Extracellular vesicles in metabolic syndrome

Circulation Research

Volumn 120, Issue 10, 2017, Pages 1674-1686

  Martínez, M Carmen ^a   Andriantsitohaina, Ramaroson ^a  

^a UNIVERSITÉ D'ANGERS   (France)

Author keywords

biomarker; exosome; metabolic syndrome; microparticles; obesity

Indexed keywords

BIOLOGICAL MARKER;

ADIPOCYTE; CELL COMMUNICATION; CELL STIMULATION; DYSLIPIDEMIA; ENDOTHELIUM CELL; EXOSOME; HUMAN; HYPERTENSION; INSULIN RESISTANCE; LIVER CELL; MACROPHAGE; METABOLIC SYNDROME X; MICROFLORA; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SKELETAL MUSCLE CELL; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE CELL; WORLD HEALTH ORGANIZATION; BLOOD; DIABETES MELLITUS; METABOLISM; PHYSIOLOGY; RISK FACTOR;

CELL COMMUNICATION; DIABETES MELLITUS; EXOSOMES; EXTRACELLULAR VESICLES; HUMANS; HYPERTENSION; METABOLIC SYNDROME X; OBESITY; RISK FACTORS;

EID: 85019892680     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.117.309419     Document Type: Review

References (119)

1. Harris MF, The metabolic syndrome. Aust Fam Physician 2013 42 524 527
2. Alberti KG, Zimmet P, Shaw J, Metabolic syndrome-A new world-wide definition. A Consensus Statement from the International Diabetes Federation. Diabet Med 2006 23 469 480. doi: 10.1111/j.1464-5491.2006.01858.x.
3. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009 120 1640 1645. doi: 10.1161/CIRCULATIONAHA.109.192644.
4. Brede S, Serfling G, Klement J, Schmid SM, Lehnert H, Clinical Scenario of the Metabolic Syndrome. Visc Med 2016 32 336 341. doi: 10.1159/000449028.
5. Deedwania PC, Metabolic syndrome and vascular disease: is nature or nurture leading the new epidemic of cardiovascular disease? Circulation 2004 109 2 4. doi: 10.1161/01.CIR.0000110642.73995.BF.
6. Li J, Flammer AJ, Lennon RJ, Nelson RE, Gulati R, Friedman PA, Thomas RJ, Sandhu NP, Hua Q, Lerman LO, Lerman A, Comparison of the effect of the metabolic syndrome and multiple traditional cardiovascular risk factors on vascular function. Mayo Clin Proc 2012 87 968 975. doi: 10.1016/j.mayocp.2012.07.004.
7. Han TS, Wu FC, Lean ME, Obesity and weight management in the elderly: a focus on men. Best Pract Res Clin Endocrinol Metab 2013 27 509 525. doi: 10.1016/j.beem.2013.04.012.
8. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr., Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003 112 1796 1808. doi: 10.1172/JCI19246.
9. Boura-Halfon S, Zick Y, Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am J Physiol Endocrinol Metab 2009 296 E581 E591. doi: 10.1152/ajpendo.90437.2008.
10. Grundy SM, Adipose tissue and metabolic syndrome: too much, too little or neither. Eur J Clin Invest 2015 45 1209 1217. doi: 10.1111/eci.12519.
11. Grundy SM, Obesity, metabolic syndrome, and cardiovascular disease. J Clin Endocrinol Metab 2004 89 2595 2600. doi: 10.1210/jc.2004-0372.
12. Landsberg L, Aronne LJ, Beilin LJ, Burke V, Igel LI, Lloyd-Jones D, Sowers J, Obesity-related hypertension: pathogenesis, cardiovascular risk, and treatment: a position paper of The Obesity Society and the American Society of Hypertension. J Clin Hypertens (Greenwich) 2013 15 14 33. doi: 10.1111/jch.12049.
13. Lim K, Barzel B, Burke SL, Armitage JA, Head GA, Origin of aberrant blood pressure and sympathetic regulation in diet-induced obesity. Hypertension 2016 68 491 500. doi: 10.1161/HYPERTENSIONAHA.116.07461.
14. Simonds SE, Pryor JT, Ravussin E, Leptin mediates the increase in blood pressure associated with obesity. Cell 2014 159 1404 1416. doi: 10.1016/j.cell.2014.10.058.
