Central blockade of TLR4 improves cardiac function and attenuates myocardial inflammation in angiotensin II-induced hypertension

Cardiovascular Research

Volumn 103, Issue 1, 2014, Pages 17-27

  Dange, Rahul B ^a   Agarwal, Deepmala ^a,b   Masson, Gustavo S ^a,c   Vila, Jorge ^a   Wilson, Brad ^a   Nair, Anand ^a   Francis, Joseph ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Angiotensin II; Cytokines; Hypertension; NF B; TLR4

Indexed keywords

ANGIOTENSIN II; ANTIINFLAMMATORY AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INHIBITOR PROTEIN; INTERLEUKIN 1BETA; NORADRENALIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRAL INHIBITORY PEPTIDE; ANTIHYPERTENSIVE AGENT; MESSENGER RNA; NITRIC OXIDE SYNTHASE; TLR4 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; HEART FUNCTION; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HYPERTENSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; M MODE ECHOCARDIOGRAPHY; MALE; MEAN ARTERIAL PRESSURE; MYOCARDITIS; NONHUMAN; NORADRENALIN BLOOD LEVEL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SYMPATHETIC TONE; TELEMETRY; TRANSTHORACIC ECHOCARDIOGRAPHY; BLOOD PRESSURE MEASUREMENT; DISEASE COURSE; ENZYME ACTIVITY; EVALUATION STUDY; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CARDIOMEGALY; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANGIOTENSIN II; ANIMALS; BLOOD PRESSURE; BRAIN; CARDIOMEGALY; HYPERTENSION; INTERLEUKIN-1BETA; MALE; MYOCARDITIS; NF-KAPPA B; NITRIC OXIDE SYNTHASE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; RENIN-ANGIOTENSIN SYSTEM; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84904003624     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu067     Document Type: Article

References (49)

