Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: a review

Aleksandra Duda-Chodak, Tomasz Tarko, Paweł Satora, Paweł Sroka, Aleksandra Duda-Chodak, Tomasz Tarko, Paweł Satora, Paweł Sroka

Abstract

The intestinal microbiome plays an important role in the metabolism of chemical compounds found within food. Bacterial metabolites are different from those that can be generated by human enzymes because bacterial processes occur under anaerobic conditions and are based mainly on reactions of reduction and/or hydrolysis. In most cases, bacterial metabolism reduces the activity of dietary compounds; however, sometimes a specific product of bacterial transformation exhibits enhanced properties. Studies on the metabolism of polyphenols by the intestinal microbiota are crucial for understanding the role of these compounds and their impact on our health. This review article presents possible pathways of polyphenol metabolism by intestinal bacteria and describes the diet-derived bioactive metabolites produced by gut microbiota, with a particular emphasis on polyphenols and their potential impact on human health. Because the etiology of many diseases is largely correlated with the intestinal microbiome, a balance between the host immune system and the commensal gut microbiota is crucial for maintaining health. Diet-related and age-related changes in the human intestinal microbiome and their consequences are summarized in the paper.

Figures

Fig. 1
Fig. 1
Proposed pathways of bacterial metabolism of daidzin and daidzein (based on [16, 103, 111]) (color figure online)
Fig. 2
Fig. 2
Ligands for estrogen receptors generated by the intestinal microbiota: a urolithin A; b 8-prenylnaringenin; and c enterolactone and enterodiol (based on 16, 97, 120) (color figure online)
Fig. 3
Fig. 3
Possible pathways of the transformation of quercetin and its glycosides due to metabolism by intestinal bacteria (based on [16, 138, 156, 157]) (color figure online)

References

    1. Hooper LV, Gordon JI. Commensal host-bacterial relationships in the gut. Science. 2001;292:1115–1118.
    1. O’Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006;7(7):688–693.
    1. Hattori M, Taylor TD. The human intestinal microbiome: a new frontier of human biology. DNA Res. 2009;16:1–12.
    1. Zhu B, Wang X, Li L. Human gut microbiome: the second genome of human body. Protein Cell. 2010;1(8):718–725.
    1. Sakata H, Yoshioka H, Fujita K. Development of the intestinal flora in very low birth weight infants compared to normal full-term newborns. Eur J Pediatr. 1985;144:186–190.
    1. Fanaro S, Chierici R, Guerrini P, Vigi V. Intestinal microflora in early infancy: composition and development. Acta Paediatr Suppl. 2003;441:48–55.
    1. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–521.
    1. Zoetendal EG, Akkermans AD, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998;64(10):3854–3859.
    1. Brown K, DeCoffe D, Molcan E, Gibson DL. Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients. 2012;4(8):1095–1119.
    1. Salminen S, Gibson GR, McCartney AL, Isolauri E. Influence of mode of delivery on gut microbiota composition in seven year old children. Gut. 2004;53(9):1388–1389.
    1. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107(26):11971–11975.
    1. Hakansson A, Molin G. Gut microbiota and inflammation. Nutrients. 2011;3(6):637–682.
    1. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci USA. 1998;95:6578–6583.
    1. Dicksved J (2008) Exploring the human intestinal microbiome in health and disease. Dissertation, Thesis Swedish University of Agricultural Sciences, Acta Universitatis Agriculturae Sueciae 2008:30. Uppsala. Accessed 24 Apr 2014
    1. Saarela M, Lähteenmäki L, Crittenden R, Salminen S, Mattila-Sandholm T. Gut bacteria and health foods—the European perspective. Int J Food Microbiol. 2002;78:99–117.
    1. Del Rio D, Rodriguez-Mateos A, Spencer JPE, Tognolini M, Borges G, Crozier A. Dietary (poly) phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal. 2013;18(14):1818–1892.
    1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635–1638.
    1. Andersson AF, Lindberg M, Jakobsson H, Bäckhed F, Nyrén P, Engstrand L. Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE. 2008;3(7):e2836.
