Advertisement

Rab11 Interacting Proteins as Regulators of Parietal Cell Apical Recycling: Lessons from the Master

  • James R. Goldenring
  • Chadwick M. Hales
  • Lynne A. Lapierre

Abstract

The gastric parietal cell in mammals is a highly differentiated cell with a specialized function: the secretion of HCl into the gastric lumen. To accomplish this highly regulated function, the parietal cell sequesters the H/K-ATPase responsible for pumping protons within a intracellular tubulovesicular membrane network (5). The tubulovesicular network lies deep to an elaborate infolding of the apical plasma membrane designated as the intracellular canaliculus. The intracellular canaliculus represents a target membrane surface for regulated fusion with tubulo vesicles (38). In response to either cAMP-dependent (histamine) or calcium-dependent (muscarinic cholinergic) agonists, tubulovesicle membrane fuse with the apical canalicular target membranes to deliver the H/K-ATPase to the luminal surface of activated parietal cells. Following the cessation of agonist stimulation, the H/K-ATPase is internalized and reassembled into the tubulovesicular system (12).

Keywords

Parietal Cell MDCK Cell Proton Transport Recycling System Gastric Parietal Cell 
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.
    Ammar,D. A.,P. N.Nguyen, and J. G. Forte. Functionally distinct pools of actin in secretory cells. Am.J.Physiol. 281: C407–C417, 2001.Google Scholar
  2. 2.
    Apodaca, G., L. A. Katz, and K. E. Mostov. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J.Cell Biol. 125: 67–86, 1994.PubMedCrossRefGoogle Scholar
  3. 3.
    Bahadoran, P., E. Aberdam, F. Mantoux, R. Busca, K. Bille, N. Yalman, G. de Sain-Basile, R. Cararoli-Marano, J. P. Ortonne, and R. Ballotti. Rab27a: A key to melanosome transport in human melanocytes. J. Cell Biol. 152: 843–850, 2001.PubMedCrossRefGoogle Scholar
  4. 4.
    Basson, M. D., J. R. Goldenring, L. H. Tang, J. J. Lewis, P. Padfield, J. D. Jamieson, and I. M. Modlin. Redistribution of 23 kDa tubulovesicle-associated GTP-binding proteins during parietal cell stimulation. Biochem.J. 279: 43–48, 1991.Google Scholar
  5. 5.
    Black, J. A., T. M. Forte, and J. G. Forte. Structure of oxyntic cell membranes during conditions of rest and secretion of HCl as revealed by freeze-fracture. Anat. Rec. 196: 163–172, 1980.PubMedCrossRefGoogle Scholar
  6. 6.
    Calhoun, B. C. and J. R. Goldenring. Two Rab proteins, VAMP-2, and SCAMPs are present on immunoisolated gastric tubulovesicles. Biochem.J. 325: 559–564, 1997.PubMedGoogle Scholar
  7. 7.
    Calhoun, B. C., L. A. Lapierre, C. S. Chew, and J. R. Goldenring. Rab11a redistributes to apical secretory canaliculus during stimulation of gastric parietal cells. Am.J.Physiol. 275: C163–C170, 1998.PubMedGoogle Scholar
  8. 8.
    Casanova, J. E., X. Wang, R. Kumar, S. G. Bhartur, J. Navarre, J. E. Woodrum, G. S. Ray, and J. R. Goldenring. Rab11a and Rab25 association with the apical recycling system of polarized MDCK cells. Mol.Biol.Cell. 10:47–61, 1999.PubMedGoogle Scholar
  9. 9.
    Cheney, R. E., M. K. O’Shea, J. E. Heuser, M. V. Coelho, J. S. Wolenski, E. M. Espreafico, P. Forscher, R. E. Larson, and M. S. Mooseker. Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75: 13–23, 1993.PubMedGoogle Scholar
  10. 10.
    Chew, C. S. Parietal cell culture: new models and directions. Annu.Rev.Physiol. 56: 445–461, 1994.PubMedCrossRefGoogle Scholar
  11. 11.
    Duman, J. G., K. Tyagarajan, M. S. Kolsi, H. H. Moore, and J. G. Forte. Expression of rab11a N124I in gastric parietal cells inhibits stimulatory recruitment of the H+-K+ -ATPase. Am.J.Physiol. 277: C361–C372, 1999.PubMedGoogle Scholar
  12. 12.
    Forte, T. M., T. E. Machen, and J. G. Forte. Ultrastructural changes in oxyntic cells associated with secretory function: a membrane recycling hypothesis. Gastroenterology. 73: 941–955, 1977.PubMedGoogle Scholar
