The difference on the osteogenic differentiation between periodontal ligament stem cells and bone marrow mesenchymal stem cells under inflammatory microenviroments

Differentiation

Volumn 88, Issue 4-5, 2014, Pages 97-105

  Zhang, Jing ^a   Li, Zhi Gang ^a   Si, Ya Meng ^a   Chen, Bin ^a   Meng, Jian ^a  

^a XUZHOU CENTRAL HOSPITAL   (China)

Author keywords

Bone marrow mesenchymal stem cells; Inflammation; Osteogenic differentiation; Periodontal ligament stem cells

Indexed keywords

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; CELL SURFACE MARKER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; RUNX2 PROTEIN, HUMAN;

ADIPOGENESIS; ADULT; ARTICLE; BONE DEVELOPMENT; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMING UNIT; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MICROENVIRONMENT; OSTEOGENIC DIFFERENTIATION; PERIODONTAL LIGAMENT; PERIODONTAL LIGAMENT STEM CELL; STEM CELL; BONE REGENERATION; CELL CULTURE; CYTOLOGY; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; TUMOR MICROENVIRONMENT;

ADIPOGENESIS; ALKALINE PHOSPHATASE; BONE REGENERATION; CELL PROLIFERATION; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; CORE BINDING FACTOR ALPHA 1 SUBUNIT; HUMANS; INFLAMMATION; INTEGRIN-BINDING SIALOPROTEIN; MESENCHYMAL STROMAL CELLS; NF-KAPPA B; OSTEOGENESIS; PERIODONTAL LIGAMENT; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84923037825     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2014.10.001     Document Type: Article

References (67)

