Ankyrin-based patterning of membrane microdomains: New insights into a novel class of cardiovascular diseases

Journal of Cardiovascular Pharmacology

Volumn 54, Issue 2, 2009, Pages 106-115

  Nilsson, Kent R ^a   Bennett, Vann ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Adherens junction; Ankyrin B; Ankyrin G; Arrhythmogenic right ventricular cardiomyopathy; Brugada; Costamere; Desmosome; Intercalated disc; Long QT syndrome

Indexed keywords

ALPHA CATENIN; ANKYRIN; ANKYRIN B; ANKYRIN G; ION CHANNEL; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; SPECTRIN; UNCLASSIFIED DRUG; VINCULIN;

BRUGADA SYNDROME; CARDIOVASCULAR DISEASE; CELL JUNCTION; CELL STRUCTURE; DESMOSOME; HEART MUSCLE CELL; LONG QT SYNDROME; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEFICIENCY; PROTEIN STRUCTURE; REVIEW; SINUS NODE DYSFUNCTION; TRANSVERSE TUBULAR SYSTEM;

ANIMALS; ANKYRINS; CARDIOVASCULAR DISEASES; HUMANS; ION CHANNELS; MEMBRANE MICRODOMAINS; MYOCYTES, CARDIAC;

EID: 74249116009     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181b2b6ed     Document Type: Review

References (91)

