Gut microbiota derived metabolites in cardiovascular health and disease
Received date: 16 Mar 2018
Accepted date: 16 Apr 2018
Published date: 08 Jun 2018
Copyright
Trillions of microbes inhabit the human gut, not only providing nutrients and energy to the host from the ingested food, but also producing metabolic bioactive signaling molecules to maintain health and elicit disease, such as cardiovascular disease (CVD). CVD is the leading cause of mortality worldwide. In this review, we presented gut microbiota derived metabolites involved in cardiovascular health and disease, including trimethylamine-N-oxide (TMAO), uremic toxins, short chain fatty acids (SCFAs), phytoestrogens, anthocyanins, bile acids and lipopolysaccharide. These gut microbiota derived metabolites play critical roles in maintaining a healthy cardiovascular function, and if dysregulated, potentially causally linked to CVD. A better understanding of the function and dynamics of gut microbiota derived metabolites holds great promise toward mechanistic predicative CVD biomarker discoveries and precise interventions.
Key words: gut microbiota; metabolites; cardiovascular health; cardiovascular disease
Zeneng Wang , Yongzhong Zhao . Gut microbiota derived metabolites in cardiovascular health and disease[J]. Protein & Cell, 2018 , 9(5) : 416 -431 . DOI: 10.1007/s13238-018-0549-0
1 |
Abrams SA
|
2 |
Ahmed K, Tunaru S, Offermanns S (2009) GPR109A, GPR109B and GPR81, a family of hydroxy-carboxylic acid receptors. Trends Pharmacol Sci 30:557–562. https://doi.org/10.1016/j.tips.2009.09.001
|
3 |
An D
|
4 |
Andreesen JR (1994) Glycine metabolism in anaerobes. Antonie Van Leeuwenhoek 66:223–237
|
5 |
Anhe FF
|
6 |
Aoki K
|
7 |
Arbabi E, Hamidi G, Talaei SA, Salami M (2016) Estrogen agonist genistein differentially influences the cognitive and motor disorders in an ovariectomized animal model of Parkinsonism. Iran J Basic Med Sci 19:1285–1290. https://doi.org/10.22038/ijbms.2016.7911
|
8 |
Aura AM
|
9 |
Axelson M, Setchell KD (1981) The excretion of lignans in rats—evidence for an intestinal bacterial source for this new group of compounds. FEBS Lett 123:337–342
|
10 |
Bakken JS, Polgreen PM, Beekmann SE, Riedo FX, Streit JA (2013) Treatment approaches including fecal microbiota transplantation for recurrent Clostridium difficile infection (RCDI) among infectious disease physicians. Anaerobe 24:20–24. https://doi.org/10.1016/j.anaerobe.2013.08.007
|
11 |
Barnard DL, Heaton KW (1973) Bile acids and vitamin A absorption in man: the effects of two bile acid-binding agents, cholestyramine and lignin. Gut 14:316–318
|
12 |
Battson ML
|
13 |
Bennett BJ
|
14 |
Beutler B, Rietschel ET (2003) Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3:169–176. https://doi.org/10.1038/nri1004
|
15 |
Bhattarai Y, Kashyap PC (2016) Germ-free mice model for studying host–microbial interactions. Methods Mol Biol 1438:123–135.https://doi.org/10.1007/978-1-4939-3661-8_8
|
16 |
Bodea S, Funk MA, Balskus EP, Drennan CL (2016) Molecular basis of C–N bond cleavage by the glycyl radical enzyme choline trimethylamine-lyase. Cell Chem Biol 23:1206–1216. https://doi.org/10.1016/j.chembiol.2016.07.020
|
17 |
Boets E
|
18 |
