Omics analysis of human bone to identify genes and molecular networks regulating skeletal remodeling in health and disease

Bone

Volumn 101, Issue , 2017, Pages 88-95

  Reppe, Sjur ^a,b   Datta, Harish K ^c,d   Gautvik, Kaare M ^b,e  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b LOVISENBERG DIAKONALE HOSPITAL   (Norway)

^c JAMES COOK UNIVERSITY HOSPITAL   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF OSLO   (Norway)

Author keywords

Bone biopsy; Epigenetics; Omics; Osteoarthritis; Osteoporosis; Review; Transcriptomics

Indexed keywords

APOLIPOPROTEIN A1; CARBONATE DEHYDRATASE I; CD14 ANTIGEN; DICKKOPF 1 PROTEIN; FRIZZLED PROTEIN; MICRORNA; MICRORNA 100; MICRORNA 122 5P; MICRORNA 125B; MICRORNA 140 3P; MICRORNA 15A; MICRORNA 198; MICRORNA 21; MICRORNA 21 5P; MICRORNA 23A; MICRORNA 24; MICRORNA 25; MICRORNA 29B; MICRORNA 30C2; MICRORNA 31; MICRORNA 335; MICRORNA 503; MICRORNA 99A; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPROTEGERIN; PARATHYROID HORMONE RECEPTOR 1; PARATHYROID HORMONE RECEPTOR 2; SCLEROSTIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; UNINDEXED DRUG; TRANSCRIPTOME;

BONE BIOPSY; BONE DENSITY; BONE REMODELING; BONE STRESS; BONE TURNOVER; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; FEMUR; FRACTURE; GENE EXPRESSION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENE STRUCTURE; GENETIC TRANSCRIPTION; GENOME-WIDE ASSOCIATION STUDY; HUMAN; ILIAC BONE; METABOLOMICS; NONHUMAN; OSTEOARTHRITIS; OSTEOPOROSIS; PROTEOMICS; QUANTITATIVE TRAIT LOCUS; REVIEW; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW; TIBIA; TRANSCRIPTOMICS; UPREGULATION; BONE; GENETICS; METABOLISM; PHYSIOLOGY; PROCEDURES;

BONE AND BONES; DNA METHYLATION; EPIGENOMICS; GENOME-WIDE ASSOCIATION STUDY; HUMANS; OSTEOARTHRITIS; OSTEOPOROSIS; TRANSCRIPTOME;

EID: 85018445935     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2017.04.012     Document Type: Review

References (64)

