Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 2019; 119(08): 1205-1211
DOI: 10.1055/s-0039-1687874

Theme Issue Article

Georg Thieme Verlag KG Stuttgart · New York

Mechanistic Links between Non-Coding RNAs and Myeloid Cell Inflammation in Atherosclerosis

Valentina Paloschi ^*

¹Department of Vascular and Endovascular Surgery, Technical University of Munich, Munich, Germany

²German Center for Cardiovascular Research, Partner Site Munich, Munich, Germany

,

Hanna Winter^*

¹Department of Vascular and Endovascular Surgery, Technical University of Munich, Munich, Germany

²German Center for Cardiovascular Research, Partner Site Munich, Munich, Germany

,

Joana Viola

²German Center for Cardiovascular Research, Partner Site Munich, Munich, Germany

³Institute for Prevention and Epidemiology of Cardiovascular Diseases, Ludwig-Maximilians-University Munich, Munich, Germany

,

Oliver Soehnlein

²German Center for Cardiovascular Research, Partner Site Munich, Munich, Germany

³Institute for Prevention and Epidemiology of Cardiovascular Diseases, Ludwig-Maximilians-University Munich, Munich, Germany

⁴Department of Physiology and Pharmacology, Karolinska Institute, Stockholm, Sweden

,

Lars Maegdefessel

¹Department of Vascular and Endovascular Surgery, Technical University of Munich, Munich, Germany

²German Center for Cardiovascular Research, Partner Site Munich, Munich, Germany

⁵Department of Medicine, Karolinska Institute, Stockholm, Sweden

› Institutsangaben

Abstract

Inflammation plays a pivotal role in the chronicity of atherosclerotic lesion development and progression. Myeloid cells are involved in all stages of atherosclerosis development: they contribute in early phases to endothelial dysfunction and create a pro-inflammatory environment responsible for disease progression. Numerous studies over the last decade have repeatedly provided evidence for the crucial importance for different classes of non-coding ribonucleic acids (RNAs) in regulating gene expression, as well as messenger RNA and protein stability. Functional studies using tools to either over-express or inhibit these non-coding RNAs showcased strong effects on tempering vascular inflammation and atherosclerosis progression. With this current review article, we want to discuss prominent examples of non-coding RNAs, being either produced by myeloid cells or affecting their recruitment and activity in the context of vascular inflammation, atherosclerosis and consequential diseases (such as myocardial infarction and stroke). All of the discussed transcripts were thoroughly studied in mechanistic explorations, indicating that they have the capability to modulate inflammatory cascades in the vasculature during disease exacerbation.

