Highlights
- •Thrombosis and inflammation are both involved in atherosclerosis progression.
- •Interaction between these two processes supports the concept of thromboinflammation.
- •Low grade inflammation promotes coagulation and platelet activation and viceversa.
- •In contrast to platelet inhibition, anti-inflammatory approaches are not applied in clinical practice.
- •Targeting both thrombosis and inflammation may address residual cardiovascular risk.
Abstract
The association between thrombosis and acute coronary syndromes is well established.
Inflammation and activation of innate and adaptive immunity are another important
factor implicated in atherosclerosis. However, the exact interactions between thrombosis
and inflammation in atherosclerosis are less well understood. Accumulating data suggest
a firm interaction between these two key pathophysiologic processes. Pro-inflammatory
cytokines, such as tumor necrosis factor α, interleukin-6 and interleukin-1, have
been implicated in the thrombotic cascade following plaque rupture and myocardial
infarction. Furthermore, cell adhesion molecules accelerate not only atheromatosis
but also thrombosis formation while activated platelets are able to trigger leukocyte
adhesion and accumulation. Additionally, tissue factor, thrombin, and activated coagulation
factors induce the release of pro-inflammatory cytokines such as prostaglandin and
C reactive protein, which may further induce von Willebrand factor secretion. Treatments
targeting immune activation (i.e. interleukin-1 inhibitors, colchicine, statins, etc.)
may also beneficially modulate platelet activation while common anti-thrombotic therapies
appear to attenuate the inflammatory process. Taken together in the context of cardiovascular
diseases, thrombosis and inflammation should be studied and managed as a common entity
under the concept of thrombo-inflammation.
Graphical abstract
Graphical Abstract
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to AtherosclerosisAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- ESC Guidelines for the management of acute myocardial infarction in patients presenting with ST-segment elevation: the Task Force for the management of acute myocardial infarction in patients presenting with ST-segment elevation of the European Society of Cardiology (ESC).Eur. Heart J. 2017; 39 (2018): 119-177
- Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolic diseases.Arterioscler. Thromb. Vasc. Biol. 2011; 31: e88-99
- Inflammatory cytokines in atherosclerosis: current therapeutic approaches.Eur. Heart J. 2016; 37: 1723-1732
- Antiinflammatory therapy with canakinumab for atherosclerotic disease.N. Engl. J. Med. 2017; 377: 1119-1131
- Assessing inflammatory status in cardiovascular disease.Heart. 2007; 93: 1001-1007
- Atherosclerosis--an inflammatory disease.N. Engl. J. Med. 1999; 340: 115-126
- The role and predictive value of cytokines in atherosclerosis and coronary artery disease.Curr. Med. Chem. 2015; 22: 2636-2650
- Signaling by the TNF receptor superfamily and T cell homeostasis.Immunity. 2000; 13: 419-422
- Recent advances on the role of cytokines in atherosclerosis.Arterioscler. Thromb. Vasc. Biol. 2011; 31: 969-979
- C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease.N. Engl. J. Med. 2004; 350: 1387-1397
- Pro-inflammatory interleukin-1 genotypes potentiate the risk of coronary artery disease and cardiovascular events mediated by oxidized phospholipids and lipoprotein(a).J. Am. Coll. Cardiol. 2014; 63: 1724-1734
- Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein.N. Engl. J. Med. 2008; 359: 2195-2207
- Increased proinflammatory cytokines in patients with chronic stable angina and their reduction by aspirin.Circulation. 1999; 100: 793-798
- Low-dose methotrexate for the prevention of atherosclerotic events.N. Engl. J. Med. 2018; 380: 752-762
- Variability of human pluripotent stem cell lines.Curr. Opin. Genet. Dev. 2017; 46: 179-185
- Leukocyte-versus microparticle-mediated tissue factor transfer during arteriolar thrombus development.J. Leukoc. Biol. 2005; 78: 1318-1326
