Generic placeholder image

Current Vascular Pharmacology

Editor-in-Chief

ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

Review Article

Smoking and Endothelial Dysfunction

Author(s): Saeid Golbidi, Lars Edvinsson and Ismail Laher*

Volume 18, Issue 1, 2020

Page: [1 - 11] Pages: 11

DOI: 10.2174/1573403X14666180913120015

Price: $65

Abstract

Cigarette smoking is one of the most important health concerns worldwide. Even though the rate of smoking is declining in developed countries, it is still experiencing growth in developing regions. Many studies have examined the relationship between smoking, as an established risk factor, and cardiovascular diseases. We provide an updated review of the underlying mechanisms of smoking-induced cardiovascular diseases, with a focus on the relationship between smoking and oxidative stress, particularly from the perspective of endothelial cell dysfunction. We review smoking-induced oxidative stress as a trigger for a generalized vascular inflammation associated with cytokine release, adhesion of inflammatory cells and, ultimately, disruption of endothelial integrity as a protective barrier layer. We also briefly discuss the harms related to the vaping of electronic cigarettes, which many erroneously consider as a safe alternative to smoking. We conclude that even though e-cigarette could be a helpful device during the transition period of cigarette quitting, it is by no means a safe substitute.

Keywords: Smoking, e-cigarette, oxidative stress, endothelial dysfunction, atherosclerosis, cardiovascular function.

Next »
Graphical Abstract
[1]
Hackshaw A, Morris JK, Boniface S, Tang JL, Milenković D. Low cigarette consumption and risk of coronary heart disease and stroke: Meta-analysis of 141 cohort studies in 55 study reports. BMJ 2018; 360: j855.
[2]
Johnson KC. Just one cigarette a day seriously elevates cardiovascular risk. BMJ 2018; 360: k167.
[3]
Valavanidis A, Vlachogianni T, Fiotakis K. Tobacco smoke: involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. Int J Environ Res Public Health 2009; 6(2): 445-62.
[4]
Celermajer DS, Sorensen KE, Gooch VM, et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 1992; 340(8828): 1111-5.
[5]
Zeiher AM, Schächinger V, Minners J. Long-term cigarette smoking impairs endothelium-dependent coronary arterial vasodilator function. Circulation 1995; 92(5): 1094-100.
[6]
Celermajer DS, Adams MR, Clarkson P, et al. Passive smoking and impaired endothelium-dependent arterial dilatation in healthy young adults. N Engl J Med 1996; 334(3): 150-4.
[7]
Johnson HM, Gossett LK, Piper ME, et al. Effects of smoking and smoking cessation on endothelial function: 1-year outcomes from a randomized clinical trial. J Am Coll Cardiol 2010; 55(18): 1988-95.
[8]
Heitzer T, Brockhoff C, Mayer B, et al. Tetrahydrobiopterin improves endothelium-dependent vasodilation in chronic smokers: evidence for a dysfunctional nitric oxide synthase. Circ Res 2000; 86(2): 36-41.
[9]
de Sousa MG, Yugar-Toledo JC, Rubira M, et al. Ascorbic acid improves impaired venous and arterial endothelium-dependent dilation in smokers. Acta Pharmacol Sin 2005; 26(4): 447-52.
[10]
Papamichael C, Karatzis E, Karatzi K, et al. Red wine’s antioxidants counteract acute endothelial dysfunction caused by cigarette smoking in healthy nonsmokers. Am Heart J 2004; 147(2)E5
[11]
Gould NS, Min E, Huang J, et al. Glutathione depletion accelerates cigarette smoke-induced inflammation and airspace enlargement. Toxicol Sci 2015; 147(2): 466-74.
[12]
Church DF, Pryor WA. Free-radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 1985; 64: 111-26.
[13]
Barua RS, Ambrose JA, Srivastava S, DeVoe MC, Eales-Reynolds LJ. Reactive oxygen species are involved in smoking-induced dysfunction of nitric oxide biosynthesis and upregulation of endothelial nitric oxide synthase: An in vitro demonstration in human coronary artery endothelial cells. Circulation 2003; 107(18): 2342-7.
[14]
Xu J, Xie Z, Reece R, Pimental D, Zou MH. Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: Role of NAD(P)H oxidase-derived superoxide and peroxynitrite. Arterioscler Thromb Vasc Biol 2006; 26(12): 2688-95.
[15]
Burke A, Fitzgerald GA. Oxidative stress and smoking-induced vascular injury. Prog Cardiovasc Dis 2003; 46(1): 79-90.
[16]
Michaud SE, Dussault S, Groleau J, Haddad P, Rivard A. Cigarette smoke exposure impairs VEGF-induced endothelial cell migration: Role of NO and reactive oxygen species. J Mol Cell Cardiol 2006; 41(2): 275-84.
