Myocardial notch signaling reprograms cardiomyocytes to a conduction-like phenotype

Circulation

Volumn 126, Issue 9, 2012, Pages 1058-1066

  Rentschler, Stacey ^a   Yen, Alberta H ^a   Lu, Jia ^b   Petrenko, Nataliya B ^a   Lu, Min Min ^a   Manderfield, Lauren J ^a   Patel, Vickas V ^a   Fishman, Glenn I ^b   Epstein, Jonathan A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Action potentials; Conduction; Pacemakers; Purkinje; Reprogramming

Indexed keywords

NOTCH RECEPTOR; TRANSCRIPTOME;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENE EXPRESSION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; UPREGULATION;

ACTION POTENTIALS; ADENOVIRIDAE; ANIMALS; ANIMALS, NEWBORN; ATRIOVENTRICULAR NODE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINEAGE; CONTACTIN 2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MYOCARDIUM; MYOCYTES, CARDIAC; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PHENOTYPE; PURKINJE FIBERS; RECEPTOR, NOTCH1; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SODIUM CHANNELS; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 84865501621     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.112.103390     Document Type: Article

References (36)

1. Rosen MR, Robinson RB, Brink PR, Cohen IS The road to biological pacing. Nat Rev Cardiol. 2011;8:656-666.
2. Gourdie RG, Mima T, Thompson RP, Mikawa T Terminal diversification of the myocyte lineage generates Purkinje fibers of the cardiac conduction system. Development. 1995;121:1423-1431.
3. Cheng G, Litchenberg WH, Cole GJ, Mikawa T, Thompson RP, Gourdie RG Development of the cardiac conduction system involves recruitment within a multipotent cardiomyogenic lineage. Development. 1999;126: 5041-5049. (Pubitemid 30000417)
4. Miquerol L, Moreno-Rascon N, Beyer S, Dupays L, Meilhac SM, Buckingham ME, Franco D, Kelly RG Biphasic development of the mammalian ventricular conduction system. Circ Res. 2010;107:153-161.
5. Gourdie RG, Wei Y, Kim D, Klatt SC, Mikawa T Endothelin-induced conversion of embryonic heart muscle cells into impulse-conducting Purkinje fibers. Proc Natl Acad Sci U S A 1998;95:6815-6818. (Pubitemid 28278063)
6. Rentschler S, Zander J, Meyers K, France D, Levine R, Porter G, Rivkees SA, Morley GE, Fishman GI Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc Natl Acad Sci U S A 2002;99: 10464-10469.
7. Zhu WZ, Xie Y, Moyes KW, Gold JD, Askari B, Laflamme MA Neuregulin/ErbB signaling regulates cardiac subtype specification in differentiating human embryonic stem cells. Circ Res. 2010;107:776-786.
8. Wiese C, Grieskamp T, Airik R, Mommersteeg MT, Gardiwal A, de Gier-de Vries C, Schuster-Gossler K, Moorman AF, Kispert A, Christoffels VM Formation of the sinus node head and differentiation of sinus node myocardium are independently regulated by Tbx18 and Tbx3. Circ Res. 2009;104:388-397.
9. Bakker ML, Boukens BJ, Mommersteeg MT, Brons JF, Wakker V, Moorman AF, Christoffels VM Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ Res. 2008;102:1340-1349.
10. Hoogaars WM, Engel A, Brons JF, Verkerk AO, de Lange FJ, Wong LY, Bakker ML, Clout DE, Wakker V, Barnett P, Ravesloot JH, Moorman AF, Verheijck EE, Christoffels VM Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria. Genes Dev. 2007;21:1098-1112. (Pubitemid 46686478)
11. Jay PY, Harris BS, Maguire CT, Buerger A, Wakimoto H, Tanaka M, Kupershmidt S, Roden DM, Schultheiss TM, O'Brien TX, Gourdie RG, Berul CI, Izumo S Nkx2-5 mutation causes anatomic hypoplasia of the cardiac conduction system. J Clin Invest. 2004;113:1130-1137. (Pubitemid 38544098)
12. Meysen S, Marger L, Hewett KW, Jarry-Guichard T, Agarkova I, Chauvin JP, Perriard JC, Izumo S, Gourdie RG, Mangoni ME, Nargeot J, Gros D, Miquerol L Nkx2.5 cell-autonomous gene function is required for the postnatal formation of the peripheral ventricular conduction system. Dev Biol. 2007;303:740-753. (Pubitemid 46350762)
13. Moskowitz IP, Kim JB, Moore ML, Wolf CM, Peterson MA, Shendure J, Nobrega MA, Yokota Y, Berul C, Izumo S, Seidman JG, Seidman CE A molecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development. Cell. 2007;129:1365-1376. (Pubitemid 46962088)
14. Milan DJ, Giokas AC, Serluca FC, Peterson RT, MacRae CA Notch1b and neuregulin are required for specification of central cardiac conduction tissue. Development. 2006;133:1125-1132.
15. Rentschler S, Harris BS, Kuznekoff L, Jain R, Manderfield L, Lu MM, Morley GE, Patel VV, Epstein JA Notch signaling regulates murine atrioventricular conduction and the formation of accessory pathways. J Clin Invest. 2011;121:525-533.
