Haem oxygenase-1 induction reverses the actions of interleukin-1β on hypoxia-inducible transcription factors and human chondrocyte metabolism in hypoxia

Clinical Science

Volumn 125, Issue 2, 2013, Pages 99-108

  CĺErigues, Victoria ^a   Murphy, Christopher L ^b   GuilĺEn, Maria Isabel ^a,c   Alcara, Maria Jośe ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

Author keywords

Chondrocyte; Cytokines; Haem oxygenase 1; Hypoxia inducible transcription factor; Inflammation; Osteoarthritis

Indexed keywords

HEME OXYGENASE 1; HYPOXIA INDUCIBLE FACTOR; INTERLEUKIN 1BETA; MATRIX METALLOPROTEINASE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; COL2A1 PROTEIN, HUMAN; COLLAGEN TYPE 2; ENDOTHELIAL PAS DOMAIN CONTAINING PROTEIN 1; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; HIF1A PROTEIN, HUMAN; HMOX1 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IL1B PROTEIN, HUMAN; SOX9 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX9;

ARTICLE; CARTILAGE CELL; CELL HYPOXIA; CELL METABOLISM; CHONDROPROTECTION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; OSTEOARTHRITIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; RNA INTERFERENCE; AGED; ANOXIA; ARTICULAR CARTILAGE; ENZYMOLOGY; FEMALE; MALE; METABOLISM; MIDDLE AGED;

AGED; ANOXIA; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARTILAGE, ARTICULAR; CHONDROCYTES; COLLAGEN TYPE II; FEMALE; HEME OXYGENASE-1; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERLEUKIN-1BETA; MALE; MATRIX METALLOPROTEINASES; MIDDLE AGED; OSTEOARTHRITIS; SOX9 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

MLCS; MLOWN;

EID: 84878070834     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120491     Document Type: Article

References (41)

1. Semenza, G. L. (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408
2. Milner, P. I., Fairfax, T. P., Browning, J. A., Wilkins, R. J. and Gibson, J. S. (2006) The effect of O2 tension on pH homeostasis in equine articular chondrocytes. Arthritis Rheum. 54, 3523-3532
3. Murphy, C. L., Thoms, B. L., Vaghjiani, R. J. and Lafont, J. E. (2009) Hypoxia. HIF-mediated articular chondrocyte function: prospects for cartilage repair. Arthritis Res. Ther. 11, 213
4. Murphy, C. L. and Sambanis, A. (2001) Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes. Tissue Eng. 7, 791-803
5. Domm, C., Schunke, M., Christesen, K. and Kurz, B. (2002) Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension. Osteoarthritis Cartilage 10, 13-22
6. Murphy, C. L. and Polak, J. M. (2004) Control of human articular chondrocyte differentiation by reduced oxygen tension. J. Cell. Physiol. 199, 451-459
7. Lafont, J. E., Talma, S., Hopfgarten, C. and Murphy, C. L. (2008) Hypoxia promotes the differentiated human articular chondrocyte phenotype through SOX9-dependent and independent pathways. J. Biol. Chem. 283, 4778-4786
8. Adesida, A. B., Grady, L. M., Khan, W. S. and Hardingham, T. E. (2006) The matrix-forming phenotype of cultured human meniscus cells is enhanced after culture with fibroblast growth factor 2 and is further stimulated by hypoxia. Arthritis Res. Ther. 8, R61
9. Lafont, J. E., Talma, S. and Murphy, C. L. (2007) Hypoxiainducible factor 2α is essential for hypoxic induction of the human articular chondrocyte phenotype. Arthritis Rheum. 56, 3297-3306
10. Masson, N. and Ratcliffe, P. J. (2003) HIF prolyl and asparaginyl hydroxylases in the biological response to intracellular O2 levels. J. Cell. Sci. 116, 3041-3049
11. Jung, Y. J., Isaacs, J. S., Lee, S., Trepel, J. and Neckers, L. (2003) IL-1β-mediated up-regulation of HIF-1α via an NFκB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J. 17, 2115-2117
12. Coimbra, I. B., Jimenez, S. A., Hawkins, D. F., Piera-Velazquez, S. and Stokes, D. G. (2004) Hypoxia inducible factor-1α expression in human normal and osteoarthritic chondrocytes. Osteoarthritis Cartilage 12, 336-345
13. Grimmer, C., Pfander, D., Swoboda, B., Aigner, T., Mueller, L., Hennig, F. F. and Gelse, K. (2007) Hypoxia-inducible factor 1α is involved in the prostaglandin metabolism of osteoarthritic cartilage through up-regulation of microsomal prostaglandin E synthase 1 in articular chondrocytes. Arthritis Rheum. 56, 4084-4094
14. Pfander, D., Cramer, T. and Swoboda, B. (2005) Hypoxia and HIF-1α in osteoarthritis. Int. Orthop. 29, 6-9
15. Bohensky, J., Terkhorn, S. P., Freeman, T. A., Adams, C. S., Garcia, J. A., Shapiro, I. M. and Srinivas, V. (2009) Regulation of autophagy in human and murine cartilage: hypoxia-inducible factor 2 suppresses chondrocyte autophagy. Arthritis Rheum. 60, 1406-1415
16. Lundvig, D. M., Immenschuh, S. and Wagener, F. A. (2012) Heme oxygenase, inflammation, and fibrosis: the good, the bad, and the ugly? Front. Pharmacol. 3, 81
17. Alcaraz, M. J., Fernandez, P. and Guillen, M. I. (2003) Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr. Pharm. Des. 9, 2541-2551
18. Guillen, M. I., Megias, J., Gomar, F. and Alcaraz, M. J. (2008) Heme oxygenase-1 regulates catabolic and anabolic processes in osteoarthritic chondrocytes. J. Pathol. 214, 515-522
19. Megias, J., Guillen, M. I., Clerigues, V., Rojo, A. I., Cuadrado, A., Castejon, M. A., Gomar, F. and Alcaraz, M. J. (2009) Heme oxygenase-1 induction modulates microsomal prostaglandin E synthase-1 expression and prostaglandin E2 production in osteoarthritic chondrocytes. Biochem. Pharmacol. 77, 1806-1813
20. Ruiz-Romero, C., Calamia, V., Rocha, B., Mateos, J., Fernandez-Puente, P. and Blanco, F. J. (2010) Hypoxia conditions differentially modulate human normal and osteoarthritic chondrocyte proteomes. J. Proteome Res. 9, 3035-3045
21. Clerigues, V., Guillen, M. I., Gomar, F. and Alcaraz, M. J. (2012) Haem oxygenase-1 counteracts the effects of interleukin-1β on inflammatory and senescence markers in cartilage-subchondral bone explants from osteoarthritic patients. Clin. Sci. 122, 239-250
22. Clerigues, V., Guillen, M. I., Castejon, M. A., Gomar, F., Mirabet, V. and Alcaraz, M. J. (2012) Heme oxygenase-1 mediates protective effects on inflammatory, catabolic and senescence responses induced by interleukin-1β in osteoarthritic osteoblasts. Biochem. Pharmacol. 83, 395-405
23. Silver, I. A. (1975) Measurement of pH and ionic composition of pericellular sites. Phil. Trans. R. Soc. Lond. B Biol. Sci. 271, 261-272
24. Tetlow, L. C., Adlam, D. J. and Woolley, D. E. (2001) Matrix metalloproteinase and proinflammatory cytokine production by chondrocytes of human osteoarthritic cartilage: associations with degenerative changes. Arthritis Rheum. 44, 585-594
25. Attur, M. G., Patel, I. R., Patel, R. N., Abramson, S. B. and Amin, A. R. (1998) Autocrine production of IL-1β by human osteoarthritis-affected cartilage and differential regulation of endogenous nitric oxide, IL-6, prostaglandin E2, and IL-8. Proc. Assoc. Am. Physicians 110, 65-72
26. Goldring, M. B., Birkhead, J., Sandell, L. J., Kimura, T. and Krane, S. M. (1988) Interleukin 1 suppresses expression of cartilage-specific types II and IX collagens and increases types I and III collagens in human chondrocytes. J. Clin. Invest. 82, 2026-2037
27. Radhakrishnan, N., Yadav, S. P., Sachdeva, A., Pruthi, P. K., Sawhney, S., Piplani, T., Wada, T. and Yachie, A. (2011) Human heme oxygenase-1 deficiency presenting with hemolysis, nephritis, and asplenia. J. Pediatr. Hematol. Oncol. 33, 74-78
28. Wang, G., Hamid, T., Keith, R. J., Zhou, G., Partridge, C. R., Xiang, X., Kingery, J. R., Lewis, R. K., Li, Q., Rokosh, D. G. et al. (2010) Cardioprotective and antiapoptotic effects of heme oxygenase-1 in the failing heart. Circulation 121, 1912-1925
29. Willoughby, D. A., Moore, A. R., Colville-Nash, P. R. and Gilroy, D. (2000) Resolution of inflammation. Int. J. Immunopharmacol. 22, 1131-1135
30. Kobayashi, H., Takeno, M., Saito, T., Takeda, Y., Kirino, Y., Noyori, K., Hayashi, T., Ueda, A. and Ishigatsubo, Y. (2006) Regulatory role of heme oxygenase 1 in inflammation of rheumatoid arthritis. Arthritis Rheum. 54, 1132-1142
31. Devesa, I., Ferrandiz, M. L., Terencio, M. C., Joosten, L. A., van den Berg, W. B. and Alcaraz, M. J. (2005) Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis Rheum. 52, 3230-3238
32. Ferŕandiz, M. L., Maicas, N., Garcia-Arnandis, I., Terencio, M. C., Motterlini, R., Devesa, I., Joosten, L. A. B., van den Berg, W. B. and Alcaraz, M. J. (2008) Treatment with a CO-releasing molecule (CORM-3) reduces joint inflammation and erosion in murine collagen-induced arthritis. Ann. Rheum. Dis. 67, 1211-1217
33. Bonelli, M., Savitskaya, A., Steiner, C. W., Rath, E., Bilban, M., Wagner, O., Bach, F. H., Smolen, J. S. and Scheinecker, C. (2012) Heme oxygenase-1 end-products carbon monoxide and biliverdin ameliorate murine collagen induced arthritis. Clin. Exp. Rheumatol. 30, 73-78
34. Exner, M., Minar, E., Wagner, O. and Schillinger, M. (2004) The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radical Biol. Med. 37, 1097-1104
35. Grochot-Przeczek, A., Dulak, J. and Jozkowicz, A. (2012) Haem oxygenase-1: non-canonical roles in physiology and pathology. Clin. Sci. 122, 93-103
36. Wagener, F. A., Toonen, E. J., Wigman, L., Fransen, J., Creemers, M. C., Radstake, T. R., Coenen, M. J., Barrera, P., van Riel, P. L. and Russel, F. G. (2008) HMOX1 promoter polymorphism modulates the relationship between disease activity and joint damage in rheumatoid arthritis. Arthritis Rheum. 58, 3388-3393
37. Kitamuro, T., Takahashi, K., Ogawa, K., Udono-Fujimori, R., Takeda, K., Furuyama, K., Nakayama, M., Sun, J., Fujita, H., Hida, W. et al. (2003) Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells. J. Biol. Chem. 278, 9125-9133
38. Lofstedt, T., Fredlund, E., Holmquist-Mengelbier, L., Pietras, A., Ovenberger, M., Poellinger, L. and Pahlman, S. (2007) Hypoxia inducible factor-2α in cancer. Cell Cycle 6, 919-926
39. Yang, S., Kim, J., Ryu, J. H., Oh, H., Chun, C. H., Kim, B. J., Min, B. H. and Chun, J. S. (2010) Hypoxia-inducible factor-2α is a catabolic regulator of osteoarthritic cartilage destruction. Nat. Med. 16, 687-693
40. Saito, T., Fukai, A., Mabuchi, A., Ikeda, T., Yano, F., Ohba, S., Nishida, N., Akune, T., Yoshimura, N., Nakagawa, T. et al. (2010) Transcriptional regulation of endochondral ossification by HIF-2α during skeletal growth and osteoarthritis development. Nat. Med. 16, 678-686
41. Murphy, C. L. (2010) HIF-2α-a mediator of osteoarthritis? Cell Res. 20, 977-979