The impact of bilirubin ditaurate on platelet quality during storage

References

• Jackson SP, Schoenwaelder SM. Procoagulant platelets: are they necrotic? Blood 2010;116(12):2011–2018. doi:10.1182/blood-2010-01-261669
   PubMed Web of Science ®Google Scholar
• Schubert P, Devine DV. Towards targeting platelet storage lesion-related signaling pathways. Blood Transfus 2010;8(Suppl 3):s69–s72. doi:10.2450/2010.011S
   PubMedGoogle Scholar
• Árnason NÁ, Sigurjónsson ÓE. New strategies to understand platelet storage lesion. ISBT Sci Ser 2017;12(4):496–500. doi:10.1111/voxs.12394
   Google Scholar
• Shrivastava M. The platelet storage lesion. Transfus Apheresis Sci 2009;41(2):105–113. doi:10.1016/j.transci.2009.07.002
   PubMed Web of Science ®Google Scholar
• Lannan KL, Refaai MA, Ture SK, Morrell CN, Blumberg N, Phipps RP, Spinelli SL. Resveratrol preserves the function of human platelets stored for transfusion. Br J Haematol 2016;172(5):794–806. doi:10.1111/bjh.13862
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1111/j.1365-3148.2010.01065.x
   PubMed Web of Science ®Google Scholar
• Mohammed BM, Sanford KW, Fisher BJ, Martin EJ, Contaifer D Jr, Warncke UO, Wijesinghe DS, Chalfant CE, Brophy DF, Fowler AA III, et al. Impact of high dose vitamin C on platelet function. World J Crit Care Med 2017;6(1):37. doi:10.5492/wjccm.v6.i1.37
   PubMedGoogle Scholar
• Matsumura K, Takayama H, Bae JY, Kurihara M, Tsutsumi S, Hyon S-H. Preservation of platelets by adding epigallocatechin-3-O-gallate to platelet concentrates. Cell Transplant 2009;18(5–6):521–528. doi:10.1177/096368970901805-606
   PubMed Web of Science ®Google Scholar
• Hosseini E, Ghasemzadeh M, Atashibarg M, Haghshenas M. ROS scavenger, N-acetyl-l-cysteine and NOX specific inhibitor, VAS2870 reduce platelets apoptosis while enhancing their viability during storage. Transfusion 2019;59(4):1333–1343. doi:10.1111/trf.15114
   PubMed Web of Science ®Google Scholar
• Johnson L, Marks D. Treatment of platelet concentrates with the mirasol pathogen inactivation system modulates platelet oxidative stress and NF-κB activation. Transfus Med Hemother 2015;42(3):167–173. doi:10.1159/000403245
   PubMed Web of Science ®Google Scholar
• Skripchenko A, Myrup A, Thompson-Montgomery D, Awatefe H, Moroff G, Wagner SJ. Periods without agitation diminish platelet mitochondrial function during storage. Transfusion 2010;50(2):390–399. doi:10.1111/j.1537-2995.2009.02450.x
   PubMed Web of Science ®Google Scholar
• Schubert P, Johnson L, Marks DC, Devine DV. Ultraviolet-based pathogen inactivation systems: untangling the molecular targets activated in platelets. Front Med 2018;5(MAY):1–10. doi:10.3389/fmed.2018.00129
   Google Scholar
• Ekaney ML, Grable MA, Powers WF, McKillop IH, Evans SL. Cytochrome c and resveratrol preserve platelet function during cold storage. J Trauma Acute Care Surg 2017;83(2):271–277. doi:10.1097/TA.0000000000001547
   PubMed Web of Science ®Google Scholar
• Kundur AR, Singh I, Bulmer AC. Bilirubin, platelet activation and heart disease: A missing link to cardiovascular protection in Gilbert’s syndrome? Atherosclerosis 2015;239(1):73–84. doi:10.1016/j.atherosclerosis.2014.12.042
   PubMed Web of Science ®Google Scholar
• Bulmer AC, Bakrania B, Du Toit EF, Boon AC, Clark PJ, Powell LW, Wagner KH, Headrick JP. Bilirubin acts as a multipotent guardian of cardiovascular integrity: more than just a radical idea. Am J Physiol Heart Circ Physiol 2018;315(3):H429–H447. doi:10.1152/ajpheart.00417.2017
