Epigenetic modifications and canonical wingless/int-1 class (WNT) signaling enable trans-differentiation of nonosteogenic cells into osteoblasts

Journal of Biological Chemistry

Volumn 289, Issue 29, 2014, Pages 20120-20128

  Cho, Young Dan ^a   Yoon, Won Joon ^a   Kim, Woo Jin ^a   Woo, Kyung Mi ^a   Baek, Jeong Hwa ^a   Lee, Gene ^a   Ku, Young ^a   Van Wijnen, Andre J ^b   Ryoo, Hyun Mo ^a  

^a Seoul National University   (South Korea)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; ALKYLATION; AMINO ACIDS; CELL CULTURE; CHEMICAL ACTIVATION; DRUG THERAPY; FIBROBLASTS; GENE EXPRESSION; METHYLATION; OSTEOBLASTS;

EPIGENETIC MODIFICATION; HISTONE DEACETYLASE INHIBITOR; OSTEOBLAST DIFFERENTIATION; OSTEOBLASTIC CELLS; OSTEOGENIC POTENTIAL; SIGNALING PATHWAYS; SKELETAL DEVELOPMENT; TRANS DIFFERENTIATIONS;

CELL SIGNALING;

ADIPOSE DERIVED STEM CELL; ALP GENE; ANIMAL CELL; ARTICLE; BMP2 GENE; CELL TRANSDIFFERENTIATION; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; FIBROBLAST; GENE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; GENETIC CONSERVATION; GENETIC MARKER; HISTONE ACETYLATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; WNT3A GENE;

BONE MORPHOGENETIC PROTEIN (BMP); CELL DIFFERENTIATION; EPIGENETICS; OSTEOBLAST; WNT SIGNALING;

3T3 CELLS; 3T3-L1 CELLS; ADIPOCYTES; ALKALINE PHOSPHATASE; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELL LINE; CELL TRANSDIFFERENTIATION; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FIBROBLASTS; GENE EXPRESSION; HISTONES; MICE; NIH 3T3 CELLS; OSTEOBLASTS; OSTEOGENESIS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84904512043     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.558064     Document Type: Article

References (43)

