Deconjugation and degradation of flavonol glycosides by pig cecal microbiota characterized by fluorescence in situ hybridization (FISH)

Journal of Agricultural and Food Chemistry

Volumn 56, Issue 6, 2008, Pages 2281-2290

  Hein, Eva Maria ^a   Rose, Katrin ^a   Van't Slot, Gordon ^a   Friedrich, Alexander W ^a   Humpf, Hans Ulrich ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Degradation; FISH; Flavonoids; Gastrointestinal tract; Intestinal metabolism; Microbiota; Pig cecum

Indexed keywords

FLAVONOID; FLAVONOL DERIVATIVE; GLYCOSIDE; PHENOL DERIVATIVE; POLYPHENOLS; QUERCETIN; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; BACTERIUM; CECUM; CHEMISTRY; FLUORESCENCE IN SITU HYBRIDIZATION; METABOLISM; MICROBIOLOGY; STRUCTURE ACTIVITY RELATION; SWINE;

ANIMALS; BACTERIA; CECUM; FLAVONOIDS; FLAVONOLS; GLYCOSIDES; IN SITU HYBRIDIZATION, FLUORESCENCE; PHENOLS; QUERCETIN; STRUCTURE-ACTIVITY RELATIONSHIP; SWINE;

SUIDAE;

EID: 41849099278     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf073444o     Document Type: Article

References (47)

