Red blood cell washing, nitrite therapy, and antiheme therapies prevent stored red blood cell toxicity after trauma-hemorrhage

Free Radical Biology and Medicine

Volumn 85, Issue , 2015, Pages 207-218

  Stapley, Ryan ^a   Rodriguez, Cilina ^b   Oh, Joo Yeun ^a   Honavar, Jaideep ^a   Brandon, Angela ^a   Wagener, Brant M ^c   Marques, Marisa B ^a   Weinberg, Jordan A ^e   Kerby, Jeffrey D ^b   Pittet, Jean Francois ^c,d   Patel, Rakesh P ^a,d  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Acute lung injury; Heme; Hemin; Hemoglobin; Nitric oxide; Resuscitation; Storage lesion

Indexed keywords

HEME; HEMIN; HEMOGLOBIN; HEMOPEXIN; METHEMOGLOBIN; NITRIC OXIDE; NITRITE; OXYHEMOGLOBIN; RESATORVID; TOLL LIKE RECEPTOR 4;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOAVAILABILITY; BLEEDING; BLOOD PRESSURE; BLOOD STORAGE; BLOOD TOXICITY; BLOOD TRANSFUSION REACTION; CONTROLLED STUDY; ERYTHROCYTE TOXICITY; ERYTHROCYTE TRANSFUSION; ERYTHROCYTE WASHING; HEMATOCRIT; HEMOLYSIS; HUMAN; HUMAN CELL; INJURY SEVERITY; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATION; OXIDATION KINETICS; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROCEDURES CONCERNING CELLS; PROTEIN DENATURATION; SIGNAL TRANSDUCTION; SURVIVAL; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CYTOLOGY; ERYTHROCYTE; HEMORRHAGE; WOUNDS AND INJURIES;

MURINAE;

ANIMALS; ERYTHROCYTES; HEME; HEMORRHAGE; HUMANS; MICE; MICE, INBRED C57BL; NITRITES; WOUNDS AND INJURIES;

EID: 84935004948     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.04.025     Document Type: Article

References (49)

