The gefitinib long-term responder (LTR)-A cancer stem-like cell story? Insights from molecular analyses of German long-term responders treated in the IRESSA expanded access program (EAP)

Lung Cancer

Volumn 77, Issue 1, 2012, Pages 183-191

  Gottschling, Sandra ^a   Herpel, Esther ^b   Eberhardt, Wilfried E E ^c   Heigener, David F ^d   Fischer, Jürgen R ^e   Köhne, Claus Henning ^f   Kortsik, Cornelius ^g   Kuhnt, Thomas ^h   Muley, Thomas ^a   Meister, Michael ^a   Bischoff, Helge G ^a   Klein, Peter ⁱ   Moldenhauer, Ines ^j   Schnabel, Philipp A ^b   Thomas, Michael ^a   Penzel, Roland ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d KRANKENHAUS GROSSHANSDORF   (Germany)

^e Hospital Löwenstein   (Germany)

^f KLINIKUM OLDENBURG   (Germany)

^g St Hildegardis Krankenhaus   (Germany)

^h UNIVERSITY OF ROSTOCK   (Germany)

ⁱ Dsh Statistical Services GmbH   (Germany)

^j ASTRAZENECA   (United Kingdom)

more..

Author keywords

Biomarker; Cancer stem like cell; Epidermal growth factor receptor tyrosine kinase inhibitor; Long term response; Non small cell lung cancer

Indexed keywords

ANTINEOPLASTIC AGENT; BREAST CANCER RESISTANCE PROTEIN 1; CD133 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; K RAS PROTEIN; PROTEIN; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ADULT; AGED; ARTICLE; CANCER RADIOTHERAPY; CANCER STEM CELL; CANCER SURGERY; CANCER SURVIVAL; CLINICAL ARTICLE; DRUG RESPONSE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE MUTATION; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; MALE; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTIGENS, CD; ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; CARCINOMA, NON-SMALL-CELL LUNG; DISEASE-FREE SURVIVAL; DNA MUTATIONAL ANALYSIS; FEMALE; GLYCOPROTEINS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; LUNG NEOPLASMS; MALE; MUTATION; NEOPLASM PROTEINS; NEOPLASTIC STEM CELLS; PEPTIDES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MET; QUINAZOLINES; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SURVIVORS; TUMOR MARKERS, BIOLOGICAL;

EID: 84861729357     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2012.03.003     Document Type: Article

References (42)

