A 7-month cigarette smoke inhalation study in C57BL/6 mice demonstrates reduced lung inflammation and emphysema following smoking cessation or aerosol exposure from a prototypic modified risk tobacco product

Food and Chemical Toxicology

Volumn 80, Issue , 2015, Pages 328-345

  Phillips, Blaine ^a   Veljkovic, Emilija ^b   Peck, Michael J ^b   Buettner, Ansgar ^c   Elamin, Ashraf ^b   Guedj, Emmanuel ^b   Vuillaume, Gregory ^b   Ivanov, Nikolai V ^b   Martin, Florian ^b   Boué, Stéphanie ^b   Schlage, Walter K ^b   Schneider, Thomas ^b   Titz, Bjoern ^b   Talikka, Marja ^b   Vanscheeuwijck, Patrick ^b   Hoeng, Julia ^b   Peitsch, Manuel C ^b  

^a PHILIP MORRIS PRODUCTS S A   (Switzerland)

^b Philip Morris Products SA   (Switzerland)

^c Histovia GmbH   (Germany)

Author keywords

Computational network model; COPD; Histopathology; Mechanistic investigations; Systems toxicology; Tobacco heating

Indexed keywords

CIGARETTE SMOKE; NICOTINE; AEROSOL;

AEROSOL; AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIGARETTE SMOKE-INDUCED EMPHYSEMA; CONTROLLED STUDY; DISEASE COURSE; FEMALE; FRESH AIR; INFLAMMATION; LUNG ALVEOLUS; LUNG DISEASE; LUNG INJURY; MOUSE; NONHUMAN; PNEUMONIA; PROTEOMICS; PROTOTYPE MODIFIED RISK TOBACCO PRODUCT; SMOKING CESSATION; TOBACCO; TOXICOLOGY; TRANSCRIPTOMICS; TREATMENT DURATION; ANIMAL; C57BL MOUSE; DRUG ADMINISTRATION; EMPHYSEMA; LUNG; LUNG BURN; PATHOLOGY; TOXICITY;

MURINAE; MUS; NICOTIANA TABACUM;

AEROSOLS; ANIMALS; DRUG ADMINISTRATION SCHEDULE; EMPHYSEMA; INFLAMMATION; LUNG; MICE; MICE, INBRED C57BL; SMOKE INHALATION INJURY; SMOKING CESSATION; TOBACCO PRODUCTS;

EID: 84927607692     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2015.03.009     Document Type: Article

References (79)

