2,941
Views
9
CrossRef citations to date
0
Altmetric
Research Paper

Thrombosis-related circulating miR-16-5p is associated with disease severity in patients hospitalised for COVID-19

ORCID Icon, , , , , , , , , & show all
Pages 963-979 | Received 15 Feb 2022, Accepted 06 Jul 2022, Published online: 07 Aug 2022

References

  • Wicik Z, Eyileten C, Jakubik D, et al. ACE2 interaction networks in COVID-19: a physiological framework for prediction of outcome in patients with cardiovascular risk factors. J Clin Med Res. 2020;9. DOI:10.3390/jcm9113743.
  • Aziz F, Aberer F, Bräuer A, et al. COVID-19 in-hospital mortality in people with diabetes is driven by comorbidities and age—propensity score-matched analysis of Austrian national public health institute data. Viruses. 2021;13(12):2401.
  • Gupta A, Madhavan MV, Sehgal K, et al. Extrapulmonary manifestations of COVID-19. Nat Med. 2020;26(7):1017–1032.
  • Gu SX, Tyagi T, Jain K, et al. Thrombocytopathy and endotheliopathy: crucial contributors to COVID-19 thromboinflammation. Nat Rev Cardiol. 2021;18(3):194–209.
  • Jackson SP, Darbousset R, Schoenwaelder SM. Thromboinflammation: challenges of therapeutically targeting coagulation and other host defense mechanisms. Blood. 2019;133(9):906–918.
  • Bikdeli B, Madhavan MV, Gupta A, et al. Pharmacological agents targeting thromboinflammation in COVID-19: Review and implications for future research. Thromb Haemost. 2020;120(7):1004–1024.
  • McGonagle D, O’Donnell JS, Sharif K, et al. Immune mechanisms of pulmonary intravascular coagulopathy in COVID-19 pneumonia. Lancet Rheumatol. 2020;2(7):e437–e445. 30121-1.
  • Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med. 2020;383(2):120–128.
  • Gómez CA, Sun C-K, Tsai I-T, et al. Mortality and risk factors associated with pulmonary embolism in coronavirus disease 2019 patients: a systematic review and meta-analysis. Sci Rep. 2021;11(1):16025.
  • Bonaventura A, Vecchié A, Dagna L, et al. Endothelial dysfunction and immunothrombosis as key pathogenic mechanisms in COVID-19. Nat Rev Immunol. 2021;21(5):319–329.
  • Thachil J, Tang N, Gando S, et al. ISTH interim guidance on recognition and management of coagulopathy in COVID-19. J Thromb Haemost. 2020;18(5):1023–1026.
  • Bikdeli B, Madhavan MV, Jimenez D, et al. COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up: JACC State-of-the-art review. J Am Coll Cardiol. 2020;75(23):2950–2973.
  • Agyemang C, van den Born B-J, Gorog DA, Storey RF, Gurbel PA, Tantry US, Berger JS, Chan MY, et al. Current and novel biomarkers of thrombotic risk in COVID-19: a consensus statement from the international COVID-19 thrombosis biomarkers colloquium. Nat Rev Cardiol. 2022;19(1):1–21.
  • Friedman RC, Farh KK-H, Burge CB, et al. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009;19(1):92–105.
  • Pordzik J, Jakubik D, Jarosz-Popek J, et al. Significance of circulating microRNAs in diabetes mellitus type 2 and platelet reactivity: bioinformatic analysis and review. Cardiovasc Diabetol. 2019;18(1):113.
  • Wang Y, Liu C, Wei W, et al. Predictive value of circulating coagulation related microRNAs expressions for major adverse cardiac and cerebral event risk in patients undergoing continuous ambulatory peritoneal dialysis: a cohort study. J Nephrol. 2020;33(1):157–165.
  • Eyileten C, Wicik Z, De Rosa S, et al. MicroRNAs as diagnostic and prognostic biomarkers in ischemic stroke-A comprehensive review and bioinformatic analysis. Cells. 2018;7. DOI:10.3390/cells7120249.
  • Pordzik J, Pisarz K, De Rosa S, et al. The potential role of platelet-related microRNAs in the development of cardiovascular events in high-risk populations, including diabetic patients: a review. Front Endocrinol. 2018;9:74.
  • Sabatino J, Wicik Z, De Rosa S, et al. MicroRNAs fingerprint of bicuspid aortic valve. J Mol Cell Cardiol. 2019;134:98–106.
  • Eyileten C, Sharif L, Wicik Z, et al. The relation of the brain-derived neurotrophic factor with microRNAs in neurodegenerative diseases and ischemic stroke. Mol Neurobiol. 2021;58(1):329–347.