- Platelets enhance neutrophil transendothelial migration via P-selectin glycoprotein ligand-1.Am. J. Physiol. Heart Circ. Physiol. 2011; 300: H468-H475
- NOX2 is critical for heterotypic neutrophil-platelet interactions during vascular inflammation.Blood. 2015; 126: 1952-1964
- Increased formation of monocyte-platelet aggregates in ischemic heart failure.Circ Heart Fail. 2013; 6: 127-135
- Association of platelet-monocyte aggregates with platelet activation, systemic inflammation, and myocardial injury in patients with non-st elevation acute coronary syndromes.Clin. Cardiol. 2007; 30: 26-31
- Neutrophil extracellular traps in atherosclerosis and atherothrombosis.Circ. Res. 2017; 120: 736-743
- Unravelling the mechanism and significance of thrombin binding to platelet glycoprotein Ib.Thromb. Haemostasis. 2010; 104: 894-902
- Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size.Circ. Res. 2015; 116: 1182-1192
- Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps.J. Thromb. Haemostasis. 2014; 12: 2074-2088
- A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin.EMBO J. 2007; 26: 1129-1139
- Disulfide HMGB1 derived from platelets coordinates venous thrombosis in mice.Blood. 2016; 128: 2435-2449
- Platelet-derived Toll-like receptor 4 (Tlr-4) is sufficient to promote microvascular thrombosis in endotoxemia.PloS One. 2012; 7e41254
- Infection and atherosclerosis: TLR-dependent pathways.Cell. Mol. Life Sci. 2020; 77: 2751-2769
- Toll-like receptors in atherosclerosis: a 'Pandora's box' of advances and controversies.Trends Pharmacol. Sci. 2013; 34: 629-636
- Treatment with a Toll-like Receptor 7 ligand evokes protective immunity against atherosclerosis in hypercholesterolaemic mice.J. Intern. Med. 2020; https://doi.org/10.1111/joim.13085
- Inflammation in acute coronary syndrome: expression of TLR2 mRNA is increased in platelets of patients with.ACS. PLoS One. 2019; 14e0224181
- TLR2 and neutrophils potentiate endothelial stress, apoptosis and detachment: implications for superficial erosion.Eur. Heart J. 2015; 36: 1394-1404
- Platelet factor 4 mediates vascular smooth muscle cell injury responses.Blood. 2013; 121: 4417-4427
- Platelet extracellular vesicles induce a pro-inflammatory smooth muscle cell phenotype.J. Extracell. Vesicles. 2017; 6: 1322454
- The missing link between atherosclerosis, inflammation and thrombosis: is it tissue factor?.Expert Rev. Cardiovasc Ther. 2011; 9: 517-523
- Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia.Blood. 2004; 103: 1342-1347
- Vascular remodeling in mice lacking the cytoplasmic domain of tissue factor.Circ. Res. 2005; 97: 293-298
- Inhibition of the tissue factor-thrombin pathway limits infarct size after myocardial ischemia-reperfusion injury by reducing inflammation.Am. J. Pathol. 2000; 157: 1849-1862
- Pathologies at the nexus of blood coagulation and inflammation: thrombin in hemostasis, cancer, and beyond.J. Mol. Med. (Berl.). 2013; 91: 1257-1271
- Coagulation factor Xa cleaves protease-activated receptor-1 and mediates signaling dependent on binding to the endothelial protein C receptor.J. Thromb. Haemostasis. 2010; 8: 379-388
- Factor Xa: at the crossroads between coagulation and signaling in physiology and disease.Trends Mol. Med. 2008; 14: 429-440
- Coagulation factor Xa stimulates interleukin-8 release in endothelial cells and mononuclear leukocytes: implications in acute myocardial infarction.Arterioscler. Thromb. Vasc. Biol. 2005; 25: 461-466
- Regulated expression of platelet factor 4 in human monocytes--role of PARs as a quantitatively important monocyte activation pathway.J. Leukoc. Biol. 2005; 78: 202-209
- Membrane-type serine protease-1/matriptase induces interleukin-6 and -8 in endothelial cells by activation of protease-activated receptor-2: potential implications in atherosclerosis.Arterioscler. Thromb. Vasc. Biol. 2007; 27: 769-775
- Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation.Nature. 2008; 452: 654-658
Burzynski LC, Humphry M, Pyrillou K, Wiggins KA, Chan JNE, Figg N, et al. The coagulation and immune systems are directly linked through the activation of interleukin-1alpha by thrombin. Immunity.50(4):1033-10342 e6.
