Abstract
When parietal cells are stimulated, the tubulovesicles containing H,K-ATPase, the essential proton pump, fuse with the apical membrane forming microvilli. In this procedure, small GTP binding proteins, Rab11, ARF, and Rho play important roles. Rab11 and ARF are considered to regulate the intracellular vesicular transport and fusion events, whereas Rho appears to conduct an inhibitory signal via the regulation of the actin cytoskeleton. The nature of F-actin is different between basolateral and apical membrane sites. The former plays a role to connect Ca2+ stores to plasma membrane making effective coupling between muscarinic receptor and IP3 receptor. The microfilaments supporting apical membrane appear to be negatively regulated by Rho/Rho-kinase in contrast to other secretory cells. For the elucidation of intracellular membrane traffic, which is the main issue of cell biology today, the parietal cell is a good model for studying this mechanism.
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Akagi, K., Nagao, T. and Urushidani, T. (1999). Responsiveness of ¯-escin-permeabilized rabbit gastric gland model: effects of functional peptide fragments, Am. J. Physiol. 277, C736–C744.
Ammar, D. A., Nguyen, P. N. and Forte, J. G. (2001). Functionally distinct pools of actin in secretory cells, Am. J. Physiol. 281, C407-C417.
Berglindh, T., Dibona, D. R., Ito, S., et al. (1980). Probes of parietal cell function, Am. J. Physiol. 238, G165–G176.
Brennwald, P., Kearns, B., Champion, K., et al. (1994). Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis, Cell 79, 245–258.
Calhoun, B. C. and Goldenring, J. R. (1997). Two Rab proteins, vesicle-associatedmembrane protein 2 (VAMP-2) and secretory carrier membrane proteins (SCAMPs), are present on immunoisolated parietal cell tubulovesicles, Biochem. J. 325, 559–564.
Calhoun, B. C., Lapierre, L. A., Chew, C. S., et al. (1998). Rab11a redistributes to apical secretory canaliculus during stimulation of gastric parietal cells, Am. J. Physiol. 275, C163–C170.
Chavrier, P. and Goud, B. (1999). The role of ARF and Rab GTPases in membrane transport, Curr. Opin. Cell Biol. 11, 466–475.
Doussau, F. and Augustine, G. J. (2000). The actin cytoskeleton and neurotransmitter release: an overview, Biochimie 82, 353–363.
Duman, J. G., Tyagarajan, K., Kolsi, M. S., et al. (1999). Expression of rab11a N124I in gastric parietal cells inhibits stimulatory recruitment of the HC-KC-ATPase, Am. J. Physiol. 277, C361–C372.
Duman, J. G., Pathak, N., Ladinsky, M. S., et al. (2002). Three-dimensional reconstruction of cytoplasmic membrane networks in parietal cells, J. Cell Sci. 115, 1251–1258.
Forte, T. M., Machen, T. E. and Forte, J. G. (1977). Ultrastructural changes in oxyntic cells associated with secretory function: a membrane recycling hypothesis, Gastroenterology 73, 941–955.
Forte, J. G., Ly, B., Rong, Q., et al. (1998). State of actin in gastric parietal cells, Am. J. Physiol. 274, C97–C104.
Frantz, C., Coppola, T. and Regazzi, R. (2002). Involvement of Rho GTPases and their effectors in the secretory process of PC12 cells, Exp. Cell Res. 273, 119–126.
Gaschet, J. and Hsu, V. W. (1999). Distribution of ARF6 between membrane and cytosol is regulated by its GTPase cycle, J. Biol. Chem. 274, 20040–20045.
Kahn, R. A. and Gilman, A. G. (1984). Purification of a protein cofactor required for ADP-ribosylation of the stimulatoryregulatory component of adenylate cyclase by cholera toxin, J. Biol. Chem. 259, 6228–6234.
Lang, P., Gesbert, F., Delespine-Carmagnat, M., et al. (1996). Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes, EMBO J. 15, 510–519.
Lapierre, L. A., Kumar, R., Hales, C. M., et al. (2001). Myosin vb is associatedwith plasma membrane recycling systems, Mol. Biol. Cell 12, 1843–1857.
Lenhard, J. M., Kahn, R. A. and Stahl, P. D. (1992). Evidence for ADP-ribosylation factor (ARF) as a regulator of in vitro endosome-endosomefusion, J. Biol. Chem. 267, 13047–13052.
