Transcriptome analysis of mouse and human sinoatrial node cells reveals a conserved genetic program
Open accessAbstract
The rate of contraction of the heart relies on proper development and function of the sinoatrial node, which consists of a small heterogeneous cell population, including Tbx3+ pacemaker cells. Here we isolated and characterized the Tbx3+ cells from Tbx3+/Venus knock-in mice. We studied electrophysiological parameters during development and found that Venus-labeled cells are genuine Tbx3+ pacemaker cells. We analyzed the transcriptomes of late fetal FACS-purified Tbx3+ sinoatrial nodal cells and Nppb-Katushka+ atrial and ventricular chamber cardiomyocytes, and identified a sinoatrial node-enriched gene program including key nodal transcription factors, BMP-signaling, and Smoc2, which disruption in mice did not affect heart rhythm. We also obtained the transcriptomes of the sinoatrial node region, including pacemaker and other cell types, and right atrium of human fetuses, and found a gene program including TBX3, SHOX2, ISL1, HOX family members, and BMP- and NOTCH-signaling components conserved between human and mouse. We conclude that a conserved gene program characterizes the sinoatrial node region and that the Tbx3+/Venus allele provides a reliable tool to visualize the sinoatrial node and to study its development and function.
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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 [43]
The supplied passages contain bibliographic metadata but no discussion of a Tbx3-Venus reporter. Searches of the indexed copy for Tbx3-Venus, its allele designation, and reporter validation returned no relevant passage, so this copy does not establish whether the system was validated. (LLM, conf=0.72)
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Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., & Miyawaki, A. (2002) · Nature Biotechnology · doi:10.1038/nbt0102-87 · Cited by 2,755 · see citing works
High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP
Rodríguez, C. I., Buchholz, F., Galloway, J. L., Sequerra, R., Kasper, J. S., Ayala, R., Stewart, A. F., & Dymecki, S. M. (2000) · Nature Genetics · doi:10.1038/75973 · Cited by 1,162 · see citing works
Wang, J., Vasaikar, S. V., Shi, Z., Greer, M., & Zhang, B. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx356 · Cited by 1,161 · see citing works
Atrial Remodeling and Atrial Fibrillation: Mechanisms and Implications
Nattel, S., Burstein, B., & Dobrev, D. (2008) · Circulation: Arrhythmia and Electrophysiology · doi:10.1161/circep.107.754564 · Cited by 1,124 · see citing works
Nonsense-mediated mRNA decayin health and disease
Frischmeyer, P. A. (1999) · Human Molecular Genetics · doi:10.1093/hmg/8.10.1893 · Cited by 991 · see citing works
The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4’ cell markers
Muñoz, J., Stange, D. E., Schepers, A. G., van de Wetering, M., Koo, B., Itzkovitz, S., Volckmann, R., Kung, K. S., Köster, J., Radulescu, S., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.166 · Cited by 758 · see citing works
Retinoic acid in development: Towards an integrated view
Niederreither, K., & Dollé, P. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2340 · Cited by 726 · see citing works
The sinoatrial node, a heterogeneous pacemaker structure
Boyett, M. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(00)00135-8 · Cited by 698 · see citing works
Lakatta, E. G., Maltsev, V. A., & Vinogradova, T. M. (2010) · Circulation Research · doi:10.1161/circresaha.109.206078 · Cited by 631 · see citing works
Genesis and Regulation of the Heart Automaticity
Mangoni, M. E., & Nargeot, J. (2008) · Physiological Reviews · doi:10.1152/physrev.00018.2007 · Cited by 602 · see citing works
How does adrenaline accelerate the heart?
Brown, H. F., DiFrancesco, D., & Noble, S. J. (1979) · Nature · doi:10.1038/280235a0 · Cited by 585 · see citing works
Stieber, J., Herrmann, S., Feil, S. C., Löster, J., Feil, R., Biel, M., Hofmann, F. B., & Ludwig, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2434235100 · Cited by 456 · see citing works
New Insights Into Pacemaker Activity
Dobrzynski, H., Boyett, M. R., & Anderson, R. H. (2007) · Circulation · doi:10.1161/circulationaha.106.616011 · Cited by 429 · see citing works
Loss of the Lkb1 tumour suppressor provokes intestinal polyposis but resistance to transformation
Bardeesy, N. M., Sinha, M., Hezel, A. F., Signoretti, S., Hathaway, N. A., Sharpless, N. E., Loda, M. F., Carrasco, D. R., & DePinho, R. A. (2002) · Nature · doi:10.1038/nature01045 · Cited by 418 · see citing works
Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse
Niederreither, K., Vermot, J., Messaddeq, N., Schuhbaur, B., Chambon, P., & Dollé, P. (2001) · Development · doi:10.1242/dev.128.7.1019 · Cited by 418 · see citing works
Moosmang, S., Stieber, J., Zong, X., Biel, M., Hofmann, F. B., & Ludwig, A. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02036.x · Cited by 415 · 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
Molecular Pathway for the Localized Formation of the Sinoatrial Node
