Identification and characterization of two ankyrin-B isoforms in mammalian heart

Cardiovascular Research

Volumn 107, Issue 4, 2015, Pages 466-477

  Wu, Henry C ^a   Yamankurt, Gokay ^b   Luo, Jialie ^b   Subramaniam, Janani ^a   Hashmi, Syed Shahrukh ^c   Hu, Hongzhen ^a   Cunha, Shane R ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative splicing; Ankyrin B; Cardiomyocytes; Obscurin; Sodium calcium exchanger

Indexed keywords

ANKYRIN; ANKYRIN B; COMPLEMENTARY DNA; OBSCURIN; SODIUM CALCIUM EXCHANGE PROTEIN; UNCLASSIFIED DRUG; ANK2 PROTEIN, HUMAN; ANK2 PROTEIN, MOUSE; ANK2 PROTEIN, RAT; ISOPROTEIN;

ADULT; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; GENE EXPRESSION; GENE SILENCING; HEART; HEART MUSCLE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MISSENSE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RAT; SKELETAL MUSCLE; TRANSVERSE TUBULAR SYSTEM; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CYTOSKELETON; GENETICS; METABOLISM;

ALTERNATIVE SPLICING; ANIMALS; ANKYRINS; CYTOSKELETON; HUMANS; MICE; MUSCLE, SKELETAL; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN ISOFORMS; RATS; SODIUM-CALCIUM EXCHANGER;

EID: 84948163575     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv184     Document Type: Article

References (33)

