Aerosol from Tobacco Heating System 2.2 has reduced impact on mouse heart gene expression compared with cigarette smoke

Food and Chemical Toxicology

Volumn 101, Issue , 2017, Pages 157-167

  Szostak, Justyna ^a   Boué, Stéphanie ^a   Talikka, Marja ^a   Guedj, Emmanuel ^a   Martin, Florian ^a   Phillips, Blaine ^a   Ivanov, Nikolai V ^a   Peitsch, Manuel C ^a   Hoeng, Julia ^a  

^a PHILIP MORRIS PRODUCTS S A   (Switzerland)

Author keywords

Apoe mice; Cardiac muscle; Cigarette smoke; Contraction; Heart; Inflammation

Indexed keywords

ALPHA ACTININ 4; BETA ACTIN; CIGARETTE SMOKE; FILAMIN; FILAMIN C; TOBACCO SMOKE; UNCLASSIFIED DRUG; AEROSOL; APOLIPOPROTEIN E; BIOLOGICAL MARKER; SMOKE;

AEROSOL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOTOXICITY; COHORT ANALYSIS; CONTROLLED STUDY; DOWN REGULATION; ENVIRONMENTAL EXPOSURE; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; HEART CONTRACTION; HEART TISSUE; INFLAMMATION; MOUSE; NONHUMAN; TOBACCO; TOBACCO HEATING SYSTEM 2.2; TRANSCRIPTOMICS; ADMINISTRATION AND DOSAGE; ADVERSE EFFECTS; ANALYSIS; ANIMAL; CARDIOVASCULAR DISEASES; DRUG EFFECTS; EXPOSURE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; HEART; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SMOKE; TOXICITY;

AEROSOLS; ANIMALS; APOLIPOPROTEINS E; BIOMARKERS; CARDIOVASCULAR DISEASES; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HEART; INHALATION EXPOSURE; MICE; MICE, KNOCKOUT; SMOKE; TOBACCO; TOBACCO PRODUCTS;

EID: 85010703428     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2017.01.013     Document Type: Article

References (66)

