Angiotensin II-induced hypertension and cardiac hypertrophy are differentially mediated by TLR3- and TLR4-dependent pathways

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 316, Issue 5, 2019, Pages H1027-H1038

  Singh, Madhu V ^a   Cicha, Michael Z ^a   Nunez, Sarah ^a   Meyerholz, David K ^a   Chapleau, Mark W ^a,b   Abboud, François M ^a  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Angiotensin ii; Cardiac hypertrophy; Hypertension; Innate immune system; Myd88; Tlr3; Tlr4; Toll like receptors; Trif

Indexed keywords

ADAPTOR PROTEIN; ANGIOTENSIN II; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; AGTR1A PROTEIN, MOUSE; ANGIOTENSIN 1 RECEPTOR; AUTACOID; TICAM-1 PROTEIN, MOUSE; TLR3 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HEART; HEART VENTRICLE HYPERTROPHY; HYPERTENSION; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; KIDNEY; MALE; MOUSE; NONHUMAN; POST HOC ANALYSIS; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE; WILD TYPE; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CARDIOMEGALY; COMPARATIVE STUDY; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANGIOTENSIN II; ANIMALS; CARDIOMEGALY; DISEASE MODELS, ANIMAL; HYPERTENSION; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; KIDNEY; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; RECEPTOR, ANGIOTENSIN, TYPE 1; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4;

EID: 85065339786     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00697.2018     Document Type: Article

References (66)

1. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738, 2001. doi:10.1038/35099560.
2. An MR, Chung YJ, Kang DG, Nam SC, Lee J. Augmented expression of cardiac atrial natriuretic peptide system in hypertensive rats. J Korean Med Sci 14: 497-501, 1999. doi:10.3346/jkms.1999.14.5.497.
3. Androulidaki A, Wachsmuth L, Polykratis A, Pasparakis M. Differential role of MyD88 and TRIF signaling in myeloid cells in the pathogenesis of autoimmune diabetes. PLoS One 13: e0194048, 2018. doi:10. 1371/journal.pone.0194048.
4. Border WA, Noble NA. Interactions of transforming growth factor-beta and angiotensin II in renal fibrosis. Hypertension 31: 181-188, 1998. doi:10.1161/01.HYP.31.1.181.
5. Bouabout G, Ayme-Dietrich E, Jacob H, Champy MF, Birling MC, Pavlovic G, Madeira L, Fertak LE, Petit-Demoulière B, Sorg T, Herault Y, Mudgett J, Monassier L. Nox4 genetic inhibition in experimental hypertension and metabolic syndrome. Arch Cardiovasc Dis 111:41-52, 2018. doi:10.1016/j.acvd.2017.03.011.
6. Caillon A, Schiffrin EL. Role of inflammation and immunity in hypertension:recent epidemiological, laboratory, and clinical evidence. Curr Hypertens Rep 18: 21, 2016. doi:10.1007/s11906-016-0628-7.
7. Cantin M, Garcia R, Thibault G, Kuchel O, Gutkowska J, Larochelle P, Hamet P, Schiffrin EL, Genest J. Atrial natriuretic factor (ANF) in experimental and human hypertension. Clin Invest Med 10: 561-567, 1987.
8. Case AJ, Zimmerman MC. Sympathetic-mediated activation versus suppression of the immune system: consequences for hypertension. J Physiol 594: 527-536, 2016. doi:10.1113/JP271516.
9. Chen F, Chen D, Zhang Y, Jin L, Zhang H, Wan M, Pan T, Wang X, Su Y, Xu Y, Ye J. Interleukin-6 deficiency attenuates angiotensin IIinduced cardiac pathogenesis with increased myocyte hypertrophy. Biochem Biophys Res Commun 494: 534-541, 2017. doi:10.1016/j.bbrc. 2017.10.119.
10. Chen W, Spitzl A, Mathes D, Nikolaev VO, Werner F, Weirather J, Špiranec K, Röck K, Fischer JW, Kämmerer U, Stegner D, Baba HA, Hofmann U, Frantz S, Kuhn M. Endothelial actions of ANP enhance myocardial inflammatory infiltration in the early phase after acute infarction. Circ Res 119: 237-248, 2016. doi:10.1161/CIRCRESAHA.115. 307196.
