Heme oxygenase-1 upregulation improves lipopolysaccharide-induced acute lung injury involving suppression of macrophage migration inhibitory factor

Molecular Immunology

Volumn 47, Issue 15, 2010, Pages 2443-2449

  Yin, Hui ^a   Li, Xiangyong ^b   Gong, Quan ^c   Jin, Xiaobao ^a   Gu, Hongbiao ^a   Yuan, Baohong ^a   Zhang, Bobin ^a   Zheng, Fang ^c   Gong, Feili ^c   Zhu, Jiayong ^a  

^a GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Acute lung injury; Heme oxygenase 1; Inflammation; Macrophage migration inhibitory factor; TLR4

Indexed keywords

ANTIINFLAMMATORY AGENT; ENZYME ACTIVATOR; HEME OXYGENASE 1; LIPOPOLYSACCHARIDE; MACROPHAGE MIGRATION INHIBITION FACTOR; MYELOPEROXIDASE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; COPP; GENE EXPRESSION; HISTOPATHOLOGY; LEUKOCYTE ACTIVATION; LUNG EDEMA; MALE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE LEVEL;

MURINAE;

EID: 77955514868     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.06.013     Document Type: Article

References (38)

1. Akira S., Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4:499-511.
2. Ashino T., Yamanaka R., Yamamoto M., Shimokawa H., Sekikawa K., Iwakura Y., Shioda S., Numazawa S., Yoshida T. Negative feedback regulation of lipopolysaccharide-induced inducible nitric oxide synthase gene expression by heme oxygenase-1 induction in macrophages. Mol. Immunol. 2008, 45:2106-2115.
3. Baugh J.A., Bucala R. Macrophage migration inhibitory factor. Crit. Care Med. 2002, 30:S27-S35.
4. Bernhagen J., Calandra T., Mitchell R.A., Martin S.B., Tracey K.J., Voelter W., Manogue K.R., Cerami A., Bucala R. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993, 365:756-759.
5. Bozza M., Satoskar A.R., Lin G., Lu B., Humbles A.A., Gerard C., David J.R. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J. Exp. Med. 1999, 189:341-346.
6. Brouard S., Otterbein L.E., Anrather J., Tobiasch E., Bach F.H., Choi A.M., Soares M.P. Carbon monoxide generated by hemeoxygenase 1 suppresses endothelial cell apoptosis. J. Exp. Med. 2000, 192:1015-1026.
7. Calandra T., Echtenacher B., Roy D.L., Pugin J., Metz C.N., Hültner L., Heumann D., Männel D., Bucala R., Glauser M.P. Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat. Med. 2000, 6:164-170.
8. Calandra T., Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 2003, 3:791-800.
9. Christou H., Morita T., Hsieh C.M., Koike H., Arkonac B., Perrella M.A., Kourembanas S. Prevention of hypoxia-induced pulmonary hypertension by enhancement of endogenous heme oxygenase-1 in the rat. Circ. Res. 2000, 86:1224-1229.
10. de Jong Y.P., Abadia-Molina A.C., Satoskar A.R., Clarke K., Rietdijk S.T., Faubion W.A., Mizoguchi E., Metz C.N., Alsahli M., ten Hove T., Keates A.C., Lubetsky J.B., Farrell R.J., Michetti P., van Deventer S.J., Lolis E., David J.R., Bhan A.K., Terhorst C. Development of chronic colitis is dependent on the cytokine MIF. Nat. Immunol. 2001, 2:1061-1066.
11. Donnelly S.C., Haslett C., Reid P.T., Grant I.S., Wallace W.A., Metz C.N., Bruce L.J., Bucala R. Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome. Nat. Med. 1997, 3:320-323.
12. Gregory J.L., Morand E.F., McKeown S.J., Ralph J.A., Hall P., Yang Y.H., McColl S.R., Hickey M.J. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J. Immunol. 2006, 177:8072-8079.
13. Hu C.M., Lin H.H., Chiang M.T., Chang P.F., Chau L.Y. Systemic expression of heme oxygenase-1 ameliorates type 1 diabetes in NOD mice. Diabetes 2007, 56:1240-1247.
14. Hudson L.D., Milberg J.A., Anardi D., Maunder R.J. Clinical risks for development of the acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 1995, 151:293-301.
15. Kapturczak M.H., Wasserfall C., Brusko T., Campbell-Thompson M., Ellis T.M., Atkinson M.A., Agarwal A. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am. J. Pathol. 2004, 165:1045-1053.
16. Korsgren M., Källström L., Uller L., Bjerke T., Sundler F., Persson C.G., Korsgren O. Role of macrophage migration inhibitory factor (MIF) in allergic and endotoxin-induced airway inflammation in mice. Mediat. Inflamm. 2000, 9:15-23.
17. Lee W.L., Downey G.P. Neutrophil activation and acute lung injury. Curr. Opin. Crit. Care 2001, 7:1-7.
