Chronic intermittent electronic cigarette exposure induces cardiac dysfunction and atherosclerosis in apolipoprotein-E knockout mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 317, Issue 2, 2019, Pages H445-H459

  Espinoza Derout, Jorge ^a   Hasan, Kamrul M ^a   Shao, Xuesi M ^a,b   Jordan, Maria C ^b   Sims, Carl ^a   Lee, Desean L ^a   Sinha, Satyesh ^a,b   Simmons, Zena ^a   Mtume, Norma ^a   Liu, Yanjun ^a,b   Roos, Kenneth P ^b   Sinha Hikim, Amiya P ^a,b   Friedman, Theodore C ^a,b  

^a CHARLES R DREW UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atherosclerosis; Cardiomyopathy; Cardiovascular disease; Inflammation; Myocardial biology

Indexed keywords

MITOCHONDRIAL DNA; NICOTINE; NICOTINIC AGENT; REACTIVE OXYGEN METABOLITE; TRANSCRIPTOME; COTININE; MALONALDEHYDE; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTIC ROOT; APOLIPOPROTEIN E KNOCKOUT MOUSE; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CARDIAC MUSCLE CELL; CARDIOMYOPATHY; CARDIOVASCULAR RISK; CIRCADIAN RHYTHM; CONTROLLED STUDY; DNA DAMAGE; GENE MUTATION; HEART DISEASE; HEART EJECTION FRACTION; HEART LEFT VENTRICLE EJECTION TIME; INFLAMMATION; LONG TERM EXPOSURE; MALE; METABOLISM; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; TRANSMISSION ELECTRON MICROSCOPY; ADVERSE EVENT; ANIMAL; C57BL MOUSE; DISEASE MODEL; ELECTRONIC CIGARETTE; EXPOSURE; GENETICS; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; ULTRASTRUCTURE; VAPING; AEROSOL; C57BL 6 MOUSE; CARDIOVASCULAR EFFECT; CARDIOVASCULAR FUNCTION; CELL ULTRASTRUCTURE; CONCENTRATION (PARAMETER); ECHOCARDIOGRAPHY; FRACTIONAL SHORTENING; GENE FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION;

ANIMALS; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; DNA, MITOCHONDRIAL; ELECTRONIC NICOTINE DELIVERY SYSTEMS; INHALATION EXPOSURE; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT, APOE; MUTATION; MYOCYTES, CARDIAC; NICOTINE; NICOTINIC AGONISTS; OXIDATIVE STRESS; PLAQUE, ATHEROSCLEROTIC; REACTIVE OXYGEN SPECIES; STROKE VOLUME; TRANSCRIPTOME; VAPING; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT;

EID: 85069907431     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00738.2018     Document Type: Article

References (84)

1. Aickin M, Gensler H. Adjusting for multiple testing when reporting research results: the Bonferroni vs Holm methods. Am J Public Health 86: 726 –728, 1996. doi:10.2105/AJPH.86.5.726.
2. Akoumianakis I, Antoniades C. The interplay between adipose tissue and the cardiovascular system: is fat always bad? Cardiovasc Res 113: 999 –1008, 2017. doi:10.1093/cvr/cvx111.
3. Alzahrani T, Pena I, Temesgen N, Glantz SA. Association between electronic cigarette use and myocardial infarction. Am J Prev Med 55: 455–461, 2018. doi:10.1016/j.amepre.2018.05.004.
4. Antoniewicz L, Bosson JA, Kuhl J, Abdel-Halim SM, Kiessling A, Mobarrez F, Lundbäck M. Electronic cigarettes increase endothelial progenitor cells in the blood of healthy volunteers. Atherosclerosis 255: 179 –185, 2016. doi:10.1016/j.atherosclerosis.2016.09.064.
5. Baglione J, Smith JD. Quantitative assay for mouse atherosclerosis in the aortic root. Methods Mol Med 129: 83–95, 2006. doi:10.1385/1-59745-213-0:83.
