E-Cigarette Vapor Induces an Apoptotic Response in Human Gingival Epithelial Cells Through the Caspase-3 Pathway

Journal of Cellular Physiology

Volumn 232, Issue 6, 2017, Pages 1539-1547

  Rouabhia, Mahmoud ^a   Park, Hyun Jin ^a   Semlali, Abdelhabib ^b   Zakrzewski, Andrew ^a   Chmielewski, Witold ^a   Chakir, Jamila ^c  

^a UNIVERSITÉ LAVAL   (Canada)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 3 INHIBITOR; DNA; LACTATE DEHYDROGENASE; NICOTINE; CASPASE INHIBITOR;

ADULT; APOPTOSIS; ARTICLE; CELL ADHESION; CELL COUNT; CELL DEATH; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; DNA FRAGMENTATION; ELECTRONIC CIGARETTE; EPITHELIUM CELL; GINGIVA; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; MOUTH DISEASE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUNEL ASSAY; VAPING; VAPOR; ADOLESCENT; CELL CULTURE; CELL SHAPE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; NECROSIS; SIGNAL TRANSDUCTION; YOUNG ADULT;

ADOLESCENT; ADULT; APOPTOSIS; CASPASE 3; CASPASE INHIBITORS; CELL SHAPE; CELLS, CULTURED; DNA FRAGMENTATION; ELECTRONIC CIGARETTES; EPITHELIAL CELLS; GINGIVA; HUMANS; L-LACTATE DEHYDROGENASE; NECROSIS; SIGNAL TRANSDUCTION; YOUNG ADULT;

EID: 85006086289     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25677     Document Type: Article

References (50)

