An update of the mechanisms of resistance to EGFR-tyrosine kinase inhibitors in breast cancer: Gefitinib (Iressa™)-induced changes in the expression and nucleo-cytoplasmic trafficking of HER-ligands (Review)

International Journal of Molecular Medicine

Volumn 20, Issue 1, 2007, Pages 3-10

  Ferrer Soler, Laura ^a,b   Vazquez Martin, Alejandro ^a   Brunet, Joan ^a   Menendez, Javier A ^a   De Llorens, Rafael ^a,b   Colomer, Ramon ^a  

^a HOSPITAL JOSEP TRUETA   (Spain)

^b UNIVERSITY OF GIRONA   (Spain)

Author keywords

Breast cancer; Epidermal growth factor receptor; Gefitinib; Iressa; Tyrosine kinase inhibitors

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; GEFITINIB; LIGAND; PROTEIN TYROSINE KINASE; QUINAZOLINE DERIVATIVE;

BIOLOGICAL MODEL; BREAST TUMOR; CELL NUCLEUS; CYTOPLASM; DRUG ANTAGONISM; DRUG RESISTANCE; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; PATHOLOGY; REVIEW;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL NUCLEUS; CYTOPLASM; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIGANDS; MODELS, BIOLOGICAL; PROTEIN-TYROSINE KINASES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3;

EID: 34548066097     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.20.1.3     Document Type: Review

References (52)