Boini KM, Hussain T, Li PL, Koka S (2017) Trimethylamine-N-oxide instigates NLRP3 inflammasome activation and endothelial dysfunction. Cell Physiol Biochem 44:152–162. https://doi.org/10.1159/000484623
|
19 |
Braune A, Blaut M (2018) Evaluation of inter-individual differences in gut bacterial isoflavone bioactivation in humans by PCR-based targeting of genes involved in equol formation. J Appl Microbiol 124:220–231. https://doi.org/10.1111/jam.13616
|
20 |
Chen JS, Faller DV, Spanjaard RA (2003) Short-chain fatty acid inhibitors of histone deacetylases: promising anticancer therapeutics? Curr Cancer Drug Targ 3:219–236
|
21 |
Chen ML
|
22 |
Chen ML
|
23 |
Cherdshewasart W, Panriansaen R, Picha P (2007) Pretreatment with phytoestrogen-rich plant decreases breast tumor incidence and exhibits lower profile of mammary ERalpha and ERbeta. Maturitas 58:174–181. https://doi.org/10.1016/j.maturitas.2007.08.001
|
24 |
Cherrington CA, Hinton M, Pearson GR, Chopra I (1991) Short-chain organic acids at ph 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation. J Appl Bacteriol 70:161–165
|
25 |
Chiang JY (2009) Bile acids: regulation of synthesis. J Lipid Res 50:1955–1966. https://doi.org/10.1194/jlr.R900010-JLR200
|
26 |
Chiechi LM, Lobascio A, Grillo A, Valerio T (1999) Phytoestrogencontaining food and prevention of postmenopausal osteoporosis and cardiovascular diseases. Minerva Ginecol 51:343–348
|
27 |
Corsini E
|
28 |
Craciun S, Marks JA, Balskus EP (2014) Characterization of choline trimethylamine-lyase expands the chemistry of glycyl radical enzymes. ACS Chem Biol 9:1408–1413. https://doi.org/10.1021/cb500113p
|
29 |
Danielsson H (1963) Influence of bile acids on digestion and absorption of lipids. Am J Clin Nutr 12:214–219
|
30 |
Dawson PA, Karpen SJ (2015) Intestinal transport and metabolism of bile acids. J Lipid Res 56:1085–1099. https://doi.org/10.1194/jlr.R054114
|
31 |
de Punder K, Pruimboom L (2015) Stress induces endotoxemia and low-grade inflammation by increasing barrier permeability. Front Immunol 6:223. https://doi.org/10.3389/fimmu.2015.00223
|
32 |
DeAngelis KM
|
33 |
DeGruttola AK, Low D, Mizoguchi A, Mizoguchi E (2016) Current understanding of dysbiosis in disease in human and animal models. Inflamm Bowel Dis 22:1137–1150. https://doi.org/10.1097/MIB.0000000000000750
|
34 |
Delgado S, Leite AM, Ruas-Madiedo P, Mayo B (2014) Probiotic and technological properties of Lactobacillus spp. strains from the human stomach in the search for potential candidates against gastric microbial dysbiosis. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00766
|
35 |
den Besten G
|
36 |
den Besten G
|
37 |
Devlin AS
|
38 |
Dolphin CT, Riley JH, Smith RL, Shephard EA, Phillips IR (1997) Structural organization of the human flavin-containing monooxygenase 3 gene (FMO3), the favored candidate for fish-odor syndrome, determined directly from genomic DNA. Genomics 46:260–267. https://doi.org/10.1006/geno.1997.5031
|
39 |
Duboc H, Tache Y, Hofmann AF (2014) The bile acid TGR5 membrane receptor: from basic research to clinical application. Dig Liver Dis 46:302–312. https://doi.org/10.1016/j.dld.2013.10.021
|
40 |
Duncan SH, Louis P, Thomson JM, Flint HJ (2009) The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol 11:2112–2122. https://doi.org/10.1111/j.1462-2920.2009.01931.x
|
41 |
Fan P
|
42 |
