Dendritic cells and isolevuglandins in immunity, inflammation, and hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 312, Issue 3, 2017, Pages H368-H374

  Dixon, Kala B ^a   Davies, Sean S ^a,b   Kirabo, Annet ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dendritic cells; Hypertension; Isolevuglandins; Neoantigens

Indexed keywords

ANTIGEN; ISOLEVUGLANDIN; NEOANTIGEN; PROSTAGLANDIN; UNCLASSIFIED DRUG; CYTOKINE;

ADAPTIVE IMMUNITY; CARDIOVASCULAR DISEASE; CELLULAR IMMUNITY; CROSS PRESENTATION; DENDRITIC CELL; HUMAN; HYPERTENSION; INFLAMMATION; INNATE IMMUNITY; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; COMPLICATION; IMMUNITY; IMMUNOLOGY; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; CYTOKINES; DENDRITIC CELLS; HUMANS; HYPERTENSION; IMMUNITY; INFLAMMATION; PROSTAGLANDINS;

EID: 85014437940     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00603.2016     Document Type: Review

References (87)

1. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 4: 499-511, 2004. doi:10.1038/nri1391.
2. Benko S, Philpott DJ, Girardin SE. The microbial and danger signals that activate Nod-like receptors. Cytokine 43: 368-373, 2008. doi:10.1016/j.cyto.2008.07.013.
3. Birmingham K. Ralph Steinman. Nat Med 7: 1078, 2001. doi:10.1038/nm1001-1078.
4. Bomfim GF, Dos Santos RA, Oliveira MA, Giachini FR, Akamine EH, Tostes RC, Fortes ZB, Webb RC, Carvalho MH. Toll-like receptor 4 contributes to blood pressure regulation and vascular contraction in spontaneously hypertensive rats. Clin Sci (Lond) 122: 535-543, 2012. doi:10.1042/CS20110523.
5. Brame CJ, Salomon RG, Morrow JD, Roberts LJ II. Identification of extremely reactive γ-ketoaldehydes (isolevuglandins) as products of the isoprostane pathway and characterization of their lysyl protein adducts. J Biol Chem 274: 13139-13146, 1999. doi:10.1074/jbc.274.19.13139.
6. Case AJ, Zimmerman MC. Redox-regulated suppression of splenic T-lymphocyte activation in a model of sympathoexcitation. Hypertension 65: 916-923, 2015. doi:10.1161/HYPERTENSIONAHA.114.05075.
7. 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.
8. - dendritic cell subsets differ in their cytokine production profiles, susceptibilities to transfection, and capacities to direct Th cell differentiation. J Immunol 165: 3584-3591, 2000. doi:10.4049/jimmunol.165.7.3584.
9. Chobanian AV. Shattuck Lecture. The hypertension paradox—more uncontrolled disease despite improved therapy. N Engl J Med 361: 878-887, 2009. doi:10.1056/NEJMsa0903829.
10. Christ A, Temmerman L, Legein B, Daemen MJ, Biessen EA. Dendritic cells in cardiovascular diseases: epiphenomenon, contributor, or therapeutic opportunity. Circulation 128: 2603-2613, 2013. doi:10.1161/CIRCULATIONAHA.113.003364.
11. Clemente-Casares X, Blanco J, Ambalavanan P, Yamanouchi J, Singha S, Fandos C, Tsai S, Wang J, Garabatos N, Izquierdo C, Agrawal S, Keough MB, Yong VW, James E, Moore A, Yang Y, Stratmann T, Serra P, Santamaria P. Expanding antigen-specific regulatory networks to treat autoimmunity. Nature 530: 434-440, 2016. doi:10.1038/nature16962.
12. 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 298: R1089-R1097, 2010. doi:10.1152/ajpregu.00373.2009.
13. Cullen SJ, Ponnappan S, Ponnappan U. Proteasome inhibition upregulates inflammatory gene transcription induced by an atypical pathway of NF-κB activation. Biochem Pharmacol 79: 706-714, 2010. doi:10.1016/j.bcp.2009.10.006.
