Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice

Journal of Clinical Investigation

Volumn 118, Issue 1, 2008, Pages 239-247

  Su, Wol Chung ^a   Liu, Xiaoli ^a   Macias, Alvaro A ^a   Baron, Rebecca M ^a   Perrella, Mark A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; HEME OXYGENASE 1;

ANIMAL MODEL; ANTIMICROBIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; HOST RESISTANCE; INFLAMMATION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEPSIS;

ANIMALS; ANTIMETABOLITES; CARBON MONOXIDE; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FIBROBLASTS; GENE TARGETING; GRAM-POSITIVE BACTERIAL INFECTIONS; HEME OXYGENASE-1; HUMANS; IMMUNITY, NATURAL; INFLAMMATION; INFLAMMATION MEDIATORS; MICE; MICE, KNOCKOUT; MYOCYTES, SMOOTH MUSCLE; PHAGOCYTOSIS; SEPSIS;

EID: 38149008232     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI32730     Document Type: Article

References (48)

1. Hotchkiss, R.S., and Karl, I.E. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348:138-150.
2. Baron, R.M., Baron, M.J., and Perrella, M.A. 2006. Pathobiology of sepsis. Are we still asking the same questions? Am. J. Respir. Cell Mol. Biol. 34:129-134.
3. Levy, M.M., et al. 2003. 2001 SCCM/ESICM/ACCP/ ATS/SIS International Sepsis Definitions Conference. Crit. Care Med. 31:1250-1256.
4. Bone, R.C., Grodzin, C.J., and Balk, R.A. 1997. Sepsis: A new hypothesis for pathogenesis of the disease process. Chest. 112:235-243.
5. Pinsky, M.R. 2001. Sepsis: a pro- and anti-inflammatory disequilibrium syndrome. Contrib. Nephrol. 132:354-366.
6. Rivers, E., et al. 2001. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N. Engl. J. Med. 345:1368-1377.
7. Rivers, E.P., McIntyre, L., Morro, D.C., and Rivers, K.K. 2005. Early and innovative interventions for severe sepsis and septic shock: taking advantage of a window of opportunity. CMAJ. 173:1054-1065.
8. Bernard, G., et al. 2001. Efficacy and safety of recombinant human activated protein C for severe sepsis. N. Engl. J. Med. 344:699-709.
9. Annane, D., Bellissant, E., and Cavaillon, J.M. 2005. Septic shock. Lancet. 365:63-78.
10. Riedemann, N.C., Guo, R.-F., and Ward, P.A. 2003. Novel strategies for the treatment of sepsis. Nat. Med. 9:517-524.
11. Strober, W., Murray, P.J., Kitani, A., and Watanabe, T. 2006. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6:9-20.
12. Takeda, K., and Akira, S. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17:1-14.
13. Elphick, D.A., and Mahida, Y.R. 2005. Paneth cells: their role in innate immunity and inflammatory disease. Gut. 54:1802-1809.
14. Kobayashi, K.S., et al. 2005. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science. 307:731-734.
15. Poss, K.D., and Tonegawa, S. 1997. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. U. S. A. 94:10925-10930.
16. Yet, S.-F., et al. 1999. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J. Clin. Invest. 103:R23-R29.
17. Wiesel, P., et al. 2000. Endotoxin-induced mortality is related to increased oxidative stress and endorgan dysfunction, not refractory hypotension, in heme oxygenase-1 deficient mice. Circulation. 102:3015-3022.
18. Abraham, N.G., and Kappas, A. 2005. Heme oxygenase and the cardiovascular-renal system. Free Radic. Biol. Med. 39:1-25.
19. Maines, M.D., and Gibbs, P.E.M. 2005. 30 years of heme oxygenase: From a "molecular wrecking ball" to a "mesmerizing" trigger of cellular events. Biochem. Biophys. Res. Commun. 338:568-577.
20. Ryter, S.W., Alam, J., and Choi, A.M.K. 2006. Heme oxygenase-1/carbon monoxide: From basic science to therapeutic implications. Physiol. Rev. 86:583-650.
21. Stocker, R., Yamamoto, Y., McDonagh, A.F., Glazer, A.N., and Ames, B.N. 1987. Bilirubin is an antioxidant of possible physiological importance. Science. 235:1043-1046.
22. Sarady-Andrews, J.K., et al. 2005. Biliverdin administration protects against endotoxin-induced acute lung injury in rats. Am. J. Physiol. Lung Cell Mol. Physiol. 289:L1131-L1137.
