Notch signaling regulates murine atrioventricular conduction and the formation of accessory pathways

Journal of Clinical Investigation

Volumn 121, Issue 2, 2011, Pages 525-533

  Rentschler, Stacey ^a,b   Harris, Brett S ^c   Kuznekoff, Laura ^d   Jain, Rajan ^a,b   Manderfield, Lauren ^a   Lu, Min Min ^b   Morley, Gregory E ^d   Patel, Vickas V ^b   Epstein, Jonathan A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 30; NOTCH RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATRIOVENTRICULAR CONDUCTION; ELECTROPHYSIOLOGY; EMBRYO; HEART ATRIOVENTRICULAR NODE; HEART ATRIUM ARRHYTHMIA; HEART MUSCLE; HEART MUSCLE CONDUCTION DISTURBANCE; HEART MUSCLE CONDUCTION SYSTEM; HEART PALPITATION; HEART PREEXCITATION; MATURATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUDDEN DEATH; SYNCOPE; TACHYCARDIA; WOLFF PARKINSON WHITE SYNDROME;

ACCESSORY ATRIOVENTRICULAR BUNDLE; ANIMALS; ATRIOVENTRICULAR NODE; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; HEART CONDUCTION SYSTEM; HUMANS; MICE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; WOLFF-PARKINSON-WHITE SYNDROME;

EID: 79551521516     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44470     Document Type: Article

References (58)