1. Alhadeff A.L., Rupprecht L.E., Hayes M.R. GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 2012, 153:647-658.
2. Barnes P.J. Mediators of chronic obstructive pulmonary disease. Pharmacol. Rev 2004, 56:515-548.
3. Barnes P.J. The cytokine network in asthma and chronic obstructive pulmonary disease. J. Clin. Invest 2008, 118:3546-3556.
4. Barnes P.J. The cytokine network in chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol 2009, 41:631-638.
5. Bartalesi B., Cavarra E., Fineschi S., Lucattelli M., Lunghi B., Martorana P., et al. Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur. Respir. J. 2005, 25:15-22.
6. Beckett E.L., Stevens R.L., Jarnicki A.G., Kim R.Y., Hanish I., Hansbro N.G., et al. A new short-term mouse model of chronic obstructive pulmonary disease identifies a role for mast cell tryptase in pathogenesis. J. Allergy Clin. Immunol 2013, 131:752-762.
7. Boue S., De Leon H., Schlage W.K., Peck M.J., Weiler H., Berges A., et al. Cigarette smoke induces molecular responses in respiratory tissues of ApoE-/- mice that are progressively deactivated upon cessation. Toxicology 2013, 314:112-124.
8. Braber S., Henricks P.A., Nijkamp F.P., Kraneveld A.D., Folkerts G. Inflammatory changes in the airways of mice caused by cigarette smoke exposure are only partially reversed after smoking cessation. Respir. Res 2010, 11:99.
9. Brusselle G.G., Bracke K.R., Maes T., D'Hulst A.I., Moerloose K.B., Joos G.F., et al. Murine models of COPD. Pulm. Pharmacol. Ther 2006, 19:155-165.
10. Brusselle G.G., Joos G.F., Bracke K.R. New insights into the immunology of chronic obstructive pulmonary disease. Lancet 2011, 378:1015-1026.
11. Cho H.Y., Jedlicka A.E., Reddy S.P., Zhang L.Y., Kensler T.W., Kleeberger S.R. Linkage analysis of susceptibility to hyperoxia. Nrf2 is a candidate gene. Am. J. Respir. Cell Mol. Biol 2002, 26:42-51.
12. Churg A., Wright J.L. Animal models of cigarette smoke-induced chronic obstructive lung disease. Contrib. Microbiol 2007, 14:113-125.
13. Churg A., Tai H., Coulthard T., Wang R., Wright J.L. Cigarette smoke drives small airway remodeling by induction of growth factors in the airway wall. Am. J. Respir. Crit. Care Med 2006, 174:1327-1334.
14. Churg A., Tai H., Coulthard T., Wang R., Wright J.L. Cigarette smoke drives small airway remodeling by induction of growth factors in the airway wall. Am. J. Respir. Crit. Care Med 2006, 174:1327-1334.
15. Churg A., Cosio M., Wright J.L. Mechanism of cigarette smoke-induced COPD: insights from animal models. Am. J. Physiol. Lung Cell. Mol. Physiol 2008, 294:L612-L631.
16. Coggins C.R., Ayres P.H., Mosberg A.T., Sagartz J.W., Burger G.T., Hayes A.W. Ninety-day inhalation study in rats, comparing smoke from cigarettes that heat tobacco with those that burn tobacco. Fundam. Appl. Toxicol 1989, 13:460-483.
17. Cremona T.P., Tschanz S.A., von Garnier C., Benarafa C. SerpinB1 deficiency is not associated with increased susceptibility to pulmonary emphysema in mice. Am. J. Physiol. Lung Cell. Mol. Physiol 2013, 305:L981-L989.
18. Di Stefano A., Caramori G., Gnemmi I., Contoli M., Vicari C., Capelli A., et al. T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin. Exp. Immunol 2009, 157:316-324.
19. Egecioglu E., Engel J.A., Jerlhag E. The glucagon-like peptide 1 analogue Exendin-4 attenuates the nicotine-induced locomotor stimulation, accumbal dopamine release, conditioned place preference as well as the expression of locomotor sensitization in mice. PLoS ONE 2013, 8:e77284.
20. Elkington P.T., Friedland J.S. Matrix metalloproteinases in destructive pulmonary pathology. Thorax 2006, 61:259-266.
21. Ezzie M.E., Crawford M., Cho J.-H., Orellana R., Zhang S., Gelinas R., et al. Gene expression networks in COPD: microRNA and mRNA regulation. Thorax 2012, 67:122-131.
