Abstract
Mesenchymal stem cells (MSCs) can be obtained from various sources. MSCs from different origins appear to have different preferences for differentiation. In this study, we have compared the in vivo osteogenic potential of adult MSCs from adipose tissue (AT) and bone marrow (BM) with fetal MSCs from umbilical cord (UC) and umbilical cord blood (UCB) by using a rat critical-sized femoral defect model. We have also sought to determine whether pretreatment with an osteogenic medium promotes osteogenesis in MSCs. Study groups were divided as follows: (1) defect only, (2) scaffold only, (3) AT MSCs in scaffolds, (4) BM MSCs in scaffolds, (5) UC MSCs in scaffolds and (6) UCB MSCs in scaffolds. Groups with MSCs were further divided with respect to their pretreatment. At 12 weeks after surgery, in vivo osteogenesis was measured radiographically and by micro-computed tomography (CT). Based on quantitative assessment by micro-CT, no significant difference of the mean bone volume fraction value (BV/TV) was seen between adult MSCs (AT and BM MSCs) and fetal MSCs (UC and UCB MSCs). The mean BV/TVs were significantly higher in non-pretreated BM MSC (14.2±1.4%) and UCB MSC (14.0±1.2%) and pretreated UC MSC (14.8±2.0%) than in those with the scaffold only (11.3±1.3%; P<0.05). In addition, AT (from 10.4±1.2% to 13.1±2.2%) and UC (from 10.3±0.7% to 14.8±2.0%) MSCs from solid tissues showed a significant increase in the mean BV/TV with pretreatment (P<0.05). In contrast, BM MSC (from 14.2±1.4% to 10.9±1.2%) and UCB MSC (from 14.0±1.2% to 11.6±1.0%) from non-solid tissues showed a significant decrease with pretreatment (P<0.05).
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References
Baksh D, Yao R, Tuan RS (2007) Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 25:1384–1392
Bruder SP, Kurth AA, Shea M, Hayes WC, Jaiswal N, Kadiyala S (1998) Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res 16:155–162
Castano-Izquierdo H, Alvarez-Barreto J, van den Dolder J, Jansen JA, Mikos AG, Sikavitsas VI (2007) Pre-culture period of mesenchymal stem cells in osteogenic media influences their in vivo bone forming potential. J Biomed Mater Res A 82:129–138
Chang YJ, Shih DT, Tseng CP, Hsieh TB, Lee DC, Hwang SM (2006) Disparate mesenchyme-lineage tendencies in mesenchymal stem cells from human bone marrow and umbilical cord blood. Stem Cells 24:679–685
Diao Y, Ma Q, Cui F, Zhong Y (2009) Human umbilical cord mesenchymal stem cells: osteogenesis in vivo as seed cells for bone tissue engineering. J Biomed Mater Res A 91:123–131
Drosse I, Volkmer E, Seitz S, Seitz H, Penzkofer R, Zahn K, Matis U, Mutschler W, Augat P, Schieker M (2008) Validation of a femoral critical size defect model for orthotopic evaluation of bone healing: a biomechanical, veterinary and trauma surgical perspective. Tissue Eng Part C Methods 14:79–88
Gnecchi M, Melo LG (2009) Bone marrow-derived mesenchymal stem cells: isolation, expansion, characterization, viral transduction, and production of conditioned medium. Methods Mol Biol 482:281–294
Guillot PV, O’Donoghue K, Kurata H, Fisk NM (2006) Fetal stem cells: betwixt and between. Semin Reprod Med 24:340–347
Im GI, 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
Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, Gimble JM, Bunnell BA (2006) Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99:1285–1297
Jo CH, Kim OS, Park EY, Kim BJ, Lee JH, Kang SB, Han HS, Rhee SH, Yoon KS (2008) Fetal mesenchymal stem cells derived from human umbilical cord sustain primitive characteristics during extensive expansion. Cell Tissue Res 334:423–433
Kim HS, Shin TH, Yang SR, Seo MS, Kim DJ, Kang SK, Park JH, Kang KS (2010) Implication of NOD1 and NOD2 for the differentiation of multipotent mesenchymal stem cells derived from human umbilical cord blood. PLoS One 5:e15369