Fiorucci S, Cipriani S, Baldelli F, Mencarelli A (2010) Bile acidactivated receptors in the treatment of dyslipidemia and related disorders. Prog Lipid Res 49:171–185. https://doi.org/10.1016/j.plipres.2009.11.001
|
43 |
Fitzpatrick LA (1999) Selective estrogen receptor modulators and phytoestrogens: new therapies for the postmenopausal women. Mayo Clin Proc 74:601–607
|
44 |
Flint HJ, Duncan SH, Scott KP, Louis P (2015) Links between diet, gut microbiota composition and gut metabolism. Proc Nutr Soc 74:13–22. https://doi.org/10.1017/S0029665114001463
|
45 |
Frankenfeld CL, Atkinson C, Wahala K, Lampe JW (2014) Obesity prevalence in relation to gut microbial environments capable of producing equol or O-desmethylangolensin from the isoflavone daidzein. Eur J Clin Nutr 68:526–530. https://doi.org/10.1038/ejcn.2014.23
|
46 |
Fukui H, Brauner B, Bode JC, Bode C (1991) Plasma endotoxin concentrations in patients with alcoholic and non-alcoholic liver disease: reevaluation with an improved chromogenic assay. J Hepatol 12:162–169
|
47 |
Funk JL, Feingold KR, Moser AH, Grunfeld C (1993) Lipopolysaccharide stimulation of RAW 264.7 macrophages induces lipid accumulation and foam cell formation. Atherosclerosis 98:67–82
|
48 |
Gaiz AA, Mosawy S, Colson N, Singh I (2018) Potential of anthocyanin to prevent cardiovascular disease in diabetes. Altern Ther Health Med
|
49 |
Gaya P, Medina M, Sanchez-Jimenez A, Landete JM (2016) Phytoestrogen metabolism by adult human gut microbiota. Molecules. https://doi.org/10.3390/molecules21081034
|
50 |
Glassock RJ (2008) Uremic toxins: what are they? An integrated overview of pathobiology and classification. J Ren Nutr 18:2–6. https://doi.org/10.1053/j.jrn.2007.10.003
|
51 |
Gonzaga-Jauregui C, Lupski JR, Gibbs RA (2012) Human genome sequencing in health and disease. Annu Rev Med 63:35–61. https://doi.org/10.1146/annurev-med-051010-162644
|
52 |
Goodman MT
|
53 |
Gregory JC
|
54 |
Gryp T, Vanholder R, Vaneechoutte M, Glorieux G (2017) p-Cresyl sulfate. Toxins (Basel). https://doi.org/10.3390/toxins9020052
|
55 |
Guadamuro L, Dohrmann AB, Tebbe CC, Mayo B, Delgado S (2017) Bacterial communities and metabolic activity of faecal cultures from equol producer and non-producer menopausal women under treatment with soy isoflavones. BMC Microbiol 17:93. https://doi.org/10.1186/s12866-017-1001-y
|
56 |
Hamilton MK
|
57 |
Han H
|
58 |
Hannum SM (2004) Potential impact of strawberries on human health: a review of the science. Crit Rev Food Sci Nutr 44:1–17. https://doi.org/10.1080/10408690490263756
|
59 |
Harrold JA
|
60 |
Hashemi Z, Fouhse J, Im HS, Chan CB, Willing BP (2017) Dietary pea fiber supplementation improves glycemia and induces changes in the composition of gut microbiota, serum short-chain fatty acid profile and expression of mucins in glucose intolerant rats. Nutrient. https://doi.org/10.3390/nu9111236
|
61 |
Hassellund SS
|
62 |
Heerdt BG, Houston MA, Augenlicht LH (1997) Short-chain fatty acid-initiated cell cycle arrest and apoptosis of colonic epithelial cells is linked to mitochondrial function. Cell Growth Differ 8:523–532
|
63 |
Herrington D (2000) Role of estrogens, selective estrogen receptor modulators and phytoestrogens in cardiovascular protection. Can J Cardiol 16(Suppl E):5E–9E
|
64 |
Hibberd MC
|
65 |
Hidalgo M
