E-cigarette use causes a unique innate immune response in the lung, involving increased neutrophilic activation and altered mucin secretion

American Journal of Respiratory and Critical Care Medicine

Volumn 197, Issue 4, 2018, Pages 492-501

  Reidel, Boris ^a   Radicioni, Giorgia ^a   Clapp, Phillip W ^a   Ford, Amina A ^a   Abdelwahab, Sabri ^a   Rebuli, Meghan E ^a   Haridass, Prashamsha ^a   Alexis, Neil E ^a   Jaspers, Ilona ^a   Kesimer, Mehmet ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

E cigarette; Lung; Mucin; NET; Neutrophil

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 3A1; ANTITHROMBIN III; AZUROCIDIN; AZUROCIDIN 1; BETA MICROSEMINOPROTEIN; CIGARETTE SMOKE; COTININE; ELASTASE; GELATINASE B; GLUTATHIONE TRANSFERASE; LACTOFERRIN; LYSOZYME; LYSOZYME C; MUCIN 5AC; MUCIN 5B; MYELOBLASTIN; MYELOPEROXIDASE; NEUTROPHIL COLLAGENASE; NUCLEOBINDIN 1; PROTEIN; PROTEIN ARGININE DEIMINASE 4; PROTEOME; THIOREDOXIN; TREFOIL FACTOR 3; UNCLASSIFIED DRUG; MUCIN;

ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIGARETTE SMOKING; CONTROLLED STUDY; ELECTRONIC CIGARETTE; EXTRACELLULAR TRAP; HUMAN; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; LIGHT SCATTERING; LUNG; MASS SPECTROMETRY; MUCUS; NEUTROPHIL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; REFRACTOMETRY; SPUTUM; UPREGULATION; URINE LEVEL; ADULT; BIOSYNTHESIS; CROSS-SECTIONAL STUDY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOLOGY; MALE; MIDDLE AGED; RESPIRATORY MUCOSA; SMOKING; YOUNG ADULT;

ADULT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROSS-SECTIONAL STUDIES; ELECTRONIC NICOTINE DELIVERY SYSTEMS; FEMALE; HUMANS; IMMUNITY, INNATE; LUNG; MALE; MASS SPECTROMETRY; MIDDLE AGED; MUCINS; NEUTROPHIL ACTIVATION; RESPIRATORY MUCOSA; SMOKING; SPUTUM; YOUNG ADULT;

EID: 85045213219     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201708-1590OC     Document Type: Article

References (50)

