Heme oxygenase-1 modulates thrombomodulin and activated protein c levels to attenuate lung injury in cecal ligation and punctureinduced acute lung injury mice

Experimental Lung Research

Volumn 38, Issue 4, 2012, Pages 173-182

  Zhao, Mingyan ^a   Fei, Dongsheng ^a   Meng, Xianglin ^a   Kang, Kai ^a   Nan, Chuanchuan ^a   Zhao, Mingran ^b   Pan, Shangha ^c   Gao, Meizhuo ^a   Yang, Songlin ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b The Maternal and Child Health Hospital of Harbin City   (China)

^c THE FIRST AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Activated protein C; Coagulation; Heme oxygenase; Lung injury; Thrombomodulin

Indexed keywords

ACTIVATED PROTEIN C; CARBOXYHEMOGLOBIN; HEME OXYGENASE 1; HEMIN; MALONALDEHYDE; MYELOPEROXIDASE; PROTOPORPHYRIN ZINC; THROMBOMODULIN;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL OXYGEN TENSION; ARTICLE; BLOOD CLOTTING; CECAL LIGATION AND PUNCTURE; CELL SURFACE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOFLUORESCENCE; LUNG EDEMA; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURGICAL TECHNIQUE; SURVIVAL RATE; THROMBOSIS; UPREGULATION; WESTERN BLOTTING;

ACUTE LUNG INJURY; ANIMALS; CECUM; ENZYME INDUCTION; ENZYME INHIBITORS; HEME OXYGENASE-1; HEMIN; LIGATION; LUNG; MALE; MICE; MICE, INBRED C57BL; PROTEIN C; PROTOPORPHYRINS; PUNCTURES; SEPSIS; THROMBOMODULIN;

EID: 84859449572     PISSN: 01902148     EISSN: 15210499     Source Type: Journal    
DOI: 10.3109/01902148.2012.660559     Document Type: Article

References (41)

