Therapeutic potential of recombinant thrombomodulin for lung injury after pneumonectomy via inhibition of high-mobility group box 1 in mice

Journal of Trauma and Acute Care Surgery

Volumn 81, Issue 5, 2016, Pages 868-875

  Takahashi, Yusuke ^a   Matsutani, Noriyuki ^a   Dejima, Hitoshi ^a   Nakayama, Takashi ^a   Okamura, Ryo ^a   Uehara, Hirofumi ^a   Kawamura, Masafumi ^a  

^a TEIKYO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Acute lung injury; HMGB1; pneumonectomy; proinflammatory cytokine; thrombomodulin

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RECOMBINANT THROMBOMODULIN; TUMOR NECROSIS FACTOR; CYTOKINE; HMGB1 PROTEIN, MOUSE; RECOMBINANT PROTEIN; THROMBOMODULIN;

ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; LUNG RESECTION; MOUSE; MOUSE MODEL; NONHUMAN; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; SURVIVAL ANALYSIS; SURVIVAL TIME; THERAPY EFFECT; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; DISEASE MODEL; IMMUNOLOGY; INJECTION; PATHOPHYSIOLOGY; PHYSIOLOGY; POSTOPERATIVE COMPLICATIONS; RANDOMIZATION; RESPIRATORY DISTRESS SYNDROME, ADULT;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HMGB1 PROTEIN; INJECTIONS; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; PNEUMONECTOMY; POSTOPERATIVE COMPLICATIONS; RANDOM ALLOCATION; RECOMBINANT PROTEINS; RESPIRATORY DISTRESS SYNDROME, ADULT; THROMBOMODULIN;

EID: 84981271696     PISSN: 21630755     EISSN: 21630763     Source Type: Journal    
DOI: 10.1097/TA.0000000000001208     Document Type: Article

References (43)

