Iressa induces cytostasis and augments Fas-mediated apoptosis in acinic cell adenocarcinoma overexpressing HER2/Neu

International Journal of Cancer

Volumn 119, Issue 2, 2006, Pages 441-454

  Piechocki, Marie P ^a   Yoo, George H ^a   Dibbley, Susan K ^a   Amjad, Esmael H ^a   Lonardo, Fulvio ^b  

^a WAYNE STATE UNIVERSITY   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cytostasis; Fas; HER2; Signal transduction

Indexed keywords

BIM PROTEIN; CASPASE 12; CASPASE 3; CASPASE 9; CYCLIN B1; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FAS ANTIGEN; GEFITINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOCORTIN 5; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN KINASE B; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ACINAR CELL CARCINOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSTASIS; ENDOPLASMIC RETICULUM; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD95; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, ACINAR CELL; CASPASES; CELL CYCLE; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEOPLASM PROTEINS; PHOSPHORYLATION; POLY(ADP-RIBOSE) POLYMERASES; QUINAZOLINES; RECEPTOR, ERBB-2; SALIVARY GLAND NEOPLASMS; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 33745223911     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21837     Document Type: Article

References (76)

1. Ullrich A, Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell 1990;61:203-12.
2. Klapper LN, Kirschbaum MH, Sela M, Yarden Y. Biochemical and clinical implications of the ErbB/HER signaling network of growth factor receptors. Adv Cancer Res 2000;77:25-79.
3. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997;16:1647-55.
4. Press MF, Pike MC, Hung G, Zhou JY, Ma Y, George J, Dietz-Band J, James W, Slamon DJ, Batsakis JG. Amplification and overexpression of HER-2/neu in carcinomas of the salivary gland: correlation with poor prognosis. Cancer Res 1994;54:5675-82.
5. Klijn JG, Look MP, Portengen H, Alexieva-Figusch J, van Putten WL, Foekens JA. The prognostic value of epidermal growth factor receptor (EGF-R) in primary breast cancer: results of a 10 year follow-up study. Breast Cancer Res Treat 1994;29:73-83.
6. Maurizi M, Almadori G, Ferrandina G, Distefano M, Romanini ME. Cadoni G, Benedetti-Panici P, Paludetti G, Scambia G, Mancuso S. Prognostic significance of epidermal growth factor receptor in laryngeal squamous cell carcinoma. Br J Cancer 1996;74:1253-7.
7. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989; 244:707-12.
8. Huang G, Chantry A, Epstein RJ. Overexpression of ErbB2 impairs ligand-dependent downregulation of epidermal growth factor receptors via a post-transcriptional mechanism. J Cell Biochem 1999;74: 23-30.
9. Wu CJ, Qian X, O'Rourke DM. Sustained mitogen-activated protein kinase activation is induced by transforming erbB receptor complexes. DNA Cell Biol 1999;18:731-41.
10. Wang Z, Zhang L, Yeung TK, Chen X. Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation. Mol Biol Cell 1999;10:1621-36.
11. Fry DW, Bridges AJ, Denny WA, Doherty A, Greis KD, Hicks JL, Hook KE, Keller PR, Leopold WR, Loo JA, McNamara DJ, Nelson JM, et al. Specific, irreversible inactivation of the epidermal growth factor receptor and erbB2, by a new class of tyrosine kinase inhibitor. Proc Natl Acad Sci USA 1998;95:12022-7.
12. Gschwind A, Fischer OM, Ullrich A. The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat Rev Cancer 2004;4:361-70.
13. Traxler P, Bold G, Buchdunger E, Caravatti G, Furet P, Manley P, O'Reilly T, Wood J, Zimmermann J. Tyrosine kinase inhibitors: from rational design to clinical trials. Med Res Rev 2001;21:499-512.
