Proteomic analysis reveals procoagulant properties of cigarette smoke-induced extracellular vesicles

References

• GBD 2015 Tobacco Collaborators. Smoking prevalence and attributable disease burden in 195 countries and territories, 1990–2015: a systematic analysis from the global burden of disease study 2015. Lancet. 2017;389(10082): 1885–16.
   PubMed Web of Science ®Google Scholar
• Moon HG, Kim S-H, Gao J, et al. CCN1 secretion and cleavage regulate the lung epithelial cell functions after cigarette smoke. Am J Physiol Lung Cell Mol Physiol. 2014;307(4):L326–L337.
   PubMed Web of Science ®Google Scholar
• Cordazzo C, Petrini S, Neri T, et al. Rapid shedding of proinflammatory microparticles by human mononuclear cells exposed to cigarette smoke is dependent on Ca2+ mobilization. Inflamm Res. 2014;63(7):539–547.
   PubMed Web of Science ®Google Scholar
• Serban KA, Rezania S, Petrusca DN, et al. Structural and functional characterization of endothelial microparticles released by cigarette smoke. Sci Rep. 2016;6:31596.
   PubMed Web of Science ®Google Scholar
• Benedikter BJ, Benedikter BJ, Volgers C, et al. Cigarette smoke extract induced exosome release is mediated by depletion of exofacial thiols and can be inhibited by thiol-antioxidants. Free Radic Biol Med. 2017. DOI:10.1016/j.freeradbiomed.2017.03.026
   Web of Science ®Google Scholar
• Gordon C, Gudi K, Krause A, et al. Circulating endothelial microparticles as a measure of early lung destruction in cigarette smokers. Am J Respir Crit Care Med. 2011;184(2):224–232.
   PubMed Web of Science ®Google Scholar
• Mobarrez F, Antoniewicz L, Bosson JA, et al. The effects of smoking on levels of endothelial progenitor cells and microparticles in the blood of healthy volunteers. PLoS One. 2014;9(2):e90314.
   PubMed Web of Science ®Google Scholar
• Yanez-Mo M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.
   PubMed Web of Science ®Google Scholar
• Li CJ, Liu Y, Chen Y, et al. Novel proteolytic microvesicles released from human macrophages after exposure to tobacco smoke. Am J Pathol. 2013;182(5):1552–1562.
   PubMed Web of Science ®Google Scholar
• Li M, Yu D, Williams KJ, et al. Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages. Arterioscler Thromb Vasc Biol. 2010;30(9):1818–1824.
   PubMed Web of Science ®Google Scholar
• Tripisciano C, Weiss R, Eichhorn T, et al. Different potential of extracellular vesicles to support thrombin generation: contributions of phosphatidylserine, tissue factor, and cellular origin. Sci Rep. 2017;7(1):6522.
   Web of Science ®Google Scholar
• Tkach M, Kowal J, Thery C. Why the need and how to approach the functional diversity of extracellular vesicles. Philos Trans R Soc Lond B Biol Sci. 2018;373:1737.
   Web of Science ®Google Scholar
• Benedikter BJ, Bouwman FG, Vajen T, et al. Ultrafiltration combined with size exclusion chromatography efficiently isolates extracellular vesicles from cell culture media for compositional and functional studies. Sci Rep. 2017;7(1):15297.
   PubMed Web of Science ®Google Scholar
• Van Deun J, Mestdagh P, Agostinis P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14(3):228–232.
   PubMed Web of Science ®Google Scholar
• Grottke O, Rossaint R, Henskens Y, et al. Thrombin generation capacity of prothrombin complex concentrate in an in vitro dilutional model. PLoS One. 2013;8(5):e64100.
   Web of Science ®Google Scholar
• Borissoff JI, Heeneman S, Kilinç E, et al. Early atherosclerosis exhibits an enhanced procoagulant state. Circulation. 2010;122(8):821–830.
   PubMed Web of Science ®Google Scholar
• Dielis AW, Castoldi E, Spronk HMH, et al. Coagulation factors and the protein C system as determinants of thrombin generation in a normal population. J Thromb Haemost. 2008;6(1):125–131.
   Web of Science ®Google Scholar
• Kammers K, Cole RN, Tiengwe C, et al. Detecting significant changes in protein abundance. EuPA Open Proteom. 2015;7:11–19.
   PubMedGoogle Scholar
• Ritchie ME, Phipson B, Wu D, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47.
   PubMed Web of Science ®Google Scholar
• Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 2003;100(16):9440–9445.
   PubMed Web of Science ®Google Scholar
• Pathan M, Keerthikumar S, Ang C-S, et al. FunRich: an open access standalone functional enrichment and interaction network analysis tool. Proteomics. 2015;15(15):2597–2601.
