[en] Cardiovascular diseases such as atherosclerosis are one of the leading causes of morbidity and mortality worldwide. The clinical manifestations of atherosclerosis, which include heart attack and stroke, occur several decades after initiation of the disease and become more severe with age. Inflammation of blood vessels plays a prominent role in atherogenesis. Activation of the endothelium by inflammatory mediators leads to the recruitment of circulating inflammatory cells, which drives atherosclerotic plaque formation and progression. Inflammatory signaling within the endothelium is driven predominantly by the pro-inflammatory transcription factor, NF-kappaB. Interestingly, activation of NF-kappaB is enhanced during the normal aging process and this may contribute to the development of cardiovascular disease. Importantly, studies utilizing mouse models of vascular inflammation and atherosclerosis are uncovering a network of noncoding RNAs, particularly microRNAs, which impinge on the NF-kappaB signaling pathway. Here we summarize the literature regarding the control of vascular inflammation by microRNAs, and provide insight into how these microRNA-based pathways might be harnessed for therapeutic treatment of disease. We also discuss emerging areas of endothelial cell biology, including the involvement of long noncoding RNAs and circulating microRNAs in the control of vascular inflammation.
Disciplines :
Cardiovascular & respiratory systems
Author, co-author :
Cheng, Henry S.; Toronto General Research Institute, University Health Network Toronto, ON, Canada ; Department of Laboratory Medicine and Pathobiology, University of Toronto Toronto, ON, Canada ; Heart and Stroke/Richard Lewar Centre of Excellence in Cardiovascular Research Toronto, ON, Canada.
Njock, Makon-Sébastien ; Toronto General Research Institute, University Health Network Toronto, ON, Canada ; Department of Laboratory Medicine and Pathobiology, University of Toronto Toronto, ON, Canada ; Heart and Stroke/Richard Lewar Centre of Excellence in Cardiovascular Research Toronto, ON, Canada.
Khyzha, Nadiya; Toronto General Research Institute, University Health Network Toronto, ON, Canada ; Department of Laboratory Medicine and Pathobiology, University of Toronto Toronto, ON, Canada ; Heart and Stroke/Richard Lewar Centre of Excellence in Cardiovascular Research Toronto, ON, Canada.
Dang, Lan T.; Toronto General Research Institute, University Health Network Toronto, ON, Canada ; Department of Laboratory Medicine and Pathobiology, University of Toronto Toronto, ON, Canada ; Heart and Stroke/Richard Lewar Centre of Excellence in Cardiovascular Research Toronto, ON, Canada.
Fish, Jason E.; Toronto General Research Institute, University Health Network Toronto, ON, Canada ; Department of Laboratory Medicine and Pathobiology, University of Toronto Toronto, ON, Canada ; Heart and Stroke/Richard Lewar Centre of Excellence in Cardiovascular Research Toronto, ON, Canada.
Language :
English
Title :
Noncoding RNAs regulate NF-kappaB signaling to modulate blood vessel inflammation.
Adler, A. S., Sinha, S., Kawahara, T. L., Zhang, J. Y., Segal, E., and Chang, H. Y. (2007). Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes Dev. 21, 3244-3257. doi: 10.1101/gad.1588507
Ahmad, M., Theofanidis, P., and Medford, R. M. (1998). Role of activating protein-1 in the regulation of the vascular cell adhesion molecule-1 gene expression by tumor necrosis factor-alpha. J. Biol. Chem. 273, 4616-4621. doi: 10.1074/jbc.273.8.4616
Albrecht, C., Preusch, M. R., Hofmann, G., Morris-Rosenfeld, S., Blessing, E., Rosenfeld, M. E.,et al. (2010). Egr-1 deficiency in bone marrow-derived cells reduces atherosclerotic lesion formation in a hyperlipidaemic mouse model. Cardiovasc. Res. 86, 321-329. doi: 10.1093/cvr/cvq032
Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., and Wood, M. J. (2011). Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29, 341-345. doi: 10.1038/nbt.1807
Arenzana-Seisdedos, F., Thompson, J., Rodriguez, M. S., Bachelerie, F., Thomas, D., and Hay, R. T. (1995). Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNA-binding and transcriptional activities of NF-kappa B. Mol. Cell. Biol. 15, 2689-2696.
Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F.,et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U.S.A. 108, 5003-5008. doi: 10.1073/pnas.1019055108
Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P., and Bartel, D. P. (2008). The impact of microRNAs on protein output. Nature 455, 64-71. doi: 10.1038/nature07242
Banerjee, S., Meng, J., Das, S., Krishnan, A., Haworth, J., Charboneau, R.,et al. (2013). Morphine induced exacerbation of sepsis is mediated by tempering endotoxin tolerance through modulation of miR-146a. Sci. Rep. 3, 1977. doi: 10.1038/srep01977
Bang, C., Batkai, S., Dangwal, S., Gupta, S. K., Foinquinos, A., Holzmann, A.,et al. (2014). Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J. Clin. Invest. 124, 2136-2146. doi: 10.1172/JCI70577
Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233. doi: 10.1016/j.cell.2009.01.002
Bazzoni, F., Rossato, M., Fabbri, M., Gaudiosi, D., Mirolo, M., Mori, L.,et al. (2009). Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc. Natl. Acad. Sci. U.S.A. 106, 5282-5287. doi: 10.1073/pnas.0810909106
Bell, R. D., Long, X., Lin, M., Bergmann, J. H., Nanda, V., Cowan, S. L.,et al. (2014). Identification and initial functional characterization of a human vascular cell-enriched long noncoding RNA. Arterioscler. Thromb. Vasc. Biol. 34, 1249-1259. doi: 10.1161/ATVBAHA.114.303240
Bernal-Mizrachi, L., Jy, W., Jimenez, J. J., Pastor, J., Mauro, L. M., Horstman, L. L.,et al. (2003). High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am. Heart J. 145, 962-970. doi: 10.1016/S0002-8703(03)00103-0
Bhaumik, D., Scott, G. K., Schokrpur, S., Patil, C. K., Orjalo, A. V., Rodier, F.,et al. (2009). MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 1, 402-411.
