Chemopreventive effects of in vitro digested and fermented bread in human colon cells

European Journal of Nutrition

Volumn 51, Issue 7, 2012, Pages 827-839

  Schlörmann, Wiebke ^a   Hiller, Beate ^b   Jahns, Franziska ^a   Zöger, Romy ^a   Hennemeier, Isabell ^a   Wilhelm, Anne ^a   Lindhauer, Meinolf G ^b   Glei, Michael ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

Apoptosis; Bread; Colon cancer; Dietary fibre; In vitro fermentation

Indexed keywords

ALKALINE PHOSPHATASE; CASPASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE;

APOPTOSIS; ARTICLE; BIOTRANSFORMATION; BREAD; CANCER PREVENTION; CELL DIFFERENTIATION; CELL GROWTH; COLON ADENOMA; CONTROLLED STUDY; ENZYME ACTIVITY; FERMENTATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTESTINE CELL; UPREGULATION;

ALKALINE PHOSPHATASE; APOPTOSIS; BREAD; CELL DIFFERENTIATION; CELL LINE, TUMOR; CHEMOPREVENTION; COLON; COLONIC NEOPLASMS; FERMENTATION; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HUMANS; MICROARRAY ANALYSIS; RNA, NEOPLASM; SECALE CEREALE; TRITICUM; UP-REGULATION;

SECALE CEREALE; TRITICUM AESTIVUM;

EID: 84870249943     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-011-0262-8     Document Type: Article

References (63)