1. D. Wang, J. Sun, S.B. Solomon, H.G. Klein, and C. Natanson Transfusion of older stored blood and risk of death: a meta-analysis Transfusion 52 2012 1184 1195
2. J.A. Weinberg, S.R. Barnum, and R.P. Patel Red blood cell age and potentiation of transfusion-related pathology in trauma patients Transfusion 51 2011 867 873
3. J.A. Weinberg, G. McGwin Jr., M.B. Marques, S.A. Cherry III, D.A. Reiff, J.D. Kerby, and L.W. Rue III Transfusions in the less severely injured: does age of transfused blood affect outcomes? J. Trauma 65 2008 794 798
4. J.A. Weinberg, G. McGwin Jr., M.J. Vandromme, M.B. Marques, S.M. Melton, D.A. Reiff, J.D. Kerby, and L.W. Rue III Duration of red cell storage influences mortality after trauma J. Trauma 69 2010 1427 1431 discussion 1431-1422
5. S.J. Wagner, S.A. Glynn, and L.A. Welniak Products, N. W. G. o. S. t. O. R. B. C. Research opportunities in optimizing storage of red blood cell products Transfusion 54 2014 483 494
6. J.H. Baek, F. D'Agnillo, F. Vallelian, C.P. Pereira, M.C. Williams, Y. Jia, D.J. Schaer, and P.W. Buehler Hemoglobin-driven pathophysiology is an in vivo consequence of the red blood cell storage lesion that can be attenuated in guinea pigs by haptoglobin therapy J. Clin. Invest. 122 2012 1444 1458
7. R.O. Francis, J.S. Jhang, H.P. Pham, E.A. Hod, J.C. Zimring, and S.L. Spitalnik Glucose-6-phosphate dehydrogenase deficiency in transfusion medicine: the unknown risks Vox Sang. 2013
8. M.T. Gladwin, and D.B. Kim-Shapiro Storage lesion in banked blood due to hemolysis-dependent disruption of nitric oxide homeostasis Curr. Opin. Hematol. 16 2009 515 523
9. E.A. Hod, N. Zhang, S.A. Sokol, B.S. Wojczyk, R.O. Francis, D. Ansaldi, K.P. Francis, P. Della-Latta, S. Whittier, S. Sheth, J.E. Hendrickson, J.C. Zimring, G.M. Brittenham, and S.L. Spitalnik Transfusion of red blood cells after prolonged storage produces harmful effects that are mediated by iron and inflammation Blood 115 2010 4284 4292
10. N.S. Mangalmurti, Z. Xiong, M. Hulver, M. Ranganathan, X.H. Liu, T. Oriss, M. Fitzpatrick, M. Rubin, D. Triulzi, A. Choi, and J.S. Lee Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation Blood 113 2009 1158 1166
11. R.M. Belizaire, P.S. Prakash, J.R. Richter, B.R. Robinson, M.J. Edwards, C.C. Caldwell, A.B. Lentsch, and T.A. Pritts Microparticles from stored red blood cells activate neutrophils and cause lung injury after hemorrhage and resuscitation J. Am. Coll. Surg. 214 2012 648 655 discussion 656-647
12. J. Laczko, C.J. Feo, and W. Phillips Discocyte-echinocyte reversibility in blood stored in CPD over a period of 56 days Transfusion 19 1979 379 388
13. S. Ghosh, O.A. Adisa, P. Chappa, F. Tan, K.A. Jackson, D.R. Archer, and S.F. Ofori-Acquah Extracellular hemin crisis triggers acute chest syndrome in sickle mice J. Clin. Invest. 123 2013 4809 4820
14. R. Larsen, R. Gozzelino, V. Jeney, L. Tokaji, F.A. Bozza, A.M. Japiassu, D. Bonaparte, M.M. Cavalcante, A. Chora, A. Ferreira, I. Marguti, S. Cardoso, N. Sepulveda, A. Smith, and M.P. Soares A central role for free heme in the pathogenesis of severe sepsis Sci. Transl. Med. 2 2010 51ra71
15. D.R. Janz, J.A. Bastarache, G. Sills, N. Wickersham, A.K. May, G.R. Bernard, and L.B. Ware Association between haptoglobin, hemopexin and mortality in adults with sepsis Crit. Care 17 2013 R272
16. D.J. Schaer, P.W. Buehler, A.I. Alayash, J.D. Belcher, and G.M. Vercellotti Hemolysis and free hemoglobin revisited: exploring hemoglobin and hemin scavengers as a novel class of therapeutic proteins Blood 121 2013 1276 1284
17. J.D. Belcher, C. Chen, J. Nguyen, L. Milbauer, F. Abdulla, A.I. Alayash, A. Smith, K.A. Nath, R.P. Hebbel, and G.M. Vercellotti Heme triggers TLR4 signaling leading to endothelial cell activation and vaso-occlusion in murine sickle cell disease Blood 123 2014 377 390
