Ahnak is critical for cardiac Ca(v)1.2 calcium channel function and its β-adrenergic regulation

FASEB Journal

Volumn 19, Issue 14, 2005, Pages 1969-1977

  Haase, Hannelore ^a,g   Alvarez, Julio ^b   Petzhold, Daria ^a   Doller, Anke ^c   Behlke, Joachim ^a   Erdmann, Jeanette ^d   Hetzer, Roland ^e   Regitz Zagrosek, Vera ^c,e   Vassort, Guy ^f   Morano, Ingo ^a,c  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b Institute of Cardiology   (Cuba)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^e DEUTSCHES HERZZENTRUM BERLIN   (Germany)

^f INSERM   (France)

^g NONE   (Germany)

Author keywords

2 subunit; Binding affinity; Missense variant; Recombinant protein

Indexed keywords

BETA ADRENERGIC RECEPTOR; CALCIUM CHANNEL L TYPE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOLEUCINE; ISOPRENALINE; PEPTIDE; PROTEIN; PROTEIN AHNAK; RECOMBINANT PROTEIN; THREONINE; UNCLASSIFIED DRUG;

ADRENERGIC ACTIVITY; ARTICLE; BINDING AFFINITY; CALCIUM CHANNEL CA(V)1.2; CALCIUM TRANSPORT; CHANNEL GATING; ENZYME PHOSPHORYLATION; GENE MUTATION; GENETIC REGULATION; GENETIC VARIABILITY; HEART CONTRACTION; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MISSENSE MUTATION; PATCH CLAMP; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SYMPATHETIC TONE;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CARDIOMYOPATHY, HYPERTROPHIC; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION REGULATION; GLUTATHIONE TRANSFERASE; HETEROZYGOTE; HUMANS; ISOLEUCINE; MALE; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTATION; MUTATION, MISSENSE; MYOCARDIUM; MYOCYTES, CARDIAC; NEOPLASM PROTEINS; PEPTIDES; PHOSPHORYLATION; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA; RECOMBINANT PROTEINS; SOFTWARE; TEMPERATURE; THREONINE; ULTRACENTRIFUGATION; UP-REGULATION; VARIATION (GENETICS);

EID: 28744458169     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-3997com     Document Type: Article

References (41)

