In vitro microbiotic fermentation causes an extensive metabolite turnover of rye bran phytochemicals

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Hanhineva, Kati ^a   Aura, Anna Marja ^b   Rogachev, Ilana ^c   Matero, Sanni ^d   Skov, Thomas ^d   Aharoni, Asaph ^c   Poutanen, Kaisa ^a,b   Mykkänen, Hannu ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHEMICAL COMPOSITION; CHEMICAL STRUCTURE; ENZYME MECHANISM; HYDROLYSIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLOMICS; MICROBIAL METABOLISM; MICROFLORA; NONHUMAN; PH; PHYTOCHEMISTRY; RYE;

DIETARY FIBER; FERMENTATION; PRINCIPAL COMPONENT ANALYSIS; SECALE CEREALE;

EID: 84862676386     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039322     Document Type: Article

References (45)

1. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, et al. (2008) Evolution of mammals and their gut microbes. Science 320(5883): 1647-1651.
2. Li P, Hotamisligil GS, (2010) Metabolism: Host and microbes in a pickle. Nature 464(7293): 1287-1288.
3. Nicholson JK, Holmes E, Wilson ID, (2005) Gut microorganisms, mammalian metabolism and personalized health care. Nat Rev Microbiol 3(5): 431-438.
4. Sekirov I, Russell SL, Antunes LC, Finlay BB, (2010) Gut microbiota in health and disease. Physiol Rev 90(3): 859-904.
5. Licht TR, Hansen M, Poulsen M, Dragsted LO, (2006) Dietary carbohydrate source influences molecular fingerprints of the rat faecal microbiota. BMC Microbiol 6: 98.
6. DiBaise JK, Zhang H, Crowell MD, Krajmalnik-Brown R, Decker GA, et al. (2008) Gut microbiota and its possible relationship with obesity. Mayo Clin Proc 83(4): 460-469.
7. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457(7228): 480-484.
8. Davis CD, Milner JA, (2009) Gastrointestinal microflora, food components and colon cancer prevention. J Nutr Biochem 20(10): 743-752.
9. Jansson J, Willing B, Lucio M, Fekete A, Dicksved J, et al. (2009) Metabolomics reveals metabolic biomarkers of crohn's disease. PLoS One 4(7): e6386.
10. Arora T, Sharma R, (2011) Fermentation potential of the gut microbiome: Implications for energy homeostasis and weight management. Nutr Rev 69(2): 99-106.
11. Aura A, (2008) Microbial metabolism of dietary phenolic compounds in the colon. Phytochemistry Reviews 7(3): 407-429.
12. Selma MV, Espin JC, Tomas-Barberan FA, (2009) Interaction between phenolics and gut microbiota: Role in human health. J Agric Food Chem 57(15): 6485-6501.
13. Rechner AR, Smith MA, Kuhnle G, Gibson GR, Debnam ES, et al. (2004) Colonic metabolism of dietary polyphenols: Influence of structure on microbial fermentation products. Free Radic Biol Med 36(2): 212-225.
14. Andreasen MF, Kroon PA, Williamson G, Garcia-Conesa MT, (2001) Intestinal release and uptake of phenolic antioxidant diferulic acids. Free Radic Biol Med 31(3): 304-314.
15. Braune A, Bunzel M, Yonekura R, Blaut M, (2009) Conversion of dehydrodiferulic acids by human intestinal microbiota. J Agric Food Chem 57(8): 3356-3362.
16. Aura AM, O'Leary KA, Williamson G, Ojala M, Bailey M, et al. (2002) Quercetin derivatives are deconjugated and converted to hydroxyphenylacetic acids but not methylated by human fecal flora in vitro. J Agric Food Chem 50(6): 1725-1730.
17. Jaganath IB, Mullen W, Lean ME, Edwards CA, Crozier A, (2009) In vitro catabolism of rutin by human fecal bacteria and the antioxidant capacity of its catabolites. Free Radic Biol Med 47(8): 1180-1189.
18. Deprez S, Brezillon C, Rabot S, Philippe C, Mila I, et al. (2000) Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J Nutr 130(11): 2733-2738.
19. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, et al. (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 106(10): 3698-3703.
20. Martin FP, Sprenger N, Yap IK, Wang Y, Bibiloni R, et al. (2009) Panorganismal gut microbiome-host metabolic crosstalk. J Proteome Res 8(4): 2090-2105.
21. Dumas ME, Barton RH, Toye A, Cloarec O, Blancher C, et al. (2006) Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc Natl Acad Sci U S A 103(33): 12511-12516.
22. Jacobs DM, Deltimple N, van Velzen E, van Dorsten FA, Bingham M, et al. (2008) (1)H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome. NMR Biomed 21(6): 615-626.