Mommersteeg, M. T. M., Hoogaars, W. M. H., Prall, O. W. J., Vries, C. D. G.-D., Wiese, C., Clout, D. E. W., Papaioannou, V. E., Brown, N. A., Harvey, R. P., Moorman, A. F. M., et al. (2007) · Circulation Research · doi:10.1161/01.res.0000258019.74591.b3 · Cited by 369 · see citing works
Self-citationProtze, S. I., Liu, J., Nussinovitch, U., Ohana, L., Backx, P. H., Gepstein, L., & Keller, G. M. (2017) · Nature Biotechnology · doi:10.1038/nbt.3745 · Cited by 366 · 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
Sun, Y., Liang, X., Najafi, N., Cass, M., Lin, L., Cai, C.-L., Chen, J., & Evans, S. Μ. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.12.048 · Cited by 332 · see citing works
Wiese, C., Grieskamp, T., Airik, R., Mommersteeg, M., Gardiwal, A., Vries, C. D. G.-D., Schuster-Gossler, K., Moorman, A., Kispert, A., & Christoffels, V. (2009) · Circulation Research · doi:10.1161/circresaha.108.187062 · Cited by 328 · see citing works
Self-citationMoorman, A. F. M., Houweling, A. C., de Boer, P. A. J., & Christoffels, V. M. (2001) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540104900101 · Cited by 321 · see citing works
Self-citationden Hoed, M., Eijgelsheim, M., Esko, T., Brundel, B. J. J. M., Peal, D. S., Evans, D. M., Nolte, I. M., Segrè, A. V., Hólm, H., Handsaker, R. E., et al. (2013) · Nature Genetics · doi:10.1038/ng.2610 · Cited by 296 · see citing works
Davenport, T. G., Jerome-Majewska, L. A., & Papaioannou, V. E. (2003) · Development · doi:10.1242/dev.00431 · Cited by 295 · see citing works
Visualization and functional characterization of the developing murine cardiac conduction system
Rentschler, S., Vaidya, D. M., Tamaddon, H. S., Degenhardt, K. R., Sassoon, D. A., Morley, G. E., Jalife, J., & Fishman, G. I. (2001) · Development · doi:10.1242/dev.128.10.1785 · Cited by 268 · see citing works
Blaschke, R. J., Hahurij, N. D., Kuijper, S. J. M., Just, S., Wisse, L. J., Deißler, K., Maxelon, T., Anastassiadis, K., Spitzer, J., Hardt, S. E., et al. (2007) · Circulation · doi:10.1161/circulationaha.106.637819 · Cited by 249 · see citing works
Shox2 is essential for the differentiation of cardiac pacemaker cells by repressing Nkx2-5
Espinoza-Lewis, R. A., Yu, L., He, F.-L., Liu, H.-B., Tang, R.-H., Shi, J., Sun, X., Martin, J. F., Wang, D.-Z., Yang, J., et al. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2008.12.028 · Cited by 240 · 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
Retinoic acid deficiency alters second heart field formation
Ryckebüsch, L., Wang, Z., Bertrand, N., Lin, S.-C., Chi, X., Schwartz, R. J., Zaffran, S., & Niederreither, K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712344105 · Cited by 210 · see citing works
Self-citationRequirement of neuronal‐ and cardiac‐type sodium channels for murine sinoatrial node pacemaking
Lei, M., Jones, S. A., Liu, J., Lancaster, M. K., Fung, S. S. ‐., Dobrzynski, H., Camelliti, P., Maier, S. K. G., Noble, D., & Boyett, M. R. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.068643 · Cited by 206 · see citing works
Maier, S. K. G., Westenbroek, R. E., Yamanushi, T. T., Dobrzynski, H., Boyett, M. R., Catterall, W. A., & Scheuer, T. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2627986100 · Cited by 205 · see citing works
Milano, A., Vermeer, A. M. C., Lodder, E. M., Barc, J., Verkerk, A. O., Postma, A. V., van der Bilt, I. A. C., Baars, M. J. H., van Haelst, P. L., Çalişkan, K., et al. (2014) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2014.05.045 · Cited by 203 · see citing works
Self-citationvan Kempen, M. J. A., Fromaget, C., Gros, D. B., Moorman, A. F. M., & Lamers, W. H. (1991) · Circulation Research · doi:10.1161/01.res.68.6.1638 · Cited by 200 · see citing works
Bakker, 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-citationNext-generation pacemakers: from small devices to biological pacemakers
Cingolani, E., Goldhaber, J. I., & Marbán, E. (2018) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.165 · Cited by 194 · see citing works
Sinus node revisited in the era of electroanatomical mapping and catheter ablation
Sánchez‐Quintana, D., Cabrera, J. A., Farré, J., Climent, V., Anderson, R. H., & Ho, S. Y. (2005) · Heart · doi:10.1136/hrt.2003.031542 · Cited by 191 · see citing works
Mommersteeg, M. T. M., Dominguez, J. N., Wiese, C., Norden, J., Vries, C. D. G.-D., Burch, J. B. E., Kispert, A., Brown, N. A., Moorman, A. F. M., & Christoffels, V. M. (2010) · Cardiovascular Research · doi:10.1093/cvr/cvq033 · Cited by 189 · see citing works
Self-citationDevelopment of the Cardiac Conduction Tissue in Human Embryos Using HNK-1 Antigen Expression
Blom, N. A., Groot, A. C. G., DeRuiter, M. C., Poelmann, R. E., Mentink, M. M. T., & Ottenkamp, J. J. (1999) · Circulation · doi:10.1161/01.cir.99.6.800 · Cited by 189 · see citing works
Identification and Functional Characterization of Cardiac Pacemaker Cells in Zebrafish
Tessadori, F., van Weerd, J. H., Burkhard, S. B., Verkerk, A. O., de Pater, E., Boukens, B. J., Vink, A., Christoffels, V. M., & Bakkers, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047644 · Cited by 186 · see citing works
Self-citationDiagnosis and treatment of sick sinus syndrome.
