Heparin-binding EGF-like growth factor and miR-1192 exert opposite effect on Runx2-induced osteogenic differentiation

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Yu, S ^a   Geng, Q ^a   Ma, J ^b   Sun, F ^b   Yu, Y ^b   Pan, Q ^b   Hong, A ^a  

^a JINAN UNIVERSITY   (China)

^b TENTH PEOPLE S HOSPITAL OF TONGJI UNIVERSITY   (China)

Author keywords

HB EGF; MiR 1192; Osteogenic differentiation; Runx2

Indexed keywords

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; CADHERIN; CADHERIN 15; DESMIN; DOXYCYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; MESSENGER RNA; MICRORNA; MICRORNA 1192; MICRORNA 132 3P; MICRORNA 212 3P; MICRORNA 27B 3P; MICRORNA 466F 3P; MICRORNA 495 3P; MICRORNA 532 3P; MITOGEN ACTIVATED PROTEIN KINASE; MYOGENIN; OSTEOCALCIN; OSTEOPONTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; BONE DEVELOPMENT; CHROMATIN IMMUNOPRECIPITATION; DOWN REGULATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXPRESSION VECTOR; GEL MOBILITY SHIFT ASSAY; GENETIC TRANSFECTION; HYPOTHESIS; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DOWN-REGULATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; OSTEOBLASTS; OSTEOGENESIS; PROTEIN BIOSYNTHESIS; REPRESSOR PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84887470714     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.363     Document Type: Article

References (45)

