Skip to main content

Advertisement

SpringerLink
Log in

Salt feedback on the renin-angiotensin-aldosterone system

  • Invited Review
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

The renin-angiotensin-aldosterone system (RAAS) is a central element in the control of the salt and water balance of the body and arterial blood pressure. The activity of the RAAS is controlled by the protease renin, which is released from renal juxtaglomerular epithelioid cells (JGE cells) into the circulation. Renin release is regulated by a complex interplay of several locally acting hormones or mechanisms and longer feedback loops one of which involves salt intake. Acute NaCl loads or longer lasting high salt intakes suppress plasma renin activity, whereas reductions in NaCl intake stimulate it. Because the activation of the RAAS conserves the salt content of the body, a classical feedback loop between salt intake/body salt content and renin is established. Despite of its important role for body fluid homeostasis, the precise signaling pathways connecting salt intake with the synthesis and release of renin are only incompletely understood. Four putative controllers of the salt-dependent regulation of the RAAS have been suggested: (1) the macula densa mechanism which adjusts renin release in response to changes in the renal tubular salt concentration; (2) salt-dependent changes in the arterial blood pressure; (3) circulating salt-dependent hormones, particularly the atrial natriuretic peptide (ANP); and (4) renal sympathetic nervous activity, which is regulated by extracellular volume and arterial blood pressure. In this review, the role of these known controllers of the RAAS will be discussed with special emphasis on their relative contributions to the salt-dependent regulation of the RAAS at different time frames.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Aldehni F, Tang T, Madsen K, Plattner M, Schreiber A, Friis UG, Hammond HK, Han PL, Schweda F (2011) Stimulation of renin secretion by catecholamines is dependent on adenylyl cyclases 5 and 6. Hypertension 57:460–468. doi:10.1161/HYPERTENSIONAHA.110.167130

    PubMed Central  CAS  PubMed  Google Scholar 

  2. Andersen LJ, Andersen JL, Pump B, Bie P (2002) Natriuresis induced by mild hypernatremia in humans. Am J Physiol Regul Integr Comp Physiol 282:R1754–R1761. doi:10.1152/ajpregu.00732.2001

    CAS  PubMed  Google Scholar 

  3. Angelis E, Tse MY, Pang SC (2005) Interactions between atrial natriuretic peptide and the renin-angiotensin system during salt-sensitivity exhibited by the proANP gene-disrupted mouse. Mol Cell Biochem 276:121–131. doi:10.1007/s11010-005-3672-1

    CAS  PubMed  Google Scholar 

  4. Antunes-Rodrigues J, de Castro M, Elias LL, Valenca MM, McCann SM (2004) Neuroendocrine control of body fluid metabolism. Physiol Rev 84:169–208. doi:10.1152/physrev.00017.2003

    CAS  PubMed  Google Scholar 

  5. Bader M (2013) ACE2, angiotensin-(1-7), and Mas: the other side of the coin. Pflugers Arch 465:79–85

    CAS  PubMed  Google Scholar 

  6. Balment RJ, Brimble MJ, Forsling ML (1980) Release of oxytocin induced by salt loading and its influence on renal excretion in the male rat. J Physiol 308:439–449

    PubMed Central  CAS  PubMed  Google Scholar 

  7. Bell PD, Lapointe JY, Sabirov R, Hayashi S, Peti-Peterdi J, Manabe K, Kovacs G, Okada Y (2003) Macula densa cell signaling involves ATP release through a maxi anion channel. Proc Natl Acad Sci U S A 100:4322–4327. doi:10.1073/pnas.0736323100

    PubMed Central  CAS  PubMed  Google Scholar 

  8. Bellini C, Ferri C, Carlomagno A, Necozione S, Lepore AR, Desideri G, Santucci A (1996) Impaired inactive to active kallikrein conversion in human salt-sensitive hypertension. J Am Soc Nephrol 7:2565–2577

    CAS  PubMed  Google Scholar 

  9. Bie P, Molstrom S, Wamberg S (2009) Normotensive sodium loading in conscious dogs: regulation of renin secretion during beta-receptor blockade. Am J Physiol Regul Integr Comp Physiol 296:R428–R435. doi:10.1152/ajpregu.90753.2008

    CAS  PubMed  Google Scholar 

  10. Boivin V, Jahns R, Gambaryan S, Ness W, Boege F, Lohse MJ (2001) Immunofluorescent imaging of beta 1- and beta 2-adrenergic receptors in rat kidney. Kidney Int 59:515–531. doi:10.1046/j.1523-1755.2001.059002515.x

    CAS  PubMed  Google Scholar 

  11. Bosse HM, Bohm R, Resch S, Bachmann S (1995) Parallel regulation of constitutive NO synthase and renin at JGA of rat kidney under various stimuli. Am J Physiol 269:F793–F805

    CAS  PubMed  Google Scholar 

  12. Brown RD, Thoren P, Steege A, Mrowka R, Sallstrom J, Skott O, Fredholm BB, Persson AE (2006) Influence of the adenosine A1 receptor on blood pressure regulation and renin release. Am J Physiol Regul Integr Comp Physiol 290:R1324–R1329. doi:10.1152/ajpregu.00313.2005

