Renal nerve stimulation leads to the activation of the Na+/H+ exchanger isoform 3 via angiotensin II type I receptor

American Journal of Physiology - Renal Physiology

Volumn 308, Issue 8, 2015, Pages 848-856

  Pontes, Roberto B ^a   Crajoinas, Renato O ^b   Nishi, Erika E ^a   Oliveira Sales, Elizabeth B ^a   Girardi, Adriana C ^b   Campos, Ruy R ^a   Bergamaschi, Cássia T ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

ANG II; AT1 receptor and NHE3; Sympathetic nervous system

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; ANGIOTENSINOGEN; CREATININE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN; LOSARTAN; SERINE; SODIUM PROTON EXCHANGE PROTEIN 3; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; SODIUM; SODIUM PROTON EXCHANGE PROTEIN; SODIUM-HYDROGEN EXCHANGER 3;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE CLEARANCE; ELECTROSTIMULATION; KIDNEY NERVE; KIDNEY PROXIMAL TUBULE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR UPREGULATION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SIGNAL TRANSDUCTION; SODIUM ABSORPTION; SODIUM EXCRETION; URINARY EXCRETION; URINE FLOW RATE; URINE PH; WATER ABSORPTION; ANIMAL; DRUG EFFECTS; INNERVATION; KIDNEY TUBULE ABSORPTION; METABOLISM; NATRIURESIS; PH; PHOSPHORYLATION; PHYSIOLOGY; TIME; URODYNAMICS; WISTAR RAT;

ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANGIOTENSINOGEN; ANIMALS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTRIC STIMULATION; HYDROGEN-ION CONCENTRATION; KIDNEY TUBULES, PROXIMAL; MALE; NATRIURESIS; PHOSPHORYLATION; RATS, WISTAR; RECEPTOR, ANGIOTENSIN, TYPE 1; RENAL REABSORPTION; RENIN-ANGIOTENSIN SYSTEM; SIGNAL TRANSDUCTION; SODIUM; SODIUM-HYDROGEN ANTIPORTER; SYMPATHETIC NERVOUS SYSTEM; TIME FACTORS; URODYNAMICS;

EID: 84927729325     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00515.2014     Document Type: Article

References (64)

