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Calcified Tissue International

, Volume 105, Issue 3, pp 223–238 | Cite as

MicroRNAs Involved in the Regulation of Angiogenesis in Bone Regeneration

  • Sepanta Hosseinpour
  • Yan He
  • Ashwin Nanda
  • Qingsong YeEmail author
Review
  • 126 Downloads

Abstract

MicroRNAs (miRNAs) as a newly founded and thriving non-coding endogenous class of molecules which regulate many cellular pathways after transcription have been extensively investigated in regenerative medicine. In this systematic review, we sought to analyze miRNAs-mediated therapeutic approaches for influencing angiogenesis in bone tissue/bone regeneration. An electronic search in MEDLINE, Scopus, EMBASE, Cochrane library, web of science, and google scholar with no time limit were done on English publications. All types of original articles which a miRNA for angiogenesis in bone regeneration were included in our review. In the process of reviewing, we used PRISMA guideline and, SYRCLE’s and science in risk assessment and policy tools for analyzing risk of bias. Among 751 initial retrieved records, 16 studies met the inclusion criteria and were fully assessed in this review. 275 miRNAs, one miRNA 195~497 cluster, and one Cysteine-rich 61 short hairpin RNA were differentially expressed during bone regeneration with 24 predicted targets reported in these studies. Among these miRNAs, miRNA-7b, -9, -21, -26a, -27a, -210, -378, -195~497 cluster, -378 and -675 positively promoted both angiogenesis and osteogenesis, whereas miRNA-10a, -222 and -494 inhibited both processes. The most common target was vasculoendothelial growth factor-signaling pathway. Recent evidence has demonstrated that miRNAs actively participated in angio-osteogenic coupling that can improve their therapeutic potentials for the treatment of bone-related diseases and bone regeneration. However, there is still need for further research to unravel the exact mechanisms.

Keywords

MicroRNA AngiomiR Angiogenesis Bone angiogenesis Bone regeneration Bone tissue engineering 

Abbreviations

AMPK

AMP-activated protein kinase

HIF

Hypoxia-inducible factor

DKK2

Dickkopf2

DC-STAMP

Dendritic cell-specific transmembrane protein

Fbxw7

F-box WD-40 domain protein

NICD

Notch intercellular cytoplasmic domain

P4HTM

Prolyl 4-hydroxylase possessing a transmembrane domain

PKC

Protein kinase C-α

Runx2

Runt-related transcription factor 2

SFRP1

Secreted frizzled-related protein 1

TAK1

Transforming growth factor-activated kinase 1

VEGF

Vasculoendothelial growth factor

Notes

Acknowledgements

This project in part is funded by The University of Queensland International (UQI) Scholarship.

Author Contributions

SH and QY initiated this study. SH, QS and HY designed the review methodology. SH and AN prepared the initial draft of the study and made revisions. QY and YH critically reviewed included articles, and proofread the final draft of the manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors have no conflicts of interest related to this study.

Research Involving Human and Animal Participants

Due to the essence of this study, as a review article, there were not any human or animal participants, but we included the studies which all of them have ethical approval.

Informed Consent

This is not applicable for this study.

Supplementary material

223_2019_571_MOESM1_ESM.pdf (330 kb)
Supplementary material 1 (PDF 330 kb)

