Immunothrombosis
Keywords:
-Downloads
References
Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol. 2013;13:34-45.
Jackson SP, Darbousset R, Schoenwaelder SM. Thromboinflammation: challenges of therapeutically targeting coagulation and other host defense mechanisms. Blood. 2019;133:906-18.
Connell NT. Taken the wrong way, a complement becomes catastrophic. Blood. 2020;135:233-4.
Delvaeye M, Conway EM. Coagulation and innate immune responses: can we view them separately? Blood. 2009;114:2367-74.
Amara U, Flierl MA, Rittirsch D, Klos A, Chen H, Acker B, et al. Molecular intercommunication between the complement and coagulation systems. J Immunol. 2010;185:5628-36.
Conway EM. Thrombin: Coagulation’s master regulator of innate immunity. J Thromb Haemost. 2019;17:1785-9.
Semeraro F, Ammollo CT, Morrissey JH, Dale GL, Friese P, Esmon NL, et al. Extracellular histones promote thrombin generation through platelet-dependent mechanisms: involvement of platelet TLR2 and TLR4. Blood. 2011;118:1952-61.
Silk E, Zhao H, Weng H, Ma D. The role of extracellular histone in organ injury. Cell Death Dis. 2017;8:e2812.
Massberg S, Grahl L, Von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nature Med. 2010;16:887-96.
Esmon CT. Molecular circuits in thrombosis and inflammation. Thromb Haemost. 2013;109:416-20.
Gaertner F, Massberg S. Blood coagulation in immunothrombosis - at the frontline of intravascular immunity. Semin Immunol. 2016;28:561-9.
Foley JH. Examining coagulation-complement crosstalk: complement activation and thrombosis. Thromb Res. 2016;141:S50-4.
Foley J H, Walton BL, Aleman MM, O’Byrne AM, Lei V, Harrasser M, et al. Complement activation in arterial and venous thrombosis is mediated by plasmin. E Bio Medicine. 2016;5:175-82.
Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med. 2006;12:682-7.
Krisinger MJ, Goebeler V, Lu Z, Meixner SC, Myles T, Pryzdial ELG, et al. Thrombin generates previously unidentified C5 products that support the terminal complement activation pathway. Blood. 2012;120:1717-25.
Nickel KF, Long AT, Fuchs TA, Butler LM, Renne T. Factor XII as a therapeutic target in thromboembolic and inflammatory diseases. Arterioscler Thromb Vasc Biol. 2017;37:13-20.
Faxalv L, Boknas N, Strom JO, Tengvall P, Theodorsson E, Ramström S, et al. Putting polyphosphates to the test: evidence against platelet-induced activation of factor XII. Blood. 2013;122:3818-24.
Mitchell JL, Lionikiene AS, Georgiev G, Klemmer A, Brain C, Kim PY, et al. Polyphosphate colocalizes with factor XII on platelet-bound fibrin and augments its plasminogen activator activity. Blood. 2016;128:2834-45.
Gajsiewicz JM, Smith SA, Morrissey JH. Polyphosphate and RNA differentially modulate the contact pathway of blood clotting. J Biol Chem. 2017;292:1808-14.
Conway EM. Reincarnation of ancient links between coagulation and complement. J Thromb Haemost. 2015;13:S121-32.
Herwald H, Dedio J, Kellner R, Loos M, Muller-Esterl W. Isolation and characterization of the kininogen-binding protein p33 from endothelial cells. Identity with the gC1q receptor. J Biol Chem. 1996;271:13040-7.
Peerschke EI, Minta JO, Zhou SZ, Bini A, Gotlieb A, Colman RW, et al. Expression of gC1q-R/p33 and its major ligands in human atherosclerotic lesions. Mol Immunol. 2004;41:759-66.
Verschoor A, Neuenhahn M, Navarini AA, Graef P, Plaumann A, Seidlmeier A, et al. A platelet-mediated system for shuttling blood-borne bacteria to CD8alpha+ dendritic cells depends on glycoprotein GPIb and complement C3. Nat Immunol. 2011;12:1194-201.
