The regulatory role of microRNA in osteogenic differentiation of mesenchymal stem cells and its application as a therapeutic target and diagnostic tool in orthopedic diseases_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Xiaolong ,  KONG Qingquan

Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

KONG Qingquan, Email: kongqqspine@163.com

Keywords：

MicroRNA; mesenchymal stem cells; osteogeneic differentiation; osteoporosis; orthopaedic disease

DOI：

10.7507/1002-1892.201912092

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of the regulatory role of microRNA (miRNA) in osteogenic differentiation of mesenchymal stem cells (MSCs) and its application as a therapeutic target and diagnostic tool in orthopedic diseases.Methods The recent literature on the regulation of MSCs osteogenic differentiation by miRNAs was extensively reviewed, and its regulatory mechanism and its application as a therapeutic target and diagnostic tool in orthopedic diseases were reviewed.Results miRNAs are small endogenous non-coding RNAs with a length of 20-22 nucleotides, which play an important role in the osteogenic differentiation of MSCs. Osteogenesis begins with the differentiation of MSCs into mature osteoblasts, and each stage of dynamic homeostasis of bone metabolism is associated with the regulation of different miRNAs. miRNAs are regulated from the post-transcriptional level by mRNAs cleavage, degradation, translational repression, or methylation. In addition, current studies suggest that miRNAs can be used as a new diagnostic tool and therapeutic target for orthopedic diseases.Conclusion Further study on the regulation mechanism of miRNAs will provide more ideas for finding new therapeutic targets and diagnostic tools for orthopedic disease.

Citation： LI Xiaolong, KONG Qingquan. The regulatory role of microRNA in osteogenic differentiation of mesenchymal stem cells and its application as a therapeutic target and diagnostic tool in orthopedic diseases. Chinese Journal of Reparative and Reconstructive Surgery, 2020, 34(10): 1332-1340. doi: 10.7507/1002-1892.201912092 Copy

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2.	Qadir AS, Um S, Lee H, et al. miR-124 negatively regulates osteogenic differentiation and in vivo bone formation of mesenchymal stem cells. J Cell Biochem, 2015, 116(5): 730-742.
3.	陆细红, 邓敏, 贺洪辉, 等. miR-125b 通过靶向抑制 Smad4 调控骨髓间充质干细胞成骨分化. 中南大学学报 (医学版), 2013, 38(4): 341-346.
4.	Wen P, Cao H, Fang L, et al. miR-125b/Ets1 axis regulates transdifferentiation and calcification of vascular smooth muscle cells in a high-phosphate environment. Exp Cell Res, 2014, 322(2): 302-312.
5.	Schmidt Y, Simunovic F, Strassburg S, et al. miR-126 regulates platelet-derived growth factor receptor-α expression and migration of primary human osteoblasts. Biol Chem, 2015, 396(1): 61-70.
6.	Laxman N, Rubin CJ, Mallmin H, et al. Global miRNA expression and correlation with mRNA levels in primary human bone cells. RNA, 2015, 21(8): 1433-1443.
7.	Ell B, Kang Y. MicroRNAs as regulators of bone homeostasis and bone metastasis. Bonekey Rep, 2014, 3: 549.
8.	Kapinas K, Delany AM. MicroRNA biogenesis and regulation of bone remodeling. Arthritis Res Ther, 2011, 13(3): 220.
9.	Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5): 843-854.
10.	Flynt AS, Lai EC. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet, 2008, 9(11): 831-842.
11.	Seitz H. Redefining microRNA targets. Current Biology, 2009, 19(10): 870-873.
12.	Boehm M, Slack FJ. MicroRNA control of lifespan and metabolism. Cell Cycle, 2006, 5(8): 837-840.
13.	Rhoades MW, Reinhart BJ, Lim LP, et al. Prediction of plant microRNA targets. Cell, 2002, 110(4): 513-520.
14.	Miyaki S, Nakasa T, Otsuki S, et al. MicroRNA-140 is expressed in differentiated human articular chondrocytes and modulates interleukin-1 responses. Arthritis Rheum, 2009, 60(9): 2723-2730.
