DOI QR코드

DOI QR Code

Modulation of osteoblastic/odontoblastic differentiation of adult mesenchymal stem cells through gene introduction: a brief review

  • Kim, Ji-Youn (Division of Oral and Maxillofacial Surgery, Department of Dentistry, St. Vincent's Hospital, The Catholic University of Korea) ;
  • Kim, Myung-Rae (Department of Oral and Maxillofacial Surgery, Ewha Womans University Mok-dong Hospital, Ewha Womans University School of Medicine) ;
  • Kim, Sun-Jong (Department of Oral and Maxillofacial Surgery, Ewha Womans University Mok-dong Hospital, Ewha Womans University School of Medicine)
  • Received : 2012.05.29
  • Accepted : 2012.07.20
  • Published : 2013.04.30

Abstract

Bone tissue engineering is one of the important therapeutic approaches to the regeneration of bones in the entire field of regeneration medicine. Mesenchymal stem cells (MSCs) are actively discussed as material for bone tissue engineering due to their ability to differentiate into autologous bone. MSCs are able to differentiate into different lineages: osteo/odontogenic, adipogenic, and neurogenic. The tissue of origin for MSCs defines them as bone marrow-derived stem cells, adipose tissue-derived stem cells, and, among many others, dental stem cells. According to the tissue of origin, DSCs are further stratified into dental pulp stem cells, periodontal ligament stem cells, stem cells from apical papilla, stem cells from human exfoliated deciduous teeth, dental follicle precursor cells, and dental papilla cells. There are numerous in vitro/in vivo reports suggesting successful mineralization potential or osteo/odontogenic ability of MSCs. Still, there is further need for the optimization of MSCs-based tissue engineering methods, and the introduction of genes related to osteo/odontogenic differentiation into MSCs might aid in the process. In this review, articles that reported enhanced osteo/odontogenic differentiation with gene introduction into MSCs will be discussed to provide a background for successful bone tissue engineering using MSCs with artificially introduced genes.

