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Current Cardiology Reviews

Editor-in-Chief

ISSN (Print): 1573-403X
ISSN (Online): 1875-6557

Review Article

Regulation of HIF-1 by MicroRNAs in Various Cardiovascular Diseases

Author(s): Vahideh Tarhriz, Leila Abkhooie and Mostafa Moradi Sarabi*

Volume 19, Issue 5, 2023

Published on: 05 May, 2023

Article ID: e300323215210 Pages: 6

DOI: 10.2174/1573403X19666230330105259

Price: $65

Abstract

Today, we see an increase in death due to cardiovascular diseases all over the world, which has a lot to do with the regulation of oxygen homeostasis. Also, hypoxia-inducing factor 1 (HIF-1) is considered a vital factor in hypoxia and its physiological and pathological changes. HIF- 1 is involved in cellular activities, including proliferation, differentiation, and cell death in endothelial cells (ECs) and cardiomyocytes. Similar to HIF-1α, which acts as a protective element against various diseases in the cardiovascular system, the protective role of microRNAs (miRNAs) has also been proved using animal models. The number of miRNAs identified in the regulation of gene expression responsive to hypoxia and the importance of investigating the involvement of the non-coding genome in cardiovascular diseases is increasing, which shows the issue's importance. In this study, the molecular regulation of HIF-1 by miRNAs is considered to improve therapeutic approaches in clinical diagnoses of cardiovascular diseases.

Keywords: Hypoxia-Inducible factor 1 (HIF-1), miRNAs, cardiovascular diseases, atherosclerosis, myocardial infarction, cardiac hypertrophy.

