Interactions between Roseburia intestinalis and diet modulate atherogenesis in a murine model

被引:411
作者
Kasahara, Kazuyuki [1 ]
Krautkramer, Kimberly A. [2 ,3 ]
Org, Elin [4 ]
Romano, Kymberleigh A. [1 ]
Kerby, Robert L. [1 ]
Vivas, Eugenio, I [1 ]
Mehrabian, Margarete [4 ]
Denu, John M. [2 ,3 ]
Backheds, Fredrik [5 ]
Lusis, Aldonsj [4 ]
Rey, Federico E. [1 ]
机构
[1] Univ Wisconsin, Dept Bacteriol, Madison, WI 53706 USA
[2] Wisconsin Inst Discovery, Madison, WI USA
[3] Univ Wisconsin, Dept Biomol Chem, Madison, WI USA
[4] Univ Calif Los Angeles, David Geffen Sch Med, Dept Med, Div Cardiol, Los Angeles, CA 90095 USA
[5] Univ Gothenburg, Dept Mol & Clin Med, Wallenberg Lab, Gothenburg, Sweden
基金
美国食品与农业研究所;
关键词
BUTYRATE-PRODUCING BACTERIA; HUMAN GUT MICROBIOTA; HISTONE MODIFICATIONS; METABOLISM; ATHEROSCLEROSIS; BARRIER; PHOSPHATIDYLCHOLINE; INFLAMMATION; MACROPHAGES; TRANSFERASE;
D O I
10.1038/s41564-018-0272-x
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Humans with metabolic and inflammatory diseases frequently harbour lower levels of butyrate-producing bacteria in their gut. However, it is not known whether variation in the levels of these organisms is causally linked with disease development and whether diet modifies the impact of these bacteria on health. Here we show that a prominent gut-associated butyrate-producing bacterial genus (Roseburia) is inversely correlated with atherosclerotic lesion development in a genetically diverse mouse population. We use germ-free apolipoprotein E-deficient mice colonized with synthetic microbial communities that differ in their capacity to generate butyrate to demonstrate that Roseburia intestinalis interacts with dietary plant polysaccharides to: impact gene expression in the intestine, directing metabolism away from glycolysis and toward fatty acid utilization; lower systemic inflammation; and ameliorate atherosclerosis. Furthermore, intestinal administration of butyrate reduces endotoxaemia and atherosclerosis development. Together, our results illustrate how modifiable diet-by-microbiota interactions impact cardiovascular disease, and suggest that interventions aimed at increasing the representation of butyrate-producing bacteria may provide protection against atherosclerosis.
引用
收藏
页码:1461 / 1471
页数:11
相关论文
共 49 条
[1]   Natural regulatory T cells control the development of atherosclerosis in mice [J].
Ait-Oufella, H ;
Salomon, BL ;
Potteaux, S ;
Robertson, AKL ;
Gourdy, P ;
Zoll, J ;
Merval, R ;
Esposito, B ;
Cohen, JL ;
Fisson, S ;
Flavell, RA ;
Hansson, GK ;
Klatzmann, D ;
Tedgui, A ;
Mallat, Z .
NATURE MEDICINE, 2006, 12 (02) :178-180
[2]   Inflammatory activation of arachidonic acid signaling in murine P388D(1) macrophages via sphingomyelin synthesis [J].
Balsinde, J ;
Balboa, MA ;
Dennis, EA .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1997, 272 (33) :20373-20377
[3]   Genetic Architecture of Atherosclerosis in Mice: A Systems Genetics Analysis of Common Inbred Strains [J].
Bennett, Brian J. ;
Davis, Richard C. ;
Civelek, Mete ;
Orozco, Luz ;
Wu, Judy ;
Qi, Hannah ;
Pan, Calvin ;
Packard, Rene R. Sevag ;
Eskin, Eleazar ;
Yan, Mujing ;
Kirchgessner, Todd ;
Wang, Zeneng ;
Li, Xinmin ;
Gregory, Jill C. ;
Hazen, Stanley L. ;
Gargalovic, Peter S. ;
Lusis, Aldons J. .
PLOS GENETICS, 2015, 11 (12)
[4]   Tumor necrosis factor-α promotes atherosclerotic lesion progression in APOE*3-leiden transgenic mice [J].
Boesten, LSM ;
Zadelaar, ASM ;
van Nieuwkoop, A ;
Gijbels, MJJ ;
de Winther, MPJ ;
Havekes, LM ;
van Vlijmen, BJM .
CARDIOVASCULAR RESEARCH, 2005, 66 (01) :179-185
[5]   SODIUM BUTYRATE INHIBITS HISTONE DEACETYLATION IN CULTURED-CELLS [J].
CANDIDO, EPM ;
REEVES, R ;
DAVIE, JR .
CELL, 1978, 14 (01) :105-113
[6]   A major role for VCAM-1, but not ICAM-1, in early atherosclerosis [J].
Cybulsky, MI ;
Iiyama, K ;
Li, HM ;
Zhu, SN ;
Chen, M ;
Iiyama, M ;
Davis, V ;
Gutierrez-Ramos, JC ;
Connelly, PW ;
Milstone, DS .
JOURNAL OF CLINICAL INVESTIGATION, 2001, 107 (10) :1255-1262
[7]   Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice [J].
Cyrus, T ;
Witztum, JL ;
Rader, DJ ;
Tangirala, R ;
Fazio, S ;
Linton, MF ;
Funk, CD .
JOURNAL OF CLINICAL INVESTIGATION, 1999, 103 (11) :1597-1604
[8]   The Microbiome and Butyrate Regulate Energy Metabolism and Autophagy in the Mammalian Colon [J].
Donohoe, Dallas R. ;
Garge, Nikhil ;
Zhang, Xinxin ;
Sun, Wei ;
O'Connell, Thomas M. ;
Bunger, Maureen K. ;
Bultman, Scott J. .
CELL METABOLISM, 2011, 13 (05) :517-526
[9]   Acetate utilization and butyryl coenzyme A (CoA):acetate-CoA transferase in butyrate-producing bacteria from the human large intestine [J].
Duncan, SH ;
Barcenilla, A ;
Stewart, CS ;
Pryde, SE ;
Flint, HJ .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2002, 68 (10) :5186-5190
[10]   Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces [J].
Duncan, Sylvia H. ;
Belenguer, Alvaro ;
Holtrop, Grietje ;
Johnstone, Alexandra M. ;
Flint, Harry J. ;
Lobley, Gerald E. .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2007, 73 (04) :1073-1078