Carbon monoxide protects against ventilator-induced lung injury via PPAR-γ and inhibition of Egr-1

American Journal of Respiratory and Critical Care Medicine

Volumn 177, Issue 11, 2008, Pages 1223-1232

  Hoetzel, Alexander ^a,b   Dolinay, Tamas ^a   Vallbracht, Simone ^b   Zhang, Yingze ^a   Hong, Pyo Kim ^a   Ifedigbo, Emeka ^a   Alber, Sean ^a   Kaynar, A Murat ^a   Schmidt, Rene ^b   Ryter, Stefan W ^a   Choi, Augustine M K ^a,c  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF FREIBURG   (Germany)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Carbon monoxide; Early growth response 1; Inflammation; Peroxysome proliferator activated receptor ; Ventilator induced lung injury

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; CARBON MONOXIDE; CHEMOKINE; CYTOKINE; EARLY GROWTH RESPONSE FACTOR 1; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN; ANTIMETABOLITE; EGR1 PROTEIN, MOUSE;

AIRWAY PRESSURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; BLOOD GAS; BLOOD PRESSURE; CONTROLLED STUDY; LUNG INJURY; LUNG LAVAGE; MALE; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; VENTILATOR; ADULT RESPIRATORY DISTRESS SYNDROME; AIRWAY RESISTANCE; ANIMAL; C57BL MOUSE; DISEASE MODEL; METABOLISM; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY;

AIRWAY RESISTANCE; ANIMALS; ANTIMETABOLITES; BLOOD PRESSURE; CARBON MONOXIDE; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; MALE; MICE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; PPAR GAMMA; RESPIRATION, ARTIFICIAL; RESPIRATORY DISTRESS SYNDROME, ADULT;

EID: 44449171400     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200708-1265OC     Document Type: Article

References (49)

