Oxygen and pH-sensitivity of human osteoarthritic chondrocytes in 3-D alginate bead culture system

Osteoarthritis and Cartilage

Volumn 21, Issue 11, 2013, Pages 1790-1798

  Collins, J A ^a   Moots, R J ^a   Winstanley, R ^a   Clegg, P D ^a   Milner, P I ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Hypoxia; Mitochondria; Osteoarthritis; PH; Redox imbalance

Indexed keywords

ADENOSINE TRIPHOSPHATE; COLLAGENASE 3; GLUTATHIONE; GLYCOSAMINOGLYCAN; INTERLEUKIN 1BETA; NITRATE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR SOX9; ALGINIC ACID; CULTURE MEDIUM; GLUCURONIC ACID; HEXURONIC ACID; MMP13 PROTEIN, HUMAN; NITRIC OXIDE;

ACIDOSIS; ANOXIA; ARTICLE; CARTILAGE CELL; CELL ISOLATION; CELL PH; CELL VIABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME RELEASE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INCUBATION TIME; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; OSTEOARTHRITIS; OXIDATION REDUCTION REACTION; OXYGEN TENSION; PH; PHENOTYPE; PRIORITY JOURNAL; TOTAL KNEE REPLACEMENT; AGED; ARTICULAR CARTILAGE; CELL CULTURE; CELL HYPOXIA; CELL SURVIVAL; CULTURE MEDIUM; KNEE OSTEOARTHRITIS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; AGED; ALGINATES; CARTILAGE, ARTICULAR; CELL HYPOXIA; CELL SURVIVAL; CELLS, CULTURED; CHONDROCYTES; CULTURE MEDIA; GLUCURONIC ACID; GLYCOSAMINOGLYCANS; HEXURONIC ACIDS; HUMANS; HYDROGEN-ION CONCENTRATION; MATRIX METALLOPROTEINASE 13; MEMBRANE POTENTIAL, MITOCHONDRIAL; NITRIC OXIDE; OSTEOARTHRITIS, KNEE; OXIDATION-REDUCTION; PHENOTYPE; REACTIVE OXYGEN SPECIES;

EID: 84884986825     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2013.06.028     Document Type: Article

References (48)

