Abstract
Background: Modern features of drug development such as low permeability, low solubility, and improved release affect the interplay of the gut microbiota and drug metabolism. In recent years, studies have established the impact of plateau hypoxia on gut microbiota, where drug use by plateau populations is affected by hypoxia- induced changes in intestinal microflora-mediated drug metabolism.
Methods: In this review, we summarized the effects of gut microbiota on drug metabolism, and of plateau hypoxia on the intestinal flora, with the aim of providing guidance for the rational use of drugs in high-altitude populations.
Results: The evidence clearly shows that alterations in gut microbiota can affect pro-drug activation, drug inactivation, and the biotransformation of xenobiotics. Additionally, plateau hypoxia alters drug metabolism by affecting intestinal flora.
Conclusion: This review provides an overview of the effects of gut microbiota on drug metabolism and provides guidance for rational drug use under hypoxic conditions at high altitudes.
Keywords: Drug metabolism, gut microbiota, plateau hypoxia, bioavailability, xenobiotics, rational drug use.
Graphical Abstract
[1]
Backhed, F.; Ley, R.E.; Sonnenburg, J.L.; Peterson, D.A.; Gordon, J.I. Host-bacterial mutualism in the human intestine. Science, 2005, 307(5717), 1915-1920.
[2]
Choi, M.S.; Yu, J.S.; Yoo, H.H.; Kim, D.H. The role of gut microbiota in the pharmacokinetics of antihypertensive drugs. Pharmacol. Res., 2018, 130, 164-171.
[3]
Sommer, F.; Backhed, F. The gut microbiota--masters of host development and physiology. Nat. Rev. Microbiol., 2013, 11(4), 227-238.
[4]
Liang, D.; Leung, R.K.; Guan, W.; Au, W.W. Involvement of gut microbiome in human health and disease: brief overview, knowledge gaps and research opportunities. Gut Pathog., 2018, 10, 3.
[5]
Walsh, J.; Griffin, B.T.; Clarke, G.; Hyland, N.P. Drug-gut microbiota interactions: Implications for neuropharmacology. Br. J. Pharmacol., 2018, 175(24), 4415-4429.
[6]
Goldin, B.R. Intestinal microflora: Metabolism of drugs and carcinogens. Ann. Med., 1990, 22(1), 43-48.
[7]
Sousa, T.; Paterson, R.; Moore, V.; Carlsson, A.; Abrahamsson, B.; Basit, A.W. The gastrointestinal microbiota as a site for the biotransformation of drugs. Int. J. Pharm., 2008, 363(1-2), 1-25.
[8]
Koppel, N.; Maini Rekdal, V.; Balskus, E.P. Chemical transformation of xenobiotics by the human gut microbiota. Science, 2017, 356(6344), 1246-1257.
[9]
Scarpellini, E.; Ianiro, G.; Attili, F.; Bassanelli, C.; De Santis, A.; Gasbarrini, A. The human gut microbiota and virome: Potential therapeutic implications. Dig. Liver Dis., 2015, 47(12), 1007-1012.
[10]
Voigt, R.M.; Forsyth, C.B.; Green, S.J.; Mutlu, E.; Engen, P.; Vitaterna, M.H.; Turek, F.W.; Keshavarzian, A. Circadian disorganization alters intestinal microbiota. PLoS One, 2014, 9(5), e97500.
[11]
Enright, E.F.; Gahan, C.G.; Joyce, S.A.; Griffin, B.T. The impact of the gut microbiota on drug metabolism and clinical outcome. Yale J. Biol. Med., 2016, 89(3), 375-382.
[12]
Yang, W.H.; Zhang, F.X. Changes of intestinal flora microecology in model rats of radical plateau. Chin. J. Gastroenterol. Hepatol., 2010, 19(6), 543-545.
[13]
Jia, W.; Xie, G.; Jia, W. Bile acid-microbiota crosstalk in gastrointestinal inflammation and carcinogenesis. Nat. Rev. Gastroenterol. Hepatol., 2018, 15(2), 111-128.
[14]
Zhang, J.; Chen, Y.; Sun, Y.; Wang, R.; Zhang, J.; Jia, Z. Plateau hypoxia attenuates the metabolic activity of intestinal flora to enhance the bioavailability of nifedipine. Drug Deliv., 2018, 25(1), 1175-1181.
[15]
Basit, A.W.; Lacey, L.F. Colonic metabolism of ranitidine: Implications for its delivery and absorption. Int. J. Pharm., 2001, 227(1-2), 157-165.
