Research progress of miRNA regulation in differentiation of adipose-derived stem cells_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHOU Lanting ^1,2 , FENG Yanting ² , DAI Jingxing ² ,  OUYANG Jun ²

1. Medical College, Hubei University of Arts and Science, Xiangyang Hubei, 441053, P.R.China;
2. Department of Anatomy, Southern Medical University, Guangzhou Guangdong, 510515, P.R.China;

Corresponding author：

OUYANG Jun, Email: jouyang@smu.edu.cn

Keywords：

miRNA; adipose-derived stem cells; multipotential differentiation

DOI：

10.7507/1002-1892.201706076

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To review the research progress of miRNA regulation in the differentiation of adipose-derived stem cells (ADSCs). Methods The recent literature associated with miRNAs and differentiation of ADSCs was reviewed. The regulatory mechanism was analyzed in detail and summarized. Results The results indicate that the expression of miRNAs changes during differentiation of ADSCs. In addition, miRNAs regulate the differentiation of ADSCs into adipocytes, osteoblasts, chondrocytes, neurons, and hepatocytes by regulating the signaling pathways involved in cell differentiation. Conclusion Through controlling the differentiation of ADSCs by miRNAs, the suitable seed cell for tissue engineering can be established. The review will provide a theoretical basis for molecular targeted therapy and stem cell therapy in clinic.

Citation： ZHOU Lanting, FENG Yanting, DAI Jingxing, OUYANG Jun. Research progress of miRNA regulation in differentiation of adipose-derived stem cells. Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(12): 1506-1511. doi: 10.7507/1002-1892.201706076 Copy

1.	Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 2001, 7(2): 211-228.
2.	Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell, 2002, 13(12): 4279-4295.
3.	Dai R, Wang Z, Samanipour R, et al. Adipose-Derived Stem Cells for Tissue Engineering and Regenerative Medicine Applications. Stem Cells International, 2016, 2016: 6737345.
4.	Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet, 2010, 11(9): 597-610.
5.	Li N, Long B, Han W, et al. microRNAs: important regulators of stem cells. Stem Cell Res Ther, 2017, 8(1): 110.
6.	Kim DY, Sung JH. Regulatory role of microRNAs in the proliferation and differentiation of adipose-derived stem cells. Histol Histopathol, 2017, 32(1): 1-10.
7.	Uzbas F, May ID, Parisi AM, et al. Molecular physiognomies and applications of adipose-derived stem cells. Stem Cell Rev, 2015, 11(2): 298-308.
8.	Chen J, Deng S, Zhang S, et al. The role of miRNAs in the differentiation of adipose-derived stem cells. Curr Stem Cell Res Ther, 2014, 9(3): 268-279.
9.	Shi C, Huang F, Gu X, et al. Adipogenic miRNA and meta-signature miRNAs involved in human adipocyte differentiation and obesity. Oncotarget, 2016, 7(26): 40830-40845.
10.	Tang YF, Zhang Y, Li XY, et al. Expression of miR-31, miR-125b-5p, and miR-326 in the adipogenic differentiation process of adipose-derived stem cells. OMICS, 2009, 13(4): 331-336.
11.	Zaragosi LE, Wdziekonski B, Brigand KL, et al. Small RNA sequencing reveals miR-642a-3p as a novel adipocyte-specific microRNA and miR-30 as a key regulator of human adipogenesis. Genome Biol, 2011, 12(7): R64.
12.	Chen L, Cui J, Hou J, et al. A novel negative regulator of adipogenesis: microRNA-363. Stem Cells, 2014, 32(2): 510-520.
13.	Kim YJ, Hwang SJ, Bae YC, et al. MiR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells, 2009, 27(12): 3093-3102.
14.	Karbiener M, Neuhold C, Opriessnig P, et al. MicroRNA-30c promotes human adipocyte differentiation and co-represses PAI-1 and ALK2. RNA Biol, 2011, 8(5): 850-860.
