MicroRNA-29a mitigates glucocorticoid induction of bone loss and fatty marrow by rescuing Runx2 acetylation

Bone

Volumn 81, Issue , 2015, Pages 80-88

  Ko, Jih Yang ^a,b   Chuang, Pei Chin ^a   Ke, Huei Jin ^a   Chen, Yu Shan ^a   Sun, Yi Chih ^a   Wang, Feng Sheng ^a,b  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Bone loss; HDAC4; Marrow fat; MiR 29a; Runx2 acetylation

Indexed keywords

BETA CATENIN; HISTONE DEACETYLASE 4; LEPTIN; MICRORNA 29A; TRANSCRIPTION FACTOR RUNX2; GLUCOCORTICOID; METHYLPREDNISOLONE; MICRORNA; MIRN29 MICRORNA, MOUSE; RUNX2 PROTEIN, MOUSE;

ACETYLATION; ADIPOCYTE; ADIPOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MARROW; BONE MARROW DERIVED MONONUCLEAR CELL; BONE MASS; BONE MINERALIZATION; BONE STRUCTURE; CELL DIFFERENTIATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CORTICAL THICKNESS (BONE); CORTICOSTEROID INDUCED OSTEOPOROSIS; DUAL ENERGY X RAY ABSORPTIOMETRY; ENZYME INHIBITION; EX VIVO STUDY; GENE EXPRESSION; GENE OVEREXPRESSION; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNOBLOTTING; LIPID METABOLISM; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRABECULAR BONE; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; BONE; BONE DEVELOPMENT; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; OSTEOPOROSIS; PATHOLOGY; PHOTON ABSORPTIOMETRY;

ABSORPTIOMETRY, PHOTON; ACETYLATION; ADIPOGENESIS; ANIMALS; BONE AND BONES; BONE MARROW; CORE BINDING FACTOR ALPHA 1 SUBUNIT; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLUCOCORTICOIDS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; METHYLPREDNISOLONE; MICE; MICE, TRANSGENIC; MICRORNAS; OSTEOGENESIS; OSTEOPOROSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; X-RAY MICROTOMOGRAPHY;

EID: 84938499406     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.06.022     Document Type: Article

References (40)

