Therapeutic implication of MicroRNA-320a antagonist in attenuating blood clots formed during venous thrombosis

ISTH Steering Committee for World Thrombosis Day (2014) Thrombosis: a major contributor to the global disease burden. J Thromb Haemost 12(10):1580–1590. https://doi.org/10.1111/jth.12698 Naess IA, Christiansen SC, Romundstad P, Cannegieter SC, Rosendaal FR, Hammerstrøm J (2007) Incidence and mortality of venous thrombosis: a population-based study. J Thromb Haemost 5(4):692–699. https://doi.org/10.1111/j.1538-7836.2007.02450.x Schulman S, Lindmarker P, Holmström M, Lärfars G, Carlsson A, Nicol P, Svensson E, Ljungberg B, Viering S, Nordlander S, Leijd B, Jahed K, Hjorth M, Linder O, Beckman M (2006) Post-thrombotic syndrome, recurrence, and death 10 years after the first episode of venous thromboembolism treated with warfarin for 6 weeks or 6 months. J Thromb Haemost 4(4):734–742. https://doi.org/10.1111/j.1538-7836.2006.01795.x Diaz JA, Obi A, Myers DD, Wrobleski SK, Henke PK, Mackman N, Wakefield TW (2012) Critical review of mouse models of venous thrombosis. Arterioscler Thromb Vasc Biol 32:556–562 Heit JA, O’Fallon WM, Petterson TM, Lohse CM, Silverstein MD, Mohr DN, Melton LJ (2002) Relative impact of risk factors for deep vein thrombosis and pulmonary embolism: a population-based study. Arch Intern Med 162:1245–1248 Zwicker I et al (2009) Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res 15:6830–6840 Zhou X et al (2010) Incidence and risk factors of venous thromboembolic events in lymphoma. Am J Med 123:935–941 Demers C et al (1998) Incidence of venographically proved deep vein thrombosis after knee arthroscopy. Arch Intern Med 158:47–50 Chan MY, Andreotti F, Becker RC (2008) Hypercoagulable states in cardiovascular disease. Circulation 118:2286–2297 Anand AC, Jha SK, Saha A, Sharma V, Adya CM (2001) Thrombosis as a complication of extended stay at high altitude. Natl Med J India 14(4):197–201 Khalil KF, Saeed W (2010) Pulmonary embolism in soldiers serving at high altitude. J Coll Physicians Surg Pak 20:7 Kumar S (2006) High altitude induced deep venous thrombosis: a study of 28 cases. Indian J Surg 68:84–88 Rao KS (2006) Other medical illnesses aggravated by high altitude. In: Anand AC, Narula AS, Kakkar R, Kalra R (eds) Textbook of environmental emergencies. Department of Internal Medicine Armed Forces Medical College, Pune, pp 26–29 Singh I, Chohan IS (1972) Blood coagulation changes at high altitude predisposing to pulmonary hypertension. Br Heart J 34:611–617 Brill A, Fuchs TA, Chauhan AK et al (2011) von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood 117:1400–1407. https://doi.org/10.1182/blood-2010-05-287623 Mammen EF (1992) Pathogenesis of venous thrombosis. Chest. https://doi.org/10.1378/chest.102.6_supplement.640s Sevitt S (1974) The structure and growth of valve-pocket thrombi in femoral veins. J Clin Pathol 27:517–528. https://doi.org/10.1136/jcp.27.7.517 Brühl MLV, Stark K, Steinhart A et al (2012) Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 209:819–835. https://doi.org/10.1084/jem.20112322 Schönfelder T, Jäckel S, Wenzel P (2017) Mouse models of deep vein thrombosis. Gefasschirurgie 22:28–33. https://doi.org/10.1007/s00772-016-0227-6 Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297 Iwakawa HO, Tomari Y (2015) The functions of microRNAs: mRNA decay and translational repression. Trends Cell Biol 25(11):651–665 Zhu W, Qian J, Ma L, Ma P, Yang F, Shu Y (2017) MiR-346 suppresses cell proliferation through SMYD3 dependent approach in hepatocellular carcinoma. Oncotarget 8(39):65218–65229. https://doi.org/10.18632/oncotarget.18060 Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233 Armand-Labit V, Pradines A (2017) Circulating cell-free MicroRNAs as clinical cancer biomarkers. Biomol Concepts 8:61–81 Loosen SH, Schueller F, Trautwein C et al (2017) Role of circulating microRNAs in liver diseases. World J Hepatol 9:586–594 Rayner K, Dimmeler S, Calin GA et al (2014) Novel biomarkers for acute myocardial infarction: is microRNA the new kid on the block? ClinChem 60:812–817 Liu X, Cheng Y, Zhang S, Lin Y, Yang J, Zhang C (2009) A necessary role of miR-221 and miR-222 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res 104:476–487 Tan M, Yan HB, Li JN et al (2016) Thrombin stimulated platelet-derived exosomes inhibit platelet-derived growth factor receptor-beta expression vascular smooth muscle cells. Cell Physiol Biochem 38:2348–2365 Weber C, Schober A, Zernecke A (2010) Micrornas in arterial remodelling, inflammation and atherosclerosis. Curr Drug Targets 11:950–956 Hembrom AA, Srivastava S, Garg I, Kumar B (2020) MicroRNAs in venous thrombo-embolism. Clin Chim Acta 504:66–72. https://doi.org/10.1016/j.cca.2020.01.034 Hembrom AA, Ghosh N, Kumar V, Garg I, Ganju L, Srivastava S (2022) Panel of regulatory miRNAs for blood coagulation under normoxic and hypoxic conditions. Def Life Sci J 7(1):17–26 Srivastava S, Garg I, Kumari B, Rai C, Singh Y, Kumar V, Yanamandra U, Singh J, Bansal A, Kumar B (2019) Diagnostic potential of circulating micro RNA hsa-miR-320 in patients of high altitude induced deep vein thrombosis: an Indian study. Gene Rep. 17:100550 Srivastava S, Garg I, Kumar B (2019) An In-Silico argument for Micro-RNAs showing pivotal role in susceptibility towards high altitude induced venous thrombo-embolism (HA-VTE). Int J Gen Sci 6(1):1–11 Sahu A, Jha PK, Prabhakar A, Singh HD, Gupta N, Chatterjee T, Tyagi T, Sharma S, Kumari B, Singh S, Nair V, Goel S, Ashraf MZ (2017) MicroRNA-145 impedes thrombus formation via targeting tissue factor in venous thrombosis. EBioMedicine 26:175–186 Sahu A, Jha PK, Prabhakar A, Singh HD, Gupta N, Chatterjee T, Tyagi T, Sharma S, Kumari B, Singh S et al (2017) MicroRNA-145 impedes thrombus formation via targeting tissue factor in venous thrombosis. EBioMedicine 26:175–186 Tyagi T, Ahmad S, Gupta N, Sahu A, Ahmad Y, Nair V, Chatterjee T, Bajaj N, Sengupta S, Ganju L, Singh SB, Ashraf MZ (2013) Altered expression of platelet proteins and calpain activity mediate hypoxia-induced prothrombotic phenotype. Blood. https://doi.org/10.1182/blood-2013-05-501924 Gupta N, Sahu A, Prabhakar A, Chatterjee T, Tyagi T, Kumari B, Khan N, Nair V, Bajaj N, Sharma M, Ashraf MZ (2017) Activation of NLRP3 inflammasome complex potentiates venous thrombosis in response to hypoxia. Proc Natl Acad Sci U S A 114(18):4763–4768. https://doi.org/10.1073/pnas.1620458114 Wang W, Zhu X, Du X, Xu A, Yuan X, Zhan Y, Liu M, Wang S (2019) MiR-150 