Complex Interdependence Regulates Heterotypic Transcription Factor Distribution and Coordinates Cardiogenesis

Cell

Volumn 164, Issue 5, 2016, Pages 999-1014

  Luna Zurita, Luis ^a,b   Stirnimann, Christian U ^c   Glatt, Sebastian ^c   Kaynak, Bogac L ^a,b   Thomas, Sean ^a   Baudin, Florence ^c,d   Samee, Md Abul Hassan ^a   He, Daniel ^a,b   Small, Eric M ^e   Mileikovsky, Maria ^f   Nagy, Andras ^f,g   Holloway, Alisha K ^a,h   Pollard, Katherine S ^a,h   Müller, Christoph W ^c   Bruneau, Benoit G ^a,b,h,i  

^a GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^b Roddenberry Center for Stem Cell Biology and Medicine at Gladstone   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^e UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^f MOUNT SINAI HOSPITAL   (Canada)

^g UNIVERSITY OF TORONTO   (Canada)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX2.5; ZINC FINGER PROTEIN; GATA4 PROTEIN, MOUSE; HOMEOBOX PROTEIN NKX-2.5; HOMEODOMAIN PROTEIN; NKX2-5 PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEIN 2; TRANSCRIPTION FACTOR GATA 4;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; HEART DEVELOPMENT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; ANIMAL; CARDIAC MUSCLE; CYTOLOGY; GENETICS; MAMMALIAN EMBRYO; METABOLISM; MOLECULAR MODEL; MOUSE; ORGANOGENESIS; PROMOTER REGION; PROTEIN DOMAIN; TRANSGENIC MOUSE; X RAY CRYSTALLOGRAPHY;

ANIMALS; CELL DIFFERENTIATION; CRYSTALLOGRAPHY, X-RAY; EMBRYO, MAMMALIAN; GATA4 TRANSCRIPTION FACTOR; HOMEOBOX PROTEIN NKX-2.5; HOMEODOMAIN PROTEINS; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MYOCARDIUM; ORGANOGENESIS; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION DOMAINS AND MOTIFS; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 84959387425     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.01.004     Document Type: Article

References (48)