[16]
Swanson, H.I. Drug metabolism by the host and gut microbiota: a partnership or rivalry? Drug Metab. Dispos., 2015, 43(10), 1499-1504.
[17]
Dogra, S.; Sakwinska, O.; Soh, S.E.; Ngom-Bru, C.; Bruck, W.M.; Berger, B.; Brussow, H.; Lee, Y.S.; Yap, F.; Chong, Y.S.; Godfrey, K.M.; Holbrook, J.D.; Group, G.S. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. MBio, 2015, 6(1), 312-314.
[18]
Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P.; Heath, A.C.; Warner, B.; Reeder, J.; Kuczynski, J.; Caporaso, J.G.; Lozupone, C.A.; Lauber, C.; Clemente, J.C.; Knights, D.; Knight, R.; Gordon, J.I. Human gut microbiome viewed across age and geography. Nature, 2012, 486(7402), 222-227.
[19]
Franzosa, E.A.; Huang, K.; Meadow, J.F.; Gevers, D.; Lemon, K.P.; Bohannan, B.J.M.; Huttenhower, C. Identifying personal microbiomes using metagenomic codes. Proc. Natl. Acad. Sci. USA, 2015, 112(22), E2930-E2938.
[20]
Conlon, M.A.; Bird, A.R. The impact of diet and lifestyle on gut microbiota and human health. Nutrients, 2015, 7(1), 17-44.
[21]
Shen, W.; Gaskins, H.R.; McIntosh, M.K. Influence of dietary fat on intestinal microbes, inflammation, barrier function and metabolic outcomes. J. Nutr. Biochem., 2014, 25(3), 270-280.
[22]
Jiang, J.K.; Hang, X.M.; Zhang, M.; Liu, X.L.; Li, D.T.; Yang, H. Diversity of bile salt hydrolase activities in different lactobacilli toward human bile salts. Ann. Microbiol., 2010, 60(1), 81-88.
[23]
Hill, M.J.; Drasar, B.S. Degradation of bile salts by human intestinal bacteria. Gut, 1968, 9(1), 22-27.
[24]
Aries, V.; Crowther, J.S.; Drasar, B.S.; Hill, M.J. Degradation of bile salts by human intestinal bacteria. Gut, 1969, 10(7), 575-576.
[25]
Tremaroli, V.; Backhed, F. Functional interactions between the gut microbiota and host metabolism. Nature, 2012, 489(7415), 242-249.
[26]
El Aidy, S.; van den Bogert, B.; Kleerebezem, M. The small intestine microbiota, nutritional modulation and relevance for health. Curr. Opin. Biotechnol., 2015, 32, 14-20.
[27]
Zhang, J.; Zhang, J.; Wang, R. Gut microbiota modulates drug pharmacokinetics. Drug Metab. Rev., 2018, 50(3), 357-368.
[29]
Goldin, B.R.; Peppercorn, M.A.; Goldman, P. Contributions of host and intestinal microflora in the metabolism of L-dopa by the rat. J. Pharmacol. Exp. Ther., 1973, 186(1), 160-166.
[30]
Caldwell, J.; Hawksworth, G.M. The demethylation of methamphetamine by intestinal microflora. J. Pharm. Pharmacol., 1973, 25(5), 422-424.
[31]
Smith, G.E.; Griffiths, L.A. Metabolism of N-acylated and O-alkylated drugs by the intestinal microflora during anaerobic incubation in vitro. Xenobiotica, 1974, 4(8), 477-487.
[32]
Walsh, C.T.; Levine, R.R. Studies of the enterohepatic circulation of morphine in the rat. J. Pharmacol. Exp. Ther., 1975, 195(2), 303-310.
[33]
Gingell, R.; Bridges, J.W.; Williams, R.T. The role of the gut flora in the metabolism of prontosil and neoprontosil in the rat. Xenobiotica, 1971, 1(2), 143-156.
[34]
Peppercorn, M.A.; Goldman, P. The role of intestinal bacteria in the metabolism of salicylazosulfapyridine. J. Pharmacol. Exp. Ther., 1972, 181(3), 555-562.
[35]
Chan, R.P.; Pope, D.J.; Gilbert, A.P.; Sacra, P.J.; Baron, J.H.; Lennard-Jones, J.E. Studies of two novel sulfasalazine analogs, ipsalazide and balsalazide. Dig. Dis. Sci., 1983, 28(7), 609-615.
[36]
Wadworth, A.N.; Fitton, A. Olsalazine. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic potential in inflammatory bowel disease. Drugs, 1991, 41(4), 647-664.