1. Böcker W., Docheva D., Prall W.C., Egea V., Pappou E., Rossmann O., Popov.C., Mutschler W., Ries C., Schieker M. IKK-2 is required for TNF-α-induced invasion and proliferation of human mesenchymal stem cells. J. Mol. Med. (Berlin) 2008, 86:1183-1192.
2. Bonizzi G., Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004, 25:280-288.
3. Boyce B.F., Li P., Yao Z., Zhang Q., Badell I.R., Schwarz E.M., O_Teles R.P., Likhari V., Socransky S.S., Haffajee A.D. Salivary cytokine levels in subjects with chronic periodontitis and in periodontally healthy individuals: A cross-sectional study. J. Periodontal. Res. 2009, 44:411-417.
4. Bleicher F., Couble ML., Farges J.C., Couble P., Magloire H. Sequential expression of matrix protein genes in developing rat teeth. Matrix Biol. 1999, 18:133-143.
5. Butler D.M., Piccoli D.S., Hart P.H., Hamilton J.A. Stimulation of human synovial fibroblast DNA synthesis by recombinant human cytokines. J. Rheumatol. 1988, 15:1463-1470.
6. Chang J., Wang Z., Tang E., Fan Z., McCauley L., Franceschi R., Guan K., Krebsbach P.H., Wang C.Y. Inhibition of osteoblastic bone formation by nuclear factor-kappaβ. Nat. Med 2009, 15:682-689.
7. Chen F.M., Sun H.H., Lu H., Yu Q. Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials 2012, 33:6320-6644.
8. Chen X., Hu C., Wang G., Li L., Kong X., Ding Y., Jin Y. Nuclear factor-κβ modulates osteogenesis of periodontal ligament stem cells through competition with β-catenin signaling in inflammatory microenvironments. Cell Death Dis 2013, 4:e510.
9. Chung V.H., Chen A.Y., Jeng L.B., Kwan C.C., Cheng S.H., Chang S.C. Engineered autologous bone marrow mesenchymal stem cells: alternative to cleft alveolar bone graft surgery. J. Craniofac. Surg 2012, 23:1558-1563.
10. Deans R.J., Moseley A.B. Mesenchymal stem cells: biology and potential clinical uses. Exp. Hematol. 2000, 28:875-884.
11. Ding J., Ghali O., Lencel P., Broux O., Chauveau C., Devedjian J.C., Hardouin P., Magne D. TNF-α and IL-1β inhibit RUNX2 and collagen expression but increase alkaline phosphatase activity and mineralization in human mesenchymal stem cells. Life Sci. 2009, 84:499-504.
12. Ducy P., Zhang R., Geoffroy V., Ridall A.L., Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997, 89:747-754.
13. Ghosh S., May M.J., Kopp E.B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 1998, 16:225-260.
14. Gilbert L., He X., Farmer P., Rubin J., Drissi H., van Wijnen A.J., Lian J.B., Stein G.S., Nanes M.S. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J. Biol. Chem. 2002, 277:2695-7201.
15. Glass G.E., Chan J.K., Freidin A., Feldmann M., Horwood N.J., Nanchahal J. TNF-alpha promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells. Proc. Natl. Acad. Sci. U.S.A 2011, 108:1585-1590.
16. Golding B., Pillemer S.R., Roussou P., Peters E.A., Tsokos G.C., Ballow J.E., Hoffman T. Inverse relationship between proliferation and differentiation in a human TNP-specific B cell line. Cell cycle dependence of antibody secretion. J. Immunol. 1988, 141:2564-2568.
17. Gronthos S., Mankani M., Brahim J., Robey P.G., Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A 2000, 97:13625-13630.
18. Haynesworth S.E., Goshima J., Goldberg V.M., Caplan A.I. Characterization of cells with osteogenic potential from human marrow. Bone 1992, 13:81-88.
19. Hess K., Ushmorov A., Fiedler J., Brenner R.E., Wirth T. TNFα promotes osteogenic differentiation of human mesenchymal stem cells by triggering the NF-κβ signaling pathway. Bone 2009, 45:367-376.
20. Huang R.L., Yuan Y., Tu J., Zou G.M., Li Q. Opposing TNF-α/IL-1β- and BMP-2-activated MAPK signaling pathways converge on Runx2 to regulate BMP-2-induced osteoblastic differentiation. Cell Death Dis 2014, 5:e1187.
21. Huo N., Tang L., Yang Z., Qian H., Wang Y., Han C., Gu Z., Duan Y., Jin Y. Differentiation of dermal multipotent cells into odontogenic lineage induced by embryonic and neonatal tooth germ cell conditioned medium. Stem Cells Dev. 2010, 19:93-104.
22. Karin M., Greten F.R. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 2005, 5:749-759.
23. Kassem M., Abdallah B.M. Human bone-marrow-derived mesenchymal stem cells: biological characteristics and potential role in therapy of degenerative diseases. Cell Tissue Res. 2008, 331:157-163.
