Fructose acutely stimulates NHE3 activity in kidney proximal tubule

Kidney and Blood Pressure Research

Volumn 36, Issue 1, 2012, Pages 320-334

  Queiroz Leite, Gabriella D ^a   Crajoinas, Renato O ^a   Neri, Elida A ^a   Bezerra, Camila N A ^a   Girardi, Adriana C C ^a   Rebouças, Nancy Amaral ^a   Malnic, Gerhard ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

CAMP; Fructose; In situ microperfusion; LLC PK1 cells; Sodium hydrogen exchangers

Indexed keywords

BICARBONATE; CYCLIC AMP DEPENDENT PROTEIN KINASE; FRUCTOSE; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; SODIUM PROTON EXCHANGE PROTEIN 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PH; CONTROLLED STUDY; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE ABSORPTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; CELL LINE; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FRUCTOKINASES; FRUCTOSE; GLUCOSE TRANSPORTER TYPE 2; GLUCOSE TRANSPORTER TYPE 5; KIDNEY TUBULES, PROXIMAL; LLC-PK1 CELLS; MALE; MODELS, ANIMAL; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SODIUM-HYDROGEN ANTIPORTER; SWINE;

EID: 84870727540     PISSN: 14204096     EISSN: 14230143     Source Type: Journal    
DOI: 10.1159/000343390     Document Type: Article

References (52)

