Renal denervation prevents immune cell activation and renal inflammation in Angiotensin II-induced hypertension

Circulation Research

Volumn 117, Issue 6, 2015, Pages 547-557

  Xiao, Liang ^a   Kirabo, Annet ^a   Wu, Jing ^a   Saleh, Mohamed A ^a,d   Zhu, Linjue ^a   Wang, Feng ^b   Takahashi, Takamune ^b   Loperena, Roxana ^c   Foss, Jason D ^e   Mernaugh, Raymond L ^c   Chen, Wei ^a   Roberts, Jackson ^a   Osborn, John W ^e   Itani, Hana A ^a   Harrison, David G ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MANSOURA UNIVERSITY   (Egypt)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

dendritic cells; inflammation; lymphocyte; norepinephrine; sympathetic nerve block

Indexed keywords

ANGIOTENSIN II; CATECHOLAMINE; CHEMOKINE RECEPTOR CCR7; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; NORADRENALIN;

ADOPTIVE TRANSFER; ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EFFERENT NERVE; HYPERTENSION; IMMUNOCOMPETENT CELL; KIDNEY DENERVATION; KIDNEY FIBROSIS; KIDNEY NERVE; MOUSE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE; SYMPATHETIC NERVE; T LYMPHOCYTE ACTIVATION; ANIMAL; C57BL MOUSE; CELLULAR IMMUNITY; DRUG EFFECTS; IMMUNOLOGY; INNERVATION; KIDNEY; KNOCKOUT MOUSE; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; SYMPATHECTOMY;

ANGIOTENSIN II; ANIMALS; HYPERTENSION; IMMUNITY, CELLULAR; KIDNEY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RANDOM ALLOCATION; SYMPATHECTOMY;

EID: 84940503305     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.306010     Document Type: Article

References (41)

