CHD7 interacts with BMP R-SMADs to epigenetically regulate cardiogenesis in mice

Human Molecular Genetics

Volumn 23, Issue 8, 2014, Pages 2145-2156

  Liu, Yuelong ^a   Harmelink, Cristina ^a   Peng, Yin ^a   Chen, Yunjia ^b   Wang, Qin ^b   Jiao, Kai ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; BONE MORPHOGENETIC PROTEIN; CHROMODOMAIN HELICASE DNA BINDING PROTEIN 7; RECEPTOR REGULATED SMAD PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BIOCHEMISTRY; ENHANCER REGION; EPIGENETICS; HAPLOINSUFFICIENCY; HEART DEVELOPMENT; HEART MUSCLE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM;

ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 1; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; EPIGENOMICS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HOMEODOMAIN PROTEINS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MICE; ORGANOGENESIS; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD PROTEINS, RECEPTOR-REGULATED; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84897835537     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt610     Document Type: Article

References (53)

1. Blake, K.D. and Prasad, C. (2006) CHARGE syndrome. Orphanet. J. Rare Diseases, 1, 34.
2. Zentner, G.E., Layman, W.S., Martin, D.M. and Scacheri, P.C. (2010) Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am. J. Med. Genet. A, 152A, 674-686.
3. Bergman, J.E., Janssen, N., Hoefsloot, L.H., Jongmans, M.C., Hofstra, R.M. and van Ravenswaaij-Arts, C.M. (2011) CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J. Med. Genet., 48, 334-342.
4. Sanlaville, D. and Verloes, A. (2007) CHARGE syndrome: an update. Eur. J. Hum. Genet., 15, 389-399.
5. Wyse, R.K., al-Mahdawi, S., Burn, J. and Blake, K. (1993) Congenital heart disease in CHARGE association. Pediatr. Cardiol., 14, 75-81.
6. Vissers, L.E., van Ravenswaaij, C.M., Admiraal, R., Hurst, J.A., de Vries, B.B., Janssen, I.M., van der Vliet, W.A., Huys, E.H., de Jong, P.J., Hamel, B.C. et al. (2004) Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat. Genet., 36, 955-957.
7. Bosman, E.A., Penn, A.C., Ambrose, J.C., Kettleborough, R., Stemple, D.L. and Steel, K.P. (2005) Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum. Mol. Genet., 14, 3463-3476.
8. Bouazoune, K. and Kingston, R.E. (2012) Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc. Natl. Acad. Sci. U S A, 109, 19238-19243.
9. Schnetz, M.P., Bartels, C.F., Shastri, K., Balasubramanian, D., Zentner, G.E., Balaji, R., Zhang, X., Song, L., Wang, Z., Laframboise, T. et al. (2009) Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res., 19, 590-601.
10. Schnetz, M.P., Handoko, L., Akhtar-Zaidi, B., Bartels, C.F., Pereira, C.F., Fisher, A.G., Adams, D.J., Flicek, P., Crawford, G.E., Laframboise, T. et al. (2010) CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS. Genet., 6, e1001023.
11. Hurd, E.A., Capers, P.L., Blauwkamp, M.N., Adams, M.E., Raphael, Y., Poucher, H.K. and Martin, D.M. (2007) Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm. Genome, 18, 94-104.
12. Engelen, E., Akinci, U., Bryne, J.C., Hou, J., Gontan, C., Moen, M., Szumska, D., Kockx, C., van Ijcken, W., Dekkers, D.H. et al. (2011) Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat. Genet., 43, 607-611.
13. Adams, M.E., Hurd, E.A., Beyer, L.A., Swiderski, D.L., Raphael, Y. and Martin, D.M. (2007) Defects in vestibular sensory epithelia and innervation in mice with loss of Chd7 function: implications for human CHARGE syndrome. J. Comp. Neurol., 504, 519-532.
14. Layman, W.S., McEwen, D.P., Beyer, L.A., Lalani, S.R., Fernbach, S.D., Oh, E., Swaroop, A., Hegg, C.C., Raphael, Y., Martens, J.R. et al. (2009) Defects in neural stem cell proliferation and olfaction in Chd7 deficient mice indicate a mechanism for hyposmia in human CHARGE syndrome. Hum. Mol. Genet., 18, 1909-1923.