1. Alamri A, Semlali A, Jacques É, Alanazi M, Zakrzewski A, Chmielewski W, Rouabhia M. 2015. Long-term exposure of human gingival fibroblasts to cigarette smoke condensate reduces cell growth by modulating bax, caspase-3 and p53 expression. J Periodontal Res 50:423–433.
2. Alharbi IA, Rouabhia M. 2016. Repeated exposure to whole cigarette smoke promotes primary humangingival epithelial cell growth and modulates keratin expression. J Periodontal Res 51:630–638.
3. Arora M, Schwarz E, Sivaneswaran S, Banks E. 2010. Cigarette smoking and tooth loss in a cohort of older Australians: The 45 and up study. J Am Dent Assoc 141:1242–1249.
4. Avezov K, Reznick AZ, Aizenbud D. 2014. Oxidative damage in keratinocytes exposed to cigarette smoke and aldehydes. Toxicol In Vitro 28:485–491.
5. Bertholon JF, Becquemin MH, Annesi-Maesano I, Dautzenberg B. 2013. Electronic cigarettes: A short review. Respiration 86:433–438.
6. Brusselle GG, Joos GF, Bracke KR. 2011. New insights into the immunology of chronic obstructive pulmonary disease. Lancet 378:1015–1026.
7. Chan FK, Moriwaki K, De Rosa MJ. 2013. Detection of necrosis by release of lactate dehydrogenase activity. Methods Mol Biol 979:65–70.
8. Checa M, Hagood JS, Velazquez-Cruz R, Ruiz V, García-De-Alba C, Rangel-Escareño C, Urrea F, Becerril C, Montaño M, García-Trejo S, Cisneros Lira J, Aquino-Gálvez A, Pardo A, Selman M. 2016. Cigarette smoke enhances the expression of profibrotic molecules in alveolar epithelial cells. PLoS ONE 11:e0150383.
9. Chen Y, Hanaoka M, Chen P, Droma Y, Voelkel NF, Kudo K. 2009. Protective effect of beraprost sodium, a stable prostacyclin analog, in the development of cigarette smoke extract-induced emphysema. Am J Physiol Lung Cell Mol Physiol 296:L648–L656.
10. Cheng T. 2014. Chemical evaluation of electronic cigarettes. Tobacco Control 23:11–17.
11. Cooper M, Harrell MB, Perry CL. 2016. Comparing young adults to older adults in e-cigarette perceptions and motivations for use: Implications for health communication. Health Educ Res 31:429–438.
12. Dentener MA, Creutzberg EC, Wesseling G, Wouters EF. 2007. Systemic effects of smoking. Chest 131:1557–1566.
13. Drent M, Cobben NA, Henderson RF, Wouters EF, van Dieijen-Visser M. 1996. Usefulness of lactate dehydrogenase and its isoenzymes as indicators of lung damage or inflammation. Eur Respir J 9:1736–1742.
14. Farris SG, Zvolensky MJ, Schmidt NB. 2016. Difficulties with emotion regulation and psychopathology interact to predict early smoking cessation lapse. Cognit Ther Res 40:357–367.
15. Flusberg DA, Sorger PK. 2015. Surviving apoptosis: Life-death signaling in single cells. Trends Cell Biol 25:446–458.
16. Giannopoulou C, Geinoz A, Cimasoni G. 1999. Effects of nicotine on periodontal ligament fibroblasts in vitro. J Clin Periodontol 26:49–55.
17. Gillman IG, Kistler KA, Stewart EW, Paolantonio AR. 2016. Effect of variable power levels on the yield of total aerosol mass and formation of aldehydes in e-cigarette aerosols. Regul Toxicol Pharmacol 75:58–65.
18. Gleitz J, Tosch C, Peters T. 1996. Continuous enzyme-linked fluorometric detection of L-(+) lactate released from rat brain vesicles under anoxic conditions. J Neurosci Methods 67:97–102.
19. Goven D, Boutten A, Lecon-Malas V, Boczkowski J, Bonay M. 2009. Prolonged cigarette smoke exposure decreases heme oxygenase-1 and alters Nrf2 and Bach1 expression in human macrophages: Roles of the MAP kinases ERK(1/2) and JNK. FEBS Lett 583:3508–3518.
20. Grana R, Benowitz N, Glantz SA. 2014. E-cigarettes: A scientific review. Circulation 129:1972–1986.
21. Imamura K, Kokubu E, Kita D, Ota K, Ishihara K, Saito A. 2015. Cigarette smoke condensate modulates migration of human gingival epithelial cells and their interactions with Porphyromonas gingivalis. J Periodontal Res 50:411–421.
22. Jensen RP, Luo W, Pankow JF, Strongin RM, Peyton DH. 2015. Hidden formaldehyde in e-cigarette aerosols. NEJM 372:392–393.
23. Jogezai U, Maxood A, Khan NA. 2013. Comparison of periodontal health status of smokers versus non-smokers. J Ayub Med Coll Abbottabad 25:183–186.
24. Kosmider B, Messier EM, Chu HW, Mason RJ. 2011. Human alveolar epithelial cell injury induced by cigarette smoke. PLoS ONE 6:e26059.
25. Lerner CA, Rutagarama P, Ahmad T, Sundar IK, Elder A, Rahman I. 2016. Electronic cigarette aerosols and copper nanoparticles induce mitochondrial stress and promote DNA fragmentation in lung fibroblasts. Biochem Biophys Res Commun 477:620–625.
26. Lerner CA, Sundar IK, Yao H, Gerloff J, Ossip DJ, McIntosh S, Robinson R, Rahman I. 2015. Vapors produced by electronic cigarettes and E-Juices with flavorings induce toxicity, oxidative stress, and inflammatory response in lung epithelial cells and in mouse lung. PLoS ONE 10:e0116732.
