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Published in: Journal of Cardiovascular Translational Research 6/2013

01-12-2013

MicroRNAs in Endothelial Senescence and Atherosclerosis

Authors: Rossella Menghini, Viviana Casagrande, Massimo Federici

Published in: Journal of Cardiovascular Translational Research | Issue 6/2013

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Abstract

Aging is an important risk factor for the development of many cardiovascular diseases as atherosclerosis and is accompanied by the decline of endothelial function. Senescence of endothelial cells has been proposed to be involved in endothelial dysfunction and atherogenesis. Therefore, the study of new target therapies to prevent or reverse this process represents a field of great interest. MicroRNAs (miRNAs), a class of short RNAs, play key roles in various biological processes and in the development of human disease through specific posttranscriptional downregulation of gene expression. In particular, miRNAs that are highly expressed by endothelial cells can be detected in high concentration in human atherosclerotic plaques and in the circulation, suggesting their potential translation to bedside to determine the dysfunction of specific signaling pathways which play a role in coronary artery disease in the individual patient, a path towards a stratified medicine approach for early preventive treatment of disease. Here, we review the most recent advances in the field of atherosclerosis that implicate a role for miRNAs with a special emphasis on endothelial senescence and its involvement in the atherosclerotic process. Finally, we briefly discuss the potential use of miRNAs signatures to map atherosclerosis progression and in particular underlying the relevance of circulating plasma miRNAs that can be used clinically as biomarkers of vascular pathology.
Literature
1.
go back to reference Davignon, J., & Ganz, P. (2004). Role of endothelial dysfunction in atherosclerosis. Circulation, 109, III27–III32.PubMedCrossRef Davignon, J., & Ganz, P. (2004). Role of endothelial dysfunction in atherosclerosis. Circulation, 109, III27–III32.PubMedCrossRef
2.
go back to reference Kim, V. N. (2005). MicroRNA biogenesis: coordinated cropping and dicing. Nature Reviews Molecular Cell Biology, 6, 376–385.PubMedCrossRef Kim, V. N. (2005). MicroRNA biogenesis: coordinated cropping and dicing. Nature Reviews Molecular Cell Biology, 6, 376–385.PubMedCrossRef
3.
go back to reference Krützfeldt, J., & Stoffel, M. (2006). MicroRNAs: a new class of regulatory genes affecting metabolism. Cell Metabolism, 4, 9–12.PubMedCrossRef Krützfeldt, J., & Stoffel, M. (2006). MicroRNAs: a new class of regulatory genes affecting metabolism. Cell Metabolism, 4, 9–12.PubMedCrossRef
4.
go back to reference Krützfeldt, J., Poy, M. N., & Stoffel, M. (2006). Strategies to determine the biological function of microRNAs. Nature Genetics, 38, S14–S19.PubMedCrossRef Krützfeldt, J., Poy, M. N., & Stoffel, M. (2006). Strategies to determine the biological function of microRNAs. Nature Genetics, 38, S14–S19.PubMedCrossRef
5.
go back to reference Vasudevan, S., Tong, Y., & Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science, 318, 1931–1934.PubMedCrossRef Vasudevan, S., Tong, Y., & Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science, 318, 1931–1934.PubMedCrossRef
6.
go back to reference Minamino, T., & Komuro, I. (2007). Vascular cell senescence: contribution to atherosclerosis. Circulation Research, 100, 15–26.PubMedCrossRef Minamino, T., & Komuro, I. (2007). Vascular cell senescence: contribution to atherosclerosis. Circulation Research, 100, 15–26.PubMedCrossRef
7.
go back to reference Minamino, T., Miyauchi, H., Yoshida, T., Ishida, Y., Yoshida, H., & Komuro, I. (2002). Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation, 105, 1541–1544.PubMedCrossRef Minamino, T., Miyauchi, H., Yoshida, T., Ishida, Y., Yoshida, H., & Komuro, I. (2002). Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation, 105, 1541–1544.PubMedCrossRef
8.
