Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지

Transformation of the Glycosides from Food Materials by Probiotics and Food Microorganisms

  • Lee Bo-Hyun (Department of Food and Nutrition, & Research Institute of Human Ecology, Seoul National University) ;
  • You Hyun-Ju (Department of Food and Nutrition, & Research Institute of Human Ecology, Seoul National University) ;
  • Park Myeong-Soo (Department of Hotel Culinary Art, Anyang Technical College, Research Institute, Bifido Inc.) ;
  • Kwon Bin (Department of Food and Nutrition, & Research Institute of Human Ecology, Seoul National University, Research Institute, Bifido Inc.) ;
  • Ji Geun-Eog (Department of Food and Nutrition, & Research Institute of Human Ecology, Seoul National University, Research Institute, Bifido Inc.)
  • Published : 2006.04.01
Download PDF
⟨ Previous Next ⟩

Abstract

Glycosides are important functional materials in foods. Transformation, especially hydrolysis, of the sugar moieties tends to improve the functional properties of the administered glycosides in vivo. Various probiotic bacteria and edible food-grade fungi such as bifidobacteria, lactobacilli, leuconostocs, yeasts, and aspergilli are potential industrial microorganisms to transform glycosides of ginsenosides from ginseng, platycodin saponins from Platycodon grandiflorum, Trignoella foenum-graecum (TFG) saponins, and isoflavones from soybeans and Puerariae radix, respectively, by fermentation or enzymatic reaction. In this review, various transformation pathways bearing potential significance with respect to the changes in structure and function of the various glycosides from the food materials will be introduced. In conclusion, the proper combination of food microorganisms and transformation conditions will improve the functionality and the sensory value and reduce the cytotoxicity of the functional glycosides present in various functional food raw materials.

Keywords

References

  1. Akao, T. 1997. Hydrolysis of glycyrrhetyl mono-glucuronide to glycyrrhetic acid by glycyrrhetyl mono-glucuronide beta- D-glucuronidase of Eubacterium sp. GLH. Biol. Pharm. Bull. 20: 1245-1249 https://doi.org/10.1248/bpb.20.1245
  2. Aling, D., Y. Min, G. Hongzhu, Z. Junhua, and G. Dean. 2003. Microbial transformation of ginsenoside Rb1 by Rhizopus stolonifer and Curvularia lunata. Biotechnol. Lett. 25: 339-344 https://doi.org/10.1023/A:1022320824000
  3. Alison, M., R. William, and S. Mindy. 2003. Phytoestrogens. Best Pract. Res. Clin. Endocrinol. Metab. 17: 253-271 https://doi.org/10.1016/S1521-690X(02)00103-3
  4. Atkinson, C., C. L. Frankenfeld, and H. W. Lampe. 2005. Gut bacterial metabolism of the soy isoflavone daidzein: Exploring the relevance to human health. Exp. Biol. Med. 230: 155-170 https://doi.org/10.1177/153537020523000302
  5. Bae, E. A., M. J. Han, E. J. Kim, and D. H. Kim. 2004. Transformation of ginseng saponins to ginsenoside Rh2 by acids and human intestinal bacteria and biological activities of their transformants. Arch. Pharm. Res. 27: 61-67 https://doi.org/10.1007/BF02980048
