CpG methylation regulates allelic expression of GDF5 by modulating binding of SP1 and SP3 repressor proteins to the osteoarthritis susceptibility SNP rs143383

Human Genetics

Volumn 133, Issue 8, 2014, Pages 1059-1073

  Reynard, Louise N ^a   Bui, Catherine ^a,b   Syddall, Catherine M ^a   Loughlin, John ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELES; CARTILAGE, ARTICULAR; CASE-CONTROL STUDIES; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENETIC PREDISPOSITION TO DISEASE; GROWTH DIFFERENTIATION FACTOR 5; HUMANS; OSTEOARTHRITIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR;

EID: 84904419387     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-014-1447-z     Document Type: Article

References (56)

1. Aoyama T, Okamoto T, Nagayama S, Nishijo K, Ishibe T et al (2004) Methylation in the core promoter region of the chondromodulin-I gene determines the cell-specific expression by regulating the binding of transcriptional activator SP3. J Biol Chem 279(27):28789-28797 (Pubitemid 38900164)
2. Barter MJ, Young DA (2013) Epigenetic mechanism and non-coding RNA s in osteoarthritis. Curr Rheumatol Rep 15(9):353
3. Bell JT, Pai A, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF et al (2011) DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 12(1):R10
4. Bui C, Barter MJ, Scott JL, Xu Y, Galler M, Reynard LN, Rowan AD, Young DA (2012) 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 J 26(7):3000-3011
5. Chapman K, Takahashi A, Meulenbelt I, Watson C, Rodriguez-Lopez J, Egli R, Tsezou A, Malizos KN, Kloppenburg M, Shi D et al (2008) A meta-analysis of European and Asian cohorts reveals a global role of a functional SNP in the 5′ UTR of GDF5 with osteoarthritis susceptibility. Hum Mol Genet 17:1497-1504 (Pubitemid 351627345)
6. Cheng X, Yang T, Meng W, Liu H, Zhang T, Shi R (2012) Overexpression of GDF5 through an adenovirus vector stimulates osteogenesis of human mesenchymal stem cells in vitro and in vivo. Cells Tissues Organs 196:56-67
7. Chujo T, An HS, Akeda K, Miyamoto K, Muehleman C, Attawia M, Andersson G, Masuda K (2006) Effects of growth differentiation factor-5 on the intervertebral disc - in vitro bovine study and in vivo rabbit disc degeneration model study. Spine 31(25):2909-2917 (Pubitemid 44885707)
8. Coleman CM, Scheremeta BH, Boyce AT, Mauck RL, Tuan RS (2011) Delayed fracture healing in growth differentiation factor 5-deficient mice: a pilot study. Clin Orthop Relat Res 469(10):2915-2924
9. Coleman CM, Vaughan E, Browe DC, Mooney E, Howard L, Barry F (2013) Growth differentiation factor-5 enhances in vitro mesenchymal stromal cell chondrogenesis and hypertrophy. Stem Cells Dev 22(13):1968-1976
10. Daans M, Luyten FP, Lories RJ (2011) GDF5 deficiency in mice is associated with instability-driven joint damage, gait and subchondral bone changes. Ann Rheum Dis 70:208-213
11. Dawson K, Seeman P, Sebald E, King L, Edwards M, Williams J 3rd, Mundlos S, Krakow D (2006) GDF5 is a second locus for multiple-synostosis syndrome. Am J Hum Genet 78(4):708-712
12. Dempster EL, Pidsley R, Schalkwyk LC, Owens S, Geogiades A, Kane F, Kalidindi S et al (2011) Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum Mol Genet 20(24):4788-4796
13. Egli R, Southam L, Wilkins JM, Lorenzen I, Pombo-Suarez M et al (2009) Functional analysis of the GDF5 regulatory polymorphism that is associated with OA susceptibility. Arthritis Rheum 60:2055-2064
14. Evangelou E, Chapman K, Meulenbelt I, Karassa FB, Loughlin J, Carr A, Doherty M, Doherty S et al (2009) Large-scale analysis of association between GDF5 and FRZB variants and osteoarthritis of the hip, knee and hand. Arthritis Rheum 60(6):1710-1721
15. Gelse K, Ekici AB, Cipa F, Swoboda B, Carl HD, Olk A, Hennig FF, Klinger P (2012) Molecular differentiation between osteophytic and articular cartilage-clues for a transient and permanent chondrocyte phenotype. Osteoarthr Cartil 20(2):162-171
