Developmental changes in proximal tubule NaCl transport
- 150 Downloads
- 17 Citations
Abstract
The proximal tubule reabsorbs two thirds of the filtered NaCl in an isoosmotic fashion. In the adult proximal tubule, active NaCl transport is mediated by the parallel operation of Na+/H+ and Cl−/base exchangers, and a substantive amount of chloride transport occurs passively across the paracellular pathway. Studies in the neonatal proximal tubule have resulted in unexpected results. The isoform of the Na+/H+ exchanger mediating proximal tubule sodium absorption, NHE3, is virtually absent in the neonatal rat kidney. NHE8, an isoform of the Na+/H+ exchange, in low abundance on the apical membrane of the adult proximal tubule, is present in high abundance in the neonatal segment. Whereas chloride permeability is high in the adult, favoring passive paracellular chloride flux, the neonatal proximal tubule is virtually impermeable to chloride ions. This is again due to a developmental change in isoforms of proteins forming the tight junction. The permeability properties of epithelia are due to a family of tight junction proteins called claudins. Claudins 6 and 9 are expressed in the neonatal proximal tubule at a time when chloride permeability is low, but these claudin isoforms are virtually absent in the adult segment. The causes for these postnatal changes in proximal tubular transport and developmental isoform changes are also discussed in this review.
Keywords
NHE3 NHE8 Permeability AcidificationNotes
Acknowledgments
This work was supported by the National Institute of Diabetes and Digestive and Kidney Disease Grants DK-41612. I thank Dr. Raymond Quigley for critiquing this manuscript.
References
- 1.Liu FY, Cogan MG (1984) Axial heterogeneity in the rat proximal convoluted tubule. I. Bicarbonate, chloride, and water transport. Am J Physiol 247:F816–F821PubMedGoogle Scholar
- 2.Rector FC Jr (1983) Sodium, bicarbonate, and chloride absorption by the proximal tubule. Am J Physiol 244:F461–F471PubMedGoogle Scholar
- 3.Preisig PA, Rector FC Jr (1988) Role of Na+-H+ antiport in rat proximal tubule NaCl absorption. Am J Physiol 255:F461–F465PubMedGoogle Scholar
- 4.Alpern RJ, Howlin KJ, Preisig PA (1985) Active and passive components of chloride transport in the rat proximal convoluted tubule. J Clin Invest 76:1360–1366PubMedGoogle Scholar
- 5.Baum M, Berry CA (1984) Evidence for neutral transcellular NaCl transport and neutral basolateral chloride exit in the rabbit convoluted tubule. J Clin Invest 74:205–211PubMedGoogle Scholar
- 6.Sheu JN, Quigley R, Baum M (1995) Heterogeneity of chloride/base exchange in rabbit superficial and juxtamedullary proximal convoluted tubules. Am J Physiol 268:F847–F853PubMedGoogle Scholar
- 7.Aronson PS, Giebisch G (1997) Mechanisms of chloride transport in the proximal tubule. Am J Physiol 273:F179–F192PubMedGoogle Scholar
- 8.Shah M, Quigley R, Baum M (2000) Maturation of proximal straight tubule NaCl transport: role of thyroid hormone. Am J Physiol Renal Physiol 278:F596–F602PubMedGoogle Scholar
- 9.Shah M, Quigley R, Baum M (1999) Neonatal rabbit proximal tubule basolateral membrane Na+/H+ antiporter and Cl-/base exchange. Am J Physiol 276:R1792–R1797PubMedGoogle Scholar
- 10.Moe OW, Baum M, Berry CA, Rector FC (2004) Renal transport of glucose, amino acids, sodium, chloride and water. In: Brenner BM (ed) The Kidney, 7th edn. Saunders, Philadelphia pp 413–452Google Scholar
- 11.Horster M (1982) Expression of ontogeny in individual nephron segments. Kidney Int 22:550–559PubMedCrossRefGoogle Scholar
- 12.Schmidt U, Horster M (1977) Na-K-activated ATPase: activity maturation in rabbit nephron segments dissected in vitro. Am J Physiol 233:F55–F60PubMedGoogle Scholar
- 13.Schwartz GH, Evan AP (1984) Development of solute transport in rabbit proximal tubule. III. Na-K-ATPase activity. Am J Physiol 246:F845–F852PubMedGoogle Scholar
