Skip to main content

Advertisement

SpringerLink
Log in

The Ca2+-binding protein calretinin is selectively enriched in a subpopulation of the epithelial rests of Malassez

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

Abstract

During tooth development, the inner and outer enamel epithelia fuse by mitotic activity to produce a bilayered epithelial sheath termed Hertwig’s epithelial root sheath (HERS). The epithelial rests of Malassez (ERM) are the developmental residues of HERS and remain in the adult periodontal ligament (PDL). Although the cellular regulation of the Ca2+-binding proteins parvalbumin, calbindin-D28k, and calretinin has been reported in the inner and outer enamel epithelia during tooth development, an involvement of Ca2+-binding proteins in the ERM has not so far been characterized. Among the three Ca2+-binding proteins tested (calbindin D28k, parvalbumin, calretinin), we have only been able to detect calretinin in a subpopulation of adult rat molar ERM, by using quantitative immunohistochemical and confocal immunofluorescence techniques. TrkA (a marker for ERM) is present in numerous epithelial cell clusters, whereas calretinin has been localized in the cytosol and perinuclear region of a subpopulation of TrkA-positive cells. We conclude that, in inner and outer enamel epithelial cells, Ca2+ is regulated by calbindin, parvalbumin, and calretinin during tooth development, whereas in the ERM of adult PDL, Ca2+ is regulated only by calretinin. The expression of Ca2+-binding proteins is restricted in a developmental manner in the ERM.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Berdal A, Balmain N, Thornasset M, Breiher A, Hotton D, Cuisinier-Gleizes P, Mathieu H (1989) Calbindins-D 9kDa and 28kDa and enamel secretion in vitamin D-deficient and control rats. Connect Tissue Res 22:165–171

    Article  CAS  PubMed  Google Scholar 

  • Berdal A, Nanci A, Smith CE, Ahluwallia JP, Thomasset M, Cuisinier-Gleizes P, Mathieu H (1991) Differential expression of calbindin-D 28kDa in rat incisor ameloblasts throughout enamel development. Anat Rec 230:149–163

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signaling. Nat Rev Mol Cell Biol 1:11–21

    Article  CAS  PubMed  Google Scholar 

  • Berchtold MW, Brinkmeier H, Muntener M (2000) Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 80:1215–1265

    CAS  PubMed  Google Scholar 

  • Bosshardt DD (2005) Are cementoblasts a subpopulation of osteoblasts or a unique phenotype? J Dent Res 84:390–406

    Article  CAS  PubMed  Google Scholar 

  • Bosshardt DD, Nanci A (1997) Immunodetection of enamel- and cementum-related (bone) proteins at the enamel-free area and cervical portion of the tooth in rat molars. J Bone Miner Res 12:367–379

    Article  CAS  PubMed  Google Scholar 

  • Bosshardt DD, Nanci A (1998) Immunodetection of epithelial and mesenchymal matrix constitutes in association with inner enamel epithelial cells. J Histochem Cytochem 46:135–142

    CAS  PubMed  Google Scholar 

  • Bosshardt DD, Schroeder HE (1996) Cementogenesis reviewed: a comparison between human premolars and rodent molars. Anat Rec 245:267–292

    Article  CAS  PubMed  Google Scholar 

  • Buchner A, Sciubba JJ (1987) Peripheral epithelial odontogenic tumors: a review. Oral Surg Oral Med Oral Pathol 63:688–697

    Article  CAS  PubMed  Google Scholar 

  • Celio MR, Heizmann CW (1982) Calcium-binding protein parvalbumin is associated with fast contracting muscle fibers. Nature 297:504–506

    Article  CAS  PubMed  Google Scholar 

  • Celio MR, Norman AW, Heizmann CW (1984) Vitamin-D-dependent calcium-binding-protein and parvalbumin occur in bones and teeth. Calcif Tissue Int 36:129–130

    Article  CAS  PubMed  Google Scholar 

  • Celio MR, Baier W, Schärer L, Viragh PA de, Gerday C (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81–86

    Article  CAS  PubMed  Google Scholar 

  • Celio MR, Baier W, Schärer L, Gregersen HJ, Viragh PA de, Norman AW (1990) Monoclonal antibodies directed against the calcium binding protein calbindin D-28k. Cell Calcium 11:599–602