|
66 |
Hollander D, Rim E, Ruble PE Jr (1977) Vitamin K2 colonic and ileal in vivo absorption: bile, fatty acids, and pH effects on transport. Am J Physiol 233:E124–E129. https://doi.org/10.1152/ajpendo.1977.233.2.E124
|
67 |
Hoverstad T, Midtvedt T (1986) Short-chain fatty acids in germfree mice and rats. J Nutr 116:1772–1776
|
68 |
Hoverstad T, Midtvedt T, Bohmer T (1985) Short-chain fatty acids in intestinal content of germfree mice monocontaminated with Escherichia coli or Clostridium difficile. Scand J Gastroenterol 20:373–380
|
69 |
Hsu CC
|
70 |
Hu S
|
71 |
Hughes CL Jr (1988) Phytochemical mimicry of reproductive hormones and modulation of herbivore fertility by phytoestrogens. Environ Health Perspect 78:171–174
|
72 |
Hung SC, Kuo KL, Wu CC, Tarng DC (2017) Indoxyl sulfate: a novel cardiovascular risk factor in chronic kidney disease. J Am Heart Assoc. https://doi.org/10.1161/jaha.116.005022
|
73 |
Isaak CK, Petkau JC, Blewett H, Karmin O, Siow YL (2017) Lingonberry anthocyanins protect cardiac cells from oxidativestress-induced apoptosis. Can J Physiol Pharmacol 95:904–910. https://doi.org/10.1139/cjpp-2016-0667
|
74 |
Itoh Y, Ezawa A, Kikuchi K, Tsuruta Y, Niwa T (2013) Correlation between serum levels of protein-bound uremic toxins in hemodialysis patients measured by LC/MS/MS. Mass Spectrom (Tokyo) 2:S0017. https://doi.org/10.5702/massspectrometry.s0017
|
75 |
Jing YJ
|
76 |
Joyce SA, Gahan CG (2016) Bile acid modifications at the microbehost interface: potential for nutraceutical and pharmaceutical interventions in host health. Annu Rev Food Sci Technol 7:313–333. https://doi.org/10.1146/annurev-food-041715-033159
|
77 |
Kalnins G
|
78 |
Kang N
|
79 |
Karaki S
|
80 |
Kasubuchi M, Hasegawa S, Hiramatsu T, Ichimura A, Kimura I (2015) Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 7:2839–2849. https://doi.org/10.3390/nu7042839
|
81 |
Kaur N, Gupta AK (2002) Applications of inulin and oligofructose in health and nutrition. J Biosci 27:703–714
|
82 |
Koeth RA
|
83 |
Koeth RA
|
84 |
Kouchaki E
|
85 |
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
|
86 |
Kummen M
|
87 |
Lakio L
|
88 |
LaRusso NF, Korman MG, Hoffman NE, Hofmann AF (1974) Dynamics of the enterohepatic circulation of bile acids. Postprandial serum concentrations of conjugates of cholic acid in health, cholecystectomized patients, and patients with bile acid malabsorption. N Engl J Med 291:689–692. https://doi.org/10.1056/NEJM197410032911401
|
89 |
Lephart ED, Adlercreutz H, Lund TD (2001) Dietary soy phytoestrogen effects on brain structure and aromatase in Long-Evans rats. NeuroReport 12:3451–3455
|
90 |
Lepper PM
|
91 |
Levi M (2016) Role of bile acid-regulated nuclear receptor FXR and G protein-coupled receptor TGR5 in regulation of cardiorenal syndrome (Cardiovascular Disease and Chronic Kidney Disease). Hypertension 67:1080–1084. https://doi.org/10.1161/HYPERTENSIONAHA.115.06417
|
92 |
Li J
|
93 |
Liber A, Szajewska H (2013) Effects of inulin-type fructans on appetite, energy intake, and body weight in children and adults: systematic review of randomized controlled trials. Ann Nutr Metab 63:42–54. https://doi.org/10.1159/000350312
|
94 |
Lin CJ
|
95 |
Louis P
|
96 |
