Phagocytosis and Inflammation: Exploring the effects of the components of E-cigarette vapor on macrophages

Physiological Reports

Volumn 5, Issue 16, 2017, Pages

  Ween, Miranda P ^a,b   Whittall, Jonathan J ^a,b   Hamon, Rhys ^a,b   Reynolds, Paul N ^a,b   Hodge, Sandra J ^b  

^a ROYAL ADELAIDE HOSPITAL   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

cytokines; E cigarettes; inflammation; macrophages; phagocytosis

Indexed keywords

CELL SURFACE MARKER; CELL SURFACE RECEPTOR; GLYCEROL; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LACTATE DEHYDROGENASE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; NICOTINE; PROPYLENE GLYCOL; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR; AUTACOID; CYTOKINE; FLAVORING AGENT;

ARTICLE; BACTERIAL COUNT; CONTROLLED STUDY; ELECTRONIC CIGARETTE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; MACROPHAGE CELL LINE; PHAGOCYTOSIS; PROTEIN EXPRESSION; THP-1 CELL LINE; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

CELL LINE; CYTOKINES; ELECTRONIC NICOTINE DELIVERY SYSTEMS; FLAVORING AGENTS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGES; NICOTINE; PHAGOCYTOSIS;

EID: 85028702109     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.13370     Document Type: Article

References (86)