Keywords

References

  1. Seong JM, Kim BC, Park JH, Kwon IK, Mantalaris A, Hwang YS. Stem cells in bone tissue engineering. Biomed Mater 2010;5: 062001. https://doi.org/10.1088/1748-6041/5/6/062001
  2. Huang GT, Gronthos S, Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 2009;88:792-806. https://doi.org/10.1177/0022034509340867
  3. Song JH, Park BW, Byun JH, Kang EJ, Rho GJ, Shin SH, et al. Isolation and characterization of human dental tissue-derived stem cells in the impacted wisdom teeth: comparison of dental follicle, dental pulp, and root apical papilla-derived cells. J Korean Assoc Oral Maxillofac Surg 2010;36:186-96. https://doi.org/10.5125/jkaoms.2010.36.3.186
  4. Izumi Y, Aoki A, Yamada Y, Kobayashi H, Iwata T, Akizuki T, et al. Current and future periodontal tissue engineering. Periodontol 2000 2011;56:166-87. https://doi.org/10.1111/j.1600-0757.2010.00366.x
  5. Yang X, van der Kraan PM, Bian Z, Fan M, Walboomers XF, Jansen JA. Mineralized tissue formation by BMP2-transfected pulp stem cells. J Dent Res 2009;88:1020-5. https://doi.org/10.1177/0022034509346258
  6. Mukherjee A, Rotwein P. Akt promotes BMP2-mediated osteoblast differentiation and bone development. J Cell Sci 2009;122:716-26. https://doi.org/10.1242/jcs.042770
  7. Kim EK, Lim S, Park JM, Seo JK, Kim JH, Kim KT, et al. Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J Cell Physiol 2012;227:1680-7. https://doi.org/10.1002/jcp.22892
  8. Chuang CK, Sung LY, Hwang SM, Lo WH, Chen HC, Hu YC. Baculovirus as a new gene delivery vector for stem cell engineering and bone tissue engineering. Gene Ther 2007;14:1417-24. https://doi.org/10.1038/sj.gt.3302996
  9. Han D, Sun X, Zhang X, Tang T, Dai K. Ectopic osteogenesis by ex vivo gene therapy using beta tricalcium phosphate as a carrier. Connect Tissue Res 2008;49:343-50. https://doi.org/10.1080/03008200802325029
  10. Kang Q, Song WX, Luo Q, Tang N, Luo J, Luo X, et al. A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells. Stem Cells Dev 2009;18:545-59. https://doi.org/10.1089/scd.2008.0130
  11. Kang Y, Liao WM, Yuan ZH, Sheng PY, Zhang LJ, Yuan XW, et al. In vitro and in vivo induction of bone formation based on adeno-associated virus-mediated BMP-7 gene therapy using human adipose-derived mesenchymal stem cells. Acta Pharmacol Sin 2007;28:839-49. https://doi.org/10.1111/j.1745-7254.2007.00583.x
  12. Kemmis CM, Vahdati A, Weiss HE, Wagner DR. Bone morphogenetic protein 6 drives both osteogenesis and chondrogenesis in murine adipose-derived mesenchymal cells depending on culture conditions. Biochem Biophys Res Commun 2010;401:20-5. https://doi.org/10.1016/j.bbrc.2010.08.135
  13. Li J, Li Y, Ma S, Gao Y, Zuo Y, Hu J. Enhancement of bone formation by BMP-7 transduced MSCs on biomimetic nano-hydroxyapatite/polyamide composite scaffolds in repair of mandibular defects. J Biomed Mater Res A 2010;95:973-81.
  14. Murray SJ, Santangelo KS, Bertone AL. Evaluation of early cellular influences of bone morphogenetic proteins 12 and 2 on equine superficial digital flexor tenocytes and bone marrow-derived mesenchymal stem cells in vitro. Am J Vet Res 2010;71:103-14. https://doi.org/10.2460/ajvr.71.1.103
  15. Qi MC, Sun H, Hu J, Zou SJ, Zhao Q, Li JH. Osteogenic differentiation of rat bone marrow mesenchymal stem cell after transfection with recombinant pAd-bone morphogenetic protein-7. Zhonghua Kou Qiang Yi Xue Za Zhi 2007;42:245-8.
  16. Shen B, Wei A, Whittaker S, Williams LA, Tao H, Ma DD, et al. The role of BMP-7 in chondrogenic and osteogenic differentiation of human bone marrow multipotent mesenchymal stromal cells in vitro. J Cell Biochem 2010;109:406-16.
  17. Lee SJ, Kang SW, Do HJ, Han I, Shin DA, Kim JH, et al. Enhancement of bone regeneration by gene delivery of BMP2/Runx2 bicistronic vector into adipose-derived stromal cells. Biomaterials 2010;31:5652-9. https://doi.org/10.1016/j.biomaterials.2010.03.019
  18. Cui F, Wang X, Liu X, Dighe AS, Balian G, Cui Q. VEGF and BMP-6 enhance bone formation mediated by cloned mouse osteoprogenitor cells. Growth Factors 2010;28:306-17. https://doi.org/10.3109/08977194.2010.484423
  19. Shi Z, Fan L, Qiang H, Tang Y, Wang K, Dang X. Study on biological activity of recombinant adeno-associated virus vector co-expressing human vascular endothelial growth factor 165 and human bone morphogenetic protein 7 genes in vitro. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2010;24:415-9.
  20. Zhang C, Ma Q, Qiang H, Li M, Dang X, Wang K. Study on effect of recombinant adeno-associated virus vector co-expressing human vascular endothelial growth factor 165 and human bone morphogenetic protein 7 genes on bone regeneration and angiopoiesis in vivo. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2010;24:1449-54.
