Skip to main content

Advertisement

Log in

Characteristics of resident dendritic cells in various regions of rat periodontal ligament

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

In the periodontal ligament (PDL) of normal rat molars, a considerable number of dendritic cells (DCs) are distributed as resident immunocompetent cells. We have hypothesized that the resident type of DCs can alter their morphology and phenotype to adapt to the microenvironment of the PDL. Thus, we have compared the characteristics of DCs in various regions of rat PDL by immunoelectron microscopy and gene expression analysis by means of reverse transcription/polymerase chain reaction. DCs in the periapical region show immature characteristics, i.e., small round profiles and few organelles. In the mesial region, which is the most stable area in the PDL, the density of DCs is the highest. DCs in the furcal region show the characteristics of activated antigen-presenting cells, i.e., CD86high expression, electron-dense lysosomes, and cell-to-cell contacts with lymphocytes. When the PDL is bacterially challenged by pulp exposure, the number of CD86+ DCs and contacts with lymphocytes increase in the furcal region. Gene expression analysis for the furcal region has also shown the up-regulation of the major histocompatibility complex class II alpha-chain, CD83, CD86, and the antigen-presenting cell-lectin-like receptor A1. Thus, we have demonstrated heterogeneity in resident DCs. This may be associated with the difference in DCs regarding their state of maturation/activation, which may further reflect microenvironmental differences such as the amount of external antigens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Azuma M, Ito D, Yagita H, Okumura K, Phillips JH, Lanier LL, Somoza C (1993) B70 antigen is a second ligand for CTLA-4 and CD28. Nature 366:76–79

    Article  PubMed  CAS  Google Scholar 

  • Austyn JM (1987) Lymphoid dendritic cells. Immunology 62:161–170

    PubMed  CAS  Google Scholar 

  • Barbe E, Damoiseaux JG, Döpp EA, Dijkstra CD (1990) Characterization and expression of the antigen present on resident rat macrophages recognized by monoclonal antibody ED2. Immunobiology 182:88–99

    PubMed  CAS  Google Scholar 

  • Bonasio R, Andrian UH von (2006) Generation, migration and function of circulating dendritic cells. Curr Opin Immunol 18:503–511

    Article  PubMed  CAS  Google Scholar 

  • Cao W, Lee SH, Lu J (2005) CD83 is preformed inside monocytes, macrophages and dendritic cells, but it is only stably expressed on activated dendritic cells. Biochem J 385:85–93

    Article  PubMed  CAS  Google Scholar 

  • Cella M, Engering A, Pinet V, Pieters J, Lanzavecchia A (1997) Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 388:782–787

    Article  PubMed  CAS  Google Scholar 

  • Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES (2005) Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307:1630–1634

    Article  PubMed  CAS  Google Scholar 

  • Flornes LM, Bryceson YT, Spurkland A, Lorentzen JC, Dissen E, Fossum S (2004) Identification of lectin-like receptors expressed by antigen presenting cells and neutrophils and their mapping to a novel gene complex.Immunogenetics 56:506–517

    Article  CAS  Google Scholar 

  • Freeman GJ, Gribben JG, Boussioitis VA, Ng JW, Restivo VA, Lomdard LA, Gray GS, Nadler LM (1993) Cloning of B7-2: a CTLA-4 counter-receptor that costimulates human T cell proliferation. Science 262:909–911

    Article  PubMed  CAS  Google Scholar 

  • Gemmell E, Carter CL, Hart DN, Drysdale KE, Seymour GJ (2002) Antigen-presenting cells in human periodontal disease tissues. Oral Microbiol Immunol 17:388–393

    Article  PubMed  CAS  Google Scholar 

  • Henderson RA, Watkins SC, Flynn JL (1997) Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J Immunol 159:635–643

    PubMed  CAS  Google Scholar 

  • Inaba K, Inaba M, Naito M, Steinman RM (1993) Dendritic cell progenitors phagocytose particulates, including bacillus Calmette-Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. J Exp Med 178:479–488

    Article  PubMed  CAS  Google Scholar 

  • Jotwani R, Cutler CW (2003) Multiple dendritic cell (DC) subpopulations in human gingiva and association of mature DCs with CD4+ T-cells in situ. J Dent Res 82:736–741

    Article  PubMed  CAS  Google Scholar 

  • Kan L, Okiji T, Kaneko T, Suda H (2001) Localization and density of myeloid leucocytes in the periodontal ligament of normal rat molars. Arch Oral Biol 46:509–520

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Okiji T, Kan L, Suda H, Takagi M (2001a) An immunoelectron microscopic study of class II major histocompatibility complex molecule-expressing macrophages and dendritic cells in experimental rat periapical lesions. Arch Oral Biol 46:713–720

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Okiji T, Kan L, Takagi M, Suda H (2001b) Ultrastructural analysis of MHC class II molecule-expressing cells in experimentally-induced periapical lesion in the rat. J Endod 27:337–342

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Okiji T, Takagi M, Suda H (2004) Ultrastructure and distribution of macrophages and dendritic cells in rat induced periapical lesion. Jpn J Conservat Dent 47:328–334

    Google Scholar 

  • Kaneko T, Okiji T, Zhao LY, Esgeurra R, Suda H (2007a) Heterogeneity of dendritic cells in rat apical periodontitis. Cell Tissue Res (in press)

  • Kaneko T, Zhang Z, Mantellini M, Karl E, Zeitlin B, Verhaegen M, Soengas MS, Lingen M, Strieter RM, Nunez G, Nör JE (2007b) Bcl-2 orchestrates a crosstalk between endothelial and tumor cells that promotes tumor growth. Cancer Res 67:9685–9693

