Clinical Application of Serum microRNAs in Atherosclerotic Coronary Artery Disease
<p>Basic scheme of classic miR biogenesis. The primary miRNA (Pri-miRNA) is produced in the cell nucleus through the transcription of a DNA strand mediated by RNA polymerase II. After transcription, Pri-miRNA is cleaved by the enzymatic complex DROSHA in a micro-RNA precursor (pre-miRNA). Pre-miRNA is exported to the cytoplasm by exportin-5 and cleaved by dicer (RNA degrading enzyme) and produces approximately 22 nucleotide RNA duplexes. A miRNA strand is transferred to the Argonaute complex (AGO), forming an RNA-induced silencing complex (RISC) and guides it to pair with the target messenger RNA (mRNA) through binding the miRNA seed sequence with the miRNA recognition site in the mRNA. miRs are secreted out of cells via exosomes (adapted from Creemers et al., 2012 [<a href="#B9-jcm-11-06849" class="html-bibr">9</a>]).</p> "> Figure 2
<p>Selected miRs that have anti- or pro-atherothrombotic impacts on the development of atherosclerotic plaques, acute coronary syndrome, and/or post-myocardial ischemic outcomes. Please note that specific miRs are important at different stages of atherosclerosis. (1) At early stages of atherosclerosis (from fatty streaks undetectable with standard imaging tools up to intima-media complex thickening), miRs enriched in ECs, VSMCs and macrophages play a key role. Anti-atherothrombotic and anti-inflammatory effects are achieved through many signaling pathways, with a major regulatory role in lipids metabolism and inflammation. (2) At advanced stages of atherosclerosis, with development of mature plaques (easily detectable with various imaging tools), there is a struggle between miRs stabilizing plaque (e.g., increasing fibrous cap thickness, lowering inflammation, or lipids uptake), and miRs destabilizing plaque (e.g., thinning fibrous cap, enlarging lipid and necrotic core, or developing angiogenesis within the plaque). (3) At the stage of plaque rupture and thrombosis, there is a huge role for ECs-, platelets- and VSMCs/cardiomyocytes-derived miRs (such as miR-223 promoting ECs apoptosis, or miR-126 promoting angiogenesis). (4) After ACS, cardiovascular outcomes are associated with myocardial injury and cardiac fibrosis, in which cardiomyocytes-, VSMCs-, ECs-, and fibroblasts-derived miRs play a crucial role. Please note that some miRs can have dual roles, or opposing (conflicting) roles, in different cells (such as miR-223 which aggravates myocardial fibrosis but protects against hypoxia-induced apoptosis and oxidative stress). * miRs that may be used as therapeutic agents are noted in bold in clear green, while miRs that possess antagonists to neutralize their negative effects are in clear orange. CVD: cardiovascular death; ECs: endothelial cells; I/R: ischemia/reperfusion; LVR: left ventricular remodeling; VSMC: vascular smooth muscle cells.</p> ">
Abstract
:1. Introduction
2. Atherosclerotic Stable CAD
2.1. miRs Diagnostic for CAD
2.1.1. Platelets Activity
2.1.2. Vascular Smooth Muscle Cells
2.1.3. Arterial Endothelial Cells
2.1.4. Macrophages
2.1.5. Cardiomyocytes
Postulated Role | microRNA | Down- vs. Up- Regulated | Diagnostic/Therapeutic | Reference |
---|---|---|---|---|
Expressed in many cells | ||||
