Gut microbiota modulates drug pharmacokinetics

References

• Adolph TE, Grander C, Moschen AR, Tilg H. 2018. Liver-microbiome axis in health and disease. Trends Immunol. DOI:10.1016/j.it.2018.05.002
   PubMed Web of Science ®Google Scholar
• Aura AM, Mattila I, Hyotylainen T, Gopalacharyulu P, Bounsaythip C, Oresic M, Oksman-Caldentey KM. 2011. Drug metabolome of the simvastatin formed by human intestinal microbiota in vitro. Mol Biosyst. 7:437–446.
   PubMed Web of Science ®Google Scholar
• Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. 2005. Host-bacterial mutualism in the human intestine. Science. 307:1915–1920.
   PubMed Web of Science ®Google Scholar
• Bakke OM. 1971. Degradation of DOPA by intestinal microorganisms in vitro. Acta Pharmacol Toxicol (Copenh). 30:115–121.
   PubMedGoogle Scholar
• Basit AW, Lacey LF. 2001. Colonic metabolism of ranitidine: implications for its delivery and absorption. Int J Pharm. 227:157–165.
   PubMed Web of Science ®Google Scholar
• Basit AW, Newton JM, Lacey LF. 2002. Susceptibility of the H2-receptor antagonists cimetidine, famotidine and nizatidine, to metabolism by the gastrointestinal microflora. Int J Pharm. 237:23–33.
   PubMed Web of Science ®Google Scholar
• Boer J, Young-Sciame R, Lee F, Bowman KJ, Yang X, Shi JG, Nedza FM, Frietze W, Galya L, Combs AP. 2016. Roles of UGT, P450, and gut microbiota in the metabolism of epacadostat in humans. Drug Metab Dispos. 44:1668–1674.
   PubMed Web of Science ®Google Scholar
• Chan RP, Pope DJ, Gilbert AP, Sacra PJ, Baron JH, Lennard-Jones JE. 1983. Studies of two novel sulfasalazine analogs, ipsalazide and balsalazide. Dig Dis Sci. 28:609–615.
   PubMed Web of Science ®Google Scholar
• Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, Paris A, Want EJ, de Waziers I, Cloarec O. 2011. Colonization-induced host-gut microbial metabolic interaction. MBio. 2:e00271–e00210.
   PubMed Web of Science ®Google Scholar
• Clayton TA, Baker D, Lindon JC, Everett JR, Nicholson JK. 2009. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc Natl Acad Sci USA. 106:14728–14733.
   PubMed Web of Science ®Google Scholar
• Clements JA, Heading RC, Nimmo WS, Prescott LF. 1978. Kinetics of acetaminophen absorption and gastric emptying in man. Clin Pharmacol Ther. 24:420–431.
   PubMed Web of Science ®Google Scholar
• Cummings AJ, King ML, Martin BK. 1967. A kinetic study of drug elimination: the excretion of paracetamol and its metabolites in man. Br J Pharmacol Chemother. 29:150–157.
   PubMed Web of Science ®Google Scholar
• David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 505:559–563.
   PubMed Web of Science ®Google Scholar
• De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA. 107:14691–14696.
   PubMed Web of Science ®Google Scholar
• de Lannoy IA, Silverman M. 1992. The MDR1 gene product, P-glycoprotein, mediates the transport of the cardiac glycoside, digoxin. Biochem Biophys Res Commun. 189:551–557.
   PubMed Web of Science ®Google Scholar
• Delomenie C, Fouix S, Longuemaux S, Brahimi N, Bizet C, Picard B, Denamur E, Dupret JM. 2001. Identification and functional characterization of arylamine N-acetyltransferases in eubacteria: evidence for highly selective acetylation of 5-aminosalicylic acid. J Bacteriol. 183:3417–3427.
   PubMed Web of Science ®Google Scholar
• Dinan TG, Cryan JF. 2017. Gut-brain axis in 2016: brain-gut-microbiota axis – mood, metabolism and behaviour. Nat Rev Gastroenterol Hepatol. 14:69–70.
   PubMed Web of Science ®Google Scholar
• Dobkin JF, Saha JR, Butler VP, Neu HC, Lindenbaum J. 1983. Digoxin-inactivating bacteria – identification in human gut flora. Science. 220:325–327.
