Tethering, recycling and activation of the epithelial sodium-proton exchanger, NHE3

Journal of Experimental Biology

Volumn 212, Issue 11, 2009, Pages 1630-1637

  Alexander, R Todd ^a   Grinstein, Sergio ^b,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 3; SODIUM-HYDROGEN EXCHANGER 3;

ANIMAL; CELL MEMBRANE; CHEMISTRY; EPITHELIUM; METABOLISM; PROTEIN CONFORMATION; REVIEW;

ANIMALS; CELL MEMBRANE; EPITHELIUM; PROTEIN CONFORMATION; SODIUM-HYDROGEN ANTIPORTER;

EID: 66449108563     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.027375     Document Type: Review

References (119)

1. + exchangers and the regulation of volume. Acta Physiol. (Oxf.) 187, 159-167.
2. Alexander, R. T., Furuya, W., Szaszi, K., Orlowski, J. and Grinstein, S. (2005). Rho GTPases dictate the mobility of the Na/H exchanger NHE3 in epithelia: role in apical retention and targeting. Proc. Natl. Acad. Sci. USA 102, 12253-12258.
3. + exchanger, NHE3. J. Biol. Chem. 282, 7376-7384.
4. + exchanger 3 (NHE3). J. Clin. Invest. 103, 429-435.
5. + exchanger NHE-3 isoform in renal cells (OK) via a dual signaling cascade involving protein kinase A and C. J. Biol. Chem. 270, 20004-20010.
6. + exchanger NHE3 isoform by binding to the PTH/PTHRP receptor type I and activating distinct signaling pathways. J. Biol. Chem. 271, 14931-14936.
7. Bacic, D., Kaissling, B., McLeroy, P., Zou, L., Baum, M. and Moe, O. W. (2003). Dopamine acutely decreases apical membrane Na/H exchanger NHE3 protein in mouse renal proximal tubule. Kidney Int. 64, 2133-2141.
8. Biemesderfer, D., Rutherford, P. A., Nagy, T., Pizzonia, J. H., Abu-Alfa, A. K. and Aronson, P. S. (1997). Monoclonal antibodies for high-resolution localization of NHE3 in adult and neonatal rat kidney. Am. J. Physiol. 273, F289-F299.
9. Biemesderfer, D., DeGray, B. and Aronson, P. S. (1998). Membrane topology of NHE3. Epitopes within the carboxyl-terminal hydrophilic domain are exoplasmic. J. Biol. Chem. 273, 12391-12396.
10. + exchanger isoform NHE3 in the proximal tubule. J. Biol. Chem. 274, 17518-17524.
11. Biemesderfer, D., DeGray, B. and Aronson, P. S. (2001). Active (9.6 s) and inactive (21 s) oligomers of NHE3 in microdomains of the renal brush border. J. Biol. Chem. 276, 10161-10167.
12. + exchanger isoform NHE-3 is species specific. J. Lab. Clin. Med. 128, 304-312.
13. + exchangers in renal regulation of acid-base balance. Semin. Nephrol. 26, 334-344.
14. Bobulescu, I. A. and Moe, O. W. (2008). Luminal Na(+)/H (+) exchange in the proximal tubule. Pflugers Arch. 458, 5-21.
15. + exchangers: physiology and link to hypertension and organ ischemia. Curr. Opin. Nephrol. Hypertens. 14, 485-494.
16. + exchanger-3 (NHE3) by activation of NHE3 exocytosis. Am. J. Physiol. Renal. Physiol. 289, F685-F691.
17. + exchanger isoform, NHE3. Am. J. Physiol. 269, C198-C206.
18. Brennan, S., Hering-Smith, K. and Hamm, L. L. (1988). Effect of pH on citrate reabsorption in the proximal convoluted tubule. Am. J. Physiol. 255, F301-F306.
19. Brett, C. L., Donowitz, M. and Rao, R. (2005). Evolutionary origins of eukaryotic sodium/proton exchangers. Am. J. Physiol. Cell Physiol. 288, C223-C239.