    CAS  PubMed  Google Scholar 

  13. Carey RM (2013) The intrarenal renin-angiotensin and dopaminergic systems: control of renal sodium excretion and blood pressure. Hypertension 61:673–680. doi:10.1161/HYPERTENSIONAHA.111.00241

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Carey RM, McGrath HE, Pentz ES, Gomez RA, Barrett PQ (1997) Biomechanical coupling in renin-releasing cells. J Clin Invest 100:1566–1574. doi:10.1172/JCI119680

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Carillo BA, Beutel A, Mirandola DA, Vidonho AF Jr, Furukawa LN, Casarini D, Campos RR, Dolnikoff MS, Heimann JC, Bergamaschi CT (2007) Differential sympathetic and angiotensinergic responses in rats submitted to low- or high-salt diet. Regul Pept 140:5–11. doi:10.1016/j.regpep.2006.11.007

    CAS  PubMed  Google Scholar 

  16. Castrop H (2007) Mediators of tubuloglomerular feedback regulation of glomerular filtration: ATP and adenosine. Acta Physiol (Oxf) 189:3–14. doi:10.1111/j.1748-1716.2006.01610.x

    CAS  Google Scholar 

  17. Castrop H, Hocherl K, Kurtz A, Schweda F, Todorov V, Wagner C (2010) Physiology of kidney renin. Physiol Rev 90:607–673. doi:10.1152/physrev.00011.2009

    CAS  PubMed  Google Scholar 

  18. Castrop H, Schweda F, Mizel D, Huang Y, Briggs J, Kurtz A, Schnermann J (2004) Permissive role of nitric oxide in macula densa control of renin secretion. Am J Physiol Renal Physiol 286:F848–F857. doi:10.1152/ajprenal.00272.2003

    CAS  PubMed  Google Scholar 

  19. Chappell MC (2012) Nonclassical renin-angiotensin system and renal function. Compr Physiol 2:2733–2752. doi:10.1002/cphy.c120002

    PubMed Central  PubMed  Google Scholar 

  20. Churchill PC, Churchill MC (1985) A1 and A2 adenosine receptor activation inhibits and stimulates renin secretion of rat renal cortical slices. J Pharmacol Exp Ther 232:589–594

    CAS  PubMed  Google Scholar 

  21. Cuneo RC, Espiner EA, Crozier IG, Yandle TG, Nicholls MG, Ikram H (1989) Chronic and acute volume expansion in normal man: effect on atrial diameter and plasma atrial natriuretic peptide. Horm Metab Res 21:148–151. doi:10.1055/s-2007-1009176

    CAS  PubMed  Google Scholar 

  22. Cuneo RC, Espiner EA, Nicholls MG, Yandle TG, Livesey JH (1987) Effect of physiological levels of atrial natriuretic peptide on hormone secretion: inhibition of angiotensin-induced aldosterone secretion and renin release in normal man. J Clin Endocrinol Metab 65:765–772. doi:10.1210/jcem-65-4-765

    CAS  PubMed  Google Scholar 

  23. Damkjaer M, Isaksson GL, Stubbe J, Jensen BL, Assersen K, Bie P (2013) Renal renin secretion as regulator of body fluid homeostasis. Pflugers Arch 465:153–165. doi:10.1007/s00424-012-1171-2

    CAS  PubMed  Google Scholar 

  24. De Mello WC, Frohlich ED (2011) On the local cardiac renin angiotensin system. Basic Clin Implications Peptides 32:1774–1779. doi:10.1016/j.peptides.2011.06.018

    Google Scholar 

  25. Demerath T, Staffel J, Schreiber A, Valletta D, Schweda F (2014) Natriuretic peptides buffer renin-dependent hypertension. Am J Physiol Renal Physiol 306:F1489–F1498. doi:10.1152/ajprenal.00668.2013

    CAS  PubMed  Google Scholar 

  26. DiBona GF, Kopp UC (1997) Neural control of renal function. Physiol Rev 77:75–197

    CAS  PubMed  Google Scholar 

  27. DiBona GF, Sawin LL (1985) Renal nerve activity in conscious rats during volume expansion and depletion. Am J Physiol 248:F15–F23

    CAS  PubMed  Google Scholar 

  28. Doi Y, Franco-Saenz R, Mulrow PJ (1984) Evidence for an extrarenal source of inactive renin in rats. Hypertension 6:627–632

    CAS  PubMed  Google Scholar 

  29. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, Donovan M, Woolf B, Robison K, Jeyaseelan R, Breitbart RE, Acton S (2000) A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res 87:E1–E9

    CAS  PubMed  Google Scholar 

  30. Doorenbos CJ, Iestra JA, Papapoulos SE, Odink J, Van Brummelen P (1990) Atrial natriuretic peptide and chronic renal effects of changes in dietary protein and sodium intake in man. Clin Sci (Lond) 78:565–572

