Skip to main content

Advertisement

SpringerLink
Log in

Essential role of ADAM28 in regulating the proliferation and differentiation of human dental papilla mesenchymal cells (hDPMCs)

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Dental papilla mesenchymal cells (DPMCs) have been supposed to possess the relatively independent and critical role for tooth development and morphogenesis. Here, we characterized the role of ADAM28, a member of a disintegrin and metalloproteinase (ADAM) family, in the regulative mechanisms of odontogenic capability of hDPMCs. Immunofluorescence staining showed the ubiquitous expression of ADAM28 in multiple human dental mesenchymal and epithelial cells. After confirming the effect of eukaryotic expression plasmid containing ADAM28 coding region and ADAM28 antisense oligodeoxynucleotide (AS-ODN), we respectively transfected them into hDPMCs and observed the biological markers for proliferation and differentiation. Overexpression of ADAM28 favored the proliferation and lineage-specific differentiation of hDPMCs, while blockage of ADAM28 exerted the opposite effects and induced apoptosis. These results identified an unrecognized hypothesis that ADAM28 may function as positive regulator of growth and differentiation of hDPMCs and act as an important molecule mediating reciprocal epithelial–mesenchymal signaling during tooth organ development.

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

  • Bei M, Maas R (1998) FGFs and BMP4 induce both Msx1-independent and Msx1-dependent signaling pathways in early tooth development. Development 125:4325–4333

    PubMed  CAS  Google Scholar 

  • Blobel CP (2005) ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 6:32–43

    Article  PubMed  CAS  Google Scholar 

  • Butler WT (1995) Dentin matrix proteins and dentinogenesis. Connect Tissue Res 33:59–65

    Article  PubMed  CAS  Google Scholar 

  • Chai Y, Zhao J, Mogharei A, Xu B, Bringas P Jr, Shuler C, Warburton D (1999) Inhibition of transforming growth factor-beta type II receptor signaling accelerates tooth formation in mouse first branchial arch explants. Mech Dev 86:63–74

    Article  PubMed  CAS  Google Scholar 

  • Cobourne MT, Sharpe PT (2005) Sonic hedgehog signaling and the developing tooth. Curr Top Dev Biol 65:255–287

    Article  PubMed  CAS  Google Scholar 

  • Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97:13625–13630

    Article  PubMed  CAS  Google Scholar 

  • Howard L, Maciewicz RA, Blobel CP (2000) Cloning and characterization of ADAM28: evidence for autocatalytic pro-domain removal and for cell surface localization of mature ADAM28. Biochem J 348(Pt 1):21–27

    Article  PubMed  CAS  Google Scholar 

  • Howard L, Zheng Y, Horrocks M, Maciewicz RA, Blobel C (2001) Catalytic activity of ADAM28. FEBS Lett 498:82–86

    Article  PubMed  CAS  Google Scholar 

  • Ikeda E, Hirose M, Kotobuki N, Shimaoka H, Tadokoro M, Maeda M, Hayashi Y, Kirita T, Ohgushi H (2006) Osteogenic differentiation of human dental papilla mesenchymal cells. Biochem Biophys Res Commun 342:1257–1262

    Article  PubMed  CAS  Google Scholar 

  • Jernvall J, Thesleff I (2000) Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 92:19–29

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi H, Sawada T, Yanagisawa T (1996) Effects of a functional agar surface on in vitro dentinogenesis induced in proteolytically isolated, agar-coated dental papillae in rat mandibular incisors. Arch Oral Biol 41:871–883

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi H, Amano H, Yamada S (2001) Putative role of basement membrane for dentinogenesis in the mesenchyme of murine dental papillae in vitro. Cell Tissue Res 303:93–107

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi H, Suzuki K, Sakai N, Yamada S (2004) Odontoblasts induced from mesenchymal cells of murine dental papillae in three-dimensional cell culture. Cell Tissue Res 317:173–185