    1. Lagier JC, Million M, Hugon P, Armougom F, Raoult D (2012) Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol 2:136. doi:10.3389/fcimb.2012.00136 Accessed 19 Dec 2014
    1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Doré J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, MetaHIT Consortium. Bork P, Ehrlich SD, Wang J. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65.
    1. Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R. Use of 16S rRNA gene-targeted group-specific primers for Real-Time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol. 2004;70(12):7220–7228.
    1. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007;104:13780–13785.
    1. Hayashi H, Takahashi R, Nishi T, Sakamoto M, Benno Y. Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol. 2005;54(Pt 11):1093–1101.
    1. Wang M, Ahrné S, Jeppsson B, Molin G. Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes. FEMS Microbiol Ecol. 2005;54(2):219–231.
    1. Jeffery IB, O’Toole PW. Diet-microbiota interactions and their implications for healthy living. Nutrients. 2013;5(1):234–252.
    1. Mariat D, Firmesse O, Levenez F, Guimarăes V, Sokol H, Doré J, Corthier G, Furet JP (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol 9:123. doi:10.1186/1471-2180-9-123. . Accessed 12 Apr 2014
    1. Agans A, Rigsbee L, Kenche H, Michail S, Khamis HJ, Paliy O. Distal gut microbiota of adolescent children is different from that of adults. FEMS Microbiol Ecol. 2011;77:404–412.
    1. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–1023.
    1. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2011;107(33):14691–14696.
    1. Laparra JM, Sanz Y. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res. 2010;61(3):219–225.
    1. Duda-Chodak A. The inhibitory effect of polyphenols on human gut microbiota. J Physiol Pharmacol. 2012;63(5):497–503.
    1. Collado MC, Calabuig M, Sanz Y. Differences between the fecal microbiota of coeliac infants and healthy controls. Curr Issues Intest Microbiol. 2007;8(1):9–14.
    1. Sanz Y. Effects of a gluten-free diet on gut microbiota and immune function in healthy adult humans. Gut Microbes. 2010;1(3):135–137.
    1. Gibson GR. Prebiotics as gut microflora management tools. J Clin Gastroenterol. 2008;42(Suppl 2):S75–S79.
    1. Moshfegh AJ, Friday JE, Goldman JP, Ahuja JK. Presence of inulin and oligofructose in the diets of Americans. J Nutr. 1999;129(7 Suppl):1407S–1411S.
    1. Rigon G, Vallone C, Lucantoni V, Signore F (2012) Maternal factors pre- and during delivery contribute to gut microbiota shaping in newborns. Front Cell Infect Microbiol 2:93. doi:10.3389/fcimb.2012.00093. Accessed 24 Apr 2014
    1. Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature. 2010;464(7290):908–912.
    1. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, Taylor TD, Noguchi H, Mori H, Ogura Y, Ehrlich DS, Itoh K, Takagi T, Sakaki Y, Hayashi T, Hattori M. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res. 2007;14(4):169–181.
    1. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, Knight R, Ahima RS, Bushman F, Wu GD. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137(5):1716–1724.
    1. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1(6):6ra14. doi:10.1126/scitranslmed.3000322
    1. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334(6052):105–108.
    1. Santacruz A, Marcos A, Wärnberg J, Martí A, Martin-Matillas M, Campoy C, Moreno LA, Veiga O, Redondo-Figuero C, Garagorri JM, Azcona C, Delgado M, García-Fuentes M, Collado MC, Sanz Y; EVASYON Study Group Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 2009;17(10):1906–1915.
    1. Ismail NA, Ragab SH, ElBaky AA, Shoeib ARS, Alhosary Y, Fekry D. Frequency of Firmicutes and Bacteroidetes in gut microbiota in obese and normal weight Egyptian children and adults. Arch Med Sci. 2011;7(3):501–507.
    1. Green CJ. Fibre in enteral nutrition. Clin Nutr. 2001;20(Suppl. 1):23–39.
    1. Zimmer J, Lange B, Frick JS, Sauer H, Zimmermann K, Schwiertz A, Rusch K, Klosterhalfen S, Enck P. A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur J Clin Nutr. 2012;66:53–60.