References

  1. 1.
    Zhu S, Yao F, Qiu H, Zhang G, Xu H, Xu J (2018) Coupling factors and exosomal packaging micro RNA s involved in the regulation of bone remodelling. Biol Rev 93:469–480CrossRefGoogle Scholar
  2. 2.
    Stegen S, van Gastel N, Carmeliet G (2015) Bringing new life to damaged bone: the importance of angiogenesis in bone repair and regeneration. Bone 70:19–27CrossRefGoogle Scholar
  3. 3.
    Götz W, Reichert C, Canullo L, Jäger A, Heinemann F (2012) Coupling of osteogenesis and angiogenesis in bone substitute healing—a brief overview. Ann Anat Anat Anz 194:171–173CrossRefGoogle Scholar
  4. 4.
    Riddle RC, Khatri R, Schipani E, Clemens TL (2009) Role of hypoxia-inducible factor-1α in angiogenic–osteogenic coupling. J Mol Med 87:583–590CrossRefGoogle Scholar
  5. 5.
    Einhorn T (1991) Mechanisms of fracture healing. Hosp Pract 26:41–45CrossRefGoogle Scholar
  6. 6.
    Hosseinpour S, Bastami F (2017) Critical-sized bone defects in mandible of canine model. Tissue Eng Part A 23:470–470CrossRefGoogle Scholar
  7. 7.
    Dimitriou R, Jones E, McGonagle D, Giannoudis PV (2011) Bone regeneration: current concepts and future directions. BMC Med 9:66CrossRefGoogle Scholar
  8. 8.
    Motamedian SR, Hosseinpour S, Ahsaie MG, Khojasteh A (2015) Smart scaffolds in bone tissue engineering: a systematic review of literature. World J Stem Cells 7:657CrossRefGoogle Scholar
  9. 9.
    De Witte T-M, Fratila-Apachitei LE, Zadpoor AA, Peppas NA (2018) Bone tissue engineering via growth factor delivery: from scaffolds to complex matrices. Regen Biomater 5:197–211CrossRefGoogle Scholar
  10. 10.
    Nakasa T, Yoshizuka M, Andry Usman M, Elbadry Mahmoud E, Ochi M (2015) MicroRNAs and bone regeneration. Curr Genom 16:441–452CrossRefGoogle Scholar
  11. 11.
    Xia M (2008) Great potential of microRNA in cancer stem cell. Mol Cancer J 4:79–89Google Scholar
  12. 12.
    Lu Y, Thomson JM, Wong HYF, Hammond SM, Hogan BL (2007) Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol 310:442–453CrossRefGoogle Scholar
  13. 13.
    Yau WWY, P-o Rujitanaroj, Lam L, Chew SY (2012) Directing stem cell fate by controlled RNA interference. Biomaterials 33:2608–2628CrossRefGoogle Scholar
  14. 14.
    Janssen HL, Reesink HW, Lawitz EJ, Zeuzem S, Rodriguez-Torres M, Patel K, van der Meer AJ, Patick AK, Chen A, Zhou Y (2013) Treatment of HCV infection by targeting microRNA. N Engl J Med 368:1685–1694CrossRefGoogle Scholar
  15. 15.
    Wang X, Guo B, Li Q, Peng J, Yang Z, Wang A, Li D, Hou Z, Lv K, Kan G (2013) miR-214 targets ATF4 to inhibit bone formation. Nat Med 19:93CrossRefGoogle Scholar
  16. 16.
    Murata K, Ito H, Yoshitomi H, Yamamoto K, Fukuda A, Yoshikawa J, Furu M, Ishikawa M, Shibuya H, Matsuda S (2014) Inhibition of miR-92a enhances fracture healing via promoting angiogenesis in a model of stabilized fracture in young mice. J Bone Miner Res 29:316–326CrossRefGoogle Scholar
  17. 17.
    Deng Y, Bi X, Zhou H, You Z, Wang Y, Gu P, Fan X (2014) Repair of critical-sized bone defects with anti-miR-31-expressing bone marrow stromal stem cells and poly(glycerol sebacate) scaffolds. Eur Cell Mater 27:13–24CrossRefGoogle Scholar
  18. 18.
