MiRNAs in aortic aneurysm and dissection: a narrative review

Huahua Zhang; Xiaoqin Cao; Shuo Ke; Jinhong  Xu; Ruixue Shi; Xiaohong  Jiang

doi:10.55092/exrna20240002

Review

Open Access

Cite

Expand

MiRNAs in aortic aneurysm and dissection: a narrative review

download PDF

Huahua Zhang¹, Xiaoqin Cao¹, Shuo Ke¹, Jinhong Xu¹, Ruixue Shi¹, Xiaohong Jiang^1,^2,³^,∗

¹ Nanjing Drum Tower Hospital Center of Molecular Diagnostic and Therapy, State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, Jiangsu 210023, China

² Cambridge University Nanjing Centre of Technology and Innovation, Jiangbei Area, Nanjing, Jiangsu 210023, China

³ Jiangsu Engineering Research Center for MicroRNA Biology and Biotechnology, NJU Advanced Institute of Life Sciences (NAILS), Nanjing, Jiangsu 210023, China

* xiaohongjiang@nju.edu.cn

Volume
Volume 6 Issue 1, 2024
Citation
Zhang H, Cao X, Ke S, Xu J, Shi R, et al. MiRNAs in aortic aneurysm and dissection: a narrative review. ExRNA 2024(1):0002, https://doi.org/10.55092/exrna20240002.
DOI
10.55092/exrna20240002
Copyright
Copyright2024 by the authors. Published by ELSP.

Abstract

Background and Objective: Aortic aneurysm and dissection are serious life-threatening cardiovascular emergencies, and their pathogenesis includes vascular inflammation, extracellular matrix remodeling and matrix metalloproteinases, phenotype switch of vascular smooth muscle cells and apoptosis, but the specific mechanisms have not been fully elucidated. As gene expression regulators, microRNAs are also key molecules in vascular function. This article not only describes the role of microRNAs in the pathogenesis and progression of aortic aneurysm and dissection, but also further illustrates the molecular mechanism of aortic aneurysm and dissection, which is of great significance for their prevention and treatment. In addition, we discuss miRNAs as a clinical biomarker for the diagnosis and monitoring of aortic aneurysms and dissection, as well as the possibility of developing new effective therapeutic targets. Methods: As of October 8, 2023, relevant publications containing miRNAs involvement in aortic aneurysms and dissection were systematically searched in the PubMed database. Key Content and Findings: Many miRNAs are involved in the pathogenesis of aortic aneurysm and dissection, including vascular inflammation, extracellular matrix remodeling, and homeostasis regulation of vascular smooth muscle cells. Among these miRNAs, some candidates have become potential biomarkers for the early diagnosis and long-term prognosis of aortic aneurysm and dissection due to their high sensitivity, specificity and stability. In addition, miRNAs are also becoming important targets for drug discovery. We have summarized miRNAs with clinical application prospects in aortic aneurysm and dissection. Conclusions: MiRNAs play a vital part in the pathogenesis of aortic aneurysm and dissection. The research on miRNAs is moving from the laboratory to the clinical, and miRNAs are expected to be used for the diagnosis and treatment of aortic aneurysm and dissection in the future.

