Non-lethal Inhibition of Gut Microbial Trimethylamine Production for the Treatment of Atherosclerosis

Cell

Volumn 163, Issue 7, 2015, Pages 1585-1595

  Wang, Zeneng ^a   Roberts, Adam B ^a   Buffa, Jennifer A ^a   Levison, Bruce S ^a   Zhu, Weifei ^a   Org, Elin ^b   Gu, Xiaodong ^a   Huang, Ying ^a   Zamanian Daryoush, Maryam ^a   Culley, Miranda K ^a   Didonato, Anthony J ^a   Fu, Xiaoming ^a   Hazen, Jennie E ^a   Krajcik, Daniel ^a   Didonato, Joseph A ^a   Lusis, Aldons J ^b   Hazen, Stanley L ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,3 DIMETHYL 1 BUTANOL; APOLIPOPROTEIN E; BUTANOL; CHOLESTEROL; CHOLINE; TRIMETHYLAMINE; UNCLASSIFIED DRUG; 3,3-DIMETHYLBUTAN-1-OL; HEXANOL; LYASE; METHYLAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CHOLESTEROL BLOOD LEVEL; COMMENSALISM; CONTROLLED STUDY; ENZYME ACTIVITY; FECES; FEMALE; INTESTINE FLORA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMISTRY; DIET; FOAM CELL; GASTROINTESTINAL TRACT; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MICROFLORA;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CHOLESTEROL; CHOLINE; DIET; FECES; FOAM CELLS; GASTROINTESTINAL TRACT; HEXANOLS; HUMANS; LYASES; METHYLAMINES; MICE; MICE, INBRED C57BL; MICROBIOTA;

EID: 84950297830     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.11.055     Document Type: Article

References (36)