15.	Chen K, He H, Xie Y, et al. miR-125a-3p and miR-483-5p promote adipogenesis via suppressing the RhoA/ROCK1/ERK1/2 pathway in multiple symmetric lipomatosis. Sci Rep, 2015, 5: 11909.
16.	Shi C, Zhang M, Tong M, et al. miR-148a is Associated with Obesity and Modulates Adipocyte Differentiation of Mesenchymal Stem Cells through Wnt Signaling. Sci Rep, 2015, 5: 9930.
17.	He H, Chen K, Wang F, et al. miR-204-5p promotes the adipogenic differentiation of human adipose-derived mesenchymal stem cells by modulating DVL3 expression and suppressing Wnt/beta-catenin signaling. Int J Mol Med, 2015, 35(6): 1587-1595.
18.	Yang Z, Bian C, Zhou H, et al. MicroRNA hsa-miR-138 inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells through adenovirus EID-1. Stem Cells Dev, 2011, 20(2): 259-267.
19.	Chen L, Hou J, Ye L, et al. MicroRNA-143 regulates adipogenesis by modulating the MAP2K5-ERK5 signaling. Sci Rep, 2014, 4: 3819.
20.	Lee EK, Lee MJ, Abdelmohsen K, et al. miR-130 suppresses adipogenesis by inhibiting peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol, 2011, 31(4): 626-638.
21.	Kang T, Lu W, Xu W, et al. MicroRNA-27 (miR-27) targets prohibitin and impairs adipocyte differentiation and mitochondrial function in human adipose-derived stem cells. J Biol Chem, 2013, 288(48): 34394-34402.
22.	Karbiener M, Fischer C, Nowitsch S, et al. microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma. Biochem Biophys Res Commun, 2009, 390(2): 247-251.
23.	Chen L, Chen Y, Zhang S, et al. MiR-540 as a novel adipogenic inhibitor impairs adipogenesis via suppression of PPARgamma. J Cell Biochem, 2015, 116(6): 969-976.
24.	Yang L, Shi CM, Chen L, et al. The biological effects of hsa-miR-1908 in human adipocytes. Mol Biol Rep, 2015, 42(5): 927-935.
25.	Li H, Li T, Wang S, et al. miR-17-5p and miR-106a are involved in the balance between osteogenic and adipogenic differentiation of adipose-derived mesenchymal stem cells. Stem Cell Res, 2013, 10(3): 313-324.
26.	Zhang ZJ, Zhang H, Kang Y, et al. miRNA expression profile during osteogenic differentiation of human adipose-derived stem cells. J Cell Biochem, 2012, 113(3): 888-898.
27.	Zhang WB, Zhong WJ, Wang L. A signal-amplification circuit between miR-218 and Wnt/beta-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation. Bone, 2014, 58: 59-66.
28.	Kim YJ, Bae SW, Yu SS, et al. miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res, 2009, 24(5): 816-825.
29.	Fan C, Jia L, Zheng Y, et al. MiR-34a Promotes Osteogenic Differentiation of Human Adipose-Derived Stem Cells via the RBP2/NOTCH1/CYCLIN D1 Coregulatory Network. Stem Cell Reports, 2016, 7(2): 236-248.
30.	Chen S, Zheng Y, Zhang S, et al. Promotion Effects of miR-375 on the Osteogenic Differentiation of Human Adipose-Derived Mesenchymal Stem Cells. Stem Cell Reports, 2017, 8(3): 773-786.
31.	Liao YH, Chang YH, Sung LY, et al. Osteogenic differentiation of adipose-derived stem cells and calvarial defect repair using baculovirus-mediated co-expression of BMP-2 and miR-148b. Biomaterials, 2014, 35(18): 4901-4910.
32.	Xie Q, Wei W, Ruan J, et al. Effects of miR-146a on the osteogenesis of adipose-derived mesenchymal stem cells and bone regeneration. Sci Rep, 2017, 7: 42840.
33.	Li H, Li T, Fan J, et al. miR-216a rescues dexamethasone suppression of osteogenesis, promotes osteoblast differentiation and enhances bone formation, by regulating c-Cbl-mediated PI3K/AKT pathway. Cell Death Differ, 2015, 22(12): 1935-1945.
