Functionalization of polycaprolactone scaffolds with hyaluronic acid and β-TCP facilitates migration and osteogenic differentiation of human dental pulp stem cells in vitro

Tissue Engineering - Part A

Volumn 21, Issue 3-4, 2015, Pages 729-739

  Jensen, Jonas ^a   Kraft, David Christian Evar ^b   Lysdahl, Helle ^a   Foldager, Casper Bindzus ^a   Chen, Muwan ^a,b   Kristiansen, Asger Albæk ^b   Rölfing, Jan Hendrik Duedal ^a   Bünger, Cody Eric ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; CELL ENGINEERING; CELL PROLIFERATION; CYTOLOGY; DEPOSITION; FUSED DEPOSITION MODELING; GENE EXPRESSION; HYALURONIC ACID; MORPHOLOGY; ORGANIC ACIDS; PHASE SEPARATION; POLYMERASE CHAIN REACTION; STEM CELLS; TRANSMISSION CONTROL PROTOCOL;

BONE TISSUE ENGINEERING; DENTAL PULP STEM CELLS; EXTRACELLULAR MATRICES; OSTEOGENIC DIFFERENTIATION; OSTEOGENIC POTENTIAL; POLYCAPROLACTONE SCAFFOLDS; QUANTITATIVE POLYMERASE CHAIN REACTION; THERMAL INDUCED PHASE SEPARATIONS;

SCAFFOLDS (BIOLOGY);

4 CARBOXYGLUTAMIC ACID; 5' NUCLEOTIDASE; ALKALINE PHOSPHATASE; BETA CALCIUM PHOSPHATE; BONE MORPHOGENETIC PROTEIN 2; BONE SIALOPROTEIN; BONE SIALOPROTEIN II; CALCIUM ION; CALCIUM PHOSPHATE; COLLAGEN TYPE 1; DNA; ENDOGLIN; HYALURONIC ACID; OSTEOCALCIN; OSTEOPONTIN; POLYCAPROLACTONE; THY 1 ANTIGEN; UNCLASSIFIED DRUG; BETA-TRICALCIUM PHOSPHATE; BONE PROSTHESIS; NANOPARTICLE; POLYESTER;

ADULT; ARTICLE; BONE MINERALIZATION; BONE TISSUE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; CHEMICAL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENTAL PULP STEM CELL; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MALE; MOLAR TOOTH; NORMAL HUMAN; OSTEOBLAST; PHASE SEPARATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCANNING ELECTRON MICROSCOPY; STEM CELL; TISSUE ENGINEERING; TOOTH PULP; YOUNG ADULT; BONE DEVELOPMENT; BONE PROSTHESIS; CELL MOTION; CHEMISTRY; CYTOLOGY; DEVICE FAILURE ANALYSIS; DEVICES; EQUIPMENT DESIGN; MATERIALS TESTING; PARTICLE SIZE; PHYSIOLOGY; SYNTHESIS; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ADULT; BONE SUBSTITUTES; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELL MOVEMENT; DENTAL PULP; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; FEMALE; HUMANS; HYALURONIC ACID; MALE; MATERIALS TESTING; NANOPARTICLES; OSTEOBLASTS; OSTEOGENESIS; PARTICLE SIZE; POLYESTERS; STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS; YOUNG ADULT;

EID: 84923307482     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2014.0177     Document Type: Article

References (51)

