Skip to main content

Advertisement

SpringerLink
Log in

The Role of Type 1 Angiotensin Receptors on T Lymphocytes in Cardiovascular and Renal Diseases

  • Hypertension and the Kidney (RM Carey and A Mimran, Section Editors)
  • Published:
Current Hypertension Reports Aims and scope Submit manuscript

Abstract

The renin–angiotensin system plays a critical role in the pathogenesis of several cardiovascular diseases, largely through activation of type I angiotensin (AT1) receptors by angiotensin II. Treatment with AT1 receptor blockers (ARBs) is a proven successful intervention for hypertension and progressive heart and kidney disease. However, the divergent actions of AT1 receptors on individual cell lineages in hypertension may present novel opportunities to optimize the therapeutic benefits of ARBs. For example, T lymphocytes make important contributions to the induction and progression of various cardiovascular diseases, but new experiments indicate that activation of AT1 receptors on T cells paradoxically limits inflammation and target organ damage in hypertension. Future studies should illustrate how these discrepant functions of AT1 receptors in target organs versus mononuclear cells can be exploited for the benefit of patients with recalcitrant hypertension and other cardiovascular diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Published papers of particular interest have been highlighted as: • Of importance •• Of major importance

  1. Probstfield JL, O'Brien KD. Progression of cardiovascular damage: the role of renin-angiotensin system blockade. Am J Cardiol. 2010;105:10A–20A.

    Article  PubMed  CAS  Google Scholar 

  2. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol. 2007;292:C82–97.

    Article  PubMed  CAS  Google Scholar 

  3. Crowley SD, Tharaux PL, Audoly LP, et al. Exploring type I angiotensin (AT1) receptor functions through gene targeting. Acta Physiol Scand. 2004;181:561–70.

    Article  PubMed  CAS  Google Scholar 

  4. Yusuf S, Teo KK, Pogue J, et al. Telmisartan, ramipril, or both in patients at high risk for vascular events. N Engl J Med. 2008;358:1547–59.

    Article  PubMed  CAS  Google Scholar 

  5. Mann JF, Schmieder RE, McQueen M, et al. Renal outcomes with telmisartan, ramipril, or both, in people at high vascular risk (the ONTARGET study): a multicentre, randomised, double-blind, controlled trial. Lancet. 2008;372:547–53.

    Article  PubMed  CAS  Google Scholar 

  6. Ito M, Oliverio MI, Mannon PJ, et al. Regulation of blood pressure by the type 1A angiotensin II receptor gene. Proc Natl Acad Sci U S A. 1995;92:3521–5.

    Article  PubMed  CAS  Google Scholar 

  7. Harada K, Sugaya T, Murakami K, et al. Angiotensin II type 1A receptor knockout mice display less left ventricular remodeling and improved survival after myocardial infarction. Circulation. 1999;100:2093–9.

    Article  PubMed  CAS  Google Scholar 

  8. Wassmann S, Czech T, van Eickels M, et al. Inhibition of diet-induced atherosclerosis and endothelial dysfunction in apolipoprotein E/angiotensin II type 1A receptor double-knockout mice. Circulation. 2004;110:3062–7.

    Article  PubMed  CAS  Google Scholar 

  9. Crowley SD, Gurley SB, Herrera MJ, et al. Angiotensin II causes hypertension and cardiac hypertrophy through its receptors in the kidney. Proc Natl Acad Sci U S A. 2006;103:17985–90.

    Article  PubMed  CAS  Google Scholar 

  10. Crowley SD, Gurley SB, Oliverio MI, et al. Distinct roles for the kidney and systemic tissues in blood pressure regulation by the renin-angiotensin system. J Clin Invest. 2005;115:1092–9.

    PubMed  CAS  Google Scholar 

  11. de Gasparo M, Catt KJ, Inagami T, et al. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev. 2000;52:415–72.