1. [1] Bonewald, L.F., Osteocytes as dynamic multifunctional cells. Ann. N. Y. Acad. Sci. 1116 (2007), 281–290.
2. [2] Reppe, S., Refvem, H., Gautvik, V.T., et al. Eight genes are highly associated with BMD variation in postmenopausal Caucasian women. Bone 46:3 (2010), 604–612.
3. [3] Hsu, Y.H., Reppe, S., Chi, C.L., et al. Metabolomics signature and risks of osteoporosis: a systems biology approach by integrating bone tissue-specific metabolomics and transcriptomics in postmenopausal Caucasian women. J. Bone Miner. Res., 28(Suppl. 1), 2013, MO0134.
4. [4] Garmilla-Ezquerra, P., Sanudo, C., Delgado-Calle, J., et al. Analysis of the bone microRNome in osteoporotic fractures. Calcif. Tissue Int. 96:1 (2015), 30–37.
5. [5] De-Ugarte, L., Yoskovitz, G., Balcells, S., et al. MiRNA profiling of whole trabecular bone: identification of osteoporosis-related changes in MiRNAs in human hip bones. BMC Med. Genet., 8, 2015, 75.
6. [6] Seeliger, C., Karpinski, K., Haug, A.T., et al. Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures. J. Bone Miner. Res. 29:8 (2014), 1718–1728.
7. [7] Balla, B., Kosa, J.P., Kiss, J., et al. Different gene expression patterns in the bone tissue of aging postmenopausal osteoporotic and non-osteoporotic women. Calcif. Tissue Int. 82:1 (2008), 12–26.
8. [8] Balla, B., Kosa, J.P., Kiss, J., et al. Transcriptional profiling of immune system-related genes in postmenopausal osteoporotic versus non-osteoporotic human bone tissue. Clin. Immunol. 131:2 (2009), 354–359.
9. [9] Hopwood, B., Tsykin, A., Findlay, D.M., Fazzalari, N.L., Gene expression profile of the bone microenvironment in human fragility fracture bone. Bone 44:1 (2009), 87–101.
10. [10] Chaput, C.D., Dangott, L.J., Rahm, M.D., et al. A proteomic study of protein variation between osteopenic and age-matched control bone tissue. Exp. Biol. Med. 237:5 (2012), 491–498.
11. [11] Delgado-Calle, J., Fernandez, A.F., Sainz, J., et al. Genome-wide profiling of bone reveals differentially methylated regions in osteoporosis and osteoarthritis. Arthritis Rheum. 65:1 (2013), 197–205.
12. [12] Garcia-Ibarbia, C., Delgado-Calle, J., Casafont, I., et al. Contribution of genetic and epigenetic mechanisms to Wnt pathway activity in prevalent skeletal disorders. Gene 532:2 (2013), 165–172.
13. [13] Velasco, J., Zarrabeitia, M.T., Prieto, J.R., et al. Wnt pathway genes in osteoporosis and osteoarthritis: differential expression and genetic association study. Osteoporos. Int. 21:1 (2010), 109–118.
14. [14] Kalogeropoulos, M., Varanasi, S.S., Olstad, O.K., et al. Zic1 transcription factor in bone: neural developmental protein regulates mechanotransduction in osteocytes. FASEB J. 24:8 (2010), 2893–2903.
15. [15] Varanasi, S.S., Olstad, O.K., Swan, D.C., et al. Skeletal site-related variation in human trabecular bone transcriptome and signaling. PLoS One, 5(5), 2010, e10692.
16. [16] Ding, C., Cicuttini, F., Jones, G., Tibial subchondral bone size and knee cartilage defects: relevance to knee osteoarthritis. Osteoarthr. Cartil. 15:5 (2007), 479–486.
17. [17] Chou, C.H., Wu, C.C., Song, I.W., et al. Genome-wide expression profiles of subchondral bone in osteoarthritis. Arthritis Res. Ther., 15(6), 2013, R190.
18. [18] Patsch, J.M., Kohler, T., Berzlanovich, A., et al. Trabecular bone microstructure and local gene expression in iliac crest biopsies of men with idiopathic osteoporosis. J. Bone Miner. Res. 26:7 (2011), 1584–1592.
19. [19] Kuliwaba, J.S., Findlay, D.M., Atkins, G.J., Forwood, M.R., Fazzalari, N.L., Enhanced expression of osteocalcin mRNA in human osteoarthritic trabecular bone of the proximal femur is associated with decreased expression of interleukin-6 and interleukin-11 mRNA. J. Bone Miner. Res. 15:2 (2000), 332–341.
20. [20] Jemtland, R., Holden, M., Reppe, S., et al. Molecular disease map of bone characterizing the postmenopausal osteoporosis phenotype. J. Bone Miner. Res. 26:8 (2011), 1793–1801.
21. [21] Andreassen, O.A., McEvoy, L.K., Thompson, W.K., et al. Identifying common genetic variants in blood pressure due to polygenic pleiotropy with associated phenotypes. Hypertension 63:4 (2014), 819–826.
22. [22] Estrada, K., Styrkarsdottir, U., Evangelou, E., et al. Genome-wide meta-analysis identifies 56 bone mineral density loci and reveals 14 loci associated with risk of fracture. Nat. Genet. 44:5 (2012), 491–501.