1. Cunha SR, Hund TJ, Hashemi S, Voigt N, Li N, Wright P, Koval O, Li J, Gudmundsson H, Gumina RJ, Karck M, Schott JJ, Probst V, Le Marec H, Anderson ME, Dobrev D, Wehrens XH, Mohler PJ. Defects in ankyrin-based membrane protein targeting pathways underlie atrial fibrillation. Circulation 2011;124:1212-1222
2. Le Scouarnec S, Bhasin N, Vieyres C, Hund TJ, Cunha SR, Koval O, Marionneau C, Chen B, Wu Y, Demolombe S, Song LS, Le Marec H, Probst V, Schott JJ, Anderson ME, Mohler PJ. Dysfunction in ankyrin-B-dependent ion channel and transporter targeting causes human sinus node disease. Proc Natl Acad Sci USA 2008;105: 15617-15622
3. Mohler PJ, Schott JJ, Gramolini AO, Dilly KW, Guatimosim S, duBell WH, Song LS, Haurogne K, Kyndt F, Ali ME, Rogers TB, Lederer WJ, Escande D, Le Marec H, Bennett V. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 2003;421:634-639
4. Otto E, Kunimoto M, McLaughlin T, Bennett V. Isolation and characterization of cDNAs encoding human brain ankyrins reveal a family of alternatively spliced genes. J Cell Biol 1991;114:241-253
5. Birkenmeier CS, Sharp JJ, Gifford EJ, Deveau SA, Barker JE. An alternative first exon in the distal end of the erythroid ankyrin gene leads to production of a small isoform containing an NH2-terminal membrane anchor. Genomics 1998;50:79-88
6. Birkenmeier CS, White RA, Peters LL, Hall EJ, Lux SE, Barker JE. Complex patterns of sequence variation and multiple 5 and 3 ends are found among transcripts of the erythroid ankyrin gene. J Biol Chem 1993;268:9533-9540
7. Cunha SR, Le Scouarnec S, Schott JJ, Mohler PJ. 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
8. Devarajan P, Stabach PR, Mann AS, Ardito T, Kashgarian M, Morrow JS. Identification of a small cytoplasmic ankyrin (AnkG119) in the kidney and muscle that binds beta I sigma spectrin and associates with the Golgi apparatus. J Cell Biol 1996;133:819-830
9. Gagelin C, Constantin B, Deprette C, Ludosky MA, Recouvreur M, Cartaud J, Cognard C, Raymond G, Kordeli E. Identification of Ank(G107), a muscle-specific ankyrin-G isoform. J Biol Chem 2002;277:12978-12987
10. Gallagher PG, Forget BG. An alternate promoter directs expression of a truncated, muscle-specific isoform of the human ankyrin 1 gene. J Biol Chem 1998;273:1339-1348
11. Hopitzan AA, Baines AJ, Ludosky MA, Recouvreur M, Kordeli E. Ankyrin-G in skeletal muscle: tissue-specific alternative splicing contributes to the complexity of the sarcolemmal cytoskeleton. Exp Cell Res 2005;309:86-98
12. Zhang X, Bennett V. Restriction of 480/270-kD ankyrin G to axon proximal segments requires multiple ankyrin G-specific domains. J Cell Biol 1998;142:1571-1581
13. Yamankurt G, Wu HC, McCarthy M, Cunha SR. Exon organization and novel alternative splicing of ank3 in mouse heart. PLoS One 2015;10:e0128177
14. Baskin KK, Taegtmeyer H. AMP-Activated protein kinase regulates E3 ligases in rodent heart. Circ Res 2011;109:1153-1161
15. Cunha SR, Bhasin N, Mohler PJ. Targeting and stability of Na/Ca exchanger 1 in cardiomyocytes requires direct interaction with the membrane adaptor ankyrin-B. J Biol Chem 2007;282:4875-4883
16. Fassina L, Di Grazia A, Naro F, Monaco L, De Angelis MG, Magenes G. Video evaluation of the kinematics and dynamics of the beating cardiac syncytium: an alternative to the Langendorff method. Int J Artif Organs 2011;34:546-558
17. Cunha SR, Mohler PJ. Obscurin targets ankyrin-B and protein phosphatase 2A to the cardiac M-line. J Biol Chem 2008;283:31968-31980
18. 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
19. Mohler PJ, Le Scouarnec S, Denjoy I, Lowe JS, Guicheney P, Caron L, Driskell IM, Schott JJ, Norris K, Leenhardt A, Kim RB, Escande D, Roden DM. 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
20. Mohler PJ, Splawski I, Napolitano C, Bottelli G, Sharpe L, Timothy K, Priori SG, Keating MT, Bennett V. A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc Natl Acad Sci USA 2004;101:9137-9142
21. Randazzo D, Giacomello E, Lorenzini S, Rossi D, Pierantozzi E, Blaauw B, Reggiani C, Lange S, Peter AK, Chen J, Sorrentino V. Obscurin is required for ankyrinB-dependent dystrophin localization and sarcolemma integrity. J Cell Biol 2013;200:523-536
22. Mohler PJ, Davis JQ, Davis LH, Hoffman JA, Michaely P, Bennett V. Inositol 1,4,5-trisphosphate receptor localization and stability in neonatal cardiomyocytes requires interaction with ankyrin-B. J Biol Chem 2004;279:12980-12987
23. Kunimoto M, Otto E, Bennett V. A new 440-kD isoform is the major ankyrin in neonatal rat brain. J Cell Biol 1991;115:1319-1331
24. Ackermann MA, Hu LY, Bowman AL, Bloch RJ, Kontrogianni-Konstantopoulos A. Obscurin interacts with a novel isoform of MyBP-C slow at the periphery of the sarcomeric M-band and regulates thick filament assembly. Mol Biol Cell 2009;20:2963-2978
25. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Randall WR, Bloch RJ. Obscurin regulates the organization of myosin into A bands. Am J Physiol Cell Physiol 2004;287:C209-C217
26. Raeker MO, Su F, Geisler SB, Borisov AB, Kontrogianni-Konstantopoulos A, Lyons SE, Russell MW. Obscurin is required for the lateral alignment of striated myofibrils in zebrafish. Dev Dyn 2006;235:2018-2029
27. Busby B, Willis CD, Ackermann MA, Kontrogianni-Konstantopoulos A, Bloch RJ. Characterization and comparison of two binding sites on obscurin for small ankyrin 1. Biochemistry 2010;49:9948-9956
28. Kordeli E, Lambert S, Bennett V, Ankyrin G. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 1995;270:2352-2359
29. Zhou D, Birkenmeier CS, WilliamsMW, Sharp JJ, Barker JE, Bloch RJ. Small, membranebound, alternatively spliced forms of ankyrin 1 associated with the sarcoplasmic reticulum of mammalian skeletal muscle. J Cell Biol 1997;136:621-631
30. Ayalon G, Davis JQ, Scotland PB, Bennett V. An ankyrin-based mechanism for functional organization of dystrophin and dystroglycan. Cell 2008;135:1189-1200
31. Li J, Kline CF, Hund TJ, Anderson ME, Mohler PJ. Ankyrin-B regulates Kir6.2 membrane expression and function in heart. J Biol Chem 2010;285:28723-28730
32. Kline CF, Kurata HT, Hund TJ, Cunha SR, Koval OM, Wright PJ, Christensen M, Anderson ME, Nichols CG, Mohler PJ. Dual role of K ATP channel C-terminal motif in membrane targeting and metabolic regulation. Proc Natl Acad Sci USA 2009;106: 16669-16674
33. Smith SA, Sturm AC, Curran J, Kline CF, Little SC, Bonilla IM, Long VP, Makara M, Polina I, Hughes LD, Webb TR, Wei Z, Wright P, Voigt N, Bhakta D, Spoonamore KG, Zhang C, Weiss R, Binkley PF, Janssen PM, Kilic A, Higgins RS, Sun M, Ma J, Dobrev D, Zhang M, Carnes CA, Vatta M, Rasband MN, Hund TJ, Mohler PJ. Dysfunction in the bII spectrin-dependent cytoskeleton underlies human arrhythmia. Circulation 2015;131:695-708