Antibiotic Suppression of Intestinal Microbiota Reduces Heme-Induced Lipoperoxidation Associated with Colon Carcinogenesis in Rats

REFERENCES

• World Cancer Research Fund/American Institute for Cancer Research: Food, Nutrition, Physical Activity, and the Prevention of Cancer: a global perspective. American Institute of Cancer Research, Washington, DC, 2007.
   Google Scholar
• Bastide NM, Pierre FH, and Corpet DE: Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer Prev Res (Phila) 4, 177–184, 2011.
   PubMed Web of Science ®Google Scholar
• Pierre F, Tache S, Petit CR, Van der Meer R, and Corpet DE: Meat and cancer: haemoglobin and haemin in a low-calcium diet promote colorectal carcinogenesis at the aberrant crypt stage in rats. Carcinogenesis 24, 1683–1690, 2003.
   PubMed Web of Science ®Google Scholar
• Pierre F, Freeman A, Tache S, Van der Meer R, and Corpet DE: Beef meat and blood sausage promote the formation of azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colons. Journal of Nutrition 134, 2711–2716, 2004.
   PubMed Web of Science ®Google Scholar
• Pierre F, Santarelli R, Tache S, Gueraud F, and Corpet DE: Beef meat promotion of dimethylhydrazine-induced colorectal carcinogenesis biomarkers is suppressed by dietary calcium. Br J Nutr 99, 1000–1006, 2008.
   PubMed Web of Science ®Google Scholar
• Romeu M, Aranda N, Giralt M, Ribot B, Nogues MR, et al.: Diet, iron biomarkers and oxidative stress in a representative sample of Mediterranean population. Nutr J 12, 102, 2013.
   PubMed Web of Science ®Google Scholar
• Pierre FH, Martin OC, Santarelli RL, Tache S, Naud N, et al.: Calcium and alpha-tocopherol suppress cured-meat promotion of chemically induced colon carcinogenesis in rats and reduce associated biomarkers in human volunteers. Am J Clin Nutr 98, 1255–1262, 2013.
   PubMed Web of Science ®Google Scholar
• Marnett LJ: Oxyradicals and DNA damage. Carcinogenesis 21, 361–370, 2000.
   PubMed Web of Science ®Google Scholar
• Traverso N, Menini S, Maineri EP, Patriarca S, Odetti P, et al.: Malondialdehyde, a lipoperoxidation-derived aldehyde, can bring about secondary oxidative damage to proteins. J Gerontol A Biol Sci Med Sci 59, B890–B895, 2004.
   PubMed Web of Science ®Google Scholar
• Dalleau S, Baradat M, Gueraud F, and Huc L: Cell death and diseases related to oxidative stress: 4-hydroxynonenal (HNE) in the balance. Cell Death Differ 20, 1615–1630, 2013.
   PubMed Web of Science ®Google Scholar
• Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al.: A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65, 2010.
   PubMed Web of Science ®Google Scholar
• Azcarate-Peril MA, Sikes M, and Bruno-Barcena JM: The intestinal microbiota, gastrointestinal environment and colorectal cancer: a putative role for probiotics in prevention of colorectal cancer? Am J Physiol Gastrointest Liver Physiol 301, G401–G424, 2011.
   PubMed Web of Science ®Google Scholar
• Davis CD and Milner JA: Gastrointestinal microflora, food components and colon cancer prevention. J Nutr Biochem 20, 743–752, 2009.
   PubMed Web of Science ®Google Scholar
• Collins D, Hogan AM, and Winter DC: Microbial and viral pathogens in colorectal cancer. Lancet Oncol 12, 504–512, 2011.
   PubMed Web of Science ®Google Scholar
• Maier BR, Flynn MA, Burton GC, Tsutakawa RK, and Hentges DJ: Effects of a high-beef diet on bowel flora: a preliminary report. Am J Clin Nutr 27, 1470–1474, 1974.
   PubMed Web of Science ®Google Scholar
• Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, et al.: Enterotypes of the human gut microbiome. Nature 473, 174–180, 2011.
   PubMed Web of Science ®Google Scholar
• Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, et al.: Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108, 2011.
