23
Views
25
CrossRef citations to date
0
Altmetric
Article

Immunosuppression-Independent Role of Regulatory T Cells against Hypertension-Driven Renal Dysfunctions

, , , , , , , , , , & ORCID Icon show all
Pages 3528-3546 | Received 19 May 2015, Accepted 24 Jul 2015, Published online: 20 Mar 2023

REFERENCES

  • Josefowicz SZ, Lu LF, Rudensky AY. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol 30:531–564. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141623.
  • Shevach EM. 2009. Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 30:636–645. http://dx.doi.org/10.1016/j.immuni.2009.04.010.
  • Burzyn D, Benoist C, Mathis D. 2013. Regulatory T cells in nonlymphoid tissues. Nat Immunol 14:1007–1013. http://dx.doi.org/10.1038/ni.2683.
  • Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y, Sefik E, Tan TG, Wagers AJ, Benoist C, Mathis D. 2013. A special population of regulatory T cells potentiates muscle repair. Cell 155:1282–1295. http://dx.doi.org/10.1016/j.cell.2013.10.054.
  • Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J. 2005. Global burden of hypertension: analysis of worldwide data. Lancet 365:217–223. http://dx.doi.org/10.1016/S0140-6736(05)70151-3.
  • Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ. 2006. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 367:1747–1757. http://dx.doi.org/10.1016/S0140-6736(06)68770-9.
  • Liu Y. 2011. Cellular and molecular mechanisms of renal fibrosis. Nat Rev Nephrol 7:684–696. http://dx.doi.org/10.1038/nrneph.2011.149.
  • Wynn TA, Ramalingam TR. 2012. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18:1028–1040. http://dx.doi.org/10.1038/nm.2807.
  • 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. 2009. Regulatory T cells ameliorate angiotensin II-induced cardiac damage. Circulation 119:2904–2912. http://dx.doi.org/10.1161/CIRCULATIONAHA.108.832782.
  • Barhoumi T, Kasal DA, Li MW, Shbat L, Laurant P, Neves MF, Paradis P, Schiffrin EL. 2011. T regulatory lymphocytes prevent angiotensin II-induced hypertension and vascular injury. Hypertension 57:469–476. http://dx.doi.org/10.1161/HYPERTENSIONAHA.110.162941.
  • Kasal DA, Barhoumi T, Li MW, Yamamoto N, Zdanovich E, Rehman A, Neves MF, Laurant P, Paradis P, Schiffrin EL. 2012. T regulatory lymphocytes prevent aldosterone-induced vascular injury. Hypertension 59:324–330. http://dx.doi.org/10.1161/HYPERTENSIONAHA.111.181123.
  • 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. 2002. Immunosuppressive treatment protects against angiotensin II-induced renal damage. Am J Pathol 161:1679–1693. http://dx.doi.org/10.1016/S0002-9440(10)64445-8.
  • Crowley SD, Frey CW, Gould SK, Griffiths R, Ruiz P, Burchette JL, Howell DN, Makhanova N, Yan M, Kim HS, Tharaux PL, Coffman TM. 2008. Stimulation of lymphocyte responses by angiotensin II promotes kidney injury in hypertension. Am J Physiol Renal Physiol 295:F515–F524. http://dx.doi.org/10.1152/ajprenal.00527.2007.
  • Mervaala E, Muller DN, Park JK, Dechend R, Schmidt F, Fiebeler A, Bieringer M, Breu V, Ganten D, Haller H, Luft FC. 2000. Cyclosporin A protects against angiotensin II-induced end-organ damage in double transgenic rats harboring human renin and angiotensinogen genes. Hypertension 35:360–366. http://dx.doi.org/10.1161/01.HYP.35.1.360.
  • Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S, Goronzy J, Weyand C, Harrison DG. 2007. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204:2449–2460. http://dx.doi.org/10.1084/jem.20070657.