1. Rizzole R., Biver E. Glucocorticoid-induced osteoporosis: who to treat with what agent?. Nat. Rev. Rheumatol. 2015, 11:98-109.
2. Seibel M.J., Cooper M.S., Zhou H. Glucocorticoid-induced osteoporosis: mechanism, management, and future perspectives. Lancet Diabetes Endocrinol 2013, 1:59-70.
3. Tamura Y., Kawao N., Yano M., Okada K., Okumoto K., Chiba Y., Matsuo O., Kaji H. Role of plasminogen activator inhibitor-1 in glucocorticoid-induced diabetes and osteopenia in mice. Diabetes 2015, 64:2194-2206.
4. Tang Q.Q., Lane M.D. Adipogenesis from stem cell to adipocyte. Annu. Rev. Biochem. 2012, 81:715-736.
5. Sinha P., Aarnisalo P., Chubb R., Ono N., Fulzele K., Selig M., Saeed H., Chen M., Weinstein L.S., Pajevic P.D., Kronenberg H.M., Wu J.Y. Loss of Gsα early in the osteoblast lineage favors adipogenic differentiation of mesenchymal progenitors and committed osteoblast precursors. J. Bone Miner. Res. 2014, 29:2414-2426.
6. Hay E., Dieudonné F.X., Saidak Z., Marty C., Brun J., Da Nascimento S., Sonnet P., Marie P.J. N-cadherin/wnt interaction controls bone marrow mesenchymal cell fate and bone mass during aging. J. Cell. Physiol. 2014, 229:1765-1775.
7. Li J., Zhang N., Huang X., Xu J., Fernandes J.C., Dai K., Zhang X. Dexamethasone shifts bone marrow stromal cells from osteoblasts to adipocytes by C/EBPalpha promoter methylation. Cell Death Dis. 2013, 4e832.
8. Esteller M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011, 12:861-874.
9. Krzeszinski J.Y., Wei W., Huyuh H., Jin Z., Wang X., Chang T.C., Xie X.J., He L., Mangala L.S., Lopez-Berestin G., Sood A.K., Mendell J.T., Wan Y. miR-34a blocks osteoporosis and bone metastasis by inhibiting osteoclastogenesis and Tgif2. Nature 2014, 512:431-435.
10. Papaioannou G., Mirzamohammadi F., Lisse T.S., Nishimori S., Wein M.N., Kobayashi T. MicroRNA-140 provides robustness to the regulation of hypertrophic chondrocyte differentiation by the PTHrP-HDAC4 pathways. J. Bone Miner. Res. 2014, 10.1002/jbmr.2438.
11. Taipaleenmaki H., Browne H., Akech J., Zustin J., van Wijnen A.J., Stein J.L., Hesse E., Stein G.S., Lian J.B. Targeting of Runx2 by miR-135 and miR-203 impairs progression of breast cancer and metastatic bone disease. Cancer Res. 2015, 75:1433-1444.
12. Jeong B.C., Kang I.H., Hwang Y.C., Kim S.H., Koh J.T. MicroRNA-194 reciprocally stimulates osteogenesis and inhibits adipogenesis via regulating COUP-TFII expression. Cell Death Dis. 2014, e5:1532.
13. Liao L., Yang X., Su X., Hu C., Zhu X., Yang N., Chen X., Shi S., Shi S., Jin Y. Redundant miR-3077-5p and miR-705 mediate the shift of mesenchymal stem cell lineage commitment to adipocyte in osteoporosis bone marrow. Cell Death Dis. 2013, 4:e600.
14. Hu W., Dooley J., Chung S.S., Chandramohan D., Cimmino L., Mukherjee S., Mason C.E., Strooper B., Liston A., Park C.Y. MiR-29a maintains mouse hematopoietic stem cell self-renewal by regulating Dnmt3a. Blood 2015, 125:2206-2216.
15. Kapinas K., Kessler C., Ricks T., Gronwicz G., Delany A.M. miR-29 modulates Wnt signaling in human osteoblasts through a positive feedback loop. J. Biol. Chem. 2010, 285:25221-25231.
16. Guêrit D., Brondello J.M., Chuchana P., Philipot D., Toupet K., Bony C., Jorgensen C., Noël D. FoxO3a regulation by miRNA-29a controls chondrogenic differentiation of mesenchymal stem cells and cartilage formation. Stem Cells Dev. 2014, 23:1195-1205.
17. Franceschetti T., Kessler C.B., Lee S.K., Delany A.M. miR-29 promotes murine osteoclastogenesis by regulating osteoclast commitment and migration. J. Biol. Chem. 2013, 288:33347-33360.
18. Yang M.W., Jeong H.U., Park S.Y., Lee W. Induction of miR-29a by saturated fatty acids impairs insulin signaling and glucose uptake through translational repression of IRS-1 in myocytes. FEBS Lett. 2014, 588:2170-2176.
19. Mattis A.N., Song G., Hitchner K., Kim R.Y., Lee A.Y., Sharma A.D., Malato Y., McManus M.T., Esau C.C., Koller E., Koliwad S., Lim L.P., Maher J.J., Raffai R.L., Willenbring H. A screen in mice uncovers repression of lipoprotein lipase by microRNA-29a as a mechanism for lipid distribution away from the liver. Hepatology 2015, 61:141-152.
20. Ko J.Y., Chuang P.C., Chen M.W., Ke H.C., Wu S.L., Chang Y.H., Chen Y.S., Wang F.S. MicroRNA-29a ameliorates glucocorticoid-induced suppression of osteoblast differentiation by regulating β-catenin acetylation. Bone 2013, 57:468-475.
21. Lin C.L., Lee P.H., Hsu Y.C., Lei C.C., Ko J.Y., Chuang P.C., Huang Y.T., Wang S.Y., Chen Y.S., Chiang W.C., Reiser J., Wang F.S. MicroRNA-29a promotion of nephrin acetylation ameliorates hyperglycemia-induced podocyte dysfunction. J. Am. Soc. Nephrol. 2014, 25:1698-1709.
