The airway transcriptome as a biomarker for early lung cancer detection

Clinical Cancer Research

Volumn 24, Issue 13, 2018, Pages 2984-2992

  Billatos, Ehab ^a   Vick, Jessica L ^a   Lenburg, Marc E ^a   Spira, Avrum E ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; GLUTATHIONE; K RAS PROTEIN; SUPEROXIDE DISMUTASE; TRANSCRIPTOME; TUMOR MARKER;

BRONCHOSCOPY; CANCER RISK; CARCINOGENESIS; CARCINOGENICITY; CELL PROLIFERATION; DNA REPAIR; EARLY CANCER DIAGNOSIS; EPITHELIUM HYPERPLASIA; GENE EXPRESSION; GENE MUTATION; GLUTATHIONE METABOLISM; HUMAN; IMMUNE RESPONSE; INTERMEDIATE RISK PATIENT; LUNG CANCER; NON SMALL CELL LUNG CANCER; NOSE EPITHELIUM; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; RESPIRATORY EPITHELIUM; REVIEW; TRANSCRIPTOMICS; TUMOR DIFFERENTIATION; XENOBIOTIC METABOLISM; ADVERSE EVENT; CELL TRANSFORMATION; CLINICAL DECISION MAKING; DISEASE MANAGEMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; MOLECULAR DIAGNOSIS; PATHOLOGY; RESPIRATORY MUCOSA; RISK FACTOR; SMOKING;

BIOMARKERS, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CLINICAL DECISION-MAKING; DISEASE MANAGEMENT; EARLY DETECTION OF CANCER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MOLECULAR DIAGNOSTIC TECHNIQUES; RESPIRATORY MUCOSA; RISK FACTORS; SMOKING; TRANSCRIPTOME;

EID: 85049656099     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-16-3187     Document Type: Review