promotes angiogensis and proliferation of endothelial progenitor cells in deep venous thrombosis by targeting SRCIN1. Microvasc Res 123:35–41 Wang X, Sundquist K, Svensson PJ et al (2019) Association of recurrent venous thromboembolism and circulating microRNAs. Clin Epigenet 11:28 Rodriguez-Rius A, Lopez S, Martinez-Perez A, Souto JC, Soria JM (2020) Identification of a plasma MicroRNA Profile associated with venous thrombosis. Arterioscler, Thromb, Vasc Biol 40:1392–1399 Rodriguez-Rius A, Lopez S, Martinez-Perez A, Souto JC, Soria JM (2020) Identification of a plasma MicroRNA profile associated with venous thrombosis. Arterioscler Thromb Vasc Biol 40(5):1392–1399. https://doi.org/10.1161/ATVBAHA.120.314092 Mussbacher M, Krammer TL, Heber S et al (2020) Impact of anticoagulation and sample processing on the quantification of human blood-derived microRNA signatures. Cells 9(8):E1915. https://doi.org/10.3390/cells9081915 Jiang Z, Ma J, Wang Q, Wu F, Ping J, Ming L (2018) Combination of circulating miRNA-320a/b and D-dimer improves diagnostic accuracy in deep vein thrombosis patients. Med Sci Monit 6(24):2031–2037 Starikova I, Jamaly S, Sorrentino A, Blondal T, Latysheva N, Sovershaev M, Hansen JB (2015) Differential expression of plasma miRNAs in patients with unprovoked venous thromboembolism and healthy control individuals. Thromb Res 136(3):566–572 Thomas PD, Ebert D, Muruganujan A, Mushayahama T, Albou L-P, Mi H (2022) PANTHER: making genome-scale phylogenetics accessible to all. Protein Soc 31(1):8–22. https://doi.org/10.1002/pro.421 Kloosterman WP, Plasterk RH (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450. https://doi.org/10.1016/j.devcel.2006.09.009 Paul P, Chakraborty A, Sarkar D, Langthasa M, Rahman M, Bari M, Singha RS, Malakar AK, Chakraborty S (2018) Interplay between miRNAs and human diseases. J Cell Physiol 233:2007–2018. https://doi.org/10.1002/jcp.25854 Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16:203–222. https://doi.org/10.1038/nrd.2016.246 Van Rooij E, Kauppinen S (2014) Development of microRNA therapeutics is coming of age. EMBO Mol Med 6:851–864. https://doi.org/10.15252/emmm.201100899 Morelli VM, Brækkan SK, Hansen JB (2020) Role of microRNAs in venous thromboembolism. Int J Mol Sci 21(7):2602 Denby L, Ramdas V, Lu R, Conway BR, Grant JS, Dickinson B, Aurora AB, McClure JD, Kipgen D, Delles C, van Rooij E, Baker AH (2014) MicroRNA-214 antagonism protects against renal fibrosis. J Am Soc Nephrol 25(1):65–80 Zhang H, Qu Y, Wang A (2018) Antagonist targeting microRNA-146a protects against lithium-pilocarpine-induced status epilepticus in rats by nuclear factor-κB pathway. Mol Med Rep 17:5356–5361 Hum C, Loiselle J, Ahmed N, Shaw TA, Toudic C, Pezacki JP (2021) MicroRNA mimics or inhibitors as antiviral therapeutic approaches against COVID-19. Drugs 81(5):517–531 Sun L, Li X, Li Q, Wang L, Li J, Shu C (2021) Multiple arterial and venous thromboembolism in a male patient with hereditary protein C deficiency. Medicine (Baltimore) 100(15):e25575. https://doi.org/10.1097/MD.0000000000025575 Du X, Hong L, Sun L, Sang H, Qian A, Li W, Zhuang H, Liang H, Song D, Li C et al (2019) miR-21 induces endothelial progenitor cells proliferation and angiogenesis via targeting FASLG