T-box transcription factor 3 governs a transcriptional program for the function of the mouse atrioventricular conduction system
Open accessAbstract
Significance: Genome-wide association studies have identified common noncoding variants associated with ECG parameters in the TBX3 locus, suggesting that a modest change in TBX3/Tbx3 expression level affects heart function. We characterized the morphology, physiology, and gene expression profile of the atrioventricular conduction system in a Tbx3 haploinsufficient mouse model. We identified Tbx3-dependent regulatory DNA elements active in the atrioventricular conduction system and validated the functionality of these elements in vivo. Using genome editing, we deleted a regulatory DNA element from the mouse genome and show it drives expression of Cacna1g in the cardiac conduction system. Our study unveils a Tbx3-dependent gene regulatory network in the AV conduction system that contributes to heart electrophysiology.
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The Tbx3-Venus reporter system is validated.
“To visualize the activity of the murine Tbx3 promoter at the protein level, we used a validated Tbx3-Venus (Tbx3tm1(Venus)Vmc) [11, 42–47] reporter system (Fig. 2a).”
From TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration (2023) · cites this paper as [44]
The available indexed passages labeled Abstract contain citation metadata and keywords, but no description or validation of a Tbx3-Venus reporter. Searches for “Venus,” “validated reporter system,” and the allele name found no relevant passage, so this copy cannot establish the claim. (LLM, conf=0.73)
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A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping
Rao, S. S. P., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., Sanborn, A. L., Machol, I., Omer, A. D., Lander, E. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.021 · Cited by 9,212 · see citing works
Topological domains in mammalian genomes identified by analysis of chromatin interactions
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., & Ren, B. (2012) · Nature · doi:10.1038/nature11082 · Cited by 6,829 · see citing works
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422 · see citing works
The Human Transcription Factors
Lambert, S. A., Jolma, A., Campitelli, L. F., Das, P. K., Yin, Y., Albu, M., Chen, X., Taipale, J., Hughes, T. R., & Weirauch, M. T. (2018) · Cell · doi:10.1016/j.cell.2018.01.029 · Cited by 3,399 · see citing works
Spatial partitioning of the regulatory landscape of the X-inactivation centre
Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N. L., Meisig, J., Sedat, J., et al. (2012) · Nature · doi:10.1038/nature11049 · Cited by 2,895 · see citing works
Ever-Changing Landscapes: Transcriptional Enhancers in Development and Evolution
Long, H. K., Prescott, S. L., & Wysocka, J. (2016) · Cell · doi:10.1016/j.cell.2016.09.018 · Cited by 945 · see citing works
Cardiomyocyte DNA synthesis and binucleation during murine development
Soonpaa, M. H., Kim, K. K., Pajak, L., Franklin, M. T., & Field, L. J. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.5.h2183 · Cited by 718 · see citing works
Enhancer redundancy provides phenotypic robustness in mammalian development
Osterwalder, M., Barozzi, I., Tissières, V., Fukuda-Yuzawa, Y., Mannion, B. J., Afzal, S. Y., Lee, E. A., Zhu, Y., Plajzer-Frick, I., Pickle, C. S., et al. (2018) · Nature · doi:10.1038/nature25461 · Cited by 642 · see citing works
Calcium Signaling and Cardiac Arrhythmias
Landstrom, A. P., Dobrev, D., & Wehrens, X. H. T. (2017) · Circulation Research · doi:10.1161/circresaha.117.310083 · Cited by 571 · see citing works
Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome
Bamshad, M., Lin, R. C., Law, D. J., Watkins, W. S., Krakowiak, P. A., Moore, M. E., Franceschini, P., Lala, R., Holmes, L. B., Gebuhr, T. C., et al. (1997) · Nature Genetics · doi:10.1038/ng0797-311 · Cited by 540 · see citing works
Genome-wide association study of PR interval
Pfeufer, A., van Noord, C., Marciante, K. D., Arking, D. E., Larson, M. G., Smith, A. V., Tarasov, K. V., Müller‐Nurasyid, M., Sotoodehnia, N., Sinner, M. F., et al. (2010) · Nature Genetics · doi:10.1038/ng.517 · Cited by 434 · see citing works
Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria
Hoogaars, W. M. H., Engel, A., Brons, J. F., Verkerk, A. O., de Lange, F. J., Wong, L. Y. E., Bakker, M. L., Clout, D. E., Wakker, V., Barnett, P., et al. (2007) · Genes & Development · doi:10.1101/gad.416007 · Cited by 409 · see citing works
Self-citationMolecular Architecture of the Human Sinus Node
Chandler, N. J., Greener, I. D., Tellez, J. O., Inada, S., Musa, H., Molenaar, P., DiFrancesco, D., Baruscotti, M., Longhi, R., Anderson, R. H., et al. (2009) · Circulation · doi:10.1161/circulationaha.108.804369 · Cited by 400 · see citing works
The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart.