18. Lue H., Kleemann R., Calandra T., Roger T., Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microb. Infect. 2002, 4:449-460.
19. Makita H., Nishimura M., Miyamoto K., Nakano T., Tanino Y., Hirokawa J., Nishihira J., Kawakami Y. Effect of anti-macrophage migration inhibitory factor antibody on lipopolysaccharide-induced pulmonary neutrophil accumulation. Am. J. Respir. Crit. Care Med. 1998, 158:573-579.
20. Mazzola S., Forni M., Albertini M., Bacci M.L., Zannoni A., Gentilini F., Lavitrano M., Bach F.H., Otterbein L.E., Clement M.G. Carbon monoxide pretreatment prevents respiratory derangement and ameliorates hyperacute endotoxic shock in pigs. FASEB J. 2005, 19:2045-2047.
21. Ollinger R., Bilban M., Erat A., Froio A., McDaid J., Tyagi S., Csizmadia E., Graça-Souza A.V., Liloia A., Soares M.P., Otterbein L.E., Usheva A., Yamashita K., Bach F.H. Bilirubin: a natural inhibitor of vascularsmooth muscle cell proliferation. Circulation 2005, 112:1030-1039.
22. Otterbein L.E., Bach F.H., Alam J., Soares M., Tao Lu.H., Wysk M., Davis R.J., Flavell R.A., Choi A.M. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 2000, 6:422-428.
23. Peng X., Hassoun P.M., Sammani S., McVerry B.J., Burne M.J., Rabb H., Pearse D., Tuder R.M., Garcia J.G. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am. J. Respir. Crit. Care Med. 2004, 169:1245-1251.
24. Piantadosi C.A., Schwartz D.A. The acute respiratory distress syndrome. Ann. Intern. Med. 2004, 141:460-470.
25. Roger T., Chanson A.L., Knaup-Reymond M., Calandra T. Macrophage migration inhibitory factorpromotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen activated protein kinase phosphatase-1. Eur. J. Immunol. 2005, 35:3405-3413.
26. Roger T., David J., Glauser M.P., Calandra T. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 2001, 414:920-924.
27. Roger T., Glauser M.P., Calandra T. Macrophage migration inhibitory factor (MIF) modulates innate immune responses induced by endotoxin and Gram-negative bacteria. J. Endotoxin Res. 2001, 7:456-460.
28. Steinberg K.P., Hudson L.D. Acute lung injury and acute respiratory distress syndrome. The clinical syndrome. Clin. Chest Med. 2000, 21:402-417. vii.
29. Sun B., Nishihira J., Yoshiki T., Kondo M., Sato Y., Sasaki F., Todo S. Macrophage migration inhibitory factor promotes tumor invasion and metastasis via the Rho-dependent pathway. Clin. Cancer Res. 2005, 11:1050-1058.
30. Szarka R.J., Wang N., Gordon L., Nation P.N., Smith R.H. A murine model of pulmonary damage induced by lipopolysaccharide via intranasal instillation. J. Immunol. Methods 1997, 202:49-57.
31. Tanino Y., Makita H., Miyamoto K., Betsuyaku T., Ohtsuka Y., Nishihira J., Nishimura M. Role of macrophage migration inhibitory factor in bleomycin-induced lung injury and fibrosis in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L156-L162.
32. Tenhunen R., Marver H.S., Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl. Acad. Sci. U.S.A. 1968, 61:748-755.
33. Tomashefski J.F. Pulmonary pathology of acute respiratory distress syndrome. Clin. Chest Med. 2000, 21:435-466.
34. Wang X., Wang Y., Kim H.P., Nakahira K., Ryter S.W., Choi A.M. Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J. Biol. Chem. 2007, 282:1718-1726.
35. Wiesel P., Patel A.P., DiFonzo N., Marria P.B., Sim C.U., Pellacani A., Maemura K., LeBlanc B.W., Marino K., Doerschuk C.M., Yet S.F., Lee M.E., Perrella M.A. Endotoxin-induced mortality is related to increased oxidative stress and end-organ dysfunction, not refractory hypotension, in heme oxygenase-1-deficient mice. Circulation 2000, 102:3015-3022.
36. Yamashita K., Ollinger R., McDaid J., Sakahama H., Wang H., Tyagi S., Csizmadia E., Smith N.R., Soares M.P., Bach F.H. Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J. 2006, 20:776-778.
37. Yet S.F., Pellacani A., Patterson C., Tan L., Folta S.C., Foster L., Lee W.S., Hsieh C.M., Perrella M.A. Induction of heme oxygenase-1 expression in vascular smooth muscle cells. A link to endotoxic shock. J. Biol. Chem. 1997, 272:4295-4301.
38. Yin H., Jin X.B., Gong Q., Yang H., Hu L.Y., Gong F.L., Zhu J.Y. Fructose-1,6-diphosphate attenuates acute lung injury induced by lipopolysaccharide in mice. Int. Immunopharmacol. 2008, 8:1842-1847.