   PubMed Web of Science ®Google Scholar
• Vasavda C, Kothari R, Malla AP, Tokhunts R, Lin A, Ji M, Ricco C, Xu R, Saavedra HG, Sbodio JI, et al. Bilirubin links heme metabolism to neuroprotection by scavenging superoxide. Cell Chem Biol 2019:1–11. doi:10.1016/j.chembiol.2019.07.006
   PubMed Web of Science ®Google Scholar
• Pennell EN, Wagner KH, Mosawy S, Bulmer AC. Acute bilirubin ditaurate exposure attenuates ex vivo platelet reactive oxygen species production, granule exocytosis and activation. Redox Biol 2019;26(April):101250. doi:10.1016/j.redox.2019.101250
   PubMedGoogle Scholar
• Kundur AR, Bulmer AC, Singh I. Unconjugated bilirubin inhibits collagen induced platelet activation. Platelets 2014;25(1):45–50. doi:10.3109/09537104.2013.764405
   PubMed Web of Science ®Google Scholar
• Čvorović J, Passamonti S. Membrane transporters for bilirubin and its conjugates: A systematic review. Front Pharmacol 2017;8(DEC). doi:10.3389/fphar.2017.00887
   PubMedGoogle Scholar
• Kundur AR, Santhakumar AB, Bulmer AC, Singh I. Mildly elevated unconjugated bilirubin is associated with reduced platelet activation-related thrombogenesis and inflammation in Gilbert’s syndrome. Platelets 2017;28(8):779–785. doi:10.1080/09537104.2017.1280146
   PubMed Web of Science ®Google Scholar
• Mosawy S, Jackson DE, Woodman OL, Linden MD. Inhibition of platelet-mediated arterial thrombosis and platelet granule exocytosis by 3ʹ,4ʹ-dihydroxyflavonol and quercetin. Platelets 2013;24(8):594–604. doi:10.3109/09537104.2012.749396
   PubMed Web of Science ®Google Scholar
• Zeck J, Schallheim J, Lew SQ, DePalma L. Whole blood platelet aggregation and release reaction testing in uremic patients. Biomed Res Int 2013;2013:1–6. doi:10.1155/2013/486290
   Web of Science ®Google Scholar
• Di Michele M, Goubau C, Waelkens E, Thys C, De Vos R, Overbergh L, Schyns T, Buyse G, Casaer P, Van Geet C, et al. Functional studies and proteomics in platelets and fibroblasts reveal a lysosomal defect with increased cathepsin-dependent apoptosis in ATP1A3 defective alternating hemiplegia of childhood. J Proteomics 2013;86:53–69. doi:10.1016/j.jprot.2013.05.005
   PubMed Web of Science ®Google Scholar
• Holme S, Moroff G, Murphy S. 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. doi:10.1046/j.1537-2995.1998.38198141495.x
   PubMed Web of Science ®Google Scholar
• Kreutz RP, Nystrom P, Kreutz Y, Miao J, Kovacs R, Desta Z, Flockhart DA, Jin Y, Kreutz RP, Nystrom P, et al. Inhibition of platelet aggregation by prostaglandin E1 (PGE1) in diabetic patients during therapy with clopidogrel and aspirin. Platelets 2013;7104(2):145–150. doi:10.3109/09537104.2012.661107
   Google Scholar
• Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA. Mitochondrial membrane potential probes and the proton gradient: A practical usage guide. BioTechniques 2011;50(2):98–115. doi:10.2144/000113610
   PubMed Web of Science ®Google Scholar
• Verhoeven AJ, Verhaar R, Gouwerok EGW, De Korte D. The mitochondrial membrane potential in human platelets: A sensitive parameter for platelet quality. Transfusion 2005;45(1):82–89. doi:10.1111/j.1537-2995.2005.04023.x
   PubMed Web of Science ®Google Scholar
• Shiels RG, Vidimce J, Pearson AG, Matthews B, Wagner KH, Battle AR, Sakellaris H, Bulmer AC. Unprecedented microbial conversion of Biliverdin into Bilirubin-10-sulfonate. Sci Rep 2019;9(1):2988. doi:10.1038/s41598-019-39548-w