Keywords

Keywords

atherosclerosis - non-coding RNAs - vascular inflammation

References
1 Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 2010; 122 (18) 1837-1845
2 Ionita MG, van den Borne P, Catanzariti LM. , et al. High neutrophil numbers in human carotid atherosclerotic plaques are associated with characteristics of rupture-prone lesions. Arterioscler Thromb Vasc Biol 2010; 30 (09) 1842-1848
3 Soehnlein O, Wantha S, Simsekyilmaz S. , et al. Neutrophil-derived cathelicidin protects from neointimal hyperplasia. Sci Transl Med 2011; 3 (103) 103ra98
4 Horckmans M, Ring L, Duchene J. , et al. Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype. Eur Heart J 2017; 38 (03) 187-197
5 Maegdefessel L, Dalman RL, Tsao PS. Pathogenesis of abdominal aortic aneurysms: microRNAs, proteases, genetic associations. Annu Rev Med 2014; 65: 49-62
6 Beermann J, Piccoli MT, Viereck J, Thum T. Non-coding RNAs in development and disease: background, mechanisms, and therapeutic approaches. Physiol Rev 2016; 96 (04) 1297-1325
7 Uchida S, Dimmeler S. Long noncoding RNAs in cardiovascular diseases. Circ Res 2015; 116 (04) 737-750
8 Holdt LM, Teupser D. Long noncoding RNA ANRIL: lnc-ing genetic variation at the chromosome 9p21 locus to molecular mechanisms of atherosclerosis. Front Cardiovasc Med 2018; 5: 145
9 Holdt LM, Beutner F, Scholz M. , et al. ANRIL expression is associated with atherosclerosis risk at chromosome 9p21. Arterioscler Thromb Vasc Biol 2010; 30 (03) 620-627
10 Congrains A, Kamide K, Oguro R. , et al. Genetic variants at the 9p21 locus contribute to atherosclerosis through modulation of ANRIL and CDKN2A/B. Atherosclerosis 2012; 220 (02) 449-455
11 Arslan S, Berkan Ö, Lalem T. , et al; Cardiolinc™ network. Long non-coding RNAs in the atherosclerotic plaque. Atherosclerosis 2017; 266: 176-181
12 Canfrán-Duque A, Rotllan N, Zhang X. , et al. Macrophage deficiency of miR-21 promotes apoptosis, plaque necrosis, and vascular inflammation during atherogenesis. EMBO Mol Med 2017; 9 (09) 1244-1262
13 Li K, Ching D, Luk FS, Raffai RL. Apolipoprotein E enhances microRNA-146a in monocytes and macrophages to suppress nuclear factor-κB-driven inflammation and atherosclerosis. Circ Res 2015; 117 (01) e1-e11
14 Cheng HS, Besla R, Li A. , et al. Paradoxical suppression of atherosclerosis in the absence of microRNA-146a. Circ Res 2017; 121 (04) 354-367
15 Nguyen MA, Karunakaran D, Geoffrion M. , et al. Extracellular vesicles secreted by atherogenic macrophages transfer microRNA to inhibit cell migration. Arterioscler Thromb Vasc Biol 2018; 38 (01) 49-63
16 Wei Y, Zhu M, Corbalán-Campos J, Heyll K, Weber C, Schober A. Regulation of Csf1r and Bcl6 in macrophages mediates the stage-specific effects of microRNA-155 on atherosclerosis. Arterioscler Thromb Vasc Biol 2015; 35 (04) 796-803
17 Loyer X, Potteaux S, Vion AC. , et al. Inhibition of microRNA-92a prevents endothelial dysfunction and atherosclerosis in mice. Circ Res 2014; 114 (03) 434-443
18 Wu W, Xiao H, Laguna-Fernandez A. , et al. Flow-dependent regulation of Kruppel-like factor 2 is mediated by microRNA-92a. Circulation 2011; 124 (05) 633-641
19 Fang Y, Davies PF. Site-specific microRNA-92a regulation of Kruppel-like factors 4 and 2 in atherosusceptible endothelium. Arterioscler Thromb Vasc Biol 2012; 32 (04) 979-987
20 Bonauer A, Carmona G, Iwasaki M. , et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 2009; 324 (5935): 1710-1713
21 Rogg EM, Abplanalp WT, Bischof C. , et al. Analysis of cell type-specific effects of microRNA-92a provides novel insights into target regulation and mechanism of action. Circulation 2018; 138 (22) 2545-2558
22 Sallam T, Jones M, Thomas BJ. , et al. Transcriptional regulation of macrophage cholesterol efflux and atherogenesis by a long noncoding RNA. Nat Med 2018; 24 (03) 304-312
23 Liu J, Huang GQ, Ke ZP. Silence of long intergenic noncoding RNA HOTAIR ameliorates oxidative stress and inflammation response in ox-LDL-treated human macrophages by upregulating miR-330–5p. J Cell Physiol 2019; 234 (04) 5134-5142
24 Gast M, Rauch BH, Nakagawa S. , et al. Immune system-mediated atherosclerosis caused by deficiency of long noncoding RNA MALAT1 in ApoE−/− mice. Cardiovasc Res 2019; 115 (02) 302-314
25 Chinetti-Gbaguidi G, Colin S, Staels B. Macrophage subsets in atherosclerosis. Nat Rev Cardiol 2015; 12 (01) 10-17
26 Bras JP, Silva AM, Calin GA, Barbosa MA, Santos SG, Almeida MI. miR-195 inhibits macrophages pro-inflammatory profile and impacts the crosstalk with smooth muscle cells. PLoS One 2017; 12 (11) e0188530
27 Zhang DD, Wang WT, Xiong J. , et al. Long noncoding RNA LINC00305 promotes inflammation by activating the AHRR-NF-κB pathway in human monocytes. Sci Rep 2017; 7: 46204