14. Daissormont IT, Christ A, Temmerman L, Sampedro Millares S, Seijkens T, Manca M, Rousch M, Poggi M, Boon L, van der Loos C, Daemen M, Lutgens E, Halvorsen B, Aukrust P, Janssen E, Biessen EA. Plasmacytoid dendritic cells protect against atherosclerosis by tuning T-cell proliferation and activity. Circ Res 109: 1387-1395, 2011. doi:10.1161/CIRCRESAHA.111.256529.
15. Davies SS, Amarnath V, Montine KS, Bernoud-Hubac N, Boutaud O, Montine TJ, Roberts LJ II. Effects of reactive γ-ketoaldehydes formed by the isoprostane pathway (isoketals) and cyclooxygenase pathway (levuglandins) on proteasome function. FASEB J 16: 715-717, 2002. doi:10.1096/fj.01-0696fje.
16. Denoeud J, Moser M. Role of CD27/CD70 pathway of activation in immunity and tolerance. J Leukoc Biol 89: 195-203, 2011. doi:10.1189/jlb.0610351.
17. Deo SH, Jenkins NT, Padilla J, Parrish AR, Fadel PJ. Norepinephrine increases NADPH oxidase-derived superoxide in human peripheral blood mononuclear cells via α-adrenergic receptors. Am J Physiol Regul Integr Comp Physiol 305: R1124-R1132, 2013. doi:10.1152/ajpregu.00347.2013.
18. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, Buck DW, Schmitz J. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 165: 6037-6046, 2000. doi:10.4049/jimmunol.165.11.6037.
19. Feau S, Garcia Z, Arens R, Yagita H, Borst J, Schoenberger SP. The CD4+ T-cell help signal is transmitted from APC to CD8+ T-cells via CD27-CD70 interactions. Nat Commun 3: 948, 2012. doi:10.1038/ncomms1948.
20. Fritz JH, Ferrero RL, Philpott DJ, Girardin SE. Nod-like proteins in immunity, inflammation and disease. Nat Immunol 7: 1250-1257, 2006. doi:10.1038/ni1412.
21. Goulopoulou S, McCarthy CG, Webb RC. Toll-like receptors in the vascular system: sensing the dangers within. Pharmacol Rev 68: 142-167, 2016. doi:10.1124/pr.114.010090.
22. 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.
23. Heart Protection Study Collaborative Group. MRC/BHF Heart Protection Study of antioxidant vitamin supplementation in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet 360: 23-33, 2002. doi:10.1016/S0140-6736(02)09328-5.
24. Heath WR, Carbone FR. Cross-presentation in viral immunity and selftolerance. Nat Rev Immunol 1: 126-134, 2001. doi:10.1038/35100512.
25. Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol 19: 47-64, 2001. doi:10.1146/annurev.immunol.19.1.47.
26. Huan T, Meng Q, Saleh MA, Norlander AE, Joehanes R, Zhu J, Chen BH, Zhang B, Johnson AD, Ying S, Courchesne P, Raghavachari N, Wang R, Liu P, O’Donnell CJ, Vasan R, Munson PJ, Madhur MS, Harrison DG, Yang X, Levy D. Integrative network analysis reveals molecular mechanisms of blood pressure regulation. Mol Syst Biol 11: 799, 2015. doi:10.15252/msb.20145399.
27. Itani HA, Xiao L, Saleh MA, Wu J, Pilkinton MA, Dale BL, Barbaro NR, Foss JD, Kirabo A, Montaniel KR, Norlander AE, Chen W, Sato R, Navar LG, Mallal SA, Madhur MS, Bernstein KE, Harrison DG. CD70 exacerbates blood pressure elevation and renal damage in response to repeated hypertensive stimuli. Circ Res 118: 1233-1243, 2016. doi:10.1161/CIRCRESAHA.115.308111.
28. Iyer RS, Ghosh S, Salomon RG. Levuglandin E2 crosslinks proteins. Prostaglandins 37: 471-480, 1989. doi:10.1016/0090-6980(89)90096-8.
29. Julius S, Nesbitt SD, Egan BM, Weber MA, Michelson EL, Kaciroti N, Black HR, Grimm RH Jr, Messerli FH, Oparil S, Schork MA; Trial of Preventing Hypertension (TROPHY) Study Investigators. Feasibility of treating prehypertension with an angiotensin-receptor blocker. N Engl J Med 354: 1685-1697, 2006. doi:10.1056/NEJMoa060838.