34.	Hoseinzadeh S, Atashi A, Soleimani M, et al. MiR-221-inhibited adipose tissue-derived mesenchymal stem cells bioengineered in a nano-hydroxy apatite scaffold. In Vitro Cell Dev Biol Anim, 2016, 52(4): 479-487.
35.	Zeng Y, Qu X, Li H, et al. MicroRNA-100 regulates osteogenic differentiation of human adipose-derived mesenchymal stem cells by targeting BMPR2. FEBS Lett, 2012, 586(16): 2375-2381.
36.	Li J, Hu C, Han L, et al. MiR-154-5p regulates osteogenic differentiation of adipose-derived mesenchymal stem cells under tensile stress through the Wnt/PCP pathway by targeting Wnt11. Bone, 2015, 78: 130-141.
37.	Li S, Hu C, Li J, et al. Effect of miR-26a-5p on the Wnt/Ca(2+) Pathway and Osteogenic Differentiation of Mouse Adipose-Derived Mesenchymal Stem Cells. Calcif Tissue Int, 2016, 99(2): 174-186.
38.	Luzi E, Marini F, Sala SC, et al. Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res, 2008, 23(2): 287-295.
39.	Wang Z, Xie Q, Yu Z, et al. A regulatory loop containing miR-26a, GSK3beta and C/EBPalpha regulates the osteogenesis of human adipose-derived mesenchymal stem cells. Sci Rep, 2015, 5: 15280.
40.	Wang Z, Zhang D, Hu Z, et al. MicroRNA-26a-modified adipose-derived stem cells incorporated with a porous hydroxyapatite scaffold improve the repair of bone defects. Mol Med Rep, 2015, 12(3): 3345-3350.
41.	Huang S, Wang S, Bian C, et al. Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev, 2012, 21(13): 2531-2540.
42.	Zhang Z, Kang Y, Zhang Z, et al. Expression of microRNAs during chondrogenesis of human adipose-derived stem cells. Osteoarthritis Cartilage, 2012, 20(12): 1638-1646.
43.	Yang Z, Hao J, Hu ZM. MicroRNA expression profiles in human adipose-derived stem cells during chondrogenic differentiation. Int J Mol Med, 2015, 35(3): 579-586.
44.	Hou C, Yang Z, Kang Y, et al. MiR-193b regulates early chondrogenesis by inhibiting the TGF-beta2 signaling pathway. FEBS Lett, 2015, 589(9): 1040-1047.
45.	Hou C, Zhang Z, Zhang Z, et al. Presence and function of microRNA-92a in chondrogenic ATDC5 and adipose-derived mesenchymal stem cells. Mol Med Rep, 2015, 12(4): 4877-4886.
46.	Xu J, Kang Y, Liao WM, et al. MiR-194 regulates chondrogenic differentiation of human adipose-derived stem cells by targeting Sox5. PLoS One, 2012, 7(3): e31861.
47.	Cho JA, Park H, Lim EH, et al. MicroRNA expression profiling in neurogenesis of adipose tissue-derived stem cells. J Genet, 2011, 90(1): 81-93.
48.	Ning H, Huang YC, Banie L, et al. MicroRNA regulation of neuron-like differentiation of adipose tissue-derived stem cells. Differentiation, 2009, 78(5): 253-259.
49.	Mondanizadeh M, Arefian E, Mosayebi G, et al. MicroRNA-124 regulates neuronal differentiation of mesenchymal stem cells by targeting Sp1 mRNA. J Cell Biochem, 2015, 116(6): 943-953.
50.	Wang Y, Wang D, Guo D. MiR-124 Promote Neurogenic Transdifferentiation of Adipose Derived Mesenchymal Stromal Cells Partly through RhoA/ROCK1, but Not ROCK2 Signaling Pathway. PLoS One, 2016, 11(1): e146646.
