1887

Abstract

Polyphenols, ubiquitously present in the food we consume, may modify the gut microbial composition and/or activity, and moreover, may be converted by the colonic microbiota to bioactive compounds that influence host health. The polyphenol content of fruit and vegetables and derived products is implicated in some of the health benefits bestowed on eating fruit and vegetables. Elucidating the mechanisms behind polyphenol metabolism is an important step in understanding their health effects. Yet, this is no trivial assignment due to the diversity encountered in both polyphenols and the gut microbial composition, which is further confounded by the interactions with the host. Only a limited number of studies have investigated the impact of dietary polyphenols on the complex human gut microbiota and these were mainly focused on single polyphenol molecules and selected bacterial populations. Our knowledge of gut microbial genes and pathways for polyphenol bioconversion and interactions is poor. Application of specific or models mimicking the human gut environment is required to analyse these diverse interactions. A particular benefit can now be gained from next-generation analytical tools such as metagenomics and metatranscriptomics allowing a wider, more holistic approach to the analysis of polyphenol metabolism. Understanding the polyphenol–gut microbiota interactions and gut microbial bioconversion capacity will facilitate studies on bioavailability of polyphenols in the host, provide more insight into the health effects of polyphenols and potentially open avenues for modulation of polyphenol bioactivity for host health.

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2010-11-01
2020-07-05
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References

  1. Arakawa H., Maeda M., Okubo S., Shimamura T.. 2004; Role of hydrogen peroxide in bactericidal action of catechin. Biol Pharm Bull27:277–281
    [Google Scholar]
  2. Beloqui A., Pita M., Polaina J., Martínez-Arias A., Golyshina O. V., Zumárraga M., Yakimov M. M., García-Arellano H., Alcalde M.. other authors 2006; Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships. J Biol Chem281:22933–22942
    [Google Scholar]
  3. Blaut M., Schoefer L., Braune A.. 2003; Transformation of flavonoids by intestinal microorganisms. Int J Vitam Nutr Res73:79–87
    [Google Scholar]
  4. Bolca S., Wyns C., Possemiers S., Depypere H., De Keukeleire D., Bracke M., Verstraete W., Heyerick A.. 2009; Cosupplementation of isoflavones, prenylflavonoids, and lignans alters human exposure to phytoestrogen-derived 17 β-estradiol equivalents. J Nutr139:2293–2300
    [Google Scholar]
  5. Bolca S., Urpi-Sarda M., Blondeel Ph., Roche N., Vanhaecke L., Possemiers S., Al-Maharik N., Botting N., Heyerick A.. other authors 2010; Disposition of soy isoflavones in normal breast tissue. Am J Clin Nutr91:976–984
    [Google Scholar]
  6. Bowey E., Adlercreutz H., Rowland I.. 2003; Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human flora associated rats. Food Chem Toxicol41:631–636
    [Google Scholar]
  7. Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., Fierer N., Pena A. G., Goodrich J. K.. other authors 2010; QIIME allows analysis of high-throughput community sequencing data. Nat Methods7:335–336
    [Google Scholar]
  8. Clavel T., Borrmann D., Braune A., Dore J., Blaut M.. 2006; Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe12:140–147
    [Google Scholar]
  9. Crozier A., Jaganath I. B., Clifford M. N.. 2009; Dietary phenolics: chemistry, bioavailability and effects on health. Nat Prod Rep26:1001–1043
    [Google Scholar]
  10. Cushnie T. P., Lamb A. J.. 2005; Antimicrobial activity of flavonoids. Int J Antimicrob Agents26:343–356
    [Google Scholar]
  11. Denef V. J., Kalnejais L. H., Mueller R. S., Wilmes P., Baker B. J., Thomas B. C., Verberkmoes N. C., Hettich R. L., Banfield J. F.. 2010; Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities. Proc Natl Acad Sci U S A107:2383–2390
    [Google Scholar]
  12. DeSantis T. Z., Brodie E. L., Moberg J. P., Zubieta I. X., Piceno Y. M., Andersen G. L.. 2007; High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb Ecol53:371–383
    [Google Scholar]
