Reversible translocation and activity-dependent localization of the calcium-myristoyl switch protein VILIP-1 to different membrane compartments in living hippocampal neurons

Journal of Neuroscience

Volumn 22, Issue 17, 2002, Pages 7331-7339

  Spilker, Christina ^a,b   Dresbach, Thomas ^b   Braunewell, Karl Heinz ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

Activity dependent; Calcium myristoyl switch; GFP; Golgi; Hippocampal neurons; Membrane compartments; NCS protein; Signaling; VILIP 1

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM IONOPHORE; CALCIUM SENSING RECEPTOR; EGTAZIC ACID; GLUTAMATE RECEPTOR; GREEN FLUORESCENT PROTEIN; UNCLASSIFIED DRUG; VISININ; VISININ LIKE PROTEIN 1;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; DEPOLARIZATION; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; GOLGI COMPLEX; HIPPOCAMPUS; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

EID: 0036758614     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-17-07331.2002     Document Type: Article

References (45)

1. Aarts LH, Verkade P, van Dalen JJ, van Rozen AJ, Gispen WH, Schrama LH, Schotman P (1999) B-50/GAP-43 potentiates cytoskeletal reorganization in raft domains. Mol Cell Neurosci 14:85-97.
2. 2+-induced extrusion of the myristoyl group of recoverin. J Biol Chem 270:30909-30913.
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, Dizhoor AM, Ikura M, Palczewski K, Stryer L (1999) Three-dimensional structure of guanylyl cyclase activating protein-2, a calcium-sensitive modulator of photoreceptor guanylyl cyclases. J Biol Chem 274:19329-19337.
5. Ames JB, Ikura M, Stryer L (2000a) Molecular structure of membrane-targeting calcium sensors in vision: Recoverin and guanylate cyclase-activating protein 2. Methods Enzymol 316:121-132.
6. Ames JB, Hendricks KB, Strahl T, Huttner IG, Hamasaki N, Thorner J (2000b) Structure and calcium-binding properties of Frq1, a novel calcium sensor in the yeast Saccharomyces cerevisiae. Biochemistry 39:12149-12161.
7. Bock JB, Klumperman J, Davanger S, Scheller RH (1997) Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol Biol Cell 8:1261-1271.
8. Boekhoff I, Braunewell K-H, Andreini I, Breer H, Gundelfinger ED (1997) The calcium-binding protein VILIP in olfactory neurons: Regulation of second messenger signaling. Eur J Cell Biol 72:151-158.
9. Bourne Y, Dannenberg J, Pollmann V, Marchot P, Pongs O (2001) Immunocytochemical localization and crystal structure of human frequenin (neuronal calcium sensor 1). J Biol Chem 276:11949-11955.
10. Braunewell KH, Gundelfinger ED (1997) Low level expression of calcium-sensor protein VILIP induces cAMP-dependent differentiation in rat C6 glioma cells. Neurosci Lett 234:139-142.
11. 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.
12. Braunewell KH, Spilker C, Behnisch T, Gundelfinger ED (1997) The neuronal calcium-sensor protein VILIP modulates cyclic AMP accumulation in stably transfected C6 glioma cells: Amino-terminal myristoylation determines functional activity. J Neurochem 68:2129-2139.
13. Braunewell KH, Brackmann M, Schaupp M, Spilker C, Anand R, Gundelfinger ED (2001a) Intracellular neuronal calcium sensor (NCS) protein VILIP-1 modulates cGMP signalling pathways in transfected neural cells and cerebellar granule neurones. J Neurochem 78:1277-1286.
14. Braunewell KH, Riederer P, Spilker C, Gundelfinger ED, Bogerts B, Bernstein HG (2001b) Abnormal localization of two neuronal calcium sensor proteins, visinin-like proteins (vilips)-1 and -3, in neocortical brain areas of Alzheimer disease patients. Dement Geriatr Cogn Disord 12:110-116.
15. 2+-binding proteins. Biochem J 353:1-12.
16. Casey PJ (1995) Protein lipidation in cell signaling. Science 268:221-225.
17. Doyle DD, Ambler SK, Upshaw-Earley J, Bastawrous A, Goings GE, Page E (1997) Type B atrial natriuretic peptide receptor in cardiac myocyte caveolae. Circ Res 81:86-91.
18. 2+ entry requires localization in cholesterol-rich domains. J Biol Chem 275:26530-26537.
19. Galbiati F, Razani B, Lisanti MP (2001) Emerging themes in lipid rafts and caveolae. Cell 106:403-411.
20. 2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron 30:241-248.
