The Cardiac TBX5 Interactome Reveals a Chromatin Remodeling Network Essential for Cardiac Septation

Developmental Cell

Volumn 36, Issue 3, 2016, Pages 262-275

  Waldron, Lauren ^a   Steimle, Jeffrey D ^d   Greco, Todd M ^c   Gomez, Nicholas C ^a   Dorr, Kerry M ^a   Kweon, Junghun ^d   Temple, Brenda ^b   Yang, Xinan Holly ^d   Wilczewski, Caralynn M ^a   Davis, Ian J ^a,b   Cristea, Ileana M ^c   Moskowitz, Ivan P ^d   Conlon, Frank L ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c PRINCETON UNIVERSITY   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE; INTERACTOME; PROTEOME; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR 5;

ALLELE; ALPHA HELIX; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; FEMALE; GENE EXPRESSION; GENE REPRESSION; GENETIC ANALYSIS; HEART DEVELOPMENT; HEART VENTRICLE SEPTUM; HUMAN; HUMAN CELL; MALE; MISSENSE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CARDIAC MUSCLE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HEART; METABOLISM; ORGANOGENESIS; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HUMANS; MICE, TRANSGENIC; MYOCARDIUM; ORGANOGENESIS; T-BOX DOMAIN PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84958661999     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.01.009     Document Type: Article

References (81)

1. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data 2010, Babraham Informatics. http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
2. Baban A., Pitto L., Pulignani S., Cresci M., Mariani L., Gambacciani C., Digilio M.C., Pongiglione G., Albanese S. Holt-Oram syndrome with intermediate atrioventricular canal defect, and aortic coarctation: functional characterization of a de novo TBX5 mutation. Am. J. Med. Genet. A 2014, 164A:1419-1424.
3. Basson C.T., Cowley G.S., Solomon S.D., Weissman B., Poznanski A.K., Traill T.A., Seidman J.G., Seidman C.E. The clinical and genetic spectrum of the Holt-Oram syndrome (heart-hand syndrome). N. Engl. J. Med. 1994, 330:885-891.
4. 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. Mutations in human TBX5 [corrected] cause limb and cardiac malformation in Holt-Oram syndrome. Nat. Genet. 1997, 15:30-35.
5. Basson C.T., Huang T., Lin R.C., Bachinsky D.R., Weremowicz S., Vaglio A., Bruzzone R., Quadrelli R., Lerone M., Romeo G., et al. Different TBX5 interactions in heart and limb defined by Holt-Oram syndrome mutations. Proc. Natl. Acad. Sci. USA 1999, 96:2919-2924.
6. Bayer E.A., Wilchek M. The use of the avidin-biotin complex as a tool in molecular biology. Methods Biochem. Anal. 1980, 26:1-45.
7. Benson D.W., Basson C.T., MacRae C.A. New understandings in the genetics of congenital heart disease. Curr. Opin. Pediatr. 1996, 8:505-511.
8. Berk A.J. Activation of RNA polymerase II transcription. Curr. Opin. Cell Biol. 1999, 11:330-335.
9. Brown D.D., Martz S.N., Binder O., Goetz S.C., Price B.M., Smith J.C., Conlon F.L. Tbx5 and Tbx20 act synergistically to control vertebrate heart morphogenesis. Development 2005, 132:553-563.
10. Bruneau B.G., Logan M., Davis N., Levi T., Tabin C.J., Seidman J.G., Seidman C.E. Chamber-specific cardiac expression of Tbx5 and heart defects in Holt-Oram syndrome. Dev. Biol. 1999, 211:100-108.
11. 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. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 2001, 106:709-721.
12. Cline M.S., Smoot M., Cerami E., Kuchinsky A., Landys N., Workman C., Christmas R., Avila-Campilo I., Creech M., Gross B., et al. Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2007, 2:2366-2382.
13. Costantini J.L., Cheung S.M., Hou S., Li H., Kung S.K., Johnston J.B., Wilkins J.A., Gibson S.B., Marshall A.J. TAPP2 links phosphoinositide 3-kinase signaling to B-cell adhesion through interaction with the cytoskeletal protein utrophin: expression of a novel cell adhesion-promoting complex in B-cell leukemia. Blood 2009, 114:4703-4712.
14. Cristea I.M., Williams R., Chait B.T., Rout M.P. Fluorescent proteins as proteomic probes. Mol. Cell Proteomics 2005, 4:1933-1941.
15. Cross S.J., Ching Y.H., Li Q.Y., Armstrong-Buisseret L., Spranger S., Lyonnet S., Bonnet D., Penttinen M., Jonveaux P., Leheup B., et al. The mutation spectrum in Holt-Oram syndrome. J. Med. Genet. 2000, 37:785-787.
