Transcriptome sequencing reveals e-cigarette vapor and mainstream-smoke from tobacco cigarettes activate different gene expression profiles in human bronchial epithelial cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Shen, Yifei ^a   Wolkowicz, Michael J ^b   Kotova, Tatyana ^b   Fan, Lonjiang ^a   Timko, Michael P ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEROSOL; SMOKE;

ADVERSE EFFECTS; AEROSOL; ANALYSIS; BRONCHUS; CYTOLOGY; DRUG EFFECTS; ELECTRONIC CIGARETTE; EPITHELIUM CELL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; HUMAN; PROCEDURES; SEQUENCE ANALYSIS; SMOKE; TOBACCO;

AEROSOLS; BRONCHI; ELECTRONIC CIGARETTES; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; SEQUENCE ANALYSIS, RNA; SMOKE; TOBACCO;

EID: 84962373610     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23984     Document Type: Article

References (79)

1. Wistuba, I. I. et al. Molecular damage in the bronchial epithelium of current and former smokers. J Natl Cancer Inst. 89, 1366-1373 (1997).
2. Shields, P. Molecular epidemiology of lung cancer. Ann Oncol 10, S7-S11 (1999).
3. Mathers, C. D. & Loncar, D. Projections of global mortality and burden of disease from 2002 to 2030. Plos Med. 3, e442 (2006).
4. World Health Organization. WHO report on the global tobacco epidemic, 2011: Warning about the dangers of tobacco. WHO Document Production Services, Geneva, Switzerland, (2011) URL: http://www.who.int/tobacco/global-report/2011/en/. Date of access: 06/07/2015.
5. Ezzati, M. & Lopez, A. D. Estimates of global mortality attributable to smoking in 2000. The Lancet 362, 847-852 (2003).
6. Jemal, A. et al. Cancer statistics, 2009. CA-Cancer J Clin 59, 225-249 (2009).
7. Wynder, E. L. & Muscat, J. E. The changing epidemiology of smoking and lung cancer histology. Environ Health Persp 103, 143 (1995).
8. Mathis, C. et al. Human bronchial epithelial cells exposed in vitro to cigarette smoke at the air-liquid interface resemble bronchial epithelium from human smokers. Am J Physiol-Lung C 304, L489-L503 (2013).
9. Vineis, P. et al. Tobacco and cancer: recent epidemiological evidence. J Natl Cancer I 96, 99-106 (2004).
10. Zhang, X. et al. Similarities and differences between smoking-related gene expression in nasal and bronchial epithelium. Physiol Genomics 41, 1-8 (2010).
11. Hoffmann, D. & Wynder, E. Chemical constituents and bioactivity of tobacco smoke. IARC scientific publications 74, 145-165 (1985).
12. Hoffmann, D. H. Ilse. The changing cigarette, 1950-1995. J Toxicol Env Heal A 50, 307-364 (1997).
13. Rodgman, A. & Perfetti, T. A. The chemical components of tobacco and tobacco smoke, Second Edition. 2332 pages. ISBN 9781466515482 CRC Press, Boca Raton, FL, USA (2013)
14. Bullen, C. et al. Effect of an electronic nicotine delivery device (e cigarette) on desire to smoke and withdrawal, user preferences and nicotine delivery: randomised cross-over trial. Tob Control 19, 98-103 (2010).
15. Benowitz, N. L. Nicotine addiction. New Engl J Med 362, 2295 (2010).
16. Waxman, D. J. & Holloway, M. G. Sex differences in the expression of hepatic drug metabolizing enzymes. Mol Pharmacol 76, 215-228 (2009).
17. Food & Drug Administration. Deeming Tobacco Products To Be Subject to the Federal Food, Drug, and Cosmetic Act, as Amended by the Family Smoking Prevention and Tobacco Control Act; Regulations on the Sale and Distribution of Tobacco Products and Required Warning Statements for Tobacco Products. Fed Regist 79, 23142-23207 (2014).
18. Food and Drug Administration. Harmful and potentially harmful constituents in tobacco products and tobacco smoke; established list. Fed Regist 77, 20034-20037 (2012).
19. IOM (Institute of Medicine). Scientific Standards for Studies on Modified Risk Tobacco Products. Washington, D.C., National Academies Press, ISBN 13: 978-0-309-22398-0 (2012).
20. Trtchounian, A., Williams, M. & Talbot, P. Conventional and electronic cigarettes (e-cigarettes) have different smoking characteristics. Nicotine Tob Res 12, 905-912 (2010).
21. Gartner, C. & Hall, W. Harm reduction policies for tobacco users. Int J Drug Policy 21, 129-130 (2010).
22. Henningfield, J. & Zaatari, G. Electronic nicotine delivery systems: emerging science foundation for policy. Tob Control 19, 89-90 (2010).
23. Yamin, C. K., Bitton, A. & Bates, D. W. E-cigarettes: a rapidly growing Internet phenomenon. Ann Intern Med 153, 607-609 (2010).
