Apolipoprotein A-I, elevated in trauma patients, inhibits platelet activation and decreases clot strength

References

• Chang R, Cardenas JC, Wade CE, Holcomb JB. Advances in the understanding of trauma-induced coagulopathy. Blood. 2016; 128(8): 1043–1049. doi: 10.1182/blood-2016-01-636423
   PubMed Web of Science ®Google Scholar
• Gonzalez E, Moore EE, Moore HB, Chapman MP, Silliman CC, Banerjee A. Trauma-induced coagulopathy: an Institution’s 35 year perspective on practice and research. Scand J Surg. 2014; 103(2): 89–103. doi: 10.1177/1457496914531927
   PubMed Web of Science ®Google Scholar
• Moore EE, Moore HB, Kornblith LZ, Neal MD, Hoffman M, Mutch NJ, Schöchl H, Hunt BJ, Sauaia A . Trauma-induced coagulopathy. Nat Rev Dis Primers 2021; 7(1):30. doi: 10.1038/s41572-021-00264-3
   PubMedGoogle Scholar
• Neal MD, Moore HB, Moore EE, Freeman, K., Cohen, M J., Sperry, J L., Zuckerbraun, B S., Park, M S., et al. Clinical assessment of trauma-induced coagulopathy and its contribution to postinjury mortality: a TACTIC proposal. J Trauma Acute Care Surg 2015; 79(3):490–492. doi: 10.1097/TA.0000000000000793
   PubMedGoogle Scholar
• Sumislawski JJ, Christie SA, Kornblith LZ, Stettler GR, Nunns GR, Moore HB, Moore EE, Silliman CC, Sauaia A, Callcut RA, et al. Discrepancies between conventional and viscoelastic assays in identifying trauma-induced coagulopathy. Am J Surg 2019; 217(6):1037–1041. doi: 10.1016/j.amjsurg.2019.01.014
   PubMed Web of Science ®Google Scholar
• Bohm JK, Schafer N, Maegele M, Stumpges B, Bauerfeind U, Caspers M. Plasmatic and cell-based enhancement by microparticles originated from platelets and endothelial cells under simulated in vitro conditions of a dilutional coagulopathy. Scand J Trauma Resusc Emerg Med. 2021; 29(1): 38. doi: 10.1186/s13049-021-00847-9
   PubMed Web of Science ®Google Scholar
• Brohi K, Cohen MJ, Davenport RA. Acute coagulopathy of trauma: mechanism, identification and effect. Curr Opin Crit Care. 2007; 13(6): 680–685. doi: 10.1097/MCC.0b013e3282f1e78f
   PubMed Web of Science ®Google Scholar
• Brohi K, Cohen MJ, Ganter MT, Schultz MJ, Levi M, Mackersie RC, Pittet J-F. Acute coagulopathy of trauma: hypoperfusion induces systemic anticoagulation and hyperfibrinolysis. J Trauma 2008; 64(5):1211–1217. doi: 10.1097/TA.0b013e318169cd3c
   PubMedGoogle Scholar
• Cotton BA, Harvin JA, Kostousouv V, Minei KM, Radwan ZA, Schöchl H, Wade CE, Holcomb JB, Matijevic N. Hyperfibrinolysis at admission is an uncommon but highly lethal event associated with shock and prehospital fluid administration. J Trauma Acute Care Surg 2012; 73(2):365–370. doi: 10.1097/TA.0b013e31825c1234
   PubMed Web of Science ®Google Scholar
• Davenport RA, Brohi K. Cause of trauma-induced coagulopathy. Curr Opin Anaesthesiol. 2016; 29(2): 212–219. doi: 10.1097/ACO.0000000000000295
   PubMed Web of Science ®Google Scholar
• Gando S, Shiraishi A, Wada T, Yamakawa K, Fujishima S, Saitoh D, Kushimoto S, Ogura H, Abe T, Otomo Y, et al. A multicenter prospective validation study on disseminated intravascular coagulation in trauma-induced coagulopathy. J Thromb Haemost 2020; 18(9):2232–2244. doi: 10.1111/jth.14931
   PubMed Web of Science ®Google Scholar
• Ives C, Inaba K, Branco BC, Okoye O, Schochl H, Talving P, Lam L, Shulman I, Nelson J, Demetriades D, et al. Hyperfibrinolysis elicited via thromboelastography predicts mortality in trauma. J Am Coll Surg 2012; 215(4):496–502. doi: 10.1016/j.jamcollsurg.2012.06.005
   PubMed Web of Science ®Google Scholar
