A multicompartment holder for spinner flasks improves expansion and osteogenic differentiation of mesenchymal stem cells in three-dimensional scaffolds

Tissue Engineering - Part C: Methods

Volumn 20, Issue 12, 2014, Pages 984-993

  Teixeira, Graciosa Q ^a,b,c   Barrias, Cristina C ^a   Lourenço, Ana H ^a   Gonçalves, Raquel M ^a  

^a INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

^b CBQF CENTRO DE BIOTECNOLOGIA E QUÍMICA FINA LABORATÓRIO ASSOCIADO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BOTTLES; CELL ENGINEERING; FLOWCHARTING; MASS TRANSFER; PHOSPHATASES; SCAFFOLDS (BIOLOGY); STEM CELLS;

ALKALINE PHOSPHATASE ACTIVITY; HUMAN MESENCHYMAL STEM CELLS; MATRIX MINERALIZATION; MESENCHYMAL STEM CELL; OSTEOGENIC DIFFERENTIATION; SUSPENSION CELL CULTURE; THREE DIMENSIONAL SCAFFOLD; THREE-DIMENSIONAL (3D) SCAFFOLDS;

CELL CULTURE;

ALKALINE PHOSPHATASE; CHITOSAN; DNA; GLUCOSE; LACTIC ACID; MOLECULAR SCAFFOLD;

ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; DNA CONTENT; ENZYME ACTIVITY; GLUCOSE INTAKE; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MOLECULAR WEIGHT; OSTEOGENIC DIFFERENTIATION; STEM CELL CULTURE; BONE DEVELOPMENT; CELL LINEAGE; CELL SURVIVAL; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; DEVICES; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES; TISSUE SCAFFOLD;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; CHITOSAN; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; TISSUE SCAFFOLDS;

EID: 84913593134     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2014.0067     Document Type: Article

References (45)