- 14.Fukuda Y, Aperia A (1988) Differentiation of Na+-K+ pump in rat proximal tubule is modulated by Na+-H+ exchanger 7. Am J Physiol 255:F552–F557PubMedGoogle Scholar
- 15.Larsson SH, Rane S, Fukuda Y, Aperia A, Lechene C (1990) Changes in Na influx precede post-natal increase in Na, K-ATPase activity in rat renal proximal tubular cells. Acta Physiol Scand 138:99–100PubMedCrossRefGoogle Scholar
- 16.Schwartz GH, Evan AP (1983) Development of solute transport in rabbit proximal tubule. I. HCO3 and glucose absorption. Am J Physiol 245:F382–F390PubMedGoogle Scholar
- 17.Baum M, Quigley R (1993) Maturation of proximal tubular acidification. Pediatr Nephrol 7:785–791PubMedCrossRefGoogle Scholar
- 18.Baum M (1992) Developmental changes in rabbit juxtamedullary proximal convoluted tubule acidification. Pediatr Res 31:411–414PubMedCrossRefGoogle Scholar
- 19.Shah M, Gupta N, Dwarakanath V, Moe OW, Baum M (2000) Ontogeny of Na+/H+ antiporter activity in rat proximal convoluted tubules. Pediatr Res 48:206–210PubMedCrossRefGoogle Scholar
- 20.Wu MS, Biemesderfer D, Giebisch G, Aronson PS (1996) Role of NHE3 in mediating renal brush border Na+-H+ exchange. Adaptation to metabolic acidosis. J Biol Chem 271:32749–32752PubMedCrossRefGoogle Scholar
- 21.Baum M, Biemesderfer D, Gentry D, Aronson PS (1995) Ontogeny of rabbit renal cortical NHE3 and NHE1: effect of glucocorticoids. Am J Physiol 268:F815–F820PubMedGoogle Scholar
- 22.Choi JY, Shah M, Lee MG, Schultheis PJ, Shull GE, Muallem S, Baum M (2000) Novel amiloride-sensitive sodium-dependent proton secretion in the mouse proximal convoluted tubule. J Clin Invest 105:1141–1146PubMedGoogle Scholar
- 23.Goyal S, Vanden Heuvel G, Aronson PS (2003) Renal expression of novel Na+/H+ exchanger isoform NHE8. Am J Physiol Renal Physiol 284:F467–F473PubMedGoogle Scholar
- 24.Goyal S, Mentone S, Aronson PS (2005) Immunolocalization of NHE8 in rat kidney. Am J Physiol Renal Physiol 288:F530–F538PubMedCrossRefGoogle Scholar
- 25.Becker AM, Zhang J, Goyal S, Dwarakanath V, Aronson PS, Moe OW, Baum M (2007) Ontogeny of NHE8 in the rat proximal tubule. Am J Physiol Renal Physiol 293:F255–261Google Scholar
- 26.Nehrke K, Melvin JE (2002) The NHX family of Na+-H+ exchangers in Caenorhabditis elegans. J Biol Chem 277:29036–29044PubMedCrossRefGoogle Scholar
- 27.Orlowski J, Grinstein S (2004) Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch 447:549–565PubMedCrossRefGoogle Scholar
- 28.Zhang J, Bobulescu IA, Goyal S, Aronson PS, Baum MG, Moe OW (2007) Characterization of Na/H Exchanger-8 (NHE8) in cultured renal epithelial cells. Am J Physiol Renal Physiol DOI 10.1152/ajprenal.00117.2007
- 29.Aronson PS (1996) Role of ion exchangers in mediating NaCl transport in the proximal tubule. Kidney Int 49:1665–1670PubMedCrossRefGoogle Scholar
- 30.Aronson PS (1995) 1994 Homer W. Smith Award. From flies to physiology-accidental findings along the trail of renal NaCl transport. J Am Soc Nephrol 5:2001–2013PubMedGoogle Scholar
- 31.Aronson PS, Kuo SM (1989) Heterogeneity of anion exchangers mediating chloride transport in the proximal tubule. Ann N Y Acad Sci 574:96–101PubMedCrossRefGoogle Scholar
- 32.Aronson PS (2002) Ion exchangers mediating NaCl transport in the renal proximal tubule. Cell Biochem Biophys 36:147–153PubMedCrossRefGoogle Scholar
- 33.Kurtz I, Nagami G, Yanagawa N, Li L, Emmons C, Lee I (1994) Mechanism of apical and basolateral Na(+)-independent Cl-/base exchange in the rabbit superficial proximal straight tubule. J Clin Invest 94:173–183PubMedGoogle Scholar
- 34.Guillery EN, Huss DJ (1995) Developmental regulation of chloride/formate exchange in guinea pig proximal tubules. Am J Physiol 269:F686–F695PubMedGoogle Scholar
- 35.Baum M, Dwarakanath V, Alpern RJ, Moe OW (1998) Effects of thyroid hormone on the neonatal renal cortical Na+/H+ antiporter. Kidney Int 53:1254–1258PubMedCrossRefGoogle Scholar
