Advertisement

Integration of purinergic and angiotensin II receptor function in renal vascular responses and renal injury in angiotensin II-dependent hypertension

  • Martha FrancoEmail author
  • Oscar Pérez-Méndez
  • Supaporn Kulthinee
  • L. Gabriel Navar
Review Article
  • 18 Downloads

Abstract

Glomerular arteriolar vasoconstriction and tubulointerstitial injury are observed before glomerular damage occurs in models of hypertension. High interstitial ATP concentrations, caused by the increase in arterial pressure, alter renal mechanisms involved in the long-term control of blood pressure, autoregulation of glomerular filtration rate and blood flow, tubuloglomerular feedback (TGF) responses, and sodium excretion. Elevated ATP concentrations and augmented expression of P2X receptors have been demonstrated under a genetic background or induction of hypertension with vasoconstrictor peptides. In addition to the alterations of the microcirculation in the hypertensive kidney, the vascular actions of elevated intrarenal angiotensin II levels may be mitigated by the administration of broad purinergic P2 antagonists or specific P2Y12, P2X1, and P2X7 receptor antagonists. Furthermore, the prevention of tubulointerstitial infiltration with immunosuppressor compounds reduces the development of salt-sensitive hypertension, indicating that tubulointerstitial inflammation is essential for the development and maintenance of hypertension. Inflammatory cells also express abundant purinergic receptors, and their activation by ATP induces cytokine and growth factor release that in turn contributes to augment tubulointerstitial inflammation. Collectively, the evidence suggests a pathophysiological activation of purinergic P2 receptors in angiotensin-dependent hypertension. Coexistent increases in intrarenal angiotensin II and activates Ang II AT1 receptors, which interacts with over-activated purinergic receptors in a complex manner, suggesting convergence of their post-receptor signaling processes.

Keywords

Hypertension ATP P2X antagonists Purinergic P2X receptors Angiotensin II Renal hemodynamics AT1 receptor antagonists 

Notes

Funding information

This work was supported by grant number 219981 (to M Franco) from the National Council of Sciences and Technology (CONACYT) Mexico and L G Navar and Suppaporn Kulthinee were supported in part by a Center of Biomedical Research Excellence grant from the National Institute of General Medical Sciences (P30-GM-103337).

Compliance with ethical standards

Conflict of interest

Martha Franco declares that she has no conflict of interest.

Oscar Pérez-Mendez declares that he has no conflict of interest.

Supaporn Kulthinee declares that he has no conflict of interest.