go back to reference Fridman, A. L., & Tainsky, M. A. (2008). Critical pathways in cellular senescence and immortalization revealed by gene expression profiling. Oncogene, 27, 5975–5987.PubMedCrossRef Fridman, A. L., & Tainsky, M. A. (2008). Critical pathways in cellular senescence and immortalization revealed by gene expression profiling. Oncogene, 27, 5975–5987.PubMedCrossRef
9.
go back to reference Gorospe, M., & Abdelmohsen, K. (2011). Microregulators come of age in senescence. Trends in Genetics, 27, 233–241.PubMedCrossRef Gorospe, M., & Abdelmohsen, K. (2011). Microregulators come of age in senescence. Trends in Genetics, 27, 233–241.PubMedCrossRef
10.
go back to reference Kuehbacher, A., Urbich, C., Zeiher, A. M., & Dimmeler, S. (2007). Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circulation Research, 101, 59–68.PubMedCrossRef Kuehbacher, A., Urbich, C., Zeiher, A. M., & Dimmeler, S. (2007). Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circulation Research, 101, 59–68.PubMedCrossRef
11.
go back to reference Suárez, Y., Fernández-Hernando, C., Pober, J. S., & Sessa, W. C. (2007). Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circulation Research, 100, 1164–1173.PubMedCrossRef Suárez, Y., Fernández-Hernando, C., Pober, J. S., & Sessa, W. C. (2007). Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circulation Research, 100, 1164–1173.PubMedCrossRef
12.
go back to reference Ji, R., Cheng, Y., Yue, J., Yang, J., Liu, X., Chen, H., et al. (2007). MicroRNA expression signature and antisense-mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circulation Research, 100, 1579–1588.PubMedCrossRef Ji, R., Cheng, Y., Yue, J., Yang, J., Liu, X., Chen, H., et al. (2007). MicroRNA expression signature and antisense-mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circulation Research, 100, 1579–1588.PubMedCrossRef
13.
go back to reference Weber, C., & Noels, H. (2011). Atherosclerosis: current pathogenesis and therapeutic options. Nature Medicine, 17, 1410–1422.PubMedCrossRef Weber, C., & Noels, H. (2011). Atherosclerosis: current pathogenesis and therapeutic options. Nature Medicine, 17, 1410–1422.PubMedCrossRef
14.
go back to reference Kong, W., Zhao, J. J., He, L., & Cheng, J. Q. (2009). Strategies for profiling microRNA expression. Journal of Cellular Physiology, 218, 22–25.PubMedCrossRef Kong, W., Zhao, J. J., He, L., & Cheng, J. Q. (2009). Strategies for profiling microRNA expression. Journal of Cellular Physiology, 218, 22–25.PubMedCrossRef
15.
go back to reference Menghini, R., Casagrande, V., Cardellini, M., Martelli, E., Terrinoni, A., Amati, F., et al. (2009). MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation, 120, 1524–1532.PubMedCrossRef Menghini, R., Casagrande, V., Cardellini, M., Martelli, E., Terrinoni, A., Amati, F., et al. (2009). MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation, 120, 1524–1532.PubMedCrossRef
16.
go back to reference Ito, T., Yagi, S., & Yamakuchi, M. (2010). MicroRNA-34a regulation of endothelial senescence. Biochemical and Biophysical Research Communications, 398, 735–740.PubMedCrossRef Ito, T., Yagi, S., & Yamakuchi, M. (2010). MicroRNA-34a regulation of endothelial senescence. Biochemical and Biophysical Research Communications, 398, 735–740.PubMedCrossRef
17.
go back to reference Haigis, M. C., & Guarente, L. P. (2006). Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes & Development, 20, 2913–2921.CrossRef Haigis, M. C., & Guarente, L. P. (2006). Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes & Development, 20, 2913–2921.CrossRef
18.