Hoogaars, W. M., Tessari, A., Moorman, A., de Boer, P. D., Hagoort, J., Soufan, A., Campione, M., & Christoffels, V. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.01.030 · Cited by 378 · see citing works
Self-citationCommon variants in 22 loci are associated with QRS duration and cardiac ventricular conduction
Sotoodehnia, N., Isaacs, A. J., de Bakker, P. I. W., Dörr, M., Newton‐Cheh, C., Nolte, I. M., van der Harst, P., Müller‐Nurasyid, M., Eijgelsheim, M., Alonso, Á., et al. (2010) · Nature Genetics · doi:10.1038/ng.716 · Cited by 349 · see citing works
Marionneau, C., Couette, B., Liu, J., Li, H., Mangoni, M. E., Nargeot, J., Lei, M., Escande, D., & Demolombe, S. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.074047 · Cited by 347 · see citing works
Regulation of disease-associated gene expression in the 3D genome
Krijger, P. H. L., & de Laat, W. L. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.138 · Cited by 316 · see citing works
Mangoni, M. E., Traboulsie, A., Léoni, A., Couette, B., Marger, L., Quang, K. L., Kupfer, E., Cohen-Solal, A., Vilar, J., Shin, H., et al. (2006) · Circulation Research · doi:10.1161/01.res.0000225862.14314.49 · Cited by 310 · see citing works
Moskowitz, I. P. G., Kim, J. B., Moore, M. L. G., Wolf, C. M., Peterson, M. A., Shendure, J., Nóbrega, M. A., Yokota, Y., Berul, C. I., Izumo, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.04.036 · Cited by 284 · see citing works
No Evidence for Cardiomyocyte Number Expansion in Preadolescent Mice
Alkass, K., Panula, J., Westman, M., Wu, T., Guerquin‐Kern, J., & Bergmann, O. (2015) · Cell · doi:10.1016/j.cell.2015.10.035 · Cited by 242 · see citing works
HCN4 Dynamically Marks the First Heart Field and Conduction System Precursors
Liang, X., Wang, G., Lin, L., Lowe, J., Zhang, Q., Bu, L., Chen, Y., Chen, J., Sun, Y., & Evans, S. Μ. (2013) · Circulation Research · doi:10.1161/circresaha.113.301588 · Cited by 237 · see citing works
Moskowitz, I. P., Pizard, A., Patel, V. V., Bruneau, B. G., Kim, J. B., Kupershmidt, S., Roden, D., Berul, C., Seidman, C., & Seidman, J. (2004) · Development · doi:10.1242/dev.01265 · Cited by 234 · see citing works
Architectural and functional asymmetry of the His–Purkinje system of the murine heart
Miquerol, L., Meysen, S., Mangoni, M. E., Bois, P., van Rijen, H. V. M., Abran, P., Jongsma, H. J., Nargeot, J., & Gros, D. B. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2004.03.007 · Cited by 212 · see citing works
Luna‐Zurita, L., Stirnimann, C. U., Glatt, S., Kaynak, B. L., Thomas, S., Baudin, F., Samee, M. A. H., He, D. X., Small, E. M., Mileikovsky, M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.01.004 · Cited by 207 · see citing works
Genetic variation in T-box binding element functionally affects SCN5A/SCN10A enhancer
van den Boogaard, M., Wong, L. Y. E., Tessadori, F., Bakker, M. L., Dreizehnter, L., Wakker, V., Bezzina, C. R., Hoen, P. A. C. ’., Bakkers, J., Barnett, P., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci62613 · Cited by 200 · see citing works
Self-citationBakker, M. L., Boukens, B. J., Mommersteeg, M. T. M., Brons, J. F., Wakker, V., Moorman, A. F. M., & Christoffels, V. M. (2008) · Circulation Research · doi:10.1161/circresaha.107.169565 · Cited by 199 · see citing works
Self-citationTbx5-dependent rheostatic control of cardiac gene expression and morphogenesis
Mori, A., Zhu, Y., Vahora, I., Nieman, B. J., Koshiba‐Takeuchi, K., Davidson, L., Pizard, A., Seidman, J. G., Seidman, C. E., Chen, X., et al. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.05.023 · Cited by 195 · see citing works