[17]
Ambrose JA, Barua RS. The pathophysiology of cigarette smoking and cardiovascular disease: An update. J Am Coll Cardiol 2004; 43(10): 1731-7.
[18]
Pryor WA1, Stone K, Zang LY, Bermúdez E. Fractionation of aqueous cigarette tar extracts: Fractions that contain the tar radical cause DNA damage. Chem Res Toxicol 1988; 11(5): 441-8.
[19]
Raij L, DeMaster EG, Jaimes EA. Cigarette smoke-induced endothelium dysfunction: Role of superoxide anion. J Hypertens 2001; 19(5): 891-7.
[20]
Czernin J, Sun K, Brunken R, Böttcher M, Phelps M, Schelbert H. Effect of acute and long-term smoking on myocardial blood flow and flow reserve. Circulation 1995; 91(12): 2891-7.
[21]
Adams MR, Jessup W, Celermajer DS. Cigarette smoking is associated with increased human monocyte adhesion to endothelial cells: reversibility with oral L-arginine but not vitamin C. J Am Coll Cardiol 1997; 29(3): 491-7.
[22]
Czernin J, Waldherr C. Cigarette smoking and coronary blood flow. Prog Cardiovasc Dis 2003; 45(5): 395-404.
[23]
Sukhovershin RA, Yepuri G, Ghebremariam YT. Endothelium-derived nitric oxide as an antiatherogenic mechanism: Implications for therapy. Methodist DeBakey Cardiovasc J 2015; 11(3): 166-71.
[24]
Luo S, Lei H, Qin H, Xia Y. Molecular mechanisms of endothelial NO synthase uncoupling. Curr Pharm Des 2014; 20(22): 3548-53.
[25]
Campisi R, Czernin J, Schöder H, Sayre JW, Schelbert HR. L-Arginine normalizes coronary vasomotion in long-term smokers. Circulation 1999; 99(4): 491-7.
[26]
Sobczak A, Prokopowicz A, Radek M, et al. Tobacco smoking decreases plasma concentration of the emerging cardiovascular risk marker, L-homoarginine. Circ J 2014; 78(5): 1254-8.
[27]
Zhang WZ, Venardos K, Chin-Dusting J, Kaye DM. Adverse effects of cigarette smoke on NO bioavailability: Role of arginine metabolism and oxidative stress. Hypertension 2006; 48(2): 278-85.
[28]
Vásquez G, Sanhueza F, Vásquez R, et al. Role of adenosine transport in gestational diabetes-induced L-arginine transport and nitric oxide synthesis in human umbilical vein endothelium. J Physiol 2004; 560(Pt 1): 111-22.
[29]
Guzmán-Gutiérrez E, Abarzúa F, Belmar C, et al. Functional link between adenosine and insulin: A hypothesis for fetoplacental vascular endothelial dysfunction in gestational diabetes. Curr Vasc Pharmacol 2011; 9(6): 750-62.
[30]
González M, Gallardo V, Rodríguez N, et al. Insulin-stimulated L-arginine transport requires SLC7A1 gene expression and is associated with human umbilical vein relaxation. J Cell Physiol 2011; 226(11): 2916-24.
[31]
Ciaraldi TP, Morales AJ, Hickman MG, Odom-Ford R, Olefsky JM, Yen SS. Cellular insulin resistance in adipocytes from obese polycystic ovary syndrome subjects involves adenosine modulation of insulin sensitivity. J Clin Endocrinol Metab 1997; 82(5): 1421-5.
[32]
Guzmán-Gutiérrez E, Westermeier F, Salomón C, et al. Insulin-increased L-arginine transport requires A(2A) adenosine receptors activation in human umbilical vein endothelium. PLoS One 2012; 7(7)e41705
[33]
Alagbonsi AI, Salman TM, Salahdeen HM, Alada AA. Effects of adenosine and caffeine on blood glucose levels in rats. Nigerian J Exp Clin Biosci 2016; 4(2): 35-41.
[34]
Haj Mouhamed D, Ezzaher A, Neffati F, Douki W, Gaha L, Najjar MF. Effect of cigarette smoking on insulin resistance risk. Ann Cardiol Angeiol (Paris) 2016; 65(1): 21-5.
[35]
Seet RC, Loke WM, Khoo CM, et al. Acute effects of cigarette smoking on insulin resistance and arterial stiffness in young adults. Atherosclerosis 2012; 224(1): 195-200.
[36]
Morimoto A, Tatsumi Y, Deura K, Mizuno S, Ohno Y, Watanabe S. Impact of cigarette smoking on impaired insulin secretion and insulin resistance in Japanese men: The saku study. J Diabetes Investig 2013; 4(3): 274-80.
[37]
Wagner L, Laczy B, Tamaskó M, et al. Cigarette smoke-induced alterations in endothelial nitric oxide synthase phosphorylation: Role of protein kinase C. Endothelium 2007; 14(4-5): 245-55.