23. [23] Medina-Gomez, C., Kemp, J.P., Estrada, K., et al. Meta-analysis of genome-wide scans for total body BMD in children and adults reveals allelic heterogeneity and age-specific effects at the WNT16 locus. PLoS Genet., 8(7), 2012, e1002718.
24. [24] Reppe, S., Hsu, Y.H., Beck, T., et al. Femoral geometry parameters correlate to bone bene expression levels and differ between osteoporotic and healthy postmenopausal women. J. Bone Miner. Res., 31(Suppl. 1), 2016.
25. [25] Reppe, S., Wang, Y., Thompson, W.K., et al. Genetic sharing with cardiovascular disease risk factors and diabetes reveals novel bone mineral density loci. PLoS One, 10(12), 2015, e0144531.
26. [26] Reppe, S., Sachse, D., Olstad, O.K., et al. Identification of transcriptional macromolecular associations in human bone using browser based in silico analysis in a giant correlation matrix. Bone 53:1 (2012), 69–78.
27. [27] Reppe, S., Noer, A., Grimholt, R.M., et al. Methylation of bone SOST, its mRNA, and serum sclerostin levels correlate strongly with fracture risk in postmenopausal women. J. Bone Miner. Res. 30:2 (2015), 249–256.
28. [28] Tharmaratnam, K., Sperrin, M., Jaki, T., Reppe, S., Frigessi, A., Tilting the lasso by knowledge-based post-processing. BMC Bioinf., 17(1), 2016, 344.
29. [29] Nielson, C.M., Liu, C.T., Smith, A.V., et al. Novel genetic variants associated with increased vertebral volumetric BMD, reduced vertebral fracture risk, and increased expression of SLC1A3 and EPHB2. J. Bone Miner. Res. 31:12 (2016), 2085–2097.
30. [30] Capulli, M., Olstad, O.K., Onnerfjord, P., et al. The C-terminal domain of chondroadherin: a new regulator of osteoclast motility counteracting bone loss. J. Bone Miner. Res. 29:8 (2014), 1833–1846.
31. [31] Rossini, M., Gatti, D., Adami, S., Involvement of WNT/beta-catenin signaling in the treatment of osteoporosis. Calcif. Tissue Int. 93:2 (2013), 121–132.
32. [32] Reppe, S., Olstad, O.K., Cockell, S.J., et al. Transcriptome profiling reveals that postmenopausal osteoporosis and bone density correlate with fat metabolism but not adiposity. J. Bone Miner. Res., 28(Suppl. 1), 2013, MO0095.
33. [33] Nissen-Meyer, L.S., Jemtland, R., Gautvik, V.T., et al. Osteopenia, decreased bone formation and impaired osteoblast development in Sox4 heterozygous mice. J. Cell Sci. 120 (2007), 2785–2795.
34. [34] Duncan, E.L., Brown, M.A., Sinsheimer, J., et al. Suggestive linkage of the parathyroid receptor type 1 to osteoporosis. J. Bone Miner. Res. 14:12 (1999), 1993–1999.
35. [35] Ritchie, M.E., Phipson, B., Wu, D., et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43(7), 2015, e47.
36. [36] Reppe, S., Holden, M., Gautvik, V.T., Datta, H., Gautvik, K.M., Postmenopausal BMD variation is strongly associated with subsets of microRNAs and other non-coding RNAs (ncRNAs) expression levels. J. Bone Miner. Res., 25(Suppl. 1), 2010 (Presentation Number: 1036).
37. [37] Reppe, S., Stilgren, L., Abrahamsen, B., et al. Abnormal muscle and hematopoietic gene expression may be important for clinical morbidity in primary hyperparathyroidism. Am. J. Physiol. Endocrinol. Metab. 292:5 (2007), E1465–E1473.
38. [38] Rucci, N., Capulli, M., Olstad, O.K., et al. The alpha2beta1 binding domain of chondroadherin inhibits breast cancer-induced bone metastases and impairs primary tumour growth: a preclinical study. Cancer Lett. 358:1 (2015), 67–75.
39. [39] Farr, J.N., Roforth, M.M., Fujita, K., et al. Effects of age and estrogen on skeletal gene expression in humans as assessed by RNA sequencing. PLoS One, 10(9), 2015, e0138347.
40. [40] Kosa, J.P., Balla, B., Speer, G., et al. Effect of menopause on gene expression pattern in bone tissue of nonosteoporotic women. Menopause 16:2 (2009), 367–377.
41. [41] Lekva, T., Bollerslev, J., Kristo, C., et al. The glucocorticoid-induced leucine zipper gene (GILZ) expression decreases after successful treatment of patients with endogenous Cushing's syndrome and may play a role in glucocorticoid-induced osteoporosis. J. Clin. Endocrinol. Metab. 95:1 (2010), 246–255.
42. [42] Lekva, T., Ueland, T., Boyum, H., et al. TXNIP is highly regulated in bone biopsies from patients with endogenous Cushing's syndrome and related to bone turnover. Eur. J. Endocrinol. 166:6 (2012), 1039–1048.
43. [43] Hopwood, B., Tsykin, A., Findlay, D.M., Fazzalari, N.L., Microarray gene expression profiling of osteoarthritic bone suggests altered bone remodelling, WNT and transforming growth factor-beta/bone morphogenic protein signalling. Arthritis Res. Ther., 9(5), 2007, R100.