Keywords

miRNAs; aortic aneurysm; aortic dissection

Preview

view pdf

References

[1] Bossone E, Eagle KA. Epidemiology and management of aortic disease: aortic aneurysms and acute aortic syndromes. Nat. Rev. Cardiol. 2021,18:331–348.
[2] Chou E, Pirruccello JP, Ellinor PT, Lindsay ME. Genetics and mechanisms of thoracic aortic disease. Nat. Rev. Cardiol. 2023,20:168–180.
[3] Goldfinger JZ, Halperin JL, Marin ML, Stewart AS, Eagle KA,et al. Thoracic aortic aneurysm and dissection. J. Am. Coll. Cardiol. 2014,64:1725-39.
[4] Rombouts KB, van Merrienboer TAR, Ket JCF, Bogunovic N, van der Velden J, et al. The role of vascular smooth muscle cells in the development of aortic aneurysms and dissections. Eur. J. Clin. Invest. 2022, 52:e13697.
[5] Erbel R, Aboyans V, Boileau C, Bossone E, Bartolomeo RD, et al. 2014 ESC Guidelines on the diagnosis and treatment of aortic diseases: Document covering acute and chronic aortic diseases of the thoracic and abdominal aorta of the adult. The Task Force for the Diagnosis and Treatment of Aortic Diseases of the European Society of Cardiology (ESC). Eur. Heart J. 2014, 35:2873–2926.
[6] Harris KM, Nienaber CA, Peterson MD, Woznicki EM, Braverman AC, et al. Early Mortality in Type A Acute Aortic Dissection: Insights From the International Registry of Acute Aortic Dissection. JAMA. Cardiol. 2022, 7:1009–1015.
[7] Xu Z, Wang Q, Pan J, Sheng X, Hou D, et al. Characterization of serum miRNAs as molecular biomarkers for acute Stanford type A aortic dissection diagnosis. Sci. Rep. 2017, 7:13659.
[8] Komatsu S, Ohara T, Takahashi S, Takewa M, Minamiguchi H, et al. Early detection of vulnerable atherosclerotic plaque for risk reduction of acute aortic rupture and thromboemboli and atheroemboli using non-obstructive angioscopy. Circ. J. 2015, 79:742–750.
[9] Milewicz DM, Ramirez F. Therapies for Thoracic Aortic Aneurysms and Acute Aortic Dissections. Arterioscler. Thromb. Vasc. Biol. 2019, 39:126–136.
[10] Barwari T, Joshi A, Mayr M. MicroRNAs in Cardiovascular Disease. J. Am. Coll. Cardiol. 2016, 68:2577–2584.
[11] Sun LL, Li WD, Lei FR, Li XQ. The regulatory role of microRNAs in angiogenesis-related diseases. J. Cell. Mol. Med. 2018, 22:4568–4587.
[12] Guo DC, Papke CL, He R, Milewicz DM. Pathogenesis of thoracic and abdominal aortic aneurysms. Ann. N. Y. Acad. Sci. 2006, 1085:339–352.
[13] Dale MA, Ruhlman MK, Baxter BT. Inflammatory cell phenotypes in AAAs: their role and potential as targets for therapy. Arterioscler. Thromb. Vasc. Biol. 2015, 35:1746–1755.
[14] Liu X, Chen W, Zhu G, Yang H, Li W, et al. Single-cell RNA sequencing identifies an Il1rn(+)/Trem1(+) macrophage subpopulation as a cellular target for mitigating the progression of thoracic aortic aneurysm and dissection. Cell Discov. 2022, 8:11.
[15] Biros E, Moran CS, Wang Y, Walker PJ, Cardinal J, et al. microRNA profiling in patients with abdominal aortic aneurysms: the significance of miR-155. Clin. Sci (Lond). 2014, 126:795–803.
[16] Maegdefessel L, Spin JM, Raaz U, Eken SM, Toh R, et al. miR-24 limits aortic vascular inflammation and murine abdominal aneurysm development. Nat. Commun. 2014, 5:5214.
[17] Jiao T, Yao Y, Zhang B, Hao DC, Sun QF, et al. Role of MicroRNA-103a Targeting ADAM10 in Abdominal Aortic Aneurysm. Biomed. Res. Int. 2017, 2017:9645874.