11. Cornelius DC, Hogg JP, Scott J, Wallace K, Herse F, Moseley J, Wallukat G, Dechend R, LaMarca B. Administration of interleukin-17 soluble receptor C suppresses TH17 cells, oxidative stress, and hypertension in response to placental ischemia during pregnancy. Hypertension 62:1068-1073, 2013. doi:10.1161/HYPERTENSIONAHA.113.01514.
12. Courtney AH, Lo WL, Weiss A. TCR signaling: mechanisms of initiation and propagation. Trends Biochem Sci 43: 108-123, 2018. doi:10. 1016/j.tibs.2017.11.008.
13. Dange RB, Agarwal D, Masson GS, Vila J, Wilson B, Nair A, Francis J. Central blockade of TLR4 improves cardiac function and attenuates myocardial inflammation in angiotensin II-induced hypertension. Cardiovasc Res 103: 17-27, 2014. doi:10.1093/cvr/cvu067.
14. Dange RB, Agarwal D, Teruyama R, Francis J. Toll-like receptor 4 inhibition within the paraventricular nucleus attenuates blood pressure and inflammatory response in a genetic model of hypertension. J Neuroinflammation 12: 31, 2015. doi:10.1186/s12974-015-0242-7.
15. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, Griendling KK. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med 45: 1340-1351, 2008. doi:10.1016/j.freeradbiomed.2008.08. 013.
16. Fakhouri F, Placier S, Ardaillou R, Dussaule JC, Chatziantoniou C. Angiotensin II activates collagen type I gene in the renal cortex and aorta of transgenic mice through interaction with endothelin and TGF-beta. J Am Soc Nephrol 12: 2701-2710, 2001.
17. Feng W, Chumley P, Hua P, Rezonzew G, Jaimes D, Duckworth MW, Xing D, Jaimes EA. Role of the transcription factor erythroblastosis virus E26 oncogen homolog-1 (ETS-1) as mediator of the renal proinflammatory and profibrotic effects of angiotensin II. Hypertension 60: 1226-1233, 2012. doi:10.1161/HYPERTENSIONAHA.112.197871.
18. Fraser TB, Turner SW, Mangos GJ, Ludbrook J, Whitworth JA. Comparison of telemetric and tail-cuff blood pressure monitoring in adrenocorticotrophic hormone-treated rats. Clin Exp Pharmacol Physiol 28: 831-835, 2001. doi:10.1046/j.1440-1681.2001.03531.x.
19. Goruppi S, Patten RD, Force T, Kyriakis JM. Helix-loop-helix protein p8, a transcriptional regulator required for cardiomyocyte hypertrophy and cardiac fibroblast matrix metalloprotease induction. Mol Cell Biol 27:993-1006, 2007. doi:10.1128/MCB.00996-06.
20. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204: 2449-2460, 2007. doi:10.1084/jem.20070657.
21. Haggerty CM, Mattingly AC, Gong MC, Su W, Daugherty A, Fornwalt BK. Telemetric blood pressure assessment in angiotensin ii-infused ApoE-/-mice: 28 day natural history and comparison to tail-cuff measurements. PLoS One 10: e0130723, 2015. doi:10.1371/journal.pone. 0130723.
22. Harwani SC, Chapleau MW, Legge KL, Ballas ZK, Abboud FM. Neurohormonal modulation of the innate immune system is proinflammatory in the prehypertensive spontaneously hypertensive rat, a genetic model of essential hypertension. Circ Res 111: 1190-1197, 2012. doi:10. 1161/CIRCRESAHA.112.277475.
23. Hu W, Jain A, Gao Y, Dozmorov IM, Mandraju R, Wakeland EK, Pasare C. Differential outcome of TRIF-mediated signaling in TLR4 and TLR3 induced DC maturation. Proc Natl Acad Sci USA 112: 13994-13999, 2015. doi:10.1073/pnas.1510760112.
24. Jain A, Pasare C. Innate control of adaptive immunity: beyond the three-signal paradigm. J Immunol 198: 3791-3800, 2017. doi:10.4049/jimmunol.1602000.