[37]
Koch, R.L.; Chrystal, E.J.; Beaulieu, B.B., Jr; Goldman, P. Acetamide-a metabolite of metronidazole formed by the intestinal flora. Biochem. Pharmacol., 1979, 28(24), 3611-3615.
[38]
Volp, R.F.; Lage, G.L. The fate of a major biliary metabolite of digitoxin in the rat intestine. Drug Metab. Dispos., 1978, 6(4), 418-424.
[39]
Koch, R.L.; Beaulieu, B.B., Jr; Goldman, P. Role of the intestinal flora in the metabolism of misonidazole. Biochem. Pharmacol., 1980, 29(24), 3281-3284.
[40]
Sahota, S.S.; Bramley, P.M.; Menzies, I.S. The fermentation of lactulose by colonic bacteria. J. Gen. Microbiol., 1982, 128(2), 319-325.
[41]
Elmer, G.W.; Remmel, R.P. Role of the intestinal microflora in clonazepam metabolism in the rat. Xenobiotica, 1984, 14(11), 829-840.
[42]
Strong, H.A.; Renwick, A.G.; George, C.F.; Liu, Y.F.; Hill, M.J. The reduction of sulphinpyrazone and sulindac by intestinal bacteria. Xenobiotica, 1987, 17(6), 685-696.
[43]
Shu, Y.Z.; Kingston, D.G.; Van Tassell, R.L.; Wilkins, T.D. Metabolism of levamisole, an anti-colon cancer drug, by human intestinal bacteria. Xenobiotica, 1991, 21(6), 737-750.
[44]
Watanabe, K.; Yamashita, S.; Furuno, K.; Kawasaki, H.; Gomita, Y. Metabolism of omeprazole by gut flora in rats. J. Pharm. Sci., 1995, 84(4), 516-517.
[45]
Delomenie, C.; Fouix, S.; Longuemaux, S.; Brahimi, N.; Bizet, C.; Picard, B.; Denamur, E.; Dupret, J.M. Identification and functional characterization of arylamine N-acetyltransferases in eubacteria: evidence for highly selective acetylation of 5-aminosalicylic acid. J. Bacteriol., 2001, 183(11), 3417-3427.
[46]
Rafii, F.; Sutherland, J.B.; Hansen, E.B., Jr; Cerniglia, C.E. Reduction of nitrazepam by Clostridium leptum, a nitroreductase-producing bacterium isolated from the human intestinal tract. Clin. Infect. Dis., 1997, 25(Suppl. 2), S121-S122.
[47]
Haiser, H.J.; Turnbaugh, P.J. Developing a metagenomic view of xenobiotic metabolism. Pharmacol. Res., 2013, 69(1), 21-31.
[48]
Meuldermans, W.; Hendrickx, J.; Mannens, G.; Lavrijsen, K.; Janssen, C.; Bracke, J.; Le Jeune, L.; Lauwers, W.; Heykants, J. The metabolism and excretion of risperidone after oral administration in rats and dogs. Drug Metab. Dispos., 1994, 22(1), 129-138.
[49]
Kitamura, S.; Sugihara, K.; Kuwasako, M.; Tatsumi, K. The role of mammalian intestinal bacteria in the reductive metabolism of zonisamide. J. Pharm. Pharmacol., 1997, 49(3), 253-256.
[50]
Tozaki, H.; Emi, Y.; Horisaka, E.; Fujita, T.; Yamamoto, A.; Muranishi, S. 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., 1997, 49(2), 164-168.
[51]
Okuda, H.; Ogura, K.; Kato, A.; Takubo, H.; Watabe, T. 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., 1998, 287(2), 791-799.
[52]
Clayton, T.A.; Baker, D.; Lindon, J.C.; Everett, J.R.; Nicholson, J.K. Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc. Natl. Acad. Sci. USA, 2009, 106(34), 14728-14733.
[53]
Roberts, A.B.; Wallace, B.D.; Venkatesh, M.K.; Mani, S.; Redinbo, M.R. Molecular insights into microbial beta-glucuronidase inhibition to abrogate CPT-11 toxicity. Mol. Pharmacol., 2013, 84(2), 208-217.
[54]
Curro, D. The role of gut microbiota in the modulation of drug action: a focus on some clinically significant issues. Expert Rev. Clin. Pharmacol., 2018, 11(2), 171-183.
[55]
Saitta, K.S.; Zhang, C.; Lee, K.K.; Fujimoto, K.; Redinbo, M.R.; Boelsterli, U.A. Bacterial beta-glucuronidase inhibition protects mice against enteropathy induced by indomethacin, ketoprofen or diclofenac: mode of action and pharmacokinetics. Xenobiotica, 2014, 44(1), 28-35.
