Anti-human neutrophil antigen-3a induced transfusion-related acute lung injury in mice by direct disturbance of lung endothelial cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 11, 2013, Pages 2538-2548

  Bayat, Behnaz ^a   Tjahjono, Yudy ^a   Sydykov, Akylbek ^b   Werth, Silke ^a   Hippenstiel, Stefan ^c   Weissmann, Nobert ^b   Sachs, Ulrich J ^a   Santoso, Sentot ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

acute lung injury; endothelium; reactive oxygen species

Indexed keywords

ALBUMIN; ANTIGEN; CHOLINE TRANSPORTER LIKE PROTEIN 2; GRANULOCYTE ANTIBODY; HUMAN NEUTROPHIL ANTIGEN 3A; HUMAN NEUTROPHIL ANTIGEN 3A ANTIBODY; HUMAN NEUTROPHIL ANTIGEN 3B ANTIBODY; MEMBRANE PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIAL DYSFUNCTION; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ENDOTHELIUM; LUNG FLUID; LUNG LAVAGE; MEMBRANE PERMEABILITY; MEMBRANE RESISTANCE; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NEUTROPHIL; NEUTROPHIL COUNT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSFUSION RELATED ACUTE LUNG INJURY;

ACUTE LUNG INJURY; ENDOTHELIUM; REACTIVE OXYGEN SPECIES;

ACTINS; ACUTE LUNG INJURY; ANIMALS; ANTIBODIES; BLOOD TRANSFUSION; BRONCHOALVEOLAR LAVAGE FLUID; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HUMANS; ISOANTIGENS; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; NADPH OXIDASE; NEUTROPHILS; RESPIRATORY MUCOSA;

EID: 84887050089     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301206     Document Type: Article

References (55)