15. Bajpai, R., Chen, D.A., Rada-lglesias, A., Zhang, J., Xiong, Y., Helms, J., Chang, C.P., Zhao, Y., Swigut, T. and Wysocka, J. (2010) CHD7 cooperates with PBAF to control multipotent nerual crest formation. Nature, 463, 958-962.
16. Li, W., Xiong, Y., Shang, C., Twu, K.Y., Hang, C.T., Yang, J., Han, P., Lin, C.Y., Lin, C.J., Tsai, F.C. et al. (2013) Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. Proc. Natl. Acad. Sci. U S A, 110, 1738-1743.
17. Hurd, E.A., Micucci, J.A., Reamer, E.N. and Martin, D.M. (2012) Delayed fusion and altered gene expression contribute to semicircular canal defects in Chd7 deficient mice. Mech. Dev., 129, 308-323.
18. Hurd, E.A., Poucher, H.K., Cheng, K., Raphael, Y. and Martin, D.M. (2010) The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear. Development, 137, 3139-3150.
19. Hurd, E.A., Adams, M.E., Layman, W.S., Swiderski, D.L., Beyer, L.A., Halsey, K.E., Benson, J.M., Gong, T.W., Dolan, D.F., Raphael, Y. et al. (2011) Mature middle and inner ears express Chd7 and exhibit distinctive pathologies in a mouse model of CHARGE syndrome. Hear Res., 282, 184-195.
20. Randall, V., McCue, K., Roberts, C., Kyriakopoulou, V., Beddow, S., Barrett, A.N., Vitelli, F., Prescott, K., Shaw-Smith, C., Devriendt, K. et al. (2009) Great vessel development requires biallelic expression of Chd7 and Tbx1 in pharyngeal ectoderm in mice. J. Clin. Invest., 119, 3301-3310.
21. Wang, J., Greene, S.B. and Martin, J.F. (2011) BMP signaling in congenital heart disease: new developments and future directions. Birth Defects Res. A Clin. Mol. Teratol., 91, 441-448.
22. Attisano, L. and Wrana, J.L. (2002) Signal transduction by the TGF-beta superfamily. Science, 296, 1646-1647.
23. Bruneau, B.G. (2010) Chromatin remodeling in heart development. Curr. Opin. Genet. Dev., 20, 505-511.
24. Chang, C.P. and Bruneau, B.G. (2012) Epigenetics and cardiovascular development. Annu. Rev. Physiol., 74, 41-68.
25. Debenedittis, P., Harmelink, C., Chen, Y., Wang, Q. and Jiao, K. (2011) Characterization of the novel interaction between muskelin and TBX20, a critical cardiogenic transcription factor. Biochem. Biophys. Res. Commun., 409, 338-343.
26. Rybkin, I.I., Markham, D.W., Yan, Z., Bassel-Duby, R., Williams, R.S. and Olson, E.N. (2003) Conditional expression of SV40 T-antigen in mouse cardiomyocytes facilitates an inducible switch from proliferation to differentiation. J. Biol. Chem., 278, 15927-15934.
27. Lien, C.L., McAnally, J., Richardson, J.A. and Olson, E.N. (2002) Cardiac-specific activity of an Nkx2-5 enhancer requires an evolutionarily conserved Smad binding site. Dev. Biol., 244, 257-266.
28. Brown, C.O. 3rd, Chi, X., Garcia-Gras, E., Shirai, M., Feng, X.H. and Schwartz, R.J. (2004) The cardiac determination factor, Nkx2-5, is activated by mutual cofactors GATA-4 and Smad1/4 via a novel upstream enhancer. J. Biol. Chem., 279, 10659-10669.
29. Liberatore, C.M., Searcy-Schrick, R.D., Vincent, E.B. and Yutzey, K.E. (2002) Nkx-2.5 gene induction in mice is mediated by a Smad consensus regulatory region. Dev. Biol., 244, 243-256.
30. Lee, K.H., Evans, S., Ruan, T.Y. and Lassar, A.B. (2004) SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2.5 enhancer. Development, 131, 4709-4723.
31. Lien, C.L., Wu, C., Mercer, B., Webb, R., Richardson, J.A. and Olson, E.N. (1999) Control of early cardiac-specific transcription of Nkx2-5 by a GATA-dependent enhancer. Development, 126, 75-84.
32. Hao, J., Ho, J.N., Lewis, J.A., Karim, K.A., Daniels, R.N., Gentry, P.R., Hopkins, C.R., Lindsley, C.W. and Hong, C.C. (2010) In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS. Chem. Biol., 5, 245-253.
33. Liu, R., Liu, H., Chen, X., Kirby, M., Brown, P.O. and Zhao, K. (2001) Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell, 106, 309-318.