L Gabriel Navar declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Tolins JP, Shultz P, Raij L (1988) Mechanisms of hypertensive glomerular injury. Am J Cardiol 62:54G–58GCrossRefGoogle Scholar
  2. 2.
    Johnson RJ, Schreiner GF (1997) Hypothesis: the role of acquired tubulointerstitial disease in the pathogenesis of salt-dependent hypertension. Kidney Int 52:1169–1179CrossRefGoogle Scholar
  3. 3.
    Johnson RJ, Herrera-Acosta J, Schreiner GF, Rodríguez-Iturbe (2002) Subtle acquired renal injury as a mechanism of salt-sensitive hypertension. N Engl J Med 346:913–923CrossRefGoogle Scholar
  4. 4.
    Franco M, Martínez F, Rodríguez-Iturbe B, Johnson RJ, Santamaría J, Montoya A, Nepomuceno T, Bautista R, Tapia E, Herrera-Acosta J (2006) Angiotensin II, interstitial inflammation and the pathogenesis of salt-sensitive hypertension. Am J Physiol Renal Physiol 291:F1281–F1287CrossRefGoogle Scholar
  5. 5.
    Franco M, Tapia E, Bautista R, Pacheco U, Santamaria J, Quiroz Y, Johnson RJ, Rodriguez-Iturbe B (2013) Impaired pressure natriuresis resulting in salt-sensitive hypertension is caused by tubulointerstitial immune cell infiltration in the kidney. Am J Physiol Renal Physiol 304:F982–F990CrossRefGoogle Scholar
  6. 6.
    Weinberg M, Fineberg NS (1991) Sodium and volume sensitivity of blood pressure. Age and pressure change over time. Hypertension 18:67–71CrossRefGoogle Scholar
  7. 7.
    Franco M, Bautista R, Pérez-Méndez O, González L, Pacheco U, Sánchez-Lozada LG, Tapia E, Morreal R, Martínez F (2008) Renal interstitial adenosine is increased in angiotensin II-induced hypertensive rats. Am J Physiol Renal Physiol 294:F84–F92CrossRefGoogle Scholar
  8. 8.
    Sealey JE, Blumenfield JD, Bell GM, Pecker MS, Sommers SC, Laragh JH (1988) On the renal basis for essential hypertension: nephron heterogeneity with discordant rennin secretion and sodium excretion causing hypertensive vasoconstriction-volume relationship. J Hypertens 6:763–777CrossRefGoogle Scholar
  9. 9.
    Franco M, Tapia E, Santamaría J, Zafra I, García-Torres R, Gordon KL, Pons H, Rodríguez-Iturbe B, Johnson JR, Herrera-Acosta J (2001) Renal cortical vasoconstriction contributes to the development of salt sensitive hypertension after angiotensin II exposure. J Am Soc Nephrol 10:2263–2271Google Scholar
  10. 10.
    Yamamoto K, Furuya K, Nakamura M, Kobatake E, Sokabe M, Ando J (2011) Visualization of flow-induced ATP release and triggering of Ca2+ waves at caveolae in vascular endothelial cells. J Cell Sci 124:3477–34832CrossRefGoogle Scholar
  11. 11.
    Yamamoto K, Sokabe T, Ohura N, Nakatsuka H, Kamiya A, Ando J (2003) Endogenously released ATP mediates shear stress-induced Ca2+ influx into pulmonary artery endothelial cells. Am J Physiol Heart Circ Physiol 285:H793–H803CrossRefGoogle Scholar
  12. 12.
    Yamamoto K, Korenaga R, Kamiya A, Ando J (2000) Fluid shear stress activates Ca (2+) influx into human endothelial cells via P2X4 purinoceptors. Circ Res 87:385–391CrossRefGoogle Scholar
  13. 13.
    Yamamoto K, Korenaga R, Kamiya A, Qi Z, Sokabe M, Ando J (2000) P2X (4) receptors mediate ATP-induced calcium influx in human vascular endothelial cells. Am J Physiol Heart Circ Physiol 279:H285–H292CrossRefGoogle Scholar
  14. 14.
    Nishiyama A, Majid DS, Taher KA, Miyatake A, Navar LG (2000) Relation between interstitial ATP concentrations and autoregulation-mediated changes in vascular resistance. Circ Res 86:656–662CrossRefGoogle Scholar
  15. 15.
