The deleterious metabolic and genotoxic effects of the bacterial metabolite p-cresol on colonic epithelial cells

Free Radical Biology and Medicine

Volumn 85, Issue , 2015, Pages 219-227

  Andriamihaja, Mireille ^a   Lan, Annaïg ^a   Beaumont, Martin ^a   Audebert, Marc ^b   Wong, Ximena ^c   Yamada, Kana ^a   Yin, Yulong ^d   Tomé, Daniel ^a   Carrasco Pozo, Catalina ^c   Gotteland, Martin ^c,e   Kong, Xiangfeng ^d   Blachier, François ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^c UNIVERSITY OF CHILE   (Chile)

^d INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^e UNIVERSITY OF CHILE   (Chile)

Author keywords

Anion superoxide production; Cell proliferation; Genotoxicity; Intestinal microbiota; Large intestine; Mitochondrial oxygen consumption

Indexed keywords

ADENOSINE TRIPHOSPHATE; OLIGOMYCIN; OXYGEN; PARA CRESOL; PROTON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE; 4-CRESOL; CRESOL; MUTAGENIC AGENT;

ADHERENT CELL; ANIMAL CELL; ARTICLE; BASAL METABOLIC RATE; CELL CYCLE S PHASE; CELL DEATH; CELL GROWTH; CELL ISOLATION; CELL PROLIFERATION; CELL RESPIRATION; CELL VIABILITY; COLON MUCOSA; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; EPITHELIUM CELL; GENOTOXICITY; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; MTS ASSAY; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAT; COLON; DRUG EFFECTS; HT 29 CELL LINE; INTESTINE MUCOSA;

BACTERIA (MICROORGANISMS); RATTUS;

COLON; CRESOLS; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; MUTAGENS;

EID: 84934924203     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.04.004     Document Type: Article

References (54)