Cheng, G., Litchenberg, W. H., Cole, G. J., Mikawa, T., Thompson, R. P., & Gourdie, R. G. (1999) · Development · doi:10.1242/dev.126.22.5041 · Cited by 190 · see citing works
Transcriptomic Profiling of the Developing Cardiac Conduction System at Single-Cell Resolution
Goodyer, W. R., Beyersdorf, B. M., Paik, D. T., Tian, L., Li, G., Buikema, J. W., Chirikian, O., Choi, S. S., Venkatraman, S., Adams, E. L., et al. (2019) · Circulation Research · doi:10.1161/circresaha.118.314578 · Cited by 184 · see citing works
TBX5 drives Scn5a expression to regulate cardiac conduction system function
Arnolds, D. E., Liu, F., Fahrenbach, J. P., Kim, G. H., Schillinger, K. J., Smemo, S., McNally, E. M., Nóbrega, M. A., Patel, V. V., & Moskowitz, I. P. G. (2012) · Journal of Clinical Investigation · doi:10.1172/jci62617 · Cited by 164 · see citing works
Frank, D. U., Carter, K. L., Thomas, K., Burr, R. M., Bakker, M., Coetzee, W., Tristani-Firouzi, M., Bamshad, M., Christoffels, V., & Moon, A. (2011) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1115165109 · Cited by 153 · see citing works
Self-citationTbx2 and Tbx3 induce atrioventricular myocardial development and endocardial cushion formation
Singh, R., Hoogaars, W. M. H., Barnett, P., Grieskamp, T., Rana, M. S., Buermans, H. P. J., Farin, H. F., Petry, M., Heallen, T. R., Martin, J. F., et al. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0884-2 · Cited by 145 · see citing works
Self-citationAanhaanen, W. T. J., Mommersteeg, M. T. M., Norden, J., Wakker, V., Vries, C. D. G.-D., Anderson, R. H., Kispert, A., Moorman, A. F. M., & Christoffels, V. M. (2010) · Circulation Research · doi:10.1161/circresaha.110.222992 · Cited by 144 · see citing works
Self-citationThe development of the conduction system in the mouse embryo heart
Virágh, S., & Challice, C. E. (1980) · Developmental Biology · doi:10.1016/0012-1606(80)90496-0 · Cited by 139 · see citing works
Transcriptional regulation of the cardiac conduction system
van Eif, V. W. W., Devalla, H. D., Boink, G. J. J., & Christoffels, V. M. (2018) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0031-y · Cited by 135 · see citing works
Self-citationBresnick, E. H., Hewitt, K. J., Mehta, C., Keleş, S., Paulson, R. F., & Johnson, K. D. (2018) · Development · doi:10.1242/dev.151423 · Cited by 133 · see citing works
Prox1 maintains muscle structure and growth in the developing heart
Risebro, C. A., Searles, R. G., Melville, A. A. D., Ehler, E., Jina, N., Shah, S. H., Pallas, J. A., Hubank, M. J. F., Dillard, M. E., Harvey, N. L., et al. (2008) · Development · doi:10.1242/dev.030007 · Cited by 130 · see citing works
52 Genetic Loci Influencing Myocardial Mass
van der Harst, P., van Setten, J., Verweij, N., Vogler, G., Franke, L., Maurano, M. T., Wang, X., Leach, I. M., Eijgelsheim, M., Sotoodehnia, N., et al. (2016) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2016.07.729 · Cited by 126 · see citing works
Self-citationMolecular architecture of the human specialised atrioventricular conduction axis
Greener, I. D., Monfredi, O., Inada, S., Chandler, N. J., Tellez, J. O., Atkinson, A. J., Taube, M., Billeter, R., Anderson, R. H., Efimov, I. R., et al. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2010.12.017 · Cited by 122 · see citing works
He, M.-L., Wen, L., Campbell, C. E., Wu, J. Y., & Rao, Y. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.18.10212 · Cited by 120 · see citing works
