Binding of αII spectrin to 14-3-3β is involved in NCAM-dependent neurite outgrowth

Molecular and Cellular Neuroscience

Volumn 45, Issue 1, 2010, Pages 66-74

  Ramser, Elisa M ^a   Buck, Friedrich ^a   Schachner, Melitta ^a,b   Tilling, Thomas ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

14 3 3 protein; NCAM; II spectrin

Indexed keywords

ALANINE; ALPHA 2 SPECTRIN; CALMODULIN; CASEIN KINASE II; CYTOSKELETON PROTEIN; NERVE CELL ADHESION MOLECULE; PROTEIN 14 3 3; PROTEIN 14 3 3BETA; SERINE; SPECTRIN; UNCLASSIFIED DRUG; HYBRID PROTEIN; ISOPROTEIN;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOPRECIPITATION; MASS SPECTROMETRY; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; AMINO ACID SEQUENCE; ANIMAL; BRAIN; CELL CULTURE; CYTOLOGY; GENETICS; HIPPOCAMPUS; HUMAN; METABOLISM; NERVE CELL; NEURITE; PROTEIN BINDING;

14-3-3 PROTEINS; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CALMODULIN; CASEIN KINASE II; CELLS, CULTURED; HIPPOCAMPUS; HUMANS; NEURAL CELL ADHESION MOLECULES; NEURITES; NEURONS; PROTEIN BINDING; PROTEIN ISOFORMS; RATS; RECOMBINANT FUSION PROTEINS; SPECTRIN;

EID: 77955091095     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.05.013     Document Type: Article

References (57)