    CAS  Google Scholar 

  31. Farhi ER, Cant JR, Paganelli WC, Dzau VJ, Barger AC (1987) Stimulus-response curve of the renal baroreceptor: effect of converting enzyme inhibition and changes in salt intake. Circ Res 61:670–677

    CAS  PubMed  Google Scholar 

  32. Finke R, Gross R, Hackenthal E, Huber J, Kirchheim HR (1983) Threshold pressure for the pressure-dependent renin release in the autoregulating kidney of conscious dogs. Pflugers Arch 399:102–110

    CAS  PubMed  Google Scholar 

  33. Friberg P, Meredith I, Jennings G, Lambert G, Fazio V, Esler M (1990) Evidence for increased renal norepinephrine overflow during sodium restriction in humans. Hypertension 16:121–130

    CAS  PubMed  Google Scholar 

  34. Friis UG, Jensen BL, Aas JK, Skott O (1999) Direct demonstration of exocytosis and endocytosis in single mouse juxtaglomerular cells. Circ Res 84:929–936

    CAS  PubMed  Google Scholar 

  35. Friis UG, Madsen K, Stubbe J, Hansen PB, Svenningsen P, Bie P, Skott O, Jensen BL (2013) Regulation of renin secretion by renal juxtaglomerular cells. Pflugers Arch 465:25–37. doi:10.1007/s00424-012-1126-7

    CAS  PubMed  Google Scholar 

  36. Friis UG, Stubbe J, Uhrenholt TR, Svenningsen P, Nusing RM, Skott O, Jensen BL (2005) Prostaglandin E2 EP2 and EP4 receptor activation mediates cAMP-dependent hyperpolarization and exocytosis of renin in juxtaglomerular cells. Am J Physiol Renal Physiol 289:F989–F997. doi:10.1152/ajprenal.00201.2005

    CAS  PubMed  Google Scholar 

  37. Golin R, Pieruzzi F, Munforti C, Busca G, Di Blasio A, Zanchetti A (2001) Role of the renal nerves in the control of renin synthesis during different sodium intakes in the rat. J Hypertens 19:1271–1277

    CAS  PubMed  Google Scholar 

  38. Graffe CC, Bech JN, Pedersen EB (2012) Effect of high and low sodium intake on urinary aquaporin-2 excretion in healthy humans. Am J Physiol Renal Physiol 302:F264–F275. doi:10.1152/ajprenal.00442.2010

    CAS  PubMed  Google Scholar 

  39. Greenberg SG, Lorenz JN, He XR, Schnermann JB, Briggs JP (1993) Effect of prostaglandin synthesis inhibition on macula densa-stimulated renin secretion. Am J Physiol 265:F578–F583

    CAS  PubMed  Google Scholar 

  40. Gubler MC, Antignac C (2010) Renin-angiotensin system in kidney development: renal tubular dysgenesis. Kidney Int 77:400–406. doi:10.1038/ki.2009.423

    CAS  PubMed  Google Scholar 

  41. Hackenthal E, Paul M, Ganten D, Taugner R (1990) Morphology, physiology, and molecular biology of renin secretion. Physiol Rev 70:1067–1116

    CAS  PubMed  Google Scholar 

  42. Harris RC, McKanna JA, Akai Y, Jacobson HR, Dubois RN, Breyer MD (1994) Cyclooxygenase-2 is associated with the macula densa of rat kidney and increases with salt restriction. J Clin Invest 94:2504–2510. doi:10.1172/JCI117620

    PubMed Central  CAS  PubMed  Google Scholar 

  43. He FJ, Li J, Macgregor GA (2013) Effect of longer-term modest salt reduction on blood pressure. Cochrane Database Syst Rev 4, CD004937. doi:10.1002/14651858.CD004937.pub2

    PubMed  Google Scholar 

  44. He XR, Greenberg SG, Briggs JP, Schnermann J (1995) Effects of furosemide and verapamil on the NaCl dependency of macula densa-mediated renin secretion. Hypertension 26:137–142

    CAS  PubMed  Google Scholar 

  45. He XR, Greenberg SG, Briggs JP, Schnermann JB (1995) Effect of nitric oxide on renin secretion. II. Studies in the perfused juxtaglomerular apparatus. Am J Physiol 268:F953–F959

    CAS  PubMed  Google Scholar 

  46. Herr D, Bekes I, Wulff C (2013) Local renin-angiotensin system in the reproductive system. Front Endocrinol (Lausanne) 4:150. doi:10.3389/fendo.2013.00150

    Google Scholar 

  47. Hocherl K, Kammerl M, Kees F, Kramer BK, Grobecker HF, Kurtz A (2002) Role of renal nerves in stimulation of renin, COX-2, and nNOS in rat renal cortex during salt deficiency. Am J Physiol Renal Physiol 282:F478–F484. doi:10.1152/ajprenal.00209.2001

    CAS  PubMed  Google Scholar 

  48. Holdaas H, DiBona GF, Kiil F (1981) Effect of low-level renal nerve stimulation on renin release from nonfiltering kidneys. Am J Physiol 241:F156–F161

