Hypertension-Linked Pathophysiological Alterations in the Gut

Circulation Research

Volumn 120, Issue 2, 2017, Pages 312-323

  Santisteban, Monica M ^a   Qi, Yanfei ^b   Zubcevic, Jasenka ^c   Kim, Seungbum ^a   Yang, Tao ^c   Shenoy, Vinayak ^d   Cole Jeffrey, Colleen T ^a   Lobaton, Gilberto O ^a   Stewart, Daniel C ^e   Rubiano, Andres ^e   Simmons, Chelsey S ^b,e   Garcia Pereira, Fernando ^c   Johnson, Richard D ^c   Pepine, Carl J ^b   Raizada, Mohan K ^a  

^a Department of Clinical and Health Psychology   (United States)

^b Division of Cardiovascular Medicine   (United States)

^c Dept of Vet Microbiol and Pathol   (United States)

^d Department of Pharmacy Practice and Science   (United States)

^e University of Florida   (United States)

Author keywords

autonomic nervous system; gut; hypertension; inflammation; intestines; microbiota

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ANGIOTENSIN II; CAPTOPRIL; CD3E PROTEIN; CD68 ANTIGEN; INTERLEUKIN 1BETA; PROTEIN; TIGHT JUNCTION PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASCENDING COLON; BLOOD PRESSURE; BLOOD PRESSURE REGULATION; CD3+ T LYMPHOCYTE; CONTROLLED STUDY; ENTERITIS; ENTEROPATHY; GENE EXPRESSION; GOBLET CELL; HYPERTENSION; HYPOTHALAMUS; INTESTINE MUCOSA PERMEABILITY; INTESTINE PERFUSION; MEAN ARTERIAL PRESSURE; MICROBIAL COMMUNITY; NONHUMAN; PATHOPHYSIOLOGY; PHRENIC NERVE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SMALL INTESTINE; SYMPATHETIC NERVE; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; INTESTINE FLORA; INTESTINE MUCOSA; MALE; METABOLISM; PERMEABILITY; PHYSIOLOGY; SPONTANEOUSLY HYPERTENSIVE RAT; SPRAGUE DAWLEY RAT; WISTAR KYOTO RAT; WISTAR RAT;

ANGIOTENSIN II; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; GASTROINTESTINAL MICROBIOME; HYPERTENSION; INTESTINAL MUCOSA; MALE; PERMEABILITY; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; RATS, WISTAR;

EID: 84994666138     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.309006     Document Type: Article

References (57)