51.	Hu F, Sun B, Xu P, et al. MiR-218 Induces Neuronal Differentiation of ASCs in a Temporally Sequential Manner with Fibroblast Growth Factor by Regulation of the Wnt Signaling Pathway. Sci Rep, 2017, 7: 39427.
52.	He X, Ao Q, Wei Y, et al. Transplantation of miRNA-34a overexpressing adipose-derived stem cell enhances rat nerve regeneration. Wound Repair Regen, 2016, 24(3): 542-550.
53.	Alizadeh E, Akbarzadeh A, Eslaminejad MB, et al. Up regulation of liver-enriched transcription factors HNF4a and HNF6 and liver-specific microRNA (miR-122) by inhibition of let-7b in mesenchymal stem cells. Chem Biol Drug Des, 2015, 85(3): 268-279.
54.	Davoodian N, Lotfi AS, Soleimani M, et al. Let-7f microRNA negatively regulates hepatic differentiation of human adipose tissue-derived stem cells. J Physiol Biochem, 2014, 70(3): 781-789.
55.	Davoodian N, Lotfi AS, Soleimani M, et al. MicroRNA-122 overexpression promotes hepatic differentiation of human adipose tissue-derived stem cells. J Cell Biochem, 2014, 115(9): 1582-1593.
56.	Chen KD, Huang KT, Lin CC, et al. MicroRNA-27b Enhances the Hepatic Regenerative Properties of Adipose-Derived Mesenchymal Stem Cells. Mol Ther Nucleic Acids, 2016, 5: e285.
57.	Chen KD, Hsu LW, Goto S, et al. Regulation of heme oxygenase 1 expression by miR-27b with stem cell therapy for liver regeneration in rats. Transplant Proc, 2014, 46(4): 1198-1200.
58.	Aji K, Zhang Y, Aimaiti A, et al. MicroRNA-145 regulates the differentiation of human adipose-derived stem cells to smooth muscle cells via targeting Kruppel-like factor 4. Mol Med Rep, 2017, 15(6): 3787-3795.
59.	Kalinina N, Klink G, Glukhanyuk E, et al. miR-92a regulates angiogenic activity of adipose-derived mesenchymal stromal cells. Exp Cell Res, 2015, 339(1): 61-66.
60.	Shin KK, Lee AL, Kim JY, et al. miR-21 modulates tumor outgrowth induced by human adipose tissue-derived mesenchymal stem cells in vivo. Biochem Biophys Res Commun, 2012, 422(4): 633-638.
61.	Ventayol M, Viñas JL, Sola A, et al. miRNA let-7e targeting MMP9 is involved in adipose-derived stem cell differentiation toward epithelia. Cell Death Dis, 2014, 5: e1048.
62.	Piran M, Enderami SE, Piran M, et al. Insulin producing cells generation by overexpression of miR-375 in adipose-derived mesenchymal stem cells from diabetic patients. Biologicals, 2017, 46: 23-28.
63.	Zhang Y, Yu M, Dai M, et al. miR-450a-5p within rat adipose tissue exosome-like vesicles promotes adipogenic differentiation by targeting WISP2. J Cell Sci, 2017, 130(6): 1158-1168.
64.	Mallinson DJ, Dunbar DR, Ridha S, et al. Identification of Potential Plasma microRNA Stratification Biomarkers for Response to Allogeneic Adipose-Derived Mesenchymal Stem Cells in Rheumatoid Arthritis. Stem Cells Transl Med, 2017, 6(4): 1202-1206.
65.	Thomou T, Mori MA, Dreyfuss JM, et al. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature, 2017, 542(7642): 450-455.
66.	Togliatto G, Dentelli P, Gili M, et al. Obesity reduces the pro-angiogenic potential of adipose tissue stem cell-derived extracellular vesicles (EVs) by impairing miR-126 content: impact on clinical applications. Int J Obes (Lond), 2016, 40(1): 102-111.
67.	Takahara K, Ii M, Inamoto T, et al. microRNA-145 Mediates the Inhibitory Effect of Adipose Tissue-Derived Stromal Cells on Prostate Cancer. Stem Cells Dev, 2016, 25(17): 1290-1298.