• Schochl H, Frietsch T, Pavelka M, Jambor C. Hyperfibrinolysis after major trauma: differential diagnosis of lysis patterns and prognostic value of thrombelastometry. J Trauma. 2009; 67(1): 125–131. doi: 10.1097/TA.0b013e31818b2483
   PubMedGoogle Scholar
• Banerjee A, Silliman CC, Moore EE . Systemic hyperfibrinolysis after trauma: a pilot study of targeted proteomic analysis of superposed mechanisms in patient plasma. J Trauma Acute Care Surg 2018; 84(6):929–938. doi: 10.1097/TA.0000000000001878
   PubMed Web of Science ®Google Scholar
• D’Alessandro A, Moore HB, Moore EE, Reisz JA, Wither MJ, Ghasasbyan A, Chandler J, Silliman CC, Hansen KC, Banerjee A, et al. Plasma succinate is a predictor of mortality in critically injured patients. J Trauma Acute Care Surg 2017; 83(3):491–495. doi: 10.1097/TA.0000000000001565
   PubMed Web of Science ®Google Scholar
• D’Alessandro A, Nemkov T, Moore HB. Metabolomics of trauma-associated death: shared and fluid-specific features of human plasma vs lymph. Blood Transfus 2016; 14(2):185–194. doi: 10.2450/2016.0208-15
   PubMedGoogle Scholar
• Nunns GR, Vigneshwar N, Kelher MR . Succinate activation of SUCNR1 predisposes severely injured patients to neutrophil-mediated ARDS. Ann Surg. 2020; Publish Ahead of Print. doi: 10.1097/SLA.0000000000004644
   Google Scholar
• Albers JJ, Wahl PW, Cabana VG, Hazzard WR, Hoover JJ. Quantitation of apolipoprotein A-I of human plasma high density lipoprotein. Metab. 1976; 25(6): 633–644. doi: 10.1016/0026-0495(76)90060-3
   PubMed Web of Science ®Google Scholar
• Fisher EA, Feig JE, Hewing B, Hazen SL, Smith JD. High-density lipoprotein function, dysfunction, and reverse cholesterol transport. Arterioscler Thromb Vasc Biol. 2012; 32(12): 2813–2820. doi: 10.1161/ATVBAHA.112.300133
   PubMed Web of Science ®Google Scholar
• Bashtovyy D, Jones MK, Anantharamaiah GM, Segrest JP. Sequence conservation of apolipoprotein A-I affords novel insights into HDL structure-function. J Lipid Res. 2011; 52(3): 435–450. doi: 10.1194/jlr.R012658
   PubMed Web of Science ®Google Scholar
• Assanasen C, Mineo C, Seetharam D, Yuhanna IS, Marcel YL, Connelly MA, Williams DL, de la Llera-Moya M, Shaul PW, Silver DL, et al. Cholesterol binding, efflux, and a PDZ-interacting domain of scavenger receptor-BI mediate HDL-initiated signaling. J Clin Invest 2005; 115(4):969–977. doi: 10.1172/JCI23858
   PubMed Web of Science ®Google Scholar
• Brill A, Yesilaltay A, De Meyer SF, Kisucka J, Fuchs TA, Kocher O, Krieger M, Wagner DD. Extrahepatic high-density lipoprotein receptor SR-BI and apoA-I protect against deep vein thrombosis in mice. Arterioscler Thromb Vasc Biol 2012; 32(8):1841–1847. doi: 10.1161/ATVBAHA.112.252130
   PubMed Web of Science ®Google Scholar
• Saddar S, Mineo C, Shaul PW. Signaling by the high-affinity HDL receptor scavenger receptor B type I. Arterioscler Thromb Vasc Biol. 2010; 30(2): 144–150. doi: 10.1161/ATVBAHA.109.196170
   PubMed Web of Science ®Google Scholar
• van der Stoep M, Korporaal SJ, Van Eck M. High-density lipoprotein as a modulator of platelet and coagulation responses. Cardiovasc Res. 2014; 103(3): 362–371. doi: 10.1093/cvr/cvu137
   PubMed Web of Science ®Google Scholar
• Brodde MF, Korporaal SJ, Herminghaus G, Fobker M, Van Berkel TJC, Tietge UJF, Robenek H, Van Eck M, Kehrel BE, Nofer J-R, et al. Native high-density lipoproteins inhibit platelet activation via scavenger receptor BI: role of negatively charged phospholipids. Atherosclerosis 2011; 215(2):374–382. doi: 10.1016/j.atherosclerosis.2010.12.026
