A novel snake venom-derived GPIb antagonist, anfibatide, protects mice from acute experimental ischaemic stroke and reperfusion injury

British Journal of Pharmacology

Volumn 172, Issue 15, 2015, Pages 3904-3916

  Li, Ting Ting ^a   Fan, Man Li ^a   Hou, Shi Xiang ^a,b   Li, Xiao Yi ^c   Barry, Devin M ^d   Jin, Hui ^e   Luo, Sheng Yong ^f   Kong, Feng ^a   Lau, Lit Fui ^c   Dai, Xiang Rong ^c   Zhang, Guo Hui ^b,c   Zhou, Lan Lan ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b Xuancheng People s Hospital   (China)

^c Zhaoke Pharmaceutical (Hefei) Co Ltd   (China)

^d WASHINGTON UNIVERSITY   (United States)

^e Department of Pharmaceutical Chemistry Jiangsu Changjiang Pharmaceutical Co Ltd   (China)

^f Anhui Academy of Medical Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANFIBATIDE; FIBRINOGEN; GLYCOPROTEIN IB ALPHA; PROTEIN INHIBITOR; TIROFIBAN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; AGKISACUCETIN PROTEIN, AGKISTRODON ACUTUS; FIBRIN; LECTIN; PROTECTIVE AGENT; SNAKE VENOM; THROMBIN RECEPTOR; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING TIME; BRAIN HEMORRHAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL COUNT; CEREBRAL ARTERY DISEASE; CEREBRAL HEMORRHAGE; DRUG EFFECTS; METABOLISM; PATHOLOGY; STROKE; THROMBOCYTE;

ANIMALS; BLEEDING TIME; BLOOD PLATELETS; BRAIN ISCHEMIA; CELL COUNT; CEREBRAL HEMORRHAGE; CROTALID VENOMS; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBRIN; INFARCTION, MIDDLE CEREBRAL ARTERY; LECTINS, C-TYPE; MALE; MICE; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PROTECTIVE AGENTS; REPERFUSION INJURY; STROKE; TYROSINE; VON WILLEBRAND FACTOR;

EID: 84936991788     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13178     Document Type: Article

References (54)

