Highly efficient multipotent differentiation of human periodontal ligament fibroblasts induced by combined BMP4 and hTERT gene transfer

Gene Therapy

Volumn 18, Issue 5, 2011, Pages 452-461

  Mi, H W ^a   Lee, M C ^a   Fu, E ^b   Chow, L P ^c   Lin, C P ^a  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^b TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

BMP4; differentiation efficiency; hTERT; human periodontal ligament fibroblast

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; COMPLEMENTARY DNA; NOGGIN; RECOMBINANT BONE MORPHOGENETIC PROTEIN 4; SMAD PROTEIN; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ASSAY; ENZYME PHOSPHORYLATION; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; GENE TRANSFER; LIGAMENT; MOUSE; NONHUMAN; PERIODONTIUM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TISSUE REGENERATION; WESTERN BLOTTING;

ADOLESCENT; ADULT; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELL TRANSPLANTATION; FIBROBLASTS; HUMANS; MICE; MICE, SCID; MULTIPOTENT STEM CELLS; NEUROGENESIS; OSTEOGENESIS; PERIODONTAL LIGAMENT; TELOMERASE; TRANSFECTION;

MUS;

EID: 79955935666     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2010.158     Document Type: Article

References (45)

1. Lekic PC, Rajshankar D, Chen H, Tenenbaum H, McCulloch CA. Transplantation of labeled periodontal ligament cells promotes regeneration of alveolar bone. Anat Rec 2001; 262: 193-202. (Pubitemid 32147736)
2. Saito Y, Yoshizawa T, Takizawa F, Ikegame M, Ishibashi O, Okuda K et al. A cell line with characteristics of the periodontal ligament fibroblasts is negatively regulated for mineralization and Runx2/Cbfa1/Osf2 activity, part of which can be overcome by bone morphogenetic protein-2. J Cell Sci 2002; 115: 4191-4200. (Pubitemid 35446813)
3. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004; 364: 149-155. (Pubitemid 38891686)
4. Lindroos B, Maenpaa K, Ylikomi T, Oja H, Suuronen R, Miettinen S. Characterisation of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 2008; 368: 329-335.
5. Techawattanawisal W, Nakahama K, Komaki M, Abe M, Takagi Y, Morita I. Isolation of multipotent stem cells from adult rat periodontal ligament by neurosphere-forming culture system. Biochem Biophys Res Commun 2007; 357: 917-923. (Pubitemid 46693659)
6. Tomokiyo A, Maeda H, Fujii S, Wada N, Shima K, Akamine A. Development of a multipotent clonal human periodontal ligament cell line. Differentiation 2008; 76: 337-347. (Pubitemid 351520929)
7. Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 2006; 1: e79.
8. Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM et al. Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 2008; 26: 1065-1073.
9. Fujii S, Maeda H, Wada N, Kano Y, Akamine A. Establishing and characterizing human periodontal ligament fibroblasts immortalized by SV40T-antigen and hTERT gene transfer. Cell Tissue Res 2006; 324: 117-125. (Pubitemid 43320247)
10. Kamata N, Fujimoto R, Tomonari M, Taki M, Nagayama M, Yasumoto S. Immortaliza¬tion of human dental papilla, dental pulp, periodontal ligament cells and gingival fibroblasts by telomerase reverse transcriptase. J Oral Pathol Med 2004; 33: 417-423. (Pubitemid 38988197)
11. Fujii S, Maeda H, Wada N, Tomokiyo A, Saito M, Akamine A. Investigating a clonal human periodontal ligament progenitor/stem cell line in vitro and in vivo. J Cell Physiol 2008; 215: 743-749. (Pubitemid 351632696)
12. Coura GS, Garcez RC, de Aguiar CB, Alvarez-Silva M, Magini RS, Trentin AG. Human periodontal ligament: a niche of neural crest stem cells. J Periodontal Res 2008; 43: 531-536.
13. Kang SK, Putnam L, Dufour J, Ylostalo J, Jung JS, Bunnell BA. Expression of telomerase extends the lifespan and enhances osteogenic differentiation of adipose tissue-derived stromal cells. Stem Cells 2004; 22: 1356-1372. (Pubitemid 39636411)
14. Gronthos S, Chen S, Wang CY, Robey PG, Shi S. Telomerase accelerates osteogenesis of bone marrow stromal stem cells by upregulation of CBFA1, osterix, and osteocalcin. J Bone Miner Res 2003; 18: 716-722. (Pubitemid 36899321)
15. Mori T, Kiyono T, Imabayashi H, Takeda Y, Tsuchiya K, Miyoshi S et al. Combination of hTERT and bmi-1, E6, or E7 induces prolongation of the life span of bone marrow stromal cells from an elderly donor without affecting their neurogenic potential. Mol Cell Biol 2005; 25: 5183-5195. (Pubitemid 40781116)
16. Isenmann S, Cakouros D, Zannettino A, Shi S, Gronthos S. hTERT transcription is repressed by Cbfa1 in human mesenchymal stem cell populations. J Bone Miner Res 2007; 22: 897-906. (Pubitemid 351339750)
17. Varga AC, Wrana JL. The disparate role of BMP in stem cell biology. Oncogene 2005; 24: 5713-5721. (Pubitemid 43086131)
18. Schmierer B, Hill CS. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 2007; 8: 970-982. (Pubitemid 350174642)
19. Chen HL, Panchision DM. Concise review: bone morphogenetic protein pleiotropism in neural stem cells and their derivatives\alternative pathways, convergent signals. Stem Cells 2007; 25: 63-68. (Pubitemid 46052975)