1. Hunt SA, Abraham WT, Chin MH, et al. ACC/AHA 2005 guideline update for the diagnosis and management of chronic heart failure in the adult: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Update the 2001 Guidelines for the Evaluation and Management of Heart Failure): developed in collaboration with the American College of Chest Physicians and the International Society for Heart and Lung Transplantation: endorsed by the Heart Rhythm Society. Circulation. 2005;112: e154-e235.
2. Anderson JL, Adams CD, Antman EM, et al. ACC/AHA 2007 guidelines for the management of patients with unstable angina/non-ST-elevation myocardial infarction: a report of the American College of Cardiology/ American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 2002 Guidelines for the Management of Patients With Unstable Angina/Non-ST-Elevation Myocardial Infarction) developed in collaboration with the American College of Emergency Physicians, the Society for Cardiovascular Angiography and Interventions, and the Society of Thoracic Surgeons endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation and the Society for Academic Emergency Medicine. J Am Coll Cardiol. 2007;50: e1-e157.
3. Epstein AE, DiMarco JP, Ellenbogen KA, et al. ACC/AHA/HRS 2008 guidelines for device-based therapy of cardiac rhythm abnormalities: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the ACC/AHA/NASPE 2002 Guideline Update for Implantation of Cardiac Pacemakers and Antiarrhythmia Devices) developed in collaboration with the American Association for Thoracic Surgery and Society of Thoracic Surgeons. J Am Coll Cardiol. 2008;51:e1-e62.
4. Zipes DP, Camm AJ, Borggrefe M, et al. ACC/AHA/ESC 2006 guidelines for management of patients with ventricular arrhythmias and the prevention of sudden cardiac death-executive summary: a report of the American College of Cardiology/American Heart Association Task Force and the European Society of Cardiology Committee for Practice Guidelines (Writing Committee to Develop Guidelines for Management of Patients with Ventricular Arrhythmias and the Prevention of Sudden Cardiac Death) developed in collaboration with the European Heart Rhythm Association and the Heart Rhythm Society. Eur Heart J. 2006;27: 2099-2140.
5. 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.
6. Mohler PJ. Ankyrins and human disease: what the electrophysiologist should know. J Cardiovasc Electrophysiol. 2006;17:1153-1159.
7. Jenkins SM, Bennett V. Ankyrin-G coordinates assembly of the spectrinbased membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol. 2001;155:739-746
8. Kizhatil K, Yoon W, Mohler PJ, et al. Ankyrin-G and beta2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J Biol Chem. 2007;282:2029-2037.
9. Cunha SR, Le Scouarnec S, Schott JJ, et al. Exon organization and novel alternative splicing of the human ANK2 gene: implications for cardiac function and human cardiac disease. J Mol Cell Cardiol. 2008;45: 724-734.
10. Hund TJ, Mohler PJ. Ankyrin-based targeting pathway regulates human sinoatrial node automaticity. Channels (Austin). 2008;2:404-406.
11. Cunha SR, Mohler PJ. Obscurin targets ankyrin-B and protein phosphatase 2A to the cardiac M-line. J Biol Chem. 2008;283:31968-31980.
12. Agre P, Orringer EP, Chui DH, et al. A molecular defect in two families with hemolytic poikilocytic anemia: reduction of high affinity membrane binding sites for ankyrin. J Clin Invest. 1981;68:1566-1576.
13. Lux SE, Tse WT, Menninger JC, et al. Hereditary spherocytosis associated with deletion of human erythrocyte ankyrin gene on chromosome 8. Nature. 1990;345:736-739.
14. Lambert S, Bennett V. Postmitotic expression of ankyrinR and beta Rspectrin in discrete neuronal populations of the rat brain. J Neurosci. 1993; 13:3725-3735.
15. Eber SW, Gonzalez JM, Lux ML, et al. Ankyrin-1 mutations are a major cause of dominant and recessive hereditary spherocytosis. Nat Genet. 1996;13:214-218.
16. 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.
17. Mohler PJ, Le Scouarnec S, 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;115:432-441.
18. 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 U S A. 2004; 101:17533-17558.
19. Mohler PJ, Schott JJ, Gramolini AO, et al. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature. 2003;421:634-639.
20. Mohler PJ, Splawski I, Napolitano C, et al. A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc Natl Acad Sci U S A. 2004;101:9137-9142.
21. Mohler PJ, Yoon W, Bennett V. Ankyrin-B targets beta2-spectrin to an intracellular compartment in neonatal cardiomyocytes. J Biol Chem. 2004; 279:40185-40193.
22. Cunha SR, Mohler PJ. Cardiac ankyrins: essential components for development and maintenance of excitable membrane domains in heart. Cardiovasc Res. 2006;71:22-29.
23. Bennett V, Baines AJ. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev. 2001;81:1353-1392.
24. Bennett V, Healy J. Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol Med. 2008;14:28-36.
25. 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;281:5741-5749.
26. 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;279:25798-25804.