go back to reference Mattagajasingh, I., Kim, C. S., Naqvi, A., Yamamori, T., Hoffman, T. A., Jung, S. B., et al. (2007). SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences of the United States of America, 104, 14855–14860.PubMedCrossRef Mattagajasingh, I., Kim, C. S., Naqvi, A., Yamamori, T., Hoffman, T. A., Jung, S. B., et al. (2007). SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences of the United States of America, 104, 14855–14860.PubMedCrossRef
19.
go back to reference Langley, E., Pearson, M., Faretta, M., Bauer, U. M., Frye, R. A., Minucci, S., et al. (2002). Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO Journal, 21, 2383–2396.PubMedCrossRef Langley, E., Pearson, M., Faretta, M., Bauer, U. M., Frye, R. A., Minucci, S., et al. (2002). Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO Journal, 21, 2383–2396.PubMedCrossRef
20.
go back to reference Alcendor, R. R., Gao, S., Zhai, P., Zablocki, D., Holle, E., Yu, X., et al. (2007). Sirt1 regulates aging and resistance to oxidative stress in the heart. Circulation Research, 100, 1512–1521.PubMedCrossRef Alcendor, R. R., Gao, S., Zhai, P., Zablocki, D., Holle, E., Yu, X., et al. (2007). Sirt1 regulates aging and resistance to oxidative stress in the heart. Circulation Research, 100, 1512–1521.PubMedCrossRef
21.
go back to reference Vasa-Nicotera, M., Chen, H., Tucci, P., Yang, A. L., Saintigny, G., Menghini, R., et al. (2011). MiR-146a is modulated in human endothelial cell with aging. Atherosclerosis, 217, 326–330.PubMedCrossRef Vasa-Nicotera, M., Chen, H., Tucci, P., Yang, A. L., Saintigny, G., Menghini, R., et al. (2011). MiR-146a is modulated in human endothelial cell with aging. Atherosclerosis, 217, 326–330.PubMedCrossRef
22.
go back to reference LaRocca, T. J., Henson, G. D., Thorburn, A., Sindler, A. L., Pierce, G. L., & Seals, D. R. (2012). Translational evidence that impaired autophagy contributes to arterial ageing. Journal de Physiologie, 590, 3305–3316.CrossRef LaRocca, T. J., Henson, G. D., Thorburn, A., Sindler, A. L., Pierce, G. L., & Seals, D. R. (2012). Translational evidence that impaired autophagy contributes to arterial ageing. Journal de Physiologie, 590, 3305–3316.CrossRef
23.
go back to reference Gibbings, D., Mostowy, S., Jay, F., Schwab, Y., Cossart, P., & Voinnet, O. (2012). Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nature Cell Biology, 14, 1314–1321.PubMedCrossRef Gibbings, D., Mostowy, S., Jay, F., Schwab, Y., Cossart, P., & Voinnet, O. (2012). Selective autophagy degrades DICER and AGO2 and regulates miRNA activity. Nature Cell Biology, 14, 1314–1321.PubMedCrossRef
24.
go back to reference Lee, I. H., Cao, L., Mostoslavsky, R., Lombard, D. B., Liu, J., Bruns, N. E., et al. (2008). A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proceedings of the National Academy of Sciences of the United States of America, 105, 3374–3379.PubMedCrossRef Lee, I. H., Cao, L., Mostoslavsky, R., Lombard, D. B., Liu, J., Bruns, N. E., et al. (2008). A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proceedings of the National Academy of Sciences of the United States of America, 105, 3374–3379.PubMedCrossRef
25.
go back to reference Federici, M., Hribal, M. L., Menghini, R., Kanno, H., Marchetti, V., Porzio, O., et al. (2005). Timp3 deficiency in insulin receptor-haploinsufficient mice promotes diabetes and vascular inflammation via increased TNF-alpha. The Journal of Clinical Investigation, 115, 3494–3505.PubMedCrossRef Federici, M., Hribal, M. L., Menghini, R., Kanno, H., Marchetti, V., Porzio, O., et al. (2005). Timp3 deficiency in insulin receptor-haploinsufficient mice promotes diabetes and vascular inflammation via increased TNF-alpha. The Journal of Clinical Investigation, 115, 3494–3505.PubMedCrossRef
26.
