Skip to main content

Advertisement

SpringerLink
Log in

Human mesenchymal progenitor cells derived from alveolar bone and human bone marrow stromal cells: a comparative study

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

Abstract

The aim of the present study was to evaluate the potential of intraoral harvested alveolar bone as an alternative source of multipotent mesenchymal stromal cells for future applications in oral and maxillofacial tissue engineering. Explant cultures were established from 20 alveolar bone samples harvested from the oblique line immediately before wisdom tooth removal. Morphology and proliferation characteristics of the in vitro expanded cells, referred to as human alveolar bone-derived cells (hABDCs), were studied using phase-contrast microscopy. Immunocytochemical analysis of their surface marker expression was conducted using monoclonal antibodies defining mesenchymal stromal cells. To evaluate their multilineage differentiation potential, hABDCs were induced to differentiate along the osteogenic, adipogenic, and chondrogenic lineage and compared to bone marrow mesenchymal stromal cells (hBMSCs) on mRNA and protein levels applying RT-PCR and cytochemical staining methods. hABDCs showed typical morphological characteristics comparable to those of hBMSCs such as being mononuclear, fibroblast-like, spindle-shaped, and plastic adherent. Immunophenotypically, cells were positive for CD105, CD90, and CD73 while negative for CD45, CD34, CD14, CD79α, and HLA-DR surface molecules, indicating an antigen expression pattern considered typical for multipotent mesenchymal stromal cells. As evidenced by RT-PCR and cytochemistry, hABDCs showed multilineage differentiation and similar chondrogenic and osteogenic differentiation potentials when compared to hBMSCs. Our findings demonstrate that human alveolar bone contains mesenchymal progenitor cells that can be isolated and expanded in vitro and are capable of trilineage differentiation, providing a reservoir of multipotent mesenchymal cells from an easily accessible tissue source.

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

  • Akintoye SO, Lam T, Shi S, Brahim J, Collins MT, Robey PG (2006) Skeletal site-specific characterization of orofacial and iliac crest human bone marrow stromal cells in same individuals. Bone 38:758–768

    Article  PubMed  CAS  Google Scholar 

  • Aubin JE (1998) Advances in the osteoblast lineage. Biochem Cell Biol 76:899–910

    Article  PubMed  CAS  Google Scholar 

  • Aubin JE, Turksen K (1996) Monoclonal antibodies as tools for studying the osteoblast lineage. Microsc Res Tech 33:128–140

    Article  PubMed  CAS  Google Scholar 

  • Cancedda R, Mastrogiacomo M, Bianchi G, Derubeis A, Muraglia A, Quarto R (2003) Bone marrow stromal cells and their use in regenerating bone. Novartis Found Symp 249:133–143, discussion 143-7, 170-4, 239-41

    Google Scholar 

  • Cicconetti A, Sacchetti B, Baetoli A, Michienzi S, Corsi A, Funari A, Robey PG, Bianco P, Riminucci M (2007) Human maxillary tuberosity and jaw periosteum as sources of osteoprogenitor cells for tissue engineering. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 104:618.e1–618.12

    Google Scholar 

  • Clausen C, Hermund NU, Donatsky O, Nielsen H (2006) Characterization of human bone cells derived from the maxillary alveolar ridge. Clin Oral Implants Res 17:533–540

    Article  PubMed  Google Scholar 

  • De Assis AF, Beloti MM, Crippa GE, De Oliveira PT, Morra M, Rosa AL (2009) Development of the osteoblastic phenotype in human alveolar bone-derived cells grown on a collagen type I-coated titanium surface. Clin Oral Implants Res 20:240–246

    Article  PubMed  Google Scholar 

  • Dezawa M, Ishikawa H, Itokazu Y, Yoshihara T, Hoshino M, Takeda S, Ide C, Nabeshima Y (2005) Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309:314–317

    Article  PubMed  CAS  Google Scholar 

  • Ding G, Liu Y, Wang W, Wei F, Liu D, Fan Z, An Y, Zhang C, Wang S (2010) Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 28:1829–1838

    Article  PubMed  CAS  Google Scholar 

  • Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317

    Article  PubMed  CAS  Google Scholar 

  • Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, Denbesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81:531–535

    Article  PubMed  CAS  Google Scholar 

  • Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A, International Society for Cellular Therapy (2005) Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 7:393–395

    Article  PubMed  CAS  Google Scholar 

  • Kato T, Hattori K, Deguchi T, Katsube Y, Matsumoto T, Ohgushi H, Numabe Y (2011) Osteogenic potential of rat stromal cells derived from periodontal ligament. J Tissue Eng Regen Med 5:798–805

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM, Gronthos S, Shi S, Wang S (2008) Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 26:1065–1073

    Article  PubMed  Google Scholar 

  • Lohberger B, Payer M, Rinner B, Kaltenegger H, Wolf E, Schallmoser K, Strunk D, Rohde E, Berghold A, Pekovits K, Wildburger A, Leithner A, Windhager R, Jakse N (2013) Tri-lineage potential of intraoral tissue-derived mesenchymal stromal cells. J Craniomaxillofac Surg 41:110–118

