A high salt diet modulates the gut microbiota and short chain fatty acids production in a salt-sensitive hypertension rat model

Nutrients

Volumn 10, Issue 9, 2018, Pages

  Bier, Ariel ^a,b   Braun, Tzipi ^a   Khasbab, Rawan ^a,b   Di Segni, Ayelet ^a   Grossman, Ehud ^a,b   Haberman, Yael ^a,b,c   Leibowitz, Avshalom ^a,b  

^a SHEBA MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Blood pressure; Microbiome; Salt; Short chain fatty acids

Indexed keywords

ACETIC ACID; BUTYRIC ACID; ISOBUTYRIC ACID; PROPIONIC ACID; RNA 16S; SHORT CHAIN FATTY ACID; ISOBUTYRIC ACID DERIVATIVE; PROPIONIC ACID DERIVATIVE; VOLATILE FATTY ACID;

ACTINOBACTERIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; CORYNEBACTERIACEAE; DATA PROCESSING; DNA EXTRACTION; ERWINIA; FECES; GENE SEQUENCE; HIGH SALT DIET; HYPERTENSION; INTESTINE FLORA; MICROBIOME; NONHUMAN; ORGANISMAL INTERACTION; POLYMERASE CHAIN REACTION; PRINCIPAL COORDINATE ANALYSIS; PROTEINURIA; RAT; ACTINOMYCETALES; ADMINISTRATION AND DOSAGE; ANIMAL; CHEMISTRY; CLOSTRIDIALES; DAHL RAT; DIET; ISOLATION AND PURIFICATION; MALE; METABOLISM; MICROBIOLOGY; SALT INTAKE;

ACETIC ACID; ACTINOMYCETALES; ANIMALS; BLOOD PRESSURE; BUTYRIC ACID; CLOSTRIDIALES; DIET; ERWINIA; FATTY ACIDS, VOLATILE; FECES; GASTROINTESTINAL MICROBIOME; HYPERTENSION; ISOBUTYRATES; MALE; PROPIONATES; RATS; RATS, INBRED DAHL; RNA, RIBOSOMAL, 16S; SODIUM CHLORIDE, DIETARY;

EID: 85052600966     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu10091154     Document Type: Article

References (30)