    CAS  PubMed  Google Scholar 

  49. Holmer S, Eckardt KU, LeHir M, Schricker K, Riegger G, Kurtz A (1993) Influence of dietary NaCl intake on renin gene expression in the kidneys and adrenal glands of rats. Pflugers Arch 425:62–67

    CAS  PubMed  Google Scholar 

  50. Holmer S, Rinne B, Eckardt KU, Le Hir M, Schricker K, Kaissling B, Riegger G, Kurtz A (1994) Role of renal nerves for the expression of renin in adult rat kidney. Am J Physiol 266:F738–F745

    CAS  PubMed  Google Scholar 

  51. Hyndman KA, Boesen EI, Elmarakby AA, Brands MW, Huang P, Kohan DE, Pollock DM, Pollock JS (2013) Renal collecting duct NOS1 maintains fluid-electrolyte homeostasis and blood pressure. Hypertension 62:91–98. doi:10.1161/HYPERTENSIONAHA.113.01291

    PubMed Central  CAS  PubMed  Google Scholar 

  52. Ingelfinger JR (2009) Angiotensin-converting enzyme 2: implications for blood pressure and kidney disease. Curr Opin Nephrol Hypertens 18:79–84. doi:10.1097/MNH.0b013e32831b70ad

    CAS  PubMed  Google Scholar 

  53. Isaksson GL, Stubbe J, Lyngs Hansen P, Jensen BL, Bie P (2013) Salt sensitivity of renin secretion, glomerular filtration rate and blood pressure in conscious Sprague-Dawley rats. Acta Physiol (Oxf). doi:10.1111/apha.12191

    Google Scholar 

  54. John SW, Krege JH, Oliver PM, Hagaman JR, Hodgin JB, Pang SC, Flynn TG, Smithies O (1995) Genetic decreases in atrial natriuretic peptide and salt-sensitive hypertension. Science 267:679–681

    CAS  PubMed  Google Scholar 

  55. Kambayashi Y, Bardhan S, Takahashi K, Tsuzuki S, Inui H, Hamakubo T, Inagami T (1993) Molecular cloning of a novel angiotensin II receptor isoform involved in phosphotyrosine phosphatase inhibition. J Biol Chem 268:24543–24546

    CAS  PubMed  Google Scholar 

  56. Kammerl MC, Nusing RM, Schweda F, Endemann D, Stubanus M, Kees F, Lackner KJ, Fischereder M, Kramer BK (2001) Low sodium and furosemide-induced stimulation of the renin system in man is mediated by cyclooxygenase 2. Clin Pharmacol Ther 70:468–474

    CAS  PubMed  Google Scholar 

  57. Karger C, Kurtz F, Steppan D, Schwarzensteiner I, Machura K, Angel P, Banas B, Risteli J, Kurtz A (2013) Procollagen I-expressing renin cell precursors. Am J Physiol Renal Physiol 305:F355–F361. doi:10.1152/ajprenal.00079.2013

    CAS  PubMed  Google Scholar 

  58. Kim SM, Chen L, Faulhaber-Walter R, Oppermann M, Huang Y, Mizel D, Briggs JP, Schnermann J (2007) Regulation of renin secretion and expression in mice deficient in beta1- and beta2-adrenergic receptors. Hypertension 50:103–109. doi:10.1161/HYPERTENSIONAHA.107.087577

    CAS  PubMed  Google Scholar 

  59. Kim SM, Chen L, Mizel D, Huang YG, Briggs JP, Schnermann J (2007) Low plasma renin and reduced renin secretory responses to acute stimuli in conscious COX-2-deficient mice. Am J Physiol Renal Physiol 292:F415–F422. doi:10.1152/ajprenal.00317.2006

    CAS  PubMed  Google Scholar 

  60. Kim SM, Eisner C, Faulhaber-Walter R, Mizel D, Wall SM, Briggs JP, Schnermann J (2008) Salt sensitivity of blood pressure in NKCC1-deficient mice. Am J Physiol Renal Physiol 295:F1230–F1238. doi:10.1152/ajprenal.90392.2008

    PubMed Central  CAS  PubMed  Google Scholar 

  61. Kim SM, Mizel D, Huang YG, Briggs JP, Schnermann J (2006) Adenosine as a mediator of macula densa-dependent inhibition of renin secretion. Am J Physiol Renal Physiol 290:F1016–F1023. doi:10.1152/ajprenal.00367.2005

    CAS  PubMed  Google Scholar 

  62. Kim SM, Mizel D, Qin Y, Huang Y, Schnermann J (2014) Blood pressure, heart rate and tubuloglomerular feedback in A1AR-deficient mice with different genetic backgrounds. Acta Physiol (Oxf). doi:10.1111/apha.12377

    Google Scholar 

  63. Kinoshita H, Fujimoto S, Nakazato M, Yokota N, Date Y, Yamaguchi H, Hisanaga S, Eto T (1997) Urine and plasma levels of uroguanylin and its molecular forms in renal diseases. Kidney Int 52:1028–1034