Graphical Abstract
[1]
Bishop T, Ratcliffe PJ. HIF hydroxylase pathways in cardiovascular physiology and medicine. Circ Res 2015; 117(1): 65-79.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.305109] [PMID: 26089364]
[2]
Taylor CT, Scholz CC. The effect of HIF on metabolism and immunity. Nat Rev Nephrol 2022; 18(9): 573-87.
[http://dx.doi.org/10.1038/s41581-022-00587-8] [PMID: 35726016]
[3]
Frost J, Frost M, Batie M, Jiang H, Rocha S. Roles of HIF and 2-oxoglutarate-dependent dioxygenases in controlling gene expression in hypoxia. Cancers 2021; 13(2): 350.
[http://dx.doi.org/10.3390/cancers13020350] [PMID: 33477877]
[4]
Bouthelier A, Aragonés J. Role of the HIF oxygen sensing pathway in cell defense and proliferation through the control of amino acid metabolism. Biochim Biophys Acta Mol Cell Res 2020; 1867(9): 118733.
[http://dx.doi.org/10.1016/j.bbamcr.2020.118733] [PMID: 32416106]
[5]
Daly L, Brownridge PJ, Sée V, Eyers CE. Oxygen-dependent changes in HIF binding partners and post-translational modifications regulate stability and transcriptional activity. bioRxiv 2020; 2020-11.
[http://dx.doi.org/10.1101/2020.11.12.379768]
[6]
Albadari N, Deng S, Li W. The transcriptional factors HIF-1 and HIF-2 and their novel inhibitors in cancer therapy. Expert Opin Drug Discov 2019; 14(7): 667-82.
[http://dx.doi.org/10.1080/17460441.2019.1613370] [PMID: 31070059]
[7]
Soni S, Padwad YS. HIF-1 in cancer therapy: Two decade long story of a transcription factor. Acta Oncol 2017; 56(4): 503-15.
[http://dx.doi.org/10.1080/0284186X.2017.1301680] [PMID: 28358664]
[8]
Li X, Zhang Q, Nasser MI, et al. Oxygen homeostasis and cardiovascular disease: A role for HIF? Biomed Pharmacother 2020; 128: 110338.
[http://dx.doi.org/10.1016/j.biopha.2020.110338] [PMID: 32526454]
[9]
Strowitzki M, Cummins E, Taylor C. Protein hydroxylation by hypoxia-inducible factor (HIF) hydroxylases: Unique or ubiquitous? Cells 2019; 8(5): 384.
[http://dx.doi.org/10.3390/cells8050384] [PMID: 31035491]
[10]
Sousa Fialho ML, Abd Jamil AH, Stannard GA, Heather LC. Hypoxia-inducible factor 1 signalling, metabolism and its therapeutic potential in cardiovascular disease. Biochim Biophys Acta Mol Basis Dis 2019; 1865(4): 831-43.
[http://dx.doi.org/10.1016/j.bbadis.2018.09.024] [PMID: 30266651]
[11]
Balamurugan K. HIF-1 at the crossroads of hypoxia, inflammation, and cancer. Int J Cancer 2016; 138(5): 1058-66.
[http://dx.doi.org/10.1002/ijc.29519] [PMID: 25784597]
[12]
Cummins EP, Keogh CE, Crean D, Taylor CT. The role of HIF in immunity and inflammation. Mol Aspects Med 2016; 47-48: 24-34.
[http://dx.doi.org/10.1016/j.mam.2015.12.004] [PMID: 26768963]
[13]
Hashimoto T, Shibasaki F. Hypoxia-inducible factor as an angiogenic master switch. Front Pediatr 2015; 3: 33.
[http://dx.doi.org/10.3389/fped.2015.00033] [PMID: 25964891]
[14]
Williams AL, Walton CB, MacCannell KA, Avelar A, Shohet RV. HIF-1 regulation of miR-29c impairs SERCA2 expression and cardiac contractility. Am J Physiol Heart Circ Physiol 2019; 316(3): H554-65.
[http://dx.doi.org/10.1152/ajpheart.00617.2018] [PMID: 30575439]
[15]
Kierans SJ, Taylor CT. Regulation of glycolysis by the hypoxia-inducible factor (HIF): Implications for cellular physiology. J Physiol 2021; 599(1): 23-37.
[http://dx.doi.org/10.1113/JP280572] [PMID: 33006160]
[16]