    Bell PD, Lapoint JY, Sabirov R, Hayashi S, Peti-Peterdy J, Manabe KI, Kovacs G, Osaka Y (2003) Macula densa signaling involves ATP release through a maxi anion channel. Proc Natl Acad Sci 100:4322–4327CrossRefGoogle Scholar
  16. 16.
    Palygin O, Evans LC, Cowley AW Jr, Staruschenko A (2017) Acute in vivo analysis of ATP release in rat kidneys in response to changes of renal perfusion pressure. J Am Heart Assoc 6:e006658CrossRefGoogle Scholar
  17. 17.
    Peti-Peterdi J (2006) Calcium wave of tubuloglomerular feedback. Am J Physiol Renal Physiol 291:F473–F480CrossRefGoogle Scholar
  18. 18.
    Dosch M, Gerber J, Jebbawi F, Beldi G (2018) Mechanisms of ATP release by inflammatory cells. Int J Mol Sci 19:1222CrossRefGoogle Scholar
  19. 19.
    McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CC, Beck PL, Muruve DA, Kubes P (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330:362–366CrossRefGoogle Scholar
  20. 20.
    Vitiello L, Gorini S, Rosano G, la Sala A (2012) Immunoregulation through extracellular nucleotides. Blood 120:511–518CrossRefGoogle Scholar
  21. 21.
    Franco M, Bautista-Pérez R, Cano-Martínez A, Pacheco U, Santamaría J, Del Valle-Mondragón L, Pérez-Méndez O, Navar LG (2017) Physiopathological implications of P2X1 and P2X7 receptors in regulation of glomerular hemodynamics in angiotensin II-induced hypertension. Am J Physiol Renal Physiol 313(F):9–F19CrossRefGoogle Scholar
  22. 22.
    Robinson LE, Murrell-Lagnado (2013) The trafficking and targeting of P2X receptors. Front Cell Neurosci 7:233Google Scholar
  23. 23.
    Takenaka T, Inoue T, Kanno Y, Osaka H, Hill CE, Suzuki H (2008) Conexin 37 and 40 transduce purinergic signals mediating renal autoregulation. Am J Physiol Integr Comp Physiol 294:R1–R11CrossRefGoogle Scholar
  24. 24.
    Graciano ML, Nishiyama A, Jackson K, Seth DM, Ortiz RM, Prieto-Carrasquero M, Kobori H, Navar LG (2008) Purinergic receptors contribute to early mesangial transformation and renal vessel hypertrophy during angiotensin II induced hypertension. Am J Physiol Renal Physiol 294:F161–F169CrossRefGoogle Scholar
  25. 25.
    Ji X, Naito Y, Hirokawa G, Weng H, Hiura Y, Takahashi R, Iwai N (2012) P2X(7) receptor antagonism attenuates the hypertension and renal injury in Dahl salt sensitive rats. Hypertens Res 35:173–179CrossRefGoogle Scholar
  26. 26.
    Guan Z, Inscho EW (2011) Role of adenosine 5′triphosphate in regulating renal microvascular function and in hypertension. Hypertension 58:333–340CrossRefGoogle Scholar
  27. 27.
    Menzies RI, Unwin RJ, Bailey MA (2015) P2 receptors and hypertension. Acta Physiol (Oxf) 213:S232–S241CrossRefGoogle Scholar
  28. 28.
    Menzies RI, Howarth AR, Unwin RJ, Frederick WK, Mullis JJ, Bailey MA (2015) Inhibition of the purinergic P2X7 receptor improves renal perfusion in angiotensin-II-infused rats. Kidney Int 88:1079–1087CrossRefGoogle Scholar
  29. 29.
    Sipos A, Vargas SL, Toma I, Hanner F, Willecke K, Peti-Peterdi J (2009) Connexin 30 deficiency impairs renal tubular ATP release and pressure natriuresis. J Am Soc Nephrol 20:1724–1732CrossRefGoogle Scholar
  30. 30.
    Vonend O, Turner CM, Chan CM, Loesch A, DellÄnna GC, Srai KS, Burnstock G, Unwin RJ (2004) Glomerular expression of the ATP-sensitive P2X receptor in diabetic and hypertensive rat models. Kidney Int 66:157–166CrossRefGoogle Scholar
  31. 31.
    Franco M, Bautista R, Tapia E, Soto V, Santamaría J, Osorio H, Pacheco U, Sánchez-Lozada LG, Kobori H, Navar LG (2011) Contribution of renal purinergic receptors to renal vasoconstriction in angiotensin II-induced hypertensive rats. Am J Physiol Renal Physiol 300:F1301–F1309CrossRefGoogle Scholar
