Endothelial cell-derived extracellular vesicles alter vascular smooth muscle cell phenotype through high-mobility group box proteins

References

• Bang C, Thum T. Exosomes: new players in cell-cell communication. Int J Biochem Cell Biol. 2012;44:2060–19.
   PubMed Web of Science ®Google Scholar
• Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164:1226–1232.
   PubMed Web of Science ®Google Scholar
• Benjamin EJ, Blaha MJ, Chiuve SE, et al. Heart Disease and Stroke Statistics-2017 Update: a Report From the American Heart Association. Circulation. 2017;135:e146–e603.
   PubMed Web of Science ®Google Scholar
• Gimbrone MA Jr., Garcia-Cardena G. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ Res. 2016;118:620–636.
   PubMed Web of Science ®Google Scholar
• Lacolley P, Regnault V, Segers P, et al. Vascular smooth muscle cells and arterial stiffening: relevance in development, aging, and disease. Physiol Rev. 2017;97:1555–1617.
   PubMed Web of Science ®Google Scholar
• Majesky MW. Adventitia and perivascular cells. Arterioscler Thromb Vasc Biol. 2015;35:e31–5.
   Web of Science ®Google Scholar
• Lilly B. We have contact: endothelial cell-smooth muscle cell interactions. Physiology (Bethesda). 2014;29:234–241.
   Web of Science ®Google Scholar
• Hutcheson JD, Aikawa E. Extracellular vesicles in cardiovascular homeostasis and disease. Curr Opin Cardiol. 2018;33:290–297.
   PubMed Web of Science ®Google Scholar
• Jansen F, Nickenig G, Werner N. Extracellular vesicles in cardiovascular disease: potential applications in diagnosis, prognosis, and epidemiology. Circ Res. 2017;120:1649–1657.
   PubMed Web of Science ®Google Scholar
• Wang JM, Su C, Wang Y, et al. Elevated circulating endothelial microparticles and brachial-ankle pulse wave velocity in well-controlled hypertensive patients. J Hum Hypertens. 2009;23:307–315.
   PubMed Web of Science ®Google Scholar
• Feng B, Chen Y, Luo Y, et al. Circulating level of microparticles and their correlation with arterial elasticity and endothelium-dependent dilation in patients with type 2 diabetes mellitus. Atherosclerosis. 2010;208:264–269.
   PubMed Web of Science ®Google Scholar
• Koga H, Sugiyama S, Kugiyama K, et al. Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol. 2005;45:1622–1630.
   PubMed Web of Science ®Google Scholar
• Tramontano AF, Lyubarova R, Tsiakos J, et al. Circulating endothelial microparticles in diabetes mellitus. Mediators Inflamm. 2010;2010:250476.
   PubMed Web of Science ®Google Scholar
• Andrews AM, Rizzo V. Microparticle-induced activation of the vascular endothelium requires Caveolin-1/Caveolae. PLoS One. 2016;11:e0149272.
   PubMed Web of Science ®Google Scholar
• Burger D, Montezano AC, Nishigaki N, et al. Endothelial microparticle formation by angiotensin II is mediated via Ang II receptor type I/NADPH oxidase/Rho kinase pathways targeted to lipid rafts. Arterioscler Thromb Vasc Biol. 2011;31:1898–1907.
   PubMed Web of Science ®Google Scholar
• Zheng B, Yin WN, Suzuki T, et al. Exosome-mediated miR-155 transfer from smooth muscle cells to endothelial cells induces endothelial injury and promotes atherosclerosis. Mol Ther. 2017;25:1279–1294.
   PubMed Web of Science ®Google Scholar
• Hergenreider E, Heydt S, Treguer K, et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol. 2012;14:249–256.
   PubMed Web of Science ®Google Scholar
• de Jong OG, Verhaar MC, Chen Y, et al. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracell Vesicles. 2012;1:1–12.
   Google Scholar
• Lee SB, Kim JJ, Kim TW, et al. Serum deprivation-induced reactive oxygen species production is mediated by Romo1. Apoptosis. 2010;15:204–218.
   PubMed Web of Science ®Google Scholar
• Russell FD, Hamilton KD. Nutrient deprivation increases vulnerability of endothelial cells to proinflammatory insults. Free Radic Biol Med. 2014;67:408–415.