20. Broere, N., Chen, M., Cinar, A., Singh, A. K., Hillesheim, J., Riederer, B., Lunnemann, M., Rottinghaus, I., Krabbenhoft, A., Engelhardt, R. et al. (2008). Defective jejunal and colonic salt absorption and altered Na(+)/H (+) exchanger 3 (NHE3) activity in NHE regulatory factor 1 (NHERF1) adaptor protein-deficient mice. Pflugers Arch. 457, 1079-1091.
21. + exchanger NHE3 isoform. J. Biol. Chem. 271, 3590-3599.
22. + exchanger regulatory factor (NHERF) proteins. Clin. Exp. Pharmacol. Physiol. 35, 863-871.
23. + exchanger isoform 3 (NHE3) determine the set point. J. Membr. Biol. 191, 49-58.
24. Cha, B., Kenworthy, A., Murtazina, R. and Donowitz, M. (2004). The lateral mobility of NHE3 on the apical membrane of renal epithelial OK cells is limited by the PDZ domain proteins NHERF1/2, but is dependent on an intact actin cytoskeleton as determined by FRAP. J. Cell Sci. 117, 3353-3365.
25. Cha, B., Tse, M., Yun, C., Kovbasnjuk, O., Mohan, S., Hubbard, A., Arpin, M. and Donowitz, M. (2006). The NHE3 juxtamembrane cytoplasmic domain directly binds ezrin: dual role in NHE3 trafficking and mobility in the brush border. Mol. Biol. Cell 17, 2661-2673.
26. Choi, J. W., Lee-Kwon, W., Jeon, E. S., Kang, Y. J., Kawano, K., Kim, H. S., Suh, P. G., Donowitz, M. and Kim, J. H. (2004). Lysophosphatidic acid induces exocytic trafficking of Na(+)/H(+) exchanger 3 by E3KARP-dependent activation of phospholipase C. Biochim. Biophys. Acta 1683, 59-68.
27. 2+ is abolished in PDZ-domain protein PDZK1-deficient murine enterocytes. J. Physiol. 581, 1235- 1246.
28. Clayburgh, D. R., Musch, M. W., Leitges, M., Fu, Y. X. and Turner, J. R. (2006). Coordinated epithelial NHE3 inhibition and barrier dysfunction are required for TNF- mediated diarrhea in vivo. J. Clin. Invest. 116, 2682-2694.
29. + exchanger NHE3 by parathyroid hormone via NHE3 phosphorylation and dynamin-dependent endocytosis. J. Biol. Chem. 275, 31601- 31608.
30. + exchanger NHE-1 possesses N- and O-linked glycosylation restricted to the first N-terminal extracellular domain. Biochemistry 33, 10463-10469.
31. -/- renal proximal tubule cells. J. Biol. Chem. 279, 37815-37821.
32. + exchanger-NHE3 and NHE2. Biochim Biophys Acta. 1664, 38-44.
33. Donowitz, M. and Li, X. (2007). Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87, 825-872.
34. Donowitz, M., Cha, B., Zachos, N. C., Brett, C. L., Sharma, A., Tse, C. M. and Li, X. (2005). NHERF family and NHE3 regulation. J. Physiol. 567, 3-11.
35. Dransfield, D. T., Bradford, A. J., Smith, J., Martin, M., Roy, C., Mangeat, P. H. and Goldenring, J. R. (1997). Ezrin is a cyclic AMP-dependent protein kinase anchoring protein. EMBO J. 16, 35-43.
36. + exchanger 3 accumulates and is functional in recycling endosomes. J. Biol. Chem. 273, 2035-2043.
37. du Cheyron, D., Chalumeau, C., Defontaine, N., Klein, C., Kellermann, O., Paillard, M. and Poggioli, J. (2003). Angiotensin II stimulates NHE3 activity by exocytic insertion of the transporter: role of PI 3-kinase. Kidney Int. 64, 939-949.