    Deng Y, Zhou H, Zou D, Xie Q, Bi X, Gu P, Fan X (2013) The role of miR-31-modified adipose tissue-derived stem cells in repairing rat critical-sized calvarial defects. Biomaterials 34:6717–6728CrossRefGoogle Scholar
  19. 19.
    Tiwari A, Mukherjee B, Dixit M (2018) MicroRNA key to angiogenesis regulation: miRNA biology and therapy. Curr Cancer Drug Targets 18:266–277CrossRefGoogle Scholar
  20. 20.
    Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G (2006) MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108:3068–3071CrossRefGoogle Scholar
  21. 21.
    Gallach S, Calabuig-Fariñas S, Jantus-Lewintre E, Camps C (2014) MicroRNAs: promising new antiangiogenic targets in cancer. Biomed Res Int.  https://doi.org/10.1155/2014/878450 Google Scholar
  22. 22.
    Chen S, Xue Y, Wu X, Le C, Bhutkar A, Bell EL, Zhang F, Langer R, Sharp PA (2014) Global microRNA depletion suppresses tumor angiogenesis. Genes Dev 28:1054–1067CrossRefGoogle Scholar
  23. 23.
    Urbich C, Kuehbacher A, Dimmeler S (2008) Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79:581–588CrossRefGoogle Scholar
  24. 24.
    Moher D, Altman DG, Liberati A, Tetzlaff J (2011) PRISMA statement. Epidemiology 22:128CrossRefGoogle Scholar
  25. 25.
    Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW (2014) SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol 14:43CrossRefGoogle Scholar
  26. 26.
    Zhang B, Li Y, Yu Y, Zhao J, Ou Y, Chao Y, Yang B, Yu X (2018) MicroRNA-378 promotes osteogenesis-angiogenesis coupling in BMMSCs for potential bone regeneration. Anal Cell Pathol.  https://doi.org/10.1155/2018/8402390 Google Scholar
  27. 27.
    Costa V, Raimondi L, Conigliaro A, Salamanna F, Carina V, De Luca A, Bellavia D, Alessandro R, Fini M, Giavaresi G (2017) Hypoxia-inducible factor 1Α may regulate the commitment of mesenchymal stromal cells toward angio-osteogenesis by mirna-675-5P. Cytotherapy 19:1412–1425CrossRefGoogle Scholar
  28. 28.
    Qu J, Lu D, Guo H, Miao W, Wu G, Zhou M (2016) MicroRNA-9 regulates osteoblast differentiation and angiogenesis via the AMPK signaling pathway. Mol Cell Biochem 411:23–33CrossRefGoogle Scholar
  29. 29.
    Liu X-D, Cai F, Liu L, Zhang Y, Yang A-L (2015) MicroRNA-210 is involved in the regulation of postmenopausal osteoporosis through promotion of VEGF expression and osteoblast differentiation. Biol Chem 396:339–347CrossRefGoogle Scholar
  30. 30.
    Li J, Zhang Y, Zhao Q, Wang J, He X (2015) MicroRNA-10a influences osteoblast differentiation and angiogenesis by regulating β-catenin expression. Cell Physiol Biochem 37:2194–2208CrossRefGoogle Scholar
  31. 31.
    Almeida MI, Silva AM, Vasconcelos DM, Almeida CR, Caires H, Pinto MT, Calin GA, Santos SG, Barbosa MA (2016) miR-195 in human primary mesenchymal stromal/stem cells regulates proliferation, osteogenesis and paracrine effect on angiogenesis. Oncotarget 7:7CrossRefGoogle Scholar
  32. 32.
    Wu X, Gu Q, Chen X, Mi W, Wu T, Huang H (2019) MiR-27a targets DKK2 and SFRP1 to promote reosseointegration in the regenerative treatment of peri-implantitis. J Bone Miner Res 34:123–134CrossRefGoogle Scholar
  33. 33.