Adan, V., & Crown, L. (1980) · PubMed · Cited by 185 · see citing works
Computer Three-Dimensional Reconstruction of the Sinoatrial Node
Dobrzynski, H., Li, J., Tellez, J. O., Greener, I. D., Nikolski, V., Wright, S., Parson, S. H., Jones, S. A., Lancaster, M. K., 山本, 充., et al. (2005) · Circulation · doi:10.1161/01.cir.0000152100.04087.db · Cited by 181 · see citing works
Hox genes define distinct progenitor sub-domains within the second heart field
Bertrand, N., Roux, M., Ryckebüsch, L., Niederreither, K., Dollé, P., Moon, A., Capecchi, M. R., & Zaffran, S. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.02.029 · Cited by 171 · see citing works
Self-citationPathology of sinoatrial node. Correlations with electrocardiographic findings in 111 patients
Théry, C., Gosselin, B. H., Lekieffre, J., & Warembourg, H. (1977) · American Heart Journal · doi:10.1016/s0002-8703(77)80070-7 · Cited by 169 · see citing works
Waxman, J. S., Keegan, B. R., Roberts, R. W., Poss, K. D., & Yelon, D. L. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.09.009 · Cited by 160 · see citing works
T-box transcription factor TBX3 reprogrammes mature cardiac myocytes into pacemaker-like cells.
Bakker, M., Boink, G. J., Boukens, B., Verkerk, A., van den Boogaard, M., den Haan, A. D., Hoogaars, W. M., Buermans, H., de Bakker, J., Seppen, J., et al. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs120 · Cited by 158 · see citing works
Self-citationEarly Mesodermal Cues Assign Avian Cardiac Pacemaker Fate Potential in a Tertiary Heart Field
Bressan, M. C., Liu, G., & Mikawa, T. (2013) · Science · doi:10.1126/science.1232877 · Cited by 156 · 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-citationDistribution of Atrial and Nodal Cells Within the Rabbit Sinoatrial Node
Verheijck, E. E., Wessels, A., van Ginneken, A. C. G., Bourier, J., Markman, M. W. M., Vermeulen, J. L. M., de Bakker, J. M. T., Lamers, W. H., Tobias Opthof, A., & Bouman, L. N. (1998) · Circulation · doi:10.1161/01.cir.97.16.1623 · Cited by 148 · see citing works
Tbx2 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-citationContactin-2 Expression in the Cardiac Purkinje Fiber Network
Pallante, B. A., Giovannone, S., Fang-Yu, L., Zhang, J., Liu, N., Kang, G., Dun, W., Boyden, P. A., & Fishman, G. I. (2010) · Circulation Arrhythmia and Electrophysiology · doi:10.1161/circep.109.928820 · Cited by 145 · see citing works
The 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-citationFunctional Properties of Mouse Connexin30.2 Expressed in the Conduction System of the Heart
Kreuzberg, M. M., Söhl, G., Kim, J.-S., Verselis, V. K., Willecke, K., & Bukauskas, F. F. (2005) · Circulation Research · doi:10.1161/01.res.0000169271.33675.05 · Cited by 127 · see citing works
Opthof, T. (1988) · Cardiovascular Drugs and Therapy · doi:10.1007/bf02125744 · Cited by 124 · see citing works
Transcription factor ISL1 is essential for pacemaker development and function
Liang, X., Zhang, Q., Cattaneo, P., Zhuang, S., Gong, X., Spann, N. J., Jiang, C., Cao, X., Zhao, X., Zhang, X., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci68257 · Cited by 122 · see citing works
Lüdtke, T. H. ‐., Christoffels, V. M., Petry, M., & Kispert, A. (2009) · Hepatology · doi:10.1002/hep.22700 · Cited by 117 · cited 1× · see citing works
“S1E), in accordance with the phenotype of Tbx3 homozygous mutants described previously (Bakker et al., 2008; Davenport et al., 2003; Frank et al., 2011; Lüdtke et al., 2009; Mesbah et al., 2008).”
ResultSelf-citationVedantham, V., Galang, G., Evangelista, M., Deo, R. C., & Srivastava, D. (2015) · Circulation Research · doi:10.1161/circresaha.116.305913 · Cited by 117 · see citing works
Shox2 mediates Tbx5 activity by regulating Bmp4 in the pacemaker region of the developing heart
Puskaric, S., Schmitteckert, S., Mori, A., Gläser, A., Schneider, K., Bruneau, B. G., Blaschke, R. J., Steinbeißer, H., & Rappold, G. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq393 · Cited by 115 · see citing works
Heart conduction system: a neural crest derivative?
