Carbon monoxide and heme oxygenase-1 prevent intestinal inflammation in mice by promoting bacterial clearance

Gastroenterology

Volumn 144, Issue 4, 2013, Pages 789-798

  Onyiah, Joseph C ^a   Sheikh, Shehzad Z ^a   Maharshak, Nitsan ^a   Steinbach, Erin C ^a   Russo, Steven M ^a   Kobayashi, Taku ^a   Mackey, Lantz C ^a   Hansen, Jonathan J ^a   Moeser, Adam J ^b   Rawls, John F ^a   Borst, Luke B ^b   Otterbein, Leo E ^c   Plevy, Scott E ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anti Inflammatory Agent; IBD; Mouse Model; Ulcerative Colitis

Indexed keywords

ALF 186; ALFAMA CARBON MONOXIDE RELEASING MOLECULE 186; BACTERIAL DNA; CARBON MONOXIDE; COBALT PROTOPORPHYRIN 9 CHLORIDE; GASTROINTESTINAL AGENT; GENOMIC DNA; HEME OXYGENASE 1; INTERLEUKIN 10; PORPHYRIN; SODIUM CHLORIDE; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CLEARANCE; BACTERICIDAL ACTIVITY; CELL CULTURE; COLITIS; COLON; CONTROLLED STUDY; EMBRYO; ENTERITIS; ENTEROCOCCUS FAECALIS; ENTEROCOLITIS; ESCHERICHIA COLI; GENE SILENCING; GERMFREE ANIMAL; INTESTINE FLORA; LAMINA PROPRIA; LIVER; MACROPHAGE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PHAGOLYSOSOME; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; SPLEEN; TYPHOID FEVER; WILD TYPE; ZEBRA FISH;

EID: 84875278108     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2012.12.025     Document Type: Article

References (33)

1. R.J. Xavier, D.K. Podolsky Unravelling the pathogenesis of inflammatory bowel disease Nature 448 2007 427 434
2. H. Jick, A.M. Walker Cigarette smoking and ulcerative colitis N Engl J Med 308 1983 261 263
3. S.W. Ryter, A.M. Choi Cytoprotective and anti-inflammatory actions of carbon monoxide in organ injury and sepsis models Novartis Found Symp 280 2007 165 181
4. L.E. Otterbein, M.P. Soares, K. Yamashita Heme oxygenase-1: unleashing the protective properties of heme Trends Immunol 24 2003 449 455
5. R.A. Hegazi, K.N. Rao, A. Mayle Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway J Exp Med 202 2005 1703 1713
6. S.Z. Sheikh, R.A. Hegazi, T. Kobayashi An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis J Immunol 186 2011 5506 5513
7. T.T. MacDonald, P.B. Carter Contact sensitivity in the germ-free mouse J Reticuloendothel Soc 24 1978 287 293
8. S.Z. Sheikh, T. Kobayashi, K. Matsuoka Characterization of an interferon-stimulated response element (ISRE) in the Il23a promoter J Biol Chem 286 2011 1174 1180
9. M. Barthel, S. Hapfelmeier, L. Quintanilla-Martinez Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host Infect Immun 71 2003 2839 2858
10. R.A. Argenzio, J.A. Liacos Endogenous prostanoids control ion transport across neonatal porcine ileum in vitro Am J Vet Res 51 1990 747 751
11. A.J. Moeser, K.A. Ryan, P.K. Nighot Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs Am J Physiol Gastrointest Liver Physiol 293 2007 G413 G421
12. A.J. Moeser, L.B. Borst, B.L. Overman Defects in small intestinal epithelial barrier function and morphology associated with peri-weaning failure to thrive syndrome (PFTS) in swine Res Vet Sci 93 2012 975 982
13. L.N. Pham, M. Kanther, I. Semova Methods for generating and colonizing gnotobiotic zebrafish Nat Protoc 3 2008 1862 1875
14. M. Kanther, X. Sun, M. Muhlbauer Microbial colonization induces dynamic temporal and spatial patterns of NF-kappaB activation in the zebrafish digestive tract Gastroenterology 141 2011 197 207
15. H. Xiong, C. Zhu, F. Li Inhibition of interleukin-12 p40 transcription and NF-{kappa}B activation by nitric oxide in murine macrophages and dendritic cells J Biol Chem 279 2004 10776 10783
16. D.N. Frank, A.L. St Amand, R.A. Feldman Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Proc Natl Acad Sci U S A 104 2007 13780 13785
17. H.P. Horz, M.E. Vianna, B.P. Gomes Evaluation of universal probes and primer sets for assessing total bacterial load in clinical samples: general implications and practical use in endodontic antimicrobial therapy J Clin Microbiol 43 2005 5332 5337
18. J. Alam, D. Stewart, C. Touchard Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene J Biol Chem 274 1999 26071 26078
19. R.K. Thimmulappa, K.H. Mai, S. Srisuma Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray Cancer Res 62 2002 5196 5203
20. T. Suzuki, Y. Takagi, H. Osanai Pi class glutathione S-transferase genes are regulated by Nrf 2 through an evolutionarily conserved regulatory element in zebrafish Biochem J 388 2005 65 73
21. R. Motterlini, L.E. Otterbein The therapeutic potential of carbon monoxide Nat Rev Drug Discov 9 2010 728 743
22. D.J. Berg, J. Zhang, J.V. Weinstock Rapid development of colitis in NSAID-treated IL-10-deficient mice Gastroenterology 123 2002 1527 1542
23. S.W. Chung, X. Liu, A.A. Macias Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice J Clin Invest 118 2008 239 247
24. M.H. Zaki, S. Fujii, T. Okamoto Cytoprotective function of heme oxygenase 1 induced by a nitrated cyclic nucleotide formed during murine salmonellosis J Immunol 182 2009 3746 3756
25. C. Abraham, R. Medzhitov Interactions between the host innate immune system and microbes in inflammatory bowel disease Gastroenterology 140 2011 1729 1737
26. Y. Ueda, H. Kayama, S.G. Jeon Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10 Int Immunol 22 2010 953 962
27. T. Kobayashi, K. Matsuoka, S.Z. Sheikh IL-10 regulates Il12b expression via histone deacetylation: implications for intestinal macrophage homeostasis J Immunol 189 2012 1792 1799
28. K.L. Madsen, D. Malfair, D. Gray Interleukin-10 gene-deficient mice develop a primary intestinal permeability defect in response to enteric microflora Inflamm Bowel Dis 5 1999 262 270
29. H.W. Mittrucker, S.H. Kaufmann Immune response to infection with Salmonella typhimurium in mice J Leukoc Biol 67 2000 457 463
30. H. Kohler, T. Sakaguchi, B.P. Hurley Salmonella enterica serovar Typhimurium regulates intercellular junction proteins and facilitates transepithelial neutrophil and bacterial passage Am J Physiol Gastrointest Liver Physiol 293 2007 G178 G187
31. C. Reinhard, J.D. Rioux Role of the IBD5 susceptibility locus in the inflammatory bowel diseases Inflamm Bowel Dis 12 2006 227 238
32. J.H. Cho The genetics and immunopathogenesis of inflammatory bowel disease Nat Rev Immunol 8 2008 458 466
33. L.E. Otterbein, A. May, B.Y. Chin Carbon monoxide increases macrophage bacterial clearance through Toll-like receptor (TLR)4 expression Cell Mol Biol (Noisy-le-grand) 51 2005 433 440