Human recombinant alkaline phosphatase inhibits ex vivo platelet activation in humans

Thrombosis and Haemostasis

Volumn 116, Issue 6, 2016, Pages 1111-1121

  Tunjungputri, Rahajeng N ^a,b   Peters, Esther ^a   Van Der Ven, Andre ^a   De Groot, Philip G ^c   De Mast, Quirijn ^a,c   Pickkers, Peter ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b DIPONEGORO UNIVERSITY   (Indonesia)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Acute kidney injury; Alkaline phosphatase; Antiplatelet agents; Platelet activation; Sepsis

Indexed keywords

BETA3 INTEGRIN; CD14 ANTIGEN; PADGEM PROTEIN; ADENOSINE DIPHOSPHATE; ALKALINE PHOSPHATASE; ANTITHROMBOCYTIC AGENT; CARRIER PROTEIN; COLLAGEN-RELATED PEPTIDE; LIPOPEPTIDE; PAM(3)CSK(4) PEPTIDE; PEPTIDE; RECOMBINANT PROTEIN;

ACUTE KIDNEY FAILURE; ADULT; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; CLINICAL ARTICLE; DEMOGRAPHY; EX VIVO STUDY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE; HEART RATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INFLAMMATION; LEUKOCYTE ACTIVATION; LIMIT OF QUANTITATION; MALE; MIDDLE AGED; PLATELET AGGREGATION ASSAY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; SEPSIS; THROMBOCYTE ACTIVATION; THROMBOCYTE COUNT; YOUNG ADULT; AGED; CHEMISTRY; DRUG EFFECTS; PATHOPHYSIOLOGY; THROMBOCYTE; THROMBOCYTE AGGREGATION;

ACUTE KIDNEY INJURY; ADENOSINE DIPHOSPHATE; ADULT; AGED; ALKALINE PHOSPHATASE; BLOOD PLATELETS; CARRIER PROTEINS; FEMALE; HUMANS; LIPOPEPTIDES; MALE; MIDDLE AGED; PEPTIDES; PLATELET ACTIVATION; PLATELET AGGREGATION; PLATELET AGGREGATION INHIBITORS; RECOMBINANT PROTEINS; SEPSIS;

EID: 85004130361     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH16-03-0206     Document Type: Article

References (61)