22. Food and Drug Administration Federal Food, Drug, and Cosmetic Act. 18 FDC Act as Amended by the Family Smoking Prevention and Tobacco Control Act (Public Law 111-31) 2012, 21. U.S.C 387 k. Food and Drug Administration (Ed.).
23. Food and Drug Administration Modified risk tobacco product applications: draft guidance for industry http://www.fda.gov/downloads/TobaccoProducts/GuidanceComplianceRegulatoryInformation/UCM297751.pdf.
24. Foronjy R., Nkyimbeng T., Wallace A., Thankachen J., Okada Y., Lemaitre V., et al. Transgenic expression of matrix metalloproteinase-9 causes adult-onset emphysema in mice associated with the loss of alveolar elastin. Am. J. Physiol. Lung Cell. Mol. Physiol 2008, 294:L1149-L1157.
25. Franceschini A., Szklarczyk D., Frankild S., Kuhn M., Simonovic M., Roth A., et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 2013, 41:D808-D815.
26. Friedrichs B., Miert E., Vanscheeuwijck P. Lung inflammation in rats following subchronic exposure to cigarette mainstream smoke. Exp. Lung Res 2006, 32:151-179.
27. GOLD Global strategy for the diagnosis, management, and prevention of chronic obstructive disease (updated 2014) Global Initiative for Chronic Obstructive Lung Disease, Inc. http://www.goldcopd.org/uploads/users/files/GOLD_Report_2014_Jan23.pdf.
28. Halwani R., Al-Muhsen S., Hamid Q. T helper 17 cells in airway diseases: from laboratory bench to bedside. Chest 2013, 143:494-501.
29. Health Canada Health Canada Test Method T-115 1999, Determination of "Tar" and Nicotine in Sidestream Tobacco Smoke.
30. Hoeng J., Deehan R., Pratt D., Martin F., Sewer A., Thomson T.M., et al. A network-based approach to quantifying the impact of biologically active substances. Drug Discov. Today 2012, 17:413-418.
31. Hoeng J., Talikka M., Martin F., Sewer A., Yang X., Iskandar A., et al. Case study: the role of mechanistic network models in systems toxicology. Drug Discov. Today 2013, 19:183-192.
32. Hogg J.C. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet 2004, 364:709-721.
33. Hong S.C., Lee S.H. Role of th17 cell and autoimmunity in chronic obstructive pulmonary disease. Immune Netw 2010, 10:109-114.
34. Hutt J.A., Vuillemenot B.R., Barr E.B., Grimes M.J., Hahn F.F., Hobbs C.H., et al. Life-span inhalation exposure to mainstream cigarette smoke induces lung cancer in B6C3F1 mice through genetic and epigenetic pathways. Carcinogenesis 2005, 26:1999-2009.
35. Iskandar A., Martin F., Talikka M., Schlage W.K., Kostadinova R., Mathis C., et al. Systems approaches evaluating the perturbation of xenobiotic metabolism in response to cigarette smoke exposure in nasal and bronchial tissues. BioMed Res. Int 2013, 2013:15.
36. John G., Kohse K., Orasche J., Reda A., Schnelle-Kreis J., Zimmermann R., et al. The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models. Clin. Sci. (Lond.) 2014, 126:207-221.
37. Kim V., Rogers T.J., Criner G.J. New concepts in the pathobiology of chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc 2008, 5:478-485.
38. Kogel U., Schlage W.K., Martin F., Xiang Y., Ansari S., Leroy P., et al. A 28-day rat inhalation study with an integrated molecular toxicology endpoint demonstrates reduced exposure effects for a prototypic modified risk tobacco product compared with conventional cigarettes. Food Chem. Toxicol 2014, 68:204-217.
39. Manigrasso M., Buonanno G., Fuoco F.C., Stabile L., Avino P. Aerosol deposition doses in the human respiratory tree of electronic cigarette smokers. Environ. Pollut 2014, 196C:257-267.
40. March T., Seagrave J. Strain-specific pulmonary inflammatory responses and emphysema development in cigarette smoke-exposed mice. Toxicol. Pathol 2007, 35:183.
41. Martin F., Thomson T.M., Sewer A., Drubin D.A., Mathis C., Weisensee D., et al. Assessment of network perturbation amplitude by applying high-throughput data to causal biological networks. BMC Syst. Biol 2012, 6:54.
