Let-7 enhances osteogenesis and bone formation while repressing adipogenesis of human stromal/mesenchymal stem cells by regulating HMGA2

Stem Cells and Development

Volumn 23, Issue 13, 2014, Pages 1452-1463

  Wei, Jianfeng ^a   Li, Hongling ^a   Wang, Shihua ^a   Li, Tangping ^a   Fan, Junfen ^a   Liang, Xiaolei ^a   Li, Jing ^a   Han, Qin ^a   Zhu, Li ^a   Fan, Linyuan ^a   Zhao, Robert Chunhua ^a,b  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP A2 PROTEIN; LENTIVIRUS VECTOR; LET 7 PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; MICRORNA; MIRNLET7 MICRORNA, HUMAN;

ADIPOGENESIS; ARTICLE; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE REPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN DEPLETION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BONE DEVELOPMENT; BONE REGENERATION; C57BL MOUSE; CELL CULTURE; EMBRYOLOGY; FEMUR; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MOUSE; NUDE MOUSE; PHYSIOLOGY; RNA INTERFERENCE;

ADIPOGENESIS; ANIMALS; BONE REGENERATION; CELLS, CULTURED; FEMUR; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HMGA2 PROTEIN; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, NUDE; MICRORNAS; OSTEOGENESIS; RNA INTERFERENCE;

EID: 84903134495     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0600     Document Type: Article

References (47)