1. Kühnau, J. The flavonoids: a class of semi-essential food components, their role in human nutrition. World. Rev. Nutr. Diet 1976, 24, 117-191.
2. Hollman, P. C. H.; Arts, I. C. W. Flavonols, flavones and flavanols-nature, occurrence and dietary burden. J. Sci. Food Agric. 2000, 80, 1081-1093.
3. Scalbert, A.; Willamson, G. Dietary intake and bioavailability of polyphenols. J. Nutr. 2000, 130, 2073S-2085S.
4. Salunkhe, D. K.; Chavan, J. K.; Kadam, S. S. In Dietary Tannins: Consequences and Remedies; Salunkhe, D. K., Ed.; CRC Press: Boca Raton, FL, 1990; pp 469-482.
5. Aherne, S. A.; O'Brien, N. Dietary flavonols: chemistry, food content, and metabolism. Nutrition 2002, 18, 75-81.
6. Rice-Evans, C. A.; Miller, N. J.; Paganga, G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biol. Med. 1996, 20, 933-956.
7. Tsuda, T.; Shiga, K.; Kawakishi, S.; Osawa, T. Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigments isolated from Phaseolus vulgaris L. Biochem. Pharmacol. 1996, 52, 1033-1039.
8. Wang, H.; Cao, G.; Prior, R. L. Oxygen radical absorbing capacity of anthocyanins. J. Agric. Food. Chem. 1997, 45, 304-309.
9. Pool-Zobel, B. L.; Bub, A.; Schroder, N.; Rechkemmer, G. Anthocyanins are potent antioxidants in model systems but do not reduce endogenous oxidative DNA damage in human colon cells. Eur. J. Nutr. 1999, 38, 227-234.
10. Rice-Evans, C. A. Flavonoid antioxidants. Curr. Med. Chem. 2001, 8, 797-807.
11. Hollman, P. C. H. Evidence for health benefits of plant phenols: local or systemic effects. J. Sci. Food Agric. 2001, 81, 842-852.
12. Walgren, R. A.; Walle, U. K.; Walle, T. Transport of quercetin and ist glucosides across human intestinal epithelial Caco-2 cells. Biochem. Pharmacol. 1998, 55, 1721-1727.
13. Manach, C.; Morand, C.; Demigne, C.; Texier, O.; Regerat, F.; Remesy, C. Bioavailability of rutin and quercetin in rats. FEBS Lett. 1997, 409, 12-16.
14. Murota, K.; Shimizu, S.; Miyamoto, S.; Izumi, T.; Obata, A. Unique uptake and transport of isoflavone aglycones by human intestinal Caco-2 cells: comparison of isoflavonoids and flavonoids. J. Nutr. 2002, 132, 1956-1961.
15. Boyer, J.; Brown, D.; Liu, R. H. Uptake of quercetin and quercetin-3-glucoside from whole onion and apple peel extracts by Caco-2 cell monolayers. J. Agric. Food Chem. 2004, 52, 7172-7179.
16. Braune, A.; Gütschow, M.; Engst, W.; Blaut, M. Degradation of quercetin and luteolin by Eubacterium ramulus. Appl. Environ. Microbiol. 2001, 67, 5558-5567.
17. Schoefer, L.; Mahan, R.; Schwiertz, A.; Braune, A.; Blaut, M. Anaerobic degradation of flavonoids by Clostridium orbiscindens. Appl. Environ. Microbiol. 2003, 69, 5849-5854.
18. Winter, J.; Moore, L. H.; Dowell, V. R.; Bokkenheuser, V. D. C-Ring cleavage of flavonoids by human intestinal bacteria. Appl. Environ. Microbiol. 1989, 55, 1203-1208.
19. Aura, A.-M.; O'Leary, K. A.; Williamson, G.; Ojala, M.; Bailey, M.; Puupponen, R.; Nuutila, A. M.; Oksman-Caldentey, K.-M.; Poutanen, K. Quercetin derivatives are deconjugated and converted to hydroxyphenylacetic acids but not methylated by human fecal flora in vitro. J. Agric. Food Chem. 2002, 50, 1725-1730.
20. Keppler, K.; Humpf, H.-U. Metabolism of anthocyanins and their polyphenolic degradation products by the intestinal microflora. Bioorg. Med. Chem. 2005, 13, 5195-5205.
21. Seefelder, W. Fumonisine und deren Reaktionsprodukte in Lebensmitteln: Vorkommen, Bedeutung, biologische Aktivität und Metabolismus. Ph.D. thesis, Universität Würzburg, Germany, 2002.
22. Labib, S.; Erb, A.; Kraus, M.; Wickert, T.; Richling, E. The pig caecum model: a suitable tool to study the intestinal metabolism of flavonoids. Mol. Nutr. Food Res. 2004, 48, 326-332.
23. Pond, W. G., Houpt, K. A., Eds. The Biology of the Pig; Cornell University Press: Ithaca, NY, 1978.
24. Almond, G. W. Research applications using pig. Vet. Clin. North Am. 1996, 12, 707-716.
25. Miller, E. R.; Ullrey, D. E. The pig as an model for human nutrition. Annu. Rev. Nutr. 1987, 7, 361-382.
26. Finegold, S. M.; Sutter, V. L.; Mathisen, G. E. In Human Intestinal Microflora in Health and Disease: Normal Indigenous Intestinal Flora; Hentges, D. J., Ed.; Academic Press: London, U.K., 1983; pp 3-31.
27. Moore, W. E.; Holdeman, L. V. Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl. Microbiol. 1974, 27, 961-979.
28. Jensen, B. B.; Jørgensen, H. Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Appl. Environ. Microbiol. 1994, 60, 1897-1904.
29. Evans, D. F.; Pye, G.; Bramley, R.; Clark, A. G.; Dyson, T. J.; Hardcastle, J. D. Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 1988, 29, 1035-1041.
30. Marteau, P.; Pochart, P.; Doré, J.; Béra-Maillet, C.; Bernalier, A.; Corthier, G. Comparative study of bacterial groups within the human cecal and fecal microbiota. Appl. Environ. Microbiol. 2001, 67, 4939-4942.
31. Bernsmann, T. Struktur, Stabilität und antioxidative Wirkung von Polyhydroxyphenolen aus Spinat. Ph.D. thesis, Westfälische Wilhelms-Universität Münster, Germany, 2002.
32. Schwarz, B.; Hofmann, T. Sensory-guided decomposition of red currant juice (Ribes rubrum) and structure determination of key astringent compounds. J. Agric. Food. Chem. 2007, 55, 1394-1404.
33. Amann, R. I.; Binder, B. J.; Olson, R. J.; Chisholm, S. W.; Devereux, R.; Stah, D. A. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 1990, 56, 1919-1925.
34. Franks, A. H.; Harmsen, H. J. M.; Raangs, G. C.; Jansen, G. J.; Schut, F.; Welling, G. W. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 1998, 64, 3336-3345.
35. Harmsen, H. J. M.; Elfferich, P.; Schut, F.; Welling, G. W. A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microb. Ecol. Health Dis. 1999, 11, 3-12.
36. Manz, W.; Amann, R.; Ludwig, W.; Vancanneyt, M.; Schleifer, K.-H. Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophagaflavobacter-bacteroides in the natural environment. Microbiology 1996, 142, 1097-1106.
37. Langendijk, P. S.; Schut, F.; Jansen, G. J.; Raangs, G. C.; Kamphuis, G. R.; Wilkinson, M. H. F.; Welling, G. W. Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl. Environ. Microbiol. 1995, 61, 3069-3075.
38. McCartney, A. L. Application of molecular biological methods for studying probiotics and the gut flora. Br. J. Nutr. 2002, 88, 29-37.
39. Zoetendal, E. G.; Cheng, B.; Koike, S.; Mackie, R. I. Molecular microbial ecology of the gastrointestinal tract: from phylogeny to function. Curr. Issues Intestinal Microbiol. 2004, 5, 31-48.
40. Zoetendal, E. G.; Akkermanns, A. D. L.; Akkermanns-van Vliet, W. M.; de Visser, A. G. M.; de Vos, W. M. The host genotype affects the bacterial community in the human gastrointestinal tract. Microbiol. Ecol. Health Dis. 2001, 13, 129-134.
41. Harmsen, H. J. M.; Raangs, G. C.; He, T.; Degener, J. E.; Welling, G. W. Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl. Environ. Microbiol. 2002, 68, 2982-2990.
42. Giesecke, D. In Tiermodelle für die menschliche Ernährungsphysiologie: Physiologische und biochemische Artunterschiede in Verdauung und Stoffwechsel; Kirchgeßner, M., Ed.; Paul Parey: Hamburg, Germany, 1990; pp 7-25.
43. Peltonen, R.; Ling, W.-H.; Hänninen, O.; Eerola, E. An uncooked vegan diet shifts the profile of human fecal microflora: computerized analysis of direct stool sample gas-liquid chromatography profiles of bacterial cellular fatty acids. Appl. Environ. Microbiol. 1992, 58, 3660-3666.
44. Bokkenheuser, V. D.; Shackleton, C. H. L.; Winter, J. Hydrolysis of dietary flavonoid glycosides by strains of intestinal Bacteroides from humans. Biochem. J. 1987, 248, 953-956.
45. Aura, A.-M.; Martin-Lopez, P.; O'Leary, K. A.; Williamson, G.; Oksman-Caldentey, K.-M.; Poutanen, K.; Santos-Buelga, C. In vitro metabolism of anthocyanins by human gut microbiota. Eur. J. Nutr 2005, 44, 133-142.
46. Keppler, K.; Hein, E. M.; Humpf, H.-U. Metabolism of quercetin and rutin by the pig caecal microflora prepared by freeze-preservation. Mol. Nutr. Food Res. 2006, 4258, 4263.
47. Simons, A. L.; Renouf, M.; Hendrich, S.; Murphy, P. A. Human gut microbial degradation of flavonoids: structure-function relationships. J. Agric. Food Chem. 2005, 53, 4258-4263.