68.	Xu Q, Wang L, Li H, et al. Mesenchymal stem cells play a potential role in regulating the establishment and maintenance of epithelial-mesenchymal transition in MCF7 human breast cancer cells by paracrine and induced autocrine TGF-beta. Int J Oncol, 2012, 41(3): 959-968.
69.	Lou G, Song X, Yang F, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J Hematol Oncol, 2015, 8: 122.
70.	Pérez LM, Bernal A, San MN, et al. Metabolic rescue of obese adipose-derived stem cells by Lin28/Let7 pathway. Diabetes, 2013, 62(7): 2368-2379.

1. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng, 2001, 7(2): 211-228.
2. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell, 2002, 13(12): 4279-4295.
3. Dai R, Wang Z, Samanipour R, et al. Adipose-Derived Stem Cells for Tissue Engineering and Regenerative Medicine Applications. Stem Cells International, 2016, 2016: 6737345.
4. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet, 2010, 11(9): 597-610.
5. Li N, Long B, Han W, et al. microRNAs: important regulators of stem cells. Stem Cell Res Ther, 2017, 8(1): 110.
6. Kim DY, Sung JH. Regulatory role of microRNAs in the proliferation and differentiation of adipose-derived stem cells. Histol Histopathol, 2017, 32(1): 1-10.
7. Uzbas F, May ID, Parisi AM, et al. Molecular physiognomies and applications of adipose-derived stem cells. Stem Cell Rev, 2015, 11(2): 298-308.
8. Chen J, Deng S, Zhang S, et al. The role of miRNAs in the differentiation of adipose-derived stem cells. Curr Stem Cell Res Ther, 2014, 9(3): 268-279.
9. Shi C, Huang F, Gu X, et al. Adipogenic miRNA and meta-signature miRNAs involved in human adipocyte differentiation and obesity. Oncotarget, 2016, 7(26): 40830-40845.
10. Tang YF, Zhang Y, Li XY, et al. Expression of miR-31, miR-125b-5p, and miR-326 in the adipogenic differentiation process of adipose-derived stem cells. OMICS, 2009, 13(4): 331-336.
11. Zaragosi LE, Wdziekonski B, Brigand KL, et al. Small RNA sequencing reveals miR-642a-3p as a novel adipocyte-specific microRNA and miR-30 as a key regulator of human adipogenesis. Genome Biol, 2011, 12(7): R64.
12. Chen L, Cui J, Hou J, et al. A novel negative regulator of adipogenesis: microRNA-363. Stem Cells, 2014, 32(2): 510-520.
13. Kim YJ, Hwang SJ, Bae YC, et al. MiR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells, 2009, 27(12): 3093-3102.
14. Karbiener M, Neuhold C, Opriessnig P, et al. MicroRNA-30c promotes human adipocyte differentiation and co-represses PAI-1 and ALK2. RNA Biol, 2011, 8(5): 850-860.
15. Chen K, He H, Xie Y, et al. miR-125a-3p and miR-483-5p promote adipogenesis via suppressing the RhoA/ROCK1/ERK1/2 pathway in multiple symmetric lipomatosis. Sci Rep, 2015, 5: 11909.
16. Shi C, Zhang M, Tong M, et al. miR-148a is Associated with Obesity and Modulates Adipocyte Differentiation of Mesenchymal Stem Cells through Wnt Signaling. Sci Rep, 2015, 5: 9930.
17. He H, Chen K, Wang F, et al. miR-204-5p promotes the adipogenic differentiation of human adipose-derived mesenchymal stem cells by modulating DVL3 expression and suppressing Wnt/beta-catenin signaling. Int J Mol Med, 2015, 35(6): 1587-1595.
18. Yang Z, Bian C, Zhou H, et al. MicroRNA hsa-miR-138 inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells through adenovirus EID-1. Stem Cells Dev, 2011, 20(2): 259-267.
