Transformation from non-small-cell lung cancer to small-cell lung cancer: Molecular drivers and cells of origin

The Lancet Oncology

Volumn 16, Issue 4, 2015, Pages e165-e172

  Oser, Matthew G ^a   Niederst, Matthew J ^a   Sequist, Lecia V ^a   Engelman, Jeffrey A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE INHIBITOR;

ADENOCARCINOMA; DRUG RESISTANCE; GENETICS; HUMAN; MUTATION; NON SMALL CELL LUNG CANCER; PATHOLOGY; SMALL CELL LUNG CANCER; SQUAMOUS CELL CARCINOMA;

ADENOCARCINOMA; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; DRUG RESISTANCE, NEOPLASM; HUMANS; MUTATION; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SMALL CELL LUNG CARCINOMA;

EID: 84934292801     PISSN: 14702045     EISSN: 14745488     Source Type: Journal    
DOI: 10.1016/S1470-2045(14)71180-5     Document Type: Review

References (64)

1. Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 2010, 362:2380-2388. the North-East Japan Study Group.
2. Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib 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. the West Japan Oncology Group.
3. Rosell R, Carcereny E, Gervais R, et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol 2012, 13:239-246. the Spanish Lung Cancer Group in collaboration with Groupe Français de Pneumo-Cancérologie and Associazione Italiana Oncologia Toracica.
4. Sequist LV, Yang JC, Yamamoto N, et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol 2013, 31:3327-3334.
5. Wu YL, Zhou C, Hu CP, et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6): an open-label, randomised phase 3 trial. Lancet Oncol 2014, 15:213-222.
6. Zhou C, Wu YL, Chen G, et al. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol 2011, 12:735-742.
7. Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009, 361:947-957.
8. Engelman JA, Jänne PA Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2008, 14:2895-2899.
9. Sequist LV, Waltman BA, Dias-Santagata D, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med 2011, 3:75ra26.
10. Yu HA, Arcila ME, Rekhtman N, et al. Analysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-mutant lung cancers. Clin Cancer Res 2013, 19:2240-2247.
11. Kalemkerian GP, Akerley W, Bogner P, et al. Small cell lung cancer. J Natl Compr Canc Netw 2013, 11:78-98. the National Comprehensive Cancer Network.
12. Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 2008, 26:3543-3551.
13. Jackman DM, Johnson BE Small-cell lung cancer. Lancet 2005, 366:1385-1396.
14. van Meerbeeck JP, Fennell DA, De Ruysscher DK Small-cell lung cancer. Lancet 2011, 378:1741-1755.
15. Goldstraw P, Ball D, Jett JR, et al. Non-small-cell lung cancer. Lancet 2011, 378:1727-1740.
16. Socinski MA, Smit EF, Lorigan P, et al. Phase III study of pemetrexed plus carboplatin compared with etoposide plus carboplatin in chemotherapy-naive patients with extensive-stage small-cell lung cancer. J Clin Oncol 2009, 27:4787-4792.
17. Byers LA, Wang J, Nilsson MB, et al. Proteomic profiling identifies dysregulated pathways in small cell lung cancer and novel therapeutic targets including PARP1. Cancer Discov 2012, 2:798-811.
18. Ozasa H, Oguri T, Uemura T, et al. Significance of thymidylate synthase for resistance to pemetrexed in lung cancer. Cancer Sci 2010, 101:161-166.
19. Adelstein DJ, Tomashefski JF, Snow NJ, Horrigan TP, Hines JD Mixed small cell and non-small cell lung cancer. Chest 1986, 89:699-704.
20. Mangum MD, Greco FA, Hainsworth JD, Hande KR, Johnson DH Combined small-cell and non-small-cell lung cancer. J Clin Oncol 1989, 7:607-612.
