Mechanism of automaticity in cardiomyocytes derived from human induced pluripotent stem cells

Journal of Molecular and Cellular Cardiology

Volumn 81, Issue , 2015, Pages 81-93

  Kim, Jong J ^a,b   Yang, Lei ^b   Lin, Bo ^b   Zhu, Xiaodong ^c   Sun, Bin ^b   Kaplan, Aaron D ^d   Bett, Glenna C L ^d   Rasmusson, Randall L ^d   London, Barry ^c   Salama, Guy ^a,b  

^a PA 15260   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cell cell coupling; Funny current; Human myocytes from stem cells; Optical mapping of calcium and action potentials; Spontaneous activity; Subcellular calcium waves

Indexed keywords

CAFFEINE; CALCIUM ION; ISOPRENALINE; IVABRADINE; POTASSIUM ION; RYANODINE RECEPTOR; TETRACAINE; 2 [4 (2,5 DIFLUOROBENZYLOXY)PHENOXY] 5 ETHOXYANILINE; ANILINE DERIVATIVE; BENZAZEPINE DERIVATIVE; CALCIUM; CARDIOVASCULAR AGENT; CONNEXIN 43; DIPHENYL ETHER DERIVATIVE; GJA1 PROTEIN, HUMAN; SODIUM CALCIUM EXCHANGE PROTEIN;

ACTION POTENTIAL; ARTICLE; CALCIUM CELL LEVEL; CELL DIFFERENTIATION; CELL MEMBRANE DEPOLARIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HEART AUTOMATICITY; HEART CONTRACTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MONOLAYER CULTURE; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; SARCOPLASMIC RETICULUM; SODIUM CALCIUM EXCHANGE; VOLTAGE CLAMP TECHNIQUE; ANIMAL; ANTAGONISTS AND INHIBITORS; CARDIAC MUSCLE CELL; CELL LINE; CYTOLOGY; DEPENDOPARVOVIRUS; DRUG EFFECTS; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MICROTUBULE; NUCLEAR REPROGRAMMING; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ACTION POTENTIALS; ANILINE COMPOUNDS; ANIMALS; BENZAZEPINES; CAFFEINE; CALCIUM; CARDIOVASCULAR AGENTS; CELL DIFFERENTIATION; CELL LINE; CELLULAR REPROGRAMMING; CONNEXIN 43; DEPENDOVIRUS; GENETIC VECTORS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; ISOPROTERENOL; MICROTUBULES; MYOCYTES, CARDIAC; PATCH-CLAMP TECHNIQUES; PHENYL ETHERS; SARCOPLASMIC RETICULUM; SODIUM-CALCIUM EXCHANGER; TETRACAINE; TRANSFECTION;

EID: 84922559369     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.01.013     Document Type: Article

References (61)

1. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
2. Reubinoff B.E., Pera M.F., Fong C.Y., Trounson A., Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol 2000, 18:399-404.
3. Kehat I., Kenyagin-Karsenti D., Snir M., Segev H., Amit M., Gepstein A., et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 2001, 108:407-414.
4. Itskovitz-Eldor J., Schuldiner M., Karsenti D., Eden A., Yanuka O., Amit M., et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 2000, 6:88-95.
5. Dolnikov K., Shilkrut M., Zeevi-Levin N., Gerecht-Nir S., Amit M., Danon A., et al. Functional properties of human embryonic stem cell-derived cardiomyocytes: intracellular Ca2+ handling and the role of sarcoplasmic reticulum in the contraction. Stem Cells 2006, 24:236-245.
6. Satin J., Kehat I., Caspi O., Huber I., Arbel G., Itzhaki I., et al. Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. J Physiol 2004, 559:479-496.
7. Lieu D.K., Fu J.D., Chiamvimonvat N., Tung K.C., McNerney G.P., Huser T., et al. Mechanism-based facilitated maturation of human pluripotent stem cell-derived cardiomyocytes. Circ Arrhythm Electrophysiol 2013, 6:191-201.
8. He J.Q., Ma Y., Lee Y., Thomson J.A., Kamp T.J. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res 2003, 93:32-39.
9. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., et al. BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat Med 2008, 14:1363-1369.
10. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
11. Gai H., Leung E.L., Costantino P.D., Aguila J.R., Nguyen D.M., Fink L.M., et al. Generation and characterization of functional cardiomyocytes using induced pluripotent stem cells derived from human fibroblasts. Cell Biol Int 2009, 33:1184-1193.
12. Yokoo N., Baba S., Kaichi S., Niwa A., Mima T., Doi H., et al. The effects of cardioactive drugs on cardiomyocytes derived from human induced pluripotent stem cells. Biochem Biophys Res Commun 2009, 387:482-488.
13. Zwi L., Caspi O., Arbel G., Huber I., Gepstein A., Park I.H., et al. Cardiomyocyte differentiation of human induced pluripotent stem cells. Circulation 2009, 120:1513-1523.
14. Zhang J., Wilson G.F., Soerens A.G., Koonce C.H., Yu J., Palecek S.P., et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res 2009, 104:e30-e41.
15. Carvajal-Vergara X., Sevilla A., D'Souza S.L., Ang Y.S., Schaniel C., Lee D.F., et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010, 465:808-812.
16. Itzhaki I., Maizels L., Huber I., Zwi-Dantsis L., Caspi O., Winterstern A., et al. Modelling the long QT syndrome with induced pluripotent stem cells. Nature 2011, 471:225-229.
17. Matsa E., Rajamohan D., Dick E., Young L., Mellor I., Staniforth A., et al. Drug evaluation in cardiomyocytes derived from human induced pluripotent stem cells carrying a long QT syndrome type 2 mutation. Eur Heart J 2011, 32:952-962.
18. Priori S.G. Induced pluripotent stem cell-derived cardiomyocytes and long QT syndrome: is personalized medicine ready for prime time?. Circ Res 2011, 109:822-824.
19. Binah O., Dolnikov K., Sadan O., Shilkrut M., Zeevi-Levin N., Amit M., et al. Functional and developmental properties of human embryonic stem cells-derived cardiomyocytes. J Electrocardiol 2007, 40:S192-S196.
20. Liu J., Fu J.D., Siu C.W., Li R.A. Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation. Stem Cells 2007, 25:3038-3044.
21. Li S., Cheng H., Tomaselli G.F., Li R.A. Mechanistic basis of excitation-contraction coupling in human pluripotent stem cell-derived ventricular cardiomyocytes revealed by Ca2+ spark characteristics: direct evidence of functional Ca2+-induced Ca2+ release. Heart Rhythm 2014, 11:133-140.
22. Weisbrod D., Peretz A., Ziskind A., Menaker N., Oz S., Barad L., et al. SK4 Ca2+ activated K+ channel is a critical player in cardiac pacemaker derived from human embryonic stem cells. Proc Natl Acad Sci U S A 2013, 110:E1685-E1694.
