Genetic isolation of stem cell-derived pacemaker-nodal cardiac myocytes

Molecular and Cellular Biochemistry

Volumn 383, Issue 1-2, 2013, Pages 161-171

  Hashem, Sherin I ^a   Claycomb, William C ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atrioventricular; Embryoid body; Embryonic stem cell; Pacemaker; Sinoatrial

Indexed keywords

CALCIUM; CELL PROTEIN; ION CHANNEL; PROTEIN CX30.2; PROTEIN SHOX2; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ARTIFICIAL HEART PACEMAKER; CALCIUM CELL LEVEL; CELL ISOLATION; CELL STRUCTURE; CONTROLLED STUDY; CX30.2 GENE; CX45 GENE; DIASTOLE; EMBRYOID BODY; EMBRYONIC STEM CELL; ENHANCER REGION; GENE; GENE EXPRESSION; HCN4 GENE; HEART ARRHYTHMIA; HEART ATRIOVENTRICULAR NODE; HEART DEPOLARIZATION; HEART MUSCLE CELL; MOUSE; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; SHOX2 GENE; SINUS NODE; TBX2 GENE; TBX3 GENE;

ARANEAE;

ANIMALS; ATRIOVENTRICULAR NODE; BIOLOGICAL CLOCKS; BLOTTING, WESTERN; CALCIUM; CELL AGGREGATION; CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CONNEXINS; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MICE; MYOCYTES, CARDIAC; SINOATRIAL NODE;

EID: 84885424479     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-013-1764-x     Document Type: Article

References (63)