   PubMed Web of Science ®Google Scholar
• Calkin AC, Drew BG, Ono A, Duffy SJ, Gordon MV, Schoenwaelder SM, Sviridov D, Cooper ME, Kingwell BA, Jackson SP, et al. Reconstituted high-density lipoprotein attenuates platelet function in individuals with type 2 diabetes mellitus by promoting cholesterol efflux. Circ 2009; 120(21):2095–2104. doi: 10.1161/CIRCULATIONAHA.109.870709
   PubMed Web of Science ®Google Scholar
• Calzada C, Vericel E, Colas R, Guillot N, El Khoury G, Drai J, Sassolas A, Peretti N, Ponsin G, Lagarde M, et al. Inhibitory effects of in vivo oxidized high-density lipoproteins on platelet aggregation: evidence from patients with abetalipoproteinemia. FASEB J 2013; 27(7):2855–2861. doi: 10.1096/fj.12-225169
   PubMed Web of Science ®Google Scholar
• Valiyaveettil M, Kar N, Ashraf MZ, Byzova TV, Febbraio M, Podrez EA. Oxidized high-density lipoprotein inhibits platelet activation and aggregation via scavenger receptor BI. Blood. 2008; 111(4): 1962–1971. doi: 10.1182/blood-2007-08-107813
   PubMed Web of Science ®Google Scholar
• Wang N, Tall AR. Cholesterol in platelet biogenesis and activation. Blood. 2016; 127(16): 1949–1953. doi: 10.1182/blood-2016-01-631259
   PubMed Web of Science ®Google Scholar
• Branchford BR, Stalker TJ, Law L, Acevedo G, Sather S, Brzezinski C, Wilson KM, Minson K, Lee-Sherick AB, Davizon-Castillo P, et al. The small-molecule MERTK inhibitor UNC2025 decreases platelet activation and prevents thrombosis. J Thromb Haemost 2018; 16(2):352–363. doi: 10.1111/jth.13875
   PubMed Web of Science ®Google Scholar
• Neeves KB, Onasoga AA, Hansen RR, Lilly JJ, Venckunaite D, Sumner MB, Irish AT, Brodsky G, Manco-Johnson MJ, Di Paola JA, et al. Sources of variability in platelet accumulation on type 1 fibrillar collagen in microfluidic flow assays. PLoS One 2013; 8(1):e54680. doi: 10.1371/journal.pone.0054680
   PubMed Web of Science ®Google Scholar
• Wohlauer MV, Moore EE, Thomas S, Sauaia A, Evans E, Harr J, Silliman CC, Ploplis V, Castellino FJ, Walsh M, et al. Early platelet dysfunction: an unrecognized role in the acute coagulopathy of trauma. J Am Coll Surg 2012; 214(5):739–746. doi: 10.1016/j.jamcollsurg.2012.01.050
   PubMed Web of Science ®Google Scholar
• Chapman MP, Moore EE, Chin TL, Ghasabyan A, Chandler J, Stringham J, Gonzalez E, Moore HB, Banerjee A, Silliman CC, et al. Combat: initial experience with a randomized clinical trial of plasma-based resuscitation in the field for traumatic hemorrhagic shock. Shock 2015; 44(Suppl 1):63–70. doi: 10.1097/SHK.0000000000000376
   PubMedGoogle Scholar
• Moore HB, Moore EE, Chapman MP, Gonzalez E, Slaughter AL, Morton AP, D’Alessandro A, Hansen KC, Sauaia A, Banerjee A, et al. Viscoelastic measurements of platelet function, not fibrinogen function, predicts sensitivity to tissue-type plasminogen activator in trauma patients. J Thromb Haemost 2015; 13(10):1878–1887. doi: 10.1111/jth.13067
   PubMed Web of Science ®Google Scholar
• Moore HB, Moore EE, Chin TL, Gonzalez E, Chapman MP, Walker CB, Sauaia A, Banerjee A. Activated clotting time of thrombelastography (T-ACT) predicts early postinjury blood component transfusion beyond plasma. Surg 2014; 156(3):564–569. doi: 10.1016/j.surg.2014.04.017
   PubMed Web of Science ®Google Scholar
• Huang RS, McDonald MM, Wetzel JS. Clot strength as measured by thrombelastography correlates with platelet reactivity in stroke patients. Ann Clin Lab Sci. 2015; 45(3):301–307.