1. Komori T. Regulation of skeletal development by the Runx family of transcription factors. J Cell Biochem 2005; 95: 445-453.
2. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997; 89: 765-771.
3. Liu W, Toyosawa S, Furuichi T, Kanatani N, Yoshida C, Liu Y et al. Overexpression of Cbfa1 in osteoblasts inhibits osteoblast maturation and causes osteopenia with multiple fractures. J Cell Biol 2001; 155: 157-166.
4. Kobayashi H, Gao Y, Ueta C, Yamaguchi A, Komori T. Multilineage differentiation of Cbfa1-deficient calvarial cells in vitro. Biochem Biophys Res Commun 2000; 273: 630-636.
5. Gersbach CA, Byers BA, Pavlath GK, García AJ. Runx2/Cbfa1 stimulates transdifferentiation of primary skeletal myoblasts into a mineralizing osteoblastic phenotype. Exp Cell Res 2004; 300: 406-417.
6. Huang YF, Lin JJ, Lin CH, Su Y, Hung SC. c-Jun N-Terminal kinase 1 negatively regulates osteoblastic differentiation induced by BMP2 via phosphorylation of Runx2 at Ser104. J Bone Miner Res 2012; 27: 1093-1105.
7. Jeon EJ, Lee KY, Choi NS, Lee MH, Kim HN, Jin YH et al. Bone morphogenetic protein-2 stimulates Runx2 acetylation. J Biol Chem 2006; 281: 16502-16511.
8. Wang CY, Yang SF, Wang Z, Tan JM, Xing SM, Chen DC et al. PCAF acetylates Runx2 and promotes osteoblast differentiation. J Bone Miner Metab 2013; 31: 381-389.
9. Jun JH, Yoon WJ, Seo SB, Woo KM, Kim GS, Ryoo HM et al. BMP2-Activated Erk/MAP kinase stabilizes Runx2 by increasing p300 levels and histone acetyltransferase activity. J Biol Chem 2010; 285: 36410-36419.
10. Zhao M, Qiao M, Harris SE, Oyajobi BO, Mundy GR, Chen D. Smurf1 inhibits osteoblast differentiation and bone formation in vitro and in vivo. J Biol Chem 2004; 279: 12854-12859.
11. Li X, Huang M, Zheng H, Wang Y, Ren F, Shang Y et al. CHIP promotes Runx2 degradation and negatively regulates osteoblast differentiation. J Cell Biol 2008; 181: 959-972.
12. 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.
13. 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.
14. Zhang Y, Xie RL, Croce CM, Stein JL, Lian JB, van Wijnen AJ et al. A program of microRNAs controls osteogenic lineage progression by targeting transcription factor Runx2. Proc Natl Acad Sci USA 2011; 108: 9863-9868.
15. Hassan MQ, Gordon JA, Beloti MM, Croce CM, van Wijnen AJ, Stein JL et al. A network connecting Runx2, SATB2, and the miR-23a-27a-24-2 cluster regulates the osteoblast differentiation program. Proc Natl Acad Sci USA 2010; 107: 19879-19884.
16. Hu R, Liu W, Li H, Yang L, Chen C, Xia ZY et al. A Runx2/miR-3960/miR- 2861 regulatory feedback loop during mouse osteoblast differentiation. J Biol Chem 2011; 286: 12328-12339.
17. Goishi K, Higashiyama S, Klagsbrun M, Nakano N, Umata T, Ishikawa M et al. Phorbol ester induces the rapid processing of cell surface heparin-binding EGF-like growth factor: Conversion from juxtacrine to paracrine growth factor activity. Mol Biol Cell 1995; 6: 967-980.
18. Miyamoto S, Yagi H, Yotsumoto F, Kawarabayashi T, Mekada E. Heparin-binding epidermal growth factor-like growth factor as a novel targeting molecule for cancer therapy. Cancer Sci 2006; 97: 341-347.
19. Jessmon P, Kilburn BA, Romero R, Leach RE, Armant DR. Function-specific intracellular signaling pathways downstream of heparin-binding EGF-like growth factor utilized by human trophoblasts. Biol Reprod 2010; 82: 921-929.
20. Nakamura T, Toita H, Yoshimoto A, Nishimura D, Takagi T, Ogawa T et al. Potential involvement of Twist2 and Erk in the regulation of osteoblastogenesis by HB-EGF-EGFR signaling. Cell Struct Funct 2010; 35: 53-61.
21. Krampera M, Pasini A, Rigo A, Scupoli MT, Tecchio C, Malpeli G et al. HB-EGF/HER-1 signaling in bone marrow mesenchymal stem cells: Inducing cell expansion and reversibly preventing multilineage differentiation. Blood 2005; 106: 59-66.
22. Wang K, Yamamoto H, Chin JR,Werb Z, Vu TH. Epidermal growth factor receptor-deficient mice have delayed primary endochondral ossification because of defective osteoclast recruitment. J Biol Chem 2004; 279: 53848-53856.
23. Baniwal SK, Shah PK, Shi Y, Haduong JH, Declerck YA, Gabet Y et al. Runx2 promotes both osteoblastogenesis and novel osteoclastogenic signals in ST2 mesenchymal progenitor cells. Osteoporos Int 2012; 23: 1399-1413.