[18] Li M, Yang Y, Zong J, Wang Z, Jiang S, et al. miR-564: A potential regulator of vascular smooth muscle cells and therapeutic target for aortic dissection. J. Mol. Cell. Cardiol. 2022, 170:100–114.
[19] Li J, Zhou Q, He X, Cheng Y, Wang D. [Expression of miR-146b in peripheral blood serum and aortic tissues in patients with acute type Stanford A aortic dissection and its clinical significance]. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2017, 42:1136–1142.
[20] Taganov KD, Boldin MP, Chang KJ, Baltimore D. 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. 2006, 103:12481–12486.
[21] Di Gregoli K, Mohamad Anuar NN, Bianco R, White SJ, Newby AC, et al. MicroRNA-181b Controls Atherosclerosis and Aneurysms Through Regulation of TIMP-3 and Elastin. Circ. Res. 2017, 120:49–65.
[22] Nakao T, Horie T, Baba O, Nishiga M, Nishino T, et al. Genetic Ablation of MicroRNA-33 Attenuates Inflammation and Abdominal Aortic Aneurysm Formation via Several Anti-Inflammatory Pathways. Arterioscler. Thromb. Vasc. Biol. 2017, 37:2161–2170.
[23] Sudhahar V, Das A, Horimatsu T, Ash D, Leanhart S, et al. Copper Transporter ATP7A (Copper-Transporting P-Type ATPase/Menkes ATPase) Limits Vascular Inflammation and Aortic Aneurysm Development: Role of MicroRNA-125b. Arterioscler. Thromb. Vasc. Biol. 2019, 39:2320–2337.
[24] Kin K, Miyagawa S, Fukushima S, Shirakawa Y, Torikai K, et al. Tissue- and plasma-specific MicroRNA signatures for atherosclerotic abdominal aortic aneurysm. J. Am. Heart Assoc. 2012, 1:e000745.
[25] Shi X, Ma W, Li Y, Wang H, Pan S, et al. MiR-144-5p limits experimental abdominal aortic aneurysm formation by mitigating M1 macrophage-associated inflammation: Suppression of TLR2 and OLR1. J. Mol. Cell. Cardiol. 2020, 143:1–14.
[26] Huang T, Liu S, Liu R, Pan B, Wang W. Inhibition of miR-188-5p Suppresses Progression of Experimental Abdominal Aortic Aneurysms. J. Cardiovasc. Pharmacol. 2021, 77:107–114.
[27] Hu M, Qiu H, He T, Zhong M. Effect of miRNA-218-5p on Proliferation, Migration, Apoptosis and Inflammation of Vascular Smooth Muscle Cells in Abdominal Aortic Aneurysm and Extracellular Matrix Protein. Iran. J. Public Health 2022, 51:2494–2503.
[28] Lee HJ, Yi JS, Lee HJ, Lee IW, Park KC, et al. Dysregulated Expression Profiles of MicroRNAs of Experimentally Induced Cerebral Aneurysms in Rats. J. Korean Neurosurg. Soc. 2013, 53:72–76.
[29] Kim CW, Kumar S, Son DJ, Jang IH, Griendling KK, et al. Prevention of abdominal aortic aneurysm by anti-microRNA-712 or anti-microRNA-205 in angiotensin II-infused mice. Arterioscler. Thromb. Vasc. Biol. 2014, 34:1412–1421.
[30] Zhang RM, Tiedemann K, Muthu ML, Dinesh NEH, Komarova S, et al. Fibrillin-1-regulated miR-122 has a critical role in thoracic aortic aneurysm formation. Cell. Mol Life Sci. 2022, 79:314.
[31] Khokha R, Murthy A, Weiss A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol. 2013, 13:649–665.
[32] Guo LL, Wu MT, Zhang LW, Chu YX, Tian P, et al. Blocking Interleukin-1 Beta Reduces the Evolution of Thoracic Aortic Dissection in a Rodent Model. Eur. J. Vasc. Endovasc. Surg. 2020, 60:916–924.
[33] Yu Y, Shi E, Gu T, Tang R, Gao S, et al. Overexpression of microRNA-30a contributes to the development of aortic dissection by targeting lysyl oxidase. J. Thorac. Cardiovasc. Surg. 2017, 154:1862–1869.
[34] Qi YF, Shu C, Xiao ZX, Luo MY, Fang K, et al. Post-Transcriptional Control of Tropoelastin in Aortic Smooth Muscle Cells Affects Aortic Dissection Onset. Mol. Cells. 2018, 41:198–206.
