Creation of a biological pacemaker by gene- or cell-based approaches

Medical and Biological Engineering and Computing

Volumn 45, Issue 2, 2007, Pages 133-144

  Marbán, Eduardo ^a   Cho, Hee Cheol ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PACEMAKER; CARDIAC RHYTHM;

BIOMATERIALS; CARDIOLOGY; CELLS; GENES;

PACEMAKERS;

2,3 BUTANEDIONE; 4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; ANTIARRHYTHMIC AGENT; BARIUM; BETA GALACTOSIDASE; CALCEIN; CALCIUM; CALCIUM CHANNEL L TYPE; CONNEXIN 43; GAP JUNCTION PROTEIN; HEPTANOL; INWARDLY RECTIFYING POTASSIUM CHANNEL; ISOPRENALINE; MACROGOL; MACROGOL 1500; MYOSIN HEAVY CHAIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL HCN; POTASSIUM CHANNEL KIR2.1; POTASSIUM CHANNEL KV1.4; SHAKER POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ACTION POTENTIAL; BETA ADRENERGIC STIMULATION; CELL BASED GENE THERAPY; CELL FUSION; CRYOABLATION; ELECTROCARDIOGRAPHY; EMBRYONIC STEM CELL; GENE REPRESSION; GENETIC TRANSDUCTION; HEART ARRHYTHMIA; HEART MUSCLE; HEART PACING; HEART VENTRICLE TACHYCARDIA; HETEROKARYON; HUMAN; NONHUMAN; PACEMAKER; POTASSIUM CURRENT; QT PROLONGATION; REVIEW; SINUS NODE; STEM CELL TRANSPLANTATION;

ARRHYTHMIA; GENE THERAPY; HUMANS; ION CHANNELS; MESENCHYMAL STEM CELL TRANSPLANTATION; MYOCYTES, CARDIAC; SINOATRIAL NODE;

EID: 33847143196     PISSN: 01400118     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11517-007-0165-2     Document Type: Review

References (81)

1. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM et al (2003) Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425(6961):968-973
2. Anversa P, Kajstura J, Leri A, Bolli R (2006) Life, death of cardiac stem cells: A paradigm shift in cardiac biology. Circulation 113(11):1451-1453
3. Azene EM, Xue T, Marban E, Tomaselli GF, Li RA (2005) Non-equilibrium behavior of HCN channels: Insights into the role of HCN channels in native and engineered pacemakers. Cardiovasc Res 67(2):263-273
4. Barr L, Dewey MM, Berger W (1965) Propagation of action potentials and the structure of the nexus in cardiac muscle. J Gen Physiol 48:797-823
5. Beltrami AP, Barlucchi L, Torella D et al (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114(6):763-776
6. Bernstein AD, Parsonnet V (2001) Survey of cardiac pacing and implanted defibrillator practice patterns in the United States in 1997. Pacing Clin Electrophysiol 24(5):842-855
7. Blaese RM, Culver KW, Miller AD et al (1995) T lymphocyte-directed gene therapy for ADA- SCID: Initial trial results after 4 years. Science 270(5235):475-480
8. Brewster AL, Bernard JA, Gall CM, Baram TZ (2005) Formation of heteromeric hyperpolarization-activated cyclic nucleotide-gated (HCN) channels in the hippocampus is regulated by developmental seizures. Neurobiol Dis 19(1-2):200-207
9. Brooks CM, Lu H-h (1972) The sinoatrial pacemaker of the heart. Charles C. Thomas, Springfield
10. Brown HF, McNaughton PA, Noble D, Noble SJ (1975) Adrenergic control of cardian pacemaker currents. Philos Trans R Soc Lond B Biol Sci 270(908):527-537
11. Brown HF, Kimura J, Noble D, Noble SJ, Taupignon A (1984) The ionic currents underlying pacemaker activity in rabbit sino-atrial node: experimental results and computer simulations. Proc R Soc Lond B Biol Sci 222(1228):329-347
12. Campbell DL, Giles WR, Shibata EF (1988) Ion transfer characteristics of the calcium current in bull-frog atrial myocytes. J Physiol 403:239-266
13. Cerbai E, Pino R, Porciatti F et al (1997) Characterization of the hyperpolarization-activated current, I(f), in ventricular myocytes from human failing heart. Circulation 95(3):568-571
14. Cho HC, Kashiwakura Y, Marban E (2005) Creation of a biological pacemaker by cell fusion. Circulation 112(17):II-307
15. Cho HC, Kashiwakura Y, Marban E (2005) Conversion of non-excitable cells to self-contained biological pacemakers. Circulation 112(17):II-307
16. Cho HC, Smith R, Abraham M, Messina E, Giacomello A, Marban E (2005) Electrophysiology of human and porcine adult cardiac stem cells isolated from endomyocardial biopsies. Heart Rhythm 2(5):S45
17. Coplen SE, Antman EM, Berlin JA, Hewitt P, Chalmers TC (1990) Efficacy and safety of quinidine therapy for maintenance of sinus rhythm after cardioversion. A meta-analysis of randomized control trials. Circulation 82(4):1106-1116
18. DiFrancesco D (1995) The pacemaker current (I(f)) plays an important role in regulating SA node pacemaker activity. Cardiovasc Res 30(2):307-308
19. Echt DS, Liebson PR, Mitchell LB et al (1991) Mortality and morbidity in patients receiving encainide, flecainide, or placebo. The cardiac arrhythmia suppression trial. N Engl J Med 324(12):781-788
20. Falk RH (2001) Atrial fibrillation. N Engl J Med 344(14):1067-1078
21. Gerecht-Nir S, Itskovitz-Eldor J (2004) Cell therapy using human embryonic stem cells. Transpl Immunol 12(3-4):203-209
22. Gibson AJ, Karasinski J, Relvas J et al (1995) Dermal fibroblasts convert to a myogenic lineage in mdx mouse muscle. J Cell Sci 108(Pt 1):207-214
23. Gussoni E, Bennett RR, Muskiewicz KR et al (2002) Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation. J Clin Invest 110(6):807-814
24. He JQ, Ma Y, Lee Y, Thomson JA, Kamp TJ (2003) Human embryonic stem cells develop into multiple types of cardiac myocytes: Action potential characterization. Circ Res 93(1):32-39
25. Heginbotham L, Lu Z, Abramson T, MacKinnon R (1994) Mutations in the K+ channel signature sequence. Biophys J 66(4):1061-1067
26. Herskowitz I (1987) Functional inactivation of genes by dominant negative mutations. Nature 329(6136):219-222
27. Hirano Y, Hiraoka M (1988) Barium-induced automatic activity in isolated ventricular myocytes from guinea-pig hearts. J Physiol 395:455-472
