Coordinating electrical activity of the heart: Ankyrin polypeptides in human cardiac disease

Expert Opinion on Therapeutic Targets

Volumn 15, Issue 7, 2011, Pages 789-801

  Curran, Jerry ^a   Mohler, Peter J ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

ankyrin polypeptides; ankyrin B syndrome; cardiac; excitation contraction coupling

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM); ANKYRIN; ANKYRIN B; ANKYRIN G; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; PHOSPHOPROTEIN PHOSPHATASE 2; POLYPEPTIDE; SODIUM CHANNEL NAV1.5; SPECTRIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BRUGADA SYNDROME; CARDIOMYOPATHY; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENE STRUCTURE; HEART CONTRACTION; HEART DISEASE; HEART EXCITATION; HEART INFARCTION; HUMAN; LONG QT SYNDROME; NONHUMAN; PACEMAKER; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SINUS NODE DISEASE;

ANKYRINS; HEART; HEART DISEASES; HUMANS;

EID: 79958263630     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2011.575363     Document Type: Review

References (93)

1. Bardou AL, Auger PM, Birkui PJ, et al. Modeling of cardiac electrophysiological mechanisms: from action potential genesis to its propagation in myocardium. Crit Rev Biomed Eng 1996;24:141-221 (Pubitemid 27175076)
2. Luo CH, Rudy Y. A dynamic model of the cardiac ventricular action potential. I. Simulations of ionic currents and concentration changes. Circ Res 1994;74:1071-96 (Pubitemid 24176903)
3. Bassani JW, Bassani RA, Bers DM. Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J.Physiol 1994;476:279-93 (Pubitemid 24129810)
4. Bers DM. Cardiac excitation-contraction coupling. Nature 2002;415:198-205 (Pubitemid 34059525)
5. Glukhov AV, Fedorov VV, Anderson ME, et al. Functional anatomy of the murine sinus node: high-resolution optical mapping of ankyrin-B heterozygous mice. Am J Physiol Heart Circ Physiol 2010;299:H482-91
6. Hund TJ, Mohler PJ. Ankyrin-based targeting pathway regulates human sinoatrial node automaticity. Channels (Austin) 2008;2:404-6
7. Hund TJ, Koval OM, Li J, et al. A betaIV-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest 2010;120:3508-19
8. Kline CF, Hund TJ, Mohler PJ. Ankyrin regulates KATP channel membrane trafficking and gating in excitable cells. Channels (Austin) 2010;4:55-7
9. Koval OM, Guan X, Wu Y, et al. CaV1.2 beta-subunit coordinates CaMKII-triggered cardiomyocyte death and afterdepolarizations. Proc Natl Acad Sci USA 2010;107:4996-5000
10. Li J, Kline CF, Hund TJ, et al. Ankyrin-B regulates Kir6.2 membrane expression and function in heart. J Biol Chem 2010;285:28723-30
11. Pogwizd SM, Qi M, Yuan W, et al. Upregulation of Na+/Ca2+ exchanger expression and function in an arrhythmogenic rabbit model of heart failure. Circ Res 1999;85:1009-19
12. Pogwizd SM, Bers DM. Na/Ca exchange in heart failure: contractile dysfunction and arrhythmogenesis. Ann NY Acad Sci 2002;976:454-65 (Pubitemid 36126930)
13. Schlotthauer K, Bers DM. Sarcoplasmic reticulum Ca2+ release causes myocyte depolarization. Underlying mechanism and threshold for triggered action potentials. Circ Res 2000;87:774-80
14. Szlufcik K, Missiaen L, Parys JB, et al. Uncoupled IP3 receptor can function as a Ca2+-leak channel: cell biological and pathological consequences. Biol Cell 2006;98:1-14 (Pubitemid 43056289)