    1. Peterson J, Dwyer J, Bhagwat S, Haytowit D, Holden J, Eldridge AL, Beecher G, Aladesanmi J. Major flavonoids in dry tea. J Food Compost Anal. 2005;18:487–501.
    1. Ankolekar C, Johnson D, Pinto Mda S, Johnson K, Labbe R, Shetty K. Inhibitory potential of tea polyphenolics and influence of extraction time against Helicobacter pylori and lack of inhibition of beneficial lactic acid bacteria. J Med Food. 2011;14(11):1321–1329.
    1. Shin JS, Chung HS. Antibacterial activities of phenolic components from Camellia sinensis L. on pathogenic microorganisms. J Food Sci Nutr. 2007;12:135–140.
    1. Nakayama M, Shigemune N, Tsugukuni T, Jun H, Matsushita T, Mekada Y, Kurahachi M, Miyamoto T. Mechanism of the combined anti-bacterial effect of green tea extract and NaCl against Staphylococcus aureus and Escherichia coli O157:H7. Food Control. 2012;25(1):225–232.
    1. Kohda C, Yanagawa Y, Shimamura T. Epigallocatechin gallate inhibits intracellular survival of Listeria monocytogenes in macrophages. Biochem Biophys Res Commun. 2008;365(2):310–315.
    1. Si W, Gong J, Tsao R, Kalab M, Yang R, Yin Y. Bioassay-guided purification and identification of antimicrobial components in Chinese green tea extract. J Chromatogr A. 2006;1125(2):204–210.
    1. Bancirova M. Comparison of the antioxidant capacity and the antimicrobial activity of black and green tea. Food Res Int. 2010;43:1379–1382.
    1. Chen YL, Tsai HL, Peng CW. EGCG debilitates the persistence of EBV latency by reducing the DNA binding potency of nuclear antigen 1. Biochem Biophys Res Commun. 2012;417(3):1093–1099.
    1. Nakayama M, Suzuki K, Toda M, Okubo S, Hara Y, Shimamura T. Inhibition of the infectivity of influenza virus by tea polyphenols. Antiviral Res. 1993;21(4):289–299.
    1. Liu S, Lu H, Zhao Q, He Y, Niu J, Debnath AK, Wu S, Jiang S. Theaflavin derivatives in black tea and catechin derivatives in green tea inhibit HIV-1 entry by targeting gp41. Biochim Biophys Acta. 2005;1723(1–3):270–281.
    1. Hamza A, Zhan CG. How can (-)-epigallocatechin gallate from green tea prevent HIV-1 infection? Mechanistic insights from computational modeling and the implication for rational design of anti-HIV-1 entry inhibitors. J Phys Chem B. 2006;110(6):2910–2917.
    1. Williamson MP, McCormick TG, Nance CL, Shearer WT. Epigallocatechin gallate, the main polyphenol in green tea, binds to the T-cell receptor, CD4: potential for HIV-1 therapy. J Allergy Clin Immunol. 2006;118(6):1369–1374.
    1. Park BJ, Park JC, Taguchi H, Fukushima K, Hyon SH, Takatori K. Antifungal susceptibility of epigallocatechin 3-O-gallate (EGCg) on clinical isolates of pathogenic yeasts. Biochem Biophys Res Commun. 2006;347(2):401–405.
    1. Lee HC, Jenner AM, Low CS, Lee YK. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res Microbiol. 2006;157(9):876–984.
    1. Bae EA, Han MJ, Kim DH. In vitro anti-Helicobacter pylori activity of some flavonoids and their metabolites. Planta Med. 1999;65(5):442–443.
    1. Parkar SG, Stevenson DE, Skinner MA. The potential influence of fruit polyphenols on colonic microflora and human gut health. Int J Food Microbiol. 2008;124(3):295–298.
    1. Rodríguez Vaquero MJ, Alberto MR, Manca de Nadra MC. Antibacterial effect of phenolic compounds from different wines. Food Control. 2007;18:93–101.