25. Jiang DS, Zhang XF, Gao L, Zong J, Zhou H, Liu Y, Zhang Y, Bian ZY, Zhu LH, Fan GC, Zhang XD, Li H. Signal regulatory protein-α protects against cardiac hypertrophy via the disruption of toll-like receptor 4 signaling. Hypertension 63: 96-104, 2014. doi:10.1161/HYPERTENSIONAHA.113. 01506.
26. Ju X, Ijaz T, Sun H, Ray S, Lejeune W, Lee C, Recinos A III, Guo D-CC, Milewicz DM, Tilton RG, Brasier AR. Interleukin-6-signal transducer and activator of transcription-3 signaling mediates aortic dissections induced by angiotensin II via the T-helper lymphocyte 17-interleukin 17 axis in C57BL/6 mice. Arterioscler Thromb Vasc Biol 33:1612-1621, 2013. doi:10.1161/ATVBAHA.112.301049.
27. Justin Rucker A, Crowley SD. The role of macrophages in hypertension and its complications. Pflugers Arch 469: 419-430, 2017. doi:10.1007/s00424-017-1950-x.
28. Krege JH, Hodgin JB, Hagaman JR, Smithies O. A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 25: 1111-1115, 1995. doi:10.1161/01.HYP.25.5.1111.
29. Krishnan SM, Sobey CG, Latz E, Mansell A, Drummond GR. IL-1β and IL-18: inflammatory markers or mediators of hypertension? Br J Pharmacol 171: 5589-5602, 2014. doi:10.1111/bph.12876.
30. Kurdi M, Booz GW. New take on the role of angiotensin II in cardiac hypertrophy and fibrosis. Hypertension 57: 1034-1038, 2011. doi:10. 1161/HYPERTENSIONAHA.111.172700.
31. Laresgoiti-Servitje E. A leading role for the immune system in the pathophysiology of preeclampsia. J Leukoc Biol 94: 247-257, 2013. doi:10.1189/jlb.1112603.
32. Lee DL, Sturgis LC, Labazi H, Osborne JB Jr, Fleming C, Pollock JS, Manhiani M, Imig JD, Brands MW. Angiotensin II hypertension is attenuated in interleukin-6 knockout mice. Am J Physiol Heart Circ Physiol 290: H935-H940, 2006. doi:10.1152/ajpheart.00708.2005.
33. Matsuda S, Umemoto S, Yoshimura K, Itoh S, Murata T, Fukai T, Matsuzaki M. Angiotensin II activates MCP-1 and induces cardiac hypertrophy and dysfunction via Toll-like receptor 4. J Atheroscler Thromb 22: 833-844, 2015. doi:10.5551/jat.27292.
34. McCarthy CG, Wenceslau CF, Goulopoulou S, Baban B, Matsumoto T, Webb RC. Chloroquine suppresses the development of hypertension in spontaneously hypertensive rats. Am J Hypertens 30: 173-181, 2017. doi:10.1093/ajh/hpw113.
35. McCarthy CG, Wenceslau CF, Goulopoulou S, Ogbi S, Baban B, Sullivan JC, Matsumoto T, Webb RC. Circulating mitochondrial DNA and Toll-like receptor 9 are associated with vascular dysfunction in spontaneously hypertensive rats. Cardiovasc Res 107: 119-130, 2015. doi:10.1093/cvr/cvv137.
36. Mehaffey E, Majid DS. Tumor necrosis factor-α, kidney function, and hypertension. Am J Physiol Renal Physiol 313: F1005-F1008, 2017. doi:10.1152/ajprenal.00535.2016.
37. Meng X, Yang J, Dong M, Zhang K, Tu E, Gao Q, Chen W, Zhang C, Zhang Y. Regulatory T cells in cardiovascular diseases. Nat Rev Cardiol 13: 167-179, 2016. doi:10.1038/nrcardio.2015.169.
38. Montezano AC, Touyz RM. Reactive oxygen species, vascular Noxs, and hypertension: focus on translational and clinical research. Antioxid Redox Signal 20: 164-182, 2014. doi:10.1089/ars.2013.5302.
