Osteogenic differentiation of mesenchymal stem cells promoted by overexpression of connective tissue growth factor

Journal of Zhejiang University: Science B

Volumn 10, Issue 5, 2009, Pages 355-367

  Wang, Jin Jing ^a   Ye, Feng ^a   Cheng, Li Jia ^a   Shi, Yu Jun ^a   Bao, Ji ^a   Sun, Huai Qiang ^a   Wang, Wei ^a   Zhang, Peng ^a   Bu, Hong ^a  

^a SICHUAN UNIVERSITY   (China)

Author keywords

Connective tissue growth factor (CTGF); Gene modification; Mesenchymal stem cells (MSCs); Osteoblasts; Osteogenic differentiation; Overexpression

Indexed keywords

ALKALINE PHOSPHATASE; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; OSTEOCALCIN; SIALOPROTEIN;

ARTICLE; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MODIFICATION; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL DIFFERENTIATION; CELLS, CULTURED; CONNECTIVE TISSUE GROWTH FACTOR; GENETIC ENHANCEMENT; HUMANS; MESENCHYMAL STEM CELLS; OSTEOBLASTS; OSTEOGENESIS; PROMOTER REGIONS, GENETIC; TISSUE ENGINEERING; UP-REGULATION;

EID: 65549150440     PISSN: 16731581     EISSN: 18621783     Source Type: Journal    
DOI: 10.1631/jzus.B0820252     Document Type: Article

References (54)