   PubMedGoogle Scholar
• Kularatnam GAM, Dilanthi HW, Vidanapathirana DM, Jayasena S, Jasinge E, Silva GNN, Liyanarachchi KLAMS, Wickramasinghe P, Devgun MS, Barbu V, et al. Dubin-Johnson syndrome and intrahepatic cholestasis of pregnancy in a Sri Lankan family: A case report. BMC Res Notes 2017;10(1):1–5. doi:10.1186/s13104-017-2811-6
   PubMedGoogle Scholar
• Chacko BK, Kramer PA, Ravi S, Johnson MS, Hardy RW, Ballinger SW, Darley-Usmar VM. Methods for defining distinct bioenergetic profiles in platelets, lymphocytes, monocytes, and neutrophils, and the oxidative burst from human blood. Lab Invest 2013;93(6):690–700. doi:10.1038/labinvest.2013.53
   PubMed Web of Science ®Google Scholar
• Fuentes E, Araya-Maturana R, Urra FA. Regulation of mitochondrial function as a promising target in platelet activation-related diseases. Free Radical Biol Med 2019;136:172–182. doi:10.1016/j.freeradbiomed.2019.01.007
   PubMed Web of Science ®Google Scholar
• Skripchenko A, Myrup A, Thompson-Montgomery D, Awatefe H, Wagner SJ. Mitochondrial dysfunction of platelets stored in first- and second-generation containers is, in part, associated with elevated carbon dioxide levels. Transfusion 2011;51(2):371–379. doi:10.1111/j.1537-2995.2010.02829.x
   PubMed Web of Science ®Google Scholar
• Amorini AM, Tuttobene M, Tomasello FM, Biazzo F, Gullotta S, De Pinto V, Lazzarino G, Tavazzi B. Glucose ameliorates the metabolic profile and mitochondrial function of platelet concentrates during storage in autologous plasma. Blood Transfus 2013;11(1):61–70. doi:10.2450/2012.0145-11
   PubMed Web of Science ®Google Scholar
• Johnson L, Loh YS, Kwok M, Marks DC. In vitro assessment of buffy-coat derived platelet components suspended in SSP+ treated with the INTERCEPT blood system. Transfus Med 2013;23(2):121–129. doi:10.1111/tme.12020
   PubMed Web of Science ®Google Scholar
• Johnson L, Schubert P, Tan S, Devine DV, Marks DC. Extended storage and glucose exhaustion are associated with apoptotic changes in platelets stored in additive solution. Transfusion 2015;56(February). doi:10.1111/trf.13345
   PubMedGoogle Scholar
• Capocelli KE, Dumont LJ. Novel platelet storage conditions: additive solutions, gas, and cold. Curr Opin Hematol 2014;21(6):491–496. doi:10.1097/MOH.0000000000000081
   PubMed Web of Science ®Google Scholar
• Saunders C, Rowe G, Wilkins K, Holme S, Collins P. In vitro storage characteristics of platelet concentrates suspended in 70% SSP+TM additive solution versus plasma over a 14-day storage period. Vox Sang 2011;101(2):112–121. doi:10.1111/j.1423-0410.2011.01468.x
   PubMed Web of Science ®Google Scholar
• Johnson L, Winter KM, Hartkopf-Theis T, Reid S, Kwok M, Marks DC. Evaluation of the automated collection and extended storage of apheresis platelets in additive solution. Transfusion 2012;52(3):503–509. doi:10.1111/j.1537-2995.2011.03314.x
   PubMed Web of Science ®Google Scholar
• Seghatchian J, Krailabsiri P. The platelet storage lesion. Clin Lab Med 2010;30(2):475–487. doi:10.1016/j.cll.2010.02.002
   PubMed Web of Science ®Google Scholar
• Smethurst PA. Aging of platelets stored for transfusion. Platelets 2016;27(6):526–534. doi:10.3109/09537104.2016.1171303
   PubMed Web of Science ®Google Scholar