[56]
Basit, A.W.; Newton, J.M.; Lacey, L.F. Susceptibility of the H2-receptor antagonists cimetidine, famotidine and nizatidine, to metabolism by the gastrointestinal microflora. Int. J. Pharm., 2002, 237(1-2), 23-33.
[57]
Kaddurah-Daouk, R.; Baillie, R.A.; Zhu, H.; Zeng, Z.B.; Wiest, M.M.; Nguyen, U.T.; Wojnoonski, K.; Watkins, S.M.; Trupp, M.; Krauss, R.M. Enteric microbiome metabolites correlate with response to simvastatin treatment. PLoS One, 2011, 6(10), e25482.
[58]
Kim, I.; Yoo, D.; Jung, I.; Lim, S.; Jeong, J.; Kim, K.; Bae, O.; Yoo, H.; Kim, D. Reduced metabolic activity of gut microbiota by antibiotics can potentiate the antithrombotic effect of aspirin. Biochem. Pharmacol., 2016, 122, 72-79.
[59]
Yoo, H.H.; Kim, I.S.; Yoo, D.H.; Kim, D.H. Effects of orally administered antibiotics on the bioavailability of amlodipine: Gut microbiota-mediated drug interaction. J. Hypertens., 2016, 34(1), 156-162.
[60]
Yoo, D.H.; Kim, I.S.; Le, T.K.V.; Jung, I.H.; Yoo, H.H.; Kim, D.H. Gut microbiota-mediated drug interactions between lovastatin and antibiotics. Drug Metab. Dispos., 2014, 42(9), 1508-1513.
[61]
Braune, A.; Blaut, M. Deglycosylation of puerarin and other aromatic C-glucosides by a newly isolated human intestinal bacterium. Environ. Microbiol., 2011, 13(2), 482-494.
[62]
Kim, D.H.; Yu, K.U.; Bae, E.A.; Han, M.J. Metabolism of puerarin and daidzin by human intestinal bacteria and their relation to in vitro cytotoxicity. Biol. Pharm. Bull., 1998, 21(6), 628-630.
[63]
Noh, K.; Kang, Y.; Nepal, M.R.; Jeong, K.S.; Oh, D.G.; Kang, M.J.; Lee, S.; Kang, W.; Jeong, H.G.; Jeong, T.C. Role of intestinal microbiota in baicalin-induced drug interaction and its pharmacokinetics. Molecules, 2016, 21(3), 337.
[64]
Jaganath, I.B.; Mullen, W.; Edwards, C.A.; Crozier, A. The relative contribution of the small and large intestine to the absorption and metabolism of rutin in man. Free Radic. Res., 2006, 40(10), 1035-1046.
[65]
Silvestro, L.; Tarcomnicu, I.; Dulea, C.; Attili, N.R.B.N.; Ciuca, V.; Peru, D.; Savu, S.R. Confirmation of diosmetin 3-O-glucuronide as major metabolite of diosmin in humans, using micro-liquid-chromatography-mass spectrometry and ion mobility mass spectrometry. Anal. Bioanal. Chem., 2013, 405(25), 8295-8310.
[66]
Spanogiannopoulos, P.; Bess, E.N.; Carmody, R.N.; Turnbaugh, P.J. The microbial pharmacists within us: A metagenomic view of xenobiotic metabolism. Nat. Rev. Microbiol., 2016, 14(5), 273-287.
[67]
Wallace, B.D.; Wang, H.W.; Lane, K.T.; Scott, J.E.; Orans, J.; Koo, J.S.; Venkatesh, M.; Jobin, C.; Yeh, L.A.; Mani, S.; Redinbo, M.R. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science, 2010, 330(6005), 831-835.
[68]
Takeno, S.; Hirano, Y.; Kitamura, A.; Sakai, T. Comparative developmental toxicity and metabolism of nitrazepam in rats and mice. Toxicol. Appl. Pharmacol., 1993, 121(2), 233-238.
[69]
Okuda, H.; Nishiyama, T.; Ogura, K.; Nagayama, S.; Ikeda, K.; Yamaguchi, S.; Nakamura, Y.; Kawaguchi, Y.; Watabe, T. Lethal drug interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. Drug Metab. Dispos., 1997, 25(5), 270-273.