Biswas, S. K., and Lopez-Collazo, E. (2009). Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol. 30, 475-487. doi: 10.1016/j.it.2009.07.009
Boldin, M. P., and Baltimore, D. (2012). MicroRNAs, new effectors and regulators of NF-kappaB. Immunol. Rev. 246, 205-220. doi: 10.1111/j.1600-065X.2011.01089.x
Boldin, M. P., Taganov, K. D., Rao, D. S., Yang, L., Zhao, J. L., Kalwani, M.,et al. (2011). miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 208, 1189-1201. doi: 10.1084/jem.20101823
Boone, D. L., Turer, E. E., Lee, E. G., Ahmad, R. C., Wheeler, M. T., Tsui, C.,et al. (2004). The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5, 1052-1060. doi: 10.1038/ni1110
Bulut, D., Tuns, H., and Mugge, A. (2009). CD31+/Annexin V+ microparticles in healthy offsprings of patients with coronary artery disease. Eur. J. Clin. Invest. 39, 17-22. doi: 10.1111/j.1365-2362.2008.02058.x
Cao, Z., Xiong, J., Takeuchi, M., Kurama, T., and Goeddel, D. V. (1996). TRAF6 is a signal transducer for interleukin-1. Nature 383, 443-446. doi: 10.1038/383443a0
Carpenter, S., Aiello, D., Atianand, M. K., Ricci, E. P., Gandhi, P., Hall, L. L.,et al. (2013). A long noncoding RNA mediates both activation and repression of immune response genes. Science 341, 789-792. doi: 10.1126/science.1240925
Cech, T. R., and Steitz, J. A. (2014). The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157, 77-94. doi: 10.1016/j.cell.2014.03.008
Ceppi, M., Pereira, P. M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M. A.,et al. (2009). MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 106, 2735-2740. doi: 10.1073/pnas.0811073106
Chen, H. H., Almontashiri, N. A., Antoine, D., and Stewart, A. F. (2014). Functional genomics of the 9p21.3 locus for atherosclerosis: clarity or confusion? Curr. Cardiol. Rep. 16, 502. doi: 10.1007/s11886-014-0502-7
Cheng, H. S., Sivachandran, N., Lau, A., Boudreau, E., Zhao, J. L., Baltimore, D.,et al. (2013). MicroRNA-146 represses endothelial activation by inhibiting pro-inflammatory pathways. EMBO Mol. Med. 5, 949-966. doi: 10.1002/emmm.201202318
Combes, V., Simon, A. C., Grau, G. E., Arnoux, D., Camoin, L., Sabatier, F.,et al. (1999). In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant. J. Clin. Invest. 104, 93-102. doi: 10.1172/JCI4985
Cowan, C., Muraleedharan, C. K., O'Donnell, J. J. III, Singh, P. K., Lum, H., Kumar, A.,et al. (2014). MicroRNA-146 inhibits thrombin-induced NF-kappaB activation and subsequent inflammatory responses in human retinal endothelial cells. Invest. Ophthalmol. Vis. Sci. 55, 4944-4951. doi: 10.1167/iovs.13-13631
Csiszar, A., Wang, M., Lakatta, E. G., and Ungvari, Z. (2008). Inflammation and endothelial dysfunction during aging: role of NF-kappaB. J. Appl. Physiol. 105, 1333-1341. doi: 10.1152/japplphysiol.90470.2008
Dahlman, J. E., Barnes, C., Khan, O. F., Thiriot, A., Jhunjunwala, S., Shaw, T. E.,et al. (2014). In vivo endothelial siRNA delivery using polymeric nanoparticles with low molecular weight. Nat. Nanotechnol. 9, 648-55. doi: 10.1038/nnano.2014.84
Dai, G., Kaazempur-Mofrad, M. R., Natarajan, S., Zhang, Y., Vaughn, S., Blackman, B. R.,et al. (2004). Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc. Natl. Acad. Sci. U.S.A. 101, 14871-14876. doi: 10.1073/pnas.0406073101
den Dekker, W. K., Cheng, C., Pasterkamp, G., and Duckers, H. J. (2010). Toll like receptor 4 in atherosclerosis and plaque destabilization. Atherosclerosis 209, 314-320. doi: 10.1016/j.atherosclerosis.2009.09.075
Devlin, C. M., Kuriakose, G., Hirsch, E., and Tabas, I. (2002). Genetic alterations of IL-1 receptor antagonist in mice affect plasma cholesterol level and foam cell lesion size. Proc. Natl. Acad. Sci. U.S.A. 99, 6280-6285. doi: 10.1073/pnas.092324399 99/9/6280
Donners, M. M., Beckers, L., Lievens, D., Munnix, I., Heemskerk, J., Janssen, B. J.,et al. (2008). The CD40-TRAF6 axis is the key regulator of the CD40/CD40L system in neointima formation and arterial remodeling. Blood 111, 4596-4604. doi: 10.1182/blood-2007-05-088906