1. M. Andriamihaja, A.M. Davila, M. Eklou-Lawson, N. Petit, S. Delpal, F. Allek, A. Blais, C. Delteil, D. Tome, and F. Blachier Colon luminal content and epithelial cell morphology are markedly modified in rats fed with a high-protein diet Am. J. Physiol. Gastrointest. Liver Physiol. 299 2010 G1030 G1037
2. A Birkett, J Muir, J Phillips, G Jones, and K. O'Dea Resistant starch lowers fecal concentrations of ammonia and phenols in humans Am. J. Clin. Nutr. 63 1996 766 772
3. F Blachier, F Mariotti, JF Huneau, and D. Tome Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences Amino Acids 33 2007 547 562
4. E Bone, A Tamm, and M. Hill The production of urinary phenols by gut bacteria and their possible role in the causation of large bowel cancer Am. J. Clin. Nutr. 29 1976 1448 1454
5. F Bouillaud, and F. Blachier Mitochondria and sulfide: a very old story of poisoning, feeding, and signaling? Antioxid. Redox Signal. 15 2011 379 391
6. F Buttgereit, and MD. Brand A hierarchy of ATP-consuming processes in mammalian cells Biochem. J. 312 1995 163 167 Pt 1
7. DK. Cadenas E Mitochondrial free radical generation, oxidative stress, and aging Free Radic. Biol. Med. 29 2000 222 230
8. C Carrasco-Pozo, ML Mizgier, H Speisky, and M. Gotteland Differential protective effects of quercetin, resveratrol, rutin and epigallocatechin gallate against mitochondrial dysfunction induced by indomethacin in Caco-2 cells Chem. Biol. Interact. 195 2012 199 205
9. MC Chang, HH Chang, CP Chan, SY Yeung, HC Hsien, BR Lin, CY Yeh, WY Tseng, SK Tseng, and JH. Jeng p-Cresol affects reactive oxygen species generation, cell cycle arrest, cytotoxicity and inflammation/atherosclerosis-related modulators production in endothelial cells and mononuclear cells PLoS One 9 2014 e114446
10. M Cheng, and AD. Kligerman Evaluation of the genotoxicity of cresols using sister-chromatid exchange (SCE) Mutat. Res. 137 1984 51 55
11. Y Cheng, G Xie, T Chen, Y Qiu, X Zou, M Zheng, B Tan, B Feng, T Dong, P He, L Zhao, A Zhao, LX Xu, Y Zhang, and W. Jia Distinct urinary metabolic profile of human colorectal cancer J. Proteome Res. 11 2012 1354 1363
12. AM Davila, F Blachier, M Gotteland, M Andriamihaja, PH Benetti, Y Sanz, and D. Tome Intestinal luminal nitrogen metabolism: role of the gut microbiota and consequences for the host Pharmacol. Res. 68 2013 95 107
13. L Dou, E Bertrand, C Cerini, V Faure, J Sampol, R Vanholder, Y Berland, and P. Brunet The uremic solutes p-cresol and indoxyl sulfate inhibit endothelial proliferation and wound repair Kidney Int. 65 2004 442 451
14. C Dubuisson, S Lioret, M Touvier, A Dufour, G Calamassi-Tran, JL Volatier, and L. Lafay Trends in food and nutritional intakes of French adults from 1999 to 2007: results from the INCA surveys Br. J. Nutr. 103 2010 1035 1048
15. S Dupre-Crochet, M Erard, and O. Nubetae ROS production in phagocytes: why, when, and where? J. Leukoc. Biol. 94 2013 657 670
16. TR BM Figueira, AA Camargo, RF Castilho, JC Ferreira, AJ Kowaltowski, FE Sluse, NC Souza-Pinto, and AE. Vercesi Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health Antioxid. Redox Signal. 16 2013 2029 2074
17. NW Gaikwad, and WJ. Bodell Formation of DNA adducts in HL-60 cells treated with the toluene metabolite p-cresol: a potential biomarker for toluene exposure Chem. Biol. Interact. 145 2003 149 158
18. B Geypens, D Claus, P Evenepoel, M Hiele, B Maes, M Peeters, P Rutgeerts, and Y. Ghoos Influence of dietary protein supplements on the formation of bacterial metabolites in the colon Gut 41 1997 70 76
19. A Gostner, M Blaut, V Schaffer, G Kozianowski, S Theis, M Klingeberg, Y Dombrowski, D Martin, S Ehrhardt, D Taras, A Schwiertz, B Kleessen, H Luhrs, J Schauber, D Dorbath, T Menzel, and W. Scheppach Effect of isomalt consumption on faecal microflora and colonic metabolism in healthy volunteers Br. J. Nutr. 95 2006 40 50
20. HM Hamer, V De Preter, K Windey, and K. Verbeke Functional analysis of colonic bacterial metabolism: relevant to health? Am. J. Physiol. Gastrointest. Liver Physiol. 302 2012 G1 G9
21. R Hughes, EA Magee, and S. Bingham Protein degradation in the large intestine: relevance to colorectal cancer Curr. Issues Intest. Microbiol 1 2000 51 58
22. M NK Kamizato, K Masuda, K Takeo, Y Yamamoto, T Kawai, S Teshima-Kondo, T Tanahashi, and K. Rokutan Interleukin 10 inhibits interferon gamma-and tumor necrosis alpha-stimulated activation of NADPH oxidase 1 in human colonic epithelial cells and the mouse colon J. Gastroenterol. 12 2009 1172 1184
23. M. Ketteler Kidney failure and the gut: p-cresol and the dangers from within Kidney Int. 69 2006 952 953
24. L Khoury, D Zalko, and M. Audebert Validation of high-throughput genotoxicity assay screening using gammaH2AX in-cell western assay on HepG2 cells Environ. Mol. Mutagen. 54 2013 737 746
25. A. Kitagawa Effects of cresols (o-, m-, and p-isomers) on the bioenergetic system in isolated rat liver mitochondria Drug Chem. Toxicol. 24 2001 39 47
26. A Lan, D Lagadic-Gossmann, C Lemaire, C Brenner, and G. Jan Acidic extracellular pH shifts colorectal cancer cell death from apoptosis to necrosis upon exposure to propionate and acetate, major end-products of the human probiotic propionibacteria Apoptosis 12 2007 573 591