[70]
Vetizou, M.; Pitt, J.M.; Daillere, R.; Lepage, P.; Waldschmitt, N.; Flament, C.; Rusakiewicz, S.; Routy, B.; Roberti, M.P.; Duong, C.P.; Poirier-Colame, V.; Roux, A.; Becharef, S.; Formenti, S.; Golden, E.; Cording, S.; Eberl, G.; Schlitzer, A.; Ginhoux, F.; Mani, S.; Yamazaki, T.; Jacquelot, N.; Enot, D.P.; Berard, M.; Nigou, J.; Opolon, P.; Eggermont, A.; Woerther, P.L.; Chachaty, E.; Chaput, N.; Robert, C.; Mateus, C.; Kroemer, G.; Raoult, D.; Boneca, I.G.; Carbonnel, F.; Chamaillard, M.; Zitvogel, L. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science, 2015, 350(6264), 1079-1084.
[71]
Shin, N.R.; Lee, J.C.; Lee, H.Y.; Kim, M.S.; Whon, T.W.; Lee, M.S.; Bae, J.W. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut, 2014, 63(5), 727-735.
[72]
Noh, K.; Kang, Y.R.; Nepal, M.R.; Shakya, R.; Kang, M.J.; Kang, W.; Lee, S.; Jeong, H.G.; Jeong, T.C. Impact of gut microbiota on drug metabolism: an update for safe and effective use of drugs. Arch. Pharm. Res., 2017, 40(12), 1345-1355.
[73]
de Lannoy, I.A.; Silverman, M. The MDR1 gene product, P-glycoprotein, mediates the transport of the cardiac glycoside, digoxin. Biochem. Biophys. Res. Commun., 1992, 189(1), 551-557.
[74]
Dobkin, J.F.; Saha, J.R.; Butler, V.P.; Neu, H.C.; Lindenbaum, J. Digoxin-inactivating bacteria - identification in human gut flora. Science, 1983, 220(4594), 325-327.
[75]
Lindenbaum, J.; Rund, D.G.; Butler, V.P.; Tseeng, D.; Saha, J.R. Inactivation of digoxin by the gut flora - reversal by antibiotic-therapy. N. Engl. J. Med., 1981, 305(14), 789-794.
[76]
Haiser, H.J.; Gootenberg, D.B.; Chatman, K.; Sirasani, G.; Balskus, E.P.; Turnbaugh, P.J. Predicting and manipulating cardiac drug inactivation by the human gut bacterium eggerthella lenta. Science, 2013, 341(6143), 295-298.
[77]
Kumar, K.; Jaiswal, S.K.; Dhoke, G.V.; Srivastava, G.N.; Sharma, A.K.; Sharma, V.K. Mechanistic and structural insight into promiscuity based metabolism of cardiac drug digoxin by gut microbial enzyme. J. Cell. Biochem., 2018, 119(7), 5287-5296.
[78]
Pollet, R.M.; D’Agostino, E.H.; Walton, W.G.; Xu, Y.M.; Little, M.S.; Biernat, K.A.; Pellock, S.J.; Patterson, L.M.; Creekmore, B.C.; Isenberg, H.N.; Bahethi, R.R.; Bhatt, A.P.; Liu, J.; Gharaibeh, R.Z.; Redinbo, M.R. An atlas of beta-glucuronidases in the human intestinal microbiome. Structure, 2017, 25(7), 967.
[79]
Stringer, A.M.; Gibson, R.J.; Logan, R.M.; Bowen, J.M.; Yeoh, A.S.; Keefe, D.M. Faecal microflora and beta-glucuronidase expression are altered in an irinotecan-induced diarrhea model in rats. Cancer Biol. Ther., 2008, 7(12), 1919-1925.
[80]
Wallace, B.D.; Wang, H.; Lane, K.T.; Scott, J.E.; Orans, J.; Koo, J.S.; Venkatesh, M.; Jobin, C.; Yeh, L.A.; Mani, S.; Redinbo, M.R. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme. Science, 2010, 330(6005), 831-835.
[81]
Hurwitz, H.; Fehrenbacher, L.; Novotny, W.; Cartwright, T.; Hainsworth, J.; Heim, W.; Berlin, J.; Baron, A.; Griffing, S.; Holmgren, E.; Ferrara, N.; Fyfe, G.; Rogers, B.; Ross, R.; Kabbinavar, F. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med., 2004, 350(23), 2335-2342.