and is a potential prognostic marker in deep venous thrombosis. J Transl Med 17:270 Kong L, Du X, Hu N, Li W, Wang W, Wei S, Zhuang H, Li X, Li C (2016) Downregulation of let-7e-5p contributes to endothelial progenitor cell dysfunction in deep vein thrombosis via targeting FASLG. Thromb Res 138:30–36 Kong L, Hu N, Du X, Wang W, Chen H, Li W, Wei S, Zhuang H, Li X, Li C (2016) Upregulation of miR-483-3p contributes to endothelial progenitor cells dysfunction in deep vein thrombosis patients via SRF. J Transl Med 14:23 Meng Q, Wang W, Yu X, Li W, Kong L, Qian A, Li C, Li X (2015) Upregulation of MicroRNA-126 contributes to endothelial progenitor cell function in deep vein thrombosis via its target PIK3R2. J Cell Biochem 116:1613–1623. https://doi.org/10.1002/jcb.25115 Wang W, Li C, Li W, Kong L, Qian A, Hu N, Meng Q, Li X (2014) MiR-150 enhances the motility of EPCs in vitro and promotes EPCs homing and thrombus resolving in vivo. Thromb Res 133:590–598 Sun S, Chai S, Zhang F, Lu L (2020) Overexpressed microRNA-103a-3p inhibits acute lower-extremity deep venous thrombosis via inhibition of CXCL12. IUBMB Life 72(3):492–504. https://doi.org/10.1002/iub.2168 Sun S, Chai S, Zhang F, Lu L (2020) Overexpressed microRNA-103a-3p inhibits acute lower-extremity deep venous thrombosis via inhibition of CXCL12. IUBMB Life 72:492–504. https://doi.org/10.1002/iub.2168 Zhang Y, Zhang Z, Wei R, Miao X, Sun S, Liang G, Chu C, Zhao L, Zhu X, Guo Q et al (2020) IL (Interleukin)-6 contributes to deep vein thrombosis and is negatively regulated by miR-338-5p. Arterioscler Thromb Vasc Biol 40:323–334 McCreight J, Schneider S, Wilburn D, Swanson W (2017) Evolution of microRNA in primates. PLoS ONE 12:e0176596. https://doi.org/10.1371/journal.pone.0176596 Chen X, Gao S, Zhao Z, Liang G, Kong J, Feng X (2020) MicroRNA-320d regulates tumor growth and invasion by promoting FoxM1 and predicts poor outcome in gastric cardiac adenocarcinoma. Cell Biosci 10:80. https://doi.org/10.1186/s13578-020-00439-7 Fang Z, Tang J, Bai Y, Lin H, You H, Jin H, Lin L, You P, Li J, Dai Z et al (2015) Plasma levels of microRNA-24, microRNA-320a, and microRNA-423-5p are potential biomarkers for colorectal carcinoma. J Exp Clin Cancer Res 34:86. https://doi.org/10.1186/s13046-015-0198-6 Hong H, Zhu H, Zhao S, Wang K, Zhang N, Tian Y, Li Y, Wang Y, Lv X, Wei T et al (2019) The novel circCLK3/miR-320a/FoxM1 axis promotes cervical cancer progression. Cell Death Dis 10:950. https://doi.org/10.1038/s41419-019-2183-z Lv Q, Du H, Liu Y, Huang Y, Wang G, Zhang X, Chen S, Zhou H (2017) Low expression of microRNA-320b correlates with tumorigenesis and unfavorable prognosis in glioma. Oncol Rep 38:959–966. https://doi.org/10.3892/or.2017.5762 Thibord F, Munsch G, Perret C, Suchon P, Roux M, Ibrahim-Kosta M, Goumidi L, Deleuze JF, Morange PE, Trégouët DA (2020) Bayesian network analysis of plasma microRNA sequencing data in patients with venous thrombosis. Eur Heart J Suppl 22(Suppl C):C34–C45 Diener C, Keller A, Meese E (2022) Emerging concepts of miRNA therapeutics: from cells to clinic. Trends Genet 38(6):613–626 Nagalla S, Shaw C, Kong X et al (2011) Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 117(19):5189–5197. https://doi.org/10.1182/blood-2010-09-299719