1. Warren GW, Alberg AJ, Kraft AS, Cummings KM. The 2014 Surgeon General's report: "The health consequences of smoking-50 years of progress": a paradigm shift in cancer care. Cancer 2014; 120: 1914-1916.
2. Singh T, Arrazola RA, Corey CG, Husten CG, Neff LJ, Homa DM, et al. Tobacco use among middle and high school students-United States, 2011-2015. MMWR Morb Mortal Wkly Rep 2016; 65: 361-367.
3. Murthy VH E-cigarette use among youth and young adults: a major public health concern. JAMA Pediatr 2017; 171:209-210.
4. Grana RA, Popova L, Ling PM. A longitudinal analysis of electronic cigarette use and smoking cessation. JAMA Intern Med 2014; 174: 812-813.
5. Ogunwale MA, Li M, Ramakrishnam Raju MV, Chen Y, Nantz MH, Conklin DJ, et al. Aldehyde detection in electronic cigarette aerosols. ACS Omega 2017; 2:1207-1214.
6. Khlystov A, Samburova V. Flavoring compounds dominate toxic aldehyde production during E-cigarette vaping. Environ Sci Technol 2016; 50:13080-13085.
7. Borchers MT, Wert SE, Leikauf GD. Acrolein-induced MUC5ac expression in rat airways. Am J Physiol 1998; 274:L573-L581.
8. Deshmukh HS, Shaver C, Case LM, Dietsch M, Wesselkamper SC, Hardie WD, et al. Acrolein-activated matrix metalloproteinase 9 contributes to persistent mucin production. Am J Respir Cell Mol Biol 2008; 38:446-454.
9. Haswell LE, Hewitt K, Thorne D, Richter A, Gaca MD. Cigarette smoke total particulate matter increases mucous secreting cell numbers in vitro: a potential model of goblet cell hyperplasia. Toxicol In Vitro 2010; 24:981-987.
10. Kesimer M, Ehre C, Burns KA, Davis CW, Sheehan JK, Pickles RJ. Molecular organization of the mucins and glycocalyx underlying mucus transport over mucosal surfaces of the airways. Mucosal Immunol 2013; 6:379-392.
11. Radicioni G, Cao R, Carpenter J, Ford AA, Wang T, Li L, Kesimer M. The innate immune properties of airway mucosal surfaces are regulated by dynamic interactions between mucins and interacting proteins: the mucin interactome. Mucosal Immunol 2016; 9:1442-1454.
12. Anderson WH, Coakley RD, Button B, Henderson AG, Zeman KL, Alexis NE, et al. The relationship of mucus concentration (hydration) to mucus osmotic pressure and transport in chronic bronchitis. Am J Respir Crit Care Med 2015; 192:182-190.
13. Kesimer M, Ford AA, Ceppe A, Radicioni G, Cao R, Davis CW, et al. Airway mucin concentration as a marker of chronic bronchitis. N Engl J Med 2017; 377:911-922.
14. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532-1535.
15. Steinberg BE, Grinstein S. Unconventional roles of the NADPH oxidase: signaling, ion homeostasis, and cell death. Sci STKE 2007; 2007:pe11.
16. Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol 2007; 28:340-345.
17. Ilumets H, Rytilä PH, Sovijärvi AR, Tervahartiala T, Myllärniemi M, Sorsa TA, et al. Transient elevation of neutrophil proteinases in induced sputum during COPD exacerbation. Scand J Clin Lab Invest 2008; 68:618-623.
18. Weiss SJ Tissue destruction by neutrophils. N Engl J Med 1989; 320: 365-376.
19. Arumugam S, Girish Subbiah K, Kemparaju K, Thirunavukkarasu C. Neutrophil extracellular traps in acrolein promoted hepatic ischemia reperfusion injury: therapeutic potential of NOX2 and p38MAPK inhibitors. J Cell Physiol 2017; 233:3244-3261.
20. Alexis NE, Bennett WD, Peden DB. Safety and benefits of inhaled hypertonic saline following airway challenges with endotoxin and allergen in asthmatics. J Asthma 2017; 54:957-960.
21. Henderson AG, Ehre C, Button B, Abdullah LH, Cai LH, Leigh MW, et al. Cystic fibrosis airway secretions exhibit mucin hyperconcentration and increased osmotic pressure. J Clin Invest 2014; 124:3047-3060.
22. Clapp PW, Pawlak EA, Lackey JT, Keating JE, Reeber SL, Glish GL, et al. Flavored e-cigarette liquids and cinnamaldehyde impair respiratory innate immune cell function. Am J Physiol Lung Cell Mol Physiol 2017; 313:L278-L292.
23. Goniewicz ML, Eisner MD, Lazcano-Ponce E, Zielinska-Danch W, Koszowski B, Sobczak A, et al. Comparison of urine cotinine and the tobacco-specific nitrosamine metabolite 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) and their ratio to discriminate active from passive smoking. Nicotine Tob Res 2011; 13:202-208.
24. Jang J-H, Bruse S, Liu Y, Duffy V, Zhang C, Oyamada N, et al. Aldehyde dehydrogenase 3A1 protects airway epithelial cells from cigarette smoke-induced DNA damage and cytotoxicity. Free Radic Biol Med 2014; 68:80-86.