- 36.Walker P, Dubois JD, Dussault JH (1980) Free thyroid hormone concentrations during postnatal development in the rat. Pediatr Res 14:247–249PubMedGoogle Scholar
- 37.Henning SJ (1978) Plasma concentrations of total and free corticosterone during development in the rat. Am J Physiol 235:E451–E456PubMedGoogle Scholar
- 38.Henning SJ, Leeper LL, Dieu DN (1986) Circulating corticosterone in the infant rat: the mechanism of age and thyroxine effects. Pediatr Res 20:87–92PubMedCrossRefGoogle Scholar
- 39.Baum M, Quigley R (1991) Prenatal glucocorticoids stimulate neonatal juxtamedullary proximal convoluted tubule acidification. Am J Physiol 261:F746–F752PubMedGoogle Scholar
- 40.Meserve LA, Juarez de Ku LM (1993) Effect of thiouracil-induced hypothyroidism on time course of adrenal response in 15 day old rats. Growth Dev Aging 57:25–30PubMedGoogle Scholar
- 41.D’Agostino J, Henning SJ (1982) Role of thyroxine in coordinate control of corticosterone and CBG in postnatal development. Am J Physiol 242:E33–E39PubMedGoogle Scholar
- 42.Mitsuma T, Nogimori T (1982) Effects of adrenalectomy on the hypothalamic-pituitary-thyroid axis in rats. Horm Metab Res 14:317–319PubMedGoogle Scholar
- 43.Gupta N, Dwarakanath V, Baum M (2004) Maturation of the Na/H antiporter (NHE3) in the proximal tubule of the hypothroid adrenalectomized rat. Am J Physiol Renal Physiol 287:F521–F527PubMedCrossRefGoogle Scholar
- 44.Gupta N, Tarif SR, Seikaly M, Baum M (2001) Role of glucocorticoids in the maturation of the rat renal Na+/H+ antiporter (NHE3). Kidney Int 60:173–181PubMedCrossRefGoogle Scholar
- 45.Baum M, Cano A, Alpern RJ (1993) Glucocorticoids stimulate Na+/H+ antiporter in OKP cells. Am J Physiol 264:F1027–F1031PubMedGoogle Scholar
- 46.Cano A, Baum M, Moe OW (1999) Thyroid hormone stimulates the renal Na/H exchanger NHE3 by transcriptional activation. Am J Physiol 276:C102–C108PubMedGoogle Scholar
- 47.Baum M, Amemiya M, Dwarakanath V, Alpern RJ, Moe OW (1996) Glucocorticoids regulate NHE-3 transcription in OKP cells. Am J Physiol 270:F164–F169PubMedGoogle Scholar
- 48.Bobulescu IA, Dwarakanath V, Zou L, Zhang J, Baum M, Moe OW (2005) Glucocorticoids acutely increase cell surface Na+/H+ exchanger-3 (NHE3) by activation of NHE3 exocytosis. Am J Physiol Renal Physiol 289:F685–F691PubMedCrossRefGoogle Scholar
- 49.Yun CC, Chen Y, Lang F (2002) Glucocorticoid activation of Na(+)/H(+) exchanger isoform 3 revisited. The roles of SGK1 and NHERF2. J Biol Chem 277:7676–7683PubMedCrossRefGoogle Scholar
- 50.Baum M, Moe OW, Gentry DL, Alpern RJ (1994) Effect of glucocorticoids on renal cortical NHE-3 and NHE-1 mRNA. Am J Physiol 267:F437–F442PubMedGoogle Scholar
- 51.Biemesderfer D, Rutherford PA, Nagy T, Pizzonia JH, Abu-Alfa AK, Aronson PS (1997) Monoclonal antibodies for high-resolution localization of NHE3 in adult and neonatal rat kidney. Am J Physiol 273:F289–F299PubMedGoogle Scholar
- 52.Chow CW, Khurana S, Woodside M, Grinstein S, Orlowski J (1999) The epithelial Na(+)/H(+) exchanger, NHE3, is internalized through a clathrin-mediated pathway. J Biol Chem 274:37551–37558PubMedCrossRefGoogle Scholar
- 53.Kurashima K, Szabo EZ, Lukacs G, Orlowski J, Grinstein S (1998) Endosomal recycling of the Na+/H+ exchanger NHE3 isoform is regulated by the phosphatidylinositol 3-kinase pathway. J Biol Chem 273:20828–20836PubMedCrossRefGoogle Scholar
- 54.Kaskel FJ, Kumar AM, Lockhart EA, Evan A, Spitzer A (1987) Factors affecting proximal tubular reabsorption during development. Am J Physiol 252:F188–F197PubMedGoogle Scholar
- 55.Quigley R, Baum M (2002) Developmental changes in rabbit proximal straight tubule paracellular permeability. Am J Physiol Renal Physiol 283:F525–F531PubMedGoogle Scholar
- 56.Baum M, Quigley R (2005) Maturation of rat proximal tubule chloride permeability. Am J Physiol Regul Integr Comp Physiol 289:R1659–R1664PubMedGoogle Scholar
