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The Schneiderian Membrane Contains Osteoprogenitor Cells: In Vivo and In Vitro Study

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Abstract

Recent studies successfully demonstrated induction of new bone formation in the maxillary sinus by mucosal membrane lifting without the use of any graft material. The aim of this work was to test the osteogenic potential of human maxillary sinus Schneiderian membrane (hMSSM) using both in vitro and in vivo assays. Samples of hMSSM were used for establishment of cell cultures and for histological studies. Flow cytometry analysis was performed on P0, P1, and P2 cultures using established mesenchymal progenitor cell markers (CD 105, CD 146, CD 71, CD 73, CD 166), and the ability of hMSSM cells to undergo osteogenic differentiation in culture was analyzed using relevant in vitro assays. Results showed that hMSSM cells could be induced to express alkaline phosphatase, bone morphogenic protein-2, osteopontin, osteonectin, and osteocalcin and to mineralize their extracellular matrix. Inherent osteogenic potential of hMSSM-derived cells was further proven by in vivo experiments, which demonstrated the formation of histology-proven bone at ectopic sites following transplantation of hMSSM-derived cells in conjunction with an osteoconductive scaffold. This study provides the biological background for understanding the observed clinical phenomena in sinus lifting. Our results show that a genuine osteogenic potential is associated with the hMSSM and can contribute to development of successful sinus augmentation techniques.

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References

  1. Artzi Z, Nemcovsky CE, Tal H, Dayan D (2001) Histopathological morphometric evaluation of 2 different hydroxyapatite-bone derivatives in sinus augmentation procedures: a comparative study in humans. J Periodontol 72:911–920

    Article  PubMed  CAS  Google Scholar 

  2. Asai S, Shimizu Y, Ooya K (2002) Maxillary sinus augmentation model in rabbits: effect of occluded nasal ostium on new bone formation. Clin Oral Implants Res 13:405–409

    Article  PubMed  Google Scholar 

  3. Bianco P, Kuznetsov SA, Riminucci M, Robey PG (2006) Postnatal skeletal stem cells. Methods Enzymol 419:117–148

    Article  PubMed  CAS  Google Scholar 

  4. Bianco P, Riminucci M, Gronthos S, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19:180–192

    Article  PubMed  CAS  Google Scholar 

  5. Bianco P, Robey PG (2001) Stem cells in tissue engineering. Nature 414:118–121

    Article  PubMed  CAS  Google Scholar 

  6. Bianco P, Robey PG (2004) Skeletal stem cells. In: Lanza RP (ed) Handbook of adult and fetal stem cells. Academic Press, San Diego, CA, pp 415–424

    Chapter  Google Scholar 

  7. Boyne PJ, James RA (1980) Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 38:613–616

    PubMed  CAS  Google Scholar 

  8. Boyne PJ, Lilly LC, Marx RE, Moy PK, Nevins M, Spagnoli DB, Triplett RG (2005) De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation. J Oral Maxillofac Surg 36:1693–1707

    Article  Google Scholar 

  9. Bruder SP, Fink DJ, Caplan AI (1994) Mesenchymal stem cells in bone development, bone repair, and skeletal regeneration therapy. J Cell Biochem 56:283–294

    Article  PubMed  CAS  Google Scholar 

  10. Cammack GV 2nd, Nevins M, Clem DS 3rd, Hatch JP, Mellonig JT (2005) Histologic evaluation of mineralized and demineralized freeze-dried bone allograft for ridge and sinus augmentations. Int J Periodont Restor Dent 25:231–237

    Google Scholar 

  11. Cawood JI, Howell RA (1991) Reconstructive preprosthetic surgery. I. Anatomical considerations. Int J Oral Maxillofac Surg 20:75–82

    Article  PubMed  CAS  Google Scholar 

  12. Cicconetti A, Sacchetti B, Bartoli 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

    Article  PubMed  Google Scholar 

  13. Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, Canfield AE (1998) Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res 13:828–838

    Article  PubMed  CAS  Google Scholar 

  14. Ellegaard B, Baelum V, Kolsen-Petersen J (2006) Non-grafted sinus implants in periodontally compromised patients: a time-to-event analysis. Clin Oral Implants Res 17:156–164

    Article  PubMed  Google Scholar 

  15. Ellegaard B, Kolsen-Petersen J, Baelum V (1997) Implant therapy involving maxillary sinus lift in periodontally compromised patients. Clin Oral Implants Res 8:305–315

    Article  PubMed  CAS  Google Scholar 

  16. Froum SJ, Wallace SS, Elian N, Cho SC, Tarnow DP (2006) Comparison of mineralized cancellous bone allograft (Puros) and anorganic bovine bone matrix (Bio-Oss) for sinus augmentation: histomorphometry at 26 to 32 weeks after grafting. Int J Periodont Restor Dent 26:543–551

    Google Scholar 

  17. Goshima J, Goldberg VM, Caplan AI (1991) Osteogenic potential of culture-expanded rat marrow cells as assayed in vivo with porous calcium phosphate ceramic. Biomaterials 12:253–258

