Cardiovascular progenitor-derived extracellular vesicles recapitulate the beneficial effects of their parent cells in the treatment of chronic heart failure

Journal of Heart and Lung Transplantation

Volumn 35, Issue 6, 2016, Pages 795-807

  Kervadec, Anaïs ^a,b   Bellamy, Valérie ^a,b   El Harane, Nadia ^a,b   Arakélian, Lousineh ^c,d   Vanneaux, Valérie ^c,d   Cacciapuoti, Isabelle ^c,d   Nemetalla, Hany ^a   Périer, Marie Cécile ^a,b   Toeg, Hadi D ^e   Richart, Adèle ^a,b   Lemitre, Mathilde ^a,b   Yin, Min ^a,b   Loyer, Xavier ^a,b   Larghero, Jérôme ^b,c,d   Hagège, Albert ^a,b   Ruel, Marc ^e   Boulanger, Chantal M ^a,b   Silvestre, Jean Sébastien ^a,b   Menasché, Philippe ^a,b   Renault, Nisa K E ^a,b  

^a HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d INSERM   (France)

^e UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

Author keywords

cardiovascular progenitor cells; cell therapy; embryonic stem cells; exosomes; extracellular vesicles; heart failure; microparticles

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR PROGENITOR DERIVED EXTRACELLULAR VESICLE; CELL PROLIFERATION; CELL SURVIVAL; CELL THERAPY; CONTROLLED STUDY; CORONARY ARTERY OCCLUSION; DNA REPAIR; ECHOCARDIOGRAPHY; EXOSOME; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HEART FAILURE; HEART INFARCTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE FIBROSIS; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; LEFT CORONARY ARTERY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACRINE SIGNALING; PRIORITY JOURNAL; STEM CELL; TISSUE REGENERATION; UPREGULATION; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CHRONIC DISEASE; EMBRYONIC STEM CELL;

ANIMALS; CHRONIC DISEASE; EMBRYONIC STEM CELLS; EXTRACELLULAR VESICLES; HEART FAILURE; HUMANS; MICE; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC;

EID: 84962006646     PISSN: 10532498     EISSN: 15573117     Source Type: Journal    
DOI: 10.1016/j.healun.2016.01.013     Document Type: Article

References (37)

