Destabilization of the epidermal growth factor receptor (EGFR) by a peptide that inhibits egfr binding to heat shock protein 90 and receptor dimerization

Journal of Biological Chemistry

Volumn 288, Issue 37, 2013, Pages 26879-26886

  Ahsan, Aarif ^a   Ray, Dipankar ^a   Ramanand, Susmita G ^a   Hegde, Ashok ^a   Whitehead, Christopher ^b   Rehemtulla, Alnawaz ^a   Morishima, Yoshihiro ^a   Pratt, William B ^a   Osawa, Yoichi ^a   Lawrence, Theodore S ^a   Nyati, Mukesh K ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Departments of Radiology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTORS; HEAT-SHOCK PROTEIN 90; LOOP REGIONS; PROTEIN KINASE;

AMINO ACIDS; DIMERIZATION;

PEPTIDES;

ANTINEOPLASTIC AGENT; DISRUPTIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHOSPHORYLATION; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; DIMERIZATION; DRUG INHIBITION; DRUG SYNTHESIS; ENZYME STABILITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION;

CANCER; EGFR DEGRADATION; EPIDERMAL GROWTH FACTOR RECEPTOR (EGFR); HSP90; PROTEIN DEGRADATION; RECEPTOR TYROSINE KINASE;

ANIMALS; ANTINEOPLASTIC AGENTS; BENZOQUINONES; CELL LINE, TUMOR; CHO CELLS; CRICETULUS; DIMERIZATION; DRUG DESIGN; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEPTIDE FRAGMENTS; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84884190245     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.492280     Document Type: Article

References (40)

1. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137
2. Schlessinger, J. (2000) Cell signaling by receptor tyrosine kinases. Cell 103, 211-225
3. Ahsan, A., Ramanand, S. G., Whitehead, C., Hiniker, S. M., Rehemtulla, A., Pratt, W. B., Jolly, S., Gouveia, C., Truong, K., Van Waes, C., Ray, D., Lawrence, T. S., and Nyati, M. K. (2012) Wild-type EGFR is stabilized by direct interaction with HSP90 in cancer cells and tumors. Neoplasia 14, 670-677
4. Zhang, X., Gureasko, J., Shen, K., Cole, P. A., and Kuriyan, J. (2006) An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149
5. Shan, Y., Eastwood, M. P., Zhang, X., Kim, E. T., Arkhipov, A., Dror, R. O., Jumper, J., Kuriyan, J., and Shaw, D. E. (2012) Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149, 860-870
6. Citri, A., Gan, J., Mosesson, Y., Vereb, G., Szollosi, J., and Yarden, Y. (2004) Hsp90 restrains ErbB-2/HER2 signalling by limiting heterodimer formation. EMBO Rep. 5, 1165-1170
7. Pratt, W. B., Morishima, Y., and Osawa, Y. (2008) The Hsp90 chaperone machinery regulates signaling by modulating ligand binding clefts. J. Biol. Chem. 283, 22885-22889
8. Xu, W., Mimnaugh, E., Rosser, M. F., Nicchitta, C., Marcu, M., Yarden, Y., and Neckers, L. (2001) Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90. J. Biol. Chem. 276, 3702-3708
9. Citri, A., Alroy, I., Lavi, S., Rubin, C., Xu, W., Grammatikakis, N., Patterson, C., Neckers, L., Fry, D. W., and Yarden, Y. (2002) Drug-induced ubiquitylation and degradation of ErbB receptor tyrosine kinases: implications for cancer therapy. EMBO J. 21, 2407-2417
10. Tikhomirov, O., and Carpenter, G. (2003) Identification of ErbB-2 kinase domain motifs required for geldanamycin-induced degradation. Cancer Res. 63, 39-43
11. Citri, A., Harari, D., Shohat, G., Ramakrishnan, P., Gan, J., Lavi, S., Eisenstein, M., Kimchi, A., Wallach, D., Pietrokovski, S., and Yarden, Y. (2006) Hsp90 recognizes a common surface on client kinases. J. Biol. Chem. 281, 14361-14369
12. Huse, M., and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275-282
13. Pratt, W. B., and Toft, D. O. (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. (Maywood) 228, 111-333
14. Kaul, S., Murphy, P. J., Chen, J., Brown, L., Pratt, W. B., and Simons, S. S., Jr. (2002) Mutations at positions 547-553 of rat glucocorticoid receptors reveal that hsp90 binding requires the presence, but not defined composition, of a seven-amino acid sequence at the amino terminus of the ligand binding domain. J. Biol. Chem. 277, 36223-36232
15. Lawrence, T. S. (1988) Reduction of doxorubicin cytotoxicity by ouabain: correlation with topoisomerase-induced DNA strand breakage in human and hamster cells. Cancer Res. 48, 725-730
16. Futaki, S., Suzuki, T., Ohashi, W., Yagami, T., Tanaka, S., Ueda, K., and Sugiura, Y. (2001) Arginine-rich peptides. An abundant source of membrane- permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 276, 5836-5840
17. Zou, J., Guo, Y., Guettouche, T., Smith, D. F., and Voellmy, R. (1998) Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 94, 471-480
18. Bagatell, R., Paine-Murrieta, G. D., Taylor, C. W., Pulcini, E. J., Akinaga, S., Benjamin, I. J., and Whitesell, L. (2000) Induction of heat shock factor 1-dependent stress response alters the cytotoxic activity of hsp90-binding agents. Clin. Cancer Res. 6, 3312-3318
19. Morishima, Y., Lau, M., Peng, H. M., Miyata, Y., Gestwicki, J. E., Pratt, W. B., and Osawa, Y. (2011) Heme-dependent activation of neuronal nitric- oxide synthase by cytosol is due to an Hsp70-dependent, thioredoxinmediated thiol-disulfide interchange in the heme/substrate binding cleft. Biochemistry 50, 7146-7156
20. Nimmanapalli, R., O'Bryan, E., and Bhalla, K. (2001) Geldanamycin and its analogue 17-allylamino-17-demethoxygeldanamycin lowers Bcr-Abl levels and induces apoptosis and differentiation of Bcr-Abl-positive human leukemic blasts. Cancer Res. 61, 1799-1804
21. Hostein, I., Robertson, D., DiStefano, F., Workman, P., and Clarke, P. A. (2001) Inhibition of signal transduction by the Hsp90 inhibitor 17-allylamino- 17-demethoxygeldanamycin results in cytostasis and apoptosis. Cancer Res. 61, 4003-4009
22. Xu, W., Yuan, X., Xiang, Z., Mimnaugh, E., Marcu, M., and Neckers, L. (2005) Surface change and hydrophobicity determine ErbB2 binding to the Hsp90 chaperone complex. Nat. Struct. Mol. Biol. 12, 120-126
