Mechanisms of platelet clearance and translation to improve platelet storage

Blood

Volumn 131, Issue 14, 2018, Pages 1512-1521

  Edward Quach, M ^a,b   Chen, Wenchun ^a,b   Li, Renhao ^a,b  

^a AFLAC   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; THROMBIN RECEPTOR; BAK1 PROTEIN, HUMAN; BAX PROTEIN, HUMAN; BCL2L1 PROTEIN, HUMAN; C22ORF29 PROTEIN, HUMAN; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X;

APOPTOSIS; HEMATOLOGICAL PROCEDURE; HUMAN; IN VIVO STUDY; LIVER CELL; MACROPHAGE; NONHUMAN; PLATELET CLEARANCE; PRIORITY JOURNAL; REFRIGERATION; REVIEW; ROOM TEMPERATURE; THROMBOCYTE PRESERVATION; BLOOD STORAGE; CELL SURVIVAL; CYTOLOGY; GLYCOSYLATION; METABOLISM; MITOCHONDRION; SIGNAL TRANSDUCTION; THROMBOCYTE;

BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BLOOD PLATELETS; BLOOD PRESERVATION; CELL SURVIVAL; GLYCOSYLATION; HEPATOCYTES; HUMANS; MACROPHAGES; MITOCHONDRIA; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION;

EID: 85047555268     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2017-08-743229     Document Type: Review

References (103)