1. Oparil, S.; Acelajado, M.C.; Bakris, G.L.; Berlowitz, D.R.; Cifkova, R.; Dominiczak, A.F.; Grassi, G.; Jordan, J.; Poulter, N.R.; Rodgers, A.; et al. Hypertension. Nat. Rev. Dis. Prim. 2018, 4, 18014. [CrossRef] [PubMed]
2. Rucker, A.J.; Rudemiller, N.P.; Crowley, S.D. Salt, Hypertension, and Immunity. Annu. Rev. Physiol. 2018, 80, 283–307. [CrossRef] [PubMed]
3. O’Donnell, M.; Mente, A.; Yusuf, S. Sodium intake and cardiovascular health. Circ. Res. 2015, 116, 1046–1057. [CrossRef] [PubMed]
4. David, L.A.; Maurice, C.F.; Carmody, R.N.; Gootenberg, D.B.; Button, J.E.; Wolfe, B.E.; Ling, A.V.; Devlin, A.S.; Varma, Y.; Fischbach, M.A.; Biddinger, S.B.; et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505, 559–563. [CrossRef] [PubMed]
5. Schroeder, B.O.; Bäckhed, F. Signals from the gut microbiota to distant organs in physiology and disease. Nat. Med. 2016, 22, 1079–1089. [CrossRef] [PubMed]
6. Marques, F.Z.; Mackay, C.R.; Kaye, D.M. Beyond gut feelings: How the gut microbiota regulates blood pressure. Nat. Rev. Cardiol. 2018, 15, 20–32. [CrossRef] [PubMed]
7. Hu, J.; Luo, H.; Wang, J.; Tang, W.; Lu, J.; Wu, S.; Xiong, Z.; Yang, G.; Chen, Z.; Lan, T.; et al. Enteric dysbiosis-linked gut barrier disruption triggers early renal injury induced by chronic high salt feeding in mice. Exp. Mol. Med. 2017, 49, e370. [CrossRef] [PubMed]
8. Wang, C.; Huang, Z.; Yu, K.; Ding, R.; Ye, K.; Dai, C.; Xu, X.; Zhou, G.; Li, C. High-Salt Diet Has a Certain Impact on Protein Digestion and Gut Microbiota: A Sequencing and Proteome Combined Study. Front. Microbiol. 2017, 8, 1838. [CrossRef] [PubMed]
9. Miranda, P.M.; De Palma, G.; Serkis, V.; Lu, J.; Louis-Auguste, M.P.; McCarville, J.L.; Verdu, E.F.; Collins, S.M.; Bercik, P. High salt diet exacerbates colitis in mice by decreasing Lactobacillus levels and butyrate production. Microbiome 2018, 6, 57. [CrossRef] [PubMed]
10. Wilck, N.; Matus, M.G.; Kearney, S.M.; Olesen, S.W.; Forslund, K.; Bartolomaeus, H.; Haase, S.; Mahler, A.; Balogh, A.; Marko, L.; et al. Salt-responsive gut commensal modulates TH17 axis and disease. Nature 2017, 551, 585–589. [CrossRef] [PubMed]
11. Iwai, J.; Dahl, L.K.; Knudsen, K.D. Genetic influence on the renin-angiotensin system: Low renin activities in hypertension-prone rats. Circ. Res. 1973, 32, 678–684. [CrossRef] [PubMed]
12. Kobori, H.; Nishiyama, A.; Abe, Y.; Navar, L.G. Enhancement of intrarenal angiotensinogen in Dahl salt-sensitive rats on high salt diet. Hypertension (Dallas TX 1979) 2003, 41, 592–597. [CrossRef] [PubMed]
13. Mell, B.; Jala, V.R.; Mathew, A.V.; Byun, J.; Waghulde, H.; Zhang, Y.; Haribabu, B.; Vijay-Kumar, M.; Pennathur, S.; Joe, B. Evidence for a link between gut microbiota and hypertension in the Dahl rat. Physiol. Genom. 2015, 47, 187–197. [CrossRef] [PubMed]
14. Macfarlane, G.T.; Macfarlane, S. Bacteria, colonic fermentation, and gastrointestinal health. J. AOAC Int. 2012, 95, 50–60. [CrossRef] [PubMed]
15. Pluznick, J.L.; Protzko, R.J.; Gevorgyan, H.; Peterlin, Z.; Sipos, A.; Han, J. Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc. Natl. Acad. Sci. USA 2013, 110, 4410–4415. [CrossRef] [PubMed]
16. Raizada, M.K.; Joe, B.; Bryan, N.S.; Chang, E.B.; Dewhirst, F.E.; Borisy, G.G.; Galis, Z.S.; Henderson, W.; Jose, P.A.; Ketchum, C.J. et al. Report of the National Heart, Lung, and Blood Institute Working Group on the Role of Microbiota in Blood Pressure Regulation: Current Status and Future Directions. Hypertension (Dallas TX 1979) 2017. [CrossRef] [PubMed]