Rane S, He M, Sayed D, et al. Downregulation of miR-199a derepresses hypoxia-inducible factor-1α and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 2009; 104(7): 879-86.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.193102] [PMID: 19265035]
[17]
Tekin D, Dursun AD, Xi L. Hypoxia inducible factor 1 (HIF-1) and cardioprotection. Acta Pharmacol Sin 2010; 31(9): 1085-94.
[http://dx.doi.org/10.1038/aps.2010.132] [PMID: 20711226]
[18]
Abkhooie L, Sarabi MM, Kahroba H, et al. Potential roles of MyomiRs in cardiac development and related diseases. Curr Cardiol Rev 2021; 17(4): e010621188335.
[http://dx.doi.org/10.2174/1573403X16999201124201021] [PMID: 33238844]
[19]
Chen Z, Lai TC, Jan YH, et al. Hypoxia-responsive miRNAs target argonaute 1 to promote angiogenesis. J Clin Invest 2013; 123(3): 1057-67.
[http://dx.doi.org/10.1172/JCI65344] [PMID: 23426184]
[20]
Akhtar S, Hartmann P, Karshovska E, et al. Endothelial hypoxia-inducible factor-1α promotes atherosclerosis and monocyte recruitment by upregulating microRNA-19a. Hypertension 2015; 66(6): 1220-6.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.115.05886] [PMID: 26483345]
[21]
Lemus-Varela ML, Flores-Soto ME, Cervantes-Munguía R, et al. Expression of HIF-1α VEGF and EPO in peripheral blood from patients with two cardiac abnormalities associated with hypoxia. Clin Biochem 2010; 43(3): 234-9.
[http://dx.doi.org/10.1016/j.clinbiochem.2009.09.022] [PMID: 19804771]
[22]
Zeng Y, Liu H, Kang K, et al. Hypoxia inducible factor-1 mediates expression of miR-322: Potential role in proliferation and migration of pulmonary arterial smooth muscle cells. Sci Rep 2015; 5(1): 12098.
[http://dx.doi.org/10.1038/srep12098] [PMID: 26166214]
[23]
Chen T, Zhou Q, Tang H, et al. miR-17/20 Controls Prolyl Hydroxylase 2 (PHD2)/Hypoxia-Inducible Factor 1 (HIF1) to regulate pulmonary artery smooth muscle cell proliferation. J Am Heart Assoc 2016; 5(12): e004510.
[http://dx.doi.org/10.1161/JAHA.116.004510] [PMID: 27919930]
[24]
Chen C, Ponnusamy M, Liu C, Gao J, Wang K, Li P. MicroRNA as a therapeutic target in cardiac remodeling. BioMed Res Int 2017; 1278436.
[http://dx.doi.org/10.1155/2017/1278436]
[25]
Serocki M, Bartoszewska S, Janaszak-Jasiecka A, Ochocka RJ, Collawn JF, Bartoszewski R. miRNAs regulate the HIF switch during hypoxia: A novel therapeutic target. Angiogenesis 2018; 21(2): 183-202.
[http://dx.doi.org/10.1007/s10456-018-9600-2] [PMID: 29383635]
[26]
Greco S, Fasanaro P, Castelvecchio S, et al. MicroRNA dysregulation in diabetic ischemic heart failure patients. Diabetes 2012; 61(6): 1633-41.
[http://dx.doi.org/10.2337/db11-0952] [PMID: 22427379]
[27]
You D, Qiao Q, Ono K, et al. miR-223-3p inhibits the progression of atherosclerosis via down-regulating the activation of MEK1/ERK1/2 in macrophages. Aging 2022; 14(4): 1865-78.
[http://dx.doi.org/10.18632/aging.203908] [PMID: 35202001]
[28]
Wang H, Sugimoto K, Lu H, et al. HDAC1-mediated deacetylation of HIF1α prevents atherosclerosis progression by promoting miR-224-3p-mediated inhibition of FOSL2. Mol Ther Nucleic Acids 2021; 23: 577-91.
[http://dx.doi.org/10.1016/j.omtn.2020.10.044] [PMID: 33510945]
[29]
Solly EL, Dimasi CG, Bursill CA, Psaltis PJ, Tan JTM. MicroRNAs as therapeutic targets and clinical biomarkers in atherosclerosis. J Clin Med 2019; 8(12): 2199.
[http://dx.doi.org/10.3390/jcm8122199] [PMID: 31847094]
[30]
Lu Y, Thavarajah T, Gu W, Cai J, Xu Q. Impact of miRNA in atherosclerosis. Arterioscler Thromb Vasc Biol 2018; 38(9): e159-70.
