Please wait a minute...
Reviews in Cardiovascular Medicine  2019, Vol. 20 Issue (3): 153-160     DOI: 10.31083/j.rcm.2019.03.528
Review Previous articles | Next articles
New insights into the immunomodulatory role of exosomes in cardiovascular disease
Wenyan Jiang1, Mei Wang2, *()
1 Tangshan People’s Hospital, Tangshan 063000, P. R. China
2 The second hospital of hebei medical university, Shijiazhuang 050011, P. R. China
Download:  PDF(342KB)  ( 760 ) Full text   ( 47 )
Export:  BibTeX | EndNote (RIS)      
Abstract:

Exosomes, nanosized lipid bilayer membranous vesicles, are secreted by a variety of cells and contain protein, lipids, mRNA, miRNA, and signaling molecules that participate in intercellular material transfer and information exchange through binding, fusion or endocytosis. Exosomes mediate the gene expression of target cells and regulate pathological and physiological processes, thereby playing a key role in the occurrence and development of various diseases. Accumulated studies has shown that exosomes hold therapeutic potential though their anti-apoptotic and anti-fibrotic roles. They also have been shown to promote angiogenesis, inhibit ventricular remodeling and improve cardiac function, as well as inhibiting local inflammation and regulating the immune response. As such, exosomes represent a new target for the treatment of cardiovascular diseases. This review summarizes the literature in this field to date, including the basic biological characteristics of exosomes, and new progress in the understanding of the mechanisms of their involvement in immune regulation in cardiovascular diseases. In this way, it servrs as a basis for future research and the development of therapeutic exosomes.

Key words:  Exosomes      immunomodulation      inflammation      cardiovascular diseases     
Submitted:  31 May 2019      Accepted:  16 August 2019      Published:  30 September 2019     
*Corresponding Author(s):  Mei Wang     E-mail:  jiangwenyan9196@sina.com

Cite this article: 

Wenyan Jiang, Mei Wang. New insights into the immunomodulatory role of exosomes in cardiovascular disease. Reviews in Cardiovascular Medicine, 2019, 20(3): 153-160.

URL: 

https://rcm.imrpress.com/EN/10.31083/j.rcm.2019.03.528     OR     https://rcm.imrpress.com/EN/Y2019/V20/I3/153

Figure 1.  Exosomes are secreted.

Figure 2.  Intercellular communication.

1 Abdelwahid, E., Kalvelyte, A., Stulpinas, A., de Carvalho, K. A., Guarita-Souza, L. C. and Foldes, G. (2016). Stem cell death and survival in heart regeneration and repair. Apoptosis: An International Journal on Programmed Cell Death 21, 252-268.
2 Ailawadi, S., Wang, X., Gu, H. and Fan, G. C. (2015) Pathologic function and therapeutic potential of exosomes in cardiovascular disease. Biochim Biophys Acta 1852, 1-11.
3 Baldrich, P., Rutter, B. D., Karimi, H. Z., Podicheti, R., Meyers, B. C. and Innes, R. W. (2019) Plant Extracellular Vesicles Contain Diverse Small RNA Species and Are Enriched in 10- to 17-Nucleotide "Tiny" RNAs. The Plant Cell 31, 315-324.
4 Barile, L., Moccetti, T., Marbán, E. and Vassalli, G. (2017) Roles of exosomes in cardioprotection. European Heart Journal 38, 1372-1379.
5 Beg, F., Wang, R., Saeed, Z., Devaraj, S., Masoor, K. and Nakshatri, H. (2017) Inflammation-associated microRNA changes in circulating exosomes of heart failure patients. BMC Research Notes 10, 751.
6 Bei, Y., Chen, T., Banciu, D. D., Cretoiu, D. and Xiao, J. (2017) Circulating exosomes in cardiovascular diseases. Advances in Experimental Medicine and Biology 998, 255-269.
