Human Pericardial Fluid Contains Exosomes Enriched with Cardiovascular-Expressed MicroRNAs and Promotes Therapeutic Angiogenesis

Molecular Therapy

Volumn 25, Issue 3, 2017, Pages 679-693

  Beltrami, Cristina ^a,b   Besnier, Marie ^a   Shantikumar, Saran ^a   Shearn, Andrew I U ^a   Rajakaruna, Cha ^a   Laftah, Abas ^b   Sessa, Fausto ^c   Spinetti, Gaia ^d   Petretto, Enrico ^b,e   Angelini, Gianni D ^a,b   Emanueli, Costanza ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c Circolo Research Hospital   (Italy)

^d IRCCS MULTIMEDICA   (Italy)

^e DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

angiogenesis; clinical samples; exosomes; extracellular vesicles; human; ischemia; let 7b; microRNAs; pericardial fluid

Indexed keywords

DICER; LET 7B 5P; MICRORNA; PROTEINASE K; RIBONUCLEASE A; RNA; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; RIBONUCLEASE III;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD FLOW; CARDIAC MUSCLE; CELL PROLIFERATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; EXOSOME; GENE EXPRESSION; GENETIC TRANSFECTION; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PERICARDIAL EFFUSION; PLASMA; RNA EXTRACTION; SURVIVAL; TGFBR1 GENE; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION; WESTERN BLOTTING; ANIMAL; CARDIOVASCULAR SYSTEM; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY);

ANIMALS; ARGONAUTE PROTEINS; CARDIOVASCULAR SYSTEM; ENDOTHELIAL CELLS; EXOSOMES; EXTRACELLULAR VESICLES; GENE EXPRESSION PROFILING; HUMANS; MALE; MICE; MICRORNAS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PERICARDIAL FLUID; RIBONUCLEASE III;

EID: 85016255446     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1016/j.ymthe.2016.12.022     Document Type: Article

References (46)