15.	Kobayashi T, Lu J, Cobb BS, et al. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci U S A, 2008, 105(6): 1949-1954.
16.	Gaur T, Hussain S, Mudhasani R, et al. Dicer inactivation in osteoprogenitor cells compromises fetal survival and bone formation, while excision in differentiated osteoblasts increases bone mass in the adult mouse. Dev Biol, 2010, 340(1): 10-21.
17.	Bonin CA, van Wijnen AJ, Lewallen EA. MicroRNA applications in marine biology. Current Molecular Biology Reports, 2019, 5: 167-175.
18.	Wei B, Wei W, Wang L, et al. Differentially expressed microRNAs in conservatively treated nontraumatic osteonecrosis compared with healthy controls. Biomed Res Int, 2018, 2018: 9015758.
19.	Taipaleenmäki H. Regulation of bone metabolism by microRNAs. Curr Osteoporos Rep, 2018, 16(1): 1-12.
20.	Valenti MT, Dalle Carbonare L, Mottes M. Role of microRNAs in progenitor cell commitment and osteogenic differentiation in health and disease (Review). Int J Mol Med, 2018, 41(5): 2441-2449.
21.	Luther G, Wagner ER, Zhu G, et al. BMP-9 induced osteogenic differentiation of mesenchymal stem cells: molecular mechanism and therapeutic potential. Curr Gene Ther, 2011, 11(3): 229-240.
22.	Liu H, Zhong L, Yuan T, et al. MicroRNA-155 inhibits the osteogenic differentiation of mesenchymal stem cells induced by BMP9 via downregulation of BMP signaling pathway. Int J Mol Med, 2018, 41(6): 3379-3393.
23.	Lin Z, Tang Y, Tan H, et al. MicroRNA-92a-1-5p influences osteogenic differentiation of MC3T3-E1 cells by regulating β-catenin. J Bone Miner Metab, 2019, 37(2): 264-272.
24.	Saiganesh S, Saathvika R, Arumugam B, et al. TGF-β₁-stimulation of matrix metalloproteinase-13 expression by down-regulation of miR-203a-5p in rat osteoblasts. Int J Biol Macromol, 2019, 132: 541-549.
25.	Huang E, Liu R, Chu Y. miRNA-15a/16: as tumor suppressors and more. Future Oncol, 2015, 11(16): 2351-2363.
26.	Duan L, Zhao H, Xiong Y, et al. miR-16-2^* Interferes with WNT5A to regulate osteogenesis of mesenchymal stem cells. Cell Physiol Biochem, 2018, 51(3): 1087-1102.
27.	Wang SN, Zhao XQ, Yu B, et al. miR-193a inhibits osteogenic differentiation of bone marrow-derived stroma cell via targeting HMGB1. Biochem Biophys Res Commun, 2018, 503(2): 536-543.
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29.	Peng S, Cao L, He S, et al. An overview of long noncoding RNAs involved in bone regeneration from mesenchymal stem cells. Stem Cells Int, 2018, 2018: 8273648.
30.	Peng W, Deng W, Zhang J, et al. Long noncoding RNA ANCR suppresses bone formation of periodontal ligament stem cells via sponging miRNA-758. Biochem Biophys Res Commun, 2018, 503(2): 815-821.
31.	Woods S, Barter MJ, Elliott HR, et al. miR-324-5p is up regulated in end-stage osteoarthritis and regulates Indian Hedgehog signalling by differing mechanisms in human and mouse. Matrix Biol, 2019, 77: 87-100.
32.	Fariyike B, Singleton Q, Hunter M, et al. Role of microRNA-141 in the aging musculoskeletal system: A current overview. Mech Ageing Dev, 2019, 178: 9-15.
33.	Daoussis D, Liossis SN, Solomou EE, et al. Evidence that Dkk-1 is dysfunctional in ankylosing spondylitis. Arthritis Rheum, 2010, 62(1): 150-158.