27. Le Scouarnec S, Bhasin N, Vieyres C, et al. Dysfunction in ankyrin-Bdependent ion channel and transporter targeting causes human sinus node disease. Proc Natl Acad Sci U S A. 2008;105:15617-15622.
28. Del Rio M, Imam A, DeLeon M, et al. The death domain of kidney ankyrin interacts with Fas and promotes Fas-mediated cell death in renal epithelia. J Am Soc Nephrol. 2004;15:41-51.
29. Davis L, Abdi K, Machius M, et al. Localization and structure of the ankyrin-binding site on beta 2-spectrin. J Biol Chem. 2008;6982-6987.
30. 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.
31. Bennett V. Purification of an active proteolytic fragment of the membrane attachment site for human erythrocyte spectrin. J Biol Chem. 1978;253: 2292-2299. (Pubitemid 8328215)
32. Stabach PR, Simonovic I, Ranieri MA, et al. The structure of the ankyrinbinding site of {beta}-spectrin reveals how tandem spectrin-repeats generate unique ligand-binding properties. Blood. 2009;5377-5384.
33. Ipsaro JJ, Huang L, Mondragon A. Structures of the spectrin-ankyrin interaction binding domains. Blood. 2009;5385-5393.
34. Kizhatil K, Davis JQ, Davis L, et al. Ankyrin-G is a molecular partner of E-cadherin in epithelial cells and early embryos. J Biol Chem. 2007;282: 26552-26561.
35. Kizhatil K, Bennett V. Lateral membrane biogenesis in human bronchial epithelial cells requires 190-kDa ankyrin-G. J Biol Chem. 2004;279: 16706-16714.
36. Komada M, Soriano P. [Beta]IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol. 2002;156:337-348.
37. Dzhashiashvili Y, Zhang Y, Galinska J, et al. Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol. 2007;177:857-870.
38. Yang Y, Ogawa Y, Hedstrom KL, et al. betaIV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG. J Cell Biol. 2007;176: 509-519.
39. Michaely P, Bennett V. The membrane-binding domain of ankyrin contains four independently folded subdomains, each comprised of six ankyrin repeats. J Biol Chem. 1993;268:22703-22709.
40. Michaely P, Bennett V. Mechanism for binding site diversity on ankyrin. Comparison of binding sites on ankyrin for neurofascin and the Cl-/ HCO3- anion exchanger. J Biol Chem. 1995;270:31298-31302.
41. Michaely P, Bennett V. The ANK repeats of erythrocyte ankyrin form two distinct but cooperative binding sites for the erythrocyte anion exchanger. J Biol Chem. 1995;270:22050-22057.
42. Michaely P, Tomchick DR, Machius M, et al. Crystal structure of a 12 ANK repeat stack from human ankyrinR. EMBO J. 2002;21: 6387-6396.
43. Lee G, Abdi K, Jiang Y, et al. Nanospring behaviour of ankyrin repeats. Nature. 2006;440:246-249.
44. 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: 1114-1122.
45. Tuvia S, Buhusi M, Davis L, et al. Ankyrin-B is required for intracellular sorting of structurally diverse Ca2+ homeostasis proteins. J Cell Biol. 1999;147:995-1008.
46. 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: 10599-10607.
47. Mohler PJ, Bennett V. Ankyrin-based cardiac arrhythmias: a new class of channelopathies due to loss of cellular targeting. Curr Opin Cardiol. 2005;20:189-193.
48. Sherman J, Tester DJ, Ackerman MJ. Targeted mutational analysis of ankyrin-B in 541 consecutive, unrelated patients referred for long QT syndrome genetic testing and 200 healthy subjects. Heart Rhythm. 2005;2: 1218-1223.
49. 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;180:173-186.
50. Calloe K, Cordeiro JM, Di Diego JM, et al. A transient outward potassium current activator recapitulates the electrocardiographic manifestations of Brugada syndrome. Cardiovasc Res. 2008;686-694.
51. Zhou D, Lambert S, Malen PL, et al. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol. 1998;143:1295-1304.
52. Pan Z, Kao T, Horvath Z, et al. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci. 2006;26:2599-2613.
53. Priori SG, Napolitano C, Gasparini M, et al. Clinical and genetic heterogeneity of right bundle branch block and ST-segment elevation syndrome: a prospective evaluation of 52 families. Circulation. 2000;102: 2509-2515.
54. Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol. 2005;289:H2291-H2301.
55. Danowski BA, Imanaka-Yoshida K, Sanger JM, et al. Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. J Cell Biol. 1992;118:1411-1420.
56. Mansour H, de Tombe PP, Samarel AM, et al. Restoration of resting sarcomere length after uniaxial static strain is regulated by protein kinase Cepsilon and focal adhesion kinase. Circ Res. 2004;94:642-649.
57. Ayalon G, Davis JQ, Scotland PB, et al. An ankyrin-based mechanism for functional organization of dystrophin and dystroglycan. Cell. 2008;135: 1189-1200.
58. Shaw RM, Fay AJ, Puthenveedu MA, et al. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell. 2007;128:547-560.
59. Severs NJ. The cardiac gap junction and intercalated disc. Int J Cardiol. 1990;26:137-173.
60. Franke WW, Borrmann CM, Grund C, et al. The area composita of adhering junctions connecting heart muscle cells of vertebrates. I. Molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins. Eur J Cell Biol. 2006;85:69-82.
61. Zuppinger C, Eppenberger-Eberhardt M, Eppenberger HM. N-Cadherin: structure, function and importance in the formation of new intercalated disc-like cell contacts in cardiomyocytes. Heart Fail Rev. 2000;5: 251-257.