    PubMed  Google Scholar 

  12. Kobori H, Nangaku M, Navar LG, et al. The intrarenal renin-angiotensin system: from physiology to the pathobiology of hypertension and kidney disease. Pharmacol Rev. 2007;59:251–87.

    Article  PubMed  CAS  Google Scholar 

  13. Daugherty A, Rateri DL, Lu H, et al. Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the AT1A receptor. Circulation. 2004;110:3849–57.

    Article  PubMed  CAS  Google Scholar 

  14. Nickenig G, Jung O, Strehlow K, et al. Hypercholesterolemia is associated with enhanced angiotensin AT1-receptor expression. Am J Physiol. 1997;272:H2701–7.

    PubMed  CAS  Google Scholar 

  15. Warnholtz A, Nickenig G, Schulz E, et al. Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system. Circulation. 1999;99:2027–33.

    Article  PubMed  CAS  Google Scholar 

  16. Caligiuri G, Paulsson G, Nicoletti A, et al. Evidence for antigen-driven T-cell response in unstable angina. Circulation. 2000;102:1114–9.

    Article  PubMed  CAS  Google Scholar 

  17. Stemme S, Faber B, Holm J, et al. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci U S A. 1995;92:3893–7.

    Article  PubMed  CAS  Google Scholar 

  18. Candido R, Allen TJ, Lassila M, et al. Irbesartan but not amlodipine suppresses diabetes-associated atherosclerosis. Circulation. 2004;109:1536–42.

    Article  PubMed  CAS  Google Scholar 

  19. Yusuf S, Sleight P, Pogue J, et al. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med. 2000;342:145–53.

    Article  PubMed  CAS  Google Scholar 

  20. Zhai P, Yamamoto M, Galeotti J, et al. Cardiac-specific overexpression of AT1 receptor mutant lacking G alpha q/G alpha i coupling causes hypertrophy and bradycardia in transgenic mice. J Clin Invest. 2005;115:3045–56.

    Article  PubMed  CAS  Google Scholar 

  21. Effect of ramipril on mortality and morbidity of survivors of acute myocardial infarction with clinical evidence of heart failure. The Acute Infarction Ramipril Efficacy (AIRE) Study Investigators. Lancet. 1993;342:821-8.

  22. Pfeffer MA, McMurray JJ, Velazquez EJ, et al. Valsartan, captopril, or both in myocardial infarction complicated by heart failure, left ventricular dysfunction, or both. N Engl J Med. 2003;349:1893–906.

    Article  PubMed  CAS  Google Scholar 

  23. Liu YH, Yang XP, Sharov VG, et al. Effects of angiotensin-converting enzyme inhibitors and angiotensin II type 1 receptor antagonists in rats with heart failure. Role of kinins and angiotensin II type 2 receptors. J Clin Invest. 1997;99:1926–35.

    Article  PubMed  CAS  Google Scholar 

  24. Schieffer B, Wirger A, Meybrunn M, et al. Comparative effects of chronic angiotensin-converting enzyme inhibition and angiotensin II type 1 receptor blockade on cardiac remodeling after myocardial infarction in the rat. Circulation. 1994;89:2273–82.

    Article  PubMed  CAS  Google Scholar 

  25. Gottlieb SS, Dickstein K, Fleck E, et al. Hemodynamic and neurohormonal effects of the angiotensin II antagonist losartan in patients with congestive heart failure. Circulation. 1993;88:1602–9.

    Article  PubMed  CAS  Google Scholar 

  26. Dickstein K, Chang P, Willenheimer R, et al. Comparison of the effects of losartan and enalapril on clinical status and exercise performance in patients with moderate or severe chronic heart failure. J Am Coll Cardiol. 1995;26:438–45.

    Article  PubMed  CAS  Google Scholar 

  27. Pitt B, Poole-Wilson PA, Segal R, et al. Effect of losartan compared with captopril on mortality in patients with symptomatic heart failure: randomised trial–the Losartan Heart Failure Survival Study ELITE II. Lancet. 2000;355:1582–7.

