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Exfoliation of gastric pit-parietal cells into the gastric lumen associated with a stimulation of isolated rat gastric mucosa in vitro: a morphological study by the application of cryotechniques

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Abstract

It is clinicopathologically important to elucidate the cell kinetics for the maintenance of normal gastric epithelium. In a rat gastric mucosa isolated after stimulation, a number of cells were exfoliated into the gastric lumen of the pit region. The present study was undertaken to clarify the origin of exfoliated cells and their histochemical profiles by taking the advantages of cryotechniques. As results, most of the exfoliated cells were identified as pit-parietal cells labeled with both peanut-lectin and anti-H+/K+-ATPase antibody. Quantitative analysis verified a time-dependent increase in the number of exfoliated cells in the gastric mucosa isolated after stimulation. The exfoliated cells exhibited a diffuse intracellular staining for E-cadherin, suggesting a dissociation of the adhesion molecule prior to the cell exfoliation. It should be noted that most of the exfoliated cells were negative to the apoptotic markers (TUNEL staining and caspase-3). Ultrastructurally, autophagosome-like structures consisting of H+/K+-ATPase positive membranes were frequently seen in the exfoliated pit-parietal cells. In addition, the pit-parietal cell exfoliation was accompanied by sealing of their basal portion with the cytoplasmic processes of adjacent surface mucous cells. The present morphological findings provide a new insight into the cell kinetics in the gastric epithelium in vitro.

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References

  • Allen A, Flemström G, Garner A, Kivilaakso E (1993) Gastroduodenal mucosal protection. Physiol Rev 73:823–857

    PubMed  CAS  Google Scholar 

  • Chew CS, Ljungström M, Smolka A, Brown MR (1989) Primary culture of secretagogue-responsive parietal cells from rabbit gastric mucosa. Am J Physiol 256:G254–G263

    PubMed  CAS  Google Scholar 

  • Clarke PGH (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195–213

    Article  PubMed  CAS  Google Scholar 

  • Coulton GR, Firth JA (1983) Cytochemical evidence for functional zonation of parietal cells within the gastric glands of the mouse. Histochem J 15:1141–1150

    Article  PubMed  CAS  Google Scholar 

  • Coulton GR, Firth JA (1988) Effects of starvation, feeding, and time of day on the activity of proton transport adenosine triphosphatase in the parietal cells of the mouse gastric glands. Anat Rec 222:42–48

    Article  PubMed  CAS  Google Scholar 

  • De Mey J, Moeremans M, Geuens R, Nuydens R, Brabander MD (1981) High resolution light and electron microscopic localization of tubulin with the IGS (immuno gold staining) method. Cell Biol Int Rep 5:889–899

    Article  PubMed  Google Scholar 

  • Forte JG, Yao X (1996) The membrane-recruitment-and recycling hypothesis of gastric HCl secretion. Trends Cell Biol 6:45–48

    Article  PubMed  CAS  Google Scholar 

  • Forte TM, Machen TE, Forte JG (1977) Ultrastructural changes in oxyntic cells associated with secretory function: a membrane-recycling hypothesis. Gastroenterology 73:941–955

    PubMed  CAS  Google Scholar 

  • Frens G (1973) Controlled nucleation for the regulation of the particle size in monodisperse gold suspensions. Nature 241:20–22

    CAS  Google Scholar 

  • Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23:2891–2906

    Article  PubMed  CAS  Google Scholar 

  • Helander HF, Hirschowitz BI (1972) Quantitative ultrastructural studies on gastric parietal cells. Gastroenterology 63:951–961

    PubMed  CAS  Google Scholar 

  • Ito S, Munro DR, Schofield GC (1977) Morphology of the isolated mouse oxyntic cell and some physiological parameters. Gastroenterology 73:887–898

    PubMed  CAS  Google Scholar 

  • Jehl B, Bauer R, Dörge A, Rick R (1981) The use of propane/isopentane mixtures for rapid freezing of biological specimens. J Microsc 123:307–309

    PubMed  CAS  Google Scholar 

  • Karam SM (1993) Dynamics of epithelial cells in the corpus of the mouse stomach. IV. Bidirectional migration of parietal cells ending in their gradual degeneration and loss. Anat Rec 236:314–332

    Article  PubMed  CAS  Google Scholar 

  • Karam SM (1999) Lineage commitment and maturation of epithelial cells in the gut. Front Biosci 4:d286–d298