  32. 32.
    Guyton AC (1991) Blood pressure control: special role of the kidneys and body fluids. Science 252:1813–1816CrossRefGoogle Scholar
  33. 33.
    Guyton AC (1990) The surprising kidney-fluid mechanism for pressure control, its infinite gain. Hypertension 16:725–730CrossRefGoogle Scholar
  34. 34.
    Ivy JR, Bailey MA (2014) Pressure natriuresis and the renal control of arterial blood pressure. J Physiol 592:3955–3396CrossRefGoogle Scholar
  35. 35.
    Menzies RI, Unwin RJ, Rash RK, Beard DA, Cowley AW Jr, Callsin BE, Mullins JJ, Bailey MA (2013) Effect of P2X4 and P2X7 receptor antagonism on the pressure diuresis relationship in rats. Front Physiol 4:235CrossRefGoogle Scholar
  36. 36.
    Mironova E, Boiko N, Bugaj V, Stockand JD (2015) Regulation of sodium excretion and arterial blood pressure by purinergic signaling intrinsic to the distal nephron: consequences and mechanisms. Acta Physiol (Oxf) 213:213–221CrossRefGoogle Scholar
  37. 37.
    Rieg T, Bundey RA, Chen Y, Deschenes G, Junger W, Insel PA, Vallon V (2007) Mice lacking P2Y2 receptors have salt-resistant hypertension and facilitated renal Na+ and water reabsorption. FASEB J 21:3717–3726CrossRefGoogle Scholar
  38. 38.
    Majid DS, Inscho EW, Navar LG (1999) P2 purinoceptor saturation by adenosine triphosphate impairs renal autoregulation in dogs. J Am Soc Nephrol 10:492–498Google Scholar
  39. 39.
    Guan Z, Fellner RC, Van Beusecum J, Inscho EW (2014) P2 receptors in renal autoregulation. Curr Vasc Pharmacol 12:818–828CrossRefGoogle Scholar
  40. 40.
    Osmond DA, Zhang S, Polloch JS, Yamamoto T, De Miguel C, Inscho EW (2014) Clopidogrel preserves kidney autoregulatory behavior in Ang II-induced hypertension. Am J Physiol Renal Physiol 306:F619–F628CrossRefGoogle Scholar
  41. 41.
    Osmond DA, Inscho EW (2010) P2X1 receptor blockade inhibits whole kidney autoregulation of renal blood flow in vivo. Am J Physiol Renal Physiol 298:F1360–F13641CrossRefGoogle Scholar
  42. 42.
    Erlinge D, Yoo H, Edvinsson L, Reis DJ, Wahlestedt C (1993) Mitogenic effects of ATP on vascular smooth muscle cells vs. other growth factors and sympathetic cotransmitters. Am J Physiol Heart Circ Physiol 265:H1089–H1097CrossRefGoogle Scholar
  43. 43.
    Wang DJ, Huang NN, Heppel LA (1992) Extracellular ATP and ADP stimulate proliferation of porcine aortic smooth muscle cells. J Cell Physiol 153:221–233CrossRefGoogle Scholar
  44. 44.
    Gomvault A, Baron L, Couillin I (2012) ATP release and purinergic signalling in NLRP3 inflammasome activation. Front Immunol 3:414Google Scholar
  45. 45.
    Harrison DG, Guzik TJ, Lob EH, Madur MS, Marvar PJ, Thabet SR, Vinh A, Weyand CM (2011) Inflammation, immunity and hypertension. Hypertension 57:132–140CrossRefGoogle Scholar
  46. 46.
    Rodríguez-Iturbe B, Johnson RJ (2010) The role of renal microvascular disease and interstitial inflammation in salt-sensitive hypertension. Hypertens Res 33:975–980CrossRefGoogle Scholar
  47. 47.
    Johnson RJ, Alpers CE, Yoshimura A, Lombardi D, Prinzl P, Floege J, Schwartz SM (1992) Renal injury from angiotensin II-mediated hypertension. Hypertension 19:664–674Google Scholar
  48. 48.
    Lombardi D, Gordon KL, Polinsky P, Suga S, Schwartz SM, Johnson RJ (1999) Salt-sensitive hypertension develops after short term exposure to angiotensin II. Hypertension 33:1013–1019CrossRefGoogle Scholar
  49. 49.