1. Mozaffarian D, Benjamin EJ, Go AS, et al; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation. 2015;131:e29-322. doi: 10.1161/CIR.0000000000000152.
2. CDC. High blood pressure facts | cdc.Gov. 2016. http://www.cdc.gov/bloodpressure/facts.htm.
3. Yoon SS, Carroll MD, Fryar CD. Hypertension prevalence and control among adults: United states, 2011-2014. NCHS Data Brief. 2015:1-8
4. Modolo R, de Faria AP, Sabbatini AR, Barbaro NR, Ritter AM, Moreno H. Refractory and resistant hypertension: characteristics and differences observed in a specialized clinic. J Am Soc Hypertens. 2015;9:397-402. doi: 10.1016/j.jash.2015.03.005.
5. Judd E, Calhoun DA. Apparent and true resistant hypertension: definition, prevalence and outcomes. J Hum Hypertens. 2014;28:463-468. doi: 10.1038/jhh.2013.140.
6. Siddiqui M, Dudenbostel T, Calhoun DA. Resistant and refractory hypertension: antihypertensive treatment resistance vs treatment failure. Can J Cardiol. 2016;32:603-606. doi: 10.1016/j.cjca.2015.06.033.
7. Santisteban MM, Kim S, Pepine CJ, Raizada MK. Brain-gut-bone marrow axis: implications for hypertension and related therapeutics. Circ Res. 2016;118:1327-1336. doi: 10.1161/CIRCRESAHA.116.307709.
8. Grassi G, Mark A, Esler M. The sympathetic nervous system alterations in human hypertension. Circ Res. 2015;116:976-990. doi: 10.1161/CIRCRESAHA.116.303604.
9. DiBona GF. Sympathetic nervous system and hypertension. Hypertension. 2013;61:556-560. doi: 10.1161/HYPERTENSIONAHA.111.00633.
10. Mancia G, Grassi G. The autonomic nervous system and hypertension. Circ Res. 2014;114:1804-1814. doi: 10.1161/CIRCRESAHA.114.302524.
11. Harrison DG. The immune system in hypertension. Trans Am Clin Climatol Assoc. 2014;125:130-38; discussion 138.
12. Zubcevic J, Jun JY, Kim S, Perez PD, Afzal A, Shan Z, Li W, Santisteban MM, Yuan W, Febo M, Mocco J, Feng Y, Scott E, Baekey DM, Raizada MK. Altered inflammatory response is associated with an impaired autonomic input to the bone marrow in the spontaneously hypertensive rat. Hypertension. 2014;63:542-550. doi: 10.1161/HYPERTENSIONAHA.113.02722.
13. Mowat AM, Agace WW. Regional specialization within the intestinal immune system. Nat Rev Immunol. 2014;14:667-685. doi: 10.1038/nri3738.
14. Alexander KL, Targan SR, Elson CO III. Microbiota activation and regulation of innate and adaptive immunity. Immunol Rev. 2014;260:206-220. doi: 10.1111/imr.12180.
15. Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242-249. doi: 10.1038/nature11552.
16. Cervi AL, Lukewich MK, Lomax AE. Neural regulation of gastrointestinal inflammation: role of the sympathetic nervous system. Auton Neurosci. 2014;182:83-88. doi: 10.1016/j.autneu.2013.12.003.
17. Schäper J, Wagner A, Enigk F, Brell B, Mousa SA, Habazettl H, Schäfer M. Regional sympathetic blockade attenuates activation of intestinal macrophages and reduces gut barrier failure. Anesthesiology. 2013;118:134-142. doi: 10.1097/ALN.0b013e3182784c93.
18. Straub RH, Wiest R, Strauch UG, Härle P, Schölmerich J. The role of the sympathetic nervous system in intestinal inflammation. Gut. 2006;55:1640-1649. doi: 10.1136/gut.2006.091322.
19. Lyte M, Vulchanova L, Brown DR. Stress at the intestinal surface: catecholamines and mucosa-bacteria interactions. Cell Tissue Res. 2011;343:23-32. doi: 10.1007/s00441-010-1050-0.
20. 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.
21. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, Xavier RJ, Teixeira MM, Mackay CR. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282-1286. doi: 10.1038/nature08530.