[http://dx.doi.org/10.1161/ATVBAHA.118.310227] [PMID: 30354259]
[31]
Bartoszewska S, Rochan K, Piotrowski A, et al. The hypoxia-inducible miR-429 regulates hypoxia-inducible factor-1α expression in human endothelial cells through a negative feedback loop. FASEB J 2015; 29(4): 1467-79.
[http://dx.doi.org/10.1096/fj.14-267054] [PMID: 25550463]
[32]
John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol 2004; 2(11): e363.
[http://dx.doi.org/10.1371/journal.pbio.0020363] [PMID: 15502875]
[33]
Krek A, Grün D, Poy MN, et al. Combinatorial microRNA target predictions. Nat Genet 2005; 37(5): 495-500.
[http://dx.doi.org/10.1038/ng1536] [PMID: 15806104]
[34]
Pullamsetti SS, Mamazhakypov A, Weissmann N, Seeger W, Savai R. Hypoxia-inducible factor signaling in pulmonary hypertension. J Clin Invest 2020; 130(11): 5638-51.
[http://dx.doi.org/10.1172/JCI137558] [PMID: 32881714]
[35]
Tang H, Babicheva A, McDermott KM, et al. Endothelial HIF-2α contributes to severe pulmonary hypertension due to endothelial-to-mesenchymal transition. Am J Physiol Lung Cell Mol Physiol 2018; 314(2): L256-75.
[PMID: 29074488]
[36]
Gorospe M, Tominaga K, Wu X, Fähling M, Ivan M. Post-transcriptional control of the hypoxic response by RNA-binding proteins and microRNAs. Front Mol Neurosci 2011; 4: 7.
[http://dx.doi.org/10.3389/fnmol.2011.00007] [PMID: 21747757]
[37]
Nie X, Fan J, Li H, et al. miR-217 promotes cardiac hypertrophy and dysfunction by targeting PTEN. Mol Ther Nucleic Acids 2018; 12: 254-66.
[http://dx.doi.org/10.1016/j.omtn.2018.05.013] [PMID: 30195764]
[38]
Saheera S, Krishnamurthy P. Cardiovascular changes associated with hypertensive heart disease and aging. Cell Trans Plant 2020 Apr 21; 29: 963689720920830.
[http://dx.doi.org/10.1177/0963689720920830] [PMID: 32393064]
[39]
Pérez-Cremades D, Chen J, Assa C, Feinberg MW. MicroRNA-mediated control of myocardial infarction in diabetes. Trends Cardiovas Med 2022. Online ahead of print
[http://dx.doi.org/10.1016/j.tcm.2022.01.004] [PMID: 35051592]
[40]
Tatsuguchi M, Seok HY, Callis TE, et al. Expression of microRNAs is dynamically regulated during cardiomyocyte hypertrophy. J Mol Cell Cardiol 2007; 42(6): 1137-41.
[http://dx.doi.org/10.1016/j.yjmcc.2007.04.004] [PMID: 17498736]
[41]
Abkhooie L, Sarabi M, Kahroba H, et al. Cyclin-dependent Kinase 9 induces regional and global genomic DNA methylation via influencing DNMT gene expression in mouse myoblast C2C12 cells during differentiation. Crescent J Med Biol Sci 2021; 9(1): 24-32.
[http://dx.doi.org/10.34172/cjmb.2022.05]
[42]
Fathi M, Gharakhanlou R, Rezaei R. The changes of heart miR-1 and miR-133 expressions following physiological hypertrophy due to endurance training. Cell J 2020; 22 (Suppl. 1): 133-40.
[PMID: 32779443]
[43]
Wehbe N, Nasser S, Pintus G, Badran A, Eid A, Baydoun E. MicroRNAs in cardiac hypertrophy. Int J Mol Sci 2019; 20(19): 4714.
[http://dx.doi.org/10.3390/ijms20194714] [PMID: 31547607]
[44]
Chen J, Gong X, Huang L, et al. MiR-199a-5p regulates sirtuin1 and PI3K in the rat hippocampus with intrauterine growth restriction. Sci Rep 2018; 8(1): 13813.
[http://dx.doi.org/10.1038/s41598-018-32189-5] [PMID: 30217997]
[45]
Asensio-Lopez MC, Sassi Y, Soler F, Fernandez del Palacio MJ, Pascual-Figal D, Lax A. The miRNA199a/SIRT1/P300/Yy1/sST2 signaling axis regulates adverse cardiac remodeling following MI. Sci Rep 2021; 11(1): 3915.