24. Kim J.H., Liu X., Wang J., Chen X., Zhang H., Kim S.H., Cui J., Li R., Zhang W., Kong Y., Zhang J., Shui W., Lamplot J., Rogers M.R., Zhao C., Wang N., Rajan P., Tomal J., Statz J., Wu N., Luu H.H., Haydon R.C., He T.C. Wnt signaling in bone formation and its therapeutic potential for bone diseases. Ther. Adv. Musculoskelet. Dis 2013, 5:13-31.
25. Kim S.H., Kim K.H., Seo B.M., Koo K.T., Kim T.I., Seol Y.J., Ku Y., Rhyu I.C., Chung C.P., Lee Y.M. Alveolar bone regeneration by transplantation of periodontal ligament stem cells and bone marrow stem cells in a canine peri-implant defect model: a pilot study. J. Periodontol. 2009, 80:1815-1823.
26. Kornman K.S., Crane A., Wang H.Y., di Giovine F.S., Newman M.G., Pirk F.W., Wilson T.G., Higginbottom F.L., Duff G.W. The interleukin-1 genotype as a severity factor in adult periodontal disease. J. Clin. Periodontol. 1997, 24:72-77.
27. Kramer P.R., Nares S., Kramer S.F., Grogan D., Kaiser M. Mesenchymal stem cells acquire characteristic of cells in the periodontal ligament in vitro. J. Dent. Res. 2004, 83:27-34.
28. Lacey D., Sampey A., Mitchell R., Bucala R., Santos L., Leech M., Morand E. Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor. Arthritis Rheum. 2003, 48:103-109.
29. Lacey D.C., Simmons P.J., Graves S.E., Hamilton J.A. Proinflammatory cytokines inhibit osteogenic differentiation from stem cells: implications for bone repair during inflammation. Osteoarthritis Cartilage 2009, 17:735-742.
30. Lencel P., Delplace S., Hardouin P., Magne D. TNF-α stimulates alkaline phosphatase and mineralization through PPARγ inhibition in human osteoblasts. Bone 2011, 48:242-249.
31. Li C., Li B., Dong Z., Gao L., He X., Liao L., Hu C., Wang Q., Jin Y. Lipopolysaccharide differentially affects the osteogenic differentiation of periodontal ligament stem cells and bone marrow mesenchymal stem cells through Toll-like receptor 4 mediated nuclear factor kappaB pathway. Stem Cell Res. Ther 2014, 27:67.
32. Liang Y., Zhou Y., Shen P. NF-kappaB and its regulation on the immune system. Cell. Mol. Immunol. 2004, 1:343-350.
33. Lin FH., Chang J.B., McGuire M.H., Yee J.A., Brigman B.E. Biphasic effects of interleukin-1beta on osteoblast differentiation in vitro. J. Orthop. Res 2010, 28:958-964.
34. Lin G.L., Hankenson K.D. Integration of BMP, Wnt, and notch signaling pathways in osteoblast differentiation. J. Cell. Biochem. 2011, 112:3491-3501.
35. Liu D.D., Zhang J.C., Zhang Q., Wang S.X., Yang M.S. TGF-β/BMP signaling pathway is involved in cerium-promoted osteogenic differentiation of mesenchymal stem cells. J. Cell. Biochem. 2013, 114:1105-1114.
36. Liu D., Xu J., Liu O., Fan Z., Liu Y., Wang F., Ding G., Wei F, Zhang C., Wang S. Mesenchymal stem cells derived from inflamed periodontal ligaments exhibit impaired immunomodulation. J. Clin. Periodontol. 2012, 39:1174-1182.
37. Liu N., Shi S., Deng M., Tang L., Zhang G., Liu N., Ding B., Liu W., Liu Y., Shi H., Liu L., Jin Y. High levels of β-catenin signaling reduce osteogenic differentiation of stem cells in inflammatory microenvironments through inhibition of the noncanonical Wnt pathway. J. Bone Miner. Res. 2011, 26:2082-2095.
38. Liu Y., Zheng Y., Ding G., Fang D., Zhang C., Bartold P.M., Gronthos S., Shi S., Wang S. Periodontal ligament stem cell-mediated treatment for periodontitis inminiature swine. Stem Cells 2008, 26:1065-1073.
39. Lu X., Gilbert L., He X., Rubin J., Nanes M.S. Transcriptional regulation of the osterix (Osx, Sp7) promoter by tumor necrosis factor identifies disparate effects of mitogen-activated protein kinase and NF kappa B pathways. J. Biol. Chem. 2006, 281:6297-6306.
40. Marion N.W., Mao J.J. Mesenchymal stem cells and tissue engineering. Methods Enzymol. 2006, 420:339-361.
41. Matsuoka F., Takeuchi I., Agata H., Kagami H., Shiono H., Kiyota Y., Honda H., Kato R. Morphology-based prediction of osteogenic differentiation potential of human mesenchymal stem cells. PLoS One 2013, 8:e55082.
42. Menicanin D., Bartold P.M., Zannettino A.C., Gronthos S. Identification of a common gene expression signature associated with immature clonal mesenchymal cell populations derived from bone marrow and dental tissues. Stem Cells Dev. 2010, 19:1501-1510.