24. Cahn, Z. & Siegel, M. Electronic cigarettes as a harm reduction strategy for tobacco control: A step forward or a repeat of past mistakes&quest. J Public Health Pol 32, 16-31 (2011).
25. Brody, J. S. & Steiling, K. Interaction of cigarette exposure and airway epithelial cell gene expression. Annu Rev Physiol 73, 437-456 (2011).
26. Nyunoya, T. et al. Molecular Processes that Drive Cigarette Smoke-Induced Epithelial Cell Fate of the Lung. Am J Resp Cell Mol. 50, 471-482 (2014).
27. Spira, A. et al. Effects of cigarette smoke on the human airway epithelial cell transcriptome. P Natl Acad Sci USA 101, 10143-10148 (2004).
28. Spira, A. et al. Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat Med. 13, 361-366 (2007).
29. Hackett, N. R. et al. Variability of antioxidant-related gene expression in the airway epithelium of cigarette smokers. Am J Resp Cell Mol. 29, 331-343 (2003).
30. Harvey, B.-G. et al. Modification of gene expression of the small airway epithelium in response to cigarette smoking. J Mol Med. 85, 39-53 (2007).
31. Beane, J. et al. Reversible and permanent effects of tobacco smoke exposure on airway epithelial gene expression. Genome Biol. 8, R201 (2007).
32. Schembri, F. et al. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. P Natl Acad Sci USA 106, 2319-2324 (2009).
33. Chari, R. et al. Effect of active smoking on the human bronchial epithelium transcriptome. BMC genomics 8, 297 (2007).
34. Lu, A. H., Salabas, E. e. L. & Schuth, F. Magnetic nanoparticles: synthesis, protection, functionalization, and application. Angew Chem Int Edit 46, 1222-1244 (2007).
35. Maunders, H., Patwardhan, S., Phillips, J., Clack, A. & Richter, A. Human bronchial epithelial cell transcriptome: gene expression changes following acute exposure to whole cigarette smoke in vitro. Am J of Physiol-Lung C 292, L1248-L1256 (2007).
36. Parsanejad, R., Fields, W. R., Morgan, W. T., Bombick, B. R. & Doolittle, D. J. The time course of expression of genes involved in specific pathways in normal human bronchial epithelial cells following exposure to cigarette smoke. Exp Lung Res 34, 513-530 (2008).
37. Pickett, G. et al. Effects of 10 cigarette smoke condensates on primary human airway epithelial cells by comparative gene and cytokine expression studies. Toxicol Sci, doi: 10.1093 (2009).
38. Sexton, K., Balharry, D. & BeruBe, K. A. Genomic biomarkers of pulmonary exposure to tobacco smoke components. Pharmacogenet Genom 18, 853-860 (2008).
39. Zhang, L. et al. Impact of smoking cessation on global gene expression in the bronchial epithelium of chronic smokers. Cancer Prev Res 1, 112-118 (2008).
40. Crawford, E. L. et al. Normal bronchial epithelial cell expression of glutathione transferase P1, glutathione transferase M3, and glutathione peroxidase is low in subjects with bronchogenic carcinoma. Cancer Res 60, 1609-1618 (2000).
41. Ammous, Z. et al. Variability in small airway epithelial gene expression among normal smokers. CHEST Journal 133, 1344-1353 (2008).
42. Jorgensen, E. D., Dozmorov, I., Frank, M. B., Centola, M. & Albino, A. P. Global gene expression analysis of human bronchial epithelial cells treated with tobacco condensates. Cell Cycle 3, 1152-1166 (2004).
43. Cressey, D. E-cigarettes affect cells. Nature 508, 159-159 (2014).
44. Wieslander, G., Norback, D. & Lindgren, T. Experimental exposure to propylene glycol mist in aviation emergency training: acute ocular and respiratory effects. Occup Environ Med 58, 649-655 (2001).
45. Wu, Q., Jiang, D., Minor, M. & Chu, H. W. Electronic cigarette liquid increases inflammation and virus infection in primary human airway epithelial cells. Plos one 9(9), e108342, doi: 10.1371/journal.pone.0108342 (2014).
46. Kogel, U. et al. Biological impact of cigarette smoke compared to an aerosol produced from a prototypic modified risk tobacco product on normal human bronchial epithelial cells. Toxicol in Vitro 29, 2102-2115 (2015).
47. Andrews, S. Fastqc: A Quality Control Tool For High Throughput Sequence Data. URL http://www.Bioinformaticsbabraham.ac.uk/ projects/fastqc. (2010) Date of access: 10/01/2015
48. Joshi, N. A. & Fass, J. N. (2011). Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (Version 1.21). URL https://github.com/najoshi/sickle.
49. Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7, 562-578 (2012).
50. Eisenberg, E. & Levanon, E. Y. Human housekeeping genes are compact. Trends Genet 19, 362-365 (2003).