25. Titz B, Sewer A, Schneider T, Elamin A, Martin F, Dijon S, et al. Alterations in the sputum proteome and transcriptome in smokers and early-stage COPD subjects. J Proteomics 2015; 128:306-320.
26. Kimura S, Nishinaga M, Ozawa T, Shimada K. Thrombin generation as an acute effect of cigarette smoking. Am Heart J 1994; 128:7-11.
27. Zhang S, Xu N, Nie J, Dong L, Li J, Tong J. Proteomic alteration in lung tissue of rats exposed to cigarette smoke. Toxicol Lett 2008; 178:191-196.
28. Harju T, Mazur W, Merikallio H, Soini Y, Kinnula VL. Glutathione-S-transferases in lung and sputum specimens, effects of smoking and COPD severity. Respir Res 2008; 9:80.
29. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009; 5:e1000639.
30. Dwyer M, Shan Q, D'Ortona S, Maurer R, Mitchell R, Olesen H, et al. Cystic fibrosis sputum DNA has NETosis characteristics and neutrophil extracellular trap release is regulated by macrophage migration-inhibitory factor. J Innate Immun 2014; 6:765-779.
31. Ford A, Radicioni G, Cao R, Ceppe A, Doerschuk C, O'Neal WK, et al. Mucin hypersecretion associated with chronic bronchitis and not emphysema in sputum from COPD patients from the SPIROMICS cohort [abstract]. Am J Respir Crit Care Med 2016; 193:A3518.
32. 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.
33. Qadir N, Tilley AE, Staudt MR, Fuller J, De BP, Crystal RG. Smoking-induced up-regulation of microseminoprotein beta gene expression in the human airway [abstract]. Am J Respir Crit Care Med 185; 2012: A6052.
34. Caughey GH Serine proteinases of mast cell and leukocyte granules. A league of their own. Am J Respir Crit Care Med 1994; 150: S138-S142.
35. Hozumi A, Nishimura Y, Nishiuma T, Kotani Y, Yokoyama M. Induction of MMP-9 in normal human bronchial epithelial cells by TNF-alpha via NF-kappa B-mediated pathway. Am J Physiol Lung Cell Mol Physiol 2001; 281:L1444-L1452.
36. Thornton DJ, Davies JR, Kirkham S, Gautrey A, Khan N, Richardson PS, et al. Identification of a nonmucin glycoprotein (gp-340) from a purified respiratory mucin preparation: evidence for an association involving the MUC5B mucin. Glycobiology 2001; 11:969-977.
37. Wright NA Interaction of trefoil family factors with mucins: clues to their mechanism of action? Gut 2001; 48:293-294.
38. Thim L, Madsen F, Poulsen SS. Effect of trefoil factors on the viscoelastic properties of mucus gels. Eur J Clin Invest 2002; 32: 519-527.
39. Wright TK, Gibson PG, Simpson JL, McDonald VM, Wood LG, Baines KJ. Neutrophil extracellular traps are associated with inflammation in chronic airway disease. Respirology 2016; 21:467-475.
40. Martinelli S, Urosevic M, Daryadel A, Oberholzer PA, Baumann C, Fey MF, et al. Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J Biol Chem 2004; 279:44123-44132.
41. Gupta AK, Giaglis S, Hasler P, Hahn S. Efficient neutrophil extracellular trap induction requires mobilization of both intracellular and extracellular calcium pools and is modulated by cyclosporine A. PLoS One 2014; 9:e97088.
42. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ 2011; 18: 581-588.
43. Porto BN, Stein RT. Neutrophil extracellular traps in pulmonary diseases: too much of a good thing? Front Immunol 2016; 7:311.
44. Gray RD, McCullagh BN, McCray PB. NETs and CF lung disease: current status and future prospects. Antibiotics (Basel) 2015; 4:62-75.
45. Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, et al. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 2011; 187:490-500.
46. Kessenbrock K, Krumbholz M, Schönermarck U, Back W, Gross WL, Werb Z, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 15:623-625.
47. Higham A, Rattray NJ, Dewhurst JA, Trivedi DK, Fowler SJ, Goodacre R, et al. Electronic cigarette exposure triggers neutrophil inflammatory responses. Respir Res 2016; 17:56.
48. Sussan TE, Gajghate S, Thimmulappa RK, Ma J, Kim JH, Sudini K, et al. Exposure to electronic cigarettes impairs pulmonary anti-bacterial and anti-viral defenses in a mouse model. PLoS One 2015; 10: e0116861.
49. Di YP, Zhao J, Harper R. Cigarette smoke induces MUC5AC protein expression through the activation of Sp1. J Biol Chem 2012; 287: 27948-27958.
50. Lachowicz-Scroggins ME, Yuan S, Kerr SC, Dunican EM, Yu M, Carrington SD, et al. Abnormalities in MUC5AC and MUC5B protein in airway mucus in asthma. Am J Respir Crit Care Med 2016; 194: 1296-1299.