    Article  PubMed  Google Scholar 

  • Matsubara T, Suardita K, Ishii M, Sugiyama M, Igarashi A, Oda R, Nishimura M, Saito M, Nakagawa K, Yamanaka K, Miyazaki K, Shimizu M, Bhawal UK, Tsuji K, Nakamura K, Kato Y (2005) Alveolar bone marrow as a cell source for regenerative medicine: differences between alveolar and iliac bone marrow stromal cells. J Bone Min Res 20:399–409

    Article  CAS  Google Scholar 

  • Noth U, Osyczka AM, Tuli R, Hickok NJ, Danielson KG, Tuan RS (2002) Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J Orthop Res 20:1060–1069

    Article  PubMed  Google Scholar 

  • Payer M, Lohberger B, Stadelmeyer E, Bartmann C, Windhager R, Jakse N (2010) Behaviour of multipotent maxillary bone-derived cells on beta-tricalcium phosphate and highly porous bovine bone mineral. Clin Oral Implants Res 21:699–708

    Article  PubMed  Google Scholar 

  • Pekovits K, Wildburger A, Payer M, Hutter H, Jakse N, Dohr G (2012) Evaluation of graft cell viability-efficacy of piezoelectric versus manual bone scraper technique. J Oral Maxillofac Surg 70:154–162

    Article  PubMed  Google Scholar 

  • Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    Article  PubMed  CAS  Google Scholar 

  • Pittenger MF, Mosca JD, McIntosh KR (2000) Human mesenchymal stem cells: progenitor cells for cartilage, bone, fat and stroma. Curr Top Microbiol Immunol 251:3–11

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Lozano FJ, Bueno C, Insausti CL, Meseguer L, Ramirez MC, Blanquer M, Marin N, Martinez S, Moraleda JM (2011) Mesenchymal stem cells derived from dental tissues. Int Endod J 44:800–806

    Article  PubMed  CAS  Google Scholar 

  • Rosa AL, Crippa GE, De Oliveira PT, Taba M Jr, Levebvre LP, Beloti MM (2009) Human alveolar bone cell proliferation, expression of osteoblastic phenotype, and matrix mineralization on porous titanium produced by powder metallurgy. Clin Oral Implants Res 20:472–481

    Article  PubMed  Google Scholar 

  • Seo BM, Miura M, Gronthos S, Bartold PM, Bartouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364:149–155

    Article  PubMed  CAS  Google Scholar 

  • Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S (2005) The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 8:191–199

    Article  PubMed  CAS  Google Scholar 

  • Song L, Young NJ, Webb NE, Tuan RS (2005) Origin and characterization of multipotential mesenchymal stem cells derived from adult human trabecular bone. Stem Cells Dev 14:712–721

    Article  PubMed  CAS  Google Scholar 

  • Sottile V, Halleux C, Bassilana F, Keller H, Seuwen K (2002) Stem cell characteristics of human trabecular bone-derived cells. Bone 30:699–704

    Article  PubMed  CAS  Google Scholar 

  • Springer IN, Terheyden H, Geiss S, Harle F, Hedderich J, Acil Y (2004) Particulated bone grafts–effectiveness of bone cell supply. Clin Oral Implants Res 15:205–212

    Article  PubMed  Google Scholar 

  • Tuli R, Tuli S, Nandi S, Wang ML, Alexander PG, Haleem-Smith H, Hozack WJ, Manner PA, Danielson KG, Tuan RS (2003) Characterization of multipotential mesenchymal progenitor cells derived from human trabecular bone. Stem Cells 21:681–693

    Article  PubMed  CAS  Google Scholar 

  • Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M (2002) Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthr Cartil 10:199–206

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Rossi FM, Putnins EE (2010) Periodontal regeneration using engineered bone marrow mesenchymal stromal cells. Biomaterials 31:8574–8582

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Mr. Rudolf Schmied for his excellent technical assistance and Dipl. Ing. Amin El-Heliebi and Dr. Martin Gauster for help in DNA preparation and analysis. Special thanks also go to Dr. Andreas Reinisch for providing hBMSCs.

Author information

Authors and Affiliations

  1. Institute of Cell Biology, Histology and Embryology, Center of Molecular Medicine, Medical University of Graz, Harrachgasse 21/7, 8010, Graz, Austria

    Karin Pekovits, Julia Maria Kröpfl, Heinz Hutter & Gottfried Dohr

  2. Clinical Institute of Medical and Chemical Laboratory Diagnostics, Medical University of Graz, Auenbruggerplatz 15, 8036, Graz, Austria

    Ingeborg Stelzer

  3. Department of Dentistry and Maxillofacial Surgery, Medical University of Graz, Auenbruggerplatz 12, 8036, Graz, Austria

    Michael Payer

Authors
  1. Karin Pekovits
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julia Maria Kröpfl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ingeborg Stelzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Payer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heinz Hutter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gottfried Dohr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karin Pekovits.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pekovits, K., Kröpfl, J.M., Stelzer, I. et al. Human mesenchymal progenitor cells derived from alveolar bone and human bone marrow stromal cells: a comparative study. Histochem Cell Biol 140, 611–621 (2013). https://doi.org/10.1007/s00418-013-1140-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-013-1140-7

Keywords

Search

Navigation