1. Ackermann, M., Strimmer, K., A general modular framework for gene set enrichment analysis. BMC Bioinforma., 10, 2009, 47.
2. Akbarzadeh, M.A., Yazdani, S., Ghaidari, M.E., et al. Acute effects of smoking on QT dispersion in healthy males. ARYA Atheroscler. 10 (2014), 89–93.
3. Al-Arifi, M.N., Maayah, Z.H., Alshamrani, A.A., Korashy, H.M., Impact of cigarette smoke exposure on the expression of cardiac hypertrophic genes, cytochrome P450 enzymes, and oxidative stress markers in rats. J. Toxicol. Sci. 37 (2012), 1083–1090.
4. Ambrose, J.A., Barua, R.S., The pathophysiology of cigarette smoking and cardiovascular disease: an update. J. Am. Coll. Cardiol. 43 (2004), 1731–1737.
5. Barth, A.S., Kuner, R., Buness, A., et al. Identification of a common gene expression signature in dilated cardiomyopathy across independent microarray studies. J. Am. Coll. Cardiol. 48 (2006), 1610–1617.
6. Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N., Golani, I., Controlling the false discovery rate in behavior genetics research. Behav. brain Res. 125 (2001), 279–284.
7. Boda, U., Vadapalli, S., Calambur, N., Nallari, P., Novel mutations in beta-myosin heavy chain, actin and troponin-I genes associated with dilated cardiomyopathy in Indian population. J. Genet. 88 (2009), 373–377.
8. Boue, S., De Leon, H., Schlage, W.K., et al. Cigarette smoke induces molecular responses in respiratory tissues of ApoE(-/-) mice that are progressively deactivated upon cessation. Toxicology 314 (2013), 112–124.
9. Brusko, T.M., Wasserfall, C.H., Agarwal, A., Kapturczak, M.H., Atkinson, M.A., An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells. J. Immunol. 174 (2005), 5181–5186.
10. Bye, A., Sorhaug, S., Ceci, M., et al. Carbon monoxide levels experienced by heavy smokers impair aerobic capacity and cardiac contractility and induce pathological hypertrophy. Inhal. Toxicol. 20 (2008), 635–646.
11. Chan, Y., Tong, H.Q., Beggs, A.H., Kunkel, L.M., Human skeletal muscle-specific alpha-actinin-2 and -3 isoforms form homodimers and heterodimers in vitro and in vivo. Biochem. biophysical Res. Commun. 248 (1998), 134–139.
12. Charlesworth, J.C., Curran, J.E., Johnson, M.P., et al. Transcriptomic epidemiology of smoking: the effect of smoking on gene expression in lymphocytes. BMC Med. genomics, 3, 2010, 29.
13. Dennis, G. Jr., Sherman, B.T., Hosack, D.A., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol., 4, 2003, P3.
14. Dickstein, K., Cohen-Solal, A., Filippatos, G., et al. ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: the task force for the diagnosis and treatment of acute and chronic heart failure 2008 of the european society of cardiology. Developed in collaboration with the heart failure association of the ESC (HFA) and endorsed by the european society of intensive Care medicine (ESICM). Eur. heart J. 29 (2008), 2388–2442.
15. Dobrin, J.S., Lebeche, D., Diabetic cardiomyopathy: signaling defects and therapeutic approaches. Expert Rev. Cardiovasc. Ther. 8 (2010), 373–391.
16. Douglas, G., Bendall, J.K., Crabtree, M.J., et al. Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE(-)/(-) mice. Cardiovasc. Res. 94 (2012), 20–29.
17. Elamin, A., Titz, B., Dijon, S., et al. Quantitative proteomics analysis using 2D-PAGE to investigate the effects of cigarette smoke and aerosol of a prototypic modified risk tobacco product on the lung proteome in C57BL/6 mice. J. Proteomics 145 (11 August 2016), 237–245.
18. Gautier, L., Cope, L., Bolstad, B.M., Irizarry, R.A., affy–analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20 (2004), 307–315.
19. Gitlin, J.M., Loftin, C.D., Cyclooxygenase-2 inhibition increases lipopolysaccharide-induced atherosclerosis in mice. Cardiovasc. Res. 81 (2009), 400–407.
20. Gordon, J.W., Shaw, J.A., Kirshenbaum, L.A., Multiple facets of NF-kappaB in the heart: to be or not to NF-kappaB. Circulation Res. 108 (2011), 1122–1132.
21. Gray, S.P., Di Marco, E., Kennedy, K., et al. Reactive oxygen species can provide atheroprotection via NOX4-dependent inhibition of inflammation and vascular remodeling. Arteriosclerosis, thrombosis, Vasc. Biol. 36 (2016), 295–307.
22. Guo, J., Jie, W., Kuang, D., et al. Ischaemia/reperfusion induced cardiac stem cell homing to the injured myocardium by stimulating stem cell factor expression via NF-kappaB pathway. Int. J. Exp. pathology 90 (2009), 355–364.