1. Kleinman S, Caulfeld T, Chan P, Davenport R, McFarland J, McPhedran S, Meade M, Morrison D, Pinsent T, Robillard P, Slinger P. Toward an understanding of transfusion-related acute lung injury: statement of a consensus panel. Transfusion. 2004;44:1774-1789.
2. Toy P. Transfusion-related acute lung injury: defnition and review. Crit Care Med. 2004; 33: 721-726.
3. Silliman CC, Fung YL, Ball JB, Khan SY. Transfusion-related acute lung injury (TRALI): current concepts and misconceptions. Blood Rev. 2009;23:245-255.
4. Vlaar AP, Schultz MJ, Juffermans NP. Transfusion-related acute lung injury: a change of perspective. Neth J Med. 2009;67:320-326.
5. Popovsky MA, Moore SB. Diagnostic and pathogenetic considerations in transfusion-related acute lung injury. Transfusion. 1985;25:573-577.
6. Sachs UJ. A threshold model for the susceptibility to transfusion-related acute lung injury. Transfus Clin Biol. 2012;19:109-116.
7. Bayat B, Sachs UJ. Transfusion-related acute lung injury: an overview. Curr Pharm Des. 2012;18:3236-3240.
8. Bux J, Sachs UJ. The pathogenesis of transfusion-related acute lung injury (TRALI). Br J Haematol. 2007;136:788-799.
9. Reil A, Keller-Stanislawski B, Günay S, Bux J. Specifcities of leucocyte alloantibodies in transfusion-related acute lung injury and results of leucocyte antibody screening of blood donors. Vo x Sang. 2008;95:313-317.
10. Davoren A, Curtis BR, Shulman IA, Mohrbacher AF, Bux J, Kwiatkowska BJ, McFarland JG, Aster RH. TRALI due to granulocyte-agglutinating human neutrophil antigen-3a (5b) alloantibodies in donor plasma: a report of 2 fatalities. Transfusion. 2003;43:641-645.
11. Makar RS, Powers A, Stowell CP. Reducing transfusion-related acute lung injury risk: evidence for and approaches to transfusion-related acute lung injury mitigation. Transfus Med Rev. 2012;26:305-320.
12. Greinacher A, Wesche J, Hammer E, Fürll B, Völker U, Reil A, Bux J. Characterization of the human neutrophil alloantigen-3a. Nat Med. 2010;16:45-48.
13. Silliman CC, Curtis BR, Kopko PM, Khan SY, Kelher MR, Schuller RM, Sannoh B, Ambruso DR. Donor antibodies to HNA-3a implicated in TRALI reactions prime neutrophils and cause PMN-mediated damage to human pulmonary microvascular endothelial cells in a two-event in vitro model. Blood. 2007;109:1752-1755.
14. Curtis BR, Cox NJ, Sullivan MJ, Konkashbaev A, Bowens K, Hansen K, Aster RH. The neutrophil alloantigen HNA-3a (5b) is located on choline transporter-like protein 2 and appears to be encoded by an R>Q154 amino acid substitution. Blood. 2010;115:2073-2076.
15. Bayat B, Tjahjono Y, Werth S, Berghöfer H, Reil A, Kroll H, Sachs UJ, Santoso S. Implication of transfected cell lines for the detection of alloantibodies against human neutrophil antigen-3. Transfusion. 2012;52:613-621.
16. Xia W, Bayat B, Sachs U, Chen Y, Shao Y, Xu X, Deng J, Ding H, Fu Y, Ye X, Santoso S. The frequencies of human neutrophil alloan-tigens in the Chinese Han population of Guangzhou. Transfusion. 2011;51:1271-1277.
17. Kommareddi PK, Nair TS, Thang LV, Galano MM, Babu E, Ganapathy V, Kanazawa T, McHugh JB, Carey TE. Isoforms, expression, gly-cosylation, and tissue distribution of CTL2/SLC44A2. Protein J. 2010;29:417-426.
18. Nakamura T, Fujiwara R, Ishiguro N, Oyabu M, Nakanishi T, Shirasaka Y, Maeda T, Tamai I. Involvement of choline transporter-like proteins, CTL1 and CTL2, in glucocorticoid-induced acceleration of phospha-tidylcholine synthesis via increased choline uptake. Biol Pharm Bull. 2010;33:691-696.
19. Zhang X, Reed EF. Effect of antibodies on endothelium. Am J Transplant. 2009;9:2459-2465.
20. Schnittler HJ, Wilke A, Gress T, Suttorp N, Drenckhahn D. Role of actin and myosin in the control of paracellular permeability in pig, rat and human vascular endothelium. J Physiol. 1990;431:379-401.
21. Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120-and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem. 2005;280:31906-31912.
22. Hatanaka K, Simons M, Murakami M. Phosphorylation of VE-cadherin controls endothelial phenotypes via p120-catenin coupling and Rac1 activation. Am J Physiol Heart Circ Physiol. 2011;300:H162-H172.
23. Boueiz A, Hassoun PM. Regulation of endothelial barrier function by reactive oxygen and nitrogen species. Microvasc Res. 2009;77:26-34.
24. Jerke U, Rolle S, Dittmar G, Bayat B, Santoso S, Sporbert A, Luft F, Kettritz R. Complement receptor Mac-1 is an adaptor for NB1 (CD177)-mediated PR3-ANCA neutrophil activation. J Biol Chem. 2011;286:7070-7081.
25. Traiffort E, Ruat M, O'Regan S, Meunier FM. Molecular characterization of the family of choline transporter-like proteins and their splice variants. J Neurochem. 2005;92:1116-1125.
26. Shakib F. The Human IgG Subclasses: Molecular Analysis of Structure, Function and Regulation. Oxford: IRL Press; 1990:280.
27. Looney MR, Su X, Van Ziffe JA, Lowell CA, Matthay MA. Neutrophils and their Fc gamma receptors are essential in a mouse model of transfusion-related acute lung injury. J Clin Invest. 2006;116:1615-1623.
28. Steiner AA, Molchanova AY, Dogan MD, Patel S, Pétervári E, Balaskó M, Wanner SP, Eales J, Oliveira DL, Gavva NR, Almeida MC, Székely M, Romanovsky AA. The hypothermic response to bacterial lipopolysaccha-ride critically depends on brain CB1, but not CB2 or TRPV1, receptors. J Physiol. 2011;589(Pt 9):2415-2431.
29. Semple JW, Kim M, Hou J, McVey M, Lee YJ, Tabuchi A, Kuebler WM, Chai ZW, Lazarus AH. Intravenous immunoglobulin prevents murine antibody-mediated acute lung injury at the level of neutrophil reactive oxygen species (ROS) production. PLoS One. 2012;7:e31357.
