BMP-mediated induction of GATA4/5/6 blocks somatic responsiveness to SHH

Development (Cambridge)

Volumn 141, Issue 20, 2014, Pages 3978-3987

  Daoud, Georges ^a,b   Kempf, Hervé ^a,c   Kumar, Deepak ^a,d   Kozhemyakina, Elena ^a   Holowacz, Tamara ^a,e   Kim, Dae Won ^a,f   Ionescu, Andreia ^a,g   Lassar, Andrew B ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^c UNIVERSITÉ DE LORRAINE   (France)

^d EMD Serono Research Institute   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f Yonsei University   (South Korea)

^g HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Chicken; Chondrogenesis; GATA factors; Mouse; NKX3.2; SHH; SOX9

Indexed keywords

BONE MORPHOGENETIC PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 5; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NKX2.3; UNCLASSIFIED DRUG; GATA4 PROTEIN, MOUSE; GATA5 PROTEIN, MOUSE; GATA6 PROTEIN, MOUSE; GLI PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; KRUPPEL LIKE FACTOR; NKX3-2 PROTEIN, MOUSE; NUCLEAR PROTEIN; SHH PROTEIN, MOUSE; ZFPM1 PROTEIN, MOUSE;

ARTICLE; CHICK; EMBRYO; GENE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; TRANSCRIPTION FACTOR GATA GENE; TRANSCRIPTION FACTOR GLI1 GENE; 3T3 CELL LINE; ANIMAL; CARTILAGE CELL; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; MOUSE;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CHONDROCYTES; GATA4 TRANSCRIPTION FACTOR; GATA5 TRANSCRIPTION FACTOR; GATA6 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; NIH 3T3 CELLS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84908093892     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.111906     Document Type: Article

References (31)