28. Hoffman LM, Carpenter MK (2005) Characterization and culture of human embryonic stem cells. Nat Biotechnol 23(6):699-708
29. Hoppe UC, Jansen E, Sudkamp M, Beuckelmann DJ (1998) Hyperpolarization-activated inward current in ventricular myocytes from normal, failing human hearts. Circulation 97(1):55-65
30. Hoppe UC, Johns DC, Marban E, O'Rourke B (1999) Manipulation of cellular excitability by cell fusion: Effects of rapid introduction of transient outward K+ current on the guinea pig action potential. Circ Res 84(8):964-972
31. Imoto Y, Ehara T, Matsuura H (1987) Voltage- and time-dependent block of iK1 underlying Ba2+-induced ventricular automaticity. Am J Physiol 252(2 Pt 2):H325-H333
32. Irisawa H, Brown HF, Giles W (1993) Cardiac pacemaking in the sinoatrial node. Physiol Rev 73(1):197-227
33. Jalife J, Sicouri S, Delmar M, Michaels DC (1989) Electrical uncoupling and impulse propagation in isolated sheep Purkinje fibers. Am J Physiol 257(1 Pt 2):H179-H189
34. Kashiwakura Y, Cho HC, Azene E, Marban E (2005) Creation of a synthetic pacemaker channel. Circulation 114(16):1682-1686
35. Kehat I, Kenyagin-Karsenti D, Snir M et al (2001) Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108(3):407-414
36. Kehat I, Khimovich L, Caspi O et al (2004) Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 22(10):1282-1289
37. Kohl P (2003) Heterogeneous cell coupling in the heart: An electrophysiological role for fibroblasts. Circ Res 93(5):381-383
38. Kubo Y, Baldwin TJ, Jan YN, Jan LY (1993) Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature 362(6416):127-133
39. Kusumoto FM, Goldschlager N (1996) Cardiac pacing. N Engl J Med 334(2):89-97
40. 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(3):e45-e50
41. Lentz BR, Lee JK (1999) Poly(ethylene glycol) (PEG)-mediated fusion between pure lipid bilayers: A mechanism in common with viral fusion and secretory vesicle release? Mol Membr Biol 16(4):279-296
42. Loewenstein WR (1981) Junctional intercellular communication: The cell-to-cell membrane channel. Physiol Rev 61(4):829-913
43. Losordo DW, Vale PR, Symes JF et al (1998) Gene therapy for myocardial angiogenesis: Initial clinical results with direct myocardial injection of phVEGF165 as sole therapy for myocardial ischemia. Circulation 98(25):2800-2804
44. Mann MJ, Whittemore AD, Donaldson MC et al (1999) Ex-vivo gene therapy of human vascular bypass grafts with E2F decoy: The PREVENT single-centre, randomised, controlled trial. Lancet 354(9189):1493-1498
45. Martin CM, Meeson AP, Robertson SM et al (2004) Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 265(1):262-275
46. Matsuura K, Nagai T, Nishigaki N et al (2004) Adult cardiac Sca-1-positive cells differentiate into beating cardiomyocytes. J Biol Chem 279(12):11384-11391
47. Messina E, De Angelis L, Frati G et al (2004) Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 95(9):911-921
48. Miake J, Marban E, Nuss HB (2002) Biological pacemaker created by gene transfer. Nature 419(6903):132-133
49. Miller AG, Aldrich RW (1996) Conversion of a delayed rectifier K+ channel to a voltage-gated inward rectifier K+ channel by three amino acid substitutions. Neuron 16(4):853-858
50. Mummery C, Ward-van Oostwaard D, Doevendans P et al (2003) Differentiation of human embryonic stem cells to cardiomyocytes: Role of coculture with visceral endoderm-like cells. Circulation 107(21):2733-2740
51. Nuss HB, Johns DC, Kaab S et al (1996) Reversal of potassium channel deficiency in cells from failing hearts by adenoviral gene transfer: A prototype for gene therapy for disorders of cardiac excitability and contractility. Gene Ther 3(10):900-912
52. Nuss HB, Marban E, Johns DC (1999) Overexpression of a human potassium channel suppresses cardiac hyperexcitability in rabbit ventricular myocytes. J Clin Invest 103(6):889-896
53. Odorico JS, Kaufman DS, Thomson JA (2001) Multilineage differentiation from human embryonic stem cell lines. Stem Cells 19(3):193-204
54. Oh H, Bradfute SB, Gallardo TD et al (2003) Cardiac progenitor cells from adult myocardium: Homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100(21):12313-12318
55. Ohno T, Gordon D, San H et al (1994) Gene therapy for vascular smooth muscle cell proliferation after arterial injury. Science 265(5173):781-784