go back to reference Menghini, R., Menini, S., Amoruso, R., Fiorentino, L., Casagrande, V., Marzano, V., et al. (2009). Tissue inhibitor of metalloproteinase 3 deficiency causes hepatic steatosis and adipose tissue inflammation in mice. Gastroenterology, 136, 663–672.PubMedCrossRef Menghini, R., Menini, S., Amoruso, R., Fiorentino, L., Casagrande, V., Marzano, V., et al. (2009). Tissue inhibitor of metalloproteinase 3 deficiency causes hepatic steatosis and adipose tissue inflammation in mice. Gastroenterology, 136, 663–672.PubMedCrossRef
27.
go back to reference Cardellini, M., Menghini, R., Luzi, A., Davato, F., Cardolini, I., D’Alfonso, R., et al. (2011). Decreased IRS2 and TIMP3 expression in monocytes from offspring of type 2 diabetic patients is correlated with insulin resistance and increased intima–media thickness. Diabetes, 60, 3265–3270.PubMedCrossRef Cardellini, M., Menghini, R., Luzi, A., Davato, F., Cardolini, I., D’Alfonso, R., et al. (2011). Decreased IRS2 and TIMP3 expression in monocytes from offspring of type 2 diabetic patients is correlated with insulin resistance and increased intima–media thickness. Diabetes, 60, 3265–3270.PubMedCrossRef
28.
go back to reference Casagrande, V., Menghini, R., Menini, S., Marino, A., Marchetti, V., Cavalera, M., et al. (2012). Overexpression of tissue inhibitor of metalloproteinase 3 in macrophages reduces atherosclerosis in low-density lipoprotein receptor knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 32, 74–81.PubMedCrossRef Casagrande, V., Menghini, R., Menini, S., Marino, A., Marchetti, V., Cavalera, M., et al. (2012). Overexpression of tissue inhibitor of metalloproteinase 3 in macrophages reduces atherosclerosis in low-density lipoprotein receptor knockout mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 32, 74–81.PubMedCrossRef
29.
go back to reference Menghini, R., Casagrande, V., Menini, S., Marino, A., Marzano, V., Hribal, M. L., et al. (2012). TIMP3 overexpression in macrophages protects from insulin resistance, adipose inflammation, and nonalcoholic fatty liver disease in mice. Diabetes, 61, 454–462.PubMedCrossRef Menghini, R., Casagrande, V., Menini, S., Marino, A., Marzano, V., Hribal, M. L., et al. (2012). TIMP3 overexpression in macrophages protects from insulin resistance, adipose inflammation, and nonalcoholic fatty liver disease in mice. Diabetes, 61, 454–462.PubMedCrossRef
30.
go back to reference Fiorentino, L., Cavalera, M., Menini, S., Marchetti, V., Mavilio, M., Fabrizi, M., et al. (2013). Loss of TIMP3 underlies diabetic nephropathy via FoxO1/STAT1 interplay. EMBO Molecular Medicine, 5, 441–455.PubMedCrossRef Fiorentino, L., Cavalera, M., Menini, S., Marchetti, V., Mavilio, M., Fabrizi, M., et al. (2013). Loss of TIMP3 underlies diabetic nephropathy via FoxO1/STAT1 interplay. EMBO Molecular Medicine, 5, 441–455.PubMedCrossRef
31.
go back to reference Cardellini, M., Menghini, R., Martelli, E., Casagrande, V., Marino, A., Rizza, S., et al. (2009). TIMP3 is reduced in atherosclerotic plaques from subjects with type 2 diabetes and increased by SirT1. Diabetes, 58, 2396–2401.PubMedCrossRef Cardellini, M., Menghini, R., Martelli, E., Casagrande, V., Marino, A., Rizza, S., et al. (2009). TIMP3 is reduced in atherosclerotic plaques from subjects with type 2 diabetes and increased by SirT1. Diabetes, 58, 2396–2401.PubMedCrossRef
32.