   PubMed Web of Science ®Google Scholar
• Rashid MU, Coombs KM. Serum-reduced media impacts on cell viability and protein expression in human lung epithelial cells. J Cell Physiol. 2019;234:7718–7724.
   Web of Science ®Google Scholar
• Forrester SJ, Elliott KJ, Kawai T, et al. Caveolin-1 deletion prevents hypertensive vascular remodeling induced by angiotensin II. Hypertension. 2017;69:79–86.
   Web of Science ®Google Scholar
• Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;30(1):3.22.1–3.22.29. Chapter 3:Unit 3 22.
   Google Scholar
• An M, Lohse I, Tan Z, et al. Quantitative proteomic analysis of serum exosomes from patients with locally advanced pancreatic cancer undergoing chemoradiotherapy. J Proteome Res. 2017;16:1763–1772.
   PubMed Web of Science ®Google Scholar
• Nakamura H, Takahashi-Jitsuki A, Makihara H, et al. Proteome and behavioral alterations in phosphorylation-deficient mutant collapsin response mediator Protein2 knock-in mice. Neurochem Int. 2018;119:207–217.
   Web of Science ®Google Scholar
• Collot M, Ashokkumar P, Anton H, et al. MemBright: A family of fluorescent membrane probes for advanced cellular imaging and neuroscience. Cell Chem Biol. 2019;26:600–614.e7. DOI:10.1016/j.chembiol.2019.01.009
   Web of Science ®Google Scholar
• Schmidt EK, Clavarino G, Ceppi M, et al. SUnSET, a nonradioactive method to monitor protein synthesis. Nat Methods. 2009;6:275–277.
   PubMed Web of Science ®Google Scholar
• Nakashima H, Frank GD, Shirai H, et al. Novel role of protein kinase C-delta Tyr 311 phosphorylation in vascular smooth muscle cell hypertrophy by angiotensin II. Hypertension. 2008;51:232–238.
   PubMed Web of Science ®Google Scholar
• Grudzenski S, Raths A, Conrad S, et al. Inducible response required for repair of low-dose radiation damage in human fibroblasts. Proc Natl Acad Sci U S A. 2010;107:14205–14210.
   PubMed Web of Science ®Google Scholar
• Mollica L, De Marchis F, Spitaleri A, et al. Glycyrrhizin binds to high-mobility group box 1 protein and inhibits its cytokine activities. Chem Biol. 2007;14:431–441.
   PubMed Web of Science ®Google Scholar
• Lee S, Nam Y, Koo JY, et al. A small molecule binding HMGB1 and HMGB2 inhibits microglia-mediated neuroinflammation. Nat Chem Biol. 2014;10:1055–1060.
   PubMed Web of Science ®Google Scholar
• Elliott KJ, Bourne AM, Takayanagi T, et al. ADAM17 silencing by adenovirus encoding miRNA-embedded siRNA revealed essential signal transduction by angiotensin II in vascular smooth muscle cells. J Mol Cell Cardiol. 2013;62:1–7.
   Web of Science ®Google Scholar
• Trajkovic K, Hsu C, Chiantia S, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319:1244–1247.
   PubMed Web of Science ®Google Scholar
• Kosaka N, Iguchi H, Yoshioka Y, et al. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285:17442–17452.
   PubMed Web of Science ®Google Scholar
• Vlassov AV, Magdaleno S, Setterquist R, et al. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta. 2012;1820:940–948.
   PubMed Web of Science ®Google Scholar
• Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010;73:1907–1920.
   PubMed Web of Science ®Google Scholar
• Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44–57. DOI:10.1038/nprot.2008.211
   PubMed Web of Science ®Google Scholar
• Libby P. Inflammation and cardiovascular disease mechanisms. Am J Clin Nutr. 2006;83:456S–460S.
   PubMed Web of Science ®Google Scholar
• Barks JL, McQuillan JJ, Iademarco MF. TNF-alpha and IL-4 synergistically increase vascular cell adhesion molecule-1 expression in cultured vascular smooth muscle cells. J Immunol. 1997;159:4532–4538.
   Web of Science ®Google Scholar
• Touyz RM, Alves-Lopes R, Rios FJ, et al. Vascular smooth muscle contraction in hypertension. Cardiovasc Res. 2018;114:529–539.