    Dou C, Ding N, Luo F, Hou T, Cao Z, Bai Y, Liu C, Xu J, Dong S (2018) Graphene-based microRNA transfection blocks preosteoclast fusion to increase bone formation and vascularization. Adv Sci 5:1700578CrossRefGoogle Scholar
  34. 34.
    Geng Z, Wang X, Zhao J, Li Z, Ma L, Zhu S, Liang Y, Cui Z, He H, Yang X (2018) The synergistic effect of strontium-substituted hydroxyapatite and microRNA-21 on improving bone remodeling and osseointegration. Biomater Sci 6:2694–2703CrossRefGoogle Scholar
  35. 35.
    Zha X, Sun B, Zhang R, Li C, Yan Z, Chen J (2018) Regulatory effect of microRNA-34a on osteogenesis and angiogenesis in glucocorticoid-induced osteonecrosis of the femoral head. J Orthop Res 36:417–424Google Scholar
  36. 36.
    Chen CY, Su CM, Hsu CJ, Huang CC, Wang SW, Liu SC, Chen WC, Fuh LJ, Tang CH (2017) CCN1 promotes VEGF production in osteoblasts and induces endothelial progenitor cell angiogenesis by inhibiting miR-126 expression in rheumatoid arthritis. J Bone Miner Res 32:34–45CrossRefGoogle Scholar
  37. 37.
    Yang M, Li C-J, Sun X, Guo Q, Xiao Y, Su T, Tu M-L, Peng H, Lu Q, Liu Q (2017) MiR-497 ∼ 195 cluster regulates angiogenesis during coupling with osteogenesis by maintaining endothelial Notch and HIF-1α activity. Nat Commun 8:16003CrossRefGoogle Scholar
  38. 38.
    He B, Zhang Z-K, Liu J, He Y-X, Tang T, Li J, Guo B-S, Lu A-P, Zhang B-T, Zhang G (2016) Bioinformatics and microarray analysis of miRNAs in aged female mice model implied new molecular mechanisms for impaired fracture healing. Int J Mol Sci 17:1260CrossRefGoogle Scholar
  39. 39.
    Yoshizuka M, Nakasa T, Kawanishi Y, Hachisuka S, Furuta T, Miyaki S, Adachi N, Ochi M (2016) Inhibition of microRNA-222 expression accelerates bone healing with enhancement of osteogenesis, chondrogenesis, and angiogenesis in a rat refractory fracture model. J Orthop Sci 21:852–858CrossRefGoogle Scholar
  40. 40.
    Li Y, Fan L, Liu S, Liu W, Zhang H, Zhou T, Wu D, Yang P, Shen L, Chen J (2013) The promotion of bone regeneration through positive regulation of angiogenic–osteogenic coupling using microRNA-26a. Biomaterials 34:5048–5058CrossRefGoogle Scholar
  41. 41.
    Cai C, Xie Y, Chen X, Liu H, Zhou Y, Zou H, Liu D, Zhao Y, Kong X, Liu P (2017) PLGA-based dual targeted nanoparticles enhance miRNA transfection efficiency in hepatic carcinoma. Sci Rep 7:46250CrossRefGoogle Scholar
  42. 42.
    Fang Z, Rajewsky N (2011) The impact of miRNA target sites in coding sequences and in 3′ UTRs. PLoS ONE 6:e18067CrossRefGoogle Scholar
  43. 43.
    Roux J, Gonzalez-Porta M, Robinson-Rechavi M (2012) Comparative analysis of human and mouse expression data illuminates tissue-specific evolutionary patterns of miRNAs. Nucleic Acids Res 40:5890–5900CrossRefGoogle Scholar
  44. 44.
    Güller I, McNaughton S, Crowley T, Gilsanz V, Kajimura S, Watt M, Russell AP (2015) Comparative analysis of microRNA expression in mouse and human brown adipose tissue. BMC Genom 16:820CrossRefGoogle Scholar
  45. 45.
    Clark EA, Kalomoiris S, Nolta JA, Fierro FA (2014) Concise review: microRNA function in multipotent mesenchymal stromal cells. Stem cells 32:1074–1082CrossRefGoogle Scholar
  46. 46.
    Dong S, Yang B, Guo H, Kang F (2012) MicroRNAs regulate osteogenesis and chondrogenesis. Biochem Biophys Res Commun 418:587–591CrossRefGoogle Scholar