1. Sriramula S, Haque M, Majid DS, Francis J. Involvement of tumor necrosis factor-alpha in angiotensin II-mediated effects on salt appetite, hypertension, and cardiac hypertrophy. Hypertension 2008;51:1345-1351.
2. Theuer J, Dechend R, Muller DN, Park JK, Fiebeler A, Barta P, Ganten D, Haller H, Dietz R, Luft FC. Angiotensin II induced inflammation in the kidney and in the heart of double transgenic rats. BMC Cardiovasc Disord 2002;2:3.
3. Muller DN, Dechend R, Mervaala EM, Park JK, Schmidt F, Fiebeler A, Theuer J, Breu V, Ganten D, Haller H, Luft FC. NF-kb inhibition ameliorates angiotensin II-induced inflammatory damage in rats. Hypertension 2000;35:193-201.
4. Coban E, Nizam I, Topal C, Akar Y. The association of low-grade systemic inflammation with hypertensive retinopathy. Clin Exp Hypertens 2010;32:528-531.
5. Agarwal D, Welsch MA, Keller JN, Francis J. Chronic exercise modulates Ras components and improves balance between pro-and anti-inflammatory cytokines in the brain of shr. Basic Res Cardiol 2011;106:1069-1085.
6. Welsh P,Woodward M, Rumley A, Lowe G. Associations of circulating TNFalpha and IL-18 with myocardial infarction and cardiovascular risk markers: The Glasgow myocardial infarction study. Cytokine 2009;47:143-147.
7. Hong HJ, Loh SH, Yen MH. Suppression of the development of hypertension by the inhibitor of inducible nitric oxide synthase. Br J Pharmacol 2000;131:631-637.
8. Agarwal D, Dange RB, Vila J, Otamendi AJ, Francis J. Detraining differentially preserved beneficial effects of exercise on hypertension: effects on blood pressure, cardiac function, brain inflammatory cytokines and oxidative stress. PLoS ONE 2012;7:e52569.
9. Cardinale JP, Sriramula S, Pariaut R, GuggilamA, Mariappan N, Elks CM, Francis J.HDAC inhibition attenuates inflammatory, hypertrophic, and hypertensive responses in spontaneously hypertensive rats. Hypertension 2010;56:437-444.
10. Kang YM, He RL, Yang LM, Qin DN, Guggilam A, Elks C, Yan N, Guo Z, Francis J. Brain tumour necrosis factor-alpha modulates neurotransmitters in hypothalamic paraventricular nucleus in heart failure. Cardiovasc Res 2009;83:737-746.
11. Bubici C, Papa S, Dean K, Franzoso G. Mutual cross-talk between reactive oxygen species and nuclear factor-kappa b: molecular basis and biological significance. Oncogene 2006; 25:6731-6748.
12. Cardinale JP, Sriramula S, Mariappan N, Agarwal D, Francis J. Angiotensin II-induced hypertension is modulated by nuclear factor-kappa b in the paraventricular nucleus. Hypertension 2012;59:113-121.
13. 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.
14. Davisson RL, Oliverio MI, Coffman TM, Sigmund CD. Divergent functions of angiotensin II receptor isoforms in the brain. J Clin Invest 2000;106:103-106.
15. Shi Z, Gan XB, Fan ZD, Zhang F, Zhou YB, Gao XY,DeW, Zhu GQ. Inflammatory cytokines in paraventricular nucleus modulate sympathetic activity and cardiac sympathetic afferent reflex in rats. Acta Physiol (Oxf) 2011;203:289-297.
16. Sriramula S, Cardinale JP, Francis J. Inhibition of TNF in the brain reverses alterations in Ras components and attenuates angiotensin II-induced hypertension. PLoS ONE 2013;8: e63847.
17. Lob HE, Schultz D, Marvar PJ, Davisson RL, Harrison DG. Role of the NADPH oxidases in the subfornical organ in angiotensin II-induced hypertension. Hypertension 2013;61: 382-387.
18. Baumgarten G, Knuefermann P, Nozaki N, Sivasubramanian N, Mann DL, Vallejo JG. In vivo expression of proinflammatory mediators in the adult heart after endotoxin administration: the role of Toll-like receptor-4. J Infect Dis 2001;183:1617-1624.
19. Medzhitov R, Preston-Hurlburt P, JanewayCAJr.Ahuman homologue of the drosophila Toll protein signals activation of adaptive immunity. Nature 1997;388:394-397.
20. Rock FL, Hardiman G, Timans JC, Kastelein RA, Bazan JF. A family of human receptors structurally related to drosophila Toll. Proc Natl Acad Sci USA 1998;95:588-593.
21. HedayatM, Netea MG, Rezaei N. Targeting of Toll-like receptors: a decade of progress in combating infectious diseases. Lancet Infect Dis 2011;11:702-712.
22. Salomao R, Brunialti MK, Rapozo MM, Baggio-Zappia GL, Galanos C, Freudenberg M. Bacterial sensing, cell signaling, and modulation of the immune response during sepsis. Shock 2012;38:227-242.