1. Rungarunlert, S., Techakumphu, M., Pirity, M.K., and Dinnyes, A. Embryoid body formation from embryonic and induced pluripotent stem cells: Benefits of bioreactors. World J Stem Cells 1, 11, 2009.
2. Yeatts, A.B., Choquette, D.T., and Fisher, J.P. Bioreactors to influence stem cell fate: augmentation of mesenchymal stem cell signaling pathways via dynamic culture systems. Biochim Biophys Acta 1830, 2470, 2013.
3. dos Santos, F., Andrade, P.Z., Abecasis, M.M., Gimble, J.M., Chase, L.G., Campbell, A.M., Boucher, S., Vemuri, M.C., Silva, C.L., and Cabral, J.M. Toward a clinical-grade expansion of mesenchymal stem cells from human sources: a microcarrier-based culture system under xeno-free conditions. Tissue Eng Part C Methods 17, 1201, 2011.
4. Gigout, A., Buschmann, M.D., and Jolicoeur, M. Chondrocytes cultured in stirred suspension with serum-free medium containing pluronic-68 aggregate and proliferate while maintaining their differentiated phenotype. Tissue Eng Part A 15, 2237, 2009.
5. Lee, T.J., Bhang, S.H., La, W.G., Yang, H.S., Seong, J.Y., Lee, H., Im, G.I., Lee, S.H., and Kim, B.S. Spinner-flask culture induces redifferentiation of de-differentiated chondrocytes. Biotechnol Lett 33, 829, 2011.
6. Chen, M., Wang, X., Ye, Z., Zhang, Y., Zhou, Y., and Tan, W. A modular approach to the engineering of a centimetersized bone tissue construct with human amniotic mesenchymal stem cells-laden microcarriers. Biomaterials 32, 7532, 2011.
7. Goh, T.K., Zhang, Z.Y., Chen, A.K., Reuveny, S., Choolani, M., Chan, J.K., and Oh, S.K. Microcarrier culture for efficient expansion and osteogenic differentiation of human fetal mesenchymal stem cells. Biores Open Access 2, 84, 2013.
8. Pörtner, R., Nagel-Heyer, S., Goepfert, C., Adamietz, P., and Meenen, N.M. Bioreactor design for tissue engineering. J Biosci Bioeng 100, 235, 2005.
9. Turner, A.E., and Flynn, L.E. Design and characterization of tissue-specific extracellular matrix-derived microcarriers. Tissue Eng Part C Methods 18, 186, 2012.
10. Chen, K.Y., Chung, C.M., Chen, Y.S., Bau, D.T., and Yao, C.H. Rat bone marrow stromal cells-seeded porous gelatin/ tricalcium phosphate/oligomeric proanthocyanidins composite scaffold for bone repair. J Tissue Eng Regen Med 7, 708, 2013.
11. Mukherjee, D.P., Smith, D.F., Rogers, S.H., Emmanual, J.E., Jadin, K.D., and Hayes, B.K. Effect of 3D-microstructure of bioabsorbable PGA:TMC scaffolds on the growth of chondrogenic cells. J Biomed Mater Res B Appl Biomater 88, 92, 2009.
12. Cxetin, D., Kahraman, A.S., and Gümüsxderelioglu, M. Novel pHEMA-gelatin SPHs as bone scaffolds in dynamic cultures. J Mater Sci Mater Med 23, 2803, 2012.
13. Kim, H.J., Kim, U.J., Leisk, G.G., Bayan, C., Georgakoudi, I., and Kaplan, D.L. Bone regeneration on macroporous aqueous-derived silk 3-D scaffolds. Macromol Biosci 7, 643, 2007.
14. Meinel, L., Karageorgiou, V., Fajardo, R., Snyder, B., Shinde-Patil, V., Zichner, L., Kaplan, D., Langer, R., and Vunjak-Novakovic, G. Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann Biomed Eng 32, 112, 2004.
15. Mygind, T., Stiehler, M., Baatrup, A., Li, H., Zou, X., Flyvbjerg, A., Kassem, M., and Bünger, C. Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 28, 1036, 2007.
16. Song, K., Liu, T., Cui, Z., Li, X., and Ma, X. Threedimensional fabrication of engineered bone with human bio-derived bone scaffolds in a rotating wall vessel bioreactor. J Biomed Mater Res A 86, 323, 2008.
17. Janjanin, S., Li, W.J., Morgan, M.T., Shanti, R.M., and Tuan, R.S. Mold-shaped, nanofiber scaffold-based cartilage engineering using human mesenchymal stem cells and bioreactor. J Surg Res 149, 47, 2008.
18. Barrias, C., and Goncalves, R.M. Container, useful in spinner flask assembly and kit for culturing cell samples in three-dimensional matrix, comprises chambers for containing cell samples, where one of the walls of chambers are perforated to allow culture media and a lid; Patent Number(s): W02013043072-A1 (2011).
19. Antunes, J.C., Pereira, C.L., Molinos, M., Ferreira-da-Silva, F., Dessì, M., Gloria, A., Ambrosio, L., Gonçalves, R.M., and Barbosa, M.A. Layer-by-layer self-assembly of chitosan and poly(g-glutamic acid) into polyelectrolyte complexes. Biomacromolecules 12, 4183, 2011.
20. Amaral, I.F., Sampaio, P., and Barbosa, M.A. Threedimensional culture of human osteoblastic cells in chitosan sponges: the effect of the degree of acetylation. J Biomed Mater Res A 76, 335, 2006.
21. Bidarra, S.J., Barrias, C.C., Barbosa, M.A., Soares, R., Amédée, J., and Granja, P.L. Phenotypic and proliferative modulation of human mesenchymal stem cells via crosstalk with endothelial cells. Stem Cell Res 7, 186, 2011.
22. Folkman, J., and Moscona, A. Role of cell shape in growth control. Nature 273, 345, 1978.