    Article  PubMed  CAS  Google Scholar 

  • Karam SM, Yao X, Forte JG (1997) Functional heterogeneity of parietal cells along the pit-gland axis. Am J Physiol 272:G161–171

    PubMed  CAS  Google Scholar 

  • Kressin M (1996) Heterogeneity and migration-related zonation of K+-ATPase activities in the oxyntic cell lineage of adult cattle. Cell Tissue Res 284:231–238

    Article  PubMed  CAS  Google Scholar 

  • Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419

    Article  PubMed  CAS  Google Scholar 

  • Lotan R, Skutelsky E, Danon D, Sharon N (1975) The purification, composition and specificity of the anti-T lectin from peanut (Arachis hypogaea). J Biol Chem 250:8518–8523

    PubMed  CAS  Google Scholar 

  • Sawaguchi A, Ide S, Kawano J, Nagaike R, Oinuma T, Tojo H, Okamoto M, Suganuma T (1999) Reappraisal of potassium permanganate oxidation applied to Lowicryl K4M embedded tissues processed by high pressure freezing/freeze substitution, with special reference to differential staining of the zymogen granules of rat gastric chief cells. Arch Histol Cytol 62:447–458

    Article  PubMed  CAS  Google Scholar 

  • Sawaguchi A, Ide S, Goto Y, Kawano J, Oinuma T, Suganuma T (2001) A simple contrast enhancement by potassium permanganate oxidation for Lowicryl K4M ultrathin sections prepared by high pressure freezing/freeze substitution. J Microsc 201:77–83

    Article  PubMed  CAS  Google Scholar 

  • Sawaguchi A, McDonald KL, Karvar S, Forte JG (2002) A new approach for high-pressure freezing of primary culture cells: the fine structure and stimulation-associated transformation of cultured rabbit gastric parietal cells. J Microsc 208:158–166

    Article  PubMed  CAS  Google Scholar 

  • Sawaguchi A, Aoyama F, Ide S, Suganuma T (2005a) The cryofixation of isolated rat gastric mucosa provides new insights into the functional transformation of gastric parietal cells: an in vitro experimental model study. Arch Histol Cytol 68:151–160

    Article  PubMed  Google Scholar 

  • Sawaguchi A, Ide S, Suganuma T (2005b) Application of 10-μm thin stainless foil to a new assembly of the specimen carrier in high-pressure freezing. J Electron Microsc 54:143–146

    Article  Google Scholar 

  • Sawaguchi A, Aoyama F, Ohashi M, Ide S, Suganuma T (2006) Ultrastructural transformation of gastric parietal cells reverting from the active to the resting state of acid secretion revealed in isolated rat gastric mucosa model processed by high-pressure freezing. J Electron Microsc 55:97–105

    Article  CAS  Google Scholar 

  • Suganuma T, Tsuyama S, Suzuki S, Murata F (1984) Lectin-peroxidase reactivity in rat gastric mucosa. Arch Histol Jpn 47:197–207

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Yoshiteru Goto (Division of Electron Microscopy in Frontier Science Research Center, University of Miyazaki), and Yasuyo Todaka (Department of Anatomy, Ultrastructural Cell Biology, Faculty of Medicine, University of Miyazaki) for their expert assistances. This research was supported by Grants-in-Aids for Scientific Research from the Japan Society for the Promotion of Science (No. 18590190 and No. 18790145) and for 21st Century COE Program (Life Science) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Authors and Affiliations

  1. Department of Anatomy, Ultrastructural Cell Biology, Faculty of Medicine, University of Miyazaki, Miyazaki, 889-1692, Japan

    Fumiyo Aoyama, Akira Sawaguchi, Soyuki Ide & Tatsuo Suganuma

  2. Department of Internal Medicine, Circulatory and Body Fluid Regulation, Faculty of Medicine, University of Miyazaki, Miyazaki, 889-1692, Japan

    Kazuo Kitamura

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  1. Fumiyo Aoyama
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  2. Akira Sawaguchi
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  3. Soyuki Ide
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  4. Kazuo Kitamura
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  5. Tatsuo Suganuma
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Correspondence to Akira Sawaguchi.

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Aoyama, F., Sawaguchi, A., Ide, S. et al. Exfoliation of gastric pit-parietal cells into the gastric lumen associated with a stimulation of isolated rat gastric mucosa in vitro: a morphological study by the application of cryotechniques. Histochem Cell Biol 129, 785–793 (2008). https://doi.org/10.1007/s00418-008-0403-1

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