Exosomal MicroRNA Transfer into Macrophages Mediates Cellular Postconditioning

Circulation

Volumn 136, Issue 2, 2017, Pages 200-214

  De Couto, Geoffrey ^a   Gallet, Romain ^a   Cambier, Linda ^a   Jaghatspanyan, Ervin ^a   Makkar, Nupur ^a   Dawkins, James Frederick ^a   Berman, Benjamin P ^a   Marbán, Eduardo ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

cardioprotection; exosome; macrophage; miRNA; myocardial infarction

Indexed keywords

CD68 ANTIGEN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERCELLULAR ADHESION MOLECULE 1; MICRORNA; MICRORNA 126; MICRORNA 146A; MICRORNA 181B; PROTECTIVE AGENT; PROTEIN KINASE C DELTA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; MIRN181 MICRORNA, RAT;

ADOPTIVE TRANSFER; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CARDIAC MUSCLE CELL; CARDIOSPHERE DERIVED CELL; CELL PHAGOCYTOSIS; CELL POLARITY; CELL THERAPY; CONTROLLED STUDY; DOWN REGULATION; EXOSOME; FEMALE; FIBROBLAST; FOLLOW UP; GENE EXPRESSION; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART PROTECTION; HEART TISSUE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACORONARY DRUG ADMINISTRATION; MACROPHAGE; MONONUCLEAR CELL; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; NEWBORN; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PARTICLE SIZE; PHOTON CORRELATION SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; RAT; RNA SEQUENCE; RNA TRANSPORT; THYMOCYTE; TRANSTHORACIC ECHOCARDIOGRAPHY; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; YUCATAN MICROPIG; ANIMAL; CELL CULTURE; GENE TRANSFER; GENETICS; MINIPIG; MYOCARDIAL INFARCTION; PHYSIOLOGY; PIG; TRANSPLANTATION; WISTAR KYOTO RAT;

ANIMALS; CELL POLARITY; CELLS, CULTURED; EXOSOMES; FEMALE; GENE TRANSFER TECHNIQUES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MACROPHAGES; MICRORNAS; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; RATS, INBRED WKY; SWINE; SWINE, MINIATURE;

EID: 85022335688     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.116.024590     Document Type: Article

References (50)

1. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ, The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007 204 3037 3047. doi: 10.1084/jem.20070885.
2. van Amerongen MJ, Harmsen MC, van Rooijen N, Petersen AH, van Luyn MJ, Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol 2007 170 818 829. doi: 10.2353/ajpath.2007.060547.
3. Ma Y, Halade GV, Zhang J, Ramirez TA, Levin D, Voorhees A, Jin YF, Han HC, Manicone AM, Lindsey ML, Matrix metalloproteinase-28 deletion exacerbates cardiac dysfunction and rupture after myocardial infarction in mice by inhibiting M2 macrophage activation. Circ Res 2013 112 675 688. doi: 10.1161/CIRCRESAHA.111.300502.
4. Aurora AB, Porrello ER, Tan W, Mahmoud AI, Hill JA, Bassel-Duby R, Sadek HA, Olson EN, Macrophages are required for neonatal heart regeneration. J Clin Invest 2014 124 1382 1392. doi: 10.1172/JCI72181.
5. Nahrendorf M, Swirski FK, Monocyte and macrophage heterogeneity in the heart. Circ Res 2013 112 1624 1633. doi: 10.1161/CIRCRESAHA.113.300890.
6. Okabe Y, Medzhitov R, Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 2014 157 832 844. doi: 10.1016/j.cell.2014.04.016.
7. Terrovitis JV, Smith RR, Marbán E, Assessment and optimization of cell engraftment after transplantation into the heart. Circ Res 2010 106 479 494. doi: 10.1161/CIRCRESAHA.109.208991.
8. Malliaras K, Ibrahim A, Tseliou E, Liu W, Sun B, Middleton RC, Seinfeld J, Wang L, Sharifi BG, Marbán E, Stimulation of endogenous cardioblasts by exogenous cell therapy after myocardial infarction. EMBO Mol Med 2014 6 760 777. doi: 10.1002/emmm.201303626.
9. Ibrahim AG, Cheng K, Marbán E, Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Reports 2014 2 606 619. doi: 10.1016/j.stemcr.2014.04.006.
10. Barile L, Lionetti V, Cervio E, Matteucci M, Gherghiceanu M, Popescu LM, Torre T, Siclari F, Moccetti T, Vassalli G, Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction. Cardiovasc Res 2014 103 530 541. doi: 10.1093/cvr/cvu167.
11. Cambier L, de Couto G, Ibrahim A, Echavez AK, Valle J, Liu W, Kreke M, Smith RR, Marbán L, Marbán E, Y RNA fragment in extracellular vesicles confers cardioprotection via modulation of IL-10 expression and secretion. EMBO Mol Med 2017 9 337 352. doi: 10.15252/emmm.201606924.
12. Théry C, Zitvogel L, Amigorena S, Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002 2 569 579. doi: 10.1038/nri855.
13. Imai T, Takahashi Y, Nishikawa M, Kato K, Morishita M, Yamashita T, Matsumoto A, Charoenviriyakul C, Takakura Y, Macrophage-dependent clearance of systemically administered B16BL6-derived exosomes from the blood circulation in mice. J Extracell Vesicles 2015 4 26238
14. Tseliou E, Fouad J, Reich H, Slipczuk L, de Couto G, Aminzadeh M, Middleton R, Valle J, Weixin L, Marbán E, Fibroblasts rendered antifibrotic, antiapoptotic, and angiogenic by priming with cardiosphere-derived extracellular membrane vesicles. J Am Coll Cardiol 2015 66 599 611. doi: 10.1016/j.jacc.2015.05.068.
15. Paggetti J, Haderk F, Seiffert M, Janji B, Distler U, Ammerlaan W, Kim YJ, Adam J, Lichter P, Solary E, Berchem G, Moussay E, Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 2015 126 1106 1117. doi: 10.1182/blood-2014-12-618025.
16. de Couto G, Liu W, Tseliou E, Sun B, Makkar N, Kanazawa H, Arditi M, Marbán E, Macrophages mediate cardioprotective cellular postconditioning in acute myocardial infarction. J Clin Invest 2015 125 3147 3162. doi: 10.1172/JCI81321.
17. Kanazawa H, Tseliou E, Malliaras K, Yee K, Dawkins JF, De Couto G, Smith RR, Kreke M, Seinfeld J, Middleton RC, Gallet R, Cheng K, Luthringer D, Valle I, Chowdhury S, Fukuda K, Makkar RR, Marbán L, Marbán E, Cellular postconditioning: allogeneic cardiosphere-derived cells reduce infarct size and attenuate microvascular obstruction when administered after reperfusion in pigs with acute myocardial infarction. Circ Heart Fail 2015 8 322 332. doi: 10.1161/CIRCHEARTFAILURE.114.001484.
