Choline Diet and Its Gut Microbe-Derived Metabolite, Trimethylamine N-Oxide, Exacerbate Pressure Overload-Induced Heart Failure

Circulation: Heart Failure

Volumn 9, Issue 1, 2016, Pages

  Organ, Chelsea L ^a   Otsuka, Hiroyuki ^a   Bhushan, Shashi ^a   Wang, Zeneng ^b   Bradley, Jessica ^a   Trivedi, Rishi ^a   Polhemus, David J ^a   Tang, W H Wilson ^b   Wu, Yuping ^c   Hazen, Stanley L ^b   Lefer, David J ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

Choline; fibrosis; left; metabolomics; pulmonary edema; ventricular dysfunction

Indexed keywords

BETAINE; BRAIN NATRIURETIC PEPTIDE; CHOLINE; TRIMETHYLAMINE OXIDE; METHYLAMINE; TRIMETHYLOXAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; BODY WEIGHT; CARDIOMEGALY; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; DISEASE EXACERBATION; ECHOCARDIOGRAPHY; HEART DILATATION; HEART FAILURE; HEART FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; HEART WEIGHT; HISTOPATHOLOGY; LUNG EDEMA; LUNG WEIGHT; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SURVIVAL; VASCULAR FIBROSIS; ADVERSE EFFECTS; ANIMAL; BACTERIUM; BLOOD; C57BL MOUSE; CARDIAC MUSCLE; CHEMICALLY INDUCED; DIET; DISEASE MODEL; FIBROSIS; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; INTESTINE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; RISK FACTOR; SEVERITY OF ILLNESS INDEX; TIME FACTOR;

ANIMALS; BACTERIA; CARDIOMEGALY; CHOLINE; DIET; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FIBROSIS; HEART FAILURE; INTESTINES; MALE; METHYLAMINES; MICE, INBRED C57BL; MYOCARDIUM; PULMONARY EDEMA; RISK FACTORS; SEVERITY OF ILLNESS INDEX; STROKE VOLUME; TIME FACTORS; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT;

EID: 84955278869     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.115.002314     Document Type: Article

References (22)

1. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI. The gut microbiota as an environmental factor that regulates fat storage. PNAS. 2004;101:15718-15723.
2. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, Wu Y, Schauer P, Smith JD, Allayee H, Tang WH, DiDonato JA, Lusis AJ, Hazen SL. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57-63. doi: 10.1038/nature09922.
3. Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368:1575-1584. doi: 10.1056/NEJMoa1109400.
4. Koeth RA, Levison BS, Culley MK, Buffa JA, Wang Z, Gregory JC, Org E, Wu Y, Li L, Smith JD, Tang WH, DiDonato JA, Lusis AJ, Hazen SL.-Butyrobetaine is a proatherogenic intermediate in gut microbial metabolism of L-carnitine to TMAO. Cell Metab. 2014;20:799-812. doi: 10.1016/j.cmet.2014.10.006.
5. Gregory JC, Buffa JA, Org E, Wang Z, Levison BS, Zhu W, Wagner MA, Bennett BJ, Li L, DiDonato JA, Lusis AJ, Hazen SL. Transmission of atherosclerosis susceptibility with gut microbial transplantation. J Biol Chem. 2015;290:5647-5660. doi: 10.1074/jbc.M114.618249.
6. Brown JM, Hazen SL. The gut microbial endocrine organ: bacterially derived signals driving cardiometabolic diseases. Annu Rev Med. 2015;66:343-359. doi: 10.1146/annurev-med-060513-093205.
7. Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, Smith JD, DiDonato JA, Chen J, Li H, Wu GD, Lewis JD, Warrier M, Brown JM, Krauss RM, Tang WH, Bushman FD, Lusis AJ, Hazen SL. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med. 2013;19:576-585. doi: 10.1038/nm.3145.
8. Shih DM, Wang Z, Lee R, Meng Y, Che N, Charugundla S, Qi H, Wu J, Pan C, Brown JM, Vallim T, Bennett BJ, Graham M, Hazen SL, Lusis AJ. Flavin containing monooxygenase 3 exerts broad effects on glucose and lipid metabolism and atherosclerosis. J Lipid Res. 2015;56:22-37. doi: 10.1194/jlr.M051680.
9. Warrier M, Shih DM, Burrows AC, Ferguson D, Gromovsky AD, Brown AL, Marshall S, McDaniel A, Schugar RC, Wang Z, Sacks J, Rong X, Vallim TA, Chou J, Ivanova PT, Myers DS, Brown HA, Lee RG, Crooke RM, Graham MJ, Liu X, Parini P, Tontonoz P, Lusis AJ, Hazen SL, Temel RE, Brown JM. The tmao-generating enzyme flavin monooxygenase 3 is a central regulator of cholesterol balance. Cell reports. 2015;10:326-338.
10. Tang WH, Wang Z, Kennedy DJ, Wu Y, Buffa JA, Agatisa-Boyle B, Li XS, Levison BS, Hazen SL. Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ Res. 2015;116:448-455. doi: 10.1161/CIRCRESAHA.116.305360.
11. Stubbs JR, House JA, Ocque AJ, Zhang S, Johnson C, Kimber C, Schmidt K, Gupta A, Wetmore JB, Nolin TD, Spertus JA, Yu AS. Serum trimethylamine-n-oxide is elevated in CKD and correlates with coronary atherosclerosis burden [published online ahead of print July 30, 2015]. J Am Soc Nephrol. doi: 10.1681/ASN.2014111063.
12. Mente A, Chalcraft K, Ak H, Davis AD, Lonn E, Miller R, Potter MA, Yusuf S, Anand SS, McQueen MJ. The relationship between trimethylamine-N-oxide and prevalent cardiovascular disease in a multiethnic population living in Canada. Can J Cardiol. 2015;31:1189-1194. doi: 10.1016/j.cjca.2015.06.016.
13. Tang WH, Wang Z, Fan Y, Levison B, Hazen JE, Donahue LM, Wu Y, Hazen SL. 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. 2014;64:1908-1914. doi: 10.1016/j.jacc.2014.02.617.
14. Lever M, George PM, Slow S, Bellamy D, Young JM, Ho M, McEntyre CJ, Elmslie JL, Atkinson W, Molyneux SL, Troughton RW, Frampton CM, Richards AM, Chambers ST. Betaine and trimethylamine-N-oxide as predictors of cardiovascular outcomes show different patterns in diabetes mellitus: an observational study. PLoS One. 2014;9:e114969. doi: 10.1371/journal.pone.0114969.
15. Tang WH, Wang Z, Shrestha K, Borowski AG, Wu Y, Troughton RW, Klein AL, Hazen SL. Intestinal microbiota-dependent phosphatidylcholine metabolites, diastolic dysfunction, and adverse clinical outcomes in chronic systolic heart failure. J Card Fail. 2015;21:91-96. doi: 10.1016/j. cardfail.2014.11.006.
16. Bhushan S, Kondo K, Polhemus DJ, Otsuka H, Nicholson CK, Tao YX, Huang H, Georgiopoulou VV, Murohara T, Calvert JW, Butler J, Lefer DJ. Nitrite therapy improves left ventricular function during heart failure via restoration of nitric oxide-mediated cytoprotective signaling. Circ Res. 2014;114:1281-1291. doi: 10.1161/CIRCRESAHA.114.301475.
17. Wang Z, Levison BS, Hazen JE, Donahue L, Li XM, Hazen SL. Measurement of trimethylamine-N-oxide by stable isotope dilution liquid chromatography tandem mass spectrometry. Anal Biochem. 2014;455:35-40. doi: 10.1016/j.ab.2014.03.016.
18. Tang WH, Dupont M, Hernandez AF, Voors AA, Hsu AP, Felker GM, Butler J, Metra M, Anker SD, Troughton RW, Gottlieb SS, McMurray JJ, Armstrong PW, Massie BM, Califf RM, O'Connor CM, Starling RC. Comparative assessment of short-term adverse events in acute heart failure with cystatin C and other estimates of renal function: results from the ASCEND-HF trial. JACC Heart Fail. 2015;3:40-49. doi: 10.1016/j. jchf.2014.06.014.
19. Romano KA, Vivas EI, Amador-Noguez D, Rey FE. Intestinal microbiota composition modulates choline bioavailability from diet and accumulation of the proatherogenic metabolite trimethylamine-N-oxide. MBio. 2015;6:e02481. doi: 10.1128/mBio.02481-14.
20. Miao J, Ling AV, Manthena PV, Gearing ME, Graham MJ, Crooke RM, Croce KJ, Esquejo RM, Clish CB, Vicent D, Biddinger SB; Morbid Obesity Study Group. Flavin-containing monooxygenase 3 as a potential player in diabetes-associated atherosclerosis. Nat Commun. 2015;6:6498. doi: 10.1038/ncomms7498.
21. Mondal J, Halverson D, Li IT, Stirnemann G, Walker GC, Berne BJ. How osmolytes influence hydrophobic polymer conformations: A unified view from experiment and theory. Proc Natl Acad Sci USA. 2015;112:9270-9275. doi: 10.1073/pnas.1511780112.
22. Ma J, Pazos IM, Gai F. Microscopic insights into the protein-stabilizing effect of trimethylamine N-oxide (TMAO). Proc Natl Acad Sci USA. 2014;111:8476-8481. doi: 10.1073/pnas.1403224111.