Histone deacetylase 3 modulates Tbx5 activity to regulate early cardiogenesis

Human Molecular Genetics

Volumn 23, Issue 14, 2014, Pages 3801-3809

  Lewandowski, Sara L ^a   Janardhan, Harish P ^a   Smee, Kevin M ^a   Bachman, Marcos ^a   Sun, Zheng ^b,c   Lazar, Mitchell A ^b,c   Trivedi, Chinmay M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; HISTONE DEACETYLASE 3; TRANSCRIPTION FACTOR TBX5; HISTONE DEACETYLASE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE; GENE DELETION; HEART DEVELOPMENT; HEART MUSCLE CELL; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MOUSE; MYH7 GENE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN TARGETING; TNNI2 GENE; TNNT1 GENE; TNNT2 GENE; UPREGULATION; ACETYLATION; ANIMAL; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEART; LETHAL GENE; METABOLISM; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, LETHAL; HEART; HEK293 CELLS; HISTONE DEACETYLASES; HUMANS; MICE; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS;

EID: 84902967294     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu093     Document Type: Article

References (40)

1. Garcia-Martinez, V. and Schoenwolf, G.C. (1993). Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol., 159, 706-719.
2. Evans, S.M., Yelon, D., Conlon, F.L. and Kirby, M.L. (2010). Myocardial lineage development. Circ. Res., 107, 1428-1444.
3. Harvey, R.P. (2002). Patterning the vertebrate heart. Nat. Rev. Genet., 3, 544-556.
4. Gourdie, R.G., Mima, T., Thompson, R.P. and Mikawa, T. (1995). Terminal diversification of the myocytelineage generates Purkinje fibers of the cardiac conduction system. Development, 121, 1423-1431.
5. Kattman, S.J., Huber, T.L. and Keller, G.M. (2006). Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell, 11, 723-732.
6. Moretti, A., Caron, L., Nakano, A., Lam, J.T., Bernshausen, A., Chen, Y., Qyang, Y., Bu, L., Sasaki, M., Martin-Puig, S. et al. (2006). Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell, 127, 1151-1165.
7. Wu, S.M., Fujiwara, Y., Cibulsky, S.M., Clapham, D.E., Lien, C.L., Schultheiss, T.M. and Orkin, S.H. (2006). Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell, 127, 1137-1150.
8. Chang, C.P. and Bruneau, B.G. (2012). Epigenetics and cardiovascular development. Annu. Rev. Physiol., 74, 41-68.
9. Suganuma, T. and Workman, J.L. (2011). Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem., 80, 473-499.
10. Haberland, M., Montgomery, R.L. and Olson, E.N. (2009). The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet., 10, 32-42.
11. Yang, X.J. and Seto, E. (2008). The Rpd3/Hda1family of lysine deacetylases:from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol., 9, 206-218.
12. Trivedi, C.M., Luo, Y., Yin, Z., Zhang, M., Zhu, W., Wang, T., Floss, T., Goettlicher, M., Noppinger, P.R., Wurst, W. et al. (2007). Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat. Med., 13, 324-331.
13. Bhaskara, S., Chyla, B.J.,Amann,J.M., Knutson, S.K., Cortez, D., Sun,Z.W. and Hiebert, S.W. (2008). Deletion of histone deacetylase 3 reveals critical roles in S phase progression andDNAdamage control. Mol. Cell, 30, 61-72.
14. Montgomery, R.L., Potthoff, M.J., Haberland, M., Qi, X., Matsuzaki, S., Humphries, K.M., Richardson, J.A., Bassel-Duby,R. and Olson, E.N. (2008). Maintenance of cardiac energy metabolismby histone deacetylase 3 in mice. J. Clin. Invest., 118, 3588-3597.
15. Sun, Z., Singh, N., Mullican, S.E., Everett, L.J., Li, L., Yuan, L., Liu, X., Epstein, J.A. and Lazar, M.A. (2011). Diet-induced lethality due to deletion of the Hdac3 gene in heart and skeletal muscle. J. Biol. Chem., 286, 33301-33309.
16. Trivedi, C.M., Zhu, W., Wang, Q., Jia, C., Kee, H.J., Li, L., Hannenhalli, S. and Epstein, J.A. (2010). Hopx and Hdac2 interact to modulate Gata4 acetylation and embryonic cardiac myocyte proliferation. Dev. Cell, 19, 450-459.
17. McCulley, D.J. and Black, B.L. (2012). Transcription factor pathways and congenital heart disease. Curr. Top. Dev. Biol., 100, 253-277.
18. Basson, C.T., Bachinsky, D.R., Lin, R.C., Levi, T., Elkins, J.A., Soults, J., Grayzel, D., Kroumpouzou, E., Traill, T.A., Leblanc-Straceski, J. et al. (1997). Mutations in human TBX5 [corrected] cause limb and cardiac malformation in Holt-Oram syndrome. Nat. Genet., 15, 30-35.