Tbx20 Interacts With Smads to Confine Tbx2 Expression to the Atrioventricular Canal
Singh, R., Horsthuis, T., Farin, H. F., Grieskamp, T., Norden, J., Petry, M., Wakker, V., Moorman, A. F. M., Christoffels, V. M., & Kispert, A. (2009) · Circulation Research · doi:10.1161/circresaha.109.196063 · Cited by 118 · see citing works
Self-citationStefanovic, S., Barnett, P., van Duijvenboden, K., Weber, D., Gessler, M., & Christoffels, V. M. (2014) · Nature Communications · doi:10.1038/ncomms4680 · Cited by 105 · see citing works
Self-citationNotch signaling regulates murine atrioventricular conduction and the formation of accessory pathways
Rentschler, S., Harris, B. S., Kuznekoff, L. M., Jain, R., Manderfield, L. J., Lu, M. M., Morley, G. E., Patel, V. V., & Epstein, J. A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44470 · Cited by 103 · see citing works
Conserved NPPB + Border Zone Switches From MEF2- to AP-1–Driven Gene Program
van Duijvenboden, K., de Bakker, D. E. M., Man, J. C. K., Janssen, R., Günthel, M., Hill, M. C., Hooijkaas, I. B., van der Made, I., van der Kraak, P. H., Vink, A., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.038944 · Cited by 102 · see citing works
Self-citationGene Regulatory Networks in Cardiac Conduction System Development
Munshi, N. V. (2012) · Circulation Research · doi:10.1161/circresaha.111.260026 · Cited by 102 · see citing works
Differentiation of the Atrioventricular Conducting System of the Heart
Eichna, L. W., & DeHaan, R. L. (1961) · Circulation · doi:10.1161/01.cir.24.2.458 · Cited by 102 · see citing works
Gillers, B. S., Chiplunkar, A. R., Aly, H., Valenta, T., Basler, K., Christoffels, V. M., Efimov, I. R., Boukens, B. J., & Rentschler, S. (2014) · Circulation Research · doi:10.1161/circresaha.116.304731 · Cited by 101 · see citing works
Self-citationNtalla, I., Weng, L.-C., Cartwright, J. H., Hall, A., Sveinbjornsson, G., Tucker, N., Choi, S.-H.-A., Chaffin, M., Roselli, C., Barnes, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15706-x · Cited by 100 · see citing works
Identification of atrial fibrillation associated genes and functional non-coding variants
van Ouwerkerk, A. F., Bosada, F. M., van Duijvenboden, K., Hill, M. C., Montefiori, L. E., Scholman, K. T., Liu, J., de Vries, A. A. F., Boukens, B. J., Ellinor, P. T., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12721-5 · Cited by 94 · see citing works
Self-citationAanhaanen, W. T. J., Boukens, B. J., Sizarov, A., Wakker, V., Vries, C. D. G.-D., van Ginneken, A. C. G., Moorman, A. F. M., Coronel, R., & Christoffels, V. M. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44350 · Cited by 93 · see citing works
Self-citationHorsthuis, T., Buermans, H. P. J., Brons, J. F., Verkerk, A. O., Bakker, M. L., Wakker, V., Clout, D. E. W., Moorman, A. F. M., Hoen, P. A. C. ’., & Christoffels, V. M. (2009) · Circulation Research · doi:10.1161/circresaha.108.192443 · Cited by 91 · see citing works
Self-citationvan Setten, J., Brody, J. A., Jamshidi, Y., Swenson, B. R., Butler, A. M., Campbell, H., Fabiola Del Greco, M., Evans, D. S., Gibson, Q., Gudbjartsson, D. F., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04766-9 · Cited by 90 · see citing works
The development of the conduction system in the mouse embryo heart
Virágh, S., & Challice, C. E. (1982) · Developmental Biology · doi:10.1016/0012-1606(82)90290-1 · Cited by 85 · see citing works
Deciphering the Epigenetic Code of Cardiac Myocyte Transcription.
