Membrane-bound trafficking regulates nuclear transport of integral epidermal growth factor receptor (EGFR) and ErbB-2

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16869-16879

  Wang, Ying Nai ^a,c   Lee, Heng Huan ^a,b   Lee, Hong Jen ^a,b   Du, Yi ^a,b   Yamaguchi, Hirohito ^a   Hung, Mien Chie ^a,b,c  

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

^b UNIVERSITY OF TEXAS   (United States)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTORS; CELL SURFACES; ENDOPLASMIC RETICULUM; EPIDERMAL GROWTH FACTOR RECEPTORS; FGF RECEPTORS; INNER NUCLEAR MEMBRANES; MEMBRANE-BOUND; NUCLEAR ENVELOPE; NUCLEAR LOCALIZATION; NUCLEAR TRANSPORT; PERMEABILIZATION; RECEPTOR-TYROSINE KINASE;

AMINO ACIDS; CYTOLOGY;

CELL MEMBRANES;

CELL SURFACE PROTEIN; DIGITONIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1;

ARTICLE; BIOTINYLATION; CELL FRACTIONATION; CELL NUCLEUS; CELL PERMEABILIZATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; FRACTIONATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOELECTRON MICROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM;

3T3 CELLS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DIGITONIN; HUMANS; INDICATORS AND REAGENTS; MICE; NUCLEAR ENVELOPE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2;

EID: 84860872206     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.314799     Document Type: Article

References (44)