34.	Tang X, Lin J, Wang G, et al. MicroRNA-433-3p promotes osteoblast differentiation through targeting DKK1 expression. PLoS One, 2017, 12(6): e0179860.
35.	Fan L, Fan J, Liu Y, et al. miR-450b promotes osteogenic differentiation in vitro and enhances bone formation in vivo by targeting BMP3. Stem Cells Dev, 2018, 27(9): 600-611.
36.	Cai Q, Zheng P, Ma F, et al. MicroRNA-224 enhances the osteoblastic differentiation of hMSCs via Rac1. Cell Biochem Funct, 2019, 37(2): 62-71.
37.	Wang H, Hu Z, Shi F, et al. Osteoblast-targeted delivery of miR-33-5p attenuates osteopenia development induced by mechanical unloading in mice. Cell Death Dis, 2018, 9(2): 170.
38.	Kuang MJ, Xing F, Wang D, et al. CircUSP45 inhibited osteogenesis in glucocorticoid-induced osteonecrosis of femoral head by sponging miR-127-5p through PTEN/AKT signal pathway: Experimental studies. Biochem Biophys Res Commun, 2019, 509(1): 255-261.
39.	Hu H, Zhao C, Zhang P, et al. miR-26b modulates OA induced BMSC osteogenesis through regulating GSK3β/β-catenin pathway. Exp Mol Pathol, 2019, 107: 158-164.
40.	Han Y, Zhang K, Hong Y, et al. miR-342-3p promotes osteogenic differentiation via targeting ATF3. FEBS Lett, 2018, 592(24): 4051-4065.
41.	Wiggins JF, Ruffino L, Kelnar K, et al. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res, 2010, 70(14): 5923-5930.
42.	Janssen HL, Reesink HW, Lawitz EJ, et al. Treatment of HCV infection by targeting microRNA. N Engl J Med, 2013, 368(18): 1685-1694.
43.	Trajkovski M, Hausser J, Soutschek J, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature, 2011, 474(7353): 649-653.
44.	Ottosen S, Parsley TB, Yang L, et al. In vitro antiviral activity and preclinical and clinical resistance profile of miravirsen, a novel anti-hepatitis C virus therapeutic targeting the human factor miR-122. Antimicrob Agents Chemother, 2015, 59(1): 599-608.
45.	Cheng G. Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv Drug Deliv Rev, 2015, 81: 75-93.
46.	Feng Q, Zheng S, Zheng J. The emerging role of microRNAs in bone remodeling and its therapeutic implications for osteoporosis. Biosci Rep, 2018, 38(3): pii: BSR20180453.
47.	Feichtinger X, Muschitz C, Heimel P, et al. Bone-related circulating microRNAs miR-29b-3p, miR-550a-3p, and miR-324-3p and their association to bone microstructure and histomorphometry. Sci Rep, 2018, 8(1): 4867.
48.	Deng L, Hu G, Jin L, et al. Involvement of microRNA-23b in TNF-α-reduced BMSC osteogenic differentiation via targeting runx2. J Bone Miner Metab, 2018, 36(6): 648-660.
49.	Wu ZH, Huang KH, Liu K, et al. DGCR5 induces osteogenic differentiation by up-regulating Runx2 through miR-30d-5p. Biochem Biophys Res Commun, 2018, 505(2): 426-431.
50.	Wang Y, Li L, Moore BT, et al. MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS One, 2012, 7(4): e34641.
51.	Seeliger C, Karpinski K, Haug AT, et al. Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures. J Bone Miner Res, 2014, 29(8): 1718-1728.
52.	Weilner S, Skalicky S, Salzer B, et al. Differentially circulating miRNAs after recent osteoporotic fractures can influence osteogenic differentiation. Bone, 2015, 79: 43-51.
53.	Kocijan R, Muschitz C, Geiger E, et al. Circulating microRNA signatures in patients with idiopathic and postmenopausal osteoporosis and fragility fractures. J Clin Endocrinol Metab, 2016, 101(11): 4125-4134.
