Deregulation of biologically significant genes and associated molecular pathways in the oral epithelium of electronic cigarette users

International Journal of Molecular Sciences

Volumn 20, Issue 3, 2019, Pages

  Tommasi, Stella ^a   Caliri, Andrew W ^a   Caceres, Amanda ^a   Moreno, Debra E ^a   Li, Meng ^b   Chen, Yibu ^b   Siegmund, Kimberly D ^a   Besaratinia, Ahmad ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Carcinogenesis; Gene regulation; RNA seq; Transcription; Vaping

Indexed keywords

CARBON MONOXIDE; CARBOXYHEMOGLOBIN; COMPLEMENTARY DNA; COTININE; SMALL NUCLEOLAR RNA; TRANSCRIPTOME; UNTRANSLATED RNA;

ADULT; ARTICLE; BLOOD; CARCINOGENESIS; CIGARETTE SMOKING; CONTROLLED STUDY; DEREGULATION; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ETHNICITY; FEMALE; GENE CONTROL; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOME; HUMAN; MALE; MOUTH EPITHELIUM; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; VAPING; WNT SIGNALING; BIOLOGY; ELECTRONIC CIGARETTE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; MOUTH MUCOSA; PROCEDURES; REPRODUCIBILITY; SMOKING;

COMPUTATIONAL BIOLOGY; ELECTRONIC NICOTINE DELIVERY SYSTEMS; FEMALE; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENE REGULATORY NETWORKS; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MOUTH MUCOSA; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; SMOKING;

EID: 85061386050     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms20030738     Document Type: Article

References (50)