    CAS  PubMed  Google Scholar 

  64. Kjolby M, Bie P (2008) Chronic activation of plasma renin is log-linearly related to dietary sodium and eliminates natriuresis in response to a pulse change in total body sodium. Am J Physiol Regul Integr Comp Physiol 294:R17–R25. doi:10.1152/ajpregu.00435.2007

    CAS  PubMed  Google Scholar 

  65. Krop M, Lu X, Danser AH, Meima ME (2013) The (pro)renin receptor. A decade of research: what have we learned? Pflugers Arch 465:87–97. doi:10.1007/s00424-012-1105-z

    PubMed Central  CAS  PubMed  Google Scholar 

  66. Kurtz A (2011) Renin release: sites, mechanisms, and control. Annu Rev Physiol 73:377–399. doi:10.1146/annurev-physiol-012110-142238

    CAS  PubMed  Google Scholar 

  67. Kurtz A, Della Bruna R, Pfeilschifter J, Bauer C (1988) Role of cGMP as second messenger of adenosine in the inhibition of renin release. Kidney Int 33:798–803

    CAS  PubMed  Google Scholar 

  68. Kurtz A, Della Bruna R, Pfeilschifter J, Taugner R, Bauer C (1986) Atrial natriuretic peptide inhibits renin release from juxtaglomerular cells by a cGMP-mediated process. Proc Natl Acad Sci U S A 83:4769–4773

    PubMed Central  CAS  PubMed  Google Scholar 

  69. Kurtz A, Wagner C (1998) Role of nitric oxide in the control of renin secretion. Am J Physiol 275:F849–F862

    CAS  PubMed  Google Scholar 

  70. Lopez MJ, Wong SK, Kishimoto I, Dubois S, Mach V, Friesen J, Garbers DL, Beuve A (1995) Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide. Nature 378:65–68. doi:10.1038/378065a0

    CAS  PubMed  Google Scholar 

  71. Lopez MLSS, Pentz ES, Nomasa T, Smithies O, Gomez RA (2004) Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened. Dev Cell 6:719–728

    CAS  Google Scholar 

  72. Lorenz JN, Kotchen TA, Ott CE (1990) Effect of Na and Cl infusion on loop function and plasma renin activity in rats. Am J Physiol 258:F1328–F1335

    CAS  PubMed  Google Scholar 

  73. Lorenz JN, Weihprecht H, Schnermann J, Skott O, Briggs JP (1991) Renin release from isolated juxtaglomerular apparatus depends on macula densa chloride transport. Am J Physiol 260:F486–F493

    CAS  PubMed  Google Scholar 

  74. Luft FC, Dechend R, Muller DN (2012) Immune mechanisms in angiotensin II-induced target-organ damage. Ann Med 44(Suppl 1):S49–S54. doi:10.3109/07853890.2011.653396

    CAS  PubMed  Google Scholar 

  75. Machura K, Neubauer B, Steppan D, Kettl R, Grobeta A, Kurtz A (2012) Role of blood pressure in mediating the influence of salt intake on renin expression in the kidney. Am J Physiol Renal Physiol 302:F1278–F1285. doi:10.1152/ajprenal.00688.2011

    CAS  PubMed  Google Scholar 

  76. Machura K, Steppan D, Neubauer B, Alenina N, Coffman TM, Facemire CS, Hilgers KF, Eckardt KU, Wagner C, Kurtz A (2009) Developmental renin expression in mice with a defective renin-angiotensin system. Am J Physiol Renal Physiol 297:F1371–F1380. doi:10.1152/ajprenal.00378.2009

    CAS  PubMed  Google Scholar 

  77. Mann B, Hartner A, Jensen BL, Kammerl M, Kramer BK, Kurtz A (2001) Furosemide stimulates macula densa cyclooxygenase-2 expression in rats. Kidney Int 59:62–68. doi:10.1046/j.1523-1755.2001.00466.x

    CAS  PubMed  Google Scholar 

  78. Matzdorf C, Kurtz A, Hocherl K (2007) COX-2 activity determines the level of renin expression but is dispensable for acute upregulation of renin expression in rat kidneys. Am J Physiol Renal Physiol 292:F1782–F1790. doi:10.1152/ajprenal.00513.2006

    CAS  PubMed  Google Scholar 

  79. Mayan H, Ling KT, Lee EY, Wiedemann E, Kalinyak JE, Humphreys MH (1996) Dietary sodium intake modulates pituitary proopiomelanocortin mRNA abundance. Hypertension 28:244–249

    CAS  PubMed  Google Scholar 

  80. Melo LG, Veress AT, Chong CK, Pang SC, Flynn TG, Sonnenberg H (1998) Salt-sensitive hypertension in ANP knockout mice: potential role of abnormal plasma renin activity. Am J Physiol 274:R255–R261

