Revisiting clinical trials using EGFR inhibitor-based regimens in patients with advanced non-small cell lung cancer: A retrospective analysis of an MD Anderson Cancer Center phase I population

Oncotarget

Volumn 4, Issue 5, 2013, Pages 772-784

  Wheler, Jennifer ^a   Falchook, Gerald ^a   Tsimberidou, Apostolia M ^a   Hong, David ^a   Naing, Aung ^a   Piha Paul, Sarina ^a   Chen, Su S ^a   Heymach, John ^a   Fu, Siqing ^a   Stephen, Bettzy ^a   Fok, Jansina Y ^a   Janku, Filip ^a   Kurzrock, Razelle ^b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

EGFR mutation; EGFR wild type; Non small cell lung cancer; Phase I trials; Resistance; Squamous cell

Indexed keywords

BEVACIZUMAB; BORTEZOMIB; CETUXIMAB; DASATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; K RAS PROTEIN; PROTEIN P53; RAPAMYCIN; TUMOR PROTEIN;

ADULT; ADVANCED CANCER; AGED; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER REGRESSION; CANCER RESISTANCE; CANCER SURVIVAL; CLINICAL ARTICLE; DISEASE DURATION; DRUG RESPONSE; EPIDERMAL GROWTH FACTOR RECEPTOR GENE; FEMALE; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LUNG NON SMALL CELL CANCER; MALE; MEDICAL RECORD REVIEW; ONCOGENE K RAS; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PIK3CA GENE; SQUAMOUS CELL CARCINOMA; TREATMENT OUTCOME; TUMOR GENE; TUMOR SUPPRESSOR GENE; WILD TYPE;

EID: 84880303931     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1028     Document Type: Article

References (48)