6. Ballinger SW, Bouder TG, Davis GS, Judice SA, Nicklas JA, Albertini RJ. Mitochondrial genome damage associated with cigarette smoking. Cancer Res 56: 5692–5697, 1996.
7. Barrera-Vilarmau S, Obregón P, de Alba E. Intrinsic order and disorder in the bcl-2 member harakiri: insights into its proapoptotic activity. PLoS One 6: e21413, 2011. doi:10.1371/journal.pone.0021413.
8. Benowitz NL, Burbank AD. Cardiovascular toxicity of nicotine: Implications for electronic cigarette use. Trends Cardiovasc Med 26: 515–523, 2016. doi:10.1016/j.tcm.2016.03.001.
9. Benowitz NL, Fraiman JB. Cardiovascular effects of electronic cigarettes. Nat Rev Cardiol 14: 447–456, 2017. doi:10.1038/nrcardio.2017.36.
10. Benowitz NL, Gourlay SG. Cardiovascular toxicity of nicotine: implications for nicotine replacement therapy. J Am Coll Cardiol 29: 1422–1431, 1997. doi:10.1016/S0735-1097(97)00079-X.
11. Benowitz NL, Zevin S, Jacob P 3rd. Sources of variability in nicotine and cotinine levels with use of nicotine nasal spray, transdermal nicotine, and cigarette smoking. Br J Clin Pharmacol 43: 259 –267, 1997. doi:10. 1111/j.1365-2125.1997.00566.x.
12. Bhatnagar A, Whitsel LP, Ribisl KM, Bullen C, Chaloupka F, Piano MR, Robertson RM, McAuley T, Goff D, Benowitz N; American Heart Association Advocacy Coordinating Committee, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology, and Council on Quality of Care and Outcomes Research. Electronic cigarettes: a policy statement from the American Heart Association. Circulation 130: 1418 –1436, 2014. doi:10.1161/CIR.0000000000000107.
13. Bitzer ZT, Goel R, Reilly SM, Foulds J, Muscat J, Elias RJ, Richie JP Jr. Effects of solvent and temperature on free radical formation in electronic cigarette aerosols. Chem Res Toxicol 31: 4 –12, 2018. doi:10. 1021/acs.chemrestox.7b00116.
14. Boden G. Obesity, insulin resistance and free fatty acids. Curr Opin Endocrinol Diabetes Obes 18: 139 –143, 2011. doi:10.1097/MED. 0b013e3283444b09.
15. Bonney S, Kominsky D, Brodsky K, Eltzschig H, Walker L, Eckle T. Cardiac Per2 functions as novel link between fatty acid metabolism and myocardial inflammation during ischemia and reperfusion injury of the heart. PLoS One 8: e71493, 2013. doi:10.1371/journal.pone.0071493.
16. Brookheart RT, Michel CI, Schaffer JE. As a matter of fat. Cell Metab 10: 9 –12, 2009. doi:10.1016/j.cmet.2009.03.011.
17. Chong CR, Clarke K, Levelt E. Metabolic remodeling in diabetic cardiomyopathy. Cardiovasc Res 113: 422–430, 2017. doi:10.1093/cvr/cvx018.
18. Chow J, Rahman J, Achermann JC, Dattani MT, Rahman S. Mitochondrial disease and endocrine dysfunction. Nat Rev Endocrinol 13: 92–104, 2017. doi:10.1038/nrendo.2016.151.
19. Colombo ES, Davis J, Makvandi M, Aragon M, Lucas SN, Paffett ML, Campen MJ. Effects of nicotine on cardiovascular remodeling in a mouse model of systemic hypertension. Cardiovasc Toxicol 13: 364 –369, 2013. doi:10.1007/s12012-013-9217-z.
