Mesenchymal stem cells-derived extracellular vesicles, via miR-210, improve infarcted cardiac function by promotion of angiogenesis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1863, Issue 8, 2017, Pages 2085-2092

  Wang, Na ^a   Chen, Caiyu ^a   Yang, Dezhong ^a   Liao, Qiao ^a   Luo, Hao ^a   Wang, Xinquan ^a   Zhou, Faying ^a   Yang, Xiaoli ^a   Yang, Jian ^a   Zeng, Chunyu ^a   Wang, Wei Eric ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Angiogenesis; Extracellular vesicles; Mesenchymal stem cells; MicroRNA; Myocardial infarction

Indexed keywords

CD31 ANTIGEN; MICRORNA 210; MICRORNA; MIRN210 MICRORNA, HUMAN; MIRN210 MICRORNA, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY PROLIFERATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; ECHOCARDIOGRAPHY; EXOSOME; GENE SILENCING; HEART FUNCTION; HEART INFARCTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TREATMENT OUTCOME; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; GENETICS; MEMBRANE MICROPARTICLE; METABOLISM; PATHOLOGY; TRANSPLANTATION;

ANIMALS; CELL-DERIVED MICROPARTICLES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MESENCHYMAL STEM CELLS; MICE; MICRORNAS; MYOCARDIAL INFARCTION; NEOVASCULARIZATION, PHYSIOLOGIC;

EID: 85014678566     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2017.02.023     Document Type: Article

References (43)