38. Durkan, A. M., Alexander, R. T., Liu, G. Y., Rui, M., Femia, G. and Robinson, L. A. (2007). Expression and targeting of CX3CL1 (Fractalkine) in renal tubular epithelial cells. J. Am. Soc. Nephrol. 18, 74-83.
39. + exchanger isoforms NHE1 and NHE3 exist as stable dimers in membranes with a high degree of specificity for homodimers. J. Biol. Chem. 269, 2589-2596.
40. + exchanger. J. Mol. Cell Cardiol. 44, 228-237.
41. Fuster, D., Moe, O. W. and Hilgemann, D. W. (2004). Lipid- and mechanosensitivities of sodium/hydrogen exchangers analyzed by electrical methods. Proc. Natl. Acad. Sci. USA 101, 10482-10487.
42. + Exchanger NHE3 by Insulin. Am. J. Physiol. Renal Physiol. 292, F577-F585.
43. Fuster, D., Moe, O. W. and Hilgemann, D. W. (2008). Steady-state function of the ubiquitous mammalian Na/H exchanger (NHE1) in relation to dimer coupling models with 2Na/2H stoichiometry. J. Gen. Physiol. 132, 465-480.
44. + exchanger supports proximal tubular protein reabsorption in vivo. Am. J. Physiol. Renal Physiol. 287, F469-F473.
45. Girardi, A. C., Degray, B. C., Nagy, T., Biemesderfer, D. and Aronson, P. S. (2001). Association of Na(+)-H(+) exchanger isoform NHE3 and dipeptidyl peptidase IV in the renal proximal tubule. J. Biol. Chem. 276, 46671-46677.
46. + exchanger isoform NHE3 in proximal tubule cells. Am. J. Physiol. Cell Physiol. 287, C1238-C1245.
47. Gomes, P. and Soares-da-Silva, P. (2004). Dopamine acutely decreases type 3 Na(+)/H(+) exchanger activity in renal OK cells through the activation of protein kinases A and C signalling cascades. Eur. J. Pharmacol. 488, 51-59.
48. + exchange. Nature 392, 626-630.
49. + exchanger 3. J. Biol. Chem. 281, 1461-1469.
50. + exchanger, by Clostridium difficile toxin B. J. Gen. Physiol. 123, 491-504.
51. + exchanger NHE1 revealed by symmetrical intermolecular cross-linking and selective co- immunoprecipitation. Biochemistry 43, 11135-11143.
52. + exchanger NHE1. Biochemistry 45, 13346-13355.
53. Hryciw, D. H., Lee, E. M., Pollock, C. A. and Poronnik, P. (2004). Molecular changes in proximal tubule function in diabetes mellitus. Clin. Exp. Pharmacol. Physiol. 31, 372-379.
54. + exchanger (NHE3) endocytosis via clathrin-coated vesicles: dependence on protein kinase A-mediated NHE3 phosphorylation. J. Biol. Chem. 276, 26906-26915.
55. + exchanger Nhe3 gene. J. Biol. Chem. 271, 10551-10559.
56. Karim, Z., Gerard, B., Bakouh, N., Alili, R., Leroy, C., Beck, L., Silve, C., Planelles, G., Urena-Torres, P., Grandchamp, B. et al. (2008). NHERF1 mutations and responsiveness of renal parathyroid hormone. N. Engl. J. Med. 359, 1128-1135.
57. + exchanger isoform NHE3 in the rat efferent ducts. J. Androl. 23, 237-241.
58. + exchanger 3 (NHE3) requires an NHE3-E3KARP-alpha-actinin-4 complex for oligomerization and endocytosis. J. Biol. Chem. 277, 23714-23724.
59. + exchanger 3 in OKP cells. J. Am. Soc. Nephrol. 14, 3008-3016.
60. + exchanger NHE3 activity by cAMP-dependent protein kinase. phosphorylation-dependent and - independent mechanisms. J. Biol. Chem. 272, 28672-28679.
61. + exchanger NHE3 isoform is regulated by the phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 273, 20828-20836.