[35] Liao M, Zou S, Bao Y, Jin J, Yang J, et al. Matrix metalloproteinases are regulated by MicroRNA 320 in macrophages and are associated with aortic dissection. Exp. Cell Res. 2018, 370:98–102.
[36] Wu J, Song HF, Li SH, Guo J, Tsang K, et al. Progressive Aortic Dilation Is Regulated by miR-17-Associated miRNAs. J. Am. Coll. Cardiol. 2016, 67:2965–2977.
[37] Jones JA, Stroud RE, O'Quinn EC, Black LE, Barth JL, et al. Selective microRNA suppression in human thoracic aneurysms: relationship of miR-29a to aortic size and proteolytic induction. Circ. Cardiovasc. Genet. 2011, 4:605–613.
[38] Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, et al. miR-29b participates in early aneurysm development in Marfan syndrome. Circ. Res. 2012, 110:312–324.
[39] Akerman AW, Collins EN, Peterson AR, Collins LB, Harrison JK, et al. miR-133a Replacement Attenuates Thoracic Aortic Aneurysm in Mice. J. Am. Heart Assoc. 2021, 10:e019862.
[40] Han ZL, Wang HQ, Zhang TS, He YX, Zhou H. Up-regulation of exosomal miR-106a may play a significant role in abdominal aortic aneurysm by inducing vascular smooth muscle cell apoptosis and targeting TIMP-2, an inhibitor of metallopeptidases that suppresses extracellular matrix degradation. Eur. Rev. Med. Pharmacol. Sci. 2020, 24:8087–8095.
[41] Zampetaki A, Attia R, Mayr U, Gomes RS, Phinikaridou A, et al. Role of miR-195 in aortic aneurysmal disease. Circ. Res. 2014, 115:857–866.
[42] Tsai HY, Wang JC, Hsu YJ, Chiu YL, Lin CY, et al. miR-424/322 protects against abdominal aortic aneurysm formation by modulating the Smad2/3/runt-related transcription factor 2 axis. Mol. Ther. Nucleic. Acids. 2022, 27:656–669.
[43] Chan CYT, Cheuk BLY, Cheng SWK. Abdominal Aortic Aneurysm-Associated MicroRNA-516a-5p Regulates Expressions of Methylenetetrahydrofolate Reductase, Matrix Metalloproteinase-2, and Tissue Inhibitor of Matrix Metalloproteinase-1 in Human Abdominal Aortic Vascular Smooth Muscle Cells. Ann. Vasc. Surg. 2017, 42:263–273.
[44] Shen YH, LeMaire SA, Webb NR, Cassis LA, Daugherty A, et al. Aortic Aneurysms and Dissections Series. Arterioscler. Thromb. Vasc. Biol. 2020, 40:e37–e46.
[45] Bennett MR, Sinha S, Owens GK. Vascular Smooth Muscle Cells in Atherosclerosis. Circ. Res. 2016, 118:692–702.
[46] Sun HJ, Ren XS, Xiong XQ, Chen YZ, Zhao MX, et al. NLRP3 inflammasome activation contributes to VSMC phenotypic transformation and proliferation in hypertension. Cell Death Dis. 2017, 8:e3074.
[47] Henderson EL, Geng YJ, Sukhova GK, Whittemore AD, Knox J, et al. Death of smooth muscle cells and expression of mediators of apoptosis by T lymphocytes in human abdominal aortic aneurysms. Circulation 1999,99: 96–104.
[48] Riches K, Angelini TG, Mudhar GS, Kaye J, Clark E, et al. Exploring smooth muscle phenotype and function in a bioreactor model of abdominal aortic aneurysm. J. Transl. Med. 2013, 11:208.
[49] Albinsson S, Suarez Y, Skoura A, Offermanns S, Miano JM, et al. MicroRNAs are necessary for vascular smooth muscle growth, differentiation, and function. Arterioscler. Thromb. Vasc. Biol. 2010, 30:1118–1126.
[50] Xiao Y, Sun Y, Ma X, Wang C, Zhang L, et al. MicroRNA-22 Inhibits the Apoptosis of Vascular Smooth Muscle Cell by Targeting p38MAPKalpha in Vascular Remodeling of Aortic Dissection. Mol. Ther. Nucleic. Acids. 2020, 22:1051–1062.
