Facilitation of murine cardiac L-type Cav1.2 channel is modulated by Calmodulin kinase II-dependent phosphorylation of S1512 and S1570

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 22, 2010, Pages 10285-10289

  Blaich, Anne ^a   Welling, Andrea ^a   Fischer, Stefanie ^a   Wegener, Jörg Werner ^a   Köstner, Katharina ^a   Hofmann, Franz ^a   Moosmang, Sven ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Calcium channels; Facilitation; Heart; Voltage dependent ion channels

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL L TYPE; SERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ELECTRIC POTENTIAL; ELECTROCARDIOGRAPHY; GENE MUTATION; HEART; HEART MUSCLE CELL; HEART RATE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QT INTERVAL;

AMINO ACID SUBSTITUTION; ANIMALS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; GENE KNOCK-IN TECHNIQUES; ION CHANNEL GATING; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MUTANT PROTEINS; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN SUBUNITS;

MURINAE; MUS;

EID: 77953439656     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914287107     Document Type: Article

References (51)

1. Catterall WA (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521-555. (Pubitemid 32037516)
2. Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198-205.
3. Catterall WA, Striessnig J, Snutch TP, Perez-Reyes E; International Union of Pharmacology (2003) International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: Calcium channels. Pharmacol Rev 55:579-581.
4. Hofmann F, Lacinová L, Klugbauer N (1999) Voltage-dependent calcium channels: From structure to function. Rev Physiol Biochem Pharmacol 139:33-87.
5. Noble S, Shimoni Y (1981) The calcium and frequency dependence of the slow inward current 'staircase' in frog atrium. J Physiol 310:57-75.
6. Lee KS (1987) Potentiation of the calcium-channel currents of internally perfused mammalian heart cells by repetitive depolarization. Proc Natl Acad Sci USA 84:3941-3945.
7. Noble S, Shimoni Y (1981) Voltage-dependent potentiation of the slow inward current in frog atrium. J Physiol 310:77-95. (Pubitemid 11166819)
8. Pietrobon D, Hess P (1990) Novel mechanism of voltage-dependent gating in L-type calcium channels. Nature 346:651-655. (Pubitemid 20266396)
9. Kleppisch T, et al. (1994) Double-pulse facilitation of smooth muscle alpha 1-subunit Ca2+ channels expressed in CHO cells. EMBO J 13:2502-2507. (Pubitemid 24188382)
10. Anderson ME (2004) Calmodulin kinase and L-type calcium channels; a recipe for arrhythmias? Trends Cardiovasc Med 14:152-161.
11. DeMaria CD, Soong TW, Alseikhan BA, Alvania RS, Yue DT (2001) Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels. Nature 411:484-489.
12. Zühlke RD, Pitt GS, Tsien RW, Reuter H (2000) Ca2+-sensitive inactivation and facilitation of L-type Ca2+ channels both depend on specific amino acid residues in a consensus calmodulin-binding motif in the(alpha)1C subunit. J Biol Chem 275:21121-21129.
13. Zühlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H (1999) Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature 399:159-162. (Pubitemid 129524348)
14. Peterson BZ, DeMaria CD, Adelman JP, Yue DT (1999) Calmodulin is the Ca2+ sensor for Ca2+ -dependent inactivation of L-type calcium channels. Neuron 22:549-558. (Pubitemid 29159853)
15. Van Petegem F, Chatelain FC, Minor DL, Jr (2005) Insights into voltage-gated calcium channel regulation from the structure of the CaV1.2 IQ domain-Ca2+/calmodulin complex. Nat Struct Mol Biol 12:1108-1115. (Pubitemid 41746782)
16. Halling DB, Aracena-Parks P, Hamilton SL (2005) Regulation of voltage-gated Ca2+ channels by calmodulin. Sci STKE, 10.1126/stke.3182006er1.
17. McCarron JG, et al. (1992) Calcium-dependent enhancement of calcium current in smooth muscle by calmodulin-dependent protein kinase II. Nature 357:74-77.
18. Xiao RP, Cheng H, Lederer WJ, Suzuki T, Lakatta EG (1994) Dual regulation of Ca2+/calmodulin-dependent kinase II activity by membrane voltage and by calcium influx. Proc Natl Acad Sci USA 91:9659-9663. (Pubitemid 2149248)
19. Yuan W, Bers DM (1994) Ca-dependent facilitation of cardiac Ca current is due to Ca-calmodulin-dependent protein kinase. Am J Physiol 267:H982-H993. (Pubitemid 2149627)
20. Anderson ME, Braun AP, Schulman H, Premack BA (1994) Multifunctional Ca2+/calmodulin-dependent protein kinase mediates Ca(2+)-induced enhancement of the L-type Ca2+ current in rabbit ventricular myocytes. Circ Res 75:854-861. (Pubitemid 2164026)
21. Dzhura I, Wu Y, Colbran RJ, Balser JR, Anderson ME (2000) Calmodulin kinase determines calcium-dependent facilitation of L-type calcium channels. Nat Cell Biol 2:173-177.
22. Hudmon A, et al. (2005) CaMKII tethers to L-type Ca2+ channels, establishing a local and dedicated integrator of Ca2+ signals for facilitation. J Cell Biol 171:537-547. (Pubitemid 41586942)
23. Lee TS, et al. (2006) Calmodulin kinase II is involved in voltage-dependent facilitation of the L-type Cav1.2 calcium channel: Identification of the phosphorylation sites. J Biol Chem 281:25560-25567.