1. C.T. Basson, D.R. Bachinsky, R.C. Lin, T. Levi, J.A. Elkins, J. Soults, D. Grayzel, E. Kroumpouzou, T.A. Traill, J. Leblanc-Straceski, and et al. Mutations in human TBX5 [corrected] cause limb and cardiac malformation in Holt-Oram syndrome Nat. Genet. 15 1997 30 35
2. L.A. Boyer, T.I. Lee, M.F. Cole, S.E. Johnstone, S.S. Levine, J.P. Zucker, M.G. Guenther, R.M. Kumar, H.L. Murray, R.G. Jenner, and et al. Core transcriptional regulatory circuitry in human embryonic stem cells Cell 122 2005 947 956
3. B.G. Bruneau The developmental genetics of congenital heart disease Nature 451 2008 943 948
4. B.G. Bruneau, G. Nemer, J.P. Schmitt, F. Charron, L. Robitaille, S. Caron, D.A. Conner, M. Gessler, M. Nemer, C.E. Seidman, and J.G. Seidman A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease Cell 106 2001 709 721
5. E.H. Davidson Emerging properties of animal gene regulatory networks Nature 468 2010 911 920
6. S. De Val, N.C. Chi, S.M. Meadows, S. Minovitsky, J.P. Anderson, I.S. Harris, M.L. Ehlers, P. Agarwal, A. Visel, S.M. Xu, and et al. Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors Cell 135 2008 1053 1064
7. D. Durocher, C.Y. Chen, A. Ardati, R.J. Schwartz, and M. Nemer The atrial natriuretic factor promoter is a downstream target for Nkx-2.5 in the myocardium Mol. Cell. Biol. 16 1996 4648 4655
8. D. Durocher, F. Charron, R. Warren, R.J. Schwartz, and M. Nemer The cardiac transcription factors Nkx2-5 and GATA-4 are mutual cofactors EMBO J. 16 1997 5687 5696
9. V. Garg, I.S. Kathiriya, R. Barnes, M.K. Schluterman, I.N. King, C.A. Butler, C.R. Rothrock, R.S. Eapen, K. Hirayama-Yamada, K. Joo, and et al. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5 Nature 424 2003 443 447
10. T.K. Ghosh, E.A. Packham, A.J. Bonser, T.E. Robinson, S.J. Cross, and J.D. Brook Characterization of the TBX5 binding site and analysis of mutations that cause Holt-Oram syndrome Hum. Mol. Genet. 10 2001 1983 1994
11. A. He, S.W. Kong, Q. Ma, and W.T. Pu Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart Proc. Natl. Acad. Sci. USA 108 2011 5632 5637
12. Y. Hiroi, S. Kudoh, K. Monzen, Y. Ikeda, Y. Yazaki, R. Nagai, and I. Komuro Tbx5 associates with Nkx2-5 and synergistically promotes cardiomyocyte differentiation Nat. Genet. 28 2001 276 280
13. M. Ieda, J.D. Fu, P. Delgado-Olguin, V. Vedantham, Y. Hayashi, B.G. Bruneau, and D. Srivastava Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors Cell 142 2010 375 386
14. A. Jolma, J. Yan, T. Whitington, J. Toivonen, K.R. Nitta, P. Rastas, E. Morgunova, M. Enge, M. Taipale, G. Wei, and et al. DNA-binding specificities of human transcription factors Cell 152 2013 327 339
15. A. Jolma, Y. Yin, K.R. Nitta, K. Dave, A. Popov, M. Taipale, M. Enge, T. Kivioja, E. Morgunova, and J. Taipale DNA-dependent formation of transcription factor pairs alters their binding specificity Nature 527 2015 384 388
16. G. Junion, M. Spivakov, C. Girardot, M. Braun, E.H. Gustafson, E. Birney, and E.E. Furlong A transcription factor collective defines cardiac cell fate and reflects lineage history Cell 148 2012 473 486
17. S.J. Kattman, A.D. Witty, M. Gagliardi, N.C. Dubois, M. Niapour, A. Hotta, J. Ellis, and G. Keller Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines Cell Stem Cell 8 2011 228 240
18. M. Levo, and E. Segal In pursuit of design principles of regulatory sequences Nat. Rev. Genet. 15 2014 453 468
19. Q.Y. Li, R.A. Newbury-Ecob, J.A. Terrett, D.I. Wilson, A.R. Curtis, C.H. Yi, T. Gebuhr, P.J. Bullen, S.C. Robson, T. Strachan, and et al. Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family Nat. Genet. 15 1997 21 29
20. I. Lyons, L.M. Parsons, L. Hartley, R. Li, J.E. Andrews, L. Robb, and R.P. Harvey Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5 Genes Dev. 9 1995 1654 1666
21. M. Maitra, M.K. Schluterman, H.A. Nichols, J.A. Richardson, C.W. Lo, D. Srivastava, and V. Garg Interaction of Gata4 and Gata6 with Tbx5 is critical for normal cardiac development Dev. Biol. 326 2009 368 377
22. A.D. Mori, Y. Zhu, I. Vahora, B. Nieman, K. Koshiba-Takeuchi, L. Davidson, A. Pizard, J.G. Seidman, C.E. Seidman, X.J. Chen, and et al. Tbx5-dependent rheostatic control of cardiac gene expression and morphogenesis Dev. Biol. 297 2006 566 586
23. I.P. Moskowitz, J.B. Kim, M.L. Moore, C.M. Wolf, M.A. Peterson, J. Shendure, M.A. Nobrega, Y. Yokota, C. Berul, S. Izumo, and et al. A molecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development Cell 129 2007 1365 1376
24. A. Nagy, M. Gertsenstein, K. Vintersten, and R. Behringer Manipulating the Mouse Embryo. A Laboratory Manual Third Edition 2003 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
