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Comparison of Osteogenic Ability of Rat Mesenchymal Stem Cells from Bone Marrow, Periosteum, and Adipose Tissue

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Abstract

Mesenchymal stem cells (MSCs) reside in many types of tissue and are able to differentiate into various functional cells including osteoblasts. Recently, adipose tissue–derived MSCs (AMSCs) have been shown to differentiate into many lineages, and they are considered a source for tissue regeneration. The purpose of this study was to compare the osteogenic differentiation capability of MSCs from bone marrow (BMSCs), MSCs from periosteum (PMSCs), and AMSCs using in vitro culture and in vivo implantation experiments. We harvested these MSCs from 7-week-old rats. The cells were seeded and cultured for 7 days in primary culture to assay a colony-forming unit. The frequency of the unit was the smallest in the BMSCs (P < 0.001). After primary culture, subculture was performed under osteogenic differentiation conditions for 1 and 2 weeks to detect mineralization as well as the bone-specific proteins of alkaline phosphatase and osteocalcin as osteogenic markers. BMSCs and PMSCs showed distinct osteogenic differentiation capability in comparison with other MSCs (P < 0.001). For the in vivo assay, composites of these cells and hydroxyapatite ceramics were subcutaneously implanted into syngeneic rats and harvested after 6 weeks. Micro-computed tomographic (CT) and histological analyses demonstrated that new bone formation was detected in the composites using BMSCs and PMSCs, although it was hard to detect in other composites. The CT analyses also demonstrated that the bone volume of BMSC composites was more than that of AMSC composites (P < 0.001). These results indicate that BMSCs and PMSCs could be ideal candidates for utilization in practical bone tissue regeneration.

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References

  1. Maniatopoulous C, Sodek J, Melcher AH (1988) Bone formation in vitro by stromal cells obtained from bone marrow of young adult rat. Cell Tissue Res 254:317–330

    Article  Google Scholar 

  2. Le Douarin NH, Houssaint E, Jotereau FV, Belo M (1975) Origin of hemapoietic stem cells in embryonic bursa of Fabricius and bone marrow studied through interspecific chimeras. Proc Natl Acad Sci USA 72:2701–2705

    Article  PubMed  CAS  Google Scholar 

  3. Caplan AI, Bruder SP (2001) Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259–264

    Article  PubMed  CAS  Google Scholar 

  4. Caplan AI, Ruben D, Haynesworth SE (1998) Cell-based tissue engineering therapies: the influence of whole body physiology. Adv Drug Deliv Rev 33:3–14

    Article  PubMed  Google Scholar 

  5. Ohgushi H, Caplan AI (1999) Stem cell technology and bioceramics: from cell to gene engineering. J Biomed Mater Res 48:913–927

    Article  PubMed  CAS  Google Scholar 

  6. 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 Cell Biol 13:4279–4295

    Article  CAS  Google Scholar 

  7. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–228

    Article  PubMed  CAS  Google Scholar 

  8. Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F (2002) Chondrogenic potential of adipose tissue–derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290:763–769

    Article  PubMed  CAS  Google Scholar 

  9. Mizuno H, Zuk PA, Zhu M, Lorenz HP, Benhaim P, Hedrick MH (2002) Myogenic differentiation of human processed lipoaspirate cells. Plast Reconstr Surg 109:199–209

    Article  PubMed  Google Scholar 

  10. Safford KM, Hiock KC, Safford SD, Halvorsen YD, Wilkinson WO, Gimble JM, Rice HE (2002) Neurogenic differentiation of murine and human adipose-derived stromal cells. Biochem Biophys Res Commun 294:371–379

    Article  PubMed  CAS  Google Scholar 

  11. Awad HA, Halvorsen YD, Gimble JM, Guilak F (2003) Effects of transforming growth factor beta 1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng 9:1301–1312

    Article  PubMed  CAS  Google Scholar 

  12. Huang JI, Zuk PA, Jones NF, Zhu M, Lorenz HP, Hedrick MH, Benhaim P (2004) Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg 113:585–594

    Article  PubMed  Google Scholar 

  13. Dragoo JL, Samimi B, Zhu M, Hame SL, Thomas BJ, Lieberman JR, Hedrick MH, Benhaim P (2003) Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads. Adv J Bone Joint Surg Br 85:740–747

    CAS  Google Scholar 

  14. Cowan CM, Shi YY, Aalami OO, Chou YF, Mari C, Thomas R, Quatro N, Contag CH, Wu B, Longaker MT (2004) Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22:560–567

    Article  PubMed  CAS  Google Scholar 

  15. Halvorsen YC, Wilkison WO, Gimble JM (2004) Adipose-derived stromal cells—their utility and potential in bone formation. Int J Obes Relat Metab Disord 24 Suppl 4:S41–S44

