The importance of bicarbonate and nonbicarbonate buffer systems in batch and continuous flow bioreactors for articular cartilage tissue engineering

Tissue Engineering - Part C: Methods

Volumn 18, Issue 5, 2012, Pages 358-368

  Khan, Aasma A ^a,b,c   Surrao, Denver C ^b,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b QUEEN S UNIVERSITY   (Canada)

^c KINGSTON GENERAL HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCONVERSION; BODY FLUIDS; CARTILAGE; CELL CULTURE; CELL PROLIFERATION; TISSUE; TISSUE ENGINEERING;

ACIDIC ENVIRONMENT; ARTICULAR CARTILAGES; BOVINE CHONDROCYTES; BUFFER SYSTEM; CARTILAGE TISSUE ENGINEERING; CARTILAGINOUS TISSUES; CHONDROCYTE PROLIFERATION; CHONDROCYTES; COMBINED EFFECT; CONTINUOUS CULTURE; CONTINUOUS FLOWS; CONTINUOUS-FLOW; CULTURE SYSTEMS; EXPANSION PHASE; EXTRACELLULAR ENVIRONMENTS; EXTRACELLULAR MATRICES; GLYCOSAMINOGLYCANS; IN-VITRO; INFINITE SUPPLY; SODIUM BICARBONATES; STATIC CONDITIONS; STATIC CULTURE; THREE-DIMENSIONAL CULTURE; TISSUE CONSTRUCTS; TISSUE GROWTH; TISSUE OUTGROWTH;

BIOREACTORS;

BOVINAE;

BICARBONATE; BUFFER;

ANIMAL; ARTICLE; ARTICULAR CARTILAGE; BATCH CELL CULTURE; BIOREACTOR; CARTILAGE CELL; CATTLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METHODOLOGY; ORGAN CULTURE TECHNIQUE; PH; PHYSIOLOGY; TISSUE ENGINEERING;

ANIMALS; BATCH CELL CULTURE TECHNIQUES; BIOREACTORS; BUFFERS; CARTILAGE, ARTICULAR; CATTLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CHONDROCYTES; CULTURE MEDIA; HYDROGEN-ION CONCENTRATION; ORGAN CULTURE TECHNIQUES; SODIUM BICARBONATE; TISSUE ENGINEERING;

EID: 84860539627     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2011.0137     Document Type: Article

References (63)