    Article  PubMed  CAS  Google Scholar 

  28. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685–95.

    Article  PubMed  CAS  Google Scholar 

  29. Guzik TJ, Hoch NE, Brown KA, et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med. 2007;204:2449–60. This landmark study demonstrated a definitive role for T lymphocytes in the pathogenesis of hypertension.

    Article  PubMed  CAS  Google Scholar 

  30. Muller DN, Shagdarsuren E, Park JK, et al. Immunosuppressive treatment protects against angiotensin II-induced renal damage. Am J Pathol. 2002;161:1679–93. This exhaustive study incorporated multiple immunosuppressive approaches to define a role for T lymphocytes in driving target organ damage during hypertension.

    Article  PubMed  CAS  Google Scholar 

  31. Okuda T, Grollman A. Passive transfer of autoimmune induced hypertension in the rat by lymph node cells. Tex Rep Biol Med. 1967;25:257–64.

    PubMed  CAS  Google Scholar 

  32. Bataillard A, Freiche JC, Vincent M, et al. Antihypertensive effect of neonatal thymectomy in the genetically hypertensive LH rat. Thymus. 1986;8:321–30.

    PubMed  CAS  Google Scholar 

  33. Crowley SD, Frey CW, Gould SK, et al. Stimulation of lymphocyte responses by angiotensin II promotes kidney injury in hypertension. Am J Physiol Ren Physiol. 2008;295:F515–24.

    Article  CAS  Google Scholar 

  34. Crowley SD, Song YS, Lin EE, et al. Lymphocyte responses exacerbate angiotensin II-dependent hypertension. Am J Physiol Regul Integr Comp Physiol. 2010;298:R1089–97.

    Article  PubMed  CAS  Google Scholar 

  35. Shao J, Nangaku M, Miyata T, et al. Imbalance of T-cell subsets in angiotensin II-infused hypertensive rats with kidney injury. Hypertension. 2003;42:31–8.

    Article  PubMed  CAS  Google Scholar 

  36. Sriramula S, Haque M, Majid DS, et al. Involvement of tumor necrosis factor-alpha in angiotensin II-mediated effects on salt appetite, hypertension, and cardiac hypertrophy. Hypertension. 2008;51:1345–51.

    Article  PubMed  CAS  Google Scholar 

  37. Marvar PJ, Thabet SR, Guzik TJ, et al. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res. 2010;107:263–70. This novel set of experiments probes interactions between the central nervous system, the vasculature, and T lymphocytes during the hypertensive response.

    Article  PubMed  CAS  Google Scholar 

  38. Kang YM, Ma Y, Elks C, et al. Cross-talk between cytokines and renin-angiotensin in hypothalamic paraventricular nucleus in heart failure: role of nuclear factor-kappaB. Cardiovasc Res. 2008;79:671–8.

    Article  PubMed  CAS  Google Scholar 

  39. Thabet SR, Wu J, Chen W et al. The Role Of CD8+ T cells, IP-10 And MMP12 In Hypertension. 65th High Blood Pressure Research Conference Conference 2011; Orlando, FL2011. p. 109. These experiments implicate CD8 + cytotoxic T cells in driving blood pressure elevation.

  40. Zhang JD, Patel MB, Song YS, et al. A novel role for type 1 Angiotensin receptors on T lymphocytes to limit target organ damage in hypertension. Circ Res. 2012;110:1604–17. This recent study revealed an unusal protective role of the angiotensin receptor on T lymphocytes in hypertension by using conditional gene deletion.

    Article  PubMed  CAS  Google Scholar 

  41. Madhur MS, Lob HE, McCann LA, et al. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension. 2010;55:500–7. These experiments explore the contributions of Th17 cells to hypertension and vascular damage.

    Article  PubMed  CAS  Google Scholar 

  42. Kasal DA, Barhoumi T, Li MW, et al. T regulatory lymphocytes prevent aldosterone-induced vascular injury. Hypertension. 2012;59:324–30.

