An activation-specific platelet inhibitor that can be turned on/off by medically used hypothermia

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 9, 2011, Pages 2015-2023

  Topcic, Denijal ^a   Kim, Wookhyun ^b,c   Holien, Jessica K ^d   Jia, Fu ^a   Armstrong, Paul C ^a   Hohmann, Jan David ^a   Straub, Andreas ^a   Krippner, Guy ^a   Haller, Carolyn A ^b,c   Domeij, Helena ^a   Hagemeyer, Christoph E ^a   Parker, Michael W ^d,e   Chaikof, Elliot L ^b,c   Peter, Karlheinz ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b EMORY UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

antibodies; antiplatelet drugs; hypothermia; platelet receptor blockers; thrombosis

Indexed keywords

ELASTIN MIMETIC POLYPEPTIDE; GLYCOPROTEIN IIB ANTIBODY; GLYCOPROTEIN IIIA ANTIBODY; POLYPEPTIDE; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY TEMPERATURE; CAROTID ARTERY THROMBOSIS; CIRCULAR DICHROISM; FLOW CYTOMETRY; HEART SURGERY; INDUCED HYPOTHERMIA; JUGULAR VEIN THROMBOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; VEIN THROMBOSIS;

ANIMALS; CIRCULAR DICHROISM; CORONARY ARTERY BYPASS; FIBRINOGEN; HUMANS; HYPOTHERMIA, INDUCED; MICE; MODELS, MOLECULAR; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES; TROPOELASTIN;

EID: 80052159187     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.226241     Document Type: Article

References (70)