    Google Scholar 

  16. Hicok KC, Laney TT, Zhou YS, Halvorsen YD, Hitt DC, Cooper LF, Gimble JM (2004) Human adipose-derived adult stem cells produce osteoid in vivo. Tissue Eng 10:371–380

    Article  PubMed  CAS  Google Scholar 

  17. Peterson B, Zhang J, Iglesias R, Kabo M, Hedrick M, Benhaim P, Lieberman JR (2005) Healing of critically sized femoral defects, using genetically modified mesenchymal stem cells from human adipose tissue. Tissue Eng 11:120–129

    Article  PubMed  CAS  Google Scholar 

  18. Rodriguez AM, Pisani D, Dechesne CA, Turc-Carel C, Kurzenne JY, Wdziekonski B, Villageosis A, Bagnis C, Breittmayer JP, Groux H, Aihaud G, Dani C (2005) Transplantation of a multipotent cell population from human adipose tissue induces dystrofin expression in the immunocompetent mdx mouse. J Exp Med 201:1397–1405

    Article  PubMed  CAS  Google Scholar 

  19. Planat-Bernard V, Menard C, Andre M, Puceat M, Perez A, Garcia-Veedugo JM, Penicaud L, Casteilla L (2004) Spontaneous cardiomyocyte differentiation from adipose tissue stroma cells. Circ Res 94:223–229

    Article  CAS  Google Scholar 

  20. Strem BM, Zhu M, Alfonso Z, Daniels EJ, Schreiber R, Begyui R, Maclellan WR, Hendrick MH, Fraser JK (2005) Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy 7:282–291

    Article  PubMed  CAS  Google Scholar 

  21. Ashjian PH, Elbarbary AS, Edmonds B, De Ugarte D, Zhu M, Zuk PA, Lorenz HP, Benhaim P, Hedrick MH (2003) In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast Reconstr Surg 111:1922–1931

    Article  PubMed  Google Scholar 

  22. Kang SK, Lee DH, Bae YC, Kim HK, Baik SY, Jung JS (2003) Improvement of neurological deficits by intracerebral transplantation of human adipose tissue–derived stromal cells after cerebral ischemia in rats. Exp Neurol 183:355–366

    Article  PubMed  CAS  Google Scholar 

  23. Miranville A, Heeschen C, Sengenes C, Curat CA, Busse R, Bouloumie A (2004) Improvement of postnatal neovascularization by human adipose tissue–derived stem cells. Circulation 110:349–355

    Article  PubMed  CAS  Google Scholar 

  24. Rehman J, Traktuev D, Li J, Merfeld-Clauss S, Temm-Grove CJ, Bovenkerk JE, Pell CL, Johnstone BH, Considine RV, March KL (2004) Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109:1292–1298

    Article  PubMed  Google Scholar 

  25. Planat-Benard V, Silvestre JS, Cousin B, Andre M, Nibbelink M, Tamarat R, Clergue M, Manneville C, Saillan-Barreau C, Duriez M, Tedgui A, Levy B, Penicaud L, Casteilla L (2004) Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation 109:656–663

    Article  PubMed  Google Scholar 

  26. Cao Y, Shu Z, Liao L, Meng Y, Han Q, Zhao RC (2005) Human adipose tissue–derived stem cells differentiate into endothelial cells in vitro and improve potential neovascularization in vivo. Biochem Biophys Res Commun 332:370–379

    Article  PubMed  CAS  Google Scholar 

  27. Seo MJ, Suh SY, Bae YC, Jung JS (2005) Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun 328:258–264

    Article  PubMed  CAS  Google Scholar 

  28. Hauner H, Entenmann G, Webitsch M, Gaillard D, Ailhaud G, Negrel R, Pfeiffer EF (1989) Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest 84:1663–1670

    Article  PubMed  CAS  Google Scholar 

  29. Uchimura E, Machida H, Kotobuki N, Kihara T, Kitamura S, Ikeuchi M, Hirose M, Miyake J, Ohgushi H (2003) In-situ visualization and quantification of mineralization of cultured osteogenic cells. Calcif Tissue Int 73:575–583

    Article  PubMed  CAS  Google Scholar 

  30. Nagaya N, Fujii T, Iwase T, Ohgushi H, Itoh T, Uematsu M, Yamagishi M, Mori H, Kanagawa K, Kitamura S (2004) Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infraction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 287:H2670–H2676

    Article  PubMed  CAS  Google Scholar 

  31. Ohgushi H, Dohi Y, Katsuda T, Tamai S, Tabata S, Suwa Y (1996) In vitro bone formation by rat marrow cell culture. J Biomed Mater Res 32:333–340