1. 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 2007 204 2449 2460. doi: 10.1084/jem.20070657
2. Marvar PJ, Thabet SR, Guzik TJ, Lob HE, McCann LA, Weyand C, Gordon FJ, Harrison DG, Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res 2010 107 263 270. doi: 10.1161/CIRCRESAHA.110.217299
3. Crowley SD, Song YS, Lin EE, Griffiths R, Kim HS, Ruiz P, Lymphocyte responses exacerbate angiotensin II-dependent hypertension. Am J Physiol Regul Integr Comp Physiol 2010 298 R1089 R1097. doi: 10.1152/ajpregu.00373.2009
4. Mattson DL, Lund H, Guo C, Rudemiller N, Geurts AM, Jacob H, Genetic mutation of recombination activating gene 1 in Dahl salt-sensitive rats attenuates hypertension and renal damage. Am J Physiol Regul Integr Comp Physiol 2013 304 R407 R414. doi: 10.1152/ajpregu.00304.2012
5. Abbas AK, Lichtman AH, Pillai S, Cellular and Molecular Immunology 2012 Philadelphia, PA Elsevier/Saunders
6. Vinh A, Chen W, Blinder Y, Weiss D, Taylor WR, Goronzy JJ, Weyand CM, Harrison DG, Guzik TJ, Inhibition and genetic ablation of the B7/CD28 T-cell costimulation axis prevents experimental hypertension. Circulation 2010 122 2529 2537. doi: 10.1161/CIRCULATIONAHA.109.930446
7. Kirabo A, Fontana V, de Faria AP, Dc isoketal-modified proteins activate t cells and promote hypertension. J Clin Invest 2014 124 4642 4656. doi: 10.1172/JCI74084
8. Lob HE, Marvar PJ, Guzik TJ, Sharma S, McCann LA, Weyand C, Gordon FJ, Harrison DG, Induction of hypertension and peripheral inflammation by reduction of extracellular superoxide dismutase in the central nervous system. Hypertension 2010 55 277 283. doi: 10.1161/HYPERTENSIONAHA.109.142646
9. 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. doi: 10.1161/HYPERTENSIONAHA.111.00546
10. Ganta CK, Lu N, Helwig BG, Blecha F, Ganta RR, Zheng L, Ross CR, Musch TI, Fels RJ, Kenney MJ, Central angiotensin II-enhanced splenic cytokine gene expression is mediated by the sympathetic nervous system. Am J Physiol Heart Circ Physiol 2005 289 H1683 H1691. doi: 10.1152/ajpheart.00125.2005
11. Grisanti LA, Evanson J, Marchus E, Jorissen H, Woster AP, DeKrey W, Sauter ER, Combs CK, Porter JE, Pro-inflammatory responses in human monocytes are beta1-adrenergic receptor subtype dependent. Mol Immunol 2010 47 1244 1254. doi: 10.1016/j.molimm.2009.12.013
12. Kohm AP, Sanders VM, Norepinephrine and beta 2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol Rev 2001 53 487 525
13. DiBona GF, Esler M, Translational medicine: the antihypertensive effect of renal denervation. Am J Physiol Regul Integr Comp Physiol 2010 298 R245 R253. doi: 10.1152/ajpregu.00647.2009
14. Xu J, Hering D, Sata Y, Walton A, Krum H, Esler MD, Schlaich MP, Renal denervation: current implications and future perspectives. Clin Sci (Lond) 2014 126 41 53. doi: 10.1042/CS20120581
15. Veelken R, Schmieder RE, Renal denervation-implications for chronic kidney disease. Nat Rev Nephrol 2014 10 305 313. doi: 10.1038/nrneph.2014.59
16. Mathis KW, Venegas-Pont M, Flynn ER, Williams JM, Maric-Bilkan C, Dwyer TM, Ryan MJ, Hypertension in an experimental model of systemic lupus erythematosus occurs independently of the renal nerves. Am J Physiol Regul Integr Comp Physiol 2013 305 R711 R719. doi: 10.1152/ajpregu.00602.2012
17. Wang H, Wang J, Guo C, Luo W, Kleiman K, Eitzman DT, Renal denervation attenuates progression of atherosclerosis in apolipoprotein E-deficient mice independent of blood pressure lowering. Hypertension 2015 65 758 765. doi: 10.1161/HYPERTENSIONAHA.114.04648
18. Jakubzick C, Gautier EL, Gibbings SL, Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 2013 39 599 610. doi: 10.1016/j.immuni.2013.08.007
19. Zhang W, Li JL, Hosaka M, Janz R, Shelton JM, Albright GM, Richardson JA, Südhof TC, Victor RG, Cyclosporine A-induced hypertension involves synapsin in renal sensory nerve endings. Proc Natl Acad Sci U S A 2000 97 9765 9770. doi: 10.1073/pnas.170160397
20. Ye S, Ozgur B, Campese VM, Renal afferent impulses, the posterior hypothalamus, and hypertension in rats with chronic renal failure. Kidney Int 1997 51 722 727
21. Campese VM, A new model of neurogenic hypertension caused by renal injury: pathophysiology and therapeutic implications. Clin Exp Nephrol 2003 7 167 171. doi: 10.1007/s10157-003-0238-y
22. Trott DW, Thabet SR, Kirabo A, Saleh MA, Itani H, Norlander AE, Wu J, Goldstein A, Arendshorst WJ, Madhur MS, Chen W, Li CI, Shyr Y, Harrison DG, Oligoclonal CD8+ T cells play a critical role in the development of hypertension. Hypertension 2014 64 1108 1115. doi: 10.1161/HYPERTENSIONAHA.114.04147