   PubMed Web of Science ®Google Scholar
• Iwasaki S, Ingolia NT. The growing toolbox for protein synthesis studies. Trends Biochem Sci. 2017;42:612–624.
   PubMed Web of Science ®Google Scholar
• Forrester SJ, Booz GW, Sigmund CD, et al. Angiotensin II signal transduction: an update on mechanisms of physiology and pathophysiology. Physiol Rev. 2018;98:1627–1738.
   PubMed Web of Science ®Google Scholar
• Bouallegue A, Simo Cheyou ER, Anand-Srivastava MB, et al. ET-1-induced growth promoting responses involving ERK1/2 and PKB signaling and Egr-1 expression are mediated by Ca2+/CaM-dependent protein kinase-II in vascular smooth muscle cells. Cell Calcium. 2013;54:428–435.
   Web of Science ®Google Scholar
• Khachigian LM. Early growth response-1 in cardiovascular pathobiology. Circ Res. 2006;98:186–191.
   PubMed Web of Science ®Google Scholar
• Kunieda T, Minamino T, Nishi J, et al. Angiotensin II induces premature senescence of vascular smooth muscle cells and accelerates the development of atherosclerosis via a p21-dependent pathway. Circulation. 2006;114:953–960.
   PubMed Web of Science ®Google Scholar
• Akopian D, Shen K, Zhang X, et al. Signal recognition particle: an essential protein-targeting machine. Annu Rev Biochem. 2013;82:693–721.
   PubMed Web of Science ®Google Scholar
• Davalos AR, Kawahara M, Malhotra GK, et al. p53-dependent release of Alarmin HMGB1 is a central mediator of senescent phenotypes. J Cell Biol. 2013;201:613–629.
   PubMed Web of Science ®Google Scholar
• Aird KM, Iwasaki O, Kossenkov AV, et al. HMGB2 orchestrates the chromatin landscape of senescence-associated secretory phenotype gene loci. J Cell Biol. 2016;215:325–334.
   PubMed Web of Science ®Google Scholar
• van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19:213–228.
   PubMed Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113:E968–77.
   PubMed Web of Science ®Google Scholar
• Kapustin AN, Shanahan CM. Emerging roles for vascular smooth muscle cell exosomes in calcification and coagulation. J Physiol. 2016;594:2905–2914.
   PubMed Web of Science ®Google Scholar
• Hoeflich A, David R, Hjortebjerg R. Current IGFBP-Related biomarker research in cardiovascular disease-we need more structural and functional information in clinical studies. Front Endocrinol (Lausanne). 2018;9:388.
   Web of Science ®Google Scholar
• Lawson C, Wolf S. ICAM-1 signaling in endothelial cells. Pharmacol Rep. 2009;61:22–32.
   PubMed Web of Science ®Google Scholar
• Li W, Sama AE, Wang H. Role of HMGB1 in cardiovascular diseases. Curr Opin Pharmacol. 2006;6:130–135.
   Web of Science ®Google Scholar
• Moore KJ, Fisher EA. The double-edged sword of fibronectin in atherosclerosis. EMBO Mol Med. 2012;4:561–563.
   Web of Science ®Google Scholar
• Di Gregoli K, George SJ, Jackson CL, et al. Differential effects of tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2 on atherosclerosis and monocyte/macrophage invasion. Cardiovasc Res. 2016;109:318–330.
   PubMed Web of Science ®Google Scholar
• Braun M, Pietsch P, Schror K. Cellular adhesion molecules on vascular smooth muscle cells. Cardiovasc Res. 1999;41:395–401.
   PubMed Web of Science ®Google Scholar
• Tummala PE, Chen XL, Sundell CL, et al. Angiotensin II induces vascular cell adhesion molecule-1 expression in rat vasculature: A potential link between the renin-angiotensin system and atherosclerosis. Circulation. 1999;100:1223–1229.
   PubMed Web of Science ®Google Scholar
• Ellison S, Gabunia K, Richards JM, et al. IL-19 reduces ligation-mediated neointimal hyperplasia by reducing vascular smooth muscle cell activation. Am J Pathol. 2014;184:2134–2143.