7 Bellin, G., Gardin, C., Ferroni, L., Chachques, J. C., Rogante, M., Mitrecic, D., Ferrari, R. and Zavan, B. 2019. Exosome in cardiovascular diseases: a complex world full of hope Cells 8, E166
8 Beretti, F., Zavatti, M., Casciaro, F., Comitini, G., Franchi, F., Barbieri, V., La Sala, G. B. and Maraldi, T. (2018) Amniotic fluid stem cell exosomes: Therapeutic perspective. BioFactors 44, 158-167.
9 Bielmann, C., Rignault-Clerc, S., Liaudet, L., Li, F., Kunieda, T., Sogawa, C., Zehnder, T., Waeber, B., Feihl, F. and Rosenblatt-Velin, N. (2015) Brain natriuretic peptide is able to stimulate cardiac progenitor cell proliferation and differentiation in murine hearts after birth. Basic Research in Cardiology 110, 455.
10 Biswas, S. K., Chittezhath, M., Shalova, I. N. and Lim, J. Y. (2012) Macrophage polarization and plasticity in health and disease. Immunologic Research. 53, 11-24.
11 Bobrie, A., Colombo, M., Raposo, G. and Thery, C. (2011) Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12, 1659-1668.
12 Caradec, J., Kharmate, G., Hosseini-Beheshti, E., Adomat, H., Gleave, M. and Guns, E. (2014) Reproducibility and efficiency of serum-derived exosome extraction methods. Clinical Biochemistry 47, 1286-1292.
13 Chan, B. D., Wong, W. Y., Lee, M. M., Cho, W. C., Yee, B. K., Kwan, Y. W. and Tai, W. C. (2019) Exosomes in Inflammation and Inflammatory Disease. Proteomics 19, e1800149.
14 Chen, T., Guo, J., Yang, M., Zhu, X. and Cao, X. (2011) Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. Journal of immunology 186, 2219-2228.
15 Chen, W., Huang, Y., Han, J., Yu, L., Li, Y., Lu, Z., Li, H., Liu, Z., Shi, C., Duan, F. and Xiao, Y. (2016) Immunomodulatory effects of mesenchymal stromal cells-derived exosome. Immunologic Research 64, 831-840.
16 Cho, D. I., Kim, M. R., Jeong, H. Y., Jeong, H. C., Jeong, M. H., Yoon, S. H., Kim, Y. S. and Ahn, Y. (2014) Mesenchymal stem cells reciprocally regulate the M1/M2 balance in mouse bone marrow-derived macrophages. Experimental and Molecular Medicine 4, e70.
17 Coumans, F. A. W., Brisson, A. R., Buzas, E. I., Dignat-George, F., Drees, E. E. E., El-Andaloussi, S., Emanueli, C., Gasecka, A., Hendrix, A., Hill, A. F., Lacroix, R., Lee, Y., van Leeuwen, T. G., Mackman, N., Mager, I., Nolan, J. P., van der Pol, E., Pegtel, D. M., Sahoo, S., Siljander, P. R. M., Sturk, G., de Wever, O. and Nieuwland, R. (2017) Methodological guidelines to study extracellular vesicles. Circulation Research 120, 1632-1648.
18 De Couto, G., Liu, W., Tseliou, E., Sun, B., Makkar, N., Kanazawa, H., Arditi, M. and Marban, E. (2015) Macrophages mediate cardioprotective cellular postconditioning in acute myocardial infarction. The Journal of Clinical Investigation 125, 3147-3162.
19 Diaz-Varela, M., de Menezes-Neto, A., Perez-Zsolt, D., Gamez-Valero, A., Segui-Barber, J., Izquierdo-Useros, N., Martinez-Picado, J., Fernandez-Becerra, C. and Del Portillo, H. A. (2018) Proteomics study of human cord blood reticulocyte-derived exosomes. Scientific Reports 8, 14046.
20 Epelman, S., Lavine,K., J. and Randolph, G. J. (2014) Origin and functions of tissue macrophages. Immunity 41, 21-35.
21 Fernandez-Llama, P., Khositseth, S., Gonzales, P. A., Star, R. A., Pisitkun, T. and Knepper, M. A. (2010) Tamm-Horsfall protein and urinary exosome isolation. Kidney International 77, 736-742.