[38]
Tsuchiya M, Asada A, Kasahara E, Sato EF, Shindo M, Inoue M. Smoking a single cigarette rapidly reduces combined concentrations of nitrate and nitrite and concentrations of antioxidants in plasma. Circulation 2002; 105(10): 1155-7.
[39]
Adams T, Wan E, Wei Y, et al. Secondhand smoking is associated with vascular inflammation. Chest 2015; 148(1): 112-9.
[40]
Chen Y, Wang H, Luo G, Dai X. SIRT4 inhibits cigarette smoke extracts-induced mononuclear cell adhesion to human pulmonary microvascular endothelial cells via regulating NF-κB activity. Toxicol Lett 2014; 226(3): 320-7.
[41]
Du J, Zhou Y, Su X, et al. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 2011; 334(6057): 806-9.
[42]
Jiang H, Khan S, Wang Y, et al. SIRT6 regulates TNF-α secretion through hydrolysis of long-chain fatty acyl lysine. Nature 2013; 496(7443): 110-3.
[43]
Rack JG1, Morra R, Barkauskaite E, et al. Identification of a class of protein ADP-ribosylating sirtuins in microbial pathogens. Mol Cell 2015; 59(2): 309-20.
[44]
Barclay AN, Wright GJ, Brooke G, Brown MH. CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol 2002; 23(6): 285-90.
[45]
Gorczynski RM. Evidence for an immunoregulatory role of OX2 with its counter ligand (OX2L) in the regulation of transplant rejection, fetal loss, autoimmunity and tumor growth. Arch Immunol Ther Exp (Warsz) 2001; 49(4): 303-9.
[46]
Jiang L, Xu F, He W, et al. CD200Fc reduces TLR4-mediated inflammatory responses in LPS-induced rat primary microglial cells via inhibition of the NF-κB pathway. Inflamm Res 2016; 65(7): 521-32.
[47]
Xu J, Lu L, Lu J, et al. CD200Fc attenuates inflammatory responses and maintains barrier function by suppressing NF-κB pathway in cigarette smoke extract induced endothelial cells. Biomed Pharmacother 2016; 84: 714-21.
[48]
Klune JR, Dhupar R, Cardinal J, Billiar TR, Tsung A. HMGB1: endogenous danger signaling. Mol Med 2008; 14(7-8): 476-84.
[49]
Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): Nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5(4): 331-42.
[50]
Yang H, Tracey KJ. Targeting HMGB1 in inflammation. Biochim Biophys Acta 2010; 1799(1-2): 149-56.
[51]
Hou C, Zhao H, Liu L, et al. High mobility group protein B1 (HMGB1) in Asthma: Comparison of patients with chronic obstructive pulmonary disease and healthy controls. Mol Med 2011; 17(7-8): 807-15.
[52]
Ko HK, Hsu WH, Hsieh CC, Lien TC, Lee TS, Kou YR. High expression of high-mobility group box 1 in the blood and lungs is associated with the development of chronic obstructive pulmonary disease in smokers. Respirology 2014; 19(2): 253-61.
[53]
Taylor OJ, Thatcher MO, Carr ST, Gibbs JL, et al. High-mobility group box 1 disrupts metabolic function with cigarette smoke exposure in a ceramide-dependent manner. Int J Mol Sci 2017; 18(5)E1099
[54]
Fiuza C, Bustin M, Talwar S, et al. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003; 101(7): 2652-60.
[55]
Wang D, Qi X, Liu F, et al. A multicenter matched case-control analysis on seven polymorphisms from HMGB1 and RAGE genes in predicting hepatocellular carcinoma risk. Oncotarget 2017; 8(30): 50109-16.
[56]
Ludwig A, Weber C. Transmembrane chemokines: Versatile ‘special agents’ in vascular inflammation. Thromb Haemost 2007; 97(5): 694-703.
[57]
Garcia GE, Xia Y, Chen S, et al. NF-kappaB-dependent fractalkine induction in rat aortic endothelial cells stimulated by IL-1beta, TNF-alpha, and LPS. J Leukoc Biol 2000; 67(4): 577-84.
[58]
Izquierdo MC, Martin-Cleary C, Fernandez-Fernandez B, et al. CXCL16 in kidney and cardiovascular injury. Cytokine Growth Factor Rev 2014; 25(3): 317-25.
[59]
Damås JK, Boullier A, Waehre T, et al. Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, is elevated in coronary artery disease and is reduced during statin therapy. Arterioscler Thromb Vasc Biol 2005; 25(12): 2567-72.
[60]
Yajima N1, Kasama T, Isozaki T, et al. Elevated levels of soluble fractalkine in active systemic lupus erythematosus: Potential involvement in neuropsychiatric manifestations. Arthritis Rheum 2005; 52(6): 1670-5.
