Journal of the American Society of Hypertension
Volume 3, Issue 2 , Pages 96-104 , March 2009

Collecting duct renin: a major player in angiotensin II–dependent hypertension

Received 8 October 2008 ,Accepted 19 November 2008.

References 

  1. Chappell MC, Tallant EA, Diz DI, Ferrario CM. The renin-angiotensin system and cardiovascular Homeostasis. In:  Husain A,  Graham RM editor. Drugs, enzymes, and receptors of the renin-angiotensin system. celebrating a century of discovery: Harwood Academic Publishers; 2000;p. 3–22
  2. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, et al. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature. 2002;417:822–828
  3. Ferrario CM. Contribution of Angiotensin-(1-7) to cardiovascular physiology and pathology. Curr Hypertens Rep. 2003;5:129–134
  4. Von Thun AM, Vari RC, El-Dahr SS, Navar LG. Augmentation of intrarenal angiotensin II levels by chronic angiotensin II infusion. Am J Physiol Renal Physiol. 1994;266:F120–F128
  5. Zou LX, Hymel A, Imig JD, Navar LG. Renal accumulation of circulating angiotensin II in angiotensin II-infused rats. Hypertension. 1996;27:658–662
  6. Imig JD, Navar GL, Zou LX, O'Reilly KC, Allen PL, Kaysen JH. Renal endosomes contain angiotensin peptides, converting enzyme, and AT1A receptors. Am J Physiol Renal Physiol. 1999;277:F303–F311
  7. Ingert C, Grima M, Coquard C, Barthelmebs M, Imbs JL. Contribution of angiotensin II internalization to intrarenal angiotensin II levels in rats. Am J Physiol Renal Physiol. 2002;283:F1003–F1010
  8. Navar LG, Harrison-Bernard LM, Wang C-T, Cervenka L, Mitchell KD. Concentrations and actions of intraluminal angiotensin II. J Am Soc Nephrol. 1999;10:S189–S195
  9. Re RN. The intracrine hypothesis and intracellular peptide hormone action. Bioessays. 2003;25:401–409
  10. Van Kats JP, Schalekamp MA, Verdouw PD, Duncker DJ, Danser AH. Intrarenal angiotensin II: interstitial and cellular levels and site of production. Kidney Int. 2001;60:2311–2317
  11. Kobori H, Harrison-Bernard LM, Navar LG. Urinary excretion of angiotensinogen reflects intrarenal angiotensinogen production. Kidney Int. 2002;61:579–585
  12. Kobori H, Nishiyama A, Harrison-Bernard LM, Navar LG. Urinary angiotensinogen as an indicator of intrarenal Angiotensin status in hypertension. Hypertension. 2003;41:42–49
  13. Komlosi P, Fuson AL, Fintha A, Peti-Peterdi J, Rosivall L, Warnock DG, et al. Angiotensin I conversion to angiotensin II stimulates cortical collecting duct sodium transport. Hypertension. 2003;42:195–199
  14. Rosivall L, Navar LG. Effects on renal hemodynamics of intra-arterial infusions of angiotensins I and II. Am J Physiol. 1983;245:F181–F187
  15. Hackenthal E, Paul M, Ganten D, Taugner R. Morphology, physiology, and molecular biology of renin secretion. Physiol Rev. 1990;70:1067–1116
  16. Kobori H, Harrison-Bernard LM, Navar LG. Expression of angiotensinogen mRNA and protein in angiotensin II-dependent hypertension. J Am Soc Nephrol. 2001;12:431–439
  17. Mitchell KD, Jacinto SM, Mullins JJ. Proximal tubular fluid, kidney, and plasma levels of angiotensin II in hypertensive ren-2 transgenic rats. Am J Physiol Renal Physiol. 1997;273:F246–F253
  18. Navar LG, Lewis L, Hymel A, Braam B, Mitchell KD. Tubular fluid concentrations and kidney contents of angiotensins I and II in anesthetized rats. J Am Soc Nephrol. 1994;5:1153–1158
  19. Kang JJ, Toma I, Sipos A, Meer EJ, Vargas SL, Peti-Peterdi J. The collecting duct is the major source of prorenin in diabetes. Hypertension. 2008;51:1597–1604
  20. Prieto-Carrasquero MC, Harrison-Bernard LM, Kobori H, Ozawa Y, Hering-Smith KS, Hamm LL, et al. Enhancement of collecting duct renin in angiotensin II-dependent hypertensive rats. Hypertension. 2004;44:223–229
