The pH in the microenvironment of human mesenchymal stem cells is a critical factor for optimal osteogenesis in tissue-engineered constructs

Tissue Engineering - Part A

Volumn 20, Issue 13-14, 2014, Pages 1827-1840

  Monfoulet, Laurent Emmanuel ^a   Becquart, Pierre ^a   Marchat, David ^b   Vandamme, Katleen ^a,c   Bourguignon, Marianne ^a   Pacard, Elodie ^d   Viateau, Véronique ^a,e   Petite, Herve ^a   Logeart Avramoglou, Delphine ^a  

^a Paris university   (France)

^b ECOLE DES MINES DE SAINT ETIENNE   (France)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d Noraker   (France)

^e ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINITY; BIOACTIVE GLASS; BONE; CYTOLOGY; ENZYME ACTIVITY; GENE EXPRESSION; PH; PHOSPHATASES; STEM CELLS;

EXTRACELLULAR MATRICES; EXTRACELLULAR MICROENVIRONMENT; HUMAN MESENCHYMAL STEM CELLS; MATERIAL DEGRADATION; OSTEOGENIC DIFFERENTIATION; OSTEOPROGENITOR CELLS; TISSUE-ENGINEERED CONSTRUCTS; TRI-CALCIUM PHOSPHATES;

TISSUE;

ALKALINE PHOSPHATASE; BIOACTIVE GLASS; BIOMATERIAL; CALCIUM PHOSPHATE; HYDROXYAPATITE; UNCLASSIFIED DRUG; CULTURE MEDIUM;

ADOLESCENT; ADULT; ALKALINITY; ALKALINIZATION; ALP GENE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; BONE TISSUE; BSP GENE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CERAMICS; CORAL; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOUSE; NONHUMAN; OSTEOPROGENITOR CELL; PH; PRIORITY JOURNAL; RUNX2 GENE; TISSUE ENGINEERING; ANIMAL; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECTS; IMPLANT; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; NUDE MOUSE; PROCEDURES; SCANNING ELECTRON MICROSCOPY; SUBCUTANEOUS TISSUE; TISSUE SCAFFOLD; TUMOR MICROENVIRONMENT;

ADOLESCENT; ADULT; ANIMALS; BIOCOMPATIBLE MATERIALS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; CULTURE MEDIA; FEMALE; HUMANS; HYDROGEN-ION CONCENTRATION; IMPLANTS, EXPERIMENTAL; MALE; MESENCHYMAL STROMAL CELLS; MICE, NUDE; MICROSCOPY, ELECTRON, SCANNING; MIDDLE AGED; OSTEOGENESIS; SUBCUTANEOUS TISSUE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84904162529     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0500     Document Type: Article

References (60)

