Evidence of platelet activation at medically used hypothermia and mechanistic data indicating ADP as a key mediator and therapeutic target

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 7, 2011, Pages 1607-1616

  Straub, Andreas ^a,b   Krajewski, Stefanie ^a,b   Hohmann, Jan David ^a   Westein, Erik ^c   Jia, Fu ^a   Bassler, Nicole ^a   Selan, Carly ^d   Kurz, Julia ^b   Wendel, Hans Peter ^b   Dezfouli, Shala ^d   Yuan, Yuping ^c   Nandurkar, Harshal ^d   Jackson, Shaun ^c   Hickey, Michael J ^c   Peter, Karlheinz ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c MONASH UNIVERSITY   (Australia)

^d ST VINCENT S HOSPITAL   (Australia)

Author keywords

ADP; CD39; hypothermia; platelet receptor blockers; platelets

Indexed keywords

2 MESAMP; 2' DEOXY 6 N METHYLADENOSINE 3',5' BISPHOSPHATE; ADENOSINE DIPHOSPHATE; CANGRELOR; CD39 ANTIGEN; ECTO NUCLEOSIDE TRIPHOSPHATE DIPHOSPHOHYDROLASE 1; FIBRINOGEN; GLYCOPROTEIN IB ALPHA; HYDROLASE; PADGEM PROTEIN; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; RECOMBINANT ANTIGEN; SOLUBLE CD39; TIROFIBAN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICOAGULATION; ARTERY THROMBOSIS; ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; ENZYME ACTIVITY; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; IN VIVO STUDY; INDUCED HYPOTHERMIA; LEUKOCYTE; LEUKOPENIA; MESENTERIC ARTERY; MICROSCOPY; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RECEPTOR BLOCKING; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTOPENIA; THROMBOGENESIS;

ADENOSINE DIPHOSPHATE; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; APYRASE; BLOOD PLATELETS; FIBRINOGEN; FIBRINOLYTIC AGENTS; HUMANS; HYDROLYSIS; HYPOTHERMIA, INDUCED; LEUKOPENIA; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; P-SELECTIN; PLATELET ACTIVATION; PLATELET ADHESIVENESS; PLATELET AGGREGATION INHIBITORS; PURINERGIC P2Y RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2Y1; RECEPTORS, PURINERGIC P2Y12; RECOMBINANT PROTEINS; THROMBOCYTOPENIA; THROMBOSIS; VON WILLEBRAND FACTOR;

EID: 79959770145     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.226373     Document Type: Article

References (57)