1. Mackman N. Triggers, targets and treatments for thrombosis. Nature. 2008;451:914-918.
2. Toyoda K, Yasaka M, Iwade K, Nagata K, Koretsune Y, Sakamoto T, Uchiyama S, Gotoh J, Nagao T, Yamamoto M, Takahashi JC, Minematsu K. Dual antithrombotic therapy increases severe bleeding events in patients with stroke and cardiovascular disease: a prospective, multicenter, observational study. Stroke. 2008;39:1740-1745.
3. Johnson S. Known knowns and known unknowns: risks associated with combination antithrombotic therapy. Thromb Res. 2008;123(suppl 1): S7-S11.
4. Levi MM, Eerenberg E, Lowenberg PW, Kamphuisen PW. Bleeding in patients using new anticoagulants or antiplatelet agents: risk factors and management. Neth J Med. 2010;68:68-76.
5. Straub A, Wendel HP, Dietz K, Schiebold D, Peter K, Schoenwaelder SM, Ziemer G. Selective inhibition of the platelet phosphoinositide 3-kinase p110βas promising new strategy for platelet protection during extracorporeal circulation. Thromb Haemost. 2008;99:609-615. (Pubitemid 351549299)
6. Alzaga AG, Cerdan M, Varon J. Therapeutic hypothermia. Resuscitation. 2006;70:369-380. (Pubitemid 44389720)
7. Auler JOC. Hypothermia in cardiac surgery. Anaesthesia, Pain, Intensive Care and Emergency Medicine. 2005;6:495-506.
8. Campos JM, Paniagua P. Hypothermia during cardiac surgery. Best Pract Res Clin Anaesthesiol. 2008;22:695-709.
9. 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)
10. Immer FF, Lippeck C, Barmettler H, Berdat PA, Eckstein FS, Kipfer B, Saner H, Schmidli J, Carrel TP. Improvement of quality of life after surgery on the thoracic aorta: effect of antegrade cerebral perfusion and short duration of deep hypothermic circulatory arrest. Circulation. 2004;110:II250-II255. (Pubitemid 39263731)
11. Choi R, Andres RH, Steinberg GK, Guzman R. Intraoperative hypothermia during vascular neurosurgical procedures. Neurosurg Focus. 2009;26:E24.
12. Zhang JN, Wood J, Bergeron AL, McBride L, Ball C, Yu Q, Pusiteri AE, Holcomb JB, Dong JF. Effects of low temperature on shear-induced platelet aggregation and activation. J Trauma. 2004;57:216-223. (Pubitemid 39166768)
13. Hall MW, Hopkins RO, Long JW, Mohammad SF, Solen KA. Hypothermiainduced platelet aggregation and cognitive decline in coronary artery bypass surgery: a pilot study. Perfusion. 2005;20:157-167. (Pubitemid 40975734)
14. 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.
15. 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)
16. 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)
17. 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)
18. Faraday N, Rosenfeld BA. In vitro hypothermia enhances platelet GPIIb-IIIa activation and P-selectin expression. Anesthesiology. 1998;88: 1579-1585. (Pubitemid 28283791)
19. Augostides JG. Fatal intraoperative thrombosis in contemporary adult thoracic aortic surgery requiring deep hypothermic circulatory arrest: observations from the literature, 1993-2006. Thorac Cardiovasc Surg. 2007;134:1069-1070.
20. 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.
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. Paparella D, Brister SJ, Buchanan MR. Coagulation disorders of cardiopulmonary bypass: a review. Intensive Care Med. 2004;30:1873-1881. (Pubitemid 39468407)
23. 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.
24. Coller BS, Shattil SJ. The GPIIb/IIIa (integrinαIIbβ3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood. 2008;112:3011-3025.
25. Schror K, Weber AA. Comparative pharmacology of GP IIb/IIIa antagonists. J Thromb Thrombolysis. 2003;15:71-80. (Pubitemid 37498175)
26. Dyke CM, Bhatia D, Lorenz TJ, Marso SP, Tardiff BE, Hogeboom C, Harrington RA. Immediate coronary artery bypass surgery after platelet inhibition with eptifibatide: results from PURSUIT: Platelet Glycoprotein IIb/IIIa in Unstable Angina: Receptor Suppression Using Integrelin Therapy. Ann Thorac Surg. 2000;70:866-871; discussion 871-862.
27. Genoni M, Zeller D, Bertel O, Maloigne M, Turina M. Tirofiban therapy does not increase the risk of hemorrhage after emergency coronary surgery. J Thorac Cardiovasc Surg. 2001;122:630-632. (Pubitemid 32843976)
28. Coller BS. Anti-GPIIb/IIIa drugs: current strategies and future directions. Thromb Haemost. 2001;86:427-443. (Pubitemid 32663972)
29. Bhatt DL, Topol EJ. Scientific and therapeutic advances in antiplatelet therapy. Nat Rev Drug Discov. 2003;2:15-28. (Pubitemid 37361621)