62. Kurashima, K., D'Souza, S., Szaszi, K., Ramjeesingh, R., Orlowski, J. and Grinstein, S. (1999). The apical Na(+)/H(+) exchanger isoform NHE3 is regulated by the actin cytoskeleton. J. Biol. Chem. 274, 29843-29849.
63. Lamprecht, G., Weinman, E. J. and Yun, C. H. (1998). The role of NHERF and E3KARP in the cAMP-mediated inhibition of NHE3. J. Biol. Chem. 273, 29972- 29978.
64. 2+-dependent inhibition of NHE3 requires PKC alpha which binds to E3KARP to decrease surface NHE3 containing plasma membrane complexes. Am. J. Physiol. Cell Physiol. 285, C1527-C1536.
65. + exchangers stably expressed in a fibroblast cell line. J. Biol. Chem. 268, 25527-25535.
66. + exchanger isoform NHE3 are involved in stimulation and inhibition by protein kinases/growth factors. J. Biol. Chem. 270, 13716-13725.
67. + exchanger 3 (NHE3) is present in lipid rafts in the rabbit ileal brush border: a role for rafts in trafficking and rapid stimulation of NHE3. J. Physiol. 537, 537-552.
68. + exchanger 3 (NHE3) occurs through changes in NHE3 trafficking and complex formation and is Src dependent. J. Physiol. 556, 791-804.
69. Lorenz, J. N., Schultheis, P. J., Traynor, T., Shull, G. E. and Schnermann, J. (1999). Micropuncture analysis of single-nephron function in NHE3-deficient mice. Am. J. Physiol. 277, F447-F453.
70. + exchanger. Can. J. Physiol. Pharmacol. 84, 1081-1095.
71. Minkoff, C., Shenolikar, S. and Weinman, E. J. (1999). Assembly of signaling complexes by the sodium-hydrogen exchanger regulatory factor family of PDZ- containing proteins. Curr. Opin. Nephrol. Hypertens. 8, 603-608.
72. + exchanger NHE3 activity and trafficking are lipid Raft-dependent. J. Biol. Chem. 281, 17845- 17855.
73. Murtazina, R., Kovbasnjuk, O., Zachos, N. C., Li, X., Chen, Y., Hubbard, A., Hogema, B. M., Steplock, D., Seidler, U., Hoque, K. M. et al. (2007). Tissue- specific regulation of sodium/proton exchanger isoform 3 activity in Na(+)/H(+) exchanger regulatory factor 1 (NHERF1) null mice. cAMP inhibition is differentially dependent on NHERF1 and exchange protein directly activated by cAMP in ileum versus proximal tubule. J. Biol. Chem. 282, 25141-25151.
74. Nagami, G. T. (1988). Luminal secretion of ammonia in the mouse proximal tubule perfused in vitro. J. Clin. Invest. 81, 159-164.
75. Niggli, V. and Rossy, J. (2008). Ezrin/radixin/moesin: versatile controllers of signaling molecules and of the cortical cytoskeleton. Int. J. Biochem. Cell Biol. 40, 344-349.
76. + exchanger isoforms (NHE1 and NHE3) in polarized epithelial cell lines. J. Cell Sci. 109, 929-939.
77. Orlowski, J. and Grinstein, S. (2004). Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch. 447, 549-565.
78. Orlowski, J. and Grinstein, S. (2007). Emerging roles of alkali cation/proton exchangers in organellar homeostasis. Curr. Opin. Cell Biol. 19, 483-492.
79. + exchanger that confer sensitivity to pharmacological antagonists. J. Biol. Chem. 271, 19922-19927.
80. Orlowski, J., Kandasamy, R. A. and Shull, G. E. (1992). Molecular cloning of putative members of the Na/H exchanger gene family. cDNA cloning, deduced amino acid sequence, and mRNA tissue expression of the rat Na/H exchanger NHE- 1 and two structurally related proteins. J. Biol. Chem. 267, 9331-9339.