1. Chen, D., Zhao, M., and Mundy, G. R. (2004) Bone morphogenetic proteins. Growth Factors 22, 233-241 (Pubitemid 40136452)
2. Ryoo, H. M., Lee, M. H., and Kim, Y. J. (2006) Critical molecular switches involved in BMP-2-induced osteogenic differentiation of mesenchymal cells. Gene 366, 51-57
3. Yavropoulou, M. P., and Yovos, J. G. (2007) The role of the Wnt signaling pathway in osteoblast commitment and differentiation. Hormones 6, 279-294
4. Baron, R., and Kneissel, M. (2013) WNT signaling in bone homeostasis and disease: from human mutations to treatments. Nat. Med. 19, 179-192
5. Nusse, R., and Varmus, H. (2012) Three decades of Wnts: a personal perspective on how a scientific field developed. EMBO J. 31, 2670-2684
6. Gaur, T., Lengner, C. J., Hovhannisyan, H., Bhat, R. A., Bodine, P. V., Komm, B. S., Javed, A., van Wijnen, A. J., Stein, J. L., Stein, G. S., and Lian, J. B. (2005) Canonical WNT signaling promotes osteogenesis by directly stimulating Runx2 gene expression. J. Biol. Chem. 280, 33132-33140 (Pubitemid 41397109)
7. Krishnan, V., Bryant, H. U., and Macdougald, O. A. (2006) Regulation of bone mass by Wnt signaling. J. Clin. Invest. 116, 1202-1209
8. Logan, C. Y., and Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810 (Pubitemid 39488658)
9. Lee, M. H., Javed, A., Kim, H. J., Shin, H. I., Gutierrez, S., Choi, J. Y., Rosen, V., Stein, J. L., van Wijnen, A. J., Stein, G. S., Lian, J. B., and Ryoo, H. M. (1999) Transient upregulation of CBFA1 in response to bone morphogenetic protein-2 and transforming growth factor β1 in C2C12 myogenic cells coincides with suppression of the myogenic phenotype but is not sufficient for osteoblast differentiation. J. Cell. Biochem. 73, 114-125 (Pubitemid 29115485)
10. Lee, K. S., Hong, S. H., and Bae, S. C. (2002) Both the Smad and p38MAPK pathways play a crucial role in Runx2 expression following induction by transforming growth factor-β and bone morphogenetic protein. Oncogene 21, 7156-7163
11. Cho, Y. D., Kim, W. J., Yoon, W. J., Woo, K. M., Baek, J. H., Lee, G., Kim, G. S., and Ryoo, H. M. (2012) Wnt3a stimulates Mepe, matrix extracellular phosphoglycoprotein, expression directly by the activation of the canonical Wnt signaling pathway and indirectly through the stimulation of autocrine Bmp-2 expression. J. Cell. Physiol. 227, 2287-2296
12. Cho, Y. D., Yoon, W. J., Woo, K. M., Baek, J. H., Lee, G., Cho, J. Y., and Ryoo, H. M. (2009) Molecular regulation of matrix extracellular phosphoglycoprotein expression by bone morphogenetic protein-2. J. Biol. Chem. 284, 25230-25240
13. Kim, Y. J., Lee, M. H., Wozney, J. M., Cho, J. Y., and Ryoo, H. M. (2004) Bone morphogenetic protein-2-induced alkaline phosphatase expression is stimulated by Dlx5 and repressed by Msx2. J. Biol. Chem. 279, 50773-50780 (Pubitemid 40017815)
14. Rawadi, G., Vayssière, B., Dunn, F., Baron, R., and Roman-Roman, S. (2003) BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J. Bone Miner. Res. 18, 1842-1853 (Pubitemid 37322562)
15. Graf, T., and Enver, T. (2009) Forcing cells to change lineages. Nature 462, 587-594
16. Jopling, C., Boue, S., and Izpisua Belmonte, J. C. (2011) Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration. Nat. Rev. Mol. Cell Biol. 12, 79-89
17. Xie, H., Ye, M., Feng, R., and Graf, T. (2004) Stepwise reprogramming of B cells into macrophages. Cell 117, 663-676 (Pubitemid 38692531)
18. Meivar-Levy, I., Sapir, T., Gefen-Halevi, S., Aviv, V., Barshack, I., Onaca, N., Mor, E., and Ferber, S. (2007) Pancreatic and duodenal homeobox gene 1 induces hepatic dedifferentiation by suppressing the expression of CCAAT/enhancer-binding protein -. Hepatology 46, 898-905 (Pubitemid 47436135)
19. Ieda, M., Fu, J. D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B. G., and Srivastava, D. (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142, 375-386
20. Garg, V., Kathiriya, I. S., Barnes, R., Schluterman, M. K., King, I. N., Butler, C. A., Rothrock, C. R., Eapen, R. S., Hirayama-Yamada, K., Joo, K., Matsuoka, R., Cohen, J. C., and Srivastava, D. (2003) GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424, 443-447 (Pubitemid 36917494)
21. Lin, Q., Schwarz, J., Bucana, C., and Olson, E. N. (1997) Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276, 1404-1407 (Pubitemid 27235406)