1. 1 Shabetai, R., The Pericardium. 2012, Springer Science & Business Media 1 pp.
2. 2 Masters, M., Riley, P.R., The epicardium signals the way towards heart regeneration. Stem Cell Res. (Amst.) 13:3 Pt B (2014), 683–692.
3. 3 Page, E., Upshaw-Earley, J., Goings, G., Permeability of rat atrial endocardium, epicardium, and myocardium to large molecules. Stretch-dependent effects. Circ. Res. 71 (1992), 159–173.
4. 4 Blair, D.M. (1925). The Lymphatics of the Heart, 1 pp.
5. 5 Mehlhorn, U., Geissler, H.J., Laine, G.A., Allen, S.J., Myocardial fluid balance. Eur. J. Cardiothorac. Surg. 20 (2001), 1220–1230.
6. 6 Stewart, R.H., Rohn, D.A., Allen, S.J., Laine, G.A., Basic determinants of epicardial transudation. Am. J. Physiol. 273 (1997), H1408–H1414.
7. 7 Weihrauch, D., Tessmer, J., Warltier, D.C., Chilian, W.M., Repetitive coronary artery occlusions induce release of growth factors into the myocardial interstitium. Am. J. Physiol. 275 (1998), H969–H976.
8. 8 Pérez-Cárceles, M.D., Noguera, J., Jiménez, J.L., Martínez, P., Luna, A., Osuna, E., Diagnostic efficacy of biochemical markers in diagnosis post-mortem of ischaemic heart disease. Forensic Sci. Int. 142 (2004), 1–7.
9. 9 Osuna, E., Pérez-Cárceles, M.D., Alvarez, M.V., Noguera, J., Luna, A., Cardiac troponin I (cTn I) and the postmortem diagnosis of myocardial infarction. Int. J. Legal Med. 111 (1998), 173–176.
10. 10 Kuosmanen, S.M., Hartikainen, J., Hippeläinen, M., Kokki, H., Levonen, A.-L., Tavi, P., MicroRNA profiling of pericardial fluid samples from patients with heart failure. PLoS ONE, 10, 2015, e0119646.
11. 11 Condorelli, G., Latronico, M.V.G., Cavarretta, E., microRNAs in cardiovascular diseases: current knowledge and the road ahead. J. Am. Coll. Cardiol. 63 (2014), 2177–2187.
12. 12 Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., Guo, J., Zhang, Y., Chen, J., Guo, X., et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 18 (2008), 997–1006.
13. 13 Emanueli, C., Shearn, A.I.U., Angelini, G.D., Sahoo, S., Exosomes and exosomal miRNAs in cardiovascular protection and repair. Vascul. Pharmacol. 71 (2015), 24–30.
14. 14 Bang, C., Batkai, S., Dangwal, S., Gupta, S.K., Foinquinos, A., Holzmann, A., Just, A., Remke, J., Zimmer, K., Zeug, A., et al. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J. Clin. Invest. 124 (2014), 2136–2146.
15. 15 Vicencio, J.M., Yellon, D.M., Sivaraman, V., Das, D., Boi-Doku, C., Arjun, S., Zheng, Y., Riquelme, J.A., Kearney, J., Sharma, V., et al. Plasma exosomes protect the myocardium from ischemia-reperfusion injury. J. Am. Coll. Cardiol. 65 (2015), 1525–1536.
16. 16 Chi, K.R., The tumour trail left in blood. Nature 532 (2016), 269–271.
17. 17 Emanueli, C., Shearn, A.I.U., Laftah, A., Fiorentino, F., Reeves, B.C., Beltrami, C., Mumford, A., Clayton, A., Gurney, M., Shantikumar, S., Angelini, G.D., Coronary artery-bypass-graft surgery increases the plasma concentration of exosomes carrying a cargo of cardiac microRNAs: an example of exosome trafficking out of the human heart with potential for cardiac biomarker discovery. PLoS ONE, 11, 2016, e0154274.
18. 18 Otsuka, M., Zheng, M., Hayashi, M., Lee, J.-D., Yoshino, O., Lin, S., Han, J., Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. J. Clin. Invest. 118 (2008), 1944–1954.
19. 19 Kuehbacher, A., Urbich, C., Zeiher, A.M., Dimmeler, S., Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ. Res. 101 (2007), 59–68.
20. 20 Ota, T., Fujii, M., Sugizaki, T., Ishii, M., Miyazawa, K., Aburatani, H., Miyazono, K., Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-beta in human umbilical vein endothelial cells. J. Cell. Physiol. 193 (2002), 299–318.
21. 21 Castañares, C., Redondo-Horcajo, M., Magán-Marchal, N., ten Dijke, P., Lamas, S., Rodríguez-Pascual, F., Signaling by ALK5 mediates TGF-beta-induced ET-1 expression in endothelial cells: a role for migration and proliferation. J. Cell Sci. 120 (2007), 1256–1266.
22. 22 Suárez, Y., Fernández-Hernando, C., Yu, J., Gerber, S.A., Harrison, K.D., Pober, J.S., Iruela-Arispe, M.L., Merkenschlager, M., Sessa, W.C., Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc. Natl. Acad. Sci. U S A 105 (2008), 14082–14087.
23. 23 Sahoo, S., Losordo, D.W., Exosomes and cardiac repair after myocardial infarction. Circ. Res. 114 (2014), 333–344.
24. 24 Barile, L., Lionetti, V., Cervio, E., Matteucci, M., Gherghiceanu, M., Popescu, L.M., 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. 103 (2014), 530–541.
25. 25 Beltrami, A.P., Barlucchi, L., Torella, D., Baker, M., Limana, F., Chimenti, S., Kasahara, H., Rota, M., Musso, E., Urbanek, K., et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114 (2003), 763–776.