18. Kanazawa H, Tseliou E, Dawkins JF, De Couto G, Gallet R, Malliaras K, Yee K, Kreke M, Valle I, Smith RR, Middleton RC, Ho CS, Dharmakumar R, Li D, Makkar RR, Fukuda K, Marban L, Marban E, Durable benefits of cellular postconditioning: long-term effects of allogeneic cardiosphere-derived cells infused after reperfusion in pigs with acute myocardial infarction. J Am Heart Assoc 2016 5 e002796
19. Gallet R, Dawkins J, Valle J, Simsolo E, de Couto G, Middleton R, Tseliou E, Luthringer D, Kreke M, Smith RR, Marban L, Ghaleh B, Marban E, Exosomes secreted by cardiosphere-derived cells reduce scarring, attenuate adverse remodelling, and improve function in acute and chronic porcine myocardial infarction. Eur Heart J 2016 ehw240
20. Chernyshev VS, Rachamadugu R, Tseng YH, Belnap DM, Jia Y, Branch KJ, Butterfield AE, Pease LF 3rd, Bernard PS, Skliar M, Size and shape characterization of hydrated and desiccated exosomes. Anal Bioanal Chem 2015 407 3285 3301. doi: 10.1007/s00216-015-8535-3.
21. Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colás E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Krämer-Albers EM, Laitinen S, Lässer C, Lener T, Ligeti E, Linē A, Lipps G, Llorente A, Lötvall J, Manček-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-'t Hoen EN, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pállinger É Del Portillo HA, Reventós J, Rigau M, Rohde E, Sammar M, Sánchez-Madrid F, Santarém N, Schallmoser K, Ostenfeld MS, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MH, De Wever O, Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015 4 27066
22. Henao-Mejia J, Williams A, Goff LA, Staron M, Licona-Limón P, Kaech SM, Nakayama M, Rinn JL, Flavell RA, The microRNA miR-181 is a critical cellular metabolic rheostat essential for NKT cell ontogenesis and lymphocyte development and homeostasis. Immunity 2013 38 984 997. doi: 10.1016/j.immuni.2013.02.021.
23. Martinez FO, Helming L, Milde R, Varin A, Melgert BN, Draijer C, Thomas B, Fabbri M, Crawshaw A, Ho LP, Ten Hacken NH, Cobos Jiménez V, Kootstra NA, Hamann J, Greaves DR, Locati M, Mantovani A, Gordon S, Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood 2013 121 e57 e69. doi: 10.1182/blood-2012-06-436212.
24. Kupershmidt I, Su QJ, Grewal A, Sundaresh S, Halperin I, Flynn J, Shekar M, Wang H, Park J, Cui W, Wall GD, Wisotzkey R, Alag S, Akhtari S, Ronaghi M, Ontology-based meta-analysis of global collections of high-throughput public data. PLoS One 2010 5 e13066
25. Arora A, Simpson DA, Individual mRNA expression profiles reveal the effects of specific microRNAs. Genome Biol 2008 9 R82. doi: 10.1186/gb-2008-9-5-r82.
26. Xiao F, Zuo Z, Cai G, Kang S, Gao X, Li T, miRecords: an integrated resource for microRNA-target interactions. Nucleic Acids Res 2009 37 Database issue D105 D110. doi: 10.1093/nar/gkn851.
27. Su R, Lin HS, Zhang XH, Yin XL, Ning HM, Liu B, Zhai PF, Gong JN, Shen C, Song L, Chen J, Wang F, Zhao HL, Ma YN, Yu J, Zhang JW, MiR-181 family: regulators of myeloid differentiation and acute myeloid leukemia as well as potential therapeutic targets. Oncogene 2015 34 3226 3239. doi: 10.1038/onc.2014.274.
28. Mittelbrunn M, Gutiérrez-Vázquez C, Villarroya-Beltri C, González S, Sánchez-Cabo F, González MÁ Bernad A, Sánchez-Madrid F, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2011 2 282. doi: 10.1038/ncomms1285.
29. Sun X, Icli B, Wara AK, Belkin N, He S, Kobzik L, Hunninghake GM, Vera MP, Blackwell TS, Baron RM, Feinberg MW, MICU Registry MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J Clin Invest 2012 122 1973 1990. doi: 10.1172/JCI61495.
30. Kontny E, Kurowska M, Szczepańska K, Maśliński W, Rottlerin, a PKC isozyme-selective inhibitor, affects signaling events and cytokine production in human monocytes. J Leukoc Biol 2000 67 249 258
31. Duquesnes N, Lezoualc'h F, Crozatier B, PKC-δ and PKC-ϵ foes of the same family or strangers? J Mol Cell Cardiol 2011 51 665 673. doi: 10.1016/j.yjmcc.2011.07.013.
32. Sivaraman V, Hausenloy DJ, Kolvekar S, Hayward M, Yap J, Lawrence D, Di Salvo C, Yellon DM, The divergent roles of protein kinase C epsilon and delta in simulated ischaemia-reperfusion injury in human myocardium. J Mol Cell Cardiol 2009 46 758 764. doi: 10.1016/j.yjmcc.2009.02.013.
