Advertisement

Clathrin And Associated Proteins On Tubulovesicles And Apical Membranes Of Parietal Cells

  • Curtis T. Okamoto
  • Rui Li
  • Catherine S. Chew

Abstract

In the unstimulated gastric parietal cell, a major proportion of the gastric H,K-ATPase resides in an intracellular tubulocisternal (tubulovesicular) membrane compartment. Upon the stimulation of the parietal cell, the H,K-ATPase is delivered to the canalicular (apical) membrane as a result of fusion of tubulocisternal membranes with the apical membrane. Upon cessation of stimulation, the H,K-ATPase is retrieved from the canalicular membrane, and the tubulocisternal compartment is re-established. This membrane recycling model of the H,K-ATPase necessitates that protein sorting machinery is present in relative abundance to regulate the trafficking of the H,K-ATPase. Thus, the identification and functional characterization of the sorting machinery should be facilitated. To a significant extent, key components of the sorting machinery in parietal cells have in fact been characterized (reviewed in ref. 21). This report summarizes the identification and characterization of clathrin and clathrin-associated proteins in the parietal cell.

Keywords

Apical Membrane Parietal Cell Canalicular Membrane Gastric Parietal Cell Clathrin Heavy Chain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Blagoveshchenskaya, A.D., Hewitt, E.W., and Cutler, D.F.. Di-leucine signals mediate targeting of tyrosinase and synaptotagmin to synaptic-like microvesicles with PC12 cells. Mol. Biol. Cell 10: 3979–3990, 1999.PubMedGoogle Scholar
  2. 2.
    Bonifacino, J.S. and Dell’Angelica, E.C. Molecular bases for the recognition of tyrosine-based sorting signals. J. Cell Biol 145: 923–926, 1999.PubMedCrossRefGoogle Scholar
  3. 3.
    Calhoun, B.C. and Goldenring, J.R. Two rab proteins, VAMP-2, and SCAMPS are present on immunoisolated parietal cell tubulovesicles. Biochem. J. 325: 559–564, 1997PubMedGoogle Scholar
  4. Calhoun, B.C., Lapierre, L.A., Chew, C.S., and Goldenring, J.R. Rab11a redistributes to apical secretory canaliculus during stimulation of gastric parietal cells. Am. J. Physiol. Cell Physiol. 275: C163–C170, 1998.Google Scholar
  5. 5.
    Cao, H., Garcia, F., and McNiven, M.A. Differential distribution of dynamin isoforms in mammalian cells. Mol. Biol. Cell 9: 2595–2609, 1998.PubMedGoogle Scholar
  6. Chew, C.S., Parente, J.A. Jr., Zhou, C.-J., Baranco, E., and Chen, X. Lasp-1 is a regulated phosphoprotein within the cAMP signaling pathway in the gastric parietal cell. Am. J. Physiol. Cell Physiol. 275: C56–C67, 1998.Google Scholar
  7. 7.
    Chew, C.S., Parente, J.A. Jr., Chen, X., Chaponnier, C, and Cameron, R.S. The LIM and SH3 domain-containing protein, lasp-1, may link the cAMP signaling pathway with dynamic membrane restructuring activities in ion transporting epithelia. J. Cell Sci. 113: 2035–2045, 2000.PubMedGoogle Scholar
  8. 8.
    Courtois-Coutry, N., Roush, D., Rajendran, V., McCarthy, J.B., Geibel, J., Kashgarian, M., and Caplan, M.J. A tyrosine-based signal targets H/K-ATPase to a regulated compartment and is required for the cessation of gastric acid secretion. Cell 90: 501–510, 1997.PubMedCrossRefGoogle Scholar
  9. Dunbar, L.A. and Caplan, M.J. Ion pumps in polarized cells: sorting and regulation oftheNa+,K+- and H+,K+-ATPases. J. Biol. Chem. 276: 29617–29620.Google Scholar
  10. 10.
    Forte, G.M., Limlomwongse, L., and Forte, J.G. The development of intracellular membranes concomitant with the appearance of HCl secretion in oxyntic cells of the metamorphosing bullfrog tadpole. J. Cell Sci. 4: 709–727, 1969.PubMedGoogle Scholar
  11. 11.
    Gout, I., Dhand, R., Hiles, I.D., Fry, M.J., Panayotou, G., Das, P., Truong, O., Totty, N.F., Hsuan, J., Booker, G.W., Campbell, I.D., and Waterfield, M.D. The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75: 25–36, 1993.PubMedGoogle Scholar
  12. 12.
    Kessels, M.M., Engqvist-Goldstein, A.E.Y., Drubin, D.G., and Qualmann, B. Mammalian Abpl, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J. Cell. Biol. 153: 351–366, 2001.PubMedCrossRefGoogle Scholar
  13. 13.
    Kirchhausen, T. Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 15: 705–732, 1999.PubMedCrossRefGoogle Scholar
  14. 14.
