Next-generation sequencing of pulmonary large cell neuroendocrine carcinoma reveals small cell carcinoma-like and non-small cell carcinoma-like subsets

Clinical Cancer Research

Volumn 22, Issue 14, 2016, Pages 3618-3629

  Rekhtman, Natasha ^a   Pietanza, Maria C ^a   Hellmann, Matthew D ^a   Naidoo, Jarushka ^a   Arora, Arshi ^a   Won, Helen ^a   Halpenny, Darragh F ^a   Wang, Hangjun ^a   Tian, Shaozhou K ^a   Litvak, Anya M ^a   Paik, Paul K ^a   Drilon, Alexander E ^a   Socci, Nicholas ^a   Poirier, John T ^a   Shen, Ronglai ^a   Berger, Michael F ^a   Moreira, Andre L ^a   Travis, William D ^a   Rudin, Charles M ^a   Marc, Ladanyi ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KELCH LIKE ECH ASSOCIATED PROTEIN 1; NOTCH RECEPTOR; PROTEIN KINASE LKB1; PROTEIN P53;

ADULT; AGED; ARTICLE; CANCER CLASSIFICATION; CANCER GENETICS; CANCER PATIENT; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE AMPLIFICATION; GENE MUTATION; GENOME ANALYSIS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KEAP1 GENE; LARGE CELL NEUROENDOCRINE CARCINOMA; LUNG CARCINOGENESIS; MALE; MEN1 GENE; MOLECULAR PATHOLOGY; MUTATION RATE; MYCL GENE; NEXT GENERATION SEQUENCING; NON SMALL CELL LUNG CANCER; NOTCH GENE; ONCOGENE K RAS; PRIORITY JOURNAL; RB1 GENE; SMALL CELL LUNG CANCER; SOMATIC MUTATION; STK11 GENE; TP53 GENE; TUMOR DIFFERENTIATION; ADENOCARCINOMA; CARCINOMA; GENETICS; HIGH THROUGHPUT SEQUENCING; LARGE CELL CARCINOMA; LUNG TUMOR; MIDDLE AGED; MUTATION; PROCEDURES; SMALL CELL CARCINOMA;

ADENOCARCINOMA; AGED; CARCINOMA, LARGE CELL; CARCINOMA, NEUROENDOCRINE; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SMALL CELL; FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; SMALL CELL LUNG CARCINOMA;

EID: 84978505017     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2946     Document Type: Article

References (50)