  21. Wang JJ, Ye F, Cheng LJ, Shi YJ, Bao J, Sun HQ, et al. Osteo genic differentiation of mesenchymal stem cells promoted by overexpression of connective tissue growth factor. J Zhejiang Univ Sci B 2009;10:355-67. https://doi.org/10.1631/jzus.B0820252
  22. Wu L, Zhu F, Wu Y, Lin Y, Nie X, Jing W, et al. Dentin sialophosphoprotein-promoted mineralization and expression of odontogenic genes in adipose-derived stromal cells. Cells Tissues Organs 2008;187:103-12. https://doi.org/10.1159/000110079
  23. Cucchiarini M, Ekici M, Schetting S, Kohn D, Madry H. Metabolic activities and chondrogenic differentiation of human mesenchymal stem cells following recombinant adeno-associated virus-mediated gene transfer and overexpression of fibroblast growth factor 2. Tissue Eng Part A 2011;17:1921-33. https://doi.org/10.1089/ten.tea.2011.0018
  24. Miraoui H, Oudina K, Petite H, Tanimoto Y, Moriyama K, Marie PJ. Fibroblast growth factor receptor 2 promotes osteogenic differentiation in mesenchymal cells via ERK1/2 and protein kinase C signaling. J Biol Chem 2009;284:4897-904. https://doi.org/10.1074/jbc.M805432200
  25. Morito A, Kida Y, Suzuki K, Inoue K, Kuroda N, Gomi K, et al. Effects of basic fibroblast growth factor on the development of the stem cell properties of human dental pulp cells. Arch Histol Cytol 2009;72:51-64. https://doi.org/10.1679/aohc.72.51
  26. Oh SA, Lee HY, Lee JH, Kim TH, Jang JH, Kim HW, et al. Collagen three-dimensional hydrogel matrix carrying basic fibroblast growth factor for the cultivation of mesenchymal stem cells and osteogenic differentiation. Tissue Eng Part A 2012;18:1087-100. https://doi.org/10.1089/ten.tea.2011.0360
  27. Hamidouche Z, Hay E, Vaudin P, Charbord P, Schule R, Marie PJ, et al. FHL2 mediates dexamethasone-induced mesenchymal cell differentiation into osteoblasts by activating Wnt/beta-catenin signaling-dependent Runx2 expression. FASEB J 2008;22:3813-22. https://doi.org/10.1096/fj.08-106302
  28. Zeng Q, Li X, Beck G, Balian G, Shen FH. Growth and differentiation factor-5 (GDF-5) stimulates osteogenic differentiation and increases vascular endothelial growth factor (VEGF) levels in fat-derived stromal cells in vitro. Bone 2007;40:374-81. https://doi.org/10.1016/j.bone.2006.09.022
  29. Hung FC, Chang Y, Lin-Chao S, Chao CC. Gas7 mediates the differentiation of human bone marrow-derived mesenchymal stem cells into functional osteoblasts by enhancing Runx2-dependent gene expression. J Orthop Res 2011;29:1528-35. https://doi.org/10.1002/jor.21425
  30. Cai JQ, Huang YZ, Chen XH, Xie HL, Zhu HM, Tang L, et al. Sonic hedgehog enhances the proliferation and osteogenic differentiation of bone marrow-derived mesenchymal stem cells. Cell Biol Int 2012;36:349-55. https://doi.org/10.1042/CBI20110284
  31. Sharff KA, Song WX, Luo X, Tang N, Luo J, Chen J, et al. Hey1 basic helix-loop-helix protein plays an important role in mediating BMP9-induced osteogenic differentiation of mesenchymal progenitor cells. J Biol Chem 2009;284:649-59. https://doi.org/10.1074/jbc.M806389200
  32. Barhanpurkar AP, Gupta N, Srivastava RK, Tomar GB, Naik SP, Joshi SR, et al. IL-3 promotes osteoblast differentiation and bone formation in human mesenchymal stem cells. Biochem Biophys Res Commun 2012;418:669-75. https://doi.org/10.1016/j.bbrc.2012.01.074
  33. Um S, Choi JR, Lee JH, Zhang Q, Seo B. Effect of leptin on differentiation of human dental stem cells. Oral Dis 2011;17:662-9. https://doi.org/10.1111/j.1601-0825.2011.01820.x
  34. Zhang ZM, Jiang LS, Jiang SD, Dai LY. Osteogenic potential and responsiveness to leptin of mesenchymal stem cells between postmenopausal women with osteoarthritis and osteoporosis. J Orthop Res 2009;27:1067-73. https://doi.org/10.1002/jor.20846
  35. Bernardini C, Saulnier N, Parrilla C, Pola E, Gambotto A, Michetti F, et al. Early transcriptional events during osteogenic differentiation of human bone marrow stromal cells induced by Lim mineralization protein 3. Gene Expr 2010;15:27-42. https://doi.org/10.3727/105221610X12819686555097
  36. Lin Z, Navarro VP, Kempeinen KM, Franco LM, Jin Q, Sugai JV, et al. LMP1 regulates periodontal ligament progenitor cell proliferation and differentiation. Bone 2010;47:55-64. https://doi.org/10.1016/j.bone.2010.03.013
  37. Lin Z, Rios HF, Park CH, Taut AD, Jin Q, Sugai JV, et al. LIM domain protein-3 (LMP3) cooperates with BMP7 to promote tissue regeneration by ligament progenitor cells. Gene Ther 2013;20:1-6. https://doi.org/10.1038/gt.2011.203
  38. Drabek K, van de Peppel J, Eijken M, van Leeuwen JP. GPM6B regulates osteoblast function and induction of mineralization by controlling cytoskeleton and matrix vesicle release. J Bone Miner Res 2011;26:2045-51. https://doi.org/10.1002/jbmr.435
  39. Rifas L. The role of noggin in human mesenchymal stem cell differentiation. J Cell Biochem 2007;100:824-34. https://doi.org/10.1002/jcb.21132