16. Denslow S.A., Wade P.A. The human Mi-2/NuRD complex and gene regulation. Oncogene 2007, 26:5433-5438.
17. Diez-Roux G., Banfi S., Sultan M., Geffers L., Anand S., Rozado D., Magen A., Canidio E., Pagani M., Peluso I., et al. A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol. 2011, 9:e1000582.
18. Dolk H., Loane M., Garne E. The prevalence of congenital anomalies in Europe. Adv. Exp. Med. Biol. 2010, 686:349-364.
19. Dorr K.M., Amin N.M., Kuchenbrod L.M., Labiner H., Charpentier M.S., Pevny L.H., Wessels A., Conlon F.L. Casz1 is required for cardiomyocyte G1-to-phase progression during mammalian cardiac development. Development 2015, 142:2037-2047.
20. Driegen S., Ferreira R., van Zon A., Strouboulis J., Jaegle M., Grosveld F., Philipsen S., Meijer D. A generic tool for biotinylation of tagged proteins in transgenic mice. Transgenic Res. 2005, 14:477-482.
21. Evans P.M., Liu C. Roles of Krupel-like factor 4 in normal homeostasis, cancer and stem cells. Acta Biochim. Biophys. Sin (Shanghai) 2008, 40:554-564.
22. Fan C., Duhagon M.A., Oberti C., Chen S., Hiroi Y., Komuro I., Duhagon P.I., Canessa R., Wang Q. Novel TBX5 mutations and molecular mechanism for Holt-Oram syndrome. J. Med. Genet. 2003, 40:e29.
23. Fan C., Liu M., Wang Q. Functional analysis of TBX5 missense mutations associated with Holt-Oram syndrome. J. Biol. Chem. 2003, 278:8780-8785.
24. Franceschini A., Szklarczyk D., Frankild S., Kuhn M., Simonovic M., Roth A., Lin J., Minguez P., Bork P., von Mering C., et al. STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 2013, 41:D808-D815.
25. Franklin S., Zhang M.J., Chen H., Paulsson A.K., Mitchell-Jordan S.A., Li Y., Ping P., Vondriska T.M. Specialized compartments of cardiac nuclei exhibit distinct proteomic anatomy. Mol. Cell Proteomics 2011, 10. M110 000703.
26. 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. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 2003, 424:443-447.
27. Ghosh T.K., Song F.F., Packham E.A., Buxton S., Robinson T.E., Ronksley J., Self T., Bonser A.J., Brook J.D. Physical interaction between TBX5 and MEF2C is required for early heart development. Mol. Cell Biol. 2009, 29:2205-2218.
28. Gittenberger-de Groot A.C., Calkoen E.E., Poelmann R.E., Bartelings M.M., Jongbloed M.R. Morphogenesis and molecular considerations on congenital cardiac septal defects. Ann. Med. 2014, 46:640-652.
29. Goetz S.C., Brown D.D., Conlon F.L. TBX5 is required for embryonic cardiac cell cycle progression. Development 2006, 133:2575-2584.
30. Hatcher C.J., Kim M.S., Mah C.S., Goldstein M.M., Wong B., Mikawa T., Basson C.T. TBX5 transcription factor regulates cell proliferation during cardiogenesis. Dev. Biol. 2001, 230:177-188.
31. Hayashi S., Lewis P., Pevny L., McMahon A.P. Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech. Dev. 2002, 119(Suppl 1):S97-S101.
32. He A., Kong S.W., Ma Q., Pu W.T. Co-occupancy by multiple cardiac transcription factors identifies transcriptional enhancers active in heart. Proc. Natl. Acad. Sci. USA 2011, 108:5632-5637.
33. Heinritz W., Shou L., Moschik A., Froster U.G. The human TBX5 gene mutation database. Hum. Mutat. 2005, 26:397.
34. Heinz S., Benner C., Spann N., Bertolino E., Lin Y.C., Laslo P., Cheng J.X., Murre C., Singh H., Glass C.K. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 2010, 38:576-589.
35. Heron M., Tejada-Vera B. Deaths: leading causes for 2005. Natl. Vital Stat. Rep. 2009, 58:1-97.
36. Hiroi Y., Kudoh S., Monzen K., Ikeda Y., Yazaki Y., Nagai R., Komuro I. Tbx5 associates with Nkx2-and synergistically promotes cardiomyocyte differentiation. Nat. Genet. 2001, 28:276-280.
37. Hoffmann A.D., Yang X.H., Burnicka-Turek O., Bosman J.D., Ren X., Steimle J.D., Vokes S.A., McMahon A.P., Kalinichenko V.V., Moskowitz I.P. Foxf genes integrate tbx5 and hedgehog pathways in the second heart field for cardiac septation. PLoS Genet. 2014, 10:e1004604.