1. Aronson PS. Energy-dependence of phlorizin binding to isolated renal microvillus membranes. Evidence concerning the mechanism of coupling between the electrochemical Na+ gradient the sugar transport. J Membr Biol 42: 81–98, 1978.
2. Aronson PS. Ion exchangers mediating NaCl transport in the renal proximal tubule. Cell Biochem Biophys 36: 147–153, 2002.
3. Barajas L. Innervation of the renal cortex. Fed Proc 37: 1192–1201, 1978.
4. Baum M, Quigley R, Quan A. Effect of luminal angiotensin II on rabbit proximal convoluted tubule bicarbonate absorption. Am J Physiol Renal Physiol 273: F595–F600, 1997.
5. Bell-Reuss E, Trevino DL, Gottschalk CW. Effect of renal sympathetic nerve stimulation on proximal water and sodium reabsorption. J Clin Invest 57: 1104–1107, 1976.
6. Bello-Reuss E, Colindres RE, Pastoriza-Munoz E, Mueller RA, Gottschalk CW. Effects of acute unilateral renal denervation in the rat. J Clin Invest 56: 208–217, 1975.
7. Bhatt DL, Kandzari DE, O’Neill WW, D’Agostino R, Flack JM, Katzen BT, Leon MB, Liu M, Mauri L, Negoita M, Cohen SA, Oparil S, Rocha-Singh K, Townsend RR, Bakris GL; SYMPLICITY HTN-3 Investigators. A controlled trial of renal denervation for resistant hypertension. N Engl J Med 370: 1393–1401, 2014.
8. Biemesderfer D, DeGray B, Aronson PS. Active (9.6 s) and inactive (21 s) oligomers of NHE3 in microdomains of the renal brush border. J Biol Chem 276: 10161–10167, 2001.
9. Bobulescu IA, Moe OW. Luminal Na+/H+ exchange in the proximal tubule. Pflügers Arch 458: 5–21, 2009.
10. Brasen JC, Burford JL, McDonough AA, Holstein-Rathlou NH, Peti- Peterdi J. Local pH domains regulate NHE3-mediated Na+ reabsorption in the renal proximal tubule. Am J Physiol Renal Physiol 307: F1249–F1262, 2014.
11. Chan YL. Adrenergic control of bicarbonate absorption in the proximal convoluted tubule of the rat kidney. Pflügers Arch 388: 159–164, 1980.
12. Chan YL. The role of norepinephrine in the regulation of fluid absorption in the rat proximal tubule. J Pharmacol Exp Ther 215: 65–70, 1980.
13. Cogan MG. Neurogenic regulation of proximal bicarbonate and chloride reabsorption. Am J Physiol Renal Fluid Electrolyte Physiol 250: F22–F26, 1986.
14. Coote JH, Johns EJ, Macleod VH, Singer B. Effect of renal nerve stimulation, renal blood flow and adrenergic blockade on plasma renin activity in the cat. J Physiol 226: 15–36, 1972.
15. Crajoinas RO, Lessa LM, Carraro-Lacroix LR, Davel AP, Pacheco BP, Rossoni LV, Malnic G, Girardi AC. Posttranslational mechanisms associated with reduced NHE3 activity in adult vs. young prehypertensive SHR. Am J Physiol Renal Physiol 299: F872–F881, 2010.
16. Crajoinas RO, Pessoa TD, Rodrigues MV, Malnic G, Girardi AC. Changes in the activity and expression of protein phosphatase-1 accompany the differential regulation of NHE3 before and after the onset of hypertension in spontaneously hypertensive rats. Acta Physiol (Oxf) 211: 395–408, 2014.
17. de Almeida Chaves Rodrigues AF, de Lima IL, Bergamaschi CT, Campos RR, Hirata AE, Schoorlemmer GH, Gomes GN. Increased renal sympathetic nerve activity leads to hypertension and renal dysfunction in offspring from diabetic mothers. Am J Physiol Renal Physiol 304: F189–F197, 2013.
18. DiBona GF. Sympathetic nervous system and hypertension. Hypertension 61: 556–560, 2013.
19. DiBona GF, Kopp UC. Neural control of renal function. Physiol Rev 77: 75–197, 1997.
20. Ditting T, Hilgers KF, Stetter A, Linz P, Schönweiss C, Veelken R. Renal sympathetic nerves modulate erythropoietin plasma levels after transient hemorrhage in rats. Am J Physiol Renal Physiol 293: F1099–F1106, 2007.
21. Franzellitti S, Fabbri E. Cyclic-AMP mediated regulation of ABCB mRNA expression in mussel haemocytes. PLoS One 8: e61634, 2013.