Hamad OA, Ekdahl KN, Nilsson PH, Andersson J, Magotti P, Lambris JD, et al. Complement activation triggered by chondroitin sulfate released by thrombin receptor-activated platelets. J Thromb Haemost. 2008;6:1413-21.
Hamad OA, Back J, Nilsson PH, Nilsson B, Ekdahl KN. Platelets, complement, and contact activation: partners in inflammation and thrombosis. Adv Exp Med Bio. 2012;946:185-205.
Foreman KE, Vaporciyan AA, Bonish BK, Jones ML, Johnson KJ, Glovsky MM, et al. C5a-induced expression of P-selectin in endothelial cells. J Clin Invest. 1994;94:1147-55.
Wiedmer T, Esmon CT, Sims PJ. Complement proteins C5b-9 stimulate procoagulant activity through platelet prothrombinase. Blood. 1986;68:875-80.
Hamilton KK, Hattori R, Esmon CT, Sims PJ. Complement proteins C5b-9 induce vesiculation of the endothelial plasma membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J Bio Chem. 1990;265:3809-14.
Noris M, Remuzzi G. Atypical hemolytic-uremic syndrome. N Engl J Med. 2009;361:1676-87.
Hill A, Kelly RJ, Hillmen P. Thrombosis in paroxysmal nocturnal hemoglobinuria. Blood. 2013;121:4985-96.
Jokiranta TS. HUS and atypical HUS. Blood. 2017;129:2847-56.
Kozarcanin H, Lood C, Munthe-Fog L, Sandholm K, Hamad OA, Bengtsson AA, et al. The lectin complement pathway serine proteases (MASPs) represent a possible crossroad between the coagulation and complement systems in thromboinflammation. J Thromb Haemost. 2016;14:531-45.
Krarup A, Gulla KC, Gal P, Hajela K, Sim RB. The action of MBL-associated serine protease 1 (MASP1) on factor XIII and fibrinogen. Biochim Biophysic Acta. 2008;1784:1294-300.
La Bonte LR, Pavlov VI, Tan YS, Takahashi K, Takahashi M, Banda NK, et al. Mannose-binding lectin associated serine protease-1 is a significant contributor to coagulation in a murine model of occlusive thrombosis. J Immunol. 2012;188:885-91.
Jenny L, Dobo J, Gal P, Schroeder V. MASP-1 of the complement system promotes clotting via prothrombin activation. Mol Immunol. 2015;65:398-405.
Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost. 2006;4:295-306.
Garcia D, Erkan D. Diagnosis and management of the antiphospholipid syndrome. N Engl J Med. 2018;378:2010-21.
Galli M, Borrelli G, Jacobsen EM, Marfisi RM, Finazzi G, Marchioli R, et al. Clinical significance of different antiphospholipid antibodies in the WAPS (warfarin in the antiphospholipid syndrome) study. Blood. 2007;110:1178-83.
McNeil HP, Simpson RJ, Chesterman CN, Krilis SA. Anti-phospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: beta 2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci U S A. 1990;87:4120-4.
Arad A, Proulle V, Furie RA, Furie BC, Furie B. Beta(2)-Glycoprotein- 1 autoantibodies from patients with antiphospholipid syndrome are sufficient to potentiate arterial thrombus formation in a mouse model. Blood. 2011;117:3453-9.
Marciniak E, Romond EH. Impaired catalytic function of activated protein C: a new in vitro manifestation of lupus anticoagulant. Blood. 1989;74:2426-32.
Urbanus RT, de Laat B. Antiphospholipid antibodies and the protein C pathway. Lupus. 2010;19:394-9.
Liestol S, Sandset PM, Jacobsen EM, Mowinckel MC, Wisloff F. Decreased anticoagulant response to tissue factor pathway inhibitor type 1 in plasmas from patients with lupus anticoagulants. Br J Haematol. 2007;136:131-7.
Bu C, Gao L, Xie W, Zhang J, He Y, Cai G, et al. Beta2-glycoprotein I is a cofactor for tissue plasminogen activator mediated plasminogen activation. Arthritis Rheum. 2009;60:559-68.