1. Lefrançais E, Ortiz-Muñoz G, Caudrillier A, et al. The lung is a site of platelet biogenesis and a reservoir for haematopoietic progenitors. Nature. 2017;544(7648):105-109.
2. Nieswandt B, Bergmeier W, Rackebrandt K, Gessner JE, Zirngibl H. Identification of critical antigen-specific mechanisms in the development of immune thrombocytopenic purpura in mice. Blood. 2000;96(7): 2520-2527.
3. Grewal PK, Aziz PV, Uchiyama S, et al. Inducing host protection in pneumococcal sepsis by preactivation of the Ashwell-Morell receptor. Proc Natl Acad Sci USA. 2013; 110(50):20218-20223.
4. Cohen JA, Leeksma CH. Determination of the life span of human blood platelets using labelled diisopropylfluorophosphonate. J Clin Invest. 1956;35(9):964-969.
5. Odell TT Jr, McDonald TP. Life span of mouse blood platelets. Proc Soc Exp Biol Med. 1961;106(1):107-108.
6. Mason KD, Carpinelli MR, Fletcher JI, et al. Programmed anuclear cell death delimits platelet life span. Cell. 2007;128(6): 1173-1186.
7. van der Meer PF, Tomson B, Brand A. In vivo tracking of transfused platelets for recovery and survival studies: an appraisal of labeling methods. Transfus Apheresis Sci. 2010;42(1): 53-61.
8. Chen W, Liang X, Syed AK, et al. Inhibiting GPIba shedding preserves post-transfusion recovery and hemostatic function of platelets after prolonged storage. Arterioscler Thromb Vasc Biol. 2016;36(9):1821-1828.
9. Baker GR, Sullam PM, Levin J. A simple, fluorescent method to internally label platelets suitable for physiological measurements. Am J Hematol. 1997;56(1):17-25.
10. Newman PJ, Aster R, Boylan B. Human platelets circulating in mice: applications for interrogating platelet function and survival, the efficacy of antiplatelet therapeutics, and the molecular basis of platelet immunological disorders. J Thromb Haemost. 2007; 5(suppl 1):305-309.
11. Zhang H, Nimmer PM, Tahir SK, et al. Bcl-2 family proteins are essential for platelet survival. Cell Death Differ. 2007;14(5): 943-951.
12. Kodama T, Takehara T, Hikita H, et al. BH3-only activator proteins Bid and Bim are dispensable for Bak/Bax-dependent throm-bocyte apoptosis induced by Bcl-xL deficiency: molecular requisites for the mitochondrial pathway to apoptosis in platelets. J Biol Chem. 2011;286(16): 13905-13913.
13. Debrincat MA, Pleines I, Lebois M, et al. BCL-2 is dispensable for thrombopoiesis and platelet survival. Cell Death Dis. 2015;6(4): e1721.
14. Print CG, Loveland KL, Gibson L, et al. Apoptosis regulator bcl-w is essential for spermatogenesis but appears otherwise redundant. Proc Natl Acad Sci USA. 1998; 95(21):12424-12431.
15. Vandenberg CJ, Cory S. ABT-199, a new Bcl-2-specific BH3 mimetic, has in vivo efficacy against aggressive Myc-driven mouse lymphomas without provoking thrombocytopenia. Blood. 2013;121(12):2285-2288.
16. Tao ZF, Hasvold L, Wang L, et al. Discovery of a potent and selective BCL-XL Inhibitor with in vivo activity. ACS Med Chem Lett. 2014; 5(10):1088-1093.
17. Wagner KU, Claudio E, Rucker EB III, et al. Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development. 2000;127(22):4949-4958.
18. Oltersdorf T, Elmore SW, Shoemaker AR, et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature. 2005;435(7042):677-681.
19. Josefsson EC, James C, Henley KJ, et al. Megakaryocytes possess a functional intrinsic apoptosis pathway that must be restrained to survive and produce platelets. J Exp Med. 2011;208(10):2017-2031.
20. Kelly PN, White MJ, Goschnick MW, et al. Individual and overlapping roles of BH3-only proteins Bim and Bad in apoptosis of lymphocytes and platelets and in suppression of thymic lymphoma development. Cell Death Differ. 2010;17(10):1655-1664.
21. Mutlu A, Gyulkhandanyan AV, Freedman J, Leytin V. Activation of caspases-9, -3 and -8 in human platelets triggered by BH3-only mimetic ABT-737 and calcium ionophore A23187: caspase-8 is activated via bypass of the death receptors. Br J Haematol. 2012; 159(5):565-571.
22. Josefsson EC, Burnett DL, Lebois M, et al. Platelet production proceeds independently of the intrinsic and extrinsic apoptosis pathways. Nat Commun. 2014;5:3455.
23. Dasgupta SK, Abdel-Monem H, Niravath P, et al. Lactadherin and clearance of platelet-derived microvesicles. Blood. 2009;113(6): 1332-1339.
24. Berger G, Hartwell DW, Wagner DD. P-Selectin and platelet clearance. Blood. 1998; 92(11):4446-4452.
25. Schoenwaelder SM, Yuan Y, Josefsson EC, et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoa-gulant function. Blood. 2009;114(3):663-666.