22. Girardi AC, Di Sole F. Deciphering the mechanisms of the Na+/H+ exchanger-3 regulation in organ dysfunction. Am J Physiol Cell Physiol 302: C1569–C1587, 2012.
23. Hall JE. Control of blood pressure by the renin-angiotensin-aldosterone system. Clin Cardiol 14: IV6–IV21; discussion IV51–IV25, 1991.
24. Healy V, Thompson C, Johns EJ. The adrenergic regulation of proximal tubular Na+/H+ exchanger 3 in the rat. Acta Physiol (Oxf) 210: 678–689, 2014.
25. Huang C, Johns EJ. Role of ANG II in mediating somatosensory-induced renal nerve-dependent antinatriuresis in the rat. Am J Physiol Regul Integr Comp Physiol 275: R194–R202, 1998.
26. Höcherl K, Kammerl M, Kees F, Krämer BK, Grobecker HF, Kurtz A. 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, 2002.
27. Katsurada A, Hagiwara Y, Miyashita K, Satou R, Miyata K, Ohashi N, Navar LG, Kobori H. Novel sandwich ELISA for human angiotensinogen. Am J Physiol Renal Physiol 293: F956–F960, 2007.
28. Kobori H, Alper AB Jr, Shenava R, Katsurada A, Saito T, Ohashi N, Urushihara M, Miyata K, Satou R, Hamm LL, Navar LG. Urinary angiotensinogen as a novel biomarker of the intrarenal renin-angiotensin system status in hypertensive patients. Hypertension 53: 344–350, 2009.
29. Kobori H, Harrison-Bernard LM, Navar LG. Enhancement of angiotensinogen expression in angiotensin II-dependent hypertension. Hypertension 37: 1329–1335, 2001.
30. Kobori H, Harrison-Bernard LM, Navar LG. Expression of angiotensinogen mRNA and protein in angiotensin II-dependent hypertension. J Am Soc Nephrol 12: 431–439, 2001.
31. Kobori H, Katsurada A, Miyata K, Ohashi N, Satou R, Saito T, Hagiwara Y, Miyashita K, Navar LG. Determination of plasma and urinary angiotensinogen levels in rodents by newly developed ELISA. Am J Physiol Renal Physiol 294: F1257–F1263, 2008.
32. Kobori H, Prieto-Carrasquero MC, Ozawa Y, Navar LG. AT1 receptor mediated augmentation of intrarenal angiotensinogen in angiotensin IIdependent hypertension. Hypertension 43: 1126–1132, 2004.
33. Kocinsky HS, Dynia DW, Wang T, Aronson PS. NHE3 phosphorylation at serines 552 and 605 does not directly affect NHE3 activity. Am J Physiol Renal Physiol 293: F212–F218, 2007.
34. Kocinsky HS, Girardi AC, Biemesderfer D, Nguyen T, Mentone S, Orlowski J, Aronson PS. Use of phospho-specific antibodies to determine the phosphorylation of endogenous Na+/H+ exchanger NHE3 at PKA consensus sites. Am J Physiol Renal Physiol 289: F249–F258, 2005.
35. Koepke JP. Renal responses to stressful environmental stimuli. Fed Proc 44: 2823–2827, 1985.
36. Koepke JP, Jones S, DiBona GF. Stress increases renal nerve activity and decreases sodium excretion in Dahl rats. Hypertension 11: 334–338, 1988.
37. Krum H, Schlaich M, Whitbourn R, Sobotka PA, Sadowski J, Bartus K, Kapelak B, Walton A, Sievert H, Thambar S, Abraham WT, Esler M. Catheter-based renal sympathetic denervation for resistant hypertension: a multicentre safety and proof-of-principle cohort study. Lancet 373: 1275–1281, 2009.
38. Le Fevre ME, Guild SJ, Ramchandra R, Barrett CJ, Malpas SC. Role of angiotensin II in the neural control of renal function. Hypertension 41: 583–591, 2003.
39. Leenen FH. Actions of circulating angiotensin II and aldosterone in the brain contributing to hypertension. Am J Hypertens 2014.
40. Leong PK, Yang LE, Landon CS, McDonough AA, Yip KP. Phenol injury-induced hypertension stimulates proximal tubule Na+/H+ exchanger activity. Am J Physiol Renal Physiol 290: F1543–F1550, 2006.
41. Li YW, Guyenet PG. Angiotensin II decreases a resting K+ conductance in rat bulbospinal neurons of the C1 area. Circ Res 78: 274–282, 1996.
42. Liu FY, Cogan MG. Angiotensin II stimulates early proximal bicarbonate absorption in the rat by decreasing cyclic adenosine monophosphate. J Clin Invest 84: 83–91, 1989.
43. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275, 1951.