1. National Academies of Sciences, Engineering, and Medicine. Public Health Consequences of e-cigarettes; National Academies Press: Washington, DC, USA, 2018.
2. Besaratinia, A.; Tommasi, S. Electronic cigarettes: The road ahead. Prev. Med. 2014, 66, 65-67.
3. Besaratinia, A.; Tommasi, S. An opportune and unique research to evaluate the public health impact of electronic cigarettes. Cancer Causes Control 2017, 28, 1167-1171.
4. Schoenborn, C.A.; Gindi, R.M. Electronic Cigarette Use Among Adults: United States; Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics: Atlanta, GA, USA, 2014; pp. 1-8.
5. Singh, T.; Arrazola, R.A.; Corey, C.G.; Husten, C.G.; Neff, L.J.; Homa, D.M.; King, B.A. Tobacco Use Among Middle and High School Students—United States, 2011-2015. MMWR Morb. Mortal. Wkly. Rep. 2016, 65, 361-367.
6. Centers for Disease Control and Prevention. Tobacco Use Among Middle and High School Students—United States, 2011-2016. MMWR Morb. Mortal. Wkly. Rep. 2017, 66, 597-603.
7. Shiffman, S.; Sembower, M.A.; Pillitteri, J.L.; Gerlach, K.K.; Gitchell, J.G. The impact of flavor descriptors on nonsmoking teens’ and adult smokers’ interest in electronic cigarettes. Nicotine Tob. Res. 2015, 17, 1255-1262.
8. Coleman, B.N.; Apelberg, B.J.; Ambrose, B.K.; Green, K.M.; Choiniere, C.J.; Bunnell, R.; King, B.A. Association Between Electronic Cigarette Use and Openness to Cigarette Smoking Among US Young Adults. Nicotine Tob. Res. 2015, 17, 212-218.
9. Schick, S.F.; Blount, B.C.; Jacob, P.R.; Saliba, N.A.; Bernert, J.T.; El Hellani, A.; Jatlow, P.; Pappas, R.S.; Wang, L.; Foulds, J. et al. Biomarkers of exposure to new and emerging tobacco delivery products. Am. J. Physiol. Lung Cell. Mol. Physiol. 2017, 313, L425-L452.
10. Timp, W.; Feinberg, A.P. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat. Rev. Cancer 2013, 13, 497-510.
11. Liu, F.; Wang, L.; Perna, F.; Nimer, S.D. Beyond transcription factors: How oncogenic signalling reshapes the epigenetic landscape. Nat. Rev. Cancer 2016, 16, 359-372.
12. Brody, J.S.; Steiling, K. Interaction of cigarette exposure and airway epithelial cell gene expression. Annu. Rev. Physiol. 2011, 73, 437-456.
13. Brothers, J.F.; Hijazi, K.; Mascaux, C.; El-Zein, R.A.; Spitz, M.R.; Spira, A. Bridging the clinical gaps: Genetic, epigenetic and transcriptomic biomarkers for the early detection of lung cancer in the post-National Lung Screening Trial era. BMC Med. 2013, 11, 168.
14. Sridhar, S.; Schembri, F.; Zeskind, J.; Shah, V.; Gustafson, A.M.; Steiling, K.; Liu, G.; Dumas, Y.M.; Zhang, X.; Brody, J.S. et al. Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC Genom. 2008, 9, 259.
15. Kupfer, D.M.; White, V.L.; Jenkins, M.C.; Burian, D. Examining smoking-induced differential gene expression changes in buccal mucosa. BMC Med. Genom. 2010, 3, 24.
16. Silverman, S. Oral Cancer, 5th ed.; BC Decker, Inc.: Hamilton, ON, Canada, 2003.
17. Proia, N.K.; Paszkiewicz, G.M.; Nasca, M.A.; Franke, G.E.; Pauly, J.L. Smoking and smokeless tobacco-associated human buccal cell mutations and their association with oral cancer—A review. Cancer Epidemiol. Biomark. Prev. 2006, 15, 1061-1077.
18. Van Schooten, F.J.; Besaratinia, A.; de Flora, S.; D’Agostini, F.; Izzotti, A.; Camoirano, A.; Balm, A.J.; Dallinga, J.W.; Bast, A.; Haenen, G.R. et al. Effects of oral administration of N-acetyl-L-cysteine: A multi-biomarker study in smokers. Cancer Epidemiol. Biomark. Prev. 2002, 11, 167-175.
19. Cancer Genome Atlas Research Network. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 2015, 517, 576-582.
20. Sakamoto, K. Notch signaling in oral squamous neoplasia. Pathol. Int. 2016, 66, 609-617.
21. Sanchez-Tena, S.; Cubillos-Rojas, M.; Schneider, T.; Rosa, J.L. Functional and pathological relevance of HERC family proteins: A decade later. Cell. Mol. Life Sci. 2016, 73, 1955-1968.
22. Benowitz, N.L.; Hukkanen, J.; Jacob, P. Nicotine Chemistry, Metabolism, Kinetics and Biomarkers, 3rd ed.; Handbook of Experimental Pharmacology; Springer: Berlin/Heidelberg, Germany, 2009; pp. 29-60.
23. Emery, R.L.; Levine, M.D. Optimal Carbon Monoxide Criteria to Confirm Smoking Status Among Postpartum Women. Nicotine Tob. Res. 2016, 18, 966-970.
24. Ripoll, J.; Girauta, H.; Ramos, M.; Medina-Bombardo, D.; Pastor, A.; Alvarez-Ossorio, C.; Gorreto, L.; Esteva, M.; Garcia, E.; Urendez, A. et al. Clinical trial on the efficacy of exhaled carbon monoxide measurement in smoking cessation in primary health care. BMC Public Health 2012, 12, 322.
25. Blumenthal, I. Carbon monoxide poisoning. J. R. Soc. Med. 2001, 94, 270-272.
26. Cairns, J. Mutation selection and the natural history of cancer. Nature 1975, 255, 197-200.