17. Braun, T.; Di Segni, A.; BenShoshan, M.; Asaf, R.; Squires, J.E.; Farage Barhom, S.; Glick Saar, E.; Cesarkas, K.; Smollan, G.; Weiss, B.; et al. Fecal microbial characterization of hospitalized patients with suspected infectious diarrhea shows significant dysbiosis. Sci. Rep. 2017, 7, 1088. [CrossRef] [PubMed]
18. Di Segni, A.; Braun, T.; BenShoshan, M.; Farage Barhom, S.; Glick Saar, E.; Cesarkas, K.; Squires, J.E.; Keller, N.; Haberman, Y. Guided Protocol for Fecal Microbial Characterization by 16S rRNA-Amplicon Sequencing. J. Vis. Exp. 2018. [CrossRef] [PubMed]
19. Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Pena, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 2010, 7, 335–336. [CrossRef] [PubMed]
20. Edgar, R.C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26, 2460–2461. [CrossRef] [PubMed]
21. McDonald, D.; Price, M.N.; Goodrich, J.; Nawrocki, E.P.; DeSantis, T.Z.; Probst, A.; Andersen, G.L.; Knight, R.; Hugenholtz, P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012, 6, 610–618. [CrossRef] [PubMed]
22. Morgan, X.C.; Tickle, T.L.; Sokol, H.; Gevers, D.; Devaney, K.L.; Ward, D.V.; Reyes, J.A.; Shah, S.A.; LeLeiko, N.; Snapper, S.B.; Bousvaros, A.; et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012, 13, R79. [CrossRef] [PubMed]
23. Haberman, Y.; Tickle, T.L.; Dexheimer, P.J.; Kim, M.-O.; Tang, D.; Karns, R.; Baldassano, R.N.; Noe, J.D.; Rosh, J.; Markowitz, J.; et al. Pediatric Crohn disease patients exhibit specific ileal transcriptome and microbiome signature. J. Clin. Investig. 2014, 124, 3617–3633. [CrossRef] [PubMed]
24. Leibowitz, A.; Volkov, A.; Voloshin, K.; Shemesh, C.; Barshack, I.; Grossman, E. Melatonin prevents kidney injury in a high salt diet-induced hypertension model by decreasing oxidative stress. J. Pineal Res. 2016, 60, 48–54. [CrossRef] [PubMed]
25. Xu, K.-Y.; Xia, G.-H.; Lu, J.-Q.; Chen, M.-X.; Zhen, X.; Wang, S.; You, C.; Nie, J.; Zhou, H.-W.; Yin, J. Impaired renal function and dysbiosis of gut microbiota contribute to increased trimethylamine-N-oxide in chronic kidney disease patients. Sci. Rep. 2017, 7, 1445. [CrossRef] [PubMed]
26. Hidalgo, M.; Prieto, I.; Abriouel, H.; Villarejo, A.B.; Ramirez-Sanchez, M.; Cobo, A.; Benomar, N.; Galvez, A.; Martinez-Canamero, M. Changes in Gut Microbiota Linked to a Reduction in Systolic Blood Pressure in Spontaneously Hypertensive Rats Fed an Extra Virgin Olive Oil-Enriched Diet. Plant Foods Hum. Nutr. 2018, 73, 1–6. [CrossRef] [PubMed]
27. Kim, S.; Goel, R.; Kumar, A.; Qi, Y.; Lobaton, G.; Hosaka, K.; Mohammed, M.; Handberg, E.M.; Richards, E.M.; Pepine, C.J.; et al. Imbalance of gut microbiome and intestinal epithelial barrier dysfunction in patients with high blood pressure. Clin. Sci. (Lond). 2018, 132, 701–718. [CrossRef] [PubMed]
28. Feng, D.; Yang, C.; Geurts, A.M.; Kurth, T.; Liang, M.; Lazar, J.; Mattson, D.L.; O’Connor, P.M.; Cowley, A.W.J. Increased expression of NAD(P)H oxidase subunit p67(phox) in the renal medulla contributes to excess oxidative stress and salt-sensitive hypertension. Cell Metab. 2012, 15, 201–208. [CrossRef] [PubMed]
29. Pluznick, J.L. Microbial Short-Chain Fatty Acids and Blood Pressure Regulation. Curr. Hypertens. Rep. 2017, 19, 25. [CrossRef] [PubMed]
30. Schwiertz, A.; Hold, G.L.; Duncan, S.H.; Gruhl, B.; Collins, M.D.; Lawson, P.A.; Flint, H.J.; Blaut, M. Anaerostipes caccae gen. nov., sp. nov., a new saccharolytic, acetate-utilising, butyrate-producing bacterium from human faeces. Syst. Appl. Microbiol. 2002, 25, 46–51. [CrossRef] [PubMed]