Preissl, S., Schwaderer, M., Raulf, A., Hesse, M., Grüning, B., Köbele, C., Backofen, R., Fleischmann, B., Hein, L., & Gilsbach, R. (2015) · Circulation Research · doi:10.1161/circresaha.115.306337 · Cited by 79 · see citing works
Cardiomyocyte Cell-Cycle Activity during Preadolescence
Soonpaa, M. H., Zebrowski, D. C., Platt, C., Rosenzweig, A., Engel, F. B., & Field, L. J. (2015) · Cell · doi:10.1016/j.cell.2015.10.037 · Cited by 76 · see citing works
Wnt signaling regulates atrioventricular canal formation upstream of BMP and Tbx2
Verhoeven, M. C., Haase, C., Christoffels, V. M., Weidinger, G., & Bakkers, J. (2011) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20804 · Cited by 74 · see citing works
Self-citationCx30.2 enhancer analysis identifies Gata4 as a novel regulator of atrioventricular delay
Munshi, N. V., McAnally, J., Bezprozvannaya, S., Berry, J. M., Richardson, J. A., Hill, J. A., & Olson, E. N. (2009) · Development · doi:10.1242/dev.038562 · Cited by 73 · see citing works
Autonomic modulation and antiarrhythmic therapy in a model of long QT syndrome type 3
Fabritz, L., Damke, D., Emmerich, M., Kaufmann, S. G., Theis, K., Blana, A., Fortmueller, L., Laakmann, S., Hermann, S., Aleynichenko, E., et al. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq029 · Cited by 66 · see citing works
Genetic Determinants of P Wave Duration and PR Segment
Verweij, N., Leach, I. M., van den Boogaard, M., van Veldhuisen, D. J., Christoffels, V. M., Study, L. C., Hillege, H. L., van Gilst, W. H., Barnett, P., de Boer, R. A., et al. (2014) · Circulation Cardiovascular Genetics · doi:10.1161/circgenetics.113.000373 · Cited by 53 · see citing works
Self-citationPanaliappan, T. K., Wittmann, W., Jidigam, V. K., Mercurio, S., Bertolini, J. A., Sghari, S., Bose, R., Patthey, C., Nicolis, S. K., & Gunhaga, L. (2018) · Development · doi:10.1242/dev.153791 · Cited by 53 · see citing works
Miquerol, L., Bellon, A., Moreno, N. D. L. C., Beyer, S., Meilhac, S. M., BUCKINGHAM, M. E., Franco, D., & Kelly, R. G. (2013) · Developmental Dynamics · doi:10.1002/dvdy.23964 · Cited by 50 · see citing works
Mohan, R. A., Mommersteeg, M. T. M., Domínguez, J. N., Choquet, C., Wakker, V., de Gier-de Vries, C., Boink, G. J. J., Boukens, B. J., Miquerol, L., Verkerk, A. O., et al. (2018) · Development · doi:10.1242/dev.167361 · Cited by 50 · see citing works
Self-citationTRANSCRIPTIONAL REGULATION OF THE CARDIAC CONDUCTION SYSTEM.