27. Holland, N.; Bolognesi, C.; Kirsch-Volders, M.; Bonassi, S.; Zeiger, E.; Knasmueller, S.; Fenech, M. The micronucleus assay in human buccal cells as a tool for biomonitoring DNA damage: The HUMN project perspective on current status and knowledge gaps. Mutat. Res. 2008, 659, 93-108.
28. Fenech, M.; Holland, N.; Zeiger, E.; Chang, W.P.; Burgaz, S.; Thomas, P.; Bolognesi, C.; Knasmueller, S.; Kirsch-Volders, M.; Bonassi, S. The HUMN and HUMNxL international collaboration projects on human micronucleus assays in lymphocytes and buccal cells—Past, present and future. Mutagenesis 2011, 26, 239-245.
29. Autrup, H.; Seremet, T.; Arenholt, D.; Dragsted, L.; Jepsen, A. Metabolism of benzo[a]pyrene by cultured rat and human buccal mucosa cells. Carcinogenesis 1985, 6, 1761-1765.
30. Spivack, S.D.; Hurteau, G.J.; Jain, R.; Kumar, S.V.; Aldous, K.M.; Gierthy, J.F.; Kaminsky, L.S. Gene-environment interaction signatures by quantitative mRNA profiling in exfoliated buccal mucosal cells. Cancer Res. 2004, 64, 6805-6813.
31. Zhang, Y.; Chen, S.Y.; Hsu, T.; Santella, R.M. Immunohistochemical detection of malondialdehyde-DNA adducts in human oral mucosa cells. Carcinogenesis 2002, 23, 207-211.
32. Schwartz, J.L.; Muscat, J.E.; Baker, V.; Larios, E.; Stephenson, G.D.; Guo, W.; Xie, T.; Gu, X.; Chung, F.L. Oral cytology assessment by flow cytometry of DNA adducts, aneuploidy, proliferation and apoptosis shows differences between smokers and non-smokers. Oral Oncol. 2003, 39, 842-854.
33. Shani, T.; Onn, A.; Kabha, A.; Ben-Dov, I.; Adam, I.; Amariglio, N.; Yahalom, R.; Rechavi, G.; Trakhtenbrot, L.; Hirshberg, A. Chromosomal numerical aberrations in apparently normal oral mucosa of heavy smokers affected by lung cancer. Oral Oncol. 2010, 46, 96-99.
34. Bonassi, S.; Coskun, E.; Ceppi, M.; Lando, C.; Bolognesi, C.; Burgaz, S.; Holland, N.; Kirsh-Volders, M.; Knasmueller, S.; Zeiger, E. et al. The HUman MicroNucleus project on eXfoLiated buccal cells (HUMN(XL)): The role of life-style, host factors, occupational exposures, health status, and assay protocol. Mutat. Res. 2011, 728, 88-97.
35. Shah, V.; Sridhar, S.; Beane, J.; Brody, J.S.; Spira, A. SIEGE: Smoking Induced Epithelial Gene Expression Database. Nucleic Acids Res. 2005, 33, D573-D579.
36. Boyle, J.O.; Gumus, Z.H.; Kacker, A.; Choksi, V.L.; Bocker, J.M.; Zhou, X.K.; Yantiss, R.K.; Hughes, D.B.; Du, B.; Judson, B.L. Effects of cigarette smoke on the human oral mucosal transcriptome. Cancer Prev. Res. 2010, 3, 266-278.
37. Garcia-Closas, M.; Egan, K.M.; Abruzzo, J.; Newcomb, P.A.; Titus-Ernstoff, L.; Franklin, T.; Bender, P.K.; Beck, J.C.; Le Marchand, L.; Lum, A. et al. Collection of genomic DNA from adults in epidemiological studies by buccal cytobrush and mouthwash. Cancer Epidemiol. Biomark. Prev. 2001, 10, 687-696.
38. Huang, B.; Zhang, R. Regulatory non-coding RNAs: Revolutionizing the RNA world. Mol. Biol. Rep. 2014, 41, 3915-3923.
39. Maute, R.L.; Dalla-Favera, R.; Basso, K. RNAs with multiple personalities. Wiley Interdiscip. Rev. RNA 2014, 5, 1-13.
40. Song, W.; Sun, Y.; Lin, J.; Bi, X. Current research on head and neck cancer-associated long noncoding RNAs. Oncotarget 2018, 9, 1403-1425.
41. Zou, A.E.; Ku, J.; Honda, T.K.; Yu, V.; Kuo, S.Z.; Zheng, H.; Xuan, Y.; Saad, M.A.; Hinton, A.; Brumund, K.T. et al. Transcriptome sequencing uncovers novel long noncoding and small nucleolar RNAs dysregulated in head and neck squamous cell carcinoma. RNA 2015, 21, 1122-1134.
42. Leemans, C.R.; Snijders, P.J.F.; Brakenhoff, R.H. The molecular landscape of head and neck cancer. Nat. Rev. Cancer 2018, 18, 269-282.
43. De, A. Wnt/Ca2+ signaling pathway: A brief overview. Acta Biochim. Biophys. Sin. 2011, 43, 745-756.
44. Guo, W.; Giancotti, F.G. Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 2004, 5, 816-826.
45. Fritz, G.; Henninger, C. Rho GTPases: Novel Players in the Regulation of the DNA Damage Response? Biomolecules 2015, 5, 2417-2434.
46. Stransky, N.; Egloff, A.M.; Tward, A.D.; Kostic, A.D.; Cibulskis, K.; Sivachenko, A.; Kryukov, G.V.; Lawrence, M.S.; Sougnez, C.; McKenna, A. et al. The mutational landscape of head and neck squamous cell carcinoma. Science 2011, 333, 1157-1160.
47. Sturner, E.; Behl, C. The Role of the Multifunctional BAG3 Protein in Cellular Protein Quality Control and in Disease. Front. Mol. Neurosci. 2017, 10, 177.
48. Eto, M. Regulation of cellular protein phosphatase-1 (PP1) by phosphorylation of the CPI-17 family, C-kinase-activated PP1 inhibitors. J. Biol. Chem. 2009, 284, 35273-35277.
49. Huang da, W.; Sherman, B.T.; Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4, 44-57.
50. Tommasi, S.; Zheng, A.; Weninger, A.; Bates, S.E.; Li, X.A.; Wu, X.; Hollstein, M.; Besaratinia, A. Mammalian cells acquire epigenetic hallmarks of human cancer during immortalization. Nucleic Acids Res. 2013, 41, 182-195.