    Article  PubMed  CAS  Google Scholar 

  32. Nishikawa M, Myoui A, Ohgushi H, Ikeuchi M, Tamai N, Yoshikawa H (2004) Bone tissue engineering using novel interconnected porous hydroxyapatite ceramics combined with marrow mesenchymal cells: quantitative and three-dimensional image analysis. Cell Transplant 13:367–376

    PubMed  Google Scholar 

  33. Ohgushi H, Dohi Y, Yoshikawa T, Tamai S, Tabata S, Okunaga K, Shibuya T (1996) Osteogenic differentiation of cultured marrow stromal stem cells on the surface of bioactive glass ceramics. J Biomed Mater Res 32:341–348

    Article  PubMed  CAS  Google Scholar 

  34. Hirose M, Kotobuki N, Machida H, Uchimura E, Ohgushi H (2003) Quantitative monitoring of in vitro mineralization process using fluorescent dyes. Key Eng Mater 240:715–718

    Article  Google Scholar 

  35. Ohgushi H, Goldberg VM, Caplan AI (1989) Heterotopic osteogenesis in porous ceramics induced by marrow cells. J Orthop Res 7:568–578

    Article  PubMed  CAS  Google Scholar 

  36. Shimaoka H, Dohi Y, Ohgushi H, Ikeuchi M, Okamoto M, Kudo A, Kirita T, Yonemasu K (2004) Recombinant growth/differentiation factor-5 (GDF-5) stimulates osteogenic differentiation of marrow mesenchymal stem cells in porous hydroxyapatite ceramic. J Biomed Mater Res A 68:168–176

    Article  PubMed  CAS  Google Scholar 

  37. Noshi T, Yoshikawa T, Ikeuchi M, Dohi Y, Ohgushi H, Horiuchi K, Sugimura M, Ichijima K, Yonemasu K (2000) Enhancement of the in vivo osteogenic potential of marrow/hydroxyapatite composites by bovine bone morphogenetic protein. J Biomed Mater Res 52:621–630

    Article  PubMed  CAS  Google Scholar 

  38. Katz AJ, Llull R, Hedrick MH, Futrell JW (1999) Emerging approaches to the tissue engineering of fat. Tissue Eng 26:587–603

    CAS  Google Scholar 

  39. Miyazaki T, Kitagawa Y, Toriyama K, Kobori M, Torii S (2005) Isolation of two human fibroblastic cell populations with multiple but distinct potential of mesenchymal differentiation by ceiling culture of mature fat cells from subcutaneous adipose tissue. Differentiation 73:69–78

    Article  PubMed  CAS  Google Scholar 

  40. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T (2005) Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52:2521–2529

    Article  PubMed  Google Scholar 

  41. De Ugarte DA, Morizono K, Elabarbary A, Alfonso Z, Zuk PA, Zhu M, Dragoo JL, Ashjian P, Thomas B, Benhaim P, Chen I, Fraser J, Hedrick MH (2003) Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174:101–109

    Article  PubMed  Google Scholar 

  42. Gun-II I, Shin YW, Lee KB (2005) Do adipose tissue–derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow–derived cells? Osteoarthritis Cartilage 13:845–853

    Article  Google Scholar 

  43. Yoshimura H, Muneta T, Nimura A, Yokoyama A, Koga H, Sekiya I (2007) Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 327:449–462

    Article  PubMed  CAS  Google Scholar 

  44. Sugiura F, Kitoh H, Ishiguro N (2004) Osteogenic potential of rat mesenchymal stem cells after several passages. Biochem Biophys Res Commun 316:233–239

    Article  PubMed  CAS  Google Scholar 

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Acknowlegements

This work was supported by grants from the New Energy and Industrial Technology Development Organization, which was established by the Japanese government in 1980.

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Authors and Affiliations

  1. Department of Orthopedic Surgery, Nippon Medical School, Tokyo, Japan

    Ousuke Hayashi & Hiromoto Ito

  2. Research Institute for Cell Engineering, National Institute of Advanced Industrial Science and Technology, 3-11-46 Nakoji, Amagasaki, Hyogo, 661-0974, Japan

    Yoshihiro Katsube, Motohiro Hirose & Hajime Ohgushi

Authors
  1. Ousuke Hayashi
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  2. Yoshihiro Katsube
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  4. Hajime Ohgushi
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Correspondence to Hajime Ohgushi.

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Hayashi, O., Katsube, Y., Hirose, M. et al. Comparison of Osteogenic Ability of Rat Mesenchymal Stem Cells from Bone Marrow, Periosteum, and Adipose Tissue. Calcif Tissue Int 82, 238–247 (2008). https://doi.org/10.1007/s00223-008-9112-y

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  • DOI: https://doi.org/10.1007/s00223-008-9112-y

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