MIR-216a rescues dexamethasone suppression of osteogenesis, promotes osteoblast differentiation and enhances bone formation, by regulating c-Cbl-mediated PI3K/AKT pathway

Cell Death and Differentiation

Volumn 22, Issue 12, 2015, Pages 1935-1945

  Li, H ^a   Li, T ^a   Fan, J ^a   Fan, L ^a   Wang, S ^a   Weng, X ^a   Han, Q ^a   Zhao, R C ^a  

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; DEXAMETHASONE; MICRORNA; MICRORNA 216A; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RING FINGER PROTEIN; SHORT HAIRPIN RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; MIRN216 MICRORNA, MOUSE;

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MARKER GENE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; UPREGULATION; ADIPOSE TISSUE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; SCID MOUSE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STEM CELL; STEM CELL TRANSPLANTATION; UMBILICAL CORD;

ADIPOSE TISSUE; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; DEXAMETHASONE; DOWN-REGULATION; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; MICRORNAS; OSTEOBLASTS; OSTEOGENESIS; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-CBL; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; STEM CELLS; UMBILICAL CORD;

EID: 84947490760     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.99     Document Type: Article

References (56)

1. Ahmed SF, Elmantaser M. Secondary osteoporosis. Endocr Dev 2009; 16: 170-190.
2. Canalis E, Delany AM. Mechanisms of glucocorticoid action in bone. Ann N YAcad Sci 2002; 966: 73-81.
3. Yun SI, Yoon HY, Jeong SY, Chung YS. Glucocorticoid induces apoptosis of osteoblast cells through the activation of glycogen synthase kinase 3beta. J Bone Miner Metab 2009; 27: 140-148.
4. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147.
5. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13: 4279-4295.
6. Mosna F, Sensebe L, Krampera M. Human bone marrow and adipose tissue mesenchymal stem cells: a user's guide. Stem Cells Dev 2010; 19: 1449-1470.
7. Hass R, Kasper C, Bohm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011; 9: 12.
8. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007; 25: 2739-2749.
9. Fink T, Rasmussen JG, Emmersen J, Pilgaard L, Fahlman A, Brunberg S et al. Adiposederived stem cells from the brown bear (Ursus arctos) spontaneously undergo chondrogenic and osteogenic differentiation in vitro. Stem Cell Res 2011; 7: 89-95.
10. Lips P, Courpron P, Meunier PJ. Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif Tissue Res 1978; 26: 13-17.
11. Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 2014; 507: 323-328.
12. Yang M, Liu R, Li X, Liao J, Pu Y, Pan E et al. miRNA-183 suppresses apoptosis and promotes proliferation in esophageal cancer by targeting PDCD4. Mol Cells 2014; 37: 873-880.
13. Mori M, Triboulet R, Mohseni M, Schlegelmilch K, Shrestha K, Camargo FD et al. Hippo signaling regulates microprocessor and links cell-density-dependent miRNA biogenesis to cancer. Cell 2014; 156: 893-906.
14. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008; 132: 875-886.
15. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 2003; 113: 25-36.
16. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE et al. A pancreatic isletspecific microRNA regulates insulin secretion. Nature 2004; 432: 226-230.
17. Carthew RW, Sontheimer EJ. Origins and mechanisms of miRNAs and siRNAs. Cell 2009; 136: 642-655.
18. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011; 12: 99-110.
19. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 2004; 5: 522-531.
20. Zamore PD, Haley B. Ribo-gnome: the big world of small RNAs. Science 2005; 309: 1519-1524.
21. Lian JB, Stein GS, van Wijnen AJ, Stein JL, Hassan MQ, Gaur T et al. MicroRNA control of bone formation and homeostasis. Nat Rev Endocrinol 2012; 8: 212-227.
22. Li Z, Hassan MQ, Volinia S, van Wijnen AJ, Stein JL, Croce CM et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA 2008; 105: 13906-13911.
23. Eskildsen T, Taipaleenmaki H, Stenvang J, Abdallah BM, Ditzel N, Nossent AY et al. MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci USA 2011; 108: 6139-6144.
24. Wei J, Shi Y, Zheng L, Zhou B, Inose H, Wang J et al. miR-34s inhibit osteoblast proliferation and differentiation in the mouse by targeting SATB2. J Cell Biol 2012; 197: 509-521.
25. Yu S, Geng Q, Ma J, Sun F, Yu Y, Pan Q et al. Heparin-binding EGF-like growth factor and miR-1192 exert opposite effect on Runx2-induced osteogenic differentiation. Cell Death Dis 2013; 4: e868.
26. Wang X, Guo B, Li Q, Peng J, Yang Z, Wang A et al. miR-214 targets ATF4 to inhibit bone formation. Nat Med 2013; 19: 93-100.
27. Chen L, Holmstrom K, Qiu W, Ditzel N, Shi K, Hokland L et al. MicroRNA-34a inhibits osteoblast differentiation and in vivo bone formation of human stromal stem cells. Stem Cells 2014; 32: 902-912.
28. Kureel J, Dixit M, Tyagi AM, Mansoori MN, Srivastava K, Raghuvanshi A et al. miR-542-3p suppresses osteoblast cell proliferation and differentiation, targets BMP-7 signaling and inhibits bone formation. Cell Death Dis 2014; 5: e1050.