1. Buckley, C.T., Thorpe, S.D., and Kelly, D.J. Engineering of large cartilaginous tissues through the use of microchanneled hydrogels and rotational culture. Tissue Eng Part A 15, 3213, 2009.
2. Concaro, S., Gustavson, F., and Gatenholm, P. Bioreactors for tissue engineering of cartilage. Adv Biochem Eng Biotechnol 112, 125, 2009.
3. Davisson, T., Sah, R.L., and Ratcliffe, A. Perfusion increases cell content and matrix synthesis in chondrocyte threedimensional cultures. Tissue Eng 8, 807, 2002.
4. Seidel, J.O., Pei, M., Gray, M.L., Langer, R., Freed, L.E., and Vunjak-Novakovic, G. Long-term culture of tissue engineered cartilage in a perfused chamber with mechanical stimulation. Biorheology 41, 445, 2004.
5. Stojkovska, J., Bugarski, B., and Obradovic, B. Evaluation of alginate hydrogels under in vivo-like bioreactor conditions for cartilage tissue engineering. J Mater Sci Mater Med 21, 2869, 2010.
6. Villanueva, I., Klement, B.J., von Deutsch, D., and Bryant, S.J. Cross-linking density alters early metabolic activities in chondrocytes encapsulated in poly(ethylene glycol) hydrogels and cultured in the rotating wall vessel. Biotechnol Bioeng 102, 1242, 2009.
7. Xu, X., Urban, J.P., Tirlapur, U., Wu, M.H., and Cui, Z. Influence of perfusion on metabolism and matrix production by bovine articular chondrocytes in hydrogel scaffolds. Biotechnol Bioeng 93, 1103, 2006.
8. Khan, A.A., Suits, J.M., Kandel, R.A., and Waldman, S.D. The effect of continuous culture on the growth and structure of tissue-engineered cartilage. Biotechnol Prog 25, 508, 2009.
9. Otte, P. Basic cell metabolism of articular cartilage. Manometric studies. Z Rheumatol 50, 304, 1991.
10. Lee, R.B., and Urban, J.P. Evidence for a negative Pasteur effect in articular cartilage. Biochem J 321(Pt 1), 95, 1997.
11. Das, R.H., van Osch, G.J., Kreukniet, M., Oostra, J., Weinans, H., and Jahr, H. Effects of individual control of pH and hypoxia in chondrocyte culture. J Orthop Res 28, 537, 2010.
12. Zhou, S., Cui, Z., and Urban, J.P. Nutrient gradients in engineered cartilage: metabolic kinetics measurement and mass transfer modeling. Biotechnol Bioeng 101, 408, 2008.
13. Gray, M.L., Pizzanelli, A.M., Grodzinsky, A.J., and Lee, R.C. Mechanical and physiochemical determinants of the chondrocyte biosynthetic response. J Orthop Res 6, 777, 1988.
14. Ohshima, H., and Urban, J.P. The effect of lactate and pH on proteoglycan and protein synthesis rates in the intervertebral disc. Spine (Phila Pa 1976) 17, 1079, 1992.
15. Razaq, S., Wilkins, R.J., and Urban, J.P. The effect of extracellular pH on matrix turnover by cells of the bovine nucleus pulposus. Eur Spine J 12, 341, 2003.
16. Schwartz, E.R., Kirkpatrick, P.R., and Thompson, R.C. The effect of environmental pH on glycosaminoglycan metabolism by normal human chondrocytes. J Lab Clin Med 87, 198, 1976.
17. Wilkins, R.J., and Hall, A.C. Measurement of intracellular pH in isolated bovine articular chondrocytes. Exp Physiol 77, 521, 1992.
18. Wilkins, R.J., and Hall, A.C. Control of matrix synthesis in isolated bovine chondrocytes by extracellular and intracellular pH. J Cell Physiol 164, 474, 1995.
19. Wu, M.H., Urban, J.P., Cui, Z.F., Cui, Z., and Xu, X. Effect of extracellular pH on matrix synthesis by chondrocytes in 3D agarose gel. Biotechnol Prog 23, 430, 2007.
20. Xu, X., Urban, J.P., Browning, J.A., Tirlapur, U., Wilkins, R.J., Wu, M.H., et al. Influences of buffer systems on chondrocyte growth during long-term culture in alginate. Osteoarthritis Cartilage 15, 396, 2007.
21. Hall, A.C., Horwitz, E.R., and Wilkins, R.J. The cellular physiology of articular cartilage. Exp Physiol 81, 535, 1996.