51. Guo, L. et al. WNT/β-catenin signaling regulates cigarette smoke-induced airway inflammation via the PPARd /p38 pathway. Lab Invest, doi: 10.1038/labinvest.2015.101 (2015)
52. Heijink, I. H. et al. Role of aberrant WNT signalling in the airway epithelial response to cigarette smoke in chronic obstructive pulmonary disease. Thorax 68, 709-716 (2013).
53. Mossman, B. T., Lounsbury, K. M. & Reddy, S. P. Oxidants and signaling by mitogen-activated protein kinases in lung epithelium. Am J Resp Cell Mol. 34, 666-669 (2006).
54. Phillips, J., Kluss, B., Richter, A. & Massey, E. Exposure of bronchial epithelial cells to whole cigarette smoke: assessment of cellular responses. Altern Lab Anim 33, 239-248 (2005).
55. Brogan, A. P., Dickerson, T. J., Boldt, G. E. & Janda, K. D. Altered retinoid homeostasis catalyzed by a nicotine metabolite: implications in macular degeneration and normal development. P Natl Acad Sci USA 102, 10433-10438 (2005).
56. Lang, U. E., Gallinat, J., Kuhn, S., Jockers-Scherubl, M. & Hellweg, R. Nerve growth factor and smoking cessation. Am J Psychiat 159, 674-675 (2002).
57. Wongtrakool, C. et al. Nicotine Stimulates Nerve Growth Factor in Lung Fibroblasts through an NFκ B-Dependent Mechanism. Plos one 9(10), e109602, doi: 10.1371/journal.pone.0109602 (2014).
58. Unwalla, H. J., Ivonnet, P., Dennis, J. S., Conner, G. E. & Salathe, M. Transforming Growth Factor-β 1 and Cigarette Smoke Inhibit the Ability of β 2-Agonists to Enhance Epithelial Permeability. Am J Resp Cell Mol 52, 65-74 (2015).
59. Yoshida, T. & Tuder, R. M. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev 87, 1047-1082 (2007).
60. Robays, L., Maes, T., Joos, G. & Vermaelen, K. Between a cough and a wheeze: dendritic cells at the nexus of tobacco smoke-induced allergic airway sensitization. Mucosal Immunol 2, 206-219 (2009).
61. Gangl, K. et al. Cigarette smoke facilitates allergen penetration across respiratory epithelium. Allergy 64, 398-405 (2009).
62. Yao, H. et al. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol-Lung C 294, L1174-L1186 (2008).
63. Boyle, J. O. et al. Effects of cigarette smoke on the human oral mucosal transcriptome. Cancer Prev Res 3, 266-278 (2010).
64. Misra, M., Leverette, R. D., Cooper, B. T., Bennett, M. B. & Brown, S. E. Comparative in vitro toxicity profile of electronic and tobacco cigarettes, smokeless tobacco and nicotine replacement therapy products: e-liquids, extracts and collected aerosols. Inter J Env Res Pub Heal 11, 11325-11347 (2014).
65. Spivack, S. D. et al. Gene-environment interaction signatures by quantitative mRNA.
66. profiling in exfoliated buccal mucosal cells. Cancer Res 64, 6805-6813 (2004).
67. Jain, R., Varma, S., Hurteau, G. & Spivack, S. D. Buccal-lung comparison of quantitative expression of carcinogen and oxidant metabolism genes in human subjects. CHEST Journal 125, 107S-108S (2004).
68. Sridhar, S. et al. Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC genomics 9, 259 (2008).
69. Cavarra, E. et al. Early response of gene clusters is associated with mouse lung resistance or sensitivity to cigarette smoke. Am J Physiol-Lung C 296, L418-L429 (2009).
70. Beane, J. et al. Characterizing the impact of smoking and lung cancer on the airway transcriptome using RNA-Seq. Cancer Prev Res 4, 803-817 (2011).
71. Hackett, N. R. et al. RNA-Seq quantification of the human small airway epithelium transcriptome. BMC genomics 13, 82 (2012).
72. Beane, J. et al. A prediction model for lung cancer diagnosis that integrates genomic and clinical features. Cancer Prev Res 1, 56-64 (2008).
73. Mascaux, C. et al. Evolution of microRNA expression during human bronchial squamous carcinogenesis. Eur Respir J 33, 352-359 (2009).
74. Gray, T. E., Guzman, K., Davis, C. W., Abdullah, L. H. & Nettesheim, P. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Resp Cell Mol 14, 104-112 (1996).
75. Zhang, H.-B., Bokowiec, M. T., Rushton, P. J., Han, S.-C. & Timko, M. P. Tobacco transcription factors NtMYC2a and NtMYC2b form nuclear complexes with the NtJAZ1 repressor and regulate multiple jasmonate-inducible steps in nicotine biosynthesis. Mol Plant 5, 73-84 (2012).
76. Huang, D. W. et al. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57 (2009).
77. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. P Natl Acad Sci USA 102, 15545-15550 (2005).
78. Croft, D. et al. Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res 39, D691-697 (2011).
79. Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13, 2498-2504 (2003).