1. Friedenstein, A.J., Chailakhyan, R.K., and Gerasimov, U.V. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 20, 263, 1987.
2. Goshima, J., Goldberg, V.M., and Caplan, A.I. Osteogenic potential of culture-expanded rat marrow cells as assayed in vivo with porous calcium phosphate ceramic. Biomaterials 12, 253, 1991.
3. Bruder, S.P., Jaiswal, N., Ricalton, N.S., Mosca, J.D., Kraus, K.H., and Kadiyala, S. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res S247, 1998.
4. Petite, H., Viateau, V., Bensaid, W., Meunier, A., de Pollak, C., Bourguignon, M., et al. Tissue-engineered bone regeneration. Nat Biotechnol 18, 959, 2000.
5. Kon, E., Muraglia, A., Corsi, A., Bianco, P., Marcacci, M., Martin, I., et al. Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J Biomed Mater Res 49, 328, 2000.
6. Quarto, R., Mastrogiacomo, M., Cancedda, R., Kutepov, S.M., Mukhachev, V., Lavroukov, A., et al. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 344, 385, 2001.
7. Agrawal, C.M., and Ray, R.B. Biodegradable polymeric scaffolds for musculoskeletal tissue engineering. J Biomed Mater Res 55, 141, 2001.
8. OBrien, F.J., Harley, B.A., Yannas, I.V., and Gibson, L.J. The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 26, 433, 2005.
9. Chang, H., and Wang, Y. Cell responses to surface and architecture of tissue engineering scaffolds. In: Eberli, D., ed. Regenerative Medicine and Tissue Engineering-Cells and Biomaterials. Intech, 2011. http://www.intechopen. com/ books/regenerative-medicine-and-tissue-engineering-cells-andbiomaterials/ cell-responses-to-surface-and-architecture-oftissue- engineering-scaffolds. ISBN: 978-953-307-663-8.
10. Shen, Y., Liu, W.,Wen, C., Pan, H.,Wang, T., Darvell, B.W., et al. Bone regeneration: importance of local pH-strontiumdoped borosilicate scaffold. J Mater Chem 22, 8662, 2012.
11. El-Ghannam, A. Bone reconstruction: from bioceramics to tissue engineering. Expert Rev Med Devices 2, 87, 2005.
12. LeGeros, R.Z. Calcium phosphate-based osteoinductive materials. Chem Rev 108, 4742, 2008.
13. Krebsbach, P.H., Kuznetsov, S.A., Satomura, K., Emmons, R.V., Rowe, D.W., and Robey, P.G. Bone formation in vivo: comparison of osteogenesis by transplantedmouse and human marrow stromal fibroblasts. Transplantation 63, 1059, 1997.
14. Mankani, M.H., Kuznetsov, S.A., and Robey, P.G. Formation of hematopoietic territories and bone by transplanted human bone marrow stromal cells requires a critical cell density. Exp Hematol 35, 995, 2007.
15. Zannettino, A.C., Paton, S., Itescu, S., and Gronthos, S. Comparative assessment of the osteoconductive properties of different biomaterials in vivo seeded with human or ovine mesenchymal stem/stromal cells. Tissue Eng Part A 16, 3579, 2010.
16. Arinzeh, T.L., Tran, T., McAlary, J., and Daculsi, G. A comparative study of biphasic calcium phosphate ceramics for human mesenchymal stem-cell-induced bone formation. Biomaterials 26, 3631, 2005.
17. Cordonnier, T., Layrolle, P., Gaillard, J., Langonne, A., Sensebe, L., Rosset, P., et al. 3D environment on human mesenchymal stem cells differentiation for bone tissue engineering. J Mater Sci Mater Med 21, 981, 2010.
18. Sladkova, M., Manassero, M., Myrtil, V., Savari, H., Fall, M., Thomas, D., et al. Coral particle size influences human mesenchymal stem cell osteogenesis but not cell survival in an ectopic mouse model. European Orthopaedic Research Society, Amsterdam, 2012.
19. Rahaman, M.N., Day, D.E., Bal, B.S., Fu, Q., Jung, S.B., Bonewald, L.F., et al. Bioactive glass in tissue engineering. Acta Biomater 7, 2355, 2011.
20. Hench, L.L., and Polak, J.M. Third-generation biomedical materials. Science 295, 1014, 2002.