30. Kirabo A, Fontana V, de Faria AP, Loperena R, Galindo CL, Wu J, Bikineyeva AT, Dikalov S, Xiao L, Chen W, Saleh MA, Trott DW, Itani HA, Vinh A, Amarnath V, Amarnath K, Guzik TJ, Bernstein KE, Shen XZ, Shyr Y, Chen SC, Mernaugh RL, Laffer CL, Elijovich F, Davies SS, Moreno H, Madhur MS, Roberts J II, Harrison DG. DC isoketal-modified proteins activate T cells and promote hypertension. J Clin Invest 124: 4642-4656, 2014. doi:10.1172/JCI74084.
31. Kleinewietfeld M, Manzel A, Titze J, Kvakan H, Yosef N, Linker RA, Muller DN, Hafler DA. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496: 518-522, 2013. doi:10.1038/nature11868.
32. Kopp C, Linz P, Dahlmann A, Hammon M, Jantsch J, Müller DN, Schmieder RE, Cavallaro A, Eckardt KU, Uder M, Luft FC, Titze J. 23Na magnetic resonance imaging-determined tissue sodium in healthy subjects and hypertensive patients. Hypertension 61: 635-640, 2013. doi:10.1161/HYPERTENSIONAHA.111.00566.
33. Kretzschmar D, Betge S, Windisch A, Pistulli R, Rohm I, Fritzenwanger M, Jung C, Schubert K, Theis B, Petersen I, Drobnik S, Mall G, Figulla HR, Yilmaz A. Recruitment of circulating dendritic cell precursors into the infarcted myocardium and pro-inflammatory response in acute myocardial infarction. Clin Sci (Lond) 123: 387-398, 2012. doi:10.1042/CS20110561.
34. Lam GY, Huang J, Brumell JH. The many roles of NOX2 NADPH oxidase-derived ROS in immunity. Semin Immunopathol 32: 415-430, 2010. doi:10.1007/s00281-010-0221-0.
35. Lenfant C, Chobanian AV, Jones DW, Roccella EJ; Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Seventh report of the Joint National Committee on the Prevention, Detection, Evaluation, and Treatment of High Blood Pressure (JNC 7): resetting the hypertension sails. Hypertension 41: 1178-1179, 2003. doi:10.1161/01.HYP.0000075790.33892.AE.
36. Lonn E, Bosch J, Yusuf S, Sheridan P, Pogue J, Arnold JM, Ross C, Arnold A, Sleight P, Probstfield J, Dagenais GR; HOPE and HOPETOO Trial Investigators. Effects of long-term vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial. JAMA 293: 1338-1347, 2005. doi:10.1001/jama.293.11.1338.
37. Lonn E, Yusuf S, Dzavik V, Doris C, Yi Q, Smith S, Moore-Cox A, Bosch J, Riley W, Teo K; SECURE Investigators. Effects of ramipril and vitamin E on atherosclerosis: the study to evaluate carotid ultrasound changes in patients treated with ramipril and vitamin E (SECURE). Circulation 103: 919-925, 2001. doi:10.1161/01.CIR.103.7.919.
38. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN. Characterization of human blood dendritic cell subsets. Blood 100: 4512-4520, 2002. doi:10.1182/blood-2001-11-0097.
39. Madhur MS, Lob HE, McCann LA, Iwakura Y, Blinder Y, Guzik TJ, Harrison DG. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 55: 500-507, 2010. doi:10.1161/HYPERTENSIONAHA.109.145094.
40. Mantegazza AR, Magalhaes JG, Amigorena S, Marks MS. Presentation of phagocytosed antigens by MHC class I and II. Traffic 14: 135-152, 2013. doi:10.1111/tra.12026.
41. Martín-Fontecha A, Sebastiani S, Höpken UE, Uguccioni M, Lipp M, Lanzavecchia A, Sallusto F. Regulation of dendritic cell migration to the draining lymph node. J Exp Med 198: 615-621, 2003. doi:10.1084/jem.20030448.