1. Bakker ML, Christoffels VM, Moorman AF. The cardiac pacemaker and conduction system develops from embryonic myocardium that retains its primitive phenotype. J Cardiovasc Pharmacol. 2010;56(1):6-15.
2. Christoffels VM, Smits GJ, Kispert A, Moorman AF. Development of the pacemaker tissues of the heart. Circ Res. 2010;106(2):240-254.
3. Aanhaanen WT, et al. The Tbx2+ primary myocardium of the atrioventricular canal forms the atrioventricular node and the base of the left ventricle. Circ Res. 2009;104(11):1267-1274.
4. Horsthuis T, et al. Gene expression profiling of the forming atrioventricular node using a novel tbx3-based node-specific transgenic reporter. Circ Res. 2009;105(1):61-69.
5. Kokubo H, Tomita-Miyagawa S, Hamada Y, Saga Y. Hesr1 and Hesr2 regulate atrioventricular boundary formation in the developing heart through the repression of Tbx2. Development. 2007;134(4):747-755. (Pubitemid 46437916)
6. Rutenberg JB, Fischer A, Jia H, Gessler M, Zhong TP, Mercola M. Developmental patterning of the cardiac atrioventricular canal by Notch and Hairy-related transcription factors. Development. 2006;133(21):4381-4390.
7. Hahurij ND, et al. Accessory atrioventricular myocardial connections in the developing human heart: relevance for perinatal supraventricular tachycardias. Circulation. 2008;117(22):2850-2858.
8. Gittenberger-de Groot AC, Vrancken Peeters MP, Mentink MM, Gourdie RG, Poelmann RE. Epicardium- derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res. 1998;82(10):1043-1052.
9. Zhou B, von Gise A, Ma Q, Hu YW, Pu WT. Genetic fate mapping demonstrates contribution of epicardium-derived cells to the annulus fibrosis of the mammalian heart. Dev Biol. 2010;338(2):251-261.
10. Kolditz DP, et al. Epicardium-derived cells in development of annulus fibrosis and persistence of accessory pathways. Circulation. 2008;117(12):1508-1517.
11. 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(6):1125-1132.
12. Watanabe Y, et al. Activation of Notch1 signaling in cardiogenic mesoderm induces abnormal heart morphogenesis in mouse. Development. 2006;133(9):1625-1634.
13. Moskowitz IP, et al. The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development. 2004;131(16):4107-4116.
14. Munshi NV, et al. Cx30.2 enhancer analysis identifies Gata4 as a novel regulator of atrioventricular delay. Development. 2009;136(15):2665-2674.
15. De Bacquer D, De Backer G, Kornitzer M. Prevalences of ECG findings in large population based samples of men and women. Heart. 2000;84(6):625-633.
16. Goudevenos JA, Katsouras CS, Graekas G, Argiri O, Giogiakas V, Sideris DA. Ventricular pre-excitation in the general population: a study on the mode of presentation and clinical course. Heart. 2000;83(1):29-34. (Pubitemid 30307635)
17. Munger TM, et al. A population study of the natural history of Wolff-Parkinson-White syndrome in Olmsted County, Minnesota, 1953-1989. Circulation. 1993;87(3):866-873.
18. Wan Q, Wu N, Fan W, Tang YY, Jin L, Fang Q. Clinical manifestations and prevalence of different types of supraventricular tachycardia among Chinese. Chin Med J (Engl). 1992;105(4):284-288.
19. Doevendans PA, Wellens HJ. Wolff-Parkinson-white syndrome: a genetic disease? Circulation. 2001;104(25):3014-3016.
20. Follath F, Hallidie-Smith KA. Unusual electrocardiographic changes in Ebstein's anomaly. Br Heart J. 1972;34(5):513-519.
21. Arad M, et al. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J Clin Invest. 2002;109(3):357-362.
22. Gollob MH, et al. Identification of a gene responsible for familial Wolff-Parkinson-White syndrome. N Engl J Med. 2001;344(24):1823-1831.
23. Blair E, et al. Mutations in the gamma(2) subunit of AMP-activated protein kinase cause familial hypertrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis. Hum Mol Genet. 2001;10(11):1215-1220. (Pubitemid 32487544)
24. Le Gloan L, et al. 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(6):651-657.
25. Lalani SR, et al. 20p12.3 microdeletion predisposes to Wolff-Parkinson-White syndrome with variable neurocognitive deficits. J Med Genet. 2009;46(3):168-175.
26. Stroud DM, et al. Abnormal conduction and morphology in the atrioventricular node of mice with atrioventricular canal targeted deletion of Alk3/Bmpr1a receptor. Circulation. 2007;116(22):2535-2543.
27. Gaussin V, et al. Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res. 2005;97(3):219-226.
28. Li L, et al. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet. 1997;16(3):243-251.
29. Oda T, et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet. 1997;16(3):235-242. (Pubitemid 27280205)
30. Maillard I, et al. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood. 2004;104(6):1696-1702.
31. High FA, et al. An essential role for Notch in neural crest during cardiovascular development and smooth muscle differentiation. J Clin Invest. 2007;117(2):353-363.
32. Chen J, Kubalak SW, Chien KR. Ventricular muscle-restricted targeting of the RXRalpha gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development. 1998;125(10):1943-1949.
33. Pashmforoush M, et al. Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block. Cell. 2004;117(3):373-386.
34. Aanhaanen WT, et al. Developmental origin, growth, and three-dimensional architecture of the atrioventricular conduction axis of the mouse heart. Circ Res. 2010;107(6):728-736.
35. Kreuzberg MM, Willecke K, Bukauskas FF. Connexin-mediated cardiac impulse propagation: connexin 30.2 slows atrioventricular conduction in mouse heart. Trends Cardiovasc Med. 2006;16(8):266-272. (Pubitemid 44572802)
36. Schrickel JW, et al. Normal impulse propagation in the atrioventricular conduction system of Cx30.2/Cx40 double deficient mice. J Mol Cell Cardiol. 2009;46(5):644-652.
37. Stanger BZ, Datar R, Murtaugh LC, Melton DA. Direct regulation of intestinal fate by Notch. Proc Natl Acad Sci U S A. 2005;102(35):12443-12448. (Pubitemid 41266378)
38. de Lange FJ, et al. Lineage and morphogenetic analysis of the cardiac valves. Circ Res. 2004;95(6):645-654.
39. Ho SY. Accessory atrioventricular pathways: getting to the origins. Circulation. 2008;117(12):1502-1504.
40. Schumacher B, Tebbenjohanns J, Pfeiffer D, Omran H, Jung W, Luderitz B. Prospective study of retrograde coronary venography in patients with posteroseptal and left-sided accessory atrioventricular pathways. Am Heart J. 1995;130(5):1031-1039.
41. Sun Y, et al. Coronary sinus-ventricular accessory connections producing posteroseptal and left posterior accessory pathways: incidence and electrophysiological identification. Circulation. 2002;106(11):1362-1367.
42. Bakker ML, et al. Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ Res. 2008;102(11):1340-1349.
43. Hanon S, Shapiro M, Schweitzer P. Early history of the pre-excitation syndrome. Europace. 2005;7(1):28-33.
44. Sidhu JS, et al. Transgenic mouse model of ventricular preexcitation and atrioventricular reentrant tachycardia induced by an AMP-activated protein kinase loss-of-function mutation responsible for Wolff-Parkinson-White syndrome. Circulation. 2005;111(1):21-29.
45. Arad M, et al. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation. 2003;107(22):2850-2856.
46. Patel VV, et al. Electrophysiologic characterization and postnatal development of ventricular pre-excitation in a mouse model of cardiac hypertrophy and Wolff-Parkinson-White syndrome. J Am Coll Cardiol. 2003;42(5):942-951.
47. Luna-Zurita L, et al. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J Clin Invest. 2010;120(10):3493-3507.
48. High FA, Epstein JA. The multifaceted role of Notch in cardiac development and disease. Nat Rev Genet. 2008;9(1):49-61.
49. Christoffels VM, Hoogaars WM, Tessari A, Clout DE, Moorman AF, Campione M. T-box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers. Dev Dyn. 2004;229(4):763-770.
50. Anderson KR, Zuberbuhler JR, Anderson RH, Becker AE, Lie JT. Morphologic spectrum of Ebstein's anomaly of the heart: a review. Mayo Clin Proc. 1979;54(3):174-180. (Pubitemid 9144490)
51. Kuo CT, et al. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 1997;11(8):1048-1060.
52. Kaartinen V, Dudas M, Nagy A, Sridurongrit S, Lu MM, Epstein JA. Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells. Development. 2004;131(14):3481-3490. (Pubitemid 39139893)
53. Chapman DL, et al. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn. 1996;206(4):379-390.
54. Ismat FA, et al. Homeobox protein Hop functions in the adult cardiac conduction system. Circ Res. 2005;96(8):898-903.
55. Braet F, De Zanger R, Wisse E. Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells. J Microsc. 1997;186(pt 1):84-87.
56. Rentschler S, et al. Visualization and functional characterization of the developing murine cardiac conduction system. Development. 2001;128(10):1785- 1792.
57. Morley GE, et al. Reduced intercellular coupling leads to paradoxical propagation across the Purkinje-ventricular junction and aberrant myocardial activation. Proc Natl Acad Sci U S A. 2005;102(11):4126-4129.
58. Fedorov VV, et al. Application of blebbistatin as an excitation- contraction uncoupler for electrophysiologic study of rat and rabbit hearts. Heart Rhythm. 2007;4(5):619-626.