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Localization of type III collagen in the lingual mucosa of rats during the morphogenesis of circumvallate papillae

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Abstract

In an effort to identify a possible role for type III collagen in the morphogenesis of circumvallate papillae on the surface of the rat tongue, we examined its appearance by fluorescent immunostaining, in conjunction with differential interference contrast images and images obtained, after staining with toluidine blue, in the transmission mode by laser-scanning microscopy. We analyzed semi-ultrathin sections of epoxy resin-embedded samples of the lingual mucosa of embryonic and juvenile rats, 13 days after conception (E13) to day 21 after birth (P21). Immunoreactivity specific for type III collagen was recognized first in the mesenchymal connective tissue just beneath the circumvallate papilla placode in fetuses on E13. At this stage, most of the lingual epithelium with the exception of the circumvallate papilla placode was pseudostratified epithelium composed of one or two layers of cuboidal cells. However, the epithelium of the circumvallate papilla placode was composed of several layers of cuboidal cells. Immunoreactivity specific for type III collagen was detected mainly on the lamina propria just beneath the lingual epithelium of the rudiment of the circumvallate papilla and the developing circumvallate papilla in fetuses on E15 and E17, and slight immunostaining was detected on the lamina propria around the rudiment. In fetuses on E19, immunoreactivity specific for type III collagen was widely and densely distributed on the connective tissue around the developing circumvallate papillae and, also, on the connective tissue that surrounded the lingual muscle. However, the immunoreactivity specific for type III collagen was sparsely distributed on the lamina propria of each central papillar structure. After birth, from P0 to P14, morphogenesis of the circumvallate papillae advanced gradually with the increase in the total volume of the tongue. At these postnatal stages, the intensity of the fluorescence due to immunoreactivity specific for type III collagen was distinctively distributed on the lamina propria around each circumvallate papilla, on each central bulge and on the connective tissue that surrounded the lingual muscle. However, immunofluorescence was less distinct on the connective tissue that surrounded the lingual muscle. Thus, type III collagen appeared in conjunction with the morphogenesis of the circumvallate papillae, as well as in the connective tissue that surrounded the lingual muscle during myogenesis of the rat tongue.

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References

  1. Iwasaki S, Yoshizawa H, Kawahara I. Study by scanning electron microscopy of the morphogenesis of three types of lingual papilla in the rat. Anat Rec. 1997;247:528–41.

    PubMed  Google Scholar 

  2. Iwasaki S, Yoshizawa H, Kawahara I. Study by scanning electron microscopy of the morphogenesis of three types of lingual papilla in the mouse. Acta Anat. 1996;157:41–52.

    PubMed  Google Scholar 

  3. Iwasaki S, Okumura Y, Kumakura M. Ultrastructural study of the relationship between the morphogenesis of filiform papillae and the keratinization of the lingual epithelium in the mouse. Cells Tissues Organs. 1999;165:91–103.

    PubMed  Google Scholar 

  4. Iwasaki S, Yoshizawa H, Kawahara I. Ultrastructural study of the relationship between the morphogenesis of filiform papillae and the keratinization of the lingual epithelium in the rat. J Anat. 1999;195:27–38.

    PubMed  Google Scholar 

  5. Iwasaki S, Aoyagi H, Yoshizawa H. Immunohistochemical detection of the expression of keratin 14 in the lingual epithelium of rats during the morphogenesis of filiform papillae. Arch Oral Biol. 2003;48:605–13.

    PubMed  Google Scholar 

  6. Iwasaki S, Yoshizawa H, Aoyagi H. Immunohistochemical expression of keratins 13 and 14 in the lingual epithelium of rats during the morphogenesis of filiform papillae. Arch Oral Biol. 2006;51:416–26.

    PubMed  Google Scholar 

  7. Garrone R, Lethias C, Guellec D. Distibution of minor collagens during skin development. Microsc Res Tech. 1997;38:407–12.

    PubMed  Google Scholar 

  8. Lochner K, Gaemlich A, Südel KM, Venzke K, Moll I, Knott A, Stäb F, Wenck H, Döring O, Böttger M, Gallinat S. Expression of decorin collagens I and III in different layers of human skin in vivo: a laser capture microdissection study. Biogerontology. 2006;8:269–82.

    PubMed  Google Scholar 

  9. Risau W, Lemmon V. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev Biol. 1988;125:441–50.

    PubMed  Google Scholar 

  10. Nicosia RF, Villaschi S. Autoregulation of angiogenesis by cells of the vessel wall. Int Rev Cytol. 1999;185:1–43.

    PubMed  Google Scholar 

  11. Anstrom JA, Thore CR, Moody DM, Challa VR, Blocks SM, Brown WR. Morphometric assessment of collagen accumulation in germinal matrix vessels of premature human neonates. Neuropathol Appl Neurobiol. 2005;31:181–90.

    PubMed  Google Scholar 

  12. Reddi AH, Gay R, Gay S, Miller EJ. Transitions in collagen types during matrix-induced cartilage, bone, and bone marrow formation. Proc Natl Acad Sci USA. 1977;74:5589–92.

