Osteoarthritis and Cartilage
Volume 18, Issue 9 , Pages 1167-1173 , September 2010

Hypoxia, RONS and energy metabolism in articular cartilage

  • B. Fermor

      Affiliations

    • Corresponding Author InformationAddress correspondence and reprint requests to: Beverley Fermor, Department of Surgery, Division of Orthopaedic Surgery, Duke University Medical Center, Box 3093, 375 Medical Sciences Research Building, Durham, NC 27710, USA. Tel: 1-919-681-6867; Fax: 1-919-684-8490.
    • ,
  • A. Gurumurthy
    • ,
  • B.O. Diekman

Received 6 January 2010 ,Accepted 9 June 2010.

References 

  1. Henrotin YE, Bruckner P, Pujol JP. The role of reactive oxygen species in homeostasis and degradation of cartilage. Osteoarthritis Cartilage. 2003;11:747–755
  2. Weinberg J, Fermor B, Guilak F. Nitric oxide synthase and cyclooxygenase interactions in cartilage and meniscus: relationships to joint physiology, arthritis, and tissue repair. In:  Harris R editors. Inflammation in the Pathogenesis of Chronic Diseases: The COX-2 Controversy – Subcellular Biochemistry. Volume 42:New York: Springer; 2007;p. 31–62
  3. Fermor B, Weinberg JB, Pisetsky DS, Misukonis MA, Banes AB, Guilak F. The effects of static and intermittent compression on nitric oxide production in articular cartilage explants. J Orthop Res. 2001;19:72–80
  4. Cernanec J, Guilak F, Weinberg JB, Pisetsky DS, Fermor B. Influence of hypoxia and reoxygenation on cytokine-induced production of proinflammatory mediators in articular cartilage. Arthritis Rheum. 2002;46:968–975
  5. Smith R, Carter D, Schurman D. Pressure and shear differentially alter human articular chondrocyte metabolism: a review. Clin Orthop Rel Res. 2004;(427 Suppl):S89–S95
  6. Abramson S, Attur M. Developments in the scientific understanding of osteoarthritis. Arthritis Res Ther. 2009;11:227–235
  7. Lotz M, Hashimoto S, Kuhn K. Mechanisms of chondrocyte apoptosis. Osteoarthritis Cartilage. 1999;7:389–391
  8. Pelletier JP, Jovanovic D, Fernandes JC, Manning P, Connor JR, Currie MG, et al. Reduction in the structural changes of experimental osteoarthritis by a nitric oxide inhibitor. Osteoarthritis Cartilage. 1999;7:416–418
  9. Studer RK, Levicoff E, Georgescu H, Miller L, Jaffurs D, Evans C. Nitric oxide inhibits chondrocyte response to IGF1: inhibition of IGF-1Rbeta tyrosine phosphorylation. Am J Physiol. 2000;279:C961–C969
  10. Davies CM, Guilak F, Weinberg JB, Fermor B. Reactive nitrogen and oxygen species in interleukin-1-mediated DNA damage associated with osteoarthritis. Osteoarthritis Cartilage. 2008;16:624–630
  11. Chen AF, Davies CM, De Lin M, Fermor B. Oxidative DNA damage in osteoarthritic porcine articular cartilage. J Cell Physiol. 2008;217:828–833
  12. Stefanovic-Racic M, Stadler J, Georgescu HI, Evans CH. Nitric oxide and energy production in articular chondrocytes. J Cell Physiol. 1994;159:274–280
  13. Silver IA. Measurement of pH and ionic composition of pericellular sites. Philos Trans R Soc Lond B Biol Sci. 1975;271:261–272
  14. Zhou S, Cui Z, Urban JP. Factors influencing the oxygen concentration gradient from the synovial surface of articular cartilage to the cartilage–bone interface: a modeling study. Arthritis Rheum. 2004;50:3915–3924
  15. Fermor B, Christensen SE, Youn I, Cernanec JM, Davies CM, Weinberg JB. Oxygen, nitric oxide and articular cartilage. Eur Cell Mater. 2007;13:56–65
  16. Hashimoto K, Fukuda K, Yamazaki K, Yamamoto N, Matsushita T, Hayakawa S, et al. Hypoxia-induced hyaluronan synthesis by articular chondrocytes: the role of nitric oxide. Inflamm Res. 2006;55:72–77
  17. Milner P, Fairfax T, Browning JA, Wilkins R, Gibson J. The effect of oxygen tension on pH homeostasis in equine articular chondrocytes. Arthritis Rheum. 2006;54:3523–3532
  18. Peansukmanee S, Vaughan-Thomas A, Carter S, Clegg P, Taylor S, Redmond C, et al. Effects of hypoxia on glucose transport in primary equine chondrocytes in vitro and evidence of reduced GLUT1 gene expression in pathologic cartilage in vivo. J Orthop Res. 2009;27:529–535
  19. Bywaters EGL. The metabolism of joint tissues. J Pathol Bacteriol. 1937;44:247–268
  20. Tushan FS, Rodnan GP, Altman M, Robin ED. Anaerobic glycolysis and lactate dehydrogenase (LDH) isoenzymes in articular cartilage. J Lab Clin Med. 1969;73:649–650
  21. Johnson K, Jung A, Murphy A, Andreyev A, Dykens J, Terkeltaub R. Mitochondrial oxidative phosphorylation is a downstream regulator of nitric oxide effects on chondrocyte matrix synthesis and mineralization. Arthritis Rheum. 2000;43:1560–1570
  22. Taylor CT. Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J. 2008;409:19–26
  23. Aigner T, Hemmel M, Neureiter D, Gebhard PM, Zeiler G, Kirchner T, et al. Apoptotic cell death is not a widespread phenomenon in normal aging and osteoarthritis human articular knee cartilage: a study of proliferation, programmed cell death (apoptosis), and viability of chondrocytes in normal and osteoarthritic human knee cartilage. Arthritis Rheum. 2001;44:1304–1312