23. Akira S. Toll-like receptor signaling. J Biol Chem 2003;278:38105-38108.
24. Sales ML, Schreiber R, Ferreira-Sae MC, Fernandes MN, Piveta CS, Cipolli JA, Cardoso CC, Matos-Souza JR, Geloneze B, Franchini KG, NadruzWJr. Toll-like receptor 6 ser249pro polymorphism is associated with lower left ventricular wall thickness and inflammatory response in hypertensive women. Am J Hypertens 2010;23:649-654.
25. Holloway JW, Yang IA, Ye S. Variation in the Toll-like receptor 4 gene and susceptibility to myocardial infarction. Pharmacogenet Genomics 2005;15:15-21.
26. Kolek MJ, Carlquist JF, Muhlestein JB, Whiting BM, Horne BD, Bair TL, Anderson JL. Tolllike receptor 4 gene asp299gly polymorphism is associated with reductions in vascular inflammation, angiographic coronary artery disease, and clinical diabetes. Am Heart J 2004;148:1034-1040.
27. Dhandapani S, Dhandapani M, Agarwal M, Chutani AM, Subbiah V, Sharma BS, Mahapatra AK. The prognostic significance of the timing of total enteral feeding in traumatic brain injury. Surg Neurol Int 2012;3:31.
28. Cardinale JP, Sriramula S, Mariappan N, Agarwal D, Francis J. Angiotensin ii-induced hypertension is modulated by nuclear factor-kappa b in the paraventricular nucleus. Hypertension 2012;59:113-U282.
29. Agarwal D, Haque M, Sriramula S, Mariappan N, Pariaut R, Francis J. Role of proinflammatory cytokines and redox homeostasis in exercise-induced delayed progression of hypertension in spontaneously hypertensive rats. Hypertension 2009;54:1393-1400.
30. Pellett AA, Tolar WG, Merwin DG, Kerut EK. The Tei index: methodology and disease state values. Echocardiography 2004;21:669-672.
31. Avlas O, Fallach R, Shainberg A, Porat E, Hochhauser E. Toll-like receptor 4 stimulation initiates an inflammatory response that decreases cardiomyocyte contractility. Antioxid Redox Signal 2011;15:1895-1909.
32. Frantz S, Kobzik L, Kim YD, Fukazawa R, Medzhitov R, Lee RT, Kelly RA. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J Clin Invest 1999; 104:271-280.
33. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, MattsonMP. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci USA 2007;104:13798-13803.
34. OgawaK, HirookaY, KishiT, IdeT, SunagawaK. Partially silencing brain Toll-like receptor 4 prevents in part left ventricular remodeling with sympathoinhibition in rats with myocardial infarction-induced heart failure. PLoS ONE 2013;8:e69053.
35. Elsik CG, Tellam RL,Worley KC, Gibbs RA, Muzny DM,Weinstock GM, Adelson DL, Eichler EE, Elnitski L, Guigo R, Hamernik DL, Kappes SM, Lewin HA, Lynn DJ, Nicholas FW, Reymond A, Rijnkels M, Skow LC, Zdobnov EM, Schook L, Womack J, Alioto T, Antonarakis SE, Astashyn A, Chapple CE, Chen HC, Chrast J, Camara F, Ermolaeva O, Henrichsen CN, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Kokocinski F, Landrum M, Maglott D, Pruitt K, Sapojnikov V, Searle SM, Solovyev V, Souvorov A, Ucla C, Wyss C, Anzola JM, Gerlach D, Elhaik E, Graur D, Reese JT, Edgar RC, McEwan JC, Payne GM, Raison JM, Junier T, Kriventseva EV, Eyras E, Plass M, Donthu R, Larkin DM, Reecy J, Yang MQ, Chen L, Cheng Z, Chitko-McKown CG, Liu GE, Matukumalli LK, Song J, Zhu B, Bradley DG, Brinkman FS, Lau LP, Whiteside MD, Walker A, Wheeler TT, Casey T, German JB, Lemay DG, Maqbool NJ, Molenaar AJ, Seo S, Stothard P, Baldwin CL, Baxter R, Brinkmeyer-Langford CL, Brown WC, Childers CP, Connelley T, Ellis SA, Fritz K, Glass EJ, Herzig CT, Iivanainen A, Lahmers KK, Bennett AK, Dickens CM, Gilbert JG, Hagen DE, Salih H, Aerts J, Caetano AR, Dalrymple B, Garcia JF, Gill CA, Hiendleder SG, Memili E, Spurlock D, Williams JL, Alexander L, Brownstein MJ, Guan L, Holt RA, Jones SJ, Marra MA, Moore R, Moore SS, Roberts A, Taniguchi M, Waterman RC, Chacko J, Chandrabose MM, Cree A, Dao MD, Dinh HH, Gabisi RA, Hines S, Hume J, Jhangiani SN, Joshi V, Kovar CL, Lewis LR, Liu YS, Lopez J, Morgan MB, Nguyen NB, Okwuonu GO, Ruiz SJ, Santibanez J, Wright RA, Buhay C, Ding Y, Dugan-Rocha S, Herdandez J, Holder M, Sabo A, Egan A, Goodell J, Wilczek-Boney K, Fowler GR, Hitchens ME, Lozado RJ, Moen C, Steffen D, Warren JT, Zhang J, Chiu R, Schein JE, Durbin KJ, Havlak P, Jiang H, Liu Y, Qin X, Ren Y, Shen Y, Song H, Bell SN, Davis C, Johnson AJ, Lee S, Nazareth LV, Patel BM, Pu LL, Vattathil S, Williams RL Jr, Curry S, Hamilton