   PubMed Web of Science ®Google Scholar
• El Aidy S, van den Bogert B, Kleerebezem M. 2015. The small intestine microbiota, nutritional modulation and relevance for health. Curr Opin Biotechnol. 32:14–20.
   PubMed Web of Science ®Google Scholar
• Elmer GW, Remmel RP. 1984. Role of the intestinal microflora in clonazepam metabolism in the rat. Xenobiotica. 14:829–840.
   PubMed Web of Science ®Google Scholar
• Fiddian-Green RG. 2007. Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations. Neurology. 68:1085.
   PubMed Web of Science ®Google Scholar
• Fu ZD, Cui JY. 2017. Remote sensing between liver and intestine: importance of microbial metabolites. Curr Pharmacol Rep. 3:101–113.
   PubMedGoogle Scholar
• Gadaleta RM, Cariello M, Sabba C, Moschetta A. 2015. Tissue-specific actions of FXR in metabolism and cancer. Biochim Biophys Acta. 1851:30–39.
   PubMed Web of Science ®Google Scholar
• Gandhi S, Fleet JL, Bailey DG, McArthur E, Wald R, Rehman F, Garg AX. 2013. Calcium-channel blocker-clarithromycin drug interactions and acute kidney injury. JAMA. 310:2544–2553.
   PubMed Web of Science ®Google Scholar
• Gingell R, Bridges JW, Williams RT. 1971. The role of the gut flora in the metabolism of prontosil and neoprontosil in the rat. Xenobiotica. 1:143–156.
   PubMedGoogle Scholar
• Goldin BR, Peppercorn MA, Goldman P. 1973. Contributions of host and intestinal microflora in the metabolism of l-dopa by the rat. J Pharmacol Exp Ther. 186:160–166.
   PubMed Web of Science ®Google Scholar
• Haiser HJ, Gootenberg DB, Chatman K, Sirasani G, Balskus EP, Turnbaugh PJ. 2013. Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science. 341:295–298.
   PubMed Web of Science ®Google Scholar
• Haiser HJ, Turnbaugh PJ. 2012. Is it time for a metagenomic basis of therapeutics? Science. 336:1253–1255.
   PubMed Web of Science ®Google Scholar
• Haiser HJ, Turnbaugh PJ. 2013. Developing a metagenomic view of xenobiotic metabolism. Pharmacol Res. 69:21–31.
   PubMed Web of Science ®Google Scholar
• Hashim H, Azmin S, Razlan H, Yahya NW, Tan HJ, Manaf MR, Ibrahim NM. 2014. Eradication of Helicobacter pylori infection improves levodopa action, clinical symptoms and quality of life in patients with Parkinson's disease. PLoS One. 9:e112330.
   PubMed Web of Science ®Google Scholar
• Holt R. 1967. The bacterial degradation of chloramphenicol. Lancet. 1:1259–1260.
   PubMed Web of Science ®Google Scholar
• Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, et al. 2004. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 350:2335–2342.
   PubMed Web of Science ®Google Scholar
• Ishii M, Toda T, Ikarashi N, Ochiai W, Sugiyama K. 2012. Effects of intestinal flora on the expression of cytochrome P450 3A in the liver. Yakugaku Zasshi. 132:301–310.
   PubMed Web of Science ®Google Scholar
• Jourová L, Anzenbacher P, Lišková B, Matušková Z, Hermanová P, Hudcovic T, Kozáková H, Hrnčířová L, Anzenbacherová E. 2017. Colonization by non-pathogenic bacteria alters mRNA expression of cytochromes P450 in originally germ-free mice. Folia Microbiol (Praha). 62:463–469.
   PubMed Web of Science ®Google Scholar
• Kaddurah-Daouk R, Baillie RA, Zhu H, Zeng ZB, Wiest MM, Nguyen UT, Wojnoonski K, Watkins SM, Trupp M, Krauss RM. 2011. Enteric microbiome metabolites correlate with response to simvastatin treatment. PLoS One. 6:e25482.