1. Spooner PM, Albert C, Benjamin EJ, Boineau R, Elston RC, George AL Jr, Jouven X, Kuller LH, MacCluer JW, Marban E, Muller JE, Schwartz PJ, Siscovick DS, Tracy RP, Zareba W, Zipes DP (2001) Sudden cardiac death, genes, and arrhythmogenesis: consideration of new population and mechanistic approaches from a national heart, lung, and blood institute workshop, part I. Circulation 103:2361-2364
2. Rosen MR, Brink PR, Cohen IS, Robinson RB (2004) Genes, stem cells and biological pacemakers. Cardiovasc Res 64:12-23
3. Rajesh G, Francis J (2006) Biological pacemakers. Indian Pacing Electrophysiol J 6:1-5
4. Reinlib L, Field L (2000) Cell transplantation as future therapy for cardiovascular disease?: a workshop of the National Heart, Lung, and Blood Institute. Circulation 101:E182-E187
5. Maltsev VA, Rohwedel J, Hescheler J, Wobus AM (1993) Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev 44:41-50
6. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L (2004) Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 22:1282-1289
7. Xue T, Cho HC, Akar FG, Tsang SY, Jones SP, Marban E, Tomaselli GF, Li RA (2005) Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation 111:11-20
8. Keith A, Flack M (1907) The form and nature of the muscular connections between the primary divisions of the vertebrate heart. J Anat Physiol 41:172-189
9. Opthof T (1988) The mammalian sinoatrial node. Cardiovasc Drugs Ther 1:573-597
10. Espinoza-Lewis RA, Yu L, He F, Liu H, Tang R, Shi J, Sun X, Martin JF, Wang D, Yang J, Chen Y (2009) Shox2 is essential for the differentiation of cardiac pacemaker cells by repressing Nk2-5. Dev Biol 327:376-385
11. Blaschke RJ, Hahurij ND, Kuijper S, Just S, Wisse LJ, Deissler K, Maxelon T, Anastassiadis K, Spitzer J, Hardt SE, Scholer H, Feitsma H, Rottbauer W, Blum M, Meijlink F, Rappold G, Gittenberger-de Groot AC (2007) Targeted mutation reveals essential functions of the homeodomain transcription factor Shox2 in sinoatrial and pacemaking development. Circulation 115:1830-1838
12. Dobrzynski H, Nikolski VP, Sambelashvili AT, Greener ID, Yamamoto M, Boyett MR, Efimov IR (2003) Site of origin and molecular substrate of atrioventricular junctional rhythm in the rabbit heart. Circ Res 93:1102-1110
13. James TN (2003) Structure and function of the sinus node, AV node and his bundle of the human heart: part II-function. Prog Cardiovasc Dis 45:327-360
14. Munshi NV, McAnally J, Bezprozvannaya S, Berry JM, Richardson JA, Hill JA, Olson EN (2009) Cx30.2 enhancer analysis identifies Gata4 as a novel regulator of atrioventricular delay. Development 136:2665-2674
15. Klug MG, Soonpaa MH, Koh GY, Field LJ (1996) Genetically selected cardiomyocytes from differentiating embryonic stem cells form stable intracardiac grafts. J Clin Invest 98:216-224
16. Jackson M, Taylor AH, Jones EA, Forrester LM (2010) The culture of mouse embryonic stem cells and formation of embryoid bodies. Methods Mol Biol 633:1-18
17. White SM, Claycomb WC (2005) Embryonic stem cells form an organized, functional cardiac conduction system in vitro. Am J Physiol Heart Circ Physiol 288:H670-H679
18. Puskaric S, Schmitteckert S, Mori AD, Glaser A, Schneider KU, Bruneau BG, Blaschke RJ, Steinbeisser H, Rappold G (2010) Shox2 mediates Tbx5 activity by regulating Bmp4 in the pacemaker region of the developing heart. Hum Mol Genet 19:4625-4633
19. White SM, Constantin PE, Claycomb WC (2004) Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 286:H823-H829
20. Lam ML, Hashem SI, Claycomb WC (2011) Embryonic stem cell-derived cardiomyocytes harbor a subpopulation of niche-forming Sca-1+ progenitor cells. Mol Cell Biochem 349:69-76
21. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408
22. DiFrancesco D, Ferroni A, Mazzanti M, Tromba C (1986) Properties of the hyperpolarizing-activated current (if) in cells isolated from the rabbit sino-atrial node. J Physiol 377:61-88