Louis P, Young P, Holtrop G, Flint HJ (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA: acetate CoA-transferase gene. Environ Microbiol 12:304–314. https://doi.org/10.1111/j.1462-2920.2009.02066.x
|
97 |
Louis P, Hold GL, Flint HJ (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12:661–672. https://doi.org/10.1038/nrmicro3344
|
98 |
Lu YC, Yeh WC, Ohashi PS (2008) LPS/TLR4 signal transduction pathway. Cytokine 42:145–151. https://doi.org/10.1016/j.cyto.2008.01.006
|
99 |
MacIver DH, McNally PG, Ollerenshaw JD, Sheldon TA, Heagerty AM (1990) The effect of short-chain fatty acid supplementation on membrane electrolyte transport and blood pressure. J Hum Hypertens 4:485–490
|
100 |
Manrique Vergara D, Gonzalez Sanchez ME (2017) Short chain fatty acids (butyric acid) and intestinal diseases. Nutr Hosp 34:58–61. https://doi.org/10.20960/nh.1573
|
101 |
Mardis ER (2008) Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 9:387–402. https://doi.org/10.1146/annurev.genom.9.081307.164359
|
102 |
Martinez-del Campo A
|
103 |
Matthies A, Loh G, Blaut M, Braune A (2012) Daidzein and genistein are converted to equol and 5-hydroxy-equol by human intestinal Slackia isoflavoniconvertens in gnotobiotic rats. J Nutr 142:40–46. https://doi.org/10.3945/jn.111.148247
|
104 |
Mayerhofer CCK
|
105 |
Mendelson MM
|
106 |
Menze ET, Esmat A, Tadros MG, Abdel-Naim AB, Khalifa AE (2015) Genistein improves 3-NPA-induced memory impairment in ovariectomized rats: impact of its antioxidant, anti-inflammatory and acetylcholinesterase modulatory properties. PLoS ONE 10: e0117223. https://doi.org/10.1371/journal.pone.0117223
|
107 |
Meyer TW, Hostetter TH (2012) Uremic solutes from colon microbes. Kidney Int 81:949–954. https://doi.org/10.1038/ki.2011.504
|
108 |
Miettinen TA (1971) Relationship between faecal bile acids, absorption of fat and vitamin B 12, and serum lipids in patients with ileal resections. Eur J Clin Invest 1:452–460
|
109 |
Miller TL, Wolin MJ (1996) Pathways of acetate, propionate, and butyrate formation by the human fecal microbial flora. Appl Environ Microbiol 62:1589–1592
|
110 |
Mills EL
|
111 |
Miyamoto J
|
112 |
Morito K
|
113 |
Moss JW, Ramji DP (2016) Nutraceutical therapies for atherosclerosis. Nat Rev Cardiol 13:513–532. https://doi.org/10.1038/nrcardio.2016.103
|
114 |
Nallu A, Sharma S, Ramezani A, Muralidharan J, Raj D (2017) Gut microbiome in chronic kidney disease: challenges and opportunities. Transl Res 179:24–37. https://doi.org/10.1016/j.trsl.2016.04.007
|
115 |
Natarajan N
|
116 |
Nilsson NE, Kotarsky K, Owman C, Olde B (2003) Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochem Biophys Res Commun 303:1047–1052
|
117 |
Oellgaard J, Winther SA, Hansen TS, Rossing P, von Scholten BJ (2017) Trimethylamine N-oxide (TMAO) as a new potential therapeutic target for insulin resistance and cancer. Curr Pharm Des 23:3699–3712. https://doi.org/10.2174/1381612823666170622095324
|
118 |
Paasche S (2013) Fecal microbiota transplantation: an innovative approach to treating Clostridium difficile disease. JAAPA 26:46–49
|
119 |
Panigrahi P
|
120 |
Pascal MC, Burini JF, Chippaux M (1984) Regulation of the trimethylamine N-oxide (TMAO) reductase in Escherichia coli: analysis of tor: Mud1 operon fusion. Mol Gen Genet 195:351–355
|
121 |
Pereira-Fantini PM
|
122 |
Peterson J
|
123 |
