Defects in cytoskeletal signaling pathways, arrhythmia, and sudden cardiac death

Frontiers in Physiology

Volumn 3 MAY, Issue , 2012, Pages

  Smith, Sakima ^a,b   Curran, Jerry ^a   Hund, Thomas J ^a,b   Mohler, Peter J ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Ankyrin; Arrhythmia; Cytoskeleton; Mouse model; Spectrin

Indexed keywords

EID: 84866347738     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00122     Document Type: Article

References (42)

1. Abdi, K. M., Mohler, P. J., Davis, J. Q., and Bennett, V. (2006). Isoform specificity of ankyrin-B: a site in the divergent C-terminal domain is required for intramolecular association.J. Biol. Chem. 281, 5741-5749.
2. Antzelevitch, C., Brugada, P., Borggrefe, M., Brugada, J., Brugada, R., Cor-rado, D., Gussak, I., Lemarec, H., Nademanee, K., Perez Riera, A. R., Shimizu, W., Schulze-Bahr, E., Tan, H., and Wilde, A. (2005). Brugada syndrome: report of the second consensus conference: endorsed by the Heart Rhythm Society and the European Heart Rhythm Association. Circulation 111, 659-670.
3. Baba, S., Dun, W., Cabo, C., and Boyden, P. A. (2005). Remodeling in cells from different regions of the reentrant circuit during ventricular tachycardia. Circulation 112, 2386-2396.
4. Bennett, V. (1979). Immunoreactive forms of human erythrocyte ankyrin are present in diverse cells and tissues. Nature 281, 597-599.
5. Bennett, V., and Chen, L. (2001). Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Curr. Opin. Cell Biol. 13, 61-67.
6. Bennett, V., and Healy, J. (2009). Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb. Perspect. Biol. 1, a003012.
7. Bernstein, A. D., and Parsonnet, V. (1992). Survey of cardiac pacing in the United States in 1989. Am. J. Cardiol. 69, 331-338.
8. Bhasin, N., Cunha, S. R., Mudannayake, M., Gigena, M. S., Rogers, T. B., and Mohler, P. J. (2007). Molecular basis for PP2A regulatory subunit B56alpha targeting in cardiomy-ocytes. Am. J. Physiol. Heart Circ. Physiol. 293, H109-H119.
9. Camors, E., Mohler, P. J., Bers, D. M., and Despa, S. (2012). Ankyrin-B reduction enhances Ca spark-mediated SR Ca release promoting cardiac myocyte arrhythmic activity. J. Mol Cell. Cardiol. PMID: 22406428. [Epub ahead of print].
10. Chauhan, V. S., Tuvia, S., Buhusi, M., Bennett, V., and Grant, A. O. (2000). Abnormal cardiac Na(+) channel properties and QT heart rate adaptation in neonatal ankyrin(B) knockout mice. Circ. Res. 86, 441-447.
11. Cunha, S. R., Hund, T. J., Hashemi, S., Voigt, N., Li, N., Wright, P., Koval, O., Li, J., Gudmundsson, H., Gumina, R. J., Karck, M., Schott, J. J., Probst, V., Le Marec, H., Anderson, M. E., Dobrev, D., Wehrens, X. H., and Mohler, P. J. (2011). Defects in ankyrin-based membrane protein targeting pathways underlie atrial fibrillation. Circulation 124, 1212-1222.
12. Cunha, S. R., and Mohler, P. J. (2006). Cardiac ankyrins: essential components for development and maintenance of excitable membrane domains in heart. Cardiovasc. Res. 71, 22-29.
13. Cunha, S. R., and Mohler, P. J. (2008). Obscurin targets ankyrin-B and protein phosphatase 2A to the cardiac M-line. J. Biol. Chem. 283, 31968-31980.
14. De Arcangelis, V., Soto, D., and Xiang, Y. (2008). Phosphodiesterase 4 and phosphatase 2A differentially regulate cAMP/protein kinase a signaling for cardiac myocyte contraction under stimulation of beta1 adren-ergic receptor. Mol. Pharmacol. 74, 1453-1462.
15. Ferreira, M. A., O'Donovan, M. C., Meng, Y. A., Jones, I. R., Ruderfer, D. M., Jones, L., Fan, J., Kirov, G., Perlis, R. H., Green, E. K., Smoller, J. W., Grozeva, D., Stone, J., Nikolov, I., Chambert, K., Hamshere, M. L., Nimgaonkar, V. L., Moskvina, V., Thase, M. E., Caesar, S., Sachs, G. S., Franklin, J., Gordon-Smith, K., Ardlie, K. G., Gabriel, S. B., Fraser, C., Blumenstiel, B., Defelice, M., Breen, G., Gill, M., Morris, D. W., Elkin, A., Muir, W J., McGhee, K. A., Williamson, R., MacIntyre, D. J., MacLean, A. W., St, C. D., Robinson, M., Van Beck, M., Pereira, A. C., Kandaswamy, R., McQuillin, A., Collier, D. A., Bass, N. J., Young, A. H., Lawrence, J., Ferrier, I. N., Anjorin, A., Farmer, A., Curtis, D., Scolnick, E. M., McGuffin, P., Daly, M. J., Corvin, A. P., Holmans, P. A., Blackwood, D. H., Gurling, H. M., Owen, M. J., Purcell, S. M., Sklar, P., Craddock, N., and Wellcome Trust Case Control Consortium. (2008). Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. Nat. Genet. 40, 1056-1058.