1. Bigelow WG, Lindsay WK, Harrison RC, Gordon RA, Greenwood WF. Oxygen transport and utilization in dogs at low body temperatures. Am J Physiol. 1950;160:125-137.
2. Gott VL. Lillehei, Lewis, and Wangensteen: the right mix for giant achievements in cardiac surgery. Ann Thorac Surg. 2005;79: S2210-S2213. (Pubitemid 40804235)
3. Foltan M, Philipp A, Birnbaum D. Extended use of ECC. Perfusion. 2007;22:173-178. (Pubitemid 350018038)
4. Xavier RG, White AE, Fox SC, Wilcox RG, Heptinstall S. Enhanced platelet aggregation and activation under conditions of hypothermia. Thromb Haemost. 2007;98:1266-1275. (Pubitemid 350252857)
5. Kim F, Olsufka M, Longstreth WT Jr, Maynard C, Carlbom D, Deem S, Kudenchuk P, Copass MK, Cobb LA. Pilot randomized clinical trial of prehospital induction of mild hypothermia in out-of-hospital cardiac arrest patients with a rapid infusion of 4 degrees C normal saline. Circulation. 2007;115:3064-3070. (Pubitemid 46956495)
6. Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med. 2002;346:557-563. (Pubitemid 34438816)
7. Lindenblatt N, Menger MD, Klar E, Vollmar B. Sustained hypothermia accelerates microvascular thrombus formation in mice. Am J Physiol Heart Circ Physiol. 2005;289:H2680-H2687. (Pubitemid 41698585)
8. Faraday N, Rosenfeld BA. In vitro hypothermia enhances platelet GPIIb-IIIa activation and P-selectin expression. Anesthesiology. 1998;88: 1579-1585. (Pubitemid 28283791)
9. Hall MW, Goodman PD, Alston SM, Solen KA. Hypothermia-induced platelet aggregation in heparinized flowing human blood: identification of a high responder subpopulation. Am J Hematol. 2002;69:45-55.
10. Straub A, Breuer M, Wendel HP, Peter K, Dietz K, Ziemer G. Critical temperature ranges of hypothermia-induced platelet activation: possible implications for cooling patients in cardiac surgery. Thromb Haemost. 2007;97:608-616. (Pubitemid 46592939)
11. Straub A, Schiebold D, Wendel HP, Hamilton C, Wagner T, Schmid E, Dietz K, Ziemer G. Using reagent-supported thromboelastometry (ROTEM((R))) to monitor haemostatic changes in congenital heart surgery employing deep hypothermic circulatory arrest. Eur J Cardiothorac Surg. 2008;34:641-647.
12. Villalobos TJ, Adelson E, Riley PA Jr, Crosby WH. A cause of the thrombocytopenia and leukopenia that occur in dogs during deep hypothermia. J Clin Invest. 1958;37:1-7.
13. Wilde JT. Hematological consequences of profound hypothermic circulatory arrest and aortic dissection. J Card Surg. 1997;12:201-206.
14. Weinberg AD. Hypothermia. Ann Emerg Med. 1993;22:370-377. (Pubitemid 23068454)
15. Harker LA, Malpass TW, Branson HE, Hessel EA II, Slichter SJ. Mechanism of abnormal bleeding in patients undergoing cardiopulmonary bypass: acquired transient platelet dysfunction associated with selective+-granule release. Blood. 1980;56:824-834. (Pubitemid 11242975)
16. Hauty MG, Esrig BC, Hill JG, Long WB. Prognostic factors in severe accidental hypothermia: experience from the Mt. Hood tragedy. J Trauma. 1987;27:1107-1112. (Pubitemid 18005105)
17. Savides EP, Hoffbrand BI. Hypothermia, thrombosis, and acute pancreatitis. BMJ. 1974;1:614.
18. Hoffmeister KM, Felbinger TW, Falet H, Denis CV, Bergmeier W, Mayadas TN, von Andrian UH, Wagner DD, Stossel TP, Hartwig JH. The clearance mechanism of chilled blood platelets. Cell. 2003;112:87-97. (Pubitemid 36106421)
19. Andrews RK, Berndt MC. Platelet physiology: in cold blood. Curr Biol. 2003;13:R282-284. (Pubitemid 36391928)
20. Hall MW, Hopkins RO, Long JW, Mohammad SF, Solen KA. Hypothermia-induced platelet aggregation and cognitive decline in coronary artery bypass surgery: a pilot study. Perfusion. 2005;20: 157-167. (Pubitemid 40975734)
21. Ranucci M, Carlucci C, Isgro G, Brozzi S, Boncilli A, Costa E, Frigiola A. Hypothermic cardiopulmonary bypass as a determinant of late thrombocytopenia following cardiac operations in pediatric patients. Acta Anaesthesiol Scand. 2009;53:1060-1067.
22. Augoustides JG. Fatal intraoperative thrombosis in contemporary adult thoracic aortic surgery requiring deep hypothermic circulatory arrest: observations from the literature, 1993-2006. J Thorac Cardiovasc Surg. 2007;134:1069-1070. (Pubitemid 47454623)
23. Jackson SP. The growing complexity of platelet aggregation. Blood. 2007;109:5087-5095. (Pubitemid 46890522)
24. Gawaz M, Neumann FJ, Schomig A. Evaluation of platelet membrane glycoproteins in coronary artery disease: consequences for diagnosis and therapy. Circulation. 1999;99:E1-E11.
25. Sachs UJ, Nieswandt B. In vivo thrombus formation in murine models. Circ Res. 2007;100:979-991. (Pubitemid 46598922)
26. Goschnick MW, Lau LM, Wee JL, Liu YS, Hogarth PM, Robb LM, Hickey MJ, Wright MD, Jackson DE. Impaired "outside-in" integrin+Iib+3 signaling and thrombus stability in TSSC6-deficient mice. Blood. 2006;108:1911-1918. (Pubitemid 44395000)
27. Straub A, Wendel HP, Dietz K, Schiebold D, Peter K, Schoenwaelder SM, Ziemer G. Selective inhibition of the platelet phosphoinositide 3-kinase p110+ as promising new strategy for platelet protection during extracorporeal circulation. Thromb Haemost. 2008;99:609-615. (Pubitemid 351549299)
28. Heptinstall S, Johnson A, Glenn JR, White AE. Adenine nucleotide metabolism in human blood: important roles for leukocytes and erythrocytes. J Thromb Haemost. 2005;3:2331-2339. (Pubitemid 41727214)