20. Daniele G, Eldor R, Merovci A, Clarke GD, Xiong J, Tripathy D, Taranova A, Abdul-Ghani M, DeFronzo RA. Chronic reduction of plasma free fatty acid improves mitochondrial function and whole-body insulin sensitivity in obese and type 2 diabetic individuals. Diabetes 63: 2812–2820, 2014. doi:10.2337/db13-1130.
21. Durgan DJ, Young ME. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 106: 647–658, 2010. doi:10.1161/CIRCRESAHA.109.209957.
22. Fowler PA, Childs AJ, Courant F, MacKenzie A, Rhind SM, Antignac JP, Le Bizec B, Filis P, Evans F, Flannigan S, Maheshwari A, Bhattacharya S, Monteiro A, Anderson RA, O’Shaughnessy PJ. In utero exposure to cigarette smoke dysregulates human fetal ovarian developmental signalling. Hum Reprod 29: 1471–1489, 2014. doi:10. 1093/humrep/deu117.
23. Friedman TC, Sinha-Hikim I, Parveen M, Najjar SM, Liu Y, Mangubat M, Shin CS, Lyzlov A, Ivey R, Shaheen M, French SW, Sinha-Hikim AP. Additive effects of nicotine and high-fat diet on hepatic steatosis in male mice. Endocrinology 153: 5809 –5820, 2012. doi:10.1210/en.2012-1750.
24. Ge F, Hu C, Hyodo E, Arai K, Zhou S, Lobdell H IV, Walewski JL, Homma S, Berk PD. Cardiomyocyte triglyceride accumulation and reduced ventricular function in mice with obesity reflect increased long chain fatty acid uptake and de novo fatty acid synthesis. J Obes 2012: 1–12, 2012. doi:10.1155/2012/205648.
25. Getz GS, Reardon CA. Animal models of atherosclerosis. Arterioscler Thromb Vasc Biol 32: 1104 –1115, 2012. doi:10.1161/ATVBAHA.111. 237693.
26. Ghosh A, Gao L, Thakur A, Siu PM, Lai CW. Role of free fatty acids in endothelial dysfunction. J Biomed Sci 24: 50, 2017. doi:10.1186/s12929-017-0357-5.
27. Glantz SA, Bareham DW. E-cigarettes: use, effects on smoking, risks, and policy implications. Annu Rev Public Health 39: 215–235, 2018. doi:10.1146/annurev-publhealth-040617-013757.
28. Gonçalves N, Silva AF, Rodrigues PG, Correia E, Moura C, Eloy C, Roncon-Albuquerque R Jr, Falcão-Pires I, Leite-Moreira AF. Early cardiac changes induced by a hypercaloric Western-type diet in “subclin-ical” obesity. Am J Physiol Heart Circ Physiol 310: H655–H666, 2016. doi:10.1152/ajpheart.00684.2015.
29. Gooley JJ, Chua EC. Diurnal regulation of lipid metabolism and applications of circadian lipidomics. J Genet Genomics 41: 231–250, 2014. doi:10.1016/j.jgg.2014.04.001.
30. Hajek P, Phillips-Waller A, Przulj D, Pesola F, Myers Smith K, Bisal N, Li J, Parrott S, Sasieni P, Dawkins L, Ross L, Goniewicz M, Wu Q, McRobbie HJ. A randomized trial of e-cigarettes versus nicotine-replace-ment therapy. N Engl J Med 380: 629 –637, 2019. doi:10.1056/NEJMoa1808779.
31. Herder C, Schamarek I, Nowotny B, Carstensen-Kirberg M, Straßburger K, Nowotny P, Kannenberg JM, Strom A, Püttgen S, Müssig K, Szendroedi J, Roden M, Ziegler D; German Diabetes Study Group. Inflammatory markers are associated with cardiac autonomic dysfunction in recent-onset type 2 diabetes. Heart 103: 63–70, 2017. doi:10.1136/heartjnl-2015-309181.