1. Angrand P.O., Segura I., Volkel P., Ghidelli S., Terry R., Brajenovic M., Vintersten K., Klein R., Superti-Furga G., Drewes G., Kuster B., Bouwmeester T., Acker-Palmer A. Transgenic mouse proteomics identifies new 14-3-3-associated proteins involved in cytoskeletal rearrangements and cell signaling. Mol. Cell. Proteomics 2006, 5:2211-2227.
2. Baxter H.C., Liu W.G., Forster J.L., Aitken A., Fraser J.R. Immunolocalisation of 14-3-3 isoforms in normal and scrapie-infected murine brain. Neuroscience 2002, 109:5-14.
3. Beguin P., Mahalakshmi R.N., Nagashima K., Cher D.H., Takahashi A., Yamada Y., Seino Y., Hunziker W. 14-3-3 and calmodulin control subcellular distribution of Kir/Gem and its regulation of cell shape and calcium channel activity. J. Cell Sci. 2005, 118:1923-1934.
4. Bennett V., Baines A.J. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 2001, 81:1353-1392.
5. Bignone P.A., King M.D., Pinder J.C., Baines A.J. Phosphorylation of a threonine unique to the short C-terminal isoform of betaII-spectrin links regulation of alpha-beta spectrin interaction to neuritogenesis. J. Biol. Chem. 2007, 282:888-896.
6. Blichenberg A., Schwanke B., Rehbein M., Garner C.C., Richter D., Kindler S. Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J. Neurosci. 1999, 19:8818-8829.
7. Boston P.F., Jackson P., Thompson R.J. Human 14-3-3 protein: radioimmunoassay, tissue distribution, and cerebrospinal fluid levels in patients with neurological disorders. J. Neurochem. 1982, 38:1475-1482.
8. Chen B.S., Roche K.W. Growth factor-dependent trafficking of cerebellar NMDA receptors via protein kinase B/Akt phosphorylation of NR2C. Neuron 2009, 62:471-478.
9. Chen S., Mantei N., Dong L., Schachner M. Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. J. Neurobiol. 1999, 38:428-439.
10. Coleman T.R., Fishkind D.J., Mooseker M.S., Morrow J.S. Functional diversity among spectrin isoforms. Cell Motil. Cytoskeleton 1989, 12:225-247.
11. Collins M.O., Yu L., Coba M.P., Husi H., Campuzano I., Blackstock W.P., Choudhary J.S., Grant S.G. Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 2005, 280:5972-5982.
12. Combet C., Blanchet C., Geourjon C., Deleage G. NPS@: network protein sequence analysis. Trends Biochem. Sci. 2000, 25:147-150.
13. Couve A., Kittler J.T., Uren J.M., Calver A.R., Pangalos M.N., Walsh F.S., Moss S.J. Association of GABA(B) receptors and members of the 14-3-3 family of signaling proteins. Mol. Cell. Neurosci. 2001, 17:317-328.
14. Darling D.L., Yingling J., Wynshaw-Boris A. Role of 14-3-3 proteins in eukaryotic signaling and development. Curr. Top. Dev. Biol. 2005, 68:281-315.
15. De Matteis M.A., Morrow J.S. The role of ankyrin and spectrin in membrane transport and domain formation. Curr. Opin. Cell Biol. 1998, 10:542-549.
16. Ditlevsen D.K., Povlsen G.K., Berezin V., Bock E. NCAM-induced intracellular signaling revisited. J. Neurosci. Res. 2008, 86:727-743.
17. Dougherty M.K., Morrison D.K. Unlocking the code of 14-3-3. J. Cell Sci. 2004, 117:1875-1884.
18. Ensslen-Craig S.E., Brady-Kalnay S.M. Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev. Biol. 2004, 275:12-22.
19. Fu H., Subramanian R.R., Masters S.C. 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 2000, 40:617-647.
20. Fuhrmann J.C., Kins S., Rostaing P., El Far O., Kirsch J., Sheng M., Triller A., Betz H., Kneussel M. Gephyrin interacts with Dynein light chains 1 and 2, components of motor protein complexes. J. Neurosci. 2002, 22:5393-5402.
21. Gehler S., Shaw A.E., Sarmiere P.D., Bamburg J.R., Letourneau P.C. Brain-derived neurotrophic factor regulation of retinal growth cone filopodial dynamics is mediated through actin depolymerizing factor/cofilin. J. Neurosci. 2004, 24:10741-10749.
22. Goodman S.R., Zimmer W.E., Clark M.B., Zagon I.S., Barker J.E., Bloom M.L. Brain spectrin: of mice and men. Brain Res. Bull. 1995, 36:593-606.
23. Hammarlund M., Davis W.S., Jorgensen E.M. Mutations in beta-spectrin disrupt axon outgrowth and sarcomere structure. J. Cell Biol. 2000, 149:931-942.
24. Harris A.S., Croall D.E., Morrow J.S. The calmodulin-binding site in alpha-fodrin is near the calcium-dependent protease-I cleavage site. J. Biol. Chem. 1988, 263:15754-15761.