Donners, M. M., Wolfs, I. M., Stoger, L. J., Van Der Vorst, E. P., Pottgens, C. C., Heymans, S.,et al. (2012). Hematopoietic miR155 deficiency enhances atherosclerosis and decreases plaque stability in hyperlipidemic mice. PLoS ONE 7:e35877. doi: 10.1371/journal.pone.0035877
Etzrodt, M., Cortez-Retamozo, V., Newton, A., Zhao, J., Ng, A., Wildgruber, M.,et al. (2012). Regulation of monocyte functional heterogeneity by miR-146a and Relb. Cell Rep. 1, 317-324. doi: 10.1016/j.celrep.2012.02.009
Fagerlund, R., Kinnunen, L., Kohler, M., Julkunen, I., and Melen, K. (2005). NF-{kappa}B is transported into the nucleus by importin {alpha}3 and importin {alpha}4. J. Biol. Chem. 280, 15942-15951. doi: 10.1074/jbc.M500814200
Fang, Y., and Davies, P. F. (2012). Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arterioscler. Thromb. Vasc. Biol. 32, 979-987. doi: 10.1161/ATVBAHA.111.244053
Fang, Y., Shi, C., Manduchi, E., Civelek, M., and Davies, P. F. (2010). MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc. Natl. Acad. Sci. U.S.A. 107, 13450-13455. doi: 10.1073/pnas.1002120107
Fichtlscherer, S., De Rosa, S., Fox, H., Schwietz, T., Fischer, A., Liebetrau, C.,et al. (2010). Circulating microRNAs in patients with coronary artery disease. Circ. Res. 107, 677-684. doi: 10.1161/CIRCRESAHA.109.215566
Gantier, M. P., Stunden, H. J., Mccoy, C. E., Behlke, M. A., Wang, D., Kaparakis-Liaskos, M.,et al. (2012). A miR-19 regulon that controls NF-kappaB signaling. Nucleic Acids Res. 40, 8048-8058. doi: 10.1093/nar/gks521
Gareus, R., Kotsaki, E., Xanthoulea, S., Van Der Made, I., Gijbels, M. J., Kardakaris, R.,et al. (2008). Endothelial cell-specific NF-kappaB inhibition protects mice from atherosclerosis. Cell Metab. 8, 372-383. doi: 10.1016/j.cmet.2008.08.016
Ge, D., Han, L., Huang, S., Peng, N., Wang, P., Jiang, Z.,et al. (2014). Identification of a novel MTOR activator and discovery of a competing endogenous RNA regulating autophagy in vascular endothelial cells. Autophagy 10, 957-971. doi: 10.4161/auto.28363
Gregory, R. I., Chendrimada, T. P., Cooch, N., and Shiekhattar, R. (2005). Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 123, 631-640. doi: 10.1016/j.cell.2005.10.022
Grishok, A., Pasquinelli, A. E., Conte, D., Li, N., Parrish, S., Ha, I.,et al. (2001). Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23-34. doi: 10.1016/S0092-8674(01)00431-7
Guil, S., and Esteller, M. (2012). Cis-acting noncoding RNAs: friends and foes. Nat. Struct. Mol. Biol. 19, 1068-1075. doi: 10.1038/nsmb.2428
Guttman, M., Donaghey, J., Carey, B. W., Garber, M., Grenier, J. K., Munson, G.,et al. (2011). lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477, 295-300. doi: 10.1038/nature10398
Hamik, A., Lin, Z., Kumar, A., Balcells, M., Sinha, S., Katz, J.,et al. (2007). Kruppel-like factor 4 regulates endothelial inflammation. J. Biol. Chem. 282, 13769-13779. doi: 10.1074/jbc.M700078200
Hamon, Y., Broccardo, C., Chambenoit, O., Luciani, M. F., Toti, F., Chaslin, S.,et al. (2000). ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat. Cell Biol. 2, 399-406. doi: 10.1038/35017029
Hansson, G. K. (2005). Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 352, 1685-1695. doi: 10.1056/NEJMra043430
Harja, E., Bucciarelli, L. G., Lu, Y., Stern, D. M., Zou, Y. S., Schmidt, A. M.,et al. (2004). Early growth response-1 promotes atherogenesis: mice deficient in early growth response-1 and apolipoprotein E display decreased atherosclerosis and vascular inflammation. Circ. Res. 94, 333-339. doi: 10.1161/01.RES.0000112405.61577.95
Harris, T. A., Yamakuchi, M., Ferlito, M., Mendell, J. T., and Lowenstein, C. J. (2008). MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc. Natl. Acad. Sci. U.S.A. 105, 1516-1521. doi: 10.1073/pnas.0707493105
Hayden, M. S., and Ghosh, S. (2004). Signaling to NF-kappaB. Genes Dev. 18, 2195-2224. doi: 10.1101/gad.1228704
Heijnen, H. F., Schiel, A. E., Fijnheer, R., Geuze, H. J., and Sixma, J. J. (1999). Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94, 3791-3799.