    Menzies RI, Tam Frederick WT, Unwin RJ, Bailey MA (2017) Purinergic signaling in kidney disease. Kidney Int 91:315–316CrossRefGoogle Scholar
  50. 50.
    Craigie E, Birch RE, Unwin RJ, Wildman SS (2013) The relationship between P2X4 and P2X7: a physiologically important interaction? Front Physiol 4:216CrossRefGoogle Scholar
  51. 51.
    De Miguel C, Guo C, Lund H, Feng D, Mattson DL (2011) Infiltrating T lymphocytes in the kidney increase oxidative stress and participate in the development of hypertension and renal disease. Am J Physiol Renal Physiol 300:F734–F742CrossRefGoogle Scholar
  52. 52.
    Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, Panther E, Di Virgilio F (2006) The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 176:3877–3883CrossRefGoogle Scholar
  53. 53.
    Kawano A, Tsukimoto M, Mori D, Noguchi T, Harada H, Takenouchi T, Kitani H, Kojima S (2012) Regulation of P2X7-dependent inflammatory functions by P2X4 receptor in mouse macrophages. Biochem Biophys Res Commun 420:102–107CrossRefGoogle Scholar
  54. 54.
    Shao W, Seth DM, Navar LG (2009) Augmentation of endogenous intrarenal angiotensin II levels in Val5-AngII-infused rats. Am J Phys Renal Phys 296:F1067–F1071Google Scholar
  55. 55.
    Kassack MU, Braun K, Ganso M, Ullmann H, Nickel P, Böing B, Müller G, Lambrecht G (2004) Structure-activity relationships of analogues of NF449 confirm NF449 as the most potent and selective known P2X1 receptor antagonist. Eur J Med Chem 39:345–357CrossRefGoogle Scholar
  56. 56.
    Donnelly-Roberts DL, Namovic MT, Han P, Jarvis MF (2009) Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br J Pharmacol 157:1203–1214CrossRefGoogle Scholar
  57. 57.
    Chan CM, Unwin RJ, Bardini M, Oglesby IB, Ford AP, Townsend-Nicholson A, Burnstock G (1998) Localization of P2X1 purinoceptors by autoradiography and immunohistochemistry in rat kidneys. Am J Physiol Renal Physiol 274:F799–F804CrossRefGoogle Scholar
  58. 58.
    Turner CM, Vonend O, Chan C, Burnstock G, Unwin RJ (2003) The pattern of distribution of selected ATP- sensitive P2 receptor subtypes in normal rat kidney: an immunohistological study. Cell Tissues Organs 175:105–117CrossRefGoogle Scholar
  59. 59.
    Taylor SR, Turner CM, Elliott JI, McDaid J, Hewitt R, Smith J, Pickering MC, Whitehouse DL, Cook HT, Burnstock G, Pusey CD, Unwin RJ, Tam FW (2009) P2X7 deficiency attenuates renal injury in experimental glomerulonephritis. J Am Soc Nephrol 20:1275–1281CrossRefGoogle Scholar
  60. 60.
    Bernier LP, Ase AR, Séguéla P (2013) Post-translational regulation of P2X receptor channels: modulation by phospholipids. Front Cell Neurosci 7:226CrossRefGoogle Scholar
  61. 61.
    Povstyan OV, Harhun MI, Gordienko DV (2011) Ca2+ entry following P2X receptor activation induces IP3 receptor-mediated Ca2+ release in myocytes from small renal arteries. Br J Pharmacol 162:1618–1638CrossRefGoogle Scholar
  62. 62.
    Lin Q, Zhao G, Fang X, Peng X, Tang H, Wang H, Jing R, Liu J, Lederer WJ, Chen J, Ouyang K (2016) IP3 receptors regulate vascular smooth muscle contractility and hypertension. J Clin Invest Insight (17):e89402Google Scholar
  63. 63.
    Solini A, Jacobini C, Ricci C, Chiozzi P, Amadio L, Pricci F, Di Mario U, Di Virgilio F, Pugliese G (2005) Purinergic modulation of mesangial extracellular matrix production: role in diabetic and other glomerular diseases. Kidney Int 67:875–885CrossRefGoogle Scholar
  64. 64.
