Red blood cells induce necroptosis of lung endothelial cells and increase susceptibility to lung inflammation

American Journal of Respiratory and Critical Care Medicine

Volumn 190, Issue 11, 2014, Pages 1243-1254

  Qing, Danielle Y ^a   Conegliano, David ^b   Shashaty, Michael G S ^a   Seo, Jeongyun ^b   Reilly, John P ^a   Worthen, G Scott ^c   Huh, Dongeun ^b   Meyer, Nuala J ^a   Mangalmurti, Nilam S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Endothelial; HMGB1; Necroptosis; RBC transfusion; RIP3

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN;

ANIMAL; CRITICAL ILLNESS; DISEASE MODEL; ENDOTHELIUM CELL; ERYTHROCYTE TRANSFUSION; HUMAN; IMMUNOLOGY; IN VITRO STUDY; LUNG; MIDDLE AGED; MOUSE; NECROSIS; PATHOLOGY; PHYSIOLOGY; PNEUMONIA; RESPIRATORY DISTRESS SYNDROME, ADULT;

ANIMALS; CRITICAL ILLNESS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ERYTHROCYTE TRANSFUSION; HMGB1 PROTEIN; HUMANS; IN VITRO TECHNIQUES; LUNG; MICE; MIDDLE AGED; NECROSIS; PNEUMONIA; RESPIRATORY DISTRESS SYNDROME, ADULT;

EID: 84916211940     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201406-1095OC     Document Type: Article

References (53)

