The class I-specific HDAC inhibitor MS-275 modulates the differentiation potential of mouse embryonic stem cells

Biology Open

Volumn 2, Issue 10, 2013, Pages 1070-1077

  Franci, Gianluigi ^a,b   Casalino, Laura ^c   Petraglia, Francesca ^a   Miceli, Marco ^a   Menafra, Roberta ^b   Radic, Branka ^a   Tarallo, Valeria ^c   Vitale, Monica ^d,e   Scarfò, Marzia ^f   Pocsfalvi, Gabriella ^g   Baldi, Alfonso ^a   Ambrosino, Concetta ^f   Zambrano, Nicola ^d,e   Patriarca, Eduardo ^c   De Falco, Sandro ^c   Minchiotti, Gabriella ^c   Stunnenberg, Hendrik G ^b   Altucci, Lucia ^a,c  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^d CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^f Grande Ospedale Metropolitano   (Italy)

^g INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

Epigenetic; HDACi; Stem cell

Indexed keywords

EID: 84979581717     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20135587     Document Type: Article

References (52)

1. Álvarez, S., Khanwalkar, H., Alvarez, R., Erb, C., Martínez, C., Rodríguez-Barrios, F., Germain, P., Gronemeyer, H. and de Lera, A. R. (2009). C3 halogen and c80 substituents on stilbene arotinoids modulate retinoic Acid receptor subtype function. ChemMedChem 4, 1630-1640.
2. Arney, K. L. and Fisher, A. G. (2004). Epigenetic aspects of differentiation. J. Cell Sci. 117, 4355-4363.
3. Atkinson, S. and Armstrong, L. (2008). Epigenetics in embryonic stem cells: regulation of pluripotency and differentiation. Cell Tissue Res. 331, 23-29.
4. Bernemann, C., Greber, B., Ko, K., Sterneckert, J., Han, D. W., Araúzo-Bravo, M. J. and Schöler, H. R. (2011). Distinct developmental ground states of epiblast stem cell lines determine different pluripotency features. Stem Cells 29, 1496-1503.
5. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
6. Bieliauskas, A. V. and Pflum, M. K. (2008). Isoform-selective histone deacetylase inhibitors. Chem. Soc. Rev. 37, 1402-1413.
7. Boiani, M. and Schöler, H. R. (2005). Regulatory networks in embryo-derived pluripotent stem cells. Nat. Rev. Mol. Cell Biol. 6, 872-881.
8. Butler, L. M., Agus, D. B., Scher, H. I., Higgins, B., Rose, A., Cordon-Cardo, C., Thaler, H. T., Rifkind, R. A., Marks, P. A. and Richon, V. M. (2000). Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res. 60, 5165-5170.
9. Casalino, L., Comes, S., Lambazzi, G., De Stefano, B., Filosa, S., De Falco, S., De Cesare, D., Minchiotti, G. and Patriarca, E. J. (2011). Control of embryonic stem cell metastability by L-proline catabolism. J. Mol. Cell Biol. 3, 108-122.
10. Chambers, I. and Smith, A. (2004). Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23, 7150-7160.
11. Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. and Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643-655.
12. Chang, Y., Zhang, X., Horton, J. R., Upadhyay, A. K., Spannhoff, A., Liu, J., Snyder, J. P., Bedford, M. T. and Cheng, X. (2009). Structural basis for G9a-like protein lysine methyltransferase inhibition by BIX-01294. Nat. Struct. Mol. Biol. 16, 312-317.
13. Cimmino, F., Spano, D., Capasso, M., Zambrano, N., Russo, R., Zollo, M. and Iolascon, A. (2007). Comparative proteomic expression profile in all-trans retinoic acid differentiated neuroblastoma cell line. J. Proteome Res. 6, 2550-2564.
14. Dovey, O. M., Foster, C. T. and Cowley, S. M. (2010). Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc. Natl. Acad. Sci. USA 107, 8242-8247.
15. Fico, A., Manganelli, G., Cigliano, L., Bergamo, P., Abrescia, P., Franceschi, C., Martini, G. and Filosa, S. (2008). 2-deoxy-d-ribose induces apoptosis by inhibiting the synthesis and increasing the efflux of glutathione. Free Radic. Biol. Med. 45, 211-217.
16. Golob, J. L., Paige, S. L., Muskheli, V., Pabon, L. and Murry, C. E. (2008). Chromatin remodeling during mouse and human embryonic stem cell differentiation. Dev. Dyn. 237, 1389-1398.
