Contrasting responses of non-small cell lung cancer to antiangiogenic therapies depend on histological subtype

EMBO Molecular Medicine

Volumn 6, Issue 4, 2014, Pages 539-550

  Larrayoz, Marta ^a,b   Pio, Ruben ^a,c   Pajares, María J ^a,b   Zudaire, Isabel ^a,c   Ajona, Daniel ^a   Casanovas, Oriol ^d   Montuenga, Luis M ^a,b   Agorreta, Jackeline ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

^d BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

Author keywords

Angiogenesis; Lung cancer; Mouse models; N nitroso tris chloroethylurea; Squamous cell carcinoma

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 1A1; CD133 ANTIGEN; CD15 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY DC101; PROTEIN KINASE B; SUNITINIB; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; ANGIOGENESIS INHIBITOR; DC101 MONOCLONAL ANTIBODY; INDOLE DERIVATIVE; MONOCLONAL ANTIBODY; PYRROLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER MODEL; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; HISTOPATHOLOGY; HYPOXEMIA; IN VITRO STUDY; IN VIVO STUDY; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; ANIMAL; BAGG ALBINO MOUSE; CARCINOMA, NON-SMALL-CELL LUNG; DRUG SCREENING; FEMALE; HUMAN; PATHOLOGY; TREATMENT OUTCOME;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; HUMANS; INDOLES; MICE; MICE, INBRED BALB C; PYRROLES; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84898596682     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201303214     Document Type: Article

References (52)