    Article  PubMed  CAS  Google Scholar 

  • Kollar EJ, Baird GR (1969) The influence of the dental papilla on the development of tooth shape in embryonic mouse tooth germs. J Embryol Exp Morphol 21:131–148

    PubMed  CAS  Google Scholar 

  • Kollar EJ, Baird GR (1970) Tissue interactions in embryonic mouse tooth germs. II. The inductive role of the dental papilla. J Embryol Exp Morphol 24:173–186

    PubMed  CAS  Google Scholar 

  • Lesot H, Vonesch JL, Peterka M, Turecková J, Peterková R, Ruch JV (1996) Mouse molar morphogenesis revisited by three-dimensional reconstruction. II. Spatial distribution of mitoses and apoptosis in cap to bell staged first and second upper molar teeth. Int J Dev Biol 40:1017–1031

    PubMed  CAS  Google Scholar 

  • Lisi S, Peterková R, Peterka M, Vonesch JL, Ruch JV, Lesot H (2003) Tooth morphogenesis and pattern of odontoblast differentiation. Connect Tissue Res 44(Suppl 1):167–170

    Article  PubMed  Google Scholar 

  • Matalova E, Tucker AS, Sharpe PT (2004) Death in the life of a tooth. J Dent Res 83:11–16

    PubMed  CAS  Google Scholar 

  • McCright B (2003) Notch signaling in kidney development. Curr Opin Nephrol Hypertens 12:5–10

    Article  PubMed  CAS  Google Scholar 

  • Mitsiadis TA, Lardelli M, Lendahl U, Thesleff I (1995) Expression of Notch 1, 2 and 3 is regulated by epithelial–mesenchymal interactions and retinoic acid in the developing mouse tooth and associated with determination of ameloblast cell fate. J Cell Biol 130:407–418

    Article  PubMed  CAS  Google Scholar 

  • Mitsiadis TA, Hirsinger E, Lendahl U, Goridis C (1998) Delta-notch signaling in odontogenesis: correlation with cytodifferentiation and evidence for feedback regulation. Dev Biol 204:420–431

    Article  PubMed  CAS  Google Scholar 

  • Mitsiadis TA, Regaudiat L, Gridley T (2005) Role of the Notch signalling pathway in tooth morphogenesis. Arch Oral Biol 50:137–140

    Article  PubMed  CAS  Google Scholar 

  • Mitsui Y, Mochizuki S, Kodama T, Shimoda M, Ohtsuka T, Shiomi T, Chijiiwa M, Ikeda T, Kitajima M, Okada Y (2006) ADAM28 is overexpressed in human breast carcinomas: implications for carcinoma cell proliferation through cleavage of insulin-like growth factor binding protein-3. Cancer Res 66:9913–9920

    Article  PubMed  CAS  Google Scholar 

  • Morsczeck C, Moehl C, Götz W, Heredia A, Schäffer TE, Eckstein N, Sippel C, Hoffmann KH (2005) In vitro differentiation of human dental follicle cells with dexamethasone and insulin. Cell Biol Int 29:567–575

    Article  PubMed  CAS  Google Scholar 

  • Ohtsuka T, Shiomi T, Shimoda M, Kodama T, Amour A, Murphy G, Ohuchi E, Kobayashi K, Okada Y (2006) ADAM28 is overexpressed in human non-small cell lung carcinomas and correlates with cell proliferation and lymph node metastasis. Int J Cancer 118:263–273

    Article  PubMed  CAS  Google Scholar 

  • Pispa J, Thesleff I (2003) Mechanisms of ectodermal organogenesis. Dev Biol 262:195–205

    Article  PubMed  CAS  Google Scholar 

  • Primakoff P, Myles DG (2000) The ADAM gene family: surface proteins with adhesion and protease activity. Trends Genet 16:83–87