1. MacIntyre, C.R., Mahimbo, A., Moa, A.M., Barnes, M., Influenza vaccine as a coronary intervention for prevention of myocardial infarction. Heart 102 (2016), 1953–1956.
2. Cortez-Dias, N., Costa, M.C., Carrilho-Ferreira, P., Silva, D., Jorge, C., Calisto, C., Pessoa, T., Robalo Martins, S., de Sousa, J.C., da Silva, P.C., Fiuza, M., Diogo, A.N., Pinto, F.J., Enquita, F.J., Circulating miR-122-5p/miR-133b ratio is a specific early prognostic biomarker in acute myocardial infarction. Circ. J. 80 (2016), 2183–2191.
3. Yuan, M.J., Wang, T., Kong, B., Wang, X., Huang, C.X., Wang, D., GHSR-1a is a novel pro-angiogenic and anti-remodeling target in rats after myocardial infarction. Eur. J. Pharmacol. 788 (2016), 218–225.
4. Heusch, G., Molecular basis of cardioprotection: signal transduction in ischemic pre-, post-, and remote conditioning. Circ. Res. 116 (2015), 674–699.
5. Senturk, T., Cavun, S., Avci, B., Yermezler, A., Serdar, Z., Savci, V., Effective inhibition of cardiomyocyte apoptosis through the combination of trimetazidine and N-acetylcysteine in a rat model of myocardial ischemia and reperfusion injury. Atherosclerosis 237 (2014), 760–766.
6. Zhao, L., Liu, X., Zhang, Y., Liang, X., Ding, Y., Xu, Y., Fang, Z., Zhang, F., Enhanced cell survival and paracrine effects of mesenchymal stem cells overexpressing hepatocyte growth factor promote cardioprotection in myocardial infarction. Exp. Cell Res. 344 (2016), 30–39.
7. Shalaby, S.M., El-Shal, A.S., Zidan, H.E., Mazen, N.F., Abd El-Haleem, M.R., Abd El Motteleb, D.M., Comparing the effects of MSCs and CD34 + cell therapy in a rat model of myocardial infarction. IUBMB Life 68 (2016), 343–354.
8. Miao, Q., Shim, W., Tee, N., Lim, S.Y., Chung, Y.Y., Ja, K.P., Ooi, T.H., Tan, G., Kong, G., Wei, H., Lim, C.H., Sin, Y.K., Wong, P., iPSC-derived human mesenchymal stem cells improve myocardial strain of infarcted myocardium. J. Cell. Mol. Med. 18 (2014), 1644–1654.
9. Motavaf, M., Pakravan, K., Babashah, S., Malekvandfard, F., Masoumi, M., Sadeghizadeh, M., Therapeutic application of mesenchymal stem cell-derived exosomes: a promising cell-free therapeutic strategy in regenerative medicine. Cell. Mol. Biol. 62 (2016), 74–79.
10. Desrochers, L.M., Bordeleau, F., Reinhart-King, C.A., Cerione, R.A., Antonyak, M.A., Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat. Commun., 7, 2016, 11958.
11. Loyer, X., Vion, A.C., Tedgui, A., Boulanger, C.M., Microvesicles as cell-cell messengers in cardiovascular diseases. Circ. Res. 114 (2014), 345–353.
12. Cantaluppi, V., Gatti, S., Medica, D., Figliolini, F., Bruno, S., Deregibus, M.C., Sordi, A., Biancone, L., Tetta, C., Camussi, G., Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 82 (2012), 412–427.
13. Mocharla, P., Briand, S., Giannotti, G., Dorries, C., Jakob, P., Paneni, F., Luscher, T., Landmesser, U., AngiomiR-126 expression and secretion from circulating CD34(+) and CD14(+) PBMCs: role for proangiogenic effects and alterations in type 2 diabetics. Blood 121 (2013), 226–236.
14. Kishore, R., Khan, M., Cardiac cell-derived exosomes: changing face of regenerative biology. Eur. Heart J., 2016 (Epub ahead of print).
15. Bian, S., Zhang, L., Duan, L., Wang, X., Min, Y., Yu, H., Extracellular vesicles derived from human bone marrow mesenchymal stem cells promote angiogenesis in a rat myocardial infarction model. J. Mol. Med. 92 (2014), 387–397.
16. Teng, X., Chen, L., Chen, W., Yang, J., Yang, Z., Shen, Z., Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation., 37, 2015, 2415–2424.
17. Yu, J.M., Zhang, X.B., Jiang, W., Wang, H.D., Zhang, Y.N., Astragalosides promote angiogenesis via vascular endothelial growth factor and basic fibroblast growth factor in a rat model of myocardial infarction. Mol. Med. Rep. 12 (2015), 6718–6726.
18. Garikipati, V.N., Krishnamurthy, P., Verma, S.K., Khan, M., Abramova, T., Mackie, A.R., Qin, G., Benedict, C., Nickoloff, E., Johnson, J., Gao, E., Losordo, D.W., Houser, S.R., Koch, W.J., Kishore, R., Negative regulation of miR-375 by interleukin-10 enhances bone marrow-derived progenitor cell-mediated myocardial repair and function after myocardial infarction. Stem Cells 33 (2015), 3519–3529.
19. Vallabhaneni, K.C., Penfornis, P., Dhule, S., Guillonneau, F., Adams, K.V., Mo, Y.Y., Xu, R., Liu, Y., Watabe, K., Vemuri, M.C., Pochampally, R., Extracellular vesicles from bone marrow mesenchymal stem/stromal cells transport tumor regulatory microRNA, proteins, and metabolites. Oncotarget 6 (2015), 4953–4967.
20. Kim, G.Y., Park, J.H., Kim, H., Lim, H.J., Park, H.Y., Coronin 1B serine 2 phosphorylation by p38alpha is critical for vascular endothelial growth factor-induced migration of human umbilical vein endothelial cells. Cell. Signal. 28 (2016), 1817–1825.
21. Yu, N., Yang, Y., Li, X., Zhang, M., Huang, J., Wang, X., Long, X., MiR-26a inhibits proliferation and migration of HaCaT keratinocytes through regulating PTEN expression. Gene 594 (2016), 117–124.
22. Kohler, E.E., Baruah, J., Urao, N., Ushio-Fukai, M., Fukai, T., Chatterjee, I., Wary, K.K., Low-dose 6-bromoindirubin-3′-oxime induces partial dedifferentiation of endothelial cells to promote increased neovascularization. Stem Cells 32 (2014), 1538–1552.