19. Chen L, Hou J, Ye L, et al. MicroRNA-143 regulates adipogenesis by modulating the MAP2K5-ERK5 signaling. Sci Rep, 2014, 4: 3819.
20. Lee EK, Lee MJ, Abdelmohsen K, et al. miR-130 suppresses adipogenesis by inhibiting peroxisome proliferator-activated receptor gamma expression. Mol Cell Biol, 2011, 31(4): 626-638.
21. Kang T, Lu W, Xu W, et al. MicroRNA-27 (miR-27) targets prohibitin and impairs adipocyte differentiation and mitochondrial function in human adipose-derived stem cells. J Biol Chem, 2013, 288(48): 34394-34402.
22. Karbiener M, Fischer C, Nowitsch S, et al. microRNA miR-27b impairs human adipocyte differentiation and targets PPARgamma. Biochem Biophys Res Commun, 2009, 390(2): 247-251.
23. Chen L, Chen Y, Zhang S, et al. MiR-540 as a novel adipogenic inhibitor impairs adipogenesis via suppression of PPARgamma. J Cell Biochem, 2015, 116(6): 969-976.
24. Yang L, Shi CM, Chen L, et al. The biological effects of hsa-miR-1908 in human adipocytes. Mol Biol Rep, 2015, 42(5): 927-935.
25. Li H, Li T, Wang S, et al. miR-17-5p and miR-106a are involved in the balance between osteogenic and adipogenic differentiation of adipose-derived mesenchymal stem cells. Stem Cell Res, 2013, 10(3): 313-324.
26. Zhang ZJ, Zhang H, Kang Y, et al. miRNA expression profile during osteogenic differentiation of human adipose-derived stem cells. J Cell Biochem, 2012, 113(3): 888-898.
27. Zhang WB, Zhong WJ, Wang L. A signal-amplification circuit between miR-218 and Wnt/beta-catenin signal promotes human adipose tissue-derived stem cells osteogenic differentiation. Bone, 2014, 58: 59-66.
28. Kim YJ, Bae SW, Yu SS, et al. miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res, 2009, 24(5): 816-825.
29. Fan C, Jia L, Zheng Y, et al. MiR-34a Promotes Osteogenic Differentiation of Human Adipose-Derived Stem Cells via the RBP2/NOTCH1/CYCLIN D1 Coregulatory Network. Stem Cell Reports, 2016, 7(2): 236-248.
30. Chen S, Zheng Y, Zhang S, et al. Promotion Effects of miR-375 on the Osteogenic Differentiation of Human Adipose-Derived Mesenchymal Stem Cells. Stem Cell Reports, 2017, 8(3): 773-786.
31. Liao YH, Chang YH, Sung LY, et al. Osteogenic differentiation of adipose-derived stem cells and calvarial defect repair using baculovirus-mediated co-expression of BMP-2 and miR-148b. Biomaterials, 2014, 35(18): 4901-4910.
32. Xie Q, Wei W, Ruan J, et al. Effects of miR-146a on the osteogenesis of adipose-derived mesenchymal stem cells and bone regeneration. Sci Rep, 2017, 7: 42840.
33. Li H, Li T, Fan J, et al. miR-216a rescues dexamethasone suppression of osteogenesis, promotes osteoblast differentiation and enhances bone formation, by regulating c-Cbl-mediated PI3K/AKT pathway. Cell Death Differ, 2015, 22(12): 1935-1945.
34. Hoseinzadeh S, Atashi A, Soleimani M, et al. MiR-221-inhibited adipose tissue-derived mesenchymal stem cells bioengineered in a nano-hydroxy apatite scaffold. In Vitro Cell Dev Biol Anim, 2016, 52(4): 479-487.
35. Zeng Y, Qu X, Li H, et al. MicroRNA-100 regulates osteogenic differentiation of human adipose-derived mesenchymal stem cells by targeting BMPR2. FEBS Lett, 2012, 586(16): 2375-2381.
36. Li J, Hu C, Han L, et al. MiR-154-5p regulates osteogenic differentiation of adipose-derived mesenchymal stem cells under tensile stress through the Wnt/PCP pathway by targeting Wnt11. Bone, 2015, 78: 130-141.