Gorza, L., Schiaffino, S., & Vitadello, M. (1988) · Brain Research · doi:10.1016/0006-8993(88)90707-x · Cited by 109 · see citing works
Verkerk, A. O., & Wilders, R. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16023071 · Cited by 107 · see citing works
Self-citationSerious workings of the funny current
DiFrancesco, D. (2005) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2005.05.001 · Cited by 103 · see citing works
Tbx3 is required for outflow tract development
Mesbah, K., Harrelson, Z., Théveniau-Ruissy, M., Papaioannou, V., & Kelly, R. (2008) · Circulation Research · doi:10.1161/circresaha.108.172858 · 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-citationBloch‐Zupan, A., Jamet, X., Etard, C., Laugel-Haushalter, V., Muller, J., Geoffroy, V., Strauss, J.-P., Pelletier, V., Marion, V., Poch, O., et al. (2011) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.11.002 · Cited by 101 · see citing works
Ye, W., Wang, J., Song, Y., Yu, D., Sun, C., Liu, C., Chen, F., Zhang, Y., Wang, F., Harvey, R. P., et al. (2015) · Development · doi:10.1242/dev.120220 · Cited by 99 · see citing works
Molecular Analysis of Patterning of Conduction Tissues in the Developing Human Heart
Sizarov, A., Devalla, H. D., Anderson, R. H., Passier, R. C., Christoffels, V. M., & Moorman, A. F. M. (2011) · Circulation Arrhythmia and Electrophysiology · doi:10.1161/circep.111.963421 · 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-citationMasson‐Pévet, M., Bleeker, W. K., & Gros, D. (1979) · Circulation Research · doi:10.1161/01.res.45.5.621 · Cited by 83 · see citing works
Hoffmann, S., Berger, I. M., Gläser, A., Bacon, C., Li, L., Gretz, N., Steinbeißer, H., Rottbauer, W., Just, S., & Rappold, G. (2013) · Basic Research in Cardiology · doi:10.1007/s00395-013-0339-z · Cited by 78 · see citing works
Embryonic Epinephrine Synthesis in the Rat Heart Before Innervation
Ebert, S. N., & Thompson, R. P. (2001) · Circulation Research · doi:10.1161/01.res.88.1.117 · Cited by 73 · see citing works
Pacemaker activity of the human sinoatrial node: Role of the hyperpolarization-activated current, If
Verkerk, A. O., van Ginneken, A. C. G., & Wilders, R. (2009) · International Journal of Cardiology · doi:10.1016/j.ijcard.2008.12.196 · Cited by 67 · see citing works
Self-citationGorza, L., & Vitadello, M. (1989) · Circulation Research · doi:10.1161/01.res.65.2.360 · Cited by 66 · see citing works
Matsuyama, T.-A. (2004) · EP Europace · doi:10.1016/j.eupc.2004.03.011 · Cited by 62 · see citing works
The past, present, and future of pacemaker therapies
Boink, G. J. J., Christoffels, V. M., Robinson, R. B., & Tan, H. L. (2015) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2015.02.005 · Cited by 57 · see citing works
Self-citationSergeeva, I. A., Hooijkaas, I. B., van der Made, I., Jong, W. M. C., Creemers, E. E., & Christoffels, V. M. (2013) · Cardiovascular Research · doi:10.1093/cvr/cvt228 · Cited by 56 · see citing works
Self-citationThe internodal pathways of the human heart
James, T. N. (2001) · Progress in Cardiovascular Diseases · doi:10.1053/pcad.2001.24598 · Cited by 52 · see citing works
Boukens, B. J., Hoogendijk, M. G., Verkerk, A. O., Linnenbank, A. C., van Dam, P. M., Remme, C. A., Fiolet, J. W. T., Tobias Opthof, A., Christoffels, V. M., & Coronel, R. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs299 · Cited by 51 · see citing works
Self-citationOrgeur, M., Martens, M., Leonte, G., Nassari, S., Bonnin, M.-A., Börno, S. T., Timmermann, B., Hecht, J., Duprez, D., & Stricker, S. (2018) · Development · doi:10.1242/dev.161208 · 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-citationIncreased Hox activity mimics the teratogenic effects of excess retinoic acid signaling
Waxman, J. S., & Yelon, D. L. (2009) · Developmental Dynamics · doi:10.1002/dvdy.21951 · Cited by 49 · see citing works
Nakagawa, M., Thompson, R., Terracio, L., & Borg, T. (1993) · Anatomy and Embryology · doi:10.1007/bf00174420 · Cited by 49 · see citing works
TRANSCRIPTIONAL REGULATION OF THE CARDIAC CONDUCTION SYSTEM.
Fishman, G. I. (2020) · PubMed Central · Cited by 47 · see citing works
Connexin 30 is expressed in the mouse sino-atrial node and modulates heart rate
Gros, D. B., Théveniau‐Ruissy, M., Bernard, M., Calmels, T., Kober, F., Söhl, G., Willecke, K., Nargeot, J., Jongsma, H. J., & Mangoni, M. E. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp280 · Cited by 42 · see citing works
Insights into cardiac conduction system formation provided by HCN4 expression
Liang, X., Evans, S. Μ., & Sun, Y. (2014) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2014.08.009 · Cited by 30 · see citing works
Qiao, Y., Lipovsky, C. E., Hicks, S., Bhatnagar, S., Li, G., Khandekar, A., Guzy, R. D., Woo, K. V., Nichols, C. G., Efimov, I. R., et al. (2017) · Circulation Research · doi:10.1161/circresaha.116.310396 · Cited by 28 · see citing works
Wnt/β-Catenin Signaling Maintains the Mesenchymal Precursor Pool for Murine Sinus Horn Formation
Norden, J., Greulich, F., Rudat, C., Taketo, M. M., & Kispert, A. (2011) · Circulation Research · doi:10.1161/circresaha.111.245340 · Cited by 27 · see citing works
IL-11 is a potential therapeutic target in cardiovascular fibrosis
Fernández-Ruíz, I. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.197 · Cited by 24 · see citing works
Shox2 Regulates the Pacemaker Gene Program in Embryoid Bodies
Hashem, S. I., Lam, M. L., Mihardja, S. S., White, S. M., Lee, R. J., & Claycomb, W. C. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0123 · Cited by 23 · see citing works
The expression of Visinin-like 1 during mouse embryonic development
Ola, R., Lefebvre, S., Braunewell, K., Sainio, K., & Sariola, H. V. (2011) · Gene Expression Patterns · doi:10.1016/j.gep.2011.11.004 · Cited by 18 · see citing works
Aoyama, N., Kikawada, R., & Yamashina, S. (1993) · Archivum histologicum japonicum · doi:10.1679/aohc.56.303 · Cited by 13 · see citing works
Morphology of mouse sinoatrial node and its expression of NF-160 and HCN4.