Fishman, G. I. (2020) · PubMed Central · Cited by 47 · see citing works
Development and Function of the Cardiac Conduction System in Health and Disease
Park, D. S., & Fishman, G. I. (2017) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd4020007 · Cited by 44 · see citing works
van Weerd, J. H., Badi, I., van den Boogaard, M., Stefanovic, S., van de Werken, H. J. G., Gómez-Velázquez, M., Badía-Careaga, C., Manzanares, M., de Laat, W. L., Barnett, P., et al. (2014) · Circulation Research · doi:10.1161/circresaha.115.303591 · Cited by 43 · see citing works
Self-citationCanale, E. D., CAMPBELL, G. R., Smolich, J. J., & Campbell, J. H. (1986) · Springer eBooks · doi:10.1007/978-3-642-50115-9 · Cited by 38 · see citing works
van Duijvenboden, K., de Boer, B. A., Capon, N., Ruijter, J. M., & Christoffels, V. M. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1144 · Cited by 35 · see citing works
Self-citationTranscriptional Patterning of the Ventricular Cardiac Conduction System
Burnicka-Turek, O., Broman, M., Steimle, J. D., Boukens, B., Petrenko, N., Ikegami, K., Nadadur, R. D., Qiao, Y., Arnolds, D., Yang, X., et al. (2020) · Circulation Research · doi:10.1161/circresaha.118.314460 · Cited by 29 · see citing works
Self-citationWu, M., Peng, S., & Zhao, Y. B. (2013) · genesis · doi:10.1002/dvg.22730 · Cited by 18 · see citing works
Ντάλλα, Ι., Weng, L.-C. C., Cartwright, J., Hall, A. W., Sveinbjörnsson, G., Tucker, N. R., Choi, S. H., Chaffin, M. D., Roselli, C., Barnes, M. R., et al. (2020) · Apollo (University of Cambridge) · doi:10.17863/cam.53684 · Cited by 11 · see citing works
Nguyen, H. H., Grange, D. K., Johnson, M. C., Hare, G. F. V., & Jay, P. Y. (2018) · HeartRhythm Case Reports · doi:10.1016/j.hrcr.2018.11.005 · Cited by 3 · see citing works
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van Ouwerkerk, A. F., Bosada, F. M., van Duijvenboden, K., Houweling, A. C., Scholman, K. T., Wakker, V., Allaart, C. P., Uhm, J., Mathijssen, I. B., Baartscheer, T., et al. (2022) · Circulation · doi:10.1161/circulationaha.121.054347 · Cited by 37 · see citing works
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Cieri, R. L., Turner, M. L., Carney, R. M., Falkingham, P. L., Kirk, A. M., Wang, T., Jensen, B. K., Novotny, J., Tveite, J., Gatesy, S. M., et al. (2021) · Journal of Morphology · doi:10.1002/jmor.21421 · Cited by 28 · see citing works
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Schröder, L. C., Frank, D., & Müller, O. J. (2023) · Pathogens · doi:10.3390/pathogens12111301 · Cited by 23 · see citing works
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Wang, Y., Venkatesh, A. K., Xu, J., Xu, M., Williams, J., Smallwood, P. M., James, A. W., & Nathans, J. (2022) · Development · doi:10.1242/dev.200340 · Cited by 20 · see citing works
How Cardiac Embryology Translates into Clinical Arrhythmias
Rivaud, M. R., Blok, M., Jongbloed, M. R. M., & Boukens, B. J. (2021) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd8060070 · Cited by 16 · see citing works
Self-citationTranscriptional regulation of the postnatal cardiac conduction system heterogeneity
Oh, Y., Abid, R., Dababneh, S., Bakr, M., Aslani, T., Cook, D. P., Vanderhyden, B. C., Park, J. G., Munshi, N. V., Hui, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50849-1 · Cited by 15 · see citing works
A Variant Noncoding Region Regulates Prrx1 and Predisposes to Atrial Arrhythmias
Bosada, F. M., Rivaud, M. R., Uhm, J., Verheule, S., van Duijvenboden, K., Verkerk, A. O., Christoffels, V. M., & Boukens, B. J. (2021) · Circulation Research · doi:10.1161/circresaha.121.319146 · Cited by 15 · see citing works
Self-citationIop, L., Iliceto, S., Civieri, G., & Tona, F. (2021) · Cells · doi:10.3390/cells10113175 · Cited by 14 · see citing works
A phenotype-based forward genetic screen identifies Dnajb6 as a sick sinus syndrome gene