33. Yogalingam G, Hwang S, Ferreira JC, Mochly-Rosen D, Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) phosphorylation by protein kinase Cδ (PKCδ) inhibits mitochondria elimination by lysosomal-like structures following ischemia and reoxygenation-induced injury. J Biol Chem 2013 288 18947 18960. doi: 10.1074/jbc.M113.466870.
34. Reimer KA, Lowe JE, Rasmussen MM, Jennings RB, The wavefront phenomenon of ischemic cell death: 1: myocardial infarct size vs duration of coronary occlusion in dogs. Circulation 1977 56 786 794
35. Frangogiannis NG, The inflammatory response in myocardial injury, repair, and remodelling. Nat Rev Cardiol 2014 11 255 265. doi: 10.1038/nrcardio.2014.28.
36. Frantz S, Hofmann U, Fraccarollo D, Schäfer A, Kranepuhl S, Hagedorn I, Nieswandt B, Nahrendorf M, Wagner H, Bayer B, Pachel C, Schön MP, Kneitz S, Bobinger T, Weidemann F, Ertl G, Bauersachs J, Monocytes/macrophages prevent healing defects and left ventricular thrombus formation after myocardial infarction. FASEB J 2013 27 871 881. doi: 10.1096/fj.12-214049.
37. Porrello ER, Mahmoud AI, Simpson E, Hill JA, Richardson JA, Olson EN, Sadek HA, Transient regenerative potential of the neonatal mouse heart. Science 2011 331 1078 1080. doi: 10.1126/science.1200708.
38. Lawrence T, Natoli G, Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat Rev Immunol 2011 11 750 761. doi: 10.1038/nri3088.
39. Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K, Batte K, Shah P, Wisler J, Eubank TD, Tridandapani S, Paulaitis ME, Piper MG, Marsh CB, Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013 121 984 995. doi: 10.1182/blood-2011-08-374793.
40. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM, Cline GW, Phillips AJ, Medzhitov R, Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014 513 559 563. doi: 10.1038/nature13490.
41. Jansen Of Lorkeers SJ, Eding JE, Vesterinen HM, van der Spoel TI, Sena ES, Duckers HJ, Doevendans PA, Macleod MR, Chamuleau SA, Similar effect of autologous and allogeneic cell therapy for ischemic heart disease: systematic review and meta-analysis of large animal studies. Circ Res 2015 116 80 86
42. Simons M, Raposo G, Exosomes: vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009 21 575 581. doi: 10.1016/j.ceb.2009.03.007.
43. Gray WD, French KM, Ghosh-Choudhary S, Maxwell JT, Brown ME, Platt MO, Searles CD, Davis ME, Identification of therapeutic covariant microRNA clusters in hypoxia-treated cardiac progenitor cell exosomes using systems biology. Circ Res 2015 116 255 263. doi: 10.1161/CIRCRESAHA.116.304360.
44. Bang C, Batkai S, Dangwal S, Gupta SK, Foinquinos A, Holzmann A, Just A, Remke J, Zimmer K, Zeug A, Ponimaskin E, Schmiedl A, Yin X, Mayr M, Halder R, Fischer A, Engelhardt S, Wei Y, Schober A, Fiedler J, Thum T, Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J Clin Invest 2014 124 2136 2146. doi: 10.1172/JCI70577.
45. Pironti G, Strachan RT, Abraham D, Mon-Wei Yu S, Chen M, Chen W, Hanada K, Mao L, Watson LJ, Rockman HA, Circulating exosomes induced by cardiac pressure overload contain functional angiotensin II type 1 receptors. Circulation 2015 131 2120 2130. doi: 10.1161/CIRCULATIONAHA.115.015687.
46. Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, Bratton DL, Oldenborg PA, Michalak M, Henson PM, Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005 123 321 334. doi: 10.1016/j.cell.2005.08.032.
47. Sun X, He S, Wara AK, Icli B, Shvartz E, Tesmenitsky Y, Belkin N, Li D, Blackwell TS, Sukhova GK, Croce K, Feinberg MW, Systemic delivery of microRNA-181b inhibits nuclear factor-κB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice. Circ Res 2014 114 32 40. doi: 10.1161/CIRCRESAHA.113.302089.
48. Kelly B, O'Neill LA, Metabolic reprogramming in macrophages and dendritic cells in innate immunity. Cell Res 2015 25 771 784. doi: 10.1038/cr.2015.68.
49. Choi DS, Kim DK, Kim YK, Gho YS, Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 2013 13 1554 1571. doi: 10.1002/pmic.201200329.
50. Vyas N, Dhawan J, Exosomes: mobile platforms for targeted and synergistic signaling across cell boundaries. Cell Mol Life Sci 2017 74 1567 1576. doi: 10.1007/s00018-016-2413-9.