[82]
Wallace, B.D.; Roberts, A.B.; Pollet, R.M.; Ingle, J.D.; Biernat, K.A.; Pellock, S.J.; Venkatesh, M.K.; Guthrie, L.; O’Neal, S.K.; Robinson, S.J.; Dollinger, M.; Figueroa, E.; McShane, S.R.; Cohen, R.D.; Jin, J.; Frye, S.V.; Zamboni, W.C.; Pepe-Ranney, C.; Mani, S.; Kelly, L.; Redinbo, M.R. Structure and inhibition of microbiome beta-glucuronidases essential to the alleviation of cancer drug toxicity. Chem. Biol., 2015, 22(9), 1238-1249.
[83]
Koch, R.L.; Goldman, P. The anaerobic metabolism of metronidazole forms N-(2-hydroxyethyl)-oxamic acid. J. Pharmacol. Exp. Ther., 1979, 208(3), 406-410.
[84]
Basit, A.W.; Newton, J.M.; Lacey, L.F. Susceptibility of the H-2-receptor antagonists cimetidine, famotidine and nizatidine, to metabolism by the gastrointestinal microflora. Int. J. Pharm., 2002, 237(1-2), 23-33.
[85]
Cummings, A.J.; King, M.L.; Martin, B.K. A kinetic study of drug elimination: The excretion of paracetamol and its metabolites in man. Br. J. Pharmacol. Chemother., 1967, 29(2), 150-157.
[86]
Clements, J.A.; Heading, R.C.; Nimmo, W.S.; Prescott, L.F. Kinetics of acetaminophen absorption and gastric emptying in man. Clin. Pharmacol. Ther., 1978, 24(4), 420-431.
[87]
Claus, S.P.; Guillou, H.; Ellero-Simatos, S. The gut microbiota: a major player in the toxicity of environmental pollutants? NPJ Biofilms Microbiomes, 2016, 2, 16003.
[88]
Kumano, T.; Fujiki, E.; Hashimoto, Y.; Kobayashi, M. Discovery of a sesamin-metabolizing microorganism and a new enzyme. Proc. Natl. Acad. Sci. USA, 2016, 113(32), 9087-9092.
[89]
Ticak, T.; Kountz, D.J.; Girosky, K.E.; Krzycki, J.A.; Ferguson, D.J., Jr A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase. Proc. Natl. Acad. Sci. USA, 2014, 111(43), E4668-E4676.
[90]
Carter, J.H.; McLafferty, M.A.; Goldman, P. Role of the gastrointestinal microflora in amygdalin (laetrile)-induced cyanide toxicity. Biochem. Pharmacol., 1980, 29(3), 301-304.
[91]
LoGuidice, A.; Wallace, B.D.; Bendel, L.; Redinbo, M.R.; Boelsterli, U.A. Pharmacologic targeting of bacterial beta-glucuronidase alleviates nonsteroidal anti-inflammatory drug-induced enteropathy in mice. J. Pharmacol. Exp. Ther., 2012, 341(2), 447-454.
[92]
Klatt, N.R.; Cheu, R.; Birse, K.; Zevin, A.S.; Perner, M.; Noel-Romas, L.; Grobler, A.; Westmacott, G.; Xie, I.Y.; Butler, J.; Mansoor, L.; McKinnon, L.R.; Passmore, J.A.S.; Karim, Q.A.; Karim, S.S.A.; Burgener, A.D. Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science, 2017, 356(6341), 938-944.
[93]
Lavrijsen, K.; van Dyck, D.; van Houdt, J.; Hendrickx, J.; Monbaliu, J.; Woestenborghs, R.; Meuldermans, W.; Heykants, J. Reduction of the prodrug loperamide oxide to its active drug loperamide in the gut of rats, dogs, and humans. Drug Metab. Dispos., 1995, 23(3), 354-362.
[94]
Maurice, C.F.; Haiser, H.J.; Turnbaugh, P.J. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell, 2013, 152(1-2), 39-50.
[95]
Perez-Cobas, A.E.; Gosalbes, M.J.; Friedrichs, A.; Knecht, H.; Artacho, A.; Eismann, K.; Otto, W.; Rojo, D.; Bargiela, R.; von Bergen, M.; Neulinger, S.C.; Daumer, C.; Heinsen, F.A.; Latorre, A.; Barbas, C.; Seifert, J.; dos Santos, V.M.; Ott, S.J.; Ferrer, M.; Moya, A. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut, 2013, 62(11), 1591-1601.
[96]
Jernberg, C.; Lofmark, S.; Edlund, C.; Jansson, J.K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J., 2007, 1(1), 56-66.
[97]
Dethlefsen, L.; Relman, D.A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl. Acad. Sci. USA, 2011, 108(Suppl. 1), 4554-4561.