1. Normanno N, Bianco C, De Luca A, Maiello MR and Salomon DS: Target-based agents against ErbB receptors and their ligands: a novel approach to cancer treatment. Endocr Relat Cancer 10: 1-21, 2003.
2. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, Maiello MR, Carotenuto A, De Feo G, Caponigro F and Salomon DS: Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366: 2-16, 2006. (Pubitemid 43199589)
3. Ciardello F and Tortora G: A novel approach in the treatment of cancer: targeting the epidermal growth factor receptor. Clin Cancer Res 7: 2958-2970, 2001.
4. Mendelsohn J and Baselga J: Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 21: 2787-2799, 2003.
5. Blackledge G and Averbuch S: Gefitinib ('Iressa', ZD1839) and new epidermal growth factor receptor inhibitors. Br J Cancer 90: 566-572, 2004.
6. Herbst RS, Fukuoka M and Baselga J: Gefitinib - a novel targeted approach to treating cancer. Nat Rev Cancer 4: 956-965, 2004.
7. Agrawal A, Gutteridge E, Gee JM, Nicholson RI and Robertson JF: Overview of tyrosine kinase inhibitors in clinical breast cancer. Endocr Relat Cancer 12: S135-S144, 2005.
8. Polychronis A, Sinnett HD, Hadjiminas D, Singhal H, Mansi JL, Shivapatham D, et al: Preoperative gefitinib versus gefitinib and anastrozole in postmenopausal patients with oestrogen-receptor positive and epidermal-growth-factor-receptor-positive primary breast cancer: A double-blind placebo-controlled phase II randomized trial. Lancet Oncol 6: 383-391, 2005.
9. Normanno N, De Luca A, Maiello MR, Mancino M, D'Antonio A, Macaluso M, et al: Epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors in breast cancer: current status and future development. Front Biosci 10: 2611-2617, 2005. (Pubitemid 40905265)
10. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al: EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304: 1458-1461, 2004.
11. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, et al: EGF receptor gene mutations are common in lung cancers from 'never smokers' and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci USA 101: 133306-133311, 2004.
12. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, et al: Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 350: 2129-2139, 2004.
13. Di Maio M, Gridelli C, Normmano N, Perrone F and Ciardello F: Trying to compose the puzzle with all the pieces: Epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. J Cell Physiol 205: 355-363, 2005.
14. Bhargava R, Gerald WL, Li AR, Pan Q, Lal P, Ladanyi M and Chen B: EGFR gene amplification in breast cancer: correlation with epidermal growth factor receptor mRNA and protein expression and HER-2 status and absence of EGFR-activating mutations. Mod Pathol 18: 1027-1033, 2005.
15. Normanno N, De Luca A, Maiello MR, Campiglio M, Napolitano M, Mancino M, et al: The MEK/MAPK pathway is involved in the resistance of breast cancer cells to the EGFR tyrosine kinase inhibitor gefitinib. J Cell Physiol 207: 420-427, 2006.
16. Moasser MM, Basso A, Averbuch SD and Rosen N: The tyrosine kinase inhibitor ZD1839 ('Iressa') inhibits HER2-driven signaling and suppresses the growth of HER2-overexpressing tumor cells. Cancer Res 61: 7184-7188, 2001.
17. Bianco R, Shin I, Ritter CA, Yakes FM, Basso A, Rosen N, et al: Loss of PTEN/MMAC1/TEP in EGF receptor-expressing tumor cells counteracts the antitumor action of EGFR tyrosine kinase inhibitors. Oncogene 22: 2812-2822, 2003.
18. She QB, Solit D, Basso A and Moasser MM: Resistance to gefitinib in PTEN-null HER-overexpressing tumor cells can be overcome through restoration of PTEN function or pharmacological modulation of constitutive phosphatidylinositol 3′-kinase/Akt pathway signaling. Clin Cancer Res 9: 4340-4346, 2003.
19. Magne N, Fischel JL, Dubreuil A, Formento P, Poupon MF, Laurent-Puig P and Milano G: Influence of epidermal growth factor receptor (EGFR), p53 and intrinsic MAP kinase pathway status of tumour cells on the proliferative effect of ZD1839 ('Iressa'). Br J Cancer 86: 1518-1523, 2002.
20. Baselga J, Albanell J, Ruiz A, Lluch A, Gascon P, Guillem V, et al: Phase II and tumor pharmacodynamic study of gefitinib in patients with advanced breast cancer. J Clin Oncol 23: 5323-5333, 2005.
21. Salomon DS, Brandt R, Ciardello F and Normanno N: Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 19: 183-232, 1995.
22. Olayioye MA, Neve RM, Lane HA and Hynes NE: The ErbB signaling network: receptor dimerization in development and cancer. EMBO J 19: 3159-3167, 2000.
23. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF and Arteaga CL: Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res 61: 8887-8895, 2001. (Pubitemid 34013905)
24. Normanno N, Campiglio M, De Luca A, Somenzi G, Maiello MR, Ciardello F, et al: Cooperative inhibitory effect of ZD1839 ('Iressa') in combination with trastuzumab ('Herceptin') on human breast cancer cell growth. Ann Oncol 13: 65-72, 2002.