- How the protease thrombin talks to cells.Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 11023-11027
- Detection of up-regulated genes in thrombin-stimulated human umbilical vein endothelial cells.Thromb. Res. 2006; 118: 715-721
- Activation of the 92 kDa type IV collagenase by tissue kallikrein.J. Cell. Physiol. 1993; 157: 587-593
- Regulation of tumor necrosis factor receptor-1 and the IKK-NF-kappaB pathway by LDL receptor-related protein explains the antiinflammatory activity of this receptor.Blood. 2008; 111: 5316-5325
- Factor XII and uPAR upregulate neutrophil functions to influence wound healing.J. Clin. Invest. 2018; 128: 944-959
- Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation.Blood. 2013; 122: 3405-3414
- Sterol regulatory element binding protein 2 activation of NLRP3 inflammasome in endothelium mediates hemodynamic-induced atherosclerosis susceptibility.Circulation. 2013; 128: 632-642
- Inflammation. Neutrophil extracellular traps license macrophages for cytokine production in atherosclerosis.Science. 2015; 349: 316-320
- NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals.Nature. 2010; 464: 1357-1361
- NLRP3 inflammasome and the IL-1 pathway in atherosclerosis.Circ. Res. 2018; 122: 1722-1740
- Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1beta-rich microparticles.J. Immunol. 2011; 186: 5489-5496
- Antithrombin acts as a negative acute phase protein as established with studies on HepG2 cells and in baboons.Thromb. Haemostasis. 1997; 78: 1088-1092
- In vivo modulation of coagulation and fibrinolysis by recombinant glycosylated human interleukin-6 in baboons.Eur. Cytokine Netw. 1994; 5: 275-281
- IL-1 and IL-6 induce hepatocyte plasminogen activator inhibitor-1 expression through independent signaling pathways converging on C/EBPdelta.Am. J. Physiol. Cell Physiol. 2007; 292: C209-C215
- NLRP3 regulates platelet integrin alphaIIbbeta3 outside-in signaling, hemostasis and arterial thrombosis.Haematologica. 2018; 103: 1568-1576
- C-reactive protein decreases prostacyclin release from human aortic endothelial cells.Circulation. 2003; 108: 1676-1678
- A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis.Circulation. 2002; 106: 913-919
- Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells.Circulation. 2002; 106: 1439-1441
- C-reactive protein induces human peripheral blood monocytes to synthesize tissue factor.Blood. 1993; 82: 513-520
- Activation of inflammation and coagulation after infusion of C-reactive protein in humans.Circ. Res. 2005; 96: 714-716
- Increased thrombosis after arterial injury in human C-reactive protein-transgenic mice.Circulation. 2003; 108: 512-515
- Generation of C-reactive protein and complement components in atherosclerotic plaques.Am. J. Pathol. 2001; 158: 1039-1051
- Dissociation of C-reactive protein localizes and amplifies inflammation: evidence for a direct biological role of C-reactive protein and its conformational changes.Front. Immunol. 2018; 9: 1351
- Association of polymorphisms in the CRP gene with circulating C-reactive protein levels and cardiovascular events.JAMA. 2006; 296: 2703-2711
- The clinical significance and potential role of C-reactive protein in chronic inflammatory and neurodegenerative diseases.Front. Immunol. 2018; 9: 1302
- Association between C reactive protein and coronary heart disease: mendelian randomisation analysis based on individual participant data.BMJ. 2011; 342: d548
- High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase.Nat. Med. 2001; 7: 853-857
- The effect of inflammation and infection on lipids and lipoproteins.in: Feingold K.R. Anawalt B. Boyce A. Chrousos G. Dungan K. Grossman A. Endotext. South Dartmouth (MA). 2000
- High-density lipoprotein modulates thrombosis by preventing von Willebrand factor self-association and subsequent platelet adhesion.Blood. 2016; 127: 637-645
- HDL cholesterol transport during inflammation.Curr. Opin. Lipidol. 2007; 18: 147-151
- LDL and HDL have opposing effects on VWF self-association.Blood. 2017; 130: 3601
- Effects of inflammatory cytokines on the release and cleavage of the endothelial cell-derived ultralarge von Willebrand factor multimers under flow.Blood. 2004; 104: 100-106