   PubMed Web of Science ®Google Scholar
• Lu D, Owens J, Kreutz RP. Plasma and whole blood clot strength measured by thrombelastography in patients treated with clopidogrel during acute coronary syndromes. Thromb Res. 2013; 132(2): e94–98. doi: 10.1016/j.thromres.2013.07.012
   PubMed Web of Science ®Google Scholar
• Harr JN, Moore EE, Ghasabyan A, Chin TL, Sauaia A, Banerjee A, Silliman CC. Functional fibrinogen assay indicates that fibrinogen is critical in correcting abnormal clot strength following trauma. Shock 2013; 39(1):45–49. doi: 10.1097/SHK.0b013e3182787122
   PubMed Web of Science ®Google Scholar
• Collyer TC, Gray DJ, Sandhu R, Berridge J, Lyons G. Assessment of platelet inhibition secondary to clopidogrel and aspirin therapy in preoperative acute surgical patients measured by thrombelastography platelet mapping. Br J Anaesth. 2009; 102(4): 492–498. doi: 10.1093/bja/aep039
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9(7): 671–675. doi: 10.1038/nmeth.2089
   PubMed Web of Science ®Google Scholar
• Naik MU, Stalker TJ, Brass LF, Naik UP. JAM-A protects from thrombosis by suppressing integrin alphaIIbbeta3-dependent outside-in signaling in platelets. Blood. 2012; 119(14): 3352–3360. doi: 10.1182/blood-2011-12-397398
   PubMed Web of Science ®Google Scholar
• O’Brien KA, Stojanovic-Terpo A, Hay N, Du X. An important role for Akt3 in platelet activation and thrombosis. Blood. 2011; 118(15): 4215–4223. doi: 10.1182/blood-2010-12-323204
   PubMed Web of Science ®Google Scholar
• Westrick RJ, Winn ME, Eitzman DT. Murine models of vascular thrombosis (Eitzman series). Arterioscler Thromb Vasc Biol. 2007; 27(10): 2079–2093. doi: 10.1161/ATVBAHA.107.142810
   PubMed Web of Science ®Google Scholar
• Sather S, Kenyon KD, Lefkowitz JB, Liang X, Varnum BC, Henson PM, Graham DK. A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation. Blood 2007; 109(3):1026–1033. doi: 10.1182/blood-2006-05-021634
   PubMed Web of Science ®Google Scholar
• Chapman MP, Moore EE, Moore HB. The “Death diamond”: rapid thrombelastography identifies lethal hyperfibrinolysis. J Trauma Acute Care Surg 2015; 79(6):925–929. doi: 10.1097/TA.0000000000000871
   PubMed Web of Science ®Google Scholar
• Chapman MP, Moore EE, Ramos CR. Fibrinolysis greater than 3% is the critical value for initiation of antifibrinolytic therapy. J Trauma Acute Care Surg. 2013; 75(6):961–967. discussion 967. doi: 10.1097/TA.0b013e3182aa9c9f
   PubMed Web of Science ®Google Scholar
• Gonzalez E, Moore EE, Moore HB, Chapman MP, Chin TL, Ghasabyan A, Wohlauer MV, Barnett CC, Bensard DD, Biffl WL, et al. Goal-directed hemostatic resuscitation of trauma-induced coagulopathy: a pragmatic randomized clinical trial comparing a viscoelastic assay to conventional coagulation assays. Ann Surg 2016; 263(6):1051–1059. doi: 10.1097/SLA.0000000000001608
   PubMed Web of Science ®Google Scholar
• Zabczyk M, Hondo L, Krzek M, Undas A. High-density cholesterol and apolipoprotein AI as modifiers of plasma fibrin clot properties in apparently healthy individuals. Blood Coagul Fibrinolysis. 2013; 24(1): 50–54. doi: 10.1097/MBC.0b013e32835a083c
