Gut microbiota dysbiosis contributes to the development of hypertension

Microbiome - 2017
Jingjing Li1, Fangqing Zhao2, Yidan Wang1, Junru Chen3, Jie Tao4, Gang Tian5, Shouling Wu6, Wenbin Liu3, Qinghua Cui7, Bin Geng1, Weili Zhang1, Ryan Weldon8, Kelda Auguste8, Lei Yang9, Xiaoyan Liu9, Li Chen8, Xinchun Yang10, Baoli Zhu11, Jun Cai1
1Hypertension Center, Fuwai Hospital, State Key Laboratory of Cardiovascular Disease of China, National Center for Cardiovascular Diseases of China, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100037, China
2Computational Genomics Laboratory, Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, 100101, China
3Novogene Bioinformatics Institute, Beijing, 100000, China
4Department of Cardiology, Baoding NO.1 Central Hospital, Baoding, 071000, China
5Department of Cardiology, The First Affiliated Hospital, Xi’an Jiaotong University, Xi’an, 710061, China
6Department of Cardiology Kailuan General Hospital, Hebei Union University, Tangshan, 063000, China
7Department of Biomedical Informatics, Centre for Noncoding RNA Medicine, School of Basic Medical Sciences, Peking University, Beijing, 100191, China
8Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA
9Medical Research Center, Beijing Chaoyang Hospital, Capital Medical University, Beijing, 100020, China
10Beijing Key Laboratory of Hypertension, Beijing, 100020, China
11CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Karlsson FH, Fak F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245.

Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.

Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202.

Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513:59–64.

Zeller G, Tap J, Voigt AY, Sunagawa S, Kultima JR, Costea PI, et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol. 2014;10:766.

Fei N, Zhao L. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J. 2013;7:880–4.

Chang CJ, Lin CS, Lu CC, Martel J, Ko YF, Ojcius DM, et al. Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun. 2015;6:7489.

Zheng P, Zeng B, Zhou C, Liu M, Fang Z, Xu X, et al. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol Psychiatry. 2016;21:786–96.

Schaubeck M, Clavel T, Calasan J, Lagkouvardos I, Haange SB, Jehmlich N, et al. Dysbiotic gut microbiota causes transmissible Crohn's disease-like ileitis independent of failure in antimicrobial defence. Gut. 2016;65:225–37.

Le Roy T, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, et al. Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut. 2013;62:1787–94.

Llopis M, Cassard AM, Wrzosek L, Boschat L, Bruneau A, Ferrere G, et al. Intestinal microbiota contributes to individual susceptibility to alcoholic liver disease. Gut. 2016;65:830–9.

Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med. 2013;19:576–85.

Wang Z, Roberts AB, Buffa JA, Levison BS, Zhu W, Org E, et al. Non-lethal inhibition of gut microbial trimethylamine production for the treatment of atherosclerosis. Cell. 2015;163:1585–95.

Hillege HL, Girbes AR, de Kam PJ, Boomsma F, de Zeeuw D, Charlesworth A, et al. Renal function, neurohormonal activation, and survival in patients with chronic heart failure. Circulation. 2000;102:203–10.

Pierdomenico SD, Di Nicola M, Esposito AL, Di Mascio R, Ballone E, Lapenna D, et al. Prognostic value of different indices of blood pressure variability in hypertensive patients. Am J Hypertens. 2009;22:842–7.

He FJ, Li J, Macgregor GA. Effect of longer-term modest salt reduction on blood pressure. Cochrane Database Syst Rev. 2013, DOI: 10.1002/14651858.CD004937.pub2 : CD004937.

Kato N, Takeuchi F, Tabara Y, Kelly TN, Go MJ, Sim X, et al. Meta-analysis of genome-wide association studies identifies common variants associated with blood pressure variation in east Asians. Nat Genet. 2011;43:531–8.

Moghadamrad S, McCoy KD, Geuking MB, Sagesser H, Kirundi J, Macpherson AJ, et al. Attenuated portal hypertension in germ-free mice: function of bacterial flora on the development of mesenteric lymphatic and blood vessels. Hepatology. 2015;61:1685–95.

Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, et al. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65:1331–40.

Mell B, Jala VR, Mathew AV, Byun J, Waghulde H, Zhang Y, et al. Evidence for a link between gut microbiota and hypertension in the Dahl rat. Physiol Genomics. 2015;47:187–97.

Khalesi S, Sun J, Buys N, Jayasinghe R. Effect of probiotics on blood pressure: a systematic review and meta-analysis of randomized, controlled trials. Hypertension. 2014;64:897–903.

Gomez-Guzman M, Toral M, Romero M, Jimenez R, Galindo P, Sanchez M, et al. Antihypertensive effects of probiotics Lactobacillus strains in spontaneously hypertensive rats. Mol Nutr Food Res. 2015;59:2326–36.

Durgan DJ, Ganesh BP, Cope JL, Ajami NJ, Phillips SC, Petrosino JF, et al. Role of the gut microbiome in obstructive sleep apnea-induced hypertension. Hypertension. 2016;67:469–74.

Weber MA, Schiffrin EL, White WB, Mann S, Lindholm LH, Kenerson JG, et al. Clinical practice guidelines for the management of hypertension in the community: a statement by the American Society of Hypertension and the International Society of Hypertension. J Clin Hypertens (Greenwich). 2014;16:14–26.