81. Pedrosa, R., Gomes, P., Hopfer, U., Jose, P. A. and Soares-da-Silva, P. (2004). Gialpha3 protein-coupled dopamine D3 receptor-mediated inhibition of renal NHE3 activity in SHR proximal tubular cells is a PLC-PKC-mediated event. Am. J. Physiol. Renal Physiol. 287, F1059-F1066.
82. Pushkin, A., Clark, I., Kwon, T. H., Nielsen, S. and Kurtz, I. (2000). Immunolocalization of NBC3 and NHE3 in the rat epididymis: colocalization of NBC3 and the vacuolar H+-ATPase. J. Androl. 21, 708-720.
83. Reczek, D., Berryman, M. and Bretscher, A. (1997). Identification of EBP50: A PDZ- containing phosphoprotein that associates with members of the ezrin-radixin-moesin family. J. Cell Biol. 139, 169-179.
84. Saotome, I., Curto, M. and McClatchey, A. I. (2004). Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 6, 855- 864.
85. Schnermann, J. (1999). Micropuncture analysis of tubuloglomerular feedback regulation in transgenic mice. J. Am. Soc. Nephrol. 10, 2614-2619.
86. + exchanger. Nat. Genet. 19, 282-285.
87. Shenolikar, S., Voltz, J. W., Minkoff, C. M., Wade, J. B. and Weinman, E. J. (2002). Targeted disruption of the mouse NHERF-1 gene promotes internalization of proximal tubule sodium-phosphate cotransporter type IIa and renal phosphate wasting. Proc. Natl. Acad. Sci. USA 99, 11470-11475.
88. + exchanger. J. Biol. Chem. 280, 17863-17872.
89. + exchanger. Biochem. J. 401, 623-633.
90. + exchange activity, blocks NHE-3 transport to the membrane, and increases NHE-3 mRNA expression in LLC- PK1 cells. J. Lab. Clin. Med. 127, 565-573.
91. Sullivan, S., Alex, P., Dassopoulos, T., Zachos, N. C., Iacobuzio-Donahue, C., Donowitz, M., Brant, S. R., Cuffari, C., Harris, M. L., Datta, L. W. et al. (2009). Downregulation of sodium transporters and NHERF proteins in IBD patients and mouse colitis models: potential contributors to IBD-associated diarrhea. Inflamm Bowel Dis. 15, 261-274.
92. + exchanger NHE3. Role of myosin light chain phosphorylation. J. Biol. Chem. 275, 28599-28606.
93. Tamura, A., Kikuchi, S., Hata, M., Katsuno, T., Matsui, T., Hayashi, H., Suzuki, Y., Noda, T., Tsukita, S. and Tsukita, S. (2005). Achlorhydria by ezrin knockdown: defects in the formation/expansion of apical canaliculi in gastric parietal cells. J. Cell Biol. 169, 21-28.
94. Thomson, R. B., Wang, T., Thomson, B. R., Tarrats, L., Girardi, A., Mentone, S., Soleimani, M., Kocher, O. and Aronson, P. S. (2005). Role of PDZK1 in membrane expression of renal brush border ion exchangers. Proc. Natl. Acad. Sci. USA 102, 13331-13336.
95. + exchanger isoform (NHE-3). J. Biol. Chem. 267, 9340-9346.
96. Tsuganezawa, H., Preisig, P. A. and Alpern, R. J. (1998). Dominant negative c-Src inhibits angiotensin II induced activation of NHE3 in OKP cells. Kidney Int. 54, 394- 398.
97. 2+ responsiveness to the apical isoform NHE3. J. Biol. Chem. 270, 26460-26465.
98. + exchangers by measurement of reverse mode reaction. J. Biol. Chem. 278, 43580-43585.
99. Wang, D., Sun, H., Lang, F. and Yun, C. C. (2005). Activation of NHE3 by dexamethasone requires phosphorylation of NHE3 at Ser663 by SGK1. Am. J. Physiol. Cell Physiol. 289, C802-C810.
100. Wang, T., Yang, C. L., Abbiati, T., Schultheis, P. J., Shull, G. E., Giebisch, G. and Aronson, P. S. (1999). Mechanism of proximal tubule bicarbonate absorption in NHE3 null mice. Am. J. Physiol. 277, F298-F302.