1. The Acute Respiratory Distress Syndrome Network. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N Engl J Med 2000;342:1301-1308.
2. Meade MO, Cook DJ, Guyatt GH, Slutsky AS, Arabi YM, Cooper DJ, Davies AR, Hand LE, Zhou Q, Thabane L, et al.; Lung Open Ventilation Study Investigators. Ventilation strategy using low tidal volumes, recruitment maneuvers, and high positive end-expiratory pressure for acute lung injury and acute respiratory distress syndrome: a randomized controlled trial. JAMA 2008;299:637-645.
3. Villar J, Kacmarek RM, Pérez-Méndez L, Aguirre-Jaime A. A high positive end-expiratory pressure, low tidal volume ventilatory strategy improves outcome in persistent acute respiratory distress syndrome: a randomized, controlled trial. Crit Care Med 2006;34:1311-1318.
4. Belperio JA, Keane MP, Burdick MD, Londhe V, Xue YY, Li K, Phillips RJ, Strieter RM. Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury. J Clin Invest 2002;110:1703-1716.
5. Hoetzel A, Dolinay T, Schmidt R, Choi AMK, Ryter SW. Carbon monoxide in sepsis. Antioxid Redox Signal 2007;9:2013-2026.
6. 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.
7. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase: characterization of the enzyme. J Biol Chem 1969;244:6388-6394.
8. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006;86:583-650.
9. Falk DJ, Deruisseau KC, Van Gammeren DL, Deering MA, Kavazis AN, Powers SK. Mechanical ventilation promotes redox status alterations in the diaphragm. J Appl Physiol 2006;101:1017-1024.
10. Keyse SM, Tyrrell RM. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 1989;86:99-103.
11. Akamatsu Y, Haga M, Tyagi S, Yamashita K, Graca-Souza AV, Ollinger R, Czismadia E, May GA, Ifedigbo E, Otterbein LE, et al. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J 2004;18:771-772.
12. Motterlini R, Mann BE, Foresti R, Motterlini R, Mann BE, Foresti R. Therapeutic applications of carbon monoxide-releasing molecules. Expert Opin Investig Drugs 2005;14:1305-1318.
13. Otterbein LE, Mantell LL, Choi AM. Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999;276:L688-L694.
14. Dolinay T, Szilasi M, Liu M, Choi AM. Inhaled carbon monoxide confers antiinflammatory effects against ventilator-induced lung injury. Am J Respir Crit Care Med 2004;170:613-620.
15. Hoetzel A, Zhang Y, Choi AM. Carbon monoxide attenuates ventilator induced lung injury [abstract]. Am J Respir Crit Care Med 2008;175:A434.
16. Hoetzel A, Choi AM. The protective role of carbon monoxide in ventilator induced lung injury. Presented at the 2007 Annual Meeting of the European Society of Anesthesiology, Munich.
17. Otterbein LE, Bach FH, Alam J, Soares M, Lu HT, Wysk M, Davis RJ, Flavell RA, Choi AMK. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000;6:422-428.
18. Slebos DJ, Ryter SW, van der Toorn M, Liu F, Guo F, Baty CJ, Karlsson JM, Watkins SC, Kim HP, Wang X, et al. Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am J Respir Cell Mol Biol 2007;36:409-417.
19. Wang X, Wang Y, Kim HP, Nakahira K, Ryter SW, Choi AM. Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J Biol Chem 2007;282:1718-1726.
20. Furchgott RF, Jothianandan D. Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light. Blood Vessels 1991;28:52-61.
21. Durante W, Johnson FK, Johnson RA. Role of carbon monoxide in cardiovascular function. J Cell Mol Med 2006;10:672-686.
22. Cardell LO, Lou YP, Takeyama K, Ueki IF, Lausier J, Nadel JA. Carbon monoxide, a cyclic GMP-related messenger, involved in hypoxic bronchodilation in vivo. Pulm Pharmacol Ther 1998;11:309-315.
23. Ameredes BT, Otterbein LE, Kohut LK, Gligonic AL, Calhoun WJ, Choi AM. Low-dose carbon monoxide reduces airway hyperresponsiveness in mice. Am J Physiol 2003;285:L1270-L1276.
24. Copland IB, Kavanagh BP, Engelberts D, McKerlie C, Belik J, Post M. Early changes in lung gene expression due to high tidal volume. Am J Respir Crit Care Med 2003;168:1051-1059.
25. Kim HP, Wang X, Zhang J, Suh GY, Benjamin IJ, Ryter SW, Choi AM. Heat shock protein-70 mediates the cytoprotective effect of carbon monoxide: involvement of p38beta MAPK and heat shock factor-1. J Immunol 2005;175:2622-2629.
26. Yan SF, Fujita T, Lu J, Okada K, Shan ZY, Mackman N, Pinsky DJ, Stern DM. Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med 2000;6:1355-1361.
27. Bilban M, Bach FH, Otterbein SL, Ifedigbo E, de Costa DJ, Esterbauer H, Chin BY, Usheva A, Robson SC, Wagner O, et al. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity 2006;24:601-610.
