Endothelial miRNAs as Cellular Messengers in Cardiometabolic Diseases.

[en] Metabolic syndrome is a clustering of risk factors that increases susceptibility to serious cardiometabolic complications, including type 2 diabetes (T2D) and myocardial infarction. Understanding the underlying mechanisms will advance the development of diagnostic and therapeutic approaches. A prominent feature of cardiometabolic diseases is endothelial dysfunction. Endothelial cell (EC) homeostasis and response to pathological stimuli are controlled by gene regulatory networks in which miRNAs play a critical role. Recently, miRNAs have been implicated as cell-cell messengers that can influence cellular function. This review investigates the known and potential roles for miRNA-based cell-cell communication in the control of cardiovascular health and explores the value of identifying miRNA biomarkers and developing therapeutics that harness or antagonize miRNA-based communication.

Disciplines :

Cardiovascular & respiratory systems

Author, co-author :

Njock, Makon-Sébastien ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Fish, Jason E.; University Health Network, Toronto, Canada > Toronto General Hospital Research Institute > Advanced Diagnostics

Language :

English

Title :

Endothelial miRNAs as Cellular Messengers in Cardiometabolic Diseases.

Publication date :

March 2017

Journal title :

Trends in Endocrinology and Metabolism

ISSN :

1043-2760

eISSN :

1879-3061

Publisher :

Elsevier, Netherlands

Volume :

Issue :

Pages :