1. Wang, S. C., and Hung, M. C. (2009) Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin. Cancer Res. 15, 6484-6489
2. Wells, A., and Marti, U. (2002) Signaling shortcuts: cell-surface receptors in the nucleus? Nat. Rev. Mol. Cell Biol. 3, 697-702 (Pubitemid 34987790)
3. Dittmann, K., Mayer, C., Fehrenbacher, B., Schaller, M., Kehlbach, R., and Rodemann, H. P. (2010) Nuclear EGFR shuttling induced by ionizing radiation is regulated by phosphorylation at residue Thr654. FEBS Lett. 584, 3878-3884
4. Huo, L., Wang, Y. N., Xia, W., Hsu, S. C., Lai, C. C., Li, L. Y., Chang, W. C., Wang, Y., Hsu, M. C., Yu, Y. L., Huang, T. H., Ding, Q., Chen, C. H., Tsai, C. H., and Hung, M. C. (2010) RNA helicase A is a DNA-binding partner for EGFR-mediated transcriptional activation in the nucleus. Proc. Natl. Acad. Sci. U.S.A. 107, 16125-16130
5. Wang, S. C., Nakajima, Y., Yu, Y. L., Xia, W., Chen, C. T., Yang, C. C., McIntush, E. W., Li, L. Y., Hawke, D. H., Kobayashi, R., and Hung, M. C. (2006) Tyrosine phosphorylation controls PCNA function through protein stability. Nat. Cell Biol. 8, 1359-1368 (Pubitemid 44835110)
6. Massie, C., and Mills, I. G. (2006) The developing role of receptors and adaptors. Nat. Rev. Cancer 6, 403-409
7. Lin, S. Y., Makino, K., Xia, W., Matin, A., Wen, Y., Kwong, K. Y., Bourguignon, L., and Hung, M. C. (2001) Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat. Cell Biol. 3, 802-808 (Pubitemid 32842685)
8. Wang, S. C., Lien, H. C., Xia, W., Chen, I. F., Lo, H. W., Wang, Z., Ali- Seyed, M., Lee, D. F., Bartholomeusz, G., Ou-Yang, F., Giri, D. K., and Hung, M. C. (2004) Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2. Cancer Cell 6, 251-261 (Pubitemid 39222038)
9. Li, L. Y., Chen, H., Hsieh, Y. H., Wang, Y. N., Chu, H. J., Chen, Y. H., Chen, H. Y., Chien, P. J., Ma, H. T., Tsai, H. C., Lai, C. C., Sher, Y. P., Lien, H. C., Tsai, C. H., and Hung, M. C. (2011) Nuclear ErbB2 enhances translation and cell growth by activating transcription of ribosomal RNA genes. Cancer Res. 71, 4269-4279
10. Huang, W. C., Chen, Y. J., Li, L. Y., Wei, Y. L., Hsu, S. C., Tsai, S. L., Chiu, P. C., Huang, W. P., Wang, Y. N., Chen, C. H., Chang, W. C., Chang, W. C., Chen, A. J., Tsai, C. H., and Hung, M. C. (2011) Nuclear translocation of epidermal growth factor receptor by Akt-dependent phosphorylation enhances breast cancer-resistant protein expression in gefitinib-resistant cells. J. Biol. Chem. 286, 20558-20568
11. Hadzisejdić, I., Mustać, E., Jonjić, N., Petković, M., and Grahovac, B. (2010) Nuclear EGFR in ductal invasive breast cancer: correlation with cyclin-D1 and prognosis. Mod. Pathol. 23, 392-403
12. Hoshino, M., Fukui, H., Ono, Y., Sekikawa, A., Ichikawa, K., Tomita, S., Imai, Y., Imura, J., Hiraishi, H., and Fujimori, T. (2007) Nuclear expression of phosphorylated EGFR is associated with poor prognosis of patients with esophageal squamous cell carcinoma. Pathobiology 74, 15-21 (Pubitemid 46742314)
13. Lo, H. W., Xia, W., Wei, Y., Ali-Seyed, M., Huang, S. F., and Hung, M. C. (2005) Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Res. 65, 338-348 (Pubitemid 40070827)
14. Psyrri, A., Egleston, B., Weinberger, P., Yu, Z., Kowalski, D., Sasaki, C., Haffty, B., Rimm, D., and Burtness, B. (2008) Correlates and determinants of nuclear epidermal growth factor receptor content in an oropharyngeal cancer tissue microarray. Cancer Epidemiol Biomarkers Prev 17, 1486-1492
15. Psyrri, A., Yu, Z., Weinberger, P. M., Sasaki, C., Haffty, B., Camp, R., Rimm, D., and Burtness, B. A. (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 (Pubitemid 41170313)
16. Xia, W., Wei, Y., Du, Y., Liu, J., Chang, B., Yu, Y. L., Huo, L. F., Miller, S., and Hung, M. C. (2009) Nuclear expression of epidermal growth factor receptor is a novel prognostic value in patients with ovarian cancer. Mol. Carcinog 48, 610-617
17. Wang, Y. N., Wang, H., Yamaguchi, H., Lee, H. J., Lee, H. H., and Hung, M. C. (2010) COPI-mediated retrograde trafficking from the Golgi to the ER regulates EGFR nuclear transport. Biochem. Biophys. Res. Commun. 399, 498-504
18. Wang, Y. N., Yamaguchi, H., Hsu, J. M., and Hung, M. C. (2010) Nuclear trafficking of the epidermal growth factor receptor family membrane proteins. Oncogene 29, 3997-4006
19. Wang, Y. N., Yamaguchi, H., Huo, L., Du, Y., Lee, H. J., Lee, H. H., Wang, H., Hsu, J. M., and Hung, M. C. (2010) The translocon Sec61β localized in the inner nuclear membrane transports membrane-embedded EGF receptor to the nucleus. J. Biol. Chem. 285, 38720-38729
20. Cook, A., Bono, F., Jinek, M., and Conti, E. (2007) Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 76, 647-671
21. Harel, A., and Forbes, D. J. (2004) Importin β: conducting a much larger cellular symphony. Mol. Cell 16, 319-330 (Pubitemid 39504787)
22. Reilly, J. F., and Maher, P. A. (2001) Importin β-mediated nuclear import of fibroblast growth factor receptor: role in cell proliferation. J. Cell Biol. 152, 1307-1312 (Pubitemid 34280187)
