T-box transcription factor TBX3 reprogrammes mature cardiac myocytes into pacemaker-like cells

Cardiovascular Research

Volumn 94, Issue 3, 2012, Pages 439-449

  Bakker, Martijn L ^a   Boink, Gerard J J ^a,b   Boukens, Bas J ^a   Verkerk, Arie O ^a   Van Den Boogaard, Malou ^a   Den Haan, A Denise ^a   Hoogaars, Willem M H ^c   Buermans, Henk P ^c   De Bakker, Jacques M T ^a,b   Seppen, Jurgen ^a   Tan, Hanno L ^a   Moorman, Antoon F M ^a   T Hoen, Peter A C ^c   Christoffels, Vincent M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ROYAL NETHERLANDS ACADEMY OF ARTS AND SCIENCES   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Conduction; Gene therapy; Ion channel; Pacemaker; Sinoatrial node

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL; SODIUM CHANNEL NAV1.5; T BOX TRANSCRIPTION FACTOR; TAMOXIFEN; TRANSCRIPTION FACTOR TBX3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOWN REGULATION; HEART CONDUCTION; HEART MUSCLE CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINUS NODE;

ANIMALS; BIOLOGICAL CLOCKS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; ION CHANNELS; MICE; MICE, TRANSGENIC; MYOCYTES, CARDIAC; SINOATRIAL NODE; T-BOX DOMAIN PROTEINS;

EID: 84861354654     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs120     Document Type: Article

References (38)