  21. Rohrwasser A, Morgan T, Dillon HF, Zhao L, Callaway CW, Hillas E, et al. Elements of a paracrine tubular renin-angiotensin system along the entire nephron. Hypertension. 1999;34:1265–1274
  22. Casarini DE, Boim MA, Stella RCR, Krieger-Azzolini MH, Krieger JE, Schor N. Angiotensin I-converting enzyme activity in tubular fluid along the rat nephron. Am J Physiol Renal Physiol. 1997;272:F405–F409
  23. Redublo Quinto BM, Camargo de Andrade MC, Ronchi FA, Santos EL, ves Correa SA, Shimuta SI, et al. Expression of angiotensin I-converting enzymes and bradykinin B2 receptors in mouse inner medullary-collecting duct cells. Int Immunopharmacol. 2008;8:254–260
  24. Barreto-Chaves MLM, Mello-Aires M. Effect of luminal angiotensin II and ANP on early and late cortical distal tubule HCO3- reabsorption. Am J Physiol Renal Physiol. 1996;271:F977–F984
  25. Peti-Peterdi J, Warnock DG, Bell PD. Angiotensin II directly stimulates ENaC activity in the cortical collecting duct via AT(1) receptors. J Am Soc Nephrol. 2002;13:1131–1135
  26. Guan S, Fox J, Mitchell KD, Navar LG. Angiotensin and angiotensin-converting enzyme tissue levels in two-kidney, one-clip hypertensive rats. Hypertension. 1992;20:763–767
  27. Huang W-C, Navar LG. Effects of unclipping and converting enzyme inhibition on bilateral renal function in two-kidney, one-clip Goldblatt hypertensive rats. Kidney Int. 1983;23:816–822
  28. Mitchell KD, Navar LG. Intrarenal actions of angiotensin II in the pathogenesis of experimental hypertension. In:  Laragh JH,  Brenner BM editor. Hypertension: pathophysiology, diagnosis, and management. 2 edn. New York, New York: Raven Press, Ltd; 1995;p. 1437–1450
  29. Zou L, Hymel A, Imig JD, Navar LG. Renal accumulation of circulating angiotensin II in angiotensin II-infused rats. Hypertension. 1996;27:658–662
  30. Zhuo JL, Imig JD, Hammond TG, Orengo S, Benes E, Navar LG. Ang II accumulation in rat renal endosomes during Ang II-induced hypertension: role of AT(1) receptor. Hypertension. 2002;39:116–121
  31. Gonzalez-Villalobos R, Klassen RB, Allen PL, Navar LG, Hammond TG. Megalin binds and internalizes angiotensin II. Am J Physiol Renal Physiol. 2005;288:F420–F427
  32. Gonzalez-Villalobos RA, Seth DM, Satou R, Horton H, Ohashi N, Miyata K, et al. Intrarenal angiotensin II and angiotensinogen augmentation in chronic angiotensin II-infused mice. Am J Physiol Renal Physiol. 2008;295:F772–F779
  33. Ingelfinger JR, Jung F, Diamant D, Haveran L, Lee E, Brem A, et al. Rat proximal tubule cell line transformed with origin-defective SV40 DNA: autocrine ANG II feedback. Am J Physiol Renal Physiol. 1999;276:F218–F227
  34. Schunkert H, Ingelfinger JR, Jacob H, Jackson B, Bouyounes B, Dzau VJ. Reciprocal feedback regulation of kidney angiotensinogen and renin mRNA expressions by angiotensin II. Am J Physiol Endocrinol Metab. 1992;263:E863–E869
  35. Kobori H, Harrison-Bernard LM, Navar LG. Enhancement of angiotensinogen expression in angiotensin II-dependent hypertension. Hypertension. 2001;37:1329–1335
  36. Davisson RL, Ding Y, Stec DE, Catterall JF, Sigmund CD. Novel mechanism of hypertension revealed by cell-specific targeting of human angiotensinogen in transgenic mice. Physiol Genomics. 1999;1:3–9
  37. Ding Y, Davisson RL, Hardy DO, Zhu L-J, Merrill DC, Catterall JF, et al. The kidney androgen-regulated protein promoter confers renal proximal tubule cell-specific and highly androgen-responsive expression on the human angiotensinogen gene in transgenic mice. J Biol Chem. 1997;272:28142–28148
  38. Kobori H, Nishiyama A, Abe Y, Navar LG. Enhancement of intrarenal angiotensinogen in Dahl salt-sensitive rats on high-salt diet. Hypertension. 2003 March;41(3):592–597