28 Zhang BY, Jin Z, Zhao Z. Long intergenic noncoding RNA 00305 sponges miR-136 to regulate the hypoxia induced apoptosis of vascular endothelial cells. Biomed Pharmacother 2017; 94: 238-243
29 Chistiakov DA, Sobenin IA, Orekhov AN, Bobryshev YV. Myeloid dendritic cells: Development, functions, and role in atherosclerotic inflammation. Immunobiology 2015; 220 (06) 833-844
30 Subramanian M, Tabas I. Dendritic cells in atherosclerosis. Semin Immunopathol 2014; 36 (01) 93-102
31 Wu C, Gong Y, Yuan J. , et al; KaiHu. microRNA-181a represses ox-LDL-stimulated inflammatory response in dendritic cell by targeting c-Fos. J Lipid Res 2012; 53 (11) 2355-2363
32 Alemdehy MF, van Boxtel NG, de Looper HW. , et al. Dicer1 deletion in myeloid-committed progenitors causes neutrophil dysplasia and blocks macrophage/dendritic cell development in mice. Blood 2012; 119 (20) 4723-4730
33 Gantier MP. The not-so-neutral role of microRNAs in neutrophil biology. J Leukoc Biol 2013; 94 (04) 575-583
34 Gurol T, Zhou W, Deng Q. MicroRNAs in neutrophils: potential next generation therapeutics for inflammatory ailments. Immunol Rev 2016; 273 (01) 29-47
35 Chen CZ, Li L, Lodish HF, Bartel DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303 (5654): 83-86
36 Naqvi AR, Fordham JB, Nares S. miR-24, miR-30b, and miR-142-3p regulate phagocytosis in myeloid inflammatory cells. J Immunol 2015; 194 (04) 1916-1927
37 Fan HB, Liu YJ, Wang L. , et al. miR-142-3p acts as an essential modulator of neutrophil development in zebrafish. Blood 2014; 124 (08) 1320-1330
38 Johnnidis JB, Harris MH, Wheeler RT. , et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008; 451 (7182): 1125-1129
39 Bauernfeind F, Rieger A, Schildberg FA, Knolle PA, Schmid-Burgk JL, Hornung V. NLRP3 inflammasome activity is negatively controlled by miR-223. J Immunol 2012; 189 (08) 4175-4181
40 De Jong OG, Van Balkom BW, Schiffelers RM, Bouten CV, Verhaar MC. Extracellular vesicles: potential roles in regenerative medicine. Front Immunol 2014; 5: 608
41 Pan Y, Liang H, Liu H. , et al. Platelet-secreted microRNA-223 promotes endothelial cell apoptosis induced by advanced glycation end products via targeting the insulin-like growth factor 1 receptor. J Immunol 2014; 192 (01) 437-446
42 Neudecker V, Brodsky KS, Clambey ET. , et al. Neutrophil transfer of miR-223 to lung epithelial cells dampens acute lung injury in mice. Sci Transl Med 2017; 9 (408) eaah5360
43 Chen L, Yang W, Guo Y. , et al. Exosomal lncRNA GAS5 regulates the apoptosis of macrophages and vascular endothelial cells in atherosclerosis. PLoS One 2017; 12 (09) e0185406
44 Sun X, Icli B, Wara AK. , et al; MICU Registry. MicroRNA-181b regulates NF-κB-mediated vascular inflammation. J Clin Invest 2012; 122 (06) 1973-1990
45 Zhou X, Han X, Wittfeldt A. , et al. Long non-coding RNA ANRIL regulates inflammatory responses as a novel component of NF-κB pathway. RNA Biol 2016; 13 (01) 98-108
46 Sun X, Sit A, Feinberg MW. Role of miR-181 family in regulating vascular inflammation and immunity. Trends Cardiovasc Med 2014; 24 (03) 105-112
47 Remus EW, Lyle AN, Weiss D. , et al. miR181a protects against angiotensin II-induced osteopontin expression in vascular smooth muscle cells. Atherosclerosis 2013; 228 (01) 168-174
48 Zernecke A, Bidzhekov K, Noels H. , et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009; 2 (100) ra81
49 Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci U S A 2008; 105 (05) 1516-1521
50 Schober A, Nazari-Jahantigh M, Wei Y. , et al. MicroRNA-126-5p promotes endothelial proliferation and limits atherosclerosis by suppressing Dlk1. Nat Med 2014; 20 (04) 368-376
51 Njock MS, Cheng HS, Dang LT. , et al. Endothelial cells suppress monocyte activation through secretion of extracellular vesicles containing antiinflammatory microRNAs. Blood 2015; 125 (20) 3202-3212
52 Shan K, Jiang Q, Wang XQ. , et al. Role of long non-coding RNA-RNCR3 in atherosclerosis-related vascular dysfunction. Cell Death Dis 2016; 7 (06) e2248
53 Allahverdian S, Chaabane C, Boukais K, Francis GA, Bochaton-Piallat ML. Smooth muscle cell fate and plasticity in atherosclerosis. Cardiovasc Res 2018; 114 (04) 540-550
54 Bennett MR, Sinha S, Owens GK. Vascular smooth muscle cells in atherosclerosis. Circ Res 2016; 118 (04) 692-702
55 Shankman LS, Gomez D, Cherepanova OA. , et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med 2015; 21 (06) 628-637
56 Ridker PM, Everett BM, Thuren T. , et al; CANTOS Trial Group. Antiinflammatory therapy with canakinumab for atherosclerotic disease. N Engl J Med 2017; 377 (12) 1119-1131