Forslund K, Hildebrand F, Nielsen T, Falony G, Le Chatelier E, Sunagawa S, et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature. 2015;528:262–6.

Tanaka S, Yoshida M, Murakami Y, Ogiwara T, Shoji M, Kobayashi S, et al. The relationship of Prevotella intermedia, Prevotella nigrescens and Prevotella melaninogenica in the supragingival plaque of children, caries and oral malodor. J Clin Pediatr Dent. 2008;32:195–200.

Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev. 1998;11:589–603.

Restuccia PA, Cunha BA. Klebsiella. Infect Control. 1984;5:343–7.

Wang X, Yue TL, Barone FC, White RF, Clark RK, Willette RN, et al. Discovery of adrenomedullin in rat ischemic cortex and evidence for its role in exacerbating focal brain ischemic damage. Proc Natl Acad Sci U S A. 1995;92:11480–4.

Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, et al. A decrease of the butyrate-producing species Roseburia hominis and Fecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63:1275–83.

Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, et al. Fecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–6.

Bryant MP, Small N. The anaerobic monotrichous butyric acid-producing curved rod-shaped bacteria of the rumen. J Bacteriol. 1956;72:16–21.

Pinzone MR, Celesia BM, Di Rosa M, Cacopardo B, Nunnari G. Microbial translocation in chronic liver diseases. Int J Microbiol. 2012;2012:694629.

Greenblum S, Turnbaugh PJ, Borenstein E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci U S A. 2012;109:594–9.

Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J, Sunagawa S, et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol. 2014;32:822–8.

Aliyu SH, Marriott RK, Curran MD, Parmar S, Bentley N, Brown NM, et al. Real-time PCR investigation into the importance of Fusobacterium necrophorum as a cause of acute pharyngitis in general practice. J Med Microbiol. 2004;53:1029–35.

Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15:382–92.

Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2008;36:D480–484.

Feng Q, Liang S, Jia H, Stadlmayr A, Tang L, Lan Z, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun. 2015;6:6528.

Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895–905.

Tang XY, Zhu YQ, Wei B, Wang H. Expression and functional research of TLR4 in human colon carcinoma. Am J Med Sci. 2010;339:319–26.

Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol. 2000;164:966–72.

Kumar S, Arya P, Mukherjee C, Singh BK, Singh N, Parmar VS, et al. Novel aromatic ester from Piper longum and its analogues inhibit expression of cell adhesion molecules on endothelial cells. Biochemistry. 2005;44:15944–52.

Wang W, Zheng JP, Zhu SX, Guan WJ, Chen M, Zhong NS. Carbocisteine attenuates hydrogen peroxide-induced inflammatory injury in A549 cells via NF-kappaB and ERK1/2 MAPK pathways. Int Immunopharmacol. 2015;24:306–13.

Lu Y, AJ, Wang G, Hao H, Huang Q, Yan B, et al. Gas chromatography/time-of-flight mass spectrometry based metabonomic approach to differentiating hypertension- and age-related metabolic variation in spontaneously hypertensive rats. Rapid Commun Mass Spectrom. 2008;22:2882–8.

De Deyn PP, Robitaille P, Vanasse M, Qureshi IA, Marescau B. Serum guanidino compound levels in uremic pediatric patients treated with hemodialysis or continuous cycle peritoneal dialysis. Correlations between nerve conduction velocities and altered guanidino compound concentrations. Nephron. 1995;69:411–7.

Qi Y, Aranda JM, Rodriguez V, Raizada MK, Pepine CJ. Impact of antibiotics on arterial blood pressure in a patient with resistant hypertension—a case report. Int J Cardiol. 2015;201:157–8.

Baez S, Gordon HA. Tone and reactivity of vascular smooth muscle in germfree rat mesentery. J Exp Med. 1971;134:846–56.

Hofer U. Microbiome: anelloviridae go viral. Nat Rev Microbiol. 2014;12:4–5.

Kohn FR, Kung AH. Role of endotoxin in acute inflammation induced by gram-negative bacteria: specific inhibition of lipopolysaccharide-mediated responses with an amino-terminal fragment of bactericidal/permeability-increasing protein. Infect Immun. 1995;63:333–9.

Cybulsky MI, Chan MK, Movat HZ. Acute inflammation and microthrombosis induced by endotoxin, interleukin-1, and tumor necrosis factor and their implication in gram-negative infection. Lab Invest. 1988;58:365–78.

Karbach SH, Schönfelder T, Brandão I, Wilms E, Hörmann N, Jäckel S, et al. Gut microbiota promote angiotensin II-induced arterial hypertension and vascular dysfunction. J Am Heart Assoc. 2016;5(9). doi: 10.1161/JAHA.116.003698 .

Brindle JT, Nicholson JK, Schofield PM, Grainger DJ, Holmes E. Application of chemometrics to 1H NMR spectroscopic data to investigate a relationship between human serum metabolic profiles and hypertension. Analyst. 2003;128:32–6.

Lim SS, Vos T, Flaxman AD, Danaei G, Shibuya K, Adair-Rohani H, et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2224–60.

Group SR, Wright Jr JT, Williamson JD, Whelton PK, Snyder JK, Sink KM, et al. A randomized trial of intensive versus standard blood-pressure control. N Engl J Med. 2015;373:2103–16.

Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 2009;25:1966–7.

Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience. 2012;1:18.

Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.

Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65.

Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–80.

Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.

Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res. 2007;17:377–86.

Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17:690–703.

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.