Heme oxygenase-1 and carbon monoxide regulate intestinal homeostasis and mucosal immune responses to the enteric microbiota

References

• Abraham C, Medzhitov R. Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 2011; 140:1729 - 37; http://dx.doi.org/10.1053/j.gastro.2011.02.012; PMID: 21530739
   PubMed Web of Science ®Google Scholar
• Cope GF, Heatley RV, Kelleher J, Lee PN. Cigarette smoking and inflammatory bowel disease: a review. Hum Toxicol 1987; 6:189 - 93; http://dx.doi.org/10.1177/096032718700600303; PMID: 3298000
   PubMedGoogle Scholar
• Pullan RD, Rhodes J, Ganesh S, Mani V, Morris JS, Williams GT, Newcombe RG, Russell MA, Feyerabend C, Thomas GA, et al. Transdermal nicotine for active ulcerative colitis. N Engl J Med 1994; 330:811 - 5; http://dx.doi.org/10.1056/NEJM199403243301202; PMID: 8114833
   PubMed Web of Science ®Google Scholar
• Lashner BA, Hanauer SB, Silverstein MD. Testing nicotine gum for ulcerative colitis patients. Experience with single-patient trials. Dig Dis Sci 1990; 35:827 - 32; http://dx.doi.org/10.1007/BF01536795; PMID: 2194767
   PubMed Web of Science ®Google Scholar
• Otterbein LE, Lee PJ, Chin BY, Petrache I, Camhi SL, Alam J, Choi AM. Protective effects of heme oxygenase-1 in acute lung injury. Chest 1999; 116:Suppl 61S - 3S; http://dx.doi.org/10.1378/chest.116.suppl_1.61S-a; PMID: 10424595
   PubMedGoogle Scholar
• Soares MP, Lin Y, Anrather J, Csizmadia E, Takigami K, Sato K, Grey ST, Colvin RB, Choi AM, Poss KD, et al. Expression of heme oxygenase-1 can determine cardiac xenograft survival. Nat Med 1998; 4:1073 - 7; http://dx.doi.org/10.1038/2063; PMID: 9734404
   PubMed Web of Science ®Google Scholar
• Ryter SW, Choi AM. Cytoprotective and anti-inflammatory actions of carbon monoxide in organ injury and sepsis models. Novartis Found Symp 2007; 280:165 - 75, discussion 175-81; http://dx.doi.org/10.1002/9780470059593.ch12; PMID: 17380794
   PubMedGoogle Scholar
• Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6:422 - 8; http://dx.doi.org/10.1038/74680; PMID: 10742149
   PubMed Web of Science ®Google Scholar
• Takagi T, Naito Y, Mizushima K, Akagiri S, Suzuki T, Hirata I, Omatsu T, Handa O, Kokura S, Ichikawa H, et al. Inhalation of carbon monoxide ameliorates TNBS-induced colitis in mice through the inhibition of TNF-α expression. Dig Dis Sci 2010; 55:2797 - 804; http://dx.doi.org/10.1007/s10620-009-1112-x; PMID: 20094779
   PubMed Web of Science ®Google Scholar
• Takagi T, Naito Y, Uchiyama K, Suzuki T, Hirata I, Mizushima K, Tsuboi H, Hayashi N, Handa O, Ishikawa T, et al. Carbon monoxide liberated from carbon monoxide-releasing molecule exerts an anti-inflammatory effect on dextran sulfate sodium-induced colitis in mice. Dig Dis Sci 2011; 56:1663 - 71; http://dx.doi.org/10.1007/s10620-010-1484-y; PMID: 21086163
   PubMed Web of Science ®Google Scholar
• Sheikh SZ, Hegazi RA, Kobayashi T, Onyiah JC, Russo SM, Matsuoka K, Sepulveda AR, Li F, Otterbein LE, Plevy SE. An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis. J Immunol 2011; 186:5506 - 13; http://dx.doi.org/10.4049/jimmunol.1002433; PMID: 21444764
   PubMed Web of Science ®Google Scholar