go back to reference Greco, S., Fasanaro, P., Castelvecchio, S., D’Alessandra, Y., Arcelli, D., Di Donato, M., et al. (2012). MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes, 61, 1633–1641.PubMedCrossRef Greco, S., Fasanaro, P., Castelvecchio, S., D’Alessandra, Y., Arcelli, D., Di Donato, M., et al. (2012). MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes, 61, 1633–1641.PubMedCrossRef
33.
go back to reference Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., et al. (2008). The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Developmental Cell, 15, 261–271.PubMedCrossRef Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., et al. (2008). The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Developmental Cell, 15, 261–271.PubMedCrossRef
34.
go back to reference Harris, T. A., Yamakuchi, M., Ferlito, M., Mendell, J. T., & Lowenstein, C. J. (2008). MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proceedings of the National Academy of Sciences of the United States of America, 105, 1516–1521.PubMedCrossRef Harris, T. A., Yamakuchi, M., Ferlito, M., Mendell, J. T., & Lowenstein, C. J. (2008). MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proceedings of the National Academy of Sciences of the United States of America, 105, 1516–1521.PubMedCrossRef
35.
go back to reference Bonauer, A., Carmona, G., Iwasaki, M., Mione, M., Koyanagi, M., Fischer, A., et al. (2009). MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science, 324, 1710–1713.PubMedCrossRef Bonauer, A., Carmona, G., Iwasaki, M., Mione, M., Koyanagi, M., Fischer, A., et al. (2009). MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science, 324, 1710–1713.PubMedCrossRef
36.
go back to reference Fang, Y., & Davies, P. F. (2012). Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arteriosclerosis, Thrombosis, and Vascular Biology, 32, 979–987.PubMedCrossRef Fang, Y., & Davies, P. F. (2012). Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arteriosclerosis, Thrombosis, and Vascular Biology, 32, 979–987.PubMedCrossRef
37.
go back to reference Sabatel, C., Malvaux, L., Bovy, N., Deroanne, C., Lambert, V., Gonzalez, M. L., et al. (2011). MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothelial cells. PLoS One, 6, e16979.PubMedCrossRef Sabatel, C., Malvaux, L., Bovy, N., Deroanne, C., Lambert, V., Gonzalez, M. L., et al. (2011). MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothelial cells. PLoS One, 6, e16979.PubMedCrossRef
38.
go back to reference Zhou, J., Wang, W. W., Subramaniam, S., Shyy, J. Y., Chiu, J. J., Li, J. Y., et al. (2011). MicroRNA-21 targets peroxisome proliferators-activated receptor-α in an autoregulatory loop to modulate flow-induced endothelial inflammation. Proceedings of the National Academy of Sciences of the United States of America, 108, 10355–10360.PubMedCrossRef Zhou, J., Wang, W. W., Subramaniam, S., Shyy, J. Y., Chiu, J. J., Li, J. Y., et al. (2011). MicroRNA-21 targets peroxisome proliferators-activated receptor-α in an autoregulatory loop to modulate flow-induced endothelial inflammation. Proceedings of the National Academy of Sciences of the United States of America, 108, 10355–10360.PubMedCrossRef
39.
go back to reference Chen, L. J., Lim, S. H., Yeh, Y. T., Lien, S. C., & Chiu, J. J. (2012). Roles of microRNAs in atherosclerosis and restenosis. Journal of Biomedical Science, 19, 79.PubMedCrossRef Chen, L. J., Lim, S. H., Yeh, Y. T., Lien, S. C., & Chiu, J. J. (2012). Roles of microRNAs in atherosclerosis and restenosis. Journal of Biomedical Science, 19, 79.PubMedCrossRef
40.