15. Brown RJ, Meehan CA, Gorden P, Leptin does not mediate hypertension associated with human obesity. Cell 2015 162 465 466. doi: 10.1016/j.cell.2015.07.007.
16. Kastorini CM, Panagiotakos DB, Dietary patterns and prevention of type 2 diabetes: from research to clinical practice; a systematic review. Curr Diabetes Rev 2009 5 221 227
17. Guilherme A, Virbasius JV, Puri V, Czech MP, Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 2008 9 367 377. doi: 10.1038/nrm2391.
18. Leonetti D, Soleti R, Clere N, Vergori L, Jacques C, Duluc L, Dourguia C, Martínez MC, Andriantsitohaina R, Estrogen receptor participates to the beneficial effect of red wine polyphenols in a mouse model of obesity-related disorders. Front Pharmacol 2016 7 529. doi: 10.3389/fphar.2016.00529.
19. Yang G, Lee J, Lee S, Kwak D, Choe W, Kang I, Kim SS, Ha J, Krill oil supplementation improves dyslipidemia and lowers body weight in mice fed a high-fat diet through activation of AMP-Activated protein kinase. J Med Food 2016 19 1120 1129. doi: 10.1089/jmf.2016.3720.
20. Rizzo M, Berneis K, Small, dense low-density-lipoproteins and the metabolic syndrome. Diabetes Metab Res Rev 2007 23 14 20. doi: 10.1002/dmrr.694.
21. Wang CC, Goalstone ML, Draznin B, Molecular mechanisms of insulin resistance that impact cardiovascular biology. Diabetes 2004 53 2735 2740
22. Li Y, Soos TJ, Li X, Wu J, Degennaro M, Sun X, Littman DR, Birnbaum MJ, Polakiewicz RD, Protein kinase C Theta inhibits insulin signaling by phosphorylating IRS1 at Ser(1101). J Biol Chem 2004 279 45304 45307. doi: 10.1074/jbc.C400186200.
23. Ruderman NB, Carling D, Prentki M, Cacicedo JM, AMPK, insulin resistance, and the metabolic syndrome. J Clin Invest 2013 123 2764 2772. doi: 10.1172/JCI67227.
24. Lopes HF, Corrêa-Giannella ML, Consolim-Colombo FM, Egan BM, Visceral adiposity syndrome. Diabetol Metab Syndr 2016 8 40. doi: 10.1186/s13098-016-0156-2.
25. Milbank E, Martinez MC, Andriantsitohaina R, Extracellular vesicles: pharmacological modulators of the peripheral and central signals governing obesity. Pharmacol Ther 2016 157 65 83. doi: 10.1016/j.pharmthera.2015.11.002.
26. Tkach M, Théry C, Communication by extracellular vesicles: where we are and where we need to go. Cell 2016 164 1226 1232. doi: 10.1016/j.cell.2016.01.043.
27. Dignat-George F, Boulanger CM, The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 2011 31 27 33. doi: 10.1161/ATVBAHA.110.218123.
28. Gaceb A, Martinez MC, Andriantsitohaina R, Extracellular vesicles: new players in cardiovascular diseases. Int J Biochem Cell Biol 2014 50 24 28. doi: 10.1016/j.biocel.2014.01.018.
29. Loyer X, Vion AC, Tedgui A, Boulanger CM, Microvesicles as cell-cell messengers in cardiovascular diseases. Circ Res 2014 114 345 353. doi: 10.1161/CIRCRESAHA.113.300858.
30. Huang-Doran I, Zhang CY, Vidal-Puig A, Extracellular vesicles: novel mediators of cell communication in metabolic disease. Trends Endocrinol Metab 2017 28 3 18. doi: 10.1016/j.tem.2016.10.003.
31. Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, Dingli F, Loew D, Tkach M, Théry C, Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A 2016 113 E968 E977. doi: 10.1073/pnas.1521230113.
32. Martinez MC, Tual-Chalot S, Leonetti D, Andriantsitohaina R, Microparticles: targets and tools in cardiovascular disease. Trends Pharmacol Sci 2011 32 659 665. doi: 10.1016/j.tips.2011.06.005.
33. Atkin-Smith GK, Poon IK, Disassembly of the dying: mechanisms and functions. Trends Cell Biol 2017 27 151 162. doi: 10.1016/j.tcb.2016.08.011.
34. Christ L, Raiborg C, Wenzel EM, Campsteijn C, Stenmark H, Cellular functions and molecular mechanisms of the ESCRT membrane-scission machinery. Trends Biochem Sci 2017 42 42 56. doi: 10.1016/j.tibs.2016.08.016.
35. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B, Simons M, Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008 319 1244 1247. doi: 10.1126/science.1153124.
36. van Niel G, Charrin S, Simoes S, Romao M, Rochin L, Saftig P, Marks MS, Rubinstein E, Raposo G, The tetraspanin CD63 regulates ESCRT-independent and-dependent endosomal sorting during melanogenesis. Dev Cell 2011 21 708 721. doi: 10.1016/j.devcel.2011.08.019.
37. Maas SL, Breakefield XO, Weaver AM, Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol 2017 27 172 188. doi: 10.1016/j.tcb.2016.11.003.
38. Tual-Chalot S, Leonetti D, Andriantsitohaina R, Martínez MC, Microvesicles: intercellular vectors of biological messages. Mol Interv 2011 11 88 94. doi: 10.1124/mi.11.2.5.
39. French KC, Antonyak MA, Cerione RA, Extracellular vesicle docking at the cellular port: Extracellular vesicle binding and uptake. Semin Cell Dev Biol 2017 pii: S1084-9521(17)30003-4. doi: 10.1016/j.semcdb.2017.01.002.
40. Abels ER, Breakefield XO, Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol 2016 36 301 312. doi: 10.1007/s10571-016-0366-z.
41. Chiba M, Watanabe N, Watanabe M, Sakamoto M, Sato A, Fujisaki M, Kubota S, Monzen S, Maruyama A, Nanashima N, Kashiwakura I, Nakamura T, Exosomes derived from SW480 colorectal cancer cells promote cell migration in HepG2 hepatocellular cancer cells via the mitogen-Activated protein kinase pathway. Int J Oncol 2016 48 305 312. doi: 10.3892/ijo.2015.3255.
42. Tahiri H, Omri S, Yang C, Lymphocytic microparticles modulate angiogenic properties of macrophages in laser-induced choroidal neovascularization. Sci Rep 2016 6 37391. doi: 10.1038/srep37391.
43. Povero D, Eguchi A, Niesman IR, Andronikou N, de Mollerat du Jeu X, Mulya A, Berk M, Lazic M, Thapaliya S, Parola M, Patel HH, Feldstein AE, Lipid-induced toxicity stimulates hepatocytes to release angiogenic microparticles that require Vanin-1 for uptake by endothelial cells. Sci Signal 2013 6 ra88. doi: 10.1126/scisignal.2004512.
44. Vasan RS, Biomarkers of cardiovascular disease: molecular basis and practical considerations. Circulation 2006 113 2335 2362. doi: 10.1161/CIRCULATIONAHA.104.482570.
45. Agouni A, Andriantsitohaina R, Martinez MC, Microparticles as biomarkers of vascular dysfunction in metabolic syndrome and its individual components. Curr Vasc Pharmacol 2014 12 483 492
46. Stepanian A, Bourguignat L, Hennou S, Coupaye M, Hajage D, Salomon L, Alessi MC, Msika S, de Prost D, Microparticle increase in severe obesity: not related to metabolic syndrome and unchanged after massive weight loss. Obesity (Silver Spring) 2013 21 2236 2243. doi: 10.1002/oby.20365.
47. Campello E, Zabeo E, Radu CM, Spiezia L, Gavasso S, Fadin M, Woodhams B, Vettor R, Simioni P, Hypercoagulability in overweight and obese subjects who are asymptomatic for thrombotic events. Thromb Haemost 2015 113 85 96. doi: 10.1160/TH14-02-0156.
48. Murakami T, Horigome H, Tanaka K, Nakata Y, Ohkawara K, Katayama Y, Matsui A, Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity. Thromb Res 2007 119 45 53. doi: 10.1016/j.thromres.2005.12.013.
49. López Andrés N, Tesse A, Regnault V, Louis H, Cattan V, Thornton SN, Labat C, Kakou A, Tual-Chalot S, Faure S, Challande P, Osborne-Pellegrin M, Martínez MC, Lacolley P, Andriantsitohaina R, Increased microparticle production and impaired microvascular endothelial function in aldosterone-salt-Treated rats: protective effects of polyphenols. PLoS One 2012 7 e39235. doi: 10.1371/journal.pone.0039235.
