Carbon monoxide has anti-inflammatory effects involving the mitogen- activated protein kinase pathway

Nature Medicine

Volumn 6, Issue 4, 2000, Pages 422-428

  Otterbein, Leo E ^a,c   Bach, Fritz H ^f   Alam, Jawed ^e   Soares, Miguel ^f   Lu, Hong Tao ^a   Wysk, Mark ^d   Davis, Roger J ^d   Flavell, Richard A ^a   Choi, Augustine M K ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e OCHSNER MEDICAL CENTER   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; COMPLEMENTARY DNA; CYCLIC GMP; CYTOKINE; HEME OXYGENASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ENZYME ACTIVITY; GENE OVEREXPRESSION; INFLAMMATORY DISEASE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CARBON MONOXIDE; CELL LINE; CELLS, CULTURED; CYCLIC GMP; ENZYME ACTIVATION; GENE EXPRESSION; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; INTERFERON TYPE II; INTERLEUKIN-1; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGE INFLAMMATORY PROTEIN-1; MACROPHAGES, PERITONEAL; MALE; MAP KINASE KINASE 3; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGENS; NITRIC OXIDE; PROTEIN-TYROSINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RNA PROCESSING, POST-TRANSCRIPTIONAL; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 0034071424     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/74680     Document Type: Article

References (45)

