Dietary Heme Induces Gut Dysbiosis, Aggravates Colitis, and Potentiates the Development of Adenomas in Mice

Marco Constante1,2, Gabriela Fragoso2, Annie Calvé2, Macha Samba-Mondonga2, Manuela M. Santos1,2
1Département de Médecine, Université de Montréal, Montréal, QC, Canada
2Nutrition and Microbiome Laboratory, Institut du Cancer de Montréal, Centre de Recherche du Centre Hospitalier de l'Université de Montréal, Montréal, QC, Canada

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Andrews, 2003, Bacterial iron homeostasis., FEMS Microbiol. Rev., 27, 215, 10.1016/S0168-6445(03)00055-X

Anzaldi, 2010, Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens., Infect. Immun., 78, 4977, 10.1128/IAI.00613-10

Armstrong, 1975, Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices., Int. J. Cancer, 15, 617, 10.1002/ijc.2910150411

Arthur, 2012, Intestinal inflammation targets cancer-inducing activity of the microbiota., Science, 338, 120, 10.1126/science.1224820

Becker, 2014, Metal limitation and toxicity at the interface between host and pathogen., FEMS Microbiol. Rev., 38, 1235, 10.1111/1574-6976.12087

Benjamini, 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing., J. R. Statist. Soc. B, 57, 289, 10.1111/j.2517-6161.1995.tb02031.x

Canani, 2011, Potential beneficial effects of butyrate in intestinal and extraintestinal diseases., World J. Gastroenterol., 17, 1519, 10.3748/wjg.v17.i12

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data., Nat. Methods, 7, 335, 10.1038/nmeth.f.303

Carmody, 2015, Diet dominates host genotype in shaping the murine gut microbiota., Cell Host Microbe, 17, 72, 10.1016/j.chom.2014.11.010

Cescau, 2007, Heme acquisition by hemophores., Biometals, 20, 603, 10.1007/s10534-006-9050-y

Chassaing, 2014, Dextran sulfate sodium (DSS)-induced colitis in mice., Curr. Protoc. Immunol., 104, 1, 10.1002/0471142735.im1525s104

Chen, 2004, Characterization and virulence of hemolysin III from Vibrio vulnificus., Curr. Microbiol., 49, 175, 10.1007/s00284-004-4288-5

Constante, 2017, Iron supplements modulate colon microbiota composition and potentiate the protective effects of probiotics in dextran sodium sulfate-induced colitis., Inflamm. Bowel Dis., 23, 753, 10.1097/MIB.0000000000001089

De Robertis, 2011, The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies., J. Carcinog., 10, 10.4103/1477-3163.78279

De Stefani, 2012, Processed meat consumption and risk of cancer: a multisite case-control study in Uruguay., Br. J. Cancer, 107, 1584, 10.1038/bjc.2012.433

Devkota, 2012, Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice., Nature, 487, 104, 10.1038/nature11225

Diaz-Ochoa, 2014, Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis., Front. Cell Infect. Microbiol., 4, 10.3389/fcimb.2014.00002

Ekbom, 1990, Ulcerative colitis and colorectal cancer. A population-based study., N. Engl. J. Med., 323, 1228, 10.1056/NEJM199011013231802

Frank, 2007, Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases., Proc. Natl. Acad. Sci. U.S.A., 104, 13780, 10.1073/pnas.0706625104

Gill, 2002, Diet and cancer: assessing the risk., Br. J. Nutr., S73, 10.1079/BJN2002632

Gulhane, 2016, High fat diets induce colonic epithelial cell stress and inflammation that is reversed by IL-22., Sci. Rep., 6, 10.1038/srep28990

Hague, 1995, Apoptosis in colorectal tumour cells: induction by the short chain fatty acids butyrate, propionate and acetate and by the bile salt deoxycholate., Int. J. Cancer, 60, 400, 10.1002/ijc.2910600322

Han, 2015, An isotope-labeled chemical derivatization method for the quantitation of short-chain fatty acids in human feces by liquid chromatography-tandem mass spectrometry., Anal. Chim. Acta, 854, 86, 10.1016/j.aca.2014.11.015

Huang, 2009, Contribution of STAT3 and SMAD4 pathways to the regulation of hepcidin by opposing stimuli., Blood, 113, 3593, 10.1182/blood-2008-08-173641

Ijssennagger, 2015, Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon., Proc. Natl. Acad. Sci. U.S.A., 112, 10038, 10.1073/pnas.1507645112