101. + exchanger requires a dissociable phosphoprotein cofactor. J. Clin. Invest. 92, 1781-1786.
102. Weinman, E. J., Minkoff, C. and Shenolikar, S. (2000a). Signal complex regulation of renal transport proteins: NHERF and regulation of NHE3 by PKA. Am. J. Physiol. Renal Physiol. 279, F393-F399.
103. Weinman, E. J., Steplock, D., Donowitz, M. and Shenolikar, S. (2000b). NHERF associations with sodium-hydrogen exchanger isoform 3 (NHE3) and ezrin are essential for cAMP-mediated phosphorylation and inhibition of NHE3. Biochemistry 39, 6123-6129.
104. Weinman, E. J., Steplock, D. and Shenolikar, S. (2001). Acute regulation of NHE3 by protein kinase A requires a multiprotein signal complex. Kidney Int. 60, 450- 454.
105. Weinman, E. J., Steplock, D. and Shenolikar, S. (2003a). NHERF-1 uniquely transduces the cAMP signals that inhibit sodium-hydrogen exchange in mouse renal apical membranes. FEBS Lett. 536, 141-144.
106. Weinman, E. J., Wang, Y., Wang, F., Greer, C., Steplock, D. and Shenolikar, S. (2003b). A C-terminal PDZ motif in NHE3 binds NHERF-1 and enhances cAMP inhibition of sodium-hydrogen exchange. Biochemistry 42, 12662-12668.
107. Weinman, E. J., Cunningham, R. and Shenolikar, S. (2005). NHERF and regulation of the renal sodium-hydrogen exchanger NHE3. Pflugers Arch. 450, 137-144.
108. Wiederkehr, M. R., Di Sole, F., Collazo, R., Quinones, H., Fan, L., Murer, H., Helmle-Kolb, C. and Moe, O. W. (2001). Characterization of acute inhibition of Na/H exchanger NHE-3 by dopamine in opossum kidney cells. Kidney Int. 59, 197- 209.
109. + antiporter sharing evolutionary origins with bacterial NhaA may be a candidate gene for essential hypertension. Proc. Natl. Acad. Sci. USA 104, 18677-18681.
110. + exchanger-NHE3 by angiotensin-II in OKP cells. Biochim Biophys Acta. 1758, 519-526.
111. + transporter subcellular distribution, abundance, and phosphorylation status. Am. J. Physiol. Renal Physiol. 295, F1003-F1016.
112. + exchanger regulatory factor 2 (NHERF2) in regulation of NHE3. Cell Physiol. Biochem. 13, 29-40.
113. Yun, C. C., Chen, Y. and Lang, F. (2002). Glucocorticoid activation of Na(+)/H(+) exchanger isoform 3 revisited. The roles of SGK1 and NHERF2. J. Biol. Chem. 277, 7676-7683.
114. + exchanger NHE3 and the cytoskeletal protein ezrin. J. Biol. Chem. 273, 25856-25863.
115. + exchange. Annu. Rev. Physiol. 67, 411-443.
116. Zhang, Y., Norian, J. M., Magyar, C. E., Holstein-Rathlou, N. H., Mircheff, A. K. and McDonough, A. A. (1999). In vivo PTH provokes apical NHE3 and NaPi2 redistribution and Na-K-ATPase inhibition. Am. J. Physiol. 276, F711-F719.
117. Zhao, H., Wiederkehr, M. R., Fan, L., Collazo, R. L., Crowder, L. A. and Moe, O. W. (1999). 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.
118. +-glucose cotransport. Proc. Natl. Acad. Sci. USA 101, 9485-9490.
119. Zizak, M., Cavet, M. E., Bayle, D., Tse, C. M., Hallen, S., Sachs, G. and Donowitz, M. (2000). Na(+)/H(+) exchanger NHE3 has 11 membrane spanning domains and a cleaved signal peptide: topology analysis using in vitro transcription/translation. Biochemistry 39, 8102-8112.