16. Gervin K, Vigeland MD, Mattingsdal M, Hammero M, Nygard H, Olsen AO et al (2012) DNA methylation and gene expression changes in monozygotic twins discordant for psoriasis: identification of epigenetically dysregulated genes. PLoS Genet 8(1):e1002454
17. Gibbs JR, van der Brug MP, Hernandez DG, Traynor BJ, Nalls MA, Lai SL, Arepalli S et al (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in the human brain. PLoS Genet 6(5):e1000952
18. Harada M, Takahara M, Zhe P, Otsuji M, Iuchi Y, Takagi M, Ogino T (2007) Osteoarthr Cartil 15(4):468-474
19. Hashimoto K, Oreffo RO, Gibson MB, Goldring MB, Roach HI (2009) DNA demethylation at specific CpG sites in the IL1B promoter in response t inflammatory cytokines in human articular chondrocytes. Arthritis Rheum 60(11):3303-3313
20. Höller M, Westin G, Jiricny J, Schaffner W (1988) Sp1 transcription factor binds DNA and activates transcription even when the binding site is CpG methylated. Genes Dev 2(9):1127-1135
21. Honda H, Pazin MJ, Wernyj RP, Morin PJ (2006) Crucial roles of Sp1 and epigenetic modifications in the regulation of the CLDN4 promoter in ovarian cancer cells. J Biol Chem 281(30):21433-21444 (Pubitemid 44115482)
22. Houard X, Goldring MB, Berenbaum F (2013) Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis. Curr Rheumatol Rep 15(11):375
23. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13(7):484-492
24. Kim KI, Park PS, Im GI (2013) Changes in the epigenetic status of the SOX-9 promoter in human osteoarthritic cartilage. J Bone Miner Res 28(5):1050-1060
25. Klug M, Rehli M (2006) Functional analysis of promoter CpG methylation using a CpG-free luciferase reporter vector. Epigenetics 1(3):127-130
26. Lee LT, Tan-Un KC, Pang RT, Lam DT, Chow BK (2004) Regulation of the human secreting gene is controlled by the combined effects of CpG methylation, Sp1/Sp3 ratio, and the E-box element. Mol Endocrinol 18(7):1740-1755 (Pubitemid 38859580)
27. Loeser RF, Goldring SR, Scanzello CR, Goldring MB (2012) Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum 64(6):1697-1707
28. Loughlin J (2005) The genetic epidemiology of human primary osteoarthritis: current status. Expert Rev Mol Med 7(9):1-12
29. Luyten FP (1997) Cartilage-derived morphogenic protein-1. Int J Biochem Cell Biol 29(11):1241-1244
30. Martin-Trujillo A, Iglesias-Platas I, Coto E, Corral-Juan M, San Nicolas H, Corral J et al (2011) Genotype of an individual single nucleotide polymorphism regulates DNA methylation at the TRPC3 alternative promoter. Epigenetics 6(10):1236-1241
31. McGuire T, Wells KB, Bruce ML, Miranda J, Scheffler R, Durham M, Ford DE, Lewis L (2002) Burden of illness. Ment Health Serv Res 4:179-185 (Pubitemid 36032780)
32. Meaburn EL, Schalkwyk LC, Mill J (2010) Allele-specific methylation in the human genome: implications for genetic studies of complex disease. Epigenetics 5:578-582
33. Plöger F, Seeman P, Schmidt-von Kegler M, Lehmann K, Seidel J, Kjaer KW, Pohl J, Mundlos S (2008) Brachydactyly type A2 associated with defect in proGDF5 processing. Hum Mol Genet 17(9):1222-1233 (Pubitemid 351566959)
34. Posthumus M, Collins M, Cook J, Handley CJ, Ribbans WJ et al (2010) Components of the transforming growth factor-b family and the pathogenesis of human Achilles tendon pathology-a genetic association study. Rheumatology (Oxford) 49:2090-2097
35. Rakyan VK, Beyan H, Down TA, Hawa MI, Maslau S, Aden D, Daunay A et al (2011) Identification of type 1 diabetes-associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet 7(9):e1002300
36. Reamon-Buettner SM, Borlak J (2008) Epigenetic silencing of cell adhesion molecule 1 in different cancer progenitor cells of transgenic c-Myc and c-Raf mouse lung tumours. Cancer Res 68(18):7587-7596
37. Reynard LN, Loughlin J (2013) The genetics and functional analysis of primary osteoarthritis susceptibility. Expert Rev Mol Med 18:15
38. Reynard LN, Bui C, Canty-Laird EG, Young DA, Loughlin J (2011) Expression of the osteoarthritis-associated gene GDF5 is modulated epigenetically by DNA methylation. Hum Mol Genet 20:3450-3460