21. Goslin K, Banker G (1998) Rat hippocampal neurons in low-density culture. In: Culturing Nerve Cells, Ed. 2 (Banker G, Goslin K, eds), pp 339-370. Cambridge, MA: MIT.
22. Hendricks KB, Wang BQ, Schnieders EA, Thorner J (1999) Yeast homologue of neuronal frequenin is a regulator of phosphatidylinositol-4-OH kinase. Nat Cell Biol 1:234-241.
23. Herreros J, Ng T, Schiavo G (2001) Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol Biol Cell 12:2947-2960.
24. Kennedy MT, Brockman H, Rusnak F (1996) Contributions of myristoylation to calcineurin structure/function. J Biol Chem 271:26517-26521.
25. Köhrmann M, Haubensak W, Hemraj I, Kaether C, Lessmann VJ, Kiebler MA (1999) Fast, convenient, and effective method to transiently transfect primary hippocampal neurons. J Neurosci Res 58:831-835.
26. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
27. 2+-binding protein VILIP: Interaction with cell membrane and actin-based cytoskeleton. Biochem Biophys Res Commun 225:1078-1083.
28. 2+-influx without disruption of Trp3-inositol trisphosphate receptor association. J Biol Chem 276:42401-42408.
29. Mathisen PM, Johnson JM, Kawczak JA, Tuohy VK (1999) Visinin-like protein (VILIP) is a neuron-specific calcium-dependent double- stranded RNA-binding protein. J Biol Chem 274:31571-31576.
30. 2+ signal transduction. J Biol Chem 274:30258-30265,
31. McLaughlin S, Aderem A (1995) The myristoyl-electrostatic switch: A modulator of reversible protein-membrane interactions. Trends Biochem Sci 20:272-276.
32. Meyer T, York JD (1999) Calcium-myristoyl switches turn on new lights. Nat Cell Biol 1:E93-E95.
33. Orito A, Kumanogoh H, Yasaka K, Sokawa J, Hidaka H, Sokawa Y, Maekawa S (2001) Calcium-dependent association of annexin VI, protein kinase C alpha, and neurocalcin alpha on the raft fraction derived from the synaptic plasma membrane of rat brain. J Neurosci Res 64:235-241.
34. Paterlini M, Revilla V, Grant AL, Wisden W (2000) Expression of the neuronal calcium sensor protein family in the rat brain. Neuroscience 99:205-216.
35. Randazzo PA, Terui T, Sturch S, Fales HM, Ferrige AG, Kahn RA (1995) The myristoylated amino terminus of ADP-ribosylation factor 1 is a phospholipid- and GTP-sensitive switch. J Biol Chem 270:14809-14815.
36. Resh MD (1999) Fatty acylation of proteins: New insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim Biophys Acta 1451:1-16.
37. Schreiber S, Fleischer J, Breer H, Boekhoff I (2000) A possible role for caveolin as a signaling organizer in olfactory sensory membranes. J Biol Chem 275:24115-24123.
38. Spilker C, Richter K, Smalla KH, Manahan-Vaughan D, Gundelfinger ED, Braunewell KH (2000) The neuronal EF-hand calcium-binding protein visinin-like protein-3 is expressed in cerebellar Purkinje cells and shows a calcium-dependent membrane association. Neuroscience 96:121-129.
39. Takasaki A, Hayashi N, Matsubara M, Yamauchi E, Taniguchi H (1999) Identification of the calmodulin-binding domain of neuron-specific protein kinase C substrate protein CAP-22/NAP-22. Direct involvement of protein myristoylation in calmodulin-target protein interaction. J Biol Chem 274:11848-11853.
40. Teruel MN, Meyer T (2000) Translocation and reversible localization of signaling proteins: A dynamic future for signal transduction. Cell 103:181-184.
41. Towler DA, Gordon JI, Adams SP, Glaser L (1988) The biology and enzymology of eukaryotic protein acylation. Annu Rev Biochem 57:69-99.
42. Vijay-Kumar S, Kumar VD (1999) Crystal structure of recombinant bovine neurocalcin. Nat Struct Biol 6:80-88.
43. Weisz OA, Gibson GA, Leung SM, Roder J, Jeromin A (2000) Overexpression of frequenin, a modulator of phosphatidylinositol 4-kinase, inhibits biosynthetic delivery of an apical protein in polarized madindarby canine kidney cells. J Biol Chem 275:24341-24347.
44. Zhao X, Varnai P, Tuymetova G, Balla A, Toth ZE, Oker-Blom C, Roder J, Jeromin A, Balla T (2001) Interaction of neuronal calcium sensor-1 (NCS-1) with phosphatidylinositol 4-kinase beta stimulates lipid kinase activity and affects membrane trafficking in COS-7 cells. J Biol Chem 276:40183-40189.
45. Zozulya S, Stryer L (1992) Calcium-myristoyl protein switch. Proc Natl Acad Sci USA 89:11569-11573.