23. Hbejan, K., Smoking effect on ischemic heart disease in young patients. Heart views official J. Gulf Heart Assoc. 12 (2011), 1–6.
24. He, J., Conklin, M.W., Foell, J.D., et al. Reduction in density of transverse tubules and L-type Ca(2+) channels in canine tachycardia-induced heart failure. Cardiovasc. Res. 49 (2001), 298–307.
25. Hechler, B., Freund, M., Ravanat, C., Magnenat, S., Cazenave, J.P., Gachet, C., Reduced atherosclerotic lesions in P2Y1/apolipoprotein E double-knockout mice: the contribution of non-hematopoietic-derived P2Y1 receptors. Circulation 118 (2008), 754–763.
26. Hu, N., Han, X., Lane, E.K., Gao, F., Zhang, Y., Ren, J., Cardiac-specific overexpression of metallothionein rescues against cigarette smoking exposure-induced myocardial contractile and mitochondrial damage. PLoS One, 8, 2013, e57151.
27. Huang, D.W., Sherman, B.T., Tan, Q., et al. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol., 8, 2007, R183.
28. Kamisago, M., Sharma, S.D., DePalma, S.R., et al. Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N. Engl. J. Med. 343 (2000), 1688–1696.
29. Kanehisa, M., Goto, S., Sato, Y., Kawashima, M., Furumichi, M., Tanabe, M., Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic acids Res. 42 (2014), D199–D205.
30. Klocke, R., Tian, W., Kuhlmann, M.T., Nikol, S., Surgical animal models of heart failure related to coronary heart disease. Cardiovasc. Res. 74 (2007), 29–38.
31. Kramer, A., Green, J., Pollard, J. Jr., Tugendreich, S., Causal analysis approaches in ingenuity pathway analysis. Bioinformatics 30 (2014), 523–530.
32. Kyaw, T., Winship, A., Tay, C., et al. Cytotoxic and proinflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoE-deficient mice. Circulation 127 (2013), 1028–1039.
33. Lough, J., Cardiomyopathy produced by cigarette smoke. Ultrastructural observations in Guinea pigs. Archives pathology laboratory Med. 102 (1978), 377–380.
34. Maier, H.J., Schips, T.G., Wietelmann, A., et al. Cardiomyocyte-specific IkappaB kinase (IKK)/NF-kappaB activation induces reversible inflammatory cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 11794–11799.
35. McCall, M.N., Bolstad, B.M., Irizarry, R.A., Frozen robust multiarray analysis (fRMA). Biostatistics 11 (2010), 242–253.
36. Meurs, I., Calpe-Berdiel, L., Habets, K.L., et al. Effects of deletion of macrophage ABCA7 on lipid metabolism and the development of atherosclerosis in the presence and absence of ABCA1. PLoS One, 7, 2012, e30984.
37. Misra, A., Haudek, S.B., Knuefermann, P., et al. Nuclear factor-kappaB protects the adult cardiac myocyte against ischemia-induced apoptosis in a murine model of acute myocardial infarction. Circulation 108 (2003), 3075–3078.
38. Mozaffarian, D., Benjamin, E.J., Go, A.S., et al. Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation 131 (2015), e29–322.
39. Mustapha, S., Kirshner, A., De Moissac, D., Kirshenbaum, L.A., A direct requirement of nuclear factor-kappa B for suppression of apoptosis in ventricular myocytes. American journal of physiology. Heart circulatory physiology 279 (2000), H939–H945.
40. Nakai, Y., Iwabuchi, K., Fujii, S., et al. Natural killer T cells accelerate atherogenesis in mice. Blood 104 (2004), 2051–2059.
41. Office of the Surgeon General U. S. (2010) Centers for Disease Control and Prevention (US), National Center for Chronic Disease Prevention and Health Promotion (US), Office on Smoking and Health (US), How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease: A Report of the Surgeon General., 2010, Centers for Disease Control and Prevention (US), Atlanta GA http://stacks.cdc.gov/view/cdc/6067/cdc_6067_DS1.pdf (Accessed 1 December 2015), Atlanta (GA).
42. Otterbein, L.E., Bach, F.H., Alam, J., et al. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6 (2000), 422–428.
43. Patten, R.D., Hall-Porter, M.R., Small animal models of heart failure: development of novel therapies, past and present. Circ. Heart Fail. 2 (2009), 138–144.
44. Phillips, B., Veljkovic, E., Boue, S., et al. An 8-month systems toxicology inhalation/cessation study in Apoe-/- mice to investigate cardiovascular and respiratory exposure effects of a candidate modified risk tobacco product, THS 2.2, compared with conventional cigarettes. Toxicol. Sci. official J. Soc. Toxicol. 149 (2016), 411–432.
45. Phillips, B., Veljkovic, E., Peck, M.J., et al. 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 Chem. Toxicol. 80 (2015), 328–345.