42. Martin F., Sewer A., Talikka M., Xiang Y., Hoeng J., Peitsch M.C. Quantification of biological network perturbations for mechanistic insight and diagnostics using two-layer causal models. BMC Bioinformatics 2014, 15:238.
43. Mathers C.D., Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006, 3:e442.
44. Morgan T.M., Crawford L., Stoller A., Toth D., Yeo K.T., Baron J.A. Acute effects of nicotine on serum glucose insulin growth hormone and cortisol in healthy smokers. Metabolism 2004, 53:578-582.
45. Mortaz E., Folkerts G., Redegeld F. Mast cells and COPD. Pulm. Pharmacol. Ther 2011, 24:367-372.
46. Ning W., Li C.-J., Kaminski N., Feghali-Bostwick C.A., Alber S.M., Di Y.P., et al. Comprehensive gene expression profiles reveal pathways related to the pathogenesis of chronic obstructive pulmonary disease. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:14895-14900.
47. Overbeek S.A., Braber S., Koelink P.J., Henricks P.A., Mortaz E., LoTam Loi A.T., et al. Cigarette smoke-induced collagen destruction; key to chronic neutrophilic airway inflammation?. PLoS ONE 2013, 8:e55612.
48. Pauwels R.A., Rabe K.F. Burden and clinical features of chronic obstructive pulmonary disease (COPD). Lancet 2004, 364:613-620.
49. Pellegrini M.P., Newby D.E., Maxwell S., Webb D.J. Short-term effects of transdermal nicotine on acute tissue plasminogen activator release in vivo in man. Cardiovasc. Res 2001, 52:321-327.
50. Prause O., Bozinovski S., Anderson G.P., Linden A. Increased matrix metalloproteinase-9 concentration and activity after stimulation with interleukin-17 in mouse airways. Thorax 2004, 59:313-317.
51. Rabe K.F., Hurd S., Anzueto A., Barnes P.J., Buist S.A., Calverley P., et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am. J. Respir. Crit. Care Med 2007, 176:532-555.
52. Rampling M.W. Clotting factors and rheology: mechanisms of damage and intervention. Cardiovascular Disease: Risk Factors and Intervention 1993, 201-213. Radcliffe Medical Press, Oxford. N. Poulter, P. Sever, S. Thom (Eds.).
53. Rustemeier K., Demetriou D., Schepers G., Voncken P. High-performance liquid chromatographic determination of nicotine and its urinary metabolites via their 1, 3-diethyl-2-thiobarbituric acid derivatives. J. Chromatogr. B. Biomed Sci. Appl 1993, 613:95-103.
54. Saetta M., Baraldo S., Corbino L., Turato G., Braccioni F., Rea F., et al. CD8+ve cells in the lungs of smokers with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med 1999, 160:711-717.
55. Saetta M., Baraldo S., Turato G., Beghe B., Casoni G.L., Bellettato C.M., et al. Increased proportion of CD8+ T-lymphocytes in the paratracheal lymph nodes of smokers with mild COPD. Sarcoidosis Vasc. Diffuse Lung Dis 2003, 20:28-32.
56. Schorp M.K., Tricker A.R., Dempsey R. Reduced exposure evaluation of an electrically heated cigarette smoking system. Part 1: non-clinical and clinical insights. Regul. Toxicol. Pharmacol 2012, 64:S1-S10.
57. Smoot M.E., Ono K., Ruscheinski J., Wang P.L., Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27:431-432.
58. Spira A., Beane J., Pinto-Plata V., Kadar A., Liu G., Shah V., et al. Gene expression profiling of human lung tissue from smokers with severe emphysema. Am. J. Respir. Cell Mol. Biol 2004, 31:601-610.
59. Stevenson C.S., Docx C., Webster R., Battram C., Hynx D., Giddings J., et al. Comprehensive gene expression profiling of rat lung reveals distinct acute and chronic responses to cigarette smoke inhalation. Am. J. Physiol. Lung Cell. Mol. Physiol 2007, 293:L1183-L1193.
60. Stinn W., Arts J.H., Buettner A., Duistermaat E., Janssens K., Kuper C.F., et al. Murine lung tumor response after exposure to cigarette mainstream smoke or its particulate and gas/vapor phase fractions. Toxicology 2010, 275:10-20.
