Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 32, 2015, Pages 10038-10043

  Ijssennagger, Noortje ^a,b,c   Belzer, Clara ^a,b   Hooiveld, Guido J ^b   Dekker, Jan ^a,b   Van Mil, Saskia W C ^c   Müller, Michael ^a,b   Kleerebezem, Michiel ^a,b,d   Van Der Meer, Roelof ^a,b   Klaenhammer, Todd R ^e  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d NIZO FOOD RESEARCH   (Netherlands)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

(Tri)sulfides; Colorectal cancer; Mucolysis; Mucus barrier; Red meat

Indexed keywords

ANTIBIOTIC AGENT; HEME; MUCIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTION FACTOR NRF2; ANTIINFECTIVE AGENT; ANTIOXIDANT; BIOLOGICAL MARKER; KI 67 ANTIGEN; SULFIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BODY WEIGHT; CELL PROLIFERATION; COLON MUCOSA; COLORECTAL CANCER; CONTROLLED STUDY; CYTOTOXICITY; DIETARY INTAKE; DISULFIDE BOND; EPITHELIUM HYPERPLASIA; IN VITRO STUDY; INTESTINE EPITHELIUM; INTESTINE FLORA; MALE; MOUSE; MUCOLYSIS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RED MEAT; ANIMAL; BACTERIAL COUNT; BIOLOGICAL MODEL; C57BL MOUSE; CELL CYCLE; CELL DEATH; COLON; DIET; DOWN REGULATION; DRUG EFFECTS; EPITHELIUM CELL; FECES; GENETICS; IMMUNOHISTOCHEMISTRY; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MICROFLORA; MUCUS; PATHOLOGY; UPREGULATION;

AKKERMANSIA; MUS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIOXIDANTS; BIOMARKERS; BODY WEIGHT; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; COLON; COLONY COUNT, MICROBIAL; DIET; DOWN-REGULATION; EPITHELIAL CELLS; FECES; HEME; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; KI-67 ANTIGEN; MALE; MICE, INBRED C57BL; MICROBIOTA; MODELS, BIOLOGICAL; MUCUS; SULFIDES; UP-REGULATION;

EID: 84938917629     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1507645112     Document Type: Article

References (38)