30. Boeken U, Litmathe J, Kurt M, Feindt P, Gams E. CABG-procedures in patients with pretreatment with the GPIIb/IIIa-receptor antagonist tirofiban (Aggrastat): modification of perioperative management? Int J Cardiol. 2008;127:257-259. (Pubitemid 351787773)
31. Schwarz M, Meade G, Stoll P, Ylanne J, Bassler N, Chen YC, Hagemeyer CE, Ahrens I, Moran N, Kenny D, Fitzgerald D, Bode C, Peter K. Conformationspecific blockade of the integrin GPIIb/IIIa: a novel antiplatelet strategy that selectively targets activated platelets. Circ Res. 2006;99:25-33. (Pubitemid 44297052)
32. Stoll P, Bassler N, Hagemeyer CE, Eisenhardt SU, Chen YC, Schmidt R, Schwarz M, Ahrens I, Katagiri Y, Pannen B, Bode C, Peter K. Targeting ligand-induced binding sites on GPIIb/IIIa via single-chain antibody allows effective anticoagulation without bleeding time prolongation. Arterioscler Thromb Vasc Biol. 2007;27:1206-1212. (Pubitemid 46641980)
33. Sandberg LB, Leslie JG, Leach CT, Alvarez VL, Torres AR, Smith DW. Elastin covalent structure as determined by solid phase amino acid sequencing. Pathol Biol (Paris). 1985;33:266-274. (Pubitemid 15080359)
34. Reiersen H, Clarke AR, Rees AR. Short elastin-like peptides exhibit the same temperature-induced structural transitions as elastin polymers: implications for protein engineering. J Mol Biol. 1998;283:255-264. (Pubitemid 28466654)
35. Meyer DE, Chilkoti A. Purification of recombinant proteins by fusion with thermally-responsive polypeptides. Nat Biotechnol. 1999;17:1112-1115. (Pubitemid 29533553)
36. Megeed Z, Winters RM, Yarmush ML. Modulation of single-chain antibody affinity with temperature-responsive elastin-like polypeptide linkers. Biomacromolecules. 2006;7:999-1004. (Pubitemid 43670783)
37. Blenner MA, Banta S. Characterization of the 4D5Flu single-chain antibody with a stimulus-responsive elastin-like peptide linker: a potential reporter of peptide linker conformation. Protein Sci. 2008;17:527-536. (Pubitemid 351281553)
38. Meyer DE, Kong GA, Dewhirst MW, Zalutsky MR, Chilkoti A. Targeting a genetically engineered elastin-like polypeptide to solid tumors by local hyperthermia. Cancer Res. 2001;61:1548-1554. (Pubitemid 34292586)
39. Betre H, Liu W, Zalutsky MR, Chilkoti A, Kraus VB, Setton LA. A thermally responsive biopolymer for intra-articular drug delivery. J Control Release. 2006;115:175-182. (Pubitemid 44537500)
40. Farady CJ, Egea PF, Schneider EL, Darragh MR, Craik CS. Structure of an Fab-protease complex reveals a highly specific non-canonical mechanism of inhibition. J Mol Biol. 2008;380:351-360.
41. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR. 1996;8:477-486. (Pubitemid 126706801)
42. Clark M, Cramer RD III, Van Opdenbosch N. Validation of the general purpose tripos 5.2 force field. J Comput Chem. 1989;10:982-1012.
43. Luan C-H, Urry DW. Molecular mechanics study of the-spiral conformations of the Phe4, Tyr4, and Trp4 analogs of elastomeric poly(Val1-Pro2-Gly3-Val4- Gly5). Int J Quantum Chem. 1992;42:1439-1448.
44. Armstrong PC, Dhanji AR, Truss NJ, Zain ZN, Tucker AT, Mitchell JA, Warner TD. Utility of 96-well plate aggregometry and measurement of thrombi adhesion to determine aspirin and clopidogrel effectiveness. Thromb Haemost. 2009;102:772-778.
45. Perczel A, Fasman GD. Quantitative analysis of cyclicβ-turn models. Protein Sci. 1992;1:378-395.
46. Ferreira I, Schutte M, Oosterloo E, Dekker W, Mooi BW, Dambrink JH, van 't Hof AW. Therapeutic mild hypothermia improves outcome after out-of-hospital cardiac arrest. Neth Heart J. 2009;17:378-384.
47. Belliard G, Catez E, Charron C, Caille V, Aegerter P, Dubourg O, Jardin F, Vieillard-Baron A. Efficacy of therapeutic hypothermia after out-ofhospital cardiac arrest due to ventricular fibrillation. Resuscitation. 2007; 75:252-259. (Pubitemid 47588627)
48. Lee R, Asare K. Therapeutic hypothermia for out-of-hospital cardiac arrest. Am J Health Syst Pharm. 2010;67:1229-1237.
49. Pugsley W, Klinger L, Paschalis C, Treasure T, Harrison M, Newman S. The impact of microemboli during cardiopulmonary bypass on neuropsychological functioning. Stroke. 1994;25:1393-1399. (Pubitemid 24198586)
50. Stygall J, Newman SP, Fitzgerald G, Steed L, Mulligan K, Arrowsmith JE, Pugsley W, Humphries S, Harrison MJ. Cognitive change 5 years after coronary artery bypass surgery. Health Psychol. 2003;22:579-586. (Pubitemid 37466945)