1. Arredouani, M. S., Z. Yang, A. Imrich, Y. Ning, G. Qin, and L. Kobzik. 2006. The macrophage scavenger receptor SR-AI/II and lung defense against pneumococci and particles. Am. J. Respir. Cell Mol. Biol. 35:474–478.
2. Bahl, V., S. Lin, N. Xu, B. Davis, Y. H. Wang, and P. Talbot. 2012. Comparison of electronic cigarette refill fluid cytotoxicity using embryonic and adult models. Reprod. Toxicol. 34:529–537.
3. Bain, W. G., A. Tripathi, P. Mandke, J. H. Gans, F. R. D'Alessio, V. K. Sidhaye, et al. 2016. Low-dose oxygen enhances macrophage-derived bacterial clearance following cigarette smoke exposure. J. Immunol. Res. 2016:1280347.
4. Bandi, V., M. A. Apicella, E. Mason, T. F. Murphy, A. Siddiqi, R. L. Atmar, et al. 2001. Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis. Am. J. Respir. Crit. Care Med. 164:2114–2119.
5. Bardelli, C., G. Gunella, F. Varsaldi, P. Balbo, E. Del Boca, I. S. Bernardone, et al. 2005. Expression of functional NK1 receptors in human alveolar macrophages: superoxide anion production, cytokine release and involvement of NF-kappaB pathway. Br. J. Pharmacol. 145:385–396.
6. Behar, R. Z., B. Davis, Y. Wang, V. Bahl, S. Lin, and P. Talbot. 2014. Identification of toxicants in cinnamon-flavored electronic cigarette refill fluids. Toxicol. In Vitro 28:198–208.
7. Behar, R. Z., M. Hua, and P. Talbot. 2015. Puffing topography and nicotine intake of electronic cigarette users. PLoS ONE 10:e0117222.
8. Berenson, C. S., R. L. Kruzel, E. Eberhardt, and S. Sethi. 2013. Phagocytic dysfunction of human alveolar macrophages and severity of chronic obstructive pulmonary disease. J. Infect. Dis. 208:2036–2045.
9. Bilton, D., A. Pye, M. M. Johnson, J. L. Mitchell, M. Dodd, A. K. Webb, et al. 1995. The isolation and characterization of non-typeable Haemophilus influenzae from the sputum of adult cystic fibrosis patients. Eur. Respir. J. 8:948–953.
10. Birrell, M. A., S. Wong, M. C. Catley, and M. G. Belvisi. 2008. Impact of tobacco-smoke on key signaling pathways in the innate immune response in lung macrophages. J. Cell. Physiol. 214:27–37.
11. Bozinovski, S., R. Vlahos, Y. Zhang, L. C. Lah, H. J. Seow, A. Mansell, et al. 2011. Carbonylation caused by cigarette smoke extract is associated with defective macrophage immunity. Am. J. Respir. Cell Mol. Biol. 45:229–236.
12. Brown, G. P., G. K. Iwamoto, M. M. Monick, and G. W. Hunninghake. 1989. Cigarette smoking decreases interleukin 1 release by human alveolar macrophages. Am. J. Physiol. 256:C260–C264.
13. Brozyna, S., J. Ahern, G. Hodge, J. Nairn, M. Holmes, P. N. Reynolds, et al. 2009. Chemotactic mediators of Th1 T-cell trafficking in smokers and COPD patients. Copd 6:4–16.
14. Cervellati, F., X. M. Muresan, C. Sticozzi, R. Gambari, G. Montagner, H. J. Forman, et al. 2014. Comparative effects between electronic and cigarette smoke in human keratinocytes and epithelial lung cells. Toxicol. In Vitro 28:999–1005.
15. Chen, H., M. J. Cowan, J. D. Hasday, S. N. Vogel, and A. E. Medvedev. 2007. Tobacco smoking inhibits expression of proinflammatory cytokines and activation of IL-1R-associated kinase, p38, and NF-kappaB in alveolar macrophages stimulated with TLR2 and TLR4 agonists. J. Immunol. 179:6097–6106.
16. Dockrell, M., R. Morrison, L. Bauld, and A. McNeill. 2013. E-cigarettes: prevalence and attitudes in Great Britain. Nicotine Tob. Res. 15:1737–1744.
17. Doz, E., N. Noulin, E. Boichot, I. Guenon, L. Fick, M. Le Bert, et al. 2008. Cigarette smoke-induced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J. Immunol. 180:1169–1178.
18. Droemann, D., T. Goldmann, T. Tiedje, P. Zabel, K. Dalhoff, and B. Schaaf. 2005. Toll-like receptor 2 expression is decreased on alveolar macrophages in cigarette smokers and COPD patients. Respir. Res. 6:68.
19. El Golli, N., D. Rahali, A. Jrad-Lamine, Y. Dallagi, M. Jallouli, Y. Bdiri, et al. 2016. Impact of electronic-cigarette refill liquid on rat testis. Toxicol. Mech. Methods 26:427–434.
20. Garcia-Gomez, D., T. Gaisl, C. Barrios-Collado, G. Vidal-de-Miguel, M. Kohler, and R. Zenobi. 2016. Real-time chemical analysis of E-cigarette aerosols by means of secondary electrospray ionization mass spectrometry. Chemistry 22:2452–2457.
21. Grumelli, S., D. B. Corry, L. Z. Song, L. Song, L. Green, J. Huh, et al. 2004. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med. 1:e8.