30. Stroncek DF. Pulmonary transfusion reactions. Semin Hematol. 2007;1:2-14.
31. Frenette PS, Mohandas N. Bad blood: a trigger for TRALI. Nat Med. 2010;16:382-383.
32. Bian H, Reed EF. Alloantibody-mediated class I signal transduction in endothelial cells and smooth muscle cells: enhancement by IFN-gamma and TNF-alpha. J Immunol. 1999;163:1010-1018.
33. Immenschuh S, Rahayu P, Bayat B, Saragih H, Rachman A, Santoso S. Antibodies against dengue nonstructural protein i induce heme oxygen-ase-1 via a redox-dependent pathway in human endothelial cells. Free Radic Biol Med. 2013;54:85-92.
34. Strait RT, Hicks W, Barasa N, Mahler A, Khodoun M, Köhl J, Stringer K, Witte D, Van Rooijen N, Susskind BM, Finkelman FD. MHC class I-specifc antibody binding to nonhematopoietic cells drives complement activation to induce transfusion-related acute lung injury in mice. J Exp Med. 2011;208:2525-2544.
35. Flesch BK, Wesche J, Berthold T, Goldmann T, Hundt M, Greinacher A, Bux J. Expression of the CTL2 transcript variants in human peripheral blood cells and human tissues. Transfusion. March 11, 2013. doi: 10.1111/trf.12160. http://onlinelibrary.wiley.com/doi/10.1111/trf.12160/abstract;jsessionid= 469A6D2E798BA8D68B25FD6E9CA60CEA. d01t04. Accessed September 10, 2013.
36. Thomas GM, Carbo C, Curtis BR, Martinod K, Mazo IB, Schatzberg D, Cifuni SM, Fuchs TA, von Andrian UH, Hartwig JH, Aster RH, Wagner DD. Extracellular DNA traps are associated with the pathogenesis of TRALI in humans and mice. Blood. 2012;119:6335-6343.
37. Caudrillier A, Kessenbrock K, Gilliss BM, Nguyen JX, Marques MB, Monestier M, Toy P, Werb Z, Looney MR. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J Clin Invest. 2012;122:2661-2671.
38. Van Buren NL, Stroncek DF, Clay ME, McCullough J, Dalmasso AP. Transfusion-related acute lung injury caused by an NB2 granulocyte-specifc antibody in a patient with thrombotic thrombocytopenic purpura. Transfusion. 1990;30:42-45.
39. Sachs UJ. Recent insights into the mechanism of transfusion-related acute lung injury. Curr Opin Hematol. 2011;18:436-442.
40. Kopko PM, Marshall CS, MacKenzie MR, Holland PV, Popovsky MA. Transfusion-related acute lung injury: report of a clinical look-back investigation. JAMA. 2002;287:1968-1971.
41. Seeger W, Schneider U, Kreusler B, von Witzleben E, Walmrath D, Grimminger F, Neppert J. Reproduction of transfusion-related acute lung injury in an ex vivo lung model. Blood. 1990;76:1438-1444.
42. Kopko PM, Paglieroni TG, Popovsky MA, Muto KN, MacKenzie MR, Holland PV. TRALI: correlation of antigen-antibody and monocyte activation in donor-recipient pairs. Transfusion. 2003;43:177-184.
43. Vlaar A P, Kuipers MT, Hofstra JJ, Wolthuis EK, Wieland CW, Roelofs JJ, Boon L, Schultz MJ, Lutter R, Juffermans N P. Mechanical ventilation and the titer of antibodies as risk factors for the development of transfusion-related lung injury. Crit Care Res Pract. 2012;2012:720950. doi: 10.1155/2012/720950.
44. Van Buul JD, Fernandez-Borja M, Anthony EC, Hordijk PL. Expression and localization of NOX2 and NOX4 in primary human endothelial cells. Antioxid Redox Signal. 2005;7:308-317.
45. Lambeth JD. Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med. 2007;43:332-347.
46. Weissmann N, Sydykov A, Kalwa H, et al. Activation of TRPC6 channels is essential for lung ischaemia-reperfusion induced oedema in mice. Nat Commun. 2012;3:649.
47. Dechend R, Viedt C, Müller DN, et al. AT1 receptor agonistic antibodies from preeclamptic patients stimulate NADPH oxidase. Circulation. 2003;107:1632-1639.
48. Tian XY, Yung LH, Wong WT, et al. Bone morphogenic protein-4 induces endothelial cell apoptosis through oxidative stress-dependent p38MAPK and JNK pathway. J Mol Cell Cardiol. 2012; 52:237-244.
49. Vischer UM, Jornot L, Wollheim CB, Theler JM. Reactive oxygen intermediates induce regulated secretion of von Willebrand factor from cultured human vascular endothelial cells. Blood. 1995;85:3164-3172.
50. Koprivica Z, Djordjevic D, Vuletic M, Zivkovic V, Barudzic N, Andjelkovic N, Djuric D, Iric-Cupic V, Krkeljic J, Jakovljevic V. Vo n Willebrand factor and oxidative stress parameters in acute coronary syndromes. Oxid Med Cell Longev. 2011;2011:918312.
51. Michel V, Yuan Z, Ramsubir S, Bakovic M. Choline transport for phospho-lipid synthesis. Exp Biol Med. 2006:231;495-404.
52. Liu RM, Choi J, Wu JH, Gaston Pravia KA, Lewis KM, Brand JD, Mochel NS, Krzywanski DM, Lambeth JD, Hagood JS, Forman HJ, Thannickal VJ, Postlethwait EM. Oxidative modifcation of nuclear mitogen-activated protein kinase phosphatase 1 is involved in transforming growth factor beta1-induced expression of plasminogen activator inhibitor 1 in fbro-blasts. J Biol Chem. 2010;285:16239-16247.
53. Kelher MR, Masuno T, Moore EE, Damle S, Meng X, Song Y, Liang X, Niedzinski J, Geier SS, Khan S Y, Gamboni-Robertson F, Silliman CC. Plasma from stored packed red blood cells and MHC class I antibodies causes acute lung injury in a 2-event in vivo rat model. Blood. 2009;113:2079-2087.
54. Shaz BH, Stowell SR, Hillyer CD. Transfusion-related acute lung injury: from bedside to bench and back. Blood. 2011;117:1463-1471.
55. Karpinich NO, Hoopes SL, Kechele DO, Lenhart PM, Caron KM. Adrenomedullin Function in Vascular Endothelial Cells: Insights from Genetic Mouse Models. Curr Hypertens Rev. 2011;7:228-239.