Highly expressed in VSMCs, ECs, cardiac fibroblasts, cardiomyocytes, and platelet apoptosis and eNOS activity | miR-21-5p | Up | D, up-regulated in CAD patients compared to controls (AUC: 0.767, p < 0.001) | Abdallah H.Y., 2022 [88] |
Platelets | ||||
Humans: collagen-induced platelet aggregation Mice: expression of the P2Y12 receptor | miR-126-3p | Up | D, monitors P2Y12 inhibition | Kaudewitz D., 2016 [26] |
Responsive to antiplatelet therapy | miR-126-3p | Up | T, an antagomir against miR-126-3p reduces platelets aggregation | Kaudewitz D., 2016 [26] |
Marker of platelet activation, that targets the COX-1 receptor through the regulation of TXS | miR-34b-3p | Up | D, miR-34b-3p may facilitate the antiplatelet efficiency of aspirin through inhibiting TXS | Liu W.W., 2009 [28] |
Marker of response to clopidogrel, that targets the P2Y12 receptor | miR-223-3p | Down | D, high on-clopidogrel platelet reactivity | Shi R., 2016 [29] |
miRs released by platelets, that are responsive to antiplatelet therapy | miR-126 miR-150 miR-191 miR-223 | Up Up Up Up | D, antiplatelet therapy significantly reduces their levels | Czajka P., 2021 [31] |
VSMCs | ||||
High expression is needed to maintain a contractile phenotype of VSMCs | miR-22 | Down | T, a stent with an miR-22 coating showed significant capability to inhibit in-stent restenosis (an animal study) | Yang F., 2018 [40] |
Mitigates atherosclerosis, VSMCs contractility, increases fibrous cap area, and reduces the necrotic core area | miR-145 | Down Down | T, delivery of miR-145 may limit atherosclerotic plaque growth, and restore contractile levels in VSMCs | Patel N., 2022 [42] |
Down-regulation of miR-145 plays a critical role in the pathogenesis of atherosclerotic plaques, and neointimal hyperplasia | miR-145 | Down | D, reduced plasma miR-145 levels correlate with an increase in CAD severity (SYNTAX score) | Gao H., 2015 [44] |
Induces VSMC senescence, promotes the expression of age-associated pro-inflammatory secretory factors, and increases the binding capacity of ox-LDL to macrophages | miR-34a | Up | D, increased expression in CAD, compared to healthy controls (AUC: 0.899, p < 0.001), associated with Gensini score (p < 0.001) | Li H., 2022 [50] |
Arterial endothelial cells | ||||
Plays a crucial anti-atherogenic role by regulating the function of ECs and enhancing endothelial repair | miR-126-3p | Down | D, reduced expression is associated with more severe and complex CAD | Li H., 2016 [57] |
Decreases size of atherosclerotic lesions, alleviates ox-LDL-induced EC injury | miR-126-3p | Down Up | D, decreased expression in CAD patients, compared to healthy controls, but up-regulated in ACS | Wang X., 2017, [58] |
Induces EC apoptosis, development of atherosclerosis | miR-142-3p | Up | T, down-regulation of miR-142-3p suppresses ECs apoptosis | Qin, B., 2018 [60] |
Induces apoptosis and oxidative stress, and is pro-atherosclerotic | miR-92a-3p miR-486 | Up Up | D, discriminate between stable and vulnerable CAD | Niculescu L.S., 2015 [66] |
Lipid metabolism | miR-122 | Up | D, increased in CAD patients, and with CAD severity (Gensini score) | Gao W., 2012 [67] |
Recovery of ischemic tissue | miR-17 | Down | D, reduced expression is associated with more severe and complex CAD | Chen J., 2015 [68] |