24. Erxleben C, et al. (2006) Cyclosporin and Timothy syndrome increase mode 2 gating of CaV1.2 calcium channels through aberrant phosphorylation of S6 helices. Proc Natl Acad Sci USA 103:3932-3937. (Pubitemid 43376658)
25. Grueter CE, et al. (2006) L-type Ca2+ channel facilitation mediated by phosphorylation of the beta subunit by CaMKII. Mol Cell 23:641-650.
26. Link S, et al. (2009) Diversity and developmental expression of L-type calcium channel beta2 proteins and their influence on calcium current in murine heart. J Biol Chem 284:30129-30137.
27. Qin N, et al. (1998) Unique regulatory properties of the type 2a Ca2+ channel beta subunit caused by palmitoylation. Proc Natl Acad Sci USA 95:4690-4695. (Pubitemid 28207975)
28. Wang WY, et al. (2009) CaMKII phosphorylates a threonine residue in the C-terminal tail of Cav1.2 Ca(2+) channel and modulates the interaction of the channel with calmodulin. J Physiol Sci 59:283-290.
29. Guo J, Duff HJ (2003) Inactivation of ICa-L is the major determinant of use-dependent facilitation in rat cardiomyocytes. J Physiol 547:797-805. (Pubitemid 36367363)
30. Jiang X, et al. (2008) Modulation of CaV2.1 channels by Ca2+/calmodulin-dependent protein kinase II bound to the C-terminal domain. Proc Natl Acad Sci USA 105:341-346.
31. Vinogradova TM, et al. (2000) Sinoatrial node pacemaker activity requires Ca(2+)/calmodulin-dependent protein kinase II activation. Circ Res 87:760-767.
32. Guo J, Duff HJ (2006) Calmodulin kinase II accelerates L-type Ca2+ current recovery from inactivation and compensates for the direct inhibitory effect of [Ca2+]i in rat ventricular myocytes. J Physiol 574:509-518.
33. Wu Y, Dzhura I, Colbran RJ, Anderson ME (2001) Calmodulin kinase and a calmodulin-binding 'IQ' domain facilitate L-type Ca2+ current in rabbit ventricular myocytes by a common mechanism. J Physiol 535:679-687.
34. Picht E, et al. (2007) CaMKII inhibition targeted to the sarcoplasmic reticulum inhibits frequency-dependent acceleration of relaxation and Ca2+ current facilitation. J Mol Cell Cardiol 42:196-205. (Pubitemid 44958618)
35. Thiel WH, et al. (2008) Proarrhythmic defects in Timothy syndrome require calmodulin kinase II. Circulation 118:2225-2234.
36. Wu Y, Kimbrough JT, Colbran RJ, Anderson ME (2004) Calmodulin kinase is functionally targeted to the action potential plateau for regulation of L-type Ca2+ current in rabbit cardiomyocytes. J Physiol 554:145-155. (Pubitemid 38081449)
37. Keating MT, Sanguinetti MC (2001) Molecular and cellular mechanisms of cardiac arrhythmias. Cell 104:569-580. (Pubitemid 32201951)
38. Fauconnier J, Bedut S, Le Guennec JY, Babuty D, Richard S (2003) Ca2+ current-mediated regulation of action potential by pacing rate in rat ventricular myocytes. Cardiovasc Res 57:670-680. (Pubitemid 36254861)
39. Maier LS, Bers DM (2002) Calcium, calmodulin, and calcium-calmodulin kinase II: Heartbeat to heartbeat and beyond. J Mol Cell Cardiol 34:919-939. (Pubitemid 35316141)
40. Marban E, Tsien RW (1982) Enhancement of calcium current during digitalis inotropy in mammalian heart: Positive feed-back regulation by intracellular calcium? J Physiol 329:589-614.
41. Hadley RW, Lederer WJ (1991) Ca2+ and voltage inactivate Ca2+ channels in guinea-pig ventricular myocytes through independent mechanisms. J Physiol 444:257-268.
42. Qin N, Olcese R, Bransby M, Lin T, Birnbaumer L (1999) Ca2+-induced inhibition of the cardiac Ca2+ channel depends on calmodulin. Proc Natl Acad Sci USA 96:2435-2438.
43. Rhoads AR, Friedberg F (1997) Sequence motifs for calmodulin recognition. FASEB J 11:331-340.
44. Zühlke RD, Reuter H (1998) Ca2+-sensitive inactivation of L-type Ca2+ channels depends on multiple cytoplasmic amino acid sequences of the alpha1C subunit. Proc Natl Acad Sci USA 95:3287-3294.
45. Hashambhoy YL, Winslow RL, Greenstein JL (2009) CaMKII-induced shift in modal gating explains L-type Ca(2+) current facilitation: A modeling study. Biophys J 96:1770-1785.
46. Abiria SA, Colbran RJ (2010) CaMKII associates with CaV1.2 L-type calcium channels via selected beta subunits to enhance regulatory phosphorylation. J Neurochem 112:150-161.
47. Cens T, Restituito S, Vallentin A, Charnet P (1998) Promotion and inhibition of L-type Ca2+ channel facilitation by distinct domains of the subunit. J Biol Chem 273:18308-18315. (Pubitemid 28334755)
48. Bers DM, Grandi E (2009) Calcium/Calmodulin-dependent kinase II regulation of cardiac ion channels. J Cardiovasc Pharmacol 54:180-187.
49. Wu Y, et al. (2002) Calmodulin kinase II and arrhythmias in a mouse model of cardiac hypertrophy. Circulation 106:1288-1293. (Pubitemid 34988650)
50. Schröder F, et al. (1998) Increased availability and open probability of single L-type calcium channels from failing compared with nonfailing human ventricle. Circulation 98:969-976. (Pubitemid 28446649)
51. Moosmang S, et al. (2003) Dominant role of smooth muscle L-type calcium channel Cav1.2 for blood pressure regulation. EMBO J 22:6027-6034. (Pubitemid 37463246)