Dynamic cellular translocation of caldendrin is facilitated by the Ca 2+-myristoyl switch of recoverin

Journal of Neurochemistry

Volumn 113, Issue 5, 2010, Pages 1150-1162

  Fries, Ramona ^a   Reddy, Pasham Parameshwar ^b   Mikhaylova, Marina ^b   Haverkamp, Silke ^c   Wei, Tao ^a   Müller, Michael ^a   Kreutz, Michael R ^b   Koch, Karl Wilhelm ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^c MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

Calcium signaling; Caldendrin; Recoverin; Retina

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; CALDENDRIN; RECOVERIN; UNCLASSIFIED DRUG;

ADULT ANIMAL; AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CELL STRAIN COS7; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GEL PERMEATION CHROMATOGRAPHY; GENE TRANSLOCATION; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MOLECULAR CLONING; NONHUMAN; PINEAL BODY; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; RETINA; RETINA BIPOLAR GANGLION CELL; SURFACE PLASMON RESONANCE; TISSUE DISTRIBUTION;

ANIMALS; CALCIUM; CALCIUM-BINDING PROTEINS; CERCOPITHECUS AETHIOPS; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, GEL; COS CELLS; CYTOSOL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MYRISTATES; PINEAL GLAND; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; RECOVERIN; RETINA; SURFACE PLASMON RESONANCE;

EID: 77951910816     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06676.x     Document Type: Article

References (57)