23. Liebau S., Tischendorf M., Ansorge D., Linta L., Stockmann M., Weidgang C., et al. An inducible expression system of the calcium-activated potassium channel 4 to study the differential impact on embryonic stem cells. Stem Cells Int 2011, 2011:456815.
24. Lee Y.K., Ng K.M., Lai W.H., Chan Y.C., Lau Y.M., Lian Q., et al. Calcium homeostasis in human induced pluripotent stem cell-derived cardiomyocytes. Stem Cell Rev 2011, 7:976-986.
25. Zhang X.H., Haviland S., Wei H., Saric T., Fatima A., Hescheler J., et al. Ca2+ signaling in human induced pluripotent stem cell-derived cardiomyocytes (iPS-CM) from normal and catecholaminergic polymorphic ventricular tachycardia (CPVT)-afflicted subjects. Cell Calcium 2013, 54:57-70.
26. Fatima A., Xu G., Shao K., Papadopoulos S., Lehmann M., Arnaiz-Cot J.J., et al. In vitro modeling of ryanodine receptor 2 dysfunction using human induced pluripotent stem cells. Cell Physiol Biochem 2011, 28:579-592.
27. Del Nido P.J., Glynn P., Buenaventura P., Salama G., Koretsky A.P. Fluorescence measurement of calcium transients in perfused rabbit heart using rhod 2. Am J Physiol 1998, 274:H728-H741.
28. Tallini Y.N., Ohkura M., Choi B.R., Ji G., Imoto K., Doran R., et al. Imaging cellular signals in the heart in vivo: cardiac expression of the high-signal Ca2+ indicator GCaMP2. Proc Natl Acad Sci U S A 2006, 103:4753-4758.
29. Lin B., Kim J., Li Y., Pan H., Carvajal-Vergara X., Salama G., et al. High-purity enrichment of functional cardiovascular cells from human iPS cells. Cardiovasc Res 2012, 95:327-335.
30. Yang L., Soonpaa M.H., Adler E.D., Roepke T.K., Kattman S.J., Kennedy M., et al. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 2008, 453:524-528.
31. Han L., Li Y., Tchao J., Kaplan A.D., Lin B., Li Y., et al. Study familial hypertrophic cardiomyopathy using patient-specific induced pluripotent stem cells. Cardiovasc Res 2014, 104:258-269.
32. Choi B.R., Salama G. Simultaneous maps of optical action potentials and calcium transients in guinea-pig hearts: mechanisms underlying concordant alternans. J Physiol 2000, 529(Pt 1):171-188.
33. Tallini Y.N., Brekke J.F., Shui B., Doran R., Hwang S.M., Nakai J., et al. Propagated endothelial Ca2+ waves and arteriolar dilation in vivo: measurements in Cx40BAC GCaMP2 transgenic mice. Circ Res 2007, 101:1300-1309.
34. Salama G., Choi B.R., Azour G., Lavasani M., Tumbev V., Salzberg B.M., et al. Properties of new, long-wavelength, voltage-sensitive dyes in the heart. J Membr Biol 2005, 208:125-140.
35. Salama G., Hwang S.M. Simultaneous optical mapping of intracellular free calcium and action potentials from Langendorff perfused hearts. Curr Protoc Cytom 2009, 49:12.17.1-12.17.32. [Chapter 12:Unit 12 7].
36. Bett G.C., Kaplan A.D., Lis A., Cimato T.R., Tzanakakis E.S., Zhou Q., et al. Electronic "expression" of the inward rectifier in cardiocytes derived from human-induced pluripotent stem cells. Heart Rhythm 2013, 10:1903-1910.
37. Kaplan A.D., Lis A., Cimato T.R., Tzanakakis E.S., Zhou Q., Morales M.J., et al. Enhanced differentiation of stem cell derived cardiac myocytes by electronic expression of IK1 reveals an atrial-specific Kv1.5-like current. Biophys J 2014, 108(2):631a. (supplement 1).
38. Ludwig A., Zong X., Stieber J., Hullin R., Hofmann F., Biel M. Two pacemaker channels from human heart with profoundly different activation kinetics. EMBO J 1999, 18:2323-2329.
39. Peters C.J., Chow S.S., Angoli D., Nazzari H., Cayabyab F.S., Morshedian A., et al. In situ co-distribution and functional interactions of SAP97 with sinoatrial isoforms of HCN channels. J Mol Cell Cardiol 2009, 46:636-643.
40. Difrancesco D., Noble D. The funny current has a major pacemaking role in the sinus node. Heart Rhythm 2012, 9:299-301.