Zhang J, McCrae KR. Annexin A2 mediates endothelial cell activation by antiphospholipid/antibeta2 glycoprotein I antibodies. Blood. 2005;105:1964-9.
Shi T, Giannakopoulos B, Yan X, Yu P, Berndt MC, Andrews RK, et al. Anti-beta2-glycoprotein I antibodies in complex with beta2-glycoprotein I can activate platelets in a dysregulated manner via glycoprotein Ib-IX-V. Arthritis Rheum. 2006;54:2558-67.
Sorice M, Longo A, Capozzi A, Garofalo T, Misasi R, Alessandri C, et al. Anti-beta2-glycoprotein I antibodies induce monocyte release of tumor necrosis factor alpha and tissue factor by signal transduction pathways involving lipid rafts. Arthritis Rheum. 2007;56:2687-97.
Chaturvedi S, Alluri R, McCrae KR. Extracellular vesicles in the antiphospholipid syndrome. Semin Thromb Hemost. 2018;44:493- 504.
Rand JH, Wu XX, Guller S, Gil J, Guha A, Scher J, et al. Reduction of annexin-V (placental anticoagulant protein-I) on placental villi of women with antiphospholipid antibodies and recurrent spontaneous abortion. Am J Obstet Gynecol. 1994;171:1566-72.
Pierangeli SS, Girardi G, Vega-Ostertag M, Liu X, Espinola RG, Salmon J. Requirement of activation of complement C3 and C5 for antiphospholipid antibody-mediated thrombophilia. Arthritis Rheum. 2005;52:2120-4.
Carrera-Marin A, Romay-Penabad Z, Papalardo E, Reyes-Maldonado E, Garcia-Latorre E, Vargas G, et al. C6 knock-out mice are protected from thrombophilia mediated by antiphospholipid antibodies. Lupus. 2012;21:1497-505.
Fischetti F, Durigutto P, Pellis V, Debeus A, Macor P, Bulla R, et al. Thrombus formation induced by antibodies to beta2-glycoprotein I is complement dependent and requires a priming factor. Blood. 2005;106:2340-6.
Agostinis C, Durigutto P, Sblattero D, Borghi MO, Grossi C, Guida F, et al. A non-complement-fixing antibody to beta2 glycoprotein I as a novel therapy for antiphospholipid syndrome. Blood. 2014;123:3478-87.
Girardi G, Berman J, Redecha P, Spruce L, Thurman JM, Kraus D, et al. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest. 2003;112:1644-54.
Girardi G, Redecha P, Salmon JE. Heparin prevents antiphospholipid antibody-induced fetal loss by inhibiting complement activation. Nat Med. 2004;10:1222-6.
Redecha P, Tilley R, Tencati M, Salmon JE, Kirchhofer D, Mackman N, et al. Tissue factor: a link between C5a and neutrophil activation in antiphospholipid antibody induced fetal injury. Blood. 2007;110:2423-31.
de Groot PG, Lutters B, Derksen RH, Lisman T, Meijers JC, Rosendaal FR. Lupus anticoagulants and the risk of a first episode of deep venous thrombosis. J Thromb Haemost. 2005;3:1993-7.
Galli M, Luciani D, Bertolini G, Barbui T. Lupus anticoagulants are stronger risk factors for thrombosis than anticardiolipin antibodies in the antiphospholipid syndrome: a systematic review of the literature. Blood. 2003;101:1827-32.
Pengo V, Ruffatti A, Legnani C, Testa S, Fierro T, Marongiu F, et al. Incidence of a first thromboembolic event in asymptomatic carriers of high-risk antiphospholipid antibody profile: a multicenter prospective study. Blood. 2011;118:4714-8.
Lee EY, Lee CK, Lee TH, Chung SM, Kim SH, Cho YS, et al. Does the anti-beta2-glycoprotein I antibody provide additional information in patients with thrombosis? Thromb Res. 2003;111:29-32.
Chaturvedi S, McCrae KR. Clinical risk assessment in the antiphospholipid syndrome: Current landscape and emerging biomarkers. Curr Rheumatol Rep. 2017;19:43.