50. Cordazzo C, Neri T, Petrini S, Lombardi S, Balìa C, Cianchetti S, Carmazzi Y, Paggiaro P, Pedrinelli R, Celi A, Angiotensin II induces the generation of procoagulant microparticles by human mononuclear cells via an angiotensin type 2 receptor-mediated pathway. Thromb Res 2013 131 e168 e174. doi: 10.1016/j.thromres.2013.01.019.
51. Osada-Oka M, Shiota M, Izumi Y, Nishiyama M, Tanaka M, Yamaguchi T, Sakurai E, Miura K, Iwao H, Macrophage-derived exosomes induce inflammatory factors in endothelial cells under hypertensive conditions. Hypertens Res 2016 40 353 360. doi: 10.1038/hr.2016.163.
52. Burger D, Montezano AC, Nishigaki N, He Y, Carter A, Touyz RM, 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. doi: 10.1161/ATVBAHA.110.222703.
53. Preston RA, Jy W, Jimenez JJ, Mauro LM, Horstman LL, Valle M, Aime G, Ahn YS, Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003 41 211 217
54. Nielsen MH, Irvine H, Vedel S, Raungaard B, Beck-Nielsen H, Handberg A, The impact of lipoprotein-Associated oxidative stress on cell-specific microvesicle release in patients with familial hypercholesterolemia. Oxid Med Cell Longev 2016 2016 2492858. doi: 10.1155/2016/2492858.
55. Ousmaal Mel F, Martínez MC, Andriantsitohaina R, Chabane K, Gaceb A, Mameri S, Giaimis J, Baz A, Increased monocyte/neutrophil and pro-coagulant microparticle levels and overexpression of aortic endothelial caveolin-1β in dyslipidemic sand rat, Psammomys obesus. J Diabetes Complications 2016 30 21 29. doi: 10.1016/j.jdiacomp.2015.09.017.
56. Li S, Wei J, Zhang C, Li X, Meng W, Mo X, Zhang Q, Liu Q, Ren K, Du R, Tian H, Li J, Cell-derived microparticles in patients with type 2 diabetes mellitus: a systematic review and meta-Analysis. Cell Physiol Biochem 2016 39 2439 2450. doi: 10.1159/000452512.
57. Jansen F, Yang X, Franklin BS, Hoelscher M, Schmitz T, Bedorf J, Nickenig G, Werner N, High glucose condition increases NADPH oxidase activity in endothelial microparticles that promote vascular inflammation. Cardiovasc Res 2013 98 94 106. doi: 10.1093/cvr/cvt013.
58. Turner M, Reid L, Munkonda M, Burger D, OS 02-03 effect of high glucose exposure on endothelial microparticle formation and composition. J Hypertens 2016 34 suppl 1-ISH 2016 Abstract Book e48. doi: 10.1097/01.hjh.0000499978.32917.c0.
59. Sabatier F, Darmon P, Hugel B, Combes V, Sanmarco M, Velut JG, Arnoux D, Charpiot P, Freyssinet JM, Oliver C, Sampol J, Dignat-George F, Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 2002 51 2840 2845
60. Martin S, Tesse A, Hugel B, Martínez MC, Morel O, Freyssinet JM, Andriantsitohaina R, Shed membrane particles from T lymphocytes impair endothelial function and regulate endothelial protein expression. Circulation 2004 109 1653 1659. doi: 10.1161/01.CIR.0000124065.31211.6E.
61. Esposito K, Maiorino MI, Di Palo C, Gicchino M, Petrizzo M, Bellastella G, Saccomanno F, Giugliano D, Effects of pioglitazone versus metformin on circulating endothelial microparticles and progenitor cells in patients with newly diagnosed type 2 diabetes-A randomized controlled trial. Diabetes Obes Metab 2011 13 439 445. doi: 10.1111/j.1463-1326.2011.01367.x.
62. Zhang X, McGeoch SC, Megson IL, MacRury SM, Johnstone AM, Abraham P, Pearson DW, de Roos B, Holtrop G, O'Kennedy N, Lobley GE, Oat-enriched diet reduces inflammatory status assessed by circulating cell-derived microparticle concentrations in type 2 diabetes. Mol Nutr Food Res 2014 58 1322 1332. doi: 10.1002/mnfr.201300820.
63. Phoonsawat W, Aoki-Yoshida A, Tsuruta T, Sonoyama K, Adiponectin is partially associated with exosomes in mouse serum. Biochem Biophys Res Commun 2014 448 261 266. doi: 10.1016/j.bbrc.2014.04.114.
