Xylitol affects the intestinal microbiota and metabolism of daidzein in adult Male mice

International Journal of Molecular Sciences

Volumn 14, Issue 12, 2013, Pages 23993-24007

  Tamura, Motoi ^a   Hoshi, Chigusa ^a   Hori, Sachiko ^a  

^a NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

Daidzein; Equol; Intestinal microbiota; Mice; Xylitol

Indexed keywords

CHOLESTEROL; DAIDZEIN; EQUOL; PHOSPHOLIPID; TRIACYLGLYCEROL; XYLITOL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIETARY INTAKE; FECES ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; INTESTINE FLORA; LIPID ANALYSIS; MALE; METABOLISM; NONHUMAN; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; URINALYSIS;

ANIMALS; CECUM; CHOLESTEROL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EQUOL; FECES; ISOFLAVONES; LIPIDS; MALE; MICE; MICE, INBRED ICR; MICROBIOTA; PHOSPHOLIPIDS; RANDOM ALLOCATION; TRIGLYCERIDES; XYLITOL;

EID: 84890240828     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141223993     Document Type: Article

References (48)

1. Goto, Y.; Anzai, M.; Chiba, M.; Ohneda, A.; Kawashima, S. Clinical effects of xylitol on carbohydrate and lipid metabolism in diabetes. Lancet 1965, 2, 918-921.
2. Amo, K.; Arai, H.; Uebanso, T.; Fukaya, M.; Koganei, M.; Sasaki, H.; Yamamoto, H.; Taketani, Y.; Takeda, E., Effects of xylitol on metabolic parameters and visceral fat accumulation. J. Clin. Biochem. Nutr. 2011, 49, 1-7.
3. Ishii, H.; Takahashi, H.; Mamori, H.; Murai, S.; Kanno, T. Effects of xylitol on carbohydrate metabolism in rat liver treated with carbon tetrachloride or alloxan. Keio J. Med. 1969, 18, 109-114.
4. Mattila, P.T.; Svanberg, M.J.; Pökkä, P.; Knuuttila, M. Dietary xylitol protects against weakening of bone biomechanical properties in ovariectomized rats. J. Nutr. 1998, 128, 1811-1814.
5. Mattila, P.T.; Svanberg, M.J.; Knuuttila, M.L. Increased bone volume and bone mineral content in xylitol-fed aged rats. Gerontology 2001, 47, 300-305.
6. Mattila, P.; Knuuttila, M.; Kovanen, V.; Svanberg, M. Improved bone biomechanical properties in rats after oral xylitol administration. Calcif. Tissue Int. 1999, 64, 340-344.
7. Svanberg, M.; Mattila, P.; Knuuttila, M. Dietary xylitol retards the ovariectomy-induced increase of bone turnover in rats. Calcif. Tissue Int. 1997, 60, 462-466.
8. Brommage, R.; Binacua, C.; Antille, S.; Carrie, A.L., Intestinal calcium absorption in rats is stimulated by dietary lactulose and other resistant sugars. J. Nutr. 1993, 123, 2186-2194.
9. Barnes, S. The biochemistry, chemistry and physiology of the isoflavones in soybeans and their food products., Lymphat. Res. Biol. 2010, 8, 89-98.
10. Uesugi, T.; Toda, T.; Tsuji, K.; Ishida, H. Comparative study on reduction of bone loss and lipid metabolism abnormality in ovariectomized rats by soy isoflavones, daidzin, genistin, and glycitin. Biol. Pharm. Bull. 2001, 24, 368-372.
11. Breinholt, V.; Larsen, J.C., Detection of weak estrogenic flavonoids using a recombinant yeast strain and a modified MCF7 cell proliferation assay. Chem. Res. Toxicol. 1998, 11, 622-629.
12. Chang, Y.C.; Nair, M.G., Metabolism of daidzein and genistein by intestinal bacteria. J. Nat. Prod. 1995, 58, 1892-1896.
13. Setchell, K.D.; Borriello, S.P.; Hulme, P.; Kirk, D.N.; Axelson, M. Nonsteroidal estrogens of dietary origin: Possible roles in hormone-dependent disease. Am. J. Clin. Nutr. 1984, 40, 569-578.
14. Bolca, S.; Possemiers, S.; Herregat, A.; Huybrechts, I.; Heyerick, A.; de Vriese, S.; Verbruggen, M.; Depypere, H.; de Keukeleire, D.; Bracke, M.; et al., Microbial and dietary factors are associated with the equol producer phenotype in healthy postmenopausal women. J. Nutr. 2007, 137, 2242-2246.