[61]
Ruth JH, Haas CS, Park CC, et al. CXCL16-mediated cell recruitment to rheumatoid arthritis synovial tissue and murine lymph nodes is dependent upon the MAPK pathway. Arthritis Rheum 2006; 54(3): 765-78.
[62]
Ruth JH, Volin MV, Haines GK 3rd, et al. Fractalkine, a novel chemokine in rheumatoid arthritis and in rat adjuvant-induced arthritis. Arthritis Rheum 2001; 44(7): 1568-81.
[63]
Fraticelli P, Sironi M, Bianchi G, et al. Fractalkine (CX3CL1) as an amplification circuit of polarized Th1 responses. J Clin Invest 2001; 107(9): 1173-81.
[64]
Bazan JF, Bacon KB, Hardiman G, et al. A new class of membrane-bound chemokine with a CX3C motif. Nature 1997; 385(6617): 640-4.
[65]
Imai T, Hieshima K, Haskell C, et al. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell 1997; 91(4): 521-30.
[66]
Marques P, Collado A, Escudero P, et al. Cigarette smoke increases endothelial CXCL16-Leukocyte CXCR6 Adhesion in vitro and in vivo. Potential consequences in chronic obstructive pulmonary disease. Front Immunol 2017; 8: 1766.
[67]
Chandrasekar B, Bysani S, Mummidi S. CXCL16 signals via Gi, phosphatidylinositol 3-kinase, Akt, I kappa B kinase, and nuclear factor-kappa B and induces cell-cell adhesion and aortic smooth muscle cell proliferation. J Biol Chem 2004; 279(5): 3188-96.
[68]
Lee SJ, Namkoong S, Kim YM, et al. Fractalkine stimulates angiogenesis by activating the Raf-1/MEK/ERK- and PI3K/Akt/eNOS-dependent signal pathways. Am J Physiol Heart Circ Physiol 2006; 291(6): 2836-46.
[69]
Rahman I. Oxidative stress in pathogenesis of chronic obstructive pulmonary disease: Cellular and molecular mechanisms. Cell Biochem Biophys 2005; 43(1): 167-88.
[70]
Postea O, Koenen RR, Hristov M, Weber C, Ludwig A. Homocysteine up-regulates vascular transmembrane chemokine CXCL16 and induces CXCR6+ lymphocyte recruitment in vitro and in vivo. J Cell Mol Med 2008; 12(5A): 1700-9.
[71]
Lehrke M, Millington SC, Lefterova M, et al. CXCL16 is a marker of inflammation, atherosclerosis, and acute coronary syndromes in humans. J Am Coll Cardiol 2007; 49(4): 442-9.
[72]
Ueland T, Smedbakken LM, Hallén J, et al. Soluble CXCL16 and long-term outcome in acute ischemic stroke. Atherosclerosis 2012; 220(1): 244-9.
[73]
Zhao L, Wu F, Jin L, et al. Serum CXCL16 as a novel marker of renal injury in type 2 diabetes mellitus. PLoS One 2014; 9(1)e87786
[74]
Naik P, Fofaria N, Prasad S, et al. Oxidative and pro-inflammatory impact of regular and denicotinized cigarettes on blood brain barrier endothelial cells: Is smoking reduced or nicotine-free products really safe? BMC Neurosci 2014; 15: 51.
[75]
Prasad S, Sajja RK, Park JH, Naik P, Kaisar MA, Cucullo L. Impact of cigarette smoke extract and hyperglycemic conditions on blood-brain barrier endothelial cells. Fluids Barriers CNS 2015; 12: 18.
[76]
Mohandas TK, Chen XN, Rowe LB, et al. Localization of the tight junction protein gene TJP1 to human chromosome 15q13, distal to the Prader-Willi/Angelman region, and to mouse chromosome 7. Genomics 1995; 30(3): 594-7.
[77]
Manda VK, Mittapalli RK, Geldenhuys WJ, Lockman PR. Chronic exposure to nicotine and saquinavir decreases endothelial Notch-4 expression and disrupts blood-brain barrier integrity. J Neurochem 2010; 115(2): 515-25.
[78]
Dobrogowska DH, Lossinsky AS, Tarnawski M, Vorbrodt AW. Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J Neurocytol 1998; 27(3): 163-73.
[79]
Proescholdt MA, Jacobson S, Tresser N, Oldfield EH, Merrill MJ. Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats. J Neuropathol Exp Neurol 2002; 61(10): 914-25.
[80]
Argaw AT, Zhang Y, Snyder BJ, et al. IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J Immunol 2006; 177(8): 5574-84.
[81]
Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci USA 2009; 106(6): 1977-82.
[82]
Barbieri SS, Weksler BB. Tobacco smoke cooperates with interleukin-1beta to alter beta-catenin trafficking in vascular endothelium resulting in increased permeability and induction of cyclooxygenase-2 expression in vitro and in vivo. FASEB J 2007; 21(8): 1831-43.