    Article  CAS  PubMed  Google Scholar 

  • Cerri PS, Freymüller E, Katchburian E (2000) Apoptosis in the early developing periodontium of rat molars. Anat Rec 258:136–144

    Article  CAS  PubMed  Google Scholar 

  • Coleman H, Altini M, Ali H, Doglioni C, Favia G, Maiorano E (2001) Use of calretinin in the differential diagnosis of unicystic ameloblastomas. Histopathology 38:312–317

    Article  CAS  PubMed  Google Scholar 

  • Davideau JL, Celio MR, Hotton D, Berdal A (1993) Developmental pattern and subcellular localization of parvalbumin in the rat tooth germ. Arch Oral Biol 38:707–715

    Article  CAS  PubMed  Google Scholar 

  • Doyle KL, Kazda A, Hort Y, McKay SM, Oleskevich S (2007) Differentiation of adult mouse olfactory precursor cells into hair cells in vitro. Stem Cells 25:621–627

    Article  CAS  PubMed  Google Scholar 

  • Gander JC, Gotzos V, Fellay B, Schwaller B (1996) Inhibition of the proliferative cycle and apoptotic events in WiDr cells after down-regulation of the calcium-binding protein calretinin using antisense oligodeoxynucleotides. Exp Cell Res 225:399–410

    Article  CAS  PubMed  Google Scholar 

  • Goldberg M, Escaig F, Feinberg J, Weinmann S (1987) Ultrastrucutral localization of calmodulin in rat incisor ameloblasts and odontoblasts during the early stages of development. Adv Dent Res 1:227–235

    CAS  PubMed  Google Scholar 

  • Goldberg M, Feinberg J, Rainteau D, Lecolle S, Dedman JR, Glenney JR, Weinmann S (1989) Differential localization of calmodulin, the 67 kDa calcimedin and calpactin II in secretory ameloblasts. Connect Tissue Res 22:157–164

    Article  CAS  PubMed  Google Scholar 

  • Goldberg M, Feinberg J, Lecolle S, Kaetzel MA, Rainteau D, Lessard JL, Dedman JR, Weinmann S (1991) Co-distribution of annexin VI and actin in secretory ameloblasts and odontoblasts of rat incisor. Cell Tissue Res 263:81–89

    Article  CAS  PubMed  Google Scholar 

  • Gotzos V, Schwaller B, Hetzel N, Bustos-Castillo M, Celio MR (1992) Expression of the calcium binding protein calretinin in WiDr cells and its correlation to their cell cycle. Exp Cell Res 202:292–302

    Article  CAS  PubMed  Google Scholar 

  • Grzesik WJ, Cheng H, Oh JS, Kuznetsov SA, Mankani MH, Uzawa K, Robey PG, Yamauchi M (2000) Cementum-forming cells are phenotypically distinct from bone-forming cells. J Bone Miner Res 15:52–59

    Article  CAS  PubMed  Google Scholar 

  • Hamamoto Y, Hamamoto N, Nakajima T, Ozawa H (1998) Morphological changes of epithelial rests of Malassez in rat molars induced by local administration of N-methylnitrosourea. Arch Oral Biol 43:899–906

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa N, Kawaguchi H, Ogawa T, Uchida T, Kurihara H (2003) Immunohistochemical characteristics of epithelial cell rests of Malassez during cementum reapir. J Periodontal Res 38:51–56

    Article  PubMed  Google Scholar 

  • Heizmann CW (1993) Calcium signaling in the brain. Acta Neurobiol Exp (Warsz) 53:15–23

    CAS  Google Scholar 

  • Hubbard MJ (1996) Abundant calcium homeostasis machinery in rat dental enamel cells. Up-regulation of calcium store proteins during enamel mineralization implicates the endoplasmic reticulum in calcium transcytosis. Eur J Biochem 239:611–623

    Article  CAS  PubMed  Google Scholar 

  • Hubbard MJ (2000) Calcium transport across the dental enamel epithelium. Crit Rev Oral Biol Med 11:437–466

    Article  CAS  PubMed  Google Scholar 

  • Hubbard MJ, Bradley MP, Kardos TB, Forrester IT (1981) Calmodulin-like activity in a mineralizing tissue: the rat molar tooth germ. Calcif Tissue Int 33:545–548