23. Deng, L., Blanco, F.J., Stevens, H., Lu, R., Caudrillier, A., McBride, M.W., McClure, J.D., Grant, J.S., Thomas, M., Frid, M.G., Stenmark, K.R., White, K., Seto, A.G., Morrell, N.W., Bradshaw, A.C., MacLean, M.R., Baker, A.H., miR-143 activation regulates smooth muscle and endothelial cell crosstalk in pulmonary arterial hypertension. Circ. Res. 117 (2015), 870–883.
24. Cai, J., Han, Y., Ren, H., Chen, C., He, D., Zhou, L.E., G. M., Asico, L.D., Jose, P.A., Zeng, C., Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J. Mol. Cell Biol. 5 (2013), 227–238.
25. Conforti, A., Scarsella, M., Starc, N., Giorda, E., Biagini, S., Proia, A., Carsetti, R., Locatelli, F., Bernardo, M.E., Microvescicles derived from mesenchymal stromal cells are not as effective as their cellular counterpart in the ability to modulate immune responses in vitro. Stem Cells Dev. 23 (2014), 2591–2599.
26. Gomes, J., Gomes-Alves, P., Carvalho, S.B., Peixoto, C., Alves, P.M., Altevogt, P., Costa, J., Extracellular vesicles from ovarian carcinoma cells display specific glycosignatures. Biomolecules 5 (2015), 1741–1761.
27. Berchem, G., Noman, M.Z., Bosseler, M., Paggetti, J., Baconnais, S., Le Cam, E., Nanbakhsh, A., Moussay, E., Mami-Chouaib, F., Janji, B., Chouaib, S., Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-beta and miR23a transfer. Oncoimmunology, 5, 2016, e1062968.
28. Bruno, S., Collino, F., Deregibus, M.C., Grange, C., Tetta, C., Camussi, G., Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev. 22 (2013), 758–771.
29. Pang, P., Abbott, M., Chang, S.L., Abdi, M., Chauhan, N., Mistri, M., Ghofrani, J., Fucci, Q.A., Walker, C., Leonardi, C., Grady, S., Halim, A., Hoffman, R., Lu, T., Cao, H., Tullius, S.G., Malek, S., Kumar, S., Steele, G., Kibel, A., Freedman, B.S., Waikar, S.S., Siedlecki, A.M., Human vascular progenitor cells derived from renal arteries are endothelial-like and assist in the repair of injured renal capillary networks. Kidney Int. 91 (2017), 129–143.
30. Belting, M., Christianson, H.C., Role of exosomes and microvesicles in hypoxia-associated tumour development and cardiovascular disease. J. Intern. Med. 278 (2015), 251–263.
31. Fasanaro, P., D'Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., Capogrossi, M.C., Martelli, F., MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3., 283, 2008, 15878–15883.
32. Hu, S., Huang, M., Li, Z., Jia, F., Ghosh, Z., Lijkwan, M.A., Fasanaro, P., Sun, N., Wang, X., Martelli, F., Robbins, R.C., Wu, J.C., MicroRNA-210 as a novel therapy for treatment of ischemic heart disease., 122, 2010, S124–S131.
33. Dang, K., Myers, K.A., The role of hypoxia-induced miR-210 in cancer progression. Int. J. Mol. Sci. 16 (2015), 6353–6372.
34. Kim, S.W., Houge, M., Brown, M., Davis, M.E., Yoon, Y.S., Cultured human bone marrow-derived CD31(+) cells are effective for cardiac and vascular repair through enhanced angiogenic, adhesion, and anti-inflammatory effects. J. Am. Coll. Cardiol. 64 (2014), 1681–1694.
35. Wang, W.E., Yang, D., Li, L., Wang, W., Peng, Y., Chen, C., Chen, P., Xia, X., Wang, H., Jiang, J., Liao, Q., Li, Y., Xie, G., Huang, H., Guo, Y., Ye, L., Duan, D.D., Chen, X., Houser, S.R., Zeng, C., Prolyl hydroxylase domain protein 2 silencing enhances the survival and paracrine function of transplanted adipose-derived stem cells in infarcted myocardium. Circ. Res. 113 (2013), 288–300.
36. Leca, J., Martinez, S., Lac, S., Nigri, J., Secq, V., Rubis, M., Bressy, C., Serge, A., Lavaut, M.N., Dusetti, N., Loncle, C., Roques, J., Pietrasz, D., Bousquet, C., Garcia, S., Granjeaud, S., Ouaissi, M., Bachet, J.B., Brun, C., Iovanna, J.L., Zimmermann, P., Vasseur, S., Tomasini, R., Cancer-associated fibroblast-derived annexin A6 + extracellular vesicles support pancreatic cancer aggressiveness. J. Clin. Invest. 126 (2016), 4140–4156.
37. Hu, G.W., Li, Q., Niu, X., Hu, B., Liu, J., Zhou, S.M., Guo, S.C., Lang, H.L., Zhang, C.Q., Wang, Y., Deng, Z.F., Exosomes secreted by human-induced pluripotent stem cell-derived mesenchymal stem cells attenuate limb ischemia by promoting angiogenesis in mice. Stem Cell Res. Ther., 6, 2015, 10.
38. Das, S., Halushka, M.K., Extracellular vesicle microRNA transfer in cardiovascular disease. Cardiovasc. Pathol. 24 (2015), 199–206.
39. Fleury, A., Martinez, M.C., Le Lay, S., Extracellular vesicles as therapeutic tools in cardiovascular diseases. Front. Immunol., 5, 2014, 370.
40. Ibrahim, A.G., Cheng, K., Marban, E., Exosomes as critical agents of cardiac regeneration triggered by cell therapy. Stem Cell Rep. 2 (2014), 606–619.
41. Chen, T.S., Lai, R.C., Lee, M.M., Choo, A.B., Lee, C.N., Lim, S.K., Mesenchymal stem cell secretes microparticlesenriched in pre-microRNAs. Nucleic Acids Res. 38 (2010), 215–224.
42. Hu, S., Huang, M., Li, Z., Jia, F., Ghosh, Z., Lijkwan, M.A., Fasanaro, P., Sun, N., Wang, X., Martelli, F., Robbins, R.C., Wu, J.C., MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 122 (2010), S124–S131.
43. Xiao, F., Qiu, H., Zhou, L., Shen, X., Yang, L., Ding, K., WSS25 inhibits Dicer, downregulating microRNA-210, which targets Ephrin-A3, to suppress human microvascular endothelial cell (HMEC-1) tube formation. Glycobiology 23 (2013), 524–535.