   PubMed Web of Science ®Google Scholar
• Wang L, Bi Y, Cao M, et al. Microparticles and blood cells induce procoagulant activity via phosphatidylserine exposure in NSTEMI patients following stent implantation. Int J Cardiol. 2016;223:121–128.
   Web of Science ®Google Scholar
• Fujita Y, Araya J, Ito S, et al. Suppression of autophagy by extracellular vesicles promotes myofibroblast differentiation in COPD pathogenesis. J Extracell Vesicles. 2015;4:28388.
   PubMed Web of Science ®Google Scholar
• Ezzati M, Henley SJ, Thun MJ, et al. Role of smoking in global and regional cardiovascular mortality. Circulation. 2005;112(4):489–497.
   PubMed Web of Science ®Google Scholar
• Owens AP 3rd, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res. 2011;108(10):1284–1297.
   PubMed Web of Science ®Google Scholar
• Lu Q, Sakhatskyy P, Grinnell K, et al. Cigarette smoke causes lung vascular barrier dysfunction via oxidative stress-mediated inhibition of RhoA and focal adhesion kinase. Am J Physiol Lung Cell Mol Physiol. 2011;301(6):L847–57.
   Web of Science ®Google Scholar
• Aghapour M, Raee P, Moghaddam SJ, et al. Airway epithelial barrier dysfunction in COPD: role of cigarette smoke exposure. Am J Respir Cell Mol Biol. 2017. DOI:10.1165/rcmb.2017-0200TR.
   Web of Science ®Google Scholar
• Baek R, Varming K, Jorgensen MM. Does smoking, age or gender affect the protein phenotype of extracellular vesicles in plasma? Transfus Apher Sci. 2016;55(1):44–52.
   PubMed Web of Science ®Google Scholar
• Badrnya S, Baumgartner R, Assinger A. Smoking alters circulating plasma microvesicle pattern and microRNA signatures. Thromb Haemost. 2014;112(1):128–136.
   PubMed Web of Science ®Google Scholar
• Novelli F, Neri T, Tavanti L, et al. Procoagulant, tissue factor-bearing microparticles in bronchoalveolar lavage of interstitial lung disease patients: an observational study. PLoS One. 2014;9(4):e95013.
   Web of Science ®Google Scholar
• Park JA, Sharif AS, Tschumperlin DJ, et al. Tissue factor-bearing exosome secretion from human mechanically stimulated bronchial epithelial cells in vitro and in vivo. J Allergy Clin Immunol. 2012;130(6):1375–1383.
   PubMed Web of Science ®Google Scholar
• Bastarache JA, Fremont RD, Kropski JA, et al. Procoagulant alveolar microparticles in the lungs of patients with acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol. 2009;297(6):L1035–41.
   PubMed Web of Science ®Google Scholar
• Gabazza EC, Taguchi O, Tamaki S, et al. Thrombin in the airways of asthmatic patients. Lung. 1999;177(4):253–262.
   Web of Science ®Google Scholar
• Brims FJ, Chauhan AJ, Higgins B, et al. Coagulation factors in the airways in moderate and severe asthma and the effect of inhaled steroids. Thorax. 2009;64(12):1037–1043.
   Web of Science ®Google Scholar
• Ahmad S, Ahmad A, Rancourt RC, et al. Tissue factor signals airway epithelial basal cell survival via coagulation and protease-activated receptor isoforms 1 and 2. Am J Respir Cell Mol Biol. 2013;48(1):94–104.
   Web of Science ®Google Scholar
• Chen J, Kasper M, Heck T, et al. Tissue factor as a link between wounding and tissue repair. Diabetes. 2005;54(7):2143–2154.
   Web of Science ®Google Scholar
• Cimmino G, Ciccarelli G, Golino P. Role of tissue factor in the coagulation network. Semin Thromb Hemost. 2015;41(7):708–717.
   Web of Science ®Google Scholar
• Giannarelli C, Alique M, Rodriguez DT, et al. Alternatively spliced tissue factor promotes plaque angiogenesis through the activation of hypoxia-inducible factor-1alpha and vascular endothelial growth factor signaling. Circulation. 2014;130(15):1274–1286.
   Web of Science ®Google Scholar
• Witkowski M, Landmesser U, Rauch U. Tissue factor as a link between inflammation and coagulation. Trends Cardiovasc Med. 2016;26(4):297–303.
   PubMed Web of Science ®Google Scholar
• Chen W, Thomas J, Sadatsafavi M, et al. Risk of cardiovascular comorbidity in patients with chronic obstructive pulmonary disease: a systematic review and meta-analysis. Lancet Respir Med. 2015;3(8):631–639.
   PubMed Web of Science ®Google Scholar