1. Dimitriou, R., Jones, E., McGonagle, D., and Giannoudis, P.V. Bone regeneration: current concepts and future directions. BMC Med 9, 66, 2011.
2. Schroeder, J.E., and Mosheiff, R. Tissue engineering approaches for bone repair: concepts and evidence. Injury 42, 609, 2011.
3. Lutolf, M.P., and Hubbell, J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23, 47, 2005.
4. Lichte, P., Pape, H.C., Pufe, T., Kobbe, P., and Fischer, H. Scaffolds for bone healing: concepts, materials and evidence. Injury 42, 569, 2011.
5. Bruinink, A., Bitar, M., Pleskova, M., Wick, P., Krug, H.F., and Maniura-Weber, K. Addition of nanoscaled bioinspired surface features: A revolution for bone-related implants and scaffolds?. J Biomed Mater Res A 102, 275, 2013.
6. Hutmacher, D.W., Schantz, T., Zein, I., Ng, K.W., Teoh, S.H., and Tan, K.C. Mechanical properties and cell cultural response of polycaprolactone scaffolds designed and fabricated via fused deposition modeling. J Biomed Mater Res 55, 203, 2001.
7. Hutmacher, D.W., Schantz, J.T., Lam, C.X.F., Tan, K.C., and Lim, T.C. State of the art and future directions of scaffold-based bone engineering from a biomaterials perspective. J Tissue Eng Regen Med 1, 245, 2007.
8. Derby, B. Printing and prototyping of tissues and scaffolds. Science 338, 921, 2012.
9. Christensen, B.B., Foldager, C.B., Hansen, O.M., Kristiansen, A.A., Le, D.Q.S., Nielsen, A.D., et al. A novel nano-structured porous polycaprolactone scaffold improves hyaline cartilage repair in a rabbit model compared to a collagen type I/III scaffold: in vitro and in vivo studies. Knee Surg Sports Traumatol Arthrosc 20, 1192, 2012.
10. Jensen, J., Rölfing, J.H.D., Svend Le, D.Q., Kristiansen, A.A., Nygaard, J.V., Hokland, L.B., et al. Surface-modified functionalized polycaprolactone scaffolds for bone repair: In vitro and in vivo experiments. J Biomed Mater Res A 102, 2993, 2014.
11. Zou, L., Zou, X., Chen, L., Li, H., Mygind, T., Kassem, M., et al. Effect of hyaluronan on osteogenic differentiation of porcine bone marrow stromal cells in vitro. J Orthop Res 26, 713, 2008.
12. Chen, M., Le, D.Q.S., Baatrup, A., Nygaard, J.V., Hein, S., Bjerre, L., et al. Self-Assembled composite matrix in a hierarchical 3-D scaffold for bone tissue engineering. Acta Biomater 7, 2244, 2011.
13. Zou, L., Luo, Y., Chen, M., Wang, G., Ding, M., Petersen, C.C., et al. A simple method for deriving functional MSCs and applied for osteogenesis in 3D scaffolds. Sci Rep 3, 2243, 2013.
14. Caplan, A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213, 341, 2007.
15. Caplan, A.I., and Dennis, J.E. Mesenchymal stem cells as trophic mediators. J Cell Biochem 98, 1076, 2006.
16. Simonsen, J.L., Rosada, C., Serakinci, N., Justesen, J., Stenderup, K., Rattan, S.I.S., et al. Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat Biotechnol 20, 592, 2002.
17. Chamberlain, G., Fox, J., Ashton, B., and Middleton, J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25, 2739, 2007.
18. Graziano, A., d'Aquino, R., Laino, G., and Papaccio, G. Dental pulp stem cells: a promising tool for bone regeneration. Stem Cell Rev 4, 21, 2008.
19. Kraft, D.C.E., Bindslev, D.A., Melsen, B., and Klein-Nulend, J. Human dental pulp cells exhibit bone cell-like responsiveness to fluid shear stress. Cytotherapy 13, 214, 2011.
20. Perry, B.C., Zhou, D., Wu, X., Yang, F.-C., Byers, M.A., Chu, T.-M.G., et al. Collection, cryopreservation, and characterization of human dental pulp-derived mesenchymal stem cells for banking and clinical use. Tissue Eng Part C Methods 14, 149, 2008.
21. Goldberg, M., and Smith, A.J. Cells and extracellular matrices of dentin and pulp: a biological basis for repair and tissue engineering. Crit Rev Oral Biol Med 15, 13, 2004.
22. Gronthos, S., Brahim, J., Li, W., Fisher, L.W., Cherman, N., Boyde, A., et al. Stem cell properties of human dental pulp stem cells. J Dent Res 81, 531, 2002.
23. Laino, G., d'Aquino, R., Graziano, A., Lanza, V., Carinci, F., Naro, F., et al. A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20, 1394, 2005.
24. d'Aquino, R., Graziano, A., Sampaolesi, M., Laino, G., Pirozzi, G., De Rosa, A., et al. Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14, 1162, 2007.
25. Kraft, D.C.E., Bindslev, D.A., Melsen, B., Abdallah, B.M., Kassem, M., and Klein-Nulend, J. Mechanosensitivity of dental pulp stem cells is related to their osteogenic maturity. Eur J Oral Sci 118, 29, 2010.
26. Mangano, C., De Rosa, A., Desiderio, V., d'Aquino, R., Piattelli, A., De Francesco, F., et al. The osteoblastic differentiation of dental pulp stem cells and bone formation on different titanium surface textures. Biomaterials 31, 3543, 2010.
27. Akkouch, A., Zhang, Z., and Rouabhia, M. Engineering bone tissue using human dental pulp stem cells and an osteogenic collagen-hydroxyapatite-poly (L-lactide-co-ecaprolactone) scaffold. J Biomater Appl 28, 922, 2014.