1. Schiller J.H., Harrington D., Belani C.P., Langer C., Sandler A., Krook J., et al. Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med 2002, 346:92-98.
2. Rosell R., Moran T., Queralt C., Porta R., Cardenal F., Camps C., et al. Screening for epidermal growth factor receptor mutations in lung cancer. N Engl J Med 2009, 361:958-967.
3. Mok T., Wu Y.L., Thongprasert S., Yang C.H., Chu D.T., Saijo N., et al. Gefitinib or carbopatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009, 361:1018-1020.
4. Mitsudomi T., Morita S., Yatabe Y., Negoro S., Okamoto I., Tsurutani J., et al. Gefi tinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol 2010, 11:121-128.
5. Hirsch F.R., Varella-Garcia M., Bunn P.A., Franklin W.A., Dziadziusko R., Thatcher N., et al. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small-cell lung cancer. J Clin Oncol 2006, 24:5034-5042.
6. Douillard J.-Y., Shepherd F.A., Hirsh V., Mok T., Socinski M.A., Gervais R., et al. Molecular predictors of outcome with gefitinib and docetaxel in previously treated non-small-cell lung cancer: data from the randomized phase III INTEREST trial. J Clin Oncol 2009, 28:744-752.
7. Jackmann D.M., Miller V.A., Cioffredi L.A., Yeap B.Y., Jänne P.A., Riely G.J., et al. Impact of epidermal growth factor receptor and KRAS mutations on clinical outcomes in previously untreated non-small cell lung cancer patients: results of an online tumor registry of clinical trials. Clin Cancer Res 2009, 15:5267-5273.
8. Morita S., Okamoto I., Kobayashi K., Yamazaki K., Asahina H., Inoue A., et al. Combined survival analysis of prospective clinical trials of gefitinib for non-small cell lung cancer with EGFR mutations. Clin Cancer Res 2009, 15:4493-4498.
9. Cappuzzo F., Ciuleanu T., Stelmakh L., Cicenas S., Szczésna A., Juhász E., et al. Erlotinib as maintenance treatment in advanced non-small cell lung cancer: a multicentre, randomised, placebo-controlled phase 3 study. Lancet Oncol 2010, 11:521-529.
10. Cappuzzo F., Hirsch F.R., Rossi E., Bartolini S., Ceresoli G.L., Bemis L., et al. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small cell lung cancer. J Natl Cancer Inst 2005, 97:643-655.
11. Hirsch F.R., Varella-Garcia M., Cappuzzo F. Predictive value of EGFR and HER2 overexpression in advanced non-small cell lung cancer. Oncogene 2009, 28(Suppl. 1):32-37.
12. Endoh H., Yatabe Y., Kosaka T., Kuwano H., Mitsudomi T. PTEN and PIK3CA expression is associated with prolonged survival after gefitnib treamtment in EGFR-mutated lung cancer patients. J Thorac Oncol 2006, 1:629-634.
13. Zeppernick F., Ahmadi R., Campos B., Dictus C., Helmke B.M., Becker N., et al. Stem cell marker CD133 affects clinical outcome in glioma patients. Clin Cancer Res 2008, 14:123-129.
14. Horst D., Kriegl L., Engel J., Kirchner T., Jung A. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer 2008, 99:1285-1289.
15. Ho M.M., Ng A.V., Lam S., Hunh J.Y. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007, 67:4827-4833.
16. Levina V., Marrangoni A.M., DeMarco R., Gorerlik E., Lokshin A.E. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS ONE 2008, 3:e3077.
17. Eramo A., Lotti F., Sette G., Pilozzi E., Biffoni M., Di Virgilio A., et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008, 15:504-514.
18. Bertolini G., Roz L., Perego P., Tortoreto M., Fontanella E., Gatti L., et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 2009, 106:16281-16286.
19. Salnikov A.V., Gladkich J., Moldenhauer G., Volm M., Mattern J., Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer 2010, 126:950-958.
20. Moreira A.L., Gonen M., Rekhtman N., Downey R. Progenitor stem cell marker expression by pulmonary carcinomas. Mod Pathol 2010, 23:889-895.
21. Zhang H.Z., Wei Y.P., Wang M., Wu C., Yang Y.Q., Chen J., et al. Association of CD133 and endothelin-converting enzyme expressions with prognosis of non-small cell lung cancer. Nan Fang Yi Ke Da Xue Xue Bao 2007, 27:696-699.
22. Woo T., Okudela K., Mitsui H., Yazawa T., Ogawa N., Tajiri M., et al. Prognostic value of CD133 expression in stage I lung adenocarcinomas. Int J Clin Exp Pathol 2010, 4:32-42.