22. Gualano, R. C., M. J. Hansen, R. Vlahos, J. E. Jones, R. A. Park-Jones, G. Deliyannis, et al. 2008. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir. Res. 9:53.
23. Halldin, C. N., E. Suarthana, K. B. Fedan, Y. C. Lo, G. Turabelidze, and K. Kreiss. 2013. Increased respiratory disease mortality at a microwave popcorn production facility with worker risk of bronchiolitis obliterans. PLoS ONE 8:e57935.
24. Harrold, T. C., A. K. Maag, S. Thackway, J. Mitchell, and L. K. Taylor. 2015. Prevalence of e-cigarette users in New South Wales. Med. J. Aust. 203:326.
25. Heguy, A., T. P. O'Connor, K. Luettich, S. Worgall, A. Cieciuch, B. G. Harvey, et al. 2006. Gene expression profiling of human alveolar macrophages of phenotypically normal smokers and nonsmokers reveals a previously unrecognized subset of genes modulated by cigarette smoking. J. Mol. Med. (Berl) 84:318–328.
26. Higham, A., N. J. Rattray, J. A. Dewhurst, D. K. Trivedi, S. J. Fowler, R. Goodacre, et al. 2016. Electronic cigarette exposure triggers neutrophil inflammatory responses. Respir. Res. 17:56.
27. Hodge, S., G. Hodge, R. Scicchitano, P. N. Reynolds, and M. Holmes. 2003. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol. Cell Biol. 81:289–296.
28. Hodge, S., G. Hodge, M. Holmes, and P. N. Reynolds. 2005. Increased airway epithelial and T-cell apoptosis in COPD remains despite smoking cessation. Eur. Respir. J. 25:447–454.
29. Hodge, S., G. Hodge, S. Brozyna, H. Jersmann, M. Holmes, and P. N. Reynolds. 2006. Azithromycin increases phagocytosis of apoptotic bronchial epithelial cells by alveolar macrophages. Eur. Respir. J. 28:486–495.
30. Hodge, S., G. Hodge, J. Ahern, H. Jersmann, M. Holmes, and P. N. Reynolds. 2007. Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 37:748–755.
31. Hodge, S., G. Matthews, V. Mukaro, J. Ahern, A. Shivam, G. Hodge, et al. 2011. Cigarette smoke-induced changes to alveolar macrophage phenotype and function are improved by treatment with procysteine. Am. J. Respir. Cell Mol. Biol. 44:673–681.
32. Hwang, J. H., M. Lyes, K. Sladewski, S. Enany, E. McEachern, D. P. Mathew, et al. 2016. Electronic cigarette inhalation alters innate immunity and airway cytokines while increasing the virulence of colonizing bacteria. J. Mol. Med. (Berl) 94:667–679.
33. Keatings, V. M., P. D. Collins, D. M. Scott, and P. J. Barnes. 1996. Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am. J. Respir. Crit. Care Med. 153:530–534.
34. Kent, L., L. Smyth, C. Clayton, L. Scott, T. Cook, R. Stephens, et al. 2008. Cigarette smoke extract induced cytokine and chemokine gene expression changes in COPD macrophages. Cytokine 42:205–216.
35. Kent, L. M., S. M. Fox, S. N. Farrow, and D. Singh. 2010. The effects of dexamethasone on cigarette smoke induced gene expression changes in COPD macrophages. Int. Immunopharmacol. 10:57–64.
36. King, P. 2012. Haemophilus influenzae and the lung (Haemophilus and the lung). Clin. Trans. Med. 1:10.
37. Kosmider, L., A. Sobczak, A. Prokopowicz, J. Kurek, M. Zaciera, J. Knysak, et al. 2016. Cherry-flavoured electronic cigarettes expose users to the inhalation irritant, benzaldehyde. Thorax 71:376–377.
38. Larcombe, A. N., M. A. Janka, B. J. Mullins, L. J. Berry, A. Bredin, and P. J. Franklin. 2017. The effects of electronic cigarette aerosol exposure on inflammation and lung function in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 00203:02016.
39. Lee, J. A., S. H. Kim, and H. J. Cho. 2016. Electronic cigarette use among Korean adults. Int J Public Health 61:151–157.
40. Lerner, C. A., I. K. Sundar, H. Yao, J. Gerloff, D. J. Ossip, S. McIntosh, et al. 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.
41. Lessmann, H., A. Schnuch, J. Geier, and W. Uter. 2005. Skin-sensitizing and irritant properties of propylene glycol. Contact Derm. 53:247–259.
42. Li, J., R. Newcombe, and D. Walton. 2015. The prevalence, correlates and reasons for using electronic cigarettes among New Zealand adults. Addict Behav. 45:245–351.
43. Li, J. R., W. X. Zhou, Z. X. Zhao, and J. M. Gao. 2014. Differential expression of the inflammation-associated chemokines/cytokines in mouse lung after exposure to cigarette smoke and smoking cessation. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 36:241–248.
44. Lim, H. B., and S. H. Kim. 2014. Inhallation of e-cigarette cartridge solution aggravates allergen-induced airway inflammation and hyper-responsiveness in mice. Toxicol. Res. 30:13–18.
