MANDIBULAR BONE REGENERATION USING AUTOGENOUS SKIN-DERIVED PRECURSOR CELLS WITH A MIXED DEMINERALIZED BONE AND FIBRIN GLUE SCAFFOLD IN MINIATURE PIGS

미니돼지에서 자가 피부유래 전구세포와 탈회골 및 피브린 스케폴드를 이용한 하악골 골결손부의 골재생에 대한 연구

  • Byun, June-Ho (Department Oral & Maxillofacial Surgery, School of Medicine and Institute of Health Science, Gyeongsang National University) ;
  • Choi, Mun-Jeong (Department Oral & Maxillofacial Surgery, School of Medicine and Institute of Health Science, Gyeongsang National University) ;
  • Choi, Young-Jin (Department Oral & Maxillofacial Surgery, School of Medicine and Institute of Health Science, Gyeongsang National University) ;
  • Shim, Kyoung-Mok (Department Oral & Maxillofacial Surgery, School of Medicine and Institute of Health Science, Gyeongsang National University) ;
  • Kim, Uk-Kyu (Department of Oral & Maxillofacial Surgery, School of Dentistry, Pusan National University) ;
  • Kim, Jong-Ryoul (Department of Oral & Maxillofacial Surgery, School of Dentistry, Pusan National University) ;
  • Park, Bong-Wook (Department Oral & Maxillofacial Surgery, School of Medicine and Institute of Health Science, Gyeongsang National University)
  • 변준호 (경상대학교 의학전문대학원 치과학교실 구강악안면외과, 경상대학교 건강과학연구원) ;
  • 최문정 (경상대학교 의학전문대학원 치과학교실 구강악안면외과, 경상대학교 건강과학연구원) ;
  • 최영진 (경상대학교 의학전문대학원 치과학교실 구강악안면외과, 경상대학교 건강과학연구원) ;
  • 심경목 (경상대학교 의학전문대학원 치과학교실 구강악안면외과, 경상대학교 건강과학연구원) ;
  • 김욱규 (부산대학교 치의학전문대학원 구강악안면외과학교실) ;
  • 김종렬 (부산대학교 치의학전문대학원 구강악안면외과학교실) ;
  • 박봉욱 (경상대학교 의학전문대학원 치과학교실 구강악안면외과, 경상대학교 건강과학연구원)
  • Received : 2009.04.13
  • Accepted : 2009.05.13
  • Published : 2009.05.30

Abstract

Purpose: The aims of this study were to assess the in vitro co-culturing pattern of isolated skin-derived precursor cells (SKPs) with a mixed demineralized bone (DMB) and fibrin glue scaffold and to evaluate in vivo osteogenesis after transplantation of autogenous SKPs with a these mixed scaffold in the animal's mandibular defects. Materials and Methods: We isolated SKPs from the ears of adult 4 miniature pigs. The isolated SKPs were co-cultured with a mixed DMB and fibrin glue scaffold in a non-osteogenic medium for 1, 2, and 4 weeks. Histological characteristics of in vitro co-cultured cells and scaffold were evaluated. $1{\times}10^7\;cells/100\;{\mu}l$ of autogenous porcine SKPs were grafted into the mandibular defects with a DMB and fibrin glue scaffold. In the control sites, only a scaffold was grafted, without SKPs. After two animals each were euthanized at 2 and 4 weeks after grafting, the in vivo osteogenesis was evaluated with histolomorphometric and osteocalcin immunohistochemical studies. Results: Homogeneously shaped skin-derived cells were isolated from porcine ear skin after 3 or 4 weeks of primary culture. In vitro osteogenic differentiation of SKPs was observed after co-culturing with a DMB and fibrin glue scaffold in a non-osteogenic medium. Von Kossa-positive bone minerals were also noted in the co-cultured medium at 4 weeks. As the culture time progressed, the number of observable cells increased. Trabecular new bone formation and osteocalcin expression were more pronounced in the SKP-grafted group compared to the control group. Conclusion: These findings suggest that autogenous SKP grafting with a DMB and fibrin glue scaffold can serve as a useful alternative to bone grafting technique.

