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Vol. 273, Issue 4, 2035-2043, January 23, 1998

The Epithelial Sodium-Hydrogen Antiporter Na+/H+ Exchanger 3 Accumulates and Is Functional in Recycling Endosomes

Sudhir D'SouzaDagger , Ana Garcia-CabadoDagger , Frank Yu, Ken Teterpar , Gergely Lukacs**, Karl SkoreckiDagger Dagger , Hsiao-Ping Moorepar , John Orlowski, and Sergio GrinsteinDagger ¶¶

From the Divisions of Dagger  Cell Biology and ** Respiratory Research, Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada, the ¶¶ Department of Biochemistry, University of Toronto, Ontario M5S 1X8, Canada, the  Department of Physiology, McGill University, Montreal, Quebec H36 1Y6, Canada, the par  Department of Cell Biology, University of California, Berkeley, California 94720, and Dagger Dagger  Bruce Rappaport Medical School, Technion, Israel Institute of Technology, Haifa 31096, Israel

Na+/H+ exchangers (NHEs) mediate electroneutral exchange of Na+ for H+ and thereby play a central role in pH regulation and Na+ homeostasis. NHE3, the predominant epithelial isoform, is found in apical membranes of renal and intestinal epithelial cells, where it contributes to NaCl (re)absorption. NHE activity has been detected in endomembrane vesicles of epithelial cells, but the precise compartment involved and its functional role have not been defined. Many aspects of the targeting machinery that defines the compartmentation and polarity of epithelia are also functional in nonepithelial cells. We therefore compared the targeting of NHE1, the basolateral isoform, with that of NHE3 in Chinese hamster ovary cells. To circumvent the confounding effects of endogenous exchangers, epitope-tagged constructs of NHE1 and NHE3 were stably expressed in antiport-deficient (AP-1) cells. While NHE1 was found almost exclusively in the surface membrane, NHE3 was also found intracellularly, accumulating in a juxtanuclear compartment. Confocal microscopy showed this compartment to be distinct from the Golgi, trans-Golgi network, and lysosomes. Instead, NHE3 colocalized with transferrin receptors and with cellubrevin, markers of recycling endosomes. The activity of NHE3 in endomembranes was assessed by targeting pH-sensitive probes to the recycling endosomes using a chimeric cellubrevin construct with an accessible extracellular epitope. Fluorescence ratio imaging indicated that cellubrevin resides intracellularly in an acidic compartment. In AP-1 cells, endosomal acidification was unaffected by omission of Na+ but was dissipated entirely by concanamycin, a blocker of H+-ATPases. In contrast, the cellubrevin compartment was more acidic in NHE3 transfectants, and the acidification was only partially reduced by concanamycin. Moreover, removal of extracellular Na+ resulted in a significant alkalization of the endocytic compartment. These results indicate that NHE3 is present and active in recycling endosomes. By recruiting NHE3 to the plasma membrane, modulation of vesicular traffic could contribute to the regulation of Na+ reabsorption across epithelia.

Copyright © 1998 by The American Society for Biochemistry and Molecular Biology, Inc.
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Acute Regulation of Na+/H+ Exchanger NHE3 by Parathyroid Hormone via NHE3 Phosphorylation and Dynamin-dependent Endocytosis
J. Biol. Chem., October 6, 2000; 275(41): 31601 - 31608.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Pol, A. Lu, M. Pons, S. Peiro, and C. Enrich
Epidermal Growth Factor-mediated Caveolin Recruitment to Early Endosomes and MAPK Activation. ROLE OF CHOLESTEROL AND ACTIN CYTOSKELETON
J. Biol. Chem., September 22, 2000; 275(39): 30566 - 30572.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Szaszi, K. Kurashima, A. Kapus, A. Paulsen, K. Kaibuchi, S. Grinstein, and J. Orlowski
RhoA and Rho Kinase Regulate the Epithelial Na+/H+ Exchanger NHE3. ROLE OF MYOSIN LIGHT CHAIN PHOSPHORYLATION
J. Biol. Chem., September 8, 2000; 275(37): 28599 - 28606.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. C. Hu, L. Fan, L. A. Crowder, Z. Karim-Jimenez, H. Murer, and O. W. Moe
Dopamine Acutely Stimulates Na+/H+ Exchanger (NHE3) Endocytosis via Clathrin-coated Vesicles. DEPENDENCE ON PROTEIN KINASE A-MEDIATED NHE3 PHOSPHORYLATION
J. Biol. Chem., July 13, 2001; 276(29): 26906 - 26915.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Numata and J. Orlowski
Molecular Cloning and Characterization of a Novel (Na+,K+)/H+ Exchanger Localized to the trans-Golgi Network
J. Biol. Chem., May 11, 2001; 276(20): 17387 - 17394.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Szaszi, K. Kurashima, K. Kaibuchi, S. Grinstein, and J. Orlowski
Role of the Cytoskeleton in Mediating cAMP-dependent Protein Kinase Inhibition of the Epithelial Na+/H+ Exchanger NHE3
J. Biol. Chem., October 26, 2001; 276(44): 40761 - 40768.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
C. L. Brett, Y. Wei, M. Donowitz, and R. Rao
Human Na+/H+ exchanger isoform 6 is found in recycling endosomes of cells, not in mitochondria
Am J Physiol Cell Physiol, May 1, 2002; 282(5): C1031 - C1041.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
L. Yang, P. K. K. Leong, J. O. Chen, N. Patel, S. F. Hamm-Alvarez, and A. A. McDonough
Acute hypertension provokes internalization of proximal tubule NHE3 without inhibition of transport activity
Am J Physiol Renal Physiol, April 1, 2002; 282(4): F730 - F740.
[Abstract] [Full Text] [PDF]


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