42. McCarthy CG, Goulopoulou S, Wenceslau CF, Spitler K, Matsumoto T, Webb RC. Toll-like receptors and damage-associated molecular patterns: novel links between inflammation and hypertension. Am J Physiol Heart Circ Physiol 306: H184-H196, 2014. doi:10.1152/ajpheart.00328.2013.
43. McCarthy CG, Webb RC. The toll of the gridiron: damage-associated molecular patterns and hypertension in American football. FASEB J 30: 34-40, 2016. doi:10.1096/fj.15-279588.
44. McMaster WG, Kirabo A, Madhur MS, Harrison DG. Inflammation, immunity, and hypertensive end-organ damage. Circ Res 116: 1022-1033, 2015. doi:10.1161/CIRCRESAHA.116.303697.
45. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826, 2007. doi:10.1038/nature06246.
46. Ménard HA, Lapointe E, Rochdi MD, Zhou ZJ. Insights into rheumatoid arthritis derived from the Sa immune system. Arthritis Res 2: 429-432, 2000. doi:10.1186/ar122.
47. Merad M, Sathe P, Helft J, Miller J, Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31: 563-604, 2013. doi:10.1146/annurev-immunol-020711-074950.
48. Mervaala E, Müller DN, Park JK, Dechend R, Schmidt F, Fiebeler A, Bieringer M, Breu V, Ganten D, Haller H, Luft FC. Cyclosporin A protects against angiotensin II-induced end-organ damage in double transgenic rats harboring human renin and angiotensinogen genes. Hypertension 35: 360-366, 2000. doi:10.1161/01.HYP.35.1.360.
49. Morrow JD, Hill KE, Burk RF, Nammour TM, Badr KF, Roberts LJ II. A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism. Proc Natl Acad Sci USA 87: 9383-9387, 1990. doi:10.1073/pnas.87.23.9383.
50. Muller DN, Shagdarsuren E, Park JK, Dechend R, Mervaala E, Hampich F, Fiebeler A, Ju X, Finckenberg P, Theuer J, Viedt C, Kreuzer J, Heidecke H, Haller H, Zenke M, Luft FC. Immunosuppressive treatment protects against angiotensin II-induced renal damage. Am J Pathol 161: 1679-1693, 2002. doi:10.1016/S0002-9440(10)64445-8.
51. Mydel P, Wang Z, Brisslert M, Hellvard A, Dahlberg LE, Hazen SL, Bokarewa M. Carbamylation-dependent activation of T cells: a novel mechanism in the pathogenesis of autoimmune arthritis. J Immunol 184: 6882-6890, 2010. doi:10.4049/jimmunol.1000075.
52. Narayan KM, Ali MK, Koplan JP. Global noncommunicable diseases— where worlds meet. N Engl J Med 363: 1196-1198, 2010. doi:10.1056/NEJMp1002024.
53. Nataraj C, Oliverio MI, Mannon RB, Mannon PJ, Audoly LP, Amuchastegui CS, Ruiz P, Smithies O, Coffman TM. Angiotensin II regulates cellular immune responses through a calcineurin-dependent pathway. J Clin Invest 104: 1693-1701, 1999. doi:10.1172/JCI7451.
54. Niessner A, Sato K, Chaikof EL, Colmegna I, Goronzy JJ, Weyand CM. Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-α. Circulation 114: 2482-2489, 2006. doi:10.1161/CIRCULATIONAHA.106.642801.
55. Niessner A, Shin MS, Pryshchep O, Goronzy JJ, Chaikof EL, Weyand CM. Synergistic proinflammatory effects of the antiviral cytokine interferon-α and Toll-like receptor 4 ligands in the atherosclerotic plaque. Circulation 116: 2043-2052, 2007. doi:10.1161/CIRCULATIONAHA.107.697789.
56. Norlander AE, Saleh MA, Kamat NV, Ko B, Gnecco J, Zhu L, Dale BL, Iwakura Y, Hoover RS, McDonough AA, Madhur MS. Interleukin-17A regulates renal sodium transporters and renal injury in angiotensin II-induced hypertension. Hypertension 68: 167-174, 2016. doi:10.1161/HYPERTENSIONAHA.116.07493.