26. van Kruchten R, Mattheij NJ, Saunders C, et al. Both TMEM16F-dependent and TMEM16F-independent pathways contribute to phosphatidylserine exposure in platelet apoptosis and platelet activation. Blood. 2013;121(10):1850-1857.
27. Suzuki J, Umeda M, Sims PJ, Nagata S. Calcium-dependent phospholipid scrambling by TMEM16F. Nature. 2010;468(7325): 834-838.
28. Fujii T, Sakata A, Nishimura S, Eto K, Nagata S. TMEM16F is required for phosphatidylserine exposure and microparticle release in activated mouse platelets. Proc Natl Acad Sci USA. 2015;112(41):12800-12805.
29. Brown SB, Clarke MC, Magowan L, Sanderson H, Savill J. Constitutive death of platelets leading to scavenger receptor-mediated phagocytosis. A caspase-
30. independent cell clearance program. J Biol Chem. 2000;275(8):5987-5996.
31. Minamikawa T, Williams DA, Bowser DN, Nagley P. Mitochondrial permeability transition and swelling can occur reversibly without inducing cell death in intact human cells. Exp Cell Res. 1999;246(1):26-37.
32. Bergmeier W, Burger PC, Piffath CL, et al. Metalloproteinase inhibitors improve the recovery and hemostatic function of in vitro-aged or -injured mouse platelets. Blood. 2003;102(12):4229-4235.
33. Harrington WJ, Minnich V, Hollingsworth JW, Moore CV. Demonstration of a thrombocytopenic factor in the blood of patients with thrombocytopenic purpura. J Lab Clin Med. 1951;38(1):1-10.
34. Ballem PJ, Segal GM, Stratton JR, Gernsheimer T, Adamson JW, Slichter SJ. Mechanisms of thrombocytopenia in chronic autoimmune thrombocytopenic purpura. Evidence of both impaired platelet production and increased platelet clearance. J Clin Invest. 1987;80(1):33-40.
35. Becker BH, Miller JL. Effects of an antiplatelet glycoprotein Ib antibody on hemostatic function in the guinea pig. Blood. 1989;74(2):690-694.
36. Cadroy Y, Hanson SR, Kelly AB, et al. Relative antithrombotic effects of monoclonal antibodies targeting different platelet glycoprotein-adhesive molecule interactions in nonhuman primates. Blood. 1994;83(11): 3218-3224.
37. Bergmeier W, Rackebrandt K, Schröder W, Zirngibl H, Nieswandt B. Structural and functional characterization of the mouse von Willebrand factor receptor GPIb-IX with novel monoclonal antibodies. Blood. 2000; 95(3):886-893.
38. Cauwenberghs N, Meiring M, Vauterin S, et al. Antithrombotic effect of platelet glycoprotein Ib-blocking monoclonal antibody Fab fragments in nonhuman primates. Arterioscler Thromb Vasc Biol. 2000;20(5): 1347-1353.
39. Provan D, Stasi R, Newland AC, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood. 2010; 115(2):168-186.
40. Segal JB, Powe NR. Prevalence of immune thrombocytopenia: analyses of administrative data. J Thromb Haemost. 2006;4(11): 2377-2383.
41. Soslau G, Giles J. The loss of sialic acid and its prevention in stored human platelets. Thromb Res. 1982;26(6):443-455.
42. Choi SI, Simone JV, Jorney LJ. Neuraminidase-induced thrombocytopenia in rats. Br J Haematol. 1972;22(1):93-101.
43. Grewal PK, Uchiyama S, Ditto D, et al. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med. 2008;14(6):648-655.
44. Rumjantseva V, Grewal PK, Wandall HH, et al. Dual roles for hepatic lectin receptors in the clearance of chilled platelets. Nat Med. 2009;15(11):1273-1280.
45. Jansen AJ, Josefsson EC, Rumjantseva V, et al. Desialylation accelerates platelet clearance after refrigeration and initiates GPIba metalloproteinase-mediated cleavage in mice. Blood. 2012;119(5): 1263-1273.
46. Li J, van der Wal DE, Zhu G, et al. Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia. Nat Commun. 2015;6(1):7737.
47. Deng W, Xu Y, Chen W, et al. Platelet clearance via shear-induced unfolding of a membrane mechanoreceptor. Nat Commun. 2016;7:12863.
48. Grewal PK. The Ashwell-Morell receptor. Methods Enzymol. 2010;479:223-241.
49. Sørensen AL, Rumjantseva V, Nayeb-Hashemi S, et al. Role of sialic acid for platelet life span: exposure of beta-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes. Blood. 2009; 114(8):1645-1654.
50. Li Y, Fu J, Ling Y, et al. Sialylation on O-glycans protects platelets from clearance by liver Kupffer cells. Proc Natl Acad Sci USA. 2017;114(31):8360-8365.
51. Lodish HF. Recognition of complex oligo-saccharides by the multi-subunit asialoglycoprotein receptor. Trends Biochem Sci. 1991;16(10):374-377.
52. Grozovsky R, Begonja AJ, Liu K, et al. The Ashwell-Morell receptor regulates hepatic thrombopoietin production via JAK2-STAT3 signaling. Nat Med. 2015;21(1):47-54.