Ding, Y., Lang, D., Yan, J., Bu, H., Li, H., Jiao, K., Yang, J., Ni, H., Morotti, S., Le, T., et al. (2022) · eLife · doi:10.7554/elife.77327 · Cited by 12 · see citing works
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Tomida, S., Ishima, T., Nagai, R., & Aizawa, K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212420 · Cited by 11 · see citing works
Single‐cell profiling of MC1R ‐inhibited melanocytes
Berns, H. M., Watkins‐Chow, D. E., Lu, S., Louphrasitthiphol, P., Zhang, T., Brown, K. M., Moura‐Alves, P., Goding, C. R., & Pavan, W. J. (2023) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.13141 · Cited by 9 · see citing works
Development of the Cardiac Conduction System
van der Maarel, L. E., & Christoffels, V. M. (2024) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-44087-8_10 · Cited by 8 · see citing works
Self-citationThe cardiac conduction system: development, function and therapeutic targets
Park, D. S., & Fishman, G. I. (2026) · Nature Reviews Cardiology · doi:10.1038/s41569-025-01227-x · Cited by 7 · see citing works
HCN4 in the atrioventricular node
Copier, J. S., Verkerk, A. O., & Lodder, E. M. (2025) · Heart Rhythm · doi:10.1016/j.hrthm.2025.02.030 · Cited by 7 · see citing works
Molecular Profiling of the Cardiac Conduction System: the Dawn of a New Era
Mantri, S., Wu, S. M., & Goodyer, W. R. (2021) · Current Cardiology Reports · doi:10.1007/s11886-021-01536-w · Cited by 7 · see citing works
Alzein, M. M., Lozano-Velasco, E., Hernández‐Torres, F., García‐Padilla, C., Dominguez, J. N., Aránega, A. E., & Franco, D. (2021) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd8050056 · Cited by 7 · see citing works
Fetal Supraventricular Tachycardia: What Do We Know up to This Day?
Tsokkou, S., Konstantinidis, I. K., Anastasiou, V., Matsas, A., Stamoula, Ε., Peteinidou, E., Sioga, A., Papamitsou, T., Ziakas, A., & Kamperidis, V. (2025) · Journal of Personalized Medicine · doi:10.3390/jpm15080341 · Cited by 6 · see citing works
The cardiac conduction system: History, development, and disease
Lee, C., Xu, S., Samad, T., Goodyer, W. R., Raissadati, A., Heinrich, P., & Wu, S. M. (2024) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2024.02.006 · Cited by 6 · see citing works
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Byatt, T. C., Razaghi, E., Tüzüner, S., & Simões, F. C. (2025) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2025.103613 · Cited by 6 · see citing works
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Melzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Günes, C., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01553-x · Cited by 5 · see citing works
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Yildiz, M. (2025) · Reviews in Cardiovascular Medicine · doi:10.31083/rcm38696 · Cited by 4 · see citing works
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Zhao, H., Jiang, J.-B., Wang, S., & Miao, C. (2025) · Cells · doi:10.3390/cells14171390 · Cited by 4 · see citing works
Role of Genetic Variation in Transcriptional Regulatory Elements in Heart Rhythm
Jonker, T., Barnett, P., Boink, G. J. J., & Christoffels, V. M. (2023) · Cells · doi:10.3390/cells13010004 · Cited by 3 · see citing works
Self-citationCardiac Development: A Glimpse on Its Translational Contributions
Franco, D., García‐Padilla, C., Dominguez, J. N., Lozano-Velasco, E., & Aránega, A. E. (2021) · Hearts · doi:10.3390/hearts2010008 · Cited by 3 · see citing works
Coordinated Tbx3/Tbx5 transcriptional control of the adult ventricular conduction systemPreprint
Burnicka-Turek, O., Trampel, K. A., Laforest, B., Broman, M., Yang, X. H., Khan, Z., Rytkin, E., Li, B., Schaffer, E., Gadek, M., et al. (2024) · eLife · doi:10.7554/elife.102027 · Cited by 3 · see citing works
Basalamah, F., Dilogo, I. H., Raharjo, S. B., Mansyur, M., Siregar, N. C., Ibrahim, N., Setianto, B. Y., & Yuniadi, Y. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03760-x · Cited by 2 · see citing works