22. Yang T, Santisteban MM, Rodriguez V, Li E, Ahmari N, Carvajal JM, Zadeh M, Gong M, Qi Y, Zubcevic J, Sahay B, Pepine CJ, Raizada MK, Mohamadzadeh M. Gut dysbiosis is linked to hypertension. Hypertension. 2015;65:1331-1340. doi: 10.1161/HYPERTENSIONAHA.115.05315.
23. Mell B, Jala VR, Mathew AV, 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 Genomics. 2015;47:187-197. doi: 10.1152/physiolgenomics.00136.2014.
24. Rubiano A, Qi Y, Guzzo D, Rowe K, Pepine C, Simmons C. Stem cell therapy restores viscoelastic properties of myocardium in rat model of hypertension. J Mech Behav Biomed Mater. 2016;59:71-77. doi: 10.1016/j. jmbbm.2015.11.041.
25. Stewart DC, Rubiano A, Santisteban MM, Shenoy V, Qi Y, Pepine CJ, Raizada MK, Simmons CS. Hypertension-linked mechanical changes of rat gut. Acta Biomater. 2016;45:296-302. doi: 10.1016/j. actbio.2016.08.045.
26. Huynh J, Nishimura N, Rana K, Peloquin JM, Califano JP, Montague CR, King MR, Schaffer CB, Reinhart-King CA. Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med. 2011;3:112ra122. doi: 10.1126/scitranslmed.3002761.
27. Canby CA, Palmer PJ, Wall KR, Tomanek RJ. Effects of captopril on left ventricular structure and function in SHR with established hypertension. Basic Res Cardiol. 1989;84:306-318.
28. Kim S, Kim SY, Pribis JP, Lotze M, Mollen KP, Shapiro R, Loughran P, Scott MJ, Billiar TR. Signaling of high mobility group box 1 (HMGB1) through toll-like receptor 4 in macrophages requires CD14. Mol Med. 2013;19:88-98. doi: 10.2119/molmed.2012.00306.
29. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock. 2006;26:174-179. doi: 10.1097/01. shk.0000225404.51320.82.
30. Palone F, Vitali R, Cucchiara S, Pierdomenico M, Negroni A, Aloi M, Nuti F, Felice C, Armuzzi A, Stronati L. Role of HMGB1 as a suitable biomarker of subclinical intestinal inflammation and mucosal healing in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2014;20:1448-1457. doi: 10.1097/MIB.0000000000000113.
31. Frosali S, Pagliari D, Gambassi G, Landolfi R, Pandolfi F, Cianci R. How the intricate interaction among toll-like receptors, microbiota, and intestinal immunity can influence gastrointestinal pathology. J Immunol Res. 2015;2015:489821. doi: 10.1155/2015/489821.
32. Kim S, Zingler M, Harrison JK, Scott EW, Cogle CR, Luo D, Raizada MK. Angiotensin II regulation of proliferation, differentiation, and engraftment of hematopoietic stem cells. Hypertension. 2016;67:574-584. doi: 10.1161/HYPERTENSIONAHA.115.06474.
33. Santisteban MM, Ahmari N, Carvajal JM, Zingler MB, Qi Y, Kim S, Joseph J, Garcia-Pereira F, Johnson RD, Shenoy V, Raizada MK, Zubcevic J. Involvement of bone marrow cells and neuroinflammation in hypertension. Circ Res. 2015;117:178-191. doi: 10.1161/CIRCRESAHA.117.305853.
34. Granger DN, Holm L, Kvietys P. The gastrointestinal circulation: physiology and pathophysiology. Compr Physiol. 2015;5:1541-1583. doi: 10.1002/cphy.c150007.
35. Sugahara H, Odamaki T, Fukuda S, Kato T, Xiao JZ, Abe F, Kikuchi J, Ohno H. Probiotic Bifidobacterium longum alters gut luminal metabolism through modification of the gut microbial community. Sci Rep. 2015;5:13548. doi: 10.1038/srep13548.
36. Fukuda S, Toh H, Hase K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469:543-547. doi: 10.1038/nature09646.
37. Pickering AE, Paton JF. A decerebrate, artificially-perfused in situ preparation of rat: utility for the study of autonomic and nociceptive processing. J Neurosci Methods. 2006;155:260-271. doi: 10.1016/j. jneumeth.2006.01.011.
38. Zubcevic J, Potts JT. Role of GABAergic neurones in the nucleus tractus solitarii in modulation of cardiovascular activity. Exp Physiol. 2010;95:909-918. doi: 10.1113/expphysiol.2010.054007.