39. Muñoz-Durango N, Barake MF, Letelier NA, Campino C, Fardella CE, Kalergis AM. Immune system alterations by aldosterone during hypertension: from clinical observations to genomic and non-genomic mechanisms leading to vascular damage. Curr Mol Med 13: 1035-1046, 2013. doi:10.2174/1566524011313060015.
40. Nishida M, Suda R, Nagamatsu Y, Tanabe S, Onohara N, Nakaya M, Kanaho Y, Shibata T, Uchida K, Sumimoto H, Sato Y, Kurose H. Pertussis toxin up-regulates angiotensin type 1 receptors through Toll-like receptor 4-mediated Rac activation. J Biol Chem 285: 15268-15277, 2010. doi:10.1074/jbc.M109.076232.
41. O’Neill LA, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7: 353-364, 2007. doi:10.1038/nri2079.
42. Ogawa K, Hirooka Y, Kishi T, Sunagawa K. Brain AT1 receptor activates the sympathetic nervous system through toll-like receptor 4 in mice with heart failure. J Cardiovasc Pharmacol 58: 543-549, 2011. doi:10.1097/FJC.0b013e31822e6b40.
43. Pasare C, Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Microbes Infect 6: 1382-1387, 2004. doi:10.1016/j.micinf. 2004.08.018.
44. Petkov PM, Cassell MA, Sargent EE, Donnelly CJ, Robinson P, Crew V, Asquith S, Haar RV, Wiles MV. Development of a SNP genotyping panel for genetic monitoring of the laboratory mouse. Genomics 83:902-911, 2004. doi:10.1016/j.ygeno.2003.11.007.
45. Pruijm M, Ponte B, Vollenweider P, Mooser V, Paccaud F, Waeber G, Marques-Vidal P, Burnier M, Bochud M. Not all inflammatory markers are linked to kidney function: results from a population-based study. Am J Nephrol 35: 288-294, 2012. doi:10.1159/000335934.
46. Pushpakumar S, Kundu S, Pryor T, Givvimani S, Lederer E, Tyagi SC, Sen U. Angiotensin-II induced hypertension and renovascular remodelling in tissue inhibitor of metalloproteinase 2 knockout mice. J Hypertens 31: 2270-2281, 2013. doi:10.1097/HJH.0b013e3283649b33.
47. Richards AM, Nicholls MG, Yandle TG, Frampton C, Espiner EA, Turner JG, Buttimore RC, Lainchbury JG, Elliott JM, Ikram H, Crozier IG, Smyth DW. Plasma N-terminal pro-brain natriuretic peptide and adrenomedullin: new neurohormonal predictors of left ventricular function and prognosis after myocardial infarction. Circulation 97: 1921-1929, 1998. doi:10.1161/01.CIR.97.19.1921.
48. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682, 2012. doi:10.1038/nmeth.2019.
49. Sergeeva IA, Hooijkaas IB, Ruijter JM, van der Made I, de Groot NE, van de Werken HJ, Creemers EE, Christoffels VM. Identification of a regulatory domain controlling the Nppa-Nppb gene cluster during heart development and stress. Development 143: 2135-2146, 2016. doi:10. 1242/dev.132019.
50. Singh MV, Abboud FM. Toll-like receptors and hypertension. Am J Physiol Regul Integr Comp Physiol 307: R501-R504, 2014. doi:10.1152/ajpregu.00194.2014.
51. Singh MV, Chapleau MW, Harwani SC, Abboud FM. The immune system and hypertension. Immunol Res 59: 243-253, 2014. doi:10.1007/s12026-014-8548-6.
52. Singh MV, Cicha MZ, Meyerholz DK, Chapleau MW, Abboud FM. Dual activation of TRIF and MyD88 adaptor proteins by angiotensin II evokes opposing effects on pressure, cardiac hypertrophy, and inflammatory gene expression. Hypertension 66: 647-656, 2015. doi:10.1161/HYPERTENSIONAHA.115.06011.