15. Wehrens XH, Marks AR. Sudden unexplained death caused by cardiac ryanodine receptor (RyR2) mutations. Mayo Clin Proc 2004;79:1367-71 (Pubitemid 39453299)
16. Lowe JS, Palygin O, Bhasin N, et al. Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway. J Cell Biol 2008;180:173-86
17. Ringer S. A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J Physiol 1883;4:29-42
18. Hodgkin AL, Huxley AF. Movement of sodium and potassium ions during nervous activity. Cold Spring Harb Symp Quant Biol 1952;17:43-52
19. Neher E, Sakmann B, Steinbach JH. The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes. Pflugers Arch 1978;375:219-28 (Pubitemid 8383955)
20. Rios E, Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 1987;325:717-20 (Pubitemid 17054040)
21. McConnachie G, Langeberg LK, Scott JD. AKAP signaling complexes: getting to the heart of the matter. Trends Mol Med 2006;12:317-23 (Pubitemid 44110003)
22. Verdonck F, Mubagwa K, Sipido KR. [Na+] in the subsarcolemmal 'fuzzy' space and modulation of [Ca2+]i and contraction in cardiac myocytes. Cell Calcium 2004;35:603-12 (Pubitemid 38618572)
23. Petrecca K, Atanasiu R, Grinstein S, et al. Subcellular localization of the Na+/H+ exchanger NHE1 in rat myocardium. Am J Physiol 1999;276:H709-17 (Pubitemid 29100641)
24. Gao T, Yatani A, Dell'Acqua ML, et al. cAMP-dependent regulation of cardiac L-type Ca2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 1997;19:185-96 (Pubitemid 27333004)
25. Wibo M, Bravo G, Godfraind T. Postnatal maturation of excitation-contraction coupling in rat ventricle in relation to the subcellular localization and surface density of 1,4-dihydropyridine and ryanodine receptors. Circ Res 1991;68:662-73
26. Mohler PJ, Davis JQ, Bennett V. Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol 2005;3:e423
27. Bennett V. Purification of an active proteolytic fragment of the membrane attachment site for human erythrocyte spectrin. J Biol Chem 1978;253:2292-9 (Pubitemid 8328215)
28. Bennett V, Stenbuck PJ. Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane. J Biol Chem 1980;255:6424-32
29. Bennett V, Davis J. Spectrin and ankyrin in brain. Cell Motil 1983;3:623-33
30. Ayalon G, Davis JQ, Scotland PB, et al. An ankyrin-based mechanism for functional organization of dystrophin and dystroglycan. Cell 2008;135:1189-200
31. Kizhatil K, Baker SA, Arshavsky VY, et al. Ankyrin-G promotes cyclic nucleotide-gated channel transport to rod photoreceptor sensory cilia. Science 2009;323:1614-17
32. Li ZP, Burke EP, Frank JS, et al. The cardiac Na+-Ca2+ exchanger binds to the cytoskeletal protein ankyrin. J Biol Chem 1993;268:11489-91 (Pubitemid 23168086)
33. Kizhatil K, Sandhu NK, Peachey NS, et al. Ankyrin-B is required for coordinated expression of beta-2-spectrin, the Na/K-ATPase and the Na/Ca exchanger in the inner segment of rod photoreceptors. Exp Eye Res 2009;88:57-64
34. Bennett V, Baines AJ. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 2001;81:1353-92 (Pubitemid 32606672)
35. Hashemi SM, Hund TJ, Mohler PJ. Cardiac ankyrins in health and disease. J Mol Cell Cardiol 2009;47:203-9
36. Bennett PM, Baines AJ, Lecomte MC, et al. Not just a plasma membrane protein: in cardiac muscle cells alpha-II spectrin also shows a close association with myofibrils. J Muscle Res Cell Motil 2004;25:119-26 (Pubitemid 39060886)