[83]
Brembeck FH, Rosário M, Birchmeier W. Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr Opin Genet Dev 2006; 16(1): 51-9.
[84]
Morin PJ. Beta-catenin signaling and cancer. BioEssays 1999; 21(12): 1021-30.
[85]
Crosby CV, Fleming PA, Argraves WS, et al. VE-cadherin is not required for the formation of nascent blood vessels but acts to prevent their disassembly. Blood 2005; 105(7): 2771-6.
[86]
Inoue M, Itoh H, Ueda M, et al. Vascular endothelial growth factor (VEGF) expression in human coronary atherosclerotic lesions: Possible pathophysiological significance of VEGF in progression of atherosclerosis. Circulation 1998; 98(20): 2108-16.
[87]
Sirotin BZ, Korneeva NV. Vascular permeability and intravascular erythrocyte aggregation in young people after smoking cessation. Ter Arkh 2017; 89(4): 35-8.
[88]
Messner B, Bernhard D. Smoking and cardiovascular disease: mechanisms of endothelial dysfunction and early atherogenesis. Arterioscler Thromb Vasc Biol 2014; 34(3): 509-15.
[89]
Lin SJ, Hong CY, Chang MS, Chiang BN, Chien S. Long-term nicotine exposure increases aortic endothelial cell death and enhances transendothelial macromolecular transport in rats. Arterioscler Thromb 1992; 12(11): 1305-12.
[90]
Weinbaum S, Tzeghai G, Ganatos P, Pfeffer R, Chien S. Effect of cell turnover and leaky junctions on arterial macromolecular transport. Am J Physiol 1985; 248(6 Pt 2): 945-60.
[91]
Minick CR, Stemerman MG, Insull W Jr. Effect of regenerated endothelium on lipid accumulation in the arterial wall. Proc Natl Acad Sci USA 1977; 74(4): 1724-8.
[92]
Hurt-Camejo E, Camejo G, Rosengren B, et al. Effect of arterial proteoglycans and glycosaminoglycans on low density lipoprotein oxidation and its uptake by human macrophages and arterial smooth muscle cells. Arterioscler Thromb 1992; 12(5): 569-83.
[93]
Mundi S, Massaro M, Scoditti E, et al. Endothelial permeability, LDL deposition, and cardiovascular risk factors-a review. Cardiovasc Res 2018; 114(1): 35-52.
[94]
Vikman P, Xu CB, Edvinsson L. Lipid-soluble cigarette smoking particles induce expression of inflammatory and extracellular-matrix-related genes in rat cerebral arteries. Vasc Health Risk Manag 2009; 5(1): 333-41.
[95]
Xu CB, Zheng JP, Zhang W, Liu E, Edvinsson L, Zhang Y. Low density lipoprotein induces upregulation of vasoconstrictive endothelin type B receptor expression. Vascul Pharmacol 2014; 60(1): 42-8.
[96]
Kitada K, Ohkita M, Matsumura Y. Pathological importance of the endothelin-1/ET(B) receptor system on vascular diseases. Cardiol Res Pract 2012; 2012731970
[97]
Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: Insights from neuroimaging. Lancet Neurol 2013; 12(5): 483-97.
[98]
Huang SH, Wang L, Chi F, et al. Circulating brain microvascular endothelial cells (cBMECs) as potential biomarkers of the blood-brain barrier disorders caused by microbial and non-microbial factors. PLoS One 2013; 8(4)e62164
[99]
Hossain M, Sathe T, Fazio V, et al. Tobacco smoke: A critical etiological factor for vascular impairment at the blood-brain barrier. Brain Res 2009; 1287: 192-205.
[100]
Spencer JI, Bell JS, DeLuca GC. Vascular pathology in multiple sclerosis: Reframing pathogenesis around the blood-brain barrier. J Neurol Neurosurg Psychiatry 2018; 89(1): 42-52.
[101]
Alvarez JI, Cayrol R, Prat A. Disruption of central nervous system barriers in multiple sclerosis. Biochim Biophys Acta 2011; 1812(2): 252-64.
[102]
Bennett S, Grant MM, Aldred S. Oxidative stress in vascular dementia and Alzheimer’s disease: A common pathology. J Alzheimers Dis 2009; 17(2): 245-57.
[103]
Graetz C, Gröger A, Luessi F, et al. Association of smoking but not HLA-DRB1*15:01, APOE or body mass index with brain atrophy in early multiple sclerosis. Mult Scler 2019; 25(5): 661-8.
[104]
Olsson T, Barcellos LF, Alfredsson L. Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis. Nat Rev Neurol 2017; 13(1): 25-36.
[105]
Ramanujam R, Hedström AK, Manouchehrinia A, et al. Effect of Smoking Cessation on Multiple Sclerosis Prognosis. JAMA Neurol 2015; 72(10): 1117-23.
[106]
Rosenberg GA. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol 2009; 8(2): 205-16.