  6. Bae, E. A., N. A. Kim, M. J. Han, M. K Choo, and D. H. Kim. 2003. Transformation of ginsenosides to compound K (IH-901) by lactic acid bacteria of human intestine. J. Microbiol. Biotechnol. 13: 9-14
  7. Bae, E. A., S. Y. Park, and D. H. Kim. 2000. Constitutive betaglucosidases hydrolyzing ginsenoside Rb1 and Rb2 from human intestinal bacteria. Biol. Pharm. Bull. 23: 1481-1485 https://doi.org/10.1248/bpb.23.1481
  8. Basch, E., C. Ulbricht, G. Kuo, P. Szapary, and M. Smith. 2003. Therapeutic applications of fenugreek. Alt. Med. Rev. 8: 20-27
  9. Cerda, B., P. Periago, J. C. Espin, and F. A. Tomas-Barberan. 2005. Identification of urolithin as a metabolite produced by human colon microflora from ellagic acid and related compounds. J. Agric. Food Chem. 53: 5571-5576
  10. Chi, H., D. H. Kim, and G. E. Ji. 2005. Transformation of Ginsenosides Rb2 and Rc from Panax ginseng by food microbial enzyme. Biol. Pharm. Bull. 28: 2102-2105 https://doi.org/10.1248/bpb.28.2102
  11. Chi, H. and G. E. Ji. 2005. Transformation of ginsenosides Rb1 and Re from Panax ginseng by food microorganisms. Biotechnol. Lett. 27: 765-771 https://doi.org/10.1007/s10529-005-5632-y
  12. Choi, E. K. and G. E. Ji. 2005. Food microorganisms that effectively hydrolyze O-glycoside but not C-glycoside isoflavones in Puerariae radix. J. Food Sci. 70: C25-C28 https://doi.org/10.1111/j.1365-2621.2005.tb09015.x
  13. Coldham, N. G., C. Darby, M. Hows, L. J. King, A. Q. Zhang, and M. J. Sauer. 2002. Comparative metabolism of genistin by human and rat gut microflora: Detection and identification of the end-products of metabolism. Xenobiotica 32: 45-62 https://doi.org/10.1080/00498250110085809
  14. Gupta, A., R. Gupta, and B. Lal. 2001. Effect of Trigonella foenum-graecum (fenugreek) seeds on glycaemic control and insulin resistance in type 2 diabetes mellitus: A double blind placebo controlled study. J. Assoc. Physicians India 49: 1057-1061
  15. Hasegawa, H., J. W. Sung, and Y. Benno. 1997. Role of human intestinal Prevotella oris in hydrolyzing ginseng saponins. Planta Medica. 63: 436-440 https://doi.org/10.1055/s-2006-957729
  16. Hasegawa, S. 1999. Limonoid glycosides, pp. 275-294. In Ikan, R. (ed.). Naturally Occurring Glycosides. John Willey & Sons, England
  17. Hattori, M., T. Akao, K. Kobashi, and T. Namba. 1993. Cleavages of the O- and C-glucosyl bonds of anthrone and 10,10'-bianthrone derivatives by human intestinal bacteria. Pharmacology 47: 125-133 https://doi.org/10.1159/000139851
  18. Hu, J., Y. L. Zheng, W. Hyde, S. Hendrich, and I. Murphy. 2004. Human fecal metabolism of soyasaponin I. J. Agric. Food Chem. 52: 2689-2696 https://doi.org/10.1021/jf035290s
  19. Ismail, B. and K. Haye. 2003. Beta-glycosidase activity toward different glycosidic forms of isoflavones. Br. J. Nutr. 90: 395-404 https://doi.org/10.1079/BJN2003900
  20. Izumi, T., M. K. Piskula, S. Osawa, A. Obata, K. Tobe, M. Saito, S. Kataoka, Y. Kubota, and M. Kikuchi. 2000. Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J. Nutr. 130: 1695-1699
  21. Jeon, K. S., G. E. Ji, and I. K. Hwang. 2002. Assay of betaglucosidase activity of bifidobacteria and the hydrolysis of isoflavone glycosides by Bifidobacterium sp. Int-57 in soymilk fermentation. J. Microbiol. Biotechnol. 12: 8-13