51. Hauer JM. Central hypothermia as a cause of acute pancreatitis in children with neurodevelopmental impairment. Dev Med Child Neurol. 2008;50:68-70.
52. Sallach RE, Wei M, Biswas N, Conticello VP, Lecommandoux S, Dluhy RA, Chaikof EL. Micelle density regulated by a reversible switch of protein secondary structure. J Am Chem Soc. 2006;128:12014-12019. (Pubitemid 44360240)
53. Sallach RE, Cui W, Balderrama F, Martinez AW, Wen J, Haller CA, Taylor JV, Wright ER, Long RC Jr, Chaikof EL. Long-term biostability of self-assembling protein polymers in the absence of covalent crosslinking. Biomaterials. 2010;31:779-791.
54. Sallach RE, Cui W, Wen J, Martinez A, Conticello VP, Chaikof EL. Elastin-mimetic protein polymers capable of physical and chemical crosslinking. Biomaterials. 2009;30:409-422.
55. Trabbic-Carlson K, Meyer DE, Liu L, Piervincenzi R, Nath N, LaBean T, Chilkoti A. Effect of protein fusion on the transition temperature of an environmentally responsive elastin-like polypeptide: a role for surface hydrophobicity? Protein Eng Des Sel. 2004;17:57-66. (Pubitemid 38173169)
56. Soar J, Nolan JP. Mild hypothermia for post cardiac arrest syndrome. BMJ. 2007;335:459-460. (Pubitemid 47401593)
57. Ramaraj R. Mild therapeutic hypothermia in patients after out-of-hospital cardiac arrest due to acute ST-segment elevation myocardial infarction. Crit Care Med. 2008;36:3280; author reply 3280-3281.
58. Wolfrum S, Pierau C, Radke PW, Schunkert H, Kurowski V. Mild therapeutic hypothermia in patients after out-of-hospital cardiac arrest due to acute ST-segment elevation myocardial infarction undergoing immediate percutaneous coronary intervention. Crit Care Med. 2008;36:1780-1786.
59. Sun JC, Whitlock R, Cheng J, Eikelboom JW, Thabane L, Crowther MA, Teoh KH. The effect of pre-operative aspirin on bleeding, transfusion, myocardial infarction, and mortality in coronary artery bypass surgery: a systematic review of randomized and observational studies. Eur Heart J. 2008;29:1057-1071. (Pubitemid 351858412)
60. Berger JC. Platelet-directed therapies and coronary artery bypass grafting. Am J Cardiol. 2009;104:44C-48C.
61. Koster A, Chew DP, Kuebler W, Habazettl H, Bauer M, Hausmann H, Hetzer R, Kuppe H, Hamm CW. Effects of tirofiban on hemostatic activation and inflammatory response during cardiopulmonary bypass. Am J Cardiol. 2003;91:346-347. (Pubitemid 36143879)
62. Silvestry SC, Smith PK. Current status of cardiac surgery in the abciximab-treated patient. Ann Thorac Surg. 2000;70:S12-S19. (Pubitemid 30662090)
63. Bizzarri FSS, Tucci E, Lucidi M, Davoli G, Toscano T, Neri E, Muzzi L, Frati G. Perioperative use of tirofiban hydrochloride (Aggrastat) does not increase surgical bleeding after emergency or urgent coronary artery bypass grafting. J Thorac Cardiovasc Surg. 2001;122:1181-1185.
64. Harder S, Klinkhardt U, Alvarez JM. Avoidance of bleeding during surgery in patients receiving anticoagulant and/or antiplatelet therapy: pharmacokinetic and pharmacodynamic considerations. Clin Pharmacokinet. 2004;43:963-981. (Pubitemid 39602013)
65. Aguirre FV TE, Ferguson JJ, Anderson K, Blankenship JC, Heuser RR, Sigmon K, Taylor M, Gottlieb R, Hanovich G, et al. Bleeding complications with the chimeric antibody to platelet glycoprotein IIb/IIIa integrin in patients undergoing percutaneous coronary intervention: EPIC Investigators. Circulation. 1995;91:2882-2890.
66. Tcheng JE. Clinical challenges of platelet glycoprotein IIb/IIIa receptor inhibitor therapy: bleeding, reversal, thrombocytopenia, and retreatment. Am Heart J. 2000;139:S38-S45. (Pubitemid 30091780)
67. Dyke CM. Safety of glycoprotein IIb-IIIa inhibitors: a heart surgeon's perspective. Am Heart J. 1999;138:307-316.
68. 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-mimeticαIIbβ3 (GPIIb/IIIa) antagonists. Arterioscler Thromb Vasc Biol. 2007;27:e9-e15.
69. Peter K, Schwarz M, Conradt C, Nordt T, Moser M, Kubler W, Bode C. Heparin inhibits ligand binding to the leukocyte integrin Mac-1 (CD11b/CD18). Circulation. 1999;100:1533-1539. (Pubitemid 29461466)
70. Lele M, Sajid M, Wajih N, Stouffer GA. Eptifibatide and 7E3, but not tirofiban, inhibit-(v)-(3) integrin-mediated binding of smooth muscle cells to thrombospondin and prothrombin. Circulation. 2001;104:582-587.