21. Yun CH, Mengwasser KE, Toms AV, et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA 2008, 105:2070-2075.
22. Engelman JA, Zejnullahu K, Mitsudomi T, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
23. Zakowski MF, Ladanyi M, Kris MG EGFR mutations in small-cell lung cancers in patients who have never smoked. N Engl J Med 2006, 355:213-215. the Memorial Sloan-Kettering Cancer Center Lung Cancer OncoGenome Group.
24. van Riel S, Thunnissen E, Heideman D, Smit EF, Biesma B A patient with simultaneously appearing adenocarcinoma and small-cell lung carcinoma harbouring an identical EGFR exon 19 mutation. Ann Oncol 2012, 23:3188-3189.
25. Morinaga R, Okamoto I, Furuta K, et al. Sequential occurrence of non-small cell and small cell lung cancer with the same EGFR mutation. Lung Cancer 2007, 58:411-413.
26. Norkowski E, Ghigna MR, Lacroix L, et al. Small-cell carcinoma in the setting of pulmonary adenocarcinoma: new insights in the era of molecular pathology. J Thorac Oncol 2013, 8:1265-1271.
27. Watanabe S, Sone T, Matsui T, et al. Transformation to small-cell lung cancer following treatment with EGFR tyrosine kinase inhibitors in a patient with lung adenocarcinoma. Lung Cancer 2013, 82:370-372.
28. Popat S, Wotherspoon A, Nutting CM, Gonzalez D, Nicholson AG, O'Brien M Transformation to "high grade" neuroendocrine carcinoma as an acquired drug resistance mechanism in EGFR-mutant lung adenocarcinoma. Lung Cancer 2013, 80:1-4.
29. Shiao TH, Chang YL, Yu CJ, et al. Epidermal growth factor receptor mutations in small cell lung cancer: a brief report. J Thorac Oncol 2011, 6:195-198.
30. Tatematsu A, Shimizu J, Murakami Y, et al. Epidermal growth factor receptor mutations in small cell lung cancer. Clin Cancer Res 2008, 14:6092-6096.
31. Araki J, Okamoto I, Suto R, Ichikawa Y, Sasaki J Efficacy of the tyrosine kinase inhibitor gefitinib in a patient with metastatic small cell lung cancer. Lung Cancer 2005, 48:141-144.
32. Okamoto I, Araki J, Suto R, Shimada M, Nakagawa K, Fukuoka M EGFR mutation in gefitinib-responsive small-cell lung cancer. Ann Oncol 2006, 17:1028-1029.
33. Fukui T, Tsuta K, Furuta K, et al. Epidermal growth factor receptor mutation status and clinicopathological features of combined small cell carcinoma with adenocarcinoma of the lung. Cancer Sci 2007, 98:1714-1719.
34. Lu HY, Sun WY, Chen B, et al. Epidermal growth factor receptor mutations in small cell lung cancer patients who received surgical resection in China. Neoplasma 2012, 59:100-104.
35. Kurahara Y, Kawaguchi T, Tachibana K, et al. Small-cell lung cancer in never-smokers: a case series with information on family history of cancer and environmental tobacco smoke. Clin Lung Cancer 2012, 13:75-79.
36. Moore AM, Einhorn LH, Estes D, et al. Gefitinib in patients with chemo-sensitive and chemo-refractory relapsed small cell cancers: a Hoosier Oncology Group phase II trial. Lung Cancer 2006, 52:93-97.
37. Niederst MJ, Sequist LV, Poirier JT, et al. RB loss in resistant EGFR mutant lung adenocarcinomas that transform to small-cell lung cancer. Nat Commun 2015, 6:6377.
38. Cerny T, Barnes DM, Hasleton P, et al. Expression of epidermal growth factor receptor (EGF-R) in human lung tumours. Br J Cancer 1986, 54:265-269.
39. Sobol RE, Astarita RW, Hofeditz C, et al. Epidermal growth factor receptor expression in human lung carcinomas defined by a monoclonal antibody. J Natl Cancer Inst 1987, 79:403-407.
40. Imielinski M, Berger AH, Hammerman PS, et al. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 2012, 150:1107-1120.
41. Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 2010, 363:1693-1703.
42. Shaw AT, Kim DW, Mehra R, et al. Ceritinib in ALK-rearranged non-small-cell lung cancer. N Engl J Med 2014, 370:1189-1197.
43. Ohashi K, Maruvka YE, Michor F, Pao W Epidermal growth factor receptor tyrosine kinase inhibitor-resistant disease. J Clin Oncol 2013, 31:1070-1080.
44. Ou SH Lung cancer in never-smokers. Does smoking history matter in the era of molecular diagnostics and targeted therapy?. J Clin Pathol 2013, 66:839-846.
45. Sequist LV, Heist RS, Shaw AT, et al. Implementing multiplexed genotyping of non-small-cell lung cancers into routine clinical practice. Ann Oncol 2011, 22:2616-2624.
46. Peifer M, Fernández-Cuesta L, Sos ML, et al. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat Genet 2012, 44:1104-1110.
47. Rudin CM, Durinck S, Stawiski EW, et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat Genet 2012, 44:1111-1116.
48. Meuwissen R, Linn SC, Linnoila RI, Zevenhoven J, Mooi WJ, Berns A Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 2003, 4:181-189.
49. Tan HL, Sood A, Rahimi HA, et al. Rb loss is characteristic of prostatic small cell neuroendocrine carcinoma. Clin Cancer Res 2014, 20:890-903.
50. Sharma A, Yeow WS, Ertel A, et al. The retinoblastoma tumor suppressor controls androgen signaling and human prostate cancer progression. J Clin Invest 2010, 120:4478-4492.
51. Gao J, Aksoy BA, Dogrusoz U, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013, 6:pl1.
52. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA Effects of an Rb mutation in the mouse. Nature 1992, 359:295-300.
53. Wikenheiser-Brokamp KA Rb family proteins differentially regulate distinct cell lineages during epithelial development. Development 2004, 131:4299-4310.
54. Choong NW, Quevedo JF, Kaur JS Small cell carcinoma of the urinary bladder. The Mayo Clinic experience. Cancer 2005, 103:1172-1178.
55. Sutherland KD, Proost N, Brouns I, Adriaensen D, Song JY, Berns A Cell of origin of small cell lung cancer: inactivation of Trp53 and Rb1 in distinct cell types of adult mouse lung. Cancer Cell 2011, 19:754-764.
56. Park KS, Liang MC, Raiser DM, et al. Characterization of the cell of origin for small cell lung cancer. Cell Cycle 2011, 10:2806-2815.
57. Mainardi S, Mijimolle N, Francoz S, Vicente-Dueñas C, Sánchez-García I, Barbacid M Identification of cancer initiating cells in K-Ras driven lung adenocarcinoma. Proc Natl Acad Sci USA 2014, 111:255-260.
58. Sutherland KD, Song JY, Kwon MC, Proost N, Zevenhoven J, Berns A Multiple cells-of-origin of mutant K-Ras-induced mouse lung adenocarcinoma. Proc Natl Acad Sci USA 2014, 111:4952-4957.
59. Song H, Yao E, Lin C, Gacayan R, Chen MH, Chuang PT Functional characterization of pulmonary neuroendocrine cells in lung development, injury, and tumorigenesis. Proc Natl Acad Sci USA 2012, 109:17531-17536.
60. Lin C, Song H, Huang C, et al. Alveolar type II cells possess the capability of initiating lung tumor development. PLoS One 2012, 7:e53817.
61. Desai TJ, Brownfield DG, Krasnow MA Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature 2014, 507:190-194.
62. Miettinen PJ, Berger JE, Meneses J, et al. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 1995, 376:337-341.
63. Miettinen PJ, Warburton D, Bu D, et al. Impaired lung branching morphogenesis in the absence of functional EGF receptor. Dev Biol 1997, 186:224-236.
64. Liu Y, Xu ML, Zhong HH, Heng WJ, Wu BQ EGFR mutations are more frequent in well-differentiated than in poor-differentiated lung adenocarcinomas. Pathol Oncol Res 2008, 14:373-379.