23. Satou R, Miyata K, Gonzalez-Villalobos RA, Ingelfinger JR, Navar LG, Kobori H, Interferon-γ biphasically regulates angiotensinogen expression via a JAK-STAT pathway and suppressor of cytokine signaling 1 (SOCS1) in renal proximal tubular cells. FASEB J 2012 26 1821 1830. doi: 10.1096/fj.11-195198
24. Kamat NV, Thabet SR, Xiao L, Saleh MA, Kirabo A, Madhur MS, Delpire E, Harrison DG, McDonough AA, Renal transporter activation during angiotensin-II hypertension is blunted in interferon-γ-/- and interleukin-17A-/- mice. Hypertension 2015 65 569 576. doi: 10.1161/HYPERTENSIONAHA.114.04975
25. Forstermann U, Sessa WC, Nitric oxide synthases: Regulation and function. Eur Heart J 2012 33 829 837, 837a 837d. doi: 10.1093/eurheartj/ehr304
26. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, Feinberg MW, Gerzsten RE, Edelman ER, Jain MK, Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem 2007 282 13769 13779. doi: 10.1074/jbc.M700078200
27. Hishikawa K, Lüscher TF, Pulsatile stretch stimulates superoxide production in human aortic endothelial cells. Circulation 1997 96 3610 3616
28. Riou S, Mees B, Esposito B, Merval R, Vilar J, Stengel D, Ninio E, van Haperen R, de Crom R, Tedgui A, Lehoux S, High pressure promotes monocyte adhesion to the vascular wall. Circ Res 2007 100 1226 1233. doi: 10.1161/01.RES.0000265231.59354.2c
29. Wu J, Thabet SR, Kirabo A, Trott DW, Saleh MA, Xiao L, Madhur MS, Chen W, Harrison DG, Inflammation and mechanical stretch promote aortic stiffening in hypertension through activation of p38 mitogen-activated protein kinase. Circ Res 2014 114 616 625. doi: 10.1161/CIRCRESAHA.114.302157
30. Harrison DG, Guzik TJ, Lob HE, Madhur MS, Marvar PJ, Thabet SR, Vinh A, Weyand CM, Inflammation, immunity, and hypertension. Hypertension 2011 57 132 140. doi: 10.1161/HYPERTENSIONAHA.110.163576
31. Ye S, Gamburd M, Mozayeni P, Koss M, Campese VM, A limited renal injury may cause a permanent form of neurogenic hypertension. Am J Hypertens 1998 11 723 728
32. Deng PY, Yu J, Ye F, Li D, Luo D, Cai WJ, Zhang JW, Luo XG, Deng HW, Li YJ, Interactions of sympathetic nerves with capsaicin-sensitive sensory nerves: neurogenic mechanisms for phenol-induced hypertension in the rat. J Hypertens 2005 23 603 609
33. Burg M, Zahm DS, Knuepfer MM, Intrathecal capsaicin enhances one-kidney renal wrap hypertension in the rat. J Auton Nerv Syst 1994 50 189 199
34. Wu W, Zhang Y, Ballew JR, Fink G, Wang DH, Development of hypertension induced by subpressor infusion of angiotensin II: role of sensory nerves. Hypertension 2000 36 549 552
35. Esler MD, Krum H, Schlaich M, Schmieder RE, Böhm M, Sobotka PA, Symplicity HTN-2 Investigators Renal sympathetic denervation for treatment of drug-resistant hypertension: one-year results from the Symplicity HTN-2 randomized, controlled trial. Circulation 2012 126 2976 2982. doi: 10.1161/CIRCULATIONAHA.112.130880
36. Symplicity HTNI Catheter-based renal sympathetic denervation for resistant hypertension: Durability of blood pressure reduction out to 24 months. Hypertension 2011 57 911 917
37. Böhm M, Mahfoud F, Ukena C, Hoppe UC, Narkiewicz K, Negoita M, Ruilope L, Schlaich MP, Schmieder RE, Whitbourn R, Williams B, Zeymer U, Zirlik A, Mancia G, GSR Investigators First report of the Global SYMPLICITY Registry on the effect of renal artery denervation in patients with uncontrolled hypertension. Hypertension 2015 65 766 774. doi: 10.1161/HYPERTENSIONAHA.114.05010
38. Persu A, Jin Y, Fadl Elmula FE, Jacobs L, Renkin J, Kjeldsen S, Renal denervation after Symplicity HTN-3: an update. Curr Hypertens Rep 2014 16 460. doi: 10.1007/s11906-014-0460-x
39. Bhatt DL, Kandzari DE, O'Neill WW, D'Agostino R, Flack JM, Katzen BT, Leon MB, Liu M, Mauri L, Negoita M, Cohen SA, Oparil S, Rocha-Singh K, Townsend RR, Bakris GL, SYMPLICITY HTN-3 Investigators A controlled trial of renal denervation for resistant hypertension. N Engl J Med 2014 370 1393 1401. doi: 10.1056/NEJMoa1402670
40. Persu A, Renkin J, Thijs L, Staessen JA, Renal denervation: ultima ratio or standard in treatment-resistant hypertension. Hypertension 2012 60 596 606. doi: 10.1161/HYPERTENSIONAHA.112.195263
41. Kandzari DE, Bhatt DL, Brar S, Predictors of blood pressure response in the symplicity htn-3 trial. Eur Heart J 2014 36 219 227. doi: 10.1093/eurheartj/ehu441