14. Baselga J. The EGFR as a target for anticancer therapy-focus on cetuximab. Eur J Cancer 2001;37 (Suppl. 4):S16-S22.
15. Baselga J. Monoclonal antibodies directed at growth factor receptors. Ann Oncol 2000;11 (Suppl. 3):187-90.
16. Baselga J. Herceptin alone or in combination with chemotherapy in the treatment of HER2-positive metastatic breast cancer: pivotal trials. Oncology 2001;61 (Suppl. 2):14-21.
17. Baselga J, Albanell J. Mechanism of action of anti-HER2 monoclonal antibodies. Ann Oncol 2001;12 (Suppl. 1):S35-S41.
18. Baselga J. Current and planned clinical trials with trastuzumab (Herceptin). Semin Oncol 2000;27:27-32.
19. Cockerill S, Stubberfield C, Stables J, Carter M, Guntrip S, Smith K, McKeown S, Shaw R, Topley P, Thomsen L, Affleck K, Jowett A, et al. Indazolylamino quinazolines and pyridopyrimidines as inhibitors of the EGFr and C-erbB-2. Bioorg Med Chem Lett 2001;11:1401-5.
20. Fry DW, Nelson JM, Slintak V, Keller PR, Rewcastle GW, Denny WA, Zhou H, Bridges AJ. Biochemical and antiproliferative properties of 4-[ar(alk)ylamino] pyridopyrimidines, a new chemical class of potent and specific epidermal growth factor receptor tyrosine kinase inhibitor. Biochem Pharmacol 1997;54:877-87.
21. Sirotnak FM, Zakowski MF, Miller VA, Scher HI, Kris MG. Efficacy of cytotoxic agents against human tumor xenografts is markedly enhanced by coadministration of ZD1839 (Iressa), an inhibitor of EGFR tyrosine kinase. Clin Cancer Res 2000;6:4885-92.
22. Ciardiello F, Caputo R, Bianco R, Damiano V, Fontanini G, Cuccato S, De Placido S, Bianco AR, Tortora G. Inhibition of growth factor production and angiogenesis in human cancer cells by ZD1839 (Iressa), a selective epidermal growth factor receptor tyrosine kinase inhibitor. Clin Cancer Res 2001;7:1459-65.
23. Naruse I, Ohmori T, Ao Y, Fukumoto H, Kuroki T, Mori M, Saijo N, Nishio K. Antitumor activity of the selective epidermal growth factor receptor-tyrosine kinase inhibitor (EGFR-TKI) Iressa (ZD1839) in an EGFR-expressing multidrug-resistant cell line in vitro and in vivo. Int J Cancer 2002;98:310-15.
24. Anderson NG, Ahmad T, Chan K, Dobson R, Bundred NJ. ZD1839 (Iressa), a novel epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor, potently inhibits the growth of EGFR-positive cancer cell lines with or without erbB2 overexpression. Int J Cancer 2001;94:774-82.
25. Moasser MM, Basso A, Averbuch SD, Rosen N. The tyrosine kinase inhibitor ZD1839 ("Iressa") inhibits HER2-driven signaling and suppresses the growth of HER2-overexpressing tumor cells. Cancer Res 2001;61:7184-8.
26. Ciardiello F, Caputo R, Bianco R, Damiano V, Pomatico G, De Placido S, Bianco AR, Tortora G. Antitumor effect and potentiation of cytotoxic drugs activity in human cancer cells by ZD1839 (Iressa), an epidermal growth factor receptor-selective tyrosine kinase inhibitor. Clin Cancer Res 2000;6:2053-63.
27. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF, 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 2001;61:8887-95.
28. Knight LA, Di Nicolantonio F, Whitehouse P, Mercer S, Sharma S, Glaysher S, Johnson P, Cree IA. The in vitro effect of gefitinib ("Iressa") alone and in combination with cytotoxic chemotherapy on human solid tumours. BMC Cancer 2004;4:83.
