Female spontaneously hypertensive rats have a compensatory increase in renal regulatory T cells in response to elevations in blood pressure

Hypertension

Volumn 64, Issue 3, 2014, Pages 557-564

  Tipton, Ashlee J ^a   Baban, Babak ^b   Sullivan, Jennifer C ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b AUGUSTA UNIVERSITY   (United States)

Author keywords

Cytokines; Hypertension; Kidney; Sex identity; T lymphocytes; Th17 cells

Indexed keywords

HYDROCHLOROTHIAZIDE; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; RESERPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HYPERTENSION; KIDNEY CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; RAT; REGULATORY T LYMPHOCYTE; SEX DIFFERENCE; SPONTANEOUSLY HYPERTENSIVE RAT; TH17 CELL; TREATMENT DURATION;

CYTOKINES; HYPERTENSION; KIDNEY; SEX IDENTITY; T-LYMPHOCYTES; TH17 CELLS;

AGE FACTORS; ANIMALS; ANTIHYPERTENSIVE AGENTS; BLOOD PRESSURE; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GONADAL STEROID HORMONES; HYDROCHLOROTHIAZIDE; HYPERTENSION; KIDNEY; MALE; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RESERPINE; SEX FACTORS; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84907598537     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.114.03512     Document Type: Article

References (39)