23. Verheijck EE, Wessels A, van Ginneken AC, Bourier J, Markman MW, Vermeulen JL, de Bakker JM, Lamers WH, Opthof T, Bouman LN (1998) Distribution of atrial and nodal cells within the rabbit sinoatrial node: models of sinoatrial transition. Circulation 97:1623-1631
24. Wu J, Schuessler RB, Rodefeld MD, Saffitz JE, Boineau JP (2001) Morphological and membrane characteristics of spider and spindle cells isolated from rabbit sinus node. Am J Physiol Heart Circ Physiol 280:H1232-H1240
25. 2+ channels in cardiac pacemaker activity. Proc Natl Acad Sci USA 100:5543-5548
26. Mangoni ME, Couette B, Marger L, Bourinet E, Striessnig J, Nargeot J (2006) Voltage-dependent calcium channels and cardiac pacemaker activity: from ionic currents to genes. Prog Biophys Mol Biol 90:38-63
27. Marger L, Mesirca P, Alig J, Torrente A, Dubel S, Engeland B, Kanani S, Fontanaud P, Striessnig J, Shin HS, Isbrandt D, Ehmke H, Nargeot J, Mangoni ME (2011) Functional roles of Ca(v)1.3, Ca(v)3.1 and HCN channels in automaticity of mouse atrioventricular cells: insights into the atrioventricular pacemaker mechanism. Channels (Austin) 5:251-261
28. Halbach M, Egert U, Hescheler J, Banach K (2003) Estimation of action potential changes from field potential recordings in multicellular mouse cardiac myocyte cultures. Cell Physiol Biochem 13:271-284
29. Lakatta EG, Maltsev VA, Bogdanov KY, Stern MD, Vinogradova TM (2003) Cyclic variation of intracellular calcium: a critical factor for cardiac pacemaker cell dominance. Circ Res 92:e45-e50
30. Maltsev VA, Vinogradova TM, Lakatta EG (2006) The emergence of a general theory of the initiation and strength of the heartbeat. J Pharmacol Sci 100:338-369
31. 2+ releases in rabbit sinoatrial nodal cells impart an exponential phase to the late diastolic depolarization that controls their chronotropic state. Circ Res 99:979-987
32. 2+ oscillations drive sinoatrial nodal cell pacemaker function to make the heart tick. Ann N Y Acad Sci 1047:138-156
33. 2+ store oscillations and spontaneous beating of cardiac pacemaker cells. Circ Res 98:505-514
34. Maltsev VA, Vinogradova TM, Bogdanov KY, Lakatta EG, Stern MD (2004) Diastolic calcium release controls the beating rate of rabbit sinoatrial node cells: numerical modeling of the coupling process. Biophys J 86:2596-2605
35. Habets PE, Moorman AF, Clout DE, van Roon MA, Lingbeek M, van Lohuizen M, Campione M, Christoffels VM (2002) Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev 16:1234-1246
36. Garg V, Kathiriya IS, Barnes R, Schluterman MK, King IN, Butler CA, Rothrock CR, Eapen RS, Hirayama-Yamada K, Joo K, Matsuoka R, Cohen JC, Srivastava D (2003) GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424:443-447
37. Lee Y, Shioi T, Kasahara H, Jobe SM, Wiese RJ, Markham BE, Izumo S (1998) The cardiac tissue-restricted homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol Cell Biol 18:3120-3129
38. Adamo RF, Guay CL, Edwards AV, Wessels A, Burch JB (2004) GATA-6 gene enhancer contains nested regulatory modules for primary myocardium and the embedded nascent atrioventricular conduction system. Anat Rec A Discov Mol Cell Evol Biol 280:1062-1071
39. Boogerd KJ, Wong LY, Christoffels VM, Klarenbeek M, Ruijter JM, Moorman AF, Barnett P (2008) Msx1 and Msx2 are functional interacting partners of T-box factors in the regulation of Connexin43. Cardiovasc Res 78:485-493
40. Choi M, Stottmann RW, Yang YP, Meyers EN, Klingensmith J (2007) The bone morphogenetic protein antagonist noggin regulates mammalian cardiac morphogenesis. Circ Res 100:220-228
41. Christoffels VM, Smits GJ, Kispert A, Moorman AF (2010) Development of the pacemaker tissues of the heart. Circ Res 106:240-254
42. Mangoni ME, Nargeot J (2008) Genesis and regulation of the heart automaticity. Physiol Rev 88:919-982
43. Yunker AM, Sharp AH, Sundarraj S, Ranganathan V, Copeland TD, McEnery MW (2003) Immunological characterization of T-type voltage-dependent calcium channel CaV3.1 (alpha 1G) and CaV3.3 (alpha 1I) isoforms reveal differences in their localization, expression, and neural development. Neuroscience 117:321-335