Wen, Y., & Li, B. (2015) · PubMed · Cited by 9 · see citing works
Flagged first, then by citations
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Spatially resolved multiomics of human cardiac niches
Kanemaru, K., Cranley, J., Muraro, D., Miranda, A. M. A., Ho, S. Y., Wilbrey-Clark, A., Patrick Pett, J., Polanski, K., Richardson, L., Litvinukova, M., et al. (2023) · Nature · doi:10.1038/s41586-023-06311-1 · Cited by 425 · 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
Innervation and Neuronal Control of the Mammalian Sinoatrial Node a Comprehensive Atlas
Hanna, P., Dacey, M. J., Brennan, J. A., Moss, A., Robbins, S., Achanta, S., Biscola, N. P., Swid, M. A., Rajendran, P. S., Mori, S., et al. (2021) · Circulation Research · doi:10.1161/circresaha.120.318458 · Cited by 119 · see citing works
Cellular and molecular landscape of mammalian sinoatrial node revealed by single-cell RNA sequencing
Liang, D., Xue, J., Li, G., Zhou, L., Lv, B., Zeng, Q., Xiong, K., Zhou, H., Xie, D., Zhang, F., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20448-x · Cited by 96 · see citing works
Evidence of Superior and Inferior Sinoatrial Nodes in the Mammalian Heart
Brennan, J. A., Chen, Q., Gams, A., Dyavanapalli, J., Mendelowitz, D., Peng, W., & Efimov, I. R. (2020) · JACC. Clinical electrophysiology · doi:10.1016/j.jacep.2020.09.012 · Cited by 68 · see citing works
Mechanisms of Sinoatrial Node Dysfunction in Heart Failure With Preserved Ejection Fraction
Mesquita, T., Zhang, R., Cho, J. H., Zhang, R., Lin, Y.-N., Sanchez, L., Goldhaber, J. I., Yu, J. K., Liang, J. A., Liu, W., et al. (2021) · Circulation · doi:10.1161/circulationaha.121.054976 · Cited by 68 · see citing works
ATAC-Seq Reveals an Isl1 Enhancer That Regulates Sinoatrial Node Development and Function
Galang, G., Mandla, R., Ruan, H., Jung, C., Sinha, T., Stone, N. R., Wu, R. S., Mannion, B. J., Allu, P. K. R., Chang, K. C., et al. (2020) · Circulation Research · doi:10.1161/circresaha.120.317145 · Cited by 55 · see citing works
Silencing miR-370-3p rescues funny current and sinus node function in heart failure
Yanni, J., D’Souza, A., Wang, Y., Li, N., Hansen, B. J., Zakharkin, S. O., Smith, M., Hayward, C. E., Whitson, B. A., Mohler, P. J., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-67790-0 · Cited by 48 · see citing works
Genome-Wide Analysis Identifies an Essential Human TBX3 Pacemaker Enhancer
van Eif, V. W. W., Protze, S. I., Bosada, F. M., Yuan, X., Sinha, T., van Duijvenboden, K., Ernault, A. C., Mohan, R. A., Wakker, V., Vries, C. D. G.-D., et al. (2020) · Circulation Research · doi:10.1161/circresaha.120.317054 · Cited by 43 · see citing works
Self-citationMechanisms of Arrhythmias in the Brugada Syndrome
Blok, M., & Boukens, B. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197051 · Cited by 41 · see citing works
Self-citationA single cell transcriptional roadmap of human pacemaker cell differentiation
Wiesinger, A., Li, J., Fokkert, L., Bakker, P., Verkerk, A. O., Christoffels, V. M., Boink, G. J. J., & Devalla, H. D. (2022) · eLife · doi:10.7554/elife.76781 · Cited by 40 · see citing works
Self-citationLi, H., Li, D., Wang, Y., Huang, Z. J., Xu, J., Yang, T., Wang, L., Tang, Q., Cai, C., Huang, H. Y., et al. (2019) · Development · doi:10.1242/dev.178145 · Cited by 39 · see citing works
Genetic Complexity of Sinoatrial Node Dysfunction
Wallace, M. J., Refaey, M. E., Mesirca, P., Hund, T. J., Mangoni, M. E., & Mohler, P. J. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.654925 · Cited by 39 · see citing works
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
Self-citationCellular Heterogeneity of the Heart
Michel, N. A., Ljubojević-Holzer, S., Bugger, H., & Zirlik, A. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.868466 · Cited by 40 · see citing works
Aminu, A. J., Petkova, M. A., Atkinson, A. J., Yanni, J., Morris, A. D., Simms, R. T., Chen, W., Yin, Z., Kuniewicz, M., Holda, M. K., et al. (2021) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2021.04.008 · Cited by 25 · see citing works
Minhas, R., Loeffler‐Wirth, H., Siddiqui, Y. H., Obrębski, T., Vashisht, S., Nahia, K. A., Paterek, A., Brzozowska, A., Bugajski, Ł., Piwocka, K., et al. (2021) · BMC Genomics · doi:10.1186/s12864-021-08016-z · Cited by 24 · see citing works