37. Kontrogianni-Konstantopoulos A, Jones EM, Van Rossum DB, et al. Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol Biol Cell 2003;14:1138-48 (Pubitemid 36337458)
38. Mohler PJ, Gramolini AO, Bennett V. Ankyrins. J Cell Sci 2002;115:1565-6 (Pubitemid 34520585)
39. Mohler PJ, Rivolta I, Napolitano C, et al. Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc Natl Acad Sci USA 2004;101:17533-8 (Pubitemid 39657438)
40. Bennett V, Stenbuck PJ. The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature 1979;280:468-73
41. Bennett V, Stenbuck PJ. Identification and partial purification of ankyrin, the high affinity membrane attachment site for human erythrocyte spectrin. J Biol Chem 1979;254:2533-41 (Pubitemid 9160057)
42. Cunha SR, Mohler PJ. Obscurin targets ankyrin-B and protein phosphatase 2A to the cardiac M-line. J Biol Chem 2008;283:31968-80
43. Bhasin N, Cunha SR, Mudannayake M, et al. Molecular basis for PP2A regulatory subunit B56alpha targeting in cardiomyocytes. Am J Physiol Heart Circ Physiol 2007;293:H109-19 (Pubitemid 47105065)
44. Abdi KM, Mohler PJ, Davis JQ, et al. Isoform specificity of ankyrin-B: a site in the divergent C-terminal domain is required for intramolecular association. J Biol Chem 2006;281:5741-9 (Pubitemid 43847673)
45. Mohler PJ, Gramolini AO, Bennett V. The ankyrin-B C-terminal domain determines activity of ankyrin-B/G chimeras in rescue of abnormal inositol 1,4,5-trisphosphate and ryanodine receptor distribution in ankyrin-B (-/-) neonatal cardiomyocytes. J Biol Chem 2002;277:10599-607 (Pubitemid 34968184)
46. Mohler PJ, Hoffman JA, Davis JQ, et al. Isoform specificity among ankyrins. An amphipathic alpha-helix in the divergent regulatory domain of ankyrin-B interacts with the molecular co-chaperone Hdj1/Hsp40. J Biol Chem 2004;279:25798-804 (Pubitemid 38756844)
47. Davis LH, Davis JQ, Bennett V. Ankyrin regulation: an alternatively spliced segment of the regulatory domain functions as an intramolecular modulator. J Biol Chem 1992;267:18966-72
48. Mohler PJ, Splawski I, Napolitano C, et al. A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc Natl Acad Sci USA 2004;101:9137-42 (Pubitemid 38781624)
49. Mohler PJ, Le SS, Denjoy I, et al. Defining the cellular phenotype of "ankyrin-B syndrome" variants: human ANK2 variants associated with clinical phenotypes display a spectrum of activities in cardiomyocytes. Circulation 2007;115:432-41 (Pubitemid 46184194)
50. Michaely P, Tomchick DR, Machius M, et al. Crystal structure of a 12 ANK repeat stack from human ankyrinR. EMBO J 2002;21:6387-96 (Pubitemid 35448417)
51. Schott JJ, Charpentier F, Peltier S, et al. Mapping of a gene for long QT syndrome to chromosome 4q25-27. Am J Hum Genet 1995;57:1114-22
52. Le Scouarnec S, Bhasin N, Vieyres C, et al. Dysfunction in ankyrin-B-dependent ion channel and transporter targeting causes human sinus node disease. Proc Natl Acad Sci USA 2008;105:15617-22
53. Mohler PJ, Schott JJ, Gramolini AO, et al. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 2003;421:634-9 (Pubitemid 36227671)
54. Eber SW, Gonzalez JM, Lux ML, et al. Ankyrin-1 mutations are a major cause of dominant and recessive hereditary spherocytosis. Nat Genet 1996;13:214-18 (Pubitemid 26000443)
55. Sedlacek K, Stark K, Cunha SR, et al. Common genetic variants in ANK2 modulate QT interval: results from the KORA study. Circ Cardiovasc Genet 2008;1:93-9