  • Madhur MS, Lob HE, McCann LA, Iwakura Y, Blinder Y, Guzik TJ, Harrison DG. 2010. Interleukin 17 promotes angiotensin II-induced hypertension and vascular dysfunction. Hypertension 55:500–507. http://dx.doi.org/10.1161/HYPERTENSIONAHA.109.145094.
  • Shao J, Nangaku M, Miyata T, Inagi R, Yamada K, Kurokawa K, Fujita T. 2003. Imbalance of T-cell subsets in angiotensin II-infused hypertensive rats with kidney injury. Hypertension 42:31–38. http://dx.doi.org/10.1161/01.HYP.0000075082.06183.4E.
  • Crowley SD, Song YS, Lin EE, Griffiths R, Kim HS, Ruiz P. 2010. Lymphocyte responses exacerbate angiotensin II-dependent hypertension. Am J Physiol Regul Integr Comp Physiol 298:R1089–R1097. http://dx.doi.org/10.1152/ajpregu.00373.2009.
  • Harrison DG, Guzik TJ, Lob HE, Madhur MS, Marvar PJ, Thabet SR, Vinh A, Weyand CM. 2011. Inflammation, immunity, and hypertension. Hypertension 57:132–140. http://dx.doi.org/10.1161/HYPERTENSIONAHA.110.163576.
  • Rodríguez-Iturbe B, Pons H, Herrera-Acosta J, Johnson RJ. 2001. Role of immunocompetent cells in nonimmune renal diseases. Kidney Int 59:1626–1640. http://dx.doi.org/10.1046/j.1523-1755.2001.0590051626.x.
  • Rodríguez-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. 2001. Mycophenolate mofetil prevents salt-sensitive hypertension resulting from angiotensin II exposure. Kidney Int 59:2222–2232. http://dx.doi.org/10.1046/j.1523-1755.2001.00737.x.
  • McMaster WG, Kirabo A, Madhur MS, Harrison DG. 2015. Inflammation, immunity, and hypertensive end-organ damage. Circ Res 116:1022–1033. http://dx.doi.org/10.1161/CIRCRESAHA.116.303697.
  • Bustelo XR. 2000. Regulatory and signaling properties of the Vav family. Mol Cell Biol 20:1461–1477. http://dx.doi.org/10.1128/MCB.20.5.1461-1477.2000.
  • Bustelo XR. 2014. Vav family exchange factors: an integrated regulatory and functional view. Small GTPases 5(2):9. http://dx.doi.org/10.4161/21541248.2014.973757.
  • Turner M, Billadeau DD. 2002. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat Rev Immunol 2:476–486. http://dx.doi.org/10.1038/nri840.
  • Tarakhovsky A, Turner M, Schaal S, Mee PJ, Duddy LP, Rajewsky K, Tybulewicz VL. 1995. Defective antigen receptor-mediated proliferation of B and T cells in the absence of Vav. Nature 374:467–470. http://dx.doi.org/10.1038/374467a0.
  • Turner M, Mee PJ, Walters AE, Quinn ME, Mellor AL, Zamoyska R, Tybulewicz VL. 1997. A requirement for the Rho-family GTP exchange factor Vav in positive and negative selection of thymocytes. Immunity 7:451–460. http://dx.doi.org/10.1016/S1074-7613(00)80367-2.
  • Fujikawa K, Miletic AV, Alt FW, Faccio R, Brown T, Hoog J, Fredericks J, Nishi S, Mildiner S, Moores SL, Brugge J, Rosen FS, Swat W. 2003. Vav1/2/3-null mice define an essential role for Vav family proteins in lymphocyte development and activation but a differential requirement in MAPK signaling in T and B cells. J Exp Med 198:1595–1608. http://dx.doi.org/10.1084/jem.20030874.
  • Sauzeau V, Sevilla MA, Rivas-Elena JV, de Alava E, Montero MJ, Lopez-Novoa JM, Bustelo XR. 2006. Vav3 proto-oncogene deficiency leads to sympathetic hyperactivity and cardiovascular dysfunction. Nat Med 12:841–845. http://dx.doi.org/10.1038/nm1426.