Pluznick J (2014) A novel SCFA receptor, the microbiota, and blood pressure regulation. Gut Microbes 5:202–207. https://doi.org/10.4161/gmic.27492
|
124 |
Pluznick JL
|
125 |
Porez G, Prawitt J, Gross B, Staels B (2012) Bile acid receptors as targets for the treatment of dyslipidemia and cardiovascular disease. J Lipid Res 53:1723–1737. https://doi.org/10.1194/jlr.R024794
|
126 |
Prohaszka L, Jayarao BM, Fabian A, Kovacs S (1990) The role of intestinal volatile fatty acids in the Salmonella shedding of pigs. Zentralbl Vet B 37:570–574
|
127 |
Qin J
|
128 |
Radtke OA, Kiderlen AF, Kayser O, Kolodziej H (2004) Gene expression profiles of inducible nitric oxide synthase and cytokines in Leishmania major-infected macrophage-like RAW 264.7 cells treated with gallic acid. Planta Med 70:924–928. https://doi.org/10.1055/s-2004-832618
|
129 |
Raspor P, Goranovic D(2008) Biotechnological applications of acetic acid bacteria. Crit Rev Biotechnol 28:101–124. https://doi.org/10.1080/07388550802046749
|
130 |
Rath S, Heidrich B, Pieper DH, Vital M (2017) Uncovering the trimethylamine-producing bacteria of the human gut microbiota. Microbiome 5:54. https://doi.org/10.1186/s40168-017-0271-9
|
131 |
Rausch C, Lerchner A, Schiefner A, Skerra A (2013) Crystal structure of the omega-aminotransferase from Paracoccus denitrificans and its phylogenetic relationship with other class III aminotransferases that have biotechnological potential. Proteins 81:774–787. https://doi.org/10.1002/prot.24233
|
132 |
Reger MK, Zollinger TW, Liu Z, Jones J, Zhang J (2017) Association between urinary phytoestrogens and C-reactive protein in the continuous national health and nutrition examination survey. J Am Coll Nutr 36:434–441. https://doi.org/10.1080/07315724.2017.1318722
|
133 |
Reichardt N
|
134 |
Rothschild D
|
135 |
Schuett K
|
136 |
Schuijt TJ
|
137 |
Schumann RR
|
138 |
Seldin MM
|
139 |
Shan Z
|
140 |
Shi J
|
141 |
Shih DM
|
142 |
Stoclet JC, Kleschyov A, Andriambeloson E, Diebolt M, Andriantsitohaina R (1999) Endothelial no release caused by red wine polyphenols. J Physiol Pharmacol 50:535–540
|
143 |
Sun X
|
144 |
Suzuki T, Heaney LM, Bhandari SS, Jones DJ, Ng LL (2016) Trimethylamine N-oxide and prognosis in acute heart failure. Heart 102:841–848. https://doi.org/10.1136/heartjnl-2015-308826
|
145 |
Suzuki T, Heaney LM, Jones DJ, Ng LL (2017) Trimethylamine Noxide and risk stratification after acute myocardial infarction. Clin Chem 63:420–428. https://doi.org/10.1373/clinchem.2016.264853
|
146 |
Tang WH
|
147 |
Tang WH
|
148 |
Tazoe H
|
149 |
Tolhurst G
|
150 |
Trieu VN, Uckun FM (1999) Genistein is neuroprotective in murine models of familial amyotrophic lateral sclerosis and stroke. Biochem Biophys Res Commun 258:685–688. https://doi.org/10.1006/bbrc.1999.0577
|
151 |
Troseid M
|
152 |
Tsuda T (2012) Dietary anthocyanin-rich plants: biochemical basis and recent progress in health benefits studies. Mol Nutr Food Res 56:159–170. https://doi.org/10.1002/mnfr.201100526
|
153 |
Tumur Z, Niwa T (2009) Indoxyl sulfate inhibits nitric oxide production and cell viability by inducing oxidative stress in vascular endothelial cells. Am J Nephrol 29:551–557. https://doi.org/10.1159/000191468
|
154 |
