Skip to main content

Fate of annular gap junctions in the papillary cells of the enamel organ in the rat incisor

Cell and Tissue Research volume 246, pages 523–530 (1986)Cite this article

Summary

To investigate the mechanisms whereby annular gap junctions in the papillary cells of the enamel organ are degraded intracellularly, continuously growing rat incisors were examined by electron microscopy of routine thin sections as well as for the cytochemical localization of inorganic trimetaphosphatase activity. Routine thin-section analysis revealed small flat or undulated gap junctions, hemi-annular gap junctions between an invaginated cell process and a cell body, and fully internalized cytoplasmic annular gap junctions. Both hemi-annular and annular gap junctions usually contain various organelles and/or inclusions, such as mitochondria, endoplasmic reticulum, ribosomes, vesicles, and lysosomes in the cytoplasm confined by the junctional membranes. Annular gap junctions are sometimes fused with vesicular or tubulovesicular structures. Cytochemistry of inorganic trimetaphosphatase activity revealed an intense enzymatic reaction within a system of tubular structures and round or oval dense bodies. Both structures are believed to correspond to primary lysosomes. A part of the Golgi apparatus also shows a weak reaction. Although hemi-annular gap junctions never show enzymatic reaction, annular gap junctions sometimes contain reaction products throughout their interior cytoplasm and inclusions. Fusion of annular gap-junctional membranes with reaction-positive tubular structures is also observed. In one instance, revealed in serial sections, an annular gap junction was encircled entirely by a reaction-positive structure. These results suggest that cytoplasmic annular gap junctions are formed by endocytosis of hemi-annular gap junctional membranes from the cell surface and then degraded intracellularly by lysosomal enzymes.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Albertini DF, Fawcett DW, Olds PJ (1975) Morphological variations in gap junctions of ovarian granulosa cells. Tissue Cell 7:389–405

    Google Scholar 

  • Archard HO, Denys FR (1979) Development of annular gap junctions in guinea pig epithelia. J Oral Pathol 8:187–197

    Google Scholar 

  • Bennett MVL, Spira ME, Spray DC (1978) Permeability of gap junctions between embryonic cells of Fundulus: A reevaluation. Dev Biol 65:114–125

    Google Scholar 

  • Berry MN, Friend DS (1969) High yield preparation of isolated rat liver parenchymal cells. J Cell Biol 43:506

    Google Scholar 

  • Doty SB, Schofield BH (1972) Electron microscopic localization of hydrolytic enzymes in osteoblasts. Histochem J 4:245–258

    Google Scholar 

  • Espey LL, Stutts RH (1972) Exchange of cytoplasm between cells of the membrana granulosa in rabbit ovarian follicles. Biol Reprod 6:168–175

    Google Scholar 

  • Garant PR, Nalbandian J (1968) The fine structure of the papillary region of the mouse enamel organ. Arch Oral Biol 13:1167–1185

    Google Scholar 

  • Garant PR, Gillespie R (1969) The presence of fenestrated capillaries in the papillary layer of the enamel organ. Anat Rec 163:71–80

    Google Scholar 

  • Garant PR (1972) The demonstration of complex gap junctions between the cells of the enamel organ with lanthanum nitrate. J Ultrastruct Res 40:333–348

    Google Scholar 

  • Garant PR, Nagy A, Cho MI (1984) A freeze-fracture study of the papillary layer of the rat incisor enamel organ. Tissue Cell 16:635–645

    Google Scholar 

  • Ginzberg RD, Gilula NB (1979) Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium. Dev Biol 68:110–129

    Google Scholar 

  • Johnson RG, Hammer M, Sheridan JD, Revel JP (1974) Gap junction formation between reaggregated Novikoff hepatoma cells. Proc Natl Acad Sci USA 71:4536–4540

    Google Scholar 

  • Kallenbach E (1966) Electron microscopy of the papillary layer of rat incisor enamel organ during enamel maturation. J Ultrastruct Res 14:518–533

    CAS  PubMed  Google Scholar 

  • Kallenbach E (1967) Cell architecture in the papillary layer of rat incisor enamel organ at the stage of enamel maturation. Anat Rec 157:685–698

    Google Scholar 

  • Kallenbach E (1980) Access of horseradish peroxidase (HRP) to the extracellular spaces of the maturation zone of the rat incisor enamel organ. Tissue Cell 12:165–174

    Google Scholar 

  • Karnovsky MJ (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. Proc 11th Am Soc Cell Biol, p 146

  • Larsen WJ (1977) Structural diversity of gap junctions. A review. Tissue Cell 9:373–394

    CAS  PubMed  Google Scholar 

  • Larsen WJ, Tung HN (1978) Origin and fate of cytoplasmic gap junctional vesicles in rabbit granulosa cells. Tissue Cell 10:585–598

    Google Scholar 

  • Leach DH, Oliphant LW (1984) Degradation of annular gap junctions of the equine hoof wall. Acta Anat 120:214–219