Cervera R, Serrano R, Pons-Estel GJ, Ceberio-Hualde L, Shoenfeld Y, de Ramón E, et al. Morbidity and mortality in the antiphospholipid syndrome during a 10-year period: a multicentre prospective study of 1000 patients. Ann Rheum Dis. 2015;74:1011-8.
Legault K, Schunemann H, Hillis C, Yeung C, Akl EA, Carrier M, et al. McMaster RARE-Bestpractices clinical practice guideline on diagnosis and management of the catastrophic antiphospholipid syndrome. J Thromb Haemost. 2018;16:1-9.
Meroni PL, Macor P, Durigutto P, Maso LD, Gerosa M, Ferraresso M, et al. Complement activation in antiphospholipid syndrome and its inhibition to prevent rethrombosis after arterial surgery. Blood. 2016;127:365-7.
Shapira I, Andrade D, Allen SL, Salmon JE. Brief report: induction of sustained remission in recurrent catastrophic antiphospholipid syndrome via inhibition of terminal complement with eculizumab. Arthritis Rheum. 2012;64:2719-23.
Wig S, Chan M, Thachil J, Bruce I, Barnes T. A case of relapsing and refractory catastrophic antiphospholipid syndrome successfully managed with eculizumab, a complement 5 inhibitor. Rheumatology (Oxford). 2016;55:382-4.
Zikos TA, Sokolove J, Ahuja N, Berube C. Eculizumab induces sustained remission in a patient with refractory primary catastrophic antiphospholipid syndrome. J Clin Rheumatol. 2015;21:311-3.
Strakhan M, Hurtado-Sbordoni M, Galeas N, Bakirhan K, Alexis K, Elrafei T. 36-year-old female with catastrophic antiphospholipid syndrome treated with eculizumab: a case report and review of
literature. Case Rep Hematol. 2014;2014:704371.
Davis WD, Brey RL. Antiphospholipid antibodies and complement activation in patients with cerebral ischemia. Clin Exp Rheumatol. 1992;10:455-60.
Breen KA, Seed P, Parmar K, Moore GW, Stuart-Smith SE, Hunt BJ. Complement activation in patients with isolated antiphospholipid antibodies or primary antiphospholipid syndrome. Thromb Haemost. 2012;107:423-9.
Devreese KM, Hoylaerts MF. Is there an association between complement activation and antiphospholipid antibody-related thrombosis? Thromb Haemost. 2010;104:1279-81.
Oku K, Atsumi T, Bohgaki M, Amengual O, Kataoka H, Horita T, et al. Complement activation in patients with primary antiphospholipid syndrome. Ann Rheum Dis. 2009;68:1030-5.
Weiler H. Tracing the molecular pathogenesis of antiphospholipid syndrome. J Clin Invest. 2008;118:3276-8.
Redecha P, Franzke CW, Ruf W, Mackman N, Girardi G. Neutrophil activation by the tissue factor/Factor VIIa/PAR2 axis mediates fetal death in a mouse model of antiphospholipid syndrome. J Clin Invest. 2008;118,3453-61.
Weiler JM, Yurt RW, Fearon DT, Austen KF. Modulation of the formation of the amplification convertase of complement, C3b, Bb, by native and commercial heparin. J Exp Med. 1978;147:409-21.
Almeda S, Rosenberg R, Bing DH. The binding properties of human complement component C1q. Interaction with mucopolysaccharides. The Journal of Biological Chemistry. 1983;258:785-91.
Kulkarni PA, Afshar-Kharghan V. Anticomplement therapy. Biologics 2008;2:671-85.
Chaturvedi S, Braunstein EM, Yuan X, et al. Complement activity and complement regulatory gene mutations are associated with thrombosis in APS and CAPS. Blood 2020;135:239-51.
Bruserud O, Lundin K. The effect of drugs used in anticoagulation therapy on T lymphocyte activation in vitro. II. Warfarin inhibits T lymphocyte activation. J Clin Lab Immunol. 1987;23:169-73.
Lever R, Hoult JR, Page CP. The effects of heparin and related molecules upon the adhesion of human polymorphonuclear leucocytes to vascular endothelium in vitro. Brit J Pharmacol. 2000;129:533-40.