23. Balla, G., et al. 1992. Ferritin: a cytoprotective antioxidant strategem of endothelium. J. Biol. Chem. 267:18148-18153.
24. Otterbein, L.E., et al. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6:422-428.
25. Morse, D., et al. 2003. Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J. Biol. Chem. 278:36993-36998.
26. Mazzola, S., et al. 2005. Carbon monoxide pretreatment prevents respiratory derangement and ameliorates hyperacute endotoxic shock in pigs. FASEB J. 19:2045-2047.
27. Foresti, R., et al. 2005. Reviewing the use of carbon monoxide-releasing molecules (CO-RMs) in biology: implications in endotoxin-mediated vascular dysfunction. Cell. Mol. Biol. 51:409-423.
28. Overhaus, M., et al. 2006. Biliverdin protects against polymicrobial sepsis by modulating inflammatory mediators. Am. J. Physiol. (Gastrointest. Liver Physiol.) 290:G695-G703.
29. Layne, M.D., et al. 2002. Characterization of the mouse aortic carboxypeptidase-like protein promoter reveals activity in differentiated and dedifferentiated vascular smooth muscle cells. Circ. Res. 90:728-736.
30. Yet, S.-F., et al. 2001. Cardiac specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ. Res. 89:168-173.
31. Yet, S.-F., Melo, L.G., Layne, M.D., and Perrella, M.A. 2002. Heme oxygenase-1 in the regulation of inflammation and oxidative damage. Methods Enzymol. 353:163-176.
32. Imai, T., et al. 2001. Vascular smooth muscle cell-directed overexpression of heme oxygenase-1 elevates blood pressure through attenuation of nitric oxide-induced vasodilation in mice. Circ. Res. 89:55-62.
33. Matute-Bello, G., et al. 2001. Septic shock and acute lung injury in rabbits with peritonitis. Am. J. Respir. Crit. Care Med. 163:234-243.
34. Minamino, T., et al. 2001. Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 98:8798-8803.
35. Stone, R. 1994. Search for sepsis drugs goes on despite past failures. Science. 264:365-367.
36. Angus, D.C., et al. 2001. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29:1303-1310.
37. Hotchkiss, R.S., et al. 1999. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 27:1230-1251.
38. Otterbein, L.E., May, A., and Chin, B.Y. 2005. Carbon monoxide increases macrophage bacterial clearance through Toll-like receptor (TLR)4 expression. Cell. Mol. Biol. 51:433-440.
39. Nakahira, K., et al. 2006. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J. Exp. Med. 203:2377-2389.
40. Cario, E. 2005. Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut. 54:1182-1193.
41. Exner, M., Minar, E., Wagner, O., and Schillinger, M. 2004. The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radic. Biol. Med. 37:1097-1104.
42. Yachie, A., et al. 1999. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103:129-135.
43. Wang, P., Ba, Z.F., and Chaudry, I.H. 1992. Hepatocellular dysfunction persists during early sepsis despite increased volume of crystalloid resuscitation. J. Trauma. 32:389-396.
44. Motterlini, R., et al. 2002. Carbon monoxide-releasing molecules. Characterization of biochemical and vascular activities. Circ. Res. 90:e17-e24.
45. Baker, C.C., Chaudry, I.H., Gaines, H.O., and Baue, A.E. 1983. Evaluation of factors affecting mortality rate after sepsis in a murine cecal ligation and puncture model. Surgery. 94:331-335.
46. Godshall, C.J., Scott, M.J., Peyton, J.C., Gardner, S.A., and Cheadle, W.G. 2002. Genetic background determines susceptibility during murine septic peritonitis. J. Surg. Res. 102:45-49.
47. Henneke, P., et al. 2002. Cellular activation, phagocytosis, and bactericidal activity against group B streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways. J. Immunol. 169:3970-3977.
48. Arikan, M.C., Shapiro, S.D., and Mariani, T.J. 2005. Induction of macrophage elastase (MMP-12) gene expression by statins. J. Cell Physiol. 204:139-145.