  47. 47.
    Anand S, Cheresh DA (2011) Emerging role of micro-RNAs in the regulation of angiogenesis. Genes Cancer 2:1134–1138CrossRefGoogle Scholar
  48. 48.
    Yan B, Wang Z-H, Zhu C-D, Guo J-T, Zhao J-L (2014) MicroRNA repertoire for functional genome research in tilapia identified by deep sequencing. Mol Biol Rep 41:4953–4963CrossRefGoogle Scholar
  49. 49.
    Dou C, Zhang C, Kang F, Yang X, Jiang H, Bai Y, Xiang J, Xu J, Dong S (2014) MiR-7b directly targets DC-STAMP causing suppression of NFATc1 and c-Fos signaling during osteoclast fusion and differentiation. Biochim Biophys Acta Gene Regulat Mech 1839:1084–1096CrossRefGoogle Scholar
  50. 50.
    Brandenburger T, Castoldi M, Brendel M, Grievink H, Schlösser L, Werdehausen R, Bauer I, Hermanns H (2012) Expression of spinal cord microRNAs in a rat model of chronic neuropathic pain. Neurosci Lett 506:281–286CrossRefGoogle Scholar
  51. 51.
    Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, Oeh J, Modrusan Z, Bais C, Sampath D (2012) Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J 31:3513–3523CrossRefGoogle Scholar
  52. 52.
    Zhao X, Zmijewski JW, Lorne E, Liu G, Park YJ, Tsuruta Y, Abraham E (2008) Activation of AMPK attenuates neutrophil proinflammatory activity and decreases the severity of acute lung injury. Am J Physiol Lung Cell Mol Physiol 295:497–504CrossRefGoogle Scholar
  53. 53.
    Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Sugimoto T (2008) Metformin enhances the differentiation and mineralization of osteoblastic MC3T3-E1 cells via AMP kinase activation as well as eNOS and BMP-2 expression. Biochem Biophys Res Commun 375:414–419CrossRefGoogle Scholar
  54. 54.
    Li X, Guo L, Liu Y, Su Y, Xie Y, Du J, Zhou J, Ding G, Wang H, Bai Y (2017) MicroRNA-21 promotes osteogenesis of bone marrow mesenchymal stem cells via the Smad7-Smad1/5/8-Runx2 pathway. Biochem Biophys Res Commun 493:928–933CrossRefGoogle Scholar
  55. 55.
    Sabatel C, Malvaux L, Bovy N, Deroanne C, Lambert V, Gonzalez M-LA, Colige A, Rakic J-M, Noël A, Martial JA (2011) MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothelial cells. PLoS ONE 6:e16979CrossRefGoogle Scholar
  56. 56.
    Hu C-H, Sui B-D, Du F-Y, Shuai Y, Zheng C-X, Zhao P, Yu X-R, Jin Y (2017) miR-21 deficiency inhibits osteoclast function and prevents bone loss in mice. Sci Rep 7:43191CrossRefGoogle Scholar
  57. 57.
    Lian JB, Stein GS, Javed A, Van Wijnen AJ, Stein JL, Montecino M, Hassan MQ, Gaur T, Lengner CJ, Young DW (2006) Networks and hubs for the transcriptional control of osteoblastogenesis. Rev Endocr Metab Disord 7:1–16CrossRefGoogle Scholar
  58. 58.
    Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97:512–523CrossRefGoogle Scholar
  59. 59.
    Su X, Liao L, Shuai Y, Jing H, Liu S, Zhou H, Liu Y, Jin Y (2015) MiR-26a functions oppositely in osteogenic differentiation of BMSCs and ADSCs depending on distinct activation and roles of Wnt and BMP signaling pathway. Cell Death Dis 6:e1851CrossRefGoogle Scholar
  60. 60.
    Icli B, Wara A, Moslehi J, Sun X, Plovie E, Cahill M, Marchini JF, Schissler A, Padera RF, Shi J (2013) MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling. Circ Res 113:1231–1241CrossRefGoogle Scholar