23. Aertgeerts, K., Skene, R., Yano, J., Sang, B. C., Zou, H., Snell, G., Jennings, A., Iwamoto, K., Habuka, N., Hirokawa, A., Ishikawa, T., Tanaka, T., Miki, H., Ohta, Y., and Sogabe, S. (2011) Structural analysis of the mechanism of inhibition and allosteric activation of the kinase domain of HER2 protein. J. Biol. Chem. 286, 18756-18765
24. Monsey, J., Shen, W., Schlesinger, P., and Bose, R. (2010) Her4 and Her2/ neu tyrosine kinase domains dimerize and activate in a reconstituted in vitro system. J. Biol. Chem. 285, 7035-7044
25. Feng, F. Y., Lopez, C. A., Normolle, D. P., Varambally, S., Li, X., Chun, P. Y., Davis, M. A., Lawrence, T. S., and Nyati, M. K. (2007) Effect of epidermal growth factor receptor inhibitor class in the treatment of head and neck cancer with concurrent radiotherapy in vivo. Clin. Cancer Res. 13, 2512-2518
26. Ahsan, A., Hiniker, S. M., Davis, M. A., Lawrence, T. S., and Nyati, M. (2009) Role of cell cycle in epidermal growth factor receptor inhibitormediated radiosensitization. Cancer Res. 69, 5108-5114
27. Ahsan, A., Hiniker, S. M., Ramanand, S. G., Nyati, S., Hegde, A., Helman, A., Menawat, R., Bhojani, M. S., Lawrence, T. S., and Nyati, M. K. (2010) Role of epidermal growth factor receptor degradation in cisplatin-induced cytotoxicity in head and neck cancer. Cancer Res. 70, 2862-2869
28. Burtness, B. (2005) The role of cetuximab in the treatment of squamous cell cancer of the head and neck. Expert Opin. Biol. Ther. 5, 1085-1093
29. Kirisits, A., Pils, D., and Krainer, M. (2007) Epidermal growth factor receptor degradation: an alternative view of oncogenic pathways. Int. J. Biochem. Cell Biol. 39, 2173-2182
30. Kim, W. Y., Oh, S. H., Woo, J. K., Hong, W. K., and Lee, H. Y. (2009) Targeting heat shock protein 90 overrides the resistance of lung cancer cells by blocking radiation-induced stabilization of hypoxia-inducible factor- 1α. Cancer Res. 69, 1624-1632
31. Bisht, K. S., Bradbury, C. M., Mattson, D., Kaushal, A., Sowers, A., Markovina, S., Ortiz, K. L., Sieck, L. K., Isaacs, J. S., Brechbiel, M. W., Mitchell, J. B., Neckers, L. M., and Gius, D. (2003) Geldanamycin and 17-allylamino- 17-demethoxygeldanamycin potentiate the in vitro and in vivo radiation response of cervical tumor cells via the heat shock protein 90-mediated intracellular signaling and cytotoxicity. Cancer Res. 63, 8984-8995
32. Sharp, S., and Workman, P. (2006) Inhibitors of the HSP90 molecular chaperone: current status. Adv. Cancer Res. 95, 323-348
33. Pacey, S., Wilson, R. H., Walton, M., Eatock, M. M., Hardcastle, A., Zetterlund, A., Arkenau, H. T., Moreno-Farre, J., Banerji, U., Roels, B., Peachey, H., Aherne, W., de Bono, J. S., Raynaud, F., Workman, P., and Judson, I. (2011) A phase 1 study of the heat shock protein 90 inhibitor alvespimycin (17-DMAG) given intravenously to patients with advanced solid tumors. Clin. Cancer Res. 17, 1561-1570
34. LaBelle, J. L., Katz, S. G., Bird, G. H., Gavathiotis, E., Stewart, M. L., Lawrence, C., Fisher, J. K., Godes, M., Pitter, K., Kung, A. L., and Walensky, L. D. (2012) A stapled BIM peptide overcomes apoptotic resistance in hematologic cancers. J. Clin. Invest. 122, 2018-2031
35. Rérole, A. L., Gobbo, J., De Thonel, A., Schmitt, E., Pais de Barros, J. P., Hammann, A., Lanneau, D., Fourmaux, E., Deminov, O., Micheau, O., Lagrost, L., Colas, P., Kroemer, G., and Garrido, C. (2011) Peptides and aptamers targeting HSP70: a novel approach for anticancer chemotherapy. Cancer Res. 71, 484-495
36. Liu, M., Li, C., Pazgier, M., Li, C., Mao, Y., Lv, Y., Gu, B., Wei, G., Yuan, W., Zhan, C., Lu, W. Y., and Lu, W. (2010) D-peptide inhibitors of the p53- MDM2 interaction for targeted therapy of malignant neoplasms. Proc. Natl. Acad. Sci. U.S.A. 107, 14321-14326
37. Shen, S., Zhang, P., Lovchik, M. A., Li, Y., Tang, L., Chen, Z., Zeng, R., Ma, D., Yuan, J., and Yu, Q. (2009) Cyclodepsipeptides toxin promotes the degradation of Hsp90 client proteins through chaperone-mediated autophagy. J. Cell Biol. 185, 629-639
38. Shrivastava, A., Nunn, A. D., and Tweedle, M. F. (2009) Designer peptides: learning from nature. Curr. Pharm. Des. 15, 675-681
39. Heitz, F., Morris, M. C., and Divita, G. (2009) Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br. J. Pharmacol. 157, 195-206
40. Sugahara, K. N., Teesalu, T., Karmali, P. P., Kotamraju, V. R., Agemy, L., Greenwald, D. R., and Ruoslahti, E. (2010) Coadministration of a tumorpenetrating peptide enhances the efficacy of cancer drugs. Science 328, 1031-1035