1. Lee JH, Ulrich B, Cho J, Park J, Kim CH. Progesterone promotes differentiation of human cord blood fetal T cells into T regulatory cells but suppresses their differentiation into Th17 cells. J Immunol. 2011;187:1778-1787.
2. Franco M, Bautista R, Pérez-Méndez O, González L, Pacheco U, Sánchez- Lozada LG, Santamaría J, Tapia E, Monreal R, Martínez F. Renal interstitial adenosine is increased in angiotensin II-induced hypertensive rats. Am J Physiol Renal Physiol. 2008;294:F84-F92.
3. Rodríguez-Iturbe B, Quiroz Y, Nava M, Bonet L, Chávez M, Herrera- Acosta J, Johnson RJ, Pons HA. Reduction of renal immune cell infiltration results in blood pressure control in genetically hypertensive rats. Am J Physiol Renal Physiol. 2002;282:F191-F201.
4. 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.
5. De Miguel C, Lund H, Mattson DL. High dietary protein exacerbates hypertension and renal damage in Dahl SS rats by increasing infiltrating immune cells in the kidney. Hypertension. 2011;57:269-274.
6. Rodríguez-Iturbe B, Quiroz Y, Ferrebuz A, Parra G, Vaziri ND. Evolution of renal interstitial inflammation and NF-kappaB activation in spontaneously hypertensive rats. Am J Nephrol. 2004;24:587-594.
7. 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. 2011;58:489-496.
8. Andrzejczak D, Górska D, Czarnecka E. Influence of amlodipine and atenolol on lipopolysaccharide (LPS)-induced serum concentrations of TNF-alpha, IL-1, IL-6 in spontaneously hypertensive rats (SHR). Pharmacol Rep. 2006;58:711-719.
9. Cardinale JP, Sriramula S, Pariaut R, Guggilam A, Mariappan N, Elks CM, Francis J. HDAC inhibition attenuates inflammatory, hypertrophic, and hypertensive responses in spontaneously hypertensive rats. Hypertension. 2010;56:437-444.
10. Liu XP, Pang YJ, Zhu WW, Zhao TT, Zheng M, Wang YB, Sun ZJ, Sun SJ. Benazepril, an angiotensin-converting enzyme inhibitor, alleviates renal injury in spontaneously hypertensive rats by inhibiting advanced glycation end-product-mediated pathways. Clin Exp Pharmacol Physiol. 2009;36:287-296.
11. Matrougui K, Abd Elmageed Z, Zakaria AE, Kassan M, Choi S, Nair D, Gonzalez-Villalobos RA, Chentoufi AA, Kadowitz P, Belmadani S, Partyka M. Natural regulatory T cells control coronary arteriolar endothelial dysfunction in hypertensive mice. Am J Pathol. 2011;178:434-441.
12. Giachini FR, Sullivan JC, Lima VV, Carneiro FS, Fortes ZB, Pollock DM, Carvalho MH, Webb RC, Tostes RC. Extracellular signal-regulated kinase . activation, via downregulation of mitogen-activated protein kinase phosphatase 1, mediates sex differences in desoxycorticosterone acetate-salt hypertension vascular reactivity. Hypertension. 2010;55:172-179.
13. Tipton AJ, Baban B, Sullivan JC. Female spontaneously hypertensive rats have greater renal anti-inflammatory T lymphocyte infiltration than males. Am J Physiol Regul Integr Comp Physiol. 2012;303:R359-R367.
14. Magen E, Feldman A, Cohen Z, Alon DB, Minz E, Chernyavsky A, Linov L, Mishal J, Schlezinger M, Sthoeger Z. Circulating endothelial progenitor cells, Th1/Th2/Th17-related cytokines, and endothelial dysfunction in resistant hypertension. Am J Med Sci. 2010;339:117-122.
15. 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. 2006;290:H935-H940.
16. 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. 2010;55:500-507.
17. Kassan M, Galan M, Partyka M, Trebak M, Matrougui K. Interleukin-10 released by CD4(+)CD25(+) natural regulatory T cells improves microvascular endothelial function through inhibition of NADPH oxidase activity in hypertensive mice. Arterioscler Thromb Vasc Biol. 2011;31:2534-2542.
18. Viel EC, Lemarié CA, Benkirane K, Paradis P, Schiffrin EL. Immune regulation and vascular inflammation in genetic hypertension. Am J Physiol Heart Circ Physiol. 2010;298:H938-H944.
19. Tai P, Wang J, Jin H, Song X, Yan J, Kang Y, Zhao L, An X, Du X, Chen X, Wang S, Xia G, Wang B. Induction of regulatory T cells by physiological level estrogen. J Cell Physiol. 2008;214:456-464.
20. Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sampognaro S, Parronchi P, Manetti R, Annunziato F, Livi C. Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J Immunol. 1995;155:128-133.
21. Page ST, Plymate SR, Bremner WJ, Matsumoto AM, Hess DL, Lin DW, Amory JK, Nelson PS, Wu JD. Effect of medical castration on CD4+ CD25+ T cells, CD8+ T cell IFN-gamma expression, and NK cells: A physiological role for testosterone and/or its metabolites. Am J Physiol Endocrinol Metab. 2006;290:E856-E863.
22. Fijak M, Schneider E, Klug J, Bhushan S, Hackstein H, Schuler G, Wygrecka M, Gromoll J, Meinhardt A. Testosterone replacement effectively inhibits the development of experimental autoimmune orchitis in rats: evidence for a direct role of testosterone on regulatory T cell expansion. J Immunol. 2011;186:5162-5172.
23. Gross ML, Adamczak M, Rabe T, Harbi NA, Krtil J, Koch A, Hamar P, Amann K, Ritz E. Beneficial effects of estrogens on indices of renal damage in uninephrectomized SHRsp rats. J Am Soc Nephrol. 2004;15:348-358.
24. Sandberg K, Ji H. Sex and the renin angiotensin system: implications for gender differences in the progression of kidney disease. Adv Ren Replace Ther. 2003;10:15-23.
25. Reckelhoff JF, Zhang H, Srivastava K. Gender differences in development of hypertension in spontaneously hypertensive rats: role of the reninangiotensin system. Hypertension. 2000;35(1 Pt 2):480-483.
26. Sullivan JC, Semprun-Prieto L, Boesen EI, Pollock DM, Pollock JS. Sex and sex hormones influence the development of albuminuria and renal macrophage infiltration in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol. 2007;293:R1573-R1579.
27. Case J, Davison CA. Estrogen alters relative contributions of nitric oxide and cyclooxygenase products to endothelium-dependent vasodilation. J Pharmacol Exp Ther. 1999;291:524-530.
28. Pollock DM, Rekito A. Hypertensive response to chronic NO synthase inhibition is different in Sprague-Dawley rats from two suppliers. Am J Physiol. 1998;275(5 Pt 2):R1719-R1723.
29. Abumiya T, Masuda J, Kawai J, Suzuki T, Ogata J. Heterogeneity in the appearance and distribution of macrophage subsets and their possible involvement in hypertensive vascular lesions in rats. Lab Invest. 1996;75:125-136.
30. Tinsley JH, South S, Chiasson VL, Mitchell BM. Interleukin-10 reduces inflammation, endothelial dysfunction, and blood pressure in hypertensive pregnant rats. Am J Physiol Regul Integr Comp Physiol. 2010;298:R713-R719.
31. Dalpiaz PL, Lamas AZ, Caliman IF, Medeiros AR, Abreu GR, Moysés MR, Andrade TU, Alves MF, Carmona AK, Bissoli NS. The chronic blockade of angiotensin I-converting enzyme eliminates the sex differences of serum cytokine levels of spontaneously hypertensive rats. Braz J Med Biol Res. 2013;46:171-177.
32. Biswas SK, de Faria JB. Which comes first: renal inflammation or oxidative stress in spontaneously hypertensive rats? Free Radic Res. 2007;41:216-224.
33. Shao J, Nangaku M, Miyata T, Inagi R, Yamada K, Kurokawa K, Fujita T. Imbalance of T-cell subsets in angiotensin II-infused hypertensive rats with kidney injury. Hypertension. 2003;42:31-38.
34. Brinson KN, Elmarakby AA, Tipton AJ, Crislip GR, Yamamoto T, Baban B, Sullivan JC. Female SHR have greater blood pressure sensitivity and renal T cell infiltration following chronic NOS inhibition than males. Am J Physiol Regul Integr Comp Physiol. 2013;305:R701-R710.
35. Rodrigues SF, de Oliveira MA, dos Santos RA, Soares AG, de Cássia Tostes R, Carvalho MH, Fortes ZB. Hydralazine reduces leukocyte migration through different mechanisms in spontaneously hypertensive and normotensive rats. Eur J Pharmacol. 2008;589:206-214.
36. Mekori YA, Blickstein D, Baram D, Alter A, Radnay J, Rozenszajn LA, Ravid M. Characterization of the interference of T cell activation by reserpine. Cell Immunol. 1989;124:308-319.
37. Crowley SD, Frey CW, Gould SK, Griffiths R, Ruiz P, Burchette JL, Howell DN, Makhanova N, Yan M, Kim HS, Tharaux PL, Coffman TM. Stimulation of lymphocyte responses by angiotensin II promotes kidney injury in hypertension. Am J Physiol Renal Physiol. 2008;295:F515-F524.
38. Krebs CF, Lange S, Niemann G, Rosendahl A, Lehners A, Meyer- Schwesinger C, Stahl RA, Benndorf RA, Velden J, Paust HJ, Panzer U, Ehmke H, Wenzel UO. Deficiency of the interleukin 17/23 axis accelerates renal injury in mice with deoxycorticosterone acetate+angiotensin ii-induced hypertension. Hypertension. 2014;63:565-571.
39. Amador CA, Barrientos V, Peña J, Herrada AA, González M, Valdés S, Carrasco L, Alzamora R, Figueroa F, Kalergis AM, Michea L. Spironolactone decreases DOCA-salt-induced organ damage by blocking the activation of T helper 17 and the downregulation of regulatory T lymphocytes. Hypertension. 2014;63:797-803.