17. Göttlicher, M., Minucci, S., Zhu, P., Krämer, O. H., Schimpf, A., Giavara, S., Sleeman, J. P., Lo Coco, F., Nervi, C., Pelicci, P. G. et al. (2001). Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 20, 6969-6978.
18. Grozinger, C. M., Chao, E. D., Blackwell, H. E., Moazed, D. and Schreiber, S. L. (2001). Identification of a class of small molecule inhibitors of the sirtuin family of NAD-dependent deacetylases by phenotypic screening. J. Biol. Chem. 276, 38837-38843.
19. Hayashi, K., Lopes, S. M., Tang, F. and Surani, M. A. (2008). Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3, 391-401.
20. Hsieh, J., Nakashima, K., Kuwabara, T., Mejia, E. and Gage, F. H. (2004). Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc. Natl. Acad. Sci. USA 101, 16659-16664.
21. Hu, E., Dul, E., Sung, C. M., Chen, Z., Kirkpatrick, R., Zhang, G. F., Johanson, K., Liu, R., Lago, A., Hofmann, G. et al. (2003). Identification of novel isoformselective inhibitors within class I histone deacetylases. J. Pharmacol. Exp. Ther. 307, 720-728.
22. Jergil, M., Forsberg, M., Salter, H., Stockling, K., Gustafson, A. L., Dencker, L. and Stigson, M. (2011). Short-time gene expression response to valproic acid and valproic acid analogs in mouse embryonic stem cells. Toxicol. Sci. 121, 328-342.
23. Karantzali, E., Schulz, H., Hummel, O., Hubner, N., Hatzopoulos, A. and Kretsovali, A. (2008). Histone deacetylase inhibition accelerates the early events of stem cell differentiation: transcriptomic and epigenetic analysis. Genome Biol. 9, R65.
24. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M. J., Ji, H., Ehrlich, L. I. et al. (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290.
25. Kubicek, S., O'Sullivan, R. J., August, E. M., Hickey, E. R., Zhang, Q., Teodoro, M. L., Rea, S., Mechtler, K., Kowalski, J. A., Homon, C. A. et al. (2007). Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol. Cell 25, 473-481.
26. Lee, S., Park, J. R., Seo, M. S., Roh, K. H., Park, S. B., Hwang, J.W., Sun, B., Seo, K., Lee, Y. S., Kang, S. K. et al. (2009). Histone deacetylase inhibitors decrease proliferation potential and multilineage differentiation capability of humanmesenchymal stem cells. Cell Prolif. 42, 711-720.
27. Lenka, N. and Ramasamy, S. K. (2007). Neural induction from ES cells portrays default commitment but instructive maturation. PLoS ONE 2, e1349.
28. Lensch, M. W., Schlaeger, T. M., Zon, L. I. and Daley, G. Q. (2007). Teratoma formation assays with human embryonic stem cells: a rationale for one type of human-animal chimera. Cell Stem Cell 1, 253-258.
29. Lin, R. J., Nagy, L., Inoue, S., Shao, W., Miller, W. H., Jr and Evans, R. M. (1998). Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature 391, 811-814.
30. Loh, Y. H., Wu, Q., Chew, J. L., Vega, V. B., Zhang, W., Chen, X., Bourque, G., George, J., Leong, B., Liu, J. et al. (2006). The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38, 431-440.
31. Manzo, F., Tambaro, F. P., Mai, A. and Altucci, L. (2009). Histone acetyltransferase inhibitors and preclinical studies. Expert Opin Ther Pat 19, 761-774.
32. Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A. F., Smith, A. et al. (2012). The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604.
33. Martens, J. H., Brinkman, A. B., Simmer, F., Francoijs, K. J., Nebbioso, A., Ferrara, F., Altucci, L. and Stunnenberg, H. G. (2010). PML-RARalpha/RXR alters the epigenetic landscape in acute promyelocytic leukemia. Cancer Cell 17, 173-185.
34. Medvedev, S. P., Grigor'eva, E. V., Shevchenko, A. I., Malakhova, A. A., Dementyeva, E. V., Shilov, A. A., Pokushalov, E. A., Zaidman, A. M., Aleksandrova, M. A., Plotnikov, E. Y. et al. (2011). Human induced pluripotent stem cells derived from fetal neural stem cells successfully undergo directed differentiation into cartilage. Stem Cells Dev. 20, 1099-1112.