37. Li S, Hu C, Li J, et al. Effect of miR-26a-5p on the Wnt/Ca(2+) Pathway and Osteogenic Differentiation of Mouse Adipose-Derived Mesenchymal Stem Cells. Calcif Tissue Int, 2016, 99(2): 174-186.
38. Luzi E, Marini F, Sala SC, et al. Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res, 2008, 23(2): 287-295.
39. Wang Z, Xie Q, Yu Z, et al. A regulatory loop containing miR-26a, GSK3beta and C/EBPalpha regulates the osteogenesis of human adipose-derived mesenchymal stem cells. Sci Rep, 2015, 5: 15280.
40. Wang Z, Zhang D, Hu Z, et al. MicroRNA-26a-modified adipose-derived stem cells incorporated with a porous hydroxyapatite scaffold improve the repair of bone defects. Mol Med Rep, 2015, 12(3): 3345-3350.
41. Huang S, Wang S, Bian C, et al. Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev, 2012, 21(13): 2531-2540.
42. Zhang Z, Kang Y, Zhang Z, et al. Expression of microRNAs during chondrogenesis of human adipose-derived stem cells. Osteoarthritis Cartilage, 2012, 20(12): 1638-1646.
43. Yang Z, Hao J, Hu ZM. MicroRNA expression profiles in human adipose-derived stem cells during chondrogenic differentiation. Int J Mol Med, 2015, 35(3): 579-586.
44. Hou C, Yang Z, Kang Y, et al. MiR-193b regulates early chondrogenesis by inhibiting the TGF-beta2 signaling pathway. FEBS Lett, 2015, 589(9): 1040-1047.
45. Hou C, Zhang Z, Zhang Z, et al. Presence and function of microRNA-92a in chondrogenic ATDC5 and adipose-derived mesenchymal stem cells. Mol Med Rep, 2015, 12(4): 4877-4886.
46. Xu J, Kang Y, Liao WM, et al. MiR-194 regulates chondrogenic differentiation of human adipose-derived stem cells by targeting Sox5. PLoS One, 2012, 7(3): e31861.
47. Cho JA, Park H, Lim EH, et al. MicroRNA expression profiling in neurogenesis of adipose tissue-derived stem cells. J Genet, 2011, 90(1): 81-93.
48. Ning H, Huang YC, Banie L, et al. MicroRNA regulation of neuron-like differentiation of adipose tissue-derived stem cells. Differentiation, 2009, 78(5): 253-259.
49. Mondanizadeh M, Arefian E, Mosayebi G, et al. MicroRNA-124 regulates neuronal differentiation of mesenchymal stem cells by targeting Sp1 mRNA. J Cell Biochem, 2015, 116(6): 943-953.
50. Wang Y, Wang D, Guo D. MiR-124 Promote Neurogenic Transdifferentiation of Adipose Derived Mesenchymal Stromal Cells Partly through RhoA/ROCK1, but Not ROCK2 Signaling Pathway. PLoS One, 2016, 11(1): e146646.
51. Hu F, Sun B, Xu P, et al. MiR-218 Induces Neuronal Differentiation of ASCs in a Temporally Sequential Manner with Fibroblast Growth Factor by Regulation of the Wnt Signaling Pathway. Sci Rep, 2017, 7: 39427.
52. He X, Ao Q, Wei Y, et al. Transplantation of miRNA-34a overexpressing adipose-derived stem cell enhances rat nerve regeneration. Wound Repair Regen, 2016, 24(3): 542-550.
53. Alizadeh E, Akbarzadeh A, Eslaminejad MB, et al. Up regulation of liver-enriched transcription factors HNF4a and HNF6 and liver-specific microRNA (miR-122) by inhibition of let-7b in mesenchymal stem cells. Chem Biol Drug Des, 2015, 85(3): 268-279.