29. Koizumi F, Kanzawa F, Ueda Y, Koh Y, Tsukiyama S, Taguchi F, Tamura T, Saijo N, Nishio K. Synergistic interaction between the EGFR tyrosine kinase inhibitor gefitinib ("Iressa") and the DNA topoisomerase I inhibitor CPT-11 (irinotecan) in human colorectal cancer cells. Int J Cancer 2004;108:464-72.
30. Shintani S, Kiyota A, Mihara M, Sumida T, Kayahara H, Nakashiro K, Hamakawa H. Enhancement of radiosensitivity in head and neck cancer cells by ZD1839 ("Iressa"), a selective epidermal growth factor receptor tyrosine kinase inhibitor. Am J Clin Oncol 2003;26(5): e150-6.
31. Hynes NE, Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 2005;5:341-54.
32. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, Naoki K, Sasaki H, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500. Epub Apr 29, 2004.
33. Stephens P, Hunter C, Bignell G, Edkins S, Davies H, Teague J, Stevens C, O'Meara S, Smith R, Parker A, Barthorpe A, Blow M, et al. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature 2004;431:525-6.
34. Amann J, Kalyankrishna S, Massion PP, Ohm JE, Girard L, Shigematsu H, Peyton M, Juroske D, Huang Y, Stuart Salmon J, Kim YH, Pollack JR, et al. Aberrant epidermal growth factor receptor signaling and enhanced sensitivity to EGFR inhibitors in lung cancer. Cancer Res 2005;65:226-35.
35. Diodoro MG, Di Carlo E, Zappacosta R, Iezzi M, Coletti A, Modesti A, D'Antuono T, Forni G, Musiani P. Salivary carcinoma in HER-2/neu transgenic male mice: an angiogenic switch is not required for tumor onset and progression. Int J Cancer 2000;88:329-35.
36. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65(1-2):55-63.
37. Zheng C, Hoffman MP, McMillan T, Kleinman HK, O'Connell BC. Growth factor regulation of the amylase promoter in a differentiating salivary acinar cell line. J Cell Physiol 1998;177:628-35.
38. Tanda N, Ohyama H, Yamakawa M, Ericsson M, Tsuji T, McBride J, Elovic A, Wong DT, Login GR. IL-1β and IL-6 in mouse parotid acinar cells: characterization of synthesis, storage, and release. Am J Physiol 1998;274(1 Part 1):G147-56.
39. Szlosarek P, Balkwill F. The inflammatory cytokine network of epithelial cancer: therapeutic implications. Novartis Found Symp 2004; 256:227-37.
40. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004;4:540-50.
41. Yang W, Klos K, Yang Y, Smith TL, Shi D, Yu D. ErbB2 overexpression correlates with increased expression of vascular endothelial growth factors A, C, and D in human breast carcinoma. Cancer 2002; 94:2855-61.
42. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat Rev Cancer 2004;4:11-22.
43. Matsumura R, Umemiya K, Goto T, Nakazawa T, Ochiai K, Kagami M, Tomioka H, Tanabe E, Sugiyama T, Sueishi M. Interferon γ and tumor necrosis factor α induce Fas expression and anti-Fas mediated apoptosis in a salivary ductal cell line. Clin Exp Rheumatol 2000;18: 311-18.
44. Yamakawa M, Weinstein R, Tsuji T, McBride J, Wong DT, Login GR. Age-related alterations in IL-1β, TNF-α, and IL-6 concentrations in parotid acinar cells from BALB/c and non-obese diabetic mice. J Histochem Cytochem 2000;48:1033-42.
45. Kamachi M, Kawakami A, Yamasaki S, Hida A, Nakashima T, Nakamura H, Ida H, Furuyama M, Nakashima K, Shibatomi K, Miyashita T, Migita K, et al. Regulation of apoptotic cell death by cytokines in a human salivary gland cell line: distinct and synergistic mechanisms in apoptosis induced by tumor necrosis factor α and interferonγ. J Lab Clin Med 2002;139:13-19.