    Article  CAS  Google Scholar 

  • Kawahara I, Takano Y, Sato O, Maeda T, Kannari K (1992) Histochemical and immunohistochemical demonstration of macrophages and dendritic cells in the lingual periodontal ligament of rat incisors. Arch Histol Cytol 55:211–217

    PubMed  CAS  Google Scholar 

  • Klinkert WE (1990) Lymphoid dendritic accessory cells of the rat. Immunol Rev 117:103–120

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi M, Asano H, Fujita Y, Hoshino T (1987) Development of ATPase-positive, immature Langerhans cells in the fetal mouse epidermis and their maturation during the early postnatal period. Cell Tissue Res 248:315–322

    Google Scholar 

  • Kummer W, Stommel C, Grau V (2004) MHC class II antigen-expressing cells in cardiac ganglia of the rat. Cell Tissue Res 319:37–48

    Article  PubMed  CAS  Google Scholar 

  • Lappin MB, Kimber I, Norval M (1996) The role of dendritic cells in cutaneous immunity. Arch Dermatol Res 288:109–121

    PubMed  CAS  Google Scholar 

  • Lekic P, McCulloch CA (1996) Periodontal ligament cell population: the central role of fibroblasts in creating a unique tissue. Anat Rec 245:327–341

    Article  PubMed  CAS  Google Scholar 

  • Nakamura K, Sahara N, Deguchi T (2001) Temporal changes in the distribution and number of macrophage-lineage cells in the periodontal membrane of the rat molar in response to experimental tooth movement. Arch Oral Biol 46:593–607

    Article  PubMed  CAS  Google Scholar 

  • Okiji T, Kawashima N, Kosaka T, Matsumoto A, Kobayashi C, Suda H, Sunada I (1990) Immunohistochemical localization of immunocompetent cells in rat molar pulp and periapical tissues. Jpn J Conservat Dent 33:1398–1405

    Google Scholar 

  • Okiji T, Kawashima N, Kosaka T, Matsumoto A, Kobayashi C, Suda H (1992) An immunohistochemical study of the distribution of immunocompetent cells, especially macrophages and Ia antigen-expressing cells of heterogeneous populations, in normal rat molar pulp. J Dent Res 71:1196–1202

    PubMed  CAS  Google Scholar 

  • Pelletier M, Tautu C, Landry D, Montplaisir S, Chartrand C, Perreault C (1986) Characterization of human thymic dendritic cells in culture. Immunology 58:263–270

    PubMed  CAS  Google Scholar 

  • Pierre P, Turley SJ, Gatti E, Hull M, Meltzer J, Mirza A, Inaba K, Steinman RM, Mellman I (1997) Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388:787–792

    Article  PubMed  CAS  Google Scholar 

  • Randolph GJ, Angeli V, Swartz MA (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 5:617–628

    Article  PubMed  CAS  Google Scholar 

  • Rescigno M, Winzler C, Delia D, Mutini C, Lutz M, Ricciardi-Castagnoli P (1997) Dendritic cell maturation is required for initiation of the immune response. J Leukoc Biol 61:415–421

    PubMed  CAS  Google Scholar 

  • Robey E, Allison JP (1995) T-cell activation: integration of signals from the antigen receptor and costimulatory molecules. Immunol Today 16:306–309

    Article  PubMed  CAS  Google Scholar 

  • Steinman RM (1991) The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271–296

    Article  PubMed  CAS  Google Scholar 

  • Sallusto F, Lanzavecchia A (1999) Mobilizing dendritic cells for tolerance, priming, and chronic inflammation. J Exp Med 189:611–614

    Article  PubMed  CAS  Google Scholar 

  • Takahashi K, Asagoe K, Zaishun J, Yanai H, Yoshino T, Hayashi K, Akagi T (1998) Heterogeneity of dendritic cells in human superficial lymph node. In vitro maturation of immature dendritic cells into mature or activated interdigitating reticulum cells. Am J Pathol 153:745–755

    PubMed  CAS  Google Scholar 

  • Vandevska-Radunovic V, Hals Kvinnsland I, Kvinnsland S, Jonsson R (1997) Immunocompetent cells in rat periodontal ligament and their recruitment incident to experimental orthodontic tooth movement. Eur J Oral Sci 105:36–44

    Article  PubMed  CAS  Google Scholar 

  • Wilson NS, El-Sukkari D, Villadangos JA (2004) Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis. Blood 103:2187–2195

    Article  PubMed  CAS  Google Scholar 

  • Zhao LY, Kaneko T, Okiji T, Takagi M, Suda H (2006) Immunoelectron microscopic analysis of CD11c-positive dendritic cells in the periapical region of the periodontal ligament of rat molars. J Endod 32:1164–1167

    Article  PubMed  Google Scholar 

  • Zhou LJ, Tedder TF (1995) Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. J Immunol 154:3821–3835

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Jacques E. Nör, Cariology, Restorative Sciences, and Endodontics, School of Dentistry, University of Michigan, for his technical advice regarding RT-PCR.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomoatsu Kaneko.

Additional information

This study was supported by Grants-in-Aid for Scientific Research (nos. 17390508 and 19659496 to T.O. and no. 18791393 to T.K.) from the Japan Society for the Promotion of Sciences.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaneko, T., Okiji, T., Kaneko, R. et al. Characteristics of resident dendritic cells in various regions of rat periodontal ligament. Cell Tissue Res 331, 413–421 (2008). https://doi.org/10.1007/s00441-007-0539-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-007-0539-7

Keywords

Navigation