    Google Scholar 

  • Marquart KH (1977) So-called annular gap junctions in bone cells of normal mice. Experientia 33:270–272

    Google Scholar 

  • Mayahara H (1972) Ultracytochemistry of mouse subcutaneous histiocytes. 2. Mechanism of autophagosome formation. J Kansai Med Sch [Suppl] 24:S98-S129

    Google Scholar 

  • Merk FB, Botticelli CR, Albright JT (1972) An intercellular response to estrogen by granulosa cells in the rat ovary. An electron microscopic study. Endocrinology 90:992–1007

    Google Scholar 

  • Merk FB, Albright JT, Botticelli CR (1973) The fine structure of granulosa cell nexuses in rat ovarian follicles. Anat Rec 175:107–126

    Google Scholar 

  • Nanci A, Warshawsky H (1984) Characterization of putative secretory sites on ameloblasts of the rat incisor. Anat Rec 171:163–189

    Google Scholar 

  • Overton J (1968) The fate of desmosomes in trypanized tissue. J Exp zool 168:203–214

    Google Scholar 

  • Pappas GD (1975) Junctions between cells. In: Weismann G, Clai-borne R (eds) Cell membranes. Hospital Practice, New York, pp 87–94

    Google Scholar 

  • Pfeifer U (1980) Autophagic sequestration of internalized gap junctions in rat liver. Eur J Cell Biol 21:244–246

    Google Scholar 

  • Reith EJ, Cotty VF (1967) The absorptive activity of ameloblasts during the maturation of enamel. Anat Rec 157:577–588

    Google Scholar 

  • Reith EJ (1970) The stage of amelogenesis as observed in molar teeth of young rats. J Ultrastruct Res 30:111–151

    Google Scholar 

  • Robinson C, Briggs HD, Atkinson PJ (1981) Histology of enamel organ and chemical composition of adjacent enamel in rat incisors. Calc Tissue Int 33:513–520

    Google Scholar 

  • Sakai M, Ogawa K (1982) Energy-dependent lysosomal wrapping mechanism (LWM) during autophagolysosome formation. Histochemistry 76:479–488

    Google Scholar 

  • Sasaki T, Higashi S (1983) A morphological, tracer and cytochemical study of the role of the papillary layer of the rat incisor enamel organ during enamel maturation. Arch Oral Biol 28:201–210

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T (1984a) Endocytotic pathways at the ruffled borders of rat maturation ameloblasts. Histochemistry 80:263–268

    Google Scholar 

  • Sasaki T (1984b) Morphology and function of maturation ameloblasts in kitten tooth germs. J Anat 138:333–342

    Google Scholar 

  • Sasaki T, Higashi S, Tachikawa T, Yoshiki S (1984) Absorptive and digestive functions of maturation ameloblasts in rat incisors. In: Tooth Enamel IV. Elsevier Science Publisher, Amsterdam, pp 266–270

    Google Scholar 

  • Sasaki T, Tominaga H, Higashi S (1984) Microvascular architecture of the enamel organ in the rat incisor maturation zone. Scanning and transmission electron microscopic studies. Acta Anat 118:205–213

    Google Scholar 

  • Shimono M, Clementi F (1976) Intercellular junctions of oral epithelium. I. Studies with freeze-fracture and tracing methods of normal rat keratinizing oral epithelium. J Ultrastruct Res 56:121–136

    Google Scholar 

  • Skobe Z, Garant PR (1974) Electron microscopy of horseradish peroxidase uptake by papillary cells of the mouse incisor enamel organ. Arch Oral Biol 19:387–395

    Google Scholar 

  • Takano Y, Ozawa H (1980) Ultrastructural and cytochemical observations on the alternating morphologic changes of the ameloblasts at the stage of enamel maturation. Arch Histol Jpn 43:385–399

    CAS  PubMed  Google Scholar 

  • Takano Y, Crenshaw MA, Reith EJ (1982) Correlation of 45Ca incorporation with maturation ameloblast morphology in the rat incisor. Calc Tissue Int 34:211–213

    Google Scholar 

  • Yancey SB, Easter D, Revel JP (1979) Cytological changes in gap junctions during liver regeneration. J Ultrastruct Res 67:229–242

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Oral Biology and Pathology, School of Dental Medicine, Health Sciences Center, State University of New York at Stony Brook, New York, USA

    Takahisa Sasaki &  Philias R. Garant

Authors
  1. Takahisa Sasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philias R. Garant
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sasaki, T., Garant, P.R. Fate of annular gap junctions in the papillary cells of the enamel organ in the rat incisor. Cell Tissue Res. 246, 523–530 (1986). https://doi.org/10.1007/BF00215192

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00215192

Key words

  • Enamel organ
  • Papillary cell
  • Annular gap junction
  • Lysosome
  • Cytochemistry
  • Rat