   Web of Science ®Google Scholar
• Scioli MG, Bielli A, Agostinelli S, et al. Antioxidant treatment prevents serum deprivation- and TNF-alpha-induced endothelial dysfunction through the inhibition of NADPH oxidase 4 and the restoration of beta-oxidation. J Vasc Res. 2014;51:327–337.
   Web of Science ®Google Scholar
• Daiber A, Steven S, Weber A, et al. Targeting vascular (endothelial) dysfunction. Br J Pharmacol. 2017;174:1591–1619.
   PubMed Web of Science ®Google Scholar
• Harja E, Bucciarelli LG, Lu Y, et al. Early growth response-1 promotes atherogenesis: mice deficient in early growth response-1 and apolipoprotein E display decreased atherosclerosis and vascular inflammation. Circ Res. 2004;94:333–339.
   PubMed Web of Science ®Google Scholar
• Wang CC, Sharma G, Draznin B. Early growth response gene-1 expression in vascular smooth muscle cells effects of insulin and oxidant stress. Am J Hypertens. 2006;19:366–372.
   Web of Science ®Google Scholar
• Wada Y, Fujimori M, Suzuki J, et al. Egr-1 in vascular smooth muscle cell proliferation in response to allo-antigen. J Surg Res. 2003;115:294–302.
   Web of Science ®Google Scholar
• Albrecht C, Preusch MR, Hofmann G, et al. Egr-1 deficiency in bone marrow-derived cells reduces atherosclerotic lesion formation in a hyperlipidaemic mouse model. Cardiovasc Res. 2010;86:321–329.
   Web of Science ®Google Scholar
• Coppe JP, Desprez PY, Krtolica A, et al. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol. 2010;5:99–118.
   PubMed Web of Science ®Google Scholar
• Katsuumi G, Shimizu I, Yoshida Y, et al. Vascular senescence in cardiovascular and metabolic diseases. Front Cardiovasc Med. 2018;5:18.
   Web of Science ®Google Scholar
• Pascal T, Debacq-Chainiaux F, Chretien A, et al. Comparison of replicative senescence and stress-induced premature senescence combining differential display and low-density DNA arrays. FEBS Lett. 2005;579:3651–3659.
   PubMed Web of Science ®Google Scholar
• Borghesan M, Fafian-Labora J, Eleftheriadou O, et al. Small extracellular vesicles are key regulators of non-cell autonomous intercellular communication in senescence via the interferon protein IFITM3. Cell Rep. 2019;27:3956–3971.e6. DOI:10.1016/j.celrep.2019.05.095
   PubMed Web of Science ®Google Scholar
• Mensa E, Guescini M, Giuliani A, et al. Small extracellular vesicles deliver miR-21 and miR-217 as pro-senescence effectors to endothelial cells. J Extracell Vesicles. 2020;9:1725285.
   PubMed Web of Science ®Google Scholar
• Bennett MR, Sinha S, Owens GK. Vascular smooth muscle cells in atherosclerosis. Circ Res. 2016;118:692–702.
   PubMed Web of Science ®Google Scholar
• Ruvinsky I, Meyuhas O. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem Sci. 2006;31:342–348.
   PubMed Web of Science ®Google Scholar
• Wiley CD, Campisi J. From ancient pathways to aging cells-connecting metabolism and cellular senescence. Cell Metab. 2016;23:1013–1021.
   PubMed Web of Science ®Google Scholar
• Franklin S, Chen H, Mitchell-Jordan S, et al. Quantitative analysis of the chromatin proteome in disease reveals remodeling principles and identifies high mobility group protein B2 as a regulator of hypertrophic growth. Mol Cell Proteomics. 2012;11(M111):014258.
   Google Scholar
• Kapustin AN, Schoppet M, Schurgers LJ, et al. Prothrombin loading of vascular smooth muscle cell-derived exosomes regulates coagulation and calcification. Arterioscler Thromb Vasc Biol. 2017;37:e22–e32.
   PubMed Web of Science ®Google Scholar
• Kang R, Chen R, Zhang Q, et al. HMGB1 in health and disease. Mol Aspects Med. 2014;40:1–116.
   PubMed Web of Science ®Google Scholar
• Agresti A, Lupo R, Bianchi ME, et al. HMGB1 interacts differentially with members of the Rel family of transcription factors. Biochem Biophys Res Commun. 2003;302:421–426.
   PubMed Web of Science ®Google Scholar