  13. 13.
    Goldenring, J. R., C. J. Soroka, W. Rodriguez, L. H. Tang, K. R. Shen, H. D. Vaughan, and I. M. Modlin. Rab11 is highly expressed in gastric parietal cells. Gastroenterology 104: A826, 1993.Google Scholar
  14. 14.
    Goldenring, J. R., K. R. Shen, H. D. Vaughan, and I. M. Modlin. Identification of a small GTP-binding protein, Rab25, expressed in the gastrointestinal mucosa, kidney and lung. J.Biol.Chem. 268: 18419–18422, 1993.PubMedGoogle Scholar
  15. 15.
    Goldenring, J. R., J. Smith, H. D. Vaughan, P. Cameron, W. Hawkins, and J. Navarre. Rab11 is an apically located small GTP-binding protein in epithelial tissues. Am.J.Physiol. 270(33): G515–G525, 1996.PubMedGoogle Scholar
  16. 16.
    Goldenring, J. R., C. J. Soroka, K. R. Shen, L. H. Tang, W. Rodriguez, H. D. Vaughan, S. A. Stoch, and I. M. Modlin. Enrichment of rab11, a small GTP-binding protein, in gastric parietal cells. Am.J.Physiol. 267: G187–G194, 1994.PubMedGoogle Scholar
  17. 17.
    Gonzales, Jr. L. and R. H. Scheller. Regulation of membrane trafficing: structural insights from a rab/effector complex. Cell. 96: 755–758, 1999.CrossRefGoogle Scholar
  18. 18.
    Hales, C. M., R. Griner, K. C. Hobdy-Henderson, M. C. Dorn, D. Hardy, R. Kumar, J. Navarre, E. K. L. Chan, L. A. Lapierre, and J. R. Goldenring. Identification and characterization of a family of Rab 11 -interacting proteins. J.Biol.Chem. 276:39067–39075, 2001PubMedCrossRefGoogle Scholar
  19. 19.
    Hirst, B. H. and J. G. Forte. Redistribution and characterization of (H+,K+)-ATPase membranes from resting and stimulated parietal cells. Biochem.J. 231: 641–649, 1985.PubMedGoogle Scholar
  20. 20.
    Hughson, E. J. and C. Hopkins. Endocytic pathways in polarized caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces. J. Cell Biol. 110: 337–348, 1990.PubMedCrossRefGoogle Scholar
  21. 21.
    Hume, A. N., L. M. Collinson, A. Rapak, A. Q. Gomes, C. R. Hopkins, and M. C. Seabra. Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J.Cell Biol. 152: 795–808, 2001.PubMedCrossRefGoogle Scholar
  22. 22.
    Knight, A., E. Hughson, C. R. Hopkins, and D. F. Cutler. Membrane protein trafficking through the common apical endosome compartment of polarized Caco-2 cells. Mol.Biol.Cell. 6: 597–610, 1995.PubMedGoogle Scholar
  23. 23.
    Lapierre, L. A., R. Kumar, C. M. Hales, J. Navarre, S. G. Bhartur, J. O. Burnette, J. A. Mercer, M. Bahler, and J. R. Goldenring. Myosin Vb is associated with and regulates plasma membrane recycling systems. Mol.Biol.Cell 12: 1843–1857, 2001.PubMedGoogle Scholar
  24. 24.
    Mammoto, A., T. Ohtsuka, I. Hotta, T. Sasaki, and Y. Takai. Rab11BP/Rabphillin- 11, a downstream target of Rab11 small G protein implicated in vesicle recycling. J.Biol.Chem. 274: 25517–25524, 1999.PubMedCrossRefGoogle Scholar
  25. 25.
    Mercer, J. A., P. K. Seperack, M. C. Strobel, N. G. Copeland, and N. A. Jenkins. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349, Feb. 21: 709–712, 1991.PubMedCrossRefGoogle Scholar
  26. 26.
    Mostov, K., G. Apodaca, B. Areoti, and C. Okamoto. Plasma membrane protein sorting in polarized epithelial cells. J Cell Biol 116: 577–583, 1992.PubMedCrossRefGoogle Scholar
  27. 27.
    Mostov, K. E. and D. L. Deitcher. Polymeric immunoglobulin receptor expressed in MDCK cells transcytoses IgA. Cell 46: 613–621, 1986.PubMedCrossRefGoogle Scholar
  28. 28.
    Nuoffer, C. and W. E. Balch. GTPases: Multifunctional molecular switches regulating vesicular traffic. Ann.Rev.Biochem. 63: 949–990, 1994.PubMedCrossRefGoogle Scholar
  29. 29.
    Odorizzi, G., A. Pearse, D. Domingo, I. D. Trowbridge, and C. R. Hopkins. Apical and basolateral endosomes of MDCK cells are interconnected and contain a polarized sorting mechanism. J Cell Biol 135: 139–152, 1996.PubMedCrossRefGoogle Scholar
  30. 30.
    Peng, X.-P., X. Yao, D.-C. Chow, J. G. Forte, and M. K. Bennett. 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