26. 26 van Berlo, J.H., Kanisicak, O., Maillet, M., Vagnozzi, R.J., Karch, J., Lin, S.-C.J., Middleton, R.C., Marbán, E., Molkentin, J.D., c-kit+ cells minimally contribute cardiomyocytes to the heart. Nature 509 (2014), 337–341.
27. 27 Keith, M.C.L., Bolli, R., “String theory” of c-kit(pos) cardiac cells: a new paradigm regarding the nature of these cells that may reconcile apparently discrepant results. Circ. Res. 116 (2015), 1216–1230.
28. 28 Sahoo, S., Klychko, E., Thorne, T., Misener, S., Schultz, K.M., Millay, M., Ito, A., Liu, T., Kamide, C., Agrawal, H., et al. Exosomes from human CD34(+) stem cells mediate their proangiogenic paracrine activity. Circ. Res. 109 (2011), 724–728.
29. 29 Wang, X., Huang, W., Liu, G., Cai, W., Millard, R.W., Wang, Y., Chang, J., Peng, T., Fan, G.C., Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J. Mol. Cell. Cardiol. 74 (2014), 139–150.
30. 30 Kamo, T., Akazawa, H., Komuro, I., Cardiac nonmyocytes in the hub of cardiac hypertrophy. Circ. Res. 117 (2015), 89–98.
31. 31 Heineke, J., Auger-Messier, M., Xu, J., Oka, T., Sargent, M.A., York, A., Klevitsky, R., Vaikunth, S., Duncan, S.A., Aronow, B.J., et al. Cardiomyocyte GATA4 functions as a stress-responsive regulator of angiogenesis in the murine heart. J. Clin. Invest. 117 (2007), 3198–3210.
32. 32 Shiojima, I., Sato, K., Izumiya, Y., Schiekofer, S., Ito, M., Liao, R., Colucci, W.S., Walsh, K., Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J. Clin. Invest. 115 (2005), 2108–2118.
33. 33 Krell, J., Stebbing, J., Carissimi, C., Dabrowska, A.F., de Giorgio, A., Frampton, A.E., Harding, V., Fulci, V., Macino, G., Colombo, T., Castellano, L., TP53 regulates miRNA association with AGO2 to remodel the miRNA-mRNA interaction network. Genome Res. 26 (2016), 331–341.
34. 34 Cai, X., Janku, F., Zhan, Q., Fan, J.-B., Accessing Genetic Information with Liquid Biopsies. Trends Genet. 31 (2015), 564–575.
35. 35 Khan, M., Nickoloff, E., Abramova, T., Johnson, J., Verma, S.K., Krishnamurthy, P., Mackie, A.R., Vaughan, E., Garikipati, V.N., Benedict, C., et al. Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ. Res. 117 (2015), 52–64.
36. 36 Gallet, R., Dawkins, J., Valle, J., Simsolo, E., de Couto, G., Middleton, R., Tseliou, E., Luthringer, D., Kreke, M., Smith, R.R., et al. 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, 10.1093/eurheartj/ehw240 Published online September 27, 2016.
37. 37 Benito-Martin, A., Di Giannatale, A., Ceder, S., Peinado, H., The new deal: a potential role for secreted vesicles in innate immunity and tumor progression. Front. Immunol., 6, 2015, 66.
38. 38 Lee, C., Mitsialis, S.A., Aslam, M., Vitali, S.H., Vergadi, E., Konstantinou, G., Sdrimas, K., Fernandez-Gonzalez, A., Kourembanas, S., Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 126 (2012), 2601–2611.
39. 39 Om, S.Y., Kim, S.-H., Choi, S.-W., Choi, H.O., Kim, Y.-G., Song, J.-M., Jung, S.H., Kim, D.H., Kang, D.H., Song, J.K., Shim, T.S., T cell-based assay of pericardial fluid mononuclear cells for the diagnosis of tuberculous pericardial effusion. J. Am. Coll. Cardiol. 64 (2014), 1966–1968.
40. 40 Fancello, L., Monteil, S., Popgeorgiev, N., Rivet, R., Gouriet, F., Fournier, P.-E., Raoult, D., Desnues, C., Viral communities associated with human pericardial fluids in idiopathic pericarditis. PLoS ONE, 9, 2014, e93367.
41. 41 Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 (2001), 402–408.
42. 42 Andersen, C.L., Jensen, J.L., Ørntoft, T.F., Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64 (2004), 5245–5250.
43. 43 Shelke, G.V., Lässer, C., Gho, Y.S., Lötvall, J., Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J. Extracell. Vesicles, 3, 2014, 3.
44. 44 Chendrimada, T.P., Gregory, R.I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K., Shiekhattar, R., TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436 (2005), 740–744.
45. 45 Emanueli, C., Salis, M.B., Stacca, T., Gaspa, L., Chao, J., Chao, L., Piana, A., Madeddu, P., Rescue of impaired angiogenesis in spontaneously hypertensive rats by intramuscular human tissue kallikrein gene transfer. Hypertension 38 (2001), 136–141.
46. 46 Caporali, A., Meloni, M., Völlenkle, C., Bonci, D., Sala-Newby, G.B., Addis, R., Spinetti, G., Losa, S., Masson, R., Baker, A.H., et al. Deregulation of microRNA-503 contributes to diabetes mellitus-induced impairment of endothelial function and reparative angiogenesis after limb ischemia. Circulation 123 (2011), 282–291.