  24. Muller M. Cellular senescence: molecular mechanisms, in vivo significance, and redox considerations. Antioxid Redox Signal. 2009;11:59–98
  25. Dai SM, Shan ZZ, Nakamura H, Masuko-Hongo K, Kato T, Nishioka K, et al. Catabolic stress induces features of chondrocyte senescence through overexpression of caveolin 1: possible involvement of caveolin 1-induced down-regulation of articular chondrocytes in the pathogenesis of osteoarthritis. Arthritis Rheum. 2006;54:818–831
  26. Martin JA, Buckwalter JA. The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. J Bone Joint Surg Am. 2003;85-A(Suppl 2):106–110
  27. Price JS, Waters JG, Darrah C, Pennington C, Edwards DR, Donell ST, et al. The role of chondrocyte senescence in osteoarthritis. Aging Cell. 2002;1:57–65
  28. Yudoh K, Nguyen T, Nakamura H, Hongo-Masuko K, Kato T, Nishioka K. Potential involvement of oxidative stress in cartilage senescence and development of osteoarthritis: oxidative stress induces chondrocyte telomere instability and downregulation of chondrocyte function. Arthritis Res Ther. 2005;7:R380–R391
  29. Liu L, Cash TP, Jones RG, Keith B, Thompson CB, Simon MC. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol Cell. 2006;21:521–531
  30. Roach H, Aigner T, Kouri JB. Chondroptosis: a variant of apoptotic cell death in chondrocytes?. Apoptosis. 2004;9:265–277
  31. Peterson RT, Schreiber SL. Translation control: connecting mitogens and the ribosome. Curr Biol. 1998;8:R248–R250
  32. Jefferies HB, Fumagalli S, Dennis PB, Reinhard C, Pearson RB, Thomas G. Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70S6K. Embo J. 1997;16:3693–3704
  33. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19:5720–5728
  34. Del Carlo M, Loeser RF. Nitric oxide-mediated chondrocyte cell death requires the generation of additional reactive oxygen species. Arthritis Rheum. 2002;46:394–403
  35. Baker MS, Feigan J, Lowther DA. The mechanism of chondrocyte hydrogen peroxide damage. Depletion of intracellular ATP due to suppression of glycolysis caused by oxidation of glyceraldehyde-3-phosphate dehydrogenase. J Rheumatol. 1989;16:7–14
  36. Davies KJ. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life. 2000;50:279–289
  37. Martin JA, Klingelhutz AJ, Moussavi-Harami F, Buckwalter JA. Effects of oxidative damage and telomerase activity on human articular cartilage chondrocyte senescence. J Gerontol A Biol Sci Med Sci. 2004;59:324–337
  38. Shohet RV, Garcia JA. Keeping the engine primed: HIF factors as key regulators of cardiac metabolism and angiogenesis during ischemia. J Mol Med. 2007;85:1309–1315
  39. Cernanec JM, Weinberg JB, Batinic-Haberle I, Guilak F, Fermor B. Influence of oxygen tension on interleukin 1-induced peroxynitrite formation and matrix turnover in articular cartilage. J Rheumatol. 2007;34:401–407
  40. Fukuda K, Kumano F, Takayama M, Saito M, Otani K, Tanaka S. Zonal differences in nitric oxide synthesis by bovine chondrocytes exposed to interleukin-1. Inflamm Res. 1995;44:434–437
  41. Wang W, Yang X, Lopez de Silanes I, Carling D, Gorospe M. Increased AMP: ATP ratio and AMP-activated protein kinase activity during cellular senescence linked to reduced HuR function. J Biol Chem. 2003;278:27016–27023
  42. White E, Lowe S. Eating to exit: autophagy-enabled senescence revealed. Genes Dev. 2009;23:784–787
  43. Bohensky J, Terkhorn SP, Freeman TA, Adams CS, Garcia JA, Shapiro IM, et al. Regulation of autophagy in human and murine cartilage: hypoxia-inducible factor 2 suppresses chondrocyte autophagy. Arthritis Rheum. 2009;60:1406–1415
  44. Carames B, Taniguchi N, Otsuki S, Blanco F, Lotz M. Autophagy is a protective mechanism in normal cartilage, and its aging-related loss is linked with cell death and osteoarthritis. Arthritis Rheum. 2010;62:791–801
  45. Almonte-Becerril M, Navarro-Garcia F, Gonzalez-Robles A, Vega-Lopez MA, Lavalle C, Kouri JB. Cell death of chondrocytes is a combination between apoptosis and autophagy during the pathogenesis of osteoarthritis within an experimental model. Apoptosis. 2010;
  46. Pfander D, Swoboda B, Cramer T. The role of HIF-1alpha in maintaining cartilage homeostasis and during the pathogenesis of osteoarthritis. Arthritis Res Ther. 2006;8:104
  47. Yudoh K, Nakamura H, Masuko-Hongo K, Kato T, Nishioka K. Catabolic stress induces expression of hypoxia-inducible factor (HIF)-1alpha in articular chondrocytes; involvement of HIF-1alpha in the pathogenesis of osteoarthritis. Arthritis Res Ther. 2005;7:R904–R914

PII: S1063-4584(10)00202-5

doi: 10.1016/j.joca.2010.06.004

Osteoarthritis and Cartilage
Volume 18, Issue 9 , Pages 1167-1173 , September 2010

Article Tools

* Image Usage & Resolution