Bioactivity and Bioavailability of Ginsenosides are Dependent on the Glycosidase Activities of the A/J Mouse Intestinal Microbiome Defined by Pyrosequencing
参考文献:1. Ahmedin Jemal RS, Jiaquan X, Ward E. Cancer statistics. CA Cancer J Clin. 2010;60:277鈥?00. CrossRef 2. Clarkand J, You M. Chemoprevention of lung cancer by tea. Mol Nutr Food Res. 2006;50:144鈥?1. CrossRef 3. Hecht SS. Inhibition of carcinogenesis by isothiocyanates. Drug Metab Rev. 2000;32:395鈥?11. CrossRef 4. Tanand XL, Spivack SD. Dietary chemoprevention strategies for induction of phase II xenobiotic-metabolizing enzymes in lung carcinogenesis: a review. Lung Cancer. 2009;65:129鈥?7. CrossRef 5. Johnson TE, Hermanson D, Wang L, Kassie F, Upadhyaya P, O鈥橲ullivan MG, / et al. Lung tumorigenesis suppressing effects of a commercial kava extract and its selected compounds in a/j mice. Am J Chin Med. 39:727鈥?2. 6. Yan Y, Wang Y, Tan Q, Hara Y, Yun TK, Lubet RA, / et al. Efficacy of polyphenon E, red ginseng, and rapamycin on benzo(a)pyrene-induced lung tumorigenesis in A/J mice. Neoplasia. 2006;8:52鈥?. CrossRef 7. Mukhtar H, Khan N, Afaq F. Cancer chemoprevention through dietary antioxidants: progress and promise. Antioxid Redox Signal. 2008;10:475鈥?10. CrossRef 8. Miller YE, Keith RL, Karoor V, Mozer AB, Hudish TM, Le M. Chemoprevention of murine lung cancer by gefitinib in combination with prostacyclin synthase overexpression. Lung Cancer. 2010;70:37鈥?2. CrossRef 9. Ohashi K, Takigawa N, Osawa M, Ichihara E, Takeda H, Kubo T, / et al. Chemopreventive effects of gefitinib on nonsmoking-related lung tumorigenesis in activating epidermal growth factor receptor transgenic mice. Cancer Res. 2009;69:7088鈥?5. CrossRef 10. Miller YE, Kelly K, Kittelson J, Franklin WA, Kennedy TC, Klein CE, / et al. A randomized phase II chemoprevention trial of 13-CIS retinoic acid with or without alpha tocopherol or observation in subjects at high risk for lung cancer. Cancer Prev Res. 2009;2:440鈥?. CrossRef 11. Scott EN, Gescher AJ, Steward WP, Brown K. Development of dietary phytochemical chemopreventive agents: biomarkers and choice of dose for early clinical trials. Cancer Prev Res (Phila). 2009;2:525鈥?0. CrossRef 12. Qi LW, Wang CZ, Yuan CS. American ginseng: potential structure-function relationship in cancer chemoprevention. Biochem Pharmacol. 2010;80:947鈥?4. CrossRef 13. Sun S, Qi LW, Du GJ, Mehendale SR, Wang CZ, Yuan CS. Red notoginseng higher ginsenoside content and stronger anticancer potential than Asian and American ginseng. Food Chem. 2011;125:1299鈥?05. CrossRef 14. Yun TK, Yun YS, Han IW. Anticarcinogenic effect of long-term oral administration of red ginseng on newborn mice exposed to various chemical carcinogens. Cancer Detect Prev. 1983;6:515鈥?5. 15. Yun TK, Kim SH, Oh YR. Medium-term (9聽weeks) method for assay of preventive agents against tumor. J Korean Cancer Assoc. 1987;19:1鈥?. 16. Yun TK, Kim SH. Inhibition of development of benzo(a)-pyrene-induced mouse pulmonary adenoma by natural products in medium-term bioassay system. J Korean Cancer Assoc. 1988;20:133鈥?2. 17. Yun TK. Usefulness of medium-term bioassay determining formations of pulmonary adenoma in NIH(GP) mice for finding anticarcinogenic agents from natural products. J Toxicol Sci. 1991;16 Suppl 1:53鈥?2. CrossRef 18. Yun TK, Kim SH, Lee YS. Trial of a new medium-term model using benzo(a)pyrene induced lung tumor in newborn mice. Anticancer Res. 1995;15:839鈥?5. 19. Kong H, Wang M, Venema K, Maathuis A, van der Heijden R, van der Greef J, / et al. Bioconversion of red ginseng saponins in the gastro-intestinal tract in vitro model studied by high-performance liquid chromatography-high resolution Fourier transform ion cyclotron resonance mass spectrometry. J Chromatogr A. 2009;1216:2195鈥?03. CrossRef 20. Li H, Lee JH, Ha JM. Effective purification of ginsenosides from cultured wild ginseng roots, red ginseng, and white ginseng with macroporous resins. J Microbiol Biotechnol. 2008;18:1789鈥?1. 