32. Herst PM, Rowe MR, Carson GM, Berridge MV. Functional mitochondria in health and disease. Front Endocrinol (Lausanne) 8: 296, 2017. doi:10.3389/fendo.2017.00296.
33. Hirabara SM, Curi R, Maechler P. Saturated fatty acid-induced insulin resistance is associated with mitochondrial dysfunction in skeletal muscle cells. J Cell Physiol 222: 187–194, 2010. doi:10.1002/jcp.21936.
34. Ho E, Karimi Galougahi K, Liu CC, Bhindi R, Figtree GA. Biological markers of oxidative stress: Applications to cardiovascular research and practice. Redox Biol 1: 483–491, 2013. doi:10.1016/j.redox.2013.07.006.
35. Hoeks J, van Herpen NA, Mensink M, Moonen-Kornips E, van Beurden D, Hesselink MK, Schrauwen P. Prolonged fasting identifies skeletal muscle mitochondrial dysfunction as consequence rather than cause of human insulin resistance. Diabetes 59: 2117–2125, 2010. doi:10. 2337/db10-0519.
36. Hukkanen J, Jacob P 3rd, Benowitz NL. Metabolism and disposition kinetics of nicotine. Pharmacol Rev 57: 79 –115, 2005. doi:10.1124/pr.57.1.3.
37. Husari A, Shihadeh A, Talih S, Hashem Y, El Sabban M, Zaatari G. Acute exposure to electronic and combustible cigarette aerosols: effects in an animal model and in human alveolar cells. Nicotine Tob Res 18: 613–619, 2016. doi:10.1093/ntr/ntv169.
38. L. EMBO J 16: 1686 – 1694, 1997. doi:10.1093/emboj/16.7.1686.
39. Jacob P 3rd, Yu L, Duan M, Ramos L, Yturralde O, Benowitz NL. Determination of the nicotine metabolites cotinine and trans-3=-hydroxy-cotinine in biologic fluids of smokers and non-smokers using liquid chromatography-tandem mass spectrometry: biomarkers for tobacco smoke exposure and for phenotyping cytochrome P450 2A6 activity. J Chromatogr B Analyt Technol Biomed Life Sci 879: 267–276, 2011. doi:10.1016/j.jchromb.2010.12.012.
40. Koskivirta I, Kassiri Z, Rahkonen O, Kiviranta R, Oudit GY, McKee TD, Kytö V, Saraste A, Jokinen E, Liu PP, Vuorio E, Khokha R. Mice with tissue inhibitor of metalloproteinases 4 (Timp4) deletion succumb to induced myocardial infarction but not to cardiac pressure overload. J Biol Chem 285: 24487–24493, 2010. doi:10.1074/jbc.M110.136820.
41. Kristjansson AL, Mann MJ, Smith ML. Prevalence of substance use among middle school-aged e-cigarette users compared with cigarette smokers, nonusers, and dual users: Implications for primary prevention. Subst Abus 38: 473–476, 2017. doi:10.1080/08897077.2017.1343218.
42. La Carrubba S, Todaro MC, Zito C, Antonini-Canterin F, Monte IP, Caso P, Colonna P, de Gregorio C, Pezzano A, Benedetto F, Salvo GD, Carerj S, Bello VD. Asymptomatic left ventricular dysfunction and metabolic syndrome: results from an Italian multicenter study. J Cardiovasc Echogr 23: 96 –101, 2013. doi:10.4103/2211-4122.127410.
43. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359, 2012. doi:10.1038/nmeth.1923.
44. Lee J, Cooke JP. The role of nicotine in the pathogenesis of atherosclerosis. Atherosclerosis 215: 281–283, 2011. doi:10.1016/j.atherosclerosis. 2011.01.003.
45. Lee SR, Kim N, Noh YH, Xu Z, Ko KS, Rhee BD, Han J. Mitochondrial DNA, mitochondrial dysfunction, and cardiac manifestations. Front Biosci 22: 1177–1194, 2017. doi:10.2741/4541.