1. Wellens HJ. Cardiac arrhythmias: the quest for a cure: a historical perspective. J Am Coll Cardiol 2004;44:1155-1163. (Pubitemid 39208867)
2. Anderson RH, Yanni J, Boyett MR, Chandler NJ, Dobrzynski H. The anatomy of the cardiac conduction system. Clin Anat 2009;22:99-113.
3. Christoffels VM, Smits GJ, Kispert A, Moorman AF. Development of the pacemaker tissues of the heart. Circ Res 2010;106:240-254.
4. Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev 2008;88:919-982.
5. Marionneau C, Couette B, Liu J, Li H, Mangoni ME, Nargeot J et al. Specific pattern of ionic channel gene expression associated with pacemaker activity in the mouse heart. J Physiol 2005;562:223-234. (Pubitemid 40207799)
6. Chandler NJ, Greener ID, Tellez JO, Inada S, Musa H, Molenaar P et al. Molecular architecture of the human sinus node: insights into the function of the cardiac pacemaker. Circulation 2009;119:1562-1575.
7. Miake J, Marban E, Nuss HB. Biological pacemaker created by gene transfer. Nature 2002;419:132-133. (Pubitemid 35025436)
8. Lakatta EG, Vinogradova TM, Maltsev VA. The missing link in the mystery of normal automaticity of cardiac pacemaker cells. Ann N Y Acad Sci 2008;1123:41-57. (Pubitemid 351431302)
9. Joyner RW, van Capelle FJL. Propagation through electrically coupled cells. How a small SA node drives a large atrium. Biophys J 1986;50:1157-1164. (Pubitemid 17206001)
10. Kreuzberg MM, Sohl G, Kim JS, Verselis VK, Willecke K, Bukauskas FF. Functional properties of mouse connexin30.2 expressed in the conduction system of the heart. Circ Res 2005;96:1169-1177. (Pubitemid 40827692)
11. Schram G, Pourrier M, Melnyk P, Nattel S. Differential distribution of cardiac ion channel expression as a basis for regional specialization in electrical function. Circ Res 2002;90:939-950. (Pubitemid 34633859)
12. Op't Hof T. The mammalian sinoatrial node. Cardiovasc Drugs Ther 1988;6:573-598.
13. Dobrzynski H, Boyett MR, Anderson RH. New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation 2007;115:1921-1932. (Pubitemid 46598906)
14. Bamshad M, Lin RC, Law DJ, Watkins WS, Krakowiak PA, Moore ME et al. Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat Genet 1997;16:311-315. (Pubitemid 27280219)
15. Hoogaars WMH, Tessari A, Moorman AFM, de Boer PAJ, Hagoort J, Soufan AT et al. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res 2004;62:489-499. (Pubitemid 38648963)
16. Hoogaars WM, Engel A, Brons JF, Verkerk AO, de Lange FJ,Wong LY et al. Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria. Genes Dev 2007;21:1098-1112. (Pubitemid 46686478)
17. Bakker ML, Boukens BJ, Mommersteeg MTM, Brons JF, Wakker V, Moorman AFM et al. Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ Res 2008;102:1340-1349.
18. Frank DU, Carter KL, Thomas KR, Burr RM, Bakker ML, Coetzee WA et al. Lethal arrhythmias in Tbx3-deficient mice reveal extreme dosage sensitivity of cardiac conduction system function and homeostasis. Proc Natl Acad Sci USA 2012;109:E154-E163.
19. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM et al. Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res 2001;89:20-25. (Pubitemid 34135487)
20. Novak A, Guo C, Yang W, Nagy A, Lobe CG. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 2000;28:147-155.
21. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ et al. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 2009;37:e45.
22. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 2002;18(Suppl 1):S96-104. (Pubitemid 41185642)
23. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:1-25.
24. Verkerk AO, Den Ruijter HM, Bourier J, Boukens BJ, Brouwer IA, Wilders R et al. Dietary fish oil reduces pacemaker current and heart rate in rabbit. Heart Rhythm 2009;6:1485-1492.
25. Boink GJ, Verkerk AO, van Amersfoorth SC, Tasseron SJ, van der RR, Bakker D et al. Engineering physiologically controlled pacemaker cells with lentiviral HCN4 gene transfer. J Gene Med 2008;10:487-497. (Pubitemid 351753518)
26. de Haan RL. Differentiation of the atrioventricular conducting system of the heart. Circulation 1961;24:458-470.
27. Briegel KJ, Baldwin HS, Epstein JA, Joyner AL. Congenital heart disease reminiscent of partial trisomy 2p syndrome in mice transgenic for the transcription factor Lbh. Development 2005;132:3305-3316. (Pubitemid 41167157)
28. Fedorov VV, Schuessler RB, Hemphill M, Ambrosi CM, Chang R, Voloshina AS et al. Structural and functional evidence for discrete exit pathways that connect the canine sinoatrial node and atria. Circ Res 2009;104:915-923.
29. Schuessler RB, Boineau JP, Bromberg BI. Origin of the sinus impulse. J Cardiovasc Electrophysiol 1996;7:263-274. (Pubitemid 26082813)
30. Tellez JO, Dobrzynski H, Greener ID, Graham GM, Laing E, Honjo H et al. Differential expression of ion channel transcripts in atrial muscle and sinoatrial node in rabbit. Circ Res 2006;99:1384-1393. (Pubitemid 44949674)
31. Lei M, Goddard C, Liu J, Leoni AL, Royer A, Fung SSM et al. Sinus node dysfunction following targeted disruption of the murine cardiac sodium channel gene Scn5a. J Physiol 2005;567:387-400. (Pubitemid 41301040)
32. Goldfarb M, Schoorlemmer J, Williams A, Diwakar S, Wang Q, Huang X et al. Fibroblast growth factor homologous factors control neuronal excitability through modulation of voltage-gated sodium channels. Neuron 2007;55:449-463. (Pubitemid 47126267)
33. Rosen MR, Robinson RB, Brink PR, Cohen IS. The road to biological pacing. Nat Rev Cardiol 2011;8:656-666.
34. Bucchi A, Plotnikov AN, Shlapakova I, Danilo P Jr, Kryukova Y, Qu J et al. Wild-type and mutant HCN channels in a tandem biological-electronic cardiac pacemaker. Circulation 2006;114:992-999. (Pubitemid 44358875)
35. Tse HF, Xue T, Lau CP, Siu CW, Wang K, Zhang QY et al. Bioartificial sinus node constructed via in vivo gene transfer of an engineered pacemaker HCN Channel reduces the dependence on electronic pacemaker in a sick-sinus syndrome model. Circulation 2006;114:1000-1011. (Pubitemid 44358876)
36. Edelberg JM, Huang DT, Josephson ME, Rosenberg RD. Molecular enhancement of porcine cardiac chronotropy. Heart 2001;86:559-562. (Pubitemid 32999871)
37. Lieu DK, Chan YC, Lau CP, Tse HF, Siu CW, Li RA. Overexpression of HCN-encoded pacemaker current silences bioartificial pacemakers. Heart Rhythm 2008;5:1310-1317.
38. Piron J, Quang KL, Briec F, Amirault JC, Leoni AL, Desigaux L et al. Biological pacemaker engineered by nonviral gene transfer in a mouse model of complete atrioventricular block. Mol Ther 2008;16:1937-1943.