• Zeddies S, De Cuyper IM, Van Der Meer PF, Daal BB, De Korte D, Gutiérrez L, Thijssen-Timmer DC. Pathogen reduction treatment using riboflavin and ultraviolet light impairs platelet reactivity toward specific agonists in vitro. Transfusion 2014;54(9):2292–2300. doi:10.1111/trf.12636
   PubMed Web of Science ®Google Scholar
• Cap AP. Platelet storage: A license to chill! Transfusion 2016;56(1):13–16. doi:10.1111/trf.13433
   PubMed Web of Science ®Google Scholar
• Pereira J, Soto M, Paloma I, Ocqueteau M, Coetzee LM, Astudillo S, Aranda E, Mezzano D. Platelet aging in vivo is associated with activation of apoptotic pathways: studies in a model of suppressed thrombopoiesis in dogs. Thromb Haemost 2002;87(5):905–909. doi:10.1055/s-0037-1613103
   PubMed Web of Science ®Google Scholar
• Schoenwaelder SM, Yuan Y, Josefsson EC, White MJ, Yao Y, Mason KD, O’Reilly LA, Henley KJ, Ono A, Hsiao S, et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. 2012;114(3):663–667. doi:10.1182/blood-2009-01-200345
   Google Scholar
• 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 metalloproteinases. J Thromb Haemost 2007;5(7):1530–1537. doi:10.1111/j.1538-7836.2007.02590.x
   PubMed Web of Science ®Google Scholar
• Bergmeier W, Piffath CL, Cheng G, Dole VS, Zhang Y, Von Andrian UH, Wagner DD. Tumor necrosis factor-α-converting enzyme (ADAM17) mediates GPIbα shedding from platelets in vitro and in vivo. Circ Res 2004;95(7):677–683. doi:10.1161/01.RES.0000143899.73453.11
   PubMed Web of Science ®Google Scholar
• Au AE, Josefsson EC. Regulation of platelet membrane protein shedding in health and disease. Platelets 2017;28(4):342–353. doi:10.1080/09537104.2016.1203401
   PubMed Web of Science ®Google Scholar
• Canault M, Duerschmied D, Brill A, Stefanini L, Schatzberg D, Cifuni SM, Bergmeier W, Wagner DD. p38 mitogen-activated protein kinase activation during platelet storage: consequences for platelet recovery and hemostatic function in vivo. Blood 2010;115(9):1835–1842. doi:10.1182/blood-2009-03-211706
   PubMed Web of Science ®Google Scholar
• Brill A, Chauhan AK, Canault M, Walsh MT, Bergmeier W, Wagner DD. Oxidative stress activates ADAM17/TACE and induces its target receptor shedding in platelets in a p38-dependent fashion. Cardiovasc Res 2009;84(1):137–144. doi:10.1093/cvr/cvp176
   PubMed Web of Science ®Google Scholar
• Bergmeier W, Burger PC, Piffath CL, Hoffmeister KM, Hartwig JH, Nieswandt B, Wagner DD. Metalloproteinase inhibitors improve the recovery and hemostatic function of in vitro-aged or -injured mouse platelets. Blood 2003;102(12):4229–4235. doi:10.1182/blood-2003-04-1305
   PubMed Web of Science ®Google Scholar
• Jansen AJG, Josefsson EC, Rumjantseva V, Liu QP, Falet H, Bergmeier W, Cifuni SM, Sackstein R, Von Andrian UH, Wagner DD, et al. Desialylation accelerates platelet clearance after refrigeration and initiates GPIbα metalloproteinase-mediated cleavage in mice. Blood 2012;119(5):1263–1273. doi:10.1182/blood-2011-05-355628
   PubMed Web of Science ®Google Scholar
• Ghasemzadeh M, Hosseini E, Roudsari ZO, Zadkhak P. Intraplatelet reactive oxygen species (ROS) correlate with the shedding of adhesive receptors, microvesiculation and platelet adhesion to collagen during storage: does endogenous ROS generation downregulate platelet adhesive function? Thromb Res 2018;163(February):153–161. doi:10.1016/j.thromres.2018.01.048
   PubMedGoogle Scholar
• Vizetto C, Duarte G. Reactivity of human fetal and adult immortalized hepatocytes to potentially toxic bilirubin and bile acid species; 2009.