1. Garcia M, Jemal A, Ward EM, Center MM, Hao Y, Siegel RL, Thun MJ (2007) Global cancer facts and figures. American Cancer Society, Atlanta
2. Glade MJ (1999) Food, nutrition, and the prevention of cancer: a global perspective. American Institute for Cancer Research/World Cancer Research Fund, American Institute for Cancer Research, 1997. Nutrition 15:523-526 (Pubitemid 29279624)
3. Corpet DE, Pierre F (2003) Point: from animal models to prevention of colon cancer. Systematic review of chemoprevention in min mice and choice of the model system. Cancer Epidemiol Biomarkers Prev 12:391-400
4. Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, Tjonneland A, Overvad K, Martinez C, Dorronsoro M, Gonzalez CA, Key TJ, Trichopoulou A, Naska A, Vineis P, Tumino R, Krogh V, Buenode- Mesquita HB, Peeters PH, Berglund G, Hallmans G, Lund E, Skeie G, Kaaks R, Riboli E (2003) Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet 361:1496-1501 (Pubitemid 36566339)
5. Slavin JL, Martini MC, Jacobs DR Jr, Marquart L (1999) Plausible mechanisms for the protectiveness of whole grains. Am J Clin Nutr 70:459S-463S (Pubitemid 29407124)
6. Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401-1412
7. Rafter JJ, Eng VW, Furrer R, Medline A, Bruce WR (1986) Effects of calcium and pH on the mucosal damage produced by deoxycholic acid in the rat colon. Gut 27:1320-1329 (Pubitemid 17175680)
8. van Munster I, Tangerman A, Nagengast FM (1994) Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig Dis Sci 39:834-842 (Pubitemid 24141790)
9. Roediger WE (1982) Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 83:424-429 (Pubitemid 12078229)
10. Kruh J (1982) Effects of sodium butyrate, a new pharmacological agent, on cells in culture. Mol Cell Biochem 42:65-82 (Pubitemid 12118742)
11. Pool-Zobel BL, Selvaraju V, Sauer J, Kautenburger T, Kiefer J, Richter KK, Soom M, Wolfl S (2005) Butyrate may enhance toxicological defence in primary, adenoma and tumor human colon cells by favourably modulating expression of glutathione S-transferases genes, an approach in nutrigenomics. Carcinogenesis 26:1064-1076 (Pubitemid 41214299)
12. Schatzkin A, Mouw T, Park Y, Subar AF, Kipnis V, Hollenbeck A, Leitzmann MF, Thompson FE (2007) Dietary fiber and wholegrain consumption in relation to colorectal cancer in the NIHAARP Diet and Health Study. Am J Clin Nutr 85:1353-1360 (Pubitemid 46740479)
13. Jacobs DR Jr, Meyer HE, Solvoll K (2001) Reduced mortality among whole grain bread eaters in men and women in the Norwegian County Study. Eur J Clin Nutr 55:137-143 (Pubitemid 32156894)
14. Dewettinck K, Van Bockstaele F, Kühne B, Van de Walle D, Courtens T, Gellynck X (2008) Nutritional value of bread: Influence of processing, food interaction and consumer perception. J Cereal Sci 48:243-257
15. Grasten SM, Juntunen KS, Poutanen KS, Gylling HK, Miettinen TA, Mykkanen HM (2000) Rye bread improves bowel function and decreases the concentrations of some compounds that are putative colon cancer risk markers in middle-aged women and men. J Nutr 130:2215-2221
16. Grasten SM, Liukkonen K-H, Chrevatidis A, El-Nezami H, Poutanen K, Mykkänen H (2003) Effects of wheat pentosan and inulin on the metabolic activity of fecal microbiota and on bowel function in healthy humans. Nutrition Res 23:1503-1514 (Pubitemid 37303888)
17. Costabile A, Klinder A, Fava F, Napolitano A, Fogliano V, Leonard C, Gibson GR, Tuohy KM (2008) Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr 99:110-120 (Pubitemid 350286144)
18. Grasten SM, Pajari A-M, Liukkonen KH, Karppinen S, Mykkä-nen HM (2002) Fibers with different solubility characteristics alter similarly the metabolic activity of intestinal microbiota in rats fed cereal brands and inulin. Nutrition Research 22:1435-1444 (Pubitemid 36042359)
19. Bach Knudsen KE, Serena A, Kjaer AK, Tetens I, Heinonen SM, Nurmi T, Adlercreutz H (2003) Rye bread in the diet of pigs enhances the formation of enterolactone and increases its levels in plasma, urine and feces. J Nutr 133:1368-1375 (Pubitemid 36548708)
20. Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, Miene C, Munjal U, Stein K, Glei M (2009) Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 682:39-53
21. BLL Bund für Lebensmittelrecht und Lebensmittelkunde (2008) Leitsätze für Brot und Kleingebäck. Behr's Verlag, Schriftenreihe des BLL Hamburg
22. Hiller B, Schlörmann W, Glei M, Lindhauer MG (2011) Comparative study of colorectal health related compounds in different types of bread: analysis of bread samples pre and post digestion in a batch fermentation model of the human intestine. Food Chem 125:1202-1212