56. Wolf RM, Mitchell CC, Christensen MD, et al. Defining new insight into atypical arrhythmia: a computational model of ankyrin-B syndrome. Am J Physiol Heart Circ Physiol 2010;299:H1505-14
57. Philipson KD, Nicoll DA. Sodium-calcium exchange: a molecular perspective. Annu Rev Physiol 2000;62:111-33 (Pubitemid 30618258)
58. Juhaszova M, Blaustein MP. Na+ pump low and high ouabain affinity alpha subunit isoforms are differently distributed in cells. Proc Natl Acad Sci USA 1997;94:1800-5 (Pubitemid 27113916)
59. Curran J, Brown KH, Santiago DJ, et al. Spontaneous Ca waves in ventricular myocytes from failing hearts depend on Ca2 +-calmodulin-dependent protein kinase II. J Mol Cell Cardiol 2010;49:25-32
60. Lehnart SE, Mongillo M, Bellinger A, et al. Leaky Ca2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice. J Clin Invest 2008;118:2230-45 (Pubitemid 351872341)
61. Katra RP, Laurita KR. Cellular mechanism of calcium-mediated triggered activity in the heart. Circ Res 2005;96:535-42 (Pubitemid 40463462)
62. Mohler PJ, Davis JQ, Davis LH, et al. Inositol 1,4,5-trisphosphate receptor localization and stability in neonatal cardiomyocytes requires interaction with ankyrin-B. J Biol Chem 2004;279:12980-7 (Pubitemid 38445874)
63. Curran J, Hinton MJ, Rios E, et al. beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ Res 2007;100:391-8
64. Zima AV, Bovo E, Bers DM, et al. Ca2+ spark dependent and independent sarcoplasmic reticulum Ca2+ leak in normal and failing rabbit ventricular myocytes. J Physiol 2010;588:4743-57
65. Shannon TR, Ginsburg KS, Bers DM. Potentiation of fractional sarcoplasmic reticulum calcium release by total and free intra-sarcoplasmic reticulum calcium concentration. Biophys J 2000;78:334-43 (Pubitemid 30207142)
66. Mackenzie L, Roderick HL, Proven A, et al. Inositol 1,4,5-trisphosphate receptors in the heart. Biol Res 2004;37:553-7
67. Davare MA, Horne MC, Hell JW. Protein phosphatase 2A is associated with class C L-type calcium channels (Cav1.2) and antagonizes channel phosphorylation by cAMP-dependent protein kinase. J Biol Chem 2000;275:39710-17 (Pubitemid 32058999)
68. Klein G, Schroder F, Vogler D, et al. Increased open probability of single cardiac L-type calcium channels in patients with chronic atrial fibrillation role of phosphatase 2A. Cardiovasc Res 2003;59:37-45 (Pubitemid 36776371)
69. Terentyev D, Belevych AE, Terentyeva R, et al. miR-1 overexpression enhances Ca2+ release and promotes cardiac arrhythmogenesis by targeting PP2A regulatory subunit B56alpha and causing CaMKII-dependent hyperphosphorylation of RyR2. Circ Res 2009;104:514-21
70. Maltsev VA, Lakatta EG. Normal heart rhythm is initiated and regulated by an intracellular calcium clock within pacemaker cells. Heart Lung Circ 2007;16:335-48 (Pubitemid 47504909)
71. Wu Y, Gao Z, Chen B, et al. Calmodulin kinase II is required for fight or flight sinoatrial node physiology. Proc Natl Acad Sci USA 2009;106:5972-7
72. Suzuki M, Li RA, Miki T, et al. Functional roles of cardiac and vascular ATP-sensitive potassium channels clarified by Kir6.2-knockout mice. Circ Res 2001;88:570-7 (Pubitemid 32275792)
73. Kline CF, Kurata HT, Hund TJ, et al. Dual role of K ATP channel C-terminal motif in membrane targeting and metabolic regulation. Proc Natl Acad Sci USA 2009;106:16669-74