21. el-Ghannam, A., Ducheyne, P., and Shapiro, I.M. Formation of surface reaction products on bioactive glass and their effects on the expression of the osteoblastic phenotype and the deposition of mineralized extracellular matrix. Biomaterials 18, 295, 1997.
22. Silver, I.A., Deas, J., and Erecinska, M. Interactions of bioactive glasses with osteoblasts in vitro: effects of 45S5 Bioglass, and 58S and 77S bioactive glasses on metabolism, intracellular ion concentrations and cell viability. Biomaterials 22, 175, 2001.
23. Zhang, D., Hupa, M., and Hupa, L. In situ pH within particle beds of bioactive glasses. Acta Biomater 4, 1498, 2008.
24. Busa, W.B., and Nuccitelli, R. Metabolic regulation via intracellular pH. Am J Physiol 246, R409, 1984.
25. Chakkalakal, D.A., Mashoof, A.A., Novak, J., Strates, B.S., and McGuire, M.H. Mineralization and pH relationships in healing skeletal defects grafted with demineralized bone matrix. J Biomed Mater Res 28, 1439, 1994.
26. Bushinsky, D.A. Metabolic alkalosis decreases bone calcium efflux by suppressing osteoclasts and stimulating osteoblasts. Am J Physiol 271, F216, 1996.
27. Brandao-Burch, A., Utting, J.C., Orriss, I.R., and Arnett, T.R. Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization. Calcif Tissue Int 77, 167, 2005.
28. Arnett, T.R. Acidosis, hypoxia and bone. Arch Biochem Biophys 503, 103, 2010.
29. Guillemin, G., Meunier, A., Dallant, P., Christel, P., Pouliquen, J.C., and Sedel, L. Comparison of coral resorption and bone apposition with two natural corals of different porosities. J Biomed Mater Res 23, 765, 1989.
30. Guillemin, G., Patat, J.L., Fournie, J., and Chetail, M. The use of coral as a bone graft substitute. J Biomed Mater Res 21, 557, 1987.
31. Hench, L.L. Bioactive materials: the potential for tissue regeneration. J Biomed Mater Res 41, 511, 1998.
32. Kokubo, T., Kushitani, H., Sakka, S., Kitsugi, T., and Yamamuro, T. Solutions able to reproduce in vivo surfacestructure changes in bioactive glass-ceramic A-W. J Biomed Mater Res 24, 721, 1990.
33. Kokubo, T., and Takadama, H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27, 2907, 2006.
34. Mačković, M., Hoppe, A., Detsch, R., Mohn, D., Stark, W.J., Spiecker, E., et al. Bioactive glass (type 45S5) nanoparticles: in vitro reactivity on nanoscale and biocompatibility. J Nanopart Res 14, 966, 2012.
35. Marchat, D., Bernache-Assollant, D., and Champion, E. Cadmium fixation by synthetic hydroxyapatite in aqueous solution-thermal behaviour. J Hazard Mater 139, 453, 2007.
36. Becquart, P., Cambon-Binder, A., Monfoulet, L.E., Bourguignon, M., Vandamme, K., Bensidhoum, M., et al. Ischemia is the prime but not the only cause of human multipotent stromal cell death in tissue-engineered constructs in vivo. Tissue Eng Part A 18, 2084, 2012.
37. Bensaid, W., Triffitt, J.T., Blanchat, C., Oudina, K., Sedel, L., and Petite, H. A biodegradable fibrin scaffold for mesenchymal stem cell transplantation. Biomaterials 24, 2497, 2003.
38. Logeart-Avramoglou, D., Oudina, K., Bourguignon, M., Delpierre, L., Nicola, M.A., Bensidhoum, M., et al. In vitro and in vivo bioluminescent quantification of viable stem cells in engineered constructs. Tissue Eng Part C Methods 16, 447, 2010.
39. Degat, M.C., Dubreucq, G., Meunier, A., Dahri-Correia, L., Sedel, L., Petite, H., et al. Enhancement of the biological activity of BMP-2 by synthetic dextran derivatives. J Biomed Mater Res Part A 88, 174, 2009.
40. Vandamme, K., Holy, X., Bensidhoum, M., Logeart-Avramoglou, D., Naert, I., Duyck, J., et al. Establishment of an in vivo model for molecular assessment of titanium implant osseointegration in compromised bone. Tissue Eng Part C Methods 17, 311, 2011.
41. Hench, L.L. Bioceramics. J Am Ceram Soc 81, 1705, 1998.
42. Mankani, M.H., Kuznetsov, S.A., Avila, N.A., Kingman, A., and Robey, P.G. Bone formation in transplants of human bone marrow stromal cells and hydroxyapatitetricalcium phosphate: prediction with quantitative CT in mice. Radiology 230, 369, 2004.
43. Ducheyne, P., and Qiu, Q. Bioactive ceramics: the effect of surface reactivity on bone formation and bone cell function. Biomaterials 20, 2287, 1999.
44. El-Gendy, R., Yang, X.B., Newby, P.J., Boccaccini, A.R., and Kirkham, J. Osteogenic differentiation of human dental pulp stromal cells on 45S5 Bioglass(R) based scaffolds in vitro and in vivo. Tissue Eng Part A 19, 707, 2013.
45. Fu, Q., Rahaman, M.N., Bal, B.S., Bonewald, L.F., Kuroki, K., and Brown, R.F. Silicate, borosilicate, and borate bioactive glass scaffolds with controllable degradation rate for bone tissue engineering applications. II. In vitro and in vivo biological evaluation. J Biomed Mater Res Part A 95, 172, 2010.
46. Gomide, V.S., Zonari, A., Ocarino, N.M., Goes, A.M., Serakides, R., and Pereira, M.M. In vitro and in vivo osteogenic potential of bioactive glass-PVA hybrid scaffolds colonized by mesenchymal stem cells. Biomed Mater 7, 015004. 2012.
47. Wilson, J., Pigott, G.H., Schoen, F.J., and Hench, L.L. Toxicology and biocompatibility of bioglasses. J Biomed Mater Res 15, 805, 1981.
48. Bosetti, M., Zanardi, L., Hench, L., and Cannas, M. Type I collagen production by osteoblast-like cells cultured in contact with different bioactive glasses. J Biomed Mater Res Part A 64, 189, 2003.
49. Xynos, I.D., Edgar, A.J., Buttery, L.D., Hench, L.L., and Polak, J.M. Gene-expression profiling of human osteoblasts following treatment with the ionic products of Bioglass 45S5 dissolution. J Biomed Mater Res 55, 151, 2001.
50. Tsigkou, O., Jones, J.R., Polak, J.M., and Stevens, M.M. Differentiation of fetal osteoblasts and formation of mineralized bone nodules by 45S5 Bioglass conditioned medium in the absence of osteogenic supplements. Biomaterials 30, 3542, 2009.
51. Day, R.M. Bioactive glass stimulates the secretion of angiogenic growth factors and angiogenesis in vitro. Tissue Eng 11, 768, 2005.
52. Leu, A., and Leach, J.K. Proangiogenic potential of a collagen/ bioactive glass substrate. Pharm Res 25, 1222, 2008.
53. Han, P., Wu, C., and Xiao, Y. The effect of silicate ions on proliferation, osteogenic differentiation and cell signalling pathways (WNT and SHH) of bone marrow stromal cells. Biomater Sci 1, 379, 2013.
54. Reffitt, D.M., Ogston, N., Jugdaohsingh, R., Cheung, H.F., Evans, B.A., Thompson, R.P., et al. Orthosilicic acid stimulates collagen type 1 synthesis and osteoblastic differentiation in human osteoblast-like cells in vitro. Bone 32, 127, 2003.
55. Frelin, C., Vigne, P., Ladoux, A., and Lazdunski, M. The regulation of the intracellular pH in cells from vertebrates. Eur J Biochem 174, 3, 1988.
56. Swenson, O., and Claff, C.L. Changes in the hydrogen ion concentration of healing fractures. Proc Soc Exp Biol Med 61, 151, 1946.
57. Arnett, T.R., and Dempster, D.W. Effect of pH on bone resorption by rat osteoclasts in vitro. Endocrinology 119, 119, 1986.
58. Newman, R.J., Francis, M.J., and Duthie, R.B. Nuclear magnetic resonance studies of experimentally induced delayed fracture union. Clin Orthop Relat Res 216, 253, 1987.
59. Kohn, D.H., Sarmadi, M., Helman, J.I., and Krebsbach, P.H. Effects of pH on human bone marrow stromal cells in vitro: implications for tissue engineering of bone. J Biomed Mater Res 60, 292, 2002.
60. Kaysinger, K.K., and Ramp, W.K. Extracellular pH modulates the activity of cultured human osteoblasts. J Cell Biochem 68, 83, 1998.