46. Tjabringa GS, Vos JB, Olthuis D, Ninaber DK, Rabe KF, Schalkwijk J, Hiemstra PS, Zeeuwen PL. Host defense effector molecules in mucosal secretions. FEMS Immunol Med Microbiol 2005;45:151-8.
47. Wozniak KL, Arribas A, Leigh JE, Fidel PL, Jr. Inhibitory effects of whole and parotid saliva on immunomodulators. Oral Microbiol Immunol 2002;17:100-7.
48. Brennan MT, Fox PC. Cytokine mRNA expression in the labial salivary glands of healthy volunteers. Oral Dis 2000;6:222-6.
49. Lin AL, Johnson DA, Stephan KT, Yeh CK. Salivary secretory leukocyte protease inhibitor increases in HIV infection. J Oral Pathol Med 2004;33:410-16.
50. Feuerhake F, Kutok JL, Monti S, Chen W, LaCasce AS, Cattoretti G, Kurtin P, Pinkus GS, de Leval L, Harris NL, Savage KJ, Neuberg D, et al. NFκB activity, function, and target-gene signatures in primary mediastinal large B-cell lymphoma and diffuse large B-cell lymphoma subtypes. Blood 2005;106:1392-9.
51. Akpek EK, Jabs DA, Gerard HC, Prendergast RA, Hudson AP, Lee B, Whittum-Hudson JA. Chemokines in autoimmune lacrimal gland disease in MRL/MpJ mice. Invest Ophthalmol Vis Sci 2004;45:185-90.
52. Bombardieri M, Barone F, Pittoni V, Alessandri C, Conigliaro P, Blades MC, Priori R, McInnes IB, Valesini G, Pitzalis C. Increased circulating levels and salivary gland expression of interleukin-18 in patients with Sjogren's syndrome: relationship with autoantibody production and lymphoid organization of the periductal inflammatory infiltrate. Arthritis Res Ther 2004;6:R447-56.
53. Beutler B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 2004;430:257-63.
54. Piechocki MP, Lonardo F, Ensley JF, Nguyen T, Kim H, Yoo GH. Anticancer activity of docetaxel in murine salivary gland carcinoma. Clin Cancer Res 2002;8:870-7.
55. Morimoto Y, Morimoto H, Okamura H, Nomiyama K, Nakamuta N, Kobayashi S, Kito S, Ohba T, Haneji T. Upregulation of the expression of Fas antigen and Fas ligand in a human submandibular gland ductal cell line by okadaic acid. Arch Oral Biol 2000;45:657-66.
56. Anido J, Matar P, Albanell J, Guzman M, Rojo F, Arribas J, Averbuch S, Baselga J. 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 2003;9:1274-83.
57. Ono M, Hirata A, Kometani T, Miyagawa M, Ueda S, Kinoshita H, Fujii T, Kuwano M. Sensitivity to gefitinib (Iressa, ZD1839) in non-small cell lung cancer cell lines correlates with dependence on the epidermal growth factor (EGF) receptor/extracellular signal-regulated kinase 1/2 and EGF receptor/Akt pathway for proliferation. Mol Cancer Ther 2004;3:465-72.
58. Yu H, Jove R. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer 2004;4:97-105.
59. Catlett-Falcone R, Dalton WS, Jove R. STAT proteins as novel targets for cancer therapy. Signal transducer an activator of transcription. Curr Opin Oncol 1999;11:490-6.
60. Amaravadi R, Thompson CB. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest 2005;115:2618-24.
61. Wang T, Niu G, Kortylewski M, Burdelya L, Shain K, Zhang S, Bhattacharya R, Gabrilovich D, Heller R, Coppola D, Dalton W, Jove R, et al. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat Med 2004;10:48-54.