1. Abe T, Kunz A, Shimamura M, Zhou P, Anrather J, Iadecola C, (2009). The neuroprotective effect of prostaglandin E2 EP1 receptor inhibition has a wide therapeutic window, is sustained in time and is not sexually dimorphic. J Cereb Blood Flow Metab 29: 66-72.
2. Adams HP Jr, Adams RJ, Brott T, del Zoppo GJ, Furlan A, Goldstein LB, et al. (2003). Guidelines for the early management of patients with ischemic stroke: a scientific statement from the Stroke Council of the American Stroke Association. Stroke 34: 1056-1083.
3. Adams HP Jr, Effron MB, Torner J, Davalos A, Frayne J, Teal P, et al. (2008). Emergency administration of abciximab for treatment of patients with acute ischemic stroke: results of an international phase III trial: abciximab in emergency treatment of stroke trial (AbESTT-II). Stroke 39: 87-99.
4. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: catalytic receptors. Br J Pharmacol 170: 1676-1705.
5. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: enzymes. Br J Pharmacol 170: 1797-1867.
6. Andrews RK, Berndt MC, (2004). Platelet physiology and thrombosis. Thromb Res 114: 447-453.
7. Baker RI, Eikelboom J, Lofthouse E, Staples N, Afshar-Kharghan V, Lõpez JA, et al. (2001). Platelet glycoprotein Iba Kozak polymorphism is associated with an increased risk of ischemic stroke. Blood 1: 36-40.
8. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H, (1986). Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17: 472-476.
9. Bergmeier W, Chauhan AK, Wagner DD, (2008). Glycoprotein Ibalpha and von Willebrand factor in primary platelet adhesion and thrombus formation: lessons from mutant mice. Thromb Haemost 99: 264-270.
10. Berndt MC, Andrews RK, (2002). Approaches to the analysis of structure/function of novel membrane receptors: a functional dissection of platelet GP Ib-IX-V. Lett Pept Sci 8: 163-169.
11. Ciccone A, Motto C, Abraha I, Cozzolino F, Santilli I, (2014). Glycoprotein IIb-IIIa inhibitors for acute ischaemic stroke. Cochrane Database Syst Rev (3): CD005208.
12. Clark WM, Lessov NS, Dixon MP, Eckenstein F, (1997). Monofilament intraluminal middle cerebral artery occlusion in the mouse. Neurol Res 19: 641-648.
13. De Meyer SF, Schwarz T, Deckmyn H, Denis CV, Nieswandt B, Stoll G, et al. (2010). Binding of von Willebrand factor to collagen and glycoprotein Ibalpha, but not to glycoprotein IIb/IIIa, contributes to ischemic stroke in mice-brief report. Arterioscler Thromb Vasc Biol 30: 1949-1951.
14. De Meyer SF, Schwarz T, Schatzberg D, Wagner DD, (2011). Platelet glycoprotein Ibα is an important mediator of ischemic stroke in mice. Exp Transl Stroke Med 3: 9.
15. De Meyer SF, Stoll G, Wagner DD, Kleinschnitz C, (2012). von Willebrand factor: an emerging target in stroke therapy. Stroke 43: 599-606.
16. Del Zoppo GJ, Mabuchi T, (2003). Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 23: 879-894.
17. Espinera AR, Ogle ME, Gu X, Wei L, (2013). Citalopram enhances neurovascular regeneration and sensorimotor functional recovery after ischemic stroke in mice. Neuroscience 247: 1-11.
18. Fisher M, (2011). New approaches to neuroprotective drug development. Stroke 42: S24-S27.
19. Fujioka M, Hayakawa K, Mishima K, Kunizawa A, Irie K, Higuchi S, et al. (2010). ADAMTS13 gene deletion aggravates ischemic brain damage: a possible neuroprotective role of ADAMTS13 by ameliorating post-ischemic hypoperfusion. Blood 115: 1650-1653.
20. Gao Y, Ge H, Chen H, Li H, Liu Y, Chen L, et al. (2012). Crystal structure of agkisacucetin, a GpIb-binding snake C-type lectin that inhibits platelet adhesion and aggregation. Proteins 80: 1707-1711.
21. Gruner S, Prostredna M, Schulte V, Krieg T, Eckes B, Brakebusch C, et al. (2003). Multiple integrin-ligand interactions synergize in shear-resistant platelet adhesion at sites of arterial injury in vivo. Blood 102: 4021-4027.
22. Hacke W, Kaste M, Bluhmki E, Brozman M, Davalos A, Guidetti D, et al. (2008). Thrombolysis with alteplase 3 to 4.5 h after acute ischemic stroke. N Engl J Med 359: 1317-1329.
23. Hernandez TD, Schallert T, (1988). Seizures and recovery from experimental brain damage. Exp Neurol 102: 318-324.
24. Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA, et al. (2006). Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 12: 225-229.
25. Kellert L, Hametner C, Rohde S, Bendszus M, Hacke W, Ringleb P, et al. (2013). Endovascular stroke therapy: tirofiban is associated with risk of fatal intracerebral hemorrhage and poor outcome. Stroke 44: 1453-1455.
26. Khan MM, Motto DG, Lentz SR, Chauhan AK, (2012). ADAMTS13 reduces VWF-mediated acute inflammation following focal cerebral ischemia in mice. J Thromb Haemost 10: 1665-1671.
27. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG, (2010). Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. J Pharmacol Pharmacother 1: 94-99.
28. Kleinschnitz C, Pozgajova M, Pham M, Bendszus M, Nieswandt B, Stoll G, (2007). Targeting platelets in acute experimental stroke: impact of glycoprotein Ib, VI, and IIb/IIIa blockade on infarct size, functional outcome, and intracranial bleeding. Circulation 115: 2323-2330.
29. Kleinschnitz C, De Meyer SF, Schwarz T, Austinat M, Vanhoorelbeke K, Nieswandt B, et al. (2009). Deficiency of von Willebrand factor protects mice from ischemic stroke. Blood 113: 3600-3603.