Ijssennagger, 2012, Dietary heme alters microbiota and mucosa of mouse colon without functional changes in host-microbe cross-talk., PLOS ONE, 7, 10.1371/journal.pone.0049868

Ijssennagger, 2013, Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon., Carcinogenesis, 34, 1628, 10.1093/carcin/bgt084

Inan, 2000, The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line., Gastroenterology, 118, 724, 10.1016/S0016-5085(00)70142-9

Ishikawa, 2010, Heme induces DNA damage and hyperproliferation of colonic epithelial cells via hydrogen peroxide produced by heme oxygenase: a possible mechanism of heme-induced colon cancer., Mol. Nutr. Food Res., 54, 1182, 10.1002/mnfr.200900348

Jia, 2008, Reduced colitis-associated colon cancer in Fat-1 (n-3 fatty acid desaturase) transgenic mice., Cancer Res., 68, 3985, 10.1158/0008-5472.CAN-07-6251

Jowett, 2004, Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study., Gut, 53, 1479, 10.1136/gut.2003.024828

Kamada, 2013, Control of pathogens and pathobionts by the gut microbiota., Nat. Immunol., 14, 685, 10.1038/ni.2608

Kanehisa, 2000, KEGG: kyoto encyclopedia of genes and genomes., Nucleic Acids Res., 28, 27, 10.1093/nar/28.1.27

Kang, 2017, Microbiome and colorectal cancer: unraveling host-microbiota interactions in colitis-associated colorectal cancer development., Semin. Immunol., 10.1016/j.smim.2017.04.003

Kim, 2013, Review of the association between meat consumption and risk of colorectal cancer., Nutr. Res., 33, 983, 10.1016/j.nutres.2013.07.018

Kim, 2014, Colorectal cancer in inflammatory bowel disease: the risk, pathogenesis, prevention and diagnosis., World J. Gastroenterol., 20, 9872, 10.3748/wjg.v20.i29.9872

Kim, 2012, High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway., PLOS ONE, 7, 10.1371/journal.pone.0047713

Langille, 2013, Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences., Nat. Biotechnol., 31, 814, 10.1038/nbt.2676

Larsson, 2006, Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies., Int. J. Cancer, 119, 2657, 10.1002/ijc.22170

Layoun, 2012, Bacterial cell wall constituents induce hepcidin expression in macrophages through MyD88 signaling., Inflammation, 35, 1500, 10.1007/s10753-012-9463-4

Lozupone, 2005, UniFrac: a new phylogenetic method for comparing microbial communities., Appl. Environ. Microbiol., 71, 8228, 10.1128/AEM.71.12.8228-8235.2005

Makui, 2005, Contribution of Hfe expression in macrophages to the regulation of hepatic hepcidin levels and iron loading., Blood, 106, 2189, 10.1182/blood-2005-02-0629

Manichanh, 2012, The gut microbiota in IBD., Nat. Rev. Gastroenterol. Hepatol., 9, 599, 10.1038/nrgastro.2012.152

Manichanh, 2006, Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach., Gut, 55, 205, 10.1136/gut.2005.073817

Manor, 2017, Systematic characterization and analysis of the taxonomic drivers of functional shifts in the human microbiome., Cell Host Microbe, 21, 254, 10.1016/j.chom.2016.12.014

McMurdie, 2012, Phyloseq: a bioconductor package for handling and analysis of high-throughput phylogenetic sequence data., Pac. Symp. Biocomput., 17, 235

Morgan, 2012, Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment., Genome Biol., 13, 10.1186/gb-2012-13-9-r79

Nath, 1998, Intracellular targets in heme protein-induced renal injury., Kidney Int., 53, 100, 10.1046/j.1523-1755.1998.00731.x

Norat, 2002, Meat consumption and colorectal cancer risk: dose-response meta-analysis of epidemiological studies., Int. J. Cancer, 98, 241, 10.1002/ijc.10126

Oksanen, 2015, vegan: Community Ecology Package. R package Version 2.3-2

Park, 2012, Effects of diet-induced obesity on colitis-associated colon tumor formation in A/J mice., Int. J. Obes., 36, 273, 10.1038/ijo.2011.83

Peters, 2016, The gut microbiota in conventional and serrated precursors of colorectal cancer., Microbiome, 4, 10.1186/s40168-016-0218-6

Peterson, 2008, Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases., Cell Host Microbe, 3, 417, 10.1016/j.chom.2008.05.001