1. Tenhunen, R., Marver, H.S. & Schmid, R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase Proc. Natl. Acad. Sci. USA 61, 748-755 (1968).
2. Nath, D.A., Balla, G., Vercelotti, G.M. & Jacob, J. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J. Clin. Invest. 90, 267-270 (1992).
3. Poss, K.D. & Tonegawa, S. Reduced stress defense in heme oxygenase deficient cells. Proc. Natl. Acad. Sci. USA 94, 10925-10930 (1997).
4. Yachie, A., Niida, Y., Wada, T., Igarashi, N. & Kaneda, H. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103, 129-135 (1999).
5. Otterbein, L.E., Sylvester, S. L. & Choi, A.M.K. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am. J. Respir. Cell. Mol. Biol. 13, 595-601 (1995).
6. Lee, P.J., Alam, J., Wiegand, C.W. & Choi, A.M.K. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc. Natl. Acad. Sci. USA. 93, 10393-10398 (1996).
7. Otterbein, L.E. et al. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J. Clin. Invest. 103, 1047-1054 (1999).
8. Parillo, J.E., Parker, M.M., Natanson, A.F., Suffredini, R.I. & Danner, R.E. Septic shock in humans. Advances in the understanding of pathogenesis, cardiovascular dysfunction and therapy. Ann. Intern. Med. 113, 991-992 (1992).
9. Beutler, B, Krochin, N., Milsark, I.W., Luedke, C. & Cerami, A. Control of cachectin (tumor necrosis factor) synthesis: mechanisms of endotoxin resistance. Science 232, 977-980 (1986).
10. Netea, M. G., Kullberg, B. J. & van der Meer, J. W. Lipopolysaccharide-induced production of tumor necrosis factor and interleukin-1 is differentially regulated at the receptor level: the role of CD14-dependent and CD14-independent pathways. Immunology 94, 340-344 (1998).
11. Howard, M., Muchamuel, T., Andrade, S. & Menon, S. Interleukin-10 protects mice from lethal endotoxemia. J. Exp. Med. 177, 1205-1208 (1993).
12. Yang, R. et al. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signaling. Nature 395, 284-288 (1998).
13. Chow, J.C., Young, D.W., Golenbock, D.T., Christ, W.J. & Gusovsky, F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274, 10689-10692 (1999).
14. Hambleton, J., Weinstein, S.L., Lem, L. & DeFranco, A.L. Activation of c-Jun N-terminal kinase in bacterial lipopolysaccharide-stimulated macrophages. Proc. Natl. Acad. Sci. USA 93, 2274-2778 (1996).
15. Han, J., Lee, J.D., Bibbs, L. & Ulevitch, R.J. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265, 808-811 (1994).
16. Raingeaud, J., Gupta, S., Han, J., Ulevitch, R.J. & Davis, R.J. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270, 7420-7426 (1995).
17. Thomassen, M.J. et al. Nitric oxide inhibits inflammatory cytokine production by human alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 17, 279-283 (1997).
18. Morita, T., Perrella, M.A., Lee, M. & Kourembanas, S. Smooth muscle cell-derived carbon monoxide is a regulator of vascular cGMP. Proc. Natl. Acad. Sci. USA 92, 1475-1479 (1995).
19. Verma, A., Hirsch, D.J., Glatt, C.E., Ronnett, G.V. & Snyder, S.H. Carbon monoxide, a putative neural messenger. Science 259, 381-384 (1993).
20. Tetreau, C., Tourbez, M., Gorren, A., Mayer, B. & Lavalette, D. Dynamics of carbon monoxide binding with neuronal nitric oxide synthase. Biochem. 38, 7210-7218 (1999).
21. Derijard, B. et al. Independent human MAP kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267, 682-685 (1995).
22. Raingeaud, J., Whitmarsh, A.J., Barrett, T., Derijard, B. & Davis, R.J. MKK3 and MKK6 regulation of gene expression is mediated by the p38 MAP kinase signal transduction pathway. Mol. Cell. Biol. 16, 1247-1255 (1996).
23. Bauss, F., Droge, W. & Manel, D.N. Tumor necrosis factor mediates endotoxic shock in mice. Infect. Immun. 55, 1622-1625 (1987).
24. Badger, A.M. et al. Pharmacological profile of SB 203580, a selective inhibitor of cytokine suppressive binding protein/p38 kinase, in animal models of arthritis, bone resorption, endotoxin shock and immune function. J. Pharm. Exp. Ther. 279, 1453-1461 (1996).
25. Wysk, M., Yang, D., Lu, H-T., Flavell, R.A. & Davis, R.J. TNF-induced cytokine expression mediated by the p38 MAP kinase activator MKK3. Proc. Natl. Acad. Sci. USA 96, 3763-3768 (1999).
26. Geppert, T.D., Whitehurst, C.E., Thompson, P. & Beutler, B. Lipopolysaccharide signals activation of tumor necrosis factor biosynthesis through the ras/raf-1/MEK/MAPK pathway. Mol. Med. 1, 93-103 (1994).
27. Stocker, R., Yamamoto, Y., McDonagh, A.F., Glazer, A.N. & Ames, B.N. Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046 (1987).
28. Llesuy, S. & Tomaro, M. Heme oxygenase and oxidative stress. Evidence of involvement of bilirubin as physiological protector against oxidative damage. Biochim. Biophys. Acta 1223, 9-14 (1994).
29. Balla, J. et al. Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. Proc. Natl. Acad. Sci. USA 90, 9285-9289 (1993).
30. Stupfel, M. & Bouley, G. Physiological and biochemical effects on rats and mice exposed to small concentrations of carbon monoxide for long periods. Ann. NY Acad. Sci. 174, 342-368 (1970).
31. Foey, A. D. et al. Regulation of monocyte IL-10 synthesis by endogenous IL-1 and TNF-alpha: role of the p38 and p42/44 mitogen-activated protein kinases. J. Immunol. 160, 920-928 (1998).
32. Elbirt, K.K., Whitmarsh, A.J. & Davis, R.J. Mechanism of sodium arsenite-mediated induction of heme oxygenase-a in hepatoma cells: involvement of MAP kinase. J. Biol. Chem. 273, 8922-8931 (1998).
33. Szabo, C., Hasko, G., Nemeth, Z.H. & Vizi, E.S. Calcium entry blockers increase interleukin-10 production in endotoxemia. Shock 7, 304-307 (1997).
34. Nemeth, Z.H., Hasko, G., Szabo, C. & Vizi, E.S. Amrinone and theophylline differentially regulate cytokine and nitric oxide production in endotoxemic mice. Shock 7, 371-375 (1997).
35. Hasko, G., Szabo, C., Nemeth, Z.H., Salzman, A.L. & Vizi, E.S. Suppression of IL-12 production by phosphodiesterase inhibition in murine endotoxemia is interleukin-10 independent. Eur. J. Immunol. 28, 468-472 (1998).
36. Jongeneel, C.V. Regulation of the TNF alpha gene. Prog. Clin. Biol. Res. 388, 367-381 (1994).
37. Han, J., Brown, T. & Beutler, B. Endotoxin-responsive sequences control cachectin/tumor necrosis factor biosynthesis at the translational level. J. Exp. Med. 171, 465-475 (1990).
38. Han, J.H., Beutler, B. & Huez, G. Complex regulation of tumor necrosis factor mRNA turnover in lipopolysaccharide-activated macrophages. Biochim. Biophys. Acta 1090, 22-28 (1991).
39. Soares, M.P. et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nature Med. 4, 1073-1077 (1998).
40. Otterbein, L.E., Mantell, L.L. & Choi, A.M.K. Carbon monoxide provides protection against hyperoxic lung injury. Am. J. Physiol. 276, L688-L694 (1999).
41. Lu, H-T. et al. Defective IL-12 production in mitogen-activated protein (MAP) kinase kinase 3 (Mkk3)-deficient mice. IMBO J. 18, 1845-1857 (1999).
42. Shibahara, S., Meller, R., Taguchi, H. & Yoshida, T. Cloning and expression of cDNA for ratheme oxygenase. Proc. Natl. Acad. Sci. USA 82, 7865-7869 (1985).
43. Fuhlbrigge, R.C., Fine, S.M., Unanue, E.R. & Chaplin, D.D. Expression of mem-brane interleukin 1 by fibroblasts transfected with murine pro-interleukin 1 alpha cDNA. Proc. Natl. Acad. Sci. USA 85, 5649-5653 (1988).
44. Alam, J. Multiple elements within the 5′ distal enhancer of the mouse heme oxygenase-1 gene mediate induction by heavy metals. J. Biol. Chem. 269, 25049-25056 (1994).
45. Gunther, S., Alexander, R.W., Atkinson, W.J. & Gimbrone, M.A. Functional angiotensin II receptors in cultured vascular smooth muscle cells. J. Cell. Biol. 92, 289-298 (1982).