   PubMed Web of Science ®Google Scholar
• Kim D. 2015. Gut microbiota-mediated drug-antibiotic interactions. Drug Metab Dispos. 43:1581–1589.
   PubMed Web of Science ®Google Scholar
• Kim I, Yoo D, Jung I, Lim S, Jeong J, Kim K, Bae O, Yoo H, Kim D. 2016. Reduced metabolic activity of gut microbiota by antibiotics can potentiate the antithrombotic effect of aspirin. Biochem Pharmacol. 122:72–79.
   PubMed Web of Science ®Google Scholar
• Kitamura S, Sugihara K, Kuwasako M, Tatsumi K. 1997. The role of mammalian intestinal bacteria in the reductive metabolism of zonisamide. J Pharm Pharmacol. 49:253–256.
   PubMed Web of Science ®Google Scholar
• Klotz U, Schwab M. 2005. Topical delivery of therapeutic agents in the treatment of inflammatory bowel disease. Adv Drug Deliv Rev. 57:267–279.
   PubMed Web of Science ®Google Scholar
• Koch RL, Chrystal EJ, Beaulieu BB Jr, Goldman P. 1979. Acetamide – a metabolite of metronidazole formed by the intestinal flora. Biochem Pharmacol. 28:3611–3615.
   PubMed Web of Science ®Google Scholar
• Koch RL, Goldman P. 1979. The anaerobic metabolism of metronidazole forms N-(2-hydroxyethyl)-oxamic acid. J Pharmacol Exp Ther. 208:406–410.
   PubMed Web of Science ®Google Scholar
• Kundu P, Blacher E, Elinav E, Pettersson S. 2017. Our gut microbiome: the evolving inner self. Cell. 171:1481–1493.
   PubMed Web of Science ®Google Scholar
• Lavrijsen K, van Dyck D, van Houdt J, Hendrickx J, Monbaliu J, Woestenborghs R, Meuldermans W, Heykants J. 1995. Reduction of the prodrug loperamide oxide to its active drug loperamide in the gut of rats, dogs, and humans. Drug Metab Dispos. 23:354–362.
   PubMed Web of Science ®Google Scholar
• Lee WY, Yoon WT, Shin HY, Jeon SH, Rhee PL. 2008. Helicobacter pylori infection and motor fluctuations in patients with Parkinson's disease. Mov Disord. 23:1696–1700.
   PubMed Web of Science ®Google Scholar
• Lindenbaum J, Rund DG, Butler VP Jr, Tse-Eng D, Saha JR. 1981. Inactivation of digoxin by the gut flora: reversal by antibiotic therapy. N Engl J Med. 305:789–794.
   PubMed Web of Science ®Google Scholar
• Lindenbaum J, Tse-Eng D, Butler VP Jr, Rund DG. 1981. Urinary excretion of reduced metabolites of digoxin. Am J Med. 71:67–74.
   PubMed Web of Science ®Google Scholar
• Matuskova Z, Anzenbacherova E, Vecera R, Tlaskalova-Hogenova H, Kolar M, Anzenbacher P. 2014. Administration of a probiotic can change drug pharmacokinetics: effect of E. coli Nissle 1917 on amidarone absorption in rats. PLoS One. 9:e87150.
   PubMed Web of Science ®Google Scholar
• McCabe M, Sane RS, Keith-Luzzi M, Xu J, King I, Whitcher-Johnstone A, Johnstone N, Tweedie DJ, Li Y. 2015. Defining the role of gut bacteria in the metabolism of Deleobuvir: in vitro and in vivo studies. Drug Metab Dispos. 43:1612–1618.
   PubMed Web of Science ®Google Scholar
• Meuldermans W, Hendrickx J, Mannens G, Lavrijsen K, Janssen C, Bracke J, Le Jeune L, Lauwers W, Heykants J. 1994. The metabolism and excretion of risperidone after oral administration in rats and dogs. Drug Metab Dispos. 22:129–138.
   PubMed Web of Science ®Google Scholar
• Noh K, Kang Y, Nepal MR, Jeong KS, Oh DG, Kang MJ, Lee S, Kang W, Jeong HG, Jeong TC. 2016. Role of intestinal microbiota in baicalin-induced drug interaction and its pharmacokinetics. Molecules. 21:337.