    PubMed  Google Scholar 

  13. Carter DH, Sloan P, Aaron E. Immunolocalization of collagen types I, III tenascin, and fibronectin in intramembranous bone. J Histochem Cytochem. 1991;39:599–606.

    PubMed  Google Scholar 

  14. Cournil I, Leblond CP, Pomponio J, Hand AR, Sederlof L, Martin GR. Immunohistochemical localization of procollagens. I. Light microscopic distribution of procollagen I, III and IV antigenicity in the rat incisor tooth by the indirect peroxidase anti-peroxidase method. J Histochem Cytochem. 1979;27:1059–69.

    PubMed  Google Scholar 

  15. Tung PS, Domenicucci C, Wasi S, Sodek J. Specific immunohistochemical localization of osteonectin and collagen type I and III in fetal and adult porcine dental tissue. J Histochem Cytochem. 1985;33:531–40.

    PubMed  Google Scholar 

  16. Takita K, Ohsaki Y, Nakata M, Kurisu K. Immunofluorescence localization of type I and type III collagens and fibronectin in mouse dental tissue in late development and during molar eruption. Arch Oral Biol. 1987;32:273–9.

    PubMed  Google Scholar 

  17. Xu LX, Ohsaki Y, Nagata K, Kurisu K. Immunohistochemical studies on the distribution and age-related changes of type I and III collagen in the oral mucosa of mice. J Dent Res. 1993;72:1336–43.

    PubMed  Google Scholar 

  18. Iwasaki S, Aoyagi H, Yoshizawa H. Immunohistochemical detection of epidermal growth factor and epidermal growth factor receptor in the lingual mucosa of rats during the morphogenesis of filiform papillae. Acta Histochem. 2007;109:37–44.

    PubMed  Google Scholar 

  19. Mayor HD, Hampton JC, Rosario B. A simple method for removing the resin from epoxy-embedded tissue. J Cell Biol. 1961;9:909–10.

    Google Scholar 

  20. Shi S-R, Key ME, Karla KL. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhanced method for immunohistochemical staining based on microwave heating of tissue sections. J Histochem Cytochem. 1991;39:741–8.

    PubMed  Google Scholar 

  21. Mbiene JP, Roberts JD. Distribution of keratin 8-containing cell clusters in mouse embryonic tongue: Evidence for a prepattern for taste bud development. J Comp Neurol. 2003;457:111–22.

    PubMed  Google Scholar 

  22. Linsenmayer TF. Collagen. In: Hay ED, editor. Cell biology of extracellular matrix. New York: Plenum; 1981. p. 5–37.

    Google Scholar 

  23. Keene DR, Sakai LY, Bächinger HP, Burgeson RE. Type III collagen can be present on banded collagen fibrils regardless of fibril diameter. J Cell Biol. 1987;105:2393–402.

    PubMed  Google Scholar 

  24. Iwasaki S, Asami T, Wanichanon C, Yoshizawa H, Aoyagi H. Immunohistochemical analysis of type III collagen expression in the lingual mucosa of rats during organogenesis of the tongue. Odontology. 2008;96:12–20.

    PubMed  Google Scholar 

  25. Aoyagi H, Asami T, Yoshizawa H, Wanichanon C, Iwasaki S. Newly developed technique for dual localization of keratins 13 and 14 by fluorescence immunohistochemistry. Acta Histochemistry. 2008;110:324–32.

    Google Scholar 

  26. Jonker L, Kist R, Aw A, Wappler I, Peters H. Pax9 is required for filiform papilla development and suppresses skin-specific differentiation of the mammalian tongue epithelium. Mech Develop. 2004;121:1313–22.

    Google Scholar 

  27. Iwasaki S, Aoyagi H, Asami T. Expression of keratin 18 in the periderm cells of the lingual epithelium of fetal rats: visualization by fluorescence immunohistochemistry and differential interference contrast microscopy. Odontology. 2006;94:64–8.

    PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to Professor T. Kimura, Department of Oral Pharmacology, The Nippon Dental University School of Life Dentistry at Niigata, for his encouragement and helpful support. This research was supported by Research Promotion Grants (nos. NDUF-07-01, NDUF-07-11 and NDUF-08-18) from the Nippon Dental University.

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Authors and Affiliations

  1. Advanced Research Center, The Nippon Dental University School of Life Dentistry at Niigata, 1-8 Hamaura-cho, Chuo-ku, Niigata, 951-8580, Japan

    Shin-ichi Iwasaki & Hidekazu Aoyagi

  2. Department of Biology, Matsumoto Dental University School of Dentistry, 80 Hirookagouhara, Shiojiri, Nagano, 399-0781, Japan

    Hideki Yoshizawa

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  1. Shin-ichi Iwasaki
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  2. Hideki Yoshizawa
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  3. Hidekazu Aoyagi
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Correspondence to Shin-ichi Iwasaki.

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Iwasaki, Si., Yoshizawa, H. & Aoyagi, H. Localization of type III collagen in the lingual mucosa of rats during the morphogenesis of circumvallate papillae. Odontology 100, 10–21 (2012). https://doi.org/10.1007/s10266-011-0020-7

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  • DOI: https://doi.org/10.1007/s10266-011-0020-7

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