41. DiFrancesco D., Ferroni A., Mazzanti M., Tromba C. Properties of the hyperpolarizing-activated current (if) in cells isolated from the rabbit sino-atrial node. J Physiol 1986, 377:61-88.
42. Frace A.M., Maruoka F., Noma A. External K+ increases Na+ conductance of the hyperpolarization-activated current in rabbit cardiac pacemaker cells. Pflugers Arch 1992, 421:97-99.
43. Hoppe U.C., Beuckelmann D.J. Characterization of the hyperpolarization-activated inward current in isolated human atrial myocytes. Cardiovasc Res 1998, 38:788-801.
44. O'Hara T., Rudy Y. Quantitative comparison of cardiac ventricular myocyte electrophysiology and response to drugs in human and nonhuman species. Am J Physiol Heart Circ Physiol 2012, 302:H1023-H1030.
45. Lakatta E.G., Maltsev V.A., Vinogradova T.M. A coupled SYSTEM of intracellular Ca2+ clocks and surface membrane voltage clocks controls the timekeeping mechanism of the heart's pacemaker. Circ Res 2010, 106:659-673.
46. Abramson J.J., Salama G. Sulfhydryl oxidation and Ca2+ release from sarcoplasmic reticulum. Mol Cell Biochem 1988, 82:81-84.
47. Zaidi N.F., Lagenaur C.F., Abramson J.J., Pessah I., Salama G. Reactive disulfides trigger Ca2+ release from sarcoplasmic reticulum via an oxidation reaction. J Biol Chem 1989, 264:21725-21736.
48. Menshikova E.V., Salama G. Cardiac ischemia oxidizes regulatory thiols on ryanodine receptors: captopril acts as a reducing agent to improve Ca2+ uptake by ischemic sarcoplasmic reticulum. J Cardiovasc Pharmacol 2000, 36:656-668.
49. Rottbauer W., Baker K., Wo Z.G., Mohideen M.A., Cantiello H.F., Fishman M.C. Growth and function of the embryonic heart depend upon the cardiac-specific L-type calcium channel alpha1 subunit. Dev Cell 2001, 1:265-275.
50. Nunes S.S., Miklas J.W., Liu J., Aschar-Sobbi R., Xiao Y., Zhang B., et al. Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods 2013, 10:781-787.
51. Maltsev V.A., Lakatta E.G. The funny current in the context of the coupled-clock pacemaker cell system. Heart Rhythm 2012, 9:302-307.
52. Rosen M.R., Nargeot J., Salama G. Point-counterpoint: the case for the funny current and the calcium clock. Heart Rhythm 2011, 9(4):616-618.
53. Cerbai E., Sartiani L., DePaoli P., Pino R., Maccherini M., Bizzarri F., et al. The properties of the pacemaker current I(F)in human ventricular myocytes are modulated by cardiac disease. J Mol Cell Cardiol 2001, 33:441-448.
54. Cerbai E., Mugelli A. I(f) in non-pacemaker cells: role and pharmacological implications. Pharmacol Res 2006, 53:416-423.
55. Qu J., Altomare C., Bucchi A., DiFrancesco D., Robinson R.B. Functional comparison of HCN isoforms expressed in ventricular and HEK 293 cells. Pflugers Arch 2002, 444:597-601.
56. Cerbai E., Pino R., Porciatti F., Sani G., Toscano M., Maccherini M., et al. Characterization of the hyperpolarization-activated current, I(f), in ventricular myocytes from human failing heart. Circulation 1997, 95:568-571.
57. Bucchi A., Baruscotti M., DiFrancesco D. Current-dependent block of rabbit sino-atrial node I(f) channels by ivabradine. J Gen Physiol 2002, 120:1-13.
58. Loughrey C.M., Otani N., Seidler T., Craig M.A., Matsuda R., Kaneko N., et al. K201 modulates excitation-contraction coupling and spontaneous Ca2+ release in normal adult rabbit ventricular cardiomyocytes. Cardiovasc Res 2007, 76:236-246.
59. Takimoto E., Kass D.A. Role of oxidative stress in cardiac hypertrophy and remodeling. Hypertension 2007, 49:241-248.
60. Kohler A.C., Sag C.M., Maier L.S. Reactive oxygen species and excitation-contraction coupling in the context of cardiac pathology. J Mol Cell Cardiol 2014, 73C:92-102.
61. Ai X., Curran J.W., Shannon T.R., Bers D.M., Pogwizd S.M. Ca2+/calmodulin-dependent protein kinase modulates cardiac ryanodine receptor phosphorylation and sarcoplasmic reticulum Ca2+ leak in heart failure. Circ Res 2005, 97:1314-1322.