    Article  CAS  PubMed  Google Scholar 

  • Korfage JAM, Koolstra JH, Langenbach GEJ, Eijden TMGJ van (2005a) Fiber-type composition of the human jaw muscles. (Part 1) Origin and functional significance of fiber-type diversity. J Dent Res 84:774–783

    Article  CAS  PubMed  Google Scholar 

  • Korfage JAM, Koolstra JH, Langenbach GEJ, Eijden TMGJ van (2005b) Fiber-type composition of the human jaw muscles. (Part 2) Role of hybrid fibers and factors responsible for inter-individual variation. J Dent Res 84:784–793

    Article  CAS  PubMed  Google Scholar 

  • Korkmaz Y, Bloch W, Behrends S, Schroeder H, Addicks K, Baumann MA (2004) NO-cGMP signaling molecules in the rat epithelial rests of Malassez. Eur J Oral Sci 112:55–60

    Article  CAS  PubMed  Google Scholar 

  • Korkmaz Y, Bloch W, Addicks K, Schneider K, Baumann MA, Raab WH (2005) The basal phosphorylation sites of endothelial nitric oxide synthase at serine (Ser) 1177, Ser116, and threonine (Thr) 495 in rat molar epithelial rests of Malassez. J Periodontol 76:1513–1519

    Article  CAS  PubMed  Google Scholar 

  • Korkmaz Y, Bloch W, Klinz F-J, Kübler AC, Schneider K, Zimmer S, Addicks K, Raab WH-M (2009) The constitutive activation of extracellular signal-regulated kinase 1 and 2 in periodontal ligament nerve fibers. J Periodontol 80:850–859

    Article  CAS  PubMed  Google Scholar 

  • Korkmaz Y, Klinz F-J, Moghbeli M, Addicks K, Raab WH-M, Bloch W (2010) The masticatory contractile load induced expression and activation of Akt1/PKBα in muscle fibers at the myotendinous junction within muscle-tendon-bone unit. J Biomed Biotechnol 2010:163203

    PubMed  Google Scholar 

  • Linde A (1995) Dentin mineralization and the role of odontoblasts in calcium transport. Connect Tissue Res 33:163–170

    Article  CAS  PubMed  Google Scholar 

  • Linde A, Lundgren T (1995) From serum to the mineral phase. The role of the odontoblast in calcium transport and mineral formation. Int J Dev Biol 392:213–222

    Google Scholar 

  • MacNeil RL, Thomas HF (1993) Development of the murine peridontium? Role of epithelial root sheath in formation of the periodontal attachment. J Periodontol 64:285–291

    CAS  PubMed  Google Scholar 

  • Magloire H, Joffre A, Azerad J, Lawson DEM (1988) Localization of 28kDa calbindin in human odontoblasts. Cell Tissue Res 254:341–346

    Article  CAS  PubMed  Google Scholar 

  • McCulloch CA, Melcher AH (1983) Continuous labelling of the periodontal ligament of mice. J Periodontal Res 18:231–241

    Article  CAS  PubMed  Google Scholar 

  • Mistry D, Altini M, Coleman HG, Ali H, Maiorano E (2001) The spatial and temporal of calretinin in developing rat molars (Rattus norvegicus). Arch Oral Biol 46:973–981

    Article  CAS  PubMed  Google Scholar 

  • Ochi K, Wakisaka S, Youn SH, Hanada K, Maeda T (1997) Calretinin-like immunoreactivity in the Ruffini endings, slowly adapting mechanoreceptors, of the periodontal ligament of the rat incisor. Brain Res 769:183–187

    Article  CAS  PubMed  Google Scholar 

  • Onishi T, Ooshima T, Sobue S, Tabata MJ, Maeda T, Kurisu K, Wakisaka S (1999) Immunohistochemical localization of calbindin D28k during root formation of rat molar teeth. Cell Tissue Res 297:503–512

    Article  CAS  PubMed  Google Scholar 

  • Onishi T, Okawa R, Murakami H, Ogawa T, Ooshima T, Wakisaka S (2003) Immunolocalization of calbindin D28k and vitamin D receptor during root formation of murine molar teeth. Anat Rec 273A:700–704