25. Campiglio M, Locatelli A, Olgiati C, Normanno N, Somenzi G, Vigano L, et al: Inhibition of proliferation and induction of apoptosis in breast cancer cells by the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor ZD1839 ('Iressa') is independent of EGFR expression level. J Cell Physiol 198: 259-268, 2004.
26. Motoyama AB, Hynes NE and Lane HA: The efficacy of ErbB receptor-targeted anticancer therapeutics is influenced by the availability of epidermal growth factor-related peptides. Cancer Res 62: 3151-3158, 2002.
27. Yarden Y and Sliwkowski MX: Untangling the ErbB signaling network. Nat Rev Mol Cell Biol 2: 127-137, 2001.
28. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, et al: Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interaction. EMBO J 15: 2452-2467, 1996.
29. Graus-Porta D, Beerli RR, Daly JM and Hynes NE: ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 16: 1647-1655, 1997.
30. Kramarski-Pinkas R, Lenferink AE, Bacus SS, Lyass L, van de Poll ML, Klapper LN, et al: The oncogenic ErbB2/ErbB3 heterodimer is a surrogate receptor of the epidermal growth factor and betacellulin. Oncogene 16: 1249-1258, 1998.
31. Anido J, Matar P, Albanell J, Guzman M, Rojo F, Arribas J, et al: ZD1839, a specific epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor, induces the formation of inactive EGFR/HER2 and EGFR/HER3 heterodimers and prevents Heregulin signaling in HER2-overexpressing breast cancer cells. Clin Cancer Res 9: 1274-1283, 2003.
32. Ritter CA, Bianco R, Dugger T, King W, Ritland S, Bargiacchi F, et al: HER2-overexpressing human breast cancer cells selected for Herceptin (trastuzumab) resistance in vivo retain HER2 gene amplification and overexpress HER1/EGFR receptor ligands. Proc Am Assoc Cancer Res 44: 1117, 2003.
33. Li W, Park JW, Nuijens A, Sliwkowski MX and Keller GA: Heregulin is rapidly translocated to the nucleus and its transport is correlated with c-myc induction in breast cancer cells. Oncogene 12: 2473-2477, 1996.
34. Adam RM, Danciu T, McLellan DL, Borer JG, Lin J, et al: 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, 2003.
35. Golding M, Ruhrberg C, Sandle J and Gullick WJ: Mapping nucleolar and spliceosome localization sequences of neuregulin1-3. Exp Cell Res 299: 110-118, 2004.
36. Breleux M, Schoumacher F, Rehn D, Kung W, Mueller H and Eppenberger U: Heregulins implicated in cellular functions other than receptor activation. Mol Cancer Res 4: 27-37, 2006.
37. Atlas E, Bojanowski K, Mehmi I and Lupu R: A deletion mutant of Heregulin increases the sensitivity of breast cancer cells to chemotherapy without promoting tumorigenicity. Oncogene 22: 3441-3451, 2003.
38. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, et al: Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3: 802-808, 2001.
39. Lo HW, Hsu SC, 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 7: 575-589, 2005.
40. Xie Y and Hung MC: Nuclear localization of p185neu tyrosine kinase and its association with transcriptional transactivation. Biochem Biophys Res Commun 203: 1589-1598, 1994.
41. Wang SC, Lien HC, Xia W, Chen IF, Lo HW, Wang Z, et al: Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2. Cancer Cell 6: 251-261, 2004.
42. Johnson HM, Subramaniam PS, Olsnes S and Jans DA: Trafficking and signaling pathways of nuclear localizing protein ligands and their receptors. Bioessays 26: 993-1004, 2004.
43. Lo HW, Hsu SC and Hung MC: EGFR signaling pathway in breast cancers: from traditional signal transduction to direct nuclear translocation. Breast Cancer Res Treat 95: 211-218, 2006.
44. Lo HW and Hung MC: 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, 2006.
45. Chinnaiyan P, Varambally S, Tomlins SA, Ray S, Huang S, Chinnaiyan AM and Harari PM: Enhancing the antitumor activity of ErbB blockade with histone deactylase (HDAC) inhibition. Int J Cancer 118: 1041-1050, 2006.
46. Witta SE, Gemmill RM, Hirsch FR, Coldren CD, Hedman K, Ravdel L, et al: Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res 66: 944-950, 2006.
47. Menendez JA, Mehmi I and Lupu R: Trastuzumab in combination with heregulin-activated Her-2 (erbB-2) triggers a receptor-enhanced chemosensitivity effect in the absence of Her-2 overexpression. J Clin Oncol 24: 3735-3746, 2006.
48. Arteaga CL: Can trastuzumab be effective against tumors with low HER2/Neu (ErbB2) receptors? J Clin Oncol 24: 3722-3725, 2006.
49. Mendelsohn J: Targeting the epidermal growth factor for cancer therapy. J Clin Oncol 20 (suppl 18): 1S-13S, 2002.
50. Siegel-Lakhai WS, Beijnen JH and Schellens JH: Current knowledge and future directions of the selective epidermal growth factor receptor inhibitors erlotinib (Tarceva) and gefitinib (Iressa). Oncologist 10: 579-589, 2005.
51. Blagosklonny MV and Darzynkiewicz Z: Cyclotherapy: protection of normal cells and unshielding of cancer cells. Cell Cycle 1: 375-382, 2002.
52. Blagosklonny MV and Darzynkiewicz Z: Why Iressa failed: Toward novel use of kinase inhibitors (outlook). Cancer Biol Ther 2: 137-140, 2003.