mediated ubiquitination regulates nuclear translocation of NRIF, the p75 receptor interactor 1. EMBO J 2005, 24:3859-3868.
69. Lohrum M.A., Woods D.B., Ludwig R.L., Balint E., Vousden K.H. C-terminal ubiquitination of p53 contributes to nuclear export 2. Mol Cell Biol 2001, 21:8521-8532.
70. Massoumi R., Chmielarska K., Hennecke K., Pfeifer A., Fassler R. Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling 2. Cell 2006, 125:665-677.
71. Trotman L.C., Wang X., Alimonti A., Chen Z., Teruya-Feldstein J., Yang H., et al. Ubiquitination regulates PTEN nuclear import and tumor suppression 1. Cell 2007, 128:141-156.
72. Dittmann K.H., Mayer C., Ohneseit P.A., Raju U., Andratschke N.H., Milas L., et al. Celecoxib induced tumor cell radiosensitization by inhibiting radiation induced nuclear EGFR transport and DNA-repair: a COX-2 independent mechanism. Int J Radiat Oncol Biol Phys 2008, 70:203-212.
73. Kucab J.E., Lee C., Chen C.S., Zhu J., Gilks C.B., Cheang M., et al. Celecoxib analogues disrupt Akt signaling, which is commonly activated in primary breast tumours. Breast Cancer Res 2005, 7:R796-R807.
74. Kuo M.T. Roles of multidrug resistance genes in breast cancer chemoresistance. Adv Exp Med Biol 2007, 608:23-30.
75. Takara K., Sakaeda T., Okumura K. An update on overcoming MDR1-mediated multidrug resistance in cancer chemotherapy. Curr Pharm Des 2006, 12:273-286.
76. Yoh K., Ishii G., Yokose T., Minegishi Y., Tsuta K., Goto K., et al. Breast cancer resistance protein impacts clinical outcome in platinum-based chemotherapy for advanced non-small cell lung cancer. Clin Cancer Res 2004, 10:1691-1697.
77. Usuda J., Ohira T., Suga Y., Oikawa T., Ichinose S., Inoue T., et al. Breast cancer resistance protein (BCRP) affected acquired resistance to gefitinib in a "never-smoked" female patient with advanced non-small cell lung cancer. Lung Cancer 2007, 58:296-299.
78. Sugimoto Y., Tsukahara S., Ishikawa E., Mitsuhashi J. Breast cancer resistance protein: molecular target for anticancer drug resistance and pharmacokinetics/pharmacodynamics. Cancer Sci 2005, 96:457-465.
79. Elkind N.B., Szentpetery Z., Apati A., Ozvegy-Laczka C., Varady G., Ujhelly O., et al. Multidrug transporter ABCG2 prevents tumor cell death induced by the epidermal growth factor receptor inhibitor Iressa (ZD1839, Gefitinib). Cancer Res 2005, 65:1770-1777.
80. Jaganathan S., Yue P., Paladino D.C., Bogdanovic J., Huo Q., Turkson J. A functional nuclear epidermal growth factor receptor, SRC and Stat3 heteromeric complex in pancreatic cancer cells. PLoS One 2011, 6:e19605.
81. Zhao H., Lo Y.H., Ma L., Waltz S.E., Gray J.K., Hung M.C., et al. Targeting tyrosine phosphorylation of PCNA inhibits prostate cancer growth. Mol Cancer Ther 2011, 10:29-36.
82. Xu S., Kitayama J., Yamashita H., Souma D., Nagawa H. Nuclear translocation of HER-4/c-erbB-4 is significantly correlated with prognosis of esophageal squamous cell carcinoma. J Surg Oncol 2008, 97:44-50.
83. Sardi S.P., Murtie J., Koirala S., Patten B.A., Corfas G. Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 2006, 127:185-197.
84. Carpenter G. Nuclear localization and possible functions of receptor tyrosine kinases. Curr Opin Cell Biol 2003, 15:143-148.
85. Ni C.Y., Murphy M.P., Golde T.E., Carpenter G. γ-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 2001, 294:2179-2181.
86. Srinivasan R., Gillett C.E., Barnes D.M., Gullick W.J. Nuclear expression of the c-erbB-4/HER-4 growth factor receptor in invasive breast cancers. Cancer Res 2000, 60:1483-1487.
87. Maher P.A. Nuclear translocation of fibroblast growth factor (FGF) receptors in response to FGF-2. J Cell Biol 1996, 134:529-536.