Keywords

References

  1. Park BW, Kim JR, Lee JH et al : Expression of nerve growth factor and vascular endothelial growth factor in the inferior alveolar nerve after distraction osteogenesis. Int J Oral Maxillofac Surg 35 : 624, 2006 https://doi.org/10.1016/j.ijom.2006.02.019
  2. Byun JH, Park BW, Kim JR et al : Expression of vascular endothelial growth factor and its receptors after mandibular distraction osteogenesis. Int J Oral Maxillofac Surg 36 : 338, 2007 https://doi.org/10.1016/j.ijom.2006.10.013
  3. Choi MJ, Byun JH, Kang EJ et al : Isolation of porcine nultipotential skin-derived precursor cells and its multilineage differentiation. J Kor Assoc Oral Maxillofac Surg 34 : 588, 2008
  4. Wagers AJ, Weissman IL : Plasticity of adult stem cells. Cell 116 : 639, 2004 https://doi.org/10.1016/S0092-8674(04)00208-9
  5. Mao JJ, Giannobile WV, Helms JA et al : Craniofacial tissue engineering by stem cells. J Dent Res 85 : 966, 2006 https://doi.org/10.1177/154405910608501101
  6. Shi C, Zhu Y, Su Y et al : Stem cells and their applications in skin-cell therapy. Trend Biotech 24 : 48, 2006 https://doi.org/10.1016/j.tibtech.2005.11.003
  7. Toma JG, Akhavan M, Fernandes KJ et al : Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3 : 778, 2001 https://doi.org/10.1038/ncb0901-778
  8. Dyce PW, Zhu H, Craig J et al : Stem cells with multilineage potential derive from porcine skin. Biochem Biophys Res Commun 316 : 651, 2004 https://doi.org/10.1016/j.bbrc.2004.02.093
  9. Buranasinsup S, Sila-asna M, Bunyaratvej N et al : In vitro osteogenesis from skin-derived precursor cells. Develop Growth Differ 48 : 263, 2006 https://doi.org/10.1111/j.1440-169X.2006.00864.x
  10. Kajahn J, Gorjup E, Tiede S et al : Skin-derived human adult stem cells surprisingly share many features with human pancreatic stem cells. Eur J Cell Biol 87 : 39, 2008 https://doi.org/10.1016/j.ejcb.2007.07.004
  11. Toma JG, McKenzie IA, Bagli D et al : Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23 : 727, 2005 https://doi.org/10.1634/stemcells.2004-0134
  12. Marchesi C, Pluderi M, Colleoni F et al : Skin-derived stem cells transplanted into resorbable guides provide functional nerve regeneration after sciatic nerve resection. GLIA 55 : 425, 2007 https://doi.org/10.1002/glia.20470
  13. Zhao M, Isom SC, Lin H et al : Tracing the stemness of porcine skin-derived progenitors (pSKP) back to specific marker gene expression. Cloning Stem Cells 11 : 111, 2009 https://doi.org/10.1089/clo.2008.0071
  14. Carlin R, Davis D, Weiss M et al : Expression of early transcription factors Oct-4, Sox-2 and Nanog by porcine umbilical cord (PUC) matrix cells. Reprod Biol Endocrinol 4 : 8, 2006 https://doi.org/10.1186/1477-7827-4-8
  15. Fernandes KJL, Mckenzie IA, Mill P et al : A dermal niche for multipotent adult-derive precursor cell. Nat. Cell Biol. 6 : 1082, 2004 https://doi.org/10.1038/ncb1181
  16. Fernandes KJL, Kobayashi NR, Gallagher CJ et al : Analysis of the neurogenic potential of multipotent skinderived precursors. Exp. Neurol. 201 : 32, 2006 https://doi.org/10.1016/j.expneurol.2006.03.018
  17. Hunt DPJ, Morris PN, Sterling J et al : A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells 26 : 163, 2008 https://doi.org/10.1634/stemcells.2007-0281
  18. Schmelzeisen R, Schimming R, Sittinger M : Making bone: implant into tissue-engineered bone for maxillary sinus floor augmentation- a preliminary report. J Cranio Maxillofac Surg 31 : 34, 2003 https://doi.org/10.1016/S1010-5182(02)00163-4
  19. Wheeler SL, Holmes RE, Calhoun CJ : Six-year clinical and histologic study of sinus-lift grafts. Int J Oral Maxillofac Implants 11 : 26, 1996