[51] Sun Y, Xiao Y, Sun H, Zhao Z, Zhu J, et al. miR-27a regulates vascular remodeling by targeting endothelial cells' apoptosis and interaction with vascular smooth muscle cells in aortic dissection. Theranostics 2019, 9:7961–7975.
[52] Wang Z, Zhuang X, Chen B, Feng D, Li G, et al. The Role of miR-107 as a Potential Biomarker and Cellular Factor for Acute Aortic Dissection. DNA Cell Biol. 2020, 39:1895–1906.
[53] Tang Y, Yu S, Liu Y, Zhang J, Han L, et al. MicroRNA-124 controls human vascular smooth muscle cell phenotypic switch via Sp1. Am. J. Physiol. Heart Circ. Physiol. 2017, 313:H641–H649.
[54] Ma Q, Liu J, Li C, Wang D. miR-140-5p inhibits the proliferation, migration and invasion of vascular smooth muscle cells by suppressing the expression of NCKAP1. Folia Histochem. Cytobiol. 2021, 59:22–29.
[55] Shen H, Lu S, Dong L, Xue Y, Yao C, et al. hsa-miR-320d and hsa-miR-582, miRNA Biomarkers of Aortic Dissection, Regulate Apoptosis of Vascular Smooth Muscle Cells. J. Cardiovasc. Pharmacol. 2018, 71:275–282.
[56] Ma R, Zhang D, Song Y, Kong J, Mu C, et al. miR-335-5p regulates the proliferation, migration and phenotypic switching of vascular smooth muscle cells in aortic dissection by directly regulating SP1. Acta Biochim. Biophys. Sin (Shanghai) 2022, 54:961–973.
[57] Wang L, Zhang L, Cui LK, Yue X, Huang L, et al. MiR-590-3p promotes the phenotypic switching of vascular smooth muscle cells by targeting LOX. J. Cardiovasc. Pharmacol. 2023, 82(5):364–374.
[58] Wang L, Wang Z, Zhang R, Huang L, Zhao Z, et al. MiR-4787-5p Regulates Vascular Smooth Muscle Cell Apoptosis by Targeting PKD1 and Inhibiting the PI3K/Akt/FKHR Pathway. J. Cardiovasc. Pharmacol. 2021, 78:288–296.
[59] Wang Y, Dong CQ, Peng GY, Huang HY, Yu YS, et al. MicroRNA-134-5p Regulates Media Degeneration through Inhibiting VSMC Phenotypic Switch and Migration in Thoracic Aortic Dissection. Mol. Ther. Nucleic. Acids. 2019, 16:284–294.
[60] Liao M, Zou S, Weng J, Hou L, Yang L, et al. A microRNA profile comparison between thoracic aortic dissection and normal thoracic aorta indicates the potential role of microRNAs in contributing to thoracic aortic dissection pathogenesis. J. Vasc. Surg. 2011, 53(5):1341–1349.
[61] Xue L, Luo S, Ding H, Liu Y, Huang W, et al. Upregulation of miR-146a-5p is associated with increased proliferation and migration of vascular smooth muscle cells in aortic dissection. J. Clin. Lab. Anal. 2019, 33:e22843.
[62] Yang P, Wu P, Liu X, Feng J, Zheng S, et al. MiR-26b Suppresses the Development of Stanford Type A Aortic Dissection by Regulating HMGA2 and TGF-beta/Smad3 Signaling Pathway. Ann. Thorac. Cardiovasc. Surg. 2020, 26:140–150.
[63] Liu Y, Tian X, Liu D, Zhang X, Yan C,et al. RelB represses miR-193a-5p expression to promote the phenotypic transformation of vascular smooth muscle cells in aortic aneurysm. Biochim. Biophys. Acta Gene Regul. Mech. 2023, 1866:194926.
[64] Aschacher T, Aschacher O, Schmidt K, Enzmann FK, Eichmair E, et al. The Role of Telocytes and Telocyte-Derived Exosomes in the Development of Thoracic Aortic Aneurysm. Int. J. Mol. Sci. 2022, 23(9):4730.
[65] Liu X, Cheng Y, Yang J, Xu L, Zhang C. Cell-specific effects of miR-221/222 in vessels: molecular mechanism and therapeutic application. J. Mol. Cell. Cardiol. 2012, 52:245–255.