20. Okamoto M, Murai J, Yoshikawa H, Tsumaki N. Bone morphogenetic proteins in bone stimulate osteoclasts and osteoblasts during bone development. J Bone Miner Res 2006; 21: 1022-1033. (Pubitemid 43962831)
21. Weible II MW, Chan-Ling T. Phenotypic characterization of neural stem cells from human fetal spinal cord: synergistic effect of LIF and BMP4 to generate astrocytes. Glia 2007; 55: 1156-1168. (Pubitemid 47204207)
22. Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJ, Tahan SR. Increased expression of stem cell markers in malignant melanoma. Mod Pathol 2007; 20: 102-107. (Pubitemid 44967955)
23. Singh S, Jones BJ, Crawford R, Xiao Y. Characterization of a mesenchymal-like stem cell population from osteophyte tissue. Stem Cells Dev 2008; 17: 245-254. (Pubitemid 351630176)
24. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000; 61: 364-370. (Pubitemid 30620221)
25. Munoz-Elias G, Woodbury D, Black IB. Marrow stromal cells, mitosis, and neuronal differentiation: stem cell and precursor functions. Stem Cells 2003; 21: 437-448. (Pubitemid 36793486)
26. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009; 219: 667-676.
27. Zheng W, Wang S, Ma D, Tang L, Duan Y, Jin Y. Loss of proliferation and differentiation capacity of aged human periodontal ligament stem cells and rejuvenation by exposure to the young extrinsic environment. Tissue Eng Part A 2009; 15: 2363-2371.
28. Kudo Y, Hiraoka M, Kitagawa S, Miyauchi M, Kakuo S, Zhao M et al. Establishment of human cementifying fibroma cell lines by transfection with temperature-sensitive simian virus-40 T-antigen gene and hTERT gene. Bone 2002; 30: 712-717. (Pubitemid 34467992)
29. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872. (Pubitemid 350138099)
30. Shi S, Gronthos S, Chen S, Reddi A, Counter CM, Robey PG et al. Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nat Biotechnol 2002; 20: 587-591. (Pubitemid 34595152)
31. Abdallah BM, Haack-Sorensen M, Burns JS, Elsnab B, Jakob F, Hokland P et al. Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite [corrected] extensive proliferation. Biochem Biophys Res Commun 2005; 326: 527-538. (Pubitemid 39642757)
32. Yang YX, Miao ZC, Zhang HJ, Wang Y, Gao JX, Feng MF. Establishment and charac-terization of a human telomerase catalytic subunit-transduced fetal bone marrow-derived osteoblastic cell line. Differentiation 2007; 75: 24-34. (Pubitemid 46115411)
33. Zhao X, Malhotra GK, Lele SM, Lele MS, West WW, Eudy JD et al. Te lo me ra se-immortalized human mammary stem/progenitor cells with ability to self-renew and differentiate. Proc Natl Acad Sci USA 2009; 107: 14146-14151.
34. Goldman O, Feraud O, Boyer-Di Ponio J, Driancourt C, Clay D, Le Bousse-Kerdiles MC et al. A boost of BMP4 accelerates the commitment of human embryonic stem cells to the endothelial lineage. Stem Cells 2009; 27: 1750-1759.
35. Li JZ, Li H, Sasaki T, Holman D, Beres B, Dumont RJ et al. Osteogenic potential of five different recombinant human bone morphogenetic protein adenoviral vectors in the rat. Gene Therapy 2003; 10: 1735-1743. (Pubitemid 37121045)
36. Samee M, Kasugai S, Kondo H, Ohya K, Shimokawa H, Kuroda S. Bone morphogenetic protein-2 (BMP-2) and vascular endothelial growth factor (VEGF) transfection to human periosteal cells enhances osteoblast differentiation and bone formation. J Pharmacol Sci 2008; 108: 18-31.
37. Widera D, Grimm WD, Moebius JM, Mikenberg I, Piechaczek C, Gassmann G et al. Highly efficient neural differentiation of human somatic stem cells, isolated by minimally invasive periodontal surgery. Stem Cells Dev 2007; 16: 447-460. (Pubitemid 47016230)
38. 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.
39. Hiraga T, Ninomiya T, Hosoya A, Takahashi M, Nakamura H. Formation of bone-like mineralized matrix by periodontal ligament cells in vivo: a morphological study in rats. J Bone Miner Metab 2009; 27: 149-157.
40. Shen HC, Peng H, Usas A, Gearhart B, Cummins J, Fu FH et al. Ex vivo gene therapy-induced endochondral bone formation: comparison of muscle-derived stem cells and different subpopulations of primary muscle-derived cells. Bone 2004; 34: 982-992. (Pubitemid 38749235)
41. Chen YL, Chen PK, Jeng LB, Huang CS, Yang LC, Chung HY et al. Periodontal regeneration using ex vivo autologous stem cells engineered to express the BMP-2 gene: an alternative to alveolaplasty. Gene Therapy 2008; 15: 1469-1477.
42. Fatherazi S, Matsa-Dunn D, Foster BL, Rutherford RB, Somerman MJ, Presland RB. Phosphate regulates osteopontin gene transcription. J Dent Res 2009; 88: 39-44.
43. Komaki M, Karakida T, Abe M, Oida S, Mimori K, Iwasaki K et al. Twist negatively regulates osteoblastic differentiation in human periodontal ligament cells. J Cell Biochem 2007; 100: 303-314. (Pubitemid 46146081)
44. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA. Creation of human tumour cells with defined genetic elements. Nature 1999; 400: 464-468. (Pubitemid 29361801)
45. Krebsbach PH, Kuznetsov SA, Satomura K, Emmons RV, Rowe DW, Robey PG. Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts. Transplantation 1997; 63: 1059-1069. (Pubitemid 27190967)