1. Alexandrovich, A., Qureishi, A., Coudert, A. E., Zhang, L., Grigoriadis, A. E., Shah, A. M., Brewer, A. C. and Pizzey, J. A. (2008). A role for GATA-6 in vertebrate chondrogenesis. Dev. Biol. 314, 457-470
2. 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
3. Briscoe, J., Pierani, A., Jessell, T. M. and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435-445
4. Brown, C. O., III, 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
5. Cairns, D. M., Sato, M. E., Lee, P. G., Lassar, A. B. and Zeng, L. (2008). A gradient of Shh establishes mutually repressing somitic cell fates induced by Nkx3.2 and Pax3. Dev. Biol. 323, 152-165
6. Carroll, J. S., Liu, X. S., Brodsky, A. S., Li, W., Meyer, C. A., Szary, A. J., Eeckhoute, J., Shao, W., Hestermann, E. V., Geistlinger, T. R. et al. (2005). Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1, Cell 122, 33-43
7. Chlon, T. M. and Crispino, J. D. (2012). Combinatorial regulation of tissue specification by GATA and FOG factors. Development 139, 3905-3916
8. Dai, P., Akimaru, H., Tanaka, Y., Maekawa, T., Nakafuku, M. and Ishii, S. (1999). Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3, J. Biol. Chem. 274, 8143-8152
9. Humke, E. W., Dorn, K. V., Milenkovic, L., Scott, M. P. and Rohatgi, R. (2010). The output of Hedgehog signaling is controlled by the dynamic association between Suppressor of Fused and the Gli proteins. Genes Dev. 24, 670-682
10. James, R. G. and Schultheiss, T. M. (2005). Bmp signaling promotes intermediate mesoderm gene expression in a dose-dependent, cell-autonomous and translation-dependent manner. Dev. Biol. 288, 113-125
11. Kamei, C. N., Kempf, H., Yelin, R., Daoud, G., James, R. G., Lassar, A. B., Tabin, C. J. and Schultheiss, T. M. (2011). Promotion of avian endothelial cell differentiation by GATA transcription factors. Dev. Biol. 353, 29-37
12. Kim, D.-W. and Lassar, A. B. (2003). Smad-dependent recruitment of a histone deacetylase/Sin3A complex modulates the bone morphogenetic proteindependent transcriptional repressor activity of Nkx3.2, Mol. Cell. Biol. 23, 8704-8717
13. Kim, D.-W., Kempf, H., Chen, R. E. and Lassar, A. B. (2003). Characterization of Nkx3.2 DNA binding specificity and its requirement for somitic chondrogenesis. J. Biol. Chem. 278, 27532-27539
14. Kozhemyakina, E., Ionescu, A. and Lassar, A. B. (2014). GATA6 is a crucial regulator of Shh in the limb bud. PLoS Genet. 10, e1004072
15. Kumar, D., Shadrach, J. L., Wagers, A. J. and Lassar, A. B. (2009). Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells. Mol. Biol. Cell 20, 3170-3177
16. 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 aGATA4/5/6-dependent chick Nkx2.5 enhancer. Development 131, 4709-4723
17. Liu, F., Massagué, J., Ruizi Altaba, A. (1998). Carboxy-terminally truncated Gli3 proteins associate with Smads. Nat. Genet. 20, 325-326
18. McMahon, J. A., Takada, S., Zimmerman, L. B., Fan, C.-M., Harland, R. M. and McMahon, A. P. (1998). Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438-1452
19. Murtaugh, L. C., Chyung, J. H. and Lassar, A. B. (1999). Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev. 13, 225-237
20. Murtaugh, L. C., Zeng, L., Chyung, J. H. and Lassar, A. B. (2001). The chick transcriptional repressor Nkx3.2 acts downstream of Shh to promote BMPdependent axial chondrogenesis. Dev. Cell 1, 411-422
21. Provot, S., Kempf, H., Murtaugh, L. C., Chung, U. I., Kim, D. W., Chyung, J., Kronenberg, H. M. and Lassar, A. B. (2006). Nkx3.2/Bapx1 acts as a negative regulator of chondrocyte maturation. Development 133, 651-662
22. Reshef, R., Maroto, M. and Lassar, A. B. (1998). Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. Genes Dev. 12, 290-303
23. Rohatgi, R., Milenkovic, L. and Scott, M. P. (2007). Patched1 regulates hedgehog signaling at the primary cilium. Science 317, 372-376
24. Sasaki, H., Hui, C., Nakafuku, M. and Kondoh, H. (1997). A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322
25. Snow, J. W., Kim, J., Currie, C. R., Xu, J. and Orkin, S. H. (2010). Sumoylation regulates interaction of FOG1 with C-terminal-binding protein (CTBP). J. Biol. Chem. 285, 28064-28075
26. Stafford, D.A., Brunet, L. J., Khokha, M.K., Economides, A. N. and Harland, R. M. (2011). Cooperative activity of noggin and gremlin 1 in axial skeleton development. Development 138, 1005-1014
27. Svärd, J., Heby-Henricson, K., Persson-Lek, M., Rozell, B., Lauth, M., Bergström, A., Ericson, J., Toftgård, R. and Teglund, S. (2006). Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev. Cell 10, 187-197
28. Tukachinsky, H., Lopez, L. V. and Salic, A. (2010). A mechanism for vertebrate Hedgehog signaling: recruitment to cilia and dissociation of SuFu-Gli protein complexes. J. Cell Biol. 191, 415-428
29. Wilm, B., James, R. G., Schultheiss, T. M. and Hogan, B. L. M. (2004). The forkhead genes, Foxc1 and Foxc2, regulate paraxial versus intermediate mesoderm cell fate. Dev. Biol. 271, 176-189
30. Zeng, L., Kempf, H., Murtaugh, L. C., Sato, M. E. and Lassar, A. B. (2002). Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis. Genes Dev. 16, 1990-2005
31. Zheng, R. and Blobel, G. A. (2010). GATA transcription factors and cancer. Genes Cancer 1, 1178-1188.