The immune system in hypertension

American Journal of Physiology - Advances in Physiology Education

Volumn 38, Issue 1, 2014, Pages 20-24

  Trott, Daniel W ^a   Harrison, David G ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin; Costimulation; Cytokines; Subfornical organ; T cell

Indexed keywords

ANGIOTENSIN; AUTACOID; CYTOKINE;

ADRENERGIC SYSTEM; ANIMAL; ARTICLE; B LYMPHOCYTE; BLOOD PRESSURE; CENTRAL NERVOUS SYSTEM; COSTIMULATION; HUMAN; HYPERTENSION; IMMUNE SYSTEM; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; SUBFORNICAL ORGAN; T LYMPHOCYTE;

ANGIOTENSIN; COSTIMULATION; CYTOKINES; SUBFORNICAL ORGAN; T CELL;

ANIMALS; B-LYMPHOCYTES; BLOOD PRESSURE; CENTRAL NERVOUS SYSTEM; CYTOKINES; HUMANS; HYPERTENSION; IMMUNE SYSTEM; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; SIGNAL TRANSDUCTION; SYMPATHETIC NERVOUS SYSTEM; T-LYMPHOCYTES;

EID: 84895132847     PISSN: 10434046     EISSN: 15221229     Source Type: Journal    
DOI: 10.1152/advan.00063.2013     Document Type: Article

References (60)