1. Poole A.R., Rosenberg L.C., Reiner A., Ionescu M., Bogoch E., Roughley P.J. Contents and distribution of the proteoglycans decorin and biglycan in normal and osteoarthritic human articular cartilage. JOrthop Res 1996, 14(5):681-689.
2. Wilkins R.J., Browning J.A., Ellory J.C. Surviving the matrix: membrane transport in articular chondrocytes. JMembr Biol 2000, 177(2):95-108.
3. Zhou S., Cui Z., Urban J.P. Factors influencing the oxygen concentration gradient from the synovial surface of articular cartilage to the cartilage-bone interface - a modelling study. Arthritis Rheum 2004, 50(12):3915-3924.
4. Hardingham T.E., Forsang A.J. Proteoglycans: many forms and functions. FASEB J 1992, 6(3):861-870.
5. Levick J.R. Hypoxia and acidosis in chronic inflammatory arthritis; relation to vascular supply and dynamic effusion pressure. JRheum 1990, 17(5):579-582.
6. Biniecka M., Kennedy A., Fearon U., Ng C.T., Veale D.J., O'Sullivan J.N. Oxidative damage in synovial tissue is associated with invivo hypoxic status in the arthritic joint. Ann Rheum Dis 2010, 69(6):1172-1178.
7. Mapp P.I., Grootveld M.C., Blake D.R. Hypoxia, oxidative stress and rheumatoid arthritis. Br Med Bull 1995, 51(2):419-436.
8. Konttinen Y.T., Mandelin J., Li T.F., Salo J., Lassus J., Liljestrom M., et al. Acidic cysteine endoproteinase cathepsin K in the degeneration of the superficial articular hyaline cartilage in osteoarthritis. Arth Rheum 2002, 46(4):953-960.
9. Schneider N., Mouithys-Mickalad A.L., Lejeune J.P., Deby-Dupont G.P., Hoebeke M., Serteyn D.A. Synoviocytes, not chondrocytes, release free radicals after cycle of anoxia/reoxygenation. Biochem Biophys Res Comm 2005, 334(2):669-673.
10. Coyle C.H., Izzo N.J., Chu C.R. Sustained hypoxia enhances chondrocyte matrix synthesis. JOrthop Res 2009, 27(6):793-799.
11. Das R.H., van Osch G.J., Kreukniet M., Oostra J., Weinans H., Jahr H. Effects of individual control of pH and hypoxia in chondrocyte culture. JOrthop Res 2010, 28(4):537-545.
12. Milner P.I., Fairfax T.P., Browning J.A., Wilkins R.J., Gibson J.S. The effect of O2 tension on pH homeostasis in equine articular chondrocytes. Arthritis Rheum 2006, 54(11):3523-3532.
13. Gibson J.S., Milner P.I., White R., Fairfax T.P., Wilkins R.J. Oxygen and reactive oxygen species in articular cartilage: modulators of ionic homeostasis. Pflugers Arch 2008, 455(4):563-573.
14. Shu Z., Jung M., Beger H.-G., Marzinzig M., Han F., Butzer U., et al. pH-dependent changes in nitric oxide, peroxynitrite and reactive oxygen species in hepatocellular damage. Am J Physiol 1997, 273(5 Pt 1):G1118-G1126.
15. Carvalho C., Santos M.S., Baldeiras I., Oliveira C.R., Seica R., Moreira P.I. Chronic hypoxia potentiates age-related oxidative imbalance in brain vessels and synaptosomes. Curr Neurovasc Res 2010, 7(4):288-300.
16. Scott J.L., Gabrielides C., Davidson R.K., Swingler T.E., Clark I.M., Wallis G.A., et al. Superoxide dismutase downregulation in osteoarthritis progression and end-stage disease. Ann Rheum Dis 2010, 69(8):1502-1510.
17. Fernandez-Moreno M., Soto-Hermida A., Pertega S., Oreiro N., Fernandez-Lopez C., Rego-Perez I., et al. Mitochondrial DNA (mtDNA) halpogroups and serum levels of anti-oxidant enzymes in patients with osteoarthritis. BMC Musculoskelet Disord 2011, 12:264.
18. Chubinskaya S., Huch K., Schulze M., Otten L., Aydelotte M.B., Cole A.A. Gene expression by human articular chondrocytes cultured in alginate beads. JHistochem Cytochem 2001, 49(10):1211-1219.
19. Farndale R.W., Sayers C.A., Barrett A.J. Adirect spectrophotometric microassay for sulphated glycosaminoglycans in cartilage cultures. Connect Tissue Res 1982, 9(4):247-248.
20. Hetrick E.M., Schoenfisch M.H. Analytical chemistry of nitric oxide. Ann Rev Anal Chem 2009, 2:409-433.
21. Chandel N.S., Schumacker P.T. Cellular oxygen sensing by mitochondria: old questions, new insight. JAppl Physiol 2000, 88(5):1880-1889.
22. Salvioli S., Ardizzoni A., Francheschi C., Cossarizza A. JC-1 but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett 1997, 411(1):77-82.
23. Tew S.R., Murdoch A.D., Rauchenberg R.P., Hardingham T.E. Cellular methods in cartilage research: primary human chondrocytes in culture and chondrogenesis in human bone marrow stem cells. Methods 2008, 45(1):2-9.
24. Mignotte F., Champagne A.M., Froger-Gaillard B., Benel L., Gueride M., Adolphe M., et al. Mitochondrial biogenesis in rabbit articular chondrocytes transferred to culture. Biol Cell 1991, 71(1-2):67-72.