- 57.Mitic LL, Van Itallie CM, Anderson JM (2000) Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins. Am J Physiol Gastrointest Liver Physiol 279:G250–G254PubMedGoogle Scholar
- 58.Mitic LL, Anderson JM (1998) Molecular architecture of tight junctions. Annu Rev Physiol 60:121–142PubMedCrossRefGoogle Scholar
- 59.Anderson JM, Van Itallie CM (1995) Tight junctions and the molecular basis for regulation of paracellular permeability. Am J Physiol 269:G467–G475PubMedGoogle Scholar
- 60.Colegio OR, Itallie CV, Rahner C, Anderson JM (2003) Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am J Physiol Cell Physiol 284:C1346–C1354PubMedGoogle Scholar
- 61.Colegio OR, Van Itallie CM, McCrea HJ, Rahner C, Anderson JM (2002) Claudins create charge-selective channels in the paracellular pathway between epithelial cells. Am J Physiol Cell Physiol 283:C142–C147PubMedGoogle Scholar
- 62.Simon DB, Lu Y, Choate KA, Velazquez H, Al Sabban E, Praga M, Casari G, Bettinelli A, Colussi G, Rodriguez-Soriano J, McCredie D, Milford D, Sanjad S, Lifton RP (1999) Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption. Science 285:103–106PubMedCrossRefGoogle Scholar
- 63.Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S (2002) Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875–886PubMedGoogle Scholar
- 64.Abuazza G, Becker A, Williams SS, Chakravarty S, Truong HT, Lin F, Baum M (2006) Claudins 6, 9, and 13 are developmentally expressed renal tight junction proteins. Am J Physiol Renal Physiol 291:F1132–F1141PubMedCrossRefGoogle Scholar
- 65.Baum M, Quigley R (2004) Thyroid hormone modulates rabbit proximal straight tubule paracellular permeability. Am J Physiol-Renal Physiol 286:F477–F482PubMedCrossRefGoogle Scholar
- 66.Arant BS Jr (1978) Developmental patterns of renal functional maturation compared in the human neonate. J Pediatr 92:705–712PubMedCrossRefGoogle Scholar
- 67.Beck JC, Lipkowitz MS, Abramson RG (1988) Characterization of the fetal glucose transporter in rabbit kidney: comparison with the adult brush border electrogenic Na+-glucose symporter. J Clin Invest 82:379–387PubMedCrossRefGoogle Scholar
- 68.Merlet-Benichou C, Pegorier M, Muffat-Joly M, Augeron C (1981) Functional and morphologic patterns of renal maturation in the developing guinea pig. Am J Physiol 241:F618–F624PubMedGoogle Scholar
- 69.Hohenauer L, Rosenberg TF, Oh W (1970) Calcium and phosphorus homeostasis on the first day of life. Biol Neonate 15:49–56PubMedCrossRefGoogle Scholar
- 70.Connelly JP, Crawford JD, Watson J (1962) Studies of neonatal hyperphosphatemia. Pediatrics 30:425–432PubMedGoogle Scholar
- 71.Dean RFA, McCance RA (1948) Phosphate clearance in infants and adults. J Physiol (London) 107:182–186Google Scholar
- 72.Richmond JB, Kravitz H, Segar W, Waisman HA (1951) Renal clearance of endogenous phosphate in infants and children. Proc Soc Exp Biol Med 77:83–87PubMedGoogle Scholar
- 73.Neiberger RE, Barac-Nieto M, Spitzer A (1989) Renal reabsorption of phosphate during development: transport kinetics in BBMV. Am J Physiol 257:F268–F274PubMedGoogle Scholar
- 74.Kaskel FJ, Kumar AM, Feld LG, Spitzer A (1988) Renal reabsorption of phosphate during development: tubular events. Pediatr Nephrol 2:129–134PubMedCrossRefGoogle Scholar
- 75.Johnson V, Spitzer A (1986) Renal reabsorption of phosphate during development: whole-kidney events. Am J Physiol 251:F251–F256PubMedGoogle Scholar
- 76.Segawa H, Kaneko I, Takahashi A, Kuwahata M, Ito M, Ohkido I, Tatsumi S, Miyamoto K (2002) Growth-related renal type II Na/Pi cotransporter. J Biol Chem 277:19665–19672PubMedCrossRefGoogle Scholar
- 77.Murer H, Hernando N, Forster I, Biber J (2003) Regulation of Na/Pi Transporter in the proximal tubule. Annu Rev Physiol 65:531–542PubMedCrossRefGoogle Scholar
- 78.Forster IC, Hernando N, Biber J, Murer H (2006) Proximal tubular handling of phosphate: A molecular perspective. Kidney Int 70:1548–1559PubMedCrossRefGoogle Scholar