45. Matsumoto, K., H. Aizawa, H. Inoue, H. Koto, S. Takata, M. Shigyo, et al. 1998. Eosinophilic airway inflammation induced by repeated exposure to cigarette smoke. Eur. Respir. J. 12:387–394.
46. McCrea, K. A., J. E. Ensor, K. Nall, E. R. Bleecker, and J. D. Hasday. 1994. Altered cytokine regulation in the lungs of cigarette smokers. Am. J. Respir. Crit. Care Med. 150:696–703.
47. McGrath-Morrow, S. A., M. Hayashi, A. Aherrera, A. Lopez, A. Malinina, J. M. Collaco, et al. 2015. The effects of electronic cigarette emissions on systemic cotinine levels, weight and postnatal lung growth in neonatal mice. PLoS ONE 10:e0118344.
48. Metcalfe, H. J., S. Lea, D. Hughes, R. Khalaf, K. Abbott-Banner, and D. Singh. 2014. Effects of cigarette smoke on Toll-like receptor (TLR) activation of chronic obstructive pulmonary disease (COPD) macrophages. Clin. Exp. Immunol. 176:461–472.
49. Mikuniya, T., S. Nagai, T. Tsutsumi, K. Morita, T. Mio, N. Satake, et al. 1999. Proinflammatory or regulatory cytokines released from BALF macrophages of healthy smokers. Respiration 66:419–426.
50. Modi, P., V. Yadava, R. Sreedhar, F. Khasawaneh, and R. A. Balk. 2008. A case of flavor-induced lung disease. South. Med. J. 101:541–542.
51. Mortaz, E., Z. Lazar, L. Koenderman, A. D. Kraneveld, F. P. Nijkamp, and G. Folkerts. 2009. Cigarette smoke attenuates the production of cytokines by human plasmacytoid dendritic cells and enhances the release of IL-8 in response to TLR-9 stimulation. Respir. Res. 10:47.
52. Nordskog, B. K., W. R. Fields, and G. M. Hellmann. 2005. Kinetic analysis of cytokine response to cigarette smoke condensate by human endothelial and monocytic cells. Toxicology 212:87–97.
53. O'Grady, N. P., M. Tropea, H. L. 2nd Preas, D. Reda, R. W. Vandivier, S. M. Banks, et al. 1999. Detection of macrophage inflammatory protein (MIP)-1alpha and MIP-1beta during experimental endotoxemia and human sepsis. J. Infect. Dis. 179:136–141.
54. Ouyang, Y., N. Virasch, P. Hao, M. T. Aubrey, N. Mukerjee, B. E. Bierer, et al. 2000. Suppression of human IL-1beta, IL-2, IFN-gamma, and TNF-alpha production by cigarette smoke extracts. J. Allergy Clin. Immunol. 106:280–287.
55. Paul-Clark, M. J., S. K. McMaster, R. Sorrentino, S. Sriskandan, L. K. Bailey, L. Moreno, et al. 2009. Toll-like receptor 2 is essential for the sensing of oxidants during inflammation. Am. J. Respir. Crit. Care Med. 179:299–306.
56. Reid, J. L., V. L. Rynard, C. D. Czoli, and D. Hammond. 2015. Who is using e-cigarettes in Canada? Nationally representative data on the prevalence of e-cigarette use among Canadians. Prev. Med. 81:180–183.
57. Sancilio, S., M. Gallorini, A. Cataldi, and V. di Giacomo. 2016. Cytotoxicity and apoptosis induction by e-cigarette fluids in human gingival fibroblasts. Clin. Oral Investig. 20:477–483.
58. Sauty, A., J. Mauel, M. M. Philippeaux, and P. Leuenberger. 1994. Cytostatic activity of alveolar macrophages from smokers and nonsmokers: role of interleukin-1 beta, interleukin-6, and tumor necrosis factor-alpha. Am. J. Respir. Cell Mol. Biol. 11:631–637.
59. Scheffler, S., H. Dieken, O. Krischenowski, C. Forster, D. Branscheid, and M. Aufderheide. 2015. Evaluation of E-cigarette liquid vapor and mainstream cigarette smoke after direct exposure of primary human bronchial epithelial cells. Int. J. Environ. Res. Public Health 12:3915–3925.
60. Schoenborn, C. A., and R. M. Gindi. 2015. Electronic cigarette use among adults: United States, 2014. NCHS Data Brief 000: 1–8.
61. Schweitzer, K. S., S. X. Chen, S. Law, M. J. Van Demark, C. Poirier, M. J. Justice, et al. 2015. Endothelial disruptive pro-inflammatory effects of nicotine and e-cigarette vapor exposures. Am. J. Physiol. Lung Cell. Mol. Physiol. 00411:02015.
62. Shang, S., D. Ordway, M. Henao-Tamayo, X. Bai, R. Oberley-Deegan, C. Shanley, et al. 2011. Cigarette smoke increases susceptibility to tuberculosis–evidence from in vivo and in vitro models. J. Infect. Dis. 203:1240–1248.
63. Sherwood, C. L., and S. Boitano. 2016. Airway epithelial cell exposure to distinct e-cigarette liquid flavorings reveals toxicity thresholds and activation of CFTR by the chocolate flavoring 2,5-dimethypyrazine. Respir. Res. 17:57.
64. Singh, T., S. Kennedy, K. Marynak, A. Persoskie, P. Melstrom, and B. A. King. 2016. Characteristics of electronic cigarette use among middle and high school students - United States, 2015. MMWR Morb. Mortal. Wkly Rep. 65:1425–1429.