1. Abreu, J.G., Ketpura, N.I., Reversade, B., de Robertis, E.M., 2002. Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat. Cell Biol., 4(8):599-604. [doi:10.1038/ncb826]
2. Alden, T.D., Varady, P., Kallmes, D.F., Jane, J.A.Jr., Helm, G.A., 2002. Bone morphogenetic protein gene therapy. Spine, 27(16S):S87-S93. [doi:10.1097/00007632-200208151-00016]
3. Arnott, J.A., Nuglozeh, E., Rico, M.C., Arango, H.I., Odgren, P.R., Safadi, F.F., Popoff, S.N., 2007. Connective tissue growth factor (CTGF/ CCN2) is a downstream mediator for TGF-beta1-induced extracellular matrix production in osteoblasts. J. Cell. Physiol., 210(3):843-852. [doi:10.1002/jcp.20917]
4. Betz, V.M., Betz, O.B., Harris, M.B., Vrahas, M.S., Evans, C.H., 2008. Bone tissue engineering and repair by gene therapy. Front Biosci., 13(13):833-841. [doi:10.2741/2724]
5. Beyer Nardi, N., da Silva Meirelles, L., 2006. Mesenchymal Stem Cells: Isolation, in Vitro Expansion and Characterization. In: Stem Cells. Handbook of Experimental Pharmacology. Springer Berlin Heidelberg, Vol. 174, p.249-282. [doi:10.1007/978-3-540-77855-4]
6. Brigstock, D.R., 2002. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis, 5(3):153-165. [doi:10.1023/A:1023823803510]
7. Brigstock, D.R., 2003. The CCN family: A new stimulus package. J. Endocrinol., 178(2):169-175. [doi:10.1677/joe.0.1780169]
8. Brigstock, D.R., Goldschmeding, R., Katsube, K.I., Lam, S.C., Lau, L.F., Lyons, K., Naus, C., Perbal, B., Riser, B., Takigawa, M., Yeger, H., 2003. Proposal for a unified CCN nomenclature. Mol. Pathol., 56(2):127-128. [doi:10.1136/mp.56.2.127]
9. Caterson, E., Nesti, L., Danielson, K., Tuan, R., 2002. Human marrow-derived mesenchymal progenitor cells. Mol. Biotechnol., 20(3):245-256. [doi:10.1385/MB:20:3:245]
10. Chan, J., O'Donoghue, K., de la Fuente, J., Roberts, I.A., Kumar, S., Morgan, J.E., Fisk, N.M., 2005. Human fetal mesenchymal stem cells as vehicles for gene delivery. Stem. Cells, 23(1):93-102. [doi:10.1634/ stemcells.2004-0138]
11. Cho, H.H., Park, H.T., Kim, Y.J., Bae, Y.C., Suh, K.T., Jung, J.S., 2005. Induction of osteogenic differentiation of human mesenchymal stem cells by histone deacetylase inhibitors. J. Cell. Biochem., 96(3):533-542. [doi:10.1002/jcb.20544]
12. Duan, X., Yang, L., Dong, S., Xin, R., Chen, G., Guo, L., 2008. Characterization of EGFP-labeled mesenchymal stem cells and redistribution of allogeneic cells after subcutaneous implantation. Archives of Orthopaedic and Trauma Surgery, 128(7):751-759. [doi:10.1007/ s00402-008-0585-y]
13. Edgar, C.M., Chakravarthy, V., Barnes, G., Kakar, S., Gerstenfeld, L.C., Einhorn, T.A., 2007. Autogenous regulation of a network of bone morphogenetic proteins (BMPs) mediates the osteogenic differentiation in murine marrow stromal cells. Bone, 40(5):1389-1398. [doi:10.1016/ j.bone.2007.01.001]
14. Gamradt, S.C., Lieberman, J.R., 2004. Genetic modification of stem cells to enhance bone repair. Ann. Biomed. Eng., 32(1):136-147. [doi:10.1023/ B:ABME.0000007798.78548.b8]
15. Gersbach, C.A., Le Doux, J.M., Guldberg, R.E., Garcia, A.J., 2006. Inducible regulation of Runx2-stimulated osteogenesis. Gene Ther., 13(11):873-882. [doi:10.1038/sj.gt.3302725]
16. Goessler, U.R., Riedel, K., Hormann, K., Riedel, F., 2006. Perspectives of gene therapy in stem cell tissue engineering. Cells Tissues Organs, 183(4):169-179. [doi:10.1159/000096508]
17. Heng, E.C., Huang, Y., Black, S.A. Jr., Trackman, P.C., 2006. CCN2, connective tissue growth factor, stimulates collagen deposition by gingival fibroblasts via module 3 and alpha6- and beta1 integrins. J. Cell. Biochem., 98(2):409-420. [doi:10.1002/jcb.20810]
18. Howard, D., Buttery, L.D., Shakesheff, K.M., Roberts, S.J., 2008. Tissue engineering: Strategies, stem cells and scaffolds. J. Anat., 213(1):66-72. [doi:10.1111/j.1469-7580.2008.00878.x]
19. Huang, W., Rudkin, G.H., Carlsen, B., Ishida, K., Ghasri, P., Anvar, B., Yamaguchi, D.T., Miller, T.A., 2002. Overexpression of BMP-2 modulates morphology, growth, and gene expression in osteoblastic cells. Exp. Cell Res., 274(2):226-234. [doi:10.1006/excr.2002.5483]