56. Pfister O, Mouquet F, Jain M et al (2005) CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97(1):52-61
57. Potapova I, Plotnikov A, Lu Z et al (2004) Human mesenchymal stem cells as a gene delivery system to create cardiac pacemakers. Circ Res 94(7):952-959
58. Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294(5550):2372-2375
59. Richardson AW, Josephson ME (1999) Ablation of ventricular tachycardia in the setting of coronary artery disease. Curr Cardiol Rep 1(2):157-164
60. Robertson JA (2001) Human embryonic stem cell research: Ethical and legal issues. Nat Rev Genet 2(1):74-78
61. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: From molecules to physiological function. Annu Rev Physiol 65:453-480
62. Rodriguez-Contreras A, Nonner W, Yamoah EN (2002) Ca2+ transport properties and determinants of anomalous mole fraction effects of single voltage-gated Ca2+ channels in hair cells from bullfrog saccule. J Physiol 538(Pt 3):729-745
63. Rosengart TK, Lee LY, Patel SR et al (1999) Six-month assessment of a phase I trial of angiogenic gene therapy for the treatment of coronary artery disease using direct intramyocardial administration of an adenovirus vector expressing the VEGF121 cDNA. Ann Surg 230(4):466-470; discussion 70-72
64. Santoro B, Tibbs GR (1999) The HCN gene family: Molecular basis of the hyperpolarization-activated pacemaker channels. Ann N Y Acad Sci 868:741-764
65. Shirahata S, Katakura Y, Teruya K (1998) Cell hybridization, hybridomas, and human hybridomas. Methods Cell Biol 57:111-145
66. Siebels J, Cappato R, Ruppel R, Schneider MA, Kuck KH (1993) Preliminary results of the Cardiac Arrest Study Hamburg (CASH). CASH Investigators. Am J Cardiol 72(16):109F-113F
67. Slesinger PA, Patil N, Liao YJ, Jan YN, Jan LY, Cox DR (1996) Functional effects of the mouse weaver mutation on G protein-gated inwardly rectifying K+ channels. Neuron 16(2):321-331
68. Smith R, Messina E, Abraham M, Cho HC, Giacomello A, Marban E (2005) Electrophysiology of human and porcine adult cardiac stem cells isolated from endomyocardial biopsies. Circulation 111(13):1720
69. Smith R, Barile L, Cho HC et al (2005) Unique phenotype of cardiospheres derived from human endomyocardial biopsies. Circulation 112(17):II-51
70. Sperelakis N (2002) An electric field mechanism for transmission of excitation between myocardial cells. Circ Res 91(11):985-987
71. Thom T, Haase N, Rosamond W et al (2006) Heart disease and stroke statistics-2006 update: A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 113(6):e85-e151
72. Ulens C, Tytgat J (2001) Functional heteromerization of HCN1 and HCN2 pacemaker channels. J Biol Chem 276(9):6069-6072
73. van der Velden HM, Jongsma HJ (2002) Cardiac gap junctions and connexins: Their role in atrial fibrillation and potential as therapeutic targets. Cardiovasc Res 54(2):270-279
74. Waldo AL, Camm AJ, deRuyter H et al (1996) Effect of d -sotalol on mortality in patients with left ventricular dysfunction after recent and remote myocardial infarction. The SWORD investigators. Survival with oral d -sotalol. Lancet 348(9019):7-12
75. Wang Z, Feng J, Shi H, Pond A, Nerbonne JM, Nattel S (1999) Potential molecular basis of different physiological properties of the transient outward K+ current in rabbit and human atrial myocytes. Circ Res 84(5):551-561
76. Weimann JM, Johansson CB, Trejo A, Blau HM (2003) Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant. Nat Cell Biol 5(11):959-966
77. Wier WG, Blatter LA (1991) Ca(2+)-oscillations and Ca(2+)-waves in mammalian cardiac and vascular smooth muscle cells. Cell Calcium 12(2-3):241-254
78. Wobus AM, Rohwedel J, Maltsev V, Hescheler J (1995) Development of cardiomyocytes expressing cardiac-specific genes, action potentials, and ionic channels during embryonic stem cell-derived cardiogenesis. Ann N Y Acad Sci 752:460-469
79. Xu C, Police S, Rao N, Carpenter MK (2002) Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res 91(6):501-508
80. Xue T, Marban E, Li RA (2002) Dominant-negative suppression of HCN1- and HCN2-encoded pacemaker currents by an engineered HCN1 construct: insights into structure-function relationships and multimerization. Circ Res 90(12):1267-1273
81. Xue T, Cho HC, Akar FG et al (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(1):11-20