1. Johnson RJ, Sanchez-Lozada LG, Nakagawa T: The effect of fructose on renal biology and disease. J Am Soc Nephrol 2010;21:2036-2039.
2. Elliott SS, Keim NL, Stern JS, Teff K, Havel PJ: Fructose, weight gain, and the insulin resistance syndrome. Am J Clin Nutr 2002;76:911-922.
3. Mayes PA: Intermediary metabolism of fructose. Am J Clin Nutr 1993;58:754S-765S.
4. Diggle CP, Shires M, Leitch D, Brooke D, Carr IM, Markham AF, Hayward BE, Asipu A, Bonthron DT: Ketohexokinase: Expression and localization of the principal fructose-metabolizing enzyme. J Histochem Cytochem 2009;57:763-774.
5. Douard V, Ferraris RP: Regulation of the fructose transporter glut5 in health and disease. Am J Physiol Endocrinol Metab 2008;295:E227-E237.
6. Manolescu AR, Witkowska K, Kinnaird A, Cessford T, Cheeseman C: Facilitated hexose transporters: New perspectives on form and function. Physiology (Bethesda) 2007;22:234-240.
7. Johnson RJ, Segal MS, Sautin Y, Nakagawa T, Feig DI, Kang DH, Gersch MS, Benner S, Sanchez-Lozada LG: Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am J Clin Nutr 2007;86:899-906.
8. Ferder L, Ferder MD, Inserra F: The role of high-fructose corn syrup in metabolic syndrome and hypertension. Curr Hypertens Rep 2010;12:105-112.
9. Tappy L, Le KA: Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 2010;90:23-46.
10. Tran LT, Yuen VG, McNeill JH: The fructose-fed rat: A review on the mechanisms of fructose-induced insulin resistance and hypertension. Mol Cell Biochem 2009;332:145-159.
11. Basciano H, Federico L, Adeli K: Fructose, insulin resistance, and metabolic dyslipidemia. Nutr Metab (Lond) 2005;2:5.
12. Chen J, Muntner P, Hamm LL, Jones DW, Batuman V, Fonseca V, Whelton PK, He J: The metabolic syndrome and chronic kidney disease in u.S. Adults. Ann Intern Med 2004;140:167-174.
13. Shoham DA, Durazo-Arvizu R, Kramer H, Luke A, Vupputuri S, Kshirsagar A, Cooper RS: Sugary soda consumption and albuminuria: Results from the national health and nutrition examination survey, 1999-2004. PLoSOne 2008;3:e3431.
14. Gersch MS, Mu W, Cirillo P, Reungjui S, Zhang L, Roncal C, Sautin YY, Johnson RJ, Nakagawa T: Fructose, but not dextrose, accelerates the progression of chronic kidney disease. Am J Physiol Renal Physiol 2007;293:F1256-F1261.
15. Sanchez-Lozada LG, Tapia E, Jimenez A, Bautista P, Cristobal M, Nepomuceno T, Soto V, Avila-Casado C, Nakagawa T, Johnson RJ, Herrera-Acosta J, Franco M: Fructose-induced metabolic syndrome is associated with glomerular hypertension and renal microvascular damage in rats. Am J Physiol Renal Physiol 2007;292:F423-F429.
16. Cirillo P, Gersch MS, Mu W, Scherer PM, Kim KM, Gesualdo L, Henderson GN, Johnson RJ, Sautin YY: Ketohexokinase-dependent metabolism of fructose induces proinflammatory mediators in proximal tubular cells. J Am Soc Nephrol 2009;20:545-553.
17. Nakayama T, Kosugi T, Gersch M, Connor T, Sanchez-Lozada LG, Lanaspa MA, Roncal C, Perez-Pozo SE, Johnson RJ, Nakagawa T: Dietary fructose causes tubulointerstitial injury in the normal rat kidney. Am J Physiol Renal Physiol 2010;298:F712-F720.
18. Meneton P, Jeunemaitre X, de Wardener HE, MacGregor GA: Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiol Rev 2005;85:679-715.
19. Soleimani M: Dietary fructose, salt absorption and hypertension in metabolic syndrome: Toward a new paradigm. Acta Physiol (Oxf) 2011;201:55-62.
20. Singh AK, Amlal H, Haas PJ, Dringenberg U, Fussell S, Barone SL, Engelhardt R, Zuo J, Seidler U, Soleimani M: Fructose-induced hypertension: Essential role of chloride and fructose absorbing transporters pat1 and glut5. Kidney Int 2008;74:438-447.
21. Soleimani M, Alborzi P: The role of salt in the pathogenesis of fructose-induced hypertension. Int J Nephrol 2011;2011:392708.
22. Catena C, Cavarape A, Novello M, Giacchetti G, Sechi LA: Insulin receptors and renal sodium handling in hypertensive fructose-fed rats. Kidney Int 2003;64:2163-2171.
23. Lessa LM, Amorim JB, Fonteles MC, Malnic G: Effect of renoguanylin on hydrogen/bicarbonate ion transport in rat renal tubules. Regul Pept 2009;157:37-43.
24. De Mello AM, Lopes MJ, Malnic G: Pco2 in renal cortex. Am J Physiol 1990;259:F357-F365.
25. Carraro-Lacroix LR, Ramirez MA, Zorn TM, Reboucas NA, Malnic G: Increased nhe1 expression is associated with serum deprivation-induced differentiation in immortalized rat proximal tubule cells. Am J Physiol Renal Physiol 2006;291:F129-F139.
26. Boyarsky G, Ganz MB, Sterzel RB, Boron WF: Ph regulation in single glomerular mesangial cells. I. Acid extrusion in absence and presence of hco3. Am J Physiol 1988;255:C844-C856.