30. Lei X, Reheman A, Hou Y, Zhou H, Wang Y, Marshall AH, et al. (2014). Anfibatide, a novel GPIb complex antagonist, inhibits platelet adhesion and thrombus formation in vitro and in vivo in murine models of thrombosis. Thromb Haemost 111: 279-289.
31. Liu Z, Chopp M, Ding X, Cui Y, Li Y, (2013). Axonal remodeling of the corticospinal tract in the spinal cord contributes to voluntary motor recovery after stroke in adult mice. Stroke 44: 1951-1956.
32. Martínez-Martínez M, Cazorla-García R, Rodríguez de Antonio LA, Martínez-Sánchez P, Fuentes B, Diez-Tejedor E, (2010). Hypercoagulability and ischemic stroke in young patients. Neurologia 25: 343-348.
33. Massberg S, Enders G, Matos FC, Tomic LI, Leiderer R, Eisenmenger S, et al. (1999). Fibrin(ogen) deposition at the postischemic vessel wall promotes platelet adhesion during ischemia-reperfusion in vivo. Blood 11: 3829-3838.
34. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
35. Momi S, Tantucci M, Van Roy M, Ulrichts H, Ricci G, Gresele P, (2013). Reperfusion of cerebral artery thrombosis by the GPIb-VWF blockade with the Nanobody ALX-0081 reduces brain infarct size in guinea pigs. Blood 121: 5088-5097.
36. Montoro-García S, Shantsila E, Lip GY, (2014). Potential value of targeting von Willebrand factor in atherosclerotic cardiovascular disease. Expert Opin Ther Targets 18: 43-53.
37. Mu FT, Cranmer SL, Andrews RK, Berndt MC, (2010). Functional association of phosphoinositide-3-kinase with platelet glycoprotein Iba, the major ligand-binding subunit of the glycoprotein Ib-IX-V complex. J Thromb Haemost 8: 324-330.
38. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR. (2014) The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl. Acids Res. 42 (Database Issue): D1098-D1106.
39. Pham M, Helluy X, Kleinschnitz C, Kraft P, Bartsch AJ, Jakob P, et al. (2011). Sustained reperfusion after blockade of glycoprotein-receptor-Ib in focal cerebral ischemia: an MRI study at 17.6 Tesla. PLoS ONE 4: e18386.
40. Ruggeri ZM, (2001). Structure of von Willebrand factor and its function in platelet adhesion and thrombus formation. Best Pract Res Clin Haematol 14: 257-279.
41. Sharma A, Fish BL, Moulder JE, Medhora M, Baker JE, Mader M, et al. (2014). Safety and blood sample volume and quality of a refined retro-orbital bleeding technique in rats using a lateral approach. Lab Anim (NY) 43: 63-66.
42. Stoll G, Kleinschnitz C, Nieswandt B, (2008). Molecular mechanisms of thrombus formation in ischemic stroke: novel insights and targets for treatment. Blood 112: 3555-3562.
43. Stoll G, Kleinschnitz C, Nieswandt B, (2010). The role of glycoprotein Ibalpha and von Willebrand factor interaction in stroke development. Hamostaseologie 30: 136-138.
44. Sugidachi A, Asai F, Ogawa T, Inoue T, Koike H, (2000). The in vivo pharmacological profile of CS-747, a novel antiplatelet agent with platelet ADP receptor antagonist properties. Br J Pharmacol 129: 1439-1446.
45. Sumii T, Lo EH, (2002). Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke 33: 831-836.
46. Suzuki Y, Hattori K, Hamanaka J, Murase T, Egashira Y, Mishiro K, et al. (2012). Pharmacological inhibition of TLR4-NOX4 signal protects against neuronal death in transient focal ischemia. Sci Rep 2: 896-905.
47. Tabrizi P, Wang L, Seeds N, McComb JG, Yamada S, Griffin JH, et al. (1999). Tissue plasminogen activator (tPA) deficiency exacerbates cerebrovascular fibrin(ogen) deposition and brain injury in a murine stroke model: studies in tPA-deficient mice and wild-type mice on a matched genetic background. Arterioscler Thromb Vasc Biol 19: 2801-2806.
48. Toth J, Kappelmayer J, Udvardy ML, Szanto T, Szarvas M, Rejto L, et al. (2009). Increased platelet glycoprotein Ib receptor number, enhanced platelet adhesion and severe cerebral ischaemia in a patient with polycythaemia vera. Platelets 4: 282-287.
49. Van Schie MC, DE Maat MP, Dippel DW, de Groot PG, Lenting PJ, Leebeek FW, et al. (2010). Von Willebrand factor propeptide and the occurrence of a first ischemic stroke. J Thromb Haemost 8: 1424-1426.
50. Varga-Szabo D, Pleines I, Nieswandt B, (2008). Cell adhesion mechanisms in platelets. Arterioscler Thromb Vasc Biol 28: 403-412.
51. Westein E, van der Meer AD, Kuijpers MJ, Frimat JP, van den Berg A, Heemskerk JW, (2013). Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor-dependent manner. Proc Natl Acad Sci U S A 110: 1357-1362.
52. Zhang ZG, Chopp M, Goussev A, Lu D, Morris D, Tsang W, et al. (1999). Cerebral microvascular obstruction by fibrin(ogen) is associated with upregulation of PAI-1 acutely after onset of focal embolic ischemia in rats. J Neurosci 19: 10898-10907.
53. Zhao BQ, Ikeda Y, Ihara H, Urano T, Fan W, Mikawa S, et al. (2004). Essential role of endogenous tissue plasminogen activator through matrix metalloproteinase 9 induction and expression on heparin-produced cerebral hemorrhage after cerebral ischemia in mice. Blood 103: 2610-2616.
54. Zhu HB, Zhang L, Wang ZH, Tian JW, Fu FH, Liu K, et al. (2005). Therapeutic effects of hydroxysafflor yellow A on focal cerebral ischemic injury in rats and its primary mechanisms. J Asian Nat Prod Res 7: 607-613.