  39. Kodama K, Adachi H, Sonoda J. Beneficial effects of long-term enalapril treatment and low-salt intake on survival rate of Dahl salt-sensitive rats with established hypertension. J Pharmacol Exp Ther. 1997;283:625–629
  40. Otsuka F, Yamauchi T, Kataoka H, Mimura Y, Ogura T, Makino H. Effects of chronic inhibition of ACE and AT1 receptors on glomerular injury in Dahl salt-sensitive rats. Am J Physiol Regulatory Integrative Comp Physiol. 1998;274:R1797–R1806
  41. Dzau VJ. Significance of the vascular renin-angiotensin pathway. Hypertension. 1986;8:553–559
  42. Inagami T, Okamura T, Clemens D, Celio MR, Naruse K, Naruse M. Local generation of angiotensin in the kidney and in tissue culture. Clin Exp Hypertens A. 1983;5:1137–1149
  43. Taugner R, Hackenthal E, Inagami T, Nobiling R, Poulsen K. Vascular and tubular renin in the kidneys of mice. Histochemistry. 1982;75:473–484
  44. Henrich WL, McAllister EA, Eskue A, Miller T, Moe OW. Renin regulation in cultured proximal tubular cells. Hypertension. 1996;27:1337–1340
  45. Moe OW, Ujiie K, Star RA, Miller RT, Widell J, Alpern RJ, et al. Renin expression in renal proximal tubule. J Clin Invest. 1993;91:774–779
  46. Prieto-Carrasquero MC, Kobori H, Ozawa Y, Gutierrez A, Seth D, Navar LG. AT1 receptor-mediated enhancement of collecting duct renin in angiotensin II-dependent hypertensive rats. Am J Physiol Renal Physiol. 2005;289:F632–F637
  47. Peti-Peterdi J. Multiphoton imaging of renal tissues in vitro. Am J Physiol Renal Physiol. 2005;288:F1079–F1083
  48. Gallagher PE, Chappell MC, Ferrario CM, Tallant EA. Distinct roles for Ang II and Ang-(1-7) in the regulation of angiotensin-converting enzyme 2 in rat astrocytes. Am J Physiol Cell Physiol. 2006;290:C420–C426
  49. Rohrwasser A, Ishigami T, Gociman B, Lantelme P, Morgan T, Cheng T, et al. Renin and kallikrein in connecting tubule of mouse. Kidney Int. 2003;64:2155–2162
  50. Leyssac PP. Micropuncture study of renin release at the single nephron level. Evidence for some release directly into the circulating blood. Renal Physiol. 1978;1:61–73
  51. Lumbers ER, Skinner SL. The occurrence and assay of renin in human urine. Aust J Exp Biol Med Sci. 1969;47:251–262
  52. Lantelme P, Rohrwasser A, Gociman B, Hillas E, Cheng T, Petty G, et al. Effects of dietary sodium and genetic background on angiotensinogen and renin in mouse. Hypertension. 2002;39:1007–1014
  53. Prieto-Carrasquero MC, Botros FT, Pagan J, Kobori H, Seth DM, Casarini DE, et al. Collecting duct renin is upregulated in both kidneys of two-kidney, one-clip Goldblatt hypertensive rats. Hypertension. 2008;51:1590–1596
  54. Catanzaro DF. Physiological relevenace of renin/prorenin binding and uptake. Hypertens Res. 2005;28:97–105
  55. Danser AHJ, van Kats JP, Admiraal PJJ, Derkx FHM, Lamers JMJ, Verdouw PD, et al. Cardiac renin and angiotensins. Uptake from plasma versus in situ synthesis. Hypertension. 1994;24:37–48
  56. Nguyen G, Delarue F, Burckle C, Bouzhir L, Giller T, Sraer JD. Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J Clin Invest. 2002;109:1417–1427
  57. Muller DN, Klanke B, Feldt S, Cordasic N, Hartner A, Schmieder RE, et al. (Pro)renin receptor peptide inhibitor “handle-region” peptide does not affect hypertensive nephrosclerosis in Goldblatt rats. Hypertension. 2008;51:676–681
  58. Krebs C, Hamming I, Sadaghiani S, Steinmetz OM, Meyer-Schwesinger C, Fehr S, et al. Antihypertensive therapy upregulates renin and (pro)renin receptor in the clipped kidney of Goldblatt hypertensive rats. Kidney Int. 2007;72:725–730
  59. Prieto-Carrasquero MC, Botros FT, Martin VL, Gonzalez-Villalobos RA, Sato R, Kobori R, et al. Prorenin Receptor in distal nephron segments of 2K1C Goldblatt hypertensive rats. Hypertension. 2008;52:e34–e131
  60. Campbell DJ. Critical review of prorenin and (pro)renin receptor research. Hypertension. 2008;51:1259–1264