16. Glukhov, A. V., Fedorov, V.V., Anderson, M. E., Mohler, P. J., and Efimov, I. R. (2010). Functional anatomy of the murine sinus node: high-resolution optical mapping of ankyrin-B heterozygous mice. Am. J. Physiol. Heart Circ. Physiol. 299, H482-H491.
17. Gudmundsson, H., Curran, J., Kashef, E, Snyder, J. S., Smith, S. A., Vargas-Pinto, P., Bonilla, I. M., Weiss, R. M., Anderson, M. E., Binkley, P., Felder, R. B., Carnes, C. A., Band, H., Hund, T. J., and Mohler, P. J. (2012). Differential regulation of EHD3 in human and mammalian heart failure.J. Mol. Cell. Cardiol. 52, 1183-1190.
18. Gudmundsson, H., Hund, T. J., Wright, P. J., Kline, C.F., Snyder, J.S., Qian, L., Koval, O. M., Cunha, S. R., George, M., Rainey, M. A., Kashef, F. E., Dun, W., Boyden, P. A., Anderson, M. E., Band, H., and Mohler, P. J. (2010). EH domain proteins regulate cardiac membrane protein targeting. Circ. Res. 107, 84-95.
19. Hashemi, S. M., Hund, T. J., and Mohler, P. J. (2009). Cardiac ankyrins in health and disease. J. Mol. Cell. Cardiol. 47, 203-209.
20. Hund, T. J., Koval, O. M., Li, J., Wright, P. J., Qian, L., Snyder, J. S., Gudmundsson, H., Kline, C. F., Davidson, N. P., Cardona, N., Rasband, M. N., Anderson, M. E., and Mohler, P. J. (2010). A beta(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J. Clin. Invest. 120, 3508-3519.
21. Hund, T. J., Wright, P. J., Dun, W., Snyder, J. S., Boyden, P. A., and Mohler, P. J. (2009). Regulation of the ankyrin-B-based targeting pathway following myocar dial infarction. Cardiovasc. Res. 81, 742-749.
22. Klein, G., Schroder, F., Vogler, D., Schae-fer, A., Haverich, A., Schieffer, B., Korte, T., and Drexler, H. (2003). Increased open probability of single cardiac L-type calcium channels in patients with chronic atrial fibrillation. Role of phosphatase 2A. Cardiovasc. Res. 59, 37-45.
23. Kline, C. F., Kurata, H. T., Hund, T. J., Cunha, S. R., Koval, O. M., Wright, P. J., Christensen, M., Anderson, M. E., Nichols, C. G., and Mohler, P. J. (2009). Dual role of K ATP channel C-terminal motif in membrane targeting and metabolic regulation. Proc. Natl. Acad. Sci. U.S.A. 106, 16669-16674.
24. Kontrogianni-Konstantopoulos, A., Jones, E. M., Van Rossum, D. B., and Bloch, R. J. (2003). Obscurin is a ligand for small ankyrin 1 in skeletal muscle. Mol. Biol. Cell 14, 1138-1148.
25. Le Scouarnec, S., Bhasin, N., Vieyres, C., Hund, T. J., Cunha, S. R., Koval, O., Marionneau, C., Chen, B., Wu, Y., Demolombe, S., Song, L. S., Le Marec, H., Probst, V., Schott, J. J., Anderson, M. E., and Mohler, P. J. (2008). Dysfunction in ankyrin-B-dependent ion channel and transporter targeting causes human sinus node disease. Proc. Natl. Acad. Sci. U.S.A. 105, 15617-15622.
26. Li, J., Kline, C. F., Hund, T. J., Anderson, M. E., and Mohler, P. J. (2010). Ankyrin-B regulates Kir6.2 membrane expression and function in heart. J. Biol. Chem. 285, 28723-28730.
27. Lowe, J. S., Palygin, O., Bhasin, N., Hund, T. J., Boyden, P. A., Shibata, E., Anderson, M. E., and Mohler, P. J. (2008). Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway.J. Cell Biol. 180, 173-186.
28. Mohler, P. J., Davis, J. Q., and Bennett, V. (2005). Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP(3) receptor in a cardiac T-Tubule/SR microdomain. PLoSBiol. 3, e423. doi:10.1371/jour-nal.pbio.0030423
29. Mohler, P. J., Le Scouarnec, S., Den-joy, I., Lowe, J. S., Guicheney P., Caron, L., Driskell, I. M., Schott, J. J., Norris, K., Leenhardt, A., Kim, R. B., Escande, D., and Roden, D. M. (2007). Defining the cellular pheno-type of "ankyrin-B syndrome" variants: human ANK2 variants associated with clinical phenotypes display a spectrum of activities in cardiomy-ocytes. Circulation 115, 432-441.