54. Davoodian N, Lotfi AS, Soleimani M, et al. Let-7f microRNA negatively regulates hepatic differentiation of human adipose tissue-derived stem cells. J Physiol Biochem, 2014, 70(3): 781-789.
55. Davoodian N, Lotfi AS, Soleimani M, et al. MicroRNA-122 overexpression promotes hepatic differentiation of human adipose tissue-derived stem cells. J Cell Biochem, 2014, 115(9): 1582-1593.
56. Chen KD, Huang KT, Lin CC, et al. MicroRNA-27b Enhances the Hepatic Regenerative Properties of Adipose-Derived Mesenchymal Stem Cells. Mol Ther Nucleic Acids, 2016, 5: e285.
57. Chen KD, Hsu LW, Goto S, et al. Regulation of heme oxygenase 1 expression by miR-27b with stem cell therapy for liver regeneration in rats. Transplant Proc, 2014, 46(4): 1198-1200.
58. Aji K, Zhang Y, Aimaiti A, et al. MicroRNA-145 regulates the differentiation of human adipose-derived stem cells to smooth muscle cells via targeting Kruppel-like factor 4. Mol Med Rep, 2017, 15(6): 3787-3795.
59. Kalinina N, Klink G, Glukhanyuk E, et al. miR-92a regulates angiogenic activity of adipose-derived mesenchymal stromal cells. Exp Cell Res, 2015, 339(1): 61-66.
60. Shin KK, Lee AL, Kim JY, et al. miR-21 modulates tumor outgrowth induced by human adipose tissue-derived mesenchymal stem cells in vivo. Biochem Biophys Res Commun, 2012, 422(4): 633-638.
61. Ventayol M, Viñas JL, Sola A, et al. miRNA let-7e targeting MMP9 is involved in adipose-derived stem cell differentiation toward epithelia. Cell Death Dis, 2014, 5: e1048.
62. Piran M, Enderami SE, Piran M, et al. Insulin producing cells generation by overexpression of miR-375 in adipose-derived mesenchymal stem cells from diabetic patients. Biologicals, 2017, 46: 23-28.
63. Zhang Y, Yu M, Dai M, et al. miR-450a-5p within rat adipose tissue exosome-like vesicles promotes adipogenic differentiation by targeting WISP2. J Cell Sci, 2017, 130(6): 1158-1168.
64. Mallinson DJ, Dunbar DR, Ridha S, et al. Identification of Potential Plasma microRNA Stratification Biomarkers for Response to Allogeneic Adipose-Derived Mesenchymal Stem Cells in Rheumatoid Arthritis. Stem Cells Transl Med, 2017, 6(4): 1202-1206.
65. Thomou T, Mori MA, Dreyfuss JM, et al. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature, 2017, 542(7642): 450-455.
66. Togliatto G, Dentelli P, Gili M, et al. Obesity reduces the pro-angiogenic potential of adipose tissue stem cell-derived extracellular vesicles (EVs) by impairing miR-126 content: impact on clinical applications. Int J Obes (Lond), 2016, 40(1): 102-111.
67. Takahara K, Ii M, Inamoto T, et al. microRNA-145 Mediates the Inhibitory Effect of Adipose Tissue-Derived Stromal Cells on Prostate Cancer. Stem Cells Dev, 2016, 25(17): 1290-1298.
68. Xu Q, Wang L, Li H, et al. Mesenchymal stem cells play a potential role in regulating the establishment and maintenance of epithelial-mesenchymal transition in MCF7 human breast cancer cells by paracrine and induced autocrine TGF-beta. Int J Oncol, 2012, 41(3): 959-968.
69. Lou G, Song X, Yang F, et al. Exosomes derived from miR-122-modified adipose tissue-derived MSCs increase chemosensitivity of hepatocellular carcinoma. J Hematol Oncol, 2015, 8: 122.
70. Pérez LM, Bernal A, San MN, et al. Metabolic rescue of obese adipose-derived stem cells by Lin28/Let7 pathway. Diabetes, 2013, 62(7): 2368-2379.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of miRNA regulation in differentiation of adipose-derived stem cells

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content