[66] Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. Induction of microRNA-221 by platelet-derived growth factor signaling is critical for modulation of vascular smooth muscle phenotype. J. Biol. Chem. 2009, 284:3728–3738.
[67] Gao C, Sun J, Zhang Z, Xu Z. NEAT1 Boosts the Development of Thoracic Aortic Aneurysm Through Targeting miR-324-5p/RAN. Arch. Med. Res. 2022, 53:93–99.
[68] Gao P, Si J, Yang B, Yu J. Upregulation of MicroRNA-15a Contributes to Pathogenesis of Abdominal Aortic Aneurysm (AAA) by Modulating the Expression of Cyclin-Dependent Kinase Inhibitor 2B (CDKN2B). Med. Sci. Monit. 2017, 23:881–888.
[69] Maegdefessel L, Azuma J, Toh R, Deng A, Merk DR, et al. MicroRNA-21 blocks abdominal aortic aneurysm development and nicotine-augmented expansion. Sci. Transl. Med. 2012, 4:122ra22.
[70] Thum T, Gross C, Fiedler J, Fischer T, Kissler S, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 2008, 456:980–984.
[71] Si X, Chen Q, Zhang J, Zhou W, Chen L, et al. MicroRNA-23b prevents aortic aneurysm formation by inhibiting smooth muscle cell phenotypic switching via FoxO4 suppression. Life Sci. 2022, 288:119092.
[72] Leeper NJ, Raiesdana A, Kojima Y, Chun HJ, Azuma J, et al. MicroRNA-26a is a novel regulator of vascular smooth muscle cell function. J. Cell. Physiol. 2011, 226:1035–1043.
[73] Yue J, Zhu T, Yang J, Si Y, Xu X, et al. CircCBFB-mediated miR-28-5p facilitates abdominal aortic aneurysm via LYPD3 and GRIA4. Life Sci. 2020, 253:117533.
[74] Wang Q, Shu C, Su J, Li X. A crosstalk triggered by hypoxia and maintained by MCP-1/miR-98/IL-6/p38 regulatory loop between human aortic smooth muscle cells and macrophages leads to aortic smooth muscle cells apoptosis via Stat1 activation. Int. J. Clin. Exp. Pathol. 2015, 8:2670–2679.
[75] Zhang Y, Liu Z, Zhou M, Liu C. MicroRNA-129-5p inhibits vascular smooth muscle cell proliferation by targeting Wnt5a. Exp. Ther. Med. 2016, 12:2651–2656.
[76] Cao X, Cai Z, Liu J, Zhao Y, Wang X, et al. miRNA-504 inhibits p53-dependent vascular smooth muscle cell apoptosis and may prevent aneurysm formation. Mol. Med. Rep. 2017, 16:2570–2578.
[77] Yang K, Ren J, Li X, Wang Z, Xue L, et al. Prevention of aortic dissection and aneurysm via an ALDH2-mediated switch in vascular smooth muscle cell phenotype. Eur. Heart J. 2020, 41:2442–2453.
[78] Vianello E, Dozio E, Rigolini R, Marrocco-Trischitta MM, Tacchini L, et al. Acute phase of aortic dissection: a pilot study on CD40L, MPO, and MMP-1, -2, 9 and TIMP-1 circulating levels in elderly patients. Immun. Ageing 2016, 13:9.
[79] Ranasinghe AM, Bonser RS. Biomarkers in acute aortic dissection and other aortic syndromes. J. Am. Coll. Cardiol. 2010, 56:1535–1541.
[80] Suzuki T, Distante A, Zizza A, Trimarchi S, Villani M, et al. Diagnosis of acute aortic dissection by D-dimer: the International Registry of Acute Aortic Dissection Substudy on Biomarkers (IRAD-Bio) experience. Circulation 2009, 119:2702–2707.
[81] Liebetrau C, Mollmann H, Dorr O, Szardien S, Troidl C, et al. Release kinetics of circulating muscle-enriched microRNAs in patients undergoing transcoronary ablation of septal hypertrophy. J. Am. Coll. Cardiol. 2013, 62:992–998.
[82] Condorelli G, Latronico MV, Cavarretta E. microRNAs in cardiovascular diseases: current knowledge and the road ahead. J. Am. Coll. Cardiol. 2014, 63:2177—2187.