22 Frangogiannis, N. G. (2014) The inflammatory response in myocardial injury, repair, and remodelling. Nature Reviews Cardiology 11, 255-265.
23 Frantz, S. and Nahrendorf, M. (2014) Cardiac macrophages and their role in ischaemic heart disease. Cardiovascular Research, 102, 240-248.
24 Furlani, D., Ugurlucan, M., Ong, L., Bieback, K., Pittermann, E., Westien, I., Wang, W., Yerebakan, C., Li, W., Gaebel, R., Li, R. K., Vollmar, B., Steinhoff, G. and Ma, N. (2009) Is the intravascular administration of mesenchymal stem cells safe? Mesenchymal stem cells and intravital microscopy. Microvascular Research 77, 370-376.
25 Gao, W., Liu, H., Yuan, J., Wu, C., Huang, D., Ma, Y., Zhu, J., Ma, L., Guo, J., Shi, H., Zou, Y. and Ge, J. (2016) Exosomes derived from mature dendritic cells increase endothelial inflammation and atherosclerosis via membrane TNF-alpha mediated NF-kappaB pathway. Journal of Cellular and Molecular Medicine 20, 2318-2327.
26 Givertz, M. M. and Mann, D. L. (2013) Epidemiology and natural history of recovery of left ventricular function in recent onset dilated cardiomyopathies. Current Heart Failure Reports 10, 321-330.
27 Go, A. S., Mozaffarian, D., Roger, V. L., Benjamin, E. J., Berry, J. D., Borden, W. B., Bravata, D. M., Dai, S., Ford, E. S., Fox, C. S., Franco, S., Fullerton, H. J., Gillespie, C., Hailpern, S. M., Heit, J. A., Howard, V. J., Huffman, M. D., Kissela, B. M., Kittner, S. J., Lackland, D. T., Lichtman, J. H., Lisabeth, L. D., Magid, D., Marcus, G. M., Marelli, A., Matchar, D. B., McGuire, D. K., Mohler, E. R., Moy, C. S., Mussolino, M. E., Nichol, G., Paynter, N. P., Schreiner, P. J., Sorlie, P. D., Stein, J., Turan, T. N., Virani, S. S., Wong, N. D., Woo, D., Turner, M. B., American heart association, s. atistics committee and stroke statistics, s. bcommittee. (2013) Heart disease and stroke statistics-2013 update: a report from the american heart association. Circulation 127, e6-e245.
28 Gurunathan, S., Kang, M. H., Jeyaraj, M., Qasim, M. and Kim, J. H. (2019) Review of the isolation, characterization, biological function, and multifarious therapeutic approaches of exosomes. Cells 8, 307.
29 Hashimoto, H., Olson, E. N. and Bassel-Duby, R. (2018) Therapeutic approaches for cardiac regeneration and repair. Nature Reviews Cardiology 15, 585-600.
30 Hong, C. S., Funk, S., Muller, L., Boyiadzis, M. and Whiteside, T. L. (2016) Isolation of biologically active and morphologically intact exosomes from plasma of patients with cancer. Journal of Extracellular Vesicles 5, 29289.
31 Horckmans, M., Ring, L., Duchene, J., Santovito, D., Schloss, M. J., Drechsler, M., Weber, C., Soehnlein, O. and Steffens, S. (2017) Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype. European Heart Journal 38, 187-197.
32 Hsu, C., Morohashi, Y., Yoshimura, S., Manrique-Hoyos, N., Jung, S., Lauterbach, M. A., Bakhti, M., Gronborg, M., Mobius, W., Rhee, J., Barr, F. A. and Simons, M. (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. The Journal of Cell Biology 189, 223-232.
33 Huang, P., Wang, L., Li, Q., Tian, X., Xu, J., Xu, J., Xiong, Y., Chen, G., Qian, H., Jin, C., Yu, Y., Cheng, K., Qian, L. and Yang, Y. (2019) Atorvastatin enhances the therapeutic efficacy of mesenchymal stem cells derived exosomes in acute myocardial infarction via up-regulating Long Non-coding RNA H19. Cardiovascular Research, cvz139.