   PubMed Web of Science ®Google Scholar
• Okuda H, Nishiyama T, Ogura K, Nagayama S, Ikeda K, Yamaguchi S, Nakamura Y, Kawaguchi Y, Watabe T. 1997. Lethal drug interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. Drug Metab Dispos. 25:270–273.
   Web of Science ®Google Scholar
• Okuda H, Ogura K, Kato A, Takubo H, Watabe T. 1998. A possible mechanism of eighteen patient deaths caused by interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. J Pharmacol Exp Ther. 287:791–799.
   PubMed Web of Science ®Google Scholar
• Peppercorn MA, Goldman P. 1972. The role of intestinal bacteria in the metabolism of salicylazosulfapyridine. J Pharmacol Exp Ther. 181:555–562.
   PubMed Web of Science ®Google Scholar
• Pierantozzi M, Pietroiusti A, Brusa L, Galati S, Stefani A, Lunardi G, Fedele E, Sancesario G, Bernardi G, Bergamaschi A, et al. 2006. Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations. Neurology. 66:1824–1829.
   PubMed Web of Science ®Google Scholar
• Pierantozzi M, Pietroiusti A, Galante A, Sancesario G, Lunardi G, Fedele E, Giacomini P, Stanzione P. 2001. Helicobacter pylori-induced reduction of acute levodopa absorption in Parkinson's disease patients. Ann Neurol. 50:686–687.
   PubMed Web of Science ®Google Scholar
• Pollet RM, D'Agostino EH, Walton WG, Xu Y, Little MS, Biernat KA, Pellock SJ, Patterson LM, Creekmore BC, Isenberg HN, et al. 2017. An atlas of beta-glucuronidases in the human intestinal microbiome. Structure. 25:967.
   PubMed Web of Science ®Google Scholar
• Prieto I, Hidalgo M, Segarra AB, Martinez-Rodriguez AM, Cobo A, Ramirez M, Abriouel H, Galvez A, Martinez CM. 2018. Influence of a diet enriched with virgin olive oil or butter on mouse gut microbiota and its correlation to physiological and biochemical parameters related to metabolic syndrome. PLoS One. 13:e0190368.
   PubMed Web of Science ®Google Scholar
• Rafii F, Cerniglia CE. 1995. Reduction of azo dyes and nitroaromatic compounds by bacterial enzymes from the human intestinal tract. Environ Health Perspect. 103:17–19.
   PubMed Web of Science ®Google Scholar
• Rafii F, Sutherland JB, Hansen EB Jr, Cerniglia CE. 1997. Reduction of nitrazepam by Clostridium leptum, a nitroreductase-producing bacterium isolated from the human intestinal tract. Clin Infect Dis. 25:S121–S122.
   PubMed Web of Science ®Google Scholar
• Roberts AB, Wallace BD, Venkatesh MK, Mani S, Redinbo MR. 2013. Molecular insights into microbial β-glucuronidase inhibition to abrogate CPT-11 toxicity. Mol Pharmacol. 84:208–217.
   PubMed Web of Science ®Google Scholar
• Sahota SS, Bramley PM, Menzies IS. 1982. The fermentation of lactulose by colonic bacteria. J Gen Microbiol. 128:319–325.
   PubMedGoogle Scholar
• Saitta KS, Zhang C, Lee KK, Fujimoto K, Redinbo MR, Boelsterli UA. 2014. Bacterial β-glucuronidase inhibition protects mice against enteropathy induced by indomethacin, ketoprofen or diclofenac: mode of action and pharmacokinetics. Xenobiotica. 44:28–35.
   PubMed Web of Science ®Google Scholar
• Sandler M, Karoum F, Ruthven CR, Calne DB. 1969. m-Hydroxyphenylacetic acid formation from l-dopa in man: suppression by neomycin. Science. 166:1417–1418.
   PubMed Web of Science ®Google Scholar
• Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. 2013. The influence of diet on the gut microbiota. Pharmacol Res. 69:52–60.
   PubMed Web of Science ®Google Scholar
• Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS, Bae JW. 2014. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 63:727–735.