38. Holt M., Oram S. Familial heart disease with skeletal malformations. Br. Heart J. 1960, 22:236-242.
39. Hu S., Li L., Yeh S., Cui Y., Li X., Chang H.C., Jin J., Chang C. Infiltrating T cells promote prostate cancer metastasis via modulation of FGF11-->miRNA-541-->androgen receptor (AR)-->MMP9 signaling. Mol. Oncol. 2015, 9:44-57.
40. Huang C.C., Tu S.H., Lien H.H., Jeng J.Y., Huang C.S., Huang C.J., Lai L.C., Chuang E.Y. Concurrent gene signatures for Han Chinese breast cancers. PLoS One 2013, 8:e76421.
41. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
42. Ieda M., Fu J.D., Delgado-Olguin P., Vedantham V., Hayashi Y., Bruneau B.G., Srivastava D. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010, 142:375-386.
43. Kaltenbrun E., Greco T.M., Slagle C.E., Kennedy L.M., Li T., Cristea I.M., Conlon F.L. A Gro/TLE-NuRD corepressor complex facilitates Tbx20-dependent transcriptional repression. J. Proteome Res. 2013, 12:5395-5409.
44. Kehle J., Beuchle D., Treuheit S., Christen B., Kennison J.A., Bienz M., Muller J. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 1998, 282:1897-1900.
45. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74:5383-5392.
46. Kim J., Cantor A.B., Orkin S.H., Wang J. Use of in vivo biotinylation to study protein-protein and protein-DNA interactions in mouse embryonic stem cells. Nat. Protoc. 2009, 4:506-517.
47. Kim D., Pertea G., Trapnell C., Pimentel H., Kelley R., Salzberg S.L. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013, 14:R36.
48. Kimura R., Kasamatsu A., Koyama T., Fukumoto C., Kouzu Y., Higo M., Endo-Sakamoto Y., Ogawara K., Shiiba M., Tanzawa H., et al. Glutamate acid decarboxylase 1 promotes metastasis of human oral cancer by beta-catenin translocation and MMP7 activation. BMC Cancer 2013, 13:555.
49. Krause A., Zacharias W., Camarata T., Linkhart B., Law E., Lischke A., Miljan E., Simon H.G. Tbx5 and Tbx4 transcription factors interact with a new chicken PDZ-LIM protein in limb and heart development. Dev. Biol. 2004, 273:106-120.
50. Krebs S., Fischaleck M., Blum H. A simple and loss-free method to remove TRIzol contaminations from minute RNA samples. Anal. Biochem. 2009, 387:136-138.
51. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
52. Lassmann T., Hayashizaki Y., Daub C.O. TagDust-program to eliminate artifacts from next generation sequencing data. Bioinformatics 2009, 25:2839-2840.
53. 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. Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat. Genet. 1997, 15:21-29.
54. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
55. Liu Z., Yang X., Li Z., McMahon C., Sizer C., Barenboim-Stapleton L., Bliskovsky V., Mock B., Ried T., London W.B., et al. CASZ1, a candidate tumor-suppressor gene, suppresses neuroblastoma tumor growth through reprogramming gene expression. Cell Death Differ. 2011, 18:1174-1183.
56. Maine G.N., Li H., Zaidi I.W., Basrur V., Elenitoba-Johnson K.S., Burstein E. A bimolecular affinity purification method under denaturing conditions for rapid isolation of a ubiquitinated protein for mass spectrometry analysis. Nat. Protoc. 2010, 5:1447-1459.
57. McDermott D.A., Bressan M.C., He J., Lee J.S., Aftimos S., Brueckner M., Gilbert F., Graham G.E., Hannibal M.C., Innis J.W., et al. TBX5 genetic testing validates strict clinical criteria for Holt-Oram syndrome. Pediatr. Res. 2005, 58:981-986.
58. Metz M., Gassmann M., Fakler B., Schaeren-Wiemers N., Bettler B. Distribution of the auxiliary GABAB receptor subunits KCTD8, 12, 12b, and 16 in the mouse brain. J. Comp. Neurol. 2011, 519:1435-1454.
59. Mori A.D., Bruneau B.G. TBX5 mutations and congenital heart disease: Holt-Oram syndrome revealed. Curr. Opin. Cardiol. 2004, 19:211-215.
60. Moskowitz I.P., Pizard A., Patel V.V., Bruneau B.G., Kim J.B., Kupershmidt S., Roden D., Berul C.I., Seidman C.E., Seidman J.G. The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development 2004, 131:4107-4116.
61. Moskowitz I.P., Kim J.B., Moore M.L., Wolf C.M., Peterson M.A., Shendure J., Nobrega M.A., Yokota Y., Berul C., Izumo S., et al. A molecular pathway including Id2, Tbx5, and Nkx2-required for cardiac conduction system development. Cell 2007, 129:1365-1376.