  • Wolska M, Jarosz-Popek J, Junger E, et al. Long non-coding RNAs as promising therapeutic approach in ischemic stroke: a comprehensive review. Mol Neurobiol. 2020;58(4):1664–1682.
  • Soplinska A, Zareba L, Wicik Z, et al. MicroRNAs as biomarkers of systemic changes in response to endurance exercise-A comprehensive review. Diagnostics (Basel). 2020;10. DOI:10.3390/diagnostics10100813.
  • Zareba L, Fitas A, Wolska M, et al. MicroRNAs and long noncoding RNAs in coronary artery disease: new and potential therapeutic targets. Cardiol Clin. 2020;38(4):601–617.
  • Gasecka A, Siwik D, Gajewska M, et al. Early biomarkers of neurodegenerative and neurovascular disorders in diabetes. J Clin Med Res. 2020;9. DOI:10.3390/jcm9092807.
  • Jarosz-Popek J, Wolska M, Gasecka A, et al. The importance of non-coding RNAs in neurodegenerative processes of diabetes-related molecular pathways. J Clin Med Res. 2020;10. DOI:10.3390/jcm10010009.
  • Morelli VM, Brækkan SK, Hansen J-B. Role of microRNAs in venous thromboembolism. Int J Mol Sci. 2020;21. DOI:10.3390/ijms21072602
  • Kim AS, Kalady MF, DeVecchio J, et al. Identifying miRNA biomarkers and predicted targets associated with venous thromboembolism in colorectal cancer patients. Blood. 2019;134(Supplement_1):3643.
  • Xiao J, Jing Z-C, Ellinor PT, et al. MicroRNA-134 as a potential plasma biomarker for the diagnosis of acute pulmonary embolism. J Transl Med. 2011;9(1). DOI:10.1186/1479-5876-9-159
  • Kessler T, Erdmann J, Vilne B, et al. Serum microRNA-1233 is a specific biomarker for diagnosing acute pulmonary embolism. J Transl Med. 2016;14(1). DOI:10.1186/s12967-016-0886-9
  • Zhou X, Wen W, Shan X, et al. MiR-28-3p as a potential plasma marker in diagnosis of pulmonary embolism. Thromb Res. 2016;138:91–95.
  • Qin J, Liang H, Shi D, et al. A panel of microRNAs as a new biomarkers for the detection of deep vein thrombosis. J Thromb Thrombolysis. 2015;39(2):215–221.
  • Ronco C, Bellomo R, and Kellum JA, et al. Critical care nephrology e-book. Elsevier health sciences; 2017 [cited 2022 July 18]. Available from: https://play.google.com/store/books/details?id=HTdDDwAAQBAJ
  • Jiang Z, Ma J, Wang Q, et al. Combination of circulating miRNA-320a/b and D-dimer improves diagnostic accuracy in deep vein thrombosis patients. Med Sci Monit. 2018;24:2031–2037.
  • Brown JAL, Bourke E. Practical bioinformatics analysis of MiRNA data using online tools. Methods Mol Biol. 2017;1509:195–208.
  • A-L B, Gulbahce N, Loscalzo J. Network medicine: a network-based approach to human disease. Nat Rev Genet. 2011;12(1):56–68.
  • Simões SN, Martins DC, Pereira CAB, et al. NERI: network-medicine based integrative approach for disease gene prioritization by relative importance. BMC Bioinformatics. 2015;16(S19):1–14.
  • Chang X, Xu T, Li Y, et al. Dynamic modular architecture of protein-protein interaction networks beyond the dichotomy of “date” and “party” hubs. Sci Rep. 2013;3(1):1–8.
  • Agarwal S, Deane CM, Porter MA, Agarwal S, Deane CM, Porter MA, Jones NS. Revisiting Date and. Party hubs: novel approaches to role assignment in protein interaction networks. PLoS Comput Biol. 2010;6(6):e1000817.
  • Schulte C, Barwari T, Joshi A, et al. Comparative analysis of circulating noncoding RNAs versus protein biomarkers in the detection of myocardial injury. Circ Res. 2019;125(3):328–340.
  • Eyileten C, Jakubik D, Shahzadi A, et al. Diagnostic performance of circulating miRNAs and extracellular vesicles in acute ischemic stroke. Int J Mol Sci. 2022;23. DOI:10.3390/ijms23094530.
  • Messner CB, Demichev V, Wendisch D, et al. Ultra-high-throughput clinical proteomics reveals classifiers of COVID-19 infection. Cell Syst. 2020;11(1):11–24.e4.