   PubMed Web of Science ®Google Scholar
• Shu YZ, Kingston DG, Van Tassell RL, Wilkins TD. 1991. Metabolism of levamisole, an anti-colon cancer drug, by human intestinal bacteria. Xenobiotica. 21:737–750.
   PubMed Web of Science ®Google Scholar
• Sousa T, Paterson R, Moore V, Carlsson A, Abrahamsson B, Basit AW. 2008. The gastrointestinal microbiota as a site for the biotransformation of drugs. Int J Pharm. 363:1–25.
   PubMed Web of Science ®Google Scholar
• Sousa T, Yadav V, Zann V, Borde A, Abrahamsson B, Basit AW. 2014. On the colonic bacterial metabolism of azo-bonded prodrugs of 5-aminosalicylic acid. J Pharm Sci. 103:3171–3175.
   PubMed Web of Science ®Google Scholar
• Spanogiannopoulos P, Bess EN, Carmody RN, Turnbaugh PJ. 2016. The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat Rev Microbiol. 14:273–287.
   PubMed Web of Science ®Google Scholar
• Swanson HI. 2015. Drug metabolism by the host and gut microbiota: a partnership or rivalry? Drug Metab Dispos. 43:1499–1504.
   PubMed Web of Science ®Google Scholar
• Takeno S, Hirano Y, Kitamura A, Sakai T. 1993. Comparative developmental toxicity and metabolism of nitrazepam in rats and mice. Toxicol Appl Pharmacol. 121:233–238.
   PubMed Web of Science ®Google Scholar
• Takeno S, Sakai T. 1991. Involvement of the intestinal microflora in nitrazepam-induced teratogenicity in rats and its relationship to nitroreduction. Teratology. 44:209–214.
   PubMedGoogle Scholar
• Tozaki H, Emi Y, Horisaka E, Fujita T, Yamamoto A, Muranishi S. 1997. Degradation of insulin and calcitonin and their protection by various protease inhibitors in rat caecal contents: Implications in peptide delivery to the colon. J Pharm Pharmacol. 49:164–168.
   PubMed Web of Science ®Google Scholar
• Tremaroli V, Backhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature. 489:242–249.
   PubMed Web of Science ®Google Scholar
• Vétizou M, Pitt JM, Daillère R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CPM, et al. 2015. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 350:1079–1084.
   PubMed Web of Science ®Google Scholar
• Wadworth AN, Fitton A. 1991. Olsalazine. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic potential in inflammatory bowel disease. Drugs. 41:647–664.
   PubMed Web of Science ®Google Scholar
• Wallace BD, Roberts AB, Pollet RM, Ingle JD, Biernat KA, Pellock SJ, Venkatesh MK, Guthrie L, O'Neal SK, Robinson SJ, et al. 2015. Structure and inhibition of microbiome β-glucuronidases essential to the alleviation of cancer drug toxicity. Chem Biol. 22:1238–1249.
   PubMedGoogle Scholar
• Wallace BD, Wang H, Lane KT, Scott JE, Orans J, Koo JS, Venkatesh M, Jobin C, Yeh LA, Mani S, et al. 2010. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science. 330:831–835.
   PubMed Web of Science ®Google Scholar
• Walsh CT, Levine RR. 1975. Studies of the enterohepatic circulation of morphine in the rat. J Pharmacol Exp Ther. 195:303–310.
   PubMed Web of Science ®Google Scholar
• Watanabe K, Yamashita S, Furuno K, Kawasaki H, Gomita Y. 1995. Metabolism of omeprazole by gut flora in rats. J Pharm Sci. 84:516–517.
   PubMed Web of Science ®Google Scholar
• Yoo DH, Kim IS, Le TKV, Jung IH, Yoo HH, Kim DH. 2014. Gut microbiota-mediated drug interactions between lovastatin and antibiotics. Drug Metab Dispos. 42:1508–1513.
   PubMed Web of Science ®Google Scholar
• Yoo HH, Kim IS, Yoo DH, Kim DH. 2016. Effects of orally administered antibiotics on the bioavailability of amlodipine: gut microbiota-mediated drug interaction. J Hypertens. 34:156–162.
   PubMed Web of Science ®Google Scholar