  • Sauzeau V, Jerkic M, Lopez-Novoa JM, Bustelo XR. 2007. Loss of Vav2 proto-oncogene causes tachycardia and cardiovascular disease in mice. Mol Biol Cell 18:943–952. http://dx.doi.org/10.1091/mbc.E06-09-0877.
  • Sauzeau V, Horta-Junior JAC, Riolobos AS, Fernandez G, Sevilla MA, Lopez DE, Montero MJ, Rico B, Bustelo XR. 2010. Vav3 is involved in GABAergic axon guidance events important for the proper function of brainstem neurons controlling cardiovascular, respiratory, and renal parameters. Mol Biol Cell 21:4251–4263. http://dx.doi.org/10.1091/mbc.E10-07-0639.
  • Sauzeau V, Sevilla MA, Montero MJ, Bustelo XR. 2010. The Rho/Rac exchange factor Vav2 controls nitric oxide-dependent responses in mouse vascular smooth muscle cells. J Clin Invest 120:315–330. http://dx.doi.org/10.1172/JCI38356.
  • Jonsson CA, Svensson L, Carlsten H. 1999. Beneficial effect of the inosine monophosphate dehydrogenase inhibitor mycophenolate mofetil on survival and severity of glomerulonephritis in systemic lupus erythematosus (SLE)-prone MRLlpr/lpr mice. Clin Exp Immunol 116:534–541. http://dx.doi.org/10.1046/j.1365-2249.1999.00901.x.
  • Kassan M, Montero MJ, Sevilla MA. 2010. In vitro antioxidant activity of pravastatin provides vascular protection. Eur J Pharmacol 630:107–111. http://dx.doi.org/10.1016/j.ejphar.2009.12.037.
  • Menacho-Márquez M, Garcia-Escudero R, Ojeda V, Abad A, Delgado P, Costa C, Ruiz S, Alarcon B, Paramio JM, Bustelo XR. 2013. The Rho exchange factors Vav2 and Vav3 favor skin tumor initiation and promotion by engaging extracellular signaling loops. PLoS Biol 11:e1001615. http://dx.doi.org/10.1371/journal.pbio.1001615.
  • Paragas N, Qiu A, Hollmen M, Nickolas TL, Devarajan P, Barasch J. 2012. NGAL-Siderocalin in kidney disease. Biochim Biophys Acta 1823:1451–1458. http://dx.doi.org/10.1016/j.bbamcr.2012.06.014.
  • Benigni A, Cassis P, Remuzzi G. 2010. Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med 2:247–257. http://dx.doi.org/10.1002/emmm.201000080.
  • Rees DD, Palmer RM, Hodson HF, Moncada S. 1989. A specific inhibitor of nitric oxide formation from l-arginine attenuates endothelium-dependent relaxation. Br J Pharmacol 96:418–424. http://dx.doi.org/10.1111/j.1476-5381.1989.tb11833.x.
  • Sintchak MD, Nimmesgern E. 2000. The structure of inosine 5′-monophosphate dehydrogenase and the design of novel inhibitors. Immunopharmacology 47:163–184. http://dx.doi.org/10.1016/S0162-3109(00)00193-4.
  • D'Alessio FR, Tsushima K, Aggarwal NR, West EE, Willett MH, Britos MF, Pipeling MR, Brower RG, Tuder RM, McDyer JF, King LS. 2009. CD4+ CD25+ Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 119:2898–2913. http://dx.doi.org/10.1172/JCI36498.
  • Lewkowicz P, Lewkowicz N, Sasiak A, Tchorzewski H. 2006. Lipopolysaccharide-activated CD4+ CD25+ T regulatory cells inhibit neutrophil function and promote their apoptosis and death. J Immunol 177:7155–7163. http://dx.doi.org/10.4049/jimmunol.177.10.7155.