64. Hubal MJ, Nadler EP, Ferrante SC, Barberio MD, Suh JH, Wang J, Dohm GL, Pories WJ, Mietus-Snyder M, Freishtat RJ, Circulating adipocyte-derived exosomal MicroRNAs associated with decreased insulin resistance after gastric bypass. Obesity (Silver Spring) 2017 25 102 110. doi: 10.1002/oby.21709.
65. Povero D, Eguchi A, Li H, Johnson CD, Papouchado BG, Wree A, Messer K, Feldstein AE, Circulating extracellular vesicles with specific proteome and liver microRNAs are potential biomarkers for liver injury in experimental fatty liver disease. PLoS One 2014 9 e113651. doi: 10.1371/journal.pone.0113651.
66. Agouni A, Lagrue-Lak-Hal AH, Ducluzeau PH, Mostefai HA, Draunet-Busson C, Leftheriotis G, Heymes C, Martinez MC, Andriantsitohaina R, Endothelial dysfunction caused by circulating microparticles from patients with metabolic syndrome. Am J Pathol 2008 173 1210 1219. doi: 10.2353/ajpath.2008.080228.
67. Helal O, Defoort C, Robert S, Marin C, Lesavre N, Lopez-Miranda J, Risérus U, Basu S, Lovegrove J, McMonagle J, Roche HM, Dignat-George F, Lairon D, Increased levels of microparticles originating from endothelial cells, platelets and erythrocytes in subjects with metabolic syndrome: relationship with oxidative stress. Nutr Metab Cardiovasc Dis 2011 21 665 671. doi: 10.1016/j.numecd.2010.01.004.
68. Diamant M, Nieuwland R, Pablo RF, Sturk A, Smit JW, Radder JK, Elevated numbers of tissue-factor exposing microparticles correlate with components of the metabolic syndrome in uncomplicated type 2 diabetes mellitus. Circulation 2002 106 2442 2447
69. Amabile N, Cheng S, Renard JM, Larson MG, Ghorbani A, McCabe E, Griffin G, Guerin C, Ho JE, Shaw SY, Cohen KS, Vasan RS, Tedgui A, Boulanger CM, Wang TJ, Association of circulating endothelial microparticles with cardiometabolic risk factors in the Framingham Heart Study. Eur Heart J 2014 35 2972 2979. doi: 10.1093/eurheartj/ehu153.
70. Kranendonk ME, de Kleijn DP, Kalkhoven E, Kanhai DA, Uiterwaal CS, van der Graaf Y, Pasterkamp G, Visseren FL, SMART Study Group Extracellular vesicle markers in relation to obesity and metabolic complications in patients with manifest cardiovascular disease. Cardiovasc Diabetol 2014 13 37. doi: 10.1186/1475-2840-13-37.
71. Zu L, Niu C, Li J, Shan L, Li L, Zhang D, Willard B, Zheng L, Proteomic research of high-glucose-Activated endothelial microparticles and related proteins to Alzheimer's disease. Diab Vasc Dis Res 2015 12 467 470. doi: 10.1177/1479164115597865.
72. de Jong OG, Verhaar MC, Chen Y, Vader P, Gremmels H, Posthuma G, Schiffelers RM, Gucek M, van Balkom BW, Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracell Vesicles 2012 1. doi: 10.3402/jev.v1i0.18396.
73. Caporali A, Meloni M, Nailor A, Mitić T, Shantikumar S, Riu F, Sala-Newby GB, Rose L, Besnier M, Katare R, Voellenkle C, Verkade P, Martelli F, Madeddu P, Emanueli C, p75(NTR)-dependent activation of NF-κB regulates microRNA-503 transcription and pericyte-endothelial crosstalk in diabetes after limb ischaemia. Nat Commun 2015 6 8024. doi: 10.1038/ncomms9024.
74. Li L, Wang Z, Hu X, Wan T, Wu H, Jiang W, Hu R, Human aortic smooth muscle cell-derived exosomal miR-221/222 inhibits autophagy via a PTEN/Akt signaling pathway in human umbilical vein endothelial cells. Biochem Biophys Res Commun 2016 479 343 350. doi: 10.1016/j.bbrc.2016.09.078.
75. Kim LK, Yoon JW, Lee DH, Kim KM, Choi SH, Park KS, Jang HC, Kim MK, Park HE, Choi SY, Lim S, Impact of metabolic syndrome on the progression of coronary calcium and of coronary artery disease assessed by repeated cardiac computed tomography scans. Cardiovasc Diabetol 2016 15 92. doi: 10.1186/s12933-016-0404-7.
