Gut Dysbiosis is Linked to Hypertension

Hypertension

Volumn 65, Issue 6, 2015, Pages 1331-1340

  Yang, Tao ^a,b   Santisteban, Monica M ^c   Rodriguez, Vermali ^c,d   Li, Eric ^e   Ahmari, Niousha ^f   Carvajal, Jessica Marulanda ^c   Zadeh, Mojgan ^a,b   Gong, Minghao ^a,b   Qi, Yanfei ^d   Zubcevic, Jasenka ^f   Sahay, Bikash ^a,b   Pepine, Carl J ^d   Raizada, Mohan K ^c   Mohamadzadeh, Mansour ^a,b  

^a Center for Comparative Medicine and Translational Research   (United States)

^b Division of Gastroenterology   (United States)

^c Department of Physiology and Functional Genomics ^*  (United States)

^d University of Florida ^*  (United States)

^e Division of Infectious Diseases and Global Medicine   (United States)

^f University of Florida College of Veterinary Medicine   (United States)

Author keywords

butyrates; dysbiosis; hypertension; microbiota; minocycline

Indexed keywords

ACETIC ACID; BACTERIAL DNA; BUTYRIC ACID; MINOCYCLINE;

ACTINOBACTERIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEROIDETES; DIET; DYSBIOSIS; ENVIRONMENTAL FACTOR; FECES ANALYSIS; FERMENTATION; FIRMICUTES; GENETIC PREDISPOSITION; GENOMICS; GUT DYSBIOSIS; HEREDITY; HUMAN; HYPERTENSION; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIAL RICHNESS; MICROBIOLOGICAL PHENOMENA AND FUNCTIONS; NONHUMAN; PRIORITY JOURNAL; RAT; RAT MODEL; RISK FACTOR; SPONTANEOUSLY HYPERTENSIVE RAT; ANIMAL; COHORT ANALYSIS; COMORBIDITY; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; FECES; GASTROINTESTINAL TRACT; MICROBIOLOGY; MICROFLORA; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; RISK ASSESSMENT; SPECIES DIFFERENCE; TREATMENT OUTCOME; WISTAR KYOTO RAT;

ANIMALS; COHORT STUDIES; COMORBIDITY; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; DYSBIOSIS; FECES; GASTROINTESTINAL TRACT; HUMANS; HYPERTENSION; MICROBIOTA; MINOCYCLINE; RANDOM ALLOCATION; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RISK ASSESSMENT; SPECIES SPECIFICITY; TREATMENT OUTCOME;

EID: 84937549863     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.05315     Document Type: Article

References (58)