References (72)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin 2017;67:7-30.
2. Howlader N, Noone AM, Krapcho M, Miller D, Bishop K, Kosary CL, et al., editors. SEER cancer statistics review, 1975-2014 [PDF on the Internet]. Bethesda (MD): National Cancer Institute; 2017 [cited 2018 Jan 12]. Available from: Https://seer.cancer.gov/csr/1975-2014/.
3. Gould MK, Ananth L, Barnett PG. A clinical model to estimate the pretest probability of lung cancer in patients with solitary pulmonary nodules. Chest 2007;131:383-8.
4. Tammemagi CM, Pinsky PF, Caporaso NE, Kvale PA, Hocking WG, Church TR, et al. Lung cancer risk prediction: Prostate, Lung, Colorectal And Ovarian Cancer Screening Trial models and validation. J Natl Cancer Inst 2011;103:1058-68.
5. SpitzMR, Hong WK, Amos CI, Wu X, Schabath MB, Dong Q, et al. A risk model for prediction of lung cancer. J Natl Cancer Inst 2007;99: 715-26.
6. National Lung Screening Trial Research Team, Aberle DR, Adams AM, Berg CD, BlackWC, Clapp JD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365: 395-409.
7. Ettinger DS, Wood DE, Aisner DL, Akerley W, Bauman J, Chirieac LR, et al. Non-Small Cell Lung Cancer, Version 5.2017, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 2017;15:504-35.
8. Pinsky PF, Berg CD. Applying the National Lung Screening Trial eligibility criteria to the US population: what percent of the population and of incident lung cancers would be covered?. J Med Screen 2012;19:154-6.
9. Gould MK, Tang T, Liu I-LA, Lee J, Zheng C, Danforth KN, et al. Recent trends in the identification of incidental pulmonary nodules. Am J Respir Crit Care Med 2015;192:1208-14.
10. Barnett PG, Ananth L, Gould MK, Veterans Affairs Positron Emission Tomography Imaging in the Management of Patients with Solitary Pulmonary Nodules (VA SNAP) Cooperative Study Group. Cost and outcomes of patients with solitary pulmonary nodules managed with PET scans. Chest 2010;137:53-9.
11. Lokhandwala T, Bittoni MA, Dann RA, D'Souza AO, Johnson M, Nagy RJ, et al. Costs of diagnostic assessment for lung cancer: A medicare claims analysis. Clin Lung Cancer 2017;18:e27-34.
12. Kikuchi T, Hassanein M, Amann JM, Liu Q, Slebos RJC, Rahman SMJ, et al. In-depth proteomic analysis of nonsmall cell lung cancer to discover molecular targets and candidate biomarkers. Mol Cell Proteomics 2012; 11:916-32.
13. Ocak S, Chaurand P, Massion PP. Mass spectrometry-based proteomic profiling of lung cancer. Proc Am Thorac Soc 2009;6:159-70.
14. Pecot CV, Li M, Zhang XJ, Rajanbabu R, Calitri C, Bungum A, et al. Added value of a serum proteomic signature in the diagnostic evaluation of lung nodules. Cancer Epidemiol Biomark Prev 2012;21:786-92.
15. Hassanein M, Rahman JSM, Chaurand P, Massion PP. Advances in proteomic strategies toward the early detection of lung cancer. Proc Am Thorac Soc 2011;8:183-8.
16. Belinsky SA. Gene-promoter hypermethylation as a biomarker in lung cancer. Nat Rev Cancer 2004;4:707-17.
17. Lin H, Tong Z-H, Xu Q-Q, Wu X-Z, Wang X-J, Jin X-G, et al. Interplay of Th1 and Th17 cells in murine models of malignant pleural effusion. Am J Respir Crit Care Med 2014;189:697-706.
18. Su Y, Fang H, Jiang F. Integrating DNA methylation and microRNA biomarkers in sputum for lung cancer detection. Clin Epigenetics 2016;8:109.
19. Su Y, Guarnera MA, Fang H, Jiang F. Small non-coding RNA biomarkers in sputum for lung cancer diagnosis. Mol Cancer 2016;15:36.
20. Rauch TA, Wang Z, Wu X, Kernstine KH, Riggs AD, Pfeifer GP. DNA methylation biomarkers for lung cancer. Tumour Biol 2012;33: 287-96.
21. Chen X, Xu Y, Liao X, Liao R, Zhang L, Niu K, et al. Plasma miRNAs in predicting radiosensitivity in non-small cell lung cancer. Tumour Biol 2016;37:11927-36.
22. Mao L, Hruban RH, Boyle JO, Tockman M, Sidransky D. Detection of oncogene mutations in sputum precedes diagnosis of lung cancer. Cancer Res 1994;54:1634-7.
23. Belinsky SA, GrimesMJ, Casas E, Stidley CA, Franklin WA, Bocklage TJ, et al. Predicting gene promoter methylation in non-small-cell lung cancer by evaluating sputum and serum. Br J Cancer 2007;96:1278-83.
24. Zhang L, Xiao H, Zhou H, Santiago S, Lee JM, Garon EB, et al. Development of transcriptomic biomarker signature in human saliva to detect lung cancer. Cell Mol Life Sci 2012;69:3341-50.
25. Diamandis EP, Goodglick L, Planque C, Thornquist MD. Pentraxin-3 is a novel biomarker of lung carcinoma. Clin Cancer Res 2011;17: 2395-9.
26. Ajona D, Pajares MJ, Corrales L, Perez-Gracia JL, Agorreta J, Lozano MD, et al. Investigation of complement activation product c4d as a diagnostic and prognostic biomarker for lung cancer. J Natl Cancer Inst 2013;105: 1385-93.