1. Fink T, JG Rasmussen, J Emmersen, L Pilgaard, A Fahlman, S Brunberg, J Josefsson, JM Arnemo, V Zachar, JE Swenson and O Frobert. (2011). Adipose-derived stem cells from the brown bear (Ursus arctos) spontaneously undergo chondrogenic and osteogenic differentiation in vitro. Stem Cell Res 7:89-95.
2. Phinney DG and DJ Prockop. (2007). Concise review: Mesenchymal stem/multipotent stromal cells: The state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25:2896-2902. (Pubitemid 350127874)
3. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147. (Pubitemid 29282067)
4. Prockop DJ. (1997). Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74. (Pubitemid 27161245)
5. Tokuzawa Y, K Yagi, Y Yamashita, Y Nakachi, I Nikaido, H Bono, Y Ninomiya, Y Kanesaki-Yatsuka, M Akita, et al. (2010). Id4, a new candidate gene for senile osteoporosis, acts as a molecular switch promoting osteoblast differentiation. PLoS Genet 6:e1001019.
6. Ambros V. (2004). The functions of animal microRNAs. Nature 431:350-355. (Pubitemid 39265675)
7. Bartel DP. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116:281-297.
8. Ivey KN and D Srivastava. (2010). MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7:36-41.
9. Esau C, X Kang, E Peralta, E Hanson, EG Marcusson, LV Ravichandran, Y Sun, S Koo, RJ Perera, et al. (2004). MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 279:52361-52365. (Pubitemid 39656612)
10. Gerin I, GT Bommer, CS McCoin, KM Sousa, V Krishnan and OA MacDougald. (2010). Roles for miRNA-378/378 in adipocyte gene expression and lipogenesis. Am J Physiol Endocrinol Metab 299:E198-E206.
11. Hu R, W Liu, H Li, L Yang, C Chen, ZY Xia, LJ Guo, H Xie, HD Zhou, XP Wu and XH Luo. (2011). A Runx2/ miR-3960/miR-2861 regulatory feedback loop during mouse osteoblast differentiation. J Biol Chem 286:12328-12339.
12. Itoh T, Y Nozawa and Y Akao. (2009). MicroRNA-141 and-200a are involved in bone morphogenetic protein-2-induced mouse pre-osteoblast differentiation by targeting distal-less homeobox 5. J Biol Chem 284:19272-19279.
13. Kim SY, AY Kim, HW Lee, YH Son, GY Lee, JW Lee, YS Lee and JB Kim. (2010). miR-27a is a negative regulator of adipocyte differentiation via suppressing PPARgamma expression. Biochem Biophys Res Commun 392:323-328.
14. Kim YJ, SW Bae, SS Yu, YC Bae and JS Jung. (2009). miR-196a regulates proliferation and osteogenic differentiation in mesenchymal stem cells derived from human adipose tissue. J Bone Miner Res 24:816-825.
15. Li Z, MQ Hassan, M Jafferji, RI Aqeilan, R Garzon, CM Croce, AJ van Wijnen, JL Stein, GS Stein and JB Lian. (2009). Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 284:15676-15684.
16. Li Z, MQ Hassan, S Volinia, AJ van Wijnen, JL Stein, CM Croce, JB Lian and GS Stein. (2008). A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci U S A 105:13906-13911.
17. Luzi E, F Marini, SC Sala, I Tognarini, G Galli and ML Brandi. (2008). 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 23:287-295. (Pubitemid 351160043)
18. Mizuno Y, K Yagi, Y Tokuzawa, Y Kanesaki-Yatsuka, T Suda, T Katagiri, T Fukuda, M Maruyama, A Okuda, et al. (2008). miR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation. Biochem Biophys Res Commun 368:267-272.
19. Sun T, M Fu, AL Bookout, SA Kliewer and DJ Mangelsdorf. (2009). MicroRNA let-7 regulates 3T3-L1 adipogenesis. Mol Endocrinol 23:925-931.
20. Yang Z, C Bian, H Zhou, S Huang, S Wang, L Liao and RC Zhao. (2011). MicroRNA hsa-miR-138 inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells through adenovirus EID-1. Stem Cells Dev 20:259-267.
21. Zaragosi LE, B Wdziekonski, KL Brigand, P Villageois, B Mari, R Waldmann, C Dani and P Barbry. (2011). Small RNA sequencing reveals miR-642a-3p as a novel adipocytespecific microRNA and miR-30 as a key regulator of human adipogenesis. Genome Biol 12:R64.
22. Zhang J, Q Tu, LF Bonewald, X He, G Stein, J Lian and J Chen. (2011). Effects of miR-335-5p in modulating osteogenic differentiation by specifically downregulating Wnt antagonist DKK1. J Bone Miner Res 26:1953-1963.
23. Huang J, L Zhao, L Xing and D Chen. (2010). MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 28:357-364.
24. Li H, T Li, S Wang, J Wei, J Fan, J Li, Q Han, L Liao, C Shao and RC Zhao. (2013). 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 10:313-324.
25. Zhang JF, WM Fu, ML He, H Wang, WM Wang, SC Yu, XW Bian, J Zhou, MC Lin, et al. (2011). MiR-637 maintains the balance between adipocytes and osteoblasts by directly targeting Osterix. Mol Biol Cell 22:3955-3961.
26. Roush S and FJ Slack. (2008). The let-7 family of micro-RNAs. Trends Cell Biol 18:505-516.
27. Esquela-Kerscher A and FJ Slack. (2006). Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6:259-269.
28. Reinhart BJ, FJ Slack, M Basson, AE Pasquinelli, JC Bettinger, AE Rougvie, HR Horvitz and G Ruvkun. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901-906. (Pubitemid 30130993)
29. Yu F, H Yao, P Zhu, X Zhang, Q Pan, C Gong, Y Huang, X Hu, F Su, J Lieberman and E Song. (2007). let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 131:1109-1123. (Pubitemid 350235025)
30. Goff LA, S Boucher, CL Ricupero, S Fenstermacher, M Swerdel, LG Chase, CC Adams, J Chesnut, U Lakshmipathy and RP Hart. (2008). Differentiating human multipotent mesenchymal stromal cells regulate microRNAs: Prediction of microRNA regulation by PDGF during osteogenesis. Exp Hematol 36:1354-1369.
31. Lee YS and A Dutta. (2007). The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev 21:1025-1030. (Pubitemid 46686471)
32. Mayr C, MT Hemann and DP Bartel. (2007). Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science 315:1576-1579. (Pubitemid 46449474)
33. Cao Y, Z Sun, L Liao, Y Meng, Q Han and RC Zhao. (2005). Human adipose tissue-derived stem cells differentiate into endothelial cells in vitro and improve postnatal neovascularization in vivo. Biochem Biophys Res Commun 332:370-379. (Pubitemid 40724988)
34. Ferguson VL, RA Ayers, TA Bateman and SJ Simske. (2003). Bone development and age-related bone loss in male C57BL/6J mice. Bone 33:387-398. (Pubitemid 37107464)
35. Kajkenova O, B Lecka-Czernik, I Gubrij, SP Hauser, K Takahashi, AM Parfitt, RL Jilka, SC Manolagas and DA Lipschitz. (1997). Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res 12:1772-1779. (Pubitemid 27500188)
36. Nuttall ME and JM Gimble. (2000). Is there a therapeutic opportunity to either prevent or treat osteopenic disorders by inhibiting marrow adipogenesis? Bone 27:177-184. (Pubitemid 30458809)
37. Kolf CM, E Cho and RS Tuan. (2007). Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: Regulation of niche, self-renewal and differentiation. Arthritis Res Ther 9:204.
38. Undale AH, JJ Westendorf, MJ Yaszemski and S Khosla. (2009). Mesenchymal stem cells for bone repair and metabolic bone diseases. Mayo Clin Proc 84:893-902.
39. Lian JB, GS Stein, AJ van Wijnen, JL Stein, MQ Hassan, T Gaur and Y Zhang. (2012). MicroRNA control of bone formation and homeostasis. Nat Rev Endocrinol 8:212-227.
40. Hammond SM and NE Sharpless. (2008). HMGA2, microRNAs, and stem cell aging. Cell 135:1013-1016.
41. Berg JP. (2000). Pygmy mouse gene mutation protects against obesity. Eur J Endocrinol 143:317-318.
42. Fusco A and M Fedele. (2007). Roles of HMGA proteins in cancer. Nat Rev Cancer 7:899-910. (Pubitemid 350165857)
43. Nishino J, I Kim, K Chada and SJ Morrison. (2008). Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf Expression. Cell 135:227-239.
44. Monzen K, Y Ito, AT Naito, H Kasai, Y Hiroi, D Hayashi, I Shiojima, T Yamazaki, K Miyazono, et al. (2008). A crucial role of a high mobility group protein HMGA2 in cardiogenesis. Nat Cell Biol 10:567-574.
45. Weedon MN, G Lettre, RM Freathy, CM Lindgren, BF Voight, JR Perry, KS Elliott, R Hackett, C Guiducci, et al. (2007). A common variant of HMGA2 is associated with adult and childhood height in the general population. Nat Genet 39:1245-1250.
46. Ligon AH, SD Moore, MA Parisi, ME Mealiffe, DJ Harris, HL Ferguson, BJ Quade and CC Morton. (2005). Constitutional rearrangement of the architectural factor HMGA2: A novel human phenotype including overgrowth and lipomas. Am J Hum Genet 76:340-348. (Pubitemid 40129560)
47. Markowski DN, BM Helmke, F Meyer, I von Ahsen, R Nimzyk, I Nolte and J Bullerdiek. (2011). BMP4 increases expression of HMGA2 in mesenchymal stem cells. Cytokine 56:811-816.