35. Milde, T., Kleber, S., Korshunov, A., Witt, H., Hielscher, T., Koch, P., Kopp, H. G., Jugold, M., Deubzer, H. E., Oehme, I. et al. (2011). A novel human high-risk ependymoma stem cell model reveals the differentiation-inducing potential of the histone deacetylase inhibitor Vorinostat. Acta Neuropathol. 122, 637-650.
36. Mummery, C. L., Feyen, A., Freund, E. and Shen, S. (1990). Characteristics of embryonic stem cell differentiation: a comparison with two embryonal carcinoma cell lines. Cell Differ. Dev. 30, 195-206.
37. Nebbioso, A., Manzo, F., Miceli, M., Conte, M., Manente, L., Baldi, A., De Luca, A., Rotili, D., Valente, S., Mai, A. et al. (2009). Selective class II HDAC inhibitors impair myogenesis by modulating the stability and activity of HDAC-MEF2 complexes. EMBO Rep. 10, 776-782.
38. Nebbioso, A., Pereira, R., Khanwalkar, H., Matarese, F., García-Rodríguez, J., Miceli, M., Logie, C., Kedinger, V., Ferrara, F., Stunnenberg, H. G. et al. (2011). Death receptor pathway activation and increase of ROS production by the triple epigenetic inhibitor UVI5008. Mol. Cancer Ther. 10, 2394-2404.
39. Niwa, H., Miyazaki, J. and Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24, 372-376.
40. O'Connor, M. D., Kardel, M. D., Iosfina, I., Youssef, D., Lu, M., Li, M. M., Vercauteren, S., Nagy, A. and Eaves, C. J. (2008). Alkaline phosphatase-positive colony formation is a sensitive, specific, and quantitative indicator of undifferentiated human embryonic stem cells. Stem Cells 26, 1109-1116.
41. Orkin, S. H. and Hochedlinger, K. (2011). Chromatin connections to pluripotency and cellular reprogramming. Cell 145, 835-850.
42. Park, J. H., Jung, Y., Kim, T. Y., Kim, S. G., Jong, H. S., Lee, J. W., Kim, D. K., Lee, J. S., Kim, N. K., Kim, T. Y. et al. (2004). Class I histone deacetylase-selective novel synthetic inhibitors potently inhibit human tumor proliferation. Clin. Cancer Res. 10, 5271-5281.
43. Park, J. H., Jong, H. S., Kim, S. G., Jung, Y., Lee, K. W., Lee, J. H., Kim, D. K., Bang, Y. J. and Kim, T. Y. (2008). Inhibitors of histone deacetylases induce tumorselective cytotoxicity through modulating Aurora-A kinase. J Mol Med (Berl) 86, 117-128.
44. Park, J. A., Kim, Y. E., Seok, H. J., Park, W. Y., Kwon, H. J. and Lee, Y. (2011). Differentiation and upregulation of heat shock protein 70 induced by a subset of histone deacetylase inhibitors in mouse and human embryonic stem cells. BMB Rep. 44, 176-181.
45. Richon, V. M., Webb, Y., Merger, R., Sheppard, T., Jursic, B., Ngo, L., Civoli, F., Breslow, R., Rifkind, R. A. and Marks, P. A. (1996). Second generation hybrid polar compounds are potent inducers of transformed cell differentiation. Proc. Natl. Acad. Sci. USA 93, 5705-5708.
46. Saito, A., Yamashita, T., Mariko, Y., Nosaka, Y., Tsuchiya, K., Ando, T., Suzuki, T., Tsuruo, T. and Nakanishi, O. (1999). A synthetic inhibitor of histone deacetylase, MS-27-275, with marked in vivo antitumor activity against human tumors. Proc. Natl. Acad. Sci. USA 96, 4592-4597.
47. Sealy, L. and Chalkley, R. (1978). The effect of sodium butyrate on histone modification. Cell 14, 115-121.
48. Shi, Y., Desponts, C., Do, J. T., Hahm, H. S., Schöler, H. R. and Ding, S. (2008). Induction of pluripotent stem cells from mouse embryonic fibroblasts by Oct4 and Klf4 with small-molecule compounds. Cell Stem Cell 3, 568-574.
49. Solter, D. (2006). From teratocarcinomas to embryonic stem cells and beyond: a history of embryonic stem cell research. Nat. Rev. Genet. 7, 319-327.
50. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. and Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
51. Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Peng, W., Zhang, M. Q. et al. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903.
52. Zhang, Y., Zhang, M., Dong, H., Yong, S., Li, X., Olashaw, N., Kruk, P. A., Cheng, J. Q., Bai, W., Chen, J. et al. (2009). Deacetylation of cortactin by SIRT1 promotes cell migration. Oncogene 28, 445-460.