  61. Nguyen G. Increased cyclooxygenase-2, hyperfiltration, glomerulosclerosis, and diabetic nephropathy: put the blame on the (pro)renin receptor?. Kidney Int. 2006;70:618–620
  62. Siragy HM, Carey RM. Protective role of the angiotensin AT2 receptor in a renal wrap hypertension model. Hypertension. 1999;33:1237–1242
  63. Nishiyama A, Seth DM, Navar LG. Renal interstitial fluid angiotensin I and angiotensin II concentrations during local angiotensin-converting enzyme inhibition. J Am Soc Nephrol. 2002;13:2207–2212
  64. Nishiyama A, Seth DM, Navar LG. Renal interstitial fluid concentrations of angiotensins I and II in anesthetized rats. Hypertension. 2002;39:129–134
  65. Mendelsohn FAO. Failure of suppression of intrarenal angiotensin II in the contralateral kidney of two-kidney one-clip, hypertensive rats. Clin Exp Pharmacol Physiol. 1980;7:219–223
  66. Morishita R, Higaki J, Okunishi H, Tanaka T, Ishii K, Nagano M, et al. Changes in gene expression of the renin-angiotensin system in two-kidney, one-clip hypertensive rats. J Hypertens. 1991;9:187–192
  67. Zou LX, Imig JD, von Thun AM, Hymel A, Ono H, Navar LG. Receptor-mediated intrarenal angiotensin II augmentation in angiotensin II-infused rats. Hypertension. 1996;28:669–677
  68. Cervenka L, Wang C-T, Mitchell KD, Navar LG. Proximal tubular angiotensin II levels and renal functional responses to AT1 receptor blockade in non-clipped kidneys of Goldblatt hypertensive rats. Hypertension. 1999;33:102–107
  69. Navar LG, Harrison-Bernard LM, Imig JD. Compartmentalization of intrarenal angiotensin II. In:  Ulfendahl HR,  Aurell M editor. Renin-angiotensin. London, England: Portland Press; 1998;p. 193–208
  70. Braam B, Mitchell KD, Fox J, Navar LG. Proximal tubular secretion of angiotensin II in rats. Am J Physiol Renal Physiol. 1993;264:F891–F898
  71. Navar LG, Imig JD, Zou L, Wang C-T. Intrarenal production of angiotensin II. Sem Nephrol. 1997;17:412–422
  72. Harrison-Bernard LM, Zhuo J, Kobori H, Ohishi M, Navar LG. Intrarenal AT1 receptor and ACE binding in angiotensin II-induced hypertensive rats. Am J Physiol Renal Physiol. 2001;281:F19–F25
  73. Pendergrass KD, Averill DB, Ferrario CM, Diz DI, Chappell MC. Differential expression of nuclear AT1 receptors and angiotensin II within the kidney of the male congenic mRen2. Lewis rat. Am J Physiol Renal Physiol. 2006;290:F1497–F1506
  74. Brosnihan KB, Neves LA, Joyner J, Averill DB, Chappell MC, Sarao R, et al. Enhanced renal immunocytochemical expression of ang-(1-7) and ACE2 during pregnancy. Hypertension. 2003;42:749–753
  75. Lely AT, Hamming I, van Goor H, Navis GJ. Renal ACE2 expression in human kidney disease. J Pathol. 2004;204:587–593
  76. Ferrario CM. Angiotension-(1-7) and antihypertensive mechanisms. J Nephrol. 1998;11:278–283
  77. Ishiyama Y, Gallagher PE, Averill DB, Tallant EA, Brosnihan KB, Ferrario CM. Upregulation of angiotensin-converting enzyme 2 after myocardial infarction by blockade of angiotensin II receptors. Hypertension. 2004;43:970–976
  78. Koka V, Huang XR, Chung ACK, Wang W, Truong LD, Lan HY. Angiotensin II up-regulates angiotensin I-converting enzyme (ACE), but down-regulates ACE2 via the AT1-ERK/p38 MAP kinase pathway. Am J Pathol. 2008;172:1174–1183

 This study was supported by the National Institute of Health through the National, Lung, and Blood Institute (HL-26371), the Eunice Kennedy Shriver National Institute of Child Health & Human Development (K12HD043451), the Institutional Developmental Award Program of the National Center for Research Resources (P20RR-017659), and the American Heart Association (0325269B).

 Conflict of interest: none.

PII: S1933-1711(08)00217-9

doi: 10.1016/j.jash.2008.11.003

Journal of the American Society of Hypertension
Volume 3, Issue 2 , Pages 96-104 , March 2009