54.	Mandourah AY, Ranganath L, Barraclough R, et al. Circulating microRNAs as potential diagnostic biomarkers for osteoporosis. Sci Rep, 2018, 8(1): 8421.
55.	Yamasaki K, Nakasa T, Miyaki S, et al. Expression of microRNA‐146a in osteoarthritis cartilage. Arthritis & Rheumatism, 2009, 60(4): 1035-1041.
56.	Kurowska-Stolarska M, Alivernini S, Ballantine LE, et al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc Natl Acad Sci U S A, 2011, 108(27): 11193-11198.
57.	Xi Y, Jiang T, Wang W, et al. Long non-coding HCG18 promotes intervertebral disc degeneration by sponging miR-146a-5p and regulating TRAF6 expression. Sci Rep, 2017, 7(1): 13234.
58.	García-Giménez JL, Rubio-Belmar PA, Peiró-Chova L, et al. Circulating miRNAs as diagnostic biomarkers for adolescent idiopathic scoliosis. Sci Rep, 2018, 8(1): 2646.
59.	Kao GS, Tu YK, Sung PH, et al. MicroRNA-mediated interacting circuits predict hypoxia and inhibited osteogenesis of stem cells, and dysregulated angiogenesis are involved in osteonecrosis of the femoral head. Int Orthop, 2018, 42(7): 1605-1614.
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63.	Nakasa T, Shibuya H, Nagata Y, et al. The inhibitory effect of microRNA-146a expression on bone destruction in collagen-induced arthritis. Arthritis Rheum, 2011, 63(6): 1582-1590.
64.	Shibuya H, Nakasa T, Adachi N, et al. Overexpression of microRNA-223 in rheumatoid arthritis synovium controls osteoclast differentiation. Mod Rheumatol, 2013, 23(4): 674-685.
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1. Moore BT, Xiao P. MiRNAs in bone diseases. Microrna, 2013, 2(1): 20-31.
2. Qadir AS, Um S, Lee H, et al. miR-124 negatively regulates osteogenic differentiation and in vivo bone formation of mesenchymal stem cells. J Cell Biochem, 2015, 116(5): 730-742.
3. 陆细红, 邓敏, 贺洪辉, 等. miR-125b 通过靶向抑制 Smad4 调控骨髓间充质干细胞成骨分化. 中南大学学报 (医学版), 2013, 38(4): 341-346.
4. Wen P, Cao H, Fang L, et al. miR-125b/Ets1 axis regulates transdifferentiation and calcification of vascular smooth muscle cells in a high-phosphate environment. Exp Cell Res, 2014, 322(2): 302-312.
5. Schmidt Y, Simunovic F, Strassburg S, et al. miR-126 regulates platelet-derived growth factor receptor-α expression and migration of primary human osteoblasts. Biol Chem, 2015, 396(1): 61-70.
6. Laxman N, Rubin CJ, Mallmin H, et al. Global miRNA expression and correlation with mRNA levels in primary human bone cells. RNA, 2015, 21(8): 1433-1443.
7. Ell B, Kang Y. MicroRNAs as regulators of bone homeostasis and bone metastasis. Bonekey Rep, 2014, 3: 549.
8. Kapinas K, Delany AM. MicroRNA biogenesis and regulation of bone remodeling. Arthritis Res Ther, 2011, 13(3): 220.
9. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5): 843-854.
10. Flynt AS, Lai EC. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat Rev Genet, 2008, 9(11): 831-842.
11. Seitz H. Redefining microRNA targets. Current Biology, 2009, 19(10): 870-873.
12. Boehm M, Slack FJ. MicroRNA control of lifespan and metabolism. Cell Cycle, 2006, 5(8): 837-840.
13. Rhoades MW, Reinhart BJ, Lim LP, et al. Prediction of plant microRNA targets. Cell, 2002, 110(4): 513-520.
14. Miyaki S, Nakasa T, Otsuki S, et al. MicroRNA-140 is expressed in differentiated human articular chondrocytes and modulates interleukin-1 responses. Arthritis Rheum, 2009, 60(9): 2723-2730.