  40. Song HY, Jeon ES, Kim JI, Jung JS, Kim JH. Oncostatin M promotes osteogenesis and suppresses adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells. J Cell Biochem 2007;101:1238-51. https://doi.org/10.1002/jcb.21245
  41. Wu L, Wu Y, Lin Y, Jing W, Nie X, Qiao J, et al. Osteogenic differentiation of adipose derived stem cells promoted by overexpression of osterix. Mol Cell Biochem 2007;301:83-92. https://doi.org/10.1007/s11010-006-9399-9
  42. Lee YM, Shin SI, Shin KS, Lee YR, Park BH, Kim EC. The role of sirtuin 1 in osteoblastic differentiation in human periodontal ligament cells. J Periodontal Res 2011;46:712-21. https://doi.org/10.1111/j.1600-0765.2011.01394.x
  43. Miyamoto S, Cooper L, Watanabe K, Yamamoto S, Inoue H, Mishima K, et al. Role of retinoic acid-related orphan receptor-alpha in differentiation of human mesenchymal stem cells along with osteoblastic lineage. Pathobiology 2010;77:28-37. https://doi.org/10.1159/000272952
  44. Pan K, Sun Q, Zhang J, Ge S, Li S, Zhao Y, et al. Multilineage differentiation of dental follicle cells and the roles of Runx2 over-expression in enhancing osteoblast/cementoblast-related gene expression in dental follicle cells. Cell Prolif 2010;43:219-28. https://doi.org/10.1111/j.1365-2184.2010.00670.x
  45. de Gorter DJ, van Dinther M, Korchynskyi O, ten Dijke P. Biphasic effects of transforming growth factor β on bone morphogenetic protein-induced osteoblast differentiation. J Bone Miner Res 2011;26:1178-87. https://doi.org/10.1002/jbmr.313
  46. Cho HH, Shin KK, Kim YJ, Song JS, Kim JM, Bae YC, et al. NF-kappaB activation stimulates osteogenic differentiation of mesenchymal stem cells derived from human adipose tissue by increasing TAZ expression. J Cell Physiol 2010;223:168-77.
  47. Hess K, Ushmorov A, Fiedler J, Brenner RE, Wirth T. TNFalpha promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-kappaB signaling pathway. Bone 2009;45:367-76. https://doi.org/10.1016/j.bone.2009.04.252
  48. Huang H, Zhao N, Xu X, Xu Y, Li S, Zhang J, et al. Dose-specific effects of tumor necrosis factor alpha on osteogenic differentiation of mesenchymal stem cells. Cell Prolif 2011;44:420-7. https://doi.org/10.1111/j.1365-2184.2011.00769.x
  49. Paula-Silva FW, Ghosh A, Silva LA, Kapila YL. TNF-alpha promotes an odontoblastic phenotype in dental pulp cells. J Dent Res 2009;88:339-44. https://doi.org/10.1177/0022034509334070
  50. Miraoui H, Severe N, Vaudin P, Pages JC, Marie PJ. Molecular silencing of Twist1 enhances osteogenic differentiation of murine mesenchymal stem cells: implication of FGFR2 signaling. J Cell Biochem 2010;110:1147-54. https://doi.org/10.1002/jcb.22628
  51. Peng L, Ren LB, Dong G, Wang CL, Xu P, Ye L, et al. Wnt5a promotes differentiation of human dental papilla cells. Int Endod J 2010;43:404-12. https://doi.org/10.1111/j.1365-2591.2010.01693.x
  52. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, et al. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 2000;20:8783-92. https://doi.org/10.1128/MCB.20.23.8783-8792.2000
  53. Li Y, Li A, Strait K, Zhang H, Nanes MS, Weitzmann MN. Endogenous TNFalpha lowers maximum peak bone mass and inhibits osteoblastic Smad activation through NF-kappaB. J Bone Miner Res 2007;22:646-55. https://doi.org/10.1359/jbmr.070121
  54. Janssens K, ten Dijke P, Janssens S, Van Hul W. Transforming growth factor-beta1 to the bone. Endocr Rev 2005;26:743-74. https://doi.org/10.1210/er.2004-0001
  55. Tang Y, Wu X, Lei W, Pang L, Wan C, Shi Z, et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 2009;15:757-65. https://doi.org/10.1038/nm.1979
  56. Ebisawa T, Tada K, Kitajima I, Tojo K, Sampath TK, Kawabata M, et al. Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation. J Cell Sci 1999;112:3519-27.
  57. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, Zhao Q, Pukac L, et al. BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 2007;120:964-72. https://doi.org/10.1242/jcs.002949
  58. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000;100:197-207. https://doi.org/10.1016/S0092-8674(00)81558-5

Cited by

  1. Secretory leukocyte protease inhibitor promotes differentiation and mineralization of MC3T3-E1 preosteoblasts on a titanium surface vol.14, pp.2, 2013, https://doi.org/10.3892/mmr.2016.5381
  2. Cross-sectional study of the association between serum perfluorinated alkyl acid concentrations and dental caries among US adolescents (NHANES 1999–2012) vol.9, pp.2, 2013, https://doi.org/10.1136/bmjopen-2018-024189
  3. Effets de l’inhibition post-natale de RANKL sur l’éruption et la formation radiculaire des molaires de souris C57BL/6 vol.90, pp.1, 2013, https://doi.org/10.1051/orthodfr/2019008
  4. Influence of resveratrol application with pulp‐capping materials on the genetic expression levels of stem cells vol.53, pp.9, 2013, https://doi.org/10.1111/iej.13345