Rate of apoptosis in ECs | miR-17-5p | Up | T, inhibition of miR-17 suppresses apoptosis, hence, decreases infarct size area, and improves microcirculation of heart tissue, decreasing heart failure symptoms | Yang S., 2018 [69] |
Macrophages | ||||
Regulator of cholesterol and fatty acid homeostasis, reverse cholesterol transport, increases HDL-cholesterol level | miR-33a miR-33b | Up Up | T, inhibition of miR-33a facilitates atherosclerotic regression | Price N.L., 2017 [72] |
Inhibits oxidized LDL-induced lipid accumulation and inflammatory response | miR-146a | Up | D, patients with stable CAD had 3.62-fold higher expression level, compared to controls (AUC:0.767) | Abdallah H.Y., 2022 [88] |
Reduced in diabetics, has a role in lipid metabolism | miR-155 | Down | D, patients with stable CAD had 1.89-fold lower expression level, compared to controls (AUC:0.767) | Abdallah H.Y., 2022 [88] |
Cardiomyocytes | ||||
Indicates myocardial damage | miR-223-5p | Up | D, increased expression, compared to healthy control group, with a AUC of 0.933 for predicting CAD severity | Guo J.F., 2018 [86] |
Suppresses EC proliferation rate, viability, and migration activity involved in heart development, and indicates myocardial damage | miR-133a | Up | D, increased expression in CAD, compared to healthy controls, but with a low AUC of 0.597 correlates with Gensini score of CAD severity (r = 0.303, p = 0.007) | Zhu L., 2017 [87] |
Indicates myocardial damage Indicates myocardial damage Fibrous cap increase Indicates myocardial damage Fibrous cap thinning Plaque neovascularization Indicates myocardial damage | miR-133a miR-182 miR-145 miR-205 miR-208a miR-21 miR-126 miR-223 | Down Up Up Up Down Up Up Up | CAD vs. controls: AUC: 0.863, p < 0.001 AUC: 0.959, p < 0.001 AUC: 0.836, p < 0.001 AUC: 0.959, p < 0.001 AUC: 0.616, p = 0.015 AUC: 0.767, p < 0.001 AUC: 0.767, p < 0.001 AUC: 0.616, p = 0.015 | Abdallah H.Y., 2022 [88] |
Induces angiogenesis and myocardial damage Indicate myocardial damage | miR-1 miR-133a | Up Up | D, increased expression, compared to a healthy control group | Kuwabara Y., 2011 [90] |
Expressed in myocardial cells | miR-23a | Up | D, up-regulated, positive correlation with CAD severity | Lu H.Q., 2013 [91] |
Cardiac myofibroblast differentiation, smooth muscle cell modulator, increases fibrous cap area, reduces necrotic core | miR-145 | Down | D, reduced in patients with cardiac ischemia | Zhang M., 2017 [92] |
Indicates myocardial damage, cardiac hypertrophy Protects against H2O2-induced apoptosis | miR-208b miR-499 | Up Up | D, independent predictors of a high SYNTAX score miR-208b: AUC: 0.775, p < 0.001 miR-499: AUC: 0.713, p < 0.001 | Wang W., 2019 [93] |
Increases foam cell formation | miR-23a | Up | D, correlates with CAD severity (Gensini score) | Wang S., 2016 [94] |
3. Acute Coronary Syndrome
3.1. miRs Diagnostic in ACS
Differences between STEMI and NSTEMI
Study Groups, N of Participants | microRNA | Down vs. Up-Regulated | Rationale for Use of Individual microRNA | AUC, or OR (95% CI), p-Value | Reference |
---|---|---|---|---|---|
STEMI/NSTEMI, 93 Healthy Controls, 66 | miR-1 | Up | D, early marker, up-regulated expression, compared to healthy control group | AUC: 0.774, p < 0.001 | Ai J., 2010 [102] |