    Article  PubMed  CAS  Google Scholar 

  • Radtke F, Wilson A, MacDonald HR (2005) Notch signaling in hematopoiesis and lymphopoiesis: lessons from Drosophila. Bioessays 27:1117–1128

    Article  PubMed  CAS  Google Scholar 

  • Ragnarsson B, Carr G, Daniel JC (1985) Isolation and growth of human periodontal ligament cells in vitro. J Dent Res 64:1026–1030

    PubMed  CAS  Google Scholar 

  • Randall LE, Hall RC (2002) Temperospatial expression of matrix metalloproteinases 1, 2, 3, and 9 during early tooth development. Connect Tissue Res 43:205–211

    Article  PubMed  CAS  Google Scholar 

  • Ruch JV, Lesot H, Bègue-Kirn C (1995) Odontoblast differentiation. Int J Dev Biol 39:51–68

    PubMed  CAS  Google Scholar 

  • Sarkar L, Sharpe PT (2000) Inhibition of Wnt signaling by exogenous Mfrzb1 protein affects molar tooth size. J Dent Res 79:920–925

    Article  PubMed  CAS  Google Scholar 

  • Schmitt R, Lesot H, Vonesch JL, Ruch JV (1999) Mouse odontogenesis in vitro: the cap-stage mesenchyme controls individual molar crown morphogenesis. Int J Dev Biol 43:255–260

    PubMed  CAS  Google Scholar 

  • Schmitt R, Fausser JL, Lesot H, Ruch JV (2000) Effects of hepatocyte growth factor anti-sense oligodeoxynucleotides or met D/D genotype on mouse molar crown morphogenesis. Int J Dev Biol 44:403–408

    PubMed  CAS  Google Scholar 

  • Shiba H, Mouri Y, Komatsuzawa H, Mizuno N, Xu W, Noguchi T, Nakamura S, Sugai M, Kato Y, Kurihara H (2003) Enhancement of alkaline phosphatase synthesis in pulp cells co-cultured with epithelial cells derived from lower rabbit incisors. Cell Biol Int 27:815–823

    Article  PubMed  CAS  Google Scholar 

  • Shigemura N, Kiyoshima T, Kobayashi I, Matsuo K, Yamaza H, Akamine A, Sakai H (1999) The distribution of BrdU- and TUNEL-positive cells during odontogenesis in mouse lower first molars. Histochem J 31:367–377

    Article  PubMed  CAS  Google Scholar 

  • Shteyer A, Gazit D, Binderman I, Bab IA (1987) Hormone-responsive cells derived from human dental papilla: characterization in vitro and in vivo in diffusion chambers. In Vitro Cell Dev Biol 23:15–20

    Article  PubMed  CAS  Google Scholar 

  • Slavkin HC (1995) Antisense oligonucleotides: an experimental strategy to advance a causal analysis of development. Int J Dev Biol 39:123–126

    PubMed  CAS  Google Scholar 

  • Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, Liu H, Gronthos S, Wang CY, Shi S, Wang S (2006) Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 1:e79

    Article  PubMed  CAS  Google Scholar 

  • Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, Huang GT (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34:166–171

    Article  PubMed  Google Scholar 

  • Stein CA (2001) The experimental use of antisense oligonucleotides: a guide for the perplexed. J Clin Invest 108:641–644

    PubMed  CAS  Google Scholar 

  • Tabata MJ, Fujii T, Liu JG, Ohmori T, Abe M, Wakisaka S, Iwamoto M, Kurisu K (2002) Bone morphogenetic protein 4 is involved in cusp formation in molar tooth germ of mice. Eur J Oral Sci 110:114–120

    Article  PubMed  CAS  Google Scholar 

  • Thesleff I, Sharpe P (1997) Signalling networks regulating dental development. Mech Dev 67:111–123

    Article  PubMed  CAS  Google Scholar 

  • Thesleff I, Pispa J (1998) The teeth as models for studies on the molecular basis of the development and evolution of organs. In: Chuong C-M (ed) Molecular basis of epithelial appendage morphogenesis. RG Landes, Austin, pp 157–179

