Differential regulation of CaV2.1 channels by calcium-binding protein 1 and visinin-like protein-2 requires N-terminal myristoylation

Journal of Neuroscience

Volumn 25, Issue 30, 2005, Pages 7071-7080

  Few, Alexandra P ^a   Lautermilch, Nathan J ^a,b   Westenbroek, Ruth E ^a   Scheuer, Todd ^a   Catterall, William A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b MDS Inc   (Canada)

Author keywords

Calcium current; Facilitation; Inactivation; Neuromodulation; Synaptic plasticity; Voltage clamp

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM BINDING PROTEIN 1; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALMODULIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; VISININ; VISININ LIKE PROTEIN 2; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; BARIUM; CA2+ BINDING PROTEIN 1; CA2+-BINDING PROTEIN-1; CALCIUM; CALCIUM CHANNEL N TYPE; MYRISTIC ACID; NEUROCALCIN; NVP2 PROTEIN, RAT; VOLTAGE DEPENDENT CALCIUM CHANNEL (P Q TYPE); VOLTAGE-DEPENDENT CALCIUM CHANNEL (P-Q TYPE);

ACCELERATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CALCIUM BINDING; CALCIUM CURRENT; CELL MEMBRANE; CONTROLLED STUDY; FACILITATION; IMMUNOHISTOCHEMISTRY; MOUSE; MYRISTYLATION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; ANIMAL; CELL CULTURE; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; HUMAN; KIDNEY; METABOLISM; PATCH CLAMP; PHYSIOLOGY; RAT; SITE DIRECTED MUTAGENESIS;

ANIMALS; BARIUM; CALCIUM; CALCIUM CHANNELS, N-TYPE; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; HUMANS; ION CHANNEL GATING; KIDNEY; MEMBRANE POTENTIALS; MUTAGENESIS, SITE-DIRECTED; MYRISTIC ACID; NEUROCALCIN; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; RATS; TRANSFECTION;

EID: 23044440123     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0452-05.2005     Document Type: Article

References (45)