Helenius, M., Kyrylenko, S., Vehvilainen, P., and Salminen, A. (2001). Characterization of aging-associated up-regulation of constitutive nuclear factor-kappa B binding activity. Antioxid. Redox. Signal. 3, 147-156. doi: 10.1089/152308601750100669
Hergenreider, E., Heydt, S., Treguer, K., Boettger, T., Horrevoets, A. J., Zeiher, A. M.,et al. (2012). Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat. Cell Biol. 14, 249-256. doi: 10.1038/ncb2441
Hinkel, R., Penzkofer, D., Zuhlke, S., Fischer, A., Husada, W., Xu, Q. F.,et al. (2013). Inhibition of microRNA-92a protects against ischemia reperfusion injury in a large-animal model. Circulation 128, 1066-1075. doi: 10.1161/CIRCULATIONAHA.113.001904
Holdt, L. M., Hoffmann, S., Sass, K., Langenberger, D., Scholz, M., Krohn, K.,et al. (2013). Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet. 9:e1003588. doi: 10.1371/journal.pgen.1003588
Hristov, M., Erl, W., Linder, S., and Weber, P. C. (2004). Apoptotic bodies from endothelial cells enhance the number and initiate the differentiation of human endothelial progenitor cells in vitro. Blood 104, 2761-2766. doi: 10.1182/blood-2003-10-3614
Huang, R. S., Hu, G. Q., Lin, B., Lin, Z. Y., and Sun, C. C. (2010). MicroRNA-155 silencing enhances inflammatory response and lipid uptake in oxidized low-density lipoprotein-stimulated human THP-1 macrophages. J. Investig. Med. 58, 961-967. doi: 10.231/JIM.0b013e3181ff46d7
Hull, C., Mclean, G., Wong, F., Duriez, P. J., and Karsan, A. (2002). Lipopolysaccharide signals an endothelial apoptosis pathway through TNF receptor-associated factor 6-mediated activation of c-Jun NH2-terminal kinase. J. Immunol. 169, 2611-2618. doi: 10.4049/jimmunol.169.5.2611
IIott, N. E., Heward, J. A., Roux, B., Tsitsiou, E., Fenwick, P. S., Lenzi, L.,et al. (2014). Long non-coding RNAs and enhancer RNAs regulate the lipopolysaccharide-induced inflammatory response in human monocytes. Nat. Commun. 5, 3979. doi: 10.1038/ncomms4979
Janssen, H. L., Reesink, H. W., Lawitz, E. J., Zeuzem, S., Rodriguez-Torres, M., Patel, K.,et al. (2013). Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 368, 1685-1694. doi: 10.1056/NEJMoa1209026
Janssens, S., Burns, K., Tschopp, J., and Beyaert, R. (2002). Regulation of interleukin-1- and lipopolysaccharide-induced NF-kappaB activation by alternative splicing of MyD88. Curr. Biol. 12, 467-471. doi: 10.1016/S0960-9822(02)00712-1
Janssens, S., Burns, K., Vercammen, E., Tschopp, J., and Beyaert, R. (2003). MyD88S, a splice variant of MyD88, differentially modulates NF-kappaB- and AP-1-dependent gene expression. FEBS Lett. 548, 103-107. doi: 10.1016/S0014-5793(03)00747-6
Jarinova, O., Stewart, A. F., Roberts, R., Wells, G., Lau, P., Naing, T.,et al. (2009). Functional analysis of the chromosome 9p21.3 coronary artery disease risk locus. Arterioscler. Thromb. Vasc. Biol. 29, 1671-1677. doi: 10.1161/ATVBAHA.109.189522
Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M., and Sarnow, P. (2005). Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309, 1577-1581. doi: 10.1126/science.1113329
Jy, W., Minagar, A., Jimenez, J. J., Sheremata, W. A., Mauro, L. M., Horstman, L. L.,et al. (2004). Endothelial microparticles (EMP) bind and activate monocytes: elevated EMP-monocyte conjugates in multiple sclerosis. Front. Biosci. 9:3137-3144. doi: 10.2741/1466
Kanters, E., Pasparakis, M., Gijbels, M. J., Vergouwe, M. N., Partouns-Hendriks, I., Fijneman, R. J.,et al. (2003). Inhibition of NF-kappaB activation in macrophages increases atherosclerosis in LDL receptor-deficient mice. J. Clin. Invest. 112, 1176-1185. doi: 10.1172/JCI18580 112/8/1176
Kirii, H., Niwa, T., Yamada, Y., Wada, H., Saito, K., Iwakura, Y.,et al. (2003). Lack of interleukin-1beta decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23, 656-660. doi: 10.1161/01.ATV.0000064374
Kobayashi, K., Hernandez, L. D., Galan, J. E., Janeway, C. A. Jr., Medzhitov, R., and Flavell, R. A. (2002). IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110, 191-202. doi: 10.1016/S0092-8674(02)00827-9
Krawczyk, M., and Emerson, B. M. (2014). p50-associated COX-2 extragenic RNA (PACER) activates COX-2 gene expression by occluding repressive NF-kappaB complexes. Elife 3, e01776. doi: 10.7554/eLife.01776
Krecic, A. M., and Swanson, M. S. (1999). hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11, 363-371. doi: 10.1016/S0955-0674(99)80051-9
Krutzfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M.,et al. (2005). Silencing of microRNAs in vivo with 'antagomirs'. Nature 438, 685-689. doi: 10.1038/nature04303
Lacroix, R., Plawinski, L., Robert, S., Doeuvre, L., Sabatier, F., Martinez De Lizarrondo, S.,et al. (2012). Leukocyte- and endothelial-derived microparticles: a circulating source for fibrinolysis. Haematologica 97, 1864-1872. doi: 10.3324/haematol.2012.066167
Lakatta, E. G., and Levy, D. (2003). Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part I: aging arteries: a "set up" for vascular disease. Circulation 107, 139-146. doi: 10.1161/01.CIR.0000048892.83521.58
Lam, M. T., Li, W., Rosenfeld, M. G., and Glass, C. K. (2014). Enhancer RNAs and regulated transcriptional programs. Trends Biochem. Sci. 39, 170-182. doi: 10.1016/j.tibs.2014.02.007
Lanford, R. E., Hildebrandt-Eriksen, E. S., Petri, A., Persson, R., Lindow, M., Munk, M. E.,et al. (2010). Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201. doi: 10.1126/science.1178178
Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J.,et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419. doi: 10.1038/nature01957
Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H.,et al. (2004). MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051-4060. doi: 10.1038/sj.emboj.7600385
Leroyer, A. S., Anfosso, F., Lacroix, R., Sabatier, F., Simoncini, S., Njock, S. M.,et al. (2010). Endothelial-derived microparticles: biological conveyors at the crossroad of inflammation, thrombosis and angiogenesis. Thromb. Haemost. 104, 456-463. doi: 10.1160/TH10-02-0111
Li, C. C., Eaton, S. A., Young, P. E., Lee, M., Shuttleworth, R., Humphreys, D. T.,et al. (2013a). Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol. 10, 1333-1344. doi: 10.4161/rna.25281
Li, W., Notani, D., Ma, Q., Tanasa, B., Nunez, E., Chen, A. Y.,et al. (2013b). Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498, 516-520. doi: 10.1038/nature12210
Liew, F. Y., Xu, D., Brint, E. K., and O'neill, L. A. (2005). Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5, 446-458. doi: 10.1038/nri1630
Lomaga, M. A., Yeh, W. C., Sarosi, I., Duncan, G. S., Furlonger, C., Ho, A.,et al. (1999). TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 13, 1015-1024. doi: 10.1101/gad.13.8.1015
Lovren, F., Pan, Y., Quan, A., Singh, K. K., Shukla, P. C., Gupta, N.,et al. (2012). MicroRNA-145 targeted therapy reduces atherosclerosis. Circulation 126, S81-S90. doi: 10.1161/CIRCULATIONAHA.111.084186
Loyer, X., Potteaux, S., Vion, A. C., Guerin, C. L., Boulkroun, S., Rautou, P. E.,et al. (2014). Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ. Res. 114, 434-443. doi: 10.1161/CIRCRESAHA.114.302213
Lu, L. F., Boldin, M. P., Chaudhry, A., Lin, L. L., Taganov, K. D., Hanada, T.,et al. (2010). Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 142, 914-929. doi: 10.1016/j.cell.2010.08.012
Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E., and Kutay, U. (2004). Nuclear export of microRNA precursors. Science 303, 95-98. doi: 10.1126/science.1090599
Mallat, Z., Benamer, H., Hugel, B., Benessiano, J., Steg, P. G., Freyssinet, J. M.,et al. (2000). Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 101, 841-843. doi: 10.1161/01.CIR.101.8.841
McPherson, R., Pertsemlidis, A., Kavaslar, N., Stewart, A., Roberts, R., Cox, D. R.,et al. (2007). A common allele on chromosome 9 associated with coronary heart disease. Science 316, 1488-1491. doi: 10.1126/science.1142447
Michalik, K. M., You, X., Manavski, Y., Doddaballapur, A., Zornig, M., Braun, T.,et al. (2014). Long noncoding RNA MALAT1 regulates endothelial cell function and vessel growth. Circ. Res. 114, 1389-1397. doi: 10.1161/CIRCRESAHA.114.303265
Michelsen, K. S., Wong, M. H., Shah, P. K., Zhang, W., Yano, J., Doherty, T. M.,et al. (2004). Lack of Toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc. Natl. Acad. Sci. U.S.A. 101, 10679-10684. doi: 10.1073/pnas.0403249101
Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L.,et al. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 105, 10513-10518. doi: 10.1073/pnas.0804549105
Mittelbrunn, M., and Sanchez-Madrid, F. (2012). Intercellular communication: diverse structures for exchange of genetic information. Nat. Rev. Mol. Cell Biol. 13, 328-335. doi: 10.1038/nrm3335
Motterle, A., Pu, X., Wood, H., Xiao, Q., Gor, S., Ng, F. L.,et al. (2012). Functional analyses of coronary artery disease associated variation on chromosome 9p21 in vascular smooth muscle cells. Hum. Mol. Genet. 21, 4021-4029. doi: 10.1093/hmg/dds224
Mousavi, K., Zare, H., Dell'orso, S., Grontved, L., Gutierrez-Cruz, G., Derfoul, A.,et al. (2013). eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell. 51, 606-617. doi: 10.1016/j.molcel.2013.07.022
Nahid, M. A., Pauley, K. M., Satoh, M., and Chan, E. K. (2009). miR-146a is critical for endotoxin-induced tolerance: IMPLICATION IN INNATE IMMUNITY. J. Biol. Chem. 284, 34590-34599. doi: 10.1074/jbc.M109.056317
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. J. Clin. Invest. 122, 4190-4202. doi: 10.1172/JCI61716
Ni, C. W., Qiu, H., and Jo, H. (2011). MicroRNA-663 upregulated by oscillatory shear stress plays a role in inflammatory response of endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 300, H1762-H1769. doi: 10.1152/ajpheart.00829.2010
Nozaki, T., Sugiyama, S., Koga, H., Sugamura, K., Ohba, K., Matsuzawa, Y.,et al. (2009). Significance of a multiple biomarkers strategy including endothelial dysfunction to improve risk stratification for cardiovascular events in patients at high risk for coronary heart disease. J. Am. Coll. Cardiol. 54, 601-608. doi: 10.1016/j.jacc.2009.05.022
O'Connell, R. M., Kahn, D., Gibson, W. S., Round, J. L., Scholz, R. L., Chaudhuri, A. A.,et al. (2010). MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33, 607-619. doi: 10.1016/j.immuni.2010.09.009
Okoye, I. S., Coomes, S. M., Pelly, V. S., Czieso, S., Papayannopoulos, V., Tolmachova, T.,et al. (2014). MicroRNA-Containing T-Regulatory-Cell-derived exosomes suppress pathogenic T helper 1 cells. Immunity 41, 89-103. doi: 10.1016/j.immuni.2014.05.019
Olivieri, F., Lazzarini, R., Recchioni, R., Marcheselli, F., Rippo, M. R., Di Nuzzo, S.,et al. (2013). MiR-146a as marker of senescence-associated pro-inflammatory status in cells involved in vascular remodelling. Age (Dordr) 35, 1157-1172. doi: 10.1007/s11357-012-9440-8