[98]
De La Cochetiere, M.F.; Durand, T.; Lepage, P.; Bourreille, A.; Galmiche, J.P.; Dore, J. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J. Clin. Microbiol., 2005, 43(11), 5588-5592.
[99]
Lu, K.; Abo, R.P.; Schlieper, K.A.; Graffam, M.E.; Levine, S.; Wishnok, J.S.; Swenberg, J.A.; Tannenbaum, S.R.; Fox, J.G. Arsenic exposure perturbs the gut Microbiome and its metabolic profile in mice: An integrated metagenomics and metabolomics analysis. Environ. Health Perspect., 2014, 122(3), 284-291.
[100]
Kim, D.H. Gut microbiota-mediated drug-drug interactions. Drug Metab. Pharm., 2017, 32(1), S18-S19.
[101]
Machavaram, K.K.; Gundu, J.; Yamsani, M.R. Effect of ketoconazole and rifampicin on the pharmacokinetics of ranitidine in healthy human volunteers: a possible role of P-glycoprotein. Drug Metabol. Drug Interact., 2006, 22(1), 47-65.
[102]
Prieto, I.; Hidalgo, M.; Segarra, A.B.; Martinez-Rodriguez, A.M.; Cobo, A.; Ramirez, M.; Abriouel, H.; Galvez, A.; Martinez-Canamero, M. 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, 2018, 13(1), e0190368.
[103]
Scott, K.P.; Gratz, S.W.; Sheridan, P.O.; Flint, H.J.; Duncan, S.H. The influence of diet on the gut microbiota. Pharmacol. Res., 2013, 69(1), 52-60.
[104]
Luo, B.F.; Wang, R.; Li, W.B.; Yang, T.; Wang, C.; Lu, H.; Zhao, A.P.; Zhang, J.H.; Jia, Z.P. Pharmacokinetic changes of norfloxacin based on expression of MRP2 after acute exposure to high altitude at 4300 m. Biomed. Pharmacother., 2017, 89, 1078-1085.
[105]
Ritschel, W.A.; Paulos, C.; Arancibia, A.; Agrawal, M.A.; Wetzelsberger, K.M.; Lucker, P.W. Pharmacokinetics of acetazolamide in healthy volunteers after short- and long-term exposure to high altitude. J. Clin. Pharmacol., 1998, 38(6), 533-539.
[106]
Arancibia, A.; Nella Gai, M.; Paulos, C.; Chavez, J.; Pinilla, E.; Angel, N.; Ritschel, W.A. Effects of high altitude exposure on the pharmacokinetics of furosemide in healthy volunteers. Int. J. Clin. Pharmacol. Ther., 2004, 42(6), 314-320.
[107]
Li, X.Y.; Gao, F.; Li, Z.Q.; Guan, W.; Feng, W.L.; Ge, R.L. Comparison of the pharmacokinetics of sulfamethoxazole in male chinese volunteers at low altitude and acute exposure to high altitude versus subjects living chronically at high altitude: An open-label, controlled, prospective study. Clin. Ther., 2009, 31(11), 2744-2754.
[108]
Li, X.Y.; Liu, Y.N.; Wang, X.J.; Zhu, J.B.; Yuan, M.; Li, Y.P.; Li, Y.F. Comparison of the pharmacokinetics of sulfamethoxazole in native Han and Tibetan male Chinese volunteers living at high altitude. Eur. J. Drug Metab. Ph., 2012, 37(4), 263-269.
[109]
Gola, S.; Gupta, A.; Keshri, G.K.; Nath, M.; Velpandian, T. Evaluation of hepatic metabolism and pharmacokinetics of ibuprofen in rats under chronic hypobaric hypoxia for targeted therapy at high altitude. J. Pharmaceut. Biomed., 2016, 121, 114-122.
[110]
Zhang, J.; Wang, R.; Xie, H.; Yin, Q.; Jia, Z.; Li, W. Effect of acute exposure to high altitude on pharmacokinetics of propranolol and metoprolol in rats. Nan Fang Yi Ke Da Xue Xue Bao, 2014, 34(11), 1616-1620.
[111]
Li, W.; Jia, Z.; Xie, H.; Zhang, J.; Wang, Y.; Hao, Y.; Wang, R. Effect of acute exposure to high altitude on the pharmacokinetics of propranolol. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2013, 38(9), 909-914.
[112]
Li, W.B.; Wang, R.; Xie, H.; Zhang, J.; Xie, X.; Wu, X.; Jia, Z. Effects on the pharmacokinetics of furosemide after acute exposure to high altitude at 4010 meters in rats. Yao Xue Xue Bao, 2012, 47(12), 1718-1721.