23. Barrias, C.C., and Gonçalves, R.M. Multi-compartment holder for 3D cell culture under dynamic conditions. Provisional patent application UK no.11163979, 2011.
24. Bidarra, S.J., Barrias, C.C., Barbosa, M.A., Soares, R., and Granja, P.L. Immobilization of human mesenchymal stem cells within RGD-grafted alginate microspheres and assessment of their angiogenic potential. Biomacromolecules 11, 1956, 2010.
25. Patel, S.D., Papoutsakis, E.T., Winter, J.N., and Miller, W.M. The lactate issue revisited: novel feeding protocols to examine inhibition of cell proliferation and glucose metabolism in hematopoietic cell cultures. Biotechnol Prog 16, 885, 2000.
26. Zhu, B., Bailey, S.R., and Mauli Agrawal, C. Calcification of primary human osteoblast cultures under flow conditions using polycaprolactone scaffolds for intravascular applications. J Tissue Eng Regen Med 6, 687, 2012.
27. Amaral, I.F., Unger, R.E., Fuchs, S., Mendonça, A.M., Sousa, S.R., Barbosa, M.A., Pêgo, A.P., and Kirkpatrick, C.J. Fibronectin-mediated endothelialisation of chitosan porous matrices. Biomaterials 30, 5465, 2009.
28. Barbosa, J.N., Amaral, I.F., Aguas, A.P., and Barbosa, M.A. Evaluation of the effect of the degree of acetylation on the inflammatory response to 3D porous chitosan scaffolds. J Biomed Mater Res A 93, 20, 2010.
29. Santos, S.G., Lamghari, M., Almeida, C.R., Oliveira, M.I., Neves, N., Ribeiro, A.C., Barbosa, J.N., Barros, R., Maciel, J., Martins, M.C., Gonçalves, R.M., and Barbosa, M.A. Adsorbed fibrinogen leads to improved bone regeneration and correlates with differences in the systemic immune response. Acta Biomater 9, 7209, 2013.
30. Di Martino, A., Sittinger, M., and Risbud, M.V. Chitosan: a versatile biopolymer for orthopaedic tissue-engineering. Biomaterials 26, 5983, 2005.
31. Eibes, G., dos Santos, F., Andrade, P.Z., Boura, J.S., Abecasis, M.M., da Silva, C.L., and Cabral, J.M. Maximizing the ex vivo expansion of human mesenchymal stem cells using a microcarrier-based stirred culture system. J Biotechnol 146, 194, 2010.
32. Ferrari, C., Balandras, F., Guedon, E., Olmos, E., Chevalot, I., and Marc, A. Limiting cell aggregation during mesenchymal stem cell expansion on microcarriers. Biotechnol Prog 28, 780, 2012.
33. Rafiq, Q.A., Brosnan, K.M., Coopman, K., Nienow, A.W., and Hewitt, C.J. Culture of human mesenchymal stem cells on microcarriers in a 5 l stirred-tank bioreactor. Biotechnol Lett 35, 1233, 2013.
34. Weber, C., Pohl, S., Pörtner, R., Wallrapp, C., Kassem, M., Geigle, P., and Czermak, P. Expansion and harvesting of hMSC-TERT. Open Biomed Eng J 1, 38, 2007.
35. Stiehler, M., Bünger, C., Baatrup, A., Lind, M., Kassem, M., and Mygind, T. Effect of dynamic 3-D culture on proliferation, distribution, and osteogenic differentiation of human mesenchymal stem cells. J Biomed Mater Res A 89, 96, 2009.
36. Hewitt, C.J., Lee, K., Nienow, A.W., Thomas, R.J., Smith, M., and Thomas, C.R. Expansion of human mesenchymal stem cells on microcarriers. Biotechnol Lett 33, 2325, 2011.
37. Schop, D., Janssen, F.W., Borgart, E., de Bruijn, J.D., and van Dijkhuizen-Radersma, R. Expansion of mesenchymal stem cells using a microcarrier-based cultivation system: growth and metabolism. J Tissue Eng Regen Med 2, 126, 2008.
38. Lamghari, M., Amaral, I.F., Sousa, S.R., Sampaio, P., and Barbosa, M.A. Rat bone marrow stromal cell osteogenic differentiation and fibronectin adsorption on chitosan membranes: the effect of the degree of acetylation. J Biomed Mater Res A 75, 387, 2005.
39. Holtorf, H.L., Sheffield, T.L., Ambrose, C.G., Jansen, J.A., and Mikos, A.G. Flow perfusion culture of marrow stromal cells seeded on porous biphasic calcium phosphate ceramics. Ann Biomed Eng 33, 1238, 2005.
40. Zhang, Z.Y., Teoh, S.H., Teo, E.Y., Khoon Chong, M.S., Shin, C.W., Tien, F.T.,Choolani, M.A., and Chan, J.K.Acomparison of bioreactors for culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials 31, 8684, 2010.
41. Fekete, N., Rojewski, M.T., Lotfi, R., and Schrezenmeier, H. Essential components for ex vivo proliferation of mesenchymal stromal cells. Tissue Eng Part C Methods 20, 129, 2013.
42. Yourek, G., McCormick, S.M., Mao, J.J., and Reilly, G.C. Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen Med 5, 713, 2010.
43. Pattappa, G., Heywood, H.K., de Bruijn, J.D., and Lee, D.A. The metabolism of human mesenchymal stem cells during proliferation and differentiation. J Cell Physiol 226, 2562, 2011.
44. Bilgen, B., and Barabino, G.A. Location of scaffolds in bioreactors modulates the hydrodynamic environment experienced by engineered tissues. Biotechnol Bioeng 98, 282, 2007.
45. Bilgen, B., Chang-Mateu, I.M., and Barabino, G.A. Characterization of mixing in a novel wavy-walled bioreactor for tissue engineering. Biotechnol Bioeng 92, 907, 2005.