1. Hébert PC, Wells G, Blajchman MA, Marshall J, Martin C, Pagliarello G, Tweeddale M, Schweitzer I, Yetisir E; Transfusion Requirements in Critical Care Investigators, Canadian Critical Care Trials Group. A multicenter, randomized, controlled clinical trial of transfusion requirements in critical care. N Engl J Med 1999;340:409-417.
2. Gong MN, Thompson BT, Williams P, Pothier L, Boyce PD, Christiani DC. Clinical predictors of and mortality in acute respiratory distress syndrome: potential role of red cell transfusion. Crit Care Med 2005;33:1191-1198.
3. Croce MA, Tolley EA, Claridge JA, Fabian TC. Transfusions result in pulmonary morbidity and death after a moderate degree of injury. J Trauma 2005;59:19-23; discussion 23-14.
4. Corwin HL, Gettinger A, Pearl RG, Fink MP, Levy MM, Abraham E, MacIntyre NR, Shabot MM, Duh MS, Shapiro MJ. The CRIT Study: Anemia and blood transfusion in the critically ill-current clinical practice in the United States. Crit Care Med 2004;32:39-52.
5. Kor DJ, Kashyap R, Weiskopf RB, Wilson GA, van Buskirk CM, Winters JL, Malinchoc M, Hubmayr RD, Gajic O. Fresh red blood cell transfusion and short-term pulmonary, immunologic, and coagulation status: a randomized clinical trial. Am J Respir Crit Care Med 2012;185:842-850.
6. Koch CG, Li L, Sessler DI, Figueroa P, Hoeltge GA, Mihaljevic T, Blackstone EH. Duration of red-cell storage and complications after cardiac surgery. N Engl J Med 2008;358:1229-1239.
7. Janz DR, Zhao Z, Koyama T, May AK, Bernard GR, Bastarache JA, Young PP, Ware LB. Longer storage duration of red blood cells is associated with an increased risk of acute lung injury in patients with sepsis. Ann Intensive Care 2013;3:33.
8. Silverboard H, Aisiku I, Martin GS, Adams M, Rozycki G, Moss M. The role of acute blood transfusion in the development of acute respiratory distress syndrome in patients with severe trauma. J Trauma 2005;59:717-723.
9. Zilberberg MD, Carter C, Lefebvre P, Raut M, Vekeman F, Duh MS, Shorr AF. Red blood cell transfusions and the risk of acute respiratory distress syndrome among the critically ill: a cohort study. Crit Care 2007;11:R63.
10. Holena DN, Netzer G, Localio R, Gallop RJ, Bellamy SL, Meyer NJ, Shashaty MG, Lanken PN, Kaplan S, Reilly PM, et al. The association of early transfusion with acute lung injury in patients with severe injury. J Trauma Acute Care Surg 2012;73:825-831.
11. Mangalmurti NS, Chatterjee S, Cheng G, Andersen E, Mohammed A, Siegel DL, Schmidt AM, Albelda SM, Lee JS. Advanced glycation end products on stored red blood cells increase endothelial reactive oxygen species generation through interaction with receptor for advanced glycation end products. Transfusion 2010;50:2353-2361.
12. Mangalmurti NS, Friedman JL, Wang LC, Stolz D, Muthukumaran G, Siegel DL, Schmidt AM, Lee JS, Albelda SM. The receptor for advanced glycation end products mediates lung endothelial activation by RBCs. Am J Physiol Lung Cell Mol Physiol 2013;304:L250-L263.
13. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418:191-195.
14. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, et al. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999;285:248-251.
15. Wang H, Yang H, Czura CJ, Sama AE, Tracey KJ. HMGB1 as a late mediator of lethal systemic inflammation. Am J Respir Crit Care Med 2001;164:1768-1773.
16. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, Sohn JW, Yamada S, Maruyama I, Banerjee A, et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 2006;290:C917-C924.
17. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004;279:7370-7377.
18. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, Liu J, Antonelli A, Preti A, Raeli L, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 2012;209:1519-1528.
19. Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, Giazzon M, Dumitriu IE, Müller S, Iannacone M, Traversari C, et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 2004;5:825-830.
20. Mangalmurti NS, Danielle Q, Worthen GS. Stored RBCs modulate the lung inflammatory response through HMGB1 release [abstract]. Am J Respir Crit Care Med 2014;189:A5759.
21. Wong HR, Lindsell CJ, Pettilä V, Meyer NJ, Thair SA, Karlsson S, Russell JA, Fjell CD, Boyd JH, Ruokonen E, et al. A multibiomarker-based outcome risk stratification model for adult septic shock. Crit Care Med 2014;42:781-789.
22. Reilly JP, Meyer NJ, Shashaty MG, Feng R, Lanken PN, Gallop R, Kaplan S, Herlim M, Oz NL, Hiciano I, et al. ABO blood type a is associated with increased risk of acute respiratory distress syndrome in caucasians following both major trauma and severe sepsis. Chest 2014;145:753-761.
23. Kaiser WJ, Sridharan H, Huang C, Mandal P, Upton JW, Gough PJ, Sehon CA, Marquis RW, Bertin J, Mocarski ES. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J Biol Chem 2013;288:31268-31279.
24. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 2009;137:1112-1123.
25. Sun L, Wang H, Wang Z, He S, Chen S, Liao D, Wang L, Yan J, Liu W, Lei X, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012;148:213-227.
26. Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat Rev Mol Cell Biol 2010;11:700-714.
27. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, Lin SC, Dong MQ, Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009;325:332-336.
28. Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG, Alvarez-Diaz S, Lewis R, Lalaoui N, Metcalf D, Webb AI, et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 2013;39:443-453.
29. Xie T, Peng W, Yan C, Wu J, Gong X, Shi Y. Structural insights into RIP3-mediated necroptotic signaling. Cell Reports 2013;5:70-78.
30. Wu YT, Tan HL, Huang Q, Sun XJ, Zhu X, Shen HM. zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFα mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ 2011;18:26-37.
31. Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005;1:112-119.
32. Kiefmann R, Rifkind JM, Nagababu E, Bhattacharya J. RBC induce hypoxic lung inflammation. Blood 2008;111:5205-5214.
33. Huh D, Leslie DC, Matthews BD, Fraser JP, Jurek S, Hamilton GA, Thorneloe KS, McAlexander MA, Ingber DE. A human disease model of drug toxicity-induced pulmonary edema in a lung-on-a-chip microdevice. Sci Transl Med 2012;4:159ra147.
34. Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science 2010;328:1662-1668.
35. Bell CW, Jiang W, Reich CF III, Pisetsky DS. The extracellular release of HMGB1 during apoptotic cell death. Am J Physiol Cell Physiol 2006;291:C1318-C1325.
36. Jiang W, Bell CW, Pisetsky DS. The relationship between apoptosis and high-mobility group protein 1 release from murine macrophages stimulated with lipopolysaccharide or polyinosinic-polycytidylic acid. J Immunol 2007;178:6495-6503.
37. Li J, McQuade T, Siemer AB, Napetschnig J, Moriwaki K, Hsiao YS, Damko E, Moquin D, Walz T, McDermott A, et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 2012;150:339-350.
38. Mangalmurti NS, Xiong Z, Hulver M, Ranganathan M, Liu XH, Oriss T, Fitzpatrick M, Rubin M, Triulzi D, Choi A, et al. Loss of red cell chemokine scavenging promotes transfusion-related lung inflammation. Blood 2009;113:1158-1166.
39. Li J, Wang H, Mason JM, Levine J, Yu M, Ulloa L, Czura CJ, Tracey KJ, Yang H. Recombinant HMGB1 with cytokine-stimulating activity. J Immunol Methods 2004;289:211-223.
40. Hreggvidsdottir HS, Ostberg T, Wähämaa H, Schierbeck H, Aveberger AC, Klevenvall L, Palmblad K, Ottosson L, Andersson U, Harris HE. The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J Leukoc Biol 2009;86:655-662.
41. Gibot S, Massin F, Cravoisy A, Barraud D, Nace L, Levy B, Bollaert PE. High-mobility group box 1 protein plasma concentrations during septic shock. Intensive Care Med 2007;33:1347-1353.
42. Nakamura T, Sato E, Fujiwara N, Kawagoe Y, Maeda S, Yamagishi S. Increased levels of soluble receptor for advanced glycation end products (sRAGE) and high mobility group box 1 (HMGB1) are associated with death in patients with acute respiratory distress syndrome. Clin Biochem 2011;44:601-604.
43. Wolfson RK, Chiang ET, Garcia JG. HMGB1 induces human lung endothelial cell cytoskeletal rearrangement and barrier disruption. Microvasc Res 2011;81:189-197.
44. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, Suffredini AF. Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 2003;101:2652-2660.
45. Treutiger CJ, Mullins GE, Johansson AS, Rouhiainen A, Rauvala HM, Erlandsson-Harris H, Andersson U, Yang H, Tracey KJ, Andersson J, et al. High mobility group 1 B-box mediates activation of human endothelium. J Intern Med 2003;254:375-385.
46. Wolfson RK, Mapes B, Garcia JG. Excessive mechanical stress increases HMGB1 expression in human lung microvascular endothelial cells via STAT3. Microvasc Res 2014;92:50-55.
47. Khan MJ, Rizwan Alam M, Waldeck-Weiermair M, Karsten F, Groschner L, Riederer M, Hallström S, Rockenfeller P, Konya V, Heinemann A, et al. Inhibition of autophagy rescues palmitic acid-induced necroptosis of endothelial cells. J Biol Chem 2012;287:21110-21120.
48. Andonegui G, Zhou H, Bullard D, Kelly MM, Mullaly SC, McDonald B, Long EM, Robbins SM, Kubes P. Mice that exclusively express TLR4 on endothelial cells can efficiently clear a lethal systemic Gram-negative bacterial infection. J Clin Invest 2009;119:1921-1930.
49. Kaiser WJ, Upton JW, Long AB, Livingston-Rosanoff D, Daley-Bauer LP, Hakem R, Caspary T, Mocarski ES. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature 2011;471:368-372.
50. Yang Y, Ma J, Chen Y, Wu M. Nucleocytoplasmic shuttling of receptor-interacting protein 3 (RIP3): identification of novel nuclear export and import signals in RIP3. J Biol Chem 2004;279:38820-38829.
51. Festjens N, Vanden Berghe T, Cornelis S, Vandenabeele P. RIP1, a kinase on the crossroads of a cell's decision to live or die. Cell Death Differ 2007;14:400-410.
52. Vanlangenakker N, Vanden Berghe T, Vandenabeele P. Many stimuli pull the necrotic trigger, an overview. Cell Death Differ 2012;19:75-86.
53. Abraham E, Arcaroli J, Carmody A, Wang H, Tracey KJ. HMG-1 as a mediator of acute lung inflammation. J Immunol 2000;165:2950-2954.