STEMI/NSTEMI, 17 Healthy Controls, 25 | miR-1 miR-126-3p | Up Down | D, early markers, changed expressions, compared to healthy control group | AUC: 0.92, p = 0.001 AUC: 0.860, p = 0.01 | Long G., 2012 [103] |
STEMI/NSTEMI, 33 Healthy Controls, 33 | miR-1 miR-133a miR-208a miR-499 | Up Up Up Up | D, early markers, increased expressions, compared to healthy control group | AUC: 0.850, p = 0.001 AUC: 0.870, p = 0.01 AUC: 0.970, p = 0.001 AUC: 0.820, p = 0.01 | Wang G.K., 2010 [105] |
STEMI/NSTEMI, 142 Non-ACS chest pain, 100 Healthy Controls, 85 | miR-499 | Up | D, early marker of ACS, 1 h after onset of chest pain, correlated with CK-MB level and cTn, but not superior to cTn (AUC: 0.90) | AUC: 0.860, p < 0.001 | Zhang L., 2015 [107] |
STEMI/NSTEMI, 27 Healthy Controls, 30 | miR-126-3p | Down | D, early marker, diagnostic effect superior to cTn (AUC 0.787) and CK-MB (AUC 0.863) | AUC: 0.992, p < 0.001 | He Y., 2017 [108] |
STEMI, 25 Healthy Controls, 11 | miR-1 miR-133a miR-208b miR-499-5p | Up Up Up Up | D, with a peak within 12 h from onset of chest pain, expression levels of miR-208b correlated with peak cTn and the LV ejection fraction | AUC: 0.980, p < 0.001 AUC: 0.859, p = 0.007 AUC: 1.000, p < 0.001 AUC: 0.989, p < 0.001 | Gidlöf O.; 2011 [109] |
STEMI, 106 NSTEMI, 68 Non-ACS chest pain, 163 | miR-1 | Up | D, early marker of ACS within 3 h since onset of chest pain, similar AUC to cTn (AUC: 0.862, p < 0.001) | AUC: 0.863, p < 0.001 | Su T., 2020 [110] |
STEMI, 15 NSTEMI, 14 Healthy Controls, 21 | miR-17-5p miR-126-5p miR-145-3p | Up Up Up | D, within 4 h after the onset of chest pain | AUC: 0.857, p < 0.001 AUC: 0.802, p < 0.001 AUC: 0.720, p = 0.01 | Xue S., 2019 [111] |
STEMI, 20 CAD, 20 Healthy Controls, 20 | miR-151-3p | Up | D, proceeded release of necrotic markers, increased expression, compared to healthy controls and stable CAD | STEMI vs. controls: AUC: 0.758, p = 0.005 STEMI vs. CAD AUC: 0.754, p = 0.006 | Horvath M., 2020 [112] |
STEMI, 20 CAD, 20 Healthy Controls, 20 | miR-331 | Up | D, proceeded release of necrotic markers, increased expression, compared to healthy and stable CAD | STEMI vs. controls: AUC: 0.790, p = 0.002 STEMI vs. CAD AUC: 0.773, p = 0.003 | Horvath M., 2020 [112] |
STEMI/NSTEMI, 78 Unstable angina, 201 Healthy Controls, 65 | miR-143 miR-145 | Down Down | D, down-regulated compared to controls, good predictive value for the onset of ACS | 0.087 (0.026–0.384), p = 0.019 0.179 (0.08–0.399), p < 0.001 | Meng L., 2022 [113] |
ACS, 500 Healthy Controls, 500 | miR-143 | Down | D, down-regulated compared to controls, good predictive value for the onset of ACS | 0.56 (0.38–0.82), p = 0.003 | Dégano I.R., 2020 [114] |
STEMI, 62 Healthy Controls, 26 | miR-23a-3p miR-30d-5p miR-146a-5p | Down Down Down | D, for STEMI vs. healthy controls; p, correlated with GRACE and APACHE scores of in-hospital mortality, and 1-month survival D, for STEMI vs. healthy controls D, for STEMI vs. healthy controls | AUC: 0.806, p < 0.05 p = 0.045 (log-rank tests) AUC 0.745, p <0.05 AUC 0.800, p < 0.05 | Bukauskas T., 2019 [115] |
NSTEMI, 137 Chest pain *, 905 | miR-126 miR-133 miR-134 | Up Up Up | D, diagnostic for NSTEMI, but not superior to cTn (AUC: 0.937) | AUC: 0.578, p = 0.003 AUC: 0.656, p < 0.001 AUC: 0.506, p = 0.032 | Biener M., 2021 [119] |