76. Leopold JA, Vascular calcification: Mechanisms of vascular smooth muscle cell calcification. Trends Cardiovasc Med 2015 25 267 274. doi: 10.1016/j.tcm.2014.10.021.
77. Kapustin AN, Chatrou ML, Drozdov I, Vascular smooth muscle cell calcification is mediated by regulated exosome secretion. Circ Res 2015 116 1312 1323. doi: 10.1161/CIRCRESAHA.116.305012.
78. Hutcheson JD, Goettsch C, Bertazzo S, Maldonado N, Ruiz JL, Goh W, Yabusaki K, Faits T, Bouten C, Franck G, Quillard T, Libby P, Aikawa M, Weinbaum S, Aikawa E, Genesis and growth of extracellular-vesicle-derived microcalcification in atherosclerotic plaques. Nat Mater 2016 15 335 343. doi: 10.1038/nmat4519.
79. Saltiel AR, Olefsky JM, Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest 2017 127 1 4. doi: 10.1172/JCI92035.
80. Niu C, Wang X, Zhao M, Cai T, Liu P, Li J, Willard B, Zu L, Zhou E, Li Y, Pan B, Yang F, Zheng L, Macrophage foam cell-derived extracellular vesicles promote vascular smooth muscle cell migration and adhesion. J Am Heart Assoc 2016 5 10 pii: e004099
81. Milbank E, Soleti R, Martinez E, Lahouel B, Hilairet G, Martinez MC, Andriantsitohaina R, Noireaud J, Microparticles from apoptotic RAW 264.7 macrophage cells carry tumour necrosis factor-functionally active on cardiomyocytes from adult mice. J Extracell Vesicles 2015 4 28621
82. Koeck ES, Iordanskaia T, Sevilla S, Ferrante SC, Hubal MJ, Freishtat RJ, Nadler EP, Adipocyte exosomes induce transforming growth factor beta pathway dysregulation in hepatocytes: a novel paradigm for obesity-related liver disease. J Surg Res 2014 192 268 275. doi: 10.1016/j.jss.2014.06.050.
83. Deng ZB, Poliakov A, Hardy RW, Adipose tissue exosome-like vesicles mediate activation of macrophage-induced insulin resistance. Diabetes 2009 58 2498 2505. doi: 10.2337/db09-0216.
84. Eguchi A, Mulya A, Lazic M, Radhakrishnan D, Berk MP, Povero D, Gornicka A, Feldstein AE, Microparticles release by adipocytes act as "find-me" signals to promote macrophage migration. PLoS One 2015 10 e0123110. doi: 10.1371/journal.pone.0123110.
85. Rinella ME, Sanyal AJ, NAFLD in 2014: Genetics, diagnostics and therapeutic advances in NAFLD. Nat Rev Gastroenterol Hepatol 2015 12 65 66. doi: 10.1038/nrgastro.2014.232.
86. Lemoinne S, Thabut D, Housset C, Moreau R, Valla D, Boulanger CM, Rautou PE, The emerging roles of microvesicles in liver diseases. Nat Rev Gastroenterol Hepatol 2014 11 350 361. doi: 10.1038/nrgastro.2014.7.
87. Kakazu E, Mauer AS, Yin M, Malhi H, Hepatocytes release ceramide-enriched pro-inflammatory extracellular vesicles in an IRE1-dependent manner. J Lipid Res 2016 57 233 245. doi: 10.1194/jlr.M063412.
88. Hirsova P, Ibrahim SH, Krishnan A, Verma VK, Bronk SF, Werneburg NW, Charlton MR, Shah VH, Malhi H, Gores GJ, Lipid-induced signaling causes release of inflammatory extracellular vesicles from hepatocytes. Gastroenterology 2016 150 956 967. doi: 10.1053/j.gastro.2015.12.037.
89. Garcia-Martinez I, Santoro N, Chen Y, Hoque R, Ouyang X, Caprio S, Shlomchik MJ, Coffman RL, Candia A, Mehal WZ, Hepatocyte mitochondrial DNA drives nonalcoholic steatohepatitis by activation of TLR9. J Clin Invest 2016 126 859 864. doi: 10.1172/JCI83885.
