Differentially circulating miRNAs after recent osteoporotic fractures can influence osteogenic differentiation

Bone

Volumn 79, Issue , 2015, Pages 43-51

  Weilner, Sylvia ^a   Skalicky, Susanna ^b   Salzer, Benjamin ^a   Keider, Verena ^a   Wagner, Michael ^b   Hildner, Florian ^d   Gabriel, Christian ^d   Dovjak, Peter ^e   Pietschmann, Peter ^f   Grillari Voglauer, Regina ^c   Grillari, Johannes ^a,b,c   Hackl, Matthias ^a,b  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b TAmiRNA GmbH   (Austria)

^c Evercyte GmbH   (Austria)

^d Red Cross Blood Transfusion Service of Upper Austria   (Austria)

^e Salzkammergut Klinikum   (Austria)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Bone; Circulating microRNA (miRNA); Mesenchymal stem cells; Osteogenic differentiation; Osteoporosis; Quantitative PCR (qPCR)

Indexed keywords

LET 7G 5P; MICRORNA; MICRORNA 10A; MICRORNA 10B 5P; MICRORNA 133B; MICRORNA 22 3P; MICRORNA 328 3P; UNCLASSIFIED DRUG;

AGED; ARTICLE; BLOOD SAMPLING; BONE DEVELOPMENT; BONE METABOLISM; CELL DIFFERENTIATION; CLINICAL ARTICLE; CLUSTER ANALYSIS; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; FRAGILITY FRACTURE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MESENCHYMAL STEM CELL; PROGNOSIS; RNA ANALYSIS; BLOOD; COMPLICATION; GENETIC TRANSFECTION; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; POLYMERASE CHAIN REACTION; POSTMENOPAUSE OSTEOPOROSIS;

AGED; CELL DIFFERENTIATION; FEMALE; HUMANS; MESENCHYMAL STROMAL CELLS; MICRORNAS; OSTEOGENESIS; OSTEOPOROSIS, POSTMENOPAUSAL; OSTEOPOROTIC FRACTURES; POLYMERASE CHAIN REACTION; TRANSFECTION;

EID: 84930670046     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.05.027     Document Type: Article

References (57)