27. Boeri M, Verri C, Conte D, Roz L, Modena P, Facchinetti F, et al. MicroRNA signatures in tissues and plasma predict development and prognosis of computed tomography detected lung cancer. Proc Natl Acad Sci U S A 2011;108:3713-8.
28. Rotunno M, Hu N, Su H, Wang C, Goldstein AM, Bergen AW, et al. A gene expression signature from peripheral whole blood for stage I lung adenocarcinoma. Cancer Prev Res (Phila) 2011;4:1599-608.
29. Montani F, Marzi MJ, Dezi F, Dama E, Carletti RM, Bonizzi G, et al. miRTest: A blood test for lung cancer early detection. J Natl Cancer Inst 2015;107:djv063.
30. Ilie M, Hofman V, Long-Mira E, Selva E, Vignaud J-M, Padovani B, et al. "Sentinel" circulating tumor cells allow early diagnosis of lung cancer in patients with chronic obstructive pulmonary disease. PLoS One 2014;9: E111597.
31. Steiling K, Ryan J, Brody JS, Spira A. The field of tissue injury in the lung and airway. Cancer Prev Res (Phila) 2008;1:396-403.
32. Lee J, Taneja V, Vassallo R. Cigarette smoking and inflammation. J Dent Res 2012;91:142-9.
33. HackettNR, Heguy A, Harvey B-G, O'Connor TP, Luettich K, FliederDB, et al. Variability of antioxidant-related gene expression in the airway epitheliumof cigarette smokers. Am J Respir Cell Mol Biol 2003;29:331-43.
34. Spira A, Beane J, Shah V, Liu G, Schembri F, Yang X, et al. Effects of cigarette smoke on the human airway epithelial cell transcriptome. Proc Natl Acad Sci U S A 2004;101:10143-8.
35. Beane J, Sebastiani P, Liu G, Brody JS, Lenburg ME, Spira A. Reversible and permanent effects of tobacco smoke exposure on airway epithelial gene expression. Genome Biol 2007;8:R201.
36. Chari R, Lonergan KM, Ng RT, MacAulay C, Lam WL, Lam S. Effect of active smoking on the human bronchial epithelium transcriptome. BMC Genomics 2007;8:297.
37. Wang X, Chorley BN, Pittman GS, Kleeberger SR, Brothers J, Liu G, et al. Genetic variation and antioxidant response gene expression in the bronchial airway epithelium of smokers at risk for lung cancer. PLoS One 2010;5:e11934.
38. Lochhead P, Chan AT, Nishihara R, Fuchs CS, Beck AH, Giovannucci E, et al. Etiologic field effect: Reappraisal of the field effect concept in cancer predisposition and progression. Mod Pathol 2015;28:14-29.
39. Blomquist T, Crawford EL, Mullins D, Yoon Y, Hernandez D-A, Khuder S, et al. Pattern of antioxidant and DNA repair gene expression in normal airway epithelium associated with lung cancer diagnosis. Cancer Res 2009;69:8629-35.
40. Crawford EL, Levin A, Safi F, LuM, Baugh A, Zhang X, et al. Lung cancer risk test trial: Study design, participant baseline characteristics, bronchoscopy safety, and establishment of a biospecimen repository. BMC Pulm Med 2016;16:16.
41. Slaughter DP, Southwick HW, Smejkal W. "Field cancerization" in oral stratified squamous epithelium. Clinical implications of multicentric origin. Cancer 1953;6:963-8.
42. Nelson HH, Christiani DC, Mark EJ, Wiencke JK, Wain JC, Kelsey KT. Implications and prognostic value of K-ras mutation for early-stage lung cancer in women. J Natl Cancer Inst 1999;91:2032-8.
43. Franklin WA, Gazdar AF, Haney J, Wistuba II, Rosa FGL, Kennedy T, et al. Widely dispersed p53 mutation in respiratory epithelium. A novel mechanism for field carcinogenesis. J Clin Invest 1997;100:2133.
44. Wistuba II, Lam S, Behrens C, Virmani AK, Fong KM, LeRiche J, et al. Molecular damage in the bronchial epithelium of current and former smokers. J Natl Cancer Inst 1997;89:1366-73.
45. Mao L, Lee JS, Kurie JM, Fan YH, Lippman SM, Lee JJ, et al. Clonal genetic alterations in the lungs of current and former smokers. J Natl Cancer Inst 1997;89:857-62.
46. Tang X, Shigematsu H, Bekele BN, Roth JA, Minna JD, Hong WK, et al. EGFR tyrosine kinase domain mutations are detected in histologically normal respiratory epithelium in lung cancer patients. Cancer Res 2005;65: 7568-72.
47. Gustafson AM, Soldi R, Anderlind C, Scholand MB, Qian J, Zhang X, et al. Airway PI3K pathway activation is an early and reversible event in lung cancer development. Sci Transl Med 2010;2:26ra25.
48. Kadara H, Shen L, Fujimoto J, Saintigny P, Chow C-W, Lang W, et al. Characterizing the molecular spatial and temporal field of injury in early-stage smoker non-small cell lung cancer patients after definitive surgery by expression profiling. Cancer Prev Res (Phila) 2013;6: 8-17.