1. Ames J. B., Ishima R., Tanaka T., Gordon J. I., Stryer L. Ikura M. (1997) Molecular mechanics of calcium-myristoyl switches. Nature 389, 198 202. (Pubitemid 27400604)
2. Ames J. B., Levay K., Wingard J. N., Lusin J. D. Slepak V. Z. (2006) Structural basis for calcium-induced inhibition of rhodopsin kinase by recoverin. J. Biol. Chem. 281, 37237 37245. (Pubitemid 46042192)
3. Bernstein H. G., Sahin J., Smalla K. H. et al. (2007) A reduced number of cortical neurons show increased caldendrin protein levels in chronic schizophrenia. Schizophr. Res. 96, 246 256. (Pubitemid 47494629)
4. Bosanac I., Yamazaki H., Matsu-Ura T., Michikawa T., Mikoshiba K. Ikura M. (2005) Crystal structure of the ligand binding suppressor domain of type 1 inositol 1,4,5-trisphosphate receptor. Mol. Cell 17, 193 203. (Pubitemid 40138615)
5. Bradford M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 73, 248 254.
6. 2+ signalling. Nat. Rev. Neurosci. 8, 182 193.
7. Bush R. A. Makino C. L. (2006) Recoverin shapes the photoresponse of retinal rods. Chapter IX, in Neuronal Calcium Sensor Proteins (Philippov P. P. Koch K.-W., eds), pp. 153 180. Nova Publishers
8. Dieterich D. C., Karpova A., Mikhaylova M. et al. (2008) Caldendrin - Jacob: a protein liaison that couples NMDA receptor signalling to the nucleus. PLoS Biol. 6, e34.
9. Dizhoor A. M., Ray S., Kumar S. et al. (1991) Recoverin: a calcium sensitive activator of retinal rod guanylate cyclase. Science 251, 915 918. (Pubitemid 21926182)
10. 2+-dependent membrane interaction. Science 259, 829 832. (Pubitemid 23066315)
11. 2+-binding protein activating photoreceptor guanylyl cyclase. J. Biol. Chem. 270, 25200 25206.
12. Erickson M. A., Lagnado L., Zozulya S., Neubert T. A., Stryer L. Baylor D. A. (1998) The effect of recombinant recoverin on the photoresponse of truncated rod photoreceptors. Proc. Natl Acad. Sci. USA 95, 6474 6479. (Pubitemid 28249038)
13. Euler T. Wässle H. (1995) Immunocytochemical identification of cone bipolar cells in the rat retina. J. Comp. Neurol. 361, 461 478.
14. Few A. P., Lautermilch N. J., Westenbroek R. E., Scheuer T. Catterall W. A. (2005) Differential regulation of CaV2.1 channels by calcium-binding protein 1 and visinin-like protein-2 requires N-terminal myristoylation. J. Neurosci. 25, 7071 7080. (Pubitemid 41077016)
15. Gorodovikova E. N., Senin I. I. Philippov P. P. (1994) Calcium-sensitive control of rhodopsin phosphorylation in the reconstituted system consisting of photoreceptor membranes, rhodopsin kinase and recoverin. FEBS Lett. 353, 171 172.
16. Haeseleer F., Sokal I., Verlinde C. L. et al. (2000) Five members of a novel Ca(2+)-binding protein (CABP) subfamily with similarity to calmodulin. J. Biol. Chem. 275, 1247 1260. (Pubitemid 30051178)
17. Haynes L. P., Tepikin A. V. Burgoyne R. D. (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.
18. Higgins M. K., Oprian D. D. Schertler G. F. X. (2006) Recoverin binds exclusively to an amphipathic peptide at the N terminus of rhodopsin kinase, inhibiting rhodopsin phosphorylation without affecting catalytic activity of the kinase. J. Biol. Chem. 281, 19426 19432.
19. Hwang J.-Y., Schlesinger R. Koch K.-W. (2004) Irregular dimerization of guanylate cyclase-activating protein 1 mutants causes loss of target activation. Eur. J. Biochem. 271, 3785 3793. (Pubitemid 39233620)
20. 2+-binding proteins. EMBO J. 23, 312 321. (Pubitemid 38294496)
21. Kawamura S., Hisatomi O., Kayada S., Tokunaga F. Kuo C.-H. (1993) Recoverin has S-modulin activity in frog rods. J. Biol. Chem. 268, 14579 14582. (Pubitemid 23206588)
22. 2+-binding protein 1 in Xenopus oocytes. Pflügers Arch. 450, 345 354. (Pubitemid 41204181)
23. Klenchin V. A., Calvert P. D. Bownds M. D. (1995) Inhibition of rhodopsin kinase by recoverin. J. Biol. Chem. 270, 16147 16152.
24. Koch K.-W. (2000) Identification and characterization of calmodulin binding sites in cGMP-gated channel using surface plasmon resonance spectroscopy. Methods Enzymol. 315, 785 797.
25. Komolov K. E., Senin I. I., Philippov P. P. Koch K.-W. (2006) Surface plasmon resonance study of G protein receptor coupling in a lipid bilayer-free system. Anal. Chem. 78, 1228 1234.
26. Komolov K. E., Senin I. I., Kovaleva N. A. et al. (2009) Mechanism of rhodopsin kinase regulation by recoverin. J. Neurochem. 110, 72 79.
27. Korf H. W., White B. H., Schaad N. C. Klein D. C. (1992) Recoverin in pineal organs and retinae of various vertebrate species including man. Brain Res. 595, 57 66.
28. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
