Variations of SOST mRNA expression in human bone are associated with DNA polymorphism and DNA methylation in the SOST gene

Bone

Volumn 92, Issue , 2016, Pages 107-115

  Lhaneche, Leila ^a,b   Hald, Jannie D ^c   Domingues, Aline ^a,b   Hannouche, Didier ^a   Delepine, Marc ^d   Zelenika, Diana ^d   Boland, Anne ^d   Ostertag, Agnes ^a,b   Cohen Solal, Martine ^a,b,e   Langdahl, Bente L ^c   Harsløf, Torben ^c   de Vernejoul, Marie Christine ^a,b,e   Geoffroy, Valérie ^a,b   Jehan, Frédéric ^a,b  

^a HÔPITAL LARIBOISIÈRE   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

^d CENTRE NATIONAL DE GÉNOTYPAGE   (France)

^e SAINT LOUIS HOSPITAL   (France)

Author keywords

Bone; DNA methylation; Gene expression; Osteogenesis imperfecta; Polymorphism; SOST

Indexed keywords

ADENINE; DNA; GUANINE; MESSENGER RNA; SCLEROSTIN; BONE MORPHOGENETIC PROTEIN; SOST PROTEIN, HUMAN;

ADULT; AGED; ALLELE; ARTICLE; BONE; BONE DENSITY; BONE FRAGILITY; BONE STRENGTH; CONTROLLED STUDY; CPG ISLAND; DISEASE SEVERITY; DNA METHYLATION; DNA MODIFICATION; DNA POLYMORPHISM; EXON; FEMALE; FRACTURE; GENE EXPRESSION; GENETIC VARIATION; HUMAN; HUMAN TISSUE; OSTEOGENESIS IMPERFECTA; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; SOST GENE; ADOLESCENT; BIOSYNTHESIS; COHORT ANALYSIS; GENETIC MARKER; GENETIC POLYMORPHISM; GENETICS; MALE; METABOLISM; MIDDLE AGED; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BONE DENSITY; BONE MORPHOGENETIC PROTEINS; COHORT STUDIES; DNA METHYLATION; FEMALE; FRACTURES, BONE; GENE EXPRESSION; GENETIC MARKERS; GENETIC VARIATION; HUMANS; MALE; MIDDLE AGED; OSTEOGENESIS IMPERFECTA; POLYMORPHISM, GENETIC; RNA, MESSENGER; YOUNG ADULT;

EID: 84983688773     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2016.08.004     Document Type: Article

References (61)