• Onyiah JC, Sheikh SZ, Maharshak N, Steinbach EC, Russo SM, Kobayashi T, Mackey LC, Hansen JJ, Moeser AJ, Rawls JF, et al. Carbon monoxide and heme oxygenase-1 prevent intestinal inflammation in mice by promoting bacterial clearance. Gastroenterology 2013; 144:789 - 98; http://dx.doi.org/10.1053/j.gastro.2012.12.025; PMID: 23266559
   PubMed Web of Science ®Google Scholar
• Zuckerbraun BS, Otterbein LE, Boyle P, Jaffe R, Upperman J, Zamora R, Ford HR. Carbon monoxide protects against the development of experimental necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2005; 289:G607 - 13; http://dx.doi.org/10.1152/ajpgi.00055.2005; PMID: 15890710
   PubMed Web of Science ®Google Scholar
• 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 Exp Med 2005; 202:1703 - 13; http://dx.doi.org/10.1084/jem.20051047; PMID: 16365149
   PubMed Web of Science ®Google Scholar
• Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 2004; 165:1045 - 53; http://dx.doi.org/10.1016/S0002-9440(10)63365-2; PMID: 15331427
   PubMed Web of Science ®Google Scholar
• Brusko TM, Wasserfall CH, Agarwal A, Kapturczak MH, Atkinson MA. An integral role for heme oxygenase-1 and carbon monoxide in maintaining peripheral tolerance by CD4+CD25+ regulatory T cells. J Immunol 2005; 174:5181 - 6; PMID: 15843512
   PubMed Web of Science ®Google Scholar
• Megías J, Busserolles J, Alcaraz MJ. The carbon monoxide-releasing molecule CORM-2 inhibits the inflammatory response induced by cytokines in Caco-2 cells. Br J Pharmacol 2007; 150:977 - 86; http://dx.doi.org/10.1038/sj.bjp.0707184; PMID: 17339836
   PubMed Web of Science ®Google Scholar
• Takamiya R, Murakami M, Kajimura M, Goda N, Makino N, Takamiya Y, Yamaguchi T, Ishimura Y, Hozumi N, Suematsu M. Stabilization of mast cells by heme oxygenase-1: an anti-inflammatory role. Am J Physiol Heart Circ Physiol 2002; 283:H861 - 70; PMID: 12181112
   PubMedGoogle Scholar
• Brandsma CA, Hylkema MN, van der Strate BW, Slebos DJ, Luinge MA, Geerlings M, Timens W, Postma DS, Kerstjens HA. Heme oxygenase-1 prevents smoke induced B-cell infiltrates: a role for regulatory T cells?. Respir Res 2008; 9:17; http://dx.doi.org/10.1186/1465-9921-9-17; PMID: 18252008
   PubMed Web of Science ®Google Scholar
• Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap’n’Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999; 274:26071 - 8; http://dx.doi.org/10.1074/jbc.274.37.26071; PMID: 10473555
   PubMed Web of Science ®Google Scholar
• Jurjus AR, Khoury NN, Reimund JM. Animal models of inflammatory bowel disease. J Pharmacol Toxicol Methods 2004; 50:81 - 92; http://dx.doi.org/10.1016/j.vascn.2003.12.002; PMID: 15385082
   PubMedGoogle Scholar
• Mombaerts P, Mizoguchi E, Grusby MJ, Glimcher LH, Bhan AK, Tonegawa S. Spontaneous development of inflammatory bowel disease in T cell receptor mutant mice. Cell 1993; 75:274 - 82; http://dx.doi.org/10.1016/0092-8674(93)80069-Q; PMID: 8104709
   PubMed Web of Science ®Google Scholar
• Mizoguchi A, Mizoguchi E, Chiba C, Spiekermann GM, Tonegawa S, Nagler-Anderson C, Bhan AK. Cytokine imbalance and autoantibody production in T cell receptor-alpha mutant mice with inflammatory bowel disease. J Exp Med 1996; 183:847 - 56; http://dx.doi.org/10.1084/jem.183.3.847; PMID: 8642289