39. Roach HI, Yamada N, Cheung KS, Tilley S, Clarke NM, Oreffo RO, Kokuban S, 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(10):3110-3124 (Pubitemid 41447092)
40. Rouault K, Scotet V, Autret S, Gaucher F, Dubrana F, Tanguy D, El Rassi CY, Fenoll B, Férec C (2010) Evidence of association between GDF5 polymorphisms and congenital dislocation of the hip in a Caucasian population. Osteoarthr Cartil 18(9):1144-1149
41. Schalkwyk LC, Meaburn EL, Smith R, Dempster EL, Jeffries AR, Davies MN et al (2010) Allelic skewing of DNA methylation is widespread across the genome. Am J Hum Genet 86(2):196-212
42. Sesselmann S, Söder S, Voigt R, Haag J, Grogan SP, Aigner T (2009) DNA methylation is not responsible for the p21WAF/CIP1 down-regulation in osteoarthritic chondrocytes. Osteoarthr Cartil 17(4):507-512
43. Southam L, Rodriguez-Lopez J, Wilkins JM, Pombo-Suarez M, Snelling S et al (2007) An SNP in the 5′-UTR of GDF5 is associated with osteoarthritis susceptibility in Europeans and with in vivo differences in allelic expression in articular cartilage. Hum Mol Genet 16:2226-2232 (Pubitemid 47354904)
44. Syddall CM, Reynard LN, Young DA, Loughlin J (2013) The identification of trans-acting factors that regulate the expression of GDF5 via the osteoarthritis susceptibility SNP rs143383. PLoS Genet 9(6):e1003557
45. Szczaluba K, Hilbert K, Obersztyn E, Zabel B, Mazurczak T, Kozlowski K (2005) Du Pan Syndrome phenotype caused by heterozygous pathogenic mutations in CDMP1 gene. Am J Med Genet A 1 138(4):379-383
46. Tan SL, Ahmad RE, Ahmad TS, Merican AM, Abbas A, Ng WM, Kamarul T (2012) Effect of growth differentiation factor 5 on the proliferation and tenogenic differentiation potential of human mesenchymal stem cells in vitro. Cells Tissues Organs 196(4):325-338
47. Tawonsawatruk T, Changthong T, Pingsuthiwong S, Trachoo O, Sura T, Wajanavisit W (2011) A genetic association study between growth differentiation factor 5 (GDF5) polymorphism and knee osteoarthritis in Thai population. J Orthop Surg Res 6:47
48. Tsumaki N, Tanaka K, Arikawa-Hirasawa E, Nakase T, Kimura T, Thomas JT, Ochi T, Luyten FP, Yamada Y (1999) Role of CDMP-1 in skeletal morphogenesis: promotion of mesenchymal recruitment and chondrocyte differentiation. J Cell Biol 144(1):161-173 (Pubitemid 29047019)
49. Tycko B (2010) Allele-specific DNA methylation: beyond imprinting. Hum Mol Genet 19(R2):R210-R220
50. Wang G, Wei LN, Loh HH (2003) Transcriptional regulation of mouse δ-Opioid receptor gene by CpG methylation: involvement of Sp3 ad a methyl-CpG-binding protein, MBD2, in transcriptional repression of mouse δ-Opioid receptor gene in Neuro2A cells. J Biol Chem 278(42):40550-40556 (Pubitemid 37280866)
51. Williams FM, Popham M, Hart DJ, de Schepper E, Bierma-Zeinstra S, Hofman A et al (2011) GDF5 single-nucleotide polymorphism rs143383 is associated with lumbar disc degeneration in Northern European women. Arthritis Rheum 63(3):708-712
52. Won J, Yim J, Kim TK (2002) SP1 and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells. J Biol Chem 277(1):38230-38238 (Pubitemid 35154677)
53. Xu Y, Barter MJ, Swan DC, Rankin KS, Rowan AD, Santibanez-Koref M, Loughlin J, Young DA (2012) Identification of the pathogenic pathways in osteoarthritic hip cartilage: commonality and discord between hip and knee OA. Osteoarthr Cartil 20(9):1029-1038
54. Yip L, Sheng D, Chang P, Atkinson M, Czesak M et al (2009) Deaf1 isoforms control the expression of genes encoding peripheral tissue antigens in the pancreatic lymph nodes during type 1 diabetes. Nat Immunol 10(9):1026-1033
55. Zhang D, Cheng L, Badner JA, Chen C, Chen Q, Luo W, Craig DW et al (2010) Genetic control of individual differences in gene-specific methylation in human brain. Am J Hum Genet 86(3):411-419
56. Zhu WG, Dai Z, Srinivasan K, Duan W, Druhan LJ, Ding H et al (2003) Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip) promoter. Mol Cell Biol 23(12):4056-4065 (Pubitemid 36666412)