46. Rahman, M.M., Laher, I., Structural and functional alteration of blood vessels caused by cigarette smoking: an overview of molecular mechanisms. Curr. Vasc. Pharmacol. 5 (2007), 276–292.
47. Rodgman, A., Perfetti, T., The Composition of Cigarette Smoke: a Catalogue of the Polycyclic Aromatic Hydrocarbons. Beiträge zur Tabakforschung. Contributions Tob. Res. 22:Issue 1 (2014), 13–69.
48. Romero, M., Leon-Gomez, E., Lobysheva, I., et al. Effects of BM-573 on endothelial dependent relaxation and increased blood pressure at early stages of atherosclerosis. PLoS One, 11, 2016, e0152579.
49. Sandhu, R.K., Jimenez, M.C., Chiuve, S.E., et al. Smoking, smoking cessation, and risk of sudden cardiac death in women. Circulation. Arrhythmia Electrophysiol. 5 (2012), 1091–1097.
50. Schaller, J.P., Keller, D., Poget, L., et al. Evaluation of the Tobacco Heating System 2.2. Part 2: Chemical Composition, Genotoxicity, Cytotoxicity, and Physical Properties of the Aerosol. 2016, Regulatory toxicology and pharmacology: RTP.
51. Schleef, R.R., Vanscheeuwijck, P.M., Schlage, W.K., Borzelleca, J.F., Coggins, C.R.E., Haussmann, H.-J., Animal models for the three major cigarette-smoke induced disease. Salem, H., Katz, S.A., (eds.) Inhalation Toxicology, second ed., 2006, CRC Press 9781420037302.
52. Sequeira, V., Nijenkamp, L.L., Regan, J.A., van der Velden, J., The physiological role of cardiac cytoskeleton and its alterations in heart failure. Biochimica Biophysica Acta (BBA)-Biomembranes 1838 (2014), 700–722.
53. Smyth, G.K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, 2004 Article3.
54. Stevenson, C.S., Birrell, M.A., Moving towards a new generation of animal models for asthma and COPD with improved clinical relevance. Pharmacol. Ther. 130 (2011), 93–105.
55. Stolle, K., Berges, A., Lietz, M., Lebrun, S., Wallerath, T., Cigarette smoke enhances abdominal aortic aneurysm formation in angiotensin II-treated apolipoprotein E-deficient mice. Toxicol. Lett. 199 (2010), 403–409.
56. Talukder, M.H., Johnson, W.M., Varadharaj, S., et al. Chronic cigarette smoking causes hypertension, increased oxidative stress, impaired NO bioavailability, endothelial dysfunction, and cardiac remodeling in mice. Am. J. Physiology-Heart Circulatory Physiology 300 (2011), H388–H396.
57. Titz, B., Sewer, A., Schneider, T., et al. Alterations in the sputum proteome and transcriptome in smokers and early-stage COPD subjects. J. proteomics 128 (2015), 306–320.
58. Varemo, L., Nielsen, J., Nookaew, I., Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic acids Res. 41 (2013), 4378–4391.
59. Wang, Q., Hu, L., Hu, Y., et al. Carbon monoxide-saturated hemoglobin-based oxygen carriers attenuate high-altitude-induced cardiac injury by amelioration of the inflammation response and mitochondrial oxidative damage. Cardiology 136 (2016), 180–191.
60. Woodiwiss, A.J., Tsotetsi, O.J., Sprott, S., et al. Reduction in myocardial collagen cross-linking parallels left ventricular dilatation in rat models of systolic chamber dysfunction. Circulation 103 (2001), 155–160.
61. Wright, J.L., Cosio, M., Churg, A., Animal models of chronic obstructive pulmonary disease. Am. J. physiology. Lung Cell. Mol. physiology 295 (2008), L1–L15.
62. Zhang, L., Zhao, J., Su, L., et al. D609 inhibits progression of preexisting atheroma and promotes lesion stability in apolipoprotein e-/- mice: a role of phosphatidylcholine-specific phospholipase in atherosclerosis. Arteriosclerosis, thrombosis, Vasc. Biol. 30 (2010), 411–418.
63. Zhu, B., Sun, Y., Sievers, R.E., et al. L-arginine decreases infarct size in rats exposed to environmental tobacco smoke. Am. heart J. 132 (1996), 91–100.
64. Zhu, B.Q., Sun, Y.P., Sievers, R.E., Glantz, S.A., Parmley, W.W., Wolfe, C.L., Exposure to environmental tobacco smoke increases myocardial infarct size in rats. Circulation 89 (1994), 1282–1290.
65. Zhu, B.Q., Sun, Y.P., Sudhir, K., et al. Effects of second-hand smoke and gender on infarct size of young rats exposed in utero and in the neonatal to adolescent period. J. Am. Coll. Cardiol. 30 (1997), 1878–1885.
66. Zornoff, L.A., Matsubara, L.S., Matsubara, B.B., et al. Beta-carotene supplementation attenuates cardiac remodeling induced by one-month tobacco-smoke exposure in rats. Toxicol. Sci. official J. Soc. Toxicol. 90 (2006), 259–266.