1. World Health Organization. WHO Cardiovascular diseases (CVDs). http://www.who.int/mediacentre/factsheets/fs317/en/. Accessed June 16, 2015.
2. S.K. Sanganalmath, and R. Bolli Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions Circ Res 113 2013 810 834
3. M. Gnecchi, Z. Zhang, A. Ni, and V.J. Dzau Paracrine mechanisms in adult stem cell signaling and therapy Circ Res 103 2008 1204 1219
4. L. Timmers, S.K. Lim, I.E. Hoefer, and et al. Human mesenchymal stem cell-conditioned medium improves cardiac function following myocardial infarction Stem Cell Res 6 2011 206 214
5. R.C. Lai, F. Arslan, M.M. Lee, and et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury Stem Cell Res 4 2010 214 223
6. A. Bobrie, M. Colombo, G. Raposo, and C. Théry Exosome secretion: molecular mechanisms and roles in immune responses Traffic Cph Den 12 2011 1659 1668
7. I. Hazan-Halevy, D. Rosenblum, S. Weinstein, O. Bairey, P. Raanani, and D. Peer Cell-specific uptake of mantle cell lymphoma-derived exosomes by malignant and non-malignant B-lymphocytes Cancer Lett 364 2015 59 69
8. A.R. Soares, T. Martins-Marques, T. Ribeiro-Rodrigues, and et al. Gap junctional protein Cx43 is involved in the communication between extracellular vesicles and mammalian cells Sci Rep 5 2015 13243
9. J. De Toro, L. Herschlik, C. Waldner, and C. Mongini Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications Front Immunol 6 2015 203
10. M. Yin, X. Loyer, and C.M. Boulanger Extracellular vesicles as new pharmacological targets to treat atherosclerosis Eur J Pharmacol 763 Pt A 2015 90 103
11. C. Akyurekli, Y. Le, R.B. Richardson, D. Fergusson, J. Tay, and D.S. Allan A systematic review of preclinical studies on the therapeutic potential of mesenchymal stromal cell-derived microvesicles Stem Cell Rev 11 2015 150 160
12. A.G.-E. Ibrahim, K. Cheng, and E. Marbán Exosomes as critical agents of cardiac regeneration triggered by cell therapy Stem Cell Rep 2 2014 606 619
13. G. Blin, D. Nury, S. Stefanovic, and et al. A purified population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates J Clin Invest 120 2010 1125 1139
14. P. Menasché, V. Vanneaux, J.-R. Fabreguettes, and et al. Towards a clinical use of human embryonic stem cell-derived cardiac progenitors: a translational experience Eur Heart J 36 2015 743 750
15. V. Bellamy, V. Vanneaux, A. Bel, and et al. Long-term functional benefits of human embryonic stem cell-derived cardiac progenitors embedded into a fibrin scaffold J Heart Lung Transplant 34 2015 1198 1207
16. P. Menasché, V. Vanneaux, A. Hagège, and et al. Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report Eur Heart J 36 2015 2011 2017
17. D. Chen, S. Liu, H. Ma, and et al. Paracrine factors from adipose-mesenchymal stem cells enhance metastatic capacity through Wnt signaling pathway in a colon cancer cell co-culture model Cancer Cell Int 15 2015 42
18. C. Cochain, C. Auvynet, L. Poupel, and et al. The chemokine decoy receptor D6 prevents excessive inflammation and adverse ventricular remodeling after myocardial infarction Arterioscler Thromb Vasc Biol 32 2012 2206 2213
19. C. Grange, M. Tapparo, S. Bruno, and et al. Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging Int J Mol Med 33 2014 1055 1063
20. H.D. Toeg, R. Tiwari-Pandey, R. Seymour, and et al. Injectable small intestine submucosal extracellular matrix in an acute myocardial infarction model Ann Thorac Surg 96 2013 1686 1694 discussion 1694
21. B.M. Bolstad, R.A. Irizarry, M. Astrand, and T.P. Speed A comparison of normalization methods for high density oligonucleotide array data based on variance and bias Bioinforma Oxf Engl 19 2003 185 193
22. Y. Zhou, H. Xu, W. Xu, and et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro Stem Cell Res Ther 4 2013 34
23. A.S. Leroyer, T.G. Ebrahimian, C. Cochain, and et al. Microparticles from ischemic muscle promotes postnatal vasculogenesis Circulation 119 2009 2808 2817
24. P.C.H. Hsieh, V.F.M. Segers, M.E. Davis, and et al. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury Nat Med 13 2007 970 974
25. J.C. Garbern, and R.T. Lee Cardiac stem cell therapy and the promise of heart regeneration Cell Stem Cell 12 2013 689 698
26. S. Bobis-Wozowicz, K. Kmiotek, M. Sekula, and et al. Human induced pluripotent stem cell-derived microvesicles transmit RNAs and proteins to recipient mature heart cells modulating cell fate and behavior Stem Cells 33 2015 2748 2761
27. B.N. Oskouei, G. Lamirault, C. Joseph, and et al. Increased potency of cardiac stem cells compared with bone marrow mesenchymal stem cells in cardiac repair Stem Cells Transl Med 1 2012 116 124
28. T.-S. Li, K. Cheng, K. Malliaras, and et al. Direct comparison of different stem cell types and subpopulations reveals superior paracrine potency and myocardial repair efficacy with cardiosphere-derived cells J Am Coll Cardiol 59 2012 942 953
29. S.-X. Zheng, Y.-L. Weng, C.-Q. Zhou, and et al. Comparison of cardiac stem cells and mesenchymal stem cells transplantation on the cardiac electrophysiology in rats with myocardial infarction Stem Cell Rev 9 2013 339 349
30. L. Citro, S. Naidu, F. Hassan, and et al. Comparison of human induced pluripotent stem-cell derived cardiomyocytes with human mesenchymal stem cells following acute myocardial infarction PloS One 9 2014 e116281
31. J. Ratajczak, M. Wysoczynski, F. Hayek, A. Janowska-Wieczorek, and M.Z. Ratajczak Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication Leukemia 20 2006 1487 1495
32. A. Alonso-Betanzos, V. Bolón-Canedo, G.R. Heyndrickx, and P.L. Kerkhof Exploring guidelines for classification of major heart failure subtypes by using machine learning Clin Med Insights Cardiol 9 Suppl 1 2015 57 71
33. F.H. Seeger, A.M. Zeiher, and S. Dimmeler MicroRNAs in stem cell function and regenerative therapy of the heart Arterioscler Thromb Vasc Biol 33 2013 1739 1746
34. A.G.-E. Ibrahim, K. Cheng, and E. Marbán Exosomes as critical agents of cardiac regeneration triggered by cell therapy Stem Cell Rep 2 2014 606 619
35. L. Gangoda, S. Boukouris, M. Liem, H. Kalra, and S. Mathivanan Extracellular vesicles including exosomes are mediators of signal transduction: are they protective or pathogenic? Proteomics 15 2015 260 271
36. M. Lichtenauer, M. Mildner, K. Hoetzenecker, and et al. Secretome of apoptotic peripheral blood cells (APOSEC) confers cytoprotection to cardiomyocytes and inhibits tissue remodelling after acute myocardial infarction: a preclinical study Basic Res Cardiol 106 2011 1283 1297
37. B.J. Haubner, M. Adamowicz-Brice, S. Khadayate, and et al. Complete cardiac regeneration in a mouse model of myocardial infarction Aging 4 2012 966 977