23. Giri, D. K., Ali-Seyed, M., Li, L. Y., Lee, D. F., Ling, P., Bartholomeusz, G., Wang, S. C., and Hung, M. C. (2005) Endosomal transport of ErbB-2: mechanism for nuclear entry of the cell surface receptor. Mol. Cell. Biol. 25, 11005-11018 (Pubitemid 41747142)
24. Stachowiak, M. K., Maher, P. A., and Stachowiak, E. K. (2007) Integrative nuclear signaling in cell development-a role for FGF receptor-1.DNACell Biol. 26, 811-826 (Pubitemid 350274413)
25. Liao, H. J., and Carpenter, G. (2007) Role of the Sec61 translocon in EGF receptor trafficking to the nucleus and gene expression. Mol. Biol. Cell 18, 1064-1072
26. Borradaile, N. M., Han, X., Harp, J. D., Gale, S. E., Ory, D. S., and Schaffer, J. E. (2006) Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J. Lipid Res. 47, 2726-2737 (Pubitemid 44936086)
27. Nigam, S. K., Goldberg, A. L., Ho, S., Rohde, M. F., Bush, K. T., and Sherman, M. (1994) A set of endoplasmic reticulum proteins possessing properties of molecular chaperones includes Ca(2+)-binding proteins and members of the thioredoxin superfamily. J. Biol. Chem. 269, 1744-1749
28. Adam, S. A., Marr, R. S., and Gerace, L. (1990) Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111, 807-816
29. Kiyokawa, N., Lee, E. K., Karunagaran, D., Lin, S. Y., and Hung, M. C. (1997) Mitosis-specific negative regulation of epidermal growth factor receptor, triggered by a decrease in ligand binding and dimerization, can be overcome by overexpression of receptor. J. Biol. Chem. 272, 18656-18665 (Pubitemid 27318208)
30. Görlich, D., Vogel, F., Mills, A. D., Hartmann, E., and Laskey, R. A. (1995) Distinct functions for the two importin subunits in nuclear protein import. Nature 377, 246-248
31. Lo, H. W., Ali-Seyed, M., Wu, Y., Bartholomeusz, G., Hsu, S. C., and Hung, M. C. (2006) Nuclear-cytoplasmic transport of EGFR involves receptor endocytosis, importin beta1 and CRM1. J. Cell. Biochem. 98, 1570-1583 (Pubitemid 44141861)
32. Saksena, S., Summers, M. D., Burks, J. K., Johnson, A. E., and Braunagel, S. C. (2006) Importin-α-16 is a translocon-associated protein involved in sorting membrane proteins to the nuclear envelope. Nat. Struct. Mol. Biol. 13, 500-508 (Pubitemid 43848904)
33. Lo, H. W., and Hung, M. C. (2006) Nuclear EGFR signaling network in cancers: linking EGFR pathway to cell cycle progression, nitric oxide pathway, and patient survival. Br. J. Cancer 94, 184-188
34. Johnson, D. E., and Williams, L. T. (1993) Structural and functional diversity in the FGF receptor multigene family. Adv. Cancer Res. 60, 1-41
35. Dunham-Ems, S. M., Pudavar, H. E., Myers, J. M., Maher, P. A., Prasad, P. N., and Stachowiak, M. K. (2006) Factors controlling fibroblast growth factor receptor-1's cytoplasmic trafficking and its regulation as revealed by FRAP analysis. Mol. Biol. Cell 17, 2223-2235 (Pubitemid 44011738)
36. Hsu, S. C., and Hung, M. C. (2007) Characterization of a novel tripartite nuclear localization sequence in the EGFR family. J. Biol. Chem. 282, 10432-10440
37. Kim, J., Jahng, W. J., Di Vizio, D., Lee, J. S., Jhaveri, R., Rubin, M. A., Shisheva, A., and Freeman, M. R. (2007) The phosphoinositide kinase PIKfyve mediates epidermal growth factor receptor trafficking to the nucleus. Cancer Res. 67, 9229-9237 (Pubitemid 47535910)
38. Citri, A., and Yarden, Y. (2006) EGF-ERBB signaling: towards the systems level. Nat. Rev. Mol. Cell Biol. 7, 505-516 (Pubitemid 44036456)
39. Adam, R. M., Danciu, T., McLellan, D. L., Borer, J. G., Lin, J., Zurakowski, D., Weinstein, M. H., Rajjayabun, P. H., Mellon, J. K., and Freeman, M. R. (2003) A nuclear form of the heparin-binding epidermal growth factor-like growth factor precursor is a feature of aggressive transitional cell carcinoma. Cancer Res. 63, 484-490 (Pubitemid 36152511)
40. Schausberger, E., Eferl, R., Parzefall, W., Chabicovsky, M., Breit, P., Wagner, E. F., Schulte-Hermann, R., and Grasl-Kraupp, B. (2003) Induction of DNA synthesis in primary mouse hepatocytes is associated with nuclear pro-transforming growth factor α and erbb-1 and is independent of c-jun. Carcinogenesis 24, 835-841 (Pubitemid 36752634)
41. Raper, S. E., Burwen, S. J., Barker, M. E., and Jones, A. L. (1987) Translocation of epidermal growth factor to the hepatocyte nucleus during rat liver regeneration. Gastroenterology 92, 1243-1250 (Pubitemid 17055915)
42. Hieda, M., Isokane, M., Koizumi, M., Higashi, C., Tachibana, T., Shudou, M., Taguchi, T., Hieda, Y., and Higashiyama, S. (2008) Membrane-anchored growth factor, HB-EGF, on the cell surface targeted to the inner nuclear membrane. J. Cell Biol. 180, 763-769 (Pubitemid 351397776)
43. Peng, H., Myers, J., Fang, X., Stachowiak, E. K., Maher, P. A., Martins, G. G., Popescu, G., Berezney, R., and Stachowiak, M. K. (2002) Integrative nuclear FGFR1 signaling (INFS) pathway mediates activation of the tyrosine hydroxylase gene by angiotensin II, depolarization and protein kinase C. J. Neurochem. 81, 506-524 (Pubitemid 34809329)
44. Myers, J. M., Martins, G. G., Ostrowski, J., and Stachowiak, M. K. (2003) Nuclear trafficking of FGFR1: a role for the transmembrane domain. J. Cell. Biochem. 88, 1273-1291 (Pubitemid 36397465)