Divalent cations and Redox conditions regulate the molecular structure and function of visinin-like protein-1

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Wang, Conan K ^a   Simon, Anne ^b   Jessen, Christian M ^c   Oliveira, Cristiano L P ^d   Mack, Lynsey ^e   Braunewell, Karl Heinz ^f   Ames, James B ^g   Pedersen, Jan Skov ^d   Hofmann, Andreas ^a,e  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d AARHUS UNIVERSITY   (Denmark)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f SOUTHERN RESEARCH INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; MONOMER; UNCLASSIFIED DRUG; VISININ; VISININ LIKE PROTEIN 1; DIVALENT CATION; NEUROCALCIN;

ADSORPTION KINETICS; ARTICLE; CALCIUM BINDING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; LIPID MEMBRANE; LIPID MONOLAYER; MEMBRANE BINDING; MOLECULAR IMAGING; MYRISTYLATION; OPTICAL RESOLUTION; OXIDATION REDUCTION STATE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; STRUCTURE ANALYSIS; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; GEL CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PROTEIN CONFORMATION; RADIATION SCATTERING; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CATIONS, DIVALENT; CELL LINE; CHROMATOGRAPHY, GEL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROCALCIN; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SCATTERING, RADIATION; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 80355123635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026793     Document Type: Article

References (43)

