Dietary Heme Alters Microbiota and Mucosa of Mouse Colon without Functional Changes in Host-Microbe Cross-Talk

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  IJssennagger, Noortje ^a,b   Derrien, Muriel ^a,b   van Doorn, Gerdien M ^a,b   Rijnierse, Anneke ^a,b   van den Bogert, Bartholomeus ^a,b   Müller, Michael ^a,b   Dekker, Jan ^a   Kleerebezem, Michiel ^a,b,c   van der Meer, Roelof ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c NIZO FOOD RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HEME; LIPOPOLYSACCHARIDE; RNA 16S;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIUM DETECTION; BACTEROIDETES; COLON CANCER; COLON DISEASE; COLON EPITHELIUM HYPERPROLIFERATION; COLON FLORA; COLON MUCOSA; CONTROLLED STUDY; DIET; EPITHELIUM HYPERPLASIA; FECES ANALYSIS; FIRMICUTES; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HISTOPATHOLOGY; HOST SUSCEPTIBILITY; IMMUNE RESPONSE; MALE; MICROARRAY ANALYSIS; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; POLYMERASE CHAIN REACTION;

ANIMALS; BACTEROIDETES; COLON; DIET; FECES; HEME; HOST-PATHOGEN INTERACTIONS; METAGENOME; MICE; MUCOUS MEMBRANE; PHILOLOGY; RNA, RIBOSOMAL, 16S;

BACTEROIDES; BACTEROIDETES; FIRMICUTES; MUS; NEGIBACTERIA; POSIBACTERIA;

EID: 84871142014     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049868     Document Type: Article