   PubMed Web of Science ®Google Scholar
• Harusato A, Naito Y, Takagi T, Uchiyama K, Mizushima K, Hirai Y, Higashimura Y, Katada K, Handa O, Ishikawa T, et al. BTB and CNC homolog 1 (Bach1) deficiency ameliorates TNBS colitis in mice: role of M2 macrophages and heme oxygenase-1. Inflamm Bowel Dis 2013; 19:740 - 53; http://dx.doi.org/10.1097/MIB.0b013e3182802968; PMID: 23446334
   PubMed Web of Science ®Google Scholar
• Oyake T, Itoh K, Motohashi H, Hayashi N, Hoshino H, Nishizawa M, Yamamoto M, Igarashi K. Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site. Mol Cell Biol 1996; 16:6083 - 95; PMID: 8887638
   PubMed Web of Science ®Google Scholar
• Khor TO, Huang MT, Kwon KH, Chan JY, Reddy BS, Kong AN. Nrf2-deficient mice have an increased susceptibility to dextran sulfate sodium-induced colitis. Cancer Res 2006; 66:11580 - 4; http://dx.doi.org/10.1158/0008-5472.CAN-06-3562; PMID: 17178849
   PubMed Web of Science ®Google Scholar
• Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, et al, International IBD Genetics Consortium (IIBDGC). Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012; 491:119 - 24; http://dx.doi.org/10.1038/nature11582; PMID: 23128233
   PubMed Web of Science ®Google Scholar
• Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P, Huett A, Green T, Kuballa P, Barmada MM, Datta LW, et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat Genet 2007; 39:596 - 604; http://dx.doi.org/10.1038/ng2032; PMID: 17435756
   PubMed Web of Science ®Google Scholar
• Hampe J, Franke A, Rosenstiel P, Till A, Teuber M, Huse K, Albrecht M, Mayr G, De La Vega FM, Briggs J, et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat Genet 2007; 39:207 - 11; http://dx.doi.org/10.1038/ng1954; PMID: 17200669
   PubMed Web of Science ®Google Scholar
• Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, Lees CW, Balschun T, Lee J, Roberts R, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn’s disease susceptibility loci. Nat Genet 2010; 42:1118 - 25; http://dx.doi.org/10.1038/ng.717; PMID: 21102463
   PubMed Web of Science ®Google Scholar
• McGovern DP, Gardet A, Törkvist L, Goyette P, Essers J, Taylor KD, Neale BM, Ong RT, Lagacé C, Li C, et al, NIDDK IBD Genetics Consortium. Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat Genet 2010; 42:332 - 7; http://dx.doi.org/10.1038/ng.549; PMID: 20228799
   PubMed Web of Science ®Google Scholar
• Chung SW, Liu X, Macias AA, Baron RM, Perrella MA. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J Clin Invest 2008; 118:239 - 47; http://dx.doi.org/10.1172/JCI32730; PMID: 18060048
   PubMed Web of Science ®Google Scholar
• Otterbein LE, May A, Chin BY. Carbon monoxide increases macrophage bacterial clearance through Toll-like receptor (TLR)4 expression. Cell Mol Biol (Noisy-le-grand) 2005; 51:433 - 40; PMID: 16309564
   PubMed Web of Science ®Google Scholar
• Hugot JP, Chamaillard M, Zouali H, Lesage S, Cézard JP, Belaiche J, Almer S, Tysk C, O’Morain CA, Gassull M, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 2001; 411:599 - 603; http://dx.doi.org/10.1038/35079107; PMID: 11385576
   PubMed Web of Science ®Google Scholar
• Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 2001; 411:603 - 6; http://dx.doi.org/10.1038/35079114; PMID: 11385577
   PubMed Web of Science ®Google Scholar
• Homer CR, Richmond AL, Rebert NA, Achkar JP, McDonald C. ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn’s disease pathogenesis. Gastroenterology 2010; 139:1630 - 41, e1-2; http://dx.doi.org/10.1053/j.gastro.2010.07.006; PMID: 20637199
   PubMed Web of Science ®Google Scholar
• Waltz P, Carchman EH, Young AC, Rao J, Rosengart MR, Kaczorowski D, Zuckerbraun BS. Lipopolysaccaride induces autophagic signaling in macrophages via a TLR4, heme oxygenase-1 dependent pathway. Autophagy 2011; 7:315 - 20; http://dx.doi.org/10.4161/auto.7.3.14044; PMID: 21307647
   PubMed Web of Science ®Google Scholar
• Zaki MH, Fujii S, Okamoto T, Islam S, Khan S, Ahmed KA, Sawa T, Akaike T. Cytoprotective function of heme oxygenase 1 induced by a nitrated cyclic nucleotide formed during murine salmonellosis. J Immunol 2009; 182:3746 - 56; http://dx.doi.org/10.4049/jimmunol.0803363; PMID: 19265153
   PubMed Web of Science ®Google Scholar
• Mittrücker HW, Kaufmann SH. Immune response to infection with Salmonella typhimurium in mice. J Leukoc Biol 2000; 67:457 - 63; PMID: 10770276
   PubMed Web of Science ®Google Scholar
• Sanjuan MA, Dillon CP, Tait SW, Moshiach S, Dorsey F, Connell S, Komatsu M, Tanaka K, Cleveland JL, Withoff S, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 2007; 450:1253 - 7; http://dx.doi.org/10.1038/nature06421; PMID: 18097414
   PubMed Web of Science ®Google Scholar
• Wang WW, Smith DL, Zucker SD. Bilirubin inhibits iNOS expression and NO production in response to endotoxin in rats. Hepatology 2004; 40:424 - 33; http://dx.doi.org/10.1002/hep.20334; PMID: 15368447
   PubMed Web of Science ®Google Scholar
• Maharshak N, Packey CD, Ellermann M, Manick S, Siddle JP, Huh EY, Plevy S, Sartor RB, Carroll IM. Altered enteric microbiota ecology in interleukin 10-deficient mice during development and progression of intestinal inflammation. Gut Microbes 2013; 4:316 - 24; http://dx.doi.org/10.4161/gmic.25486; PMID: 23822920
   PubMed Web of Science ®Google Scholar
• Li E, Hamm CM, Gulati AS, Sartor RB, Chen H, Wu X, Zhang T, Rohlf FJ, Zhu W, Gu C, et al. Inflammatory bowel diseases phenotype, C. difficile and NOD2 genotype are associated with shifts in human ileum associated microbial composition. PLoS One 2012; 7:e26284; http://dx.doi.org/10.1371/journal.pone.0026284; PMID: 22719818
   PubMed Web of Science ®Google Scholar
• Pang QF, Ji Y, Bermúdez-Humarán LG, Zhou QM, Hu G, Zeng Y. Protective effects of a heme oxygenase-1-secreting Lactococcus lactis on mucosal injury induced by hemorrhagic shock in rats. J Surg Res 2009; 153:39 - 45; http://dx.doi.org/10.1016/j.jss.2008.03.042; PMID: 18694575
   PubMed Web of Science ®Google Scholar
• Motterlini R, Otterbein LE. The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 2010; 9:728 - 43; http://dx.doi.org/10.1038/nrd3228; PMID: 20811383
   PubMed Web of Science ®Google Scholar
• 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 - 24; http://dx.doi.org/10.1161/hh0202.104530; PMID: 11834719
   PubMed Web of Science ®Google Scholar