  • Gutmann C, Takov K, Burnap SA, et al. SARS-CoV-2 RNAemia and proteomic trajectories inform prognostication in COVID-19 patients admitted to intensive care. Nat Commun. 2021;12(1):3406.
  • de Gonzalo-Calvo D, Benítez ID, Pinilla L, Gonzalo-Calvo D de, Benítez ID, Pinilla L, Carratalá A, Moncusí-Moix A, Gort-Paniello C, et al. Circulating microRNA profiles predict the severity of COVID-19. in hospitalized patients. Transl Res. 2021;236:147–159.
  • Badimon L, Robinson EL, Jusic A, et al. Cardiovascular RNA markers and artificial intelligence may improve COVID-19 outcome: a position paper from the EU-CardioRNA COST Action CA17129. Cardiovasc Res. 2021;117(8):1823–1840.
  • Gutmann C, Khamina K, Theofilatos K, et al. Association of cardiometabolic microRNAs with COVID-19 severity and mortality. Cardiovasc Res. 2022;118(2):461–474.
  • Palasca O, Santos A, Stolte C, et al. 2.0: an integrative web resource on mammalian tissue expression. Database. 2018;2018. DOI:10.1093/database/bay003.
  • Shannon P, Markiel A, Ozier O, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–2504.
  • Doncheva NT, Morris JH, Gorodkin J, et al. Cytoscape stringApp: network analysis and visualization of proteomics data. J Proteome Res. 2019;18(2):623–632.
  • Reghunathan R, Jayapal M, Hsu L-Y, Chng H-H, Tai D, Leung BP, et al. BMC Immunology. p. 2. 2005. DOI:10.1186/1471-2172-6-2
  • Sharma A, Garcia G, Wang Y, Plummer J T, Morizono K, Arumugaswami V, Svendsen C N. (2020). Human iPSC-Derived Cardiomyocytes Are Susceptible to SARS-CoV-2 Infection. Cell Rep Med, 1(4), 100052 10.1016/j.xcrm.2020.100052
  • Desai N et al . (2020). Temporal and spatial heterogeneity of host response to SARS-CoV-2 pulmonary infection. Nat Commun, 11(1), 6319 10.1038/s41467-020-20139-7
  • Wicik Z, Jales Neto LH, Guzman LEF, et al. The crosstalk between bone metabolism, lncRNAs, microRNAs and mRNAs in coronary artery calcification. Genomics. 2021;113(1):503–513.
  • Ru Y, Kechris KJ, Tabakoff B, et al. The multiMiR R package and database: integration of microRNA–target interactions along with their disease and drug associations. Nucleic Acids Res. 2014;42(17):e133.
  • Chen E Y, Tan C M, Kou Y, Duan Q, Wang Z, Meirelles G Vaz, Clark N R, Ma'ayan A. (2013). Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics, 14 128 10.1186/1471-2105-14-128
  • wma) WMA, World Medical Association (WMA). Declaration of Helsinki. Ethical Principles for Medical Research Involving Human Subjects. Jahrbuch für Wissenschaft und Ethik. pp. 233–238. 2009. DOI:10.1515/9783110208856.233
  • De Rosa S, Eposito F, Carella C, et al. Transcoronary concentration gradients of circulating microRNAs in heart failure. Eur J Heart Fail. 2018;20(6):1000–1010.
  • De Rosa R, De Rosa S, Leistner D, et al. Transcoronary concentration gradient of microRNA-133a and outcome in patients with coronary artery disease. Am J Cardiol. 2017;120(1):15–24.
  • Eyileten C, Fitas A, Jakubik D, et al. Alterations in circulating MicroRNAs and the relation of MicroRNAs to maximal oxygen consumption and intima–media thickness in ultra-marathon runners. Int J Environ Res Public Health. 2021;18(14):7234.
  • Pordzik J, Eyileten-Postuła C, Jakubik D, et al. MiR-126 is an independent predictor of long-term all-cause mortality in patients with type 2 diabetes mellitus. J Clin Med Res. 2021;10. DOI:10.3390/jcm10112371.
  • Eyileten C, Wicik Z, Keshwani D, et al. Alteration of circulating platelet-related and diabetes-related microRNAs in individuals with type 2 diabetes mellitus: a stepwise hypoglycaemic clamp study. Cardiovasc Diabetol. 2022;21(1):79.
  • Jafarinejad-Farsangi S, Jazi MM, Rostamzadeh F, et al. High affinity of host human microRNAs to SARS-CoV-2 genome: an in silico analysis. Noncoding RNA Res. 2020;5(4):222–231.