34 International Stem Cell, Initiative. (2018) Assessment of established techniques to determine developmental and malignant potential of human pluripotent stem cells. Nature communications 9, 1925.
35 Jeong, J. O., Han, J. W., Kim, J. M., Cho, H. J., Park, C., Lee, N., Kim, D. W. and Yoon, Y. S. (2011) Malignant tumor formation after transplantation of short-term cultured bone marrow mesenchymal stem cells in experimental myocardial infarction and diabetic neuropathy. Circulation Research 108, 1340-1347.
36 Ju, C., Li, Y., Shen, Y., Liu, Y., Cai, J., Liu, N., Ma, G. and Tang, Y. (2018) Transplantation of cardiac mesenchymal stem cell-derived exosomes for angiogenesis. Journal of Cardiovascular Translational Research 11, 429-437.
37 Kalluri, R. (2016) The biology and function of exosomes in cancer. The Journal of clinical investigation 126, 1208-1215.
38 Khalyfa, A. and Gozal, D. (2014) Exosomal miRNAs as potential biomarkers of cardiovascular risk in children. Journal of Translational Medicine 12, 162.
39 Khan, M., Nickoloff, E., Abramova, T., Johnson, J., Verma, S. K., Krishnamurthy, P., Mackie, A. R., Vaughan, E., Garikipati, V. N., Benedict, C., Ramirez, V., Lambers, E., Ito, A., Gao, E., Misener, S., Luongo, T., Elrod, J., Qin, G., Houser, S. R., Koch, W. J. and Kishore, R. (2015) Embryonic stem cell-derived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circulation Research 117, 52-64.
40 Koelwyn, G. J., Corr, E. M., Erbay, E. and Moore, K. J. (2018) Regulation of macrophage immunometabolism in atherosclerosis. Nature Immunology 19, 526-537.
41 Konala, V. B., Mamidi, M. K., Bhonde, R., Das, A. K., Pochampally, R. and Pal, R. (2016) The current landscape of the mesenchymal stromal cell secretome: A new paradigm for cell-free regeneration. Cytotherapy 18, 13-24.
42 Kowal, J., Tkach, M. and Thery, C. (2014) Biogenesis and secretion of exosomes. Current Opinion in Cell Biology 29, 116-125.
43 Lalit, P. A., Hei, D. J., Raval, A. N. and Kamp, T. J. (2014) Induced pluripotent stem cells for post-myocardial infarction repair: remarkable opportunities and challenges. Circulation Research 114, 1328-1345.
44 Lamichhane, T. N., Sokic, S., Schardt, J. S., Raiker, R. S., Lin, J. W. and Jay, S. M. (2015) Emerging roles for extracellular vesicles in tissue engineering and regenerative medicine. Tissue Engineering. Part B, Reviews 21, 45-54.
45 Lankford, K. L., Arroyo, E. J., Nazimek, K., Bryniarski, K., Askenase, P. W. and Kocsis, J. D. (2018) Intravenously delivered mesenchymal stem cell-derived exosomes target M2-type macrophages in the injured spinal cord. PloS One 13, e0190358.
46 Lazar, E., Benedek, T., Korodi, S., Rat, N., Lo, J. and Benedek, I. (2018) Stem cell-derived exosomes - an emerging tool for myocardial regeneration. World Journal of Stem Cells 10, 106-115.
47 Lespagnol, A., Duflaut, D., Beekman, C., Blanc, L., Fiucci, G., Marine, J. C., Vidal, M., Amson, R. and Telerman, A. (2008) Exosome secretion, including the DNA damage-induced p53-dependent secretory pathway, is severely compromised in TSAP6/Steap3-null mice. Cell Death and Differentiation 15, 1723-1733.
48 Li, J., Xue, H., Li, T., Chu, X., Xin, D., Xiong, Y., Qiu, W., Gao, X., Qian, M., Xu, J., Wang, Z. and Li, G. (2019 a) Exosomes derived from mesenchymal stem cells attenuate the progression of atherosclerosis in ApoE(-/-) mice via miR-let7 mediated infiltration and polarization of M2 macrophage. Biochemical and Biophysical Research Communications 510, 565-572.