  61. 61.
    Qin W, Yang F, Deng R, Li D, Song Z, Tian Y, Wang R, Ling J, Lin Z (2012) Smad 1/5 is involved in bone morphogenetic protein-2-induced odontoblastic differentiation in human dental pulp cells. J Endod 38:66–71CrossRefGoogle Scholar
  62. 62.
    Min J-K, Park H, Choi H-J, Kim Y, Pyun B-J, Agrawal V, Song B-W, Jeon J, Maeng Y-S, Rho S-S (2011) The WNT antagonist Dickkopf2 promotes angiogenesis in rodent and human endothelial cells. J Clin Investig 121:1882–1893CrossRefGoogle Scholar
  63. 63.
    Petković A, Matić S, Stamatović N, Vojvodić D, Todorović T, Lazić Z, Kozomara R (2010) Proinflammatory cytokines (IL-1β and TNF-α) and chemokines (IL-8 and MIP-1α) as markers of peri-implant tissue condition. Int J Oral Maxillofac Surg 39:478–485CrossRefGoogle Scholar
  64. 64.
    Mo J, Zhang D, Yang R (2016) MicroRNA-195 regulates proliferation, migration, angiogenesis and autophagy of endothelial progenitor cells by targeting GABARAPL1. Biosci Rep 36:e00396CrossRefGoogle Scholar
  65. 65.
    Grunhagen J, Bhushan R, Degenkolbe E, Jager M, Knaus P, Mundlos S, Robinson PN, Ott CE (2015) MiR-497 approximately 195 cluster microRNAs regulate osteoblast differentiation by targeting BMP signaling. J Bone Miner Res 30:796–808CrossRefGoogle Scholar
  66. 66.
    Yang M, Li CJ, Sun X, Guo Q, Xiao Y, Su T, Tu ML, Peng H, Lu Q, Liu Q, He HB, Jiang TJ, Lei MX, Wan M, Cao X, Luo XH (2017) MiR-497 approximately 195 cluster regulates angiogenesis during coupling with osteogenesis by maintaining endothelial Notch and HIF-1alpha activity. Nat Commun 8:16003CrossRefGoogle Scholar
  67. 67.
    Almeida MI, Silva AM, Vasconcelos DM, Almeida CR, Caires H, Pinto MT, Calin GA, Santos SG, Barbosa MA (2016) miR-195 in human primary mesenchymal stromal/stem cells regulates proliferation, osteogenesis and paracrine effect on angiogenesis. Oncotarget 7:7–22CrossRefGoogle Scholar
  68. 68.
    Yamasaki K, Nakasa T, Miyaki S, Yamasaki T, Yasunaga Y, Ochi M (2012) Angiogenic microRNA-210 is present in cells surrounding osteonecrosis. J Orthop Res 30:1263–1270CrossRefGoogle Scholar
  69. 69.
    Mizuno Y, Tokuzawa Y, Ninomiya Y, Yagi K, Yatsuka-Kanesaki Y, Suda T, Fukuda T, Katagiri T, Kondoh Y, Amemiya T, Tashiro H, Okazaki Y (2009) miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b. FEBS Lett 583:2263–2268CrossRefGoogle Scholar
  70. 70.
    Lee DY, Deng Z, Wang CH, Yang BB (2007) MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc Natl Acad Sci USA 104:20350–20355CrossRefGoogle Scholar
  71. 71.
    You L, Gu W, Chen L, Pan L, Chen J, Peng Y (2014) MiR-378 overexpression attenuates high glucose-suppressed osteogenic differentiation through targeting CASP3 and activating PI3 K/Akt signaling pathway. Int J Clin Exp Pathol 7:7249–7261Google Scholar
  72. 72.
    Zhang B, Li Y, Yu Y, Zhao J, Ou Y, Chao Y, Yang B, Yu X (2018) MicroRNA-378 promotes osteogenesis-angiogenesis coupling in BMMSCs for potential bone regeneration. Anal Cell Pathol 2018:8402390CrossRefGoogle Scholar
  73. 73.
    Costa V, Raimondi L, Conigliaro A, Salamanna F, Carina V, De Luca A, Bellavia D, Alessandro R, Fini M, Giavaresi G (2017) Hypoxia-inducible factor 1Alpha may regulate the commitment of mesenchymal stromal cells toward angio-osteogenesis by mirna-675-5P. Cytotherapy 19:1412–1425CrossRefGoogle Scholar