1. Hotchkiss RS, Karl IE: The pathophysiology and treatment of sepsis. N Engl J Med. 2003;348:138-150. (Pubitemid 36056721)
2. Lewandowski K, Lewandowski M: Epidemiology of ARDS. Minerva Anestesiol. 2006;72:473-477.
3. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, Lamy M, Legall JR, Morris A, Spragg R: The American-European Consensus Conference on ARDS. Defnitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med. 1994;149(3 Pt 1):818-824. (Pubitemid 24082248)
4. Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med. 2000;342:1334-1349. (Pubitemid 30408719)
5. Idell S, Peters J, James KK, Fair DS, Coalson JJ: Local abnormalities of coagulation and fbrinolytic pathways that promote alveolar fbrin deposition in the lungs of baboons with diffuse alveolar damage. J Clin Invest. 1989;84:181-193. (Pubitemid 19170108)
6. Esteban A, Fernández-Segoviano P, Frutos-Vivar F, Aramburu JA, Nájera L, Ferguson ND, Aĺia I, Gordo F, Ŕios F: Comparison of clinical criteria for the acute respiratory distress syndrome with autopsy fndings. Ann Intern Med. 2004;141:440-445.
7. Tsushima K, King LS, Aggarwal NR, De Gorordo A, D'Alessio FR, Kubo K: Acute lung injury review. Intern Med. 2009;48:621-630.
8. Chopra M, Reuben JS, Sharma AC: Acute lung injury: apop-tosis and signaling mechanisms. Exp Biol Med (Maywood). 2009;234:361-371.
9. Cepkova M, Matthay MA: Pharmacotherapy of acute lung injury and the acute respiratory distress syndrome. J Intensive Care Med. 2006;21:119-143.
10. Matthay MA, Zemans RL: The acute respiratory distress syndrome: pathogenesis and treatment. Annu Rev Pathol. 2011;6:147-163.
11. Rittirsch D, Hoesel LM, Ward PA: The disconnect between animal models of sepsis and human sepsis. J Leukoc Biol. 2007;81:137-143. (Pubitemid 46021262)
12. Dejager L, Pinheiro I, Dejonckheere E, Libert C: Cecal ligation and puncture: the gold standard model for polymicrobial sepsis? Trends Microbiol. 2011;19:198-208.
13. Willis D, Moore AR, Frederick R, Willoughby DA: Heme oxy-genase: a novel target for the modulation of the infammatory response. Nat Med. 1996;2:87-90. (Pubitemid 26029572)
14. Morse D, Lin L, Choi AM, Ryter SW: Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease. Free Radic Biol Med. 2009;47:1-12.
15. Choi AM, Alam J: Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol. 1996;15: 9-19. (Pubitemid 126439851)
16. Otterbein LE, Lee PJ, Chin BY, Petrache I, Camhi SL, Alam J, Choi AM: Protective effects of heme oxygenase-1 in acute lung injury. Chest. 1999;116(1 Suppl):61S-63S. (Pubitemid 29340213)
17. Ryter SW, Choi AM: Heme oxygenase-1/carbon monoxide: novel therapeutic strategies in critical care medicine. Curr Drug Targets. 2010;11:1485-1494.
18. An L, Liu CT, Qin XB, Liu QH, Liu Y, Yu SY: Protective effects of hemin in an experimental model of ventilator-induced lung injury. Eur J Pharmacol. 2011;661:102-108.
19. La P, Fernando AP, Wang Z, Salahudeen A, Yang G, Lin Q, Wright CJ, Dennery PA: Zinc protoporphyrin regulates cyclin D1 expression independent of heme oxygenase inhibition. J Biol Chem. 2009;284:36302-36311.
20. Ware LB, Fang X, Matthay MA: Protein C and thrombomod-ulin in human acute lung injury. Am J Physiol Lung Cell Mol Physiol. 2003;285:L514-L521. (Pubitemid 37022850)
21. Ware LB, Bastarache JA, Wang L: Coagulation and fbrinolysis in human acute lung injury-new therapeutic targets? Keio J Med. 2005;54:142-149. (Pubitemid 41542714)
22. Conway EM, Van de Wouwer M, Pollefeyt S, Jurk K, Van Aken H, De Vriese A, Weitz JI, Weiler H, Hellings PW, Schaeffer P, Herbert JM, Collen D, Theilmeier G: The lectin-like domain of thrombomodulin confers protection from neutrophil-mediated tissue damage by suppressing adhesion molecule expression via nuclear factor kappaB and mitogen-activated protein kinase pathways. J Exp Med. 2002;196:565-577. (Pubitemid 35024436)
23. Liaw PC, Esmon CT, Kahnamoui K, Schmidt S, Kahnamoui S, Ferrell G, Beaudin S, Julian JA, Weitz JI, Crowther M, Loeb M, Cook D: Patients with severe sepsis vary markedly in their ability to generate activated protein C. Blood. 2004;104:3958-3964. (Pubitemid 39620144)
24. Ding BS, Hong N, Christofdou-Solomidou M, Gottstein C, Albelda SM, Cines DB, Fisher AB, Muzykantov VR: Anchoring fusion thrombomodulin to the endothelial lumen protects against injury-induced lung thrombosis and infammation. Am J Respir Crit Care Med. 2009;180:247-256.
25. Sambuceti G, Morbelli S, Vanella L, Kusmic C, Marini C, Massollo M, Augeri C, Corselli M, Ghersi C, Chiavarina B, Rodella LF, L'Abbate A, Drummond G, Abraham NG, Frassoni F: Diabetes impairs the vascular recruitment of normal stem cells by oxidant damage, reversed by increases in pAMPK, heme oxygenase-1, and adiponectin. Stem Cells. 2009;27: 399-407.
26. Rodella LF, Vanella L, Peterson SJ, Drummond G, Rezzani R, Falck JR, Abraham NG: Heme oxygenase-derived carbon monoxide restores vascular function in type 1 diabetes. Drug Metab Lett. 2008;2:290-300.
27. Beutler E, West C: Simplifed determination of carboxyhe-moglobin. Clin Chem. 1984; 30:871-874.
28. Hagiwara S, Iwasaka H, Matsumoto S, Hasegawa A, Yasuda N, Noguchi T: In vivo and in vitro effects of the anticoagulant, thrombomodulin, on the infammatory response in rodent models. Shock. 2010;33:282-288.
29. Okutan H, Savas C, Delibas N: The antioxidant effect of mela-tonin in lung injury after aortic occlusion-reperfusion. Interact Cardiovasc Thorac Surg. 2004;3:519-522. (Pubitemid 39094747)
30. Scott JR, Chin BY, Bilban MH, Otterbein LE: Restoring home-ostasis: is heme oxygenase-1 ready for the clinic? Trends Pharmacol Sci. 2007;28:200-205. (Pubitemid 46661005)
31. Zegdi R, Perrin D, Burdin M, Boiteau R, Tenaillon A: Increased endogenous carbon monoxide production in severe sepsis. Intensive Care Med. 2002;28:793-796. (Pubitemid 34639495)
32. Takaki S, Takeyama N, Kajita Y, Yabuki T, Noguchi H, Miki Y, Inoue Y, Nakagawa T, Noguchi H: Benefcial effects of the heme oxygenase-1/carbon monoxide system in patients with severe sepsis/septic shock. Intensive Care Med. 2010;36: 42-48.
33. Tomashefski JF Jr: Pulmonary pathology of acute respiratory distress syndrome. Clin Chest Med. 2000;21:435-466.
34. Ruf W: New players in the sepsis-protective activated protein C pathway. J Clin Invest. 2010;120:3084-3087.
35. Mosnier LO, Zlokovic BV, Griffn JH: The cytoprotective protein C pathway. Blood. 2007;109:3161-3172. (Pubitemid 46572500)
36. Faust SN, Levin M, Harrison OB, Goldin RD, Lockhart MS, Kondaveeti S, Laszik Z, Esmon CT, Heyderman RS: Dysfunction of endothelial protein C activation in severe meningococcal sepsis. N Engl J Med. 2001;345:408-416. (Pubitemid 32747604)
37. Furuichi M, Yokozuka M, TakemoriK, Yamanashi Y, Sakamoto A: The reciprocal relationship between heme oxygenase and nitric oxide synthase in the organs of lipopolysaccharide-treated rodents. Biomed Res. 2009;30:235-243.
38. Johnson FK, Johnson RA: Carbon monoxide promotes endothelium-dependent constriction of isolated gracilis muscle arterioles. Am J Physiol Regul Integr Comp Physiol. 2003;285:R536-R541. (Pubitemid 37040561)
39. Fujita T, Toda K, Karimova A, Yan SF, Naka Y, Yet SF&Pinsky D: Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fbrinolysis. Nat Med. 2001;7:598-604. (Pubitemid 32448328)
40. Sun BW, Shi GS, Zhang P, Zou XQ, Chen X: [Inhibitive effect of exogenous carbon monoxide-releasing molecules 2 on tissue factor expression in sepsis]. Zhonghua Shao Shang Za Zhi. 2009;25:111-114.
41. Lindenblatt N, Bordel R, Schareck W, Menger MD, Vollmar B: Vascular heme oxygenase-1 induction suppresses microvascu-lar thrombus formation in vivo. Arterioscler Thromb Vasc Biol. 2004;24:601-606. (Pubitemid 38326159)