49 Li, N., Rochette, L., Wu, Y. and Rosenblatt-Velin, N. (2019b) New Insights into the Role of Exosomes in the Heart After Myocardial Infarction. Journal of Cardiovascular Translational Research 12, 18-27.
50 Li, P., Kaslan, M., Lee, S. H., Yao, J. and Gao, Z. (2017) Progress in Exosome Isolation Techniques. Theranostics 7, 789-804.
51 Li, S., Li, Y., Chen, B., Zhao, J., Yu, S., Tang, Y., Zheng, Q., Li, Y., Wang, P., He, X. and Huang, S. (2018) exoRBase: a database of circRNA, lncRNA and mRNA in human blood exosomes. Nucleic Acids Research 46, D106-D112.
52 Liu, J., Jiang, M., Deng, S., Lu, J., Huang, H., Zhang, Y., Gong, P., Shen, X., Ruan, H., Jin, M. and Wang, H. (2018) miR-93-5p-Containing exosomes treatment attenuates acute myocardial infarction-induced myocardial damage. molecular therapy. Nucleic Acids 11, 103-115.
53 Luo, Z., Wu, F., Xue, E., Huang, L., Yan, P., Pan, X. and Zhou, Y. (2019) Hypoxia preconditioning promotes bone marrow mesenchymal stem cells survival by inducing HIF-1alpha in injured neuronal cells derived exosomes culture system. Cell Death & Disease 10, 134.
54 Ma, T., Chen, Y., Chen, Y., Meng, Q., Sun, J., Shao, L., Yu, Y., Huang, H., Hu, Y., Yang, Z., Yang, J. and Shen, Z. (2018) MicroRNA-132, Delivered by mesenchymal stem cell-derived exosomes, promote angiogenesis in myocardial infarction. Stem Cells International 2018,3290372.
55 Maas, S. L. N., Breakefield, X. O. and Weaver, A. M. (2017) Extracellular vesicles: unique intercellular delivery vehicles. Trends in Cell Biology 27, 172-188.
56 Mashouri, L., Yousefi, H., Aref, A. R., Ahadi, A. M., Molaei, F. and Alahari, S. K. (2019) Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Molecular Cancer 18, 75.
57 Mentkowski, K. I., Snitzer, J. D., Rusnak, S. and Lang, J. K. (2018) Therapeutic potential of engineered extracellular vesicles. The AAPS journal 20, 50.
58 Namazi, H., Mohit, E., Namazi, I., Rajabi, S., Samadian, A., Hajizadeh-Saffar, E., Aghdami, N. and Baharvand, H. (2018) Exosomes secreted by hypoxic cardiosphere-derived cells enhance tube formation and increase pro-angiogenic miRNA. Journal of Cellular Biochemistry 119, 4150-4160.
59 Nichols, M., Townsend, N., Scarborough, P. and Rayner, M. (2014) Cardiovascular disease in Europe 2014: epidemiological update. European Heart Journal 35, 2929.
60 Ostrowski, M., Carmo, N. B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C. F., Schauer, K., Hume, A. N., Freitas, R. P., Goud, B., Benaroch, P., Hacohen, N., Fukuda, M., Desnos, C., Seabra, M. C., Darchen, F., Amigorena, S., Moita, L. F. and Thery, C. (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nature Cell Biology 12, 19-30.
61 Pan, J., Alimujiang, M., Chen, Q., Shi, H. and Luo, X. (2019a). Exosomes derived from miR-146a-modified adipose-derived stem cells attenuate acute myocardial infarction-induced myocardial damage via downregulation of early growth response factor 1. Journal of Cellular Biochemistry 120, 4433-4443.
62 Pan, W., Zhu, Y., Meng, X., Zhang, C., Yang, Y. and Bei, Y. (2019b) Immunomodulation by exosomes in myocardial infarction. Journal of Cardiovascular Translational Research 12, 28-36.
63 Pant, S., Hilton, H. and Burczynski, M. E. (2012) The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochemical Pharmacology 83, 1484-1494.