    CAS  PubMed  Google Scholar 

  81. Mente A, O'Donnell MJ, Rangarajan S, McQueen MJ, Poirier P, Wielgosz A, Morrison H, Li W, Wang X, Di C, Mony P, Devanath A, Rosengren A, Oguz A, Zatonska K, Yusufali AH, Lopez-Jaramillo P, Avezum A, Ismail N, Lanas F, Puoane T, Diaz R, Kelishadi R, Iqbal R, Yusuf R, Chifamba J, Khatib R, Teo K, Yusuf S, Investigators P (2014) Association of urinary sodium and potassium excretion with blood pressure. N Engl J Med 371:601–611. doi:10.1056/NEJMoa1311989

    CAS  PubMed  Google Scholar 

  82. Molstrom S, Larsen NH, Simonsen JA, Washington R, Bie P (2009) Normotensive sodium loading in normal man: regulation of renin secretion during beta-receptor blockade. Am J Physiol Regul Integr Comp Physiol 296:R436–R445. doi:10.1152/ajpregu.90754.2008

    PubMed  Google Scholar 

  83. Morgan T, Barrett G, Zhang YL, Alcorn D (1991) The role of the macula densa in renin synthesis. Clin Exp Pharmacol Physiol 18:123–126

    CAS  PubMed  Google Scholar 

  84. Nash FD, Rostorfer HH, Bailie MD, Wathen RL, Schneider EG (1968) Renin release: relation to renal sodium load and dissociation from hemodynamic changes. Circ Res 22:473–487

    CAS  PubMed  Google Scholar 

  85. Neubauer B, Machura K, Kettl R, Lopez ML, Friebe A, Kurtz A (2013) Endothelium-derived nitric oxide supports renin cell recruitment through the nitric oxide-sensitive guanylate cyclase pathway. Hypertension 61:400–407. doi:10.1161/HYPERTENSIONAHA.111.00221

    PubMed Central  CAS  PubMed  Google Scholar 

  86. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD (2002) Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest 109:1417–1427. doi:10.1172/JCI14276

    PubMed Central  CAS  PubMed  Google Scholar 

  87. Ni XP, Pearce D, Butler AA, Cone RD, Humphreys MH (2003) Genetic disruption of gamma-melanocyte-stimulating hormone signaling leads to salt-sensitive hypertension in the mouse. J Clin Invest 111:1251–1258. doi:10.1172/JCI16993

    PubMed Central  CAS  PubMed  Google Scholar 

  88. Oliver JA, Pinto J, Sciacca RR, Cannon PJ (1980) Increased renal secretion of norepinephrine and prostaglandin E2 during sodium depletion in the dog. J Clin Invest 66:748–756. doi:10.1172/JCI109912

    PubMed Central  CAS  PubMed  Google Scholar 

  89. Oppermann M, Mizel D, Huang G, Li C, Deng C, Theilig F, Bachmann S, Briggs J, Schnermann J, Castrop H (2006) Macula densa control of renin secretion and preglomerular resistance in mice with selective deletion of the B isoform of the Na,K,2Cl co-transporter. J Am Soc Nephrol 17:2143–2152. doi:10.1681/ASN.2006040384

    CAS  PubMed  Google Scholar 

  90. Oppermann M, Mizel D, Kim SM, Chen L, Faulhaber-Walter R, Huang Y, Li C, Deng C, Briggs J, Schnermann J, Castrop H (2007) Renal function in mice with targeted disruption of the A isoform of the Na-K-2Cl co-transporter. J Am Soc Nephrol 18:440–448. doi:10.1681/ASN.2006091070

    CAS  PubMed  Google Scholar 

  91. Overlack A, Ruppert M, Kolloch R, Gobel B, Kraft K, Diehl J, Schmitt W, Stumpe KO (1993) Divergent hemodynamic and hormonal responses to varying salt intake in normotensive subjects. Hypertension 22:331–338

    CAS  PubMed  Google Scholar 

  92. Padia SH, Carey RM (2013) AT2 receptors: beneficial counter-regulatory role in cardiovascular and renal function. Pflugers Arch 465:99–110. doi:10.1007/s00424-012-1146-3

    PubMed Central  CAS  PubMed  Google Scholar 

  93. Paul M, Poyan Mehr A, Kreutz R (2006) Physiology of local renin-angiotensin systems. Physiol Rev 86:747–803. doi:10.1152/physrev.00036.2005

    CAS  PubMed  Google Scholar 

  94. Peters J (2012) Local renin-angiotensin systems in the adrenal gland. Peptides 34:427–432. doi:10.1016/j.peptides.2012.01.023

    CAS  PubMed  Google Scholar 

  95. Peti-Peterdi J, Komlosi P, Fuson AL, Guan Y, Schneider A, Qi Z, Redha R, Rosivall L, Breyer MD, Bell PD (2003) Luminal NaCl delivery regulates basolateral PGE2 release from macula densa cells. J Clin Invest 112:76–82. doi:10.1172/JCI18018