  74. 74.
    Aguado-Fraile E, Ramos E, Conde E, Rodríguez M, Liaño F, García-Bermejo ML (2013) MicroRNAs in the kidney: novel biomarkers of acute kidney injury. Nefrología (English Edition) 33:826–834Google Scholar
  75. 75.
    Tang H (2013) miR-10a regulates epithelial-mesenchymal transition and adhesion and angiogenesis in hepatoma. In: Federation of American Societies for Experimental Biology, p lb153-lb153Google Scholar
  76. 76.
    Day TF, Guo X, Garrett-Beal L, Yang Y (2005) Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 8:739–750CrossRefGoogle Scholar
  77. 77.
    Sun W, Ma Y, Chen P, Wang D (2015) MicroRNA-10a silencing reverses cisplatin resistance in the A549/cisplatin human lung cancer cell line via the transforming growth factor-β/Smad2/STAT3/STAT5 pathway. Mol Med Rep 11:3854–3859CrossRefGoogle Scholar
  78. 78.
    Yoshizuka M, Nakasa T, Kawanishi Y, Hachisuka S, Furuta T, Miyaki S, Adachi N, Ochi M (2016) Inhibition of microRNA-222 expression accelerates bone healing with enhancement of osteogenesis, chondrogenesis, and angiogenesis in a rat refractory fracture model. J Orthop Sci 21:852–858CrossRefGoogle Scholar
  79. 79.
    Yu F, Cui Y, Zhou X, Zhang X, Han J (2011) Osteogenic differentiation of human ligament fibroblasts induced by conditioned medium of osteoclast-like cells. BioSci Trends 5:46–51CrossRefGoogle Scholar
  80. 80.
    Welten SM, Bastiaansen AJ, de Jong RC, de Vries MR, Peters EA, Boonstra MC, Sheikh SP, La Monica N, Kandimalla ER, Quax PH, Nossent AY (2014) Inhibition of 14q32 MicroRNAs miR-329, miR-487b, miR-494, and miR-495 increases neovascularization and blood flow recovery after ischemia. Circ Res 115:696–708CrossRefGoogle Scholar
  81. 81.
    He B, Zhang ZK, Liu J, He YX, Tang T, Li J, Guo BS, Lu AP, Zhang BT, Zhang G (2016) Bioinformatics and microarray analysis of miRNAs in aged female mice model implied new molecular mechanisms for impaired fracture healing. Int J Mol Sci 17:1260CrossRefGoogle Scholar
  82. 82.
    Cash DE, Bock CB, Schughart K, Linney E, Underhill TM (1997) Retinoic acid receptor alpha function in vertebrate limb skeletogenesis: a modulator of chondrogenesis. J Cell Biol 136:445–457CrossRefGoogle Scholar
  83. 83.
    Wei J, Shi Y, Zheng L, Zhou B, Inose H, Wang J, Guo XE, Grosschedl R, Karsenty G (2012) miR-34 s inhibit osteoblast proliferation and differentiation in the mouse by targeting SATB2. J Cell Biol 197:509–521CrossRefGoogle Scholar
  84. 84.
    Chen L, HolmstrØm K, Qiu W, Ditzel N, Shi K, Hokland L, Kassem M (2014) MicroRNA-34a inhibits osteoblast differentiation and in vivo bone formation of human stromal stem cells. Stem Cells 32:902–912CrossRefGoogle Scholar
  85. 85.
    Chen L, Holmstrom K, Qiu W, Ditzel N, Shi K, Hokland L, Kassem M (2014) MicroRNA-34a inhibits osteoblast differentiation and in vivo bone formation of human stromal stem cells. Stem Cells 32:902–912CrossRefGoogle Scholar
  86. 86.
    Lu X, Deng M, He H, Zeng D, Zhang W (2013) miR-125b regulates osteogenic differentiation of human bone marrow mesenchymal stem cells by targeting Smad4. J Cent South Univ Med Sci 38:341–346Google Scholar