  22. Joint FAO/WHO. 2001. Expert Consultation on 'Evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria.'
  23. Kanaoda, M., T. Akao, and K. Kobashi. 1994. Metabolism of ginseng saponins, ginsenosides, by human intestinal bacteria. J. Trad. Med. 11: 241-245
  24. Karikura, M., T. Miyase, H. Tanizawa, T. Taniyama, and Y. Takino. 1991. Studies on absorption, distribution, excretion and metabolism of ginseng saponins. VII. Comparison of the decomposition modes of ginsenoside-Rb1 and -Rb2 in the digestive tract of rats. Chem. Pharm. Bull. 39: 2357- 2361 https://doi.org/10.1248/cpb.39.2357
  25. Keppler, K. and H. U. Humpf. 2005. Metabolism of anthocyanins and their phenolic degradation products by the intestinal microflora. Bioorg. Med. Chem. 13: 5195- 5205 https://doi.org/10.1016/j.bmc.2005.05.003
  26. Kim, D. H., K. U. Yu, E. A. Bae, and M. J. Han. 1998. Metabolism of puerarin and daidzin by human intestinal bacteria and their relation to in vitro cytotoxicity. Biol. Pharm. Bull. 21: 628-630 https://doi.org/10.1248/bpb.21.628
  27. Kim, H. S., E. H. Lee, S. R. Ko, K. J. Choi, J. H. Park, and D. S. Im. 2004. Effects of ginsenosides Rg3 and Rh2 on the proliferation of prostate cancer cells. Arch. Pharm. Res. 27: 429-435 https://doi.org/10.1007/BF02980085
  28. Kim, H. Y., K. B. Kwack, D. Y. Kim, and G. E. Ji. 2005. Oral probiotic bacterial administration suppressed allergic responses in an ovalbumin-induced allergy mouse model. FEMS Immunol. Med. Mic. 45: 259-267 https://doi.org/10.1016/j.femsim.2005.05.005
  29. Kudo, K., E. Tachikawa, T. Kashimoto, and E. Takahashi. 1998. Properties of ginseng saponin inhibition of catecholamine secretion in bovine adrenal chromaffin cells. Eur. J. Pharmacol. 341: 139-144 https://doi.org/10.1016/S0014-2999(97)01350-2
  30. Kurzer M. S. 2003. Phytoestrogen supplement use by women. J. Nutr. 133: 1983S-1986S
  31. Kurzer, M. S. and X. Xu. 1997. Dietary phytoestrogens. Annu. Rev. Nutr. 17: 353-381 https://doi.org/10.1146/annurev.nutr.17.1.353
  32. Lai, D. M., Y. K. Tu, I. M. Liu, P. F. Chen, and J. T. Cheng. 2006. Mediation of beta-endorphin by ginsenoside Rh2 to lower plasma glucose in streptozotocin-induced diabetic rats. Planta Med. 72: 9-13 https://doi.org/10.1055/s-2005-916177
  33. Lee, D. S., Y. S. Kim, C. N. Ko, K. H. Cho, H. S. Bae, K. S. Lee, J. J. Kim, E. K. Park, and D. H. Kim. 2002. Fecal metabolic activities of herbal components to bioactive compounds. Arch. Pharm. Res. 25: 165-169 https://doi.org/10.1007/BF02976558
  34. Lee, E. B. 1973. Pharmacological studies on Platycodon grandiflorum A. DC: IV. A comparison of experimental pharmacological effects of crude platycodin with clinical indications of platycodi radix. Yakugaku Zasshi 93: 1188- 1194 https://doi.org/10.1248/yakushi1947.93.9_1188
  35. Lee, H., F. J. Gonzalez, and M. Yoon. 2006. Ginsenoside Rf, a component of ginseng, regulates lipoprotein metabolism through peroxisome proliferator-activated receptor alpha. Biochem. Biophys. Res. Commun. 339: 196-203 https://doi.org/10.1016/j.bbrc.2005.10.197
  36. Lee, H. U., E. A. Bae, M. J. Han, N. J. Kim, and D. H. Kim. 2005. Hepatoprotective effect of ginsenoside Rb1 and compound K on tert-butyl hydroperoxide-induced liver injury. Liver Int. 25: 1069-1073 https://doi.org/10.1111/j.1478-3231.2005.01068.x