15. Kobayashi T, Lu J, Cobb BS, et al. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci U S A, 2008, 105(6): 1949-1954.
16. Gaur T, Hussain S, Mudhasani R, et al. Dicer inactivation in osteoprogenitor cells compromises fetal survival and bone formation, while excision in differentiated osteoblasts increases bone mass in the adult mouse. Dev Biol, 2010, 340(1): 10-21.
17. Bonin CA, van Wijnen AJ, Lewallen EA. MicroRNA applications in marine biology. Current Molecular Biology Reports, 2019, 5: 167-175.
18. Wei B, Wei W, Wang L, et al. Differentially expressed microRNAs in conservatively treated nontraumatic osteonecrosis compared with healthy controls. Biomed Res Int, 2018, 2018: 9015758.
19. Taipaleenmäki H. Regulation of bone metabolism by microRNAs. Curr Osteoporos Rep, 2018, 16(1): 1-12.
20. Valenti MT, Dalle Carbonare L, Mottes M. Role of microRNAs in progenitor cell commitment and osteogenic differentiation in health and disease (Review). Int J Mol Med, 2018, 41(5): 2441-2449.
21. Luther G, Wagner ER, Zhu G, et al. BMP-9 induced osteogenic differentiation of mesenchymal stem cells: molecular mechanism and therapeutic potential. Curr Gene Ther, 2011, 11(3): 229-240.
22. Liu H, Zhong L, Yuan T, et al. MicroRNA-155 inhibits the osteogenic differentiation of mesenchymal stem cells induced by BMP9 via downregulation of BMP signaling pathway. Int J Mol Med, 2018, 41(6): 3379-3393.
23. Lin Z, Tang Y, Tan H, et al. MicroRNA-92a-1-5p influences osteogenic differentiation of MC3T3-E1 cells by regulating β-catenin. J Bone Miner Metab, 2019, 37(2): 264-272.
24. Saiganesh S, Saathvika R, Arumugam B, et al. TGF-β₁-stimulation of matrix metalloproteinase-13 expression by down-regulation of miR-203a-5p in rat osteoblasts. Int J Biol Macromol, 2019, 132: 541-549.
25. Huang E, Liu R, Chu Y. miRNA-15a/16: as tumor suppressors and more. Future Oncol, 2015, 11(16): 2351-2363.
26. Duan L, Zhao H, Xiong Y, et al. miR-16-2^* Interferes with WNT5A to regulate osteogenesis of mesenchymal stem cells. Cell Physiol Biochem, 2018, 51(3): 1087-1102.
27. Wang SN, Zhao XQ, Yu B, et al. miR-193a inhibits osteogenic differentiation of bone marrow-derived stroma cell via targeting HMGB1. Biochem Biophys Res Commun, 2018, 503(2): 536-543.
28. Hassan MQ, Tye CE, Stein GS, et al. Non-coding RNAs: Epigenetic regulators of bone development and homeostasis. Bone, 2015, 81: 746-756.
29. Peng S, Cao L, He S, et al. An overview of long noncoding RNAs involved in bone regeneration from mesenchymal stem cells. Stem Cells Int, 2018, 2018: 8273648.
30. Peng W, Deng W, Zhang J, et al. Long noncoding RNA ANCR suppresses bone formation of periodontal ligament stem cells via sponging miRNA-758. Biochem Biophys Res Commun, 2018, 503(2): 815-821.
31. Woods S, Barter MJ, Elliott HR, et al. miR-324-5p is up regulated in end-stage osteoarthritis and regulates Indian Hedgehog signalling by differing mechanisms in human and mouse. Matrix Biol, 2019, 77: 87-100.
32. Fariyike B, Singleton Q, Hunter M, et al. Role of microRNA-141 in the aging musculoskeletal system: A current overview. Mech Ageing Dev, 2019, 178: 9-15.