  • Ahmadi A, Moradi S. In silico analysis suggests the RNAi-enhancing antibiotic enoxacin as a potential inhibitor of SARS-CoV-2 infection. Sci Rep. 2021;11(1):10271.
  • Hamdy NM, El-Wakeel L, Suwailem SM. Involvement of depressive catecholamines as thrombosis risk/inflammatory markers in non-smoker, non-obese congestive heart failure, linked to increased epidermal growth factor-receptor (EGF-R) production. Indian J Clin Biochem. 2011;26(2):140–145.
  • Mitchell HD, Eisfeld AJ, Stratton KG, et al. The role of EGFR in influenza pathogenicity: multiple network-based approaches to identify a key regulator of non-lethal infections. Front Cell Dev Biol. 2019;7:200.
  • Venkataraman T, Coleman CM, Frieman MB. Overactive epidermal growth factor receptor signaling leads to increased fibrosis after severe acute respiratory syndrome coronavirus infection. J Virol. 2017;91(12). DOI:10.1128/jvi.00182-17
  • Wicik Z, Czajka P, Eyileten C, et al. The role of miRNAs in regulation of platelet activity and related diseases - a bioinformatic analysis. Platelets. 2022 [citied 2022 Jun 11];1–13. DOI:10.1080/09537104.2022.2042233
  • Inyushin M, Zayas-Santiago A, Rojas L, et al. Platelet-generated amyloid beta peptides in Alzheimer’s disease and glaucoma. Histol Histopathol. 2019;34(8):843–856.
  • Zamolodchikov D, Renné T, The Alzheimer’s SS. disease peptide β-amyloid promotes thrombin generation through activation of coagulation factor XII. J Thromb Haemost. 2016;14(5):995–1007.
  • Kam T-I, Song S, Gwon Y, et al. FcγRIIb mediates amyloid-β neurotoxicity and memory impairment in Alzheimer’s disease. J Clin Invest. 2013;123(7):2791–2802.
  • Ahn HJ, Chen Z-L, Zamolodchikov D, et al. Interactions of β-amyloid peptide with fibrinogen and coagulation factor XII may contribute to Alzheimer’s disease. Curr Opin Hematol. 2017;24(5):427–431.
  • Zuehlke AD, Beebe K, Neckers L, et al. Regulation and function of the human HSP90AA1 gene. Gene. 2015;570(1):8–16.
  • Wyler E, Mösbauer K, Franke V, et al. Transcriptomic profiling of SARS-CoV-2 infected human cell lines identifies HSP90 as target for COVID-19 therapy. iScience. 2021;24(3):102151.
  • Ramos CHI, Ayinde KS. Are Hsp90 inhibitors good candidates against Covid-19? Curr Protein Pept Sci. 2020. cited 2022 Jun 11. DOI:10.2174/1389203721666201111160925.
  • Li C, Chu H, Liu X, et al. Human coronavirus dependency on host heat shock protein 90 reveals an antiviral target. Emerg Microbes Infect. 2020;9(1):2663–2672.
  • Goswami R, Russell VS, and Tu JJ, et al. Oral Hsp90 inhibitor, SNX-5422, attenuates SARS-CoV-2 replication and dampens inflammation in airway cells. iScience. 24(12) 103412. DOI:10.1016/j.isci.2021.103412.
  • Lan C, Shi X, Guo N, et al. [Value of serum miR-155-5p and miR-133a-3p expression for the diagnosis and prognosis evaluation of sepsis]. Zhonghua Wei Zhong Bing Ji Jiu Yi Xue. 2016;28(8):694–698.
  • Hori K, Shimaoka K, Hoshino M, Aloufi N, Haidar Z, Ding J, Nair P, Benedetti A, Eidelman DH, et al. Role of human antigen r (hur) in the regulation of pulmonary ACE2 expression. Cells. 2021;11(1):11.
  • Chattopadhyay S, Basak T, Nayak MK, et al. Identification of cellular calcium binding protein calmodulin as a regulator of rotavirus A infection during comparative proteomic study. PLoS One. 2013;8(2):e56655.
  • Gardiner EE, Arthur JF, Berndt MC, et al. Role of calmodulin in platelet receptor function. Curr Med Chem Cardiovasc Hematol Agents. 2005;3(4):283–287.
  • Tousoulis D, Kampoli A-M, Tentolouris C, et al. The role of nitric oxide on endothelial function. Curr Vasc Pharmacol. 2012;10(1):4–18.
  • Lambert DW, Clarke NE, Hooper NM, et al. Calmodulin interacts with angiotensin-converting enzyme-2 (ACE2) and inhibits shedding of its ectodomain. FEBS Lett. 2008;582(2):385–390.
