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J Biol Chem, Vol. 273, Issue 15, 8790-8798, April 10, 1998
,
From the Departments of Medicine and Physiology, Division of
Gastroenterology, The Johns Hopkins University School of Medicine,
Baltimore, Maryland 21205, the Na+/H+ exchanger isoform
3 (NHE3), an epithelial brush border isoform of the
Na+/H+ exchanger gene family, plays an
important role in reabsorption of Na+ in the small
intestine, the colon, and the kidney. In several cell types, phorbol
12-myristate 13-acetate (PMA) acutely inhibits NHE3 activity by changes
in Vmax, but the mechanism of this inhibition is unknown. We investigated the role of subcellular redistribution of
NHE3 in the PMA-induced inhibition of endogenous brush border NHE3 in a
model human colon adenocarcinoma cell line, Caco-2. Subcellular
localization of NHE3 was examined by confocal morphometric analysis
complemented with cell surface biotinylation and compared with NHE3
activity evaluated by fluorometric measurement of intracellular pH. PMA
inhibited NHE3 activity by 28% (p < 0.01), which was
associated with a decrease of the ratio of the brush border/subapical
cytoplasmic compartment of NHE3 from ~4.3 to ~2.4. This
translocation resulted in 10-15% of the total cell NHE3 being shifted
from the brush border pool to the cytoplasmic pool. These effects were
mediated by protein kinase C, since they were blocked by the protein
kinase C inhibitor H7. We conclude that inhibition of NHE3 by protein kinase C in Caco-2 cells involves redistribution of the exchanger from
brush border into a subapical cytoplasmic compartment, and that this
mechanism contributes ~50% to the overall protein kinase C-induced
inhibition of the exchanger.
Department of Medicine,
University of Arkansas for Medical Sciences, Little Rock, Arkansas
72205, and § Unité de Recherches sur la
Différenciation Cellulaire Intestinale, INSERM U178, 94807 Villejuif Cedex, France
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D. W. Good, J. F. Di Mari, and B. A. Watts III Hyposmolality stimulates Na+/H+ exchange and HCO3- absorption in thick ascending limb via PI 3-kinase Am J Physiol Cell Physiol, November 1, 2000; 279(5): C1443 - C1454. [Abstract] [Full Text] [PDF]
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E. J. Weinman, C. Minkoff, and S. Shenolikar Signal complex regulation of renal transport proteins: NHERF and regulation of NHE3 by PKA Am J Physiol Renal Physiol, September 1, 2000; 279(3): F393 - F399. [Abstract] [Full Text] [PDF]
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X. Yang, M. Amemiya, Y. Peng, O. W. Moe, P. A. Preisig, and R. J. Alpern Acid incubation causes exocytic insertion of NHE3 in OKP cells Am J Physiol Cell Physiol, August 1, 2000; 279(2): C410 - C419. [Abstract] [Full Text] [PDF]
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A. J. Janecki, M. Janecki, S. Akhter, and M. Donowitz Basic Fibroblast Growth Factor Stimulates Surface Expression and Activity of Na+/H+ Exchanger NHE3 via Mechanism Involving Phosphatidylinositol 3-Kinase J. Biol. Chem., March 10, 2000; 275(11): 8133 - 8142. [Abstract] [Full Text] [PDF]
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C.-W. Chow, S. Khurana, M. Woodside, S. Grinstein, and J. Orlowski The Epithelial Na+/H+ Exchanger, NHE3, Is Internalized through a Clathrin-mediated Pathway J. Biol. Chem., December 31, 1999; 274(53): 37551 - 37558. [Abstract] [Full Text] [PDF]
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C. R. L. Webster and M. S. Anwer Role of the PI3K/PKB signaling pathway in cAMP-mediated translocation of rat liver Ntcp Am J Physiol Gastrointest Liver Physiol, December 1, 1999; 277(6): G1165 - G1172. [Abstract] [Full Text] [PDF]
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M. E. Cavet, S. Akhter, F. S. de Medina, M. Donowitz, and C.-M. Tse Na+/H+ exchangers (NHE1-3) have similar turnover numbers but different percentages on the cell surface Am J Physiol Cell Physiol, December 1, 1999; 277(6): C1111 - C1121. [Abstract] [Full Text] [PDF]
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 P. J. Mohler, S. M. Kreda, R. C. Boucher, M. Sudol, M. J. Stutts, and S. L. Milgram Yes-associated Protein 65 Localizes p62c-Yes to the Apical Compartment of Airway Epithelia by Association with EBP50 J. Cell Biol., November 15, 1999; 147(4): 879 - 890. [Abstract] [Full Text] [PDF]
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O. W. MOE Acute Regulation of Proximal Tubule Apical Membrane Na/H Exchanger NHE-3: Role of Phosphorylation, Protein Trafficking, and RegulatoryFactors J. Am. Soc. Nephrol., November 1, 1999; 10(11): 2412 - 2425. [Full Text]
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K. Kurashima, S. D'Souza, K. Szaszi, R. Ramjeesingh, J. Orlowski, and S. Grinstein The Apical Na+/H+ Exchanger Isoform NHE3 Is Regulated by the Actin Cytoskeleton J. Biol. Chem., October 15, 1999; 274(42): 29843 - 29849. [Abstract] [Full Text] [PDF]
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A. J. Janecki, M. H. Montrose, C. M. Tse, F. S. de Medina, A. Zweibaum, and M. Donowitz Development of an endogenous epithelial Na+/H+ exchanger (NHE3) in three clones of Caco-2 cells Am J Physiol Gastrointest Liver Physiol, August 1, 1999; 277(2): G292 - G305. [Abstract] [Full Text] [PDF]
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R. Collazo, L. Fan, M. C. Hu, H. Zhao, M. R. Wiederkehr, and O. W. Moe 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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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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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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W. Lee-Kwon, D. C. Johns, B. Cha, M. Cavet, J. Park, P. Tsichlis, and M. Donowitz Constitutively Active Phosphatidylinositol 3-Kinase and AKT Are Sufficient to Stimulate the Epithelial Na+/H+ Exchanger 3 J. Biol. Chem., August 10, 2001; 276(33): 31296 - 31304. [Abstract] [Full Text] [PDF]
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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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