25. Lin Z., Fitzgerald J.B., Xu J., Willers C., Wood D., Grodzinsky A.J., et al. Gene expression profiles of human chondrocytes during passaged monolayer cultivation. JOrthop Res 2008, 26(9):1230-1237.
26. Wilkins R.J., Hall A.C. Control of matrix synthesis in isolated bovine articular chondrocytes by extracellular and intracellular pH. JCell Physiol 1995, 164(3):474-481.
27. Geborek P., Saxne T., Pettersson H., Wollheim F.A. Synovial fluid acidosis correlates with radiological joint destruction in rheumatoid arthritis knee joints. JRheumatol 1989, 16(4):468-472.
28. Mansson B., Geborek P., Saxne T., Bjornsson S. Cytidine deaminase activity in synovial fluid of patients with rheumatoid arthritis: relation to lactoferrin, acidosis, and cartilage proteoglycan release. Ann Rheum Dis 1990, 49(8):594-597.
29. Blanco F.J., Ochs R.L., Schwarz R.L., Lotz M. Chondrocyte apoptosis induced by nitric oxide. Am J Pathol 1995, 146(1):75-85.
30. Mathy-Hartert M., Martin G., Devel P., Deby-Dupont G., Pujol J.P., Reginster J.Y., et al. Reactive oxygen species down-regulate pro-inflammatory gene expression by human chondrocytes. Inflamm Res 2003, 52(3):111-118.
31. Jetti S.K., Swain S.M., Majumder S., Chatterjee S., Poornima V., Bera A.K. Evaluation of the role of nitric oxide in acid sensing ion channel mediated cell death. Nitric Oxide 2010, 22(1):213-219.
32. Hu W., Chen F.H., Yuan F.L., Zhang T.Y., Fr Wu, Rong C., et al. Blockade of acid-sensing ion channels protects articular chondrocytes from acid-induced apoptotic injury. Inflamm Res 2012, 61(4):327-335.
33. Goldenthal M.J., Marin-Garcia J. Mitochondrial signaling pathways: a receiver/integrator organelle. Mol Cell Biochem 2004, 262(1-2):1-16.
34. Lee R.B., Urban J.P. Evidence for a negative Pasteur effect in articular cartilage. Biochem J 1997, 321(1):95-102.
35. Martin J.A., Martini A., Molinari A., Morgan W., Ramalingam W., Buckwalter J.A., et al. Mitochondrial electron transport and glycolysis are coupled in articular cartilage. Osteoarthritis Cartilage 2012, 20(4):323-329.
36. Rong C., Chen F.H., Jiang S., Hu W., Wu F.R., Chen T.Y., et al. Inhibition of acid-sensing ion channels by amiloride protects rat articular chondrocytes from acid-induced apoptosis via a mitochondrial-mediated pathway. Cell Biol Int 2012, 36(7):635-641.
37. Luperchio S., Tamir S., Tannenbaum S.R. NO-induced oxidative stress and glutathione metabolism in rodent and human cells. Free Rad Biol Med 1996, 21(4):513-519.
38. Cutaia M., Parks N. Oxidant stress decreases Na+/H+ antiport activity in bovine pulomonary artery endothelial cells. Am J Physiol 1994, 267(6 Pt 1):L649-L659.
39. Grimshaw M.J., Mason R.M. Bovine articular chondrocyte function invitro depends on oxygen tension. Osteoarthritis Cartilage 2000, 8(5):386-393.
40. Saini S., Wick T.M. Effect of low oxygen tension on tissue-engineered cartilage construct development in the concentric cylinder bioreactor. Tissue Eng 2004, 10(5-6):825-832.
41. Schneider N., Lejune J.P., Deby C., Deby-Dupont G.P., Serteyn D. Viability of equine articular chondrocytes in alginate beads exposed to different oxygen tensions. Vet J 2004, 168(2):167-173.
42. Boubriak O.A., Brooks J.T., Urban J.P. Cytochrome c oxidase levels in chondrocytes during monolayer expansion and after return to three dimensional culture. Osteoarthritis Cartilage 2009, 17(8):1084-1092.
43. Heywood H.K., Lee D.A. Monolayer expansion induces an oxidative metabolism and ROS in chondrocytes. Biochem Biophys Res Comm 2008, 373(2):224-229.
44. Heywood H.K., Lee D.A. Low oxygen reduces the modulation to an oxidative phenotype in monolayer-expanded chondrocytes. JCell Physiol 2010, 222(1):248-253.
45. Milner P.I., Wilkins R.J., Gibson J.S. The role of mitochondrial reactive oxygen species in pH regulation in articular chondrocytes. Osteoarthritis Cartilage 2007, 15(7):735-742.
46. Bindoli A., Fukuto J.M., Forman H.J. Thiol chemistry in peroxidise catalysis and redox signaling. Antioxid Redox Signal 2008, 10(9):1549-1564.
47. Shan X., Aw T.Y., Smith E.R., Ingelman-Sundberg M., Mannervik B., Iyanagi T., et al. Effect of chronic hypoxia on detoxification enzymes in rat liver. Biochem Pharmacol 1992, 43(11):2421-2426.
48. Mathy-Hartert M., Hogge L., Sanchez C., Deby-Dupont G., Crielaard J.M., Henrotin Y. Interleukin-1beta and interleukin-6 disturb the antioxidant enzyme system in bovine chondrocytes: a possible explanation for oxidative stress generation. Osteoarthritis Cartilage 2008, 16(7):756-763.