1. [1] Balemans, W., Ebeling, M., Patel, N., Van Hul, E., Olson, P., Dioszegi, M., Lacza, C., Wuyts, W., Van Den Ende, J., Willems, P., et al. Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum. Mol. Genet. 10 (2001), 537–543.
2. [2] Balemans, W., Patel, N., Ebeling, M., Van Hul, E., Wuyts, W., Lacza, C., Dioszegi, M., Dikkers, F.G., Hildering, P., Willems, P.J., et al. Identification of a 52 kb deletion downstream of the SOST gene in patients with van Buchem disease. J. Med. Genet. 39 (2002), 91–97.
3. [3] Ball, M.P., Li, J.B., Gao, Y., Lee, J.H., LeProust, E.M., Park, I.H., Xie, B., Daley, G.Q., Church, G.M., Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat. Biotechnol. 27 (2009), 361–368.
4. [4] Brunkow, M.E., Gardner, J.C., Van Ness, J., Paeper, B.W., Kovacevich, B.R., Proll, S., Skonier, J.E., Zhao, L., Sabo, P.J., Fu, Y., et al. Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am. J. Hum. Genet. 68 (2001), 577–589.
5. [5] Collette, N.M., Genetos, D.C., Economides, A.N., Xie, L., Shahnazari, M., Yao, W., Lane, N.E., Harland, R.M., Loots, G.G., Targeted deletion of Sost distal enhancer increases bone formation and bone mass. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 14092–14097.
6. [6] Dahl, H.J., Folkestad, L., Harsløf, T., Lund, A.M., Dunø, M., Beck Jensen, J.-E., Nhegebat, S., Brixen, K., Langdahl, B., Skeletal phenotype and genotype correlations in adult patients with osteogenesis imperfect. ECTS-IBMS Bonekeys, 12, 2015, P422.
7. [7] Dallas, S.L., Prideaux, M., Bonewald, L.F., The osteocyte: an endocrine cell. and more. Endocr. Rev. 34 (2013), 658–690.
8. [8] Deaton, A.M., Bird, A., CpG islands and the regulation of transcription. Genes Dev. 25 (2011), 1010–1022.
9. [9] Delgado-Calle, J., Sañudo, C., Bolado, A., Fernández, A.F., Arozamena, J., Pascual-Carra, M.A., Rodriguez-Rey, J.C., Fraga, M.F., Bonewald, L., Riancho, J.A., DNA methylation contributes to the regulation of sclerostin expression in human osteocytes. J. Bone Miner. Res. 27 (2012), 926–937.
10. [10] Estrada, K., Styrkarsdottir, U., Evangelou, E., Hsu, Y.H., Duncan, E.L., Ntzani, E.E., Oei, L., Albagha, O.M., Amin, N., Kemp, J.P., et al. Genome-wide meta-analysis identifies 56 bone mineral density loci and reveals 14 loci associated with risk of fracture. Nat. Genet. 44 (2012), 491–501.
11. [11] Forlino, A., Marini, J.C., Osteogenesis imperfecta. Lancet, 2015 pii: S0140-6736(15)00728-X.
12. [12] Grafe, I., Alexander, S., Yang, T., Lietman, C., Homan, E.P., Munivez, E., Chen, Y., Jiang, M.M., Bertin, T., Dawson, B., Asuncion, F., Ke, H.Z., Ominsky, M.S., Lee, B., Sclerostin antibody treatment improves the bone phenotype of Crtap(−/−) mice, a model of recessive osteogenesis imperfecta. J Bone Miner Res 31:5 (2016), 1030–1040.
13. [13] Gualeni, B., de Vernejoul, M.C., Marty-Morieux, C., De Leonardis, F., Franchi, M., Monti, L., Forlino, A., Houillier, P., Rossi, A., Geoffroy, V., Alteration of proteoglycan sulfation affects bone growth and remodeling. Bone 54 (2013), 83–91.
14. [14] Hartikka, H., Kuurila, K., Korkko, J., Kaitila, I., Grenman, R., Pynnonen, S., Hyland, J.C., Ala-Kokko, L., Lack of correlation between the type of COL1A1 or COL1A2 mutation and hearing loss in osteogenesis imperfecta patients. Hum. Mutat. 24 (2004), 147–154.
15. [15] Jacobsen, C.M., Barber, L.A., Ayturk, U.M., Roberts, H.J., Deal, L.E., Schwartz, M.A., Weis, M., Eyre, D., Zurakowski, D., Robling, A.G., Warman, M.L., Targeting the LRP5 pathway improves bone properties in a mouse model of osteogenesis imperfecta. J. Bone Miner. Res. 29 (2014), 2297–2306.