53. Josefsson EC, Gebhard HH, Stossel TP, Hartwig JH, Hoffmeister KM. The macrophage alphaMbeta2 integrin alphaM lectin domain mediates the phagocytosis of chilled platelets. J Biol Chem. 2005;280(18): 18025-18032.
54. Hoffmeister KM, Felbinger TW, Falet H, et al. The clearance mechanism of chilled blood platelets. Cell. 2003;112(1):87-97.
55. Casari C, Du V, Wu YP, et al. Accelerated uptake of VWF/platelet complexes in macrophages contributes to VWD type 2B-associated thrombocytopenia. Blood. 2013; 122(16):2893-2902.
56. Yan R, Chen M, Ma N, et al. Glycoprotein Iba clustering induces macrophage-mediated platelet clearance in the liver. Thromb Haemost. 2015;113(1):107-117.
57. Wandall HH, Hoffmeister KM, Sørensen AL, et al. Galactosylation does not prevent the rapid clearance of long-term, 4 degrees C-stored platelets. Blood. 2008;111(6): 3249-3256.
58. Gangarosa EJ, Landerman NS, Rosch PJ, Herndon EG Jr. Hematologic complications arising during ristocetin therapy; relation between dose and toxicity. N Engl J Med. 1958;259(4):156-161.
59. Sanders WE, Read MS, Reddick RL, Garris JB, Brinkhous KM. Thrombotic thrombocytopenia with von Willebrand factor deficiency induced by botrocetin. An animal model. Lab Invest. 1988;59(4):443-452.
60. Lillicrap D. von Willebrand disease: advances in pathogenetic understanding, diagnosis, and therapy. Blood. 2013;122(23): 3735-3740.
61. Tischer A, Madde P, Moon-Tasson L, Auton M. Misfolding of vWF to pathologically disordered conformations impacts the severity of von Willebrand disease. Biophys J. 2014; 107(5):1185-1195.
62. Sanders WE Jr, Reddick RL, Nichols TC, Brinkhous KM, Read MS. Thrombotic thrombocytopenia induced in dogs and pigs. The role of plasma and platelet vWF in animal models of thrombotic thrombocytopenic purpura. Arterioscler Thromb Vasc Biol. 1995;15(6):793-800.
63. Nascimbene A, Neelamegham S, Frazier OH, Moake JL, Dong JF. Acquired von Willebrand syndrome associated with left ventricular assist device. Blood. 2016; 127(25):3133-3141.
64. Webster ML, Sayeh E, Crow M, et al. Relative efficacy of intravenous immunoglobulin G in ameliorating thrombocytopenia induced by antiplatelet GPIIbIIIa versus GPIbalpha antibodies. Blood. 2006;108(3):943-946.
65. Zeng Q, Zhu L, Tao L, et al. Relative efficacy of steroid therapy in immune thrombocytopenia mediated by anti-platelet GPIIbIIIa versus GPIba antibodies. Am J Hematol. 2012;87(2):206-208.
66. Peng J, Ma SH, Liu J, et al. Association of autoantibody specificity and response to intravenous immunoglobulin G therapy in immune thrombocytopenia: a multicenter cohort study. J Thromb Haemost. 2014; 12(4):497-504.
67. Quach ME, Dragovich MA, Chen W, et al. Fc-independent immune thrombocytopenia via mechanomolecular signaling in platelets. Blood. 2018;131(7):787-796.
68. Maurer E, Tang C, Schaff M, et al. Targeting platelet GPIbb reduces platelet adhesion, GPIb signaling and thrombin generation and prevents arterial thrombosis. Arterioscler Thromb Vasc Biol. 2013;33(6):1221-1229.
69. Liang X, Syed AK, Russell SR, Ware J, Li R. Dimerization of glycoprotein Iba is not sufficient to induce platelet clearance. J Thromb Haemost. 2016;14(2):381-386.
70. Shrimpton CN, Borthakur G, Larrucea S, Cruz MA, Dong JF, López JA. Localization of the adhesion receptor glycoprotein Ib-IX-V complex to lipid rafts is required for platelet adhesion and activation. J Exp Med. 2002; 196(8):1057-1066.
71. Jin W, Inoue O, Tamura N, et al. A role for glycosphingolipid-enriched microdomains in platelet glycoprotein Ib-mediated platelet activation. J Thromb Haemost. 2007;5(5): 1034-1040.
72. Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood. 1996;88(5):1525-1541.
73. Zhang W, Deng W, Zhou L, et al. Identification of a juxtamembrane mecha-nosensitive domain in the platelet mecha-nosensor glycoprotein Ib-IX complex. Blood. 2015;125(3):562-569.
74. Bergmeier W, Piffath CL, Cheng G, et al. Tumor necrosis factor-a-converting enzyme (ADAM17) mediates GPIbalpha shedding from platelets in vitro and in vivo. Circ Res. 2004;95(7):677-683.
75. Gardiner EE, Karunakaran D, Shen Y, Arthur JF, Andrews RK, Berndt MC. Controlled shedding of platelet glycoprotein (GP)VI and GPIb-IX-V by ADAM family metal-loproteinases. J Thromb Haemost. 2007;5(7): 1530-1537.
76. Tao Y, Zhang X, Liang X, Zang J, Mo X, Li R. Structural basis for the specific inhibition of glycoprotein Iba shedding by an inhibitory antibody. Sci Rep. 2016;6(1):24789.
77. Li S, Wang Z, Liao Y, et al. The glycoprotein Ibalpha-von Willebrand factor interaction induces platelet apoptosis. J Thromb Haemost. 2010;8(2):341-350.