34. Gaussin, V., Van de Putte, T., Mishina, Y., Hanks, M.C., Zwijsen, A., Huylebroeck, D., Behringer, R.R. and Schneider, M.D. (2002) Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc. Natl. Acad. Sci. U S A, 99, 2878-2883.
35. Song, L., Yan, W., Chen, X., Deng, C.X., Wang, Q. and Jiao, K. (2007) Myocardial Smad4 is essential for cardiogenesis in mouse embryos. Circ. Res., 101, 277-285.
36. Ma, L., Lu, M.F., Schwartz, R.J. and Martin, J.F. (2005) Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development, 132, 5601-5611.
37. Song, L., Fassler, R., Mishina, Y., Jiao, K. and Baldwin, H.S. (2007) Essential functions of Alk3 during AV cushion morphogenesis in mouse embryonic hearts. Dev. Biol., 301, 276-286.
38. Sugi, Y., Yamamura, H., Okagawa, H. and Markwald, R.R. (2004) Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Dev. Biol., 269, 505-518.
39. Cai, C.L., Zhou, W., Yang, L., Bu, L., Qyang, Y., Zhang, X., Li, X., Rosenfeld, M.G., Chen, J. and Evans, S. (2005) T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis. Development, 132, 2475-2487.
40. Benchabane, H. and Wrana, J.L. (2003) GATA- and Smad1-dependent enhancers in the Smad7 gene differentially interpret bone morphogenetic protein concentrations. Mol. Cell. Biol., 23, 6646-6661.
41. Chen, Q., Chen, H., Zheng, D., Kuang, C., Fang, H., Zou, B., Zhu, W., Bu, G., Jin, T., Wang, Z. et al. (2009) Smad7 is required for the development and function of the heart. J. Biol. Chem., 284, 292-300.
42. Justin, N., De Marco, V., Aasland, R. and Gamblin, S.J. (2010) Reading, writing and editing methylated lysines on histone tails: new insights from recent structural studies. Curr. Opin. Struct. Biol., 20, 730-738.
43. Eissenberg, J.C. and Shilatifard, A. (2010) Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev. Biol., 339, 240-249.
44. Tremblay, K.D., Dunn, N.R. and Robertson, E.J. (2001) Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development, 128, 3609-3621.
45. Umans, L., Cox, L., Tjwa, M., Bito, V., Vermeire, L., Laperre, K., Sipido, K., Moons, L., Huylebroeck, D. and Zwijsen, A. (2007) Inactivation of Smad5 in endothelial cells and smooth muscle cells demonstrates that Smad5 is required for cardiac homeostasis. Am. J. Pathol., 170, 1460-1472.
46. Hester, M., Thompson, J.C., Mills, J., Liu, Y., El-Hodiri, H.M. and Weinstein, M. (2005) Smad1 and Smad8 function similarly in mammalian central nervous system development. Mol. Cell. Biol., 25, 4683-4692.
47. Song, L., Zhao, M., Wu, B., Zhou, B., Wang, Q. and Jiao, K. (2011) Cell autonomous requirement of endocardial Smad4 during atrioventricular cushion development in mouse embryos. Dev. Dyn., 240, 211-220.
48. Moskowitz, I.P., Wang, J., Peterson, M.A., Pu, W.T., Mackinnon, A.C., Oxburgh, L., Chu, G.C., Sarkar, M., Berul, C., Smoot, L. et al. (2011) Transcription factor genes Smad4 and Gata4 cooperatively regulate cardiac valve development. Proc. Natl. Acad. Sci. U S A, 108, 4006-4011.
49. Chen, H., Shi, S., Acosta, L., Li, W., Lu, J., Bao, S., Chen, Z., Yang, Z., Schneider, M.D., Chien, K.R. et al. (2004) BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development, 131, 2219-2231.
50. Harmelink, C., Peng, Y., Debenedittis, P., Chen, H., Shou, W. and Jiao, K. (2013) Myocardial Mycn is essential for mouse ventricular wall morphogenesis. Dev. Biol., 373, 53-63.
51. Jiao, K., Zhou, Y. and Hogan, B.L. (2002) Identification of mZnf8, a mouse Kruppel-like transcriptional repressor, as a novel nuclear interaction partner of Smad1. Mol. Cell. Biol., 22, 7633-7644.
52. Tsai, R.Y. and Reed, R.R. (1997) Using a eukaryotic GST fusion vector for proteins difficult to express in E. coli. BioTechniques, 23, 794-796., 798, 800.
53. Jiao, K., Kulessa, H., Tompkins, K., Zhou, Y., Batts, L., Baldwin, H.S. and Hogan, B.L. (2003) An essential role of Bmp4 in the atrioventricular septation of the mouse heart. Genes Dev., 17, 2362-2367.