33. Daoussis D, Liossis SN, Solomou EE, et al. Evidence that Dkk-1 is dysfunctional in ankylosing spondylitis. Arthritis Rheum, 2010, 62(1): 150-158.
34. Tang X, Lin J, Wang G, et al. MicroRNA-433-3p promotes osteoblast differentiation through targeting DKK1 expression. PLoS One, 2017, 12(6): e0179860.
35. Fan L, Fan J, Liu Y, et al. miR-450b promotes osteogenic differentiation in vitro and enhances bone formation in vivo by targeting BMP3. Stem Cells Dev, 2018, 27(9): 600-611.
36. Cai Q, Zheng P, Ma F, et al. MicroRNA-224 enhances the osteoblastic differentiation of hMSCs via Rac1. Cell Biochem Funct, 2019, 37(2): 62-71.
37. Wang H, Hu Z, Shi F, et al. Osteoblast-targeted delivery of miR-33-5p attenuates osteopenia development induced by mechanical unloading in mice. Cell Death Dis, 2018, 9(2): 170.
38. Kuang MJ, Xing F, Wang D, et al. CircUSP45 inhibited osteogenesis in glucocorticoid-induced osteonecrosis of femoral head by sponging miR-127-5p through PTEN/AKT signal pathway: Experimental studies. Biochem Biophys Res Commun, 2019, 509(1): 255-261.
39. Hu H, Zhao C, Zhang P, et al. miR-26b modulates OA induced BMSC osteogenesis through regulating GSK3β/β-catenin pathway. Exp Mol Pathol, 2019, 107: 158-164.
40. Han Y, Zhang K, Hong Y, et al. miR-342-3p promotes osteogenic differentiation via targeting ATF3. FEBS Lett, 2018, 592(24): 4051-4065.
41. Wiggins JF, Ruffino L, Kelnar K, et al. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res, 2010, 70(14): 5923-5930.
42. Janssen HL, Reesink HW, Lawitz EJ, et al. Treatment of HCV infection by targeting microRNA. N Engl J Med, 2013, 368(18): 1685-1694.
43. Trajkovski M, Hausser J, Soutschek J, et al. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature, 2011, 474(7353): 649-653.
44. Ottosen S, Parsley TB, Yang L, et al. In vitro antiviral activity and preclinical and clinical resistance profile of miravirsen, a novel anti-hepatitis C virus therapeutic targeting the human factor miR-122. Antimicrob Agents Chemother, 2015, 59(1): 599-608.
45. Cheng G. Circulating miRNAs: roles in cancer diagnosis, prognosis and therapy. Adv Drug Deliv Rev, 2015, 81: 75-93.
46. Feng Q, Zheng S, Zheng J. The emerging role of microRNAs in bone remodeling and its therapeutic implications for osteoporosis. Biosci Rep, 2018, 38(3): pii: BSR20180453.
47. Feichtinger X, Muschitz C, Heimel P, et al. Bone-related circulating microRNAs miR-29b-3p, miR-550a-3p, and miR-324-3p and their association to bone microstructure and histomorphometry. Sci Rep, 2018, 8(1): 4867.
48. Deng L, Hu G, Jin L, et al. Involvement of microRNA-23b in TNF-α-reduced BMSC osteogenic differentiation via targeting runx2. J Bone Miner Metab, 2018, 36(6): 648-660.
49. Wu ZH, Huang KH, Liu K, et al. DGCR5 induces osteogenic differentiation by up-regulating Runx2 through miR-30d-5p. Biochem Biophys Res Commun, 2018, 505(2): 426-431.
50. Wang Y, Li L, Moore BT, et al. MiR-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis. PLoS One, 2012, 7(4): e34641.
51. Seeliger C, Karpinski K, Haug AT, et al. Five freely circulating miRNAs and bone tissue miRNAs are associated with osteoporotic fractures. J Bone Miner Res, 2014, 29(8): 1718-1728.