1. Kanis J.A., McCloskey E.V., Johansson H., Cooper C., Rizzoli R., Reginster J.-Y., et al. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 2013, 24:23-57. 10.1007/s00198-012-2074-y.
2. Hernlund E., Svedbom A., Ivergård M., Compston J., Cooper C., Stenmark J., et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 2013, 8:136. 10.1007/s11657-013-0136-1.
3. Cooper C., Harvey N.C. Osteoporosis risk assessment 2012, 4191:1-2. 10.1136/bmj.e4191.
4. Harvey N., Dennison E., Cooper C. Osteoporosis: impact on health and economics. Nat Rev Rheumatol 2010, 6:99-105. 10.1038/nrrheum.2009.260.
5. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 10.1016/j.cell.2009.01.002.
6. Dong S., Yang B., Guo H., Kang F. MicroRNAs regulate osteogenesis and chondrogenesis. Biochem Biophys Res Commun 2012, 418:587-591. 10.1016/j.bbrc.2012.01.075.
7. Zhao X., Xu D., Li Y., Zhang J., Liu T., Ji Y., et al. MicroRNAs regulate bone metabolism. J Bone Miner Metab 2013, 10.1007/s00774-013-0537-7.
8. Van Wijnen A.J., van de Peppel J., van Leeuwen J.P., Lian J.B., Stein G.S., Westendorf J.J., et al. MicroRNA functions in osteogenesis and dysfunctions in osteoporosis. Curr Osteoporos Rep 2013, 11:72-82. 10.1007/s11914-013-0143-6.
9. Trompeter H.-I., Dreesen J., Hermann E., Iwaniuk K.M., Hafner M., Renwick N., et al. MicroRNAs miR-26a, miR-26b, and miR-29b accelerate osteogenic differentiation of unrestricted somatic stem cells from human cord blood. BMC Genomics 2013, 14:111. 10.1186/1471-2164-14-111.
10. Li Z., Hassan M.Q., Volinia S., van Wijnen A.J., Stein J.L., Croce C.M., et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci U S A 2008, 105:13906-13911. 10.1073/pnas.0804438105.
11. Kapinas K., Kessler C.B., Delany A.M. miR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling. J Cell Biochem 2009, 108:216-224. 10.1002/jcb.22243.
12. Mizoguchi F., Izu Y., Hayata T., Hemmi H., Nakashima K., Nakamura T., et al. Osteoclast-specific Dicer gene deficiency suppresses osteoclastic bone resorption. J Cell Biochem 2010, 109:866-875. 10.1002/jcb.22228.
13. Weilner S., Schraml E., Redl H., Grillari-Voglauer R., Grillari J. Secretion of microvesicular miRNAs in cellular and organismal aging. Exp Gerontol 2013, 48:626-633. 10.1016/j.exger.2012.11.017.
14. Olivieri F., Spazzafumo L., Santini G., Lazzarini R., Albertini M.C., Rippo M.R., et al. Age-related differences in the expression of circulating microRNAs: miR-21 as a new circulating marker of inflammaging. Mech Ageing Dev 2012, 133:675-685. 10.1016/j.mad.2012.09.004.
15. Seeliger C., Karpinski K., Haug A.T., Vester H., Schmitt A., Bauer J.S., et al. Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures. J Bone Miner Res 2014, 29:1718-1728. 10.1002/jbmr.2175.
16. Li H., Wang Z., Fu Q., Zhang J. Plasma miRNA levels correlate with sensitivity to bone mineral density in postmenopausal osteoporosis patients. Biomarkers 2014, 19:553-556. 10.3109/1354750X.2014.935957.
17. Ismail N., Wang Y., Dakhlallah D., Moldovan L., Agarwal K., Batte K., et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013, 121:984-995. 10.1182/blood-2011-08-374793.
18. Zhu H., Fan G.-C. Extracellular/circulating microRNAs and their potential role in cardiovascular disease. Am J Cardiovasc Dis 2011, 1:138-149.
19. Canalis E. Wnt signalling in osteoporosis: mechanisms and novel therapeutic approaches. Nat Rev Endocrinol 2013, 9:575-583. 10.1038/nrendo.2013.154.
20. Asagiri M., Takayanagi H. The molecular understanding of osteoclast differentiation. Bone 2007, 40:251-264. 10.1016/j.bone.2006.09.023.