23. Stein K, Borowicki B, Scharlau D, Glei M (2010) Fermented wheat aleurone induces enzymes involved in detoxification of carcinogens and in antioxidative defence in human colon cells. Br J Nutr 104:1101-1111
24. Richter M, Jurek D, Wrba F, Kaserer K, Wurzer G, Karner- Hanusch J, Marian B (2002) Cells obtained from colorectal microadenomas mirror early premalignant growth patterns in vitro. Eur J Cancer 38:1937-1945 (Pubitemid 35247480)
25. Klenow S, Pool-Zobel BL, Glei M (2009) Influence of inorganic and organic iron compounds on parameters of cell growth and survival in human colon cells. Toxicol In Vitro 23:400-407
26. Schaeferhenrich A, Sendt W, Scheele J, Kuechler A, Liehr T, Claussen U, Rapp A, Greulich KO, Pool-Zobel BL (2003) Putative colon cancer risk factors damage global DNA and TP53 in primary human colon cells isolated from surgical samples. Food Chem Toxicol 41:655-664 (Pubitemid 36349546)
27. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139
28. Ebert MN, Klinder A, Peters WH, Schaferhenrich A, Sendt W, Scheele J, Pool-Zobel BL (2003) Expression of glutathione S-transferases (GSTs) in human colon cells and inducibility of GSTM2 by butyrate. Carcinogenesis 24:1637-1644 (Pubitemid 37304668)
29. Beyer-Sehlmeyer G, Glei M, Hartmann E, Hughes R, Persin C, Bohm V, Rowland I, Schubert R, Jahreis G, Pool-Zobel BL (2003) Butyrate is only one of several growth inhibitors produced during gut flora-mediated fermentation of dietary fibre sources. Br J Nutr 90:1057-1070 (Pubitemid 37548038)
30. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
31. Borowicki A, Stein K, Scharlau D, Glei M (2010) Fermentation supernatants of wheat (Triticum aestivum L.) aleurone beneficially modulate cancer progression in human colon cells. J Agric Food Chem 58:2001-2007
32. Rogler G, Daig R, Aschenbrenner E, Vogl D, Schlottmann K, Falk W, Gross V, Scholmerich J, Andus T (1998) Establishment of long-term primary cultures of human small and large intestinal epithelial cells. Lab Invest 78:889-890 (Pubitemid 28347886)
33. Alberts DS, Martinez ME, Roe DJ, Guillen-Rodriguez JM, Marshall JR, van Leeuwen JB, Reid ME, Ritenbaugh C, Vargas PA, Bhattacharyya AB, Earnest DL, Sampliner RE (2000) Lack of effect of a high-fiber cereal supplement on the recurrence of colorectal adenomas. Phoenix colon cancer prevention physicians' network. N Engl J Med 342:1156-1162 (Pubitemid 30211046)
34. Schatzkin A, Lanza E, Corle D, Lance P, Iber F, Caan B, Shike M, Weissfeld J, Burt R, Cooper MR, Kikendall JW, Cahill J (2000) Lack of effect of a low-fat, high-fiber diet on the recurrence of colorectal adenomas. Polyp Prevention Trial Study Group. N Engl J Med 342:1149-1155 (Pubitemid 30211045)
35. Howe GR, Benito E, Castelleto R, Cornee J, Esteve J, Gallagher RP, Iscovich JM, Ng-ao J, Kaaks R, Kune GA (1992) Dietary intake of fiber and decreased risk of cancers of the colon and rectum: evidence from the combined analysis of 13 case-control studies. J Natl Cancer Inst 84:1887-1896 (Pubitemid 23004616)
36. Grasten SM, Juntunen KS, Mättö J, Mykkänen OT, El-Nezami H, Adlercreutz H, Poutanen K, Mykkanen HM (2007) High-fiber rye bread improves bowel function in postmenopausal women but does not cause other putatively positive changes in the metabolic activity of intestinal microbiota. Nutr Res 27:454-461 (Pubitemid 47126672)
37. Dallas PB, Gottardo NG, Firth MJ, Beesley AH, Hoffmann K, Terry PA, Freitas JR, Boag JM, Cummings AJ, Kees UR (2005) Gene expression levels assessed by oligonucleotide microarray analysis and quantitative real-time RT-PCR-how well do they correlate? BMC Genomics 6:59
38. Glei M, Hofmann T, Kuster K, Hollmann J, Lindhauer MG, Pool- Zobel BL (2006) Both wheat (Triticum aestivum) bran arabinoxylans and gut flora-mediated fermentation products protect human colon cells from genotoxic activities of 4-hydroxynonenal and hydrogen peroxide. J Agric Food Chem 54:2088-2095
39. Bordonaro M, Lazarova DL, Sartorelli AC (2008) Butyrate and Wnt signaling: a possible solution to the puzzle of dietary fiber and colon cancer risk? Cell Cycle 7:1178-1183 (Pubitemid 351749270)
40. Helsby NA, Zhu S, Pearson AE, Tingle MD, Ferguson LR (2000) Antimutagenic effects of wheat bran diet through modification of xenobiotic metabolising enzymes. Mutat Res 454:77-88
41. Ebert MN, Beyer-Sehlmeyer G, Liegibel UM, Kautenburger T, Becker TW, Pool-Zobel BL (2001) Butyrate induces glutathione S-transferase in human colon cells and protects from genetic damage by 4-hydroxy-2-nonenal. Nutr Cancer 41:156-164 (Pubitemid 34666236)