[107]
Chen SH, Murphy DA, Lassoued W, Thurston G, Feldman MD, Lee WM. Activated STAT3 is a mediator and biomarker of VEGF endothelial activation. Cancer Biol Ther 2008; 7(12): 1994-2003.
[108]
Xu Y, Yamada T, Satoh T, Okuda Y. Measurement of serum amyloid A1 (SAA1), a major isotype of acute phase SAA. Clin Chem Lab Med 2006; 44(1): 59-63.
[109]
Abboud S, Viiri LE, Lütjohann D, et al. Associations of apolipoprotein E gene with ischemic stroke and intracranial atherosclerosis. Eur J Hum Genet 2008; 16(8): 955-60.
[110]
Naik P, Cucullo L. Pathobiology of tobacco smoking and neurovascular disorders: Untied strings and alternative products. Fluids Barriers CNS 2015; 12: 25.
[111]
Bernhard D, Csordas A, Henderson B, Rossmann A, Kind M, Wick G. Cigarette smoke metal-catalyzed protein oxidation leads to vascular endothelial cell contraction by depolymerization of microtubules. FASEB J 2005; 19(9): 1096-107.
[112]
Pittilo RM, Bull HA, Gulati S, et al. Nicotine and cigarette smoking: Effects on the ultrastructure of aortic endothelium. Int J Exp Pathol 1990; 71(4): 573-86.
[113]
Wang Z, Wang D, Wang Y. Cigarette smoking and adipose tissue: The emerging role in progression of atherosclerosis. Mediators Inflamm 2017; 20173102737
[114]
Mjos OD. Lipid effects of smoking. Am Heart J 1988; 115(1 Pt 2): 272-5.
[115]
Jeremy JY, Mikhailidis DP, Dandona P. Simulating the diabetic environment modifies in vitro prostacyclin synthesis. Diabetes 1983; 32(3): 217-21.
[116]
Barradas MA, Mikhailidis DP, Dandona P. The effect of non-esterified fatty acids on vascular ADP-degrading enzyme activity. Diabetes Res Clin Pract 1987; 3(1): 9-19.
[117]
Mikhailidis DP, Mikhailidis AM, Barradas MA, Dandona P. Effect of nonesterified fatty acids on the stability of prostacyclin activity. Metabolism 1983; 32(7): 717-21.
[118]
Daiber A, Di Lisa F, Ferdinandy P. Pharmacology of oxidative stress: Translational opportunities. Br J Pharmacol 2017; 174(12): 1511-3.
[119]
Ma Q, Battelli L, Hubbs AF. Multiorgan autoimmune inflammation, enhanced lymphoproliferation, and impaired homeostasis of reactive oxygen species in mice lacking the antioxidant-activated transcription factor Nrf2. Am J Pathol 2006; 168(6): 1960-74.
[120]
Rangasamy T, Cho CY, Thimmulappa RK, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 2004; 114(9): 1248-59.
[121]
Garbin U, Fratta Pasini A, Stranieri C, et al. Cigarette smoking blocks the protective expression of Nrf2/ARE pathway in peripheral mononuclear cells of young heavy smokers favouring inflammation. PLoS One 2009; 4(12)e8225
[122]
Goven D, Boutten A, Leçon-Malas V, et al. Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema. Thorax 2008; 63(10): 916-24.
[123]
Fratta Pasini A, Albiero A, Stranieri C, et al. Serum oxidative stress-induced repression of Nrf2 and GSH depletion: A mechanism potentially involved in endothelial dysfunction of young smokers. PLoS One 2012; 7(1)e30291
[124]
Kuosmanen SM, Kansanen E, Kaikkonen MU, et al. NRF2 regulates endothelial glycolysis and proliferation with miR-93 and mediates the effects of oxidized phospholipids on endothelial activation. Nucleic Acids Res 2018; 46(3): 1124-38.
[125]
Andreou I, Sun X, Stone PH, Edelman ER, Feinberg MW. miRNAs in atherosclerotic plaque initiation, progression, and rupture. Trends Mol Med 2015; 21(5): 307-18.
[126]
Schrottmaier WC, Oskolkova OV, Schabbauer G, Afonyushkin T. MicroRNA miR-320a modulates induction of HO-1, GCLM and OKL38 by oxidized phospholipids in endothelial cells. Atherosclerosis 2014; 235(1): 1-8.
[127]
Schober A, Nazari-Jahantigh M, Weber C. MicroRNA-mediated mechanisms of the cellular stress response in atherosclerosis. Nat Rev Cardiol 2015; 12(6): 361-74.
[128]
Yokoyama Y, Mise N, Suzuki Y, et al. MicroRNAs as Potential Mediators for Cigarette Smoking Induced Atherosclerosis. Int J Mol Sci 2018; 19(4)E1097
[129]
Liu Y, Pan Q, Zhao Y, et al. MicroRNA-155 regulates ROS production, NO generation, apoptosis and multiple functions of human brain microvessel endothelial cells under physiological and pathological conditions. J Cell Biochem 2015; 116(12): 2870-81.