NSTEMI, 145 Healthy Controls, 30 | miR-1 miR-133 miR-208 miR-499 | Up Up Up Up | D, for NSTEMI vs. healthy controls, miR-133, miR-208 and miR-499 superior to cTn (AUC: 0.778) | AUC: 0.772, p < 0.05 AUC: 0.928, p < 0.05 AUC: 0.994, p < 0.05 AUC: 0.994, p < 0.05 | Liu G., 2018 [120] |
STEMI, 16 NSTEMI, 27 | miR-134 miR-134 miR-124 miR-133b | Up Up Up Up | D, for STEMI, but not superior to cTn D, for occluded IRA D, for occluded IRA D, for occluded IRA | AUC: 0.725, p = 0.002 AUC: 0.686, p = 0.016 AUC: 0.787, p < 0.001 AUC: 0.704, p = 0.006 | Gacoń J., 2016 [122] |
NSTEMI | miR-223-3p | Down | Marker of response to clopidogrel, targets P2Y12 receptor D, lower response to clopidogrel in NSTEMI | 0.111, (0.018–0.692), p = 0.019 | Zhang Y.Y., 2014 [123] |
3.2. MiRs Worth of Examination as They Might Be Prognostic for Outcomes
3.2.1. miRs Predictive of Plaque Instability and Myocardial Infarction in Patients with Stable CAD or after Index ACS
Study Groups | microRNA | Down vs. Up-Regulated | Prognostic/Therapeutic | Statistical Analysis AUC, or HR/OR (95% CI), p-Value | Reference |
---|---|---|---|---|---|
Cardiovascular events | |||||
2812 general population subjects | miR-423-3p | Up | p, for ACS during a median follow-up of 6 y. | Better model including miR-423 (AUC: 0.806) vs. traditional risk factors (AUC: 0.782) | Wang X., 2020 [125] |
62 STEMI patients 26 healthy controls | miR-23a-3p | Down | p, correlates with GRACE and APACHE scores of in-hospital mortality, and 1-month survival | AUC 0.806, p < 0.05 p = 0.045 (log-rank tests) | Bukauskas T., 2019 [115] |
598 ACS patients randomized to ticagrelor vs. prasugrel treatment | miR-223-3p | Up | p, CVD/re-MI/IS at 30d. CVD/re-MI/IS at 1 y. | 15.74 (2.07–119.9), p = 0.008 3.18 (1.40–7.19), p = 0.006 | Hromadka M., 2021 [127] |
598 ACS patients randomized to ticagrelor vs. prasugrel treatment | miR-126 to miR-223 ratio | Low | p, CVD/re-MI/IS at 30d. CVD/re-MI/IS at 1 y. | 0.14 (0.03–0.61), p = 0.009 0.37 (0.17–0.82), p = 0.014 | Hromadka M., 2021 [127] |
50 STEMI patients 10 healthy controls | miR-223-3p miR-142-3p miR-146a-5p | Up Up Up | p, for CVD/readmission for HF/new cardiovascular intervention | AUC 0.832, p =0.002 AUC 0.732, p = 0.031 AUC 0.848, p = 0.001 | Scărlătescu A.I., 2022 [128] |
340 ACS patients 533 patients with stable CAD | miR-197 miR-223 miR-126 miR-197 miR-223 | Up Up Up Up Up | p, for CVD after MI at 4 y. p, for CVD after adjustment to age at 4 y. | 2.24 (1.25; 4.01), p = 0.006 4.94 (1.42; 17.2), p = 0.012 3.47 (1.39; 8.66), p = 0.008 3.37 (1.35; 8.39), p = 0.009 3.54 (1.41; 8.92), p = 0.007 | Schulte C., 2015 [129] |
430 ACS patients 682 patients with stable CAD | miR-19b miR-132 miR-140-3p miR-150 miR-186 miR-210 | Up Up Up Up Up Up | p, for CVD at 4 years | 3.59 (1.27–10.15), 0.025 2.85 (1.33–6.08), 0.022 2.88 (1.36–6.09), 0.022 2.14 (1.21–3.79), 0.022 2.08 (1.18–3.66), 0.022 3.10 (1.12–8.55), 0.039 | Karakas M., 2017 [130] |
7 STEMI patients 7 healthy controls | miR-146a | Up | p, MACE at 3 years | 1.329 (1.06–1.664), p = 0.01 | Xiao S., 2021 [132] |
21 ACS patients 8 healthy controls | miR-208b | Up | p, elevated miR-208b expression was associated with reduced 6-month survival | 5.08 (1.13–22.82), p = 0.03 | Alavi-Moghaddam M., 2018 [133] |