1. Adham SA, Sher I, Coomber BL (2010) Molecular blockade of VEGFR2 in human epithelial ovarian carcinoma cells. Lab Invest 90: 709-723
2. Artaechevarria X, Blanco D, Perez-Martin D, de Biurrun G, Montuenga LM, de Torres JP, Zulueta JJ, Bastarrika G, Munoz-Barrutia A, Ortiz-de-Solorzano C (2010) Longitudinal study of a mouse model of chronic pulmonary inflammation using breath hold gated micro-CT. Eur Radiol 20: 2600-2608
3. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S et al (2009) Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 106: 16281-16286
4. Casanovas O (2012) Cancer: limitations of therapies exposed. Nature 484: 44-46
5. Catena R, Larzabal L, Larrayoz M, Molina E, Hermida J, Agorreta J, Montes R, Pio R, Montuenga LM, Calvo A (2010) VEGF(1)(2)(1)b and VEGF(1)(6)(5)b are weakly angiogenic isoforms of VEGF-A. Mol Cancer 9: 320
6. Chatterjee S, Heukamp LC, Siobal M, Schottle J, Wieczorek C, Peifer M, Frasca D, Koker M, Konig K, Meder L et al (2013) Tumor VEGF:VEGFR2 autocrine feed-forward loop triggers angiogenesis in lung cancer. J Clin Invest 123: 1732-1740
7. Chen Z, Cheng K, Walton Z, Wang Y, Ebi H, Shimamura T, Liu Y, Tupper T, Ouyang J, Li J et al (2012) A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 483: 613-617
8. Christensen JG (2007) A preclinical review of sunitinib, a multitargeted receptor tyrosine kinase inhibitor with anti-angiogenic and antitumour activities. Ann Oncol 18(Suppl 10): x3-x10
9. Cohen MH, Gootenberg J, Keegan P, Pazdur R (2007) FDA drug approval summary: bevacizumab (Avastin) plus Carboplatin and Paclitaxel as first-line treatment of advanced/metastatic recurrent nonsquamous non-small cell lung cancer. Oncologist 12: 713-718
10. Conley SJ, Gheordunescu E, Kakarala P, Newman B, Korkaya H, Heath AN, Clouthier SG, Wicha MS (2012) Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia. Proc Natl Acad Sci USA 109: 2784-2789
11. Ebos JM, Kerbel RS (2011) Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Oncol 8: 210-221
12. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15: 232-239
13. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M et al (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45: 228-247
14. Farago AF, Snyder EL, Jacks T (2012) SnapShot: Lung cancer models. Cell 149: 246-246 e241
15. Fritz JM, Dwyer-Nield LD, Russell BM, Malkinson AM (2010) The Kras mutational spectra of chemically induced lung tumors in different inbred mice mimics the spectra of KRAS mutations in adenocarcinomas in smokers versus nonsmokers. J Thorac Oncol 5: 254-257
16. Gandhi L, McNamara KL, Li D, Borgman CL, McDermott U, Brandstetter KA, Padera RF, Chirieac LR, Settleman JE, Wong KK (2009) Sunitinib prolongs survival in genetically engineered mouse models of multistep lung carcinogenesis. Cancer Prev Res (Phila) 2: 330-337
17. Goel HL, Mercurio AM (2013) VEGF targets the tumour cell. Nat Rev Cancer 13: 871-882
18. Hammerman PS, Lawrence MS, Voet D, Jing R, Cibulskis K, Sivachenko A, Stojanov P, McKenna A, Lander ES, Gabriel S et al (2012) Comprehensive genomic characterization of squamous cell lung cancers. Nature 489: 519-525
19. Hammerman PS, Sos ML, Ramos AH, Xu C, Dutt A, Zhou W, Brace LE, Woods BA, Lin W, Zhang J et al (2011) Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discov 1: 78-89
20. Iida H, Suzuki M, Goitsuka R, Ueno H (2012) Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int J Oncol 40: 71-79
21. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, Cho J, Suh J, Capelletti M, Sivachenko A et al (2012) Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 150: 1107-1120
22. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90
23. Johnson DH, Fehrenbacher L, Novotny WF, Herbst RS, Nemunaitis JJ, Jablons DM, Langer CJ, DeVore RF III, Gaudreault J, Damico LA et al (2004) Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. J Clin Oncol 22: 2184-2191
24. Karoor V, Le M, Merrick D, Dempsey EC, Miller YE (2010) Vascular endothelial growth factor receptor 2-targeted chemoprevention of murine lung tumors. Cancer Prev Res (Phila) 3: 1141-1147
25. Keith B, Simon MC (2007) Hypoxia-inducible factors, stem cells, and cancer. Cell 129: 465-472
26. Kwon MC, Berns A (2013) Mouse models for lung cancer. Mol Oncol 7: 165-177
27. Langer CJ, Besse B, Gualberto A, Brambilla E, Soria JC (2010) The evolving role of histology in the management of advanced non-small-cell lung cancer. J Clin Oncol 28: 5311-5320
28. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ (2006) Global Burden of Disease and Risk Factors. New York, NY: Oxford University Press and the World Bank
29. Masood R, Cai J, Zheng T, Smith DL, Hinton DR, Gill PS (2001) Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood 98: 1904-1913