Kraus KH, Kirker-Head C (2006) Mesenchymal stem cells and bone regeneration. Vet Surg 35:232–242
Laib A, Hauselmann HJ, Ruegsegger P (1998) In vivo high resolution 3D-QCT of the human forearm. Technol Health Care 6:329–337
Lane JM, Yasko AW, Tomin E, Cole BJ, Waller S, Browne M, Turek T, Gross J (1999) Bone marrow and recombinant human bone morphogenetic protein-2 in osseous repair. Clin Orthop Relat Res 361:216–227
Levi B, James AW, Nelson ER, Vistnes D, Wu B, Lee M, Gupta A, Longaker MT (2010) Human adipose derived stromal cells heal critical size mouse calvarial defects. PLoS One 5:e11177
Lu LL, Liu YJ, Yang SG, Zhao QJ, Wang X, Gong W, Han ZB, Xu ZS, Lu YX, Liu D, Chen ZZ, Han ZC (2006) Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 91:1017–1026
Mendes SC, Tibbe JM, Veenhof M, Bakker K, Both S, Platenburg PP, Oner FC, de Bruijn JD, van Blitterswijk CA (2002) Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age. Tissue Eng 8:911–920
Park KS, Lee YS, Kang KS (2006) In vitro neuronal and osteogenic differentiation of mesenchymal stem cells from human umbilical cord blood. J Vet Sci 7:343–348
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
Prigozhina TB, Khitrin S, Elkin G, Eizik O, Morecki S, Slavin S (2008) Mesenchymal stromal cells lose their immunosuppressive potential after allotransplantation. Exp Hematol 36:1370–1376
Roura S, Farre J, Soler-Botija C, Llach A, Hove-Madsen L, Cairo JJ, Godia F, Cinca J, Bayes-Genis A (2006) Effect of aging on the pluripotential capacity of human CD105+ mesenchymal stem cells. Eur J Heart Fail 8:555–563
Uchiyama T, Tanizawa T, Muramatsu H, Endo N, Takahashi HE, Hara T (1997) A morphometric comparison of trabecular structure of human ilium between microcomputed tomography and conventional histomorphometry. Calcif Tissue Int 61:493–498
van den Dolder J, Vehof JW, Spauwen PH, Jansen JA (2002) Bone formation by rat bone marrow cells cultured on titanium fiber mesh: effect of in vitro culture time. J Biomed Mater Res 62:350–358
Wright V, Peng H, Usas A, Young B, Gearhart B, Cummins J, Huard J (2002) BMP4-expressing muscle-derived stem cells differentiate into osteogenic lineage and improve bone healing in immunocompetent mice. Mol Ther 6:169–178
Yoon E, Dhar S, Chun DE, Gharibjanian NA, Evans GR (2007) In vivo osteogenic potential of human adipose-derived stem cells/poly lactide-co-glycolic acid constructs for bone regeneration in a rat critical-sized calvarial defect model. Tissue Eng 13:619–627
Zhang ZY, Teoh SH, Chong MS, Schantz JT, Fisk NM, Choolani MA, Chan J (2009) Superior osteogenic capacity for bone tissue engineering of fetal compared with perinatal and adult mesenchymal stem cells. Stem Cells 27:126–137
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
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Chris Hyunchul Jo and Pil Whan Yoon contributed equally to this study and should be considered as co-first authors.
This work was supported by grants from the Seoul R&BD Program (no. 10548), the Basic Science Research Program (no. 2011-0022184) and the Bio & Medical Technology Development Program (no. 2011-0019773) of the National Research Foundation (NRF) funded by the Korean government (MEST).
Each author certifies that neither he nor a member of his immediate family has any commercial associations (e.g., consultancies, stock ownership, equity interest, patent/licensing arrangements) that might pose a conflict of interest in connection with this article.
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Jo, C.H., Yoon, P.W., Kim, H. et al. Comparative evaluation of in vivo osteogenic differentiation of fetal and adult mesenchymal stem cell in rat critical-sized femoral defect model. Cell Tissue Res 353, 41–52 (2013). https://doi.org/10.1007/s00441-013-1619-5
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DOI: https://doi.org/10.1007/s00441-013-1619-5