28. van Bel F, Latour V, Vreman HJ, Wong RJ, Stevenson DK, Steendijk P, Egberts J, Krediet TG. Is carbon monoxide-mediated cyclic guanosine monophosphate production responsible for low blood pressure in neonatal respiratory distress syndrome? J Appl Physiol 2005;98:1044-1049.
29. Hashiba T, Suzuki M, Nagashima Y, Suzuki S, Inoue S, Tsuburai T, Matsuse T, Ishigatubo Y. Adenovirus-mediated transfer of heme oxygenase-1 cDNA attenuates severe lung injury induced by the influenza virus in mice. Gene Ther 2001;8:1499-1507.
30. Hayashi Y, Sawa Y, Fukuyama N, Nakazawa H, Matsuda H. Preoperative glutamine administration induces heat-shock protein 70 expression and attenuates cardiopulmonary bypass-induced inflammatory response by regulating nitric oxide synthase activity. Circulation 2002;106:2601-2607.
31. Singleton KD, Wischmeyer PE. Glutamine's protection against sepsis and lung injury is dependent on heat shock protein 70 expression. Am J Physiol 2007;292:R1839-R1845.
32. Zuckerbraun BS, Billiar TR, Otterbein SL, Kim PK, Liu F, Choi AM, Bach FH, Otterbein LE. Carbon monoxide protects against liver failure through nitric oxide-induced heme oxygenase 1. J Exp Med 2003;198:1707-1716.
33. Uhlig U, Fehrenbach H, Lachmann RA, Goldmann T, Lachmann B, Vollmer E, Uhlig S. Phosphoinositide 3-OH kinase inhibition prevents ventilation-induced lung cell activation. Am J Respir Crit Care Med 2004;169:201-208.
34. Reutershan J, Ley K. Bench-to-bedside review: acute respiratory distress syndrome - how neutrophils migrate into the lung. Crit Care 2004;8:453-461.
35. Held HD, Boettcher S, Hamann L, Uhlig S. Ventilation-induced chemokine and cytokine release is associated with activation of nuclear factor-κB and is blocked by steroids. Am J Respir Crit Care Med 2001;163:711-716.
36. Tremblay L, Valenza F, Ribeiro SP, Li J, Slutsky AS. Injurious ventilatory strategies increase cytokines and c-fos m-RNA expression in an isolated rat lung model. J Clin Invest 1997;99:944-952.
37. Copland IB, Post M. Stretch-activated signaling pathways responsible for early response gene expression in fetal lung epithelial cells. J Cell Physiol 2007;210:133-143.
38. Mishra S, Fujita T, Lama VN, Nam D, Liao H, Okada M, Minamoto K, Yoshikawa Y, Harada H, Pinsky DJ. Carbon monoxide rescues ischemic lungs by interrupting MAPK-driven expression of early growth response 1 gene and its downstream target genes. Proc Natl Acad Sci USA 2006;103:5191-5196.
39. Friedman AD. Transcriptional regulation of granulocyte and monocyte development. Oncogene 2002;21:3377-3390.
40. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, Gantner BN, Dinner AR, Singh H. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 2006;126:755-766.
41. Standiford TJ, Keshamouni VG, Reddy RC. Peroxisome proliferator-activated receptor-γ as a regulator of lung inflammation and repair. Proc Am Thorac Soc 2005;2:226-231.
42. Delerive P, Fruchart JC, Staels B. Peroxisome proliferator-activated receptors in inflammation control. J Endocrinol 2001;169:453-459.
43. Okada M, Yan SF, Pinsky DJ. Peroxisome proliferator-activated receptor-gamma (PPAR-gamma) activation suppresses ischemic induction of Egr-1 and its inflammatory gene targets. FASEB J 2002;16:1861-1868.
44. Zingarelli B, Sheehan M, Hake PW, O'Connor M, Denenberg A, Cook JA. Peroxisome proliferator activator receptor-gamma ligands, 15-deoxy-Delta(12,14)- prostaglandin J2 and ciglitazone, reduce systemic inflammation in polymicrobial sepsis by modulation of signal transduction pathways. J Immunol 2003;171:6827-6837.
45. Liu D, Zeng BX, Zhang SH, Wang YL, Zeng L, Geng ZL, Zhang SF. Rosiglitazone, a peroxisome proliferator-activated receptor-gamma agonist, reduces acute lung injury in endotoxemic rats. Crit Care Med 2005;33:2309-2316.
46. Rehan VK, Wang Y, Patel S, Santos J, Torday JS. Rosiglitazone, a peroxisome proliferator-activated receptor-gamma agonist, prevents hyperoxia-induced neonatal rat lung injury in vivo. Pediatr Pulmonol 2006;41:558-569.
47. Dolinay T, Wu W, Kaminski N, Ifedigbo E, Kaynar AM, Szilasi M, Watkins SC, Ryter SW, Hoetzel A, Choi AMK. Mitogen-activated protein kinases regulate susceptibility to ventilator-induced lung injury. PloS ONE 2008;3:e1601.
48. Li M, Lee TW, Mok TS, Warner TD, Yim AP, Chen GG. Activation of peroxisome proliferator-activated receptor-gamma by troglitazone (TGZ) inhibits human lung cell growth. J Cell Biochem 2005;96:760-774.
49. Azuma Y, Watanabe K, Date M, Daito M, Ohura K. Induction of proliferation by 15-deoxy-delta12,14-prostaglandin J2 and the precursors in monocytic leukemia U937. Pharmacology 2004;71:181-191.