46. Lee Y, Gustafsson AB. Role of apoptosis in cardiovascular disease. Apoptosis 14: 536 –548, 2009. doi:10.1007/s10495-008-0302-x.
47. Lerner CA, Sundar IK, Yao H, Gerloff J, Ossip DJ, McIntosh S, Robinson R, Rahman I. 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, 2015. doi:10.1371/journal.pone.0116732.
48. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323, 2011. doi:10.1186/1471-2105-12-323.
49. Li L, Fan D, Wang C, Wang JY, Cui XB, Wu D, Zhou Y, Wu LL. Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF-β1 pathways in cardiac fibroblasts. Cardiovasc Res 91: 80 –89, 2011. doi:10.1093/cvr/cvr067.
50. Lo Sasso G, Schlage WK, Boué S, Veljkovic E, Peitsch MC, Hoeng J. The Apoe(-/-) mouse model: a suitable model to study cardiovascular and respiratory diseases in the context of cigarette smoke exposure and harm reduction. J Transl Med 14: 146, 2016. doi:10.1186/s12967-016-0901-1.s
51. Lukyanenko V, Chikando A, Lederer WJ. Mitochondria in cardiomyocyte Ca2+ signaling. Int J Biochem Cell Biol 41: 1957–1971, 2009. doi:10.1016/j.biocel.2009.03.011.
52. Madrigal-Matute J, Fernandez-Laso V, Sastre C, Llamas-Granda P, Egido J, Martin-Ventura JL, Zalba G, Blanco-Colio LM. TWEAK/ Fn14 interaction promotes oxidative stress through NADPH oxidase activation in macrophages. Cardiovasc Res 108: 139 –147, 2015. doi:10. 1093/cvr/cvv204.
53. Mak KM, Png CY, Lee DJ. Type V collagen in health, disease, and fibrosis. Anat Rec (Hoboken) 299: 613–629, 2016. doi:10.1002/ar.23330.
54. Mandl A, Huong Pham L, Toth K, Zambetti G, Erhardt P. Puma deletion delays cardiac dysfunction in murine heart failure models through attenuation of apoptosis. Circulation 124: 31–39, 2011. doi:10.1161/CIRCULATIONAHA.110.988303.
55. Mangubat M, Lutfy K, Lee ML, Pulido L, Stout D, Davis R, Shin CS, Shahbazian M, Seasholtz S, Sinha-Hikim A, Sinha-Hikim I, O’Dell LE, Lyzlov A, Liu Y, Friedman TC. Effect of nicotine on body composition in mice. J Endocrinol 212: 317–326, 2012. doi:10.1530/JOE-11-0350.
56. Miedema MD, Maziarz M, Biggs ML, Zieman SJ, Kizer JR, Ix JH, Mozaffarian D, Tracy RP, Psaty BM, Siscovick DS, Mukamal KJ, Djousse L. Plasma-free fatty acids, fatty acid-binding protein 4, and mortality in older adults (from the Cardiovascular Health Study). Am J Cardiol 114: 843–848, 2014. doi:10.1016/j.amjcard.2014.06.012.
57. Mitchell T, Johnson MS, Ouyang X, Chacko BK, Mitra K, Lei X, Gai Y, Moore DR, Barnes S, Zhang J, Koizumi A, Ramanadham S, Darley-Usmar VM. Dysfunctional mitochondrial bioenergetics and oxidative stress in Akita(+/Ins2)-derived β-cells. Am J Physiol Endocrinol Metab 305: E585–E599, 2013. doi:10.1152/ajpendo.00093.2013.
58. Miyazaki M, Esser KA. REDD2 is enriched in skeletal muscle and inhibits mTOR signaling in response to leucine and stretch. Am J Physiol Cell Physiol 296: C583–C592, 2009. doi:10.1152/ajpcell.00464.2008.
59. Morton LF, Barnes MJ. Collagen polymorphism in the normal and diseased blood vessel wall. Investigation of collagens types I, III and V. Atherosclerosis 42: 41–51, 1982. doi:10.1016/0021-9150(82)90124-1.