61. Stokes M.E., Davis C.S., Koch G.C. Categorical Data Analysis Using the SAS® System 1995, SAS Institute Inc., Cary, NC.
62. Stratton K., Shetty P., St Claire A.W., Martinez R.M., Pellmar T. Clearing the Smoke: assessing the science base for tobacco harm reduction 2001, 636. National Academy Press, Washington, DC. Institute of Medicine (Ed.).
63. Sturla S.J., Boobis A.R., Fitzgerald R.E., Hoeng J., Kavlock R.J., Schirmer K., et al. Systems toxicology: from basic research to risk assessment. Chem. Res. Toxicol 2014, 27:314-329.
64. Suzuki M., Betsuyaku T., Nagai K., Fuke S., Nasuhara Y., Kaga K., et al. Decreased airway expression of vascular endothelial growth factor in cigarette smoke-induced emphysema in mice and COPD patients. Inhal. Toxicol 2008, 20:349-359.
65. Terpstra P.M., Teredesai A., Vanscheeuwijck P.M., Verbeeck J., Schepers G., Radtke F., et al. Toxicological evaluation of an electrically heated cigarette. Part 4: subchronic inhalation toxicology. J. Appl. Toxicol 2003, 23:349-362.
66. Thomson T.M., Sewer A., Martin F., Belcastro V., Frushour B., Gebel S., et al. Quantitative assessment of biological impact using transcriptomic data and mechanistic network models. Toxicol. Appl. Pharmacol 2013, 272:863-878.
67. Tuder R.M., Yoshida T., Arap W., Pasqualini R., Petrache I. State of the art. Cellular and molecular mechanisms of alveolar destruction in emphysema: an evolutionary perspective. Proc. Am. Thorac. Soc 2006, 3:503-510.
68. Turton M.D., O'Shea D., Gunn I., Beak S.A., Edwards C.M., Meeran K., et al. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 1996, 379:69-72.
69. U.S.Office of the Surgeon General The health consequences of smoking: a report of the Surgeon General 2004, Centers for Disease Control and Prevention (US), Atlanta (GA).
70. Vanoirbeek J.A., Rinaldi M., De Vooght V., Haenen S., Bobic S., Gayan-Ramirez G., et al. Noninvasive and invasive pulmonary function in mouse models of obstructive and restrictive respiratory diseases. Am. J. Respir. Cell Mol. Biol 2010, 42:96-104.
71. Vanscheeuwijck P.M., Teredesai A., Terpstra P.M., Verbeeck J., Kuhl P., Gerstenberg B., et al. Evaluation of the potential effects of ingredients added to cigarettes. Part 4: subchronic inhalation toxicity. Food Chem. Toxicol 2002, 40:113-131.
72. Vecchio D., Arezzini B., Pecorelli A., Valacchi G., Martorana P.A., Gardi C. Reactivity of mouse alveolar macrophages to cigarette smoke is strain dependent. Am. J. Physiol. Lung Cell. Mol. Physiol 2010, 298:L704-L713.
73. Vestbo J., Hurd S.S., Agusti A.G., Jones P.W., Vogelmeier C., Anzueto A., et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am. J. Respir. Crit. Care Med 2013, 187:347-365.
74. Vlahos R., Bozinovski S. Recent advances in pre-clinical mouse models of COPD. Clin. Sci. (Lond.) 2014, 126:253-265.
75. Werley M.S., Freelin S.A., Wrenn S.E., Gerstenberg B., Roemer E., Schramke H., et al. Smoke chemistry, in vitro and in vivo toxicology evaluations of the Electrically Heated Cigarette Smoking System Series K. Regul. Toxicol. Pharmacol 2008, 52:122-139.
76. Yao H., Edirisinghe I., Rajendrasozhan S., Yang S.-R., Caito S., Adenuga D., et al. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am. J. Physiol. Lung Cell. Mol. Physiol 2008, 294:L1174-L1186.
77. Yoshida T., Tuder R.M. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol. Rev 2007, 87:1047-1082.
78. Zhou S., Wright J.L., Liu J., Sin D.D., Churg A. Aging does not Enhance Experimental Cigarette Smoke-Induced COPD in the Mouse. PLoS ONE 2013, 8:e71410.
79. Zidovetzki R., Chen P., Fisher M., Hofman F.M., Faraci F.M. Nicotine increases plasminogen activator inhibitor-1 production by human brain endothelial cells via protein kinase C-associated pathway. Stroke 1999, 30:651-655.