  13. Dolara P., Luceri C., De F. C., Femia A. P., Giovannelli L., Caderni G., Cecchini C., Silvi S., Orpianesi C.. other authors 2005; Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats. Mutat Res591:237–246
    [Google Scholar]
  14. Evensen N. A., Braun P. C.. 2009; The effects of tea polyphenols on Candida albicans: inhibition of biofilm formation and proteasome inactivation. Can J Microbiol55:1033–1039
    [Google Scholar]
  15. Fava F., Lovegrove J. A., Gitau R., Jackson K. G., Tuohy K. M.. 2006; The gut microbiota and lipid metabolism: implications for human health and coronary heart disease. Curr Med Chem13:3005–3021
    [Google Scholar]
  16. Feng W. Y.. 2006; Metabolism of green tea catechins: an overview. Curr Drug Metab7:755–809
    [Google Scholar]
  17. Fleschhut J., Kratzer F., Rechkemmer G., Kulling S. E.. 2006; Stability and biotransformation of various dietary anthocyanins in vitro. Eur J Nutr45:7–18
    [Google Scholar]
  18. Gross G., Jacobs D. M., Peters S., Possemiers S., van Duynhoven J. P. M., Vaughan E. E., van de Wiele T.. 2010; In vitro bioconversion of polyphenols from black tea and red wine/grape juice by human intestinal microbiota displays strong inter-individual variability. J Agric Food Chem (in press ). doi: 10.1021/jf101475m
  19. Herles C., Braune A., Blaut M.. 2004; First bacterial chalcone isomerase isolated from Eubacterium ramulus. Arch Microbiol181:428–434
    [Google Scholar]
  20. Hirayama K., Itoh K.. 2005; Human flora-associated (HFA) animals as a model for studying the role of intestinal flora in human health and disease. Curr Issues Intest Microbiol6:69–75
    [Google Scholar]
  21. Kumazawa S., Kajiya K., Naito A., Saito H., Tuzi S., Tanio M., Suzuki M., Nanjo F., Suzuki E.. other authors 2004; Direct evidence of interaction of a green tea polyphenol, epigallocatechin gallate, with lipid bilayers by solid-state Nuclear Magnetic Resonance. Biosci Biotechnol Biochem68:1743–1747
    [Google Scholar]
  22. Lampe J. W.. 2009; Interindividual differences in response to plant-based diets: implications for cancer risk. Am J Clin Nutr89:1553S–1557S
    [Google Scholar]
  23. Lhoste E. F., Ouriet V., Bruel S., Flinois J. P., Brezillon C., Magdalou J., Cheze C., Nugon-Baudon L.. 2003; The human colonic microflora influences the alterations of xenobiotic-metabolizing enzymes by catechins in male F344 rats. Food Chem Toxicol41:695–702
    [Google Scholar]
  24. Li M., Wang B., Zhang M., Rantalainen M., Wang S., Zhou H., Zhang Y., Shen J., Pang X.. other authors 2008; Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A105:2117–2122
    [Google Scholar]
  25. Macfarlane G. T., Macfarlane S., Gibson G. R.. 1998; Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb Ecol35:180–187
    [Google Scholar]
  26. Manach C., Scalbert A., Morand C., Remesy C., Jimenez L.. 2004; Polyphenols: food sources and bioavailability. Am J Clin Nutr79:727–747
    [Google Scholar]
  27. Manach C., Hubert J., Llorach R., Scalbert A.. 2009; The complex links between dietary phytochemicals and human health deciphered by metabolomics. Mol Nutr Food Res53:1303–1315
    [Google Scholar]
  28. Manichanh C., Rigottier-Gois L., Bonnaud E., Gloux K., Pelletier E., Frangeul L., Nalin R., Jarrin C., Chardon P.. other authors 2006; Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut55:205–211
    [Google Scholar]
  29. Minekus M., Smeets-Peeters M., Bernalier A., Marol-Bonnin S., Havenaar R., Marteau P., Alric M., Fonty G., Veld J. H. J. H.. 1999; A computer-controlled system to simulate conditions of the large intestine with peristaltic mixing, water absorption and absorption of fermentation products. Appl Microbiol Biotechnol53:108–114
    [Google Scholar]
  30. Molly K., Woestyne M. V., Verstraete W.. 1993; Development of a 5-step multichamber reactor as a simulation of the human intestinal microbial ecosystem. Appl Microbiol Biotechnol39:254–258
    [Google Scholar]
  31. Nadkarni M. A., Martin F. E., Jacques N. A., Hunter N.. 2002; Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology148:257–266
    [Google Scholar]
  32. Navarro-Martínez M. D., Navarro-Péran E., Cabezas-Herrera J., Ruiz-Gómez J., Garcia-Cánovas F., Rodríguez-López J. N.. 2005; Antifolate activity of epigallocatechin gallate against Stenotrophomonas maltophilia. Antimicrob Agents Chemother49:2914–2920