  37. Lee, S. J., W. G. Ko, J. H. Kim, J. H. Sung, C. K. Moon, and B. H. Lee. 2000. Induction of apoptosis by a novel intestinal metabolite of ginseng saponin via cytochrome c-mediated activation of caspase-3 protease. Biochem. Pharmacol. 60: 677-685 https://doi.org/10.1016/S0006-2952(00)00362-2
  38. Lee, W. K., S. T. Kao, I. M. Liu, and J. T. Cheng. 2006. Increase of insulin secretion by ginsenoside Rh2 to lower plasma glucose in Wistar rats. Clin. Exp. Pharmacol. Physiol. 33: 27-32
  39. Lei, V., W. K. Amoa-Awua, and L. Brimer. 1999. Degradation of cyanogenic glycosides by Lactobacillus plantarum strains from spontaneous cassava fermentation and other microorganisms. Int. J. Food Microbiol. 53: 169-184 https://doi.org/10.1016/S0168-1605(99)00156-7
  40. Liu, Y., Y. Liu, Y. Dai, L. Xun, and M. Hu. 2003. Enteric disposition and recycling of flavonoids and ginkgo flavonoids. J. Altern. Complement. Med. 9: 631-640 https://doi.org/10.1089/107555303322524481
  41. McKay, A. M. 1992. Hydrolysis of vicine and convicine from fababeans by microbial beta-glucosidase enzymes. J. Appl. Bacteriol. 72: 475-478 https://doi.org/10.1111/j.1365-2672.1992.tb01861.x
  42. Mochizuki, M., C. Y. Yoo, K. Mtsuzawa, K. Sato, I. Saiki, S. Tono-oda, K. Samukiwa, and I. Azuma. 1995. Inhibitory effect of tumor metastasis in mice by saponins, ginsenoside Rb2, 20(R)- and 20(S)-ginsenoside Rg3, of Red ginseng. Biol. Pharm. Bull. 18: 1197-1202 https://doi.org/10.1248/bpb.18.1197
  43. Murakami, T., A. Kishi, H. Matsuda, H. Matsuda, and M. Yoshikawa. 2000. Medicinal foodstuffs. X. Fenugreek seed. (3): Structures of new furostanol-type steroid saponin, Trigoneosides Xa, Xb, XIb, Xa, Xb, and Xa, from the seeds of Egyptian Trigonella foenum-graecum L. Chem. Pharm. Bull. 48: 994-1000 https://doi.org/10.1248/cpb.48.994
  44. Nettleton, H. A., K. A. Greany, W. Thomas, K. E. Wangen, H. Adlercreutz, and M. S. Kurzer. 2004. Plasma phytoestrogens are not altered by probiotic consumption in postmenopausal women with and without a history of breast cancer. J. Nutr. 134: 1998-2003
  45. Park, E. K., M. K. Choo, M. J. Han, and D. H. Kim. 2004. Ginsenoside Rh1 possesses antiallergic and anti-inflammatory activities. Int. Arch. Allergy Immunol. 133: 113-120 https://doi.org/10.1159/000076383
  46. Park, K. R. 2005. Transformation of fenugreek saponins by food microorganisms and the properties of the transformed metabolites. M.S. Thesis, Seoul National University
  47. Park, M. S., J. M. Seo, J. Y. Kim, and G. E. Ji. 2005. Heterologous gene expression and secretion in the genus Bifidobacterium. Lait 85: 1-8 https://doi.org/10.1051/lait:2004027
  48. Park, Y. C., C. H. Lee, H. S. Kang, K. W. Kim, H. T. Chung, and H. D. Kim. 1996. Ginsenoside-Rh1 and Rh2 inhibit the induction of nitric oxide synthesis in murine peritoneal macrophages. Biochem. Mol. Biol. Int. 40: 751-757
  49. Sato, K., M., Mochizuki, I. Saiki, Y. C. Yoo, K. Samukawa, and I. Azuma. 1994. Inhibition of tumor angiogenesis and metastasis by a saponin of Panax ginseng-ginsenoside-Rb2. Biol. Pharm. Bull. 17: 635-639 https://doi.org/10.1248/bpb.17.635