References (57)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71-96.
2. Fund WCR (2007) Food, Nutrition, Physical Activity and the Prevention of Cancer: a Global Perspective. Washington, DC: American Institute for Cancer Research.
3. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, et al. (1994) Intake of fat, meat, and fiber in relation to risk of colon cancer in men. Cancer Res 54: 2390-2397.
4. Larsson SC, Rafter J, Holmberg L, Bergkvist L, Wolk A, (2005) Red meat consumption and risk of cancers of the proximal colon, distal colon and rectum: the Swedish Mammography Cohort. Int J Cancer 113: 829-834.
5. Lee DH, Anderson KE, Harnack LJ, Folsom AR, Jacobs DR Jr, (2004) Heme iron, zinc, alcohol consumption, and colon cancer: Iowa Women's Health Study. J Natl Cancer Inst 96: 403-407.
6. Balder HF, Vogel J, Jansen MC, Weijenberg MP, van den Brandt PA, et al. (2006) Heme and chlorophyll intake and risk of colorectal cancer in the Netherlands cohort study. Cancer Epidemiol Biomarkers Prev 15: 717-725.
7. Zhang X, Giovannucci EL, Smith-Warner SA, Wu K, Fuchs CS, et al. (2011) A prospective study of intakes of zinc and heme iron and colorectal cancer risk in men and women. Cancer Causes Control 22: 1627-1637.
8. Sesink AL, Termont DS, Kleibeuker JH, Van der Meer R, (1999) Red meat and colon cancer: the cytotoxic and hyperproliferative effects of dietary heme. Cancer Res 59: 5704-5709.
9. IJssennagger N, Rijnierse A, de Wit N, Jonker-Termont D, Dekker J, et al. (2011) Dietary haem stimulates epithelial cell turnover by downregulating feedback inhibitors of proliferation in murine colon. Gut.
10. Young G, Rose I, St John D, (1989) Haem in the gut. I. Fate of haemoproteins and the absorption of haem. J Gastroenterol Hepatol 4: 537-545.
11. McGarr SE, Ridlon JM, Hylemon PB, (2005) Diet, Anaerobic Bacterial Metabolism, and Colon Cancer: A Review of the Literature. Journal of Clinical Gastroenterology 39: 98-109.
12. Collins D, Hogan AM, Winter DC, (2011) Microbial and viral pathogens in colorectal cancer. Lancet Oncol 12: 504-512.
13. Ridlon JM, Kang D-J, Hylemon PB, (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47: 241-259.
14. O'Keefe SJ, (2008) Nutrition and colonic health: the critical role of the microbiota. Current opinion in gastroenterology 24: 51-58.
15. Lewin MH, Bailey N, Bandaletova T, Bowman R, Cross AJ, et al. (2006) Red meat enhances the colonic formation of the DNA adduct O6-carboxymethyl guanine: implications for colorectal cancer risk. Cancer research 66: 1859-1865.
16. Attene-Ramos MS, Nava GM, Muellner MG, Wagner ED, Plewa MJ, et al. (2010) DNA damage and toxicogenomic analyses of hydrogen sulfide in human intestinal epithelial FHs 74 Int cells. Environmental and Molecular Mutagenesis 51: 304-314.
17. Bernstein H, Bernstein C, Payne CM, Dvorakova K, Garewal H, (2005) Bile acids as carcinogens in human gastrointestinal cancers. Mutation Research/Reviews in Mutation Research 589: 47-65.
18. Schepens MA, Vink C, Schonewille AJ, Dijkstra G, van der Meer R, et al. (2011) Dietary heme adversely affects experimental colitis in rats, despite heat-shock protein induction. Nutrition 27: 590-597.
19. de Vogel J, Jonker-Termont DSML, van Lieshout EMM, Katan MB, van der Meer R, (2005) Green vegetables, red meat and colon cancer: chlorophyll prevents the cytotoxic and hyperproliferative effects of haem in rat colon. Carcinogenesis 26: 387-393.
20. Lapre JA, Termont DS, Groen AK, Van der Meer R, (1992) Lytic effects of mixed micelles of fatty acids and bile acids. The American journal of physiology 263: G333-337.
21. de Vogel J, van-Eck WB, Sesink AL, Jonker-Termont DS, Kleibeuker J, et al. (2008) Dietary heme injures surface epithelium resulting in hyperproliferation, inhibition of apoptosis and crypt hyperplasia in rat colon. Carcinogenesis 29: 398-403.
22. Lin K, Kools H, de Groot PJ, Gavai AK, Basnet RK, et al. (2011) MADMAX- Management and analysis database for multiple ~omics experiments. J Integr Bioinform 8: 160.
23. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
24. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
25. Dai M, Wang P, Boyd AD, Kostov G, Athey B, et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33: e175.
26. Salonen A, Nikkila J, Jalanka-Tuovinen J, Immonen O, Rajilic-Stojanovic M, et al. (2010) Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: effective recovery of bacterial and archaeal DNA using mechanical cell lysis. Journal of microbiological methods 81: 127-134.
27. Rajilic-Stojanovic M, Heilig H, Molenaar D, Kajander K, Surakka A, et al. (2009) Development and application of the human intestinal tract chip, a phylogenetic microarray: analysis of universally conserved phylotypes in the abundant microbiota of young and elderly adults. Environmental Microbiology 11: 1736-1751.
28. Carter RL, Morris R, Blashfield RK, (1989) On the Partitioning of Squared Euclidean Distance and Its Applications in Cluster-Analysis. Psychometrika 54: 9-23.
29. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, et al. (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proceedings of the National Academy of Sciences of the United States of America 100: 1990-1995.
30. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate- a Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289-300.
31. Vandenabeele P, Declercq W, Van Herreweghe F, Vanden Berghe T, (2010) The role of the kinases RIP1 and RIP3 in TNF-induced necrosis. Science signaling 3: re4.
32. Marchiando AM, Shen L, Graham WV, Edelblum KL, Duckworth CA, et al. (2011) The epithelial barrier is maintained by in vivo tight junction expansion during pathologic intestinal epithelial shedding. Gastroenterology 140: 1208-1202, 1208-1218, e1201-1202.
33. Geurts L, Lazarevic V, Derrien M, Everard A, Van Roye M, et al. (2011) Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Frontiers in microbiology 2: 149.
34. Aljalili TAR, Shah HN, (1988) Protoheme, a Dispensable Growth-Factor for Bacteroides-Fragilis Grown by Batch and Continuous Culture in a Basal Medium. Current Microbiology 17: 13-18.
35. Nobles CL, Maresso AW, (2011) The theft of host heme by Gram-positive pathogenic bacteria. Metallomics: integrated biometal science 3: 788-796.
36. Bovee-Oudenhoven IM, Wissink ML, Wouters JT, Van der Meer R, (1999) Dietary calcium phosphate stimulates intestinal lactobacilli and decreases the severity of a salmonella infection in rats. The Journal of nutrition 129: 607-612.
37. McGuckin MA, Linden SK, Sutton P, Florin TH, (2011) Mucin dynamics and enteric pathogens. Nature reviews Microbiology 9: 265-278.
38. Meijerink M, Wells JM, (2010) Probiotic modulation of dendritic cells and T cell responses in the intestine. Benef Microbes 1: 317-326.
39. Poelstra K, Bakker WW, Klok PA, Kamps JA, Hardonk MJ, et al. (1997) Dephosphorylation of endotoxin by alkaline phosphatase in vivo. The American journal of pathology 151: 1163-1169.
40. Lalles JP, (2010) Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutrition reviews 68: 323-332.
41. Harada T, Koyama I, Kasahara T, Alpers DH, Komoda T, (2003) Heat shock induces intestinal-type alkaline phosphatase in rat IEC-18 cells. American journal of physiology Gastrointestinal and liver physiology 284: G255-262.
42. Maier BR, Flynn MA, Burton GC, Tsutakawa RK, Hentges DJ, (1974) Effects of a high-beef diet on bowel flora: a preliminary report. Am J Clin Nutr 27: 1470-1474.
43. Zimmer J, Lange B, Frick JS, Sauer H, Zimmermann K, et al. (2011) A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. European journal of clinical nutrition.
44. Huycke MM, Gaskins HR, (2004) Commensal Bacteria, Redox Stress, and Colorectal Cancer: Mechanisms and Models. Exp Biol Med 229: 586-597.
45. Levitt MD, Furne J, Springfield J, Suarez F, DeMaster E, (1999) Detoxification of hydrogen sulfide and methanethiol in the cecal mucosa. The Journal of clinical investigation 104: 1107-1114.
46. Parham NJ, Gibson GR, (2000) Microbes involved in dissimilatory nitrate reduction in the human large intestine. FEMS Microbiology Ecology 31: 21-28.
47. Nitzan Y, Wexler HM, Finegold SM, (1994) Inactivation of anaerobic bacteria by various photosensitized porphyrins or by hemin. Curr Microbiol 29: 125-131.
48. Aderem A, Ulevitch RJ, (2000) Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
49. Williams SE, Brown TI, Roghanian A, Sallenave J-M, (2006) SLPI and elafin: one glove, many fingers. Clin Sci 110: 21-35.
50. Xu W, He B, Chiu A, Chadburn A, Shan M, et al. (2007) Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat Immunol 8: 294-303.
51. Nakamura A, Mori Y, Hagiwara K, Suzuki T, Sakakibara T, et al. (2003) Increased susceptibility to LPS-induced endotoxin shock in secretory leukoprotease inhibitor (SLPI)-deficient mice. The Journal of experimental medicine 197: 669-674.
52. Si-Tahar M, Merlin D, Sitaraman S, Madara JL, (2000) Constitutive and regulated secretion of secretory leukocyte proteinase inhibitor by human intestinal epithelial cells. Gastroenterology 118: 1061-1071.
53. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, et al. (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proceedings of the National Academy of Sciences of the United States of America 105: 15064-15069.
54. Vaishnava S, Hooper LV, (2007) Alkaline phosphatase: keeping the peace at the gut epithelial surface. Cell host & microbe 2: 365-367.
55. Bates JM, Akerlund J, Mittge E, Guillemin K, (2007) Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell host & microbe 2: 371-382.
56. Pierre F, Tache S, Petit CR, Van der Meer R, Corpet DE, (2003) 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.
57. Schwartz S, Ellefson M, (1985) Quantitative fecal recovery of ingested hemoglobin-heme in blood: comparisons by HemoQuant assay with ingested meat and fish. Gastroenterology 89: 19-26.