Browse > Article
http://dx.doi.org/10.14348/molcells.2015.2315

Osteogenic Potency of Nacre on Human Mesenchymal Stem Cells  

Green, David W. (Oral Biosciences, Faculty of Dentistry, The University of Hong Kong)
Kwon, Hyuk-Jae (Division of Developmental Biology, Cincinnati Children's Hospital Medical Center)
Jung, Han-Sung (Oral Biosciences, Faculty of Dentistry, The University of Hong Kong)
Abstract
Nacre seashell is a natural osteoinductive biomaterial with strong effects on osteoprogenitors, osteoblasts, and osteoclasts during bone tissue formation and morphogenesis. Although nacre has shown, in one study, to induce bridging of new bone across large non-union bone defects in 8 individual human patients, there have been no succeeding human surgical studies to confirm this outstanding potency. But the molecular mechanisms associated with nacre osteoinduction and the influence on bone marrow-derived mesenchymal stem cells (BMSC's), skeletal stem cells or bone marrow stromal cells remain elusive. In this study we highlight the phenotypic and biochemical effects of Pinctada maxima nacre chips and the global nacre soluble protein matrix (SPM) on primary human bone marrow-derived stromal cells (hBMSCs) in vitro. In static co-culture with nacre chips, the hBMSCs secreted Alkaline phosphatase (ALP) at levels that exceeded bone morphogenetic protein (rhBMP-2) treatment. Concentrated preparation of SPM applied to Stro-1 selected hBMSC's led to rapid ALP secretions, at concentrations exceeding the untreated controls even in osteogenic conditions. Within 21 days the same population of Stro-1 selected hBMSCs proliferated and secreted collagens I-IV, indicating the premature onset of an osteoblast phenotype. The same SPM was found to promote unselected hBMSC differentiation with osteocalcin detected at 7 days, and proliferation increased at 7 days in a dose-dependent manner. In conclusion, nacre particles and nacre SPM induced the early stages of human bone cell differentiation, indicating that they may be promising soluble factors with osteoinductive capacity in primary human bone cell progenitors such as, hBMSC's.
Keywords
bone morphogenetic protein; human bone marrow stromal cells; mesenchymal stem cells; nacre; nacre soluble matrix proteins; osteoinduction;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Almeida, M.J., Pereira, L., Milet, C., Haigle, J., Barbosa, M., and Lopez, E. (2001). Comparative effects of nacre water-soluble matrix and dexamethasone on the alkaline phosphatase activity of MRC-5 fibroblasts. J. Biomed. Mater. Res. 57, 306-312.   DOI
2 Atlan, G., Balmain, N., Berland, S., Vidal, B., and Lopez, E. (1997). Reconstruction of human maxillary defects with nacre powder: histological evidence for bone regeneration. C. R. Acad. Sci. III. 320, 253-258   DOI   ScienceOn
3 Bedouet, L., Rusconi, F., Rousseau, M., Duplat, D., Marie, A., Dubost, L., Le Ny, K., Berland, S., Peduzzi, J., and Lopez, E. (2006). Identification of low molecular weight molecules as new components of the nacre organic matrix. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 144, 532-543.   DOI   ScienceOn
4 Bedouet, L., Marie, A., Dubost, L., Peduzzi, J., Duplat, D., Berland, S., Puissegur, M., Boulzageut, H., Rousseau, M., Milet, C., et al. (2007). Proteomics analysis of the nacre soluble and insoluble proteins from the oyster Pinctada margaritifera. Mar. Biotechnol. 9, 638-649   DOI
5 Duplat, D., Gallet, M., Berland, S., Marie, A., Dubost, L., Rousseau, M., Kamel, S., Milet, C., Brazier, M., Lopez, E., et al. (2007). The effect of molecules in mother-of-pearl on the decrease in bone resorption through the inhibition of osteoclast cathepsin K. Biomaterials 28, 4769-4778   DOI   ScienceOn
6 Kim, H., Lee, K., Ko, C.Y., Kim, H.S., Shin, H.I., Kim, T., Lee, S.H., and Jeong, D. (2012) The role of nacreous factors in preventing osteoporotic bone loss through both osteoblast activation and osteoclast inactivation. Biomaterials 33, 7489-7496.   DOI   ScienceOn
7 Lamghari, M., Almeida, M.J., Berland, S., Huet, H., Laurent, A., Milet, C., and Lopez, E. (1999). Stimulation of bone marrow cells and bone formation by nacre: in vivo and in vitro studies. Bone 25, 91S-94S.   DOI   ScienceOn
8 Lamghari, M., Antonietti, P., Berland, S., Laurent, A., and Lopez, E. (2001a). Arthrodesis of lumbar spine transverse processes using nacre in rabbit. J. Bone Miner. Res. 16, 2232-2237   DOI   ScienceOn
9 Lamghari, M., Berland, S., Laurent, A., Huet H., and Lopez E. (2001b). Bone reactions to nacre injected percutaneously into the vertebrae of sheep. Biomaterials 22, 555-562.   DOI   ScienceOn
10 Lao, Y., Zhang, X., Zhou, J., Su, W., Chen, R., Wang, Y., Zhou, W., and Xu, Z.F. (2007). Characterization and in vitro mineralization function of a soluble protein complex P60 from the nacre of Pinctada fucata. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 148, 201-208   DOI   ScienceOn
11 Lopez, E., Antoinetti, P., Delattre, O., Milet, C., and Berland, S. (2004a). Nacre as a bone supply. Argos Spine News 8, 32-34.