19. Bruneau, B.G., Nemer, G., Schmitt, J.P., Charron, F., Robitaille, L., Caron, S., Conner, D.A., Gessler, M., Nemer, M., Seidman, C.E. et al. (2001). A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell, 106, 709-721.
20. Takeuchi, J.K. and Bruneau, B.G. (2009). Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature, 459, 708-711.
21. Herrmann, F., Bundschu, K., Kuhl, S.J. and Kuhl, M. (2011). Tbx5 overexpression favors a first heart field lineage in murine embryonic stem cells and in Xenopus laevis embryos. Dev. Dyn., 240, 2634-2645.
22. Niu, Z., Yu, W., Zhang, S.X., Barron, M., Belaguli, N.S., Schneider, M.D., Parmacek, M., Nordheim, A. and Schwartz, R.J. (2005). Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J. Biol. Chem., 280, 32531-32538.
23. He, A., Kong, S.W., Ma, Q. and Pu, W.T. (2011). Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart. Proc. Natl. Acad. Sci. USA., 108, 5632-5637.
24. Plageman, T.F. Jr and Yutzey, K.E. (2006). Microarray analysis of Tbx5-induced genes expressed in the developing heart. Dev. Dyn., 235, 2868-2880.
25. Mori, A.D. and Bruneau, B.G. (2004). TBX5 mutations and congenital heart disease: Holt-Oramsyndrome revealed. Curr. Opin. Cardiol., 19, 211-215.
26. Heinritz, W., Shou, L., Moschik, A. and Froster, U.G. (2005) The human TBX5 gene mutation database. Hum. Mutat., 26, 397.
27. Postma, A.V., van de Meerakker, J.B., Mathijssen, I.B., Barnett, P., Christoffels, V.M., Ilgun, A., Lam, J., Wilde, A.A., Lekanne Deprez, R.H. and Moorman, A.F. (2008). Again-of-function TBX5 mutation is associated with atypical Holt-Oram syndrome and paroxysmal atrial fibrillation. Circ. Res., 102, 1433-1442.
28. Kawamura, T., Ono, K., Morimoto, T., Wada, H., Hirai, M., Hidaka, K., Morisaki, T., Heike, T., Nakahata, T., Kita, T. et al. (2005). Acetylation of GATA-4 is involved in the differentiation of embryonic stem cells into cardiac myocytes. J. Biol. Chem., 280, 19682-19688.
29. Barron, M.R., Belaguli, N.S., Zhang, S.X., Trinh, M., Iyer, D., Merlo, X., Lough, J.W., Parmacek, M.S., Bruneau, B.G. and Schwartz, R.J. (2005). Serum response factor, an enriched cardiac mesoderm obligatory factor, is a downstream gene target for Tbx genes. J. Biol. Chem., 280, 11816-11828.
30. Murakami, M., Nakagawa, M., Olson, E.N. and Nakagawa, O. (2005). AWW domain protein TAZ is a critical coactivator for TBX5, a transcription factor implicated in Holt-Oram syndrome. Proc. Natl. Acad. Sci. USA., 102, 18034-18039.
31. Wu, S.M., Chien, K.R. and Mummery, C. (2008). Origins and fates of cardiovascular progenitor cells. Cell, 132, 537-543.
32. Greulich, F., Rudat, C. and Kispert, A. (2011). Mechanisms of T-box gene function in the developing heart. Cardiovasc. Res., 91, 212-222.
33. Hiroi, Y., Kudoh, S., Monzen, K., Ikeda, Y., Yazaki, Y., Nagai, R. and Komuro, I. (2001). Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation. Nat. Genet., 28, 276-280.
34. Li, Q.Y., Newbury-Ecob, R.A., Terrett, J.A., Wilson, D.I., Curtis, A.R., Yi, C.H., Gebuhr, T., Bullen, P.J., Robson, S.C., Strachan, T. et al. (1997). Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat. Genet., 15, 21-29.
35. 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. et al. (2003). GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature, 424, 443-447.
36. Wang, Z., Zang, C., Cui, K., Schones, D.E., Barski, A., Peng, W. and Zhao, K. (2009). Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell, 138, 1019-1031.
37. You, S.H., Lim, H.W., Sun, Z., Broache, M., Won, K.J. and Lazar, M.A. (2013). Nuclear receptor co-repressors are required for the histone-deacetylase activity of HDAC3 in vivo. Nat. Struct. Mol. Biol., 20, 182-187.
38. Sun, Z., Feng, D., Fang, B., Mullican, S.E., You, S.H., Lim, H.W., Everett, L.J., Nabel, C.S., Li, Y., Selvakumaran, V. et al. (2013). Deacetylase-independent Function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol. Cell, 52, 769-782.
39. McFadden, D.G., Barbosa, A.C., Richardson, J.A., Schneider, M.D., Srivastava, D. and Olson, E.N. (2005). The Hand1 and Hand2 transcription factors regulate expansion of the embryonic cardiac ventricles in a gene dosage-dependent manner. Development, 132, 189-201.
40. Mullican, S.E., Gaddis, C.A., Alenghat, T., Nair, M.G., Giacomin, P.R., Everett, L.J., Feng, D., Steger, D.J., Schug, J., Artis, D. et al. (2011). Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev., 25, 2480-2488.