    1. Tzounis X, Vulevic J, Kuhnle GG, George T, Leonczak J, Gibson GR, Kwik-Uribe C, Spencer JP. Flavanol monomer-induced changes to the human faecal microflora. Br J Nutr. 2008;99(4):782–792.
    1. Smith AH, Zoetendal E, Mackie RI. Bacterial mechanisms to overcome inhibitory effects of dietary tannins. Microb Ecol. 2005;50:197–205.
    1. Dolara P, Luceri C, De Filippo C, Femia AP, Giovannelli L, Caderni G, Cecchini C, Silvi S, Orpianesi C, Cresci A. Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats. Mutat Res. 2005;591(1–2):237–246.
    1. Sanchez-Patan F, Cueva C, Monagas M, Walton GE, Gibson GR, Quintanilla-López JE, Lebrón-Aguilar R, Martín-Álvarez PJ, Moreno-Arribas MV, Bartolomé B. In vitro fermentation of a red wine extract by human gut microbiota: changes in microbial groups and formation of phenolic metabolites. J Agric Food Chem. 2012;60:2136–2147.
    1. Queipo-Ortuño MI, Boto-Ordóñez M, Murri M, Gomez-Zumaquero JM, Clemente-Postigo M, Estruch R, Cardona Diaz F, Andrés-Lacueva C, Tinahones FJ. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am J Clin Nutr. 2012;95(6):1323–1334.
    1. Bustos I, García-Cayuela T, Hernández-Ledesma B, Peláez C, Requena T, Martínez-Cuesta MC. Effect of flavan-3-ols on the adhesion of potential probiotic lactobacilli to intestinal cells. J Agric Food Chem. 2012;60(36):9082–9088.
    1. Puupponen-Pimiä R, Nohynek L, Meier C, Kähkönen M, Heinonen M, Hopia A, Oksman-Caldentey KM. Antimicrobial properties of phenolic compounds from berries. J Appl Microbiol. 2001;90(4):494–507.
    1. Kim SH, Park M, Woo H, Tharmalingam N, Lee G, Rhee KJ, Eom YB, Han SI, Seo WD, Kim JB. Inhibitory effects of anthocyanins on secretion of Helicobacter pylori CagA and VacA toxins. Int J Med Sci. 2012;9(10):838–842.
    1. Hidalgo M, Oruna-Concha MJ, Kolida S, Walton GE, Kallithraka S, Spencer JP, de Pascual-Teresa S. Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J Agric Food Chem. 2012;60(15):3882–3890.
    1. Vivas N, Lonvaud-Funel A, Glories Y. Effect of phenolic acids and anthocyanins on growth, viability and malolactic activity of a lactic acid bacterium. Food Microbiol. 1997;14:291–300.
    1. Howell AB. Bioactive compounds in cranberries and their role in prevention of urinary tract infections. Mol Nutr Food Res. 2007;51:732–737.
    1. Foo LY, Lu Y, Howell AB, Vorsa N. The structure of cranberry proanthocyanidins which inhibit adherence of uropathogenic P-fimbriated Escherichia coli in vitro. Phytochemistry. 2000;54:173–181.
    1. Howell AB, Reed JD, Krueger CG, Winterbottom R, Cunningham DG, Leahy M. A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity. Phytochemistry. 2005;66(18):2281–2291.
    1. Candela M, Maccaferri S, Turroni S, Carnevali P, Brigidi P. Functional intestinal microbiome, new frontiers in prebiotic design. Int J Food Microbiol. 2010;140:93–101.
    1. Flint HJ. The impact of nutrition on the human microbiome. Nutr Rev. 2012;70(Suppl 1):S10–S13.
    1. Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012;3(4):289–306.
    1. Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol. 2011;17(12):1519–1528.
    1. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, Wolvers D, Watzl B, Szajewska H, Stahl B, Guarner F, Respondek F, Whelan K, Coxam V, Davicco MJ, Léotoing L, Wittrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A. Prebiotic effects: metabolic and health benefits. Br J Nutr. 2010;104(Suppl. 2):S1–S63.
    1. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125(6):1401–1412.
    1. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. 2004;17:259–275.