  • Junger WG. 2011. Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 11:201–212. http://dx.doi.org/10.1038/nri2938.
  • Noris M, Casiraghi F, Todeschini M, Cravedi P, Cugini D, Monteferrante G, Aiello S, Cassis L, Gotti E, Gaspari F, Cattaneo D, Perico N, Remuzzi G. 2007. Regulatory T cells and T cell depletion: role of immunosuppressive drugs. J Am Soc Nephrol 18:1007–1018. http://dx.doi.org/10.1681/ASN.2006101143.
  • Barrat FJ, Cua DJ, Boonstra A, Richards DF, Crain C, Savelkoul HF, de Waal-Malefyt R, Coffman RL, Hawrylowicz CM, O'Garra A. 2002. In vitro generation of interleukin 10-producing regulatory CD4+ T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J Exp Med 195:603–616. http://dx.doi.org/10.1084/jem.20011629.
  • Hafiz MM, Faradji RN, Froud T, Pileggi A, Baidal DA, Cure P, Ponte G, Poggioli R, Cornejo A, Messinger S, Ricordi C, Alejandro R. 2005. Immunosuppression and procedure-related complications in 26 patients with type 1 diabetes mellitus receiving allogeneic islet cell transplantation. Transplantation 80:1718–1728. http://dx.doi.org/10.1097/01.tp.0000187881.97068.77.
  • Banerjee R, Halil O, Bain BJ, Cummins D, Banner NR. 2000. Neutrophil dysplasia caused by mycophenolate mofetil. Transplantation 70:1608–1610. http://dx.doi.org/10.1097/00007890-200012150-00012.
  • Nogueras F, Espinosa MD, Mansilla A, Torres JT, Cabrera MA, Martin-Vivaldi R. 2005. Mycophenolate mofetil-induced neutropenia in liver transplantation. Transplant Proc 37:1509–1511. http://dx.doi.org/10.1016/j.transproceed.2005.02.038.
  • Cowley AW, Jr. 1992. Long-term control of arterial blood pressure. Physiol Rev 72:231–300.
  • Hwang S, Song KD, Lesourne R, Lee J, Pinkhasov J, Li L, El-Khoury D, Love PE. 2012. Reduced TCR signaling potential impairs negative selection but does not result in autoimmune disease. J Exp Med 209:1781–1795. http://dx.doi.org/10.1084/jem.20120058.
  • Ruiz S, Santos E, Bustelo XR. 2009. The use of knockout mice reveals a synergistic role of the Vav1 and Rasgrf2 gene deficiencies in lymphomagenesis and metastasis. PLoS One 4:e8229. http://dx.doi.org/10.1371/journal.pone.0008229.
  • Sommers CL, Lee J, Steiner KL, Gurson JM, Depersis CL, El-Khoury D, Fuller CL, Shores EW, Love PE, Samelson LE. 2005. Mutation of the phospholipase C-γ1-binding site of LAT affects both positive and negative thymocyte selection. J Exp Med 201:1125–1134. http://dx.doi.org/10.1084/jem.20041869.
  • Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, Sakihama T, Matsutani T, Negishi I, Nakatsuru S, Sakaguchi S. 2003. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 426:454–460. http://dx.doi.org/10.1038/nature02119.
  • Pan D, Amison RT, Riffo-Vasquez Y, Spina D, Cleary SJ, Wakelam MJ, Page CP, Pitchford SC, Welch HC. 2015. P-Rex and Vav Rac-GEFs in platelets control leukocyte recruitment to sites of inflammation. Blood 125:1146–1158. http://dx.doi.org/10.1182/blood-2014-07-591040.
  • Lawson CD, Donald S, Anderson KE, Patton DT, Welch HC. 2011. P-Rex1 and Vav1 cooperate in the regulation of formyl-methionyl-leucyl-phenylalanine-dependent neutrophil responses. J Immunol 186:1467–1476. http://dx.doi.org/10.4049/jimmunol.1002738.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.