27. Lerner L, Weiner D, Katz R, Reznick AZ, Pollack S. 2009. Increased pro-inflammatory activity and impairment of human monocyte differentiation induced by in vitro exposure to cigarette smoke. J Physiol Pharmacol 60:81–86.
28. Malas M, van der Tempel J, Schwartz R, Minichiello A, Lightfoot C, Noormohamed A, Andrews J, Zawertailo L, Ferrence R. 2016. Electronic cigarettes for smoking cessation: A systematic review. Nicotine Tob Res 18:1926–1936.
29. Manzoli L, Flacco ME, Ferrante M, La Vecchia C, Siliquini R, Ricciardi W, Marzuillo C, Villari P, Fiore M; ISLESE Working Group. 2016. Cohort study of electronic cigarette use: Effectiveness and safety at 24 months. Tob Control DOI: 10.1136/tobaccocontrol-2015-052822
30. Mikheev VB, Brinkman MC, Granville CA, Gordon SM, Clark PI. 2016. Real-time measurement of electronic cigarette aerosol size distribution and metals content analysis. Nicotine Tob Res 18:1895–1902.
31. Palmer RM, Scott DA, Meekin TN, Poston RN, Odell EW, Wilson RF. 1999. Potential mechanisms of susceptibility to periodontitis in tobacco smokers. J Periodontal Res 34:363–369.
32. Preber H, Bergström J. 1986. Cigarette smoking in patients referred for periodontal treatment. Scand J Dent Res 94:102–108.
33. Raulin LA, McPherson JC, McQuade MJ, Hanson BS. 1988. The effect of nicotine on the attachment of human fibroblasts to glass and human root surfaces in vitro. J Periodontol 59:318–325.
34. Rodu B. 2011. The scientific foundation for tobacco harm reduction, 2006–2011. Harm Reduct J DOI: 10.1186/1477-7517-8-19
35. Roys M, Weed K, Carrigan M, MacKillop J. 2016. Associations between nicotine dependence, anhedonia, urgency and smoking motives. Addict Behav 62:145–151.
36. Ryder MI, Fujitaki R, Lebus S, Mahboub M, Faia B, Muhaimin D, Hamada M, Hyun W. 1998. Alterations of neutrophil L-selectin and CD18 expression by tobacco smoke: Implications for periodontal diseases. J Periodontal Res 33:359–368.
37. Schlage WK, Iskandar AR, Kostadinova R, Xiang Y, Sewer A, Majeed S, Kuehn D, Frentzel S, Talikka M, Geertz M, Mathis C, Ivanov N, Hoeng J, Peitsch MC. 2014. In vitro systems toxicology approach to investigate the effects of repeated cigarette smoke exposure on human buccal and gingival organotypic epithelial tissue cultures. Toxicol Mech Methods 24:470–487.
38. Schober W, Szendei K, Matzen W, Osiander-Fuchs H, Heitmann D, Schettgen T, Jörres RA, Fromme H. 2014. Use of electronic cigarettes (e-cigarettes) impairs indoor air quality and increases FeNO levels of e-cigarette consumers. Int J Hyg Environ Health 217:628–637.
39. Semlali A, Witoled C, Alanazi M, Rouabhia M. 2012. Whole cigarette smoke increased the expression of TLRs, HBDs, and proinflammory cytokines by human gingival epithelial cells through different signaling pathways. PLoS ONE 7:e52614.
40. Semlali A, Chakir J, Rouabhia M. 2011. Effects of whole cigarette smoke on human gingival fibroblast adhesion, growth, and migration. J Toxicol Environ Health A 74:848–862.
41. Stämpfli MR, Anderson GP. 2009. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9:377–384.
42. Stankovic Stojanovic K, Lionnet F. 2016. Lactate dehydrogenase in sickle cell disease. Clin Chim Acta 458:99–102.
43. Suzanne M, Steller H. 2013. Shaping organisms with apoptosis. Cell Death Differ 20:669–675.
44. Talhout R, Schulz T, Florek E, van Benthem J, Wester P, Opperhuizen A. 2011. Hazardous compounds in tobacco smoke. Int J Environ Res Public Health 8:613–628.
45. Tanni SE, Correa CR, Angeleli AY, Vale SA, Coelho LS, Godoy I. 2012. Increased production of hydrogen peroxide by peripheral blood monocytes associated with smoking exposure intensity in smokers. J Inflamm (Lond) 9:45.
46. Teughels W, Van Eldere J, van Steenberghe D, Cassiman JJ, Fives-Taylor P, Quirynen M. 2005. Influence of nicotine and cotinine on epithelial colonization by periodontopathogens. J Periodontol 76:1315–1322.
47. Uchiyama S, Senoo Y, Hayashida H, Inaba Y, Nakagome H, Kunugita N. 2016. Determination of chemical compounds generated from second-generation E-cigarettes using a sorbent cartridge followed by a two-step elution method. Anal Sci 32:549–555.
48. Vogtmann E, Graubard B, Loftfield E, Chaturvedi A, Dye BA, Abnet CC, Freedman ND. 2016. Contemporary impact of tobacco use on periodontal disease in the USA. Tob Control DOI: 10.1136/tobaccocontrol-2015-052750
49. Williams M, Villarreal A, Bozhilov K, Lin S, Talbot P. 2013. Metal and silicate particles including nanoparticles are present in electronic cigarette cartomizer fluid and aerosol. PLoS ONE 8:e57987.
50. World Health Organization Framework Convention on Tobacco Control. 2013. http://www.who.int/fctc/en/ (accessed 26 November, 2013).