1. Stevenson EK, Rubenstein AR, Radin GT, et al. Two decades of mortality trends among patients with severe sepsis: a comparative meta-analysis*. Cri Care Med 2014; 42: 625-631.
2. Goldberg R, Dennen P. Long-term outcomes of acute kidney injury. Adv Chron Kidney Dis 2008; 15: 297-307.
3. Case J, Khan S, Khalid R, et al. Epidemiology of Acute Kidney Injury in the Intensive Care Unit. Crit Care Res Pract 2013; 2013: 9.
4. Millán JL. Alkaline Phosphatases: Structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2006; 2: 335-341.
5. Heemskerk S, Masereeuw R, Moesker O, et al. Alkaline phosphatase treatment improves renal function in severe sepsis or septic shock patients. Crit Care Med 2009; 37: 417-423, e1.
6. Pickkers P, Heemskerk S, Schouten J, et al. Alkaline phosphatase for treatment of sepsis-induced acute kidney injury: a prospective randomized double-blindplacebo-controlled trial. Crit Care 2012; 16: R14.
7. Kiffer-Moreira T, Sheen CR, da Silva Gasque KC, et al. Catalytic signature of a heat-stable, chimeric human alkaline phosphatase with therapeutic potential. PloS one 2014; 9: e89374.
8. Bentala H, Verweij WR, Huizinga-Van der Vlag A, et al. Removal of phosphate from lipid A as a strategy to detoxify lipopolysaccharide. Shock 2002; 18: 561-566.
9. Bours MJ, Swennen EL, Di Virgilio F, et al. Adenosine 5’-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 2006; 112: 358-404.
10. Peters E, Geraci S, Heemskerk S, et al. Alkaline phosphatase protects against renal inflammation through dephosphorylation of lipopolysaccharide and adenosine triphosphate. Br J Pharmacol 2015; Epub ahead of print.
11. Dorsam RT, Kunapuli SP. Central role of the P2Y(12) receptor in platelet activation. J Clin Invest 2004; 113: 340-345.
12. Michelson AD. Antiplatelet therapies for the treatment of cardiovascular disease. Nat Rev Drug Discov 2010; 9: 154-169.
13. Haslam RJ, Rosson GM. Effects of adenosine on levels of adenosine cyclic 3’, 5’-monophosphate in human blood platelets in relation to adenosine incorporation and platelet aggregation. Mol Pharmacol 1975; 11: 528-544.
14. Weitberg AB. The effect of alkaline phosphatase on platelet aggregation. Haematologia 1989; 22: 65-68.
15. Hatmi M, Haye B, Gavaret JM, et al. Alkaline phosphatase prevents platelet stimulation by thromboxane mimetics. Br J Pharmacol 1991; 104: 554-558.
16. Margolin N, True TA, Saussy DL, Jr., et al. Effect of alkaline phosphatase on thromboxane mimetic induced platelet activation. Prostaglandins 1994; 48: 235-246.
17. Semeraro N, Ammollo CT, Semeraro F, et al. Sepsis, thrombosis and organ dysfunction. Thromb Res 2012; 129: 290-295.
18. Levi M, Schultz M, van der Poll T. Sepsis and thrombosis. Semin Thromb Hemost 2013; 2013.
19. Mavrommatis AC, Theodoridis T, Orfanidou A, et al. Coagulation system and platelets are fully activated in uncomplicated sepsis. Cri Care Med 2000; 28: 451-457.
20. van Bladel ER, de Jager RL, Walter D, et al. Platelets of patients with chronic kidney disease demonstrate deficient platelet reactivity in vitro. BMC Nephrol 2012; 13: 127.
21. Tunjungputri RN, Van Der Ven AJ, Schonsberg A, et al. Reduced platelet hyperreactivity and platelet-monocyte aggregation in HIV-infected individuals receiving a raltegravir-based regimen. AIDS 2014; 28: 2091-2096.
22. Michelson AD, Barnard MR, Krueger LA, et al. Circulating monocyte-platelet aggregates are a more sensitive marker of in vivo platelet activation than platelet surface P-selectin studies in baboons, human coronary intervention, and human acute myocardial infarction. Circulation 2001; 104: 1533-1537.
23. Rondina MT, Weyrich AS, Zimmerman GA. Platelets as cellular effectors of inflammationin vascular diseases. Circulation Res 2013; 112: 1506-1519.
24. American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference: definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992; 20: 864-874.
25. Handa M, Guidotti G. Purification and cloning of a soluble ATP-diphosphohydrolase (apyrase) from potato tubers (Solanum tuberosum). Biochem Biophys Res Commun 1996; 218: 916-923.
26. Marcus AJ, Broekman MJ, Drosopoulos JH, et al. The endothelial cell ecto-ADPase responsible for inhibition of platelet function is CD39. J Clin Invest 1997; 99: 1351-1360.
27. Yang D, Chen H, Koupenova M, et al. A new role for the A2b adenosine receptor in regulating platelet function. J Thromb Haemost 2010; 8: 817-827.
28. Peters E, Mehta RL, Murray PT, et al. Study protocol for a multicentre randomized controlled trial: Safety, Tolerability, efficacy and quality of life Of a human recombinant alkaline Phosphatase in patients with sepsis-associated Acute Kidney Injury (STOP-AKI). BMJ Open 2016; 6: e012371.
29. Hechler B, Léon C, Vial C, et al. The P2Y1 Receptor Is Necessary for Adenosine 5’-Diphosphate-Induced Platelet Aggregation. Blood 1998; 92: 152-159.
30. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood 2003; 102: 449-461.
31. Blair P, Rex S, Vitseva O, et al. Stimulation of Toll-Like Receptor 2 in Human Platelets Induces a Thromboinflammatory Response Through Activation of Phosphoinositide 3-Kinase. Circulation Res 2009; 104: 346-354.