1. World Cancer Research Fund (2007) Food, Nutrition, Physical Activity and the Prevention of Cancer: A Global Perspective (American Institute for Cancer Research, Washington, DC).
2. Giovannucci E, et al. (1994) Intake of fat, meat, and fiber in relation to risk of colon cancer in men. Cancer Res 54(9): 2390-2397.
3. 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(5): 403-407.
4. Balder HF, et al. (2006) Heme and chlorophyll intake and risk of colorectal cancer in the Netherlands cohort study. Cancer Epidemiol Biomarkers Prevent 15(4): 717-725.
5. 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(22): 5704-5709.
6. IJssennagger N, et al. (2012) Dietary haem stimulates epithelial cell turnover by downregulating feedback inhibitors of proliferation in murine colon. Gut 61(7): 1041-1049.
7. Young GP, Rose IS, St John DJ (1989) Haem in the gut. I. Fate of haemoproteins and the absorption of haem. J Gastroenterol Hepatol 4(6): 537-545.
8. McGarr SE, Ridlon JM, Hylemon PB (2005) Diet, anaerobic bacterial metabolism, and colon cancer: A review of the literature. J Clin Gastroenterol 39(2): 98-109.
9. Zimmer J, et al. (2012) A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur J Clin Nutr 66(1): 53-60.
10. Ssennagger N, et al. (2012) Dietary heme alters microbiota and mucosa of mouse colon without functional changes in host-microbe cross-talk. PLoS One 7(12): E49868.
11. Ijssennagger N, et al. (2013) Dietary heme induces acute oxidative stress, but delayed cytotoxicity and compensatory hyperproliferation in mouse colon. Carcinogenesis 34(7): 1628-1635.
12. Sesink AL, Termont DS, Kleibeuker JH, Van der Meer R (2001) Red meat and colon cancer: Dietary haem-induced colonic cytotoxicity and epithelial hyperproliferation are inhibited by calcium. Carcinogenesis 22(10): 1653-1659.
13. Kindon H, Pothoulakis C, Thim L, Lynch-Devaney K, Podolsky DK (1995) Trefoil peptide protection of intestinal epithelial barrier function: Cooperative interaction with mucin glycoprotein. Gastroenterology 109(2): 516-523.
14. Nakamura A, et al. (2003) Increased susceptibility to LPS-induced endotoxin shock in secretory leukoprotease inhibitor (SLPI)-deficient mice. J Exp Med 197(5): 669-674.
15. Johansson ME, Larsson JM, Hansson GC (2011) The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci USA 108(Suppl 1): 4659-4665.
16. Sheffner AL (1963) The reduction in vitro in viscosity of mucoprotein solutions by a new mucolytic agent, N-acetyl-L-cysteine. Ann N Y Acad Sci 106: 298-310.
17. Ellman GL (1958) A colorimetric method for determining low concentrations of mercaptans. Arch Biochem Biophys 74(2): 443-450.
18. Jespersen AM, et al. (1994) Characterisation of a trisulphide derivative of biosynthetic human growth hormone produced in Escherichia coli. Eur J Biochem FEBS 219(1-2): 365-373.
19. Tracy O (1969) Pigment production in bacteroides. J Med Microbiol 2(3): 309-315.
20. Kinzler KW, Vogelstein B (1996) Lessons from hereditary colorectal cancer. Cell 87(2): 159-170.
21. Pierre F, Taché 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(10): 1683-1690.
22. Lichtenstein L, et al. (2010) Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages. Cell Metab 12(6): 580-592.
23. Velcich A, et al. (2002) Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 295(5560): 1726-1729.
24. García-Lafuente A, et al. (1998) Derangement of mucosal barrier function by bacteria colonizing the rat colonic mucosa. Eur J Clin Invest 28(12): 1019-1026.
25. Bel S, et al. (2014) Reprogrammed and transmissible intestinal microbiota confer diminished susceptibility to induced colitis in TMF-/- mice. Proc Natl Acad Sci USA 111(13): 4964-4969.
26. Devkota S, et al. (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487(7405): 104-108.
27. Johansson ME, et al. (2014) Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 63(2): 281-291.
28. Arumugam M, et al.; MetaHIT Consortium (2011) Enterotypes of the human gut microbiome. Nature 473(7346): 174-180.
29. Swidsinski A, et al. (2007) Comparative study of the intestinal mucus barrier in normal and inflamed colon. Gut 56(3): 343-350.
30. de Vogel J, Jonker-Termont DS, van Lieshout EM, 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(2): 387-393.
31. Lapré JA, Termont DS, Groen AK, Van der Meer R (1992) Lytic effects of mixed micelles of fatty acids and bile acids. Am J Physiol 263(3 Pt 1): G333-G337.
32. Menckeberg CL, et al. (2015) Human buccal epithelium acquires microbial hyporesponsiveness at birth, a role for secretory leukocyte protease inhibitor. Gut 64(6): 884-893.
33. Salonen A, et al. (2010) Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: Effective recovery of bacterial and archaeal DNA using mechanical cell lysis. J Microbiol Methods 81(2): 127-134.
34. Dekker R, Van der Meer R, Olieman C (1991) Sensitive pulsed amperometric detection of free and conjugated bile-acids in combination with gradient reversed-phase Hplc. Chromatographia 31(11-12): 549-553.
35. Bovee-Oudenhoven IM, Termont DS, Heidt PJ, Van der Meer R (1997) Increasing the intestinal resistance of rats to the invasive pathogen Salmonella enteritidis: Additive effects of dietary lactulose and calcium. Gut 40(4): 497-504.
36. Johnson WE, Li C, Rabinovic A (2007) Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8(1): 118-127.
37. Dai M, et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33(20): E175.
38. van Klinken BJ, et al. (1999) Gastrointestinal expression and partial cDNA cloning of murine Muc2. Am J Physiol 276(1 Pt 1): G115-G124.