    Ishida K, Matsumoto T, Taguchi K, Kamata K, Kobayashi T (2011) Mechanisms underlying altered extracellular nucleotide-induced contractions in mesenteric arteries from rats in later-stage type 2 diabetes: effect of ANG II type 1 receptor antagonism. Am J Physiol Heart Circ Physiol 301:H1850–H1861CrossRefGoogle Scholar
  65. 65.
    Chao CC, Huang CC, Lu DY, Wong KL, Chen YR, Chen TH, Leung YM (2012) Ca2+ store depletion and endoplasmic reticulum stress are involved in the P2X7 receptors-mediated neurotoxicity in differentiated NG108.15 cells. J Cell Biochem 113:1377–1385CrossRefGoogle Scholar
  66. 66.
    Hoesch RE, Yinger K, Weinreich D, Kao JP (2002) Coexistence of functional IP(3) receptor and ryanodine receptors in vagal sensory neurons and their activation by ATP. J Neurophysiol 88:1212–1219CrossRefGoogle Scholar
  67. 67.
    Sukhanova KY, Bouryi VA, Gordienko DV (2014) Convergence of ionotropic and metabotropic signal pathways upon activation of P2X receptors in vascular smooth muscle cells. Neurophysiololy 46:398–404CrossRefGoogle Scholar
  68. 68.
    Gómez GI, Fernández P, Velarde V, Sáenz JC (2018) Angiotensin II-induced mesangial cell damage is preceded by cell membrane permeabilization due to upregulation of non-selective channels. Int J Mol Sci 19:e957CrossRefGoogle Scholar
  69. 69.
    Inscho EW, Cook AK, Webb RC, Jin LM (2009) Rho-kinase inhibition reduces pressure-mediated autoregulatory adjustments in afferent arteriolar diameter. Am J Physiol Renal Physiol 296:F590–F597CrossRefGoogle Scholar
  70. 70.
    Fuller AJ, Benjamin C, Hauschild BC, Gonzalez-Villalobos R, Awayda MS, Imig JD, Inscho EW, Navar LG (2005) Calcium and chloride channel activation by angiotensin II-AT1 receptors in preglomerular vascular smooth muscle cells. Am J Physiol-Renal physiol 289:F760–F767CrossRefGoogle Scholar
  71. 71.
    Bours MJ, Dagnelie PC, Giuliani AL, Wesselius A, Di Virgilio F (2011) P2 receptors and extracellular ATP: a novel homeostatic pathway in inflammation. Front Biosci (Schol Ed) 3:1443–1456Google Scholar
  72. 72.
    Luttikhuizen DT, Harmsen MC, de Leij LF, van Luy MJ (2004) Expression of P2 receptors at sites of chronic inflammation. Cell Tissue Res 317:289–298CrossRefGoogle Scholar
  73. 73.
    Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, Isakson BE, Bayliss DA, Ravichandran KS (2010) Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 467:863–867CrossRefGoogle Scholar
  74. 74.
    Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, Lysiak JJ, Harden TK, Leitinger N, Ravichandran KS (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461:282–286CrossRefGoogle Scholar
  75. 75.
    Idzko M, Ferrari D, Eltzschig HK (2014) Nucleotide signaling during inflammation. Nature 509:310–317CrossRefGoogle Scholar
  76. 76.
    Wang L, Jacobsen SE, Bengtsson A, Erlinge D (2004) P2 receptor mRNA expression profiles in human lymphocytes, monocytes and CD34+ stem and progenitor cells. BMC Immunol 5:16CrossRefGoogle Scholar
  77. 77.
    Di Virgilio F (2015) P2X receptors and inflammation. Curr Med Chem 22:866–877CrossRefGoogle Scholar
  78. 78.
    Jacob F, Pérez Novo C, Bachert C, Van Crombruggen K (2013) Purinergic signaling in inflammatory cells. P2 receptor expression, functional effects, and modulation of inflammatory responses. Purinergic Signal 9:285–306CrossRefGoogle Scholar
  79. 79.
    Burnstock G (2016) P2X ion channel receptors and inflammation. Purinergic Signal 12:59–67CrossRefGoogle Scholar
  80. 80.
    Feng MG, Navar LG (2010) Afferent arteriolar vasodilator effect of adenosine predominantly involves A2B receptor activation. Am J Physiol Renal Physiol 299:F310–F315CrossRefGoogle Scholar