62. Kostetskii I, Li J, Xiong Y, et al. Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ Res. 2005;96:346-354.
63. Sheikh F, Chen Y, Liang X, et al. alpha-E-catenin inactivation disrupts the cardiomyocyte adherens junction, resulting in cardiomyopathy and susceptibility to wall rupture. Circulation. 2006;114:1046-1055.
64. van den Borne SW, Narula J, Voncken JW, et al. Defective intercellular adhesion complex in myocardium predisposes to infarct rupture in humans. J Am Coll Cardiol. 2008;51:2184-2192.
65. Ziegler WH, Liddington RC, Critchley DR. The structure and regulation of vinculin. Trends Cell Biol. 2006;16:453-460.
66. Zemljic-Harpf AE, Miller JC, Henderson SA, et al. Cardiac-myocytespecific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy. Mol Cell Biol. 2007;27: 7522-7537.
67. Melo TG, Almeida DS, de Meirelles Mde N, et al. Trypanosoma cruzi infection disrupts vinculin costameres in cardiomyocytes. Eur J Cell Biol. 2004;83:531-540.
68. Sen-Chowdhry S, Syrris P, McKenna WJ. Role of genetic analysis in the management of patients with arrhythmogenic right ventricular dysplasia/ cardiomyopathy. J Am Coll Cardiol. 2007;50:1813-1821.
69. Yamamoto Y, Aoyama Y, Shu E, et al. Anti-desmoglein 3 (Dsg3) monoclonal antibodies deplete desmosomes of Dsg3 and differ in their Dsg3-depleting activities related to pathogenicity. J Biol Chem. 2007;282: 17866-17876.
70. Chernyavsky AI, Arredondo J, Kitajima Y, et al. Desmoglein versus nondesmoglein signaling in pemphigus acantholysis: characterization of novel signaling pathways downstream of pemphigus vulgaris antigens. J Biol Chem. 2007;282:13804-13812.
71. Jonkman MF, Pasmooij AM, Pasmans SG, et al. Loss of desmoplakin tail causes lethal acantholytic epidermolysis bullosa. Am J Hum Genet. 2005; 77:653-660.
72. Kirchhof P, Fabritz L, Zwiener M, et al. Age- and training-dependent development of arrhythmogenic right ventricular cardiomyopathy in heterozygous plakoglobin-deficient mice. Circulation. 2006;114: 1799-1806.
73. Garcia-Gras E, Lombardi R, Giocondo MJ, et al. Suppression of canonical Wnt/beta-catenin signaling by nuclear plakoglobin recapitulates phenotype of arrhythmogenic right ventricular cardiomyopathy. J Clin Invest. 2006;116:2012-2021.
74. Green KJ, Gaudry CA. Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol. 2000;1:208-216.
75. Green KJ, Simpson CL. Desmosomes: new perspectives on a classic. J Invest Dermatol. 2007;127:2499-2515.
76. Syed SE, Trinnaman B, Martin S, et al. Molecular interactions between desmosomal cadherins. Biochem J. 2002;362:317-327.
77. +-dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollin, contributes to cell-cell adhesion. J Cell Biol. 1997;138:193-201.
78. Simpson MA, Mansour S, Ahnood D, et al. Homozygous mutation of desmocollin-2 in arrhythmogenic right ventricular cardiomyopathy with mild palmoplantar keratoderma and woolly hair. Cardiology. 2008;113: 28-34.
79. Syrris P, Ward D, Asimaki A, et al. Desmoglein-2 mutations in arrhythmogenic right ventricular cardiomyopathy: a genotype-phenotype characterization of familial disease. Eur Heart J. 2007;28:581-588.
80. Asimaki A, Syrris P, Wichter T, et al. A novel dominant mutation in plakoglobin causes arrhythmogenic right ventricular cardiomyopathy. Am J Hum Genet. 2007;81:964-973.
81. Kannankeril PJ, Bhuiyan ZA, Darbar D, et al. Arrhythmogenic right ventricular cardiomyopathy due to a novel plakophilin 2 mutation: wide spectrum of disease in mutation carriers within a family. Heart Rhythm. 2006;3:939-944.
82. Norman M, Simpson M, Mogensen J, et al. Novel mutation in desmoplakin causes arrhythmogenic left ventricular cardiomyopathy. Circulation. 2005;112:636-642.
83. Moric-Janiszewska E, Markiewicz-Loskot G. Review on the genetics of arrhythmogenic right ventricular dysplasia. Europace. 2007;9:259-266. (Pubitemid 47079239)
84. Gerull B, Heuser A,Wichter T, et al. Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy. Nat Genet. 2004;36:1162-1164.
85. Oyama MA, Reiken S, Lehnart SE, et al. Arrhythmogenic right ventricular cardiomyopathy in Boxer dogs is associated with calstabin2 deficiency. J Vet Cardiol. 2008;10:1-10.
86. Basso C, Fox PR, Meurs KM, et al. Arrhythmogenic right ventricular cardiomyopathy causing sudden cardiac death in boxer dogs: a new animal model of human disease. Circulation. 2004;109:1180-1185.
87. Asimaki A, Tandri H, Huang H, et al. A new diagnostic test for arrhythmogenic right ventricular cardiomyopathy. N Engl J Med. 2009; 360:1075-1084.
88. Fidler LM,Wilson GJ, Liu F, et al. Abnormal connexin43 in arrhythmogenic right ventricular cardiomyopathy caused by plakophilin-2 mutations. J Cell Mol Med. 2008.
89. Kaplan SR, Gard JJ, Protonotarios N, et al. Remodeling of myocyte gap junctions in arrhythmogenic right ventricular cardiomyopathy due to a deletion in plakoglobin (Naxos disease). Heart Rhythm. 2004;1:3-11.
90. Yao JA, Hussain W, Patel P, et al. Remodeling of gap junctional channel function in epicardial border zone of healing canine infarcts. Circ Res. 2003;92:437-443.
91. Peters NS, Green CR, Poole-Wilson PA, et al. Reduced content of connexin43 gap junctions in ventricular myocardium from hypertrophied and ischemic human hearts. Circulation. 1993;88:864-875.