    PubMed Central  CAS  PubMed  Google Scholar 

  96. Pieruzzi F, Munforti C, Di Blasio A, Busca G, Dadone V, Zanchetti A, Golin R (2002) Neuronal nitric oxide synthase and renin stimulation by sodium deprivation are dependent on the renal nerves. J Hypertens 20:2039–2045

    CAS  PubMed  Google Scholar 

  97. Prieto MC, Gonzalez AA, Navar LG (2013) Evolving concepts on regulation and function of renin in distal nephron. Pflugers Arch 465:121–132. doi:10.1007/s00424-012-1151-6

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Ruster C, Wolf G (2011) Angiotensin II as a morphogenic cytokine stimulating renal fibrogenesis. J Am Soc Nephrol 22:1189–1199. doi:10.1681/ASN.2010040384

    PubMed  Google Scholar 

  99. Sagnella GA, Markandu ND, Shore AC, MacGregor GA (1985) Effects of changes in dietary sodium intake and saline infusion on immunoreactive atrial natriuretic peptide in human plasma. Lancet 2:1208–1211

    CAS  PubMed  Google Scholar 

  100. Sallstrom J, Carlstrom M, Jensen BL, Skott O, Brown RD, Persson AE (2008) Neuronal nitric oxide synthase-deficient mice have impaired renin release but normal blood pressure. Am J Hypertens 21:111–116. doi:10.1038/ajh.2007.16

    PubMed  Google Scholar 

  101. Santos RA, Brosnihan KB, Chappell MC, Pesquero J, Chernicky CL, Greene LJ, Ferrario CM (1988) Converting enzyme activity and angiotensin metabolism in the dog brainstem. Hypertension 11:I153–I157

    CAS  PubMed  Google Scholar 

  102. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, Heringer-Walther S, Pinheiro SV, Lopes MT, Bader M, Mendes EP, Lemos VS, Campagnole-Santos MJ, Schultheiss HP, Speth R, Walther T (2003) Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci U S A 100:8258–8263. doi:10.1073/pnas.1432869100

    PubMed Central  CAS  PubMed  Google Scholar 

  103. Scheuer DA, Thrasher TN, Quillen EW Jr, Metzler CH, Ramsay DJ (1987) Atrial natriuretic peptide blocks renin response to renal hypotension. Am J Physiol 252:R423–R427

    CAS  PubMed  Google Scholar 

  104. Schmid J, Oelbe M, Saftig P, Schwake M, Schweda F (2013) Parallel regulation of renin and lysosomal integral membrane protein 2 in renin-producing cells: further evidence for a lysosomal nature of renin secretory vesicles. Pflugers Arch 465:895–905. doi:10.1007/s00424-012-1192-x

    CAS  PubMed  Google Scholar 

  105. Schnermann J, Briggs JP (2013) Tubular control of renin synthesis and secretion. Pflugers Arch 465:39–51. doi:10.1007/s00424-012-1115-x

    PubMed Central  CAS  PubMed  Google Scholar 

  106. Schnermann J, Levine DZ (2003) Paracrine factors in tubuloglomerular feedback: adenosine, ATP, and nitric oxide. Annu Rev Physiol 65:501–529. doi:10.1146/annurev.physiol.65.050102.085738

    CAS  PubMed  Google Scholar 

  107. Schweda F, Kammerl M, Wagner C, Kramer BK, Kurtz A (2004) Upregulation of macula densa cyclooxygenase-2 expression is not dependent on glomerular filtration. Am J Physiol Renal Physiol 287:F95–F101. doi:10.1152/ajprenal.00404.2003

    CAS  PubMed  Google Scholar 

  108. Schweda F, Klar J, Narumiya S, Nusing RM, Kurtz A (2004) Stimulation of renin release by prostaglandin E2 is mediated by EP2 and EP4 receptors in mouse kidneys. Am J Physiol Renal Physiol 287:F427–F433. doi:10.1152/ajprenal.00072.2004

    CAS  PubMed  Google Scholar 

  109. Schweda F, Kurtz A (2011) Regulation of renin release by local and systemic factors. Rev Physiol Biochem Pharmacol 161:1–44

    CAS  PubMed  Google Scholar 

  110. Schweda F, Segerer F, Castrop H, Schnermann J, Kurtz A (2005) Blood pressure-dependent inhibition of Renin secretion requires A1 adenosine receptors. Hypertension 46:780–786. doi:10.1161/01.HYP.0000183963.07801.65

    CAS  PubMed  Google Scholar 

  111. Schweda F, Wagner C, Kramer BK, Schnermann J, Kurtz A (2003) Preserved macula densa-dependent renin secretion in A1 adenosine receptor knockout mice. Am J Physiol Renal Physiol 284:F770–F777. doi:10.1152/ajprenal.00280.2002

    CAS  PubMed  Google Scholar 

  112. Seeliger E, Lohmann K, Nafz B, Persson PB, Reinhardt HW (1999) Pressure-dependent renin release: effects of sodium intake and changes of total body sodium. Am J Physiol 277:R548–R555