12 Liao, H., Mutvei, H., Hammarstrom, L., Wurtz, T., and Li, J. (2002). Tissue responses to nacreous implants in rat femur: an in situ hybridization and histochemical study. Biomaterials 23, 2693-2701.   DOI   ScienceOn
13 Lopez, E., Vidal, B., Berland, S., Camprasse, S., Camprasse, G., and Silve, C. (1992). Demonstration of the capacity of nacre to induce bone formation by human osteoblasts maintained in vitro. Tissue Cell. 24, 667-679   DOI   ScienceOn
14 Lopez, E., Giraud, M., Le Faou, A., Berland, S., and Gutierrez, J. (1995). French Patent No FR 9515650, WO 97/24133-10/07/97
15 Lopez, E., Milet, C., Lamghari, M., Pereira-Mouries, L., Borzeix, S., and Berland, S. (2004b). The dualism of nacre. Key Eng. Mater. 733, 254-256.
16 Milet, C., Berland, S., Lamghari, M., Mouries, L., Jolly, C., and Borzeix, S. (2004). Conservation of signal molecules involved in biomineralization control in calcifying matrices of bone and shell. C. R. Palevol. 3, 493.   DOI   ScienceOn
17 Oliveira, D.V., Silva, T.S., Cordeiro, O.D., Cavaco, S.I., and Simes, D.C. (2012). Identification of proteins with potential osteogenic activity present in the water-soluble matrix proteins from Cras sostrea gigas nacre using a proteomic approach. Scientific World Journal 2012, 765909
18 Rousseau, M., Pereira-Mouries, L., Almeida, M.J., Milet, C., and Lopez, E. (2003). The water-soluble matrix fraction from the nacre of Pinctada maxima produces earlier mineralization of MC3T3-E1 mouse pre-osteoblasts. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 135, 1-7
19 Shen, Y., Zhu, J., Zhang, H., and Zhao, F. (2006). In vitro osteogenic activity of pearl. Biomaterials 27, 281-287   DOI   ScienceOn
20 Rousseau, M., Boulzaguet, H., Biagianti, J., Duplat, D., Milet, C., Lopez, E., and Bedouet, L. (2008). Low molecular weight molecules of oyster nacre induce mineralization of the MC3T3-E1 cells. J. Biomed. Mater. Res. A 85, 487-497
21 Silve, C., Lopez, E., Vidal, B., Smith, D.C., Camprasse, S., Camprasse, G., and Couly, G. (1992). Nacre initiates biomineralization by human osteoblasts maintained in vitro. Calcif. Tissue Int. 51, 363-369   DOI
22 Stewart, K., Monk, P., Walsh, S., Jefferiss, C.M., Letchford, J., and Beresford, J.N. (2003). STRO-1, HOP-26 (CD63), CD49a and SB-10 (CD166) as markers of primitive human marrow stromal cells and their more differentiated progeny: a comparative investigation in vitro. Cell Tissue Res. 313, 281-290.   DOI
23 Wang, J.J., Chen, J.T., and Yang, C.L. (2007). Effects of soluble matrix of nacre on bone morphogenetic protein-2 and Cbfa1 gene expressions in rabbit marrow mesenchymal stem cells. Nan Fang Yi Ke Da Xue Xue Bao 27, 1838-1840.
24 Yang, X.B., Tare, R.S., Partridge, K.A.P., Roach, H.I., Clarke, N.M., Howdle, S.M., and Oreffo, R.O. (2003). Induction of human osteoprogenitor chemotaxis, proliferation, differentiation, and bone formation by osteoblast stimulating factor-1/pleiotrophin: osteoconductive biomimetic scaffolds for tissue engineering. J. Bone Miner. Res. 18, 47-57   DOI   ScienceOn
25 Zhang, C., Li, S., Ma, Z., Xie, L., and Zhang, R. (2006). A novel matrix protein p10 from the nacre of pearl oyster (Pinctada fucata) and its effects on both CaCO3 crystal formation and mineralogenic cells. Mar. Biotechnol. 8, 624-633.   DOI