   Google Scholar
• NaveenKumar, S., Thushara, R., Sundaram, M., Hemshekhar, M., Paul, M., Thirunavukkarasu, C., Basappa, B., Nagaraju, G., Raghavan, S., Girish, K., Kemparaju, K. and Rangappa, K. Unconjugated bilirubin exerts pro-apoptotic effect on platelets via p38-MAPK activation. Sci Rep 2015;5:15045. doi:10.1038/srep15045
   PubMed Web of Science ®Google Scholar
• Lang E, Gatidis S, Freise NF, Bock H, Kubitz R, Lauermann C, Orth HM, Klindt C, Schuier M, Keitel V, et al. Conjugated bilirubin triggers anemia by inducing erythrocyte death. Hepatology 2015;61(1):275–284. doi:10.1002/hep.27338
   PubMed Web of Science ®Google Scholar
• Maghzal GJ, Leck MC, Collinson E, Li C, Stocker R. Limited role for the bilirubin-biliverdin redox amplification cycle in the cellular antioxidant protection by biliverdin reductase. J Biol Chem 2009;284(43):29251–29259. doi:10.1074/jbc.M109.037119
   PubMed Web of Science ®Google Scholar
• Neubrand MW, Carey MC, Laue TM. Self-assembly of aqueous bilirubin ditaurate, a natural conjugated bile pigment, to contraposing enantiomeric dimers and M(-) and P(+) tetramers and their selective hydrophilic disaggregation by monomers and micelles of bile salts. Biochemistry 2015;54(7):1542–1557. doi:10.1021/bi501251v
   PubMed Web of Science ®Google Scholar
• Benzie IFF, Strain JJ. Ferric reducing (antioxidant) power as a measure of antioxidant capacity: the FRAP assay. Anal Biochem 1999;299:15–36. doi:10.1006/abio.1996.0292
   Google Scholar
• Bulmer AC, Blanchfield JT, Coombes JS, Toth I. In vitro permeability and metabolic stability of bile pigments and the effects of hydrophilic and lipophilic modification of biliverdin. Bioorg Med Chem 2008;16(7):3616–3625. doi:10.1016/j.bmc.2008.02.008
   PubMed Web of Science ®Google Scholar
• Strassburg CP. Hyperbilirubinemia syndromes (Gilbert-Meulengracht, Crigler-Najjar, Dubin-Johnson, and Rotor syndrome). Best Pract Res Clin Gastroenterol 2010;24(5):555–571. doi:10.1016/j.bpg.2010.07.007
   PubMed Web of Science ®Google Scholar
• Gaughen K, Albeiruti R, Greenwood C, Kelbel TE. Index of suspicion in the nursery. NeoReviews 2014;15(12):e546–e549. doi:10.1542/neo.15-12-e546
   Google Scholar