   PubMed Web of Science ®Google Scholar
• Ijssennagger N, Derrien M, van Doorn GM, Rijnierse A, van den Bogert B, et al.: Dietary heme alters microbiota and mucosa of mouse colon without functional changes in host-microbe cross-talk. PLoS One 7, e49868, 2012.
   PubMed Web of Science ®Google Scholar
• Ito M, Ohishi K, Yoshida Y, Yokoi W, and Sawada H: Antioxidative effects of lactic acid bacteria on the colonic mucosa of iron-overloaded mice. Journal of Agricultural and Food Chemistry 51, 4456–4460, 2003.
   PubMed Web of Science ®Google Scholar
• Ito M, Sawada H, Ohishi K, Yoshida Y, Yokoi W, et al.: Suppressive effects of bifidobacteria on lipid peroxidation in the colonic mucosa of iron-overloaded mice. J Dairy Sci 84, 1583–1589, 2001.
   PubMed Web of Science ®Google Scholar
• Lee IA, Bae EA, Hyun YJ, and Kim DH: Dextran sulfate sodium and 2,4,6-trinitrobenzene sulfonic acid induce lipid peroxidation by the proliferation of intestinal gram-negative bacteria in mice. J Inflamm (Lond) 7, 7, 2010.
   Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, and Yagi K: Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95, 351–358, 1979.
   PubMed Web of Science ®Google Scholar
• Van den Berg JW, Koole-Lesuis R, Edixhoven-Bosdijk A, and Brouwers N: Automating the quantification of heme in feces. Clin Chem 34, 2125–2126, 1988.
   PubMed Web of Science ®Google Scholar
• Julia V, McSorley SS, Malherbe L, Breittmayer JP, Girard-Pipau F, et al.: Priming by microbial antigens from the intestinal flora determines the ability of CD4+ T cells to rapidly secrete IL-4 in BALB/c mice infected with Leishmania major. J Immunol 165, 5637–5645, 2000.
   PubMed Web of Science ®Google Scholar
• Bashir ME, Louie S, Shi HN, and Nagler-Anderson C: Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J Immunol 172, 6978–6987, 2004.
   PubMed Web of Science ®Google Scholar
• Reeves AE, Theriot CM, Bergin IL, Huffnagle GB, Schloss PD, et al.: The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile Infection. Gut Microbes 2, 145–158, 2011.
   PubMed Web of Science ®Google Scholar
• Smith K, McCoy KD, and Macpherson AJ: Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 19, 59–69, 2007.
   PubMed Web of Science ®Google Scholar
• Reikvam DH, Erofeev A, Sandvik A, Grcic V, Jahnsen FL, et al.: Depletion of murine intestinal microbiota: Effects on gut mucosa and epithelial gene expression. PLoS One 6, e17996, 2011.
   PubMed Web of Science ®Google Scholar
• Radulescu S, Brookes MJ, Salgueiro P, Ridgway RA, McGhee E, et al.: Luminal iron levels govern intestinal tumorigenesis after Apc loss in vivo. Cell Rep 2, 270–282, 2012.
   Web of Science ®Google Scholar
• Lapre JA and Vandermeer R: Diet-induced increase of colonic bile acids stimulates lytic activity of fecal water and proliferation of colonic cells. Carcinogenesis 13, 41–44, 1992.
   PubMed Web of Science ®Google Scholar
• de Vogel J, van-Eck WB, Sesink AL, Jonker-Termont DS, Kleibeuker J, et al.: Dietary heme injures surface epithelium resulting in hyperproliferation, inhibition of apoptosis and crypt hyperplasia in rat colon. Carcinogenesis 29, 398–403, 2008.
   PubMed Web of Science ®Google Scholar
• Ijssennagger N, Rijnierse A, de Wit NJ, Boekschoten MV, Dekker J, et al.: Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon. Carcinogenesis 34, 1628–1635, 2013.
   PubMed Web of Science ®Google Scholar
• Pierre FH, Santarelli RL, Allam O, Tache S, Naud N, et al.: Freeze-dried ham promotes azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colon. Nutr Cancer 62, 567–573, 2010.
   PubMed Web of Science ®Google Scholar
• Corpet DE: Red meat and colon cancer: Should we become vegetarians, or can we make meat safer? Meat Sci 89, 310–316, 2011.
   PubMed Web of Science ®Google Scholar