1. Sharma SV, Bell DW, Settleman J and Haber DA. Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer. 2007; 7(3):169-181.
2. Chintala L and Kurzrock R. Epidermal growth factor receptor mutation and diverse tumors: case report and concise literature review. Mol Oncol. 2010; 4(4):306-308.
3. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, Settleman J and Haber DA. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004; 350(21):2129-2139.
4. Riely GJ, Pao W, Pham D, Li AR, Rizvi N, Venkatraman ES, Zakowski MF, Kris MG, Ladanyi M and Miller VA. Clinical course of patients with non-small cell lung cancer and epidermal growth factor receptor exon 19 and exon 21 mutations treated with gefitinib or erlotinib. Clin Cancer Res. 2006; 12(3 Pt 1):839-844.
5. Janku F, Garrido-Laguna I, Petruzelka LB, Stewart DJ and Kurzrock R. Novel therapeutic targets in non-small cell lung cancer. J Thorac Oncol. 2011; 6(9):1601-1612.
6. Okamoto I, Araki J, Suto R, Shimada M, Nakagawa K and Fukuoka M. EGFR mutation in gefitinib-responsive smallcell lung cancer. Ann Oncol. 2006; 17(6):1028-1029.
7. Hammerman PS, Janne PA and Johnson BE. Resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res. 2009; 15(24):7502-7509.
8. Mumenthaler SM, Foo J, Leder K, Choi NC, Agus DB, Pao W, Mallick P and Michor F. Evolutionary modeling of combination treatment strategies to overcome resistance to tyrosine kinase inhibitors in non-small cell lung cancer. Mol Pharm. 2011; 8(6):2069-2079.
9. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, Tan EH, Hirsh V, Thongprasert S, Campos D, Maoleekoonpiroj S, Smylie M, Martins R, van Kooten M, Dediu M, Findlay B, Tu D, Johnston D, Bezjak A, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med. 2005; 353(2):123-132.
10. Weihua Z, Tsan R, Huang WC, Wu Q, Chiu CH, Fidler IJ and Hung MC. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell. 2008; 13(5):385-393.
11. Song L, Morris M, Bagui T, Lee FY, Jove R and Haura EB. Dasatinib (BMS-354825) selectively induces apoptosis in lung cancer cells dependent on epidermal growth factor receptor signaling for survival. Cancer Res. 2006; 66(11):5542-5548.
12. Cascone T, Morelli MP, Morgillo F, Kim WY, Rodolico G, Pepe S, Tortora G, Berrino L, Lee HY, Heymach JV and Ciardiello F. Synergistic anti-proliferative and proapoptotic activity of combined therapy with bortezomib, a proteasome inhibitor, with anti-epidermal growth factor receptor (EGFR) drugs in human cancer cells. J Cell Physiol. 2008; 216(3):698-707.
13. Yasuda H, Kobayashi S and Costa DB. EGFR exon 20 insertion mutations in non-small-cell lung cancer: preclinical data and clinical implications. Lancet Oncol. 2012; 13(1):e23-31.
14. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno- Jones S and Sawyers CL. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001; 344(14):1031- 1037.
15. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, Heinrich MC, Tuveson DA, Singer S, Janicek M, Fletcher JA, Silverman SG, Silberman SL, Capdeville R, Kiese B, Peng B, et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med. 2002; 347(7):472-480.
16. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O'Dwyer PJ, Lee RJ, Grippo JF, Nolop K and Chapman PB. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med. 2010; 363(9):809-819.
17. Falchook GS, Long GV, Kurzrock R, Kim KB, Arkenau TH, Brown MP, Hamid O, Infante JR, Millward M, Pavlick AC, O'Day SJ, Blackman SC, Curtis CM, Lebowitz P, Ma B, Ouellet D, et al. Dabrafenib in patients with melanoma, untreated brain metastases, and other solid tumours: a phase 1 dose-escalation trial. Lancet. 2012; 379(9829):1893-1901.
18. Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, Engelman JA, Shapiro GI, Costa DB, Ou SH, Butaney M, Salgia R, Maki RG, Varella-Garcia M, Doebele RC, Bang YJ, Kulig K, et al. Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol. 2011; 12(11):1004-1012.
19. Janku F, Tsimberidou AM, Garrido-Laguna I, Wang X, Luthra R, Hong DS, Naing A, Falchook GS, Moroney JW, Piha-Paul SA, Wheler JJ, Moulder SL, Fu S and Kurzrock R. PIK3CA mutations in patients with advanced cancers treated with PI3K/AKT/mTOR axis inhibitors. Mol Cancer Ther. 2011; 10(3):558-565.
20. Braiteh F and Kurzrock R. Uncommon tumors and exceptional therapies: paradox or paradigm? Mol Cancer Ther. 2007; 6(4):1175-1179.
21. Garrido-Laguna I, Hidalgo M and Kurzrock R. The inverted pyramid of biomarker-driven trials. Nat Rev Clin Oncol. 2011; 8(9):562-566.
22. Janku F, Wheler JJ, Westin SN, Moulder SL, Naing A, Tsimberidou AM, Fu S, Falchook GS, Hong DS, Garrido- Laguna I, Luthra R, Lee JJ, Lu KH and Kurzrock R. PI3K/AKT/mTOR inhibitors in patients with breast and gynecologic malignancies harboring PIK3CA mutations. J Clin Oncol. 2012; 30(8):777-782.
23. Moroney J, Wheler J, Hong D, Naing A, Falchook G, Bodurka D, Coleman R, Lu KR, Xiao LC and Kurzrock R. Phase I clinical trials in 85 patients with gynecologic cancer: The M. D. Anderson Cancer Center experience. Gynecologic Oncology. 2010; 117(3):467-472.
24. Tsimberidou AM, Iskander NG, Hong DS, Wheler JJ, Falchook GS, Fu S, Piha-Paul S, Naing A, Janku F, Luthra R, Ye Y, Wen S, Berry D and Kurzrock R. Personalized medicine in a phase I clinical trials program: the MD Anderson Cancer Center initiative. Clin Cancer Res. 2012; 18(22):6373-6383.
25. Sordella R, Bell DW, Haber DA and Settleman J. Gefitinibsensitizing EGFR mutations in lung cancer activate antiapoptotic pathways. Science. 2004; 305(5687):1163-1167.
26. Jiang J, Greulich H, Janne PA, Sellers WR, Meyerson M and Griffin JD. Epidermal growth factor-independent transformation of Ba/F3 cells with cancer-derived epidermal growth factor receptor mutants induces gefitinib-sensitive cell cycle progression. Cancer Res. 2005; 65(19):8968- 8974.