    Long, K.R. Trofatter, J.A., Ramesh, V., McCormick, M.K., Buckler, A.J. Cloning and characterization of a novel human clathrin heavy chain gene (CLTCL). Genomics 35: 466–472, 1996.PubMedCrossRefGoogle Scholar
  15. Marsh, M. and McMahon, H.T. The structural era of endocytosis. Science 285: 215–219.Google Scholar
  16. 16.
    McNiven, M.A., Kim, L., Krueger, E.W., Orth, J.D., Cao, H., and Wong, T.W. Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J. Cell Biol 151: 187–198, 2000.PubMedCrossRefGoogle Scholar
  17. 17.
    Ochoa, G.-C., Slepnev, V.I., Neff, L., Ringstad, N., Takei, K., Daniell, L., Kim, W., Cao, H., McNiven, M., Baron, R., and De Camilli, P. A functional link between dynamin and the actin cytoskeleton at podosomes J. Cell Biol. 150: 377–389, 2000.PubMedCrossRefGoogle Scholar
  18. 18.
    Okamoto, C.T., Karam, S.M., Jeng, Y.Y., Forte, J.G., and Goldenring, J.R. Identification of clathrin and clathrin adaptors on tubulovesicles of gastric acid secretory (oxyntic) cells. Am. J. Physiol. Cell Physiol 274: C1017–C1029, 1998.Google Scholar
  19. 19.
    Okamoto, C.T. and Jeng, Y.Y. An immunologically distinct β-adaptin on tubulovesicles of gastric oxyntic cells. Am. J. Physiol. Cell Physiol. 275: C1323–C1329, 1998.Google Scholar
  20. 20.
    Okamoto, C.T., Duman, J.G., Tyagarajan, K., McDonald, K.L., Jeng, Y.Y., McKinney, J., Forte, T.M., and Forte, J.G. Clathrin in gastric acid secretory (parietal) cells: biochemical characterization and subcellular localization. Am. J. Physiol. Cell Physiol. 279: C833–C851, 2000PubMedGoogle Scholar
  21. 21.
    Okamoto, C.T. and Forte, J.G. Vesicular trafficking machinery, the actin cytoskeleton, and H+-K+-ATPase recycling in the gastric parietal cell. J. Physiol. 532: 287–296, 2001.PubMedCrossRefGoogle Scholar
  22. 22.
    Peng, X.-R., Yao, X., Chow, D.-C., Forte, J.G., and Bennett, M.K. Association of syntaxin 3 and vesicle-associated membrane protein (VAMP) with H+/K+-ATPase-containing tubulovesicles in gastric parietal cells. Mol. Biol. Cell. 8: 399–407, 1997.PubMedGoogle Scholar
  23. 23.
    Qualmann, B. and Kelly, R.B. Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J. Cell Biol. 148: 1047–1061, 2000.PubMedCrossRefGoogle Scholar
  24. 24.
    Qualmann, B., Kessels, M.M., and Kelly, R.B. Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150: F111–F1116, 2000.PubMedCrossRefGoogle Scholar
  25. 25.
    Robinson, M.S. Coats and vesicle budding. Trends Cell Biol. 7: 99–102, 1997.PubMedCrossRefGoogle Scholar
  26. 26.
    Roush, D.L., Gottardi, C.J., Nairn, H.Y., Roth, M.G., and Caplan, M.J.. Tyrosine-based membrane protein sorting signals are differentially interpreted by polarized Madin-Darby canine kidney and LLC-PKj epithelial cells. J. Biol. Chem. 273: 26862–26869, 1998.PubMedCrossRefGoogle Scholar
  27. 27.
    Schmid, S.L., McNiven, M.A., and DeCamilli, P. Dynamin and its partners: a progress report. Curr. Op. Cell Biol. 10: 504–512, 1998.PubMedCrossRefGoogle Scholar
  28. 28.
    Sever, S., Damke, H., and Schmid, S. Garrotes, springs, ratchets, and whips: putting dynamin models to the test. Traffic 1: 385–392, 2000.PubMedCrossRefGoogle Scholar
  29. 29.
    Shupliakov, O., Löw, P., Grabs, D., Gad, H., Chen, H., David, C., Takei, K., De Camilli, P., and Brodin, L. Synaptic vesicle endocytosis impaired by disruption ofdynamin-SH3 domain interactions. Science 276: 259–263, 1997.PubMedCrossRefGoogle Scholar
  30. 30.
    Simpson, F., Hussain, N.K., Qualmann, B., Kelly, R.B., Kay, B.K., McPherson, P.S., and Schmid, S.L. SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nature Cell Biol. 1: 119–124, 1999.PubMedCrossRefGoogle Scholar
  31. 31.
    van Ijzendoorn, S.C.D. and Hoekstra, D. The subapical compartment: a novel sorting centre? Trends Cell Biol. 9: 144–149, 1999.PubMedCrossRefGoogle Scholar
  32. 32.
    Vowels, J.J. and Payne, G.S. A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. EMBO J. 17: 2482–2493, 1997.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Curtis T. Okamoto
    • 1
  • Rui Li
    • 1
  • Catherine S. Chew
    • 2
  1. 1.Department of Pharmaceutical SciencesUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Institute of Molecular Medicine and GeneticsMedical College of GeorgiaAugustaUSA

Personalised recommendations