16. [16] Jjingo, D., Conley, A.B., Yi, S.V., Lunyak, V.V., Jordan, I.K., On the presence and role of human gene-body DNA methylation. Oncotarget 3 (2012), 462–474.
17. [17] Jones, P.A., Functions of DNA methylation: Islands, start sites, gene bodies and beyond. Nat Rev Genet 13 (2012), 484–492.
18. [18] Kramer, I., Halleux, C., Keller, H., Pegurri, M., Gooi, J.H., Weber, P.B., Feng, J.Q., Bonewald, L.F., Kneissel, M., Osteocyte Wnt/beta-catenin signaling is required for normal bone homeostasis. Mol. Cell. Biol. 30 (2010), 3071–3085.
19. [19] Kulis, M., Queirós, A.C., Beekman, R., Martín-Subero, J.I., Intragenic DNA methylation in transcriptional regulation, normal differentiation and cancer. Biochim. Biophys. Acta 1829 (2013), 1161–1174.
20. [20] Laurent, L., Wong, E., Li, G., Huynh, T., Tsirigos, A., Ong, C.T., Low, H.M., Kin Sung, K.W., Rigoutsos, I., Loring, J., et al. Dynamic changes in the human methylome during differentiation. Genome Res. 20 (2010), 320–331.
21. [21] Li, L.C., Dahiya, R., MethPrimer: designing primers for methylation PCRs. Bioinformatics 18 (2002), 1427–1431.
22. [22] Li, X., Zhang, Y., Kang, H., Liu, W., Liu, P., Zhang, J., Harris, S.E., Wu, D., Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J. Biol. Chem. 280 (2005), 19883–19887.
23. [23] Mardia, K.V., Kent, J.T., Bibby, J., Multivariate Analysis London. 1979, Academic Press.
24. [24] McClung, M.R., Grauer, A., Boonen, S., Bolognese, M.A., Brown, J.P., Diez-Perez, A., Langdahl, B.L., Reginster, J.Y., Zanchetta, J.R., Wasserman, S.M., Katz, L., Maddox, J., Yang, Y.C., Libanati, C., Bone, H.G., Romosozumab in postmenopausal women with low bone mineral density. N. Engl. J. Med. 370 (2014), 412–420.
25. [26] Minisola, S., Piccioni, A.L., Rosso, R., Romagnoli, E., Pacitti, M.T., Scarnecchia, L., Mazzuoli, G., Reduced serum levels of carboxy-terminal propeptide of human type I procollagen in a family with type I-A osteogenesis imperfecta. Metabolism 43 (1994), 1261–1265.
26. [27] Nadeau, J.H., Modifier genes in mice and humans. Nat Rev Genet 2 (2001), 165–174.
27. [28] Padhi, D., Allison, M., Kivitz, A.J., Gutierrez, M.J., Stouch, B., Wang, C., Jang, G., Multiple doses of sclerostin antibody romosozumab in healthy men and postmenopausal women with low bone mass: a randomized, double-blind, placebo-controlled study. J. Clin. Pharmacol. 54 (2014), 168–178.
28. [29] Piters, E., Culha, C., Moester, M., Van Bezooijen, R., Adriaensen, D., Mueller, T., Weidauer, S., Jennes, K., de Freitas, F., Löwik, C., et al. First missense mutation in the SOST gene causing sclerosteosis by loss of sclerostin function. Hum. Mutat. 31 (2010), E1526–E1543.
29. [30] Pollitt, R., McMahon, R., Nunn, J., Bamford, R., Afifi, A., Bishop, N., Dalton, A., Mutation analysis of COL1A1 and COL1A2 in patients diagnosed with osteogenesis imperfecta type I-IV. Hum. Mutat., 27, 2006, 716.
30. [31] R Development Core Team, R Foundation for Statistical Computing, Vienna, Austria. 2010, 2010.
31. [32] Rauch, F., Travers, R., Plotkin, H., Glorieux, F.H., The effects of intravenous pamidronate on the bone tissue of children and adolescents with osteogenesis imperfecta. J. Clin. Invest. 110 (2002), 1293–1299.
32. [33] Rauch, F., Cornibert, S., Cheung, M., Glorieux, F.H., Long-bone changes after pamidronate discontinuation in children and adolescents with osteogenesis imperfecta. Bone 40 (2007), 821–827.