29. Zuo B, Zhu JF, Li J, Wang CD, Zhao XY, Cai GQ et al. MicroRNA-103a functions as a mechanosensitive microRNA to inhibit bone formation through targeting Runx2. J Bone Miner Res 2015; 30: 330-345.
30. Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 2010; 28: 357-364.
31. Li HL, Li TP, Wang SH, Wei JF, Fan JF, Li J 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: 313-324.
32. Zhang JF, Fu WM, He ML, Wang H, Wang WM, Yu SC et al. MiR-637 maintains the balance between adipocytes and osteoblasts by directly targeting Osterix. Mol Biol Cell 2011; 22: 3955-3961.
33. Wang FS, Chuang PC, Lin CL, Chen MW, Ke HJ, Chang YH et al. MicroRNA-29a protects against glucocorticoid-induced bone loss and fragility in rats by orchestrating bone acquisition and resorption. Arthritis Rheum 2013; 65: 1530-1540.
34. Ko JY, Chuang PC, Chen MW, Ke HC, Wu SL, Chang YH et al. MicroRNA-29a ameliorates glucocorticoid-induced suppression of osteoblast differentiation by regulating beta-catenin acetylation. Bone 2013; 57: 468-475.
35. Overman RA, Toliver JC, Yeh JY, Gourlay ML, Deal CL. U.S. adults meeting 2010 American College of Rheumatology criteria for treatment and prevention of glucocorticoid-induced osteoporosis. Arthritis Care Res (Hoboken) 2014; 66: 1644-1652.
36. Li J, Zhang N, Huang X, Xu J, Fernandes JC, Dai K et al. Dexamethasone shifts bone marrow stromal cells from osteoblasts to adipocytes by C/EBPalpha promoter methylation. Cell Death Dis 2013; 4: e832.
37. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2001; 2: 294-307.
38. Schmidt MH, Dikic I. The Cbl interactome and its functions. Nat Rev Mol Cell Biol 2005; 6: 907-918.
39. Brennan T, Adapala NS, Barbe MF, Yingling V, Sanjay A. Abrogation of Cbl-PI3K interaction increases bone formation and osteoblast proliferation. Calcif Tissue Int 2011; 89: 396-410.
40. Adapala NS, Holland D, Scanlon V, Barbe MF, Langdon WY, Tsygankov AY et al. Loss of Cbl-PI3K interaction in mice prevents significant bone loss following ovariectomy. Bone 2014; 67: 1-9.
41. Dieudonne FX, Severe N, Biosse-Duplan M, Weng JJ, Su Y, Marie PJ. Promotion of osteoblast differentiation in mesenchymal cells through Cbl-mediated control of STAT5 activity. Stem Cells 2013; 31: 1340-1349.
42. Kang IH, Jeong BC, Hur SW, Choi H, Choi SH, Ryu JH et al. MicroRNA-302a stimulates osteoblastic differentiation by repressing COUP-TFII expression. J Cell Physiol 2015; 230: 911-921.
43. Cheung KS, Sposito N, Stumpf PS, Wilson DI, Sanchez-Elsner T, Oreffo RO. MicroRNA-146a regulates human foetal femur derived skeletal stem cell differentiation by down-regulating SMAD2 and SMAD3. PLoS One 2014; 9: e98063.
44. Shapiro F. Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur Cell Mater 2008; 15: 53-76.
45. Park D, Spencer JA, Koh BI, Kobayashi T, Fujisaki J, Clemens TL et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012; 10: 259-272.
46. O'Brien CA, Jia D, Plotkin LI, Bellido T, Powers CC, Stewart SA et al. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 2004; 145: 1835-1841.
47. Grigoriadis AE, Heersche JN, Aubin JE. Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone. J Cell Biol 1988; 106: 2139-2151.
48. Kato M, Putta S, Wang M, Yuan H, Lanting L, Nair I et al. TGF-beta activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 2009; 11: 881-889.
49. Zhang J, Ning X, Cui W, Bi M, Zhang D. Transforming growth factor (TGF)-beta-induced microRNA-216a promotes acute pancreatitis via Akt and TGF-beta pathway in mice. Dig Dis Sci 2015; 60: 127-135.
50. Ueno H, Sasaki K, Honda H, Nakamoto T, Yamagata T, Miyagawa K et al. c-Cbl is tyrosinephosphorylated by interleukin-4 and enhances mitogenic and survival signals of interleukin-4 receptor by linking with the phosphatidylinositol 3 '-kinase pathway. Blood 1998; 91: 46-53.
51. Adapala NS, Barbe MF, Langdon WY, Nakamura MC, Tsygankov AY, Sanjay A. The loss of Cbl-phosphatidylinositol 3-kinase interaction perturbs RANKL-mediated signaling, inhibiting bone resorption and promoting osteoclast survival. J Biol Chem 2010; 285: 36745-36758.
52. Adapala NS, Barbe MF, Tsygankov AY, Lorenzo JA, Sanjay A. Loss of Cbl-PI3K interaction enhances osteoclast survival due to p21-Ras mediated PI3K activation independent of Cbl-b. J Cell Biochem 2014; 115: 1277-1289.
53. Huang S, Wang S, Bian C, Yang Z, Zhou H, Zeng Y et al. Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissuederived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev 2012; 21: 2531-2540.
54. Can A, Balci D. Isolation, culture, and characterization of human umbilical cord stromaderived mesenchymal stem cells. Methods Mol Biol 2011; 698: 51-62.
55. Addison WN, Azari F, Sorensen ES, Kaartinen MT, McKee MD. Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, up-regulating osteopontin, and inhibiting alkaline phosphatase activity. J Biol Chem 2007; 282: 15872-15883.
56. Abdallah BM, Ditzel N, Kassem M. Assessment of bone formation capacity using in vivo transplantation assays: procedure and tissue analysis. Methods Mol Biol 2008; 455: 89-100.