    1. Ito M, Deguchi Y, Matsumoto K, Kimura M, Onodera N, Yajima T. Influence of galactooligosaccharides on the human fecal microflora. J Nutr Sci Vitaminol (Tokyo) 1993;39(6):635–640.
    1. Rowland IR, Tanaka R. The effects of transgalactosylated oligosaccharides on gut flora metabolism in rats associated with a human faecal microflora. J Appl Bacteriol. 1993;74(6):667–674.
    1. Bouhnik Y, Flourié B, D’Agay-Abensour L, Pochart P, Gramet G, Duran M, Rambaud J-C. Administration of trans-galacto-oligosaccharides increases fecal bifidobacteria and modifies colonic fermentation metabolism in healthy humans. J Nutr. 1997;127:444–448.
    1. Boehm G, Lidestri M, Casetta P, Jelinek J, Negretti F, Stahl B, Marini A. Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of fecal bifidobacteria in preterm infants. Arch Dis Child Fetal Neonatal Ed. 2002;86(3):F178–F181.
    1. Ito Y, Moriwaki H, Muto Y, Kato N, Watanabe K, Ueno K. Effect of lactulose on short-chain fatty acids and lactate production and on the growth of faecal flora, with special reference to Clostridium difficile. J Med Microbiol. 1997;46(1):80–84.
    1. Gibson GR, Beatty ER, Wang X, Cummings JH. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology. 1995;108(4):975–982.
    1. Kleessen B, Sykura B, Zunft HJ, Blaut M. Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Clin Nutr. 1997;65(5):1397–1402.
    1. Langlands SJ, Hopkins MJ, Coleman N, Cummings JH. Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut. 2004;53(11):1610–1616.
    1. Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol. 2004;70(10):5810–5817.
    1. Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol. 2006;72(5):3593–3599.
    1. Kankaanpää P, Yang B, Kallio H, Isolauri E, Salminen S. Effects of polyunsaturated fatty acids in growth medium on lipid composition and on physicochemical surface properties of lactobacilli. Appl Environ Microbiol. 2004;70(1):129–136.
    1. Gorissen L, De Vuyst L, Raes K, De Smet S, Leroy F. Conjugated linoleic and linolenic acid production kinetics by bifidobacteria differ among strains. Int J Food Microbiol. 2012;155(3):234–240.
    1. Wahle KW, Heys SD, Rotondo D. Conjugated linoleic acids: are they beneficial or detrimental to health? Prog Lipid Res. 2004;43(6):553–587.
    1. Ross RP, Mills S, Hill C, Fitzgerald GF, Stanton C. Specific metabolite production by gut microbiota as a basis for probiotic function. Int Dairy J. 2010;20(4):269–276.
    1. Possemiers S, Bolca S, Verstraete W, Heyerick A. The intestinal microbiome: a separate organ inside the body with the metabolic potential to influence the bioactivity of botanicals. Fitoterapia. 2011;82:53–66.
    1. Hervert-Hernández D, Goñi I. Dietary polyphenols and human gut microbiota: a review. Food Rev Int. 2011;27(2):154–169.
    1. Young IS, Woodside JV. Antioxidants in health and disease. J Clin Pathol. 2001;54:176–186.
    1. Willcox JK, Ash SL, Catignani GL. Antioxidants and prevention of chronic disease. Crit Rev Food Sci Nutr. 2004;44:275–295.
    1. Zafra-Stone S, Yasmin T, Bagchi M, Chatterjee A, Vinson JA, Bagchi D. Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol Nutr Food Res. 2007;51(6):675–683.
    1. Wang LS, Stoner GD. Anthocyanins and their role in cancer prevention. Cancer Lett. 2008;269(2):281–290.
    1. Wang XL, Kim HJ, Kang SI, Kim SI, Hur HG. Production of phytoestrogen S-equol from daidzein in mixed culture of two anaerobic bacteria. Arch Microbiol. 2007;187(2):155–160.
    1. Yokoyama S, Niwa T, Osawa T, Suzuki T. Characterization of an O-desmethylangolensin-producing bacterium isolated from human feces. Arch Microbiol. 2010;192(1):15–22.