33. [34] Reppe, S., Noer, A., Grimholt, R.M., Halldórsson, B.V., Medina-Gomez, C., Gautvik, V.T., Olstad, O.K., Berg, J.P., Datta, H., Estrada, K., Hofman, A., Uitterlinden, A.G., Rivadeneira, F., Lyle, R., Collas, P., Gautvik, K.M., Methylation of bone SOST, its mRNA, and serum sclerostin levels correlate strongly with fracture risk in postmenopausal women. J. Bone Miner. Res. 30 (2015), 249–256.
34. [35] Richards, J.B., Kavvoura, F.K., Rivadeneira, F., Styrkársdóttir, U., Estrada, K., Halldórsson, B.V., Hsu, Y.H., Zillikens, M.C., Wilson, S.G., Mullin, B.H., et al. Collaborative meta-analysis: associations of 150 candidate genes with osteoporosis and osteoporotic fracture. Ann. Intern. Med. 151 (2009), 528–537.
35. [36] Roforth, M.M., Fujita, K., McGregor, U.I., Kirmani, S., McCready, L.K., Peterson, J.M., Drake, M.T., Monroe, D.G., Khosla, S., Effects of age on bone mRNA levels of sclerostin and other genes relevant to bone metabolism in humans. Bone 59 (2014), 1–6.
36. [37] Roschger, A., Roschger, P., Keplingter, P., Klaushofer, K., Abdullah, S., Kneissel, M., Rauch, F., Effect of sclerostin antibody treatment in a mouse model of severe osteogenesis imperfecta. Bone 66 (2014), 182–188.
37. [38] Rowe, D.W., Shapiro, J.R., Poirier, M., Schlesinger, S., Diminished type I collagen synthesis and reduced alpha 1(I) collagen messenger RNA in cultured fibroblasts from patients with dominantly inherited (type I) osteogenesis imperfecta. J. Clin. Invest. 76 (1985), 604–611.
38. [39] Semënov, M., Tamai, K., He, X., SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J. Biol. Chem. 280 (2005), 26770–26775.
39. [40] Sims, A.M., Shephard, N., Carter, K., Doan, T., Dowling, A., Duncan, E.L., Eisman, J., Jones, G., Nicholson, G., Prince, R., et al. Genetic analyses in a sample of individuals with high or low BMD shows association with multiple Wnt pathway genes. J. Bone Miner. Res. 23 (2008), 499–506.
40. [41] Sinder, B.P., Eddy, M.M., Ominsky, M.S., Caird, M.S., Marini, J.C., Kozloff, K.M., Sclerostin antibody improves skeletal parameters in a Brtl/+ mouse model of osteogenesis imperfecta. J. Bone Miner. Res. 28 (2013), 73–80.
41. [42] Singer, M., Kosti, I., Pachter, L., Mandel-Gutfreund, Y., A diverse epigenetic landscape at human exons with implication for expression. Nucleic Acids Res. 43 (2015), 3498–3508.
42. [43] Smith, Z.D., Meissner, A., DNA methylation: roles in mammalian development. Nat Rev Genet 14 (2013), 204–220.
43. [44] Staehling-Hampton, K., Proll, S., Paeper, B.W., Zhao, L., Charmley, P., Brown, A., Gardner, J.C., Galas, D., Schatzman, R.C., Beighton, P., et al. A 52-kb deletion in the SOST-MEOX1 intergenic region on 17q12-q21 is associated with van Buchem disease in the Dutch population. Am. J. Med. Genet. 110 (2002), 144–152.
44. [45] Styrkarsdottir, U., Halldorsson, B.V., Gretarsdottir, S., Gudbjartsson, D.F., Walters, G.B., Ingvarsson, T., Jonsdottir, T., Saemundsdottir, J., Snorradóttir, S., Center, J.R., et al. New sequence variants associated with bone mineral density. Nat. Genet. 41 (2009), 15–17.
45. [46] Titeux, M., Pendaries, V., Tonasso, L., Decha, A., Bodemer, C., Hovnanian, A., A frequent functional SNP in the MMP1 promoter is associated with higher disease severity in recessive dystrophic epidermolysis bullosa. Hum. Mutat. 29 (2008), 267–276.
46. [47] Trummer, T., Brenner, R., Just, W., Vogel, W., Kennerknecht, I., Recurrent mutations in the COL1A2 gene in patients with osteogenesis imperfecta. Clin. Genet. 59 (2001), 338–343.