44. Mamenko M, Zaika O, Ilatovskaya DV, Staruschenko A, Pochynyuk O. Angiotensin II increases activity of the epithelial Na+ channel (ENaC) in distal nephron additively to aldosterone. J Biol Chem 287: 660–671, 2012.
45. McDonough AA. Mechanisms of proximal tubule sodium transport regulation that link extracellular fluid volume and blood pressure. Am J Physiol Regul Integr Comp Physiol 298: R851–R861, 2010.
46. Moe OW. Acute regulation of proximal tubule apical membrane Na/H exchanger NHE-3: role of phosphorylation, protein trafficking, and regulatory factors. J Am Soc Nephrol 10: 2412–2425, 1999.
47. Navar LG, Kobori H, Prieto-Carrasquero M. Intrarenal angiotensin II and hypertension. Curr Hypertens Rep 5: 135–143, 2003.
48. 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 5: 1153–1158, 1994.
49. Nishiyama A, Konishi Y, Ohashi N, Morikawa T, Urushihara M, Maeda I, Hamada M, Kishida M, Hitomi H, Shirahashi N, Kobori H, Imanishi M. Urinary angiotensinogen reflects the activity of intrarenal renin-angiotensin system in patients with IgA nephropathy. Nephrol Dial Transplant 26: 170–177, 2011.
50. Porstmann T, Kiessig ST. Enzyme immunoassay techniques. An overview. J Immunol Methods 150: 5–21, 1992.
51. Quan A, Baum M. Renal nerve stimulation augments effect of intraluminal angiotensin II on proximal tubule transport. Am J Physiol Renal Physiol 282: F1043–F1048, 2002.
52. Quan A, Baum M. The renal nerve is required for regulation of proximal tubule transport by intraluminally produced ANG II. Am J Physiol Renal Physiol 280: F524–F529, 2001.
53. Saccomani G, Mitchell KD, Navar LG. Angiotensin II stimulation of Na+-H+ exchange in proximal tubule cells. Am J Physiol Renal Fluid Electrolyte Physiol 258: F1188–F1195, 1990.
54. Schuster VL, Kokko JP, Jacobson HR. Angiotensin II directly stimulates sodium transport in rabbit proximal convoluted tubules. J Clin Invest 73: 507–515, 1984.
55. Schwark JR, Jansen HW, Lang HJ, Krick W, Burckhardt G, Hropot M. S3226, a novel inhibitor of Na+/H+ exchanger subtype 3 in various cell types. Pflügers Arch 436: 797–800, 1998.
56. Thekkumkara T, Linas SL. Role of internalization in AT1A receptor function in proximal tubule epithelium. Am J Physiol Renal Physiol 282: F623–F629, 2002.
57. Veelken R, Hilgers KF, Porst M, Krause H, Hartner A, Schmieder RE. Effects of sympathetic nerves and angiotensin II on renal sodium and water handling in rats with common bile duct ligature. Am J Physiol Renal Physiol 288: F1267–F1275, 2005.
58. Veelken R, Hilgers KF, Stetter A, Siebert HG, Schmieder RE, Mann JF. Nerve-mediated antidiuresis and antinatriuresis after air-jet stress is modulated by angiotensin II. Hypertension 28: 825–832, 1996.
59. Woodcock EA, Johnston CI. Inhibition of adenylate cyclase by angiotensin II in rat renal cortex. Endocrinology 111: 1687–1691, 1982.
60. Wu XC, Harris PJ, Johns EJ. Nitric oxide and renal nerve-mediated proximal tubular reabsorption in normotensive and hypertensive rats. Am J Physiol Renal Physiol 277: F560–F566, 1999.
61. Xie MH, Liu FY, Wong PC, Timmermans PB, Cogan MG. Proximal nephron and renal effects of DuP 753, a nonpeptide angiotensin II receptor antagonist. Kidney Int 38: 473–479, 1990.
62. Yang LE, Zhong H, Leong PK, Perianayagam A, Campese VM, McDonough AA. Chronic renal injury-induced hypertension alters renal NHE3 distribution and abundance. Am J Physiol Renal Physiol 284: F1056–F1065, 2003.
63. Yang Z, Coote JH. Paraventricular nucleus influence on renal sympathetic activity in vasopressin gene-deleted rats. Exp Physiol 92: 109–117, 2007.
64. Zhao H, Wiederkehr MR, Fan L, Collazo RL, Crowder LA, Moe OW. Acute inhibition of Na/H exchanger NHE-3 by cAMP. Role of protein kinase a and NHE-3 phosphoserines 552 and 605. J Biol Chem 274: 3978–3987, 1999.