Inflammatory environment induces gingival tissue-specific mesenchymal stem cells to differentiate towards a pro-fibrotic phenotype

Biology of the Cell

Volumn 105, Issue 6, 2013, Pages 261-275

  Li, Nan ^a   Liu, Na ^b   Zhou, Jun ^a   Tang, Liang ^a   Ding, Bofu ^a   Duan, Yinzhong ^a   Jin, Yan ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

Extracellular matrix; Gingival mesenchymal stem cells; Inflammatory gingival hyperplasia; Matrix metalloproteinases; TIMPs

Indexed keywords

BETA1 INTEGRIN; COLLAGEN TYPE 1; ENDOGLIN; GELATINASE A; HERMES ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 6; INTERSTITIAL COLLAGENASE; OSTEOCALCIN; THY 1 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GINGIVA; GINGIVA HYPERPLASIA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LAMINA PROPRIA; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TOOTH PULP;

ADULT; CELL DIFFERENTIATION; CELLS, CULTURED; FEMALE; FIBROSIS; GINGIVA; GINGIVAL HYPERPLASIA; HUMANS; INTERLEUKIN-1; INTERLEUKIN-6; MALE; MESENCHYMAL STROMAL CELLS; PHENOTYPE; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84878633906     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201200064     Document Type: Article

References (31)