1. Travis WD, Linnoila RI, Tsokos MG, Hitchcock CL, Cutler GBJr, Nieman L, et al. Neuroendocrine tumors of the lung with proposed criteria for largecell neuroendocrine carcinoma. An ultrastructural, immunohistochemical, and flow cytometric study of 35 cases. Am J Surg Pathol 1991;15:529-53.
2. Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG, editors. WHO Classification of tumours of the lung, pleura, thymus and heart. 4th ed. Lyon, France: IARC Press; 2015.
3. McDowell EM, Wilson TS, Trump BF. Atypical endocrine tumors of the lung. Arch Pathol Lab Med 1981;105:20-8.
4. Rekhtman N. Neuroendocrine tumors of the lung: an update. Arch Pathol Lab Med 2010;134:1628-38.
5. Pelosi G, Hiroshima K, Mino-Kenudson M. Controversial issues and new discoveries in lung neuroendocrine tumors. Diagn Histopathol 2014;20: 392-7.
6. Travis WD, Gal AA, Colby TV, Klimstra DS, Falk R, Koss MN. Reproducibility of neuroendocrine lung tumor classification. Human Pathol 1998; 29:272-9.
7. Iyoda A, Hiroshima K, Nakatani Y, Fujisawa T. Pulmonary large cell neuroendocrine carcinoma: its place in the spectrum of pulmonary carcinoma. Ann Thorac Surg 2007;84:702-7.
8. Varlotto JM, Medford-Davis LN, Recht A, Flickinger JC, Schaefer E, Zander DS, et al. Should large cell neuroendocrine lung carcinoma be classified and treated as a small cell lung cancer or with other large cell carcinomas? J Thorac Oncol 2011;6:1050-8.
9. Rossi G, Cavazza A, Marchioni A, Longo L, Migaldi M, Sartori G, et al. Role of chemotherapy and the receptor tyrosine kinases KIT, PDGFRalpha, PDGFRbeta, and Met in large-cell neuroendocrine carcinoma of the lung. J Clin Oncol 2005;23:8774-85.
10. Naidoo J, Santos-Zabala ML, Iyriboz T, Woo KM, Sima CS, Fiore JJ, et al. Large cell neuroendocrine carcinoma of the lung: Clinico-pathologic features, treatment, and outcomes. Clin Lung Cancer 2016; Epub ahead of print.
11. Sarkaria IS, Iyoda A, Roh MS, Sica G, Kuk D, Sima CS, et al. Neoadjuvant and adjuvant chemotherapy in resected pulmonary large cell neuroendocrine carcinomas: a single institution experience. Ann Thorac Surg 2011; 92:1180-6.
12. Gazdar AF, Savage TK, Johnson JE, Berns A, Sage J, Linnoila RI, et al. The comparative pathology of genetically engineered mouse models for neuroendocrine carcinomas of the lung. J Thorac Oncol 2015;10:553-64.
13. Jones MH, Virtanen C, Honjoh D, Miyoshi T, Satoh Y, Okumura S, et al. Two prognostically significant subtypes of high-grade lung neuroendocrine tumours independent of small-cell and large-cell neuroendocrine carcinomas identified by gene expression profiles. Lancet 2004;363: 775-81.
14. Bari MF, Brown H, Nicholson AG, Kerr KM, Gosney JR, Wallace WA, et al. BAI3, CDX2 and VIL1: a panel of three antibodies to distinguish small cell from large cell neuroendocrine lung carcinomas. Histopathology 2014; 64:547-56.
15. Przygodzki RM, Finkelstein SD, Langer JC, Swalsky PA, Fishback N, Bakker A, et al. Analysis of p53, K-ras-2, and C-raf-1 in pulmonary neuroendocrine tumors. Correlation with histological subtype and clinical outcome. Am J Pathol 1996;148:1531-41.
16. Rusch VW, Klimstra DS, Venkatraman ES. Molecular markers help characterize neuroendocrine lung tumors. Ann Thorac Surg 1996;62:798-809.
17. Clinical Lung Cancer Genome P, Network Genomic M. A genomics-based classification of human lung tumors. Sci Transl Med 2013;5:209ra153.
18. De Pas TM, Giovannini M, Manzotti M, Trifiro G, Toffalorio F, Catania C, et al. Large-cell neuroendocrine carcinoma of the lung harboring EGFR mutation and responding to gefitinib. J Clin Oncol 2011;29:e819-22.
19. Aroldi F, Bertocchi P, Meriggi F, Abeni C, Ogliosi C, Rota L, et al. Tyrosine kinase inhibitors in EGFR-mutated large-cell neuroendocrine carcinoma of the lung? A case report. Case Rep Oncol 2014;7: 478-83.
20. Omachi N, Shimizu S, Kawaguchi T, Tezuka K, Kanazu M, Tamiya A, et al. A case of large-cell neuroendocrine carcinoma harboring an EML4-ALK rearrangement with resistance to the ALK inhibitor crizotinib. J Thorac Oncol 2014;9:e40-2.
21. Karlsson A, Brunnstrom H, Lindquist KE, Jirstrom K, Jonsson M, Rosengren F, et al. Mutational and gene fusion analyses of primary large cell and large cell neuroendocrine lung cancer. Oncotarget 2015; 6:22028-37.
22. George J, Lim JS, Jang SJ, Cun Y, Ozretic L, Kong G, et al. Comprehensive genomic profiles of small cell lung cancer. Nature 2015;524:47-53.
23. Rudin CM, Durinck S, Stawiski EW, Poirier JT, Modrusan Z, Shames DS, et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat Genet 2012;44:1111-6.
24. PietanzaMC,WonHH,RekhtmanN,WangL,TravisWD,KrugLM,etal. Prospective molecular analysis of small cell lung cancer (SCLC) using next generation sequencing (NGS). J Clin Oncol 33, 2015(suppl; abstr 7518).