    1. Yokoyama S, Suzuki T. Isolation and characterization of a novel equol-producing bacterium from human feces. Biosci Biotechnol Biochem. 2008;72(10):2660–2666.
    1. Matthies A, Blaut M, Braune A. Isolation of a human intestinal bacterium capable of daidzein and genistein conversion. Appl Environ Microbiol. 2009;75(6):1740–1744.
    1. Raimondi S, Roncaglia L, De Lucia M, Amaretti A, Leonardi A, Pagnoni UM, Rossi M. Bioconversion of soy isoflavones daidzin and daidzein by Bifidobacterium strains. Appl Microbiol Biotechnol. 2009;81(5):943–950.
    1. Setchell KD, Clerici C. Equol: history, chemistry, and formation. J Nutr. 2010;140(7):1355S–1362S.
    1. Setchell KD, Clerici C. Equol: pharmacokinetics and biological actions. J Nutr. 2010;140(7):1363S–1368S.
    1. Frankenfeld CL, Atkinson C, Thomas WK, Gonzalez A, Jokela T, Wähälä K, Schwartz SM, Li SS, Lampe JW. High concordance of daidzein-metabolizing phenotypes in individuals measured 1–3 years apart. Br J Nutr. 2005;94(6):873–876.
    1. Yuan JP, Wang JH, Liu X. Metabolism of dietary soy isoflavones to equol by human intestinal microflora—implications for health. Mol Nutr Food Res. 2007;51(7):765–781.
    1. Setchell KD, Clerici C, Lephart ED, Cole SJ, Heenan C, Castellani D, Wolfe BE, Nechemias-Zimmer L, Brown NM, Lund TD, Handa RJ, Heubi JE. S-equol, a potent ligand for estrogen receptor beta, is the exclusive enantiomeric form of the soy isoflavone metabolite produced by human intestinal bacterial flora. Am J Clin Nutr. 2005;81(5):1072–1079.
    1. Hwang CS, Kwak HS, Lim HJ, Lee SH, Kang YS, Choe TB, Hur HG, Han KO. Isoflavone metabolites and their in vitro dual functions: they can act as an estrogenic agonist or antagonist depending on the estrogen concentration. J Steroid Biochem Mol Biol. 2006;101:246–253.
    1. Chang YC, Nair MG, Nitiss JL. Metabolites of daidzein and genistein and their biological activities. J Nat Prod. 1995;58:1901–1905.
    1. Lund TD, Blake C, Bu L, Hamaker AN, Lephart ED (2011) Equol an isoflavonoid: potential for improved prostate health, in vitro and in vivo evidence. Reprod Biol Endocrinol 9:4. doi:10.1186/1477-7827-9-4 Accessed 19 Dec 2014
    1. Kang NJ, Lee KW, Rogozin EA, Cho YY, Heo YS, Bode AM, Lee HJ, Dong Z. Equol, a metabolite of the soybean isoflavone daidzein, inhibits neoplastic cell transformation by targeting the MEK/ERK/p90RSK/activator protein-1 pathway. J Biol Chem. 2007;282(45):32856–32866.
    1. Zheng W, Zhang Y, Ma D, Shi Y, Liu C, Wang P. (±)Equol inhibits invasion in prostate cancer DU145 cells possibly via down-regulation of matrix metalloproteinase-9, matrix metalloproteinase-2 and urokinase-type plasminogen activator by antioxidant activity. J Clin Biochem Nutr. 2012;51(1):61–67.
    1. Kang JS, Yoon YD, Han MH, Han SB, Lee K, Park SK, Kim HM. Equol inhibits nitric oxide production and inducible nitric oxide syn-thase gene expression through down-regulating the activation of Akt. Int Immunopharmacol. 2007;7:491–499.
    1. Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, Dore J, Blaut M. Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol. 2005;71:6077–6085.
    1. Landete JM. Plant and mammalian lignans: a review of source, intake, metabolism, intestinal bacteria and health. Food Res Int. 2012;46(1):410–424.