1. J. Baglione, and J.D. Smith Quantitative assay for mouse atherosclerosis in the aortic root Methods Mol. Med. 129 2006 83 95
2. M.A. Bain, G. Fornasini, and A.M. Evans Trimethylamine: metabolic, pharmacokinetic and safety aspects Curr. Drug Metab. 6 2005 227 240
3. P. Barlow, and R.M. Marchbanks The effects of inhibiting choline dehydrogenase on choline metabolism in mice Biochem. Pharmacol. 34 1985 3117 3122
4. B.J. Bennett, T.Q. de Aguiar Vallim, Z. Wang, D.M. Shih, Y. Meng, J. Gregory, H. Allayee, R. Lee, M. Graham, R. Crooke, and et al. Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation Cell Metab. 17 2013 49 60
5. J.M. Brown, and S.L. Hazen The gut microbial endocrine organ: bacterially derived signals driving cardiometabolic diseases Annu. Rev. Med. 66 2015 343 359
6. M. Cafiero [Choline dehydrogenase of the liver] Boll. Soc. Ital. Biol. Sper. 27 1951 1426 1427
7. J.R. Cashman, K. Camp, S.S. Fakharzadeh, P.V. Fennessey, R.N. Hines, O.A. Mamer, S.C. Mitchell, G.P. Nguyen, D. Schlenk, R.L. Smith, and et al. Biochemical and clinical aspects of the human flavin-containing monooxygenase form 3 (FMO3) related to trimethylaminuria Curr. Drug Metab. 4 2003 151 170
8. I. Cho, and M.J. Blaser The human microbiome: at the interface of health and disease Nat. Rev. Genet. 13 2012 260 270
9. L.M. Cox, S. Yamanishi, J. Sohn, A.V. Alekseyenko, J.M. Leung, I. Cho, S.G. Kim, H. Li, Z. Gao, D. Mahana, and et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences Cell 158 2014 705 721
10. S. Craciun, and E.P. Balskus Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme Proc. Natl. Acad. Sci. USA 109 2012 21307 21312
11. M.E. Dumas, R.H. Barton, A. Toye, O. Cloarec, C. Blancher, A. Rothwell, J. Fearnside, R. Tatoud, V. Blanc, J.C. Lindon, and et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice Proc. Natl. Acad. Sci. USA 103 2006 12511 12516
12. J.C. Gregory, J.A. Buffa, E. Org, Z. Wang, B.S. Levison, W. Zhu, M.A. Wagner, B.J. Bennett, L. Li, J.A. DiDonato, and et al. Transmission of atherosclerosis susceptibility with gut microbial transplantation J. Biol. Chem. 290 2015 5647 5660
13. R. Koch Investigations into the Etiology of Traumatic Infective Diseases 1880 Cambridge Scholars Publishing
14. R.A. Koeth, Z. Wang, B.S. Levison, J.A. Buffa, E. Org, B.T. Sheehy, E.B. Britt, X. Fu, Y. Wu, L. Li, and et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis Nat. Med. 19 2013 576 585
15. R.A. Koeth, B.S. Levison, M.K. Culley, J.A. Buffa, Z. Wang, J.C. Gregory, E. Org, Y. Wu, L. Li, J.D. Smith, and et al. γ-Butyrobetaine is a proatherogenic intermediate in gut microbial metabolism of L-carnitine to TMAO Cell Metab. 20 2014 799 812
16. O. Koren, A. Spor, J. Felin, F. Fåk, J. Stombaugh, V. Tremaroli, C.J. Behre, R. Knight, B. Fagerberg, R.E. Ley, and F. Bäckhed Human oral, gut, and plaque microbiota in patients with atherosclerosis Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4592 4598
17. M. Lever, P.M. George, S. Slow, D. Bellamy, J.M. Young, M. Ho, C.J. McEntyre, J.L. Elmslie, W. Atkinson, S.L. Molyneux, and et al. Betaine and trimethylamine-N-oxide as predictors of cardiovascular outcomes show different patterns in diabetes mellitus: an observational study PLoS ONE 9 2014 e114969
18. A. Mente, K. Chalcraft, H. Ak, A.D. Davis, E. Lonn, R. Miller, M.A. Potter, S. Yusuf, S.S. Anand, and M.J. McQueen The relationship between trimethylamine-N-oxide and prevalent cardiovascular disease in a multiethnic population living in Canada Can. J. Cardiol. 31 2015 1189 1194
19. J. Miao, A.V. Ling, P.V. Manthena, M.E. Gearing, M.J. Graham, R.M. Crooke, K.J. Croce, R.M. Esquejo, C.B. Clish, D. Vicent, S.B. Biddinger Morbid Obesity Study Group Flavin-containing monooxygenase 3 as a potential player in diabetes-associated atherosclerosis Nat. Commun. 6 2015 6498
20. B. Möller, H. Hippe, and G. Gottschalk Degradation of various amine compounds by mesophilic clostridia Arch. Microbiol. 145 1986 85 90
21. B. Petschow, J. Doré, P. Hibberd, T. Dinan, G. Reid, M. Blaser, P.D. Cani, F.H. Degnan, J. Foster, G. Gibson, and et al. Probiotics, prebiotics, and the host microbiome: the science of translation Ann. N Y Acad. Sci. 1306 2013 1 17
22. R.R. Renshaw, and R.A. Bishop The phosphorus analogs and homologs of choline and betaine. Onium Compounds J. Am. Chem. Soc. 60 1938 946 947
23. K.A. Romano, E.I. Vivas, D. Amador-Noguez, and F.E. Rey Intestinal microbiota composition modulates choline bioavailability from diet and accumulation of the proatherogenic metabolite trimethylamine-N-oxide MBio 6 2015 e02481
24. S.S. Sandhu, and T. Chase Jr. Aerobic degradation of choline by Proteus mirabilis: enzymatic requirements and pathway Can. J. Microbiol. 32 1986 743 750
25. D.M. Shih, Z. Wang, R. Lee, Y. Meng, N. Che, S. Charugundla, H. Qi, J. Wu, C. Pan, J.M. Brown, and et al. Flavin containing monooxygenase 3 exerts broad effects on glucose and lipid metabolism and atherosclerosis J. Lipid Res. 56 2015 22 37
26. Q.H. Tan, L. Penkovsky, and M.S. Zedeck Histochemical findings suggesting that methylazoxymethanol, a liver and kidney carcinogen, is a substrate for hepatic and renal choline dehydrogenase Carcinogenesis 2 1981 1135 1139
27. W.H. Tang, Z. Wang, B.S. Levison, R.A. Koeth, E.B. Britt, X. Fu, Y. Wu, and S.L. Hazen Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk N. Engl. J. Med. 368 2013 1575 1584
28. W.H. Tang, Z. Wang, Y. Fan, B. Levison, J.E. Hazen, L.M. Donahue, Y. Wu, and S.L. Hazen Prognostic value of elevated levels of intestinal microbe-generated metabolite trimethylamine-N-oxide in patients with heart failure: refining the gut hypothesis J. Am. Coll. Cardiol. 64 2014 1908 1914
29. M. Trøseid, T. Ueland, J.R. Hov, A. Svardal, I. Gregersen, C.P. Dahl, S. Aakhus, E. Gude, B. Bjørndal, B. Halvorsen, and et al. Microbiota-dependent metabolite trimethylamine-N-oxide is associated with disease severity and survival of patients with chronic heart failure J. Intern. Med. 277 2015 717 726
30. Z. Wang, S.J. Nicholls, E.R. Rodriguez, O. Kummu, S. Hörkkö, J. Barnard, W.F. Reynolds, E.J. Topol, J.A. DiDonato, and S.L. Hazen Protein carbamylation links inflammation, smoking, uremia and atherogenesis Nat. Med. 13 2007 1176 1184
31. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, B. Dugar, A.E. Feldstein, E.B. Britt, X. Fu, Y.M. Chung, and et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 2011 57 63
32. Z. Wang, B.S. Levison, J.E. Hazen, L. Donahue, X.M. Li, and S.L. Hazen Measurement of trimethylamine-N-oxide by stable isotope dilution liquid chromatography tandem mass spectrometry Anal. Biochem. 455 2014 35 40
33. Z. Wang, W.H. Tang, J.A. Buffa, X. Fu, E.B. Britt, R.A. Koeth, B.S. Levison, Y. Fan, Y. Wu, and S.L. Hazen Prognostic value of choline and betaine depends on intestinal microbiota-generated metabolite trimethylamine-N-oxide Eur. Heart J. 35 2014 904 910
34. M. Warrier, D.M. Shih, A.C. Burrows, D. Ferguson, A.D. Gromovsky, A.L. Brown, S. Marshall, A. McDaniel, R.C. Schugar, Z. Wang, and et al. The TMAO-Generating Enzyme Flavin Monooxygenase 3 Is a Central Regulator of Cholesterol Balance Cell Rep. 10 2015 326 338
35. G.D. Wu, J. Chen, C. Hoffmann, K. Bittinger, Y.Y. Chen, S.A. Keilbaugh, M. Bewtra, D. Knights, W.A. Walters, R. Knight, and et al. Linking long-term dietary patterns with gut microbial enterotypes Science 334 2011 105 108
36. Y. Zhu, E. Jameson, M. Crosatti, H. Schäfer, K. Rajakumar, T.D. Bugg, and Y. Chen Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota Proc. Natl. Acad. Sci. USA 111 2014 4268 4273