47. [48] Uitterlinden, A.G., Arp, P.P., Paeper, B.W., Charmley, P., Proll, S., Rivadeneira, F., Fang, Y., van Meurs, J.B., Britschgi, T.B., Latham, J.A., et al. Polymorphisms in the sclerosteosis/van Buchem disease gene (SOST) region are associated with bone-mineral density in elderly whites. Am. J. Hum. Genet. 75 (2004), 1032–1045.
48. [49] Valero, C., Zarrabeitia, M.T., Hernández, J.L., Pineda, B., Cano, A., García-Pérez, M.A., Riancho, J.A., Relationship of sclerostin and secreted frizzled protein polymorphisms with bone mineral density: an association study with replication in postmenopausal women. Menopause 18 (2011), 802–807.
49. [50] van Bezooijen, R.L., ten Dijke, P., Papapoulos, S.E., Löwik, C.W., SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev. 16 (2005), 319–327.
50. [51] Van Hul, W., Identification of genetic modifiers of monogenic (bone) diseases: new tools available, but with limitations. J. Bone Miner. Res. 26 (2011), 918–919.
51. [52] van Lierop, A.H., Hamdy, N.A., van Egmond, M.E., Bakker, E., Dikkers, F.G., Papapoulos, S.E., Van Buchem disease: clinical, biochemical, and densitometric features of patients and disease carriers. J. Bone Miner. Res. 28 (2013), 848–854.
52. [53] Venables, W.N., Ripley, B.D., Modern Applied Statistics with S. 2002, Springer-Verlag.
53. [54] Venturi, G., Tedeschi, E., Mottes, M., Valli, M., Camilot, M., Viglio, S., Antoniazzi, F., Tato, L., Osteogenesis imperfecta: clinical, biochemical and molecular findings. Clin. Genet. 70 (2006), 131–139.
54. [55] Weatherall, D.J., Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat Rev Genet 2 (2001), 245–255.
55. [56] Whyte, M.P., Totty, W.G., Novack, D.V., Zhang, X., Wenkert, D., Mumm, S., Camurati-Engelmann disease: unique variant featuring a novel mutation in TGFbeta1 encoding transforming growth factor beta 1 and a missense change in TNFSF11 encoding RANK ligand. J. Bone Miner. Res. 26 (2011), 920–933.
56. [57] Willing, M.C., Cohn, D.H., Byers, P.H., Frameshift mutation near the 3′ end of the COL1A1 gene of type I collagen predicts an elongated Pro alpha 1(I) chain and results in osteogenesis imperfecta type I. J. Clin. Invest. 85 (1990), 282–290.
57. [58] Winkler, D.G., Sutherland, M.K., Geoghegan, J.C., Yu, C., Hayes, T., Skonier, J.E., Shpektor, D., Jonas, M., Kovacevich, B.R., Staehling-Hampton, K., et al. Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J. 22 (2003), 6267–6276.
58. [59] Wright, F.A., Strug, L.J., Doshi, V.K., Commander, C.W., Blackman, S.M., Sun, L., Berthiaume, Y., Cutler, D., Cojocaru, A., Collaco, J.M., et al. Genome-wide association and linkage identify modifier loci of lung disease severity in cystic fibrosis at 11p13 and 20q13.2. Nat. Genet. 43 (2011), 539–546.
59. [60] Yerges, L.M., Klei, L., Cauley, J.A., Roeder, K., Kammerer, C.M., Moffett, S.P., Ensrud, K.E., Nestlerode, C.S., Marshall, L.M., Hoffman, A.R., et al. High-density association study of 383 candidate genes for volumetric BMD at the femoral neck and lumbar spine among older men. J. Bone Miner. Res. 24 (2009), 2039–2049.
60. [61] Harper, A.R., Nayee, S., Topol, E.J., Protective alleles and modifier variants in human health and disease. Nat Rev Genet. 16:12 (2015), 689–701.
61. [62] Hald, J.D., Folkestad, L., Harsløf, L., Lund, A.M., Duno, M., Jensen, J.B., Neghabat, S., Brixen, K., Langdahl, B., Skeletal phenotypes in adult patients with osteogenesis imperfecta-correlations with COL1A1/COL1A2 genotype and collagen structure. Osteoporos Int., 2016 [Epub ahead of print].