20. Igarashi, M., Kamiya, N., Hasegawa, M., Kasuya, T., Takahashi, T., Takagi, M., 2004. Inductive effects of dexamethasone on the gene expression of Cbfa1, osterix and bone matrix proteins during differentiation of cultured primary rat osteoblasts. J. Mol. Histol., 35(1):3-10. [doi:10.1023/B:HIJO.0000020883.33256.fe]
21. Ivkovic, S., Yoon, B.S., Popoff, S.N., Safadi, F.F., Libuda, D.E., Stephenson, R.C., Daluiski, A., Lyons, K.M., 2003. Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development, 130(12):2779-2791. [doi:10.1242/ dev.00505]
22. Jiang, C.Y., Gui, C., He, A.N., Hu, X.Y., Chen, J., Jiang, Y., Wang, J.A., 2008. Optimal time for mesenchymal stem cell transplantation in rats with myocardial infarction. J. Zhejiang Univ. Sci. B, 9(8):630-637. [doi:10.1631/jzus.B0820004]
23. Kanaan, R.A., Aldwaik, M., Al-Hanbali, O.A., 2006. The role of connective tissue growth factor in skeletal growth and development. Med. Sci. Monit., 12(12):RA277-RA281.
24. Kanczler, J.M., Oreffo, R.O., 2008. Osteogenesis and angiogenesis: The potential for engineering bone. Eur. Cell Mater., 15:100-114.
25. Karp, J.M., Tanaka, T.S., Zohar, R., Sodek, J., Shoichet, M.S., Davies, J.E., Stanford, W.L., 2005. Thrombin mediated migration of osteogenic cells. Bone, 37(3):337-348. [doi:10.1016/j.bone.2005.04.022]
26. Kawaki, H., Kubota, S., Suzuki, A., Yamada, T., Matsumura, T., Mandai, T., Yao, M., Maeda, T., Lyons, K.M., Takigawa, M., 2008. Functional requirement of CCN2 for intramembranous bone formation in embryonic mice. Biochem. Biophys. Res. Commun., 366(2):450-456. [doi:10.1016/ j.bbrc.2007.11.155]
27. Kofron, M.D., Laurencin, C.T., 2006. Bone tissue engineering by gene delivery. Adv. Drug Deliv. Rev., 58(4):555-576. [doi:10.1016/ j.addr.2006.03.008]
28. Kubota, S., Takigawa, M., 2007. Role of CCN2/CTGF/Hcs24 in bone growth. Int. Rev. Cytol., 257:1-41. [doi:10.1016/S0074-7696(07)57001-4]
29. Lee, H.S., Huang, G.T., Chiang, H., Chiou, L.L., Chen, M.H., Hsieh, C.H., Jiang, C.C., 2003. Multipotential mesenchymal ctem cells from femoral cone carrow cear the cite of osteonecrosis. Stem. Cells, 21(2):190-199. [doi:10.1634/stemcells.21-2-190]
30. Lee, R.H., Kim, B., Choi, I., Kim, H., Choi, H.S., Suh, K., Bae, Y.C., Jung, J.S., 2004. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol. Biochem., 14(4-6):311-324. [doi:10.1159/000080341]
31. Lin, Y., Luo, E., Chen, X., Liu, L., Qiao, J., Yan, Z., Li, Z., Tang, W., Zheng, X., Tian, W., 2005. Molecular and cellular characterization during chondrogenic differentiation of adipose tissue-derived stromal cells in vitro and cartilage formation in vivo. J. Cell. Mol. Med., 9(4):929-939. [doi:10.1111/j.1582-4934.2005.tb00389.x]
32. Liu, L.D., Shi, H.J., Jiang, L., Wang, L.C., Ma, S.H., Dong, C.H., Wang, J.J., Zhao, H.L., Liao, Y., Li, Q.H., 2007. The repairing effect of a recombinant human connective-tissue growth factor in a burn-wounded rhesus-monkey (Macaca mulatta) model. Biotechnol. Appl. Biochem., 47(2):105-112. [doi:10.1042/BA20060114]
33. Luft, F.C., 2008. CCN2, the connective tissue growth factor. J. Mol. Med., 86(1):1-3. [doi:10.1007/s00109-007-0287-x]
34. Luo, Q., Kang, Q., Si, W., Jiang, W., Park, J.K., Peng, Y., Li, X., Luu, H.H., Luo, J., Montag, A.G., Haydon, R.C., He, T.C., 2004. Connective tissue growth factor (CTGF) is regulated by WNT and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J. Biol. Chem., 279(53):55958-55968. [doi:10.1074/jbc.M407810200]
35. Mauney, J.R., Volloch, V., Kaplan, D.L., 2005. Role of adult mesenchymal stem cells in bone tissue engineering applications: Current status and future prospects. Tissue Eng., 11(5-6):787-802. [doi:10.1089/ ten.2005.11.787]
36. Meijer, G.J., de Bruijn, J.D., Koole, R., van Blitterswijk, C.A., 2007. Cell-based bone tissue engineering. PLoS. Med., 4(2):e9. [doi:10.1371/ journal.pmed.0040009]
37. Mercurio, S., Latinkic, B., Itasaki, N., Krumlauf, R., Smith, J.C., 2004. Connective-tissue growth factor modulates WNT signalling and interacts with the WNT receptor complex. Development, 131(9):2137-2147. [doi:10.1242/dev.01045]