    1. Högger P (2013) Nutrition-derived bioactive metabolites produced by gut microbiota and their potential impact on human health. Nutr Med 1(1):1 . Accessed 24 Apr 2014
    1. Wang LQ. Mammalian phytoestrogens: enterodiol and enterolactone. J Chromatogr B. 2002;777(1–2):289–309.
    1. Brunelli E, Minassi A, Appendino G, Moro L. 8-Prenylnaringenin, inhibits estrogen receptor-alpha mediated cell growth and induces apoptosis in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol. 2007;107:140–148.
    1. Nunes C, Almeida L, Laranjinha J. Synergistic inhibition of respiration in brain mitochondria by nitric oxide and dihydroxyphenylacetic acid (DOPAC). Implications for Parkinson’s disease. Neurochem Int. 2005;47(3):173–182.
    1. Nunes C, Almeida L, Laranjinha J. 3,4-Dihydroxyphenylacetic acid (DOPAC) modulates the toxicity induced by nitric oxide in PC-12 cells via mitochondrial dysfunctioning. Neurotoxicology. 2008;29(6):998–1007.
    1. Nunes C, Barbosa RM, Almeida L, Laranjinha J. Nitric oxide and DOPAC-induced cell death: from GSH depletion to mitochondrial energy crisis. Mol Cell Neurosci. 2011;48(1):94–103.
    1. Appeldoorn MM, Vincken JP, Aura AM, Hollman PCH, Gruppen H. Procyanidin dimers are metabolized by human microbiota with 2-(3,4-dihydroxyphenyl)acetic acid and 5-(3,4-Dihydroxyphenyl)-γ-valerolactone as the major metabolites. J Agric Food Chem. 2009;57(3):1084–1092.
    1. Galati G, O’Brien PJ. Potential toxicity of flavonoids and other dietary phenolics: significance for their chemopreventive and anticancer properties. Free Radic Biol Med. 2004;37(3):287–303.
    1. Bailey DG, Arnold MO, Spence D. Grapefruit juice-drug interactions. Br J Clin Pharmacol. 1998;46:101–110.
    1. Castañeda-Ovando A, Pacheco-Hernández M, Páez-Hernández ME, Rodríguez JA, Galán-Vidal CA. Chemical studies of anthocyanins: a review. Food Chem. 2009;113(4):859–871.
    1. Faria A, Fernandes I, Norberto S, Mateus N, Calhau C. Interplay between anthocyanins and gut microbiota. J Agric Food Chem. 2014;62(29):6898–6902.
    1. Keppler K, Humpf HU. Metabolism of anthocyanins and their phenolic degradation products by the intestinal microflora. Bioorg Med Chem. 2005;13(17):5195–5205.
    1. Seeram NP, Bourquin LD, Nair MG. Degradation products of cyanidin glycosides from tart cherries and their bioactivities. J Agric Food Chem. 2001;49(10):4924–4929.
    1. Vitaglione P, Donnarumma G, Napolitano A, Galvano F, Gallo A, Scalfi L, Fogliano V. Protocatechuic acid is the major human metabolite of cyanidin-glucosides. J Nutr. 2007;137(9):2043–2048.
    1. Masella R, Santangelo C, D’Archivio M, Li Volti G, Giovannini C, Galvano F. Protocatechuic acid and human disease prevention: biological activities and molecular mechanisms. Curr Med Chem. 2012;19(18):2901–2917.
    1. Wang D, Wei X, Yan X, Jin T, Ling W. Protocatechuic acid, a metabolite of anthocyanins, inhibits monocyte adhesion and reduces atherosclerosis in apolipoprotein E-deficient mice. J Agric Food Chem. 2010;58:12722–12728.
    1. Williamson G, Clifford MN. Colonic metabolites of berry polyphenols: the missing link to biological activity? Br J Nutr. 2010;104(Suppl 3):S48–S66.
    1. Bokkenheuser VD, Shacketon CHL, Winter J. Hydrolysis of dietary flavonoid glycosides by strains of intestinal bacteroides from humans. Biochem J. 1987;248:953–956.