27. Weintraub WH, Machen TE: Ph regulation in hepatoma cells: Roles for na-h exchange, cl-hco3 exchange, and na-hco3 cotransport. Am J Physiol 1989;257:G317-G327.
28. Girardi AC, Knauf F, Demuth HU, Aronson PS: Role of dipeptidyl peptidase iv in regulating activity of na+/h+ exchanger isoform nhe3 in proximal tubule cells. Am J Physiol Cell Physiol 2004;287:C1238-C1245.
29. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol reagent. J Biol Chem 1951;193:265-275.
30. 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 2005;289:F249-F258.
31. Biemesderfer D, Rutherford PA, Nagy T, Pizzonia JH, Abu-Alfa AK, Aronson PS: Monoclonal antibodies for high-resolution localization of nhe3 in adult and neonatal rat kidney. Am J Physiol 1997;273:F289-F299.
32. 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. Pflugers Arch 1998;436:797-800.
33. Wang T, Hropot M, Aronson PS, Giebisch G: Role of nhe isoforms in mediating bicarbonate reabsorption along the nephron. Am J Physiol Renal Physiol 2001;281:F1117-F1122.
34. Reilly RF, Hildebrandt F, Biemesderfer D, Sardet C, Pouyssegur J, Aronson PS, Slayman CW, Igarashi P: Cdna cloning and immunolocalization of a na(+)-h+ exchanger in llc-pk1 renal epithelial cells. Am J Physiol 1991;261:F1088-F1094.
35. Shugrue CA, Obermuller N, Bachmann S, Slayman CW, Reilly RF: Molecular cloning of nhe3 from llc-pk1 cells and localization in pig kidney. J Am Soc Nephrol 1999;10:1649-1657.
36. Carraro-Lacroix LR, Malnic G, Girardi AC: Regulation of na+/h+ exchanger nhe3 by glucagon-like peptide 1 receptor agonist exendin-4 in renal proximal tubule cells. Am J Physiol Renal Physiol 2009;297:F1647-1655.
37. Di SF, Girardi AC: Uncovering the pathway of sepsis-induced renal tubular dysfunction. Focus on "basolateral lps inhibits nhe3 and hcoformula absorption through tlr4/myd88-dependent erk activation in medullary thick ascending limb". Am J Physiol Cell Physiol 2011;301:C1290-C1292.
38. Davies SP, Reddy H, Caivano M, Cohen P: Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000;351:95-105.
39. Ulate G, Fernandez R, Malnic G: Effect of bafilomycin on proximal bicarbonate absorption in the rat. Braz J Med Biol Res 1993;26:773-777.
40. Wakabayashi S, Shigekawa M, Pouyssegur J: Molecular physiology of vertebrate na+/h+ exchangers. Physiol Rev 1997;77:51-74.
41. Kurashima K, Yu FH, Cabado AG, Szabo EZ, Grinstein S, Orlowski J: Identification of sites required for down-regulation of na+/h+ exchanger nhe3 activity by camp-dependent protein kinase. Phosphorylation-dependent and -independent mechanisms. J Biol Chem 1997;272:28672-28679.
42. Moe OW, Amemiya M, Yamaji Y: Activation of protein kinase a acutely inhibits and phosphorylates na/h exchanger nhe-3. J Clin Invest 1995;96:2187-2194.
43. 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 1999;274:3978-3987.
44. 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 2010;299:F872-F881.
45. 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 2007;293:F212-F218.
46. Le KA, Ith M, Kreis R, Faeh D, Bortolotti M, Tran C, Boesch C, Tappy L: Fructose overconsumption causes dyslipidemia and ectopic lipid deposition in healthy subjects with and without a family history of type 2 diabetes. Am J Clin Nutr 2009;89:1760-1765.
47. Stanhope KL, Schwarz JM, Keim NL, Griffen SC, Bremer AA, Graham JL, Hatcher B, Cox CL, Dyachenko A, Zhang W, McGahan JP, Seibert A, Krauss RM, Chiu S, Schaefer EJ, Ai M, Otokozawa S, Nakajima K, Nakano T, Beysen C, Hellerstein MK, Berglund L, Havel PJ: Consuming fructose-sweetened, not glucose-sweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J Clin Invest 2009;119:1322-1334.
48. Brown CM, Dulloo AG, Yepuri G, Montani JP: Fructose ingestion acutely elevates blood pressure in healthy young humans. Am J Physiol Regul Integr Comp Physiol 2008;294:R730-R737.
49. Hwang IS, Ho H, Hoffman BB, Reaven GM: Fructose-induced insulin resistance and hypertension in rats. Hypertension 1987;10:512-516.
50. Horita S, Seki G, Yamada H, Suzuki M, Koike K, Fujita T: Insulin resistance, obesity, hypertension, and renal sodium transport. Int J Hypertens 2011;2011:391762.
51. Girardi AC, Di Sole F: Deciphering the mechanisms of the na+/h+ exchanger-3 regulation in organ dysfunction. Am J Physiol Cell Physiol 2012;302:C1569-1587.
52. Gurley SB, Riquier-Brison AD, Schnermann J, Sparks MA, Allen AM, Haase VH, Snouwaert JN, Le TH, McDonough AA, Koller BH, Coffman TM: At1a angiotensin receptors in the renal proximal tubule regulate blood pressure. Cell Metab 2011;13:469-475.