27. Sequist LV, Bell DW, Lynch TJ and Haber DA. Molecular predictors of response to epidermal growth factor receptor antagonists in non-small-cell lung cancer. J Clin Oncol. 2007; 25(5):587-595.
28. Huang S, Armstrong EA, Benavente S, Chinnaiyan P and Harari PM. Dual-agent molecular targeting of the epidermal growth factor receptor (EGFR): combining anti-EGFR antibody with tyrosine kinase inhibitor. Cancer Res. 2004; 64(15):5355-5362.
29. Matar P, Rojo F, Cassia R, Moreno-Bueno G, Di Cosimo S, Tabernero J, Guzman M, Rodriguez S, Arribas J, Palacios J and Baselga J. Combined epidermal growth factor receptor targeting with the tyrosine kinase inhibitor gefitinib (ZD1839) and the monoclonal antibody cetuximab (IMC-C225): superiority over single-agent receptor targeting. Clin Cancer Res. 2004; 10(19):6487-6501.
30. Sequist LV, Waltman BA, Dias-Santagata D, Digumarthy S, Turke AB, Fidias P, Bergethon K, Shaw AT, Gettinger S, Cosper AK, Akhavanfard S, Heist RS, Temel J, Christensen JG, Wain JC, Lynch TJ, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med. 2011; 3(75):75ra26.
31. Zou ZQ, Zhang XH, Wang F, Shen QJ, Xu J, Zhang LN, Xing WH, Zhuo RJ and Li D. A novel dual PI3Kalpha/ mTOR inhibitor PI-103 with high antitumor activity in nonsmall cell lung cancer cells. Int J Mol Med. 2009; 24(1):97- 101.
32. Pao W and Girard N. New driver mutations in non-smallcell lung cancer. Lancet Oncol. 2011; 12(2):175-180.
33. Chaft JE, Arcila ME, Paik PK, Lau C, Riely GJ, Pietanza MC, Zakowski MF, Rusch V, Sima CS, Ladanyi M and Kris MG. Coexistence of PIK3CA and other oncogene mutations in lung adenocarcinoma-rationale for comprehensive mutation profiling. Mol Cancer Ther. 2012; 11(2):485-491.
34. Tabernero J. The role of VEGF and EGFR inhibition: implications for combining anti-VEGF and anti-EGFR agents. Mol Cancer Res. 2007; 5(3):203-220.
35. Saltz LB, Lenz HJ, Hochster H, Wadler S, Hoff P, Kemeny N, Hollywood E, Gonen M, Wetherbee S and Chen H. Randomized phase II trial of cetuximab/bevacizumab/ irinotecan (CBI) versus cetuximab/bevacizumab (CB) in irinotecan-refractory colorectal cancer. Journal of Clinical Oncology. 2005; 23(16):248s-248s.
36. Herbst RS, Johnson DH, Mininberg E, Carbone DP, Henderson T, Kim ES, Blumenschein G, Jr., Lee JJ, Liu DD, Truong MT, Hong WK, Tran H, Tsao A, Xie D, Ramies DA, Mass R, et al. Phase I/II trial evaluating the anti-vascular endothelial growth factor monoclonal antibody bevacizumab in combination with the HER-1/ epidermal growth factor receptor tyrosine kinase inhibitor erlotinib for patients with recurrent non-small-cell lung cancer. J Clin Oncol. 2005; 23(11):2544-2555.
37. Janku F, Stewart DJ and Kurzrock R. Targeted therapy in non-small-cell lung cancer--is it becoming a reality? Nat Rev Clin Oncol. 2010; 7(7):401-414.
38. Jackman D, Pao W, Riely GJ, Engelman JA, Kris MG, Janne PA, Lynch T, Johnson BE and Miller VA. Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. J Clin Oncol. 2010; 28(2):357-360.
39. Wang F, Wang J, Bai H, Zhao J, Wang Z, Zhuo M, An T, Duan J, Yang L, Wu M, Wang Y, Wang S and Liu X. An evaluation of phosphorylated EGFR expression in predicting outcome of EGFR-TKI therapy for the advanced NSCLC patients with EGFR wild type [abstract 7532]. J Clin Oncol 2011; 29:s 2011.
40. Falchook GS, Naing A, Hong DS, Zinner R, Fu S, Piha-Paul SA, Tsimberidou AM, Morgan-Linnell SK, Jiang Y, Bastida C, Wheler JJ and Kurzrock R. Dual EGFR inhibition in combination with anti-VEGF treatment: A phase I clinical trial in non-small cell lung cancer. Oncotarget. 2013; 4(1):118-127
41. Ramalingam S, Forster J, Naret C, Evans T, Sulecki M, Lu H, Teegarden P, Weber MR and Belani CP. Dual inhibition of the epidermal growth factor receptor with cetuximab, anIgG1 monoclonal antibody, and gefitinib, a tyrosine kinase inhibitor, in patients with refractory non-small cell lung cancer (NSCLC): a phase I study. J Thorac Oncol. 2008; 3(3):258-264.
42. Rekhtman N, Paik PK, Arcila ME, Tafe LJ, Oxnard GR, Moreira AL, Travis WD, Zakowski MF, Kris MG and Ladanyi M. Clarifying the spectrum of driver oncogene mutations in biomarker-verified squamous carcinoma of lung: lack of EGFR/KRAS and presence of PIK3CA/AKT1 mutations. Clin Cancer Res. 2012; 18(4):1167-1176.
43. Gurpide A, Massuti B, Pallares C, Salinas P, Montes A, Lopez-Vivanco G, Baron MG, Cobo M, Amador ML and Paz-Ares L. Erlotinib in patients with advanced squamous cell carcinoma of the lung. J Clin Oncol. 2006; 24(18):407s-407s.
44. Pirker R, Pereira JR, Szczesna A, von Pawel J, Krzakowski M, Ramlau R, Vynnychenko I, Park K, Yu CT, Ganul V, Roh JK, Bajetta E, O'Byrne K, de Marinis F, Eberhardt W, Goddemeier T, et al. Cetuximab plus chemotherapy in patients with advanced non-small-cell lung cancer (FLEX): an open-label randomised phase III trial. Lancet. 2009; 373(9674):1525-1531.
45. Said R, Hong D, Wheler J, Naing A, Falchook G, Fu S, Janku F, Zinner R, Piha-Paul S, Warneke CL, Tsimberidou A and Kurzrock R. (2012). p53 mutations in advanced cancers: clinical characteristics and outcomes in a phase I setting. J Clin Oncol 30, 2012 (suppl; abstr 10607)
46. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC and Gwyther SG. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst. 2000; 92(3):205-216.
47. Kaplan EL and Meier P. Nonparametric estimation from incomplete observations Journal of the American Statistical Association 1958; 53(282):457-481.
48. Mantel N. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother Rep. 1966; 50(3):163-170.