18. F.F. Dutra, L.S. Alves, D. Rodrigues, P.L. Fernandez, R.B. de Oliveira, D.T. Golenbock, D.S. Zamboni, and M.T. Bozza Hemolysis-induced lethality involves inflammasome activation by heme Proc. Natl. Acad. Sci. USA 2014
19. C. Donadee, N.J. Raat, T. Kanias, J. Tejero, J.S. Lee, E.E. Kelley, X. Zhao, C. Liu, H. Reynolds, I. Azarov, S. Frizzell, E.M. Meyer, A.D. Donnenberg, L. Qu, D. Triulzi, D.B. Kim-Shapiro, and M.T. Gladwin Nitric oxide scavenging by red blood cell microparticles and cell-free hemoglobin as a mechanism for the red cell storage lesion Circulation 124 2011 465 476
20. R. Stapley, B.Y. Owusu, A. Brandon, M. Cusick, C. Rodriguez, M.B. Marques, J.D. Kerby, S.R. Barnum, J.A. Weinberg, J.R. Lancaster Jr., and R.P. Patel Erythrocyte storage increases rates of NO and nitrite scavenging: implications for transfusion-related toxicity Biochem. J. 446 2012 499 508
21. C. Liu, X. Liu, J. Janes, R. Stapley, R.P. Patel, M.T. Gladwin, and D.B. Kim-Shapiro Mechanism of faster NO scavenging by older stored red blood cells Redox Biol. 2 2014 211 219
22. J.T. Alexander, A.M. El-Ali, J.L. Newman, S. Karatela, B.L. Predmore, D.J. Lefer, R.L. Sutliff, and J.D. Roback Red blood cells stored for increasing periods produce progressive impairments in nitric oxide-mediated vasodilation Transfusion 53 2013 2619 2628
23. H. Zhu, R. Zennadi, B.X. Xu, J.P. Eu, J.A. Torok, M.J. Telen, and T.J. McMahon Impaired adenosine-5'-triphosphate release from red blood cells promotes their adhesion to endothelial cells: a mechanism of hypoxemia after transfusion Crit. Care Med. 39 2011 2478 2486
24. J.D. Reynolds, G.S. Ahearn, M. Angelo, J. Zhang, F. Cobb, and J.S. Stamler S-nitrosohemoglobin deficiency: a mechanism for loss of physiological activity in banked blood Proc. Natl. Acad. Sci. USA 104 2007 17058 17062
25. E. Bennett-Guerrero, T.H. Veldman, A. Doctor, M.J. Telen, T.L. Ortel, T.S. Reid, M.A. Mulherin, H. Zhu, R.D. Buck, R.M. Califf, and T.J. McMahon Evolution of adverse changes in stored RBCs Proc. Natl. Acad. Sci. USA 104 2007 17063 17068
26. I. Cortes-Puch, D. Wang, J. Sun, S.B. Solomon, K.E. Remy, M. Fernandez, J. Feng, T. Kanias, L. Bellavia, D. Sinchar, A. Perlegas, M.A. Solomon, W.E. Kelley, M.A. Popovsky, M.T. Gladwin, D.B. Kim-Shapiro, H.G. Klein, and C. Natanson Washing older blood units before transfusion reduces plasma iron and improves outcomes in experimental canine pneumonia Blood 123 2014 1403 1411
27. R.M. Belizaire, A.T. Makley, E.M. Campion, D.I. Sonnier, M.D. Goodman, W.C. Dorlac, L.A. Friend, A.B. Lentsch, and T.A. Pritts Resuscitation with washed aged packed red blood cell units decreases the proinflammatory response in mice after hemorrhage J. Trauma Acute Care Surg. 73 2012 S128 S133
28. T.S. Isbell, M.T. Gladwin, and R.P. Patel Hemoglobin oxygen fractional saturation regulates nitrite-dependent vasodilation of aortic ring bioassays Am. J. Physiol. Heart Circ. Physiol 293 2007 H2565 H2572
29. R.P. Patel, N. Hogg, N.Y. Spencer, B. Kalyanaraman, S. Matalon, and V.M. Darley-Usmar Biochemical characterization of human S-nitrosohemoglobin. Effects on oxygen binding and transnitrosation J. Biol. Chem. 274 1999 15487 15492
30. B.Y. Owusu, R. Stapley, J. Honavar, and R.P. Patel Effects of erythrocyte aging on nitric oxide and nitrite metabolism Antioxid. Redox Signal. 19 2013 1198 1208
31. C. Rodriguez, D.A. Vitturi, J. He, M. Vandromme, A. Brandon, A. Hutchings, L.W. Rue III, J.D. Kerby, and R.P. Patel Sodium nitrite therapy attenuates the hypertensive effects of HBOC-201 via nitrite reduction Biochem. J. 422 2009 423 432
32. J.C. Zimring, and S.L. Spitalnik On the appropriate use and interpretation of animal models in transfusion medicine research Transfusion 53 2013 2334 2339
33. A.T. Makley, M.D. Goodman, L.A. Friend, J.A. Johannigman, W.C. Dorlac, A.B. Lentsch, and T.A. Pritts Murine blood banking: characterization and comparisons to human blood Shock 34 2010 40 45