    Google Scholar 

  • Thomas HF, Kollar EJ (1989) Differentiation of odontoblasts in grafted recombinants of murine epithelial root sheath and dental mesenchyme. Arch Oral Biol 34:27–35

    Article  PubMed  CAS  Google Scholar 

  • Tucker A, Sharpe P (2004) The cutting-edge of mammalian development; how the embryo makes teeth. Nat Rev Genet 5:499–508

    Article  PubMed  CAS  Google Scholar 

  • Vaahtokari A, Aberg T, Thesleff I (1996) Apoptosis in the developing tooth: association with an embryonic signaling center and suppression by EGF and FGF-4. Development 122:121–129

    PubMed  CAS  Google Scholar 

  • Vasyutina E, Lenhard DC, Birchmeier C (2007) Notch function in myogenesis. Cell Cycle 6:1451–1454

    PubMed  CAS  Google Scholar 

  • Viriot L, Peterková R, Vonesch JL, Peterka M, Ruch JV, Lesot H (1997) Mouse molar morphogenesis revisited by three-dimensional reconstruction. III. Spatial distribution of mitoses and apoptoses up to bell-staged first lower molar teeth. Int J Dev Biol 41:679–690

    PubMed  CAS  Google Scholar 

  • Yamamoto H, Kim EJ, Cho SW, Jung HS (2003) Analysis of tooth formation by reaggregated dental mesenchyme from mouse embryo. J Electron Microsc (Tokyo) 52:559–566

    Article  CAS  Google Scholar 

  • Yu JH, Shi JN, Deng ZH, Zhuang H, Nie X, Wang RN, Jin Y (2006) Cell pellets from dental papillae can reexhibit dental morphogenesis and dentinogenesis. Biochem Biophys Res Commun 346:116–124

    Article  PubMed  CAS  Google Scholar 

  • Yuan GH, Zhang L, Zhang YD, Fan MW, Bian Z, Chen Z (2008) Mesenchyme is responsible for tooth suppression in the mouse lower diastema. J Dent Res 87:386–390

    PubMed  CAS  Google Scholar 

  • Zhao Z, Wen LY, Jin M, Deng ZH, Jin Y (2006) ADAM28 participates in the regulation of tooth development. Arch Oral Biol 51:996–1005

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the Nature Science Foundation of China (project no. 30572046 and no. 30725042).

Author information

Authors and Affiliations

  1. Research and Development Center for Tissue Engineering, Fourth Military Medical University, 145 West Changle Road, 710032, Xi’an, China

    Zheng Zhao, Liang Tang & Yan Jin

  2. Department of Paediatric Dentistry, School of Stomatology, Fourth Military Medical University, 145 West Changle Road, 710032, Xi’an, China

    Zheng Zhao & Lingying Wen

  3. Department of Stomatology, The 401st Hospital of PLA, 266071, Qing Dao, China

    Zheng Zhao

  4. Department of Otolaryngology, Xijing Hospital, Fourth Military Medical University, 17 West Changle Road, 710032, Xi’an, China

    Zhihong Deng

  5. Department of Oral Histology and Pathology, School of Stomatology, Research and Development Center for Tissue Engineering, Fourth Military Medical University, 145 West Changle Road, 710032, Xi’an, China

    Liang Tang & Yan Jin

Authors
  1. Zheng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liang Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhihong Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lingying Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yan Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Lingying Wen or Yan Jin.

Additional information

Zheng Zhao and Liang Tang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, Z., Tang, L., Deng, Z. et al. Essential role of ADAM28 in regulating the proliferation and differentiation of human dental papilla mesenchymal cells (hDPMCs). Histochem Cell Biol 130, 1015–1025 (2008). https://doi.org/10.1007/s00418-008-0467-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-008-0467-y

Keywords

Search

Navigation