Osorio, F. G., Barcena, C., Soria-Valles, C., Ramsay, A. J., De Carlos, F., Cobo, J.,et al. (2012). Nuclear lamina defects cause ATM-dependent NF-kappaB activation and link accelerated aging to a systemic inflammatory response. Genes Dev. 26, 2311-2324. doi: 10.1101/gad.197954.112
Pigati, L., Yaddanapudi, S. C., Iyengar, R., Kim, D. J., Hearn, S. A., Danforth, D.,et al. (2010). Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS ONE 5:e13515. doi: 10.1371/journal.pone.0013515
Pober, J. S., and Sessa, W. C. (2007). Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 7, 803-815. doi: 10.1038/nri2171
Qin, X., Wang, X., Wang, Y., Tang, Z., Cui, Q., Xi, J.,et al. (2010). MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 107, 3240-3244. doi: 10.1073/pnas.0914882107
Raitoharju, E., Lyytikainen, 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. doi: 10.1016/j.atherosclerosis.2011.07.020
Rapicavoli, N. A., Qu, K., Zhang, J., Mikhail, M., Laberge, R. M., and Chang, H. Y. (2013). A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. Elife 2, e00762. doi: 10.7554/eLife.00762
Rau, C. S., Yang, J. C., Chen, Y. C., Wu, C. J., Lu, T. H., Tzeng, S. L.,et al. (2014). Lipopolysaccharide-induced microRNA-146a targets CARD10 and regulates angiogenesis in human umbilical vein endothelial cells. Toxicol. Sci. 140, 315-326. doi: 10.1093/toxsci/kfu097
Rinn, J. L., and Chang, H. Y. (2012). Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81, 145-166. doi: 10.1146/annurev-biochem-051410-092902
Rodriguez, A., Vigorito, E., Clare, S., Warren, M. V., Couttet, P., Soond, D. R.,et al. (2007). Requirement of bic/microRNA-155 for normal immune function. Science 316, 608-611. doi: 10.1126/science.1139253
Sabin, L. R., Delas, M. J., and Hannon, G. J. (2013). Dogma derailed: the many influences of RNA on the genome. Mol. Cell. 49, 783-794. doi: 10.1016/j.molcel.2013.02.010
Salminen, A., Kauppinen, A., and Kaarniranta, K. (2012). Emerging role of NF-kappaB signaling in the induction of senescence-associated secretory phenotype (SASP). Cell. Signal. 24, 835-845. doi: 10.1016/j.cellsig.2011.12.006
Sarlon-Bartoli, G., Bennis, Y., Lacroix, R., Piercecchi-Marti, M. D., Bartoli, M. A., Arnaud, L.,et al. (2013). Plasmatic level of leukocyte-derived microparticles is associated with unstable plaque in asymptomatic patients with high-grade carotid stenosis. J. Am. Coll. Cardiol. 62, 1436-1441. doi: 10.1016/j.jacc.2013.03.078
Sato, S., Sanjo, H., Takeda, K., Ninomiya-Tsuji, J., Yamamoto, M., Kawai, T.,et al. (2005). Essential function for the kinase TAK1 in innate and adaptive immune responses. Nat. Immunol. 6, 1087-1095. doi: 10.1038/ni1255
Schonrock, N., Harvey, R. P., and Mattick, J. S. (2012). Long noncoding RNAs in cardiac development and pathophysiology. Circ. Res. 111, 1349-1362. doi: 10.1161/CIRCRESAHA.112.268953
Schulz, S., Schagdarsurengin, U., Suss, T., Muller-Werdan, U., Werdan, K., and Glaser, C. (2004). Relation between the tumor necrosis factor-alpha (TNF-alpha) gene and protein expression, and clinical, biochemical, and genetic markers: age, body mass index and uric acid are independent predictors for an elevated TNF-alpha plasma level in a complex risk model. Eur. Cytokine Netw. 15, 105-111.
SenBanerjee, S., Lin, Z., Atkins, G. B., Greif, D. M., Rao, R. M., Kumar, A.,et al. (2004). KLF2 Is a novel transcriptional regulator of endothelial proinflammatory activation. J. Exp. Med. 199, 1305-1315. doi: 10.1084/jem.20031132
Serhan, C. N., Brain, S. D., Buckley, C. D., Gilroy, D. W., Haslett, C., O'neill, L. A.,et al. (2007). Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21, 325-332. doi: 10.1096/fj.06-7227rev
Simoncini, S., Njock, M. S., Robert, S., Camoin-Jau, L., Sampol, J., Harle, J. R.,et al. (2009). TRAIL/Apo2L mediates the release of procoagulant endothelial microparticles induced by thrombin in vitro: a potential mechanism linking inflammation and coagulation. Circ. Res. 104, 943-951. doi: 10.1161/CIRCRESAHA.108.183285
Simons, M., and Raposo, G. (2009). Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581. doi: 10.1016/j.ceb.2009.03.007
Sprague, A. H., and Khalil, R. A. (2009). Inflammatory cytokines in vascular dysfunction and vascular disease. Biochem. Pharmacol. 78, 539-552. doi: 10.1016/j.bcp.2009.04.029
Stadthagen, G., Tehler, D., Hoyland-Kroghsbo, N. M., Wen, J., Krogh, A., Jensen, K. T.,et al. (2013). Loss of miR-10a activates lpo and collaborates with activated Wnt signaling in inducing intestinal neoplasia in female mice. PLoS Genet. 9:e1003913. doi: 10.1371/journal.pgen.1003913
Suarez, Y., Wang, C., Manes, T. D., and Pober, J. S. (2010). Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J. Immunol. 184, 21-25. doi: 10.4049/jimmunol.0902369
Sun, X., He, S., Wara, A. K., Icli, B., Shvartz, E., Tesmenitsky, Y.,et al. (2014). Systemic delivery of microRNA-181b inhibits nuclear factor-kappaB activation, vascular inflammation, and atherosclerosis in apolipoprotein E-deficient mice. Circ. Res. 114, 32-40. doi: 10.1161/CIRCRESAHA.113.302089
Sun, X., Icli, B., Wara, A. K., Belkin, N., He, S., Kobzik, L.,et al. (2012). MicroRNA-181b regulates NF-kappaB-mediated vascular inflammation. J. Clin. Invest. 122, 1973-1990. doi: 10.1172/JCI61495
Swirski, F. K., Libby, P., Aikawa, E., Alcaide, P., Luscinskas, F. W., Weissleder, R.,et al. (2007). Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J. Clin. Invest. 117, 195-205. doi: 10.1172/JCI29950
Tabet, F., Vickers, K. C., Cuesta Torres, L. F., Wiese, C. B., Shoucri, B. M., Lambert, G.,et al. (2014). HDL-transferred microRNA-223 regulates ICAM-1 expression in endothelial cells. Nat. Commun. 5, 3292. doi: 10.1038/ncomms4292