    Article  PubMed  CAS  Google Scholar 

  43. Barhoumi T, Kasal DA, Li MW, et al. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension. 2011;57:469–76. This was the first study to suggest that T regulatory cells could blunt the chronic hypertensive response to Ang II.

    Article  PubMed  CAS  Google Scholar 

  44. Schiffrin EL. T lymphocytes: a role in hypertension? Curr Opin Nephrol Hypertens. 2010;19:181–6.

    Article  PubMed  CAS  Google Scholar 

  45. Kvakan H, Kleinewietfeld M, Qadri F, et al. Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation. 2009;119:2904–12. In this study, adoptive transfer of T regulatory cells protected against hypertensive cardiac injury through a blood pressure-independent mechanism.

    Article  PubMed  CAS  Google Scholar 

  46. Hansson GK, Holm J, Jonasson L. Detection of activated T lymphocytes in the human atherosclerotic plaque. Am J Pathol. 1989;135:169–75.

    PubMed  CAS  Google Scholar 

  47. Zhou X, Nicoletti A, Elhage R, et al. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation. 2000;102:2919–22. These key experiments illustrated how CD4 + T cells potentiate the development of atherosclerosis.

    Article  PubMed  CAS  Google Scholar 

  48. Zhou X, Stemme S, Hansson GK. Evidence for a local immune response in atherosclerosis. CD4+ T cells infiltrate lesions of apolipoprotein-E-deficient mice. Am J Pathol. 1996;149:359–66.

    PubMed  CAS  Google Scholar 

  49. Gupta S, Pablo AM, Jiang X, et al. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest. 1997;99:2752–61.

    Article  PubMed  CAS  Google Scholar 

  50. Lee TS, Yen HC, Pan CC, et al. The role of interleukin 12 in the development of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 1999;19:734–42.

    Article  PubMed  CAS  Google Scholar 

  51. Whitman SC, Ravisankar P, Daugherty A. Interleukin-18 enhances atherosclerosis in apolipoprotein E(-/-) mice through release of interferon-gamma. Circ Res. 2002;90:E34–8.

    Article  PubMed  CAS  Google Scholar 

  52. Buono C, Binder CJ, Stavrakis G, et al. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci U S A. 2005;102:1596–601.

    Article  PubMed  CAS  Google Scholar 

  53. de Boer OJ, van der Meer JJ, Teeling P, et al. Differential expression of interleukin-17 family cytokines in intact and complicated human atherosclerotic plaques. J Pathol. 2010;220:499–508.

    PubMed  Google Scholar 

  54. Erbel C, Chen L, Bea F, et al. Inhibition of IL-17A attenuates atherosclerotic lesion development in apoE-deficient mice. J Immunol. 2009;183:8167–75.

    Article  PubMed  CAS  Google Scholar 

  55. Smith E, Prasad KM, Butcher M, et al. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2010;121:1746–55.

    Article  PubMed  CAS  Google Scholar 

  56. Butcher MJ, Gjurich BN, Phillips T, et al. The IL-17A/IL-17RA axis plays a proatherogenic role via the regulation of aortic myeloid cell recruitment. Circ Res. 2012;110:675–87.

    Article  PubMed  CAS  Google Scholar 

  57. Danzaki K, Matsui Y, Ikesue M, et al. Interleukin-17A deficiency accelerates unstable atherosclerotic plaque formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2012;32:273–80.

    Article  PubMed  CAS  Google Scholar 

  58. Madhur MS, Funt SA, Li L, et al. Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein e-deficient mice. Arterioscler Thromb Vasc Biol. 2011;31:1565–72.

    Article  PubMed  CAS  Google Scholar 

  59. Ait-Oufella H, Salomon BL, Potteaux S, et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006;12:178–80.

    Article  PubMed  CAS  Google Scholar 

  60. Grainger DJ. Transforming growth factor beta and atherosclerosis: so far, so good for the protective cytokine hypothesis. Arterioscler Thromb Vasc Biol. 2004;24:399–404.