C, Sodergren E, Wheeler DA, Barris W, Bennett GL, Eggen A, Green RD, Harhay GP, Hobbs M, Jann O, Keele JW, Kent MP, Lien S, McKay SD, McWilliam S, Ratnakumar A, Schnabel RD, Smith T, Snelling WM, Sonstegard TS, Stone RT, Sugimoto Y, Takasuga A, Taylor JF, Van Tassell CP, Macneil MD, Abatepaulo AR, Abbey CA, Ahola V, Almeida IG, Amadio AF, Anatriello E, Bahadue SM, Biase FH, Boldt CR, Carroll JA, CarvalhoWA, Cervelatti EP, Chacko E, Chapin JE, Cheng Y, Choi J, Colley AJ, de Campos TA, De Donato M, Santos IK, de Oliveira CJ, Deobald H, Devinoy E, Donohue KE, Dovc P, Eberlein A, Fitzsimmons CJ, Franzin AM, Garcia GR, Genini S, Gladney CJ, Grant JR, Greaser ML, Green JA, Hadsell DL, Hakimov HA, Halgren R, Harrow JL, Hart EA, Hastings N, Hernandez M, Hu ZL, Ingham A, Iso-Touru T, Jamis C, Jensen K, Kapetis D, Kerr T, Khalil SS, Khatib H, Kolbehdari D, Kumar CG, Kumar D, Leach R, Lee JC, Li C, Logan KM, Malinverni R, Marques E, Martin WF, Martins NF, Maruyama SR, Mazza R, McLean KL, Medrano JF, Moreno BT, More DD, Muntean CT, Nandakumar HP, Nogueira MF, Olsaker I, Pant SD, Panzitta F, Pastor RC, Poli MA, Poslusny N, Rachagani S, Ranganathan S, Razpet A, Riggs PK, Rincon G, Rodriguez-Osorio N, Rodriguez-Zas SL, Romero NE, Rosenwald A, Sando L, Schmutz SM, Shen L, Sherman L, Southey BR, Lutzow YS, Sweedler JV, Tammen I, Telugu BP, Urbanski JM, Utsunomiya YT, Verschoor CP, Waardenberg AJ, Wang Z, Ward R, Weikard R, Welsh TH Jr, White SN, Wilming LG, Wunderlich KR, Yang J, Zhao FQ. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 2009; 324:522-528.
36. Boissiere J, Eder V, Machet MC, Courteix D, Bonnet P. Moderate exercise training does not worsen left ventricle remodeling and function in untreated severe hypertensive rats. J Appl Physiol 2008;104:321-327.
37. Ha T, Liu L, Kelley J, Kao R, WilliamsD, Li C. Toll-like receptors: new players in myocardial ischemia/reperfusion injury. Antioxid Redox Signal 2011;15:1875-1893.
38. Rysa J, Leskinen H, Ilves M, Ruskoaho H. Distinct upregulation of extracellular matrix genes in transition from hypertrophy to hypertensive heart failure. Hypertension 2005; 45:927-933.
39. Edwards KM, Ziegler MG, Mills PJ. The potential anti-inflammatory benefits of improving physical fitness in hypertension. J Hypertens 2007;25:1533-1542.
40. Shimamoto A, Chong AJ, Yada M, Shomura S, Takayama H, Fleisig AJ, Agnew ML, Hampton CR, Rothnie CL, Spring DJ, Pohlman TH, Shimpo H, Verrier ED. Inhibition of Toll-like receptor 4 with eritoran attenuates myocardial ischemia-reperfusion injury. Circulation 2006;114:I270-I274.
41. Dias FA, Urboniene D, Yuzhakova MA, Biesiadecki BJ, Pena JR, Goldspink PH, Geenen DL, Wolska BM. Ablation of iNOS delays cardiac contractile dysfunction in chronic hypertension. Front Biosci (Elite Ed) 2010;2:312-324.
42. Danilczyk U, Penninger JM. Angiotensin-converting enzyme ii in the heart and the kidney. Circ Res 2006;98:463-471.
43. Zimmerman MC, Lazartigues E, SharmaRV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res 2004;95:210-216.
44. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 2007;292:C82-C97.
45. Murdoch CE, Alom-Ruiz SP,Wang M, ZhangM,Walker S, Yu B, BrewerA, Shah AM. Role of endothelial Nox2 NADPH oxidase in angiotensin II-induced hypertension and vasomotor dysfunction. Basic Res Cardiol 2011;106:527-538.
46. Fu YC, Chi CS, Yin SC, Hwang B, Chiu YT, Hsu SL. Norepinephrine induces apoptosis in neonatal rat cardiomyocytes through a reactive oxygen species-TNF alpha-caspase signaling pathway. Cardiovasc Res 2004;62:558-567.
47. GuptaMK,NeelakantanTV, SanghamitraM,Tyagi RK, DindaA,Maulik S,MukhopadhyayCK, Goswami SK. An assessment of the role of reactive oxygen species and redox signaling in norepinephrine-induced apoptosis and hypertrophy of H9c2 cardiac myoblasts. Antioxid Redox Signal 2006;8:1081-1093.
48. Aceros H, Farah G, Cobos-Puc L, Stabile AM, Noiseux N, Mukaddam-Daher S. Moxonidine improves cardiac structure and performance in SHR through inhibition of cytokines, p38 MAPK and Akt. Br J Pharmacol 2011;164:946-957.
49. Kang YM, GaoF, LiHH,Cardinale JP, Elks C, Zang WJ,Yu XJ,XuYY,Qi J, YangQ, Francis J. NF-kappab in the paraventricular nucleus modulates neurotransmitters and contributes to sympathoexcitation in heart failure. Basic Res Cardiol 2011;106:1087-1097.