    1. Terao J. Flavonols: Metabolism, Bioavailability, and Health Impacts. In: Fraga CG, editor. Plant phenolics and human health: biochemistry, nutrition, and pharmacology. Hoboken: Wiley Inc; 2010. pp. 185–196.
    1. Forester SC, Waterhouse AL. Gut metabolites of anthocyanins, gallic acid, 3-O-methylgallic acid, and 2,4,6-trihydroxybenzaldehyde, inhibit cell proliferation of Caco-2 cells. J Agric Food Chem. 2010;58(9):5320–5327.
    1. Verzelloni E, Pellacani C, Tagliazucchi D, Tagliaferri S, Calani L, Costa LG, Brighenti F, Borges G, Crozier A, Conte A, Del Rio D. Antiglycative and neuroprotective activity of colon-derived polyphenol catabolites. Mol Nutr Food Res. 2011;55(Suppl 1):S35–S43.
    1. Day AJ, Bao Y, Morgan MR, Williamson G. Conjugation position of quercetin glucuronides and effect on biological activity. Free Radic Biol Med. 2000;29(12):1234–1243.
    1. Kawai Y, Nishikawa T, Shiba Y, Saito S, Murota K, Shibata N, Kobayashi M, Kanayama M, Uchida K, Terao J. Macrophage as a target of quercetin glucuronides in human atherosclerotic arteries: implication in the anti-atherosclerotic mechanism of dietary flavonoids. J Biol Chem. 2008;283(14):9424–9434.
    1. Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Açil Y, Glüer CC, Schrezenmeir J. Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr. 2007;137(3 Suppl 2):838S–846S.
    1. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol. 2013;24(2):160–168.
    1. LeBlanc JG, de Giori GS, Smid EJ, Hugenholtz J, Sesma F (2007) Folate production by lactic acid bacteria and other food-grade microorganisms. In: Mendez-Vilas A (ed) Communicating current research and educational topics and trends in applied microbiology, microbiology series No. 1, vol 1, Formatex, Badajos, Spain, pp 329–339
    1. Pompei A, Cordisco L, Amaretti A, Zanoni S, Matteuzzi D, Rossi M. Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol. 2007;73(1):179–185.
    1. Rossi M, Amaretti A, Raimondi S. Folate production by probiotic bacteria. Nutrients. 2011;3(1):118–134.
    1. Hill MJ. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev. 1997;6(Suppl 1):S43–S45.
    1. Ramotar K, Conly JM, Chubb H, Louie TJ. Production of menaquinones by intestinal anaerobes. J Infect Dis. 1984;150(2):213–218.
    1. Mathers JC, Fernandez F, Hill MJ, McCarthy PT, Shearer MJ, Oxley A. Dietary modification of potential vitamin K supply from enteric bacterial menaquinones in rats. Br J Nutr. 1990;63(3):639–652.
    1. Millette M, Dupont C, Archambault D, Lacroix M. Partial characterization of bacteriocins produced by human Lactococcus lactis and Pediococccus acidilactici isolates. J Appl Microbiol. 2007;102(1):274–282.
    1. Millette M, Cornut G, Dupont C, Shareck F, Archambault D, Lacroix M. Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci. Appl Environ Microbiol. 2008;74(7):1997–2003.
    1. Björksten B, Naaber P, Sepp E, Mikelsaar M. The intestinal microflora in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy. 1999;29(3):342–346.
    1. McGarr SE, Ridlon JM, Hylemon PB. Diet, anaerobic bacterial metabolism, and colon cancer: a review of the literature. J Clin Gastroenterol. 2005;39(2):98–109.
    1. Serra A, Macia A, Romero M, Reguant J, Ortega N, Motilva M. Metabolic pathways of the colonic metabolism of flavonoids (flavonols, flavones and flavanones) and phenolic acids. Food Chem. 2012;130:383–393.
    1. Peng X, Zhang Z, Zhang N, Liu L, Li S, Wei H. In vitro catabolism of quercetin by human fecal bacteria and the antioxidant capacity of its catabolites. Food Nutr Res. 2014;58:23406.

Source: PubMed

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