34. E. Bennett-Guerrero, B.S. Kirby, H. Zhu, A.E. Herman, N. Bandarenko, and T.J. McMahon Randomized study of washing 40- to 42-day-stored red blood cells Transfusion 2014
35. K.L. Lannan, J. Sahler, S.L. Spinelli, R.P. Phipps, and N. Blumberg Transfusion immunomodulation - the case for leukoreduced and (perhaps) washed transfusions Blood Cells Mol. Dis. 50 2013 61 68
36. V. Harper, J.Y. Oh, R. Stapley, M.B. Marques, L. Wilson, S. Barnes, C.W. Sun, T.M. Townes, and R.P. Patel Peroxiredoxin-2 recycling is inhibited during erythrocyte storage Antioxid. Redox Signal. 2014
37. J.D. Kurach, A.L. Hansen, T.R. Turner, C. Jenkins, and J.P. Acker Segments from red blood cell units should not be used for quality testing Transfusion 54 2014 451 455
38. X. Hu, S.R. Barnum, R.P. Patel, M.B. Marques, and J.A. Weinberg The level of complement activation fragments is higher in red blood cell units than segments Transfus. Apher. Sci. 49 2013 692 693
39. J.A. Weinberg, P.A. MacLennan, M.J. Vandromme-Cusick, J.M. Angotti, L.J. Magnotti, J.D. Kerby, L.W. Rue III, S.R. Barnum, and R.P. Patel Microvascular response to red blood cell transfusion in trauma patients Shock 37 2012 276 281
40. J.A. Weinberg, P.A. MacLennan, M.J. Vandromme-Cusick, L.J. Magnotti, J.D. Kerby, L.W. Rue III, J.M. Angotti, C.A. Garrett, L.E. Hendrick, M.A. Croce, T.C. Fabian, S.R. Barnum, and R.P. Patel The deleterious effect of red blood cell storage on microvascular response to transfusion J. Trauma Acute Care Surg 75 2013 807 812
41. S.E. Nicholson, R.A. Johnson, T. Craig, J.G. Myers, W. Durante, R.M. Stewart, and F.K. Johnson Transfusion-related acute lung injury in a rat model of trauma-hemorrhage J. Trauma 70 2011 466 471
42. C. Lei, B. Yu, M. Shahid, A. Beloiartsev, K.D. Bloch, and W.M. Zapol Inhaled nitric oxide attenuates the adverse effects of transfusing stored syngeneic erythrocytes in mice with endothelial dysfunction after hemorrhagic shock Anesthesiology 117 2012 1190 1202
43. J.A. Weinberg, G. McGwin Jr., R.L. Griffin, V.Q. Huynh, S.A. Cherry III, M.B. Marques, D.A. Reiff, J.D. Kerby, and L.W. Rue III Age of transfused blood: an independent predictor of mortality despite universal leukoreduction J. Trauma 65 2008 279 282 discussion 282-274
44. A.T. Makley, M.D. Goodman, R.M. Belizaire, L.A. Friend, J.A. Johannigman, W.C. Dorlac, A.B. Lentsch, and T.A. Pritts Damage control resuscitation decreases systemic inflammation after hemorrhage J. Surg. Res. 175 2012 e75-82
45. A. Cauwels, E.S. Buys, R. Thoonen, L. Geary, J. Delanghe, S. Shiva, and P. Brouckaert Nitrite protects against morbidity and mortality associated with TNF- or LPS-induced shock in a soluble guanylate cyclase-dependent manner J. Exp. Med. 206 2009 2915 2924
46. P.A. Pickerodt, M.J. Emery, R. Zarndt, W. Martin, R.C. Francis, W. Boemke, and E.R. Swenson Sodium nitrite mitigates ventilator-induced lung injury in rats Anesthesiology 117 2012 592 601
47. A.A. Samal, J. Honavar, A. Brandon, K.M. Bradley, S. Doran, Y. Liu, C. Dunaway, C. Steele, E.M. Postlethwait, G.L. Squadrito, M.V. Fanucchi, S. Matalon, and R.P. Patel Administration of nitrite after chlorine gas exposure prevents lung injury: effect of administration modality Free Radic. Biol. Med. 53 2012 1431 1439
48. J.H. Crawford, T.S. Isbell, Z. Huang, S. Shiva, B.K. Chacko, A.N. Schechter, V.M. Darley-Usmar, J.D. Kerby, J.D. Lang Jr., D. Kraus, C. Ho, M.T. Gladwin, and R.P. Patel Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation Blood 107 2006 566 574
49. I. Yazji, C.P. Sodhi, E.K. Lee, M. Good, C.E. Egan, A. Afrazi, M.D. Neal, H. Jia, J. Lin, C. Ma, M.F. Branca, T. Prindle, W.M. Richardson, J. Ozolek, T.R. Billiar, D.G. Binion, M.T. Gladwin, and D.J. Hackam Endothelial TLR4 activation impairs intestinal microcirculatory perfusion in necrotizing enterocolitis via eNOS-NO-nitrite signaling Proc. Natl. Acad. Sci. USA 110 2013 9451 9456