   PubMed Web of Science ®Google Scholar
• Durrant TN, van den Bosch MT, Hers I. Integrin alphaIIbbeta3 outside-in signaling. Blood. 2017; 130(14): 1607–1619. doi: 10.1182/blood-2017-03-773614
   PubMed Web of Science ®Google Scholar
• Li Z, Delaney MK, O’Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol. 2010; 30(12): 2341–2349. doi: 10.1161/ATVBAHA.110.207522
   PubMed Web of Science ®Google Scholar
• Zou Z, Chen H, Schmaier AA, Hynes RO, Kahn ML. Structure-function analysis reveals discrete beta3 integrin inside-out and outside-in signaling pathways in platelets. Blood. 2007; 109(8): 3284–3290. doi: 10.1182/blood-2006-10-051664
   PubMed Web of Science ®Google Scholar
• Ginsberg MH, Du X, Plow EF. Inside-out integrin signalling. Curr Opin Cell Biol. 1992; 4(5): 766–771. doi: 10.1016/0955-0674(92)90099-X
   PubMedGoogle Scholar
• Pienimaeki-Roemer A, Fischer A, Tafelmeier M, Orsó E, Konovalova T, Böttcher A, Liebisch G, Reidel A, Schmitz G. High-density lipoprotein 3 and apolipoprotein A-I alleviate platelet storage lesion and release of platelet extracellular vesicles. Transfusion 2014; 54(9):2301–2314. doi: 10.1111/trf.12640
   PubMed Web of Science ®Google Scholar
• Barry FA, Gibbins JM. Protein kinase B is regulated in platelets by the collagen receptor glycoprotein VI. J Biol Chem. 2002; 277(15): 12874–12878. doi: 10.1074/jbc.M200482200
   PubMed Web of Science ®Google Scholar
• Cho MJ, Pestina TI, Steward SA, Lowell CA, Jackson CW, Gartner TK. Role of the Src family kinase Lyn in TxA2 production, adenosine diphosphate secretion, Akt phosphorylation, and irreversible aggregation in platelets stimulated with gamma-thrombin. Blood. 2002; 99(7): 2442–2447. doi: 10.1182/blood.V99.7.2442
   PubMed Web of Science ®Google Scholar
• Kim S, Jin J, Kunapuli SP. Akt activation in platelets depends on Gi signaling pathways. J Biol Chem. 2004; 279(6): 4186–4195. doi: 10.1074/jbc.M306162200
   PubMed Web of Science ®Google Scholar
• Chung DW, Chen J, Ling M, Fu X, Blevins T, Parsons S, Le J, Harris J, Martin TR, Konkle BA, et al. High-density lipoprotein modulates thrombosis by preventing von Willebrand factor self-association and subsequent platelet adhesion. Blood 2016; 127(5):637–645. doi: 10.1182/blood-2014-09-599530
   PubMed Web of Science ®Google Scholar
• Deguchi H, Pecheniuk NM, Elias DJ, Averell PM, Griffin JH. High-density lipoprotein deficiency and dyslipoproteinemia associated with venous thrombosis in men. Circ. 2005; 112(6): 893–899. doi: 10.1161/CIRCULATIONAHA.104.521344
   PubMed Web of Science ®Google Scholar
• Li D, Weng S, Yang B. Inhibition of arterial thrombus formation by ApoA1 Milano. Arterioscler Thromb Vasc Biol 1999; 19(2):378–383. doi: 10.1161/01.ATV.19.2.378
   PubMed Web of Science ®Google Scholar
• Henson D, Tahhan AS, Nardo D, Quyyumi AA, Venditto VJ. Association between ApoA-I (Apolipoprotein A-I) immune complexes and adverse cardiovascular events-brief report. Arterioscler Thromb Vasc Biol. 2019; 39(9): 1884–1892. doi: 10.1161/ATVBAHA.119.312964