30. Mountzios G, Dimopoulos MA, Soria JC, Sanoudou D, Papadimitriou CA (2010) Histopathologic and genetic alterations as predictors of response to treatment and survival in lung cancer: a review of published data. Crit Rev Oncol Hematol 75: 94-109
31. Nolte SM, Venugopal C, McFarlane N, Morozova O, Hallett RM, O'Farrell E, Manoranjan B, Murty NK, Klurfan P, Kachur E et al (2013) A cancer stem cell model for studying brain metastases from primary lung cancer. J Natl Cancer Inst 105: 551-562
32. Oie HK, Russell EK, Carney DN, Gazdar AF (1996) Cell culture methods for the establishment of the NCI series of lung cancer cell lines. J Cell Biochem Suppl 24: 24-31
33. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, Inoue M, Bergers G, Hanahan D, Casanovas O (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15: 220-231
34. Pajares MJ, Agorreta J, Larrayoz M, Vesin A, Ezponda T, Zudaire I, Torre W, Lozano MD, Brambilla E, Brambilla C et al (2012) Expression of tumor-derived vascular endothelial growth factor and its receptors is associated with outcome in early squamous cell carcinoma of the lung. J Clin Oncol 30: 1129-1136
35. Park SY, Lee HE, Li H, Shipitsin M, Gelman R, Polyak K (2010) Heterogeneity for stem cell-related markers according to tumor subtype and histologic stage in breast cancer. Clin Cancer Res 16: 876-887
36. Prewett M, Huber J, Li Y, Santiago A, O'Connor W, King K, Overholser J, Hooper A, Pytowski B, Witte L et al (1999) Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer Res 59: 5209-5218
37. Reck M, von Pawel J, Zatloukal P, Ramlau R, Gorbounova V, Hirsh V, Leighl N, Mezger J, Archer V, Moore N et al (2009) Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil. J Clin Oncol 27: 1227-1234
38. Reckamp KL (2012) Antiangiogenic agents as second-line therapy for advanced non-small cell lung cancer. Cancer Lett 321: 101-109
39. Rehm S, Lijinsky W, Singh G, Katyal SL (1991) Mouse bronchiolar cell carcinogenesis. Histologic characterization and expression of Clara cell antigen in lesions induced by N-nitrosobis-(2-chloroethyl) ureas. Am J Pathol 139: 413-422
40. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, Lilenbaum R, Johnson DH (2006) Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 355: 2542-2550
41. Scagliotti G, Novello S, von Pawel J, Reck M, Pereira JR, Thomas M, Abrao Miziara JE, Balint B, De Marinis F, Keller A et al (2010) Phase III study of carboplatin and paclitaxel alone or with sorafenib in advanced non-small-cell lung cancer. J Clin Oncol 28: 1835-1842
42. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V, Tabruyn SP, You WK, Chapman HA, Christensen JG et al (2012) Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2: 270-287
43. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63: 11-30
44. Silva SR, Bowen KA, Rychahou PG, Jackson LN, Weiss HL, Lee EY, Townsend CM Jr, Evers BM (2011) VEGFR-2 expression in carcinoid cancer cells and its role in tumor growth and metastasis. Int J Cancer 128: 1045-1056
45. Sos ML, Michel K, Zander T, Weiss J, Frommolt P, Peifer M, Li D, Ullrich R, Koker M, Fischer F et al (2009) Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. J Clin Invest 119: 1727-1740
46. Sos ML, Thomas RK (2012) Genetic insight and therapeutic targets in squamous-cell lung cancer. Oncogene 31: 4811-4814
47. Takahashi T, Sonobe M, Kobayashi M, Yoshizawa A, Menju T, Nakayama E, Mino N, Iwakiri S, Sato K, Miyahara R et al (2010) Clinicopathologic features of non-small-cell lung cancer with EML4-ALK fusion gene. Ann Surg Oncol 17: 889-897
48. Van der Veldt AA, Lubberink M, Bahce I, Walraven M, de Boer MP, Greuter HN, Hendrikse NH, Eriksson J, Windhorst AD, Postmus PE et al (2012) Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of anti-angiogenic drugs. Cancer Cell 21: 82-91
49. Wang Y, Zhang Z, Yan Y, Lemon WJ, LaRegina M, Morrison C, Lubet R, You M (2004) A chemically induced model for squamous cell carcinoma of the lung in mice: histopathology and strain susceptibility. Cancer Res 64: 1647-1654
50. Weiss J, Sos ML, Seidel D, Peifer M, Zander T, Heuckmann JM, Ullrich RT, Menon R, Maier S, Soltermann A et al (2010) Frequent and focal FGFR1 amplification associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med 2: 62ra93
51. Wu W, Onn A, Isobe T, Itasaka S, Langley RR, Shitani T, Shibuya K, Komaki R, Ryan AJ, Fidler IJ et al (2007) Targeted therapy of orthotopic human lung cancer by combined vascular endothelial growth factor and epidermal growth factor receptor signaling blockade. Mol Cancer Ther 6: 471-483
52. You MS, Rouggly LC, You M, Wang Y (2013) Mouse models of lung squamous cell carcinomas. Cancer Metast Rev 32: 77-82