Taganov, K. D., Boldin, M. P., Chang, K. J., and Baltimore, D. (2006). NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U.S.A. 103, 12481-12486. doi: 10.1073/pnas.0605298103
Thai, T. H., Calado, D. P., Casola, S., Ansel, K. M., Xiao, C., Xue, Y.,et al. (2007). Regulation of the germinal center response by microRNA-155. Science 316, 604-608. doi: 10.1126/science.1141229
Tian, F. J., An, L. N., Wang, G. K., Zhu, J. Q., Li, Q., Zhang, Y. Y.,et al. (2014). Elevated microRNA-155 promotes foam cell formation by targeting HBP1 in atherogenesis. Cardiovasc. Res. 103, 100-110. doi: 10.1093/cvr/cvu070
Tilstra, J. S., Robinson, A. R., Wang, J., Gregg, S. Q., Clauson, C. L., Reay, D. P.,et al. (2012). NF-kappaB inhibition delays DNA damage-induced senescence and aging in mice. J. Clin. Invest. 122, 2601-2612. doi: 10.1172/JCI45785
Turer, E. E., Tavares, R. M., Mortier, E., Hitotsumatsu, O., Advincula, R., Lee, B.,et al. (2008). Homeostatic MyD88-dependent signals cause lethal inflammation in the absence of A20. J. Exp. Med. 205, 451-464. doi: 10.1084/jem.20071108
Valastyan, S., Reinhardt, F., Benaich, N., Calogrias, D., Szasz, A. M., Wang, Z. C.,et al. (2009). A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137, 1032-1046. doi: 10.1016/j.cell.2009.03.047
van Rooij, E., and Kauppinen, S. (2014). Development of microRNA therapeutics is coming of age. EMBO Mol. Med. 6, 851-864. doi: 10.15252/emmm.201100899
van Rooij, E., Sutherland, L. B., Qi, X., Richardson, J. A., Hill, J., and Olson, E. N. (2007). Control of stress-dependent cardiac growth and gene expression by a microRNA. Science 316, 575-579. doi: 10.1126/science.1139089
VanderLaan, P. A., Reardon, C. A., and Getz, G. S. (2004). Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler. Thromb. Vasc. Biol. 24, 12-22. doi: 10.1161/01.ATV.0000105054.43931
VanWijk, M. J., Vanbavel, E., Sturk, A., and Nieuwland, R. (2003). Microparticles in cardiovascular diseases. Cardiovasc. Res. 59, 277-287. doi: 10.1016/S0008-6363(03)00367-5
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. doi: 10.1016/j.atherosclerosis.2011.03.034
Vickers, K. C., Palmisano, B. T., Shoucri, B. M., Shamburek, R. D., and Remaley, A. T. (2011). MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 13, 423-433. doi: 10.1038/ncb2210
Vigorito, E., Perks, K. L., Abreu-Goodger, C., Bunting, S., Xiang, Z., Kohlhaas, S.,et al. (2007). microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27, 847-859. doi: 10.1016/j.immuni.2007.10.009
Wang, J., An, F. S., Zhang, W., Gong, L., Wei, S. J., Qin, W. D.,et al. (2011a). Inhibition of c-Jun N-terminal kinase attenuates low shear stress-induced atherogenesis in apolipoprotein E-deficient mice. Mol. Med. 17, 990-999. doi: 10.2119/molmed.2011.00073
Wang, J. G., Williams, J. C., Davis, B. K., Jacobson, K., Doerschuk, C. M., Ting, J. P.,et al. (2011b). Monocytic microparticles activate endothelial cells in an IL-1beta-dependent manner. Blood 118, 2366-2374. doi: 10.1182/blood-2011-01-330878
Wang, K., Zhang, S., Weber, J., Baxter, D., and Galas, D. J. (2010a). Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 38, 7248-7259. doi: 10.1093/nar/gkq601
Wang, K. C., Garmire, L. X., Young, A., Nguyen, P., Trinh, A., Subramaniam, S.,et al. (2010b). Role of microRNA-23b in flow-regulation of Rb phosphorylation and endothelial cell growth. Proc. Natl. Acad. Sci. U.S.A. 107, 3234-3239. doi: 10.1073/pnas.0914825107
Wang, L., Zhang, H., Rodriguez, S., Cao, L., Parish, J., Mumaw, C.,et al. (2014). Notch-dependent repression of miR-155 in the bone marrow niche regulates hematopoiesis in an NF-kappaB-dependent manner. Cell Stem Cell 15, 51-65. doi: 10.1016/j.stem.2014.04.021
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. Dev. Cell 15, 261-271. doi: 10.1016/j.devcel.2008.07.002
Weber, C., and Noels, H. (2011). Atherosclerosis: current pathogenesis and therapeutic options. Nat. Med. 17, 1410-1422. doi: 10.1038/nm.2538
Weber, J. A., Baxter, D. H., Zhang, S., Huang, D. Y., Huang, K. H., Lee, M. J.,et al. (2010a). The microRNA spectrum in 12 body fluids. Clin. Chem. 56, 1733-1741. doi: 10.1373/clinchem.2010.147405
Weber, M., Baker, M. B., Moore, J. P., and Searles, C. D. (2010b). MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem. Biophys. Res. Commun. 393, 643-648. doi: 10.1016/j.bbrc.2010.02.045
Wertz, I. E., O'rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S.,et al. (2004). De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 430, 694-699. doi: 10.1038/nature02794
Wesche, H., Gao, X., Li, X., Kirschning, C. J., Stark, G. R., and Cao, Z. (1999). IRAK-M is a novel member of the Pelle/interleukin-1 receptor-associated kinase (IRAK) family. J. Biol. Chem. 274, 19403-19410. doi: 10.1074/jbc.274.27.19403
White, S. J., Nicklin, S. A., Buning, H., Brosnan, M. J., Leike, K., Papadakis, E. D.,et al. (2004). Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109, 513-519. doi: 10.1161/01.CIR.0000109697.68832
Wieland, G. D., Nehmann, N., Muller, D., Eibel, H., Siebenlist, U., Suhnel, J.,et al. (2005). Early growth response proteins EGR-4 and EGR-3 interact with immune inflammatory mediators NF-kappaB p50 and p65. J. Cell Sci. 118, 3203-3212. doi: 10.1242/jcs.02445
Winsauer, G., and de Martin, R. (2007). Resolution of inflammation: intracellular feedback loops in the endothelium. Thromb. Haemost. 97, 364-369.