Coordinated Tbx3/Tbx5 transcriptional control of the adult ventricular conduction system
Burnicka-Turek, O., Trampel, K. A., Laforest, B., Broman, M., Yang, X., Khan, Z., Rytkin, E., Li, B., Schaffer, E., Gadek, M., et al. (2025) · eLife · doi:10.7554/elife.102027.3 · Cited by 1 · see citing works
Cardiac conduction system malformations in heterotaxy result from dysregulated Pitx2 expression
Joo, K., Matsuoka, R., Kitajima, K., Yashiro, K., Shiose, A., Tominaga, R., Shen, M. M., Oki, S., & Meno, C. (2026) · JCI Insight · doi:10.1172/jci.insight.199072 · Cited by 1 · see citing works
Sabarigirivasan, V., Brunet, J., Dejea, H., Crucean, A. C., Jegatheeswaran, A., Capelli, C., Pajaziti, E., Urban, T., Purzycka, J., Tafforeau, P., et al. (2026) · JTCVS structural and endovascular. · doi:10.1016/j.xjse.2026.100111 · Cited by 1 · see citing works
TRANSCRIPTIONAL REGULATION OF THE POSTNATAL CARDIAC CONDUCTION SYSTEM HETEROGENEITY
Oh, Y., Abid, R., Dababneh, S., Cook, D. P., Park, J., Vanderhyden, B. C., Munshi, N., & Kim, K. (2023) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2023.10.377
Coordinated Tbx3 / Tbx5 transcriptional control of the adult ventricular conduction systemPreprint
Burnicka-Turek, O., Trampel, K. A., Laforest, B., Broman, M., Khan, Z., Rytkin, E., Li, B., Schaffer, E., Gadek, M., Shen, K. M., et al. (2024) · eLife · doi:10.7554/elife.102027.1
Coordinated Tbx3/Tbx5 transcriptional control of the adult ventricular conduction systemPreprint
Burnicka-Turek, O., Trampel, K. A., Laforest, B., Broman, M., Yang, X. H., Khan, Z., Rytkin, E., Li, B., Schaffer, E., Gadek, M., et al. (2025) · eLife · doi:10.7554/elife.102027.2
Savettiere, A., Lam, J. C., Nguyen, M. H.-H., Schulte, T., Hirst, R. B., & Fairchild, J. K. (2025) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0000000000000688
Melzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576153
Self-citationMelzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576156
Self-citationMelzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576162
Self-citationMelzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576159
Self-citationRegulatory networks in the cardiac conduction system
Christoffels, V. M. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-24142-0.00013-8
Self-citation
- Authors
- Mohan, R. A., Bosada, F. M., van Weerd, J. H., van Duijvenboden, K., Wang, J., Mommersteeg, M. T. M., Hooijkaas, I. B., Wakker, V., de Gier-de Vries, C., Coronel, R., Boink, G. J. J., Bakkers, J., Barnett, P., Boukens, B. J., & Christoffels, V. M.
- Affiliations
- Amsterdam University Medical Centers (NL)
- Department of Medical Biology, Amsterdam University Medical Centers, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands;
- University of Oxford (GB)
- University Medical Center Utrecht (NL)
- Corresponding author
- Christoffels, Vincent M.
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2020-07-16
- Volume
- 117
- Issue
- 31
- Pages
- 18617-18626
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC7414162
- OpenAlex
- W3042543031
- Cited by
- 39
- References
- 71
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 8 · 2023: 6 · 2022: 4 · 2021: 8
- FWCI
- 2.78
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Funders
- Fondation Leducq (14CVD01)
- Hartstichting (2016T047, 2014T065)
- ZonMw (016.156.162)
- EC | FP7 | FP7 Ideas: European Research Council (714866)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- TBX3, atrioventricular conduction system, haploinsufficiency, gene regulatory networks, CACNA1G, cardiac electrophysiology, non-coding variants, ECG parameters, transcriptional regulation, mouse model
- MeSH terms
- Animals, Arrhythmias, Cardiac, Atrioventricular Node, Mice, Transgenic, Mutation, Ryanodine Receptor Calcium Release Channel, Calcium Channels, T-Type, T-Box Domain Proteins, Mice, Transcriptome
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