Assembly of the Cardiac Pacemaking Complex: Electrogenic Principles of Sinoatrial Node Morphogenesis
Easterling, M. R., Rossi, S., Mazzella, A. J., & Bressan, M. C. (2021) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd8040040 · Cited by 24 · see citing works
Implementing Biological Pacemakers: Design Criteria for Successful Transition From Concept to Clinic
Komosa, E. R., Wolfson, D. W., Bressan, M. C., Cho, H. C., & Ogle, B. M. (2021) · Circulation Arrhythmia and Electrophysiology · doi:10.1161/circep.121.009957 · Cited by 23 · see citing works
Transcriptional profile of the rat cardiovascular system at single-cell resolution
Arduini, A., Fleming, S. J., Xiao, L., Hall, A. W., Akkad, A.-D., Chaffin, M. D., Bendinelli, K. J., Tucker, N. R., Papangeli, I., Mantineo, H., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.115091 · Cited by 22 · see citing works
Non-canonical role of the sympathetic nervous system in the day–night rhythm in heart rate
Anderson, C., Forte, G. M. A., Hu, W., Zhang, H., Boyett, M. R., & D’Souza, A. (2023) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2022.0179 · Cited by 21 · see citing works
Genetics of sinoatrial node function and heart rate disorders
van der Maarel, L. E., Postma, A. V., & Christoffels, V. M. (2023) · Disease Models & Mechanisms · doi:10.1242/dmm.050101 · Cited by 21 · see citing works
Self-citationMandla, R., Jung, C., & Vedantham, V. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.712666 · Cited by 20 · see citing works
Understanding the Adult Mammalian Heart at Single-Cell RNA-Seq Resolution
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Rad-GTPase contributes to heart rate via L-type calcium channel regulation
Levitan, B. M., Ahern, B. M., Aloysius, A., Brown, L. P., Wen, Y., Andres, D., & Satin, J. (2021) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2021.01.005 · Cited by 18 · see citing works
Li, J., Wiesinger, A., Fokkert, L., Boukens, B. J., Verkerk, A. O., Christoffels, V. M., Boink, G. J. J., & Devalla, H. D. (2022) · Journal of Tissue Engineering · doi:10.1177/20417314221127908 · Cited by 17 · see citing works
Self-citationTranscriptional regulation of the postnatal cardiac conduction system heterogeneity
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GOing Forward With the Cardiac Conduction System Using Gene Ontology
Li, K. Y. C., Cook, A. C., & Lovering, R. C. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.802393 · Cited by 16 · see citing works
Tagirova, S., Tsutsui, K., Tarasov, K. V., Yang, D., Wirth, A., Maltsev, V. A., Ziman, B. D., Yaniv, Y., & Lakatta, E. G. (2021) · JACC. Clinical electrophysiology · doi:10.1016/j.jacep.2021.02.016 · Cited by 15 · see citing works
Gastruloids are competent to specify both cardiac and skeletal muscle lineages
Argiro, L., Chevalier, C., Choquet, C., Nandkishore, N., Ghata, A. S., Baudot, A., Zaffran, S., & Lescroart, F. (2024) · Nature Communications · doi:10.1038/s41467-024-54466-w · 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
Novel Candidate Regulators and Developmental Trajectory of Pituitary Thyrotropes
Cheung, L., Menage, L., Rizzoti, K., Hamilton, G., Dumontet, T., Basham, K. J., Daly, A. Z., Brinkmeier, M. L., Masser, B. E., Treier, M., et al. (2023) · Endocrinology · doi:10.1210/endocr/bqad076 · Cited by 14 · see citing works
Thomas, D., & Wu, J. C. (2025) · iScience · doi:10.1016/j.isci.2025.113003 · Cited by 14 · see citing works
Lim, A. A., Pouyabahar, D., Ashraf, M., Huang, K., Lohbihler, M., Murareanu, B. M., Chang, M. L., Kwan, M., Alibhai, F. J., Tran, T. H., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54337-4 · Cited by 12 · see citing works
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van Weerd, J. H., Mohan, R. A., van Duijvenboden, K., Hooijkaas, I. B., Wakker, V., Boukens, B. J., Barnett, P., & Christoffels, V. M. (2020) · eLife · doi:10.7554/elife.56697 · Cited by 12 · see citing works
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Abassah‐Oppong, S., Zoia, M., Mannion, B. J., Rouco, R., Tissières, V., Spurrell, C. H., Roland, V., Darbellay, F., Itum, A., Gamart, J., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53009-7 · Cited by 14 · see citing works
Multi-modal refinement of the human heart atlas during the first gestational trimester