64 Parolini, I., Federici, C., Raggi, C., Lugini, L., Palleschi, S., De Milito, A., Coscia, C., Iessi, E., Logozzi, M., Molinari, A., Colone, M., Tatti, M., Sargiacomo, M. and Fais, S. (2009) Microenvironmental pH is a key factor for exosome traffic in tumor cells. The Journal of Biological Chemistry 284, 34211-34222.
65 Pathan, M., Fonseka, P., Chitti, S. V., Kang, T., Sanwlani, R., Van Deun, J., Hendrix, A. and Mathivanan, S. (2019) Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic Acids Research 47, D516-D519.
66 Poe, A. J. and Knowlton, A. A. (2018) Exosomes and cardiovascular cell-cell communication. Essays in Biochemistry 62, 193-204.
67 Prabhu, S. D. and Frangogiannis, N. G. (2016) The biological basis for cardiac repair after myocardial infarction: from inflammation to fibrosis. Circulation Research 119, 91-112.
68 Raggi, P., Genest, J., Giles, J. T., Rayner, K. J., Dwivedi, G., Beanlands, R. S. and Gupta, M. (2018) Role of inflammation in the pathogenesis of atherosclerosis and therapeutic interventions. Atherosclerosis 276, 98-108.
69 Raposo, G. and Stoorvogel, W. (2013) Extracellular vesicles: exosomes, microvesicles, and friends. The Journal of Cell Biology 200, 373-383.
70 Record, M. (2014) Intercellular communication by exosomes in placenta: a possible role in cell fusion? Placenta 35, 297-302.
71 Ren, K. (2018) Exosomes in perspective: a potential surrogate for stem cell therapy. Odontology 107, 271-284.
72 Ren, K. (2019) Exosomes in perspective: a potential surrogate for stem cell therapy. Odontology 107, 271-284.
73 Sahoo, S. and Losordo, D. W. (2014) Exosomes and cardiac repair after myocardial infarction. Circulation Research 114, 333-344.
74 Savina, A., Furlan, M., Vidal, M. and Colombo, M. I. (2003) Exosome release is regulated by a calcium-dependent mechanism in K562 cells. The Journal of Biological Chemistry 278, 20083-20090.
75 Schageman, J., Zeringer, E., Li, M., Barta, T., Lea, K., Gu, J., Magdaleno, S., Setterquist, R. and Vlassov, A. V.(2013) The complete exosome workflow solution: from isolation to characterization of RNA cargo. Biomed Research International 2013,253957.
76 Segura, E., Guerin, C., Hogg, N., Amigorena, S. and Thery, C. (2007) CD 8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo. Journal of Immunology 179, 1489-1496.
77 Shao, L., Zhang, Y., Lan, B., Wang, J., Zhang, Z., Zhang, L., Xiao, P., Meng, Q., Geng, Y. J., Yu, X. Y. and Li, Y. (2017) MiRNA-sequence indicates that mesenchymal stem cells and exosomes have similar mechanism to enhance cardiac repair. Biomed Research International 2017,4150705.
78 van de Vrie, M., Heymans, S. and Schroen, B. (2011) MicroRNA involvement in immune activation during heart failure. Cardiovascular Drugs and Therapy 25, 161-170.
79 Vlassov, A. V., Magdaleno, S., Setterquist, R. and Conrad, R. (2012) Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochimica et Biophysica Acta 1820, 940-948.
80 Wang, W., Zheng, Y., Wang, M., Yan, M., Jiang, J. and Li, Z. (2019) Exosomes derived miR-126 attenuates oxidative stress and apoptosis from ischemia and reperfusion injury by targeting ERRFI1. Gene 690, 75-80.
81 Wang, X., Chen, Y., Zhao, Z., Meng, Q., Yu, Y., Sun, J., Yang, Z., Chen, Y., Li, J., Ma, T., Liu, H., Li, Z., Yang, J. and Shen, Z. (2018) Engineered exosomes with ischemic myocardium-targeting peptide for targeted therapy in myocardial infarction. Journal of the American Heart Association 7, e008737.