   PubMed Web of Science ®Google Scholar
• Ng DS, Vezina C, Wolever TS, Kuksis A, Hegele RA, Connelly PW. Apolipoprotein A-I deficiency. Biochemical and metabolic characteristics. Arterioscler Thromb Vasc Biol. 1995; 15(12): 2157–2164. doi: 10.1161/01.ATV.15.12.2157
   PubMed Web of Science ®Google Scholar
• Rubin EM, Krauss RM, Spangler EA, Verstuyft JG, Clift SM. Inhibition of early atherogenesis in transgenic mice by human apolipoprotein AI. Nat. 1991; 353(6341): 265–267. doi: 10.1038/353265a0
   Google Scholar
• Barrett TJ, Distel E, Murphy AJ, Hu J, Garshick MS, Ogando Y, Liu J, Vaisar T, Heinecke JW, Berger JS, et al. Apolipoprotein AI) promotes atherosclerosis regression in diabetic mice by suppressing myelopoiesis and plaque inflammation. Circ 2019; 140(14):1170–1184. doi: 10.1161/CIRCULATIONAHA.119.039476
   PubMed Web of Science ®Google Scholar
• Beviglia L, Poggi A, Rossi C, McLane MA, Calabrese R, Scanziani E, Cook JJ, Niewiarowski S. Mouse antithrombotic assay. Inhibition of platelet thromboembolism by disintegrins. Thromb Res 1993; 71(4):301–315. doi: 10.1016/0049-3848(93)90199-X
   PubMed Web of Science ®Google Scholar
• Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, et al. Heart disease and stroke statistics-2017 update: a report from the American Heart Association. Circ 2017; 135(10):e146–e603. doi: 10.1161/CIR.0000000000000485
   PubMed Web of Science ®Google Scholar
• Ageno W, Becattini C, Brighton T, Selby R, Kamphuisen PW. Cardiovascular risk factors and venous thromboembolism: a meta-analysis. Circ. 2008; 117(1): 93–102. doi: 10.1161/CIRCULATIONAHA.107.709204
   PubMed Web of Science ®Google Scholar
• Doggen CJ, Smith NL, Lemaitre RN, Heckbert SR, Rosendaal FR, Psaty BM. Serum lipid levels and the risk of venous thrombosis. Arterioscler Thromb Vasc Biol. 2004; 24(10): 1970–1975. doi: 10.1161/01.ATV.0000143134.87051.46
   PubMed Web of Science ®Google Scholar
• Eichinger S, Pecheniuk NM, Hron G. High-density lipoprotein and the risk of recurrent venous thromboembolism. Circ 2007; 115(12):1609–1614. doi: 10.1161/CIRCULATIONAHA.106.649954
   PubMed Web of Science ®Google Scholar
• Sacks FM, Rudel LL, Conner A. Selective delipidation of plasma HDL enhances reverse cholesterol transport in vivo. J Lipid Res 2009; 50(5):894–907. doi: 10.1194/jlr.M800622-JLR200
   PubMed Web of Science ®Google Scholar
• Yamashita S, Tsubakio-Yamamoto K, Ohama T, Nakagawa-Toyama Y, Nishida M. Molecular mechanisms of HDL-cholesterol elevation by statins and its effects on HDL functions. J Atheroscler Thromb. 2010; 17(5): 436–451. doi: 10.5551/jat.5405
   PubMed Web of Science ®Google Scholar
• Naqvi TZ, Shah PK, Ivey PA, Molloy MD, Thomas AM, Panicker S, Ahmed A, Cercek B, Kaul S. Evidence that high-density lipoprotein cholesterol is an independent predictor of acute platelet-dependent thrombus formation. Am J Cardiol 1999; 84(9):1011–1017. doi: 10.1016/S0002-9149(99)00489-0
   PubMed Web of Science ®Google Scholar