38. Nishida, T., Nakanishi, T., Asano, M., Shimo, T., Takigawa, M., 2000. Effects of CTGF/Hcs24, a hypertrophic chondrocyte-specific gene product, on the proliferation and differentiation of osteoblastic cells in vitro. J. Cell. Physiol., 184(2):197-206. [doi:10.1002/ 1097-4652(200008)184:2<197::AID-JCP7>3.0.CO;2-R]
39. Nishida, T., Kawaki, H., Baxter, R.M., Deyoung, R.A., Takigawa, M., Lyons, K.M., 2007. CCN2 (connective cissue crowth cactor) is essential for extracellular matrix production and integrin signaling in chondrocytes. J. Cell Commun. Signal., 1(1):45-58. [doi:10.1007/ s12079-007-0005-z]
40. Oakes, D.A., Lieberman, J.R., 2000. Osteoinductive applications of regional gene therapy: Ex vivo gene transfer. Clin. Orthop. Relat. Res., 379(Suppl.):S101-S112. [doi:10.1097/00003086-200010001-00014]
41. Ono, M., Kubota, S., Fujisawa, T., Sonoyama, W., Kawaki, H., Akiyama, K., Oshima, M., Nishida, T., Yoshida, Y., Suzuki, K., et al., 2007. Promotion of attachment of human bone marrow stromal cells by CCN2. Biochem. Biophys. Res. Commun., 357(1):20-25. [doi:10.1016/ j.bbrc.2007.03.052]
42. Ono, M., Kubota, S., Fujisawa, T., Sonoyama, W., Kawaki, H., Akiyama, K., Shimono, K., Oshima, M., Nishida, T., Yoshida, Y., et al., 2008. Promotion of hydroxyapatiteassociated, stem cell-based bone regeneration by CCN2. Cell Transplant., 17(1-2):231-240. [doi:10.3727/ 000000008783907143]
43. Pelled, G.G., Turgeman, G., Aslan, H., Gazit, Z., Gazit, D., 2002. Mesenchymal stem cells for bone gene therapy and tissue engineering. Curr. Pharm. Des., 8(21):1917-1928. [doi:10.2174/1381612023393666]
44. Perbal, B., Brigstock, D.R., Lau, L.F., 2003. Report on the second international workshop on the CCN family of genes. Mol. Pathol., 56(2):80-85. [doi:10.1136/mp.56.2.80]
45. Pountos, I., Corscadden, D., Emery, P., Giannoudis, P.V., 2007. Mesenchymal stem cell tissue engineering: Techniques for isolation, expansion and application. Injury, 38(S4):23-33. [doi:10.1016/ S0020-1383(08)70006-8]
46. Rachfal, A.W., Brigstock, D.R., 2005. Structural and functional properties of CCN proteins. Vitam. Horm., 70:69-103. [doi:10.1016/ S0083-6729(05)70003-0]
47. Rose, F.R., Oreffo, R.O., 2002. Bone tissue engineering: Hope vs hype. Biochem. Biophys. Res. Commun., 292(1):1-7. [doi:10.1006/bbrc.2002.6519]
48. Rydziel, S., Stadmeyer, L., Zanotti, S., Durant, D., Smerdel-Ramoya, A., Canalis, E., 2007. Nephroblastoma overexpressed (Nov) inhibits osteoblastogenesis and causes osteopenia. J. Biol. Chem., 282(27):19762-19772. [doi:10.1074/jbc.M700212200]
49. Safadi, F.F., Xu, J., Smock, S.L., Kanaan, R.A., Selim, A.H., Odgren, P.R., Marks, S.C. Jr., Owen, T.A., Popoff, S.N., 2003. Expression of connective tissue growth factor in bone: Its role in osteoblast proliferation and differentiation in vitro and bone formation in vivo. J. Cell. Physiol., 196(1):51-62. [doi:10.1002/jcp.10319]
50. Slater, B.J., Kwan, M.D., Gupta, D.M., Panetta, N.J., Longaker, M.T., 2008. Mesenchymal cells for skeletal tissue engineering. Expert. Opin. Biol. Ther., 8(7):885-893. [doi:10.1517/14712598.8.7.885]
51. van Damme, A., van den Driessche, T., Collen, D., Chuah, M.K., 2002. Bone marrow stromal cells as targets for gene therapy. Curr. Gene Ther., 2(2):195-209. [doi:10.2174/1566523024605645]
52. Xiang, Y., Zheng, Q., Jia, B.B., Huang, G.P., Xu, Y.L., Wang, J.F., Pan, Z.J., 2007. Ex vivo expansion and pluripotential differentiation of cryopreserved human bone marrow mesenchymal stem cells. J. Zhejiang Univ. Sci. B, 8(2):136-146. [doi:10.1631/jzus.2007.B0136]
53. Yamaai, T., Nakanishi, T., Asano, M., Nawachi, K., Yoshimichi, G., Ohyama, K., Komori, T., Sugimoto, T., Takigawa, M., 2005. Gene expression of connective tissue growth factor (CTGF/CCN2) in calcifying tissues of normal and cbfa1-null mutant mice in late stage of embryonic development. J. Bone Miner. Metab., 23(4):280-288. [doi:10.1007/ s00774-004-0600-5]
54. Yamanaka, O., Saika, S., Ikeda, K., Miyazaki, K., Kitano, A., Ohnishi, Y., 2008. Connective tissue growth factor modulates extracellular matrix production in human subconjunctival fibroblasts and their proliferation and migration in vitro. Jpn. J. Ophthalmol, 52(1):8-15. [doi:10.1007/ s10384-007-0497-3]