Bono, C. D., Xu, Y., Kausar, S., Herbane, M., Humbert, C., Rafatov, S., Missirian, C., Moreno, M., Shi, W., Gitton, Y., et al. (2025) · Development · doi:10.1242/dev.204555 · Cited by 11 · see citing works
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Ghazizadeh, Z., Zhu, J., Fattahi, F., Tang, A., Sun, X., Amin, S., Tsai, S., Khalaj, M., Zhou, T., Samuel, R. M., et al. (2022) · iScience · doi:10.1016/j.isci.2022.104153 · Cited by 10 · see citing works
High cardiomyocyte diversity in human early prenatal heart development
Sylvén, C., Wärdell, E., Månsson‐Broberg, A., Cingolani, E., Ampatzis, K., Larsson, L., Björklund, Å. K., & Giacomello, S. (2022) · iScience · doi:10.1016/j.isci.2022.105857 · Cited by 10 · see citing works
Marchal, G. A., Verkerk, A. O., Mohan, R. A., Wolswinkel, R., Boukens, B. J., & Remme, C. A. (2020) · Acta Physiologica · doi:10.1111/apha.13493 · Cited by 10 · see citing works
Self-citationGlobal chromatin landscapes identify candidate noncoding modifiers of cardiac rhythm
Bhattacharyya, S., Kollipara, R. K., Orquera-Tornakian, G., Goetsch, S. C., Zhang, M., Perry, C., Li, B., Shelton, J. M., Bhakta, M., Duan, J., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci153635 · Cited by 13 · see citing works
Local tissue mechanics control cardiac pacemaker cell embryonic patterning
Henley, T., Goudy, J., Easterling, M. R., Donley, C. L., Wirka, R. C., & Bressan, M. C. (2023) · Life Science Alliance · doi:10.26508/lsa.202201799 · Cited by 9 · see citing works
Human Cardiac Transcription Factor Networks
Varshney, A., Chahal, G., Santos, L. N., Stolper, J. S., Hallab, J., Nim, H. T., Nikolov, M., Yip, A., & Ramialison, M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.11597-1 · Cited by 9 · see citing works
Adherens junction engagement regulates functional patterning of the cardiac pacemaker cell lineage
Thomas, K., Henley, T., Rossi, S., Costello, M. J., Polacheck, W. J., Griffith, B. E., & Bressan, M. C. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.04.004 · Cited by 9 · see citing works
Li, T., Marashly, Q., Kim, J. A., Li, N., & Chelu, M. G. (2024) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2024.2351501 · Cited by 9 · see citing works
Development of the Cardiac Conduction System
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Self-citationEpilepsy-associated Kv1.1 channel subunits regulate intrinsic cardiac pacemaking in mice
Si, M., Darvish, A., Paulhus, K., Kumar, P., Hamilton, K. A., & Glasscock, E. (2024) · The Journal of General Physiology · doi:10.1085/jgp.202413578 · Cited by 7 · see citing works
Proteomic profile of human sinoatrial and atrioventricular nodes in comparison to working myocardium
Krawczyk‐Ożóg, A., Stachowicz, A., Szoniec, G., Batko, J., Stachyra, K., Bolechała, F., Strona, M., Wołkow, P. P., Yin, Z., Dobrzynski, H., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-89255-y · Cited by 7 · see citing works
Scholman, K. T., Meijborg, V. M. F., Gálvez‐Montón, C., Lodder, E. M., & Boukens, B. J. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00557 · Cited by 7 · see citing works
Self-citationMolecular 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
The 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
Differentiation of Sinoatrial-like Cardiomyocytes as a Biological Pacemaker Model
Sleiman, Y., Reisqs, J., & Boutjdir, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179155 · Cited by 6 · see citing works
Li, X., Gao, F., Wang, X., Liang, Q., Bai, A., Liu, Z., Chen, X., Li, E., Chen, S., Lü, C., et al. (2021) · EBioMedicine · doi:10.1016/j.ebiom.2021.103575 · Cited by 6 · see citing works
Wakimizu, T., Morikawa, K., Fukumura, K., Yuki, T., Adachi, T., Kurata, Y., Miake, J., Hisatome, I., Tsuneto, M., & Shirayoshi, Y. (2022) · Regenerative Therapy · doi:10.1016/j.reth.2022.07.012 · Cited by 6 · see citing works
Comparative Study of Transcriptome in the Hearts Isolated from Mice, Rats, and Humans
Okada, D., Okamoto, Y., Io, T., Oka, M., Kobayashi, D., Ito, S., Yamada, R., Ishii, K., & Ono, K. (2022) · Biomolecules · doi:10.3390/biom12060859 · Cited by 6 · see citing works
TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration
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
“a Schematic representation of the Tbx3 [42, 43] reporter mouse model employed to assess TBX3 expression patterns shown in c–h.”