62. Murakami M., Nakagawa M., Olson E.N., Nakagawa O. A WW domain protein TAZ is a critical coactivator for TBX5, a transcription factor implicated in Holt-Oram syndrome. Proc. Natl. Acad. Sci. USA 2005, 102:18034-18039.
63. Polo S.E., Kaidi A., Baskcomb L., Galanty Y., Jackson S.P. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 2010, 29:3130-3139.
64. Qian L., Huang Y., Spencer C.I., Foley A., Vedantham V., Liu L., Conway S.J., Fu J.D., Srivastava D. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485:593-598.
65. Roesli C., Neri D., Rybak J.N. In vivo protein biotinylation and sample preparation for the proteomic identification of organ- and disease-specific antigens accessible from the vasculature. Nat. Protoc. 2006, 1:192-199.
66. Saunders A., Werner J., Andrulis E.D., Nakayama T., Hirose S., Reinberg D., Lis J.T. Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 2003, 301:1094-1096.
67. Smallwood P.M., Munoz-Sanjuan I., Tong P., Macke J.P., Hendry S.H., Gilbert D.J., Copeland N.G., Jenkins N.A., Nathans J. Fibroblast growth factor (FGF) homologous factors: new members of the FGF family implicated in nervous system development. Proc. Natl. Acad. Sci. USA 1996, 93:9850-9857.
68. Sopher B.L., Koszdin K.L., McClain M.E., Myrick S.B., Martinez R.A., Smith A.C., La Spada A.R. Genomic organization, chromosome location, and expression analysis of mouse beta-synuclein, a candidate for involvement in neurodegeneration. Cytogenet. Cell Genet. 2001, 93:117-123.
69. Stirnimann C.U., Ptchelkine D., Grimm C., Muller C.W. Structural basis of TBX5-DNA recognition: the T-box domain in its DNA-bound and -unbound form. J. Mol. Biol. 2010, 400:71-81.
70. Takeuchi J.K., Lou X., Alexander J.M., Sugizaki H., Delgado-Olguin P., Holloway A.K., Mori A.D., Wylie J.N., Munson C., Zhu Y., et al. Chromatin remodelling complex dosage modulates transcription factor function in heart development. Nat. Commun. 2011, 2:187.
71. Trapnell C., Roberts A., Goff L., Pertea G., Kim D., Kelley D.R., Pimentel H., Salzberg S.L., Rinn J.L., Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 2012, 7:562-578.
72. Trifonov S., Yamashita Y., Kase M., Maruyama M., Sugimoto T. Glutamic acid decarboxylase 1 alternative splicing isoforms: characterization, expression and quantification in the mouse brain. BMC Neurosci. 2014, 15:114.
73. van Werven F.J., Timmers H.T. The use of biotin tagging in Saccharomyces cerevisiae improves the sensitivity of chromatin immunoprecipitation. Nucleic Acids Res. 2006, 34:e33.
74. Wade P.A., Jones P.L., Vermaak D., Wolffe A.P. A multiple subunit Mi-histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr. Biol. 1998, 8:843-846.
75. Wang J., Rao S., Chu J., Shen X., Levasseur D.N., Theunissen T.W., Orkin S.H. A protein interaction network for pluripotency of embryonic stem cells. Nature 2006, 444:364-368.
76. Wang C., Cao D., Wang Q., Wang D.Z. Synergistic activation of cardiac genes by myocardin and tbx5. PLoS One 2011, 6:e24242.
77. Wang S., Sun H., Ma J., Zang C., Wang C., Wang J., Tang Q., Meyer C.A., Zhang Y., Liu X.S. Target analysis by integration of transcriptome and ChIP-seq data with BETA. Nat. Protoc. 2013, 8:2502-2515.
78. Wang W., Kim H.J., Lee J.H., Wong V., Sihn C.R., Lv P., Perez Flores M.C., Mousavi-Nik A., Doyle K.J., Xu Y., et al. Functional significance of K+ channel beta-subunit KCNE3 in auditory neurons. J. Biol. Chem. 2014, 289:16802-16813.
79. Xue Y., Wong J., Moreno G.T., Young M.K., Cote J., Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol. Cell 1998, 2:851-861.
80. Ying C.Y., Dominguez-Sola D., Fabi M., Lorenz I.C., Hussein S., Bansal M., Califano A., Pasqualucci L., Basso K., Dalla-Favera R. MEF2B mutations lead to deregulated expression of the oncogene BCL6 in diffuse large B cell lymphoma. Nat. Immunol. 2013, 14:1084-1092.
81. Zhang Y., Liu T., Meyer C.A., Eeckhoute J., Johnson D.S., Bernstein B.E., Nusbaum C., Myers R.M., Brown M., Li W., et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008, 9:R137.