39. Zoccal DB, Simms AE, Bonagamba LG, Braga VA, Pickering AE, Paton JF, Machado BH. Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J Physiol. 2008;586:3253-3265. doi: 10.1113/jphysiol.2008.154187.
40. Simms AE, Paton JF, Allen AM, Pickering AE. Is augmented central respiratory-sympathetic coupling involved in the generation of hypertension? Respir Physiol Neurobiol. 2010;174:89-97. doi: 10.1016/j. resp.2010.07.010.
41. Tsuda K, Tsuda S, Ura M, Shima H, Nishio I, Masuyama Y. Inhibitory actions of captopril on norepinephrine release from adrenergic nerve endings in spontaneously hypertensive rats. Jpn Heart J. 1988;29:475-483.
42. Richer C, Doussau MP, Giudicelli JF. Postsynaptic alpha adrenoceptors and attenuation of vascular sympathetic responses in SHRs by captopril and enalapril. Eur Heart J. 1983;4(suppl G):55-60.
43. Wall R, Cryan JF, Ross RP, Fitzgerald GF, Dinan TG, Stanton C. Bacterial neuroactive compounds produced by psychobiotics. Adv Exp Med Biol. 2014;817:221-239. doi: 10.1007/978-1-4939-0897-4-10.
44. Lyte M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. Bioessays. 2011;33:574-581. doi: 10.1002/bies.201100024.
45. Özogul F. Effects of specific lactic acid bacteria species on biogenic amine production by foodborne pathogen. Int J Food Sci Technol. 2011;46:478-484.
46. Rossi F, Gardini F, Rizzotti L, La Gioia F, Tabanelli G, Torriani S. Quantitative analysis of histidine decarboxylase gene (hdcA) transcription and histamine production by Streptococcus thermophilus PRI60 under conditions relevant to cheese making. Appl Environ Microbiol. 2011;77:2817-2822. doi: 10.1128/AEM.02531-10.
47. Kandler O. Carbohydrate metabolism in lactic acid bacteria. Antonie Van Leeuwenhoek. 1983;49:209-224.
48. Tsai YT, Cheng PC, Pan TM. The immunomodulatory effects of lactic acid bacteria for improving immune functions and benefits. Appl Microbiol Biotechnol. 2012;96:853-862. doi: 10.1007/s00253-012-4407-3.
49. Schiffrin EJ, Brassart D, Servin AL, Rochat F, Donnet-Hughes A. Immune modulation of blood leukocytes in humans by lactic acid bacteria: criteria for strain selection. Am J Clin Nutr. 1997;66:515S-520S.
50. Iraporda C, Errea A, Romanin DE, Cayet D, Pereyra E, Pignataro O, Sirard JC, Garrote GL, Abraham AG, Rumbo M. Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiology. 2015;220:1161-1169. doi: 10.1016/j.imbio.2015.06.004.
51. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014;111:2247-2252. doi: 10.1073/pnas.1322269111.
52. Karbach SH, Schonfelder T, Brandao I, Wilms E, Hormann N, Jackel S, Schuler R, Finger S, Knorr M, Lagrange J, Brandt M, Waisman A, Kossmann S, Schafer K, Munzel T, Reinhardt C, Wenzel P. Gut microbiota promote angiotensin ii-induced arterial hypertension and vascular dysfunction. J Am Heart Assoc. 2016;5
53. Durgan DJ, Ganesh BP, Cope JL, Ajami NJ, Phillips SC, Petrosino JF, Hollister EB, Bryan RM Jr. Role of the Gut Microbiome in Obstructive Sleep Apnea-Induced Hypertension. Hypertension. 2016;67:469-474. doi: 10.1161/HYPERTENSIONAHA.115.06672.
54. Mayer EA, Knight R, Mazmanian SK, Cryan JF, Tillisch K. Gut microbes and the brain: paradigm shift in neuroscience. J Neurosci. 2014;34:15490-15496. doi: 10.1523/JNEUROSCI.3299-14.2014.
55. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125:926-938. doi: 10.1172/JCI76304.
56. Forsythe P, Kunze WA. Voices from within: gut microbes and the CNS. Cell Mol Life Sci. 2013;70:55-69. doi: 10.1007/s00018-012-1028-z.
57. Matteoli G, Gomez-Pinilla PJ, Nemethova A, Di Giovangiulio M, Cailotto C, van Bree SH, Michel K, Tracey KJ, Schemann M, Boesmans W, Vanden Berghe P, Boeckxstaens GE. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut. 2014;63:938-948. doi: 10.1136/gutjnl-2013-304676.