    Article  PubMed  CAS  Google Scholar 

  61. Mallat Z, Besnard S, Duriez M, et al. Protective role of interleukin-10 in atherosclerosis. Circ Res. 1999;85:e17–24.

    Article  PubMed  CAS  Google Scholar 

  62. Mor A, Planer D, Luboshits G, et al. Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscler Thromb Vasc Biol. 2007;27:893–900.

    Article  PubMed  CAS  Google Scholar 

  63. Gewaltig J, Kummer M, Koella C, et al. Requirements for CD8 T-cell migration into the human arterial wall. Hum Pathol. 2008;39:1756–62.

    Article  PubMed  CAS  Google Scholar 

  64. Fyfe AI, Qiao JH, Lusis AJ. Immune-deficient mice develop typical atherosclerotic fatty streaks when fed an atherogenic diet. J Clin Invest. 1994;94:2516–20.

    Article  PubMed  CAS  Google Scholar 

  65. Chyu KY, Zhao X, Dimayuga PC, et al. CD8+ T cells mediate the athero-protective effect of immunization with an ApoB-100 peptide. PLoS One. 2012;7:e30780.

    Article  PubMed  CAS  Google Scholar 

  66. Olofsson PS, Soderstrom LA, Wagsater D, et al. CD137 is expressed in human atherosclerosis and promotes development of plaque inflammation in hypercholesterolemic mice. Circulation. 2008;117:1292–301.

    Article  PubMed  CAS  Google Scholar 

  67. Nahrendorf M, Swirski FK, Aikawa E, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med. 2007;204:3037–47.

    Article  PubMed  CAS  Google Scholar 

  68. Ince H, Petzsch M, Kleine HD, et al. Prevention of left ventricular remodeling with granulocyte colony-stimulating factor after acute myocardial infarction: final 1-year results of the Front-Integrated Revascularization and Stem Cell Liberation in Evolving Acute Myocardial Infarction by Granulocyte Colony-Stimulating Factor (FIRSTLINE-AMI) Trial. Circulation. 2005;112:I73–80.

    Article  PubMed  Google Scholar 

  69. Kolpakov MA, Seqqat R, Rafiq K, et al. Pleiotropic effects of neutrophils on myocyte apoptosis and left ventricular remodeling during early volume overload. J Mol Cell Cardiol. 2009;47:634–45.

    Article  PubMed  CAS  Google Scholar 

  70. Frangogiannis NG, Smith CW, Entman ML. The inflammatory response in myocardial infarction. Cardiovasc Res. 2002;53:31–47.

    Article  PubMed  CAS  Google Scholar 

  71. Abbate A, Bonanno E, Mauriello A, et al. Widespread myocardial inflammation and infarct-related artery patency. Circulation. 2004;110:46–50. These authors identified T cells in the tissues surrounding infarcted myocardium.

    Article  PubMed  Google Scholar 

  72. Wynn TA. Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol. 2004;4:583–94.

    Article  PubMed  CAS  Google Scholar 

  73. Hofmann U, Beyersdorf N, Weirather J, et al. Activation of CD4+ T lymphocytes improves wound healing and survival after experimental myocardial infarction in mice. Circulation. 2012;125:1652–63. These comprehensive experiments demonstrated that activated CD4 + T lymphocytes improve the outcome of myocardial infarction.

    Article  PubMed  CAS  Google Scholar 

  74. Tang TT, Yuan J, Zhu ZF, et al. Regulatory T cells ameliorate cardiac remodeling after myocardial infarction. Basic Res Cardiol. 2012;107:232.

    Article  PubMed  Google Scholar 

  75. Matsumoto K, Ogawa M, Suzuki J, et al. Regulatory T lymphocytes attenuate myocardial infarction-induced ventricular remodeling in mice. Int Heart J. 2011;52:382–7.