30. Mohler, P. J., Rivolta, I., Napolitano, C., Lemaillet, G., Lambert, S., Priori, S. G., and Bennett, V. (2004a). Nav1.5E. 1053K 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. 101, 17533-17538.
31. Mohler, P. J., Splawski, I., Napolitano, C., Bottelli, G., Sharpe, L., Timothy, K., Priori, S. G., Keating, M. T., and Bennett, V. (2004b). A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc. Natl. Acad. Sci. U.S.A. 101, 9137-9142.
32. Mohler, P. J., Yoon, W., and Bennett, V. (2004c). Ankyrin-B targets {beta}2-spectrin to an intracellular compartment in neonatal cardiomyocytes. J. Biol. Chem. 279, 40185-40193.
33. Mohler, P. J., Schott, J. J., Gramolini, A. O., Dilly, K. W., Guatimosim, S., Dubell, W. H., Song, L. S., Haurogne, K., Kyndt, F., Ali, M. E., Rogers, T. B., Lederer, W. J., Escande, D., Le Marec, H., and Bennett, V. (2003). Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 421, 634-639.
34. Pilichou, K., Nava, A., Basso, C., Beffagna, G., Bauce, B., Lorenzon, A., Frigo, G., Vettori, A., Valente, M., Towbin, J., Thiene, G., Danieli, G. A., andRampazzo, A. (2006). Mutations in desmoglein-2 gene are associated with arrhythmogenic right ventricular cardiomyopathy. Circulation 113, 1171-1179.
35. Sato, P. Y., Coombs, W., Lin, X., Nekrasova, O., Green, K. J., Isom, L. L., Taffet, S. M., and Delmar, M. (2011). Interactions between ankyrin-G, plakophilin-2, and con-nexin43 at the cardiac intercalated disc. Circ. Res. 109, 193-201.
36. Scott, L. J., Muglia, P., Kong, X. Q., Guan, W., Flickinger, M., Upmanyu, R., Tozzi, F., Li, J. Z., Burmeister, M., Absher, D., Thompson, R. C., Francks, C., Meng, F., Antoniades, A., Southwick, A. M., Schatzberg, A. F., Bunney, W. E., Barchas, J. D., Jones, E. G., Day, R., Matthews, K., McGuf-fin, P., Strauss, J. S., Kennedy, J. L., Middleton, L., Roses, A. D., Watson, S. J., Vincent, J. B., Myers, R. M., Farmer, A. E., Akil, H., Burns, D. K., and Boehnke, M. (2009). Genome-wide association and meta-analysis of bipolar disorder in individuals of European ancestry. Proc. Natl. Acad. Sci. U.S. A. 106, 7501-7506.
37. Sedlacek, K., Stark, K., Cunha, S. R., Pfeufer, A., Weber, S., Berger, I., Perz, S., Kaab, S., Wichmann, H. E., Mohler, P. J., Hengstenberg, C., and Jeron, A. (2008). Common genetic variants in ANK2 modulate QT interval: results from the KORA Study. Circ. Cardiovasc. Genet. 1, 93-99.
38. Sen-Chowdhry, S., Syrris, P., Pantazis, A., Quarta, G., Mckenna, W J., and Chambers, J. C. (2010). Mutational heterogeneity, modifier genes, and environmental influences contribute to phenotypic diversity of arrhythmogenic cardiomyopathy. Circ. Cardiovasc. Genet. 3, 323-330.
39. Splawski, I., Shen, J., Timothy, K. W., Lehmann, M. H., Priori, S., Robinson, J. L., Moss, A. J., Schwartz, P. J., Towbin, J. A., Vincent, G. M., and Keating, M. T. (2000). Spectrum of mutations in long-QT syndrome genes. KVLQT1, HERG, SCN5A, KCNE1, and KCNE2. Circulation 102, 1178-1185.
40. Suzuki, M., Li, R. A., Miki, T., Uemura, H., Sakamoto, N., Ohmoto-Sekine, Y., Tamagawa, M., Ogura, T., Seino, S., Marban, E., and Nakaya, H. (2001). Functional roles of cardiac and vascular ATP-sensitive potassium channels clarified by Kir6.2-knockout mice. Circ. Res. 88, 570-577.
41. Terentyev, D., Belevych, A. E., Teren-tyeva, R., Martin, M. M., Malana, G. E., Kuhn, D. E., Abdellatif, M., Feldman, D. S., Elton, T. S., and Gyorke, S. (2009). MiR-1 over-expression enhances Ca2+ release and promotes cardiac arrhythmo-genesis by targeting PP2A regulatory subunit B56{alpha} and causing CaMKII-dependent hyperphos-phorylation of RyR2. Circ. Res. 104, 514-521.
42. Wolf, R. M., Mitchell, C. C., Chris-tensen, M. D., Mohler, P. J., and Hund, T. J. (2010). Defining new insight into atypical arrhythmia: a computational model of ankyrin-B-syndrome. Am. J. Physiol. Heart Circ. Physiol. 299, H1505-H1514.