25. Cheng DT, Mitchell TN, Zehir A, Shah RH, Benayed R, Syed A, et al. Memorial sloan kettering-integrated mutation profiling of actionable cancer targets (MSK-IMPACT): a hybridization capture-based next-generation sequencing clinical assay for solid tumor molecular oncology. J Mol Diagn 2015;17:251-64.
26. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signaling 2013;6:pl1.
27. Hyman DM, Solit DB, Arcila ME, Cheng DT, Sabbatini P, Baselga J, et al. Precision medicine at Memorial Sloan Kettering Cancer Center: clinical next-generation sequencing enabling next-generation targeted therapy trials. Drug Discov Today 2015;20:1422-8.
28. Paik PK, Shen R, Won H, Rekhtman N, Wang L, Sima CS, et al. Next-Generation sequencing of stage IV squamous cell lung cancers reveals an association of PI3K aberrations and evidence of clonal heterogeneity in patients with brain metastases. Cancer Discov 2015;5:610-21.
29. Poirier JT, Gardner EE, Connis N, Moreira AL, de Stanchina E, Hann CL, et al. DNA methylation in small cell lung cancer defines distinct disease subtypes and correlates with high expression of EZH2. Oncogene 2015; 34:5869-78.
30. Skoulidis F, Byers LA, Diao L, Papadimitrakopoulou VA, Tong P, Izzo J, et al. Co-occurring genomic alterations define major subsets of KRASmutant lung adenocarcinoma with distinct biology, immune profiles, and therapeutic vulnerabilities. Cancer Discov 2015;5:860-77.
31. Kaufman JM, Amann JM, Park K, Arasada RR, Li H, Shyr Y, et al. LKB1 Loss induces characteristic patterns of gene expression in human tumors associated with NRF2 activation and attenuation of PI3K-AKT. J Thorac Oncol 2014;9:794-804.
32. Wang NJ, Sanborn Z, Arnett KL, Bayston LJ, Liao W, Proby CM, et al. Lossof-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc Natl Acad Sci U S A 2011;108:17761-6.
33. Cancer Genome Atlas Research N. Comprehensive molecular profiling of lung adenocarcinoma. Nature 2014;511:543-50.
34. Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, Vasa P, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 2001;98:13790-5.
35. Augustyn A, Borromeo M, Wang T, Fujimoto J, Shao C, Dospoy PD, et al. ASCL1 is a lineage oncogene providing therapeutic targets for high-grade neuroendocrine lung cancers. Proc Natl Acad Sci U S A 2014;111:14788-93.
36. Kosari F, Ida CM, Aubry MC, Yang L, Kovtun IV, Klein JL, et al. ASCL1 and RET expression defines a clinically relevant subgroup of lung adenocarcinoma characterized by neuroendocrine differentiation. Oncogene 2014; 33:3776-83.
37. Joubert P, Wang H, Roh MS, Pietanza MC, Sarkaria I, Travis WD, et al. Napsin A expression in neuroendocrine tumors of the lung. Mod Pathol 2013;26:456A(suppl; abstr 7518).
38. Lai D, Chen Y, Wang F, Jiang L, Wei C. LKB1 controls the pluripotent state of human embryonic stem cells. Cell Reprogram 2012; 14:164-70.
39. Ji H, Ramsey MR, Hayes DN, Fan C, McNamara K, Kozlowski P, et al. LKB1 modulates lung cancer differentiation and metastasis. Nature 2007; 448:807-10.
40. Calles A, Sholl LM, Rodig SJ, Pelton AK, Hornick JL, Butaney M, et al. Immunohistochemical loss of LKB1 is a biomarker for more aggressive biology in KRAS-mutant lung adenocarcinoma. Clin Cancer Res 2015; 21:2851-60.
41. Meder L, Konig K, Ozretic L, Schultheis AM, Ueckeroth F, Ade CP, et al. NOTCH, ASCL1, p53 and RB alterations define an alternative pathway driving neuroendocrine and small cell lung carcinomas. Int J Cancer 2016;138:927-38.
42. Marchetti A, Felicioni L, Pelosi G, Del Grammastro M, Fumagalli C, Sciarrotta M, et al. Frequent mutations in the neurotrophic tyrosine receptor kinase gene family in large cell neuroendocrine carcinoma of the lung. Hum Mut 2008;29:609-16.
43. Ball DW. Achaete-scute homolog-1 and Notch in lung neuroendocrine development and cancer. Cancer Lett 2004;204:159-69.
44. Fernandez-Cuesta L, Peifer M, Lu X, Sun R, Ozretic L, Seidel D, et al. Frequent mutations in chromatin-remodelling genes in pulmonary carcinoids. Nat Commun 2014;5:3518.
45. Pietanza MC, Ladanyi M. Bringing the genomic landscape of small-cell lung cancer into focus. Nat Genet 2012;44:1074-5.
46. Wikenheiser-Brokamp KA. Rb family proteins differentially regulate distinct cell lineages during epithelial development. Development 2004;131: 4299-310.
47. Basturk O, Yang Z, Tang LH, Hruban RH, Adsay V, McCall CM, et al. The high-grade (WHO G3) pancreatic neuroendocrine tumor category is morphologically and biologically heterogenous and includes both well differentiated and poorly differentiated neoplasms. Am J Surg Pathol 2015;39:683-90.
48. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348:124-8.
49. Forde PM, Brahmer JR, Kelly RJ. New strategies in lung cancer: epigenetic therapy for non-small cell lung cancer. Clin Cancer Res 2014; 20:2244-8.
50. Rekhtman N, Tafe LJ, Chaft JE, Wang L, Arcila ME, Colanta A, et al. Distinct profile of driver mutations and clinical features in immunomarker-defined subsets of pulmonary large-cell carcinoma. Mod Pathol 2013;26:511-22.