57. O’Keeffe M, Mok WH, Radford KJ. Human dendritic cell subsets and function in health and disease. Cell Mol Life Sci 72: 4309-4325, 2015. doi:10.1007/s00018-015-2005-0.
58. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S, Ahn K. Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127: 369-382, 2006. doi:10.1016/j.cell.2006.08.041.
59. Paul K, Kretzschmar D, Yilmaz A, Bärthlein B, Titze S, Wolf G, Busch M; GCKD-Study Investigators. Circulating dendritic cell precursors in chronic kidney disease: a cross-sectional study. BMC Nephrol 14: 274, 2013. doi:10.1186/1471-2369-14-274.
60. Piccioli D, Tavarini S, Borgogni E, Steri V, Nuti S, Sammicheli C, Bardelli M, Montagna D, Locatelli F, Wack A. Functional specialization of human circulating CD16 and CD1c myeloid dendritic-cell subsets. Blood 109: 5371-5379, 2007. doi:10.1182/blood-2006-08-038422.
61. Rapola JM, Virtamo J, Ripatti S, Huttunen JK, Albanes D, Taylor PR, Heinonen OP. Randomised trial of α-tocopherol and β-carotene supplements on incidence of major coronary events in men with previous myocardial infarction. Lancet 349: 1715-1720, 1997. doi:10.1016/S0140-6736(97)01234-8.
62. Roberts LJ II, Oates JA, Linton MF, Fazio S, Meador BP, Gross MD, Shyr Y, Morrow JD. The relationship between dose of vitamin E and suppression of oxidative stress in humans. Free Radic Biol Med 43: 1388-1393, 2007. doi:10.1016/j.freeradbiomed.2007.06.019.
63. Saleh MA, McMaster WG, Wu J, Norlander AE, Funt SA, Thabet SR, Kirabo A, Xiao L, Chen W, Itani HA, Michell D, Huan T, Zhang Y, Takaki S, Titze J, Levy D, Harrison DG, Madhur MS. Lymphocyte adaptor protein LNK deficiency exacerbates hypertension and end-organ inflammation. J Clin Invest 125: 1189-1202, 2015. doi:10.1172/JCI76327.
64. Salomon RG, Miller DB. Levuglandins: isolation, characterization, and total synthesis of new secoprostanoid products from prostaglandin endoperoxides. Adv Prostaglandin Thromboxane Leukot Res 15: 323-326, 1985.
65. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2: 151-161, 2002. doi:10.1038/nri746.
66. Stephens NG, Parsons A, Brown MJ, Schofield PM, Kelly F, Cheeseman K, Mitchinson MJ. Randomised controlled trial of vitamin E in patients with coronary disease: Cambridge Heart Antioxidant Study (CHAOS). Lancet 347: 781-786, 1996. doi:10.1016/S0140-6736(96)90866-1.
67. Takeuchi O, Akira S. Innate immunity to virus infection. Immunol Rev 227: 75-86, 2009. doi:10.1111/j.1600-065X.2008.00737.x.
68. Thompson JA, Webb RC. Potential role of Toll-like receptors in programming of vascular dysfunction. Clin Sci (Lond) 125: 19-25, 2013. doi:10.1042/CS20120673.
69. Tian M, Zhang Y, Liu Z, Sun G, Mor G, Liao A. The PD-1/PD-L1 inhibitory pathway is altered in pre-eclampsia and regulates T cell responses in pre-eclamptic rats. Sci Rep 6: 27683, 2016. doi:10.1038/srep27683.
70. 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 64: 1108-1115, 2014. doi:10.1161/HYPERTENSIONAHA.114.04147.
71. 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 122: 2529-2537, 2010. doi:10.1161/CIRCULATIONAHA.109.930446.
72. Virtamo J, Rapola JM, Ripatti S, Heinonen OP, Taylor PR, Albanes D, Huttunen JK. Effect of vitamin E and beta carotene on the incidence of primary nonfatal myocardial infarction and fatal coronary heart disease. Arch Intern Med 158: 668-675, 1998. doi:10.1001/archinte.158.6.668.