15. Setchell, K.D.; Clerici, C.; Lephart, E.D.; Cole, S.J.; Heenan, C.; Castellani, D.; Wolfe, B.E.; Nechemias-Zimmer, L.; Brown, N.M.; Lund, T.D., et al., S-equol, a potent ligand for estrogen receptor β, is the exclusive enantiomeric form of the soy isoflavone metabolite produced by human intestinal bacterial flora. Am. J. Clin. Nutr. 2005, 81, 1072-1079.
16. Atkinson, C.; Frankenfeld, C.L.; Lampe, J.W., Gut bacterial metabolism of the soy isoflavone daidzein: Exploring the relevance to human health. Exp. Biol. Med. 2005, 230, 155-170.
17. Bowey, E.; Adlercreutz, H.; Rowland, I., Metabolism of isoflavones and lignans by the gut microflora: A study in germ-free and human flora associated rats. Food Chem. Toxicol. 2003, 41, 631-636.
18. Akaza, H.; Miyanaga, N.; Takashima, N.; Naito, S.; Hirao, Y.; Tsukamoto, T.; Fujioka, T.; Mori, M.; Kim, W.J.; Song, J.M., et al., Comparisons of percent equol producers between prostate cancer patients and controls: Case-controlled studies of isoflavones in Japanese, Korean and American residents. Jpn. J. Clin. Oncol. 2004, 34, 86-89.
19. Frankenfeld, C.L.; Atkinson, C.; Thomas, W.K.; Goode, E.L.; Gonzalez, A.; Jokela, T.; Wahala, K.; Schwartz, S.M.; Li, S.S.; Lampe, J.W., Familial correlations, segregation analysis, and nongenetic correlates of soy isoflavone-metabolizing phenotypes. Exp. Biol. Med. 2004, 229, 902-913.
20. Turnbaugh, P.J.; Ley, R.E.; Mahowald, M.A.; Magrini, V.; Mardis, E.R.; Gordon, J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444, 1027-1031.
21. Salminen, S.; Salminen, E.; Koivistoinen, P.; Bridges, J.; Marks, V. Gut microflora interactions with xylitol in the mouse, rat and man. Food Chem. Toxicol. 1985, 23, 985-990.
22. Wang, X.L.; Hur, H.G.; Lee, J.H.; Kim, K.T.; Kim, S.I. Enantioselective synthesis of S-equol from dihydrodaidzein by a newly isolated anaerobic human intestinal bacterium. Appl. Environ. Microbiol. 2005, 71, 214-219.
23. Rafii, F.; Jackson, L.D.; Ross, I.; Heinze, T.M.; Lewis, S.M.; Aidoo, A.; Lyn-Cook, L.; Manjanatha, M. Metabolism of daidzein by fecal bacteria in rats. Comp. Med. 2007, 57, 282-286.
24. Mäkeläinen, H.S.; Mäkivuokko, H.A.; Salminen, S.J.; Rautonen, N.E.; Ouwehand, A.C. The effects of polydextrose and xylitol on microbial community and activity in a 4-stage colon simulator. J. Food Sci. 2007, 72, M153-M159.
25. Minamida, K.; Tanaka, M.; Abe, A.; Sone, T.; Tomita, F.; Hara, H.; Asano, K. Production of equol from daidzein by Gram-positive rod-shaped bacterium isolated from rat intestine. J. Biosci. Bioeng. 2006, 102, 247-250.
26. Salminen, E.K.; Salminen, S.J.; Porkka, L.; Kwasowski, P.; Marks, V.; Koivistoinen, P.E. Xylitol vs glucose: Effect on the rate of gastric emptying and motilin, insulin, and gastric inhibitory polypeptide release. Am. J. Clin. Nutr. 1989, 49, 1228-1232.
27. Mattila, P.T.; Svanberg, M.J.; Jämsä, T.; Knuuttila, M.L. Improved bone biomechanical properties in xylitol-fed aged rats. Metabolism 2002, 51, 92-96.
28. Svanberg, M.; Knuuttila, M. Dietary xylitol prevents ovariectomy induced changes of bone inorganic fraction in rats. Bone Miner. 1994, 26, 81-88.
29. Fujioka, M.; Uehara, M.; Wu, J.; Adlercreutz, H.; Suzuki, K.; Kanazawa, K.; Takeda, K.; Yamada, K.; Ishimi, Y. Equol, a metabolite of daidzein, inhibits bone loss in ovariectomized mice. J. Nutr. 2004, 134, 2623-2627.
30. Ohta, A.; Uehara, M.; Sakai, K.; Takasaki, M.; Adlercreutz, H.; Morohashi, T.; Ishimi, Y. A combination of dietary fructooligosaccharides and isoflavone conjugates increases femoral bone mineral density and equol production in ovariectomized mice. J. Nutr. 2002, 132, 2048-2054.