Wolfrum, S., Teupser, D., Tan, M., Chen, K. Y., and Breslow, J. L. (2007). The protective effect of A20 on atherosclerosis in apolipoprotein E-deficient mice is associated with reduced expression of NF-kappaB target genes. Proc. Natl. Acad. Sci. U.S.A. 104, 18601-18606. doi: 10.1073/pnas.0709011104
Won, D., Zhu, S. N., Chen, M., Teichert, A. M., Fish, J. E., Matouk, C. C.,et al. (2007). Relative reduction of endothelial nitric-oxide synthase expression and transcription in atherosclerosis-prone regions of the mouse aorta and in an in vitro model of disturbed flow. Am. J. Pathol. 171, 1691-1704. doi: 10.2353/ajpath.2007.060860
Work, L. M., Buning, H., Hunt, E., Nicklin, S. A., Denby, L., Britton, N.,et al. (2006). Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses. Mol. Ther. 13, 683-693. doi: 10.1016/j.ymthe.2005.11.013
Wu, X., Fan, W., Fang, R., and Wu, G. (2014b). Regulation of microRNA-155 in endothelial inflammation by targeting nuclear factor (NF)-kappaB P65. J. Cell. Biochem. 115, 1928-1936. doi: 10.1002/jcb.24864
Wu, W., Xiao, H., Laguna-Fernandez, A., Villarreal, G. Jr., Wang, K. C., Geary, G. G.,et al. (2011). Flow-dependent regulation of kruppel-like factor 2 is mediated by microRNA-92a. Circulation 124, 633-641. doi: 10.1161/CIRCULATIONAHA.110.005108
Xiao, B., Liu, Z., Li, B. S., Tang, B., Li, W., Guo, G.,et al. (2009). Induction of microRNA-155 during Helicobacter pylori infection and its negative regulatory role in the inflammatory response. J. Infect. Dis. 200, 916-925. doi: 10.1086/605443
Xue, X., Feng, T., Yao, S., Wolf, K. J., Liu, C. G., Liu, X.,et al. (2011). Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J. Immunol. 187, 5879-5886. doi: 10.4049/jimmunol.1100535
Yamin, T. T., and Miller, D. K. (1997). The interleukin-1 receptor-associated kinase is degraded by proteasomes following its phosphorylation. J. Biol. Chem. 272, 21540-21547. doi: 10.1074/jbc.272.34.21540
Yang, K., He, Y. S., Wang, X. Q., Lu, L., Chen, Q. J., Liu, J.,et al. (2011). MiR-146a inhibits oxidized low-density lipoprotein-induced lipid accumulation and inflammatory response via targeting toll-like receptor 4. FEBS Lett. 585, 854-860. doi: 10.1016/j.febslet.2011.02.009
Yang, L., Boldin, M. P., Yu, Y., Liu, C. S., Ea, C. K., Ramakrishnan, P.,et al. (2012). miR-146a controls the resolution of T cell responses in mice. J. Exp. Med. 209, 1655-1670. doi: 10.1084/jem.20112218
Yang, L., Froberg, J. E., and Lee, J. T. (2014). Long noncoding RNAs: fresh perspectives into the RNA world. Trends Biochem. Sci. 39, 35-43. doi: 10.1016/j.tibs.2013.10.002
Yaron, A., Hatzubai, A., Davis, M., Lavon, I., Amit, S., Manning, A. M.,et al. (1998). Identification of the receptor component of the IkappaBalpha-ubiquitin ligase. Nature 396, 590-594. doi: 10.1038/25159
Yoon, J. H., Abdelmohsen, K., and Gorospe, M. (2014). Functional interactions among microRNAs and long noncoding RNAs. Semin. Cell Dev. Biol. 34, 9-14. doi: 10.1016/j.semcdb.2014.05.015
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. Sci. Signal. 2, ra81. doi: 10.1126/scisignal.2000610
Zhao, J. L., Rao, D. S., Boldin, M. P., Taganov, K. D., O'connell, R. M., and Baltimore, D. (2011). NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc. Natl. Acad. Sci. U.S.A. 108, 9184-9189. doi: 10.1073/pnas.1105398108
Zhou, G., Hamik, A., Nayak, L., Tian, H., Shi, H., Lu, Y.,et al. (2012). Endothelial Kruppel-like factor 4 protects against atherothrombosis in mice. J. Clin. Invest. 122, 4727-4731. doi: 10.1172/JCI66056
Zhou, J., Li, Y. S., Nguyen, P., Wang, K. C., Weiss, A., Kuo, Y. C.,et al. (2013). Regulation of vascular smooth muscle cell turnover by endothelial cell-secreted microRNA-126: role of shear stress. Circ. Res. 113, 40-51. doi: 10.1161/CIRCRESAHA.113.280883