Ludwig RJ. Therapeutic use of heparin beyond anticoagulation. Curr Drug Discov Technol. 2009;6:281-9.
Zarychanski R, Abou-Setta AM, Kanji S, Turgeon AF, Kumar A, Houston DS, et al. The efficacy and safety of heparin in patients with sepsis: a systematic review and metaanalysis. Crit Care Med. 2015;43:511-8.
Jaimes F, De La Rosa G, Morales C, Fortich F, Arango C, Aguirre D, et al. Unfractioned heparin for treatment of sepsis: a randomized clinical trial (The HETRASE Study). Crit Care Med. 2009; 37:1185-96.
Bobek V, Kovarik J. Antitumor and antimetastatic effect of warfarin and heparins. Biomed Pharmacother. 2004;58:213-9.
Madan S, Shah S, Dale P, Partovi S, Parikh SA. Use of novel oral anticoagulant agents in venous thromboembolism. Cardiovasc Diag Therapy. 2016;6:570-81.
Dittmeier M, Kraft P, Schuhmann MK, Fluri F, Kleinschnitz C. Pretreatment with rivaroxaban attenuates stroke severity in rats by a dual antithrombotic and anti-inflammatory mechanism. Thromb Haemost. 2016;115:835-43.
Arachchillage DR, Mackie IJ, Efthymiou M, Chitolie A, Hunt BJ, Isenberg DA, et al. Rivaroxaban limits complement activation compared with warfarin in antiphospholipid syndrome patients with venous thromboembolism. J Thromb Haemost. 2016;14:2177- 86.
Dufrost V, Risse J, Reshetnyak T, Satybaldyeva M, Du Y, Yan XX, et al. Increased risk of thrombosis in antiphospholipid syndrome patients treated with direct oral anticoagulants. Results from an international patient-level data meta-analysis. Autoimmun Rev 2018;17:1011-21.
Pengo V, Denas G, Zoppellaro G, Jose SP, Hoxha A, Ruffatti A, et al. Rivaroxaban vs warfarin in high-risk patients with antiphospholipid syndrome. Blood. 2018;132:1365-71.
Arachchillage DRJ, Gomez K, Alikhan R, Anderson JAM, Lester W, Laffan M. Addendum to British Society for Haematology Guidelines on Investigation and Management of Antiphospholipid syndrome, 2012 (Br J Haematol. 2012;157:47-58): use of direct acting oral anticoagulants. Br J Haematol 2020 Jan 13. doi:10.1111/
bjh.16308. [Epub ahead of print].
Hill A, Dezern AE, Kinoshita T, Brodsky RA. Paroxysmal nocturnal haemoglobinuria. Nat Rev Dis Primers. 2017;3:17028.
Melis JP, Strumane K, Ruuls SR, Beurskens FJ, Schuurman J, Parren PW. Complement in therapy and disease: regulating the complement system with antibody-based therapeutics. Mol Immunol. 2015;67:117-30.
Sciascia S, Radin M, Yazdany J, Tektonidou M, Cecchi I, Roccatello D, et al. Expanding the therapeutic options for renal involvement in lupus: eculizumab, available evidence. Rheumatol Int. 2017;37:1249-55.
Weitz IC, Razavi P, Rochanda L, Zwicker J, Furie B, Manly D, et al. Eculizumab therapy results in rapid and sustained decreases in markers of thrombin generation and inflammation in patients with PNH independent of its effects on hemolysis and microparticle formation. Thromb Res. 2012;130:361-8.
Mastellos DC, Yancopoulou D, Kokkinos P, Huber-Lang M, Hajishengallis G, Biglarnia AR, et al. Compstatin: a C3-targeted complement inhibitor reaching its prime for bedside intervention. Eur J Clin Invest. 2015;45:423-40.
Ghebrehiwet B. The complement system: an evolution in progress. F1000Res. 2016;5:2840.
Harris CL. Expanding horizons in complement drug discovery: challenges and emerging strategies. Semin Immunopathol 2018;40:125-40.