1. Abbas AK, Lichtman AH, Pillai S. Cellular and Molecular Immunology. Philadelphia, PA: Saunders Elsevier, 2007, p. viii.
2. Ba D, Takeichi N, Kodama T, Kobayashi H. Restoration of T cell depression and suppression of blood pressure in spontaneously hypertensive rats (SHR) by thymus grafts or thymus extracts. J Immunol 128: 1211-1216, 1982.
3. Barhoumi T, Kasal DA, Li MW, Shbat L, Laurant P, Neves MF, Paradis P, Schiffrin EL. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 57: 469-476, 2011.
4. Bautista LE, Vera LM, Arenas IA, Gamarra G. Independent association between inflammatory markers (C-reactive protein, interleukin-6, and TNF-α) and essential hypertension. J Hum Hypertens 19: 149-154, 2005.
5. Bendich A, Belisle EH, Strausser HR. Immune system modulation and its effect on the blood pressure of the spontaneously hypertensive male and female rat. Biochem Biophys Res Commun 99: 600-607, 1981.
6. Brands MW, Banes-Berceli AK, Inscho EW, Al-Azawi H, Allen AJ, Labazi H. Interleukin 6 knockout prevents angiotensin II hypertension: role of renal vasoconstriction and janus kinase 2/signal transducer and activator of transcription 3 activation. Hypertension 56: 879-884, 2010.
7. Brody M, Fink G, Buggy J, Haywood J, Gordon F, Knuepfer M, Mow M, Mahoney L, Johnson A. Critical role of the anteroventral third ventricle (AV3V) region in development and maintenance of experimental hypertension. Perspect Nephrol Hypertens 6: 76-84, 1979.
8. Chatterjee P, Chiasson VL, Kopriva SE, Young KJ, Chatterjee V, Jones KA, Mitchell BM. Interleukin 10 deficiency exacerbates toll-like receptor 3-induced preeclampsia-like symptoms in mice. Hypertension 58: 489-496, 2011.
9. Chatterjee P, Kopriva SE, Chiasson VL, Young KJ, Tobin RP, Newell-Rogers K, Mitchell BM. Interleukin-4 deficiency induces mild preeclampsia in mice. J Hypertens 31: 1414-1423, 2013.
10. 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.
11. Dhillion P, Wallace K, Herse F, Scott J, Wallukat G, Heath J, Mosely J, Martin JN Jr, Dechend R, LaMarca B. IL-17-mediated oxidative stress is an important stimulator of AT1-AA and hypertension during pregnancy. Am J Physiol Regul Integr Comp Physiol 303: R353-R358, 2012.
12. Dzielak DJ. Immune mechanisms in experimental and essential hypertension. Am J Physiol Regul Integr Comp Physiol 260: R459-R467, 1991.
13. Eid RE, Rao DA, Zhou J, Lo SF, Ranjbaran H, Gallo A, Sokol SI, Pfau S, Pober JS, Tellides G. Interleukin-17 and interferon-γ are produced concomitantly by human coronary artery-infiltrating T cells and act synergistically on vascular smooth muscle cells. Circulation 119: 1424- 1432, 2009.
14. Felten DL, Livnat S, Felten SY, Carlson SL, Bellinger DL, Yeh P. Sympathetic innervation of lymph nodes in mice. Brain Res Bull 13: 693-699, 1984.
15. Frauwirth KA, Thompson CB. Activation and inhibition of lymphocytes by costimulation. J Clin Invest 109: 295-299, 2002.
16. Fujita M, Ando K, Kawarazaki H, Kawarasaki C, Muraoka K, Ohtsu H, Shimizu H, Fujita T. Sympathoexcitation by brain oxidative stress mediates arterial pressure elevation in salt-induced chronic kidney disease. Hypertension 59: 105-112, 2012.
17. 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 289: H1683-H1691, 2005.
18. 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.
19. 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: 1190-1202, 2012.
20. Herrera J, Ferrebuz A, MacGregor EG, Rodriguez-Iturbe B. Mycophenolate mofetil treatment improves hypertension in patients with psoriasis and rheumatoid arthritis. J Am Soc Nephrol 17: S218-225, 2006.
21. Jensen F, Wallukat G, Herse F, Budner O, El-Mousleh T, Costa SD, Dechend R, Zenclussen AC. CD19+CD5+ cells as indicators of preeclampsia. Hypertension 59: 861-868, 2012.
22. Kvakan H, Kleinewietfeld M, Qadri F, Park JK, Fischer R, Schwarz I, Rahn HP, Plehm R, Wellner M, Elitok S, Gratze P, Dechend R, Luft FC, Muller DN. Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation 119: 2904-2912, 2009.
23. LaMarca B, Wallace K, Herse F, Wallukat G, Martin JN Jr, Weimer A, Dechend R. Hypertension in response to placental ischemia during pregnancy: role of B lymphocytes. Hypertension 57: 865-871, 2011.
24. 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.
25. 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 55: 277-283, 2010.
26. 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 61: 382-387, 2013.
27. Lob HE, Vinh A, Li L, Blinder Y, Offermanns S, Harrison DG. Role of vascular extracellular superoxide dismutase in hypertension. Hypertension 58: 232-239, 2011.
28. 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.
29. Marko L, Kvakan H, Park JK, Qadri F, Spallek B, Binger KJ, Bowman EP, Kleinewietfeld M, Fokuhl V, Dechend R, Muller DN. Interferon-γ signaling inhibition ameliorates angiotensin II-induced cardiac damage. Hypertension 60: 1430-1436, 2012.
30. 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 107: 263-270, 2010.
31. Marvar PJ, Vinh A, Thabet S, Lob HE, Geem D, Ressler KJ, Harrison DG. T lymphocytes and vascular inflammation contribute to stressdependent hypertension. Biol Psychiatry 71: 774-782, 2012.
32. 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 304: R407-R414, 2013.