    CAS  PubMed  Google Scholar 

  113. Shade RE, Davis JO, Johnson JA, Witty RT (1972) Effects of renal arterial infusion of sodium and potassium on renin secretion in the dog. Circ Res 31:719–727. doi:10.1161/01.RES.31.5.719

    CAS  PubMed  Google Scholar 

  114. Skott O, Briggs JP (1987) Direct demonstration of macula densa-mediated renin secretion. Science 237:1618–1620

    CAS  PubMed  Google Scholar 

  115. Skrabal F, Herholz H, Neumayr M, Hamberger L, Ledochowski M, Sporer H, Hortnagl H, Schwarz S, Schonitzer D (1984) Salt sensitivity in humans is linked to enhanced sympathetic responsiveness and to enhanced proximal tubular reabsorption. Hypertension 6:152–158

    CAS  PubMed  Google Scholar 

  116. Stichtenoth DO, Marhauer V, Tsikas D, Gutzki FM, Frolich JC (2005) Effects of specific COX-2-inhibition on renin release and renal and systemic prostanoid synthesis in healthy volunteers. Kidney Int 68:2197–2207. doi:10.1111/j.1523-1755.2005.00676.x

    CAS  PubMed  Google Scholar 

  117. Tamura N, Ogawa Y, Chusho H, Nakamura K, Nakao K, Suda M, Kasahara M, Hashimoto R, Katsuura G, Mukoyama M, Itoh H, Saito Y, Tanaka I, Otani H, Katsuki M (2000) Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc Natl Acad Sci U S A 97:4239–4244. doi:10.1073/pnas.070371497

    PubMed Central  CAS  PubMed  Google Scholar 

  118. Thurau K, Schnermann J (1965) The sodium concentration in the macula densa cells as a regulating factor for glomerular filtration (micropuncture experiments). Klin Wochenschr 43:410–413

    CAS  PubMed  Google Scholar 

  119. Tkacs NC, Kim M, Denzon M, Hargrave B, Ganong WF (1990) Pharmacological evidence for involvement of the sympathetic nervous system in the increase in renin secretion produced by a low sodium diet in rats. Life Sci 47:2317–2322

    CAS  PubMed  Google Scholar 

  120. Traynor TR, Smart A, Briggs JP, Schnermann J (1999) Inhibition of macula densa-stimulated renin secretion by pharmacological blockade of cyclooxygenase-2. Am J Physiol 277:F706–F710

    CAS  PubMed  Google Scholar 

  121. Vandongen R, Peart WS, Boyd GW (1973) Andrenergic stimulation of renin secretion in the isolated perfused rat kidney. Circ Res 32:290–296

    CAS  PubMed  Google Scholar 

  122. Weihprecht H, Lorenz JN, Schnermann J, Skott O, Briggs JP (1990) Effect of adenosine1-receptor blockade on renin release from rabbit isolated perfused juxtaglomerular apparatus. J Clin Invest 85:1622–1628. doi:10.1172/JCI114613

    PubMed Central  CAS  PubMed  Google Scholar 

  123. Weinberger MH, Miller JZ, Luft FC, Grim CE, Fineberg NS (1986) Definitions and characteristics of sodium sensitivity and blood pressure resistance. Hypertension 8:II127–II134

    CAS  PubMed  Google Scholar 

  124. Wright JW, Harding JW (2013) The brain renin-angiotensin system: a diversity of functions and implications for CNS diseases. Pflugers Arch 465:133–151. doi:10.1007/s00424-012-1102-2

    CAS  PubMed  Google Scholar 

  125. Yang T, Endo Y, Huang YG, Smart A, Briggs JP, Schnermann J (2000) Renin expression in COX-2-knockout mice on normal or low-salt diets. Am J Physiol Renal Physiol 279:F819–F825

    CAS  PubMed  Google Scholar 

  126. Zhang Y, Morgan T (1994) Role of the macula densa in renin synthesis and secretion. Am J Hypertens 7:448–452

    CAS  PubMed  Google Scholar 

  127. Zhang Y, Morgan TO (1994) Sodium depletion, renal denervation, beta adrenergic blockage and renin secretion and synthesis. Blood Press 3:67–71

    CAS  PubMed  Google Scholar 

  128. Zhang Y, Wu J, Wang X, Morgan T (2009) Effects of enalapril and sodium depletion on the renin-angiotensin system in hydronephrotic mice. Can J Physiol Pharmacol 87:515–521. doi:10.1139/y09-037

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The author’s work is financially supported by the German Research Foundation DFG (SFB699, Schw 778/4-1).

Author information

Authors and Affiliations

  1. Institut für Physiologie, Universität Regensburg, 93040, Regensburg, Germany

    Frank Schweda

Authors
  1. Frank Schweda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frank Schweda.

Additional information

This article is published as part of the Special Issue on “SALT!”

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schweda, F. Salt feedback on the renin-angiotensin-aldosterone system. Pflugers Arch - Eur J Physiol 467, 565–576 (2015). https://doi.org/10.1007/s00424-014-1668-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-014-1668-y

Keywords

Search

Navigation