  87. 87.
    Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132:875–886CrossRefGoogle Scholar
  88. 88.
    Mao G, Wu P, Zhang Z, Zhang Z, Liao W, Li Y, Kang Y (2017) MicroRNA-92a-3p regulates aggrecanase-1 and aggrecanase-2 expression in chondrogenesis and IL-1beta-induced catabolism in human articular chondrocytes. Cell Physiol Biochem 44:38–52CrossRefGoogle Scholar
  89. 89.
    Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K, Chavakis E, Potente M, Tjwa M, Urbich C, Zeiher AM, Dimmeler S (2009) MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324:1710–1713CrossRefGoogle Scholar
  90. 90.
    Chen CY, Su CM, Hsu CJ, Huang CC, Wang SW, Liu SC, Chen WC, Fuh LJ, Tang CH (2017) CCN1 promotes VEGF production in osteoblasts and induces endothelial progenitor cell angiogenesis by inhibiting miR-126 expression in rheumatoid arthritis. J Bone Miner Res 32:34–45CrossRefGoogle Scholar
  91. 91.
    Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ (2008) MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 105:1516–1521CrossRefGoogle Scholar
  92. 92.
    Marzi MJ, Ghini F, Cerruti B, De Pretis S, Bonetti P, Giacomelli C, Gorski MM, Kress T, Pelizzola M, Muller H (2016) Degradation dynamics of microRNAs revealed by a novel pulse-chase approach. Genome Res 26:554–565CrossRefGoogle Scholar
  93. 93.
    Curtin CM, Castaño IM, O’brien FJ (2018) Scaffold-based microRNA therapies in regenerative medicine and cancer. Adv Healthc Mater 7:1700695CrossRefGoogle Scholar
  94. 94.
    Laufs S, Guenechea G, Gonzalez-Murillo A, Nagy KZ, Lozano ML, del Val C, Jonnakuty S, Hotz-Wagenblatt A, Zeller WJ, Bueren JA (2006) Lentiviral vector integration sites in human NOD/SCID repopulating cells. J Gene Med 8:1197–1207CrossRefGoogle Scholar
  95. 95.
    Kulkarni M, Greiser U, O’Brien T, Pandit A (2010) Liposomal gene delivery mediated by tissue-engineered scaffolds. Trends Biotechnol 28:28–36CrossRefGoogle Scholar
  96. 96.
    Putnam D, Gentry CA, Pack DW, Langer R (2001) Polymer-based gene delivery with low cytotoxicity by a unique balance of side-chain termini. Proc Natl Acad Sci USA 98:1200–1205CrossRefGoogle Scholar
  97. 97.
    Liang C, Guo B, Wu H, Shao N, Li D, Liu J, Dang L, Wang C, Li H, Li S (2015) Aptamer-functionalized lipid nanoparticles targeting osteoblasts as a novel RNA interference-based bone anabolic strategy. Nat Med 21:288CrossRefGoogle Scholar
  98. 98.
    Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, Obad S, Lindholm M, Hedtjärn M, Hansen HF, Berger U (2008) LNA-mediated microRNA silencing in non-human primates. Nature 452:896CrossRefGoogle Scholar
  99. 99.
    Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36:D149–153CrossRefGoogle Scholar
  100. 100.
    Wang FS, Chuang PC, Lin CL, Chen MW, Ke HJ, Chang YH, Chen YS, Wu SL, Ko JY (2013) MicroRNA-29a protects against glucocorticoid-induced bone loss and fragility in rats by orchestrating bone acquisition and resorption. Arthritis Rheum 65:1530–1540CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of DentistryThe University of QueenslandBrisbaneAustralia

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