142 patients with ACS or ischemic carotid event | miR-1-3p | Up | p, expression levels during incident ischemia are risk factors of CVD at 6 y. | 2.73 (1.22–6.12), p = 0.014 | Badacz R., 2021 [134] |
Left ventricular remodeling | |||||
80 patients with STEMI | miR-1 | Up | p, for LVEDV increase >10% at 6 months, better value in combination with CK-MB, Nt-pro-BNP and CMR | miR-1: AUC: 0.680 miR-1 + CMR + NT-pro-BNP+ CK-MB: AUC: 0.890 | Ma Q., 2020 [136] |
44 ACS patients | miR-1 miR-21 miR-29a | Up Up Up | p, for absolute change for LVEDV at 6 months | miR-1 and miR-29b correlated with lower infarct zone, miR-29b correlated with absolute change in LVEDV | Grabmaier, U., 2017 [137] |
14 patients with STEMI | miR-30a-5p | Up | p, for LVEF < 50%, and NT-proBNP > 150pg/mL at 6 months | AUC: 0.750 (0.58–0.92) | Maciejak A., 2018 [138] |
198 ACS patients | miR-21 miR-146a | Up Up | miR-21 and miR-146a are early biomarkers of LVR p, for LVEDV increase >20% at 1 year | miR-146a: AUC: 0.818 miR-21: AUC: 0.719 in combination they have a higher predictive power | Liu, X., 2015 [139] |
359 patients with MI | miR-34a miR-208a | Up Up | p, for CVD and LVEDV increase >10% at 6 months | miR-34a: OR 17.91 (2.07–98.81), p = 0.003 miR-208b: OR 4.18 (1.36–12.83), p = 0.012 combination of the two miRs: OR 18.73 (1.96–101.23), p < 0.001) | Lv P., 2014 [140] |
113 MI patients 59 healthy controls | miR-150 | Down | p, for HF and LVEF at 1-year, better value in combination with BNP | HR: 1.233 (1.125–1.352) miR-150 alone: AUC: 0.764 miR-150 plus BNP: AUC: 0.807 | Lin X., 2019 [141] |
12 ACS patients 12 healthy controls | miR-29a | Up | The greater increase in miR-29a, the greater increase in LVEDV at 90 days post MI | early miR-29a increase correlates with a negative outcome of post-MI LVR | Zile M.R., 2011 [142] |
Ischemia/reperfusion injury | |||||
44 patients deceased (19 for ACS, 25 as SCD) 18 trauma victims | miR-1 miR-499 miR-208 | Up Up Up | p, miR-1 and miR-499 are sensitive markers to diagnose SCD compared ACS, and miR-208 for ACS vs. controls | SCD vs. ACS (AUC: 0.917) SCD vs. ACS (AUC: 0.898) ACS vs. controls (AUC: 0.855) | Pinchi E., 2019 [143] |
24 patients deceased for ACS 8 patients deceased in accidents | miR-1 | Up | p, might play role in cardiac remodeling | 3.8-fold increase in miR-1 in remote myocardium | Boštjancic E., 2010 [144] |
47 patients deceased for ACS, including 23 from VF 8 trauma victims | miR-133a/b | Down | p, may contribute to VF | For VF, 2.9-fold decrease in miR-133a/b level in remote myocardium | Boštjancic E., 2018 [145] |
3.2.2. miRs Associated with Myocardial I/R Injury and LVR
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Kabłak-Ziembicka, A.; Badacz, R.; Przewłocki, T. Clinical Application of Serum microRNAs in Atherosclerotic Coronary Artery Disease. J. Clin. Med. 2022, 11, 6849. https://doi.org/10.3390/jcm11226849
Kabłak-Ziembicka A, Badacz R, Przewłocki T. Clinical Application of Serum microRNAs in Atherosclerotic Coronary Artery Disease. Journal of Clinical Medicine. 2022; 11(22):6849. https://doi.org/10.3390/jcm11226849
Chicago/Turabian StyleKabłak-Ziembicka, Anna, Rafał Badacz, and Tadeusz Przewłocki. 2022. "Clinical Application of Serum microRNAs in Atherosclerotic Coronary Artery Disease" Journal of Clinical Medicine 11, no. 22: 6849. https://doi.org/10.3390/jcm11226849