    Article  CAS  Google Scholar 

  • Quyang H, McCauley LK, Berry JE, Saygin NE, Tokiyasu Y, Somerman MJ (2000) Parathyroid hormone-related protein regulates extracellular matrix gene expression in cementoblasts and inhibits cementoblast-mediated mineralization in vitro. J Bone Miner Res 15:2140–2153

    Article  Google Scholar 

  • Rogers JH (1987) Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J Cell Biol 105:1343–1353

    Article  CAS  PubMed  Google Scholar 

  • Schiffmann SN, Cheron G, Lohof A, d’Alcantara P, Meyer M, Parmentier M, Schurmans S (1999) Impaired motor coordination and Purkinje cell excitability in mice lacking calretinin. Proc Natl Acad Sci USA 96:5257–5262

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B (2009) The continuing disappearance of “pure” Ca2+ buffers. Cell Mol Life Sci 66:275–300

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B, Buchwald P, Blümcke I, Celio MR, Hunziker W (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639–648

    Article  CAS  PubMed  Google Scholar 

  • Shinmura Y, Tsuchiya S, Hata K-I, Honda MJ (2008) Quiescent epithelial cell rests of Malassez can differentiate into ameloblast-like cells. J Cell Physiol 217:728–738

    Article  CAS  PubMed  Google Scholar 

  • Talic NF, Evans CA, Daniel JC, Zaki AE (2003) Proliferation of epithelial rests of Malassez during experimental tooth movement. Am J Orthod Dentofacial Orthop 123:527–533

    Article  PubMed  Google Scholar 

  • Ten Cate AR (1972) The epithelial cell rests of Malassez and the genesis of the dental cyst. Oral Surg 34:956–964

    Article  PubMed  Google Scholar 

  • Thomas HF (1995) Root formation. Int J Dev Biol 39:231–237

    CAS  PubMed  Google Scholar 

  • Trowbridge HO, Shibata F (1967) Mitotic activity in epithelial rests of Malassez. Periodontics 5:109–112

    CAS  PubMed  Google Scholar 

  • Wesselink PR, Beertsen W (1993) The prevalence and distribution of rests of Malassez in the mouse molar and their possible role in repair and maintenance of the periodontal ligament. Arch Oral Biol 38:399–403

    Article  CAS  PubMed  Google Scholar 

  • Yamashiro T, Fujiyama K, Fukunaga T, Wang Y, Takano-Yamamoto T (2000) Epithelial rests of Malassez express immunoreactivity of TrkA and its distribution is regulated by sensory nerve innervation. J Histochem Cytochem 48:979–984

    CAS  PubMed  Google Scholar 

  • Zeichner-David M, Oishi K, Su Z, Zakartchenko V, Chen LS, Arzate H, Bringas P Jr (2003) Role of Hertwig’s epithelial root sheath cells in tooth root development. Dev Dyn 228:651–663

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann L, Schwaller B (2002) Monoclonal antibodies recognizing epitopes of calretinins: dependence on Ca2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium 31:13–25

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The technical assistance of E. Janßen, J. Kozlowski, and Ch. Hoffmann is gratefully appreciated.

Author information

Authors and Affiliations

  1. Department of Operative Dentistry, Periodontics and Endodontics, Heinrich Heine University, Moorenstrasse 5, 40225, Düsseldorf, Germany

    Yüksel Korkmaz, Thomas Beikler, Thorsten Blauhut, Kurt Schneider & Wolfgang H-M Raab

  2. Department I of Anatomy, University of Cologne, Cologne, Germany

    Franz-Josef Klinz & Klaus Addicks

  3. Department of Molecular and Cellular Sports Medicine, German Sports University, Cologne, Germany

    Wilhelm Bloch

Authors
  1. Yüksel Korkmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Franz-Josef Klinz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Beikler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thorsten Blauhut
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kurt Schneider
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Klaus Addicks
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wilhelm Bloch
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Wolfgang H-M Raab
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yüksel Korkmaz.

Additional information

This study was supported by the Forschungskommission of the Heinrich Heine University of Düsseldorf.

The authors state no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Korkmaz, Y., Klinz, FJ., Beikler, T. et al. The Ca2+-binding protein calretinin is selectively enriched in a subpopulation of the epithelial rests of Malassez. Cell Tissue Res 342, 391–400 (2010). https://doi.org/10.1007/s00441-010-1076-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-010-1076-3

Keywords

Search

Navigation