- Oxidative modification of von Willebrand factor by neutrophil oxidants inhibits its cleavage by ADAMTS13.Blood. 2010; 115: 706-712
- Inflammation and acute phase proteins in haemostasis.in: Janciauskiene S. Acute Phase Proteins. IntechOpen, 2013
- Immune functions of platelets.Thromb. Haemostasis. 2014; 112: 678-691
- Reactive thrombocytosis associated with acute myocardial infarction following STEMI with percutaneous coronary intervention.Case Rep Cardiol. 2013; 2013: 707438
- Persistent reactive thrombocytosis may increase the risk of coronary artery disease among inflammatory bowel disease patients.Dig. Dis. Sci. 2015; 60: 3062-3068
- Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men.N. Engl. J. Med. 1997; 336: 973-979
- Effect of low-dose aspirin on vascular inflammation, plaque stability, and atherogenesis in low-density lipoprotein receptor-deficient mice.Circulation. 2002; 106: 1282-1287
- Inhibition of platelets by clopidogrel suppressed ang II-induced vascular inflammation, oxidative stress, and remodeling.J Am Heart Assoc. 2018; 7e009600
- Effect of clopidogrel on the expression of inflammatory markers in rabbit ischemic coronary artery.Br. J. Pharmacol. 2005; 146: 419-424
- P2Y12 inhibition beyond thrombosis: effects on inflammation.Int. J. Mol. Sci. 2020; 21
- Ticagrelor attenuates myocardial ischaemia-reperfusion injury possibly through downregulating galectin-3 expression in the infarct area of rats.Br. J. Clin. Pharmacol. 2018; 84: 1180-1186
- Platelet P2Y12 inhibitors reduce systemic inflammation and its prothrombotic effects in an experimental human model.Arterioscler. Thromb. Vasc. Biol. 2015; 35: 2562-2570
- Comparison of ticagrelor versus prasugrel for inflammation, vascular function, and circulating endothelial progenitor cells in diabetic patients with non-ST-segment elevation acute coronary syndrome requiring coronary stenting: a prospective, randomized, crossover trial.JACC Cardiovasc. Interv. 2017; 10: 1646-1658
- Effect of clopidogrel vs ticagrelor on platelet aggregation and inflammation markers after percutaneous coronary intervention for ST-elevation myocardial infarction.Can. J. Cardiol. 2018; 34: 1606-1612
- Effects of clopidogrel on soluble CD40 ligand and on high-sensitivity C-reactive protein in patients with stable coronary artery disease.Am. Heart J. 2006; 151: 521 e1-e4
- Effect of aspirin plus clopidogrel on inflammatory markers in patients with non-ST-segment elevation acute coronary syndrome.Chin Med J (Engl). 2006; 119: 32-36
- Platelet inhibition with prasugrel (CS-747) compared with clopidogrel in patients undergoing coronary stenting: the subset from the JUMBO study.Postgrad Med J. 2006; 82: 404-410
- Evaluation of plaque stability of advanced atherosclerotic lesions in apo E-deficient mice after treatment with the oral factor Xa inhibitor rivaroxaban.Mediat. Inflamm. 2011; 2011: 432080
- Rivaroxaban, a novel oral anticoagulant, attenuates atherosclerotic plaque progression and destabilization in ApoE-deficient mice.Atherosclerosis. 2015; 242: 639-646
- Statin therapy, LDL cholesterol, C-reactive protein, and coronary artery disease.N. Engl. J. Med. 2005; 352: 29-38
- Platelet reactivity in response to loading dose of atorvastatin or rosuvastatin in patients with stable coronary disease before percutaneous coronary intervention: the STATIPLAT randomized study.Clin. Cardiol. 2017; 40: 605-611
- Effects of statin therapy on platelet reactivity after percutaneous coronary revascularization in patients with acute coronary syndrome.J. Thromb. Thrombolysis. 2017; 44: 355-361
- Impact of high-dose statins on vitamin D levels and platelet function in patients with coronary artery disease.Thromb. Res. 2017; 150: 90-95
- Interest of colchicine in the treatment of acute myocardial infarct responsible for heart failure in a mouse model.Int. J. Cardiol. 2017; 240: 347-353
- Anti-inflammatory treatment with colchicine in acute myocardial infarction: a pilot study.Circulation. 2015; 132: 1395-1403