44. [44] Dragojevic, J., Logar, D.B., Komadina, R., Marc, J., Osteoblastogenesis and adipogenesis are higher in osteoarthritic than in osteoporotic bone tissue. Arch. Med. Res. 42:5 (2011), 392–397.
45. [45] Zupan, J., Komadina, R., Marc, J., The relationship between osteoclastogenic and anti-osteoclastogenic pro-inflammatory cytokines differs in human osteoporotic and osteoarthritic bone tissues. J. Biomed. Sci., 19, 2012.
46. [46] Dragojevic, J., Zupan, J., Haring, G., et al. Triglyceride metabolism in bone tissue is associated with osteoblast and osteoclast differentiation: a gene expression study. J. Bone Miner. Metab. 31:5 (2013), 512–519.
47. [47] Giner, M., Montoya, M.J., Vazquez, M.A., Miranda, C., Perez-Cano, R., Differences in osteogenic and apoptotic genes between osteoporotic and osteoarthritic patients. BMC Musculoskelet. Disord., 14, 2013, 41.
48. [48] Foger-Samwald, U., Patsch, J.M., Schamall, D., et al. Molecular evidence of osteoblast dysfunction in elderly men with osteoporotic hip fractures. Exp. Gerontol. 57 (2014), 114–121.
49. [49] Panach, L., Mifsut, D., Tarin, J.J., Cano, A., Garcia-Perez, M.A., Serum circulating microRNAs as biomarkers of osteoporotic fracture. Calcif. Tissue Int. 97:5 (2015), 495–505.
50. [50] Laxman, N., Rubin, C.J., Mallmin, H., et al. Global miRNA expression and correlation with mRNA levels in primary human bone cells. RNA 21:8 (2015), 1433–1443.
51. [51] Meng, Z., Veenstra, T.D., Targeted mass spectrometry approaches for protein biomarker verification. J. Proteome 74:12 (2011), 2650–2659.
52. [52] Alves, R.D., Demmers, J.A., Bezstarosti, K., et al. Unraveling the human bone microenvironment beyond the classical extracellular matrix proteins: a human bone protein library. J. Proteome Res. 10:10 (2011), 4725–4733.
53. [53] Lhaneche, L., Hald, J.D., Domingues, A., et al. Variations of SOST mRNA expression in human bone are associated with DNA polymorphism and DNA methylation in the SOST gene. Bone 92 (2016), 107–115.
54. [54] Del Real, A., Perez-Campo, F.M., Fernandez, A.F., et al. Differential analysis of genome-wide methylation and gene expression in mesenchymal stem cells of patients with fractures and osteoarthritis. Epigenetics, 0, 2016.
55. [55] Kundaje, A., Meuleman, W., Ernst, J., et al. Integrative analysis of 111 reference human epigenomes. Nature 518:7539 (2015), 317–330.
56. [56] Zhang, J.G., Tan, L.J., Xu, C., et al. Integrative analysis of transcriptomic and epigenomic data to reveal regulation patterns for BMD variation. PLoS One, 10(9), 2015, e0138524.
57. [57] Hsu, Y.H., Zillikens, M.C., Wilson, S.G., et al. An integration of genome-wide association study and gene expression profiling to prioritize the discovery of novel susceptibility Loci for osteoporosis-related traits. PLoS Genet., 6(6), 2010, e1000977.
58. [58] Zheng, H.F., Forgetta, V., Hsu, Y.H., et al. Whole-genome sequencing identifies EN1 as a determinant of bone density and fracture. Nature 526:7571 (2015), 112–117.
59. [59] Kemp, J.P., Medina-Gomez, C., Estrada, K., et al. Phenotypic dissection of bone mineral density reveals skeletal site specificity and facilitates the identification of novel loci in the genetic regulation of bone mass attainment. PLoS Genet., 10(6), 2014, e1004423.
60. [60] Walton, E., Hass, J., Liu, J., et al. Correspondence of DNA methylation between blood and brain tissue and its application to schizophrenia research. Schizophr. Bull. 42:2 (2016), 406–414.
61. [61] Riese, H., van den Heuvel, E.R., Snieder, H., et al. Association between methylation of the SLC6A4 promoter region in peripheral blood leukocytes and methylation in amygdala tissue. Psychosom. Med. 76:3 (2014), 244–246.
62. [62] Brown, T.A., Lee, J.W., Holian, A., et al. Alterations in DNA methylation corresponding with lung inflammation and as a biomarker for disease development after MWCNT exposure. Nanotoxicology 10:4 (2016), 453–461.
63. [63] Li, X., Wang, Y., Zhang, Z., et al. Correlation of MLH1 and MGMT methylation levels between peripheral blood leukocytes and colorectal tissue DNA samples in colorectal cancer patients. Oncol. Lett. 6:5 (2013), 1370–1376.
64. [64] Ring, M., Saito, H., Taipaleenmäki, H., et al. Characterizing the osteoanabolic epigenome of aging-related bone loss in humans. J. Bone Miner. Res., 31(Suppl. 1), 2016, MO0255.