82 Yanan, W., Yingyu, X., Ao, Z., Mingyang, W., Zihan, F. and Junping, Z. (2019) Exosomes: an emerging factor in atherosclerosis. Biomedicine & Pharmacotherapy 115, 108951.
83 Yanez-Mo, M., Siljander, P. R., Andreu, Z., Zavec, A. B., Borras, F. E., Buzas, E. I., Buzas, K., Casal, E., Cappello, F., Carvalho, J., Colas, E., Cordeiro-da Silva, A., Fais, S., Falcon-Perez, J. M., Ghobrial, I. M., Giebel, B., Gimona, M., Graner, M., Gursel, I., Gursel, M., Heegaard, N. H., Hendrix, A., Kierulf, P., Kokubun, K., Kosanovic, M., Kralj-Iglic, V., Kramer-Albers, E. M., Laitinen, S., Lasser, C., Lener, T., Ligeti, E., Line, A., Lipps, G., Llorente, A., Lotvall, J., Mancek-Keber, M., Marcilla, A., Mittelbrunn, M., Nazarenko, I., Nolte-'t Hoen, E. N., Nyman, T. A., O'Driscoll, L., Olivan, M., Oliveira, C., Pallinger, E., Del Portillo, H. A., Reventos, J., Rigau, M., Rohde, E., Sammar, M., Sanchez-Madrid, F., Santarem, N., Schallmoser, K., Ostenfeld, M. S., Stoorvogel, W., Stukelj, R., Van der Grein, S. G., Vasconcelos, M. H., Wauben, M. H. and De Wever, O. (2015) Biological properties of extracellular vesicles and their physiological functions. Journal of Extracellular Vesicles 4, 27066.
84 Yang, J., Zhang, X., Chen, X., Wang, L. and Yang, G. (2017) Exosome mediated delivery of miR-124 promotes neurogenesis after ischemia. Molecular Therapy-Nucleic Acids 7, 278-287.
85 Yang, P. C. (2018) Induced pluripotent stem cell (iPSC)-derived exosomes for precision medicine in heart failure. Circulation Research 122, 661-663.
86 Ye, W., Tang, X., Yang, Z., Liu, C., Zhang, X., Jin, J. and Lyu, J. (2017) Plasma-derived exosomes contribute to inflammation via the TLR9-NF-kappaB pathway in chronic heart failure patients. Molecular Immunology 87, 114-121.
87 Yellon, D. M. and Davidson, S. M. (2014) Exosomes: nanoparticles involved in cardioprotection? Circulation Research 114, 325-332.
88 Yuan, O., Lin, C., Wagner, J., Archard, J. A., Deng, P., Halmai, J., Bauer, G., Fink, K. D., Fury, B., Perotti, N. H., Walker, J. E., Pollock, K., Apperson, M., Butters, J., Belafsky, P., Farwell, D. G., Kuhn, M., Nolta, J. and Anderson, J. D. (2019) Exosomes derived from human primed mesenchymal stem cells induce mitosis and potentiate growth factor secretion. Stem Cells and Development 28, 398-409.
89 Zaim, M., Karaman, S., Cetin, G. and Isik, S. (2012) Donor age and long-term culture affect differentiation and proliferation of human bone marrow mesenchymal stem cells. Annals of Hematology 91, 1175-1186.
90 Zhang, Y., Liu, Y., Liu, H. and Tang, W. H. (2019) Exosomes: biogenesis, biologic function and clinical potential. Cell & Bioscience 9, 19.
91 Zhao, J., Li, X., Hu, J., Chen, F., Qiao, S., Sun, X., Gao, L., Xie, J. and Xu, B. (2019) Mesenchymal stromal cell-derived exosomes attenuate myocardial ischaemia-reperfusion injury through miR-182-regulated macrophage polarization. Cardiovascular Research 115, 1205-1216.
92 Zhu, L. P., Tian, T., Wang, J. Y., He, J. N., Chen, T., Pan, M., Xu, L., Zhang, H. X., Qiu, X. T., Li, C. C., Wang, K. K., Shen, H., Zhang, G. G. and Bai, Y. P. (2018) Hypoxia-elicited mesenchymal stem cell-derived exosomes facilitates cardiac repair through miR-125b-mediated prevention of cell death in myocardial infarction. Theranostics 8, 6163-6177.