- Effect of colchicine on platelet-platelet and platelet-leukocyte interactions: a pilot study in healthy subjects.Inflammation. 2016; 39: 182-189
- Colchicine reduces platelet aggregation by modulating cytoskeleton rearrangement via inhibition of cofilin and LIM domain kinase 1.Vasc. Pharmacol. 2018; 111: 62-70
- Efficacy and safety of low-dose colchicine after myocardial infarction.N. Engl. J. Med. 2019; 381: 2497-2505
- Systemic autoinflammation with intractable epilepsy managed with interleukin-1 blockade.J. Neuroinflammation. 2018; 15: 38
- The in vitro effect of antirheumatic drugs on platelet function.Platelets. 2020; 31: 248-257
- Effect of a single dose of the interleukin-6 receptor antagonist tocilizumab on inflammation and troponin T release in patients with non-ST-elevation myocardial infarction: a double-blind, randomized, placebo-controlled phase 2 trial.Eur. Heart J. 2016; 37: 2406-2413
- Nonhemostatic activities of factor Xa: are there pleiotropic effects of anti-FXa direct oral anticoagulants?.Angiology. 2019; 70 (3319719840861): 896-907
- Nitric oxide activates diverse signaling pathways to regulate gene expression.J. Biol. Chem. 2003; 278: 42321-42329
- Sphingosine-1-phosphate: an enigmatic signalling lipid.Nat. Rev. Mol. Cell Biol. 2003; 4: 397-407
- Sphingosine 1-phosphate receptors mediate stimulatory and inhibitory signalings for expression of adhesion molecules in endothelial cells.Cell. Signal. 2006; 18: 841-850
- Rivaroxaban attenuates leukocyte adhesion in the microvasculature and thrombus formation in an experimental mouse model of type 2 diabetes mellitus.Thromb. Res. 2014; 133: 276-280
- Influence of vitamin K antagonists and direct oral anticoagulation on coronary artery disease: a CTA analysis.Int. J. Cardiol. 2018; 260: 11-15
- Evaluation of plaque stability of advanced atherosclerotic lesions in apo E-deficient mice after treatment with the oral factor Xa inhibitor rivaroxaban.Mediat. Inflamm. 2011; : 432080
- Apixaban versus warfarin in evaluation of progression of atherosclerotic and calcified plaques (prospective randomized trial).Am. Heart J. 2019; 212: 129-133
- Differential cellular effects of old and new oral anticoagulants: consequences to the genesis and progression of atherosclerosis.Thromb. Haemostasis. 2014; 112: 909-917
- Melagatran reduces advanced atherosclerotic lesion size and may promote plaque stability in apolipoprotein E-deficient mice.Arterioscler. Thromb. Vasc. Biol. 2006; 26: 2787-2792
Borissoff JI, Otten JJ, Heeneman S, Leenders P, van Oerle R, Soehnlein O, et al. Genetic and pharmacological modifications of thrombin formation in apolipoprotein e-deficient mice determine atherosclerosis severity and atherothrombosis onset in a neutrophil-dependent manner. PloS One.8(2):e55784.
- Rivaroxaban in patients with a recent acute coronary syndrome.N. Engl. J. Med. 2012; 366: 9-19
- Rivaroxaban with or without aspirin in stable cardiovascular disease.N. Engl. J. Med. 2017; 377: 1319-1330
- Statins as anti-inflammatory agents in atherogenesis: molecular mechanisms and lessons from the recent clinical trials.Curr. Pharmaceut. Des. 2012; 18: 1519-1530
- Statin-induced Kruppel-like factor 2 expression in human and mouse T cells reduces inflammatory and pathogenic responses.J. Clin. Invest. 2010; 120: 1961-1970
- Endothelium-dependent effects of statins.Arterioscler. Thromb. Vasc. Biol. 2003; 23: 729-736
- Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment.Circulation. 2003; 108: 1567-1574
- Atorvastatin enhances interleukin-10 levels and improves cardiac function in rats after acute myocardial infarction.Clin. Sci. (Lond.). 2009; 116: 45-52
- Simvastatin attenuates cardiopulmonary bypass-induced myocardial inflammatory injury in rats by activating peroxisome proliferator-activated receptor gamma.Eur. J. Pharmacol. 2010; 649: 255-262
- Early and late benefits of high-dose atorvastatin in patients with acute coronary syndromes: results from the PROVE IT-TIMI 22 trial.J. Am. Coll. Cardiol. 2005; 46: 1405-1410
- The influence of statin therapy on platelet activity markers in hyperlipidemic patients after ischemic stroke.Arch. Med. Sci. 2015; 11: 115-121