32. Klarstrom Engstrom K, Brommesson C, Kalvegren H, et al. Toll like receptor 2/1 mediated platelet adhesion and activation on bacterial mimetic surfaces is dependent on src/Syk-signaling and purinergic receptor P2X1 and P2Y12 activation. Biointerphases 2014; 9: 041003.
33. Altieri D, Edgington T. The saturable high affinity association of factor X to ADP-stimulated monocytes defines a novel function of the Mac-1 receptor. J Biol Chem 1988; 263: 7007-7015.
34. Wang L, Jacobsen SE, Bengtsson A, et al. P2 receptor mRNA expression profiles in human lymphocytes, monocytes and CD34+ stem and progenitor cells. BMC Immunol 2004; 5: 16.
35. Sluyter R. P2X and P2Y receptor signaling in red blood cells. Front Mol Biosci 2015; Epub ahead of print.
36. Eltzschig HK, Sitkovsky MV, Robson SC. Purinergic Signaling during Inflammation. N Engl J Med 2012; 367: 2322-2333.
37. Johnston Cox HA, Yang D, Ravid K. Physiological implications of adenosine receptor mediated platelet aggregation. J Cell Physiol 2011; 226: 46-51.
38. de Stoppelaar SF, van’t Veer C, van der Poll T. The role of platelets in sepsis. Thromb Haemost 2014; 112: 666-677.
39. Singbartl K, Ley K. Leukocyte recruitment and acute renal failure. J Mol Med 2004; 82: 91-101.
40. Singbartl K, Forlow SB, Ley K. Platelet, but not endothelial, P-selectin is critical for neutrophil-mediated acute postischemic renal failure. FASEB J 2001; 15: 2337-2344.
41. Beumer C, Wulferink M, Raaben W, et al. Calf intestinal alkaline phosphatase, a novel therapeutic drug for lipopolysaccharide (LPS)-mediated diseases, attenuates LPS toxicity in mice and piglets. J Pharmacol Exp Therap 2003; 307: 737-744.
42. Tunjungputri R, van der Ven A, Riksen N, et al. Differential effects of platelets and platelet inhibition by ticagrelor on TLR2-and TLR4-mediated inflammatory responses. Thromb Haemost 2015; 113: 1035-1045.
43. Montrucchio G, Bosco O, Del Sorbo L, et al. Mechanisms of the priming effect of low doses of lipopoly-saccharides on leukocyte-dependent platelet aggregation in whole blood. Thromb Haemost 2003; 90: 872-881.
44. Boldt J, Muller M, Heesen M, et al. Influence of different volume therapies on platelet function in the critically ill. Inten Care Med 1996; 22: 1075-1081.
45. Yaguchi A, Lobo F, VINCENT JL, et al. Platelet function in sepsis. J Thromb Haemost 2004; 2: 2096-2102.
46. Woth G, Varga A, Ghosh S, et al. Platelet aggregation in severe sepsis. J Thromb Thromb 2011; 31: 6-12.
47. Gawaz M, Fateh-Moghadam S, Pilz G, et al. Platelet activation and interaction with leucocytes in patients with sepsis or multiple organ failure. Eur J Clin Invest 1995; 25: 843-851.
48. Russwurm S, Vickers J, Meier-Hellmann A, et al. Platelet and leukocyte activation correlate with the severity of septic organ dysfunction. Shock 2002; 17: 263-268.
49. de Stoppelaar SF, Van’t Veer C, van den Boogaard FE, et al. Protease activated receptor 4 limits bacterial growth and lung pathology during late stage Streptococcus pneumoniae induced pneumonia in mice. Thromb Haemost 2013; 110: 582-592.
50. Picker SM. In-vitro assessment of platelet function. Transfusion Apheresis Sci 2011; 44: 305-319.
51. Stafford NP, Pink AE, White AE, et al. Mechanisms involved in adenosine triphosphate-induced platelet aggregation in whole blood. Arterioscler Thromb Vasc Biol 2003; 23: 1928-1933.
52. Glenn JR, White AE, Johnson A, et al. Leukocyte count and leukocyte ecto-nucleotidase are major determinants of the effects of adenosine triphosphate and adenosine diphosphate on platelet aggregation in human blood. Platelets 2005; 16: 159-170.
53. Thomas MR, Storey RF. Effect of P2Y12 inhibitors on inflammation and immunity. Thromb Haemost 2015; 114: 490-497.
54. Winning J, Neumann J, Kohl M, et al. Antiplatelet drugs and outcome in mixed admissions to an intensive care unit*. Crit Care Med 2010; 38: 32-37.
55. Winning J, Reichel J, Eisenhut Y, et al. Anti-platelet drugs and outcome in severe infection: clinical impact and underlying mechanisms. Platelets 2009; 20: 50-57.
56. Valerio-Rojas JC, Jaffer IJ, Kor DJ, et al. Outcomes of severe sepsis and septic shock patients on chronic antiplatelet treatment: a historical cohort study. Crit Care Res Pract 2013; 2013: 782573.
57. Sossdorf M, Otto GP, Boettel J, et al. Benefit of low-dose aspirin and non-steroidal anti-inflammatory drugs in septic patients. Crit Care 2013; 17: 1-2.
58. Otto GP, Sossdorf M, Boettel J, et al. Effects of low-dose acetylsalicylic acid and atherosclerotic vascular diseases on the outcome in patients with severe sepsis or septic shock. Platelets 2013; 24: 480-485.
59. Gross AK, Dunn SP, Feola DJ, et al. Clopidogrel treatment and the incidence and severity of community acquired pneumonia in a cohort study and metaanalysis of antiplatelet therapy in pneumonia and critical illness. J Thromb Thromb 2013; 35: 147-154.
60. Xiao Z, Théroux P. Clopidogrel inhibits platelet-leukocyte interactions and thrombin receptor agonist peptide-induced platelet activation in patients with an acute coronary syndrome. J Am Coll Cardiol 2004; 43: 1982-1988.
61. Nylander S, Femia EA, Scavone M, et al. Ticagrelor inhibits human platelet aggregation via adenosine in addition to P2Y12 antagonism. J Thromb Haemost 2013; 11: 1867-1876.