  50. Schneider, H., A. Schwiertz, M. D. Collins, and M. Blaut. 1999. Anaerobic transformation of quercetin-3-glucoside by bacteria from the human intestinal tract. Arch. Microbiol. 171: 81-91 https://doi.org/10.1007/s002030050682
  51. Setchell, K. D., C. Clerici, E. D. Lephart, S. J. Cole, C. Heenan, D. Castellani, B. E. Wolfe, L. Nechemias-Zimmer, N. M. Brown, T. D. Lund, R. J. Handa, and J. E. Heubi. 2005. 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. 81: 1072-1079 https://doi.org/10.1093/ajcn/81.5.1072
  52. Setchell, K. D. R., N. M. Brown, P. Desai, L. Zimmer- Nechemias, B. E. Wolfe, W. T. Brashear, A. S. Kirschner, A. Cassidy, and J. E. Heubi. 2001. Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements. J. Nutr. 131(suppl.): 1362S- 1375S
  53. Sievenpiper, J. L., J. T. Arnason, L. A. Leiter, and V. Vuksan. 2004. Decreasing, null and increasing effects of eight popular types of ginseng on acute postprandial glycemic indices in healthy humans: The role of ginsenosides. J. Am. Coll. Nutr. 23: 248-258 https://doi.org/10.1080/07315724.2004.10719368
  54. Tachikawa, E., K. Kudo, H. Hasegawa, T. Kashimoto, K. Sasaki, M. Miyazaki, H. Taira, and J. M. Lindstrom. 2003. In vitro inhibition of adrenal catecholamine secretion by steroidal metabolites of ginseng saponins. Biochem. Pharmacol. 68: 441-452
  55. Tawab, M. A., U. Bahr, M. Karas, M. Wurglics, and M. Schubert-Zsilavecz. 2003. Degradation of ginsenosides in humans after oral administration. Drug Metab. Dispos. 31: 1065-1071 https://doi.org/10.1124/dmd.31.8.1065
  56. Tian, Q., E. G. Miller, H. Ahmad, L. Tang, and B. S. Patil. 2001. Differential inhibition of human cancer cell proliferation by citrus limonoids. Nutr. Cancer 40: 180-184 https://doi.org/10.1207/S15327914NC402_15
  57. Tsangalis, D., J. F. Ashton, A. E. J. McGill, and N. P. Shah. 2002. Enzymatic transformation of isoflavone phytoestrogens in soymilk by beta-glucosidase-producing bifidobacteria. J. Food Sci. 67: 3104-3113 https://doi.org/10.1111/j.1365-2621.2002.tb08866.x
  58. Yasuda, T., Y. Kano, K. Saito, and K. Ohsawa. 1995. Urinary and biliary metabolites of puerarin in rats. Biol. Pharm. Bull. 18: 300-303 https://doi.org/10.1248/bpb.18.300
  59. You, H. J., D. K. Oh, and G. E. Ji. 2004. Anticancerogenic effect of a novel chiro-inositol containing polysaccharide from Bifidobacterium bifidum BGN4. FEMS Microbiol. Lett. 240: 131-136 https://doi.org/10.1016/j.femsle.2004.09.020
  60. Walle, T., A. M. Browning, L. L. Steed, S. G. Reed, and U. K. Walle. 2005. Flavonoid glycosides are hydrolyzed and thus activated in the oral cavity in humans. J. Nutr. 135: 48- 52
  61. Wang, X., J. Wu, H. Chiba, K. Umegaki, K. Yamada, and Y. Ishimi. 2003. Puerariae radix prevents bone loss in ovariectomized mice. J. Bone Miner. Metab. 21: 268-275 https://doi.org/10.1007/s00774-003-0420-z
  62. Wang, Z., Y. Kurosaki, T. Nakayama, and T. Kimura. 1994. Mechanism of gastrointestinal absorption of glycyrrhizin in rats. Biol. Pharm. Bull. 17: 1399-1403 https://doi.org/10.1248/bpb.17.1399
  63. Wie, H. J. 2005. Transformation of saponin (platycodin) from Platycodi radix by Aspergillus niger. M.S. Thesis, Seoul National University
  64. Xu, X., K. S. Harris, H. J. Wang, P. A. Murphy, and S. Hendrich. 1995. Bioavailability of soybean isoflavones depends upon gut microflora in women. J. Nutr. 125: 2307- 2315