65. Soliman, D. M., and H. L. 3rd Twigg. 1992. Cigarette smoking decreases bioactive interleukin-6 secretion by alveolar macrophages. Am. J. Physiol. 263:L471–L478.
66. Sunakawa, K., Y. Takeuchi, and S. Iwata. 2011. Nontypeable haemophilus influenzae (NTHi) epidemiology. Kansenshogaku Zasshi 85:227–237.
67. Sussan, T. E., S. Gajghate, R. K. Thimmulappa, J. Ma, J. H. Kim, K. Sudini, et al. 2015. Exposure to electronic cigarettes impairs pulmonary anti-bacterial and anti-viral defenses in a mouse model. PLoS ONE 10:e0116861.
68. Tabuchi, T., K. Kiyohara, T. Hoshino, K. Bekki, Y. Inaba, and N. Kunugita. 2016. Awareness and use of electronic cigarettes and heat-not-burn tobacco products in Japan. Addiction 111:706–713.
69. Taylor, A. E., T. K. Finney-Hayward, J. K. Quint, C. M. Thomas, S. J. Tudhope, J. A. Wedzicha, et al. 2010. Defective macrophage phagocytosis of bacteria in COPD. Eur. Respir. J. 35:1039–1047.
70. Thimmulappa, R. K., X. Gang, J. H. Kim, T. E. Sussan, J. L. Witztum, and S. Biswal. 2012. Oxidized phospholipids impair pulmonary antibacterial defenses: evidence in mice exposed to cigarette smoke. Biochem. Biophys. Res. Commun. 426:253–259.
71. Thomas, C. A., Y. Li, T. Kodama, H. Suzuki, S. C. Silverstein, and J. El Khoury. 2000. Protection from lethal gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J. Exp. Med. 191:147–156.
72. Tran, H. B., J. Barnawi, M. Ween, R. Hamon, E. Roscioli, G. Hodge, et al. 2016. Cigarette smoke inhibits efferocytosis via deregulation of sphingosine kinase signaling: reversal with exogenous S1P and the S1P analogue FTY720. J. Leukoc. Biol. 100:195–202.
73. Traves, S. L., S. V. Culpitt, R. E. Russell, P. J. Barnes, and L. E. Donnelly. 2002. Increased levels of the chemokines GROalpha and MCP-1 in sputum samples from patients with COPD. Thorax 57:590–595.
74. Varughese, S., K. Teschke, M. Brauer, Y. Chow, C. van Netten, and S. M. Kennedy. 2005. Effects of theatrical smokes and fogs on respiratory health in the entertainment industry. Am. J. Ind. Med. 47:411–418.
75. Walsberger, S., and M. Havill. 2015. NSW community behaviors, beliefs & attitudes towards E-cigarettes: results of an online survey cancer council. NSW, Sydney.
76. Walters, M. J., M. J. Paul-Clark, S. K. McMaster, K. Ito, I. M. Adcock, and J. A. Mitchell. 2005. Cigarette smoke activates human monocytes by an oxidant-AP-1 signaling pathway: implications for steroid resistance. Mol. Pharmacol. 68:1343–1353.
77. Ween, M., J. Ahern, A. Carroll, G. Hodge, S. Pizzutto, H. Jersmann, et al. 2016. A small volume technique to examine and compare alveolar macrophage phagocytosis of apoptotic cells and non typeable Haemophilus influenzae (NTHi). J. Immunol. Methods 429:7–14.
78. Welz, C., M. Canis, S. Schwenk-Zieger, S. Becker, V. Stucke, F. Ihler, et al. 2016. Cytotoxic and genotoxic effects of electronic cigarette liquids on human mucosal tissue cultures of the oropharynx. J. Environ. Pathol. Toxicol. Oncol. 35:343–354.
79. Wesselius, L. J., M. E. Nelson, K. Bailey, and A. R. O'Brien-Ladner. 1997. Rapid lung cytokine accumulation and neutrophil recruitment after lipopolysaccharide inhalation by cigarette smokers and nonsmokers. J. Lab. Clin. Med. 129:106–114.
80. Wieslander, G., D. Norback, and T. Lindgren. 2001. Experimental exposure to propylene glycol mist in aviation emergency training: acute ocular and respiratory effects. Occup. Environ. Med. 58:649–655.
81. Wilson, F. A., and Y. Wang. 2017. Recent findings on the prevalence of E-cigarette use among adults in the U.S. Am. J. Prev. Med. 52:385–390.
82. Wright, J. L., J. P. Sun, and A. Churg. 1999. Cigarette smoke exposure causes constriction of rat lung. Eur. Respir. J. 14:1095–1099.
83. Wu, Z. X., and L. Y. Lee. 1985. Airway hyperresponsiveness induced by chronic exposure to cigarette smoke in guinea pigs: role of tachykinins. J. Appl. Physiol. 87(1621–1628):1999.
84. Wu, Q., D. Jiang, M. Minor, and H. W. Chu. 2014. Electronic cigarette liquid increases inflammation and virus infection in primary human airway epithelial cells. PLoS ONE 9:e108342.
85. Yamaguchi, E., A. Itoh, K. Furuya, H. Miyamoto, S. Abe, and Y. Kawakami. 1993. Release of tumor necrosis factor-alpha from human alveolar macrophages is decreased in smokers. Chest 103:479–483.
86. Yang, S. R., J. Wright, M. Bauter, K. Seweryniak, A. Kode, and I. Rahman. 2007. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am. J. Physiol. Lung Cell. Mol. Physiol. 292:L567–L576.