1. Needham DM, Yang T, Dinglas VD, Mendez-Tellez PA, Shanholtz C, Sevransky JE, Brower RG, Pronovost PJ, Colantuoni E. Timing of low tidal volume ventilation and intensive care unit mortality in acute respiratory distress syndrome. A prospective cohort study. Am J Respir Crit Care Med. 2015;191:177-185
2. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, LamyM, Legall JR,Morris A, Spragg R. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med. 1994;149:818-824
3. Dulu A, Pastores SM, Park B, Riedel E, Rusch V, Halpern NA. Prevalence and mortality of acute lung injury and ARDS after lung resection. Chest. 2006;130:73-78
4. Park SY, Lee HS, Jang HJ, Joo J, Zo JI. Efficacy of intraoperative, singlebolus corticosteroid administration to prevent postoperative acute respiratory failure after oesophageal cancer surgery. Interact Cardiovasc Thorac Surg. 2012;15:639-643
5. Takahashi Y, Matsuda M, Aoki S, Dejima H, Nakayama T, Matsutani N, KawamuraM. Qualitative analysis of preoperative high-resolution computed tomography: risk factors for pulmonary complications after major lung resection. Ann Thorac Surg. 2015;101:1068-1074
6. Kim JY, Park JS, Strassheim D, Douglas I, Diaz del Valle F, Asehnoune K, Mitra S, Kwak SH, Yamada S, Maruyama I, et al. HMGB1 contributes to the development of acute lung injury after hemorrhage. Am J Physiol Lung Cell Mol Physiol. 2005;288:L958-L965
7. Takano K, ShinodaM, TanabeM, Miyasho T, Yamada S, Ono S,Masugi Y, Suda K, Fukunaga K, Hayashida T, et al. Protective effect of high-mobility group box 1 blockade on acute liver failure in rats. Shock. 2010;34:573-579
8. Hagiwara S, Iwasaka H, Hasegawa A, Asai N, Noguchi T. High-dose intravenous immunoglobulin G improves systemic inflammation in a rat model of CLP-induced sepsis. Intensive Care Med. 2008;34:1812-1819
9. Suda K, Takeuchi H, Ishizaka A, Kitagawa Y. High-mobility-group box chromosomal protein 1 as a new target for modulating stress response. Surg Today. 2010;40:592-601
10. Hatada T, Wada H, Nobori T, Okabayashi K, Maruyama K, Abe Y, Uemoto S, Yamada S, Maruyama I. Plasma concentrations and importance of high mobility group box protein in the prognosis of organ failure in patients with disseminated intravascular coagulation. Thromb Haemost. 2005;94:975-979
11. Yamato M, Minematsu Y, Fujii J, Mori K, Minato T, Miyagawa S, Fujimura R, Morikage N, Arata Y, Nakano C, et al. Effective combination therapy of polymyxin-B direct hemoperfusion and recombinant thrombomodulin for septic shock accompanied by disseminated intravascular coagulation: a historical controlled trial. Ther Apher Dial. 2013;17:472-476
12. Kudo D, Toyama M, Aoyagi T, Akahori Y, Yamamoto H, Ishii K, Kanno E, Maruyama R, Kaku M, Kushimoto S, et al. Involvement of high mobility group box 1 and the therapeutic effect of recombinant thrombomodulin in a mouse model of severe acute respiratory distress syndrome. Clin Exp Immunol. 2013;173:276-287
13. Iwashita Y, Zhang E,Maruyama J, Yokochi A, Yamada Y, Sawada H,Mitani Y, Imai H, Suzuki K, Maruyama K. Thrombomodulin protects against lung damage created by high level of oxygen with large tidal volume mechanical ventilation in rats. J Intensive Care. 2014;2:57
14. Takahashi Y, Izumi Y, KohnoM, Kimura T, KawamuraM, OkadaY, Nomori H, Ikeda E. Thyroid transcription factor-1 influences the early phase of compensatory lung growth in adult mice. Am J Respir Crit Care Med. 2010;181: 1397-1406
15. Takahashi Y, Izumi Y, Kohno M, Kawamura M, Ikeda E, Nomori H. Airway administration of dexamethasone, 3′-5′-cyclic adenosine monophosphate, and isobutylmethylxanthine facilitates compensatory lung growth in adult mice. Am J Physiol Lung Cell Mol Physiol. 2011;300:L453-L461
16. TajimaA, KohnoM,WatanabeM, Izumi Y, Tasaka S,Maruyama I,Miyasho T, Kobayashi K. Occult injury in the residual lung after pneumonectomy in mice. Interact Cardiovasc Thorac Surg. 2008;7:1114-1120
17. Gomi K, Zushi M, Honda G, Kawahara S, Matsuzaki O, Kanabayashi T, Yamamoto S, Maruyama I, Suzuki K. Antithrombotic effect of recombinant human thrombomodulin on thrombin-induced thromboembolism in mice. Blood. 1990;75:1396-1399
18. Thille AW, Esteban A, Fernández-Segoviano P, Rodriguez JM, Aramburu JA, Peñuelas O, Cortés-Puch I, Cardinal-Fernández P, Lorente JA, Frutos-Vivar F. Comparison of the Berlin definition for acute respiratory distress syndrome with autopsy. Am J Respir Crit Care Med. 2013;187:761-767
19. Lorente JA, Ballén-BarragánA,Herrero R, Esteban A.Acute respiratory distress syndrome: does histology matter? Crit Care. 2015;19:337
20. Kimura T,Nojiri T, HosodaH, Ishikane S, ShintaniY, InoueM,MiyazatoM, OkumuraM, Kangawa K. C-type natriuretic peptide attenuates lipopolysaccharideinduced acute lung injury in mice. J Surg Res. 2015;194:631-637
21. Kimura T, Nojiri T, Hosoda H, Shintani Y, Inoue M,Miyazato M, Okumura M, Kangawa K. Exacerbation of bleomycin-induced injury by lipopolysaccharide in mice: establishment of a mouse model for acute exacerbation of interstitial lung diseases. Eur J Cardiothorac Surg. 2015;48:e85-e91
22. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med. 2000;192:565-570
23. Ueno H, Matsuda T, Hashimoto S, Amaya F, Kitamura Y, Tanaka M, Kobayashi A, Maruyama I, Yamada S, Hasegawa N, et al. Contributions of high mobility group box protein in experimental and clinical acute lung injury. Am J Respir Crit Care Med. 2004;170:1310-1316
24. Oh B, Lee M. Combined delivery of HMGB-1 box A peptide and S1PLyase siRNA in animal models of acute lung injury. J Control Release. 2014;175:25-35
25. McGhan LJ, Jaroszewski DE. The role of toll-like receptor-4 in the development of multi-organ failure following traumatic haemorrhagic shock and resuscitation. Injury. 2012;43:129-136
26. Kao RL,XuX,XenocostasA, ParryN,Mele T,Martin CM, Rui T. Induction of acute lung inflammation in mice with hemorrhagic shock and resuscitation: role of HMGB1. J Inflamm (Lond). 2014;11:30
27. Ruffini E, Parola A, Papalia E, Filosso PL, Mancuso M, Oliaro A, Actis-Dato G, Maggi G. Frequency and mortality of acute lung injury and acute respiratory distress syndrome after pulmonary resection for bronchogenic carcinoma. Eur J Cardiothorac Surg. 2001;20:30-36
28. Takahata R, Ono S, Tsujimoto H, Hiraki S, Kimura A, Kinoshita M, Miyazaki H, Saitoh D, Hase K. Postoperative serum concentrations of high mobility group box chromosomal protein-1 correlates to the duration of SIRS and pulmonary dysfunction following gastrointestinal surgery. J Surg Res. 2011;170:e135-e140
29. Luo L, Zhang S,Wang Y, Rahman M, Syk I, Zhang E, Thorlacius H. Proinflammatory role of neutrophil extracellular traps in abdominal sepsis. Am J Physiol Lung Cell Mol Physiol. 2014;307:L586-L596
30. QingDY, Conegliano D, ShashatyMG, Seo J, Reilly JP,WorthenGS, HuhD, Meyer NJ, Mangalmurti NS. Red blood cells induce necroptosis of lung endothelial cells and increase susceptibility to lung inflammation. Am J Respir Crit Care Med. 2014;190:1243-1254
31. Entezari M, Javdan M, Antoine DJ, Morrow DM, Sitapara RA, Patel V, Wang M, Sharma L, Gorasiya S, Zur M, et al. Inhibition of extracellular HMGB1 attenuates hyperoxia-induced inflammatory acute lung injury. Redox Biol. 2014;2:314-322
32. Achouiti A, van der Meer AJ, Florquin S, Yang H, Tracey KJ, Veer C, Vos AF, van der Poll T. High-mobility group box 1 and the receptor for advanced glycation end products contribute to lung injury during Staphylococcus aureus pneumonia. Crit Care. 2013;17:R296
33. Ogawa EN, Ishizaka A, Tasaka S, Koh H, Ueno H, Amaya F, Ebina M, Yamada S, Funakoshi Y, Soejima J, et al. Contribution of high-mobility group box-1 to the development of ventilator-induced lung injury. Am J Respir Crit Care Med. 2006;174:400-407
34. Yamakawa K, Aihara M, Ogura H, Yuhara H, Hamasaki T, Shimazu T. Recombinant human soluble thrombomodulin in severe sepsis: a systematic review and meta-analysis. J Thromb Haemost. 2015;13:508-519
35. Miyoshi S, Ito R, Katayama H, Dote K, Aibiki M, Hamada H, Okura T, Higaki J. Combination therapy with sivelestat and recombinant human soluble thrombomodulin for ARDS and DIC patients. Drug Des Devel Ther. 2014;8:1211-1219
36. Blum JM, Stentz MJ, Dechert R, Jewell E, Engoren M, Rosenberg AL, Park PK. Preoperative and intraoperative predictors of postoperative acute respiratory distress syndrome in a general surgical population. Anesthesiology. 2013;118:19-29
37. Jordan S, Mitchell JA, Quinlan GJ, Goldstraw P, Evans TW. The pathogenesis of lung injury following pulmonary resection. Eur Respir J. 2000;15: 790-799
38. Abeyama K, Stern DM, Ito Y, Kawahara K, Yoshimoto Y, Tanaka M, Uchimura T, Ida N, Yamazaki Y, Yamada S, et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest. 2005;115:1267-1274
39. Nosaka N, YashiroM, YamadaM, Fujii Y, Tsukahara H, Liu K, NishiboriM, Matsukawa A, Morishima T. Anti-high mobility group box-1 monoclonal antibody treatment provides protection against influenza Avirus (H1N1)-induced pneumonia in mice. Crit Care. 2015;19:249
40. Horiuchi K, Kimura T,Miyamoto T, Takaishi H, Okada Y, Toyama Y, Blobel CP. Cutting edge: TNF-alpha-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J Immunol. 2007;179:2686-2689
41. Hagiwara S, Iwasaka H, Goto K, Ochi Y, Mizunaga S, Saikawa T, Noguchi T. Recombinant thrombomodulin prevents heatstroke by inhibition of highmobility group box 1 protein in sera of rats. Shock. 2010;34:402-406
42. Yanai H, Matsuda A, An J, Koshiba R, Nishio J, Negishi H, Ikushima H, Onoe T, Ohdan H, Yoshida N, et al. Conditional ablation of HMGB1 in mice reveals its protective function against endotoxemia and bacterial infection. Proc Natl Acad Sci U S A. 2013;110:20699-20704
43. Shimazaki J, Matsumoto N, Ogura H, Muroya T, Kuwagata Y, Nakagawa J, Yamakawa K, Hosotsubo H, Imamura Y, Shimazu T. Systemic involvement of high-mobility group box 1 protein and therapeutic effect of anti-highmobility group box 1 protein antibody in a rat model of crush injury. Shock. 2012;37:634-638