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Qu, J.-H., Tarasov, K. V., Tarasova, Y. S., Chakir, K., & Lakatta, E. G. (2023) · Fortune Journal of Health Sciences · doi:10.26502/fjhs.134 · Cited by 5 · see citing works
Engel, J. D., Zhang, X., Mohan, R. A., Lally, N., Soe, A. W., Yang, G., Lu, D., Vila, O. F., Arias, V., Lee, J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.01.547335 · Cited by 5 · see citing works
Li, H., Tang, Q., Yang, T., Wang, Z., Li, D., Wang, L., Li, L., Chen, Y., Huang, H. Y., Zhang, Y., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06039-2 · Cited by 4 · see citing works
Fan, W., Yang, C., Hou, X., Wan, J., & Liao, B. (2022) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd9110402 · Cited by 4 · see citing works
Ryvkin, A. M., Furman, A., Лебедева, Е. А., & Gonotkov, M. (2024) · Developmental Dynamics · doi:10.1002/dvdy.701 · Cited by 3 · see citing works
A new paradigm for generating high-quality cardiac pacemaker cells from mouse pluripotent stem cells
Lin, Z., Lin, B., Hang, C., Lu, R., Xiong, H., Liu, J., Wang, S., Gong, Z., Zhang, M., Li, D., et al. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01942-w · Cited by 3 · see citing works
Analysing Genetic Programs of Cell Differentiation to Study Cardiac Cell Diversification
Wu, Z., Shen, S., Sun, Y., Werner, T. R., Bradford, S. T., & Palpant, N. J. (2022) · Springer eBooks · doi:10.1007/978-3-030-86140-7_8 · Cited by 2 · see citing works
Bello, R. O., Frew, S., Siddiqui, Y. H., & Minhas, R. (2023) · Muscles · doi:10.3390/muscles2040026 · Cited by 2 · see citing works
A gene desert required for regulatory control of pleiotropic Shox2 expression and embryonic survivalPreprint
Abassah‐Oppong, S., Mannion, B. J., Zoia, M., Rouco, R., Tissières, V., Spurrell, C. H., Roland, V., Darbellay, F., Ljubojevic, A., Gamart, J., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.22.393173 · Cited by 2 · see citing works
Hu, J., He, H., Xu, J., MacDonald, W. A., He, Y., Liu, T., Chen, W. C. W., & Li, G. (2026) · Communications Biology · doi:10.1038/s42003-026-10259-z · Cited by 1 · see citing works
Minhas, R., Loeffler‐Wirth, H., Siddiqui, Y. H., Obrębski, T., Vhashist, S., Nahia, K. A., Paterek, A., Brzozowska, A., Bugajski, Ł., Piwocka, K., et al. (2020) · Research Square · doi:10.21203/rs.3.rs-130687/v1 · Cited by 1 · see citing works
Editorial: Cardiac Pacemaking in Health and Disease: From Genes to Function
D’Souza, A., Boink, G. J. J., Toyoda, F., & Mesirca, P. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.913506 · Cited by 1 · see citing works
Cardiopharyngeal Mesoderm specification into cardiac and skeletal muscle lineages in gastruloidsPreprint
Argiro, L., Chevalier, C., Choquet, C., Nandkishore, N., Ghata, A. S., Baudot, A., Zaffran, S., & Lescroart, F. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.15.540476 · Cited by 1 · see citing works
Self-citationRad Modulation of the L-type Calcium Channel Confers Systolic Advantage in the Heart
Ahern, B. M. (2021) · UKnowledge (University of Kentucky) · doi:10.13023/etd.2021.146
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
Kalyanasundaram, A., Li, N., & Fedorov, V. V. (2023) · Springer eBooks · doi:10.1007/978-3-031-33588-4_6
Making sense of ‘genetic programs’: biomolecular Post–Newell production systems
Capraru, M. D. I. (2024) · Biology & Philosophy · doi:10.1007/s10539-024-09943-3
Odz4 upregulates SAN ‐specific genes to promote differentiation into cardiac pacemaker‐like cells
Dong, A., Yoshizumi, M., & Kokubo, H. (2024) · FEBS Letters · doi:10.1002/1873-3468.15036
Chandrakumar, R., Shenwai, R., Farshidfar, F., Zhang, L., Figarska, S. M., Budan, A., Cisne-Thompson, O., Tefera, A. E., Hoey, T. C., Priest, J. R., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.03.668361
- Authors
- van Eif, V., Stefanovic, S., van Duijvenboden, K., Bakker, M., Wakker, V., de Gier-de Vries, C., Zaffran, S., Verkerk, A. O., Boukens, B. J., & Christoffels, V.
- Affiliations
- Department of Medical Biology, University of Amsterdam, Amsterdam University Medical Centers, Amsterdam, The Netherlands
- Inserm (FR)
- Amsterdam University Medical Centers (NL)
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2019-01-01
- Volume
- 146
- Issue
- 8
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2930421965
- Cited by
- 76
- References
- 95
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 14 · 2023: 12 · 2022: 13 · 2021: 18 · 2020: 11 · 2019: 2
- FWCI
- 8.06
- Type
- journal article
- Language
- en
- Open access
- green
- pure.amsterdamumc.nl
- Licence
- Locations
- Development (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- HAL (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Hartstichting (2016T047)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (TOP 40-00812-98-12086)
- Fondation Leducq (14CVD01)
- 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 › Developmental Biology and Gene Regulation
- Keywords
- sinoatrial node, pacemaker cells, TBX3, transcriptome, BMP signaling, SMOC2, Notch signaling, heart rate, fetal heart development, cardiomyocytes, SHOX2, Isl1, Hox genes
- MeSH terms
- Animals, Calcium-Binding Proteins, Electrocardiography, Female, Flow Cytometry, Humans, Immunohistochemistry, Mice, Mutant Strains, Microscopy, Fluorescence, Sinoatrial Node, Transcription Factors, Homeodomain Proteins, T-Box Domain Proteins, Mice, Transcriptome, LIM-Homeodomain Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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