21. Wolbank S., Ph D., Stadler G., Peterbauer A., Sc M., Katinger H., et al. Telomerase immortalized human amnion- and adipose-derived mesenchymal stem cells: maintenance of differentiation and immunomodulatory characteristics. Tissue Eng Part A 2009, 15:1843-1854. 10.1089/ten.tea.2008.0205.Telomerase.
22. Blondal T., Jensby Nielsen S., Baker A., Andreasen D., Mouritzen P., Wrang Teilum M., et al. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods 2013, 59:S1-S6. 10.1016/j.ymeth.2012.09.015.
23. Reynoso R., Laufer N., Hackl M., Skalicky S., Monteforte R., Turk G., et al. MicroRNAs differentially present in the plasma of HIV elite controllers reduce HIV infection in vitro. Sci Rep 2014, 4:5915. 10.1038/srep05915.
24. Andersen C.L., Jensen J.L., Ørntoft T.F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 2004, 64:5245-5250. 10.1158/0008-5472.CAN-04-0496.
25. Sanders R., Mason D.J., Foy C.A., Huggett J.F. Considerations for accurate gene expression measurement by reverse transcription quantitative PCR when analysing clinical samples. Anal Bioanal Chem 2014, 10.1007/s00216-014-7857-x.
26. Zhang J., Fu W., He M., Wang H., Wang W., Yu S., et al. MiR-637 maintains the balance between adipocytes and osteoblasts by directly targeting Osterix. Mol Biol Cell 2011, 22:3955-3961. 10.1091/mbc.E11-04-0356.
27. Wei J., Li H., Wang S., Li T., Fan J., Liang X., et al. let-7 enhances osteogenesis and bone formation while repressing adipogenesis of human stromal/mesenchymal stem cells by regulating HMGA2. Stem Cells Dev 2014, 23:1452-1463. 10.1089/scd.2013.0600.
28. Zeng Y., Qu X., Li H., Huang S., Wang S., Xu Q., et al. MicroRNA-100 regulates osteogenic differentiation of human adipose-derived mesenchymal stem cells by targeting BMPR2. FEBS Lett 2012, 586:2375-2381. 10.1016/j.febslet.2012.05.049.
29. Lee Y., Kim H.J., Park C.K., Kim Y.-G., Lee H.-J., Kim J.-Y., et al. MicroRNA-124 regulates osteoclast differentiation. Bone 2013, 56:383-389. 10.1016/j.bone.2013.07.007.
30. Mizuno Y., Yagi K., Tokuzawa Y., Kanesaki-Yatsuka Y., Suda T., Katagiri T., et al. miR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation. Biochem Biophys Res Commun 2008, 368:267-272. 10.1016/j.bbrc.2008.01.073.
31. Cheng P., Chen C., He H.-B., Hu R., Zhou H.-D., Xie H., et al. miR-148a regulates osteoclastogenesis by targeting V-maf musculoaponeurotic fibrosarcoma oncogene homolog B. J Bone Miner Res 2013, 28:1180-1190. 10.1002/jbmr.1845.
32. Trohatou O., Zagoura D., Bitsika V., Pappa K.I., Antsaklis A., Anagnou N.P., et al. Sox2 suppression by miR-21 governs human mesenchymal stem cell properties. Stem Cells Transl Med 2014, 3:54-68. 10.5966/sctm.2013-0081.
33. Hassan M.Q., Gordon J.A.R., Beloti M.M., Croce C.M., van Wijnen A.J., Stein J.L., et al. A network connecting Runx2, SATB2, and the miR-23a~27a~24-2 cluster regulates the osteoblast differentiation program. Proc Natl Acad Sci U S A 2010, 107:19879-19884. 10.1073/pnas.1007698107.
34. Yang L., Cheng P., Chen C., He H.-B., Xie G.-Q., Zhou H.-D., et al. miR-93/Sp7 function loop mediates osteoblast mineralization. J Bone Miner Res 2012, 27:1598-1606. 10.1002/jbmr.1621.
35. De Guire V., Robitaille R., Tétreault N., Guérin R., Ménard C., Bambace N., et al. Circulating miRNAs as sensitive and specific biomarkers for the diagnosis and monitoring of human diseases: promises and challenges. Clin Biochem 2013, 46:846-860. 10.1016/j.clinbiochem.2013.03.015.
36. Hackl M., Brunner S., Fortschegger K., Schreiner C., Micutkova L., Mück C., et al. miR-17, miR-19b, miR-20a, and miR-106a are down-regulated in human aging. Aging Cell 2010, 9:291-296. 10.1111/j.1474-9726.2010.00549.x.
37. Grillari J., Hackl M., Grillari-Voglauer R. miR-17-92 cluster: ups and downs in cancer and aging. Biogerontology 2010, 11:501-506.