  • Perrin-Cocon L, Diaz O, Jacquemin C, et al. The current landscape of coronavirus-host protein–protein interactions. J Transl Med. 2020;18(1):1–15.
  • Wang M, Li J, Cai J, et al. Overexpression of MicroRNA-16 alleviates atherosclerosis by inhibition of inflammatory pathways. Biomed Res Int. 2020;2020:8504238.
  • Yang Y, Yang F, Yu X, et al. miR-16 inhibits NLRP3 inflammasome activation by directly targeting TLR4 in acute lung injury. Biomed Pharmacother. 2019;112:108664.
  • Möhnle P, Hirschberger S, Hinske LC, et al. MicroRNAs 143 and 150 in whole blood enable detection of T-cell immunoparalysis in sepsis. Mol Med. 2018;24(1):54.
  • Jaguszewski M, Osipova J, Ghadri J-R, et al. A signature of circulating microRNAs differentiates takotsubo cardiomyopathy from acute myocardial infarction. Eur Heart J. 2014;35(15):999–1006.
  • Yang J, Yang X-S, Fan S-W, et al. Prognostic value of microRNAs in heart failure: a meta-analysis. Medicine (Baltimore). 2021;100(46):e27744.
  • Telkoparan-Akillilar P, Cevik D. Identification of miR-17, miR-21, miR-27a, miR-106b and miR-222 as endoplasmic reticulum stress-related potential biomarkers in circulation of patients with atherosclerosis. Mol Biol Rep. 2021;48(4):3503–3513.
  • Kim WR, Park EG, Kang K-W, et al. Expression analyses of MicroRNAs in hamster lung tissues infected by SARS-CoV-2. Mol Cells. 2020;43(11):953–963.
  • Zheng C, Zheng Z, Sun J, et al. MiR-16-5p mediates a positive feedback loop in EV71-induced apoptosis and suppresses virus replication. Sci Rep. 2017. DOI:10.1038/s41598-017-16616-7.
  • Farr RJ, Rootes CL, Rowntree LC, et al. Altered microRNA expression in COVID-19 patients enables identification of SARS-CoV-2 infection. PLoS Pathog. 2021;17(7):e1009759.
  • Chow JT-S, Prediction SL. Analysis of SARS-CoV-2-targeting MicroRNA in human lung epithelium. Genes (Basel). 2020;11. DOI:10.3390/genes11091002
  • Li C, Hu X, Li L, et al. Differential microRNA expression in the peripheral blood from human patients with COVID-19. J Clin Lab Anal. 2020;34(10):e23590.
  • Wang Z, Ruan Z, Mao Y, et al. miR-27a is up regulated and promotes inflammatory response in sepsis. Cell Immunol. 2014;290(2):190–195.
  • Chauhan N, Jaggi M, Chauhan SC, et al. COVID-19: fighting the invisible enemy with microRNAs. Expert Rev Anti Infect Ther. 2021;19(2):137–145.
  • Chen B, Han J, Chen S, et al. MicroLet-7b regulates neutrophil function and dampens neutrophilic inflammation by suppressing the canonical TLR4/NF-κB pathway. Front Immunol. 2021;12:653344.
  • Xie C, Chen Y, Luo D, et al. Therapeutic potential of C1632 by inhibition of SARS-CoV-2 replication and viral-induced inflammation through upregulating let-7. Signal Transduct Target Ther. 2021;6(1):84.
  • Katze MG, He Y, Jr GM. Viruses and interferon: a fight for supremacy. Nat Rev Immunol. 2002;2(9):675–687.
  • Mitash N, Donovan E, Swiatecka-Urban A J. The role of MicroRNA in the airway surface liquid homeostasis. Int J Mol Sci. 2020 21;21(11):3848.
  • Gracias DT, Stelekati E, Hope JL, et al. The microRNA miR-155 controls CD8(+) T cell responses by regulating interferon signaling. Nat Immunol. 2013;14(6):593–602.
  • Garg A, Seeliger B, Derda AA, et al. Circulating cardiovascular microRNAs in critically ill COVID −19 patients. Eur J Heart Fail. 2021;23(3):468–475.
  • Donyavi T, Bokharaei-Salim F, Baghi HB, et al. Acute and post-acute phase of COVID-19: analyzing expression patterns of miRNA-29a-3p, 146a-3p, 155-5p, and let-7b-3p in PBMC. Int Immunopharmacol. 2021;97:107641.
  • Tacke F, Spehlmann ME, Vucur M, et al. miR-155 predicts long-term mortality in critically Ill patients younger than 65 years. Mediators Inflamm. 2019;2019:6714080.