27. JM Lecerf, F Depeint, E Clerc, Y Dugenet, CN Niamba, L Rhazi, A Cayzeele, G Abdelnour, A Jaruga, H Younes, H Jacobs, G Lambrey, AM Abdelnour, and PR. Pouillart Xylo-oligosaccharide (XOS) in combination with inulin modulates both the intestinal environment and immune status in healthy subjects, while XOS alone only shows prebiotic properties Br. J. Nutr. 108 2012 1847 1858
28. X Leschelle, S Delpal, M Goubern, HM Blottiere, and F. Blachier Butyrate metabolism upstream and downstream acetyl-CoA synthesis and growth control of human colon carcinoma cells Eur. J. Biochem. 267 2000 6435 6442
29. X Leschelle, M Goubern, M Andriamihaja, HM Blottiere, E Couplan, MD Gonzalez-Barroso, C Petit, A Pagniez, C Chaumontet, B Mignotte, F Bouillaud, and F. Blachier Adaptative metabolic response of human colonic epithelial cells to the adverse effects of the luminal compound sulfide Biochim. Biophys. Acta 1725 2005 201 212
30. P Louis, GL Hold, and HJ. Flint The gut microbiota, bacterial metabolites and colorectal cancer Nat. Rev. Microbiol. 12 2014 661 672
31. GT Macfarlane, and S. Macfarlane Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria Scand. J. Gastroenterol. Suppl. 222 1997 3 9
32. LB BJ Meira, SL Green, CW Lee, B Pang, D Borenshtein, BH Rickman, AB Rogers, CA Moroski-Erkul, JL MacFaline, DB Schauer, PC Dedon, JG Fox, and LD. Samson DNA damage induced by chronic inflammation contributes to colon carcinogenesis J. Clin. Invest. 7 2008 2516 2525
33. S Mimoun, M Andriamihaja, C Chaumontet, C Atanasiu, R Benamouzig, JM Blouin, D Tome, F Bouillaud, and F. Blachier Detoxification of H(2)S by differentiated colonic epithelial cells: implication of the sulfide oxidizing unit and of the cell respiratory capacity Antioxid. Redox Signal. 17 2012 1 10
34. S Miwa, and MD. Brand Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling Biochem. Soc. Trans. 31 2003 1300 1301
35. B Mouille, V Robert, and F. Blachier Adaptative increase of ornithine production and decrease of ammonia metabolism in rat colonocytes after hyperproteic diet ingestion Am. J. Physiol. Gastrointest. Liver Physiol. 287 2004 G344 G351
36. HA Mutsaers, MJ Wilmer, D Reijnders, J Jansen, PH van den Broek, M Forkink, E Schepers, G Glorieux, R Vanholder, LP van den Heuvel, JG Hoenderop, and R. Masereeuw Uremic toxins inhibit renal metabolic capacity through interference with glucuronidation and mitochondrial respiration Biochim. Biophys. Acta 1832 2013 142 150
37. F Radtke, and H. Clevers Self-renewal and cancer of the gut: two sides of a coin Science 307 2005 1904 1909
38. S Raha, and BH. Robinson Mitochondria, oxygen free radicals, disease and ageing Trends Biochem. Sci. 25 2000 502 508
39. A Ramezani, and DS. Raj The gut microbiome, kidney disease, and targeted interventions J. Am. Soc. Nephrol. 25 2014 657 670
40. WM Rand, PL Pellett, and VR. Young Meta-analysis of nitrogen balance studies for estimating protein requirements in healthy adults Am. J. Clin. Nutr. 77 2003 109 127
41. EG. Schmidt Urinary phenols; the simultaneous determination of phenol and p-cresol in urine J. Biol. Chem. 179 1949 211 215
42. T Shiba, K Kawakami, T Sasaki, I Makino, I Kato, T Kobayashi, K Uchida, and K. Kaneko Effects of intestinal bacteria-derived p-cresyl sulfate on Th1-type immune response in vivo and in vitro Toxicol. Appl. Pharmacol. 274 2014 191 199
43. VP. Skulachev Uncoupling: new approaches to an old problem of bioenergetics Biochim. Biophys. Acta 1363 1998 100 124
44. E Smit, FJ Nieto, CJ Crespo, and P. Mitchell Estimates of animal and plant protein intake in US adults: results from the Third National Health and Nutrition Examination Survey, 1988-1991 J. Am. Diet. Assoc. 99 1999 813 820
45. EA Smith, and GT. Macfarlane Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism J. Appl. Bacteriol. 81 1996 288 302
46. EA Smith, and GT. Macfarlane Formation of phenolic and indolic compounds by anaerobic bacteria in the human large intestine Microb. Ecol. 33 1997 180 188
47. AA Starkov, and G. Fiskum Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state J. Neurochem. 86 2003 1101 1107
48. J Terzic, S Grivennikov, E Karin, and M. Karin Inflammation and colon cancer Gastroenterology 138 2010 2101 2114
49. S Toden, AR Bird, DL Topping, and MA. Conlon Resistant starch attenuates colonic DNA damage induced by higher dietary protein in rats Nutr. Cancer 51 2005 45 51
50. JF. Turrens Superoxide production by the mitochondrial respiratory chain Biosci. Rep. 17 1997 3 8
51. P Venditti, L Di Stefano, and S. Di Meo Mitochondrial metabolism of reactive oxygen species Mitochondrion 13 2013 71 82
52. H Vidal, B Comte, M Beylot, and JP. Riou Inhibition of glucose oxidation by vasoactive intestinal peptide in isolated rat enterocytes J. Biol. Chem. 263 1988 9206 9211
53. AM Westbrook, B Wei, J Braun, and RH. Schiestl Intestinal mucosal inflammation leads to systemic genotoxicity in mice Cancer Res. 69 2009 4827 4834
54. J Winter, L Nyskohus, GP Young, Y Hu, MA Conlon, AR Bird, DL Topping, and RK. Le Leu Inhibition by resistant starch of red meat-induced promutagenic adducts in mouse colon Cancer Prev. Res. (Phila.) 4 2011 1920 1928