    Article  PubMed  CAS  Google Scholar 

  18. Gruber R, Kandler B, Fuerst G, Fischer MB, Watzek G (2004) Porcine sinus mucosa holds cells that respond to bone morphogenetic protein (BMP)-6 and BMP-7 with increased osteogenic differentiation in vitro. Clin Oral Implants Res 15:575–580

    Article  PubMed  Google Scholar 

  19. Haas R, Baron M, Donath K, Zechner W, Watzek G (2002) Porous hydroxyapatite for grafting the maxillary sinus: a comparative histomorphometric study in sheep. Int J Oral Maxillofac Implants 17:337–346

    PubMed  Google Scholar 

  20. Hallman M, Cederlund A, Lindskog S, Lundgren S, Sennerby L (2001) A clinical histologic study of bovine hydroxyapatite in combination with autogenous bone and fibrin glue for maxillary sinus floor augmentation. Results after 6 to 8 months of healing. Clin Oral Implants Res 12:135–143

    Article  PubMed  CAS  Google Scholar 

  21. Hallman M, Sennerby L, Zetterqvist L, Lundgren S (2005) A 3-year prospective follow-up study of implant-supported fixed prostheses in patients subjected to maxillary sinus floor augmentation with a 80:20 mixture of deproteinized bovine bone and autogenous bone. Clinical, radiographic and resonance frequency analysis. Int J Oral Maxillofac Surg 34:273–280

    Article  PubMed  CAS  Google Scholar 

  22. Hatano N, Shimizu Y, Ooya K (2004) A clinical long-term radiographic evaluation of graft height changes after maxillary sinus floor augmentation with a 2:1 autogenous bone/xenograft mixture and simultaneous placement of dental implants. Clin Oral Implants Res 15:339–345

    Article  PubMed  Google Scholar 

  23. Hurzeler MB, Quinones CR, Kirsch A, Gloker C, Schupbach P, Strub JR, Caffesse RG (1997) Maxillary sinus augmentation using different grafting materials and dental implants in monkeys. Part I. Evaluation of anorganic bovine-derived bone matrix. Clin Oral Implants Res 8:476–486

    Article  PubMed  CAS  Google Scholar 

  24. Jung YS, Chung SW, Nam W, Cho IH, Cha IH, Park HS (2007) Spontaneous bone formation on the maxillary sinus floor in association with an extraction socket. Int J Oral Maxillofac Surg 36:656–657

    Article  PubMed  Google Scholar 

  25. Krebsbach PH, Kuznetsov SA, Satomura K, Emmons RV, Rowe DW, Robey PG (1997) Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 63:1059–1069

    Article  PubMed  CAS  Google Scholar 

  26. Lundgren S, Andersson S, Gualini F, Sennerby L (2004) Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation. Clin Implant Dent Relat Res 6:165–173

    PubMed  Google Scholar 

  27. Lundgren S, Andersson S, Sennerby L (2003) Spontaneous bone formation in the maxillary sinus after removal of a cyst: Coincidence or consequence? Clin Implant Dent Relat Res 5:78–81

    Article  PubMed  Google Scholar 

  28. Muraglia A, Martin I, Cancedda R, Quarto R (1998) A nude mouse model for human bone formation in unloaded conditions. Bone 22:131S–134S

    Article  PubMed  CAS  Google Scholar 

  29. Palma VC, Magro-Filho O, de Oliveria JA, Lundgren S, Salata LA, Sennerby L (2006) Bone reformation and implant integration following maxillary sinus membrane elevation: an experimental study in primates. Clin Implant Dent Relat Res 8:11–24

    PubMed  Google Scholar 

  30. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131:324–336

    Article  PubMed  CAS  Google Scholar 

  31. Tatum H Jr (1986) Maxillary and sinus implant reconstructions. Dent Clin North Am 30:207–229

    PubMed  Google Scholar 

  32. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Cell Biology, Faculty of Medicine, Technion – Israel Institute of Technology, P.O. Box 9649, Haifa, 32000, Israel

    S. Srouji, T. Kizhner, D. Ben David & E. Livne

  2. Department of Oral & Maxillofacial Surgery, Carmel Medical Center, Haifa, 34354, Israel

    S. Srouji

  3. Department of Experimental Medicine and Pathology, La Sapienza University, Rome, Italy

    M. Riminucci & P. Bianco

Authors
  1. S. Srouji
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  2. T. Kizhner
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  3. D. Ben David
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  4. M. Riminucci
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  5. P. Bianco
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  6. E. Livne
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Correspondence to S. Srouji.

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Srouji, S., Kizhner, T., Ben David, D. et al. The Schneiderian Membrane Contains Osteoprogenitor Cells: In Vivo and In Vitro Study. Calcif Tissue Int 84, 138–145 (2009). https://doi.org/10.1007/s00223-008-9202-x

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  • DOI: https://doi.org/10.1007/s00223-008-9202-x

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