21. Cheng CC, Yang SM, Huang CY, Chen JC, Chang WM, Hsu SL. Molecular mechanisms of ginsenoside Rh2-mediated G1 growth arrest and apoptosis in human lung adenocarcinoma A549 cells. Cancer Chemother Pharmacol. 2005;55:531鈥?0. CrossRef 22. Yun TK, Lee YS, Lee YH, Kim SI, Yun HY. Anticarcinogenic effect of Panax ginseng C.A. Meyer and identification of active compounds. J Korean Med Sci. 2001;16(Suppl):S6鈥?8. 23. Park CS, Yoo MH, Noh KH, Oh DK. Biotransformation of ginsenosides by hydrolyzing the sugar moieties of ginsenosides using microbial glycosidases. Appl Microbiol Biotechnol. 2010;87:9鈥?9. CrossRef 24. Henrissat B. A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1991;280(Pt 2):309鈥?6. 25. Henrissatand B, Bairoch A. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1993;293(Pt 3):781鈥?. 26. Henrissatand B, Bairoch A. Updating the sequence-based classification of glycosyl hydrolases. Biochem J. 1996;316(Pt 2):695鈥?. 27. Bhatia Y, Mishra S, Bisaria VS. Microbial beta-glucosidases: cloning, properties, and applications. Crit Rev Biotechnol. 2002;22:375鈥?07. CrossRef 28. Akao T, Kida H, Kanaoka M, Hattori M, Kobashi K. Intestinal bacterial hydrolysis is required for the appearance of compound K in rat plasma after oral administration of ginsenoside Rb1 from Panax ginseng. J Pharm Pharmacol. 1998;50:1155鈥?0. CrossRef 29. Chi H, Kim DH, Ji GE. Transformation of ginsenosides Rb2 and Rc from Panax ginseng by food microorganisms. Biol Pharm Bull. 2005;28:2102鈥?. CrossRef 30. Cheng LQ, Na JR, Kim MK, Bang MH, Yang DC. Microbial conversion of ginsenoside Rb1 to minor ginsenoside F2 and gypenoside XVII by Intrasporangium sp. GS603 isolated from soil. J Microbiol Biotechnol. 2007;17:1937鈥?3. 31. Chen G, Yang M, Song Y, Lu Z, Zhang J, Huang H, / et al. Comparative analysis on microbial and rat metabolism of ginsenoside Rb1 by high-performance liquid chromatography coupled with tandem mass spectrometry. Biomed Chromatogr. 2008;22:779鈥?5. CrossRef 32. Zhou P, Zhou W, Yan Q, Li JY, Zhang XC. Biotransformation of Panax notoginseng saponins into ginsenoside compound K production by Paecilomyces bainier sp 229. J Appl Microbiol. 2008;104:699鈥?06. CrossRef 33. Son JW, Kim HJ, Oh DK. Ginsenoside Rd production from the major ginsenoside Rb(1) by beta-glucosidase from Thermus caldophilus. Biotechnol Lett. 2008;30:713鈥?. CrossRef 34. Kim YS, Kim JJ, Cho KH, Jung WS, Moon SK, Park EK, / et al. Biotransformation of ginsenoside Rb1, crocin, amygdalin, geniposide, puerarin, ginsenoside Re, hesperidin, poncirin, glycyrrhizin, and baicalin by human fecal microflora and its relation to cytotoxicity against tumor cells. J Microbiol Biotechnol. 2008;18:1109鈥?4. 35. Hasegawa H, Sung JH, Benno Y. Role of human intestinal Prevotella oris in hydrolyzing ginseng saponins. Planta Med. 1997;63:436鈥?0. CrossRef 36. Bae EA, Choo MK, Park EK, Park SY, Shin HY, Kim DH. Metabolism of ginsenoside R(c) by human intestinal bacteria and its related antiallergic activity. Biol Pharm Bull. 2002;25:743鈥?. CrossRef 37. Relman DA, Dethlefsen L, Huse S, Sogin ML. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. Plos Biol. 2008;6:2383鈥?00. 38. Castagnini C, Luceri C, Toti S, Bigagli E, Caderni G, Femia AP, / et al. Reduction of colonic inflammation in HLA-B27 transgenic rats by feeding Marie Menard apples, rich in polyphenols. Br J Nutr. 2009;102:1620鈥?. CrossRef 39. Bolam DN, Sonnenburg ED, Zheng HJ, Joglekar P, Higginbottom SK, Firbank SJ, / et al. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell. 2010;141:1241鈥?6. CrossRef 40. Yang Z, Gao S, Yin TJ, Kulkarni KH, Teng Y, You M, / et al. Biopharmaceutical and pharmacokinetic characterization of matrine as determined by a sensitive and robust UPLC-MS/MS method. J Pharm Biomed Anal. 2010;51:1120鈥?. CrossRef 41. Yang Z, Gao S, Wang J, Yin T, Teng Y, Wu B, / et al. Enhancement of oral bioavailability of ginsenoside 20(s)-Rh2 through improved understanding of its absorption and efflux mechanisms. Drug Metab Dispos. 2011;39:1866鈥?2. 42. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, / et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537鈥?1. CrossRef 43. Angiuoli SV, Matalka M, Gussman A, Galens K, Vangala M, Riley DR, / et al. CloVR: a virtual machine for automated and portable sequence analysis from the desktop using cloud computing. BMC Bioinforma. 2011;12. 44. McDoniels-Silvers AL, Herzog CR, Tyson FL, Malkinson AM, You M. Inactivation of both Rb and p53 pathways in mouse lung epithelial cell lines. Exp Lung Res. 2001;27:297鈥?18. CrossRef 45. Hu M, Chen J, Zhu Y, Dantzig AH, Stratford Jr RE, Kuhfeld MT. Mechanism and kinetics of transcellular transport of a new beta-lactam antibiotic loracarbef across an intestinal epithelial membrane model system (Caco-2). Pharm Res. 1994;11:1405鈥?3. CrossRef 46. Arturssonand P, Karlsson J. Correlation between oral-drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelial (Caco-2) cells. Biochem Biophys Res Commun. 1991;175:880鈥?. CrossRef 47. Yang Z, Wang JR, Niu T, Gao S, Yin T, You M, / et al. Inhibition of p-glycoprotein leads to improved oral bioavailability of compound k, an anticancer metabolite of red ginseng extract produced by gut microflora. Drug Metab Dispos. 40:1538鈥?4. 48. Hou JG, Xue JJ, Sun MQ, Wang CY, Liu L, Zhang DL, / et al. Highly selective microbial transformation of major ginsenoside Rb(1) to gypenoside LXXV by Esteya vermicola CNU120806. J Appl Microbiol. 2012;113:807鈥?4. 49. McBainand AJ, Macfarlane GT. Ecological and physiological studies on large intestinal bacteria in relation to production of hydrolytic and reductive enzymes involved in formation of genotoxic metabolites. J Med Microbiol. 1998;47:407鈥?6. CrossRef 50. Goossens D, Jonkers D, Russel M, Stobberingh E, Van Den Bogaard A, StockbrUgger R. The effect of Lactobacillus plantarum 299v on the bacterial composition and metabolic activity in faeces of healthy volunteers: a placebo-controlled study on the onset and duration of effects. Aliment Pharmacol Ther. 2003;18:495鈥?05. CrossRef 51. Marteau P, Pochart P, Flourie B, Pellier P, Santos L, Desjeux JF, / et al. Effect of chronic ingestion of a fermented dairy product containing Lactobacillus acidophilus and Bifidobacterium bifidum on metabolic activities of the colonic flora in humans. Am J Clin Nutr. 1990;52:685鈥?. 52. Chen G, Yang M, Lu Z, Zhang J, Huang H, Liang Y, / et al. Microbial transformation of 20(S)-protopanaxatriol-type saponins by Absidia coerulea. J Nat Prod. 2007;70:1203鈥?. CrossRef 53. Chen GT, Yang M, Song Y, Lu ZQ, Zhang JQ, Huang HL, / et al. Microbial transformation of ginsenoside Rb(1) by Acremonium strictum. Appl Microbiol Biotechnol. 2008;77:1345鈥?0. CrossRef 54. Cheng LQ, Kim MK, Lee JW, Lee YJ, Yang DC. Conversion of major ginsenoside Rb1 to ginsenoside F2 by Caulobacter leidyia. Biotechnol Lett. 2006;28:1121鈥?. CrossRef 55. Cheng LQ, Na JR, Bang MH, Kim MK, Yang DC. Conversion of major ginsenoside Rb1 to 20(S)-ginsenoside Rg3 by Microbacterium sp. GS514. Phytochemistry. 2008;69:218鈥?4. CrossRef 56. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837鈥?8. CrossRef 57. Chiand H, Ji GE. Transformation of ginsenosides Rb1 and Re from Panax ginseng by food microorganisms. Biotechnol Lett. 2005;27:765鈥?1. CrossRef
作者单位:Tao Niu (1) Diane L. Smith (2) Zhen Yang (1) Song Gao (1) Taijun Yin (1) Zhi-Hong Jiang (3) Ming You (4) Richard A. Gibbs (5) Joseph F. Petrosino (6) Ming Hu (1)
1. Department of Pharmacological and Pharmaceutical Sciences, College of Pharmacy, University of Houston, 1441 Moursund Street, Houston, Texas, 77030, USA 2. Program in Translational Biology and Molecular Medicine, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA 3. School of Chinese Medicine, Hong Kong Baptist University, 7 Baptist University Road, Kowloon Tong, Hong Kong 4. Medical College of Wisconsin Cancer Center, 8701 West Watertown Plank Road, Milwaukee, Wisconsin, 53226, USA 5. Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA 6. Alkek Center for Metagenomics and Microbiome Research Department of Molecular Virology and Microbiology, Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas, 77030, USA