22. Gardiner-Garden, M., and Frommer, M. (1987) CpG islands in vertebrate genomes. J. Mol. Biol. 196, 261-282 (Pubitemid 17122132)
23. Bestor, T., Laudano, A., Mattaliano, R., and Ingram, V. (1988) Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203, 971-983
24. Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Urven, L., McCarrey, J., Cedar, H., and Razin, A. (1992) Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 6, 705-714
25. Shiota, K. (2004) DNA methylation profiles of CpG islands for cellular differentiation and development in mammals. Cytogenet. Genome Res. 105, 325-334
26. Ohgane, J., Yagi, S., and Shiota, K. (2008) Epigenetics: the DNA methylation profile of tissue-dependent and differentially methylated regions in cells. Placenta 29, S29-S35
27. Li, L. C., and Dahiya, R. (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427-1431
28. Cho, Y.-D., Kim, W.-J., Yoon, W.-J., Woo, K. M., Baek, J.-H., and Ryoo, H.-M. (2011) Wnt3a stimulates Bmp2 expression in osteogenic cells that are epigenetically ready. J. Bone Miner. Res. 26, Suppl. 1, 161
29. Moon, C., Kim, S. H., Park, K. S., Choi, B. K., Lee, H. S., Park, J. B., Choi, G. S., Kwan, J. H., Joh, J. W., and Kim, S. J. (2009) Use of epigenetic modification to induce FOXP3 expression in nalive T cells. Transplant. Proc. 41, 1848-1854
30. Cedar, H., and Bergman, Y. (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304
31. DiNardo, D. N., Butcher, D. T., Robinson, D. P., Archer, T. K., and Rodenhiser, D. I. (2001) Functional analysis of CpG methylation in the BRCA1 promoter region. Oncogene 20, 5331-5340 (Pubitemid 32844064)
32. Fujita, N., Takebayashi, S., Okumura, K., Kudo, S., Chiba, T., Saya, H., and Nakao, M. (1999) Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBD1 isoforms. Mol. Cell. Biol. 19, 6415-6426 (Pubitemid 29399345)
33. Chen, Y., Whetstone, H. C., Youn, A., Nadesan, P., Chow, E. C., Lin, A. C., and Alman, B. A. (2007) β-Catenin signaling pathway is crucial for bone morphogenetic protein 2 to induce new bone formation. J. Biol. Chem. 282, 526-533 (Pubitemid 47076655)
34. Zhang, M., Yan, Y., Lim, Y. B., Tang, D., Xie, R., Chen, A., Tai, P., Harris, S. E., Xing, L., Qin, Y. X., and Chen, D. (2009) BMP-2 modulates β-catenin signaling through stimulation of Lrp5 expression and inhibition of β-TrCP expression in osteoblasts. J. Cell. Biochem. 108, 896-905
35. Kamiya, N., Kobayashi, T., Mochida, Y., Yu, P. B., Yamauchi, M., Kronenberg, H. M., and Mishina, Y. (2010) Wnt inhibitors Dkk1 and sost are downstream targets of BMP signaling through the type IA receptor (BMPRIA) in osteoblasts. J. Bone Miner. Res. 25, 200-210
36. Li, G., Peng, H., Corsi, K., Usas, A., Olshanski, A., and Huard, J. (2005) Differential effect of BMP4 on NIH/3T3 and C2C12 cells: implications for endochondral bone formation. J. Bone Miner. Res. 20, 1611-1623 (Pubitemid 41243550)
37. Zhang, R., Oyajobi, B. O., Harris, S. E., Chen, D., Tsao, C., Deng, H. W., and Zhao, M. (2013) Wnt/β-catenin signaling activates bone morphogenetic protein 2 expression in osteoblasts. Bone 52, 145-156
38. Bain, G., Müller, T., Wang, X., and Papkoff, J. (2003) Activated β-catenin induces osteoblast differentiation of C3H10T1/2 cells and participates in BMP2 mediated signal transduction. Biochem. Biophys. Res. Commun. 301, 84-91 (Pubitemid 36268851)
39. Winkler, D. G., Sutherland, M. S., Ojala, E., Turcott, E., Geoghegan, J. C., Shpektor, D., Skonier, J. E., Yu, C., and Latham, J. A. (2005) Sclerostin inhibition of Wnt-3a-induced C3H10T1/2 cell differentiation is indirect and mediated by bone morphogenetic proteins. J. Biol. Chem. 280, 2498-2502 (Pubitemid 40189350)
40. Kim, J. S., Crooks, H., Dracheva, T., Nishanian, T. G., Singh, B., Jen, J., and Waldman, T. (2002) Oncogenic β-catenin is required for bone morphogenetic protein 4 expression in human cancer cells. Cancer Res. 62, 2744-2748 (Pubitemid 34525754)
41. Kuroda, K., Kuang, S., Taketo, M. M., and Rudnicki, M. A. (2013) Canonical Wnt signaling induces BMP-4 to specify slow myofibrogenesis of fetal myoblasts. Skelet. Muscle 3, 5
42. Fuks, F., Hurd, P. J., Wolf, D., Nan, X., Bird, A. P., and Kouzarides, T. (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035-4040 (Pubitemid 36801137)
43. Khavinson, V., Solov'ev AIu., Zhilinskiǐ, D. V., Shataeva, L. K., and Vaniushin, B. F. (2012) Epigenetic aspects of peptide regulation of aging. Adv. Gerontol. 25, 11-22