IRG1 induced by heme oxygenase-1/carbon monoxide inhibits LPS-mediated sepsis and pro-inflammatory cytokine production

Cellular and Molecular Immunology

Volumn 13, Issue 2, 2016, Pages 170-179

  Uddin, Md Jamal ^a   Joe, Yeonsoo ^a   Kim, Seul Ki ^a   Jeong, Sun Oh ^b   Ryter, Stefan W ^c   Pae, Hyun Ock ^b   Chung, Hun Taeg ^a  

^a University of Ulsan   (South Korea)

^b Wonkwang University   (South Korea)

^c NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

A20; anti inflammatory effects; carbon monoxide; HO 1; IRG1

Indexed keywords

CARBON MONOXIDE; HEME OXYGENASE 1; IMMUNORESPONSIVE GENE 1 PROTEIN; MESSENGER RNA; NITRIC OXIDE; PROTOPORPHYRIN ZINC; REGULATOR PROTEIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN A20; HMOX1 PROTEIN, MOUSE; HYDROLYASE; IRG1 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; TNFAIP3 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA INDUCED PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINE RAW 264.7; CONTROLLED STUDY; CYTOKINE PRODUCTION; LIPOPOLYSACCHARIDE-INDUCED SEPSIS; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; IMMUNOLOGY; PATHOLOGY; SEPSIS;

ANIMALS; CARBON MONOXIDE; CELL LINE; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; HYDRO-LYASES; LIPOPOLYSACCHARIDES; MALE; MEMBRANE PROTEINS; MICE; SEPSIS; TUMOR NECROSIS FACTOR ALPHA-INDUCED PROTEIN 3; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84959872829     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2015.02     Document Type: Article

References (46)