78. Li Z, Delaney MK, O’Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol. 2010; 30(12):2341-2349.
79. Murphy S, Gardner FH. Platelet storage at 22 degrees C; metabolic, morphologic, and functional studies. J Clin Invest. 1971;50(2): 370-377.
80. Holme S, Moroff G, Murphy S; Biomedical Excellence for Safer Transfusion Working Party of the International Society of Blood Transfusion. A multi-laboratory evaluation of in vitro platelet assays: the tests for extent of shape change and response to hypotonic shock. Transfusion. 1998;38(1):31-40.
81. Snyder EL, Hezzey A, Katz AJ, Bock J. Occurrence of the release reaction during preparation and storage of platelet concentrates. Vox Sang. 1981;41(3):172-177.
82. Seghatchian J, Krailadsiri P. The platelet storage lesion. Transfus Med Rev. 1997; 11(2):130-144.
83. Li J, Xia Y, Bertino AM, Coburn JP, Kuter DJ. The mechanism of apoptosis in human platelets during storage. Transfusion. 2000; 40(11):1320-1329.
84. Shiri R, Yari F, Ahmadinejad M, Vaeli S, Tabatabaei MR. The caspase-3 inhibitor (peptide Z-DEVD-FMK) affects the survival and function of platelets in platelet concentrate during storage. Blood Res. 2014; 49(1):49-53.
85. Catani MV, Gasperi V, Evangelista D, Finazzi Agrò A, Avigliano L, Maccarrone M. Anandamide extends platelets survival through CB(1)-dependent Akt signaling. Cell Mol Life Sci. 2010;67(4):601-610.
86. Zhuang Y, Ren G, Li H, et al. In vitro properties of apheresis platelet during extended storage in plasma treated with anandamide. Transfus Apheresis Sci. 2014;51(1):58-64.
87. Bradley AJ, Read BL, Levin E, Devine DV. Small-molecule complement inhibitors cannot prevent the development of the platelet storage lesion. Transfusion. 2008;48(4): 706-714.
88. Perrotta PL, Perrotta CL, Snyder EL. Apoptotic activity in stored human platelets. Transfusion. 2003;43(4):526-535.
89. Leaver HA, Schou AC, Rizzo MT, Prowse CV. Calcium-sensitive mitochondrial membrane potential in human platelets and intrinsic signals of cell death. Platelets. 2006;17(6): 368-377.
90. Perales Villarroel JP, Figueredo R, Guan Y, et al. Increased platelet storage time is associated with mitochondrial dysfunction and impaired platelet function. J Surg Res. 2013; 184(1):422-429.
91. Hayashi T, Tanaka S, Hori Y, Hirayama F, Sato EF, Inoue M. Role of mitochondria in the maintenance of platelet function during in vitro storage. Transfus Med. 2011;21(3): 166-174.
92. Hartley PS, Savill J, Brown SB. The death of human platelets during incubation in citrated plasma involves shedding of CD42b and aggregation of dead platelets. Thromb Haemost. 2006;95(1):100-106.
93. Michelson AD, Adelman B, Barnard MR, Carroll E, Handin RI. Platelet storage results in a redistribution of glycoprotein Ib
94. molecules. Evidence for a large intraplatelet pool of glycoprotein Ib. J Clin Invest. 1988; 81(6):1734-1740.
95. Kostelijk EH, Folman CC, Gouwerok CW, Kramer CM, Verhoeven AJ, de Korte D. Increase in glycocalicin levels in platelet concentrates stored in plasma or synthetic medium for 8 days: comparison with other platelet activation markers. Vox Sang. 2000;79(1):21-26.
96. Canault M, Duerschmied D, Brill A, et al. p38 mitogen-activated protein kinase activation during platelet storage: consequences for platelet recovery and hemostatic function in vivo. Blood. 2010;115(9):1835-1842.
97. Liang X, Russell SR, Estelle S, et al. Specific inhibition of ectodomain shedding of glycoprotein Iba by targeting its juxtamembrane shedding cleavage site. J Thromb Haemost. 2013;11(12):2155-2162.
98. Murphy S, Gardner FH. Effect of storage temperature on maintenance of platelet viability–deleterious effect of refrigerated
99. storage. N Engl J Med. 1969;280(20): 1094-1098.
100. van der Wal DE, Du VX, Lo KS, Rasmussen JT, Verhoef S, Akkerman JW. Platelet apoptosis by cold-induced glycoprotein Iba clustering. J Thromb Haemost. 2010;8(11): 2554-2562.
101. Badlou BA, Spierenburg G, Ulrichts H, Deckmyn H, Smid WM, Akkerman JW. Role of glycoprotein Ibalpha in phagocytosis of platelets by macrophages. Transfusion. 2006;46(12):2090-2099.
102. van der Wal DE, Gitz E, Du VX, et al. Arachidonic acid depletion extends survival of cold-stored platelets by interfering with the [glycoprotein Iba–14-3-3z] association. Haematologica. 2012;97(10):1514-1522.
103. Chen W, Druzak SA, Wang Y, et al. Refrigeration-induced binding of von Willebrand factor facilitates fast clearance of refrigerated platelets. Arterioscler Thromb Vasc Biol. 2017;37(12):2271-2279.