53. Singh MV, Swaminathan PD, Luczak ED, Kutschke W, Weiss RM, Anderson ME. MyD88 mediated inflammatory signaling leads to CaMKII oxidation, cardiac hypertrophy and death after myocardial infarction. J Mol Cell Cardiol 52: 1135-1144, 2012. doi:10.1016/j.yjmcc.2012.01. 021.
54. Sousa T, Oliveira S, Afonso J, Morato M, Patinha D, Fraga S, Carvalho F, Albino-Teixeira A. Role of H(2)O(2) in hypertension, renin-angiotensin system activation and renal medullary disfunction caused by angiotensin II. Br J Pharmacol 166: 2386-2401, 2012. doi:10. 1111/j.1476-5381.2012.01957.x.
55. Squire IB, O’Brien RJ, Demme B, Davies JE, Ng LL. N-terminal pro-atrial natriuretic peptide (N-ANP) and N-terminal pro-B-type natriuretic peptide (N-BNP) in the prediction of death and heart failure in unselected patients following acute myocardial infarction. Clin Sci (Lond) 107: 309-316, 2004. doi:10.1042/CS20040087.
56. 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 51: 1345-1351, 2008. doi:10.1161/HYPERTENSIONAHA.107.102152.
57. Umesalma S, Houwen FK, Baumbach GL, Chan SL. Roles of caveolin-1 in angiotensin ii-induced hypertrophy and inward remodeling of cerebral pial arterioles. Hypertension 67: 623-629, 2016. doi:10.1161/HYPERTENSIONAHA.115.06565.
58. von Vietinghoff S, Ley K. Interleukin 17 in vascular inflammation. Cytokine Growth Factor Rev 21: 463-469, 2010. doi:10.1016/j.cytogfr. 2010.10.003.
59. Wenzel U, Turner JE, Krebs C, Kurts C, Harrison DG, Ehmke H. Immune Mechanisms in Arterial Hypertension. J Am Soc Nephrol 27:677-686, 2016. doi:10.1681/ASN.2015050562.
60. Yaghooti H, Firoozrai M, Fallah S, Khorramizadeh MR. Angiotensin II differentially induces matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 production and disturbs MMP/TIMP balance. Avicenna J Med Biotechnol 2: 79-85, 2010.
61. Yamamoto M, Sato S, Hemmi H, Uematsu S, Hoshino K, Kaisho T, Takeuchi O, Takeda K, Akira S. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat Immunol 4: 1144-1150, 2003. doi:10.1038/ni986.
62. Yao W, Sun Y, Wang X, Niu K. Elevated serum level of interleukin 17 in a population with prehypertension. J Clin Hypertens (Greenwich) 17:770-774, 2015. doi:10.1111/jch.12612.
63. Yoshida T, Yamashita M, Horimai C, Hayashi M. Kruppel-like factor 4 protein regulates isoproterenol-induced cardiac hypertrophy by modulating myocardin expression and activity. J Biol Chem 289: 26107-26118, 2014. doi:10.1074/jbc.M114.582809.
64. Zhang J, Patel MB, Griffiths R, Mao A, Song YS, Karlovich NS, Sparks MA, Jin H, Wu M, Lin EE, Crowley SD. Tumor necrosis factor-α produced in the kidney contributes to angiotensin II-dependent hypertension. Hypertension 64: 1275-1281, 2014. doi:10.1161/HYPERTENSIONAHA.114.03863.
65. Zhang J, Rudemiller NP, Patel MB, Karlovich NS, Wu M, Mc-Donough AA, Griffiths R, Sparks MA, Jeffs AD, Crowley SD. Interleukin-1 receptor activation potentiates salt reabsorption in angiotensin ii-induced hypertension via the NKCC2 co-transporter in the nephron. Cell Metab 23: 360-368, 2016. doi:10.1016/j.cmet.2015.11.013.
66. Zhao QD, Viswanadhapalli S, Williams P, Shi Q, Tan C, Yi X, Bhandari B, Abboud HE. NADPH oxidase 4 induces cardiac fibrosis and hypertrophy through activating Akt/mTOR and NFαB signaling pathways. Circulation 131: 643-655, 2015. doi:10.1161/CIRCULATIONAHA.114. 011079.