29. Robson SC, Sevigny J, Zimmermann H. The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal. 2006;2:409-430.
30. Bassler N, Loeffler C, Mangin P, Yuan Y, Schwarz M, Hagemeyer CE, Eisenhardt SU, Ahrens I, Bode C, Jackson SP, Peter K. A mechanistic model for paradoxical platelet activation by ligand-mimetic+IIb+3 (GPIIb/IIIa) antagonists. Arterioscler Thromb Vasc Biol. 2007;27: e9-e15.
31. Kulkarni S, Nesbitt WS, Dopheide SM, Hughan SC, Harper IS, Jackson SP. Techniques to examine platelet adhesive interactions under flow. Methods Mol Biol. 2004;272:165-186.
32. Gorman MW, Marble DR, Ogimoto K, Feigl EO. Measurement of adenine nucleotides in plasma. Luminescence. 2003;18:173-181. (Pubitemid 40326831)
33. Massberg S, Brand K, Gruner S, Page S, Muller E, Muller I, Bergmeier W, Richter T, Lorenz M, Konrad I, Nieswandt B, Gawaz M. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med. 2002;196:887-896.
34. Berndt MC, Karunakaran D, Gardiner EE, Andrews RK. Programmed autologous cleavage of platelet receptors. J Thromb Haemost. 5(suppl 1): 212-219, 2007. (Pubitemid 46958836)
35. Bhatt DL, Topol EJ. Scientific and therapeutic advances in antiplatelet therapy. Nat Rev Drug Discov. 2003;2:15-28. (Pubitemid 37361621)
36. Gayle RB III, Maliszewski CR, Gimpel SD, Schoenborn MA, Caspary RG, Richards C, Brasel K, Price V, Drosopoulos JH, Islam N, Alyonycheva TN, Broekman MJ, Marcus AJ. Inhibition of platelet function by recombinant soluble ecto-ADPase/CD39. J Clin Invest. 1998;101: 1851-1859. (Pubitemid 28226103)
37. Coade SB, Pearson JD. Metabolism of adenine nucleotides in human blood. Circ Res. 1989;65:531-537. (Pubitemid 19226429)
38. Valles J, Santos MT, Aznar J, Marcus AJ, Martinez-Sales V, Portoles M, Broekman MJ, Safier LB. Erythrocytes metabolically enhance collageninduced platelet responsiveness via increased thromboxane production, adenosine diphosphate release, and recruitment. Blood. 1991;78: 154-162.
39. Banz Y, Beldi G, Wu Y, Atkinson B, Usheva A, Robson SC. CD39 is incorporated into plasma microparticles where it maintains functional properties and impacts endothelial activation. Br J Haematol. 2008;142: 627-637. (Pubitemid 352020213)
40. Meadows TA, Bhatt DL. Clinical aspects of platelet inhibitors and thrombus formation. Circ Res. 2007;100:1261-1275. (Pubitemid 46742917)
41. Fugate SE, Cudd LA. Cangrelor for treatment of coronary thrombosis. Ann Pharmacother. 2006;40:925-930. (Pubitemid 43765010)
42. Woulfe D, Yang J, Brass L. ADP and platelets: the end of the beginning. J Clin Invest. 2001;107:1503-1505. (Pubitemid 32574635)
43. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol. 2010;30: 2341-2349.
44. Hansen TN, Brockbank KG. Increased platelet aggregation due to chilling to 20 degrees C is not related to increased sensitivity to agonists. Transfusion. 1997;37:696-702. (Pubitemid 27297608)
45. Brown CH III, Leverett LB, Lewis CW, Alfrey CP Jr, Hellums JD. Morphological, biochemical, and functional changes in human platelets subjected to shear stress. J Lab Clin Med. 1975;86:462-471.
46. Reimers RC, Sutera SP, Joist JH. Potentiation by red blood cells of shear-induced platelet aggregation: relative importance of chemical and physical mechanisms. Blood. 1984;64:1200-1206. (Pubitemid 15224530)
47. Hall MW, Goodman PD, Solen KA, Mohammad SF. Formation of occlusive platelet aggregates in whole blood caused by low concentrations of ADP. Asaio J. 2000;46:693-695.
48. Drosopoulos JH, Kraemer R, Shen H, Upmacis RK, Marcus AJ, Musi E. Human solCD39 inhibits injury-induced development of neointimal hyperplasia. Thromb Haemost. 2010;103:426-434.
49. Belayev L, Khoutorova L, Deisher TA, Belayev A, Busto R, Zhang Y, Zhao W, Ginsberg MD. Neuroprotective effect of SolCD39, a novel platelet aggregation inhibitor, on transient middle cerebral artery occlusion in rats. Stroke. 2003;34:758-763. (Pubitemid 36307407)
50. Alty JE, Ford HL. Multi-system complications of hypothermia: a case of recurrent episodic hypothermia with a review of the pathophysiology of hypothermia. Postgrad Med J. 2008;84:282-286.
51. Schneider DJ, Taatjes DJ, Sobel BE. Paradoxical inhibition of fibrinogen binding and potentiation of-granule release by specific types of inhibitors of glycoprotein IIb-IIIa. Cardiovasc Res. 2000;45:437-446.
52. Mossad EB, Machado S, Apostolakis J. Bleeding following deep hypothermia and circulatory arrest in children. Semin Cardiothorac Vasc Anesth. 2007;11:34-46. (Pubitemid 46280506)
53. Rajagopalan S, Mascha E, Na J, Sessler DI. The effects of mild perioperative hypothermia on blood loss and transfusion requirement. Anesthesiology. 2008;108:71-77.
54. Paparella D, Brister SJ, Buchanan MR. Coagulation disorders of cardiopulmonary bypass: a review. Intensive Care Med. 2004;30:1873-1881. (Pubitemid 39468407)
55. Polderman KH. Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med. 2009;37:S186-S202.
56. Shimokawa M, Kitaguchi K, Kawaguchi M, Sakamoto T, Kakimoto M, Furuya H. The influence of induced hypothermia for hemostatic function on temperature-adjusted measurements in rabbits. Anesth Analg. 2003; 96:1209-1213. (Pubitemid 36359069)
57. Romlin B, Petruson K, Nilsson K. Moderate superficial hypothermia prolongs bleeding time in humans. Acta Anaesthesiol Scand. 2007;51: 198-201. (Pubitemid 46143924)