1. Aimond, F., Alvarez, J. L., Rauzier, J. M., Lorente, P., and Vassort, G. (1999) Ionic basis of ventricular arrhythmias in remodeled rat heart during long-term myocardial infarction. Cardiovasc. Res. 42, 402-415
2. Van Wagoner, D. R., and Nerbonne, J. M. (2000) Molecular basis of electrical remodeling in atrial fibrillation. J. Mol. Cell. Cardiol. 32, 1101-1117
3. 2+ channel in transgenic mice. J. Biol. Chem. 274, 21503-21506
4. Schröder, F., Handrock, R., Beuckelmann, D. J., Hirt, S., Hullin, R., Priebe, L., Schwinger, R. H. G., Weil, J., and Herzig, S. (1998) Increased availability and open probability of single L-type calcium channels from failing compared with nonfailing human ventricle. Circulation 98, 969-976
5. 2+ channels. Annu. Rev. Cell Dev. Biol. 16, 521-555
6. Trautwein, W., and Hescheler, J. (1990) Regulation of the cardiac L-type calcium current by phosphorylation and G-proteins. Annu. Rev. Physiol. 52, 257-274
7. 2+ channels require membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19, 185-196
8. Hulme, J. T., Lin, T. W. C., Westenbroek, R. E., Scheuer, T., and Catterall, W. A. (2003) β-Adrenergic regulation requires direct anchoring of PKA to cardiac Cav.1.2. channels via leucine zipper interaction with A kinase-anchoring protein 15. Proc. Natl. Acad. Sci. USA 100, 13093-13098
9. Haase, H., Karczewki, P., Beckert, R., and Krause, E. G. (1993) Phosphorylation of the L-type calcium channel β subunit is involved in β-adrenergic signal transduction in canine myocardium. FEBS Lett. 335, 217-222
10. Bünemann, M., Gerhardstein, B. L., Gao, T., and Hosey, M. M. (1999) Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the β2 subunit. J. Biol. Chem. 274, 33851-33854
11. Charnet, P., Lory, P., Bourinet, E., Collin, T., and Nargeot, J. (1995) cAMP-dependent phosphorylation of the cardiac L-type Ca channel: a missing link? Biochimie 77, 957-962
12. Haase, H., Podzuweit, T., Lutsch, U., Hohaus, A., Kostka, S., Lindschau, C., Kott, M., Kraft, R., and Morano, I. (1999) Signaling from β-adrenoceptor to L-type calcium channel: identification of a novel protein kinase A target possessing similarities to AHNAK. FASEB J. 13, 2161-2172
13. Shtivelman, E., Cohen, F. E., and Bishop, J. M. (1992) A human gene (AHNAK)encoding an unusually large protein with 1.2-μm polyionic rod structure. Proc. Natl. Acad. Sci. USA 89, 5472-5476
14. Shtivelman, E., and Bishop, J. M. (1993) The human gene AHNAK encodes a large phosphoprotein located primarily in the nucleus. J. Cell Biol. 120, 625-630
15. Benaud, C., Gentil, B. J., Assard, N., Court, M., Garin, J., Delphin, C., and Baudier, J. (2004) AHNAK interaction with the annexin 2/S100A10 complex regulates cell membrane cytoarchitecture. J. Cell Biol. 164, 133-144
16. Straub, B. K., Boda, J., Kuhn, C., Schnoelzer, M., Korf, U., Kempf, T., Spring, H., Hatzfeld, M., and Franke, W. W. (2003) A novel cell-cell junction system: the cortex adhaerens mosaic of lens fiber cells. J. Cell Sci. 116, 4985-4995
17. Hashimoto, T., Gamou, S., Shimizu, N., Kitajima, Y., and Nishikawa, T. (1995) Regulation of translocation of the desmoyokin/AHNAK protein to the plasma membrane in keratinocytes by protein kinase C. Exp. Cell Res. 217, 258-266
18. Sekiya, F., Bae, Y. S., Jhon, D. Y., Hwang, S. C., and Rhee, S. G. (1999) AHNAK, a protein that binds and activates phospholipase C-γ1 in the presence of arachidonic acid. J. Biol. Chem. 274, 13900-13907
19. Sussman, J., Stokoe, D., Ossina, N., and Shtivelman, E. (2001) Protein kinase B phosphorylates AHNAK and regulates its subcellular localization. J. Cell Biol. 154, 1019-1030
20. 2+ channels and the actin-based cytoskeleton. FASEB J. 16, 1205-1216
21. Gentil, J. B., Delphin, C., Benaud, C., and Baudier, J. (2003) Expression of the Giant Protein AHNAK (Desmoyokin) in muscle and lining epithelial cells. J. Histochem. Cytochem. 51, 339-348
22. Alvarez, J. L., Hamplova, J., Hohaus, A., Morano, I., Haase, H., and Vassort, G. (2004) Calcium current in rat cardiomyocytes is modulated by the carboxyl-terminal ahnak domain. J. Biol. Chem. 279, 12456-12461
23. Erdmann, J., Raible, J., Maki-Abadi, J., Hummel, M., Hammann, J., Wollnick, B., Frantz, E., Fleck, E., Hetzer, R., and Regitz-Zagrosek, V. (2001) Spectrum of clinical phenotypes and gene variants in cardiac myosin-binding protein C mutation carriers with hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 38, 322-330
24. 2+ channel α1 subunit (α1C-b) by the β2a subunit: a peptide which inhibits binding of β to the I-II linker of α1 induces functional uncoupling. Biochem. J. 348, 657-665
25. Hullin, R., Singer-Lahat, D., Freichel, M., Biel, M., Dascal, M., Hofmann, F., and Flockerzi, V. (1992) Calcium channel β subunit heterogeneity: functional expression of cloned cDNA from heart, aorta and brain. EMBO J. 11, 885-890
26. Behlke, J., Ristau, O., and Schönfeld, H. J. (1997) Nucleotide-dependent complex formation between the Escherichia coli chaperonins GroEL and GroES studied under equilibrium conditions. Biochemistry 36, 5149-5156
27. Hamill, O. P., Marry, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch. 391, 85-100
28. Hescheler, J., Kameyama, M., and Trautwein, W. (1986) On the mechanism of muscarinic inhibition of the cardiac Ca current. Pfluegers Arch. 407, 182-189
29. 2+ current enhancement by alpha 2/delta and beta subunits in Xenopus oocytes: contribution of changes in channel gating and alpha 1 protein level. J. Physiol. (London) 489, 55-62
30. Kamp, T. J., Perez-Garcia, M. T., and Marban, E. (1996) Enhancement of ionic current and charge movement by coexpression of calcium channel beta 1A subunit with alpha 1C subunit in a human embryonic kidney cell line. J. Physiol. (London) 492, 89-96
31. Colecraft, H. M., Alseikhan, B., Takahashi, S. X., Chaudhuri, D., Mittman, S., Yegnasubramanian, V., Alvania, R. S., Johns, D. C., Marban, E., and Yue, D. T. (2002) Novel functional properties of Ca(2+) channel beta subunits revealed by their expression in adult rat heart cells. J. Physiol. (London) 541, 435-452
32. 2+ channel and its modulation by protein kinase C. J. Biol. Chem. 273, 17901-17909
33. 2+ channel activity by deletions at the carboxyl terminus of the cardiac alpha 1 subunit. J. Biol. Chem. 269, 1635-1640
34. 2+ channel inactivation gate. J. Neurosci. 20, 9046-9052
35. 2+ channel inactivation. Biophys. J. 87, 844-857
36. Luo, W., Grupp, I. L., Harrer, J., Ponniah, S., Grupp, G., Duffy, J. J., Doetschman, T., and Kranias, E. G. (1994) Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ. Res. 75, 401-409
37. Marx, S. O., Reiken, S., Hisamatsu, Y., Jayaraman, T., Burkhoff, D., Rosemblit, N., and Marks, A. R. (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor):defective regulation in failing hearts. Cell 101, 365-376
38. Komuro, A., Masuda, Y., Kobayashi, K., Babbitt, R., Gunel, M., Flavell, R. A., and Marchesi, V. T. (2004) The AHNAKs are a class of giant propeller-like proteins that associate with calcium channel proteins of cardiomyocytes and other cells. Proc. Natl. Acad. Sci. USA 101, 4053-4058
39. Haase, H., Pagel, I., Khalina, Y., Zacharzowsky, U., Person, V., Lutsch, G., Petzhold, D., Kott, M., Schaper, J., and Morano, I. (2004) The carboxyl-terminal ahnak domain induces actin bundling and stabilizes muscle contraction. FASEB J. 18, 839-841
40. Splawski, I., Timothy, K. W., Sharpe, L. M., Decher, N., Kumar, P., Bloise, R., Napolitano, C., Schwartz, P. J., Joseph, R. M., Condouris, K., et al. (2004) Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119, 19-31
41. Gerhardstein, B. L., Puri, T. S., Chien, A. J., and Hosey, M. M. (1999) Identification of the sites phosphorylated by cyclic AMP-dependent protein kinase on the β2 subunit of L-type voltage-dependent calcium channels. Biochemistry 38, 10361-10370