1. Mendizábal Y, Llorens S, Nava E. Hypertension in metabolic syndrome: vascular pathophysiology. Int J Hypertens. 2013;2013:230868. doi: 10.1155/2013/230868.
2. Anderson EA, Sinkey CA, Lawton WJ, Mark AL. Elevated sympathetic nerve activity in borderline hypertensive humans. Evidence from direct intraneural recordings. Hypertension. 1989;14:177-183.
3. Schlaich MP, Lambert E, Kaye DM, Krozowski Z, Campbell DJ, Lambert G, Hastings J, Aggarwal A, Esler MD. Sympathetic augmentation in hypertension: role of nerve firing, norepinephrine reuptake, and angiotensin neuromodulation. Hypertension. 2004;43:169-175. doi: 10.1161/01. HYP.0000103160.35395.9E.
4. Harrison DG. The immune system in hypertension. Trans Am Clin Climatol Assoc. 2014;125:130-38; discussion 138.
5. Singh MV, Chapleau MW, Harwani SC, Abboud FM. The immune system and hypertension. Immunol Res. 2014;59:243-253. doi: 10.1007/s12026-014-8548-6.
6. Chow J, Lee SM, Shen Y, Khosravi A, Mazmanian SK. Host-bacterial symbiosis in health and disease. Adv Immunol. 2010;107:243-274. doi: 10.1016/B978-0-12-381300-8.00008-3.
7. McDermott AJ, Huffnagle GB. The microbiome and regulation of mucosal immunity. Immunology. 2014;142:24-31. doi: 10.1111/imm.12231.
8. Mariat D, Firmesse O, Levenez F, Guimar?es V, Sokol H, Doré J, Corthier G, Furet JP. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009;9:123. doi: 10.1186/1471-2180-9-123.
9. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90:859-904. doi: 10.1152/physrev.00045.2009.
10. Collado MC, Rautava S, Isolauri E, Salminen S. Gut microbiota: a source of novel tools to reduce the risk of human disease? Pediatr Res. 2015;77:182-188. doi: 10.1038/pr.2014.173.
11. 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.
12. Tilg H, Kaser A. Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest. 2011;121:2126-2132. doi: 10.1172/JCI58109.
13. Everard A, Cani PD. Diabetes, obesity and gut microbiota. Best Pract Res Clin Gastroenterol. 2013;27:73-83. doi: 10.1016/j.bpg.2013.03.007.
14. Howitt MR, Garrett WS. A complex microworld in the gut: gut microbiota and cardiovascular disease connectivity. Nat Med. 2012;18:1188-1189. doi: 10.1038/nm.2895.
15. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature. 2007;449:804-810. doi: 10.1038/nature06244.
16. Sanz Y, Moya-Pérez A. Microbiota, inflammation and obesity. Adv Exp Med Biol. 2014;817:291-317. doi: 10.1007/978-1-4939-0897-4-14.
17. 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. doi: 10.1161/HYPERTENSIONAHA.114.03469.
18. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-336. doi: 10.1038/nmeth.f.303.
19. Grönlund MM, Gueimonde M, Laitinen K, Kociubinski G, Grönroos T, Salminen S, Isolauri E. Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease. Clin Exp Allergy. 2007;37:1764-1772. doi: 10.1111/j.1365-2222.2007.02849.x.
20. Grangette C. Bifidobacteria and subsets of dendritic cells: friendly players in immune regulation! Gut. 2012;61:331-332. doi: 10.1136/gutjnl-2011-301476.
21. L KA, Li Y, Xu X, Yang W, Liu T, Zhao X, Tang YG, Cai D, Go VL, Pandol S, Hui H. Alterations in fecal Lactobacillus and Bifidobacterium species in type 2 diabetic patients in Southern China population. Front Physiol. 2012;3:496. doi: 10.3389/fphys.2012.00496.
22. Million M, Maraninchi M, Henry M, Armougom F, Richet H, Carrieri P, Valero R, Raccah D, Vialettes B, Raoult D. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes (Lond). 2012;36:817-825. doi: 10.1038/ijo.2011.153.
23. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, Cefalu WT, Ye J. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009;58:1509-1517. doi: 10.2337/db08-1637.
24. Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory t cells. Nature. 2013;504:446-450. doi: 10.1038/nature12721.
25. Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ. Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr. 2004;91:915-923. doi: 10.1079/BJN20041150.
26. Liao TV, Forehand CC, Hess DC, Fagan SC. Minocycline repurposing in critical illness: focus on stroke. Curr Top Med Chem. 2013;13:2283-2290.
27. Shi P, Diez-Freire C, Jun JY, Qi Y, Katovich MJ, Li Q, Sriramula S, Francis J, Sumners C, Raizada MK. Brain microglial cytokines in neurogenic hypertension. Hypertension. 2010;56:297-303. doi: 10.1161/HYPERTENSIONAHA.110.150409.
28. Hu P, Thinschmidt JS, Yan Y, et al. CNS inflammation and bone marrow neuropathy in type 1 diabetes. Am J Pathol. 2013;183:1608-1620. doi: 10.1016/j.ajpath.2013.07.009. doi: 10.1016/j.ajpath.2013.07.009.
29. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118:229-241. doi: 10.1016/j.cell.2004.07.002.
30. Reikvam DH, Erofeev A, Sandvik A, Grcic V, Jahnsen FL, Gaustad P, McCoy KD, Macpherson AJ, Meza-Zepeda LA, Johansen FE. Depletion of murine intestinal microbiota: effects on gut mucosa and epithelial gene expression. PLoS One. 2011;6:e17996. doi: 10.1371/journal. pone.0017996.
31. Million M, Lagier JC, Yahav D, Paul M. Gut bacterial microbiota and obesity. Clin Microbiol Infect. 2013;19:305-313. doi: 10.1111/1469-0691.12172.
32. Seekatz AM, Aas J, Gessert CE, Rubin TA, Saman DM, Bakken JS, Young VB. Recovery of the gut microbiome following fecal microbiota transplantation. MBio. 2014;5:e00893-e00814. doi: 10.1128/mBio.00893-14.
33. Duca FA, Sakar Y, Lepage P, Devime F, Langelier B, Doré J, Covasa M. Replication of obesity and associated signaling pathways through transfer of microbiota from obese-prone rats. Diabetes. 2014;63:1624-1636. doi: 10.2337/db13-1526.
34. Pedersen R, Andersen AD, Mølbak L, Stagsted J, Boye M. Changes in the gut microbiota of cloned and non-cloned control pigs during development of obesity: gut microbiota during development of obesity in cloned pigs. BMC Microbiol. 2013;13:30. doi: 10.1186/1471-2180-13-30.
35. Leclercq S, Matamoros S, Cani PD, Neyrinck AM, Jamar F, Stärkel P, Windey K, Tremaroli V, Bäckhed F, Verbeke K, de Timary P, Delzenne NM. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci U S A. 2014;111:E4485-E4493. doi: 10.1073/pnas.1415174111.
36. Petriz BA, Castro AP, Almeida JA, Gomes CP, Fernandes GR, Kruger RH, Pereira RW, Franco OL. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genomics. 2014;15:511. doi: 10.1186/1471-2164-15-511.
37. Xu J, Ahrén IL, Prykhodko O, Olsson C, Ahrné S, Molin G. Intake of blueberry fermented by lactobacillus plantarum affects the gut microbiota of L-NAME treated rats. Evid Based Complement Alternat Med. 2013;2013:809128. doi: 10.1155/2013/809128.
38. Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55-60. doi: 10.1038/nature11450. doi: 10.1038/nature11450.
39. Jansson PA, Larsson A, Lönnroth PN. Relationship between blood pressure, metabolic variables and blood flow in obese subjects with or without non-insulin-dependent diabetes mellitus. Eur J Clin Invest. 1998;28:813-818.
40. Juraschek SP, Bower JK, Selvin E, Subash Shantha GP, Hoogeveen RC, Ballantyne CM, Young JH. Plasma lactate and incident hypertension in the atherosclerosis risk in communities study. Am J Hypertens. 2015;28:216-224. doi: 10.1093/ajh/hpu117.
41. Vinolo MA, Rodrigues HG, Nachbar RT, Curi R. Regulation of inflammation by short chain fatty acids. Nutrients. 2011;3:858-876. doi: 10.3390/nu3100858.
42. Henagan TM, Stefanska B, Fang Z, Navard AM, Ye J, Lenard NR, Devarshi PP. Sodium butyrate epigenetically modulates high fat diet-induced skeletal muscle mitochondrial adaptation, obesity and insulin resistance through nucleosome positioning [published online ahead of print February 27, 2015]. Br J Pharmacol. doi: 10.1111/bph.13058. http://onlinelibrary.wiley.com/doi/10.1111/bph.13058/full. Accessed April 7, 2015.