  20. Chen F, Feng X, Wu W et al : Segmental bone tissue engineering by seeding osteoblast precursor cells into titanium mesh-coral composite scaffolds. Int J Oral Maxillofac Surg 36 : 822, 2007 https://doi.org/10.1016/j.ijom.2007.06.019
  21. Yamada Y, Ueda M, Naiki T et al : Tissue-engineered injectable bone regeneration for osseointegrated dental implants. Clin Oral Impl Res 15 : 589, 2004 https://doi.org/10.1111/j.1600-0501.2004.01038.x
  22. Park BW, Hah YS, Kim DY et al : Osteogenic phenotypes and mineralization of cultured human periosteal-derived cells. Arch Oral Biol 52 :983, 2007 https://doi.org/10.1016/j.archoralbio.2007.04.007
  23. Schimming R, Schmelzeisen R : Tissue-engineered bone for maxillary sinus augmentation. J Oral Maxillofac Surg 62 : 724, 2004 https://doi.org/10.1016/j.joms.2004.01.009
  24. Zizelmann C, Schoen R, Metzger MC et al : Bone formation after sinus augmentation with engineered bone. Clin Oral Impl Res 18 : 69, 2007 https://doi.org/10.1111/j.1600-0501.2006.01295.x
  25. Fuerst G, Tangl S, Gruber R et al : Bone formation following sinus grafting with autogenous bone-derived cells and bovine bone mineral in minipigs: preliminary findings. Clin Oral Impl Res 15 : 733, 2004 https://doi.org/10.1111/j.1600-0501.2004.01077.x
  26. Springer IN, Nocini PF, Schlegel KA et al : Two techniques for the preparation of cell-scaffold constructs suitable for sinus augmentation: step to clinical application. Tissue Engineering 12 : 2649, 2006 https://doi.org/10.1089/ten.2006.12.2649
  27. Perka C, Schultz O, Spitzer RS et al : Segmental bone repair by tissue-engineered periosteal cell transplants with biosorbable fleece and fibrin scaffolds in rabbits. Biomaterials 21 : 1145, 2000 https://doi.org/10.1016/S0142-9612(99)00280-X
  28. Yamada Y, Boo JS, Ozawa R et al : Bone regeneration following injection of mesenchymal stem cells and fibrin glue with a biodegradable scaffold. J Cranio Maxillofac Surg 31 : 27, 2003 https://doi.org/10.1016/S1010-5182(02)00143-9
  29. Schwarz N, Redl H, Schlag G et al : The influence of fibrin sealant on demineralized bone matrix-dependent osteoinduction. A quantitative and qualitative study in rats. Clin Orthop Relat Res 238 : 282, 1989
  30. Yamada, Y, Nakamura S, Ito K et al : Injectable tissueengineered bone using autogenous bone marrow-derived stromal cells for maxillary sinus augmentation: clinical application report from a 2-6-year follow-up. Tissue Eng Part A 14 : 1699, 2008 https://doi.org/10.1089/ten.tea.2007.0189
  31. Pieri F, Lucarelli E, Corinaldesi G et al : Effect of mesenchymal stem cells and platelet-rich plasma on the healing of standardized bone defects in the alveolar ridge: a comparative histomorphometric study in minipigs. J Oral Maxillofac Surg 67 : 265, 2009 https://doi.org/10.1016/j.joms.2008.06.036
  32. Klongnoi B, Rupprecht S, Kessler P et al : Influence of platelet-rich plasma on a bioglass and autogenous bone in sinus augmentation. An explorative study. Clin Oral Impl Res 17 : 312, 2006 https://doi.org/10.1111/j.1600-0501.2005.01215.x
  33. Furst G., Gruber R, Tangl S et al : Sinus grafting with autogenous platelet-rich plasma and bovine hydroxyapatite. A histomorphometric study in minipigs. Clin Oral Impl Res 14 : 500, 2003 https://doi.org/10.1034/j.1600-0501.2003.00859.x
  34. Schaaf H, Streckbein P, Lendeckel S et al : Topical use of platelet-rich plasma to influence bone volume in maxillary augmentation: a prospective randomized trial. Vox Sang 94 : 64, 2008 https://doi.org/10.1111/j.1423-0410.2007.00997.x