Miller, M. D. and Hersey, S. J. (1996). Differential effects of GTPγS on acid and pepsinogensecretion by permeable gastric glands, Am. J. Physiol. 270, G962–G968.
Muto, Y., Nagao, T., Yamada, M., et al. (2001). A proposed mechanism for the potentiationof cAMP-mediated acid secretion by carbachol, Am. J. Physiol. 280, C155–C165.
Ogata, T. and Yamasaki, Y. (1993). Ultra-high-resolutionscanning electron microscopic studies on the membrane system of the parietal cells of the rat in the resting state and shortly after stimulation, Anat. Rec. 237, 208–219.
Ogata, T. and Yamasaki, Y. (2000). Scanning EM of resting gastric parietal cells reveals a network of cytoplasmic tubules and cisternae connected to the intracellular canaliculus, Anat. Rec. 258, 15–24.
Okamoto, C. T. and Forte, J. G. (2001). Vesicular trafficking machinery, the actin cytoskeleton, and HC-KC-ATPase recycling in the gastric parietal cell, J. Physiol. 532, 287–296.
Pausawasdi, N., Ramamoorthy, S., Stepan, V., et al. (2000). Regulation and function of p38 protein kinase in isolated canine gastric parietal cells, Am. J. Physiol. 278, G24–G31.
Pettitt, J. M., Humphris, D. C., Barrett, S. P., et al. (1995). Fast freeze-fixation/ freeze-substitution reveals the secretory membranes of the gastric parietal cell as a network of helically coiled tubule. A new model for parietal cell transformation, J. Cell Sci. 108, 1127–1141.
Price, L. S., Norman, J. C., Ridley, A. J., et al. (1995). The small GTPases Rac and Rho as regulators of secretion in mast cells, Curr. Biol. 5, 68–73.
Ribeiro, C. M. P., Reece, J. and Putney, Jr. J. W. (1997). Role of the cytoskeleton in calciumsignaling in NIH 3T3 cells, J. Biol. Chem. 272, 26555–26561.
Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors, Cell 70, 389–399.
Takai, Y., Sasaki, T. and Matozaki, T. (2001). Small GTP-binding proteins, Physiol. Rev. 81, 153–208.
Torii, S., Zhao, S., Yi, Z., et al. (2002). Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a, Mol. Cell. Biol. 22, 5518–5526.
Urushidani, T. and Forte, J. G. (1997). Signal transduction and activation of acid secretion in the parietal cell, J. Membr. Biol. 159, 99–111.
van Leeuwen, F. N., van Delft, S., Kain, H. E., et al. (1999). Rac regulates phosphorylation of the myosin-II heavy chain, actinomyosin disassembly and cell spreading, Nature Cell Biol. 1, 242–248.
Vitale, N., Gasman, S., Caumont, A. S., et al. (2000). Insight in the exocytotic process in chromaffin cells: regulation by trimeric and monomeric G proteins, Biochimie 82, 365–373.
Yamaguchi, Y., Katoh, H., Yasui, H., et al. (2000). Gα12 and Gα13 inhibit Ca 2+-dependent exocytosis through Rho/ Rho-associated kinase-dependent pathway, J. Neurochem. 75, 708–717.
Yao, X., Chaponnier, C., Gabbiani, G., et al. (1995). Polarized distributionof actin isoforms in gastric parietal cells, Mol. Biol. Cell 6, 541–557.
Zerial, M. and McBride, H. (2001). Rab proteins as membrane organizers, Nature Rev. Mol. Cell Biol. 2, 107–117.
Zhang, C. J., Rosenwald, A. G., Willingham, M. C., et al. (1994). Expression of a dominant allele of human ARF1 inhibits membrane traffic in vivo, J. Cell Biol. 124, 289–300.
Zhao, L. P., Koslovsky, J. S., Reinhard, J., et al. (1996). Cloning and characterization of myr 6, an unconventional myosin of the dilute/ myosin-V family, Proc. Natl. Acad. Sci. USA 93, 10826–10831.
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Matsukawa, J., Tashiro, K., Nagao, T. et al. Role of small GTP-binding proteins and cytoskeleton in gastric acid secretion. Inflammopharmacology 10, 333–341 (2002). https://doi.org/10.1163/156856002321544800
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DOI: https://doi.org/10.1163/156856002321544800