33. Miguel-Carrasco JL, Zambrano S, Blanca AJ, Mate A, Vazquez CM. Captopril reduces cardiac inflammatory markers in spontaneously hypertensive rats by inactivation of NF-κB. J Inflamm (Lond) 7: 21, 2010.
34. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 136: 2348- 2357, 1986.
35. Muller DN, Dechend R, Mervaala EM, Park JK, Schmidt F, Fiebeler A, Theuer J, Breu V, Ganten D, Haller H, Luft FC. NF-κB inhibition ameliorates angiotensin II-induced inflammatory damage in rats. Hypertension 35: 193-201, 2000.
36. Muller DN, Mervaala EM, Schmidt F, Park JK, Dechend R, Genersch E, Breu V, Loffler BM, Ganten D, Schneider W, Haller H, Luft FC. Effect of bosentan on NF-κB, inflammation, and tissue factor in angiotensin II-induced end-organ damage. Hypertension 36: 282-290, 2000.
37. Nguyen H, Chiasson VL, Chatterjee P, Kopriva SE, Young KJ, Mitchell BM. Interleukin-17 causes Rho-kinase-mediated endothelial dysfunction and hypertension. Cardiovasc Res 97: 696-704, 2013.
38. Nicolls MR, Taraseviciene-Stewart L, Rai PR, Badesch DB, Voelkel NF. Autoimmunity and pulmonary hypertension: a perspective. Eur Respir J 26: 1110-1118, 2005.
39. Novotny SR, Wallace K, Heath J, Moseley J, Dhillon P, Weimer A, Wallukat G, Herse F, Wenzel K, Martin JN Jr, Dechend R, Lamarca B. Activating autoantibodies to the angiotensin II type I receptor play an important role in mediating hypertension in response to adoptive transfer of CD4+ T lymphocytes from placental ischemic rats. Am J Physiol Regul Integr Comp Physiol 302: R1197-R1201, 2012.
40. Okuda T, Grollman A. Passive transfer of autoimmune induced hypertension in the rat by lymph node cells. Tex Rep Biol Med 25: 257-264, 1967.
41. Peeters AC, Netea MG, Janssen MC, Kullberg BJ, Van der Meer JW, Thien T. Pro-inflammatory cytokines in patients with essential hypertension. Eur J Clin Invest 31: 31-36, 2001.
42. Purcell ES, Gattone VH, 2nd. Immune system of the spontaneously hypertensive rat. I. Sympathetic innervation. Exp Neurol 117: 44-50, 1992.
43. Rodriguez-Iturbe B, Pons H, Quiroz Y, Gordon K, Rincon J, Chavez M, Parra G, Herrera-Acosta J, Gomez-Garre D, Largo R, Egido J, Johnson RJ. Mycophenolate mofetil prevents salt-sensitive hypertension resulting from angiotensin II exposure. Kidney Int 59: 2222-2232, 2001.
44. Sanchez-Lemus E, Benicky J, Pavel J, Larrayoz IM, Zhou J, Baliova M, Nishioku T, Saavedra JM. Angiotensin II AT1 blockade reduces the lipopolysaccharide-induced innate immune response in rat spleen. Am J Physiol Regul Integr Comp Physiol 296: R1376-R1384, 2009.
45. Schrader LI, Kinzenbaw DA, Johnson AW, Faraci FM, Didion SP. IL-6 deficiency protects against angiotensin II induced endothelial dysfunction and hypertrophy. Arterioscler Thromb Vasc Biol 27: 2576-2581, 2007.
46. Svendsen UG. The role of thymus for the development and prognosis of hypertension and hypertensive vascular disease in mice following renal infarction. Acta Pathol Microbiol Scand A 84: 235-243, 1976.
47. Tamosiuniene R, Tian W, Dhillon G, Wang L, Sung YK, Gera L, Patterson AJ, Agrawal R, Rabinovitch M, Ambler K, Long CS, Voelkel NF, Nicolls MR. Regulatory T cells limit vascular endothelial injury and prevent pulmonary hypertension. Circ Res 109: 867-879, 2011.
48. Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev 223: 87-113, 2008.
49. 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 2: 3, 2002.
50. Tran LT, MacLeod KM, McNeill JH. Chronic etanercept treatment prevents the development of hypertension in fructose-fed rats. Mol Cell Biochem 330: 219-228, 2009.
51. Tuder RM, Groves B, Badesch DB, Voelkel NF. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol 144: 275-285, 1994.
52. Venegas-Pont M, Manigrasso MB, Grifoni SC, LaMarca BB, Maric C, Racusen LC, Glover PH, Jones AV, Drummond HA, Ryan MJ. Tumor necrosis factor-α antagonist etanercept decreases blood pressure and protects the kidney in a mouse model of systemic lupus erythematosus. Hypertension 56: 643-649, 2010.
53. Viel EC, Lemarie CA, Benkirane K, Paradis P, Schiffrin EL. Immune regulation and vascular inflammation in genetic hypertension. Am J Physiol Heart Circ Physiol 298: H938-H944, 2010.
54. 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.
55. Wallukat G, Homuth V, Fischer T, Lindschau C, Horstkamp B, Jupner A, Baur E, Nissen E, Vetter K, Neichel D, Dudenhausen JW, Haller H, Luft FC. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest 103: 945- 952, 1999.
56. White FN, Grollman A. Autoimmune factors associated with infarction of the kidney. Nephron 1: 93-102, 1964.
57. Winer S, Paltser G, Chan Y, Tsui H, Engleman E, Winer D, Dosch HM. Obesity predisposes to Th17 bias. Eur J Immunol 39: 2629-2635, 2009.
58. Youn JC, Yu HT, Lim BJ, Koh MJ, Lee J, Chang DY, Choi YS, Lee SH, Kang SM, Jang Y, Yoo OJ, Shin EC, Park S. Immunosenescent CD8+ T cells and C-X-C chemokine receptor type 3 chemokines are increased in human hypertension. Hypertension 62: 126-133, 2013.
59. Zhang JD, Patel MB, Song YS, Griffiths R, Burchette J, Ruiz P, Sparks MA, Yan M, Howell DN, Gomez JA, Spurney RF, Coffman TM, Crowley SD. A novel role for type 1 angiotensin receptors on T lymphocytes to limit target organ damage in hypertension. Circ Res 110: 1604-1617, 2012.
60. Zhou CC, Zhang Y, Irani RA, Zhang H, Mi T, Popek EJ, Hicks MJ, Ramin SM, Kellems RE, Xia Y. Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat Med 14: 855-862, 2008.