1. Ahmed, S., Rahman, A., Hasnain, A., Goldberg, V.M. and Haqqi, T.M. (2003) Phenyl N-tert-butylnitrone down-regulates interleukin-1 beta-stimulated matrix metalloproteinase-13 gene expression in human chondrocytes: suppression of c-Jun NH2-terminal kinase, p38-mitogen-activated protein kinase and activating protein-1. J. Pharmacol. Exp. Ther. 305, 981-988
2. Akahane, M., Nakamura, A., Ohgushi, H., Shigematsu, H., Dohi, Y. and Takakura, Y. (2008) Osteogenic matrix sheet-cell transplantation using osteoblastic cell sheet resulted in bone formation without scaffold at an ectopic site. J. Tissue. Eng. Regen. Med. 2, 196-201
3. Al Haj Zen, A., Lafonta, A., Duranda, E., Brasselet, C., Lemarchand, P., Godeau, G. and Gogly, B. (2003) Effect of adenovirus-mediated overexpression of decorin on metalloproteinases, tissue inhibitors of metalloproteinases and cytokines secretion by human gingival fibroblasts. Matrix Biol. 22, 251-258
4. Alhadlaq, A. and Mao, J.J. (2004) Mesenchymal stem cells: isolation and therapeutics. Stem Cells Dev. 13, 436-448
5. Cao, Z., Xiang, J. and Li, C. (2007) A potential role of EMMPRIN by regulating ECM degradation in periodontitis. Med. Hypotheses 69, 1102-1104
6. Chae, H.J., Ha, M.S., Yun, D.H., Pae, H.O., Chung, H.T., Chae, S.W., Jung, Y.K. and Kim, H.R. (2006) Mechanism of cyclosporine-induced overgrowth in gingiva. J. Dent. Res. 85, 515-519
7. Dahan, I.B., Nawrocki, R., Elkaim, M., Soell, A.L., Bolcato-Bellemin, P. and Birembaut, H. (2001) Tenenbaum. Expression of matrix metalloproteinases in healthy and diseased human gingiva1. J. Clin. Periodontol 28, 128-136
8. Ghali, O, Chauveau, C, Hardouin, P, Broux, O. and Devedjian, J.C. (2010) TNF-alpha's effects on proliferation and apoptosis in human mesenchymal stem cells depend on RUNX2 expression. J. Bone Miner Res. 25, 1616-1626
9. Guo, X.K., Zha, W.Q., Kondo, C., Shimojo, N., Yamashita, K., Aoki, T. and Hayakawa, T. (2006) Tissue inhibitors of metalloproteinases-1 (TIMP-1) and -2 (TIMP-2) are major serum factors that stimulate the TIMP-1 gene in human gingival fibroblasts. Biochim Biophys Acta 1763, 296-304
10. Huo, N., Tang, L., Yang, Z., Qian, H., Wang, Y., Han, C., Gu, Z., Duan, Y. and Jin, Y. (2010) Differentiation of dermal multipotent cells into odontogenic lineage induced by embryonic and neonatal tooth germ cell conditioned medium. Stem Cells Dev. 19, 93-104
11. Kastrinaki, M.C., Sidiropoulos, P., Roche, S., Ringe, J., Lehmann, S., Kritikos, H., Vlahava, V.M., Delorme, B., Eliopoulos, G.D., Jorgensen, C., Charbord, P., HäUpl, T., Boumpas, D.T. and Papadaki, H.A. (2008) Functional, molecular and proteomic characterisation of bone marrow mesenchymal stem cells in rheumatoid arthritis. Ann. Rheum. Dis. 67, 741-749
12. Kato, T., Okahashi, N., Kawai, S., Kato, T., Inaba, H., Morisaki, I. and Amano, A. (2005) Impaired degradation of matrix collagen in human gingival fibroblasts by the antiepileptic drug phenytoin. J. Periodontol. 76, 941-950
13. Kim, J.Y., Park, S.H., Cho, K.S., Kim, H.J., Lee, C.K., Park, K.K., Choi, S.H. and Chung, W.Y. (2008) Mechanism of azithromycin treatment on gingival overgrowth. J. Dent. Res. 87, 1075-1079
14. Krishnan, V., Ambili, R., Davidovitch, Z. and Murphy, N.C. (2007) Gingiva and orthodontic treatment. Semin. Orthodont. 13, 257-271
15. Leivonen, S.K., Chantry, A., Hakkinen, L., Han, J. and Kahari, V.M. (2002) Smad3 mediates transforming growth factor-beta-induced collagenase-3 (matrix metalloproteinase-13) expression in human gingival fibroblasts. Evidence for cross-talk between Smad3 and p38 signaling pathways. J. Biol. Chem. 277, 46338-46346
16. Liu, N., Shi, S., Deng, M., Tang, L., Zhang, G., Liu, N., Ding, B., Liu, W., Liu, Y., Shi, H., Liu, L. and Jin, Y. (2011) 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. 26, 2082-2095
17. Liu, Y, Wang, L, Kikuiri, T, Akiyama, K, Chen, C, Xu, X, Yang, R, Chen, W, Wang, S. and Shi, S. (2012) Mesenchymal stem cell-based tissue regeneration is governed by recipient T lymphocytes via IFN-γ and TNF-α. Nat. Med. 17, 1594-1601
18. Liu, Y., Liu, W., Hu, C., Xue, Z., Wang, G., Ding, B., Luo, H., Tang, L., Kong, X., Chen, X., Liu, N., Ding, Y. and Jin, Y. (2011) MiR-17 modulates osteogenic differentiation through a coherent feed-forward loop in mesenchymal stem cells isolated from periodontal ligaments of patients with periodontitis. Stem Cells 29, 1804-1816
19. Nares, S., Ng, M.C., Dill, R.E., Park, B., Cutler, C.W. and Iacopino, A.M. (1996) Cyclosporine A upregulates platelet-derived growth factor B chain in hyperplastic human gingiva. J. Periodontol. 67, 271-278
20. Rossa, C., Jr., Liu, M., Patil, C. and Kirkwood, K.L. (2005) MKK3/6-p38 MAPK negatively regulates murine MMP-13 gene expression induced by IL-1h and TNF-a in immortalized periodontal ligament fibroblasts. Matrix Biol. 24, 478-488
21. Seymour, R.A., Thomason, J.M. and Ellis, J.S. (1996) The pathogenesis of drug-induced gingival overgrowth. J. Clin. Periodontol. 23, 165-175
22. Suzawa, M., Takada, I., Yanagisawa, J., Ohtake, F., Ogawa, S., Yamauchi, T., Kadowaki, T., Takeuchi, Y., Shibuya, H., Gotoh, Y., Matsumoto, K. and Kato, S. (2003) Cytokines suppress adipogenesis and PPAR-gamma function through the TAK1/TAB1/NIK cascade. Nat. Cell Biol. 5, 224-230
23. Tang, L., Li, N., Xie, H. and Jin, Y. (2011) Characterization of mesenchymal stem cells from human normal and hyperplastic gingiva. J. Cell Physiol. 226, 832-842
24. Tewari, M., Tuncay, O.C., Milchman, A., Reddy, P.J., Reddy, C.D., Cressman, D.E., Taub, R., Newton, R.C. and Tewari, D.S. (1996) Association of interleukin-1-induced, NFκB DNA-binding activity with collagenase gene expression in human gingival fibroblasts. Arch. Oral Biol. 41, 461-468
25. Varghese, S. and Canalis, E. (2003) Transcriptional regulation of collagenase-3 by interleukin-1 alpha in osteoblasts. J. Cell. Biochem. 90, 1007-1014
26. Wang, P.L., Azuma, Y., Shinohara, M. and Ohura, K. (2000) Toll-like receptor 4-mediated signal pathway induced by porphyromonas gingivalis lipopolysaccharide in human gingival fibroblasts. Biochim. Biophys. Acta 273, 1161-1167
27. Yang, N., Wang, G., Hu, C., Shi, Y., Liao, L., Shi, S., Cai, Y., Cheng, S., Wang, X., Liu, Y., Tang, L., Ding, Y. and Jin, Y. (2012) TNF-α suppresses the mesenchymal stem cell osteogenesis promoter miR-21 in estrogen deficiency-induced osteoporosis. J. Bone Miner. Res. 28, 559-573
28. Yu, Y.L., Xu, L.H., Wang, J.X., You, H., Yu, Y. and Dong, R. (2010) Influence of lipopolysaccharide on the proliferation rate and the expression of MMPs by the human gingival fibroblasts. J. Modem Stomatol. 24, 60-63
29. Zaragoza, C., Soria, E., López, E., Browning, D., Balbín, M., López-Otín, C. and Lamas, S. (2002) Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide-cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells. Mol. Pharmacol. 62, 927-935
30. Zhao, L., Huang, J., Zhang, H., Wang, Y., Matesic, L.E., Takahata, M., Awad, H., Chen, D., Xing, L. (2011) Tumor necrosis factor inhibits mesenchymal stem cell differentiation into osteoblasts via the ubiquitin E3 ligase Wwp1. Stem Cells 29, 1601-1610
31. Zhou, J., Shi, S., Shi, Y., Xie, H., Chen, L., He, Y., Guo, W., Wen, L. and Jin, Y. (2011) Role of bone marrow-derived progenitor cells in the maintenance and regeneration of dental mesenchymal tissues. J. Cell. Physiol. 226, 2081-2090