    Article  PubMed  CAS  Google Scholar 

  76. Nataraj C, Oliverio MI, Mannon RB, et al. Angiotensin II regulates cellular immune responses through a calcineurin-dependent pathway. J Clin Invest. 1999;104:1693–701.

    Article  PubMed  CAS  Google Scholar 

  77. Crowley SD, Song YS, Sprung G, et al. A role for angiotensin II type 1 receptors on bone marrow-derived cells in the pathogenesis of angiotensin II-dependent hypertension. Hypertension. 2010;55:99–108.

    Article  PubMed  CAS  Google Scholar 

  78. Jurewicz M, McDermott DH, Sechler JM, et al. Human T and natural killer cells possess a functional renin-angiotensin system: further mechanisms of angiotensin II-induced inflammation. J Am Soc Nephrol. 2007;18:1093–102.

    Article  PubMed  CAS  Google Scholar 

  79. Hoch NE, Guzik TJ, Chen W, et al. Regulation of T-cell function by endogenously produced angiotensin II. Am J Physiol Regul Integr Comp Physiol. 2009;296:R208–16.

    Article  PubMed  CAS  Google Scholar 

  80. Platten M, Youssef S, Hur EM, et al. Blocking angiotensin-converting enzyme induces potent regulatory T cells and modulates TH1- and TH17-mediated autoimmunity. Proc Natl Acad Sci U S A. 2009;106:14948–53.

    Article  PubMed  CAS  Google Scholar 

  81. Bachmann MF, Kundig TM. In vivo versus in vitro assays for assessment of T- and B- cell function. Curr Opin Immunol. 1994;6:320–6.

    Article  PubMed  CAS  Google Scholar 

  82. Kato H, Ishida J, Nagano K, et al. Deterioration of atherosclerosis in mice lacking angiotensin II type 1A receptor in bone marrow-derived cells. Lab Investig. 2008;88:731–9. This provocative study indicated that the type 1 angiotensin receptor in bone marrow-derived cells could protect from atherosclerosis.

    Article  PubMed  CAS  Google Scholar 

  83. Lu H, Rateri DL, Feldman DL, et al. Renin inhibition reduces hypercholesterolemia-induced atherosclerosis in mice. J Clin Invest. 2008;118:984–93.

    PubMed  CAS  Google Scholar 

  84. Cassis LA, Rateri DL, Lu H, et al. Bone marrow transplantation reveals that recipient AT1a receptors are required to initiate angiotensin II-induced atherosclerosis and aneurysms. Arterioscler Thromb Vasc Biol. 2007;27:380–6.

    Article  PubMed  CAS  Google Scholar 

  85. June CH. Adoptive T, cell therapy for cancer in the clinic. J Clin Invest. 2007;117:1466–76.

    Article  PubMed  CAS  Google Scholar 

  86. Ehninger A, Trumpp A. The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J Exp Med. 2011;208:421–8.

    Article  PubMed  CAS  Google Scholar 

  87. Harrison DG, Guzik TJ. Studies of the T-cell angiotensin receptor using cre-lox technology: an unan-T-cellpated result. Circ Res. 2012;110:1543–5.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Institutes of Health Grant DK087783, the Medical Research Service of the Department of Veterans Affairs, and the Edna and Fred L. Mandel Center for Hypertension and Atherosclerosis Research.

Disclosure

No potential conflicts of interest relevant to this article were reported.

Author information

Authors and Affiliations

  1. Division of Nephrology, Department of Medicine, Duke University and Durham VA Medical Centers, DUMC Box 103015, Durham, NC, 27710, USA

    Jiandong Zhang & Steven D. Crowley

Authors
  1. Jiandong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven D. Crowley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Steven D. Crowley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, J., Crowley, S.D. The Role of Type 1 Angiotensin Receptors on T Lymphocytes in Cardiovascular and Renal Diseases. Curr Hypertens Rep 15, 39–46 (2013). https://doi.org/10.1007/s11906-012-0318-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11906-012-0318-z

Keywords

Search

Navigation