60. Nelluri B, Murphy K, Mookadam F, Mookadam M. The current literature regarding the cardiovascular effects of electronic cigarettes. Future Cardiol 12: 167–179, 2016. doi:10.2217/fca.15.83.
61. Nojiri H, Shimizu T, Funakoshi M, Yamaguchi O, Zhou H, Kawakami S, Ohta Y, Sami M, Tachibana T, Ishikawa H, Kurosawa H, Kahn RC, Otsu K, Shirasawa T. Oxidative stress causes heart failure with impaired mitochondrial respiration. J Biol Chem 281: 33789 –33801, 2006. doi:10.1074/jbc.M602118200.
62. OECD. Guidance Document on Acute Inhalation Toxicity Testing Vol. Series on Testing and Assessment. Series on Testing and Assesment 39: 1–71, 2009.
63. Olfert IM, DeVallance E, Hoskinson H, Branyan KW, Clayton S, Pitzer CR, Sullivan DP, Breit MJ, Wu ZX, Klinkhachorn P, Mandler WK, Erdreich BH, Ducatman BS, Bryner RW, Dasgupta P, Chantler PD. Chronic exposure to electronic cigarette (E-cig) results in impaired cardiovascular function in mice. J Appl Physiol 124: 573–582, 2018. doi:10.1152/japplphysiol.00713.2017.
64. Patenge N. Quantification of DNA damage and repair in mitochondrial, nuclear, and bacterial genomes by real-time PCR. Methods Mol Biol 1644: 159 –166, 2017. doi:10.1007/978-1-4939-7187-9_14.
65. Pendse AA, Arbones-Mainar JM, Johnson LA, Altenburg MK, Maeda N. Apolipoprotein E knock-out and knock-in mice: atherosclerosis, metabolic syndrome, and beyond. J Lipid Res 50, Suppl: S178 –S182, 2009. doi:10.1194/jlr.R800070-JLR200.
66. Rapti K, Diokmetzidou A, Kloukina I, Milner DJ, Varela A, Davos CH, Capetanaki Y. Opposite effects of catalase and MnSOD ectopic expression on stress induced defects and mortality in the desmin deficient cardiomyopathy model. Free Radic Biol Med 110: 206 –218, 2017. doi: 10.1016/j.freeradbiomed.2017.06.010.
67. Redmann M, Benavides GA, Wani WY, Berryhill TF, Ouyang X, Johnson MS, Ravi S, Mitra K, Barnes S, Darley-Usmar VM, Zhang J. Methods for assessing mitochondrial quality control mechanisms and cellular consequences in cell culture. Redox Biol 17: 59 –69, 2018. doi: 10.1016/j.redox.2018.04.005.
68. Ren MY, Sui SJ. The role of TWEAK/Fn14 in cardiac remodeling. Mol Biol Rep 39: 9971–9977, 2012. doi:10.1007/s11033-012-1867-6.
69. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139 –140, 2010. doi:10.1093/bioinformatics/btp616.
70. Roos KP, Jordan MC, Fishbein MC, Ritter MR, Friedlander M, Chang HC, Rahgozar P, Han T, Garcia AJ, Maclellan WR, Ross RS, Philipson KD. Hypertrophy and heart failure in mice overexpressing the cardiac sodium-calcium exchanger. J Card Fail 13: 318 –329, 2007. doi:10.1016/j.cardfail.2007.01.004.
71. Schönfeld P, Wojtczak L. Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radic Biol Med 45: 231–241, 2008. doi:10.1016/j.freeradbiomed.2008.04.029.
72. Schroeder AM, Wang HB, Park S, Jordan MC, Gao F, Coppola G, Fishbein MC, Roos KP, Ghiani CA, Colwell CS. Cardiac dysfunction in the BACHD mouse model of Huntington’s disease. PLoS One 11: e0147269, 2016. doi:10.1371/journal.pone.0147269.