- Effect of statins on platelet function in patients with hyperlipidemia.Arch. Med. Sci. 2013; 9: 622-628
- Statin prevents tissue factor expression in human endothelial cells: role of Rho/Rho-kinase and Akt pathways.Circulation. 2002; 105: 1756-1759
- Immediate antioxidant and antiplatelet effect of atorvastatin via inhibition of Nox2.Circulation. 2012; 126: 92-103
- Effects of atorvastatin and rosuvastatin on thromboxane-dependent platelet activation and oxidative stress in hypercholesterolemia.Atherosclerosis. 2011; 214: 122-128
- Rosuvastatin decreases mean platelet volume in patients with diabetes mellitus.Angiology. 2016; 67: 116-120
- Platelet hyperactivity after statin treatment discontinuation.Thromb. Haemostasis. 2003; 90: 476-482
- Platelet tissue factor activity and membrane cholesterol are increased in hypercholesterolemia and normalized by rosuvastatin, but not by atorvastatin.Atherosclerosis. 2017; 257: 164-171
- Differential effects of interleukin-1 receptor antagonist and tumor necrosis factor binding protein on fatty-streak formation in apolipoprotein E-deficient mice.Circulation. 1998; 97: 242-244
- Stage-dependent differential effects of interleukin-1 isoforms on experimental atherosclerosis.Eur. Heart J. 2019; 40: 2482-2491
- Effect of colchicine (0.5 mg twice daily) on high-sensitivity C-reactive protein independent of aspirin and atorvastatin in patients with stable coronary artery disease.Am. J. Cardiol. 2007; 99: 805-807
- Colchicine acutely suppresses local cardiac production of inflammatory cytokines in patients with an acute coronary syndrome.J Am Heart Assoc. 2015; 4e002128
- Procoagulant effects of low-level platelet activation and its inhibition by colchicine.Thromb. Haemostasis. 2018; 118: 723-733
- Effects of interleukin-1beta inhibition with canakinumab on hemoglobin A1c, lipids, C-reactive protein, interleukin-6, and fibrinogen: a phase IIb randomized, placebo-controlled trial.Circulation. 2012; 126: 2739-2748
- Relationship of C-reactive protein reduction to cardiovascular event reduction following treatment with canakinumab: a secondary analysis from the CANTOS randomised controlled trial.Lancet. 2018; 391: 319-328
- Canakinumab for acute gouty arthritis in patients with limited treatment options: results from two randomised, multicentre, active-controlled, double-blind trials and their initial extensions.Ann. Rheum. Dis. 2012; 71: 1839-1848
- The Inter-relationship of platelets with interleukin-1beta-mediated inflammation in humans.Thromb. Haemostasis. 2018; 118: 2112-2125
- Tocilizumab improves the proatherothrombotic profile of rheumatoid arthritis patients modulating endothelial dysfunction, NETosis, and inflammation.Transl. Res. 2017; 183: 87-103
- Effect of interleukin-6 inhibition on coronary microvascular and endothelial function in myocardial infarction.Heart. 2017; 103: 1521-1527
- Short-term application of tocilizumab during myocardial infarction (STAT-MI).Rheumatol. Int. 2018; 38: 59-66
- Unlike tocilizumab, etanercept slightly increases experimental thrombin-induced aggregation in healthy individuals.Joint Bone Spine. 2017; 84: 373-375
- Disruption of tumor necrosis factor-alpha gene diminishes the development of atherosclerosis in ApoE-deficient mice.Atherosclerosis. 2005; 180: 11-17
- Critical role of TNF inhibition in combination therapy for elderly mice with atherosclerosis.Cardiovasc Ther. 2017; 35
- Adiponectin inhibits TNF-alpha-activated PAI-1 expression via the cAMP-PKA-AMPK-NF-kappaB Axis in human umbilical vein endothelial cells.Cell. Physiol. Biochem. 2017; 42: 2342-2352
- Cardiovascular outcomes and systemic anti-inflammatory drugs in patients with severe psoriasis: 5-year follow-up of a Danish nationwide cohort.J. Eur. Acad. Dermatol. Venereol. 2015; 29: 1128-1134
- Treatment with tumor necrosis factor blockers is associated with a lower incidence of first cardiovascular events in patients with rheumatoid arthritis.J. Rheumatol. 2005; 32: 1213-1218
- Response to biological treatment and subsequent risk of coronary events in rheumatoid arthritis.Ann. Rheum. Dis. 2016; 75: 2087-2094