  31. 31.
    Prekeris, R., Davies, J. M., and Scheller, R. H. Identification of a novel Rab11/25 binding domain in eferin and Rip proteins. J.Biol.Chem. 276:38966–38970, 2001PubMedCrossRefGoogle Scholar
  32. 32.
    Prekeris, R., J. Klumperman, and R. H. Scheller. A Rab11/Rip11 complex regulates apical membrane trafficking via recycling endosomes. Molec.Cell 6: 1437–1448, 2000.PubMedCrossRefGoogle Scholar
  33. 33.
    Provance, D. W. Jr., M. Wei, V. Ipe, and J. A. Mercer. Cultured melanocytes from dilute mice exhibit dendritic morphology and altered melanosome distribution.Proc.Natl.Acad.Sci.,USA 93: 14554–14558, 1996.PubMedCrossRefGoogle Scholar
  34. 34.
    Reck-Peterson, S. L., D. W. Provance, M. S. Mooseker, and J. A. Mercer. Class V myosins. Biochem.Biophys.Acta 1496: 36–51, 2000.Google Scholar
  35. 35.
    Rothman, J. E. and G. Warren. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr.Biol. 4: 220–233, 1994.PubMedCrossRefGoogle Scholar
  36. 36.
    Schott, D., J. Ho, D. Pruyne, and A. Bretscher. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147:791–807, 1999.PubMedCrossRefGoogle Scholar
  37. 37.
    Smolka, A., H. F. Helander, and G. Sachs. Monoclonal antibodies against gastric H/K-ATPase. Am.J.Physiol. 245: G589–G596, 1983.PubMedGoogle Scholar
  38. 38.
    Soroka, C. J., C. S. Chew, I. M. Modlin, D. Hanzel, A. Smolka, and J. R. Goldenring. Characterization of membrane and cytoskeletal compartments in cultured parietal cells using immunofluorescence and confocal microscopy. Eur.J.Cell Biol. 60: 76–87, 1993.PubMedGoogle Scholar
  39. 39.
    Tang, L. H., S. A. Stoch, I. M. Modlin, and J. R. Goldenring. Identification of rab2 as a tubulovesicle-membrane associated protein in rabbit gastric parietal cells. Biochem. J. 285: 715–719, 1992.PubMedGoogle Scholar
  40. 40.
    Tisdale, E. J. and W. E.Balch. Rab2 is essential for the maturation of pre-Golgi intermediates. J.Biol.Chem. 271: 29372–29379, 1996.PubMedCrossRefGoogle Scholar
  41. 41.
    Wang, D., J. P. Buyon, W. Zhu, and E. K. Chan. Defining a novel 75 kDa phosphoprotein assocaited with SS-A/Ro and identification of distinct human autoantibodies. J.Clin.Invest 104: 1265–1275, 1999.PubMedCrossRefGoogle Scholar
  42. 42.
    Wang, E., P. S. Brown, B. Aroeti, S. J. Chapin, K. E. Mostov, and K. W. Dunn. Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly neutral apical recycling endosome. Traffic. 1: 480–493, 2000.PubMedCrossRefGoogle Scholar
  43. 43.
    Wang, X., R. Kumar, J. Navarre, J. E. Casanova, and J. R. Goldenring. Regulation of vesicle trafficking in Madin-Darby Canine Kidney cells by Rab11a and Rab25. J.Biol.Chem. 275: 29138–29146, 2000.PubMedCrossRefGoogle Scholar
  44. 44.
    Wu, X., K. Rao, M. B. Bowers, N. G. Copeland, N. A. Jenkins, and J. A. Hammer. Rab27a enables myosin Va-dependent melanosome capture by recruiting the myosin to the organelle. J.Cell Sci. 114: 1091–1100, 2001.PubMedGoogle Scholar
  45. 45.
    Zeng, X., M. Ren, D. Gravotta, C. De Lemos-Chiarandini, M. Lui, H. Erdjument-Bromage, P. Tempst, G. Xu, T. H. Shen, T. Morimoto, M. Adesnick, and D. D. Sabatini. Identification of a putative effector protein for rabí 1 that participates in transferrin recycling. Proc.Natl.Acad.Sci., USA 96: 2840–2845, 1999.PubMedCrossRefGoogle Scholar
  46. 46.
    Zhao, L. P., J. S. Koslovsky, J. Reinhard, M. Bahler, A. E. Witt, D. W. Jr. Provance, and J. A. Mercer. Cloning and characterization of myr6, an unconventional myosin of the dilute/myosin-V family. Proc.Natl.Acad.Sci., USA 93: 10826–10831, 1996.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • James R. Goldenring
    • 1
  • Chadwick M. Hales
    • 1
  • Lynne A. Lapierre
    • 1
  1. 1.Institute of Molecular Medicine and GeneticsMedical College of Georgia and the Augusta Department of Veterans Affairs Medical CenterAugustaUSA

Personalised recommendations