  81. 81.
    Mattson DL, James L, Berdan EA, Meister CJ (2006) Immune suppression attenuates hypertension and renal disease in the Dahl salt-sensitive rat. Hypertension 48:149–156CrossRefGoogle Scholar
  82. 82.
    Pechman KR, Basile DP, Lund H, Mattson DL (2008) Immune suppression blocks sodium-sensitive hypertension following recovery from ischemic acute renal failure. Am J Physiol Regul Integr Comp Physiol 294:R1234–R1239CrossRefGoogle Scholar
  83. 83.
    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–R1097CrossRefGoogle Scholar
  84. 84.
    Quiroz Y, Pons H, Gordon KL, Rincón J, Chávez M, Parra G, Herrera-Acosta J, Gómez-Garre D, Largo R, Egido J, Johnson RJ, Rodríguez-Iturbe B (2002) Mycophenolate mofetil prevents salt-sensitive hypertension resulting from nitric oxide synthesis inhibition. Am J Physiol Renal Physiol 282:F191–F201CrossRefGoogle Scholar
  85. 85.
    Rodríguez-Iturbe B, Vaziri ND, Herrera-Acosta J, Johnson RJ (2004) Oxidative stress, renal infiltration of immune cells, and salt-sensitive hypertension: all for one and one for all. Am J Pyhsiol Renal Physiol 286:F606–F616CrossRefGoogle Scholar
  86. 86.
    Franco M, Martínez F, Quiroz Y, Galicia O, Bautista R, Johnson RJ, Rodríguez-Iturbe B (2007) Renal angiotensin II concentration and interstitial infiltration of immune cells are correlated with blood pressure levels in salt-sensitive hypertension. Am J Physiol Regul Integr Comp Physiol 293:R251–R256CrossRefGoogle Scholar
  87. 87.
    Vaziri ND, Rodriguez-Iturbe B (2006) Mechanisms of disease: oxidative stress and inflammation in the pathogenesis of hypertension. Nat Clin Pract Nephrol 2:582–593CrossRefGoogle Scholar
  88. 88.
    Hoch NE, Guzik TJ, Chen W, Deans T, Maalouf SA, Gratze P, Weyand C, Harrison DG (2009) Regulation of T-cell function by endogenously produced angiotensin II. Am J Physiol Regul Integr Comp Physiol 296:R208–R216CrossRefGoogle Scholar
  89. 89.
    Lara LS, McCormack M, Semprum-Prieto LS, Shenouda S, Majid DS, Kobori H, Navar LG, Prieto MC (2012) AT1 receptor-mediated augmentation of angiotensinogen, oxidative stress, and inflammation in ANG II-salt hypertension. Am J Physiol Renal Physiol 302:F85–F94CrossRefGoogle Scholar
  90. 90.
    Song J, Lu Y, Lai EY, Wei J, Wang L, Chandrashekar K, Wang S, Shen C, Juncos LA, Liu R (2015) Oxidative status in the macula densa modulates tubuloglomerular feedback responsiveness in angiotensin II-induced hypertension. Acta Physiol (Oxf) 213:249–258CrossRefGoogle Scholar
  91. 91.
    Matavelli LC, Zhou X, Varagic J, Susic D, Frohlich ED (2007) Salt loading produces severe renal hemodynamic dysfunction independent of arterial pressure in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 292:H814–H819CrossRefGoogle Scholar
  92. 92.
    Sannai T, Kimura G (1996) Renal function reserve and sodium sensitivity in essential hypertension. J Lab Clin Med 128:89–97CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Nephrology, Renal Pathophysiology LaboratoryInstituto Nacional de Cardiología “Ignacio Chávez”Mexico CityMexico
  2. 2.Department Molecular BiologyInstituto Nacional de Cardiología “Ignacio Chávez”Mexico CityMexico
  3. 3.Department of Physiology and Hypertension and Renal CenterTulane University School of MedicineNew OrleansUSA
  4. 4.Department of Cardiovascular and Thoracic Technology, Chulabhorn International College of MedicineThammasat UniversityRangsitThailand

Personalised recommendations