[130]
Badrnya S, Baumgartner R, Assinger A. Smoking alters circulating plasma microvesicle pattern and microRNA signatures. Thromb Haemost 2014; 112(1): 128-36.
[131]
Sugiura T, Dohi Y, Yamashita S, et al. Circulating level of microRNA-126 may be a potential biomarker for recovery from smoking-related vascular damage in middle-aged habitual smokers. Int J Cardiol Heart Vasc 2015; 83-7.
[132]
Golbidi S, Mesdaghinia A, Laher I. Exercise in the metabolic syndrome. Oxid Med Cell Longev 2012; 2012349710
[133]
Després JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature 2006; 444(7121): 881-7.
[134]
Keaney JF Jr, Larson MG, Vasan RS, et al. Obesity and systemic oxidative stress: Clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol 2003; 23(3): 434-9.
[135]
Monteiro R1, Azevedo I. Chronic inflammation in obesity and the metabolic syndrome. Mediators Inflamm 2010; 2010pii: 289645
[136]
Wilsgaard T, Jacobsen BK. Lifestyle factors and incident metabolic syndrome. The Tromsø Study 1979-2001. Diabetes Res Clin Pract 2007; 78(2): 217-24.
[137]
Miyatake N, Wada J, Kawasaki Y, Nishii K, Makino H, Numata T. Relationship between metabolic syndrome and cigarette smoking in the Japanese population. Intern Med 2006; 45(18): 1039-43.
[138]
Sun K, Liu J, Ning G. Active smoking and risk of metabolic syndrome: A meta-analysis of prospective studies. PLoS One 2012; 7(10)e47791
[139]
Xie B, Palmer PH, Pang Z, Sun P, Duan H, Johnson CA. Environmental tobacco use and indicators of metabolic syndrome in Chinese adults. Nicotine Tob Res 2010; 12(3): 198-206.
[140]
Wada T, Urashima M, Fukumoto T. Risk of metabolic syndrome persists twenty years after the cessation of smoking. Intern Med 2007; 46(14): 1079-82.
[141]
Chen CC, Li TC, Chang PC, et al. Association among cigarette smoking, metabolic syndrome, and its individual components: The metabolic syndrome study in Taiwan. Metabolism 2008; 57(4): 544-8.
[142]
Woodward M, Rumley A, Lowe GD, Tunstall-Pedoe H. C-reactive protein: Associations with haematological variables, cardiovascular risk factors and prevalent cardiovascular disease. Br J Haematol 2003; 122(1): 135-41.
[143]
Pretorius E, Oberholzer HM, van der Spuy WJ, Meiring JH. Smoking and coagulation: The sticky fibrin phenomenon. Ultrastruct Pathol 2010; 34(4): 236-9.
[144]
Meltzer ME, Doggen CJ, de Groot PG, Rosendaal FR, Lisman T. Reduced plasma fibrinolytic capacity as a potential risk factor for a first myocardial infarction in young men. Br J Haematol 2009; 145(1): 121-7.
[145]
Chakkarwar VA. Fenofibrate attenuates nicotine-induced vascular endothelial dysfunction in the rat. Vascul Pharmacol 2011; 55(5-6): 163-8.
[146]
Kilicarslan A, Yavuz B, Guven GS, et al. Fenofibrate improves endothelial function and decreases thrombin-activatable fibrinolysis inhibitor concentration in metabolic syndrome. Blood Coagul Fibrinolysis 2008; 19(4): 310-4.
[147]
National center for chronic disease prevention and health promotion (US) office on smoking and health. The health consequences of smoking -50 years of progress: A report of the surgeon general. Reports of the Surgeon General 2014.
[148]
Eaton DK, Kann L, Kinchen S, et al. Youth risk behavior surveillance - United States, 2011. MMWR Surveill Summ 2012; 61(4): 1-162.
[149]
Amrock SM, Zakhar J, Zhou S, Weitzman M. Perception of e-cigarette harm and its correlation with use among U.S. adolescents. Nicotine Tob Res 2015; 17(3): 330-6.
[150]
Anand V, McGinty KL, O’Brien K, Guenthner G, Hahn E, Martin CA. E-cigarette use and beliefs among urban public high school students in North Carolina. J Adolesc Health 2015; 57(1): 46-51.
[151]
Arrazola RA, Singh T, Corey CG, et al. Tobacco use among middle and high school students - United States, 2011-2014. MMWR Morb Mortal Wkly Rep 2015; 64(14): 381-5.