90. Baron M, Leroyer AS, Majd Z, Lalloyer F, Vallez E, Bantubungi K, Chinetti-Gbaguidi G, Delerive P, Boulanger CM, Staels B, Tailleux A, PPAR activation differently affects microparticle content in atherosclerotic lesions and liver of a mouse model of atherosclerosis and NASH. Atherosclerosis 2011 218 69 76. doi: 10.1016/j.atherosclerosis.2011.03.009.
91. Chen L, Charrier A, Zhou Y, Chen R, Yu B, Agarwal K, Tsukamoto H, Lee LJ, Paulaitis ME, Brigstock DR, Epigenetic regulation of connective tissue growth factor by MicroRNA-214 delivery in exosomes from mouse or human hepatic stellate cells. Hepatology 2014 59 1118 1129. doi: 10.1002/hep.26768.
92. Nojima H, Freeman CM, Schuster RM, Japtok L, Kleuser B, Edwards MJ, Gulbins E, Lentsch AB, Hepatocyte exosomes mediate liver repair and regeneration via sphingosine-1-phosphate. J Hepatol 2016 64 60 68. doi: 10.1016/j.jhep.2015.07.030.
93. Gao W, Liu H, Yuan J, Wu C, Huang D, Ma Y, Zhu J, Ma L, Guo J, Shi H, Zou Y, Ge J, Exosomes derived from mature dendritic cells increase endothelial inflammation and atherosclerosis via membrane TNF-mediated NF-κB pathway. J Cell Mol Med 2016 20 2318 2327. doi: 10.1111/jcmm.12923.
94. Aswad H, Forterre A, Wiklander OP, Exosomes participate in the alteration of muscle homeostasis during lipid-induced insulin resistance in mice. Diabetologia 2014 57 2155 2164. doi: 10.1007/s00125-014-3337-2.
95. Jalabert A, Vial G, Guay C, Exosome-like vesicles released from lipid-induced insulin-resistant muscles modulate gene expression and proliferation of beta recipient cells in mice. Diabetologia 2016 59 1049 1058. doi: 10.1007/s00125-016-3882-y.
96. Guay C, Menoud V, Rome S, Regazzi R, Horizontal transfer of exosomal microRNAs transduce apoptotic signals between pancreatic beta-cells. Cell Commun Signal 2015 13 17. doi: 10.1186/s12964-015-0097-7.
97. Safiedeen Z, Rodríguez-Gómez I, Vergori L, Soleti R, Vaithilingam D, Douma I, Agouni A, Leiber D, Dubois S, Simard G, Zibara K, Andriantsitohaina R, Martínez MC, Temporal cross talk between endoplasmic reticulum and mitochondria regulates oxidative stress and mediates microparticle-induced endothelial dysfunction. Antioxid Redox Signal 2017 26 15 27. doi: 10.1089/ars.2016.6771.
98. Agouni A, Ducluzeau PH, Benameur T, Faure S, Sladkova M, Duluc L, Leftheriotis G, Pechanova O, Delibegovic M, Martinez MC, Andriantsitohaina R, Microparticles from patients with metabolic syndrome induce vascular hypo-reactivity via Fas/Fas-ligand pathway in mice. PLoS One 2011 6 e27809. doi: 10.1371/journal.pone.0027809.
99. Herrema H, IJzerman RG, Nieuwdorp M, Emerging role of intestinal microbiota and microbial metabolites in metabolic control. Diabetologia 2017 60 613 617. doi: 10.1007/s00125-016-4192-0.
100. Ley RE, Turnbaugh PJ, Klein S, Gordon JI, Microbial ecology: human gut microbes associated with obesity. Nature 2006 444 1022 1023. doi: 10.1038/4441022a.
101. Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, Guy CD, Seed PC, Rawls JF, David LA, Hunault G, Oberti F, Calès P, Diehl AM, The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology 2016 63 764 775. doi: 10.1002/hep.28356.
102. Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, Comstock LE, Gandhi R, Weiner HL, The Host Shapes the Gut Microbiota via Fecal MicroRNA. Cell Host Microbe 2016 19 32 43. doi: 10.1016/j.chom.2015.12.005.
103. Choi Y, Kwon Y, Kim DK, Jeon J, Jang SC, Wang T, Ban M, Kim MH, Jeon SG, Kim MS, Choi CS, Jee YK, Gho YS, Ryu SH, Kim YK, Gut microbe-derived extracellular vesicles induce insulin resistance, thereby impairing glucose metabolism in skeletal muscle. Sci Rep 2015 5 15878. doi: 10.1038/srep15878.