38. Qin B., Yang H., Xiao B. Role of microRNAs in endothelial inflammation and senescence. Mol Biol Rep 2012, 39:4509-4518. 10.1007/s11033-011-1241-0.
39. Fang Y., Shi C., Manduchi E., Civelek M., Davies P.F. MicroRNA-10a regulation of proinflammatory phenotype in athero-susceptible endothelium in vivo and in vitro. Proc Natl Acad Sci U S A 2010, 107:13450-13455. 10.1073/pnas.1002120107.
40. McCarthy J.J. MicroRNA-206: the skeletal muscle-specific myomiR. Biochim Biophys Acta 1779, 2008:682-691. 10.1016/j.bbagrm.2008.03.001.
41. Lin Q., Wei W., Coelho C.M., Li X., Baker-Andresen D., Dudley K., et al. The brain-specific microRNA miR-128b regulates the formation of fear-extinction memory. Nat Neurosci 2011, 14:1115-1117. 10.1038/nn.2891.
42. Mikaelian I., Scicchitano M., Mendes O., Thomas R.A., LeRoy B.E. Frontiers in preclinical safety biomarkers: microRNAs and messenger RNAs. Toxicol Pathol 2012, 18-31. 10.1177/0192623312448939.
43. Zaharieva I.T., Calissano M., Scoto M., Preston M., Cirak S., Feng L., et al. Dystromirs as serum biomarkers for monitoring the disease severity in duchenne muscular dystrophy. PLoS ONE 2013, 8:e80263. 10.1371/journal.pone.0080263.
44. Liang Y., Ridzon D., Wong L., Chen C. Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 2007, 8:166. 10.1186/1471-2164-8-166.
45. Eguchi T., Watanabe K., Hara E.S., Ono M., Kuboki T., Calderwood S.K. OstemiR: a novel panel of microRNA biomarkers in osteoblastic and osteocytic differentiation from mesenchymal stem cells. PLoS ONE 2013, 8:e58796. 10.1371/journal.pone.0058796.
46. Lei S.-F., Papasian C.J., Deng H.-W. Polymorphisms in predicted miRNA binding sites and osteoporosis. J Bone Miner Res 2011, 26:72-78. 10.1002/jbmr.186.
47. Tragante V., Barnes M.R., Ganesh S.K., Lanktree M.B., Guo W., Franceschini N., et al. Gene-centric meta-analysis in 87,736 individuals of European ancestry identifies multiple blood-pressure-related loci. Am J Hum Genet 2014, 94:349-360. 10.1016/j.ajhg.2013.12.016.
48. Wang Y., Li L., Moore B.T., Peng X.-H., Fang X., Lappe J.M., et al. MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS ONE 2012, 7:e34641. 10.1371/journal.pone.0034641.
49. Kornfeld J.-W., Brüning J.C. MyomiRs-133a/b turn off the heat. Nat Cell Biol 2012, 14:1248-1249. 10.1038/ncb2642.
50. Tokarz P., Blasiak J. The role of microRNA in metastatic colorectal cancer and its significance in cancer prognosis and treatment. Acta Biochim Pol 2012, 59:467-474.
51. Delic S., Lottmann N., Stelzl A., Liesenberg F., Wolter M., Götze S., et al. MiR-328 promotes glioma cell invasion via SFRP1-dependent Wnt-signaling activation. Neuro Oncol 2014, 16:179-190. 10.1093/neuonc/not164.
52. Ishimoto T., Sugihara H., Watanabe M., Sawayama H., Iwatsuki M., Baba Y., et al. Macrophage-derived reactive oxygen species suppress miR-328 targeting CD44 in cancer cells and promote redox adaptation. Carcinogenesis 2014, 35:1003-1011. 10.1093/carcin/bgt402.
53. Hughes D.E., Salter D.M., Simpson R. CD44 expression in human bone: a novel marker of osteocytic differentiation. J Bone Miner Res 1994, 9:39-44. 10.1002/jbmr.5650090106.
54. Boyerinas B., Park S.-M., Hau A., Murmann A.E., Peter M.E. The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer 2010, 17:F19-F36. 10.1677/ERC-09-0184.
55. Bakhshandeh B., Soleimani M., Hafizi M., Paylakhi S.H., Ghaemi N. MicroRNA signature associated with osteogenic lineage commitment. Mol Biol Rep 2012, 39:7569-7581. 10.1007/s11033-012-1591-2.
56. Garnero P. New developments in biological markers of bone metabolism in osteoporosis. Bone 2014, 66:46-55. 10.1016/j.bone.2014.05.016.
57. Huang J., Chen D. miRNAs in circulation: mirroring bone conditions?. J Bone Miner Res 2014, 29:1718-1728. 10.1002/jbmr.2297.