Pryde, 2002, The microbiology of butyrate formation in the human colon., FEMS Microbiol. Lett., 217, 133, 10.1111/j.1574-6968.2002.tb11467.x

2015, R: A Language and Environment for Statistical Computing

Reniere, 2007, Intracellular metalloporphyrin metabolism in Staphylococcus aureus., Biometals, 20, 333, 10.1007/s10534-006-9032-0

Saemann, 2000, Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production., FASEB J., 14, 2380, 10.1096/fj.00-0359fje

Sandhu, 2001, Systematic review of the prospective cohort studies on meat consumption and colorectal cancer risk: a meta-analytical approach., Cancer Epidemiol. Biomarkers Prev., 10, 439

Sartor, 2008, Microbial influences in inflammatory bowel diseases., Gastroenterology, 134, 577, 10.1053/j.gastro.2007.11.059

Scanlan, 2006, Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn’s disease., J. Clin. Microbiol., 44, 3980, 10.1128/JCM.00312-06

Schepens, 2011, Dietary heme adversely affects experimental colitis in rats, despite heat-shock protein induction., Nutrition, 27, 590, 10.1016/j.nut.2010.05.002

Schetter, 2009, Association of inflammation-related and microRNA gene expression with cancer-specific mortality of colon adenocarcinoma., Clin. Cancer Res., 15, 5878, 10.1158/1078-0432.CCR-09-0627

Segain, 2000, Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease., Gut, 47, 397, 10.1136/gut.47.3.397

Sinha, 2009, Meat intake and mortality: a prospective study of over half a million people., Arch. Intern. Med., 169, 562, 10.1001/archinternmed.2009.6

Terzic, 2010, Inflammation and colon cancer., Gastroenterology, 138, 2101, 10.1053/j.gastro.2010.01.058

Thorsvik, 2017, Fecal neutrophil gelatinase-associated lipocalin as a biomarker for inflammatory bowel disease., J. Gastroenterol. Hepatol., 32, 128, 10.1111/jgh.13598

Tong, 2009, Bacterial heme-transport proteins and their heme-coordination modes., Arch. Biochem. Biophys., 481, 1, 10.1016/j.abb.2008.10.013

van den Berg, 1988, Automating the quantification of heme in feces., Clin. Chem., 34, 2125, 10.1093/clinchem/34.10.2125

van der Logt, 2013, Westernized high-fat diet accelerates weight loss in dextran sulfate sodium-induced colitis in mice, which is further aggravated by supplementation of heme., J. Nutr. Biochem., 24, 1159, 10.1016/j.jnutbio.2012.09.001

Walters, 2014, Meta-analyses of human gut microbes associated with obesity and IBD., FEBS Lett., 588, 4223, 10.1016/j.febslet.2014.09.039

Wandersman, 2004, Bacterial iron sources: from siderophores to hemophores., Annu. Rev. Microbiol., 58, 611, 10.1146/annurev.micro.58.030603.123811

Weinberg, 1977, Infection and iron metabolism., Am. J. Clin. Nutr., 30, 1485, 10.1093/ajcn/30.9.1485

Weinberg, 2009, Iron availability and infection., Biochim. Biophys. Acta, 1790, 600, 10.1016/j.bbagen.2008.07.002

Wilks, 2007, Heme and virulence: how bacterial pathogens regulate, transport and utilize heme., Nat. Prod. Rep., 24, 511, 10.1039/b604193k

Winter, 2014, Dysbiosis in the inflamed intestine: chance favors the prepared microbe., Gut Microbes, 5, 71, 10.4161/gmic.27129

Zhan, 2013, Gut microbiota protects against gastrointestinal tumorigenesis caused by epithelial injury., Cancer Res., 73, 7199, 10.1158/0008-5472.can-13-0827

Zhang, 2014, PEAR: a fast and accurate Illumina Paired-End reAd mergeR., Bioinformatics, 30, 614, 10.1093/bioinformatics/btt593

Zhang, 2014, Heme oxygenase-1 ameliorates dextran sulfate sodium-induced acute murine colitis by regulating Th17/Treg cell balance., J. Biol. Chem., 289, 26847, 10.1074/jbc.M114.590554

Zhang, 2016, Sodium butyrate reduces colitogenic immunoglobulin A-coated bacteria and modifies the composition of microbiota in IL-10 deficient mice., Nutrients, 8, 10.3390/nu8120728