43. Lin HV, Frassetto A, Kowalik EJ Jr, Nawrocki AR, Lu MM, Kosinski JR, Hubert JA, Szeto D, Yao X, Forrest G, Marsh DJ. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One. 2012;7:e35240. doi: 10.1371/journal.pone.0035240.
44. Berni Canani R, Di Costanzo M, Leone L. The epigenetic effects of butyrate: potential therapeutic implications for clinical practice. Clin Epigenetics. 2012;4:4. doi: 10.1186/1868-7083-4-4.
45. Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol. 2011;17:1519-1528. doi: 10.3748/wjg.v17. i12. 1519.
46. Vieira EL, Leonel AJ, Sad AP, Beltro NR, Costa TF, Ferreira TM, Gomes-Santos AC, Faria AM, Peluzio MC, Cara DC, Alvarez-Leite JI. Oral administration of sodium butyrate attenuates inflammation and mucosal lesion in experimental acute ulcerative colitis. J Nutr Biochem. 2012;23:430-436. doi: 10.1016/j.jnutbio.2011.01.007.
47. Andrade-Oliveira V, Amano MT, Correa-Costa M, Castoldi A, Felizardo RJ, de Almeida DC, Bassi EJ, Moraes-Vieira PM, Hiyane MI, Rodas AC, Peron JP, Aguiar CF, Reis MA, Ribeiro WR, Valduga CJ, Curi R, Vinolo MA, Ferreira CM, Camara NO. Gut bacteria products prevent aki induced by ischemia-reperfusion [published online ahead of print January 14, 2015]. J Am Soc Nephrol. doi: 10.1681/ASN.2014030288. http://jasn.asnjournals.org/content/early/2015/01/13/ASN.2014030288.long. Accessed April 7, 2015.
48. Pluznick JL, Protzko RJ, Gevorgyan H, et al. Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation. Proc Natl Acad Sci U S A. 2013;110:4410-4415. doi: 10.1073/pnas.1215927110.
49. Garrido-Mesa N, Zarzuelo A, Gálvez J. Minocycline: far beyond an antibiotic. Br J Pharmacol. 2013;169:337-352. doi: 10.1111/bph.12139.
50. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110:9066-9071. doi: 10.1073/pnas.1219451110.
51. Bordin M, DAtri F, Guillemot L, Citi S. Histone deacetylase inhibitors up-regulate the expression of tight junction proteins. Mol Cancer Res. 2004;2:692-701.
52. Garrido-Mesa N, Camuesco D, Arribas B, Comalada M, Bailón E, Cueto-Sola M, Utrilla P, Nieto A, Zarzuelo A, Rodríguez-Cabezas ME, Gálvez J. The intestinal anti-inflammatory effect of minocycline in experimental colitis involves both its immunomodulatory and antimicrobial properties. Pharmacol Res. 2011;63:308-319. doi: 10.1016/j.phrs.2010.12.011.
53. Garrido-Mesa N, Utrilla P, Comalada M, Zorrilla P, Garrido-Mesa J, Zarzuelo A, Rodríguez-Cabezas ME, Gálvez J. The association of minocycline and the probiotic Escherichia coli Nissle 1917 results in an additive beneficial effect in a DSS model of reactivated colitis in mice. Biochem Pharmacol. 2011;82:1891-1900. doi: 10.1016/j.bcp.2011.09.004.
54. Huang TY, Chu HC, Lin YL, Ho WH, Hou HS, Chao YC, Liao CL. Minocycline attenuates 5-fluorouracil-induced small intestinal mucositis in mouse model. Biochem Biophys Res Commun. 2009;389:634-639. doi: 10.1016/j.bbrc.2009.09.041.
55. Galpern WR, Singhal AB. Neuroprotection: lessons from a spectrum of neurological disorders. Int J Stroke. 2006;1:97-99. doi: 10.1111/j.1747-4949.2006.00023.x.
56. Jun JY, Zubcevic J, Qi Y, Afzal A, Carvajal JM, Thinschmidt JS, Grant MB, Mocco J, Raizada MK. Brain-mediated dysregulation of the bone marrow activity in angiotensin II-induced hypertension. Hypertension. 2012;60:1316-1323. doi: 10.1161/HYPERTENSIONAHA.112.199547.
57. Santisteban MM, Zubcevic J, Kim S, Marulanda-Carvajal J, Zingler M, Joseph J, Raizada MK. Iba1+ microglia/macrophages in the rat hypothalamic paraventricular nucleus are both resident and bone marrow-derived in ang ii induced hypertension. FASEB J. 2014;28:1.
58. Katsumoto A, Lu H, Miranda AS, Ransohoff RM. Ontogeny and functions of central nervous system macrophages. J Immunol. 2014;193:2615-2621. doi: 10.4049/jimmunol.1400716.