25. M. Pashmforoush, J.T. Lu, H. Chen, T.S. Amand, R. Kondo, S. Pradervand, S.M. Evans, B. Clark, J.R. Feramisco, W. Giles, and et al. Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block Cell 117 2004 373 386
26. L. Pradhan, C. Genis, P. Scone, E.O. Weinberg, H. Kasahara, and H.J. Nam Crystal structure of the human NKX2.5 homeodomain in complex with DNA target Biochemistry 51 2012 6312 6319
27. O.W. Prall, M.K. Menon, M.J. Solloway, Y. Watanabe, S. Zaffran, F. Bajolle, C. Biben, J.J. McBride, B.R. Robertson, H. Chaulet, and et al. An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation Cell 128 2007 947 959
28. L. Qian, Y. Huang, C.I. Spencer, A. Foley, V. Vedantham, L. Liu, S.J. Conway, J.D. Fu, and D. Srivastava In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes Nature 485 2012 593 598
29. H.S. Rhee, and B.F. Pugh Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution Cell 147 2011 1408 1419
30. N.J. Sakabe, I. Aneas, T. Shen, L. Shokri, S.Y. Park, M.L. Bulyk, S.M. Evans, and M.A. Nobrega Dual transcriptional activator and repressor roles of TBX20 regulate adult cardiac structure and function Hum. Mol. Genet. 21 2012 2194 2204
31. J.-J. Schott, D.W. Benson, C.T. Basson, W. Pease, G.M. Silberbach, J.P. Moak, B.J. Maron, C.E. Seidman, and J.G. Seidman Congenital heart disease caused by mutations in the transcription factor NKX2-5 Science 281 1998 108 111
32. A.A. Serandour, G.D. Brown, J.D. Cohen, and J.S. Carroll Development of an Illumina-based ChIP-exonuclease method provides insight into FoxA1-DNA binding properties Genome Biol. 14 2013 R147
33. P. Shankaranarayanan, M.A. Mendoza-Parra, M. Walia, L. Wang, N. Li, L.M. Trindade, and H. Gronemeyer Single-tube linear DNA amplification (LinDA) for robust ChIP-seq Nat. Methods 8 2011 565 567
34. T. Shen, I. Aneas, N. Sakabe, R.J. Dirschinger, G. Wang, S. Smemo, J.M. Westlund, H. Cheng, N. Dalton, Y. Gu, and et al. Tbx20 regulates a genetic program essential to adult mouse cardiomyocyte function J. Clin. Invest. 121 2011 4640 4654
35. R. Siersbæk, A. Rabiee, R. Nielsen, S. Sidoli, S. Traynor, A. Loft, L. La Cour Poulsen, A. Rogowska-Wrzesinska, O.N. Jensen, and S. Mandrup Transcription factor cooperativity in early adipogenic hotspots and super-enhancers Cell Rep. 7 2014 1443 1455
36. K. Song, Y.J. Nam, X. Luo, X. Qi, W. Tan, G.N. Huang, A. Acharya, C.L. Smith, M.D. Tallquist, E.G. Neilson, and et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors Nature 485 2012 599 604
37. F. Spitz, and E.E. Furlong Transcription factors: from enhancer binding to developmental control Nat. Rev. Genet. 13 2012 613 626
38. K. Stefflova, D. Thybert, M.D. Wilson, I. Streeter, J. Aleksic, P. Karagianni, A. Brazma, D.J. Adams, I. Talianidis, J.C. Marioni, and et al. Cooperativity and rapid evolution of cobound transcription factors in closely related mammals Cell 154 2013 530 540
39. C.U. Stirnimann, D. Ptchelkine, C. Grimm, and C.W. Müller Structural basis of TBX5-DNA recognition: the T-box domain in its DNA-bound and -unbound form J. Mol. Biol. 400 2010 71 81
40. J.K. Takeuchi, and B.G. Bruneau Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors Nature 459 2009 708 711
41. M. Tanaka, Z. Chen, S. Bartunkova, N. Yamasaki, and S. Izumo The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development Development 126 1999 1269 1280
42. M.R. Tijssen, A. Cvejic, A. Joshi, R.L. Hannah, R. Ferreira, A. Forrai, D.C. Bellissimo, S.H. Oram, P.A. Smethurst, N.K. Wilson, and et al. Genome-wide analysis of simultaneous GATA1/2, RUNX1, FLI1, and SCL binding in megakaryocytes identifies hematopoietic regulators Dev. Cell 20 2011 597 609
43. A.M. Tsankov, H. Gu, V. Akopian, M.J. Ziller, J. Donaghey, I. Amit, A. Gnirke, and A. Meissner Transcription factor binding dynamics during human ES cell differentiation Nature 518 2015 344 349
44. M. van den Boogaard, L.Y. Wong, F. Tessadori, M.L. Bakker, L.K. Dreizehnter, V. Wakker, C.R. Bezzina, P.A. 't Hoen, J. Bakkers, P. Barnett, and V.M. Christoffels Genetic variation in T-box binding element functionally affects SCN5A/SCN10A enhancer J. Clin. Invest. 122 2012 2519 2530
45. J.A. Wamstad, J.M. Alexander, R.M. Truty, A. Shrikumar, F. Li, K.E. Eilertson, H. Ding, J.N. Wylie, A.R. Pico, J.A. Capra, and et al. Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage Cell 151 2012 206 220
46. N.K. Wilson, S.D. Foster, X. Wang, K. Knezevic, J. Schütte, P. Kaimakis, P.M. Chilarska, S. Kinston, W.H. Ouwehand, E. Dzierzak, and et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators Cell Stem Cell 7 2010 532 544
47. K.S. Zaret, and M. Grompe Generation and regeneration of cells of the liver and pancreas Science 322 2008 1490 1494
48. R.P. Zinzen, C. Girardot, J. Gagneur, M. Braun, and E.E. Furlong Combinatorial binding predicts spatio-temporal cis-regulatory activity Nature 462 2009 65 70