237-246

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 05 January 2018

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Bibliography

1 Ebert, M.S., Sharp, P.A., Roles for microRNAs in conferring robustness to biological processes. Cell 149 (2012), 515–524.
2 Araldi, E., Suárez, Y., MicroRNAs as regulators of endothelial cell functions in cardiometabolic diseases. Biochim. Biophys. Acta 1861 (2016), 2094–2103.
3 Huang, X., et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics, 14, 2013, 319.
4 Uchida, S., Dimmeler, S., Long noncoding RNAs in cardiovascular diseases. Circ. Res. 116 (2015), 737–750.
5 Broadbent, H.M., et al. Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum. Mol. Genet. 17 (2008), 806–814.
6 Holdt, L.M., et al. ANRIL expression is associated with atherosclerosis risk at chromosome 9p21. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 620–627.
7 Kotake, Y., et al. Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15INK4B tumor suppressor gene. Oncogene 30 (2011), 1956–1962.
8 Nie, F.Q., et al. Long noncoding RNA ANRIL promotes non-small cell lung cancer cell proliferation and inhibits apoptosis by silencing KLF2 and P21 expression. Mol. Cancer Ther. 14 (2015), 268–277.
9 Holdt, L.M., et al. Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet., 9, 2013, e1003588.
10 Zhou, X., et al. Long non-coding RNA ANRIL regulates inflammatory responses as a novel component of NF-κB pathway. RNA Biol. 13 (2016), 98–108.
11 Cahill, P.A., Redmond, E.M., Vascular endothelium – gatekeeper of vessel health. Atherosclerosis 248 (2016), 97–109.
12 Martin, B.J., Anderson, T.J., Risk prediction in cardiovascular disease: the prognostic significance of endothelial dysfunction. Can. J. Cardiol. 25:Suppl. A (2009), 15A–20A.
13 Tziomalos, K., et al. Endothelial dysfunction in metabolic syndrome: prevalence, pathogenesis and management. Nutr. Metab. Cardiovasc. Dis. 20 (2010), 140–146.
14 Aguilar, M., et al. Prevalence of the metabolic syndrome in the United States, 2003-2012. JAMA 313 (2015), 1973–1974.
15 Isomaa, B., et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 24 (2001), 683–689.
16 Kaur, J., A comprehensive review on metabolic syndrome. Cardiol. Res. Pract., 2014, 2014, 943162.
17 Raal, F.J., Pathogenesis and management of the dyslipidemia of the metabolic syndrome. Metab. Syndr. Relat. Disord. 7 (2009), 83–88.
18 Valadi, H., et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9 (2007), 654–659.
19 Mitchell, P.S., et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 10513–10518.
20 Chen, 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.
21 Colombo, M., et al. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30 (2014), 255–289.
22 Vickers, K.C., et al. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 13 (2011), 423–433.
23 Arroyo, J.D., et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 5003–5008.
24 Wang, K., et al. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 38 (2010), 7248–7259.
25 Gallo, A., et al. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS ONE, 7, 2012, e30679.
26 Zernecke, A., et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci. Signal., 2, 2009, ra81.
27 Jansen, F., et al. Endothelial microparticle-mediated transfer of microRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 128 (2013), 2026–2038.
28 Tabet, F., et al. HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nat. Commun., 5, 2014, 3292.
29 He, S., et al. MicroRNAs activate natural killer cells through Toll-like receptor signaling. Blood 121 (2013), 4663–4671.
30 Fabbri, M., et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), E2110–E2116.
31 O'Neill, S., et al. Blood-based biomarkers for metabolic syndrome. Trends Endocrinol. Metab. 27 (2016), 363–374.
32 Njock, M-S., et al. Endothelial cells suppress monocyte activation through secretion of extracellular vesicles containing antiinflammatory microRNAs. Blood 125 (2015), 3202–3212.
33 Fichtlscherer, S., et al. Circulating microRNAs in patients with coronary artery disease. Circ. Res. 107 (2010), 677–684.
34 Jansen, F., et al. MicroRNA expression in circulating microvesicles predicts cardiovascular events in patients with coronary artery disease. J. Am. Heart Assoc., 3, 2014, e001249.
35 Zhu, H., Leung, S.W., Identification of microRNA biomarkers in type 2 diabetes: a meta-analysis of controlled profiling studies. Diabetologia 58 (2015), 900–911.
36 Barutta, F., et al. MicroRNA-126 and micro-/macrovascular complications of type 1 diabetes in the EURODIAB Prospective Complications Study. Acta Diabetol., 2016, 10.1007/s00592-016-0915-4 Published online October 1, 2016.
37 Zampetaki, A., et al. Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ. Res. 107 (2010), 810–817.
38 Jansen, F., et al. Vascular endothelial microparticles-incorporated microRNAs are altered in patients with diabetes mellitus. Cardiovasc. Diabetol., 15, 2016, 49.
39 Rottiers, V., Naar, A.M., MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 13 (2012), 239–250.
40 Karolina, D.S., et al. Circulating miRNA profiles in patients with metabolic syndrome. J. Clin. Endocrinol. Metab. 97 (2012), E2271–E2276.
41 Raitoharju, E., et al. Blood microRNA profile associates with the levels of serum lipids and metabolites associated with glucose metabolism and insulin resistance and pinpoints pathways underlying metabolic syndrome: the cardiovascular risk in Young Finns Study. Mol. Cell. Endocrinol. 391 (2014), 41–49.
42 Zhu, G.F., et al. microRNA-155 is inversely associated with severity of coronary stenotic lesions calculated by the Gensini score. Coron. Artery Dis. 25 (2014), 304–310.
43 Luo, L., et al. Plasma miR-10a: a potential biomarker for coronary artery disease. Dis. Markers, 2016, 2016, 3841927.
44 Sun, X., et al. Systemic delivery of microRNA-181b inhibits nuclear factor-κB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice. Circ. Res. 114 (2014), 32–40.
45 Baldeon, R.L., et al. Decreased serum level of miR-146a as sign of chronic inflammation in type 2 diabetic patients. PLoS ONE, 9, 2014, e115209.
46 Ma, S., et al. E-selectin-targeting delivery of microRNAs by microparticles ameliorates endothelial inflammation and atherosclerosis. Sci. Rep., 6, 2016, 22910.
47 Sun, X., et al. MicroRNA-181b improves glucose homeostasis and insulin sensitivity by regulating endothelial function in white adipose tissue. Circ. Res. 118 (2016), 810–821.
48 Jansen, F., et al. Endothelial microparticles reduce ICAM-1 expression in a microRNA-222-dependent mechanism. J. Cell. Mol. Med. 19 (2015), 2202–2214.
49 Hergenreider, E., et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14 (2012), 249–256.
50 van Balkom, B.W., et al. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood 121 (2013), 3997–4006.
51 Halkein, J., et al. MicroRNA-146a is a therapeutic target and biomarker for peripartum cardiomyopathy. J. Clin. Invest. 123 (2013), 2143–2154.
52 Bang, C., et al. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J. Clin. Invest. 124 (2014), 2136–2146.
53 Gray, W.D., et al. Identification of therapeutic covariant microRNA clusters in hypoxia-treated cardiac progenitor cell exosomes using systems biology. Circ. Res. 116 (2015), 255–263.
54 Ong, S.G., et al. Cross talk of combined gene and cell therapy in ischemic heart disease: role of exosomal microRNA transfer. Circulation 130:11 Suppl. 1 (2014), S60–S69.
55 Finn, N.A., et al. Coronary heart disease alters intercellular communication by modifying microparticle-mediated microRNA transport. FEBS Lett. 587 (2013), 3456–3463.
56 Alexy, T., et al. TNF-α alters the release and transfer of microparticle-encapsulated miRNAs from endothelial cells. Physiol. Genomics 46 (2014), 833–840.
57 Wang, X., et al. 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.
58 Caporali, A., et al. p75NTR-dependent activation of NF-κB regulates microRNA-503 transcription and pericyte-endothelial crosstalk in diabetes after limb ischaemia. Nat. Commun., 6, 2015, 8024.
59 Zhou, Y., et al. Exosome-mediated small RNA delivery for gene therapy. Wiley Interdiscip. Rev. RNA 7 (2016), 758–771.
60 Alvarez-Erviti, L., et al. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29 (2011), 341–345.
61 Trajkovski, M., et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474 (2011), 649–653.
62 Janssen, H.L., et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 368 (2013), 1685–1694.
63 van der Ree, M.H., et al. Long-term safety and efficacy of microRNA-targeted therapy in chronic hepatitis C patients. Antiviral Res. 111 (2014), 53–59.
64 Ottosen, S., et al. In vitro antiviral activity and preclinical and clinical resistance profile of miravirsen, a novel anti-hepatitis C virus therapeutic targeting the human factor miR-122. Antimicrob. Agents Chemother. 59 (2015), 599–608.
65 Adams, B.D., et al. The tumor-suppressive and potential therapeutic functions of miR-34a in epithelial carcinomas. Expert Opin. Ther. Targets 20 (2016), 737–753.
66 Elmén, J., et al. LNA-mediated microRNA silencing in non-human primates. Nature 452 (2008), 896–899.
67 Cheng, H.H., et al. Plasma processing conditions substantially influence circulating microRNA biomarker levels. PLoS ONE, 8, 2013, e64795.
68 Mitchell, A.J., et al. Platelets confound the measurement of extracellular miRNA in archived plasma. Sci. Rep., 6, 2016, 32651.
69 Willeit, P., et al. Circulating microRNAs as novel biomarkers for platelet activation. Circ. Res. 112 (2013), 595–600.
70 Sun, X., et al. Systemic delivery of microRNA-181b inhibits nuclear factor-kappaB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice. Circ. Res. 114 (2014), 32–40.
71 He, Q.F., et al. Circulating microRNA-21 is downregulated in patients with metabolic syndrome. Biomed. Environ. Sci. 29 (2016), 385–389.