49. Gomperts BN, Walser TC, Spira A, Dubinett SM. Enriching the molecular definition of the airway "Field of Cancerization:" establishing new paradigms for the patient at risk for lung cancer. Cancer Prev Res (Phila) 2013;6:4-7.
50. Kadara H, Fujimoto J, Yoo S-Y, Maki Y, Gower AC, Kabbout M, et al. Transcriptomic architecture of the adjacent airway field cancerization in non-small cell lung cancer. J Natl Cancer Inst 2014;106:dju004.
51. Detterbeck FC, Lewis SZ, Diekemper R, Addrizzo-Harris D, Alberts WM. Executive summary: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:7S-37S.
52. ten Haaf K, Jeon J, Tammem€agi MC, Han SS, Kong CY, Plevritis SK, et al. Risk prediction models for selection of lung cancer screening candidates: A retrospective validation study. PLoS Med 2017;14:e1002277.
53. Ost DE, Ernst A, Lei X, Kovitz KL, Benzaquen S, Diaz-Mendoza J, et al. Diagnostic yield and complications of bronchoscopy for peripheral lung lesions. Results of the AQuIRE Registry. Am J Respir Crit Care Med 2016; 193:68.
54. Spira A, Beane JE, Shah V, Steiling K, Liu G, Schembri F, et al. Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat Med 2007;13:361-6.
55. Beane J, Sebastiani P, Whitfield TH, Steiling K, Dumas Y-M, Lenburg ME, et al. A prediction model for lung cancer diagnosis that integrates genomic and clinical features. Cancer Prev Res (Phila) 2008;1:56-64.
56. Whitney DH, Elashoff MR, Porta-Smith K, Gower AC, Vachani A, Ferguson JS, et al. Derivation of a bronchial genomic classifier for lung cancer in a prospective study of patients undergoing diagnostic bronchoscopy. BMC Med Genomics 2015;8:18.
57. Silvestri GA, Vachani A, Whitney D, ElashoffM, Porta Smith K, Ferguson JS, et al. A bronchial genomic classifier for the diagnostic evaluation of lung cancer. N Engl J Med 2015;373:243-51.
58. Stahl DL, Richard KM, Papadimos TJ. Complications of bronchoscopy: A concise synopsis. Int J Crit Illn Inj Sci 2015;5:189-95.
59. Boskovic T, Stanic J, Pena-Karan S, Zarogoulidis P, Drevelegas K, Katsikogiannis N, et al. Pneumothorax after transthoracic needle biopsy of lung lesions under CT guidance. J Thorac Dis 2014;6:S99-107.
60. Vachani A, Whitney DH, Parsons EC, Lenburg M, Ferguson JS, Silvestri GA, et al. Clinical utility of a bronchial genomic classifier in patients with suspected lung cancer. Chest 2016;150:210-8.
61. Ferguson JS, Van Wert R, Choi Y, Rosenbluth MJ, Smith KP, Huang J, et al. Impact of a bronchial genomic classifier on clinical decision making in patients undergoing diagnostic evaluation for lung cancer. BMC PulmMed 2016;16:66.
62. Feller-Kopman D, Liu S, Geisler BP, DeCamp MM, Pietzsch JB. Costeffectiveness of a bronchial genomic classifier for the diagnostic evaluation of lung cancer. J Thorac Oncol 2017;12:1223-32.
63. Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: A new source of biomarkers. Mutat Res 2011;717:85-90.
64. Perdomo C, Campbell JD, Gerrein J, Tellez CS, Garrison CB, Walser TC, et al. MicroRNA 4423 is a primate-specific regulator of airway epithelial cell differentiation and lung carcinogenesis. Proc Natl Acad Sci U S A 2013; 110:18946-51.
65. Schembri F, Sridhar S, Perdomo C, Gustafson AM, Zhang X, Ergun A, et al. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc Natl Acad Sci U S A 2009;106:2319-24.
66. Pavel AB, Campbell JD, Liu G, Elashoff DA, Dubinett SM, Smith K, et al. Alterations in bronchial airway microRNA expression for lung cancer detection. Cancer Prev Res (Phila) 2017;10:651-9.
67. Zhang X, Sebastiani P, Liu G, Schembri F, Zhang X, Dumas YM, et al. Similarities and differences between smoking-related gene expression in nasal and bronchial epithelium. Physiol Genomics 2010;41:1-8.
68. AEGIS Study Team, Perez-Rogers JF, Gerrein J, Anderlind C, Liu G, Zhang S, et al. Shared gene expression alterations in nasal and bronchial epithelium for lung cancer detection. J Natl Cancer Inst 2017;109. doi: 10.1093/jnci/ djw327.
69. Sridhar S, Schembri F, Zeskind J, Shah V, Gustafson AM, Steiling K, et al. Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC Genomics 2008;9:259.
70. Wang TW, Vermeulen RCH, Hu W, Liu G, Xiao X, Alekseyev Y, et al. Geneexpression profiling of buccal epithelium among non-smoking women exposed to household air pollution from smoky coal. Carcinogenesis 2015;36:1494-501.
71. Mumford JL, He XZ, Chapman RS, Cao SR, Harris DB, Li XM, et al. Lung cancer and indoor air pollution in Xuan Wei, China. Science 1987;235: 217-20.
72. Beane J, Mazzilli SA, Tassinari AM, Liu G, Zhang X, Liu H, et al. Detecting the presence and progression of premalignant lung lesions via airway gene expression. Clin Cancer Res 2017;23:5091-100.