1. Burgoyne RD, (2007) Neuronal calcium sensor proteins: generating diversity in neuronal Ca2+ signalling. Nat Rev Neurosci 8: 182-93.
2. Genin A, Davis S, Meziane H, Doyere V, Jeromin A, et al. (2001) Regulated expression of the neuronal calcium sensor-1 gene during long-term potentiation in the dentate gyrus in vivo. Neuroscience 106: 571-7.
3. Braunewell KH, Brackmann M, Manahan-Vaughan D, (2003) Group I mGlu receptors regulate the expression of the neuronal calcium sensor protein VILIP-1 in vitro and in vivo: implications for mGlu receptor-dependent hippocampal plasticity? Neuropharmacology 44: 707-15.
4. Kabbani N, Negyessy L, Lin R, Goldman-Rakic P, Levenson R, (2002) Interaction with neuronal calcium sensor NCS-1 mediates desensitization of the D2 dopamine receptor. J Neurosci 22: 8476-86.
5. Bahi N, Friocourt G, Carrie A, Graham ME, Weiss JL, et al. (2003) IL1 receptor accessory protein like, a protein involved in X-linked mental retardation, interacts with Neuronal Calcium Sensor-1 and regulates exocytosis. Hum Mol Genet 12: 1415-25.
6. Cheng HY, Pitcher GM, Laviolette SR, Whishaw IQ, Tong KI, et al. (2002) DREAM is a critical transcriptional repressor for pain modulation. Cell 108: 31-43.
7. Mahloogi H, Gonzalez-Guerrico AM, Lopez De Cicco R, Bassi DE, Goodrow T, et al. (2003) Overexpression of the calcium sensor visinin-like protein-1 leads to a cAMP-mediated decrease of in vivo and in vitro growth and invasiveness of squamous cell carcinoma cells. Cancer Res 63: 4997-5004.
8. Spilker C, Dresbach T, Braunewell KH, (2002) Reversible translocation and activity-dependent localization of the calcium-myristoyl switch protein VILIP-1 to different membrane compartments in living hippocampal neurons. J Neurosci 22: 7331-9.
9. Braunewell KH, Brackmann M, Schaupp M, Spilker C, Anand R, et al. (2001) Intracellular neuronal calcium sensor (NCS) protein VILIP-1 modulates cGMP signalling pathways in transfected neural cells and cerebellar granule neurones. J Neurochem 78: 1277-86.
10. Ramamurthy V, Tucker C, Wilkie SE, Daggett V, Hunt DM, et al. (2001) Interactions within the coiled-coil domain of RetGC-1 guanylyl cyclase are optimized for regulation rather than for high affinity. J Biol Chem 276: 26218-29.
11. Brackmann M, Schuchmann S, Anand R, Braunewell KH, (2005) Neuronal Ca2+ sensor protein VILIP-1 affects cGMP signalling of guanylyl cyclase B by regulating clathrin-dependent receptor recycling in hippocampal neurons. J Cell Sci 118: 2495-505.
12. Olshevskaya EV, Ermilov AN, Dizhoor AM, (1999) Dimerization of guanylyl cyclase-activating protein and a mechanism of photoreceptor guanylyl cyclase activation. J Biol Chem 274: 25583-7.
13. Osawa M, Dace A, Tong KI, Valiveti A, Ikura M, et al. (2005) Mg2+ and Ca2+ differentially regulate DNA binding and dimerization of DREAM. J Biol Chem 280: 18008-14.
14. Brackmann M, Hofmann A, Braunewell KH, (2006) Structure, function and expression of members of the VILIP (Visinin-like Protein) subfamily of neuronal calcium sensor proteins., in Neuronal calcium sensor proteins, In: Philippov P, Koch K, editors. Nova Science Publisher pp. 115-138.
15. Ames JB, Ishima R, Tanaka T, Gordon JI, Stryer L, et al. (1997) Molecular mechanics of calcium-myristoyl switches. Nature 389: 198-202.
16. Krylov DM, Hurley JB, (2001) Identification of proximate regions in a complex of retinal guanylyl cyclase 1 and guanylyl cyclase-activating protein-1 by a novel mass spectrometry-based method. J Biol Chem 276: 30648-54.
17. Ermilov AN, Olshevskaya EV, Dizhoor AM, (2001) Instead of binding calcium, one of the EF-hand structures in guanylyl cyclase activating protein-2 is required for targeting photoreceptor guanylyl cyclase. J Biol Chem 276: 48143-8.
18. Cox JA, Durussel I, Comte M, Nef S, Nef P, et al. (1994) Cation binding and conformational changes in VILIP and NCS-1, two neuron-specific calcium-binding proteins. J Biol Chem 269: 32807-13.
19. Chen KC, Wang LK, Chang LS, (2009) Regulatory elements and functional implication for the formation of dimeric visinin-like protein-1. J Pept Sci 15: 89-94.
20. Li C, Pan W, Braunewell KH, Ames JB, (2010) Structural analysis of Mg2+ and Ca2+ binding, myristoylation, and dimerization of the neuronal calcium sensor and visinin-like protein 1 (VILIP-1). J Biol Chem 286: 6354-66.
21. Permyakov SE, Nazipova AA, Denesyuk AI, Bakunts AG, Zinchenko DV, et al. (2007) Recoverin as a redox-sensitive protein. J Proteome Res 6: 1855-63.
22. Vijay-Kumar S, Kumar VD, (1999) Crystal structure of recombinant bovine neurocalcin. Nat Struct Biol 6: 80-8.
23. Lusin JD, Vanarotti M, Li C, Valiveti A, Ames JB, (2008) NMR structure of DREAM: Implications for Ca(2+)-dependent DNA binding and protein dimerization. Biochemistry 47: 2252-64.
24. Studier FW, (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-34.
25. Perkins D, Pappin D, Creasy D, Cottrell J, (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
26. Hofmann A, Wlodawer A, (2002) PCSB-a program collection for structural biology and biophysical chemistry. Bioinformatics 18: 209-10.
27. Pedersen J, (2004) A flux- and background-optimised version of the nanoSTAR small-angle X-ray scattering camera for solution scattering. J Appl Crystallogr 37: 369-380.
28. Glatter O, (1977) A new method for the evaluation of small-angle scattering data. J Appl Crystallogr 10: 415-421.
29. Pedersen J, Hansen S, Bauer R, (1994) The aggregation behavior of zinc-free insulin studied by small-angle neutron scattering. Eur Biophys J 22: 379-389.
30. Svergun DI, Petoukhov MV, Koch MH, (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80: 2946-53.
31. Svergun D, Barberato C, Koch M, (1995) CRYSOL- a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Crystallogr 28: 768-773.
32. Braunewell KH, Brackmann M, Hofmann A, (2006) VILIP-1, A novel regulator of the guanylate cyclase transduction system in neurons. Calcium Binding Proteins 1: 12-15.
33. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
34. Laskowski RA, MacArthur MW, Moss D, Thornton JM, (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
35. Jones TA, Zou JY, Cowan SW, Kjeldgaard M, (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47 (Pt 2): 110-9.
36. Lin L, Jeanclos EM, Treuil M, Braunewell KH, Gundelfinger ED, et al. (2002) The calcium sensor protein visinin-like protein-1 modulates the surface expression of agonist sensitivity of alpha4beta 2 nicotinic acetylcholine receptor. J Biol Chem 2002: 41872-41878.
37. McFerran BW, Weiss JL, Burgoyne RD, (1999) Neuronal Ca(2+) sensor 1. Characterization of the myristoylated protein, its cellular effects in permeabilized adrenal chromaffin cells, Ca(2+)-independent membrane association, and interaction with binding proteins, suggesting a role in rapid Ca(2+) signal transduction. J Biol Chem 274: 30258-65.
38. 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: 126-8.
39. Vogel A, Schroder T, Lange C, Huster D, (2007) Characterization of the myristoyl lipid modification of membrane-bound GCAP-2 by 2H solid-state NMR spectroscopy. Biochim Biophys Acta 1768: 3171-81.
40. Meyer T, York JD, (1999) Calcium-myristoyl switches turn on new lights. Nat Cell Biol 1: E93-5.
41. Zhao CJ, Noack C, Brackmann M, Gloveli T, Maelicke A, et al. (2009) Neuronal Ca2+ sensor VILIP-1 leads to the upregulation of functional alpha4beta2 nicotinic acetylcholine receptors in hippocampal neurons. Mol Cell Neurosci 40: 280-92.
42. Ames JB, Levay K, Wingard JN, Lusin JD, Slepak VZ, (2006) Structural basis for calcium-induced inhibition of rhodopsin kinase by recoverin. J Biol Chem 281: 37237-45.
43. Strahl T, Huttner IG, Lusin JD, Osawa M, King D, et al. (2007) Structural insights into activation of phosphatidylinositol 4-kinase (Pik1) by yeast frequenin (Frq1). J Biol Chem 282: 30949-59.