22. Simpkin, V.L., Murray, D.H., Hall, A.P., and Hall, A.C. Bicarbonate-dependent pH(i) regulation by chondrocytes within the superficial zone of bovine articular cartilage. J Cell Physiol 212, 600, 2007.
23. Freyria, A.M., Yang, Y., Chajra, H., Rousseau, C.F., Ronziere, M.C., Herbage, D., et al. Optimization of dynamic culture conditions: effects on biosynthetic activities of chondrocytes grown in collagen sponges. Tissue Eng 11, 674, 2005.
24. Mahmood, T.A., Shastri, V.P., van Blitterswijk, C.A., Langer, R., and Riesle, J. Tissue engineering of bovine articular cartilage within porous poly(ether ester) copolymer scaffolds with different structures. Tissue Eng 11, 1244, 2005.
25. Nagel-Heyer, S., Goepfert, C., Adamietz, P., Meenen, N.M., and Portner, R. Cultivation of three-dimensional cartilagecarrier-constructs under reduced oxygen tension. J Biotechnol 121, 486, 2006.
26. Pazzano, D., Mercier, K.A., Moran, J.M., Fong, S.S., DiBiasio, D.D., Rulfs, J.X., et al. Comparison of chondrogensis in static and perfused bioreactor culture. Biotechnol Prog 16, 893, 2000.
27. Schulz, R.M., Wustneck, N., van Donkelaar, C.C., Shelton, J.C., and Bader, A. Development and validation of a novel bioreactor system for load-and perfusion-controlled tissue engineering of chondrocyte-constructs. Biotechnol Bioeng 101, 714, 2008.
28. Tigli, R.S., and Gumusderelioglu, M. Chondrogenesis on BMP-6 loaded chitosan scaffolds in stationary and dynamic cultures. Biotechnol Bioeng 104, 601, 2009.
29. Cordat, E., and Casey, J.R. Bicarbonate transport in cell physiology and disease. Biochem J 417, 423, 2009.
30. Lelong, I.H., and Rebel, G. pH drift of "physiological buffers" and culture media used for cell incubation during in vitro studies. J Pharmacol Toxicol Methods 39, 203, 1998.
31. Levraut, J., Labib, Y., Chave, S., Payan, P., Raucoules-Aime, M., and Grimaud, D. Effect of sodium bicarbonate on intracellular pH under different buffering conditions. Kidney Int 49, 1262, 1996.
32. Mather, J.P., and Barnes, D. Methods in Cell Biology. San Diego: Academic Press, 1998.
33. Levraut, J., Giunti, C., Ciebiera, J.P., de Sousa, G., Ramhani, R., Payan, P., et al. Initial effect of sodium bicarbonate on intracellular pH depends on the extracellular nonbicarbonate buffering capacity. Crit Care Med 29, 1033, 2001.
34. Amadio, P.C., Ehrlich, M.G., and Mankin, H.J. Matrix synthesis in high density cultures of bovine epiphyseal plate chondrocytes. Connect Tissue Res 11, 11, 1983.
35. Waldman, S.D., Couto, D.C., Omelon, S.J., and Kandel, R.A. Effect of sodium bicarbonate on extracellular pH, matrix accumulation, and morphology of cultured articular chondrocytes. Tissue Eng 10, 1633, 2004.
36. Ham, R.G. Clonal growth of mammalian cells in a chemically defined, synthetic medium. Proc Natl Acad Sci USA 53, 288, 1965.
37. Dessau, W., Sasse, J., Timpl, R., Jilek, F., and von der Mark, K. Synthesis and extracellular deposition of fibronectin in chondrocyte cultures. Response to the removal of extracellular cartilage matrix. J Cell Biol 79, 342, 1978.
38. Boyle, J., Luan, B., Cruz, T.F., and Kandel, R.A. Characterization of proteoglycan accumulation during formation of cartilagenous tissue in vitro. Osteoarthritis Cartilage 3, 117, 1995.
39. Farndale, R.W., Buttle, D.J., and Barrett, A.J. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883, 173, 1986.
40. Goldberg, R.L., and Kolibas, L.M. An improved method for determining proteoglycans synthesized by chondrocytes in culture. Connect Tissue Res 24, 265, 1990.
41. Composition and structure of articular cartilage. In: Brandt, K.D., Doherty, M., and Lohmander, L.S., eds. Osteoarthritis. New York: Oxford University Press Inc., 1998, pp. 110-111.