- The platelet functions in patients with ankylosing spondylitis: anti-TNF-alpha therapy decreases the mean platelet volume and platelet mass.Platelets. 2010; 21: 126-131
- Mean platelet volume in patients with rheumatoid arthritis: the effect of anti-TNF-alpha therapy.Rheumatol. Int. 2010; 30: 1125-1129
- Targeting P-selectin glycoprotein ligand-1/P-selectin interactions as a novel therapy for metabolic syndrome.Transl. Res. 2017; 183: 1-13
- Effects of the P-selectin antagonist inclacumab on myocardial damage after percutaneous coronary intervention according to Timing of infusion: Insights from the SELECT-ACS trial.J Am Heart Assoc. 2016; 5
- Akkermansia muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in apoe-/- mice.Circulation. 2016; 133: 2434-2446
- Berberine mitigates high glucose-potentiated platelet aggregation and apoptosis by modulating aldose reductase and NADPH oxidase activity.Free Radic. Biol. Med. 2019; 130: 196-205
- The ketone metabolite beta-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease.Nat. Med. 2015; 21: 263-269
- Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease.Gut. 2000; 47: 397-403
- Dietary Fiber for the Prevention of Cardiovascular Disease.Academic Press, Los Angeles2017 (2017)
- Chemokines control mobilization, recruitment, and fate of monocytes in atherosclerosis.Arterioscler. Thromb. Vasc. Biol. 2015; 35: 1050-1055
- Systemic inflammation in metabolic syndrome: increased platelet and leukocyte activation, and key role of CX3CL1/CX3CR1 and CCL2/CCR2 axes in arterial platelet-proinflammatory monocyte adhesion.J. Clin. Med. 2019; 8
- Chemokine CC-motif ligand 2 participates in platelet function and arterial thrombosis by regulating PKCalpha-P38MAPK-HSP27 pathway.Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 2018; 1864: 2901-2912
- Blocking CCL5-CXCL4 heteromerization preserves heart function after myocardial infarction by attenuating leukocyte recruitment and NETosis.Sci. Rep. 2018; 8: 10647
- Soluble CD40 ligand impairs the anti-platelet function of peripheral blood angiogenic outgrowth cells via increased production of reactive oxygen species.Thromb. Haemostasis. 2013; 109: 940-947
- The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation.Proc. Natl. Acad. Sci. U. S. A. 2010; 107: 228-233
- Impact of the gut microbiota on inflammation, obesity, and metabolic disease.Genome Med. 2016; 8: 42
- Risk factors, prognosis, and secondary prevention of myocardial infarction in young adults in Poland.Kardiol. Pol. 2016; 74: 1148-1153
- Berberine treatment increases Akkermansia in the gut and improves high-fat diet-induced atherosclerosis in Apoe(-/-) mice.Atherosclerosis. 2018; 268: 117-126
- Interactions between Roseburia intestinalis and diet modulate atherogenesis in a murine model.Nat Microbiol. 2018; 3: 1461-1471
- Effect of CC chemokine receptor 2 CCR2 blockade on serum C-reactive protein in individuals at atherosclerotic risk and with a single nucleotide polymorphism of the monocyte chemoattractant protein-1 promoter region.Am. J. Cardiol. 2011; 107: 906-911
- Effects of therapy with maraviroc on the carotid Intima media thickness in HIV-1/HCV Co-infected patients.Vivo. 2017; 31: 125-131
- Inflammatory role and prognostic value of platelet chemokines in acute coronary syndrome.Thromb. Haemostasis. 2014; 112: 1277-1287
- Reduction of atherosclerosis in mice by inhibition of CD40 signalling.Nature. 1998; 394: 200-203
- Inhibition of CD40 signaling limits evolution of established atherosclerosis in mice.Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 7458-7463
- Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile.J. Exp. Med. 2010; 207: 391-404
- Targeting CD40-induced TRAF6 signaling in macrophages reduces atherosclerosis.J. Am. Coll. Cardiol. 2018; 71: 527-542
- Efficacy and safety assessment of a TRAF6-targeted nanoimmunotherapy in atherosclerotic mice and non-human primates.Nat Biomed Eng. 2018; 2: 279-292
Article Info
Publication History
Published online: August 01, 2020
Accepted:
July 29,
2020
Received in revised form:
July 22,
2020
Received:
March 17,
2020
Identification
Copyright
© 2020 Elsevier B.V. All rights reserved.