[83] Zhang W, Shang T, Huang C, Yu T, Liu C, et al. Plasma microRNAs serve as potential biomarkers for abdominal aortic aneurysm. Clin. Biochem. 2015, 48:988–992.
[84] Wang XJ, Huang B, Yang YM, Zhang L, Su WJ, et al. Differential expression of microRNAs in aortic tissue and plasma in patients with acute aortic dissection. J. Geriatr. Cardiol. 2015, 12:655–661.
[85] Tasopoulou KM, Argiriou C, Tsaroucha AK, Georgiadis GS. Circulating miRNAs as Biomarkers for Diagnosis, Surveillance, and Postoperative Follow-Up of Abdominal Aortic Aneurysms. Ann. Vasc. Surg. 2023, 93:387–404.
[86] Tian Y, Li X, Bai C, Yang Z, Zhang L, et al. lncRNA MIR503HG Targets miR-191-5p/PLCD1 Axis and Negatively Modulates Apoptosis, Extracellular Matrix Disruption, and Inflammation in Abdominal Aortic Aneurysm. Mediators. Inflamm. 2023, 2023:4003618.
[87] Iyer V, Rowbotham S, Biros E, Bingley J, Golledge J. A systematic review investigating the association of microRNAs with human abdominal aortic aneurysms. Atherosclerosis 2017, 261:78–89.
[88] Spear R, Boytard L, Blervaque R, Chwastyniak M, Hot D, et al. Adventitial Tertiary Lymphoid Organs as Potential Source of MicroRNA Biomarkers for Abdominal Aortic Aneurysm. Int. J. Mol. Sci. 2015, 16:11276–11293.
[89] Stather PW, Sylvius N, Sidloff DA, Dattani N, Verissimo A, et al. Identification of microRNAs associated with abdominal aortic aneurysms and peripheral arterial disease. Br. J. Surg. 2015, 102:755–766.
[90] Dong J, Bao J, Feng R, Zhao Z, Lu Q, et al. Circulating microRNAs: a novel potential biomarker for diagnosing acute aortic dissection. Sci. Rep. 2017, 7:12784.
[91] Dong J, Li S, Lu Z, Du P, Liu G, et al. HCMV-miR-US33-5p promotes apoptosis of aortic vascular smooth muscle cells by targeting EPAS1/SLC3A2 pathway. Cell. Mol. Biol. Lett. 2022, 27:40.
[92] Zhang D, Zhao X, Wang B, Liu X, Aizezi A,et al. Circulating exosomal miRNAs as novel biomarkers for acute aortic dissection: A diagnostic accuracy study. Medicine (Baltimore) 2023, 102:e34474.
[93] Wang L, Zhang S, Xu Z, Zhang J, Li L, et al. The diagnostic value of microRNA-4787-5p and microRNA-4306 in patients with acute aortic dissection. Am. J. Transl. Res. 2017, 9:5138–5149.
[94] Senturk T, Antal A, Gunel T. Potential function of microRNAs in thoracic aortic aneurysm and thoracic aortic dissection pathogenesis. Mol. Med. Rep. 2019, 20:5353–5362.
[95] Boileau A, Lino Cardenas CL, Courtois A, Zhang L, Rodosthenous RS, et al. MiR-574-5p: A Circulating Marker of Thoracic Aortic Aneurysm. Int. J. Mol. Sci. 2019, 20(16):3924.
[96] Boon RA, Seeger T, Heydt S, Fischer A, Hergenreider E, et al. MicroRNA-29 in aortic dilation: implications for aneurysm formation. Circ. Res. 2011, 109:1115–1119.
[97] Maegdefessel L, Azuma J, Toh R, Merk DR, Deng A, et al. Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J. Clin. Invest. 2012, 122:497–506.
[98] Thum T. MicroRNA therapeutics in cardiovascular medicine. EMBO Mol. Med. 2012, 4:3–14.
[99] Visseren FLJ, Mach F, Smulders YM, Carballo D, Koskinas KC, et al. 2021 ESC Guidelines on cardiovascular disease prevention in clinical practice. Eur. Heart J. 2021, 42:3227–3337.
[100]Hashimoto Y, Akiyama Y, Yuasa Y. Multiple-to-multiple relationships between microRNAs and target genes in gastric cancer. PLoS One 2013, 8:e62589.
[101]Winkle M, El-Daly SM, Fabbri M, Calin GA. Noncoding RNA therapeutics - challenges and potential solutions. Nat. Rev. Drug. Discov. 2021, 20:629–651.