43. Mountziaris P.M., Tzouanas S.N., Mikos A.G. Dose effect of tumor necrosis factor-alpha on in vitro osteogenic differentiation of mesenchymal stem cells on biodegradable polymeric microfiber scaffolds. Biomaterials 2010, 31:1666-1675.
44. Moe K.T., Khairunnisa K., Yin N.O., Chin-Dusting J., Wong P., Wong M.C. Tumor necrosis factor-α-induced nuclear factor kappa B activation in human cardiomyocytes is mediated by NADPH oxidase. J. Physiol. Biochem. 2014, 70:769-779.
45. Mrozik K., Gronthos S., Shi S., Bartold P.M. A method to isolate, purify, and characterize human periodontal ligament stem cells. Methods Mol. Biol. 2010, 666:269-284.
46. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29.
47. Nakase T., Takaoka K., Hirakawa K., Hirota S., Takemura T., Onoue H., Takebayashi K., Kitamura Y., Nomura S. Alterations in the expression of osteonectin, osteopontin and osteocalcin mRNAs during the development of skeletal tissues in vivo. Bone Miner 1994, 26:109-122.
48. Owen M., Friedenstein A.J. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found. Symp. 1988, 136:42-60.
49. Papadopoulou A.1., Yiangou M., Athanasiou E., Zogas N., Kaloyannidis P., Batsis I., Fassas A., Anagnostopoulos A., Yannaki E. Mesenchymal stem cells are conditionally therapeutic in preclinical models of rheumatoid arthritis. Ann. Rheum. Dis. 2012, 71:1733-1740.
50. Park J.Y., Jeon S.H., Choung P.H. Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant. 2011, 20:271-285.
51. Pihlstrom B.L., Michalowicz B.S., Johnson N.W. Periodontal disease. Lancet 2005, 366:1809-1820.
52. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
53. Platt I.D., El-Sohemy A. Regulation of osteoblast and adipocyte differentiation from human mesenchymal stem cells by conjugated linoleic acid. J. Nutr. Biochem. 2009, 20:956-964.
54. Rodríguez J.P., González M., Ríos S., Cambiazo V. Cytoskeletal organization of human mesenchymal stem cells (MSC) changes during their osteogenic differentiation. J. Cell. Biochem. 2004, 93:721-731.
55. Schett G. Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur. J. Clin. Invest. 2011, 41:1361-1366.
56. Seo B.M., Miura M., Gronthos S., Bartold P.M., Batouli S., Brahim J., Young M., Robey P.G., Wang C.Y., Shi S. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004, 364:149-155.
57. Short B., Brouard N., Occhiodoro-Scott T., Ramakrishnan A., Simmons P.J. Mesenchymal stem cells. Arch. Med. Res. 2003, 34:565-571.
58. Soga Y., Nishimura F., Ohyama H., Maeda H., Takashiba S., Murayama Y. Tumor necrosis factor-alpha gene (TNF-α) -1031/-863, -857 single-nucleotide polymorphisms (SNPs) are associated with severe adult periodontitis in Japanese. J. Clin. Periodontol. 2003, 30:524-531.
59. Sommer B., Bickel M., Hofstetter W., Wetterwald A. Expression of matrix proteins during the development of mineralized tissues. Bone 1996, 19:371-380.
60. Tamaki Y., Nakahara T., Ishikawa H., Sato S. In vitro analysis of mesenchymal stem cells derived from human teeth and bone marrow. Odontology 2013, 101:121-132.
61. Welter J.F., Penick K.J., Solchaga L.A. Assessing adipogenic potential of mesenchymal stem cells: a rapid three-dimensional culture screening technique. Stem Cells Int 2013, 2013:806525.
62. Wu G., Cui Y., Ma L., Pan X., Wang X., Zhang B. Repairing cartilage defects with bone marrow mesenchymal stem cells induced by CDMP and TGF-β1. Cell Tissue Bank. 2014, 15:51-57.
63. Xu J., Wu H.F., Ang E.S., Yip K., Woloszyn M., Zheng M.H., Tan R.X. NF-kappa B modulators in osteolytic bone diseases. Cytokine Growth Factor Rev. 2009, 20:7-17.
64. Yang Y., Rossi F.M., Putnins E.E. Periodontal regeneration using engineered bone marrow mesenchymal stromal cells. Biomaterials 2010, 31:8574-8582.
65. Yang Z.H., Zhang X.J., Dang N.N., Ma Z.F., Xu L., Wu J.J., Sun Y.J., Duan Y.Z., Lin Z., Jin Y. Apical tooth germ cell- conditioned medium enhances the differentiation of periodontal ligament stem cells into cementum/periodontal ligament-like tissues. J. Periodont. Res 2009, 44:199-210.
66. Zhang S., Barros S.P., Moretti A.J., Yu N., Zhou J., Preisser J.S., Niculescu M.D., Offenbacher S. Epigenetic regulation of TNFA expression in periodontal disease. J. Periodontol. 2013, 84:1606-1616.
67. Zhao B., Grimes S.N., Li S., Hu X., Ivashkiv L.B. TNF-induced osteoclastogenesis sand inflammatory bone resorption are inhibited by transcription factor RBP-J. J. Exp. Med. 2012, 209:319-334.