29. Lambrecht H.-G. Koch K.-W. (1991) A 26 kd calcium binding protein from bovine rod outer segments as modulator of photoreceptor guanylate cyclase. EMBO J. 10, 793 798.
30. Lambrecht H.-G. Koch K.-W. (1992) Recoverin, a novel calcium-binding protein from vertebrate photoreceptors. Biochim. Biophys. Acta 1160, 63 66.
31. Lange C. Koch K.-W. (1997) Calcium-dependent binding of recoverin to membranes monitored by surface plasmon resonance spectroscopy in real time. Biochemistry 36, 12019 12026. (Pubitemid 27440939)
32. 2+-binding protein caldendrin: gene structure, splice isoforms and expression in the rat central nervous system. Mol. Cell. Neurosci. 19, 459 475. (Pubitemid 34293466)
33. 2+-binding proteins. Nat. Neurosci. 3, 210 217. (Pubitemid 34171133)
34. Leukert N., Vogl T., Strupat K. et al. (2006) Calcium-dependent tetramer formation of S100A8 and S100A9 is essential for biological activity. J. Mol. Biol. 359, 961 972. (Pubitemid 43831924)
35. Levay K., Satpaev D. K., Pronin A. N., Benovic J. L. Slepak V. Z. (1998) Localization of the sites for Ca+-binding on G protein-coupled receptor kinases. Biochemistry 37, 13650 13659.
36. Makino C. L., Dodd R. L., Chen J. et al. (2004) Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J. Gen. Physiol. 123, 729 741. (Pubitemid 38781377)
37. Menger N., Seidenbecher C. I., Gundelfinger E. D. Kreutz M. R. (1999) The cytoskeleton-associated neuronal calcium-binding protein caldendrin is expressed in a subset of amacrine, bipolar and ganglion cells of the rat retina. Cell Tissue Res. 298, 21 32. (Pubitemid 29460501)
38. 2+ signaling via caldendrin and calneurons. Biochim. Biophys. Acta 1763, 1229 1237. (Pubitemid 44779861)
39. Mikhaylova M., Reddy P. P., Munsch T. et al. (2009) Calneurons provide a calcium threshold for trans-Golgi network to plasma membrane trafficking. Proc. Natl Acad. Sci. USA 106, 9093 9098.
40. Milam A. H., Dacey D. M. Dizhoor A. (1993) Recoverin immunoreactivity in mammalian cone bipolar cells. Vis. Neurosci. 10, 1 12.
41. O′Callaghan D. W., Tepikin A. V. Burgoyne R. D. (2003) Dynamics and calcium-sensitivity of the calcium-myristoyl switch protein hippocalcin in living cells. J. Cell Biol. 163, 715 721. (Pubitemid 37517879)
42. Palczewski K., Subbaraya I., Gorczyca W. A. et al. (1994) Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13, 395 404. (Pubitemid 24275096)
43. Philippov P. P. Koch K.-W. (2006) Neuronal Calcium Sensor Proteins. Nova Publishers
44. Sampath A. P., Strissel K. J., Elias R. et al. (2005) Recoverin improves rod-mediated vision by enhancing signal transmission in the mouse retina. Neuron 46, 413 420. (Pubitemid 40616885)
45. Schmitz F., Bechmann M. Drenckhahn D. (1996) Purification of synaptic ribbons, structural components of the photoreceptor active zone complex. J. Neurosci. 16, 7109 7116. (Pubitemid 26382888)
46. Schultz K., Janssen-Bienhold U., Gundelfinger E. D. et al. (2004) The calcium-binding protein caldendrin and CaMKII are localized in spinules of the carp retina. J. Comp. Neurol. 479, 84 93. (Pubitemid 39305123)
47. Seidenbecher C. I., Langnaese K., Sanmartí-Vila L. et al. (1998) Caldendrin, a novel neuronal calcium-binding protein confined to the somato-dendritic compartment. J. Biol. Chem. 273, 21324 21331. (Pubitemid 28385426)
48. 2+-sensor proteins. J. Mol. Biol. 336, 957 970. (Pubitemid 38201542)
49. 2+-dependent control of rhodopsin phosphorylation: recoverin and rhodopsin kinase. Adv. Exp. Med. Biol. 514, 69 99. (Pubitemid 36438820)
50. 2+-binding sites. J. Biol. Chem. 277, 50365 50372. (Pubitemid 36042186)
51. Strissel K. J., Lishko P. V., Trieu L. H. et al. (2005) Recoverin undergoes light-dependent intracellular translocation in rod photoreceptors. J. Biol. Chem. 280, 29250 29255. (Pubitemid 41161378)
52. Tanaka T., Ames J. B., Harvey T. S., Stryer L. Ikura M. (1995) Sequestration of the membrane-targeting myristoyl group of recoverin in the calcium-free state. Nature 376, 444 447.
53. 2+ channels. J. Biol. Chem. 282, 8464 8473.
54. Wässle H., Grünert U., Martin P. R. Boycott B. B. (1994) Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Res. 34, 561 579. (Pubitemid 24052162)
55. Weitz D., Zoche M., Müller F. et al. (1998) Calmodulin controls the rod photoreceptor CNG channel through an unconventional binding site in the N-terminus of the β-subunit. EMBO J. 17, 2273 2284. (Pubitemid 28171912)
56. 2+ channels. J. Neurosci. 24, 4698 4708. (Pubitemid 38656625)
57. Zozulya S. Stryer L. (1992) Calcium-myristoyl protein switch. Proc. Natl Acad. Sci. USA 89, 11569 11573.