16. Rentschler S, Vaidya DM, Tamaddon H, Degenhardt K, Sassoon D, Morley GE, Jalife J, Fishman GI Visualization and functional characterization of the developing murine cardiac conduction system. Development. 2001;128:1785-1792. (Pubitemid 32514858)
17. Pallante BA, Giovannone S, Fang-Yu L, Zhang J, Liu N, Kang G, Dun W, Boyden PA, Fishman GI Contactin-2 expression in the cardiac Purkinje fiber network. Circ Arrhythm Electrophysiol. 2010;3:186-194.
18. Stanger BZ, Datar R, Murtaugh LC, Melton DA Direct regulation of intestinal fate by Notch. Proc Natl Acad Sci U S A 2005;102: 12443-12448. (Pubitemid 41266378)
19. Aster JC, Xu L, Karnell FG, Patriub V, Pui JC, Pear WS Essential roles for ankyrin repeat and transactivation domains in induction of T-cell leukemia by notch1. Mol Cell Biol. 2000;20:7505-7515.
20. Mitra R, Morad M A uniform enzymatic method for dissociation of myocytes from hearts and stomachs of vertebrates. Am J Physiol. 1985; 249:H1056-H1060. (Pubitemid 16197350)
21. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981;391:85-100. (Pubitemid 11012976)
22. Ismat FA, Zhang M, Kook H, Huang B, Zhou R, Ferrari VA, Epstein JA, Patel VV Homeobox protein Hop functions in the adult cardiac conduction system. Circ Res. 2005;96:898-903. (Pubitemid 40604974)
23. Herrmann S, Layh B, Ludwig A Novel insights into the distribution of cardiac HCN channels: an expression study in the mouse heart. J Mol Cell Cardiol. 2011;51:997-1006.
24. Kwon C, Cheng P, King IN, Andersen P, Shenje L, Nigam V, Srivastava D Notch post-translationally regulates beta-catenin protein in stem and progenitor cells. Nat Cell Biol. 2011;13:1244-1251.
25. Qu J, Plotnikov AN, Danilo P Jr, Shlapakova I, Cohen IS, Robinson RB, Rosen MR Expression and function of a biological pacemaker in canine heart. Circulation. 2003;107:1106-1109. (Pubitemid 36297200)
26. Plotnikov AN, Sosunov EA, Qu J, Shlapakova IN, Anyukhovsky EP, Liu L, Janse MJ, Brink PR, Cohen IS, Robinson RB, Danilo P Jr, Rosen MR Biological pacemaker implanted in canine left bundle branch provides ventricular escape rhythms that have physiologically acceptable rates. Circulation. 2004;109:506-512. (Pubitemid 38168514)
27. Bucchi A, Plotnikov AN, Shlapakova I, Danilo P Jr, Kryukova Y, Qu J, Lu Z, Liu H, Pan Z, Potapova I, KenKnight B, Girouard S, Cohen IS, Brink PR, Robinson RB, Rosen MR Wild-type and mutant HCN channels in a tandem biological-electronic cardiac pacemaker. Circulation. 2006;114: 992-999. (Pubitemid 44358875)
28. Pashmforoush M, Lu JT, Chen H, Amand TS, Kondo R, Pradervand S, Evans SM, Clark B, Feramisco JR, Giles W, Ho SY, Benson DW, Silberbach M, Shou W, Chien KR Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell. 2004;117: 373-386. (Pubitemid 38534543)
29. Bruneau BG, Nemer G, Schmitt JP, Charron F, Robitaille L, Caron S, Conner DA, Gessler M, Nemer M, Seidman CE, Seidman JG 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. (Pubitemid 32900662)
30. Briggs LE, Takeda M, Cuadra AE, Wakimoto H, Marks MH, Walker AJ, Seki T, Oh SP, Lu JT, Sumners C, Raizada MK, Horikoshi N, Weinberg EO, Yasui K, Ikeda Y, Chien KR, Kasahara H Perinatal loss of Nkx2-5 results in rapid conduction and contraction defects. Circ Res. 2008;103: 580-590.
31. Munshi NV, McAnally J, Bezprozvannaya S, Berry JM, Richardson JA, Hill JA, Olson EN Cx30.2 enhancer analysis identifies Gata4 as a novel regulator of atrioventricular delay. Development. 2009;136:2665-2674.
32. Hahurij ND, Gittenberger-De Groot AC, Kolditz DP, Bokenkamp R, Schalij MJ, Poelmann RE, Blom NA Accessory atrioventricular myocardial connections in the developing human heart: relevance for perinatal supraventricular tachycardias. Circulation. 2008;117:2850-2858. (Pubitemid 351787077)
33. Light PE, Wallace CH, Dyck Jr. Constitutively active adenosine monophosphate-activated protein kinase regulates voltage-gated sodium channels in ventricular myocytes. Circulation. 2003;107:1962-1965. (Pubitemid 36506067)
34. Aanhaanen WT, Boukens BJ, Sizarov A, Wakker V, de Gier-de Vries C, van Ginneken AC, Moorman AF, Coronel R, Christoffels VM Defective Tbx2-dependent patterning of the atrioventricular canal myocardium causes accessory pathway formation in mice. J Clin Invest. 2011;121: 534-544.
35. Le Gloan L, Pichon O, Isidor B, Boceno M, Rival JM, David A, Le Caignec C A 8.26Mb deletion in 6q16 and a 4.95Mb deletion in 20p12 including JAG1 and BMP2 in a patient with Alagille syndrome and Wolff-Parkinson-White syndrome. Eur J Med Genet. 2008;51:651-657.
36. Palatinus JA, O'Quinn MP, Barker RJ, Harris BS, Jourdan J, Gourdie RG ZO-1 determines adherens and gap junction localization at intercalated disks. Am J Physiol Heart Circ Physiol. 2011;300:H583-H594.