93 Zysset, D., Weber, B., Rihs, S., Brasseit, J., Freigang, S., Riether, C., Banz, Y., Cerwenka, A., Simillion, C., Marques-Vidal, P., Ochsenbein, A. F., Saurer, L. and Mueller, C. (2016) TREM-1 links dyslipidemia to inflammation and lipid deposition in atherosclerosis. Nature Communications 7, 13151.
[1] Adila A Hamid, Amilia Aminuddin, Mohd Heikal Mohd Yunus, Jaya Kumar Murthy, Chua Kien Hui, Azizah Ugusman. Antioxidative and anti-inflammatory activities of Polygonum minus: a review of literature[J]. Reviews in Cardiovascular Medicine, 2020, 21(2): 275-287.
[2] Shanna J. Hardin, Mahavir Singh, Wintana Eyob, Jack C. Molnar, Rubens P. Homme, Akash K. George, Suresh C. Tyagi. Diet-induced chronic syndrome, metabolically transformed trimethylamine-N-oxide, and the cardiovascular functions[J]. Reviews in Cardiovascular Medicine, 2019, 20(3): 121-128.
[3] Jing Jin, Yufeng Liu, Lihong Huang, Hong Tan. Advances in epigenetic regulation of vascular aging[J]. Reviews in Cardiovascular Medicine, 2019, 20(1): 19-25.
[4] Alberto Palazzuoli, Helen Hashemi, Lauren C. Jameson, Peter A. McCullough. Hyperuricemia and Cardiovascular Disease[J]. Reviews in Cardiovascular Medicine, 2017, 18(4): 134-145.
[5] Virginia A. Triant. Epidemiology of Coronary Heart Disease in Patients With Human Immunodeficiency Virus[J]. Reviews in Cardiovascular Medicine, 2014, 15(S1): 1-8.
[6] Paolo Gresele, Emanuela Falcinelli, Stefania Momi, Daniela Francisci, Franco Baldelli. Highly Active Antiretroviral Therapy–related Mechanisms of Endothelial and Platelet Function Alterations[J]. Reviews in Cardiovascular Medicine, 2014, 15(S1): 9-20.
[7] Shrinivas Hebsur, Erik Vakil, William J. Oetgen, Princy N. Kumar, Daisy F. Lazarous. Influenza and Coronary Artery Disease: Exploring a Clinical Association With Myocardial Infarction and Analyzing the Utility of Vaccination in Prevention of Myocardial Infarction[J]. Reviews in Cardiovascular Medicine, 2014, 15(2): 168-175.
[8] Sophie Mavrogeni, Fabrizio Cantini, Gerald M. Pohost. Systemic Vasculitis: An Underestimated Cause of Heart Failure—Assessment by Cardiovascular Magnetic Resonance[J]. Reviews in Cardiovascular Medicine, 2013, 14(1): 49-55.
[9] Karol E. Watson, Benjamin J. Ansell, Andrew D. Watson, Gregg C. Fonarow. HDL Function as a Target of Lipid-Modifying Therapy[J]. Reviews in Cardiovascular Medicine, 2007, 8(1): 1-8.
[10] Dean J. Kereiakes. Effects of GP IIb/IIIa Inhibitors on Vascular Inflammation, Coronary Microcirculation, and Platelet Function[J]. Reviews in Cardiovascular Medicine, 2006, 7(S4): 3-11.
[11] David M. Herrington, Karen Potvin Klein. Effects of Estrogen on Thrombosis and Inflammation[J]. Reviews in Cardiovascular Medicine, 2002, 3(1): 49-56.
[12] Kuang-Yuh Chyu, Prediman K. Shah. The Role of Inflammation in Plaque Disruption and Thrombosis[J]. Reviews in Cardiovascular Medicine, 2001, 2(2): 82-91.
[13] Robert A. Vogel. Update on Inflammatory Markers[J]. Reviews in Cardiovascular Medicine, 2001, 2(2): 94-96.
No Suggested Reading articles found!