31. Tousen, Y.; Ezaki, J.; Fujii, Y.; Ueno, T.; Nishimuta, M.; Ishimi, Y. Natural S-equol decreases bone resorption in postmenopausal, non-equol-producing Japanese women: A pilot randomized, placebo-controlled trial. Menopause 2011, 18, 563-574.
32. Shafer, R.B.; Levine, A.S.; Marlette, J.M.; Morley, J.E., Effects of xylitol on gastric emptying and food intake. Am. J. Clin. Nutr. 1987, 45, 744-747.
33. Yamakoshi, J.; Piskula, M.K.; Izumi, T.; Tobe, K.; Saito, M.; Kataoka, S.; Obata, A.; Kikuchi, M. Isoflavone aglycone-rich extract without soy protein attenuates atherosclerosis development in cholesterol-fed rabbits. J. Nutr. 2000, 130, 1887-1893.
34. Mäkinen, K.K.; Hämäläinen, M.M., Metabolic effects in rats of high oral doses of galactitol, mannitol and xylitol. J. Nutr. 1985, 115, 890-899.
35. Islam, M.S., Effects of xylitol as a sugar substitute on diabetes-related parameters in nondiabetic rats. J. Med. Food 2011, 14, 505-511.
36. Torok, V.A.; Ophel-Keller, K.; Loo, M.; Hughes, R.J. Application of methods for identifying broiler chicken gut bacterial species linked with increased energy metabolism. Appl. Environ. Microbiol. 2008, 74, 783-791.
37. Nagashima, K.; Hisada, T.; Sato, M.; Mochizuki, J. Application of new primer-enzyme combinations to terminal restriction fragment length polymorphism profiling of bacterial populations in human feces. Appl. Environ. Microbiol. 2003, 69, 1251-1262.
38. Nagashima, K.; Mochizuki, J.; Hisada, T.; Suzuki, S.; Shimomura, K., Phylogenetic analysis of 16S ribosomal RNA gene sequences from human fecal microbiota and improved utility of terminal restriction fragment length polymorphism profiling. Biosci. Microflora 2006, 25, 99-107.
39. Walker, A.W.; Ince, J.; Duncan, S.H.; Webster, L.M.; Holtrop, G.; Ze, X.; Brown, D.; Stares, M.D.; Scott, P.; Bergerat, A., et al., Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011, 5, 220-230.
40. Turnbaugh, P.J.; Ridaura, V.K.; Faith, J.J.; Rey, F.E.; Knight, R.; Gordon, J.I. The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009, doi:10.1126/scitranslmed.3000322.
41. De La Serre, C.B.; Ellis, C.L.; Lee, J.; Hartman, A.L.; Rutledge, J.C.; Raybould, H.E. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G440-G448.
42. Reeves, P.G.; Nielsen, F.H.; Fahey, G.C., Jr. AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 1993, 123, 1939-1951.
43. Allain, C.C.; Poon, L.S.; Chan, C.S.; Richmond, W.; Fu, P.C. Enzymatic determination of total serum cholesterol. Clin. Chem. 1974, 20, 470-475.
44. Spayd, R.W.; Bruschi, B.; Burdick, B.A.; Dappen, G.M.; Eikenberry, J.N.; Esders, T.W.; Figueras, J.; Goodhue, C.T.; LaRossa, D.D.; Nelson, R.W., et al., Multilayer film elements for clinical analysis: Applications to representative chemical determinations. Clin. Chem. 1978, 24, 1343-1350.
45. Takayama, M.; Itoh, S.; Nagasaki, T.; Tanimizu, I. A new enzymatic method for determination of serum choline-containing phospholipids. Clin. Chim. Acta 1977, 79, 93-98.
46. Bligh, E.G.; Dyer, W.J., A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37, 911-917.
47. Tamura, M.; Hori, S.; Nakagawa, H. Dihydrodaidzein-producing Clostridium-like intestinal bacterium, strain TM-40, affects in vitro metabolism of daidzein by fecal microbiota of human male equol producer and non-producers Biosci. Microflora 2011, 30, 65-71.
48. Matsuki, T. Procedure of DNA extraction from fecal sample for the analysis of intestinal microflora J. Intest. Microbiol. 2006, 20, 259-262.