[http://dx.doi.org/10.1038/s41598-021-82745-9] [PMID: 33594087]
[46]
Rawal S, Manning P, Katare R. Cardiovascular microRNAs: As modulators and diagnostic biomarkers of diabetic heart disease. Cardiovasc Diabetol 2014; 13(1): 44.
[http://dx.doi.org/10.1186/1475-2840-13-44] [PMID: 24528626]
[47]
Guo R, Nair S. Role of microRNA in diabetic cardiomyopathy: From mechanism to intervention Biochimica et biophysica acta (BBA)-molecular basis of disease 2017; 1863(8): 2070-7.
[http://dx.doi.org/10.1016/j.bbadis.2017.03.013]
[48]
Zhou Q, Lv D, Chen P, et al. MicroRNAs in diabetic cardiomyopathy and clinical perspectives. Frontiers Media: SA 2014; p. 185.
[49]
Heather LC, Clarke K. Metabolism, hypoxia and the diabetic heart. J Mol Cell Cardiol 2011; 50(4): 598-605.
[http://dx.doi.org/10.1016/j.yjmcc.2011.01.007] [PMID: 21262230]
[50]
Le Brigand K, Robbe-Sermesant K, Mari B, Barbry P. MiRonTop: Mining microRNAs targets across large scale gene expression studies. Bioinformatics 2010; 26(24): 3131-2.
[http://dx.doi.org/10.1093/bioinformatics/btq589] [PMID: 20959382]
[51]
Cerychova R, Pavlinkova G. HIF-1, metabolism, and diabetes in the embryonic and adult heart. Front Endocrinol 2018; 9: 460.
[http://dx.doi.org/10.3389/fendo.2018.00460] [PMID: 30158902]
[52]
de Gonzalo-Calvo D, van der Meer RW, Rijzewijk LJ, et al. Serum microRNA-1 and microRNA-133a levels reflect myocardial steatosis in uncomplicated type 2 diabetes. Sci Rep 2017; 7(1): 47.
[http://dx.doi.org/10.1038/s41598-017-00070-6] [PMID: 28246388]
[53]
Al-kafaji G, Al-Muhtaresh H, Salem A. Expression and clinical significance of miR 1 and miR-133 in pre diabetes. Biomed Rep 2021; 14(3): 33.
[http://dx.doi.org/10.3892/br.2021.1409] [PMID: 33585035]
[54]
Liu M, Galli G, Wang Y, et al. Novel therapeutic targets for hypoxia-related cardiovascular diseases: The role of HIF-1. Front Physiol 2020; 11: 774.
[http://dx.doi.org/10.3389/fphys.2020.00774] [PMID: 32760290]
[55]
Howell NJ, Tennant DA. The role of HIFs in ischemia-reperfusion injury. Hypoxia 2014; 2: 107-15.
[PMID: 27774470]
[56]
Martin-Puig S, Tello D, Aragonés J. Novel perspectives on the PHD-HIF oxygen sensing pathway in cardioprotection mediated by IPC and RIPC. Front Physiol 2015; 6: 137.
[http://dx.doi.org/10.3389/fphys.2015.00137] [PMID: 26042040]
[57]
Jain T, Nikolopoulou EA, Xu Q, Qu A. Hypoxia inducible factor as a therapeutic target for atherosclerosis. Pharmacol Ther 2018; 183: 22-33.
[http://dx.doi.org/10.1016/j.pharmthera.2017.09.003] [PMID: 28942242]
[58]
Ham PB III, Raju R. Mitochondrial function in hypoxic ischemic injury and influence of aging. Prog Neurobiol 2017; 157: 92-116.
[http://dx.doi.org/10.1016/j.pneurobio.2016.06.006] [PMID: 27321753]
[59]
Ahmad A, Ahmad S, Malcolm KC, et al. Differential regulation of pulmonary vascular cell growth by hypoxia-inducible transcription factor-1α and hypoxia-inducible transcription factor-2α. Am J Respir Cell Mol Biol 2013; 49(1): 78-85.
[http://dx.doi.org/10.1165/rcmb.2012-0107OC] [PMID: 23492195]
[60]
Dai Z, Zhu MM, Peng Y, et al. Therapeutic targeting of vascular remodeling and right heart failure in pulmonary arterial hypertension with a HIF-2α inhibitor. Am J Respir Crit Care Med 2018; 198(11): 1423-34.
[http://dx.doi.org/10.1164/rccm.201710-2079OC] [PMID: 29924941]

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