73. Vivekananthan DP, Penn MS, Sapp SK, Hsu A, Topol EJ. Use of antioxidant vitamins for the prevention of cardiovascular disease: metaanalysis of randomised trials. Lancet 361: 2017-2023, 2003. doi:10.1016/S0140-6736(03)13637-9.
74. Widder JD, Harrison DG. Can vitamin E prevent cardiovascular events and cancer? Nat Clin Pract Cardiovasc Med 2: 510-511, 2005. doi:10.1038/ncpcardio0291.
75. Wu C, Yosef N, Thalhamer T, Zhu C, Xiao S, Kishi Y, Regev A, Kuchroo VK. Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 496: 513-517, 2013. doi:10.1038/nature11984.
76. Wu J, Saleh MA, Kirabo A, Itani HA, Montaniel KR, Xiao L, Chen W, Mernaugh RL, Cai H, Bernstein KE, Goronzy JJ, Weyand CM, Curci JA, Barbaro NR, Moreno H, Davies SS, Roberts LJ II, Madhur MS, Harrison DG. Immune activation caused by vascular oxidation promotes fibrosis and hypertension. J Clin Invest 126: 50-67, 2016. doi:10.1172/JCI80761.
77. Xiao L, Kirabo A, Wu J, Saleh MA, Zhu L, Wang F, Takahashi T, Loperena R, Foss JD, Mernaugh RL, Chen W, Roberts J II, Osborn JW, Itani HA, Harrison DG. Renal denervation prevents immune cell activation and renal inflammation in angiotensin II-induced hypertension. Circ Res 117: 547-557, 2015. doi:10.1161/CIRCRESAHA.115.306010.
78. Yilmaz A, Dietel B, Cicha I, Schubert K, Hausmann R, Daniel WG, Garlichs CD, Stumpf C. Emergence of dendritic cells in the myocardium after acute myocardial infarction-implications for inflammatory myocardial damage. Int J Biomed Sci 6: 27-36, 2010.
79. Yilmaz A, Fuchs T, Dietel B, Altendorf R, Cicha I, Stumpf C, Schellinger PD, Blümcke I, Schwab S, Daniel WG, Garlichs CD, Kollmar R. Transient decrease in circulating dendritic cell precursors after acute stroke: potential recruitment into the brain. Clin Sci (Lond) 118: 147-157, 2009. doi:10.1042/CS20090154.
80. + T cells in coronary artery lesions in patients with Kawasaki disease. Exp Mol Pathol 83: 93-103, 2007. doi:10.1016/j.yexmp.2007.01.007.
81. Yilmaz A, Schaller T, Cicha I, Altendorf R, Stumpf C, Klinghammer L, Ludwig J, Daniel WG, Garlichs CD. Predictive value of the decrease in circulating dendritic cell precursors in stable coronary artery disease. Clin Sci (Lond) 116: 353-363, 2009. doi:10.1042/CS20080392.
82. Yilmaz A, Weber J, Cicha I, Stumpf C, Klein M, Raithel D, Daniel WG, Garlichs CD. Decrease in circulating myeloid dendritic cell precursors in coronary artery disease. J Am Coll Cardiol 48: 70-80, 2006. doi:10.1016/j.jacc.2006.01.078.
83. Yoon PW, Gillespie CD, George MG, Wall HK; Centers for Disease Control and Prevention (CDC). Control of hypertension among adults— National Health and Nutrition Examination Survey, United States, 2005-2008. MMWR Suppl 61: 19-25, 2012.
84. Yusuf S, Dagenais G, Pogue J, Bosch J, Sleight P; The Heart Outcomes Prevention Evaluation Study Investigators. Vitamin E supplementation and cardiovascular events in high-risk patients. N Engl J Med 342: 154-160, 2000. doi:10.1056/NEJM200001203420302.
85. 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.
86. Zhang Q, Vignali DA. Co-stimulatory and co-inhibitory pathways in autoimmunity. Immunity 44: 1034-1051, 2016. doi:10.1016/j.immuni.2016.04.017.
87. Zhang Y, Zhang C. Role of dendritic cells in cardiovascular diseases. World J Cardiol 2: 357-364, 2010. doi:10.4330/wjc.v2.i11.357.