go back to reference Raitoharju, E., Lyytikäinen, L. P., Levula, M., Oksala, N., Mennander, A., Tarkka, M., et al. (2011). MiR-21, miR-210, miR-34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis, 219, 211–217.PubMedCrossRef Raitoharju, E., Lyytikäinen, L. P., Levula, M., Oksala, N., Mennander, A., Tarkka, M., et al. (2011). MiR-21, miR-210, miR-34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study. Atherosclerosis, 219, 211–217.PubMedCrossRef
41.
go back to reference Li, T., Cao, H., Zhuang, J., Wan, J., Guan, M., Yu, B., et al. (2011). Identification of miR-130a, miR-27b and miR-210 as serum biomarkers for atherosclerosis obliterans. Clinica Chimica Acta, 412, 66–70.CrossRef Li, T., Cao, H., Zhuang, J., Wan, J., Guan, M., Yu, B., et al. (2011). Identification of miR-130a, miR-27b and miR-210 as serum biomarkers for atherosclerosis obliterans. Clinica Chimica Acta, 412, 66–70.CrossRef
42.
go back to reference Takahashi, Y., Satoh, M., Minami, Y., Tabuchi, T., Itoh, T., & Nakamura, M. (2010). Expression of miR-146a/b is associated with the Toll-like receptor 4 signal in coronary artery disease: effect of renin-angiotensin system blockade and statins on miRNA-146a/b and Toll-like receptor 4 levels. Clinical Science (London, England), 119, 395–405.CrossRef Takahashi, Y., Satoh, M., Minami, Y., Tabuchi, T., Itoh, T., & Nakamura, M. (2010). Expression of miR-146a/b is associated with the Toll-like receptor 4 signal in coronary artery disease: effect of renin-angiotensin system blockade and statins on miRNA-146a/b and Toll-like receptor 4 levels. Clinical Science (London, England), 119, 395–405.CrossRef
43.
go back to reference Guo, M., Mao, X., Ji, Q., Lang, M., Li, S., Peng, Y., et al. (2010). MiR-146a in PBMCs modulates Th1 function in patients with acute coronary syndrome. Immunology and Cell Biology, 88, 555–564.PubMedCrossRef Guo, M., Mao, X., Ji, Q., Lang, M., Li, S., Peng, Y., et al. (2010). MiR-146a in PBMCs modulates Th1 function in patients with acute coronary syndrome. Immunology and Cell Biology, 88, 555–564.PubMedCrossRef
44.
go back to reference Du, F., Zhou, J., Gong, R., Huang, X., Pansuria, M., Virtue, A., et al. (2012). Endothelial progenitor cells in atherosclerosis. Frontiers in Bioscience, 17, 2327–2349.CrossRef Du, F., Zhou, J., Gong, R., Huang, X., Pansuria, M., Virtue, A., et al. (2012). Endothelial progenitor cells in atherosclerosis. Frontiers in Bioscience, 17, 2327–2349.CrossRef
45.
go back to reference Zhang, Q., Kandic, I., & Kutryk, M. J. (2011). Dysregulation of angiogenesis-related microRNAs in endothelial progenitor cells from patients with coronary artery disease. Biochemical and Biophysical Research Communications, 405, 42–46.PubMedCrossRef Zhang, Q., Kandic, I., & Kutryk, M. J. (2011). Dysregulation of angiogenesis-related microRNAs in endothelial progenitor cells from patients with coronary artery disease. Biochemical and Biophysical Research Communications, 405, 42–46.PubMedCrossRef
46.
go back to reference Zhao, T., Li, J., & Chen, A. F. (2010). MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. American Journal of Physiology, Endocrinology and Metabolism, 299, E110–E116.CrossRef Zhao, T., Li, J., & Chen, A. F. (2010). MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. American Journal of Physiology, Endocrinology and Metabolism, 299, E110–E116.CrossRef
47.