Tumur Z, Shimizu H, Enomoto A, Miyazaki H, Niwa T (2010) Indoxyl sulfate upregulates expression of ICAM-1 and MCP-1 by oxidative stress-induced NF-kappaB activation. Am J Nephrol 31:435–441. https://doi.org/10.1159/000299798
|
155 |
Turnbaugh PJ
|
156 |
Ulman CA, Trevino JJ, Miller M, Gandhi RK (2014) Fish odor syndrome: a case report of trimethylaminuria. Dermatol Online J 20:21260
|
157 |
Vamanu E, Pelinescu D, Sarbu I (2016) Comparative fingerprinting of the human microbiota in diabetes and cardiovascular disease. J Med Food 19:1188–1195. https://doi.org/10.1089/jmf.2016.0085
|
158 |
van der Schouw YT
|
159 |
Vanharanta M
|
160 |
Vanharanta M, Voutilainen S, Rissanen TH, Adlercreutz H, Salonen JT (2003) Risk of cardiovascular disease-related and all-cause death according to serum concentrations of enterolactone: Kuopio Ischaemic Heart Disease Risk Factor Study. Arch Intern Med 163:1099–1104. https://doi.org/10.1001/archinte.163.9.1099
|
161 |
Vital M, Howe AC, Tiedje JM (2014) Revealing the bacterial butyrate synthesis pathways by analyzing (meta)genomic data. MBio 5: e00889. https://doi.org/10.1128/mBio.00889-14
|
162 |
Vonaesch P, Anderson M, Sansonetti PJ (2018) Pathogens, microbiome and the host: emergence of the ecological Koch’s postulates. FEMS Microbiol Rev. https://doi.org/10.1093/femsre/fuy003
|
163 |
Wahlstrom A, Sayin SI, Marschall HU, Backhed F (2016) Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab 24:41–50. https://doi.org/10.1016/j.cmet.2016.05.005
|
164 |
Wampach L
|
165 |
Wang XL, Shin KH, Hur HG, Kim SI (2005) Enhanced biosynthesis of dihydrodaidzein and dihydrogenistein by a newly isolated bovine rumen anaerobic bacterium. J Biotechnol 115:261–269. https://doi.org/10.1016/j.jbiotec.2004.08.014
|
166 |
Wang Z
|
167 |
Wang Q, Zhang Y, Gao L, Xue Y (2011b) Effects of phytoestrogen, genistein combined with calcium and vitamin D3 on preventing osteoporosis in ovariectomized mice. Wei Sheng Yan Jiu 40:587–590
|
168 |
Wang D
|
169 |
Wang Z
|
170 |
Wang Z
|
171 |
Wang L
|
172 |
Ward HA, Kuhnle GG (2010) Phytoestrogen consumption and association with breast, prostate and colorectal cancer in EPIC Norfolk. Arch Biochem Biophys 501:170–175. https://doi.org/10.1016/j.abb.2010.05.018
|
173 |
Ward HA
|
174 |
Warrier M
|
175 |
Webster LT, Siddiqui UA, Lucas SV, Strong JM, Mieyal JJ (1976) Identification of separate acyl-CoA: glycine and acyl-CoA: Lglutamine N-acyltransferase activities in mitochondrial fractions from liver of rhesus monkey and man. J Biol Chem 251:3352–3358
|
176 |
Wu IW
|
177 |
Yang T
|
178 |
Yang K
|
179 |
Yisireyili M
|
180 |
Yokota A
|
181 |
Zdobnov EM
|
182 |
Zhang J, Wang YJ, Xu JL (2004) Experimental study on prevention and treatment of osteoporosis by phytoestrogen. Zhongguo Zhong Xi Yi Jie He Za Zhi 24:241–243
|
183 |
Zhang FM
|
184 |
Zhang M, Wang K, Chen L, Yin B, Song Y (2016) Is phytoestrogen intake associated with decreased risk of prostate cancer? A systematic review of epidemiological studies based on 17,546 cases. Andrology 4:745–756. https://doi.org/10.1111/andr.12196
|
185 |
Zhang H
|
186 |
Zhao Y
|
187 |
Zhao L
|
188 |
Zhu Y
|
189 |
Zhu W
|
190 |
Zhu W, Wang Z, Tang WHW, Hazen SL (2017) Gut microbegenerated trimethylamine N-oxide from dietary choline is prothrombotic in subjects. Circulation 135:1671–1673. https://doi.org/10.1161/CIRCULATIONAHA.116.025338
|
/
〈 | 〉 |