42. Schaeferhenrich A, Beyer-Sehlmeyer G, Festag G, Kuechler A, Haag N, Weise A, Liehr T, Claussen U, Marian B, Sendt W, Scheele J, Pool-Zobel BL (2003) Human adenoma cells are highly susceptible to the genotoxic action of 4-hydroxy-2-nonenal. Mutat Res 526:19-32 (Pubitemid 36507208)
43. Falletti O, Douki T (2008) Low glutathione level favors formation of DNA adducts to 4-hydroxy-2(E)-nonenal, a major lipid peroxidation product. Chem Res Toxicol 21:2097-2105
44. Knoll N, Ruhe C, Veeriah S, Sauer J, Glei M, Gallagher EP, Pool- Zobel BL (2005) Genotoxicity of 4-hydroxy-2-nonenal in human colon tumor cells is associated with cellular levels of glutathione and the modulation of glutathione S-transferase A4 expression by butyrate. Toxicol Sci 86:27-35 (Pubitemid 41511346)
45. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51-88 (Pubitemid 40261798)
46. Wattenberg LW (1996) Chemoprevention of cancer. Prev Med 25:44-45 (Pubitemid 26114807)
47. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57-70 (Pubitemid 30046295)
48. Heerdt BG, Houston MA, Augenlicht LH (1994) Potentiation by specific short-chain fatty acids of differentiation and apoptosis in human colonic carcinoma cell lines. Cancer Res 54:3288-3293
49. Orchel A, Dzierzewicz Z, Parfiniewicz B, Weglarz L, Wilczok T (2005) Butyrate-induced differentiation of colon cancer cells is PKC and JNK dependent. Dig Dis Sci 50:490-498 (Pubitemid 40543737)
50. Kautenburger T, Beyer-Sehlmeyer G, Festag G, Haag N, Kuhler S, Kuchler A, Weise A, Marian B, Peters WH, Liehr T, Claussen U, Pool-Zobel BL (2005) The gut fermentation product butyrate, a chemopreventive agent, suppresses glutathione S-transferase theta (hGSTT1) and cell growth more in human colon adenoma (LT97) than tumor (HT29) cells. J Cancer Res Clin Oncol 131:692-700 (Pubitemid 41502213)
51. Munjal U, Glei M, Pool-Zobel BL, Scharlau D (2009) Fermentation products of inulin-type fructans reduce proliferation and induce apoptosis in human colon tumour cells of different stages of carcinogenesis. Br J Nutr 102:663-671
52. Borowicki A, Stein K, Scharlau D, Scheu K, Brenner-Weiss G, Obst U, Hollmann J, Lindhauer M, Wachter N, Glei M (2010) Fermented wheat aleurone inhibits growth and induces apoptosis in human HT29 colon adenocarcinoma cells. Br J Nutr 103:360-369
53. Briviba K, Abrahamse SL, Pool-Zobel BL, Rechkemmer G (2001) Neurotensin-and EGF-induced metabolic activation of colon carcinoma cells is diminished by dietary flavonoid cyanidin but not by its glycosides. Nutr Cancer 41:172-179 (Pubitemid 34666238)
54. Miene C, Klenow S, Veeriah S, Richling E, Glei M (2009) Impact of apple polyphenols on GSTT2 gene expression, subsequent protection of DNA and modulation of proliferation using LT97 human colon adenoma cells. Mol Nutr Food Res 53:1254-1262
55. Kim YH, Park JW, Lee JY, Kwon TK (2004) Sodium butyrate sensitizes TRAIL-mediated apoptosis by induction of transcription from the DR5 gene promoter through Sp1 sites in colon cancer cells. Carcinogenesis 25:1813-1820 (Pubitemid 39405899)
56. Williams EA, Coxhead JM, Mathers JC (2003) Anti-cancer effects of butyrate: use of micro-array technology to investigate mechanisms. Proc Nutr Soc 62:107-115 (Pubitemid 36569816)
57. Gibson PR, Rosella O, Wilson AJ, Mariadason JM, Rickard K, Byron K, Barkla DH (1999) Colonic epithelial cell activation and the paradoxical effects of butyrate. Carcinogenesis 20:539-544 (Pubitemid 29151287)
58. Chen LC, Hao CY, Chiu YS, Wong P, Melnick JS, Brotman M, Moretto J, Mendes F, Smith AP, Bennington JL, Moore D, Lee NM (2004) Alteration of gene expression in normal-appearing colon mucosa of APC(min) mice and human cancer patients. Cancer Res 64:3694-3700 (Pubitemid 38657950)
59. Wong JM, Jenkins DJ (2007) Carbohydrate digestibility and metabolic effects. J Nutr 137:2539S-2546S (Pubitemid 350058732)
60. Cummings JH, Macfarlane GT (1991) The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol 70:443-459
61. Ferguson LR, Chavan RR, Harris PJ (2001) Changing concepts of dietary fiber: implications for carcinogenesis. Nutr Cancer 39:155-169 (Pubitemid 33694030)
62. Aura AM, Oikarinen S, Mutanen M, Heinonen SM, Adlercreutz HC, Virtanen H, Poutanen KS (2006) Suitability of a batch in vitro fermentation model using human faecal microbiota for prediction of conversion of flaxseed lignans to enterolactone with reference to an in vivo rat model. Eur J Nutr 45:45-51 (Pubitemid 43221283)
63. McBurney MI, Thompson LU (1987) Effect of human faecal inoculum on in vitro fermentation variables. Br J Nutr 58:233-243 (Pubitemid 18020754)