44. Bogdanov KY, Vinogradova TM, Lakatta EG (2001) Sinoatrial nodal cell ryanodine receptor and Na(+)-Ca(2+) exchanger: molecular partners in pacemaker regulation. Circ Res 88:1254-1258
45. Miake J, Marban E, Nuss HB (2003) Functional role of inward rectifier current in heart probed by Kir2.1 overexpression and dominant-negative suppression. J Clin Invest 111:1529-1536
46. Wolf CM, Berul CI (2006) Inherited conduction system abnormalities: one group of diseases, many genes. J Cardiovasc Electrophysiol 17:446-455
47. Bucchi A, Barbuti A, Difrancesco D, Baruscotti M (2012) Funny current and cardiac rhythm: insights from HCN knockout and transgenic mouse models. Front Physiol 3:240
48. Herrmann S, Hofmann F, Stieber J, Ludwig A (2012) HCN channels in the heart: lessons from mouse mutants. Br J Pharmacol 166:501-509
49. Baruscotti M, Bucchi A, Viscomi C, Mandelli G, Consalez G, Gnecchi-Rusconi T, Montano N, Casali KR, Micheloni S, Barbuti A, DiFrancesco D (2011) Deep bradycardia and heart block caused by inducible cardiac-specific knockout of the pacemaker channel gene Hcn4. Proc Natl Acad Sci USA 108:1705-1710
50. Singh R, Hoogaars WM, Barnett P, Grieskamp T, Rana MS, Buermans H, Farin HF, Petry M, Heallen T, Martin JF, Moorman AF, 't Hoen PA, Kisper A, Christoffels VM (2012) Tbx2 and Tbx3 induce atrioventricular myocardial development and endocardial cushion formation. Cell Mol Life Sci 69:1377-1389
51. Aanhaanen WT, Brons JF, Dominguez JN, Rana MS, Norden J, Airik R, Wakker V, de Gier-de Vries C, Brown NA, Kispert A, Moorman AF, Christoffels VM (2009) The Tbx2+ primary myocardium of the atrioventricular canal forms the atrioventricular node and the base of the left ventricle. Circ Res 104:1267-1274
52. 2+ channels in neonatal rat heart. J Mol Cell Cardiol 42:1045-1053
53. 2+ exchanger gene. J Biol Chem 274:12819-12826
54. Yamada M, Revelli JP, Eichele G, Barron M, Schwartz RJ (2000) Expression of chick Tbx-2, Tbx-3, and Tbx-5 genes during early heart development: evidence for BMP2 induction of Tbx2. Dev Biol 228:95-105
55. Harrelson Z, Kelly RG, Goldin SN, Gibson-Brown JJ, Bollag RJ, Silver LM, Papaioannou VE (2004) Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development 131:5041-5052
56. Kreuzberg MM, Schrickel JW, Ghanem A, Kim JS, Degen J, Janssen-Bienhold U, Lewalter T, Tiemann K, Willecke K (2006) Connexin30.2 containing gap junction channels decelerate impulse propagation through the atrioventricular node. Proc Natl Acad Sci USA 103:5959-5964
57. Kreuzberg MM, Willecke K, Bukauskas FF (2006) Connexin-mediated cardiac impulse propagation: connexin 30.2 slows atrioventricular conduction in mouse heart. Trends Cardiovasc Med 16:266-272
58. Herrmann S, Layh B, Ludwig A (2011) Novel insights into the distribution of cardiac HCN channels: an expression study in the mouse heart. J Mol Cell Cardiol 51:997-1006
59. Vicente-Steijn R, Passier R, Wisse LJ, Schalij MJ, Poelmann RE, Gittenberger-de Groot AC, Jongbloed MR (2011) Funny current channel HCN4 delineates the developing cardiac conduction system in chicken heart. Heart Rhythm 8:1254-1263
60. Liu J, Dobrzynski H, Yanni J, Boyett MR, Lei M (2007) Organisation of the mouse sinoatrial node: structure and expression of HCN channels. Cardiovasc Res 73:729-738
61. Yamamoto M, Dobrzynski H, Tellez J, Niwa R, Billeter R, Honjo H, Kodama I, Boyett MR (2006) Extended atrial conduction system characterised by the expression of the HCN4 channel and connexin45. Cardiovasc Res 72:271-281
62. Boyett MR, Inada S, Yoo S, Li J, Liu J, Tellez J, Greener ID, Honjo H, Billeter R, Lei M, Zhang H, Efimov IR, Dobrzynski H (2006) Connexins in the sinoatrial and atrioventricular nodes. Adv Cardiol 42:175-197
63. Moorman AF, Christoffels VM (2003) Cardiac chamber formation: development, genes, and evolution. Physiol Rev 83:1223-1267