52. Weilner S, Skalicky S, Salzer B, et al. Differentially circulating miRNAs after recent osteoporotic fractures can influence osteogenic differentiation. Bone, 2015, 79: 43-51.
53. Kocijan R, Muschitz C, Geiger E, et al. Circulating microRNA signatures in patients with idiopathic and postmenopausal osteoporosis and fragility fractures. J Clin Endocrinol Metab, 2016, 101(11): 4125-4134.
54. Mandourah AY, Ranganath L, Barraclough R, et al. Circulating microRNAs as potential diagnostic biomarkers for osteoporosis. Sci Rep, 2018, 8(1): 8421.
55. Yamasaki K, Nakasa T, Miyaki S, et al. Expression of microRNA‐146a in osteoarthritis cartilage. Arthritis & Rheumatism, 2009, 60(4): 1035-1041.
56. Kurowska-Stolarska M, Alivernini S, Ballantine LE, et al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc Natl Acad Sci U S A, 2011, 108(27): 11193-11198.
57. Xi Y, Jiang T, Wang W, et al. Long non-coding HCG18 promotes intervertebral disc degeneration by sponging miR-146a-5p and regulating TRAF6 expression. Sci Rep, 2017, 7(1): 13234.
58. García-Giménez JL, Rubio-Belmar PA, Peiró-Chova L, et al. Circulating miRNAs as diagnostic biomarkers for adolescent idiopathic scoliosis. Sci Rep, 2018, 8(1): 2646.
59. Kao GS, Tu YK, Sung PH, et al. MicroRNA-mediated interacting circuits predict hypoxia and inhibited osteogenesis of stem cells, and dysregulated angiogenesis are involved in osteonecrosis of the femoral head. Int Orthop, 2018, 42(7): 1605-1614.
60. Ou M, Zhang X, Dai Y, et al. Identification of potential microRNA-target pairs associated with osteopetrosis by deep sequencing, iTRAQ proteomics and bioinformatics. Eur J Hum Genet, 2014, 22(5): 625-632.
61. Roodman GD, Windle JJ. Paget disease of bone. J Clin Invest, 2005, 115(2): 200-208.
62. Bianciardi S, Merlotti D, Sebastiani G, et al. Micro-RNA expression profiling in Paget’s disease of bone. Bone Abstracts, 2016, 5: 452.
63. Nakasa T, Shibuya H, Nagata Y, et al. The inhibitory effect of microRNA-146a expression on bone destruction in collagen-induced arthritis. Arthritis Rheum, 2011, 63(6): 1582-1590.
64. Shibuya H, Nakasa T, Adachi N, et al. Overexpression of microRNA-223 in rheumatoid arthritis synovium controls osteoclast differentiation. Mod Rheumatol, 2013, 23(4): 674-685.
65. Jiang H, Zhang G, Wu JH, et al. Diverse roles of miR-29 in cancer (review). Oncol Rep, 2014, 31(4): 1509-1516.
66. Nugent M. MicroRNA function and dysregulation in bone tumors: the evidence to date. Cancer Manag Res, 2014, 6: 15-25.
67. Jones KB, Salah Z, Del Mare S, et al. miRNA signatures associate with pathogenesis and progression of osteosarcoma. Cancer Res, 2012, 72(7): 1865-1877.
68. Leonardo L, Laura P, Serena BM. miR-1 and miR-133b expression in canine osteosarcoma. Res Vet Sci, 2018, 117: 133-137.
69. Chuang TD, Panda H, Luo X, et al. miR-200c is aberrantly expressed in leiomyomas in an ethnic-dependent manner and targets ZEBs, VEGFA, TIMP2, and FBLN5. Endocr Relat Cancer, 2012, 19(4): 541-556.
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Chinese Journal of Reparative and Reconstructive Surgery

The regulatory role of microRNA in osteogenic differentiation of mesenchymal stem cells and its application as a therapeutic target and diagnostic tool in orthopedic diseases

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