104. Barile L, Vassalli G, Exosomes: Therapy delivery tools and biomarkers of diseases. Pharmacol Ther 2017 pii: S0163-7258(17)30034-7. doi: 10.1016/j.pharmthera.2017.02.020.
105. O'Loughlin AJ, Woffindale CA, Wood MJ, Exosomes and the emerging field of exosome-based gene therapy. Curr Gene Ther 2012 12 262 274
106. Boulanger CM, Loyer X, Rautou PE, Amabile N, Extracellular vesicles in coronary artery disease. Nat Rev Cardiol 2017 14 259 272. doi: 10.1038/nrcardio.2017.7.
107. Munagala R, Aqil F, Jeyabalan J, Agrawal AK, Mudd AM, Kyakulaga AH, Singh IP, Vadhanam MV, Gupta RC, Exosomal formulation of anthocyanidins against multiple cancer types. Cancer Lett 2017 393 94 102. doi: 10.1016/j.canlet.2017.02.004.
108. Mirzaei H, Sahebkar A, Jaafari MR, Goodarzi M, Mirzaei HR, Diagnostic and therapeutic potential of exosomes in cancer: the beginning of a new tale? J Cell Physiol 2016. doi: 10.1002/jcp.25739.
109. Yang Z, Xie J, Zhu J, Kang C, Chiang C, Wang X, Wang X, Kuang T, Chen F, Chen Z, Zhang A, Yu B, Lee RJ, Teng L, Lee LJ, Functional exosome-mimic for delivery of siRNA to cancer: in vitro and in vivo evaluation. J Control Release 2016 243 160 171. doi: 10.1016/j.jconrel.2016.10.008.
110. Wang X, Huang W, Liu G, Cai W, Millard RW, Wang Y, Chang J, Peng T, Fan GC, Cardiomyocytes mediate anti-Angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J Mol Cell Cardiol 2014 74 139 150. doi: 10.1016/j.yjmcc.2014.05.001.
111. Fleury A, Hoch L, Martinez MC, Faure H, Taddei M, Petricci E, Manetti F, Girard N, Mann A, Jacques C, Larghero J, Ruat M, Andriantsitohaina R, Le Lay S, Hedgehog associated to microparticles inhibits adipocyte differentiation via a non-canonical pathway. Sci Rep 2016 6 23479. doi: 10.1038/srep23479.
112. Geiger A, Walker A, Nissen E, Human fibrocyte-derived exosomes accelerate wound healing in genetically diabetic mice. Biochem Biophys Res Commun 2015 467 303 309. doi: 10.1016/j.bbrc.2015.09.166.
113. Kalani A, Chaturvedi P, Maldonado C, Bauer P, Joshua IG, Tyagi SC, Tyagi N, Dementia-like pathology in type-2 diabetes: A novel microRNA mechanism. Mol Cell Neurosci 2017 80 58 65. doi: 10.1016/j.mcn.2017.02.005.
114. Wang X, Gu H, Huang W, Peng J, Li Y, Yang L, Qin D, Essandoh K, Wang Y, Peng T, Fan GC, Hsp20-mediated activation of exosome biogenesis in cardiomyocytes improves cardiac function and angiogenesis in diabetic mice. Diabetes 2016 65 3111 3128. doi: 10.2337/db15-1563.
115. Liga A, Vliegenthart AD, Oosthuyzen W, Dear JW, Kersaudy-Kerhoas M, Exosome isolation: a microfluidic road-map. Lab Chip 2015 15 2388 2394. doi: 10.1039/c5lc00240k.
116. Kanwar SS, Dunlay CJ, Simeone DM, Nagrath S, Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip 2014 14 1891 1900. doi: 10.1039/c4lc00136b.
117. Davies RT, Kim J, Jang SC, Choi EJ, Gho YS, Park J, Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip 2012 12 5202 5210. doi: 10.1039/c2lc41006k.
118. Wang Z, Wu HJ, Fine D, Schmulen J, Hu Y, Godin B, Zhang JX, Liu X, Ciliated micropillars for the microfluidic-based isolation of nanoscale lipid vesicles. Lab Chip 2013 13 2879 2882. doi: 10.1039/c3lc41343h.
119. Choi H, Lee DS, Illuminating the physiology of extracellular vesicles. Stem Cell Res Ther 2016 7 55. doi: 10.1186/s13287-016-0316-1.