62. Selander KS, Li L, Watson L, Merrell M, Dahmen H, Heinrich PC, Muller-Newen G, Harris KW. Inhibition of gp130 signaling in breast cancer blocks constitutive activation of Stat3 and inhibits in vivo malignancy. Cancer Res 2004;64:6924-33.
63. Sriuranpong V, Park JI, Amornphimoltham P, Patel V, Nelkin BD, Gutkind JS. Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system. Cancer Res 2003;63:2948-56.
64. Ozoren N, El-Deiry WS. Cell surface death receptor signaling in normal and cancer cells. Semin Cancer Biol 2003;13:135-47.
65. Yoo GH, Piechocki MP, Oliver J, Lonardo F, Zumstein L, Lin HS, Kim H, Shibuya TY, Shehadeh N, Ensley JF. Enhancement of Ad-p53 therapy with docetaxel in head and neck cancer. Laryngoscope 2004;114:1871-9.
66. She QB, Solit D, Basso A, Moasser MM. Resistance to gefitinib in PTEN-null HER-overexpressing tumor cells can be overcome through restoration of PTEN function or pharmacologic modulation of constitutive phosphatidylinositol 3′-kinase/Akt pathway signaling. Clin Cancer Res 2003;9:4340-6.
67. Fukazawa H, Noguchi K, Masumi A, Murakami Y, Uehara Y. BimEL is an important determinant for induction of anoikis sensitivity by mitogen-activated protein/extracellular signal-regulated kinase kinase inhibitors. Mol Cancer Ther 2004;3:1281-8.
68. Ciardiello F, Caputo R, Bordello G, Del Bufalo D, Biroccio A, Zupi G, Bianco AR, Tortora G. ZD1839 (Iressa), an EGFR-selective tyrosine kinase inhibitor, enhances taxane activity in bcl-2 overexpressing, multidrug-resistant MCF-7 ADR human breast cancer cells. Int J Cancer 2002;98:463-9.
69. Gilmore AP, Valentijn AJ, Wang P, Ranger AM, Bundred N, O'Hare MJ, Wakeling A, Korsmeyer SJ, Streuli CH. Activation of BAD by therapeutic inhibition of epidermal growth factor receptor and transactivation by insulin-like growth factor receptor. J Biol Chem 2002;277:27643-50.
70. Chang GC, Hsu SL, Tsai JR, Liang FP, Lin SY, Sheu GT, Chen CY. Molecular mechanisms of ZD1839-induced G1-cell cycle arrest and apoptosis in human lung adenocarcinoma A549 cells. Biochem Pharmacol 2004;68:1453-64.
71. Barton C, Davies D, Balkwill F, Burke F. Involvement of both intrinsic and extrinsic pathways in IFN-γ-induced apoptosis that are enhanced with cisplatin. Eur J Cancer 2005;41:1474-86.
72. Beere HM. Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 2005;115:2633-9.
73. Janmaat ML, Kruyt FA, Rodriguez JA, Giaccone G. Response to epidermal growth factor receptor inhibitors in non-small cell lung cancer cells: limited antiproliferative effects and absence of apoptosis associated with persistent activity of extracellular signal-regulated kinase or Akt kinase pathways. Clin Cancer Res 2003;9:2316-26.
74. Mizutani Y, Wu XX, Yoshida O, Shirasaka T, Bonavida B. Chemoimmunosensitization of the T24 human bladder cancer line to Fas-mediated cytotoxicity and apoptosis by cisplatin and 5-fluorouracil. Oncol Rep 1999;6:979-82.
75. Costa-Pereira AP, Cotter TG. Camptothecin sensitizes androgen-independent prostate cancer cells to anti-Fas-induced apoptosis. Br J Cancer 1999;80:371-8.
76. Liu J, Guo L, Jun-Wei L, Liu N, Li H. All-trans retinoic acid modulates fas expression and enhances chemosensitivity of human medulloblastoma cells. Int J Mol Med 2000;5:145-9.