42. Woessner, J.F., Jr. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93, 440, 1961.
43. Kim, Y.J., Sah, R.L., Doong, J.Y., and Grodzinsky, A.J. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174, 168, 1988.
44. Hayes, A.J., Hall, A., Brown, L., Tubo, R., and Caterson, B. Macromolecular organization and in vitro growth characteristics of scaffold-free neocartilage grafts. J Histochem Cytochem 55, 853, 2007.
45. Hoch, D.H., Grodzinsky, A.J., Koob, T.J., Albert, M.L., and Eyre, D.R. Early changes in material properties of rabbit articular cartilage after meniscectomy. J Orthop Res 1, 4, 1983.
46. Hayes, W.C., Keer, L.M., Herrmann, G., and Mockros, L.F. A mathematical analysis for indentation tests of articular cartilage. J Biomech 5, 541, 1972.
47. Chen, T., Zhou, Y., and Tan, W.S. Influence of lactic acid on the proliferation, metabolism, and differentiation of rabbit mesenchymal stem cells. Cell Biol Toxicol 25, 573, 2009.
48. Kallos, M.S., and Behie, L.A. Inoculation and growth conditions for high-cell-density expansion of mammalian neural stem cells in suspension bioreactors. Biotechnol Bioeng 63, 473, 1999.
49. Shrode, L.D., Tapper, H., and Grinstein, S. Role of intracellular pH in proliferation, transformation, and apoptosis. J Bioenerg Biomembr 29, 393, 1997.
50. Xu, X., Urban, J.P., Tirlapur, U.K., and Cui, Z. Osmolarity effects on bovine articular chondrocytes during threedimensional culture in alginate beads. Osteoarthritis Cartilage 18, 433, 2010.
51. Wilkins, R.J., and Hall, A.C. Bovine articular chondrocytes demonstrate only minimal bicarbonate-dependent recovery from changes to intracellular pH. J Physiol 459, 289, 1993.
52. Wilkins, R.J., Browning, J.A., and Ellory, J.C. Surviving in a matrix: membrane transport in articular chondrocytes. J Membr Biol 177, 95, 2000.
53. Dascalu, A., Nevo, Z., and Korenstein, R. The control of intracellular pH in cultured avian chondrocytes. J Physiol 461, 583, 1993.
54. Oppenheimer, S.B., Edidin, M., Orr, C.W., and Roseman, S. An L-glutamine requirement for intercellular adhesion. Proc Natl Acad Sci USA 63, 1395, 1969.
55. Swietach, P., Tiffert, T., Mauritz, J.M., Seear, R., Esposito, A., Kaminski, C.F., et al. Hydrogen ion dynamics in human red blood cells. J Physiol 588, 4995, 2010.
56. Zhao, Y., and Baltz, J.M. Bicarbonate/chloride exchange and intracellular pH throughout preimplantation mouse embryo development. Am J Physiol 271, C1512, 1996.
57. Browning, J.A., and Wilkins, R.J. Mechanisms contributing to intracellular pH homeostasis in an immortalised human chondrocyte cell line. Comp Biochem Physiol A Mol Integr Physiol 137, 409, 2004.
58. Bush, P.G., and Hall, A.C. The osmotic sensitivity of isolated and in situ bovine articular chondrocytes. J Orthop Res 19, 768, 2001.
59. Urban, J.P., Hall, A.C., and Gehl, K.A. Regulation of matrix synthesis rates by the ionic and osmotic environment of articular chondrocytes. J Cell Physiol 154, 262, 1993.
60. Vunjak-Novakovic, G., Martin, I., Obradovic, B., Treppo, S., Grodzinsky, A.J., Langer, R., et al. Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage. J Orthop Res 17, 130, 1999.
61. Vunjak-Novakovic, G., Obradovic, B., Martin, I., and Freed, L.E. Bioreactor studies of native and tissue engineered cartilage. Biorheology 39, 259, 2002.
62. Obradovic, B., Carrier, R.L., Vunjak-Novakovic, G., and Freed, L.E. Gas exchange is essential for bioreactor cultivation of tissue engineered cartilage. Biotechnol Bioeng 63, 197, 1999.
63. Razaq, S., Urban, J.P., and Wilkins, R.J. Regulation of intracellular pH by bovine intervertebral disc cells. Cell Physiol Biochem 10, 109, 2000.