22. Tiao M.M., Wang F.S., Huang L.T., Chuang J.H., Ko H.C., Yang Y.L., Huang Y.H. MicroRN-29a protects against acute liver injury in a mouse model of obstructive jaundice via inhibition of the extrinsic apoptosis pathway. Apoptosis 2014, 19:30-41.
23. Dempster D.W., Compston J.E., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., Ott S.M., Recker R.R., Parfitt A.M. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2013, 28:1-16.
24. Ko J.Y., Wu R.W., Kuo S.J., Chen M.W., Yeh D.W., Ke H.C.Wu.S.L., Wang F.S. Cannabinoid receptor 1 mediates glucocorticoid-induced bone loss in rats by perturbing bone mineral acquisition and marrow adipogenesis. Arthritis Rheum. 2012, 64:1204-1214.
25. Choi Y.H., Kim Y.J., Jeong H.M., Jin Y.H., Yeo C.Y., Lee K.Y. Akt enhances Runx2 protein stability by regulating Smurf2 function during osteoblast differentiation. FEBS J. 2014, 281:3655-3666.
26. Buehring B., Viswanathan R., Binkley N.T., Busse W. Glucocorticoid-induced osteoporosis: an update on effects and management. J. Allergy Clin. Immunol. 2013, 132:1019-1030.
27. Sato A.Y., Tu X., McAndrews K.A., Plotkin L.O., Bellido T. Prevention of glucocorticoid induced-apoptosis of osteoblast and osteocytes by protecting against endoplasmic reticulum (ER) stress in vitro and in vivo in female mice. Bone 2015, 73:60-68.
28. Piemontese M., Onal M., Xiong J., Wang Y., Almeida M., Thostenson J.D., Weinstein R.S., Manolagas S.C., O'Brien C.A. Suppression of autophagy in osteocytes does not modify the adverse effects of glucocorticoids on cortical bone. Bone 2015, 75C:18-26.
29. Roderburg C., Urban G.W., Bettermann K., Vucur M., Zimmermann H., Janssen J., Koppe C., Knolle P., Castoldi M., Tacke F., Tautwein C., Luedde T. MicroRNA profiling reveals a role for miR-29 in human and murine live fibrosis. Hepatology 2011, 53:209-218.
30. Wang B., Komers Carew R., Winbanks C.E., Xu B., Herman-Edelstein M., Koh P., Thomas M., Jandeleit-Dahm K., Gregorevic P., Cooper M.E., Kantharidis P. Suppression of microRNA-29 expression by TGF-β1 promotes collagen expression and renal fibrosis. J. Am. Soc. Nephrol. 2012, 23:252-265.
31. Maurer B., Stanczyk J., Jungel A., Akhmetshina A., Trenkmann M., Brock M., Kowal-Bielecka O., Gay R.E., Michel B.A., Distler J.H., Gay S., Distler O. MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum. 2010, 62:1733-1743.
32. Li Z., Hassan M.O., Jafferji M., Aqwilan R.I., Garzon R., Croce C.M., von Wijnen A.J., Stein J.L., Stein G.S., Lian J.B. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J. Biol. Chem. 2009, 284:15676-15684.
33. Yao W., Cheng Z., Busse C., Pham A., Nakamura M.C., Lane N.E. Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum. 2008, 58:1674-1686.
34. Li G.W., Chang S.X., Fan J.Z., Tian Y.N., Xu Z., He Y.M. Marrow adiposity recovery after early zoledronic acid treatment of glucocorticoid-induced bone loss in rabbits assessed by magnetic resonance spectroscopy. Bone 2013, 52:668-675.
35. Kurtz C.L., Peck B.C., Fannin E.E., Beysen C., Miao J., Landstreet S.R., Ding S., Turaga V., Lund P.K., Turner S., Biddinger S.B., Vickers K.C., Sethupathy P. MicroRNA-29 fine tunes the expression of key FOXA2-activated lipid metabolism genes and is dysregulated in animals of insulin resistance and diabetes. Diabetes 2014, 63:3141-3148.
36. Yoon W.J., Cho Y.D., Kim W.J., Bae H.S., Islam R., Woo K.M., Baek J.H., Bae S.C., Ryoo H.M. Prolyl isomerase Pin1-mediated conformational change and subnuclear focal accumulation of Runx2 are crucial for fibroblast growth factor 2 (FGF2)-induced osteoblast differentiation. J. Biol. Chem. 2014, 289:8828-8838.
37. Shimizu E., Nakatani T., He Z., Partridge N.C. Parathyroid hormone regulates histone deacetylase (HDAC) 4 through protein kinase A-mediated phosphorylation and dephosphorylation in osteoblastic cells. J. Biol. Chem. 2014, 289:21340-21350.
38. Makinistoglu M.P., Karsenty G. The class II histone deacetylase HDAC4 regulates cognitive, metabolic and endocrine functions through its expression in osteoblasts. Mole. Metab. 2014, 4:64-69.
39. Song L., Liu M., Ono N., Bringhurst F.R., Kronenbergy H.M., Guo J. Loss of wnt/β-catenin signaling causes cell fate shift of preosteoblasts from osteoblast to adipocytes. J. Bone Miner. Res. 2012, 27:2344-2358.
40. Winbanks C.E., Wang B., Beyer C., Koh P., White L., Kantharidis P., Gregorevic P. TGF-β regulates miR-206 and miR-29 to control myogenic differentiation through regulation of HDAC4. J. Biol. Chem. 2011, 286:13806-13814.