[113]
Xiong, J.; Lu, H.; Wang, R.; Jia, Z. Efficacy of ibuprofen on prevention of high altitude headache: A systematic review and meta-analysis. PLoS One, 2017, 12(6), e0179788.
[114]
Wang, R.; Sun, Y.; Yin, Q.; Xie, H.; Li, W.; Wang, C.; Guo, J.; Hao, Y.; Tao, R.; Jia, Z. The effects of metronidazole on Cytochrome P450 Activity and Expression in rats after acute exposure to high altitude of 4300m. Biomed. Pharmacother., 2017, 85, 296-302.
[115]
Wang, C.; Wang, R.; Xie, H.; Sun, Y.; Tao, R.; Liu, W.; Li, W.; Lu, H.; Jia, Z. Effect of acetazolamide on cytokines in rats exposed to high altitude. Cytokine, 2016, 83, 110-117.
[116]
Xie, H.; Hao, Y.; Yin, Q.; Li, W.; Lu, H.; Jia, Z.; Wang, R. Expression of plateau adaptation gene of rat tissues after plain acute exposure to high altitude. Zhejiang Da Xue Xue Bao Yi Xue Ban, 2015, 44(5), 571-577.
[117]
Wang, C.; Wang, R.; Xie, H.; Yin, Q.; Jia, Z.; Li, W.; Wang, Y.; Lu, H.; Tao, R. Effect of aminophylline on physiological and pathological changes in acute exposure to high altitude in rats. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2015, 40(1), 39-45.
[118]
Li, W.; Jia, Z.; Xie, H.; Zhang, J.; Wang, Y.; Hao, Y.; Wang, R. Effects of acute exposure to high altitude on hepatic function and CYP1A2 and CYP3A4 activities in rats. Nan Fang Yi Ke Da Xue Xue Bao, 2014, 34(8), 1203-1206.
[119]
Ishii, M.; Toda, T.; Ikarashi, N.; Ochiai, W.; Sugiyama, K. Effects of intestinal flora on the expression of cytochrome P450 3A in the liver. Yakugaku Zasshi, 2012, 132(3), 301-310.
[120]
Arancibia, A.; Paulos, C.; Chavez, J.; Ritschel, W.A. Pharmacokinetics of lithium in healthy volunteers after exposure to high altitude. Int. J. Clin. Pharmacol. Ther., 2003, 41(5), 200-206.
[121]
Ritschel, W.A.; Paulos, C.; Arancibia, A.; Pezzani, M.; Agrawal, M.; Wetzelsberger, K.; Lucker, P.W. Urinary excretion of meperidine and normeperidine in man upon acute and chronic exposure to high altitude. Method Find Exp. Clin., 1996, 18(1), 49-53.
[122]
Jurgens, G.; Christensen, H.R.; Brosen, K.; Sonne, J.; Loft, S.; Olsen, N.V. Acute hypoxia and cytochrome P450-mediated hepatic drug metabolism in humans. Clin. Pharmacol. Ther., 2002, 71(4), 214-220.
[123]
Arancibia, A.; Gai, M.N.; Chavez, J.; Paulos, C.; Pinilla, E.; Gonzalez, C.; Villanueva, S.; Ritschel, W.A. Pharmacokinetics of prednisolone in man during acute and chronic exposure to high altitude. Int. J. Clin. Pharmacol. Ther., 2005, 43(2), 85-91.
[124]
Streit, M.; Goggelmann, C.; Dehnert, C.; Burhenne, J.; Riedel, K.D.; Menold, E.; Mikus, G.; Bartsch, P.; Haefeli, W.E. Cytochrome P-450 enzyme-mediated drug metabolism at exposure to acute hypoxia (corresponding to an altitude of 4,500 m). Eur. J. Clin. Pharmacol., 2005, 61(1), 39-46.
[125]
Kamimori, G.H.; Eddington, N.D.; Hoyt, R.W.; Fulco, C.S.; Lugo, S.; Durkot, M.J.; Brunhart, A.E.; Cymerman, A. Effects of altitude (4300 m) on the pharmacokinetics of caffeine and cardio-green in humans. Eur. J. Clin. Pharmacol., 1995, 48(2), 167-170.
[126]
Lu, H.; Wang, R.; Jia, Z.; Xiong, J.; Xie, H. Effects of high altitude exposure on physiology and pharmacokinetics. Curr. Drug Metab., 2016, 17(6), 559-565.
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