go back to reference Zernecke, A., Bidzhekov, K., Noels, H., Shagdarsuren, E., Gan, L., Denecke, B., et al. (2009). Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Science Signaling, 2, ra81.PubMedCrossRef Zernecke, A., Bidzhekov, K., Noels, H., Shagdarsuren, E., Gan, L., Denecke, B., et al. (2009). Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Science Signaling, 2, ra81.PubMedCrossRef
48.
go back to reference Hunter, M. P., Ismail, N., Zhang, X., Aguda, B. D., Lee, E. J., Yu, L., et al. (2008). Detection of microRNA expression in human peripheral blood microvesicles. PLoS One, 3, e3694.PubMedCrossRef Hunter, M. P., Ismail, N., Zhang, X., Aguda, B. D., Lee, E. J., Yu, L., et al. (2008). Detection of microRNA expression in human peripheral blood microvesicles. PLoS One, 3, e3694.PubMedCrossRef
49.
go back to reference Zampetaki, A., Kiechl, S., Drozdov, I., Willeit, P., Mayr, U., Prokopi, M., et al. (2010). Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circulation Research, 107, 810–817.PubMedCrossRef Zampetaki, A., Kiechl, S., Drozdov, I., Willeit, P., Mayr, U., Prokopi, M., et al. (2010). Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circulation Research, 107, 810–817.PubMedCrossRef
50.
go back to reference Fichtlscherer, S., De Rosa, S., Fox, H., Schwietz, T., Fischer, A., Liebetrau, C., et al. (2010). Circulating microRNAs in patients with coronary artery disease. Circulation Research, 107, 677–684.PubMedCrossRef Fichtlscherer, S., De Rosa, S., Fox, H., Schwietz, T., Fischer, A., Liebetrau, C., et al. (2010). Circulating microRNAs in patients with coronary artery disease. Circulation Research, 107, 677–684.PubMedCrossRef
51.
go back to reference Yao, R., Ma, Y., Du, Y., Liao, M., Li, H., Liang, W., et al. (2011). The altered expression of inflammation-related microRNAs with microRNA-155 expression correlates with Th17 differentiation in patients with acute coronary syndrome. Cellular and molecular immunology, 8, 486–495.PubMedCrossRef Yao, R., Ma, Y., Du, Y., Liao, M., Li, H., Liang, W., et al. (2011). The altered expression of inflammation-related microRNAs with microRNA-155 expression correlates with Th17 differentiation in patients with acute coronary syndrome. Cellular and molecular immunology, 8, 486–495.PubMedCrossRef
52.
go back to reference Wang, H., Lu, H. M., Yang, W. H., Luo, C., Lu, S. H., Zhou, Y., et al. (2012). The influence of statin therapy on circulating microRNA-92a expression in patients with coronary heart disease. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue, 24, 215–218.PubMed Wang, H., Lu, H. M., Yang, W. H., Luo, C., Lu, S. H., Zhou, Y., et al. (2012). The influence of statin therapy on circulating microRNA-92a expression in patients with coronary heart disease. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue, 24, 215–218.PubMed
53.
go back to reference Nazari-Jahantigh, M., Wei, Y., Noels, H., Akhtar, S., Zhou, Z., Koenen, R. R., et al. (2012). MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. The Journal of Clinical Investigation, 122, 4190–4202.PubMedCrossRef Nazari-Jahantigh, M., Wei, Y., Noels, H., Akhtar, S., Zhou, Z., Koenen, R. R., et al. (2012). MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. The Journal of Clinical Investigation, 122, 4190–4202.PubMedCrossRef
Metadata
Title
MicroRNAs in Endothelial Senescence and Atherosclerosis
Authors
Rossella Menghini
Viviana Casagrande
Massimo Federici
Publication date
01-12-2013
Publisher
Springer US
Published in
Journal of Cardiovascular Translational Research / Issue 6/2013
Print ISSN: 1937-5387
Electronic ISSN: 1937-5395
DOI
https://doi.org/10.1007/s12265-013-9487-7

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Journal of Cardiovascular Translational Research 6/2013 Go to the issue

Acknowledgments

Reviewers for JCTR