23. Aura A-, Myllymäki O, Bailey M, Penalvo J-, Adlercreutz H, et al. (2007) Interrelationships between carbohydrate type, phenolic acids and initial pH on in vitro conversion of enterolactone from rye lignans. In: Salovaara H, Gates F, Tenkanen M, editors. pp. 235-245 editors. Dietary Fibre Components and Functions. The Netherlands: Wageningen Academic Publishers.
24. Wold S, Esbensen K, Geladi P, (1987) Principal component analysis. Chemometrics Intellig Lab Syst 2(1-3): 37-52.
25. Barker M, Rayens W, (2003) Partial least squares for discrimination. J Chemometrics 17(3): 166-173.
26. Mateo Anson N, Aura AM, Selinheimo E, Mattila I, Poutanen K, et al. (2011) Bioprocessing of wheat bran in whole wheat bread increases the bioavailability of phenolic acids in men and exerts antiinflammatory effects ex vivo. J Nutr 141(1): 137-143.
27. Hanhineva K, Rogachev I, Aura A, Aharoni A, Poutanen K,et al. Identification of novel lignans in the whole grain rye bran by non-targeted LC-MS metabolite profiling. Metabolomics pp. 1-11.
28. Pan JY, Chen SL, Yang MH, Wu J, Sinkkonen J, et al. (2009) An update on lignans: Natural products and synthesis. Nat Prod Rep 26(10): 1251-1292.
29. Smeds AI, Jauhiainen L, Tuomola E, Peltonen-Sainio P, (2009) Characterization of variation in the lignan content and composition of winter rye, spring wheat, and spring oat. J Agric Food Chem 57(13): 5837-5842.
30. Heinonen S, Nurmi T, Liukkonen K, Poutanen K, Wahala K, et al. (2001) In vitro metabolism of plant lignans: New precursors of mammalian lignans enterolactone and enterodiol. J Agric Food Chem 49(7): 3178-3186.
31. Penalvo JL, Heinonen SM, Aura AM, Adlercreutz H, (2005) Dietary sesamin is converted to enterolactone in humans. J Nutr 135(5): 1056-1062.
32. Penalvo JL, Haajanen KM, Botting N, Adlercreutz H, (2005) Quantification of lignans in food using isotope dilution gas chromatography/mass spectrometry. J Agric Food Chem 53(24): 9342-9347.
33. Aura AM, Oikarinen S, Mutanen M, Heinonen SM, Adlercreutz HC, et al. (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(1): 45-51.
34. Clavel T, Dore J, Blaut M, (2006) Bioavailability of lignans in human subjects. Nutr Res Rev 19(2): 187-196.
35. Hanhineva K, Rogachev I, Aura AM, Aharoni A, Poutanen K, et al. (2011) Qualitative characterization of benzoxazinoid derivatives in whole grain rye and wheat by LC-MS metabolite profiling. J Agric Food Chem 59(3): 921-927.
36. Adhikari KB, Laursen BB, Laerke HN, Fomsgaard IS, (2012) Bioactive benzoxazinoids in rye bread are absorbed and metabolized in pigs. J Agric Food Chem.
37. Hanhineva K, Soininen P, Anttonen MJ, Kokko H, Rogachev I, et al. (2009) NMR and UPLC-qTOF-MS/MS characterisation of novel phenylethanol derivatives of phenylpropanoid glucosides from the leaves of strawberry (fragaria x ananassa cv. jonsok). Phytochem Anal 20(5): 353-364.
38. van Duynhoven J, Vaughan EE, Jacobs DM, Kemperman RA, van Velzen EJ, et al. (2011) Metabolic fate of polyphenols in the human superorganism. Proc Natl Acad Sci U S A 108: 4531-4538.
39. Jacobs DM, Gaudier E, van Duynhoven J, Vaughan EE, (2009) Non-digestible food ingredients, colonic microbiota and the impact on gut health and immunity: A role for metabolomics. Curr Drug Metab 10(1): 41-54.
40. Wishart DS, Knox C, Guo AC, Eisner R, Young N, et al. (2009) HMDB: A knowledgebase for the human metabolome. Nucleic Acids Res 37(Database issue) pp. D603-10.
41. Oikarinen S, Heinonen S, Karppinen S, Matto J, Adlercreutz H, et al. (2003) Plasma enterolactone or intestinal bifidobacterium levels do not explain adenoma formation in multiple intestinal neoplasia (min) mice fed with two different types of rye-bran fractions. Br J Nutr 90(1): 119-125.
42. Aura A, Karppinen S, Virtanen H, Forssell P, Heinonen S, et al. (2005) Processing of rye bran influences both the fermentation of dietary fibre and the bioconversion of lignans by human faecal flora in vitro. J Sci Food Agric 85(12): 2085-2093.
43. Barry JL, Hoebler C, Macfarlane GT, Macfarlane S, Mathers JC, et al. (1995) Estimation of the fermentability of dietary fibre in vitro: A european interlaboratory study. Br J Nutr 74(3): 303-322.
44. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, et al. (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
45. Hanhineva K, Rogachev I, Kokko H, Mintz-Oron S, Venger I, et al. (2008) Non-targeted analysis of spatial metabolite composition in strawberry (fragaria x ananassa) flowers. Phytochemistry 69(13): 2463-2481.