    [Google Scholar]
  33. Pérez-Jiménez J., Neveu V., Vos F., Scalbert A.. 2010; Systematic analysis of the content of 502 polyphenols in 452 foods and beverages: an application of the phenol-explorer database. J Agric Food Chem58:4959–4969
    [Google Scholar]
  34. Possemiers S., Rabot S., Espín J. C., Bruneau A., Philippe C., González-Sarrías A., Heyerick A., Tomás-Barberán F. A., De Kukeleire D., Verstraete W.. 2008; Eubacterium limosum activates isoxanthohumol from hops ( Humulus lupulus L.) into the potent phytoestrogen 8-prenylnaringenin in vitro and in rat intestine. J Nutr138:1310–1316
    [Google Scholar]
  35. Qin J., Li R., Raes J., Arumugam M., Burgdorf K. S., Manichanh C., Nielsen T., Pons N., Levenez F.. other authors 2010; A human gut microbial gene catalogue established by metagenomic sequencing. Nature464:59–65
    [Google Scholar]
  36. Rajilić-Stojanović M., Heilig H. G., Molenaar D., Kajander K., Surakka A., Smidt H., de Vos W. M.. 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. Environ Microbiol11:1736–1751
    [Google Scholar]
  37. Romier B., Schneider Y. J., Larondelle Y., During A.. 2009; Dietary polyphenols can modulate the intestinal inflammatory response. Nutr Rev67:363–378
    [Google Scholar]
  38. Schoefer L., Braune A., Blaut M.. 2004; Cloning and expression of a phloretin hydrolase gene from Eubacterium ramulus and characterization of the recombinant enzyme. Appl Environ Microbiol70:6131–6137
    [Google Scholar]
  39. Selma M. V., Espin J. C., Tomás-Barberán F. A.. 2009; Interaction between phenolics and gut microbiota: role in human health. J Agric Food Chem57:6485–6501
    [Google Scholar]
  40. Sirk T. W., Brown E. F., Friedman M., Sum A. K.. 2009; Molecular binding of catechins to biomembranes: relationship to biological activity. J Agric Food Chem57:6720–6728
    [Google Scholar]
  41. Smith A. H., Zoetendal E., Mackie R. I.. 2005; Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microb Ecol50:197–205
    [Google Scholar]
  42. Stapleton P. D., Shah S., Ehlert K., Hara Y., Taylor P. W.. 2007; The beta-lactam-resistance modifier (−)-epicatechin gallate alters the architecture of the cell wall of Staphylococcus aureus. Microbiology153:2093–2103
    [Google Scholar]
  43. Steiner C., Arnould S., Scalbert A., Manach C.. 2008; Isoflavones and the prevention of breast and prostate cancer: new perspectives opened by nutrigenomics. Br J Nutr99:ES78–ES108
    [Google Scholar]
  44. Turnbaugh P. J., Gordon J. I.. 2009; The core gut microbiome, energy balance and obesity. J Physiol587:4153–4158
    [Google Scholar]
  45. Tzounis X., Vulevic J., Kuhnle G. G., George T., Leonczak J., Gibson G. R., Kwik-Uribe C., Spencer J. P.. 2008; Flavanol monomer-induced changes to the human faecal microflora. Br J Nutr99:782–792
    [Google Scholar]
  46. van Dorsten F. A., Grün C. H., van Velzen E. J. J., Jacobs D. M., Draijer R., van Duynhoven J. P. M.. 2010; The metabolic fate of red wine and grape juice polyphenols in humans assessed by metabolomics. Mol Nutr Food Res54:897–908
    [Google Scholar]
  47. van Duynhoven J. P., Vaughan E. E., Jacobs M., Kemperman R. A., van Velzen E. J., Gross G., Roger L. C., Possemiers S., Smilde A. K.. other authors 2010; Microbes and health sackler colloquium: metabolic fate of polyphenols in the human superorganism. Proc Natl Acad Sci U S A (in press). doi: 10.1073/pnas.1000098107
    [Google Scholar]
  48. van Velzen E. J., Westerhuis J. A., van Duynhoven J. P., Dorsten F. A., Grun C. H., Jacobs D. M., Duchateau G. S., Vis D. J., Smilde A. K.. 2009; Phenotyping tea consumers by nutrikinetic analysis of polyphenolic end-metabolites. J Prvan oteome Res8:3317–3330
    [Google Scholar]
  49. Verberkmoes N. C., Russell A. L., Shah M., Godzik A., Rosenquist M., Halfvarson J., Lefsrud M. G., Apajalahti J., Tysk C.. other authors 2009; Shotgun metaproteomics of the human distal gut microbiota. ISME J3:179–189
    [Google Scholar]
  50. Wang W. B., Lai H. C., Hsueh P. R., Chiou R. Y., Lin S. B., Liaw S. J.. 2006; Inhibition of swarming and virulence factor expression in Proteus mirabilis by resveratrol. J Med Microbiol55:1313–1321
    [Google Scholar]
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