1. Ames JB, Porumb T, Tanaka T, Ikura M, Stryer L (1995) Amino-terminal myristoylation induces cooperative calcium binding to recoverin. J Biol Chem 270:4526-4533.
2. Ames JB, Tanaka T, Stryer L, Ikura M (1996) Portrait of a myristoyl switch protein. Curr Opin Struct Biol 6:432-438.
3. Ames JB, Ishima R, Tanaka T, Gordon JI, Stryer L, Ikura M (1997) Molecular mechanics of calcium-myristoyl switches. Nature 389:198-202.
4. Ames JB, Hendricks KB, Strahl T, Huttner IG, Hamasaki N, Thorner J (2000) Structure and calcium-binding properties of Frq1, a novel calcium sensor in the yeast Saccharomyces cerevisiae. Biochemistry 39:12149-12161.
5. Braunewell KH, Gundelfinger ED (1999) Intracellular neuronal calcium sensor proteins: a family of EF-hand calcium-binding proteins in search of a function. Cell Tissue Res 295:1-12.
6. Burgoyne RD, Weiss JL (2001) The neuronal calcium sensor family of calcium-binding proteins. Biochem J 353:1-12.
7. Burgoyne RD, O'Callaghan DW, Hasdemir B, Haynes LP, Tepikin AV (2004) Neuronal calcium-sensor proteins: multitalented regulators of neuronal function. Trends Neurosci 27:203-209.
8. Calvert PD, Klenchin VA, Bownds MD (1995) Rhodopsin kinase inhibition by recoverin. Function of recoverin myristoylation. J Biol Chem 270:24127-24129.
9. Chen CK, Inglese J, Lefkowitz RJ, Hurley JB (1995) Calcium-dependent interaction of recoverin with rhodopsin kinase. J Biol Chem 270:18060-18066.
10. Cox JA, Durussel I, Comte M, Nef S, Nef P, Lenz SE, Gundelfinger ED (1994) Cation binding and conformational changes in VILIP and NCS-1, two neuron-specific calcium-binding proteins. J Biol Chem 269:32807-32813.
11. DeMaria CD, Soong TW, Alseikhan BA, Alvania RS, Yue DT (2001) Calmodulin bifurcates the local calcium signal that modulates P/Q-type calcium channels. Nature 411:484-489.
12. Dizhoor AM, Chen CK, Olshevskaya E, Sinelnikova W, Phillipov P, Hurley JB (1993) Role of the acylated amino terminus of recoverin in calcium-dependent membrane interaction. Science 259:829-832.
13. Dodge Jr FA, Rahamimoff R (1967) Cooperative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond) 193:419-432.
14. Dunlap K, Luebke JI, Turner TJ (1995) Exocytotic calcium channels in mammalian central neurons. Trends Neurosci 18:89-98.
15. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T (1998) Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20:797-807.
16. Haeseleer F, Palczewski K (2002) Calmodulin and calcium-binding proteins (CaBPs): variations on a theme. Adv Exp Med Biol 514:303-317.
17. Haeseleer F, Sokal I, Verlinde CL, Erdjument-Bromage H, Tempst P, Pronin AN, Benovic JL, Fariss RN, Palczewski K (2000) Five members of a novel calcium-binding protein (CABP) subfamily with similarity to calmodulin. J Biol Chem 275:1247-1260.
18. Haeseleer F, Imanishi Y, Sokal I, Filipek S, Palczewski K (2002) Calcium-binding proteins: intracellular sensors from the calmodulin superfamily. Biochem Biophys Res Commun 290:615-623.
19. Haynes LP, Tepikin AV, Burgoyne RD (2004) Calcium-binding protein 1 is an inhibitor of agonist-evoked, inositol 1,4,5-trisphosphate-mediated calcium signaling. J Biol Chem 279:547-555.
20. Kawamura S, Cox JA, Nef P (1994) Inhibition of rhodopsin phosphorylation by non-myristoylated recombinant recoverin. Biochem Biophys Res Commun 203:121-127.
21. Kobayashi M, Takamatsu K, Saitoh S, Noguchi T (1993) Myristoylation of hippocalcin is linked to its calcium-dependent membrane association properties. J Biol Chem 268:18898-18904.
22. Ladant D (1995) Calcium and membrane binding properties of bovine neurocalcin delta expressed in Escherichia coli. J Biol Chem 270:3179-3185.
23. V2.1 channels by the neuronal calcium-binding protein visinin-like protein-2. J Neurosci 25:7062-7070.
24. Lee A, Wong ST, Gallagher D, Li B, Storm DR, Scheuer T, Catterall WA (1999) Calcium/calmodulin binds to and modulates P/Q-type calcium channels. Nature 399:155-159.
25. Lee A, Scheuer T, Catterall WA (2000) Calcium/calmodulin-dependent facilitation and inactivation of P/Q-type calcium channels. J Neurosci 20:6830-6838.
26. V2.1 channels by calmodulin and calcium-binding protein 1. Nat Neurosci 5:210-217.
27. V2.1 channels. Proc Natl Acad Sci USA 100:16059-16064.
28. Liang H, DeMaria CD, Erickson MG, Mori MX, Alseikhan BA, Yue DT (2003) Unified mechanisms of calcium regulation across the calcium channel family. Neuron 39:951-960.
29. Mintz IM, Sabatini BL, Regehr WG (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron 15:675-688.
30. O'Callaghan DW, Burgoyne RD (2003) Role of myristoylation in the intracellular targeting of neuronal calcium sensor (NCS) proteins. Biochem Soc Trans 31:963-965.
31. O'Callaghan DW, Burgoyne RD (2004) Identification of residues that determine the absence of a calcium/myristoyl switch in neuronal calcium sensor-1. J Biol Chem 279:14347-14354.
32. O'Callaghan DW, Ivings L, Weiss JL, Ashby MC, Tepikin AV, Burgoyne RD (2002) Differential use of myristoyl groups on neuronal calcium sensor proteins as a determinant of spatio-temporal aspects of calcium signal transduction. J Biol Chem 277:14227-14237.
33. + channels. J Cell Sci 116:4833-4845.
34. Olshevskaya EV, Hughes RE, Hurley JB, Dizhoor AM (1997) Calcium binding, but not a calcium-myristoyl switch, controls the ability of guanylyl cyclase-activating protein GCAP-2 to regulate photoreceptor guanylyl cyclase. J Biol Chem 272:14327-14333.
35. Rocque WJ, McWherter CA, Wood DC, Gordon JI (1993) A comparative analysis of the kinetic mechanism and peptide substrate specificity of human and Saccharomyces cerevisiae myristoyl-CoA:protein N-myristoyltransferase. J Biol Chem 268:9964-9971.
36. Rousset M, Cens T, Gavarini S, Jeromin A, Charnet P (2003) Down-regulation of voltage-gated calcium channels by neuronal calcium sensor-1 is beta subunit-specific. J Biol Chem 278:7019-7026.
37. Sakurai T, Westenbroek RE, Rettig J, Hell J, Catterall WA (1996) Biochemical properties and subcellular distribution of the BI and rbA isoforms of alpha 1A subunits of brain calcium channels. J Cell Biol 134:511-528.
38. Senin II, Zargarov AA, Alekseev AM, Gorodovikova EN, Lipkin VM, Philippov PP (1995) N-myristoylation of recoverin enhances its efficiency as an inhibitor of rhodopsin kinase. FEBS Lett 376:87-90.
39. Spilker C, Gundelfinger ED, Braunewell KH (1997) Calcium- and myristoyl-dependent subcellular localization of the neuronal calcium-binding protein VILIP in transfected PC12 cells. Neurosci Lett 225:126-128.
40. Takahashi T, Momiyama A (1993) Different types of calcium channels mediate central synaptic transmission. Nature 366:156-158.
41. Tsujimoto T, Jeromin A, Saitoh N, Roder JC, Takahashi T (2002) Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295:2276-2279.
42. Wang CY, Yang F, He X, Chow A, Du J, Russell JT, Lu B (2001) Calcium binding protein frequenin mediates GDNF-induced potentiation of calcium channels and transmitter release. Neuron 32:99-112.
43. Weiss JL, Burgoyne RD (2001) Voltage-independent inhibition of P/Q-type calcium channels in adrenal chromaffin cells via a neuronal calcium sensor-1-dependent pathway involves Src family tyrosine kinase. J Biol Chem 276:44804-44811.
44. Westenbroek RE, Sakurai T, Elliott EM, Hell JW, Starr TV, Snutch TP, Catterall WA (1995) Immunochemical identification and subcellular distribution of the alpha 1A subunits of brain calcium channels. J Neurosci 15:6403-6418.
45. Zucker RS (2003) NCS-1 stirs somnolent synapses. Nat Neurosci 6:1006-1008.