28. Pfaffl, M.W., Tichopad, A., Prgomet, C., and Neuvians, T.P. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: Best-Keeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26, 509, 2004.
29. Huang, G.T.J., Gronthos, S., and Shi, S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 88, 792, 2009.
30. Ishaug-Riley, S.L., Crane-Kruger, G.M., Yaszemski, M.J., and Mikos, A.G. Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers. Biomaterials 19, 1405, 1998.
31. Zhang, Z.-Y., Teoh, S.H., Chong, W.-S., Foo, T.-T., Chng, Y.-C., Choolani, M., et al. A biaxial rotating bioreactor for the culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 30, 2694, 2009.
32. Papadimitropoulos, A., Riboldi, S.A., Tonnarelli, B., Piccinini, E., Woodruff, M.A., Hutmacher, D.W., et al. A collagen network phase improves cell seeding of open-pore structure scaffolds under perfusion. J Tissue Eng Regen Med 7, 183, 2013.
33. Bjerre, L., Bünger, C., Baatrup, A., Kassem, M., and Mygind, T. Flow perfusion culture of human mesenchymal stem cells on coralline hydroxyapatite scaffolds with various pore sizes. J Biomed Mater Res A 97A, 251, 2011.
34. Zhang, W., Walboomers, X.F., van Osch, G.J.V.M., van den Dolder, J., and Jansen, J.A. Hard tissue formation in a porous HA/TCP ceramic scaffold loaded with stromal cells derived from dental pulp and bone marrow. Tissue Eng Part A 14, 285, 2008.
35. Chatakun, P., Núñez-Toldrà, R., Díaz López, E.J., Gil-Recio, C., Martínez-Sarrà, E., Hernández-Alfaro, F., et al. The effect of five proteins on stem cells used for osteoblast differentiation and proliferation: a current review of the literature. Cell Mol Life Sci 71, 113, 2014.
36. Suzuki, K., Zhu, B., Rittling, S.R., Denhardt, D.T., Goldberg, H.A., McCulloch, C.A.G., et al. Colocalization of intracellular osteopontin with CD44 is associated with migration, cell fusion, and resorption in osteoclasts. J Bone Miner Res 17, 1486, 2002.
37. Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C.B., and Seed, B. CD44 is the principal cell surface receptor for hyaluronate. Cell 61, 1303, 1990.
38. Underhill, C.B., and Toole, B.P. Binding of hyaluronate to the surface of cultured cells. J Cell Biol 82, 475, 1979.
39. Turley, E.A., Noble, P.W., and Bourguignon, L.Y.W. Signaling properties of hyaluronan receptors. J Biol Chem 277, 4589, 2002.
40. Komori, T. Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 99, 1233, 2006.
41. Hunter, G.K., and Goldberg, H.A. Modulation of crystal formation by bone phosphoproteins: role of glutamic acid-rich sequences in the nucleation of hydroxyapatite by bone sialoprotein. Biochem J 302 (Pt 1), 175, 1994.
42. Wang, S., Sasaki, Y., Zhou, L., Matsumura, H., Araki, S., Mezawa, M., et al. Transcriptional regulation of bone sialoprotein gene by interleukin-11. Gene 476, 46, 2011.
43. Hunter, G.K., Wong, K.S., and Kim, J.J. Binding of calcium to glycosaminoglycans: an equilibrium dialysis study. Arch Biochem Biophys 260, 161, 1988.
44. Lee, C.H., Hajibandeh, J., Suzuki, T., Fan, A., Shang, P., and Mao, J.J. Three-dimensional printed multiphase scaffolds for regeneration of periodontium complex. Tissue Eng Part A 20, 1342, 2014.
45. Yang, X., Han, G., Pang, X., and Fan, M. Chitosan/collagen scaffold containing bone morphogenetic protein-7 DNA supports dental pulp stem cell differentiation in vitro and in vivo. J Biomed Mater Res A 2012 [Epub ahead of print]; DOI: 10.1002/jbm.a.34064.
46. Zheng, L., Yang, F., Shen, H., Hu, X., Mochizuki, C., Sato, M., et al. The effect of composition of calcium phosphate composite scaffolds on the formation of tooth tissue from human dental pulp stem cells. Biomaterials 32, 7053, 2011.
47. Wang, J., Liu, X., Jin, X., Ma, H., Hu, J., Ni, L., et al. The odontogenic differentiation of human dental pulp stem cells on nanofibrous poly(L-lactic acid) scaffolds in vitro and in vivo. Acta Biomater 6, 3856, 2010.
48. Yang, X., Yang, F., Walboomers, X.F., Bian, Z., Fan, M., and Jansen, J.A. The performance of dental pulp stem cells on nanofibrous PCL/gelatin/nHA scaffolds. J Biomed Mater Res A 93, 247, 2010.
49. Yamada, Y., Fujimoto, A., Ito, A., Yoshimi, R., and Ueda, M. Cluster analysis and gene expression profiles: a cDNA microarray system-based comparison between human dental pulp stem cells (hDPSCs) and human mesenchymal stem cells (hMSCs) for tissue engineering cell therapy. Biomaterials 27, 3766, 2006.
50. Ito, K., Yamada, Y., Nakamura, S., and Ueda, M. Osteogenic potential of effective bone engineering using dental pulp stem cells, bone marrow stem cells, and periosteal cells for osseointegration of dental implants. Int J Oral Maxillofac Implants 26, 947, 2011.
51. Bjerre, L., Nygaard, J.V., and Bünger, C.E. Three-dimensional nanostructured hybrid scaffold and manufacture thereof. EP Patent UA20120128739, 2010.