23. Li F., Zeng H., Ying K. The combination of stem cell markers CD133 and ABCG2 predicts relapse in stage I non-small cell lung carcinomas. Med Oncol 2010, 10.1007/s12032-010-9646-5.
24. Soeda A., Inagaki A., Oka N., Ikegame Y., Aoki H., Yoshimura S., et al. Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J Biol Chem 2008, 283:10958-10966.
25. Mazzoleni S., Politi L.S., Pala M., Cominelli M., Franzin A., Sergi Sergi L., et al. Epidermal growth factor receptor expression identifies functionally and molecularly distinct tumor-initiating cells in human glioblastoma multiforme and is required for gliomagenesis. Cancer Res 2010, 70:7500-7513.
26. Chen J.S., Pardo F.S., Wang-Rodriguez J., Chu T.S., Lopez J.P., Aguilera J., et al. EGFR regulates the side population in head and neck squamous cell carcinoma. Laryngoscope 2006, 116:401-406.
27. ClinicalTrials.gov [database online] Bethesda, MD: U.S. National Institutes of Health; 1997.
28. Hirsch F.R., Dziadziuszko R., Thatcher N., Mann H., Watkins C., Parums D.V., et al. Epidermal growth factor receptor immunohistochemistry: comparison of antibodies and cutoff points to predict benefit from gefitinib in a phase 3 placebo-controlled study in advanced nonsmall-cell lung cancer. Cancer 2008, 112:1114-1121.
29. Eberhard D.A., Johnson B.E., Amler L.C., Goddard A.D., Heldens S.L., Herbst R.S., et al. Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with non-small-cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol 2005, 23:5900-5909.
30. Gandara D.R., Grimminger P., Mack P.C., Lara P.N., Li T., Danenberg P.V., et al. Association of epidermal growth factor receptor activating mutations with low ERCC1 gene expression in non-small cell lung cancer. J Thorac Oncol 2010, 5:1933-1938.
31. Postmus E.P., Brambilla E., Chansky K., Crowley J., Goldstraw P., Patz E.F., et al. The IASLC Lung Cancer Staging Project: proposals for revision of the M descriptors in the forthcoming (seventh) edition of the TNM classification of lung cancer. J Thorac Oncol 2007, 2:686-693.
32. Pao W., Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nature 2010, 10:760-774.
33. Cappuzzo F., Jänne P.A., Skokan M., Finocchiaro G., Rossi E., Ligorio C., et al. MET increased gene copy number and primary resistance to gefitinib therapy in non-small-cell lung cancer patients. Ann Oncol 2009, 20:298-304.
34. Sequist L.V., Waltman B.A., Dias-Santagata D., Digumarthy S., Turke A.B., Fidias P., et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011, 3:75ra26.
35. Huang W.C., Chen Y.J., Li L.Y., Wei Y.L., Hsu S.C., Tsai S.L., et al. Nuclear translocation of epidermal growth factor receptor by Akt-dependent phosphorylation enhances breast cancer-resistant protein expression in gefitinib-resistant cells. J Biol Chem 2011, 286:20558-20568.
36. Griffero F., Daga A., Marubbi D., Capra M.C., Melotti A., Pattarozzi A., et al. Different response of human glioma tumor-initiating cells to epidermal growth factor receptor kinase inhibitors. J Biol Chem 2009, 284:7138-7148.
37. Elkind N.B., Szentpétery Z., Apáti A., Ozvegy-Laczka C., Várady 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.
38. McQualter J.L., Yuen K., Williams B., Bertoncello I. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc Natl Acad Sci USA 2010, 107:1414-1419.
39. Teisanu R.M., Chen H., Matsumoto K., McQualter J.L., Potts E., Foster W.M., et al. Functional analysis of two distinct bronchiolar progenitors during lung injury and repair. Am J Respir Cell Mol Biol 2011, 44:794-803.
40. Curtis S.J., Sinkevicius K.W., Li D., Lau A.N., Roach R.R., Zamponi R., et al. Primary tumor genotype is an important determinant in identification of lung cancer propagating cells. Cell Stem Cell 2010, 7:127-133.
41. Pirozzi G., Tirino V., Camerlingo R., Franco R., La Rocca A., Liguori E., et al. Epithelial to mesenchymal transition by TGFβ-1 induction increases stemness characteristics in primary non small cell lung cancer cell line. PLoS ONE 2011, 6(6):e21548. [Epub 2011 June 30].
42. Yauch R.L., Januario T., Eberhard D.A., Cavet G., Zhu W., Fu L., et al. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin Cancer Res 2005, 11:8686-8698.