74. Healy JA, Nilsson KR, Hohmeier HE, et al. Cholinergic augmentation of insulin release requires ankyrin-B. Sci Signal 2010;3:ra19
75. Mohler PJ, Healy JA, Xue H, et al. Ankyrin-B syndrome: enhanced cardiac function balanced by risk of cardiac death and premature senescence. PLoS One 2007;2:e1051
76. Vaxillaire M, Populaire C, Busiah K, et al. Kir6.2 mutations are a common cause of permanent neonatal diabetes in a large cohort of French patients. Diabetes 2004;53:2719-22 (Pubitemid 39299285)
77. Wang Q, Shen J, Splawski I, et al. SCN5A mutations associated with an inherited cardiac arrhythmia, long QT syndrome. Cell 1995;80:805-11
78. Priori SG, Napolitano C, Gasparini M, et al. Natural history of Brugada syndrome: insights for risk stratification and management. Circulation 2002;105:1342-7 (Pubitemid 34260426)
79. Yang Y, Lacas-Gervais S, Morest DK, et al. betaIV spectrins are essential for membrane stability and the molecular organization of nodes of Ranvier. J Neurosci 2004;24:7230-40 (Pubitemid 39100693)
80. Wagner S, Dybkova N, Rasenack EC, et al. Ca2+/calmodulin-dependent protein kinase II regulates cardiac Na+ channels. J Clin Invest 2006;116:3127-38 (Pubitemid 44878627)
81. Sossalla S, Maurer U, Schotola H, et al. Diastolic dysfunction and arrhythmias caused by overexpression of CaMKIIdeltaC can be reversed by inhibition of late Na + current. Basic Res Cardiol 2011;106:263-72
82. Pinto JM, Boyden PA. Electrical remodeling in ischemia and infarction. Cardiovasc Res 1999;42:284-97 (Pubitemid 29243157)
83. Nattel S, Maguy A, Le BS, et al. Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 2007;87:425-56 (Pubitemid 47084677)
84. Hund TJ, Wright PJ, Dun W, et al. Regulation of the ankyrin-B-based targeting pathway following myocardial infarction. Cardiovasc Res 2009;81:742-9
85. Ruediger R, Brewis N, Ohst K, et al. Increasing the ratio of PP2A core enzyme to holoenzyme inhibits Tat-stimulated HIV-1 transcription and virus production. Virology 1997;238:432-43 (Pubitemid 28218160)
86. Brewis N, Ohst K, Fields K, et al. Dilated cardiomyopathy in transgenic mice expressing a mutant A subunit of protein phosphatase 2A. Am J Physiol Heart Circ Physiol 2000;279:H1307-18
87. Gudmundsson H, Hund TJ, Wright PJ, et al. EH domain proteins regulate cardiac membrane protein targeting. Circ Res 2010;107:84-95
88. Miliaras NB, Wendland B. EH proteins: multivalent regulators of endocytosis (and other pathways). Cell Biochem Biophys 2004;41:295-318 (Pubitemid 41270763)
89. Daumke O, Lundmark R, Vallis Y, et al. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 2007;449:923-7 (Pubitemid 47598607)
90. Bennett V, Lambert S. Physiological roles of axonal ankyrins in survival of premyelinated axons and localization of voltage-gated sodium channels. J Neurocytol 1999;28:303-18 (Pubitemid 30321012)
91. Harada K, Fukuda S, Kunimoto M, et al. Distribution of ankyrin isoforms and their proteolysis after ischemia and reperfusion in rat brain. J Neurochem 1997;69:371-6 (Pubitemid 27274193)
92. Inserte J, Garcia-Dorado D, Hernando V, et al. Calpain-mediated impairment of Na+/K+-ATPase activity during early reperfusion contributes to cell death after myocardial ischemia. Circ Res 2005;97:465-73 (Pubitemid 41298177)
93. Porter NC, Resneck WG, O'Neill A, et al. Association of small ankyrin 1 with the sarcoplasmic reticulum. Mol Membr Biol 2005;22:421-32 (Pubitemid 41747104)