[152]
Jones L. BBC New [Online]. 2018 [cited 2018 Jun 1]; Available from: https://www. bbc.com/news/business-44295336
[153]
Weaver SR, Majeed BA, Pechacek TF, Nyman AL, Gregory KR, Eriksen MP. Use of electronic nicotine delivery systems and other tobacco products among USA adults, 2014: Results from a national survey. Int J Public Health 2016; 61(2): 177-88.
[154]
Siegel MB, Tanwar KL, Wood KS. Electronic cigarettes as a smoking-cessation: Tool results from an online survey. Am J Prev Med 2011; 40(4): 472-5.
[155]
Zhu SH, Sun JY, Bonnevie E, et al. Four hundred and sixty brands of e-cigarettes and counting: Implications for product regulation. Tob Control 2014; 23(Suppl. 3): 3-9.
[156]
Clapp PW, Jaspers I. Electronic cigarettes: Their constituents and potential links to asthma. Curr Allergy Asthma Rep 2017; 17(11): 79.
[157]
Sleiman M, Logue JM, Montesinos VN, et al. Emissions from electronic cigarettes: Key parameters affecting the release of harmful chemicals. Environ Sci Technol 2016; 50(17): 9644-51.
[158]
Farsalinos KE, Kistler KA, Gillman G, Voudris V. Evaluation of electronic cigarette liquids and aerosol for the presence of selected inhalation toxins. Nicotine Tob Res 2015; 17(2): 168-74.
[159]
Barrington-Trimis JL, Samet JM, McConnell R. Flavorings in electronic cigarettes: An unrecognized respiratory health hazard? JAMA 2014; 312(23): 2493-4.
[160]
López-Sáez MP, Carrillo P, Huertas AJ, Fernández-Nieto M, López JD. Occupational asthma and dermatitis induced by eugenol in a cleaner. J Investig Allergol Clin Immunol 2015; 25(1): 64-5.
[161]
Quirce S, Fernández-Nieto M, del Pozo V, Sastre B, Sastre J. Occupational asthma and rhinitis caused by eugenol in a hairdresser. Allergy 2008; 63(1): 137-8.
[162]
Schraufnagel DE, Blasi F, Drummond MB, Lam DC, et al. Electronic cigarettes. A position statement of the forum of international respiratory societies. Am J Respir Crit Care Med 2014; 190(6): 611-8.
[163]
Harrell PT, Simmons VN, Correa JB, Padhya TA, Brandon TH. Electronic nicotine delivery systems (“e-cigarettes”): Review of safety and smoking cessation efficacy. Otolaryngol Head Neck Surg 2014; 151(3): 381-93.
[164]
Goniewicz ML, Knysak J, Gawron M, et al. Levels of selected carcinogens and toxicants in vapour from electronic cigarettes. Tob Control 2014; 23(2): 133-9.
[165]
WHO. WHO global report on trends in prevalence of tobacco smoking 2000-2025 Second edition. Report No 978-92-4-151417-0 2018; [cited: 10th Sep 2018]. Available from:www.who.int/tobacco/publications/.../trends-tobacco-smoking-second-edition/
[166]
Anderson C, Majeste A, Hanus J, Wang S. E-cigarette aerosol exposure induces reactive oxygen species, dna damage, and cell death in vascular endothelial cells. Toxicol Sci 2016; 154(2): 332-40.
[167]
Farsalinos KE, Romagna G, Allifranchini E, et al. Comparison of the cytotoxic potential of cigarette smoke and electronic cigarette vapour extract on cultured myocardial cells. Int J Environ Res Public Health 2013; 10(10): 5146-62.
[168]
Putzhammer R, Doppler C, Jakschitz T, et al. Vapours of US and EU market leader electronic cigarette brands and liquids are cytotoxic for human vascular endothelial cells. PLoS One 2016; 11(6)e0157337
[169]
Schweitzer KS, Chen SX, Law S, et al. Endothelial disruptive proinflammatory effects of nicotine and e-cigarette vapor exposures. Am J Physiol Lung Cell Mol Physiol 2015; 309(2): 175-87.
[170]
Lerner CA, Sundar IK, Yao H, et al. 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 2015; 10(2)e0116732
[171]
Sancilio S, Gallorini M, Cataldi A, di Giacomo V. Cytotoxicity and apoptosis induction by e-cigarette fluids in human gingival fibroblasts. Clin Oral Investig 2016; 20(3): 477-83.
[172]
Antoniewicz L, Bosson JA, Kuhl J, et al. Electronic cigarettes increase endothelial progenitor cells in the blood of healthy volunteers. Atherosclerosis 2016; 255: 179-85.
[173]
Carnevale R, Sciarretta S, Violi F, et al. Acute impact of tobacco vs. electronic cigarette smoking on oxidative stress and vascular function. Chest 2016; 150(3): 606-12.
[174]
Scott A, Lugg ST, Aldridge K, et al. Pro-inflammatory effects of e-cigarette vapour condensate on human alveolar macrophages. Thorax 2018; 73(12): 1161-9.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy