cAMP response element-binding (CREB) recruitment following a specific CpG demethylation leads to the elevated expression of the matrix metalloproteinase 13 in human articular chondrocytes and osteoarthritis

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 3000-3011

  Bui, Catherine ^a   Barter, Matt J ^a   Scott, Jenny L ^a,b   Xu, Yaobo ^a   Galler, Martin ^a   Reynard, Louise N ^a   Rowan, Andrew D ^a   Young, David A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

Cartilage; Collagenase; Epigenetic; Transcription

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CALCIMYCIN; COLLAGENASE 3; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LUCIFERASE;

AGED; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CARTILAGE DEGENERATION; CHONDROSARCOMA; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; EPIGENETICS; FEMALE; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; OSTEOARTHRITIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METHYLATION; SARCOMA CELL;

AZACITIDINE; BASE SEQUENCE; CALCIUM; CHONDROCYTES; CPG ISLANDS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA PRIMERS; ENZYME INHIBITORS; HUMANS; MATRIX METALLOPROTEINASE 13; OSTEOARTHRITIS; PROMOTER REGIONS, GENETIC; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 84863189550     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-206367     Document Type: Article

References (54)

1. Goldring, M. B., and Goldring, S. R. (2007) Osteoarthritis. J. Cell. Physiol. 213, 626-634 (Pubitemid 350058254)
2. Visse, R., and Nagase, H. (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827-839 (Pubitemid 36542523)
3. Stickens, D., Behonick, D. J., Ortega, N., Heyer, B., Hartenstein, B., Yu, Y., Fosang, A. J., Schorpp-Kistner, M., Angel, P., and Werb, Z. (2004) Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development. 131, 5883-5895 (Pubitemid 40123905)
4. Vincenti, M. P., and Brinckerhoff, C. E. (2002) Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res. 4, 157-164 (Pubitemid 34460754)
5. Knauper, V., Lopez-Otin, C., Smith, B., Knight, G., and Murphy, G. (1996) Biochemical characterization of human collagenase- 3. J. Biol. Chem. 271, 1544-1550
6. Kevorkian, L., Young, D. A., Darrah, C., Donell, S. T., Shepstone, L., Porter, S., Brockbank, S. M., Edwards, D. R., Parker, A. E., and Clark, I. M. (2004) Expression profiling of metalloproteinases and their inhibitors in cartilage. Arthritis Rheum. 50, 131-141 (Pubitemid 38084297)
7. Little, C. B., Barai, A., Burkhardt, D., Smith, S. M., Fosang, A. J., Werb, Z., Shah, M., and Thompson, E. W. (2009) Matrix metalloproteinase 13-deficient mice are resistant to osteoarthritic cartilage erosion but not chondrocyte hypertrophy or osteophyte development. Arthritis Rheum. 60, 3723-3733
8. Murphy, G., and Nagase, H. (2008) Reappraising metalloproteinases in rheumatoid arthritis and osteoarthritis: destruction or repair? Nat. Clin. Practi. 4, 128-135 (Pubitemid 351338627)
9. Ooi, S. K., and Bestor, T. H. (2008) The colorful history of active DNA demethylation. Cell 133, 1145-1148 (Pubitemid 351852922)
10. Miranda, T. B., and Jones, P. A. (2007) DNA methylation: the nuts and bolts of repression. J. Cell. Physiol. 213, 384-390 (Pubitemid 47509717)
11. Portela, A., and Esteller, M. (2010) Epigenetic modifications and human disease. Nat. Biotechnol. 28, 1057-1068
12. Irizarry, R. A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., Ji, H., Potash, J. B., Sabunciyan, S., and Feinberg, A. P. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 41, 178-186
13. Tate, P. H., and Bird, A. P. (1993) Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev. 3, 226-231 (Pubitemid 23108662)
14. Roach, H. I., Yamada, N., Cheung, K. S., Tilley, S., Clarke, N. M., Oreffo, R. O., Kokubun, S., and Bronner, F. (2005) Association between the abnormal expression of matrix-degrading enzymes by human osteoarthritic chondrocytes and demethylation of specific CpG sites in the promoter regions. Arthritis Rheum. 52, 3110-3124 (Pubitemid 41447092)
15. Reynard, L. N., Bui, C., Canty-Laird, E. G., Young, D. A., and Loughlin, J. (2011) Expression of the osteoarthritis-associated gene GDF5 is modulated epigenetically by DNA methylation. Hum. Mol. Genet. 20, 3450-3460
16. Iliopoulos, D., Malizos, K. N., and Tsezou, A. (2007) Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention. Ann. Rheum. Dis. 66, 1616-1621 (Pubitemid 350205450)
17. Hashimoto, K., Oreffo, R. O., Gibson, M. B., Goldring, M. B., and Roach, H. I. (2009) DNA demethylation at specific CpG sites in the IL1B promoter in response to inflammatory cytokines in human articular chondrocytes. Arthritis Rheum. 60, 3303-3313
18. Nile, C. J., Read, R. C., Akil, M., Duff, G. W., and Wilson, A. G. (2008) Methylation status of a single CpG site in the IL6 promoter is related to IL6 messenger RNA levels and rheumatoid arthritis. Arthritis Rheum. 58, 2686-2693
19. Takami, N., Osawa, K., Miura, Y., Komai, K., Taniguchi, M., Shiraishi, M., Sato, K., Iguchi, T., Shiozawa, K., Hashiramoto, A., and Shiozawa, S. (2006) Hypermethylated promoter region of DR3, the death receptor 3 gene, in rheumatoid arthritis synovial cells. Arthritis Rheum. 54, 779-787
20. Rowan, A. D., Koshy, P. J., Shingleton, W. D., Degnan, B. A., Heath, J. K., Vernallis, A. B., Spaull, J. R., Life, P. F., Hudson, K., and Cawston, T. E. (2001) Synergistic effects of glycoprotein 130 binding cytokines in combination with interleukin-1 on cartilage collagen breakdown. Arthritis Rheum. 44, 1620-1632 (Pubitemid 32642224)
21. Young, D. A., Lakey, R. L., Pennington, C. J., Jones, D., Kevorkian, L., Edwards, D. R., Cawston, T. E., and Clark, I. M. (2005) Histone deacetylase inhibitors modulate metalloprotei- nase gene expression in chondrocytes and block cartilage resorption. Arthritis Res. Ther. 7, R503-512
22. Zhang, Q., Hui, W., Litherland, G. J., Barter, M. J., Davidson, R., Darrah, C., Donell, S. T., Clark, I. M., Cawston, T. E., Robinson, J. H., Rowan, A. D., and Young, D. A. (2008) Differential Toll-like receptor-dependent collagenase expression in chondrocytes. Ann. Rheum. Dis. 67, 1633-1641
23. Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J., and Zhang, J. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80
24. Hansen, K. D., Irizarry, R. A., and Wu, Z. (2012) Removing technical variability in RNA-seq data using conditional quantile normalization. Biostatistics 13, 204-216
25. Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140
26. Bock, C., Reither, S., Mikeska, T., Paulsen, M., Walter, J., and Lengauer, T. (2005) BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 21, 4067-4068 (Pubitemid 41631851)
27. McKay, J. A., Waltham, K. J., Williams, E. A., and Mathers, J. C. (2011) Folate depletion during pregnancy and lactation reduces genomic DNA methylation in murine adult offspring. Genes Nutr. 6, 189-196
28. Klug, M., and Rehli, M. (2006) Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 1, 127-130
29. Litherland, G. J., Dixon, C., Lakey, R. L., Robson, T., Jones, D., Young, D. A., Cawston, T. E., and Rowan, A. D. (2008) Synergistic collagenase expression and cartilage collagenolysis are phosphatidylinositol 3-kinase/Akt signaling-dependent. J. Biol. Chem. 283, 14221-14229
30. Young, D. A., Phillips, B. W., Lundy, C., Nuttall, R. K., Hogan, A., Schultz, G. A., Leco, K. J., Clark, I. M., and Edwards, D. R. (2002) Identification of an initiator-like element essential for the expression of the tissue inhibitor of metalloproteinases-4 (Timp-4) gene. Biochem. J. 364, 89-99 (Pubitemid 34538950)
31. Yano, S., Ghosh, P., Kusaba, H., Buchholz, M., and Longo, D. L. (2003) Effect of promoter methylation on the regulation of IFN-gamma gene during in vitro differentiation of human peripheral blood T cells into a Th2 population. J. Immunol. 171, 2510-2516 (Pubitemid 37025560)
32. Chrivia, J. C., Kwok, R. P., Lamb, N., Hagiwara, M., Montminy, M. R., and Goodman, R. H. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-859 (Pubitemid 23341031)
33. Kasper, L. H., Lerach, S., Wang, J., Wu, S., Jeevan, T., and Brindle, P. K. (2010) CBP/p300 double null cells reveal effect of coactivator level and diversity on CREB transactivation. EMBO J. 29, 3660-3672
34. Sheng, M., McFadden, G., and Greenberg, M. E. (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4, 571-582 (Pubitemid 20160846)
35. Billinghurst, R. C., Dahlberg, L., Ionescu, M., Reiner, A., Bourne, R., Rorabeck, C., Mitchell, P., Hambor, J., Diekmann, O., Tschesche, H., Chen, J., Van Wart, H., and Poole, A. R. (1997) Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. J. Clin. Invest. 99, 1534-1545 (Pubitemid 27163804)
36. Imagawa, K., de Andres, M. C., Hashimoto, K., Pitt, D., Itoi, E., Goldring, M. B., Roach, H. I., and Oreffo, R. O. (2011) The epigenetic effect of glucosamine and a nuclear factor-kappa B (NF-kB) inhibitor on primary human chondrocytes-implications for osteoarthritis. Biochem. Biophys. Res. Commun. 405, 362-367
37. Mancini, D. N., Rodenhiser, D. I., Ainsworth, P. J., O'Malley, F. P., Singh, S. M., Xing, W., and Archer, T. K. (1998) CpG methylation within the 5′ regulatory region of the BRCA1 gene is tumor specific and includes a putative CREB binding site. Oncogene 16, 1161-1169 (Pubitemid 28127515)
38. Boileau, C., Martel-Pelletier, J., Brunet, J., Tardif, G., Schrier, D., Flory, C., El-Kattan, A., Boily, M., and Pelletier, J. P. (2005) Oral treatment with PD-0200347, an alpha2delta ligand, reduces the development of experimental osteoarthritis by inhibiting metalloproteinases and inducible nitric oxide synthase gene expression and synthesis in cartilage chondrocytes. Arthritis Rheum. 52, 488-500 (Pubitemid 40216313)
39. Tsuda, M., Takahashi, S., Takahashi, Y., and Asahara, H. (2003) Transcriptional co-activators CREB-binding protein and p300 regulate chondrocyte-specific gene expression via association with Sox9. J. Biol. Chem. 278, 27224-27229 (Pubitemid 36876879)
40. Chan, H. M., and La Thangue, N. B. (2001) p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell Sci. 114, 2363-2373 (Pubitemid 32684792)
41. Long, F., Schipani, E., Asahara, H., Kronenberg, H., and Montminy, M. (2001) The CREB family of activators is required for endochondral bone development. Development 128, 541-550 (Pubitemid 32229596)
42. Inada, M., Wang, Y., Byrne, M. H., Rahman, M. U., Miyaura, C., Lopez-Otin, C., and Krane, S. M. (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc. Natl. Acad. Sci. U. S. A. 101, 17192-17197 (Pubitemid 39627796)
43. Li, Y., Ahrens, M. J., Wu, A., Liu, J., and Dudley, A. T. (2011) Calcium/calmodulin-dependent protein kinase II activity regulates the proliferative potential of growth plate chondrocytes. Development 138, 359-370
44. Dreier, R. (2010) Hypertrophic differentiation of chondrocytes in osteoarthritis: the developmental aspect of degenerative joint disorders. Arthritis Res. Ther. 12, 216
45. 2+/calmodulin-dependent protein kinases type I, II, and IV. J. Biol. Chem. 271, 3066-3073
46. Takeda, H., Kitaoka, Y., Hayashi, Y., Kumai, T., Munemasa, Y., Fujino, H., Kobayashi, S., and Ueno, S. (2007) Calcium/calmodulin-dependent protein kinase II regulates the phosphorylation of CREB in NMDA-induced retinal neurotoxicity. Brain Res. 1184, 306-315 (Pubitemid 350160572)
47. Wu, X., and McMurray, C. T. (2001) Calmodulin kinase II attenuation of gene transcription by preventing cAMP response element-binding protein (CREB) dimerization and binding of the CREB-binding protein. J. Biol. Chem. 276, 1735-1741 (Pubitemid 32109644)
48. Schmucker, A. C., Wright, J. B., Cole, M. D., and Brinckerhoff, C. E. (2012) Distal interleukin-1beta (IL-1beta) response element of human matrix metalloproteinase-13 (MMP-13) binds activator protein 1 (AP-1) transcription factors and regulates gene expression. J. Biol. Chem. 287, 1189-1197
49. Ramage, L., Nuki, G., and Salter, D. M. (2009) Signalling cascades in mechanotransduction: cell-matrix interactions and mechanical loading. Scand. J. Med. Sci. Sports 19, 457-469
50. Whitmarsh, A. J., and Davis, R. J. (1996) Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J. Mol. Med. (Berl.) 74, 589-607 (Pubitemid 26343761)
51. Sato, K., Suematsu, A., Nakashima, T., Takemoto-Kimura, S., Aoki, K., Morishita, Y., Asahara, H., Ohya, K., Yamaguchi, A., Takai, T., Kodama, T., Chatila, T. A., Bito, H., and Takayanagi, H. (2006) Regulation of osteoclast differentiation and function by the CaMK-CREB pathway. Nat. Med. 12, 1410-1416 (Pubitemid 44924500)
52. Matsuo, N., Tanaka, S., Gordon, M. K., Koch, M., Yoshioka, H., and Ramirez, F. (2006) CREB-AP1 protein complexes regulate transcription of the collagen XXIV gene (Col24a1) in osteoblasts. J. Biol. Chem. 281, 5445-5452 (Pubitemid 43847639)
53. Rowan, A. D., and Young, D. A. (2007) Collagenase gene regulation by pro-inflammatory cytokines in cartilage. Front. Biosci. 12, 536-550 (Pubitemid 46852804)
54. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M., and Haussler, D. (2002) The human genome browser at UCSC. Genome Res. 12, 996-1006 (Pubitemid 34662293)