24. Zhao Z, Zhao M, Xiao G, Franceschi RT. Gene transfer of the Runx2 transcription factor enhances osteogenic activity of bone marrow stromal cells in vitro and in vivo. Mol Ther 2005; 12: 247-253.
25. Chen X, Raab G, Deutsch U, Zhang J, Ezzell RM, Klagsbrun M. Induction of heparinbinding EGF-like growth factor expression during myogenesis. Activation of the gene by MyoD and localization of the transmembrane form of the protein on the myotube surface. J Biol Chem 1995; 270: 18285-18294.
26. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N et al. A twist code determines the onset of osteoblast differentiation. Dev Cell 2004; 6: 423-435.
27. Jones DC, Wein MN, Oukka M, Hofstaetter JG, Glimcher MJ, Glimcher LH. Regulation of adult bone mass by the zinc finger adapter protein Schnurri-3. Science 2006; 312: 1223-1227.
28. Nishikawa K, Nakashima T, Takeda S, Isogai M, Hamada M, Kimura A et al. Maf promotes osteoblast differentiation in mice by mediating the age-related switch in mesenchymal cell differentiation. J Clin Invest 2010; 12: 3455-3465.
29. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol 2004; 2: E363.
30. Dweep H, Sticht C, Pandey P, Gretz N. miRWalk - database: Prediction of possible miRNA binding sites by 'walking' the genes of three genomes. J Biomed Inform 2011; 44: 839-847.
31. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003; 115: 787-798.
32. Heinemeyer T, Wingender E, Reuter I, Hermjakob H, Kel AE, Kel OV et al. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res 1998; 26: 362-367.
33. Sandelin A, Wasserman WW, Lenhard B. ConSite: Web-based prediction of regulatory elements using cross-species comparison. Nucleic Acids Res 2004; 32: W249-W252.
34. O'Connor MD, Wederell E, Robertson G, Delaney A, Morozova O, Poon SS et al. Retinoblastoma-binding proteins 4 and 9 are important for human pluripotent stem cell maintenance. Exp Hematol 2011; 39: 866-879.
35. Watanabe R, Chano T, Inoue H, Isono T, Koiwai O, Okabe H. Rb1cc1 is critical for myoblast differentiation through Rb1 regulation. Virchows Arch 2005; 447: 643-648.
36. Kang JS, Bae GU, Yi MJ, Yang YJ, Oh JE, Takaesu G et al. A Cdo-Bnip-2-Cdc42 signaling pathway regulates p38alpha/beta MAPK activity and myogenic differentiation. J Cell Biol 2008; 182: 497-507.
37. Hinoi E, Fujimori S, Wang L, Hojo H, Uno K, Yoneda Y. Nrf2 negatively regulates osteoblast differentiation via interfering with Runx2-dependent transcriptional activation. J Biol Chem 2006; 281: 18015-18024.
38. Deepak V, Zhang Z, Meng L, Zeng X, Liu W. Reduced activity and cytoplasmic localization of Runx2 is observed in C3h10t1/2 cells overexpressing Tbx3. Cell Biochem Funct 2011; 29: 348-350.
39. Ornskov D, Nexo E, Sorensen BS. Insulin induces a transcriptional activation of epiregulin, HB-EGF and amphiregulin, by a PI3K-dependent mechanism: Identification of a specific insulin-responsive promoter element. Biochem Biophys Res Commun 2007; 354: 885-891.
40. Hatakeyama H, Cheng H, Wirth P, Counsell A, Marcrom SR, Wood CB et al. Regulation of heparin-binding EGF-like growth factor by miR-212 and acquired cetuximab-resistance in head and neck squamous cell carcinoma. PloS One 2010; 5: E12702.
41. Horikawa M, Higashiyama S, Nomura S, Kitamura Y, Ishikawa M, Taniguchi N. Upregulation of endogenous heparin-binding EGF-like growth factor and its role as a survival factor in skeletal myotubes. FEBS Lett 1999; 459: 100-104.
42. Zhu J, Shimizu E, Zhang X, Partridge NC, Qin L. EGFR signaling suppresses osteoblast differentiation and inhibits expression of master osteoblastic transcription factors Runx2 and Osterix. J Cell Biochem 2011; 112: 1749-1760.
43. Galindo M, Pratap J, Young DW, Hovhannisyan H, Im HJ, Choi JY et al. The bone-specific expression of Runx2 oscillates during the cell cycle to support a G1-related antiproliferative function in osteoblasts. J Biol Chem 2005; 280: 20274-20285.
44. Yu S, Geng Q, Sun F, Yu Y, Pan Q, Hong A. Osteogenic differentiation of C2C12 myogenic progenitor cells requires the Fos-related antigen Fra-1-A novel target of Runx2. Biochem Biophys Res Commun 2013; 430: 173-178.
45. Sun F, Xie Q, Ma J, Yang S, Chen Q, Hong A. Nuclear factor Y is required for basal activation and chromatin accessibility of fibroblast growth factor receptor 2 promoter in osteoblast-like cells. J Biol Chem 2008; 284: 3136-3147.