1. Hotchkiss RS, Opal S. Immunotherapy for sepsis-a new approach against an ancient foe. N Engl J Med 2010; 363: 87-89.
2. Riedemann NC, Guo RF, Ward PA. Novel strategies for the treatment of sepsis. Nat Med 2003; 9: 517-524.
3. David S, Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 2011; 12: 388-399.
4. Lee CG, Jenkins NA, Gilbert DJ, Copeland NG, O'Brien WE. Cloning and analysis of gene regulation of a novel LPS-inducible cDNA. Immunogenetics 1995; 41: 263-270.
5. Tangsudjai S, Pudla M, Limposuwan K, Woods DE, Sirisinha S, Utaisincharoen P. Involvement of the MyD88-independent pathway in controlling the intracellular fate of Burkholderia pseudomallei infection in the mouse macrophage cell line RAW 264.7. Microbiol Immunol 2010; 54: 282-290.
6. Degrandi D, Hoffmann R, Beuter-Gunia C, Pfeffer K. The proinflammatory cytokine-induced IRG1 protein associates with mitochondria. J Interferon Cytokine Res 2009; 29: 55-67.
7. Matulova M, Rajova J, Vlasatikova L, Volf J, Stepanova H, Havlickova H et al. Characterization of chicken spleen transcriptome after infection with Salmonella enterica serovar Enteritidis. PLoS One 2012; 7: e48101.
8. Cheon YP, Xu X, Bagchi MK, Bagchi IC. Immune-responsive gene 1 is a novel target of progesterone receptor and plays a critical role during implantation in the mouse. Endocrinology 2003; 144: 5623-5630.
9. Mor G, Cardenas I, Abrahams V, Guller S. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann NY Acad Sci 2011; 1221: 80-87.
10. Li H, Gang Z, Yuling H, Luokun X, Jie X, Hao L et al. Different neurotropic pathogens elicit neurotoxic CCR9- or neurosupportive CXCR3-expressing microglia. J Immunol 2006; 177: 3644-3656.
11. Li Y, Zhang P, Wang C, Han C, Meng J, Liu X et al. Immune responsive gene 1 (IRG1) promotes endotoxin tolerance by increasing A20 expression in macrophages through reactive oxygen species. J Biol Chem 2013; 288: 16225-16234.
12. Maines MD. The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997; 37: 517-554.
13. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006; 86: 583-650.
14. Devesa I, Ferrandiz ML, Terencio MC, Joosten LA, van den Berg WB, Alcaraz MJ. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis Rheum 2005; 52: 3230-3238.
15. Hegazi RA, Rao KN, Mayle A, Sepulveda AR, Otterbein LE, Plevy SE. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Expe Med 2005; 202: 1703-1713.
16. Lee TS, Chau LY. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 2002; 8: 240-246.
17. Mandal P, Park PH, McMullen MR, Pratt BT, Nagy LE. The antiinflammatory effects of adiponectin are mediated via a heme oxygenase-1-dependent pathway in rat Kupffer cells. Hepatology 2010; 51: 1420-1429.
18. Koch A, Boehm O, Zacharowski PA, Loer SA, Weimann J, Rensing H et al. Inducible nitric oxide synthase and heme oxygenase-1 in the lung during lipopolysaccharide tolerance and cross tolerance. Crit Care Med 2007; 35: 2775-2784.
19. Soriano RN, Ravanelli MI, Batalhao ME, Carnio EC, Branco LG. Glucocorticoids downregulate systemic nitric oxide synthesis and counteract overexpression of hepatic heme oxygenase-1 during endotoxin tolerance. Can J Physiol Pharmacol 2013; 91: 861-865.
20. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, Green CJ. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res 2002; 90: E17-E24.
21. Ewing P, Hildebrandt GC, Planke S, Andreesen R, Holler E, Gerbitz A. Cobalt protoporphyrine IX-mediated heme oxygenase-I induction alters the inflammatory cytokine response, but not antigen presentation after experimental allogeneic bone marrow transplantation. Int J Mol Med 2007; 20: 301-308.
22. Anderson KE, Collins S. Open-label study of hemin for acute porphyria: clinical practice implications. Am J Med 2006; 119: 801.e819-801.e 824.
23. Devadas K, Dhawan S. Hemin activation ameliorates HIV-1 infection via heme oxygenase-1 induction. J Immunol 2006; 176: 4252-4257.
24. Paxinou E, Weisse M, Chen Q, Souza JM, Hertkorn C, Selak M et al. Dynamic regulation of metabolism and respiration by endogenously produced nitric oxide protects against oxidative stress. Proc Natl Acad Sci USA 2001; 98: 11575-11580.
25. Beltran B, Mathur A, Duchen MR, Erusalimsky JD, Moncada S. The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death. Proc Natl Acad Sci USA 2000; 97: 14602-14607.
26. Hartsfield CL, Alam J, Cook JL, Choi AM. Regulation of heme oxygenase-1 gene expression in vascular smooth muscle cells by nitric oxide. Am J Physiol 1997; 273(5 Pt 1): L980-L988.
27. Sun SC. Deubiquitylation and regulation of the immune response. Nat Rev Immunol 2008; 8: 501-511.
28. Opipari AW Jr, Hu HM, Yabkowitz R, Dixit VM. The A20 zinc finger protein protects cells from tumor necrosis factor cytotoxicity. J Biol Chem 1992; 267: 12424-12427.
29. Otterbein L, Sylvester SL, Choi AM. Hemoglobin provides protection against lethal endotoxemia in rats: the role of heme oxygenase-1. Am J Respir Cell Mol Biol 1995; 13: 595-601.
30. Yu JB, Yao SL. Protective effects of hemin pretreatment combined with ulinastatin on septic shock in rats. Chin Med J 2008; 121: 49-55.
31. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008; 13: 453-461.
32. Park MK, Kang YJ, Ha YM, Jeong JJ, Kim HJ, Seo HG et al. EP2 receptor activation by prostaglandin E2 leads to induction of HO-1 via PKA and PI3K pathways in C6 cells. Biochem Biophys Res Commun 2009; 379: 1043-1047.
33. Tsoyi K, Jang HJ, Kim JW, Chang HK, Lee YS, Pae HO et al. Stimulation of alpha7 nicotinic acetylcholine receptor by nicotine attenuates inflammatory response in macrophages and improves survival in experimental model of sepsis through heme oxygenase-1 induction. Antioxid Redox Signal 2011; 14: 2057-2070.
34. Shih RH, Yang CM. Induction of heme oxygenase-1 attenuates lipopolysaccharide-induced cyclooxygenase-2 expression in mouse brain endothelial cells. J Neuroinflamm 2010; 7: 86.
35. Kantrow SP, Taylor DE, Carraway MS, Piantadosi CA. Oxidative metabolism in rat hepatocytes and mitochondria during sepsis. Arch Biochem Biophys 1997; 345: 278-288.
36. Piantadosi CA, Carraway MS, Babiker A, Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 2008; 103: 1232-1240.
37. Piantadosi CA, Withers CM, Bartz RR, MacGarvey NC, Fu P, Sweeney TE et al. Heme oxygenase-1 couples activation of mitochondrial biogenesis to anti-inflammatory cytokine expression. J Biol Chem 2011; 286: 16374-16385.
38. Hall CJ, Boyle RH, Astin JW, Flores MV, Oehlers SH, Sanderson LE et al. Immunoresponsive gene 1 augments bactericidal activity of macrophage-lineage cells by regulating beta-oxidation-dependent mitochondrial ROS production. Cell Metab 2013; 18: 265-278.
39. Naik E, Dixit VM. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J Exp Med 2011; 208: 417-420.
40. Michelucci A, Cordes T, Ghelfi J, Pailot A, Reiling N, Goldmann O et al. Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proc Natl Acad Sci USA 2013; 110: 7820-7825.
41. Yang G, Nguyen X, Ou J, Rekulapelli P, Stevenson DK, Dennery PA. Unique effects of zinc protoporphyrin on HO-1 induction and apoptosis. Blood 2001; 97: 1306-1313.
42. Hara E, Takahashi K, Takeda K, Nakayama M, Yoshizawa M, Fujita H et al. Induction of heme oxygenase-1 as a response in sensing the signals evoked by distinct nitric oxide donors. Biochem Pharmacol 1999; 58: 227-236.
43. Opipari AW Jr, Boguski MS, Dixit VM. The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J Biol Chem 1990; 265: 14705-14708.
44. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP et al. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 2000; 289: 2350-2354.
45. Beyaert R, Heyninck K, van Huffel S. A20 and A20-binding proteins as cellular inhibitors of nuclear factor-kappa B-dependent gene expression and apoptosis. Biochem Pharmacol 2000; 60: 1143-1151.
46. Oberholzer A, Oberholzer C, Moldawer LL. Sepsis syndromes: understanding the role of innate and acquired immunity. Shock 2001; 16: 83-96.