73. Shao XM, Liu S, Lee ES, Fung D, Pei H, Liang J, Mudgway R, Zhang J, Feldman JL, Zhu Y, Louie S, Xie XS. Chronic intermittent nicotine delivery via lung alveolar region-targeted aerosol technology produces circadian pharmacokinetics in rats resembling human smokers. J Appl Physiol (1985) 125: 1555–1562, 2018. doi:10.1152/japplphysiol.00357. 2018.
74. Shao XM, Xu B, Liang J, Xie XS, Zhu Y, Feldman JL. Nicotine delivery to rats via lung alveolar region-targeted aerosol technology produces blood pharmacokinetics resembling human smoking. Nicotine Tob Res 15: 1248 –1258, 2013. doi:10.1093/ntr/nts261.
75. Sinha-Hikim I, Friedman TC, Falz M, Chalfant V, Hasan MK, Espinoza-Derout J, Lee DL, Sims C, Tran P, Mahata SK, Sinha-Hikim AP. Nicotine plus a high-fat diet triggers cardiomyocyte apoptosis. Cell Tissue Res 368: 159 –170, 2017. doi:10.1007/s00441-016-2536-1.
76. Sinha-Hikim I, Friedman TC, Shin CS, Lee D, Ivey R, Sinha-Hikim AP. Nicotine in combination with a high-fat diet causes intramyocellular mitochondrial abnormalities in male mice. Endocrinology 155: 865–872, 2014. doi:10.1210/en.2013-1795.
77. Swirski FK, Nahrendorf M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 339: 161–166, 2013. doi:10.1126/science.1230719.
78. Trtchounian A, Williams M, Talbot P. Conventional and electronic cigarettes (e-cigarettes) have different smoking characteristics. Nicotine Tob Res 12: 905–912, 2010. doi:10.1093/ntr/ntq114.
79. USEPA. Health Effects Test Guidelines OPPTS 870.1300 Acute Inhalation Toxicity. Washington, DC: Environmental Protection Agency, Prevention, Pesticides, and Toxic Substance, 1998.
80. Wang C, Chen H, Zhu W, Xu Y, Liu M, Zhu L, Yang F, Zhang L, Liu X, Zhong Z, Zhao J, Jiang J, Xiang M, Yu H, Hu X, Lu H, Wang J. Nicotine accelerates atherosclerosis in apolipoprotein E-deficient mice by activating α7 nicotinic acetylcholine receptor on mast cells. Arterioscler Thromb Vasc Biol 37: 53–65, 2017. doi:10.1161/ATVBAHA.116.307264.
81. Wang Z, Wang D, Wang Y. Cigarette smoking and adipose tissue: the emerging role in progression of atherosclerosis. Mediators Inflamm 2017: 1–11, 2017. doi:10.1155/2017/3102737.
82. Wu Y, Song P, Zhang W, Liu J, Dai X, Liu Z, Lu Q, Ouyang C, Xie Z, Zhao Z, Zhuo X, Viollet B, Foretz M, Wu J, Yuan Z, Zou MH. Activation of AMPKα2 in adipocytes is essential for nicotine-induced insulin resistance in vivo. Nat Med 21: 373–382, 2015. doi:10.1038/nm.3826.
83. Young ME, Wilson CR, Razeghi P, Guthrie PH, Taegtmeyer H. Alterations of the circadian clock in the heart by streptozotocin-induced diabetes. J Mol Cell Cardiol 34: 223–231, 2002. doi:10.1006/jmcc.2001.1504.
84. Zaragoza C, Gomez-Guerrero C, Martin-Ventura JL, Blanco-Colio L, Lavin B, Mallavia B, Tarin C, Mas S, Ortiz A, Egido J. Animal models of cardiovascular diseases. J Biomed Biotechnol 2011: 1–13, 2011. doi: 10.1155/2011/497841.