25. Harris A.S., Morrow J.S. Calmodulin and calcium-dependent protease I coordinately regulate the interaction of fodrin with actin. Proc Natl Acad Sci U S A 1990, 87:3009-3013.
26. Kajiwara Y., Buxbaum J.D., Grice D.E. SLITRK1 binds 14-3-3 and regulates neurite outgrowth in a phosphorylation-dependent manner. Biol. Psychiatry 2009, 66:918-925.
27. Kleene R., Loers G., Langer J., Frobert Y., Buck F., Schachner M. Prion protein regulates glutamate-dependent lactate transport of astrocytes. J. Neurosci. 2007, 27:12331-12340.
28. Kleene R., Yang H., Kutsche M., Schachner M. The neural recognition molecule L1 is a sialic acid-binding lectin for CD24, which induces promotion and inhibition of neurite outgrowth. J. Biol. Chem. 2001, 276:21656-21663.
29. Lacas-Gervais S., Guo J., Strenzke N., Scarfone E., Kolpe M., Jahkel M., De Camilli P., Moser T., Rasband M.N., Solimena M. BetaIVSigma1 spectrin stabilizes the nodes of Ranvier and axon initial segments. J. Cell Biol. 2004, 166:983-990.
30. Leshchyns'ka I., Sytnyk V., Morrow J.S., Schachner M. Neural cell adhesion molecule (NCAM) association with PKCbeta2 via betaI spectrin is implicated in NCAM-mediated neurite outgrowth. J. Cell Biol. 2003, 161:625-639.
31. Lupas A. Coiled coils: new structures and new functions. Trends Biochem. Sci. 1996, 21:375-382.
32. Malchiodi-Albedi F., Ceccarini M., Winkelmann J.C., Morrow J.S., Petrucci T.C. The 270kDa splice variant of erythrocyte beta-spectrin (beta I sigma 2) segregates in vivo and in vitro to specific domains of cerebellar neurons. J. Cell Sci. 1993, 106(Pt 1):67-78.
33. Muslin A.J., Tanner J.W., Allen P.M., Shaw A.S. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 1996, 84:889-897.
34. Nedrelow J.H., Cianci C.D., Morrow J.S. c-Src binds alpha II spectrin's Src homology 3 (SH3) domain and blocks calpain susceptibility by phosphorylating Tyr1176. J. Biol. Chem. 2003, 278:7735-7741.
35. Neuhoff H., Sassoe-Pognetto M., Panzanelli P., Maas C., Witke W., Kneussel M. The actin-binding protein profilin I is localized at synaptic sites in an activity-regulated manner. Eur. J. Neurosci. 2005, 21:15-25.
36. Nicolas G., Fournier C.M., Galand C., Malbert-Colas L., Bournier O., Kroviarski Y., Bourgeois M., Camonis J.H., Dhermy D., Grandchamp B., Lecomte M.C. Tyrosine phosphorylation regulates alpha II spectrin cleavage by calpain. Mol. Cell. Biol. 2002, 22:3527-3536.
37. Niethammer P., Delling M., Sytnyk V., Dityatev A., Fukami K., Schachner M. Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J. Cell Biol. 2002, 157:521-532.
38. O'Donnell M., Chance R.K., Bashaw G.J. Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 2009, 32:383-412.
39. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., Mann M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
40. Petosa C., Masters S.C., Bankston L.A., Pohl J., Wang B., Fu H., Liddington R.C. 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J. Biol. Chem. 1998, 273:16305-16310.
41. Pinna L.A. Casein kinase 2: an 'eminence grise' in cellular regulation?. Biochim. Biophys. Acta 1990, 1054:267-284.
42. Pollerberg E.G., Sadoul R., Goridis C., Schachner M. Selective expression of the 180-kD component of the neural cell adhesion molecule N-CAM during development. J. Cell Biol. 1985, 101:1921-1929.
43. Pollerberg G.E., Schachner M., Davoust J. Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature 1986, 324:462-465.
44. Purcell A.L., Carew T.J. Tyrosine kinases, synaptic plasticity and memory: insights from vertebrates and invertebrates. Trends Neurosci. 2003, 26:625-630.
45. Rong J., Li S., Sheng G., Wu M., Coblitz B., Li M., Fu H., Li X.J. 14-3-3 protein interacts with Huntingtin-associated protein 1 and regulates its trafficking. J. Biol. Chem. 2007, 282:4748-4756.
46. Simonovic M., Zhang Z., Cianci C.D., Steitz T.A., Morrow J.S. Structure of the calmodulin alphaII-spectrin complex provides insight into the regulation of cell plasticity. J. Biol. Chem. 2006, 281:34333-34340.
47. Simsek-Duran F., Linden D.J., Lonart G. Adapter protein 14-3-3 is required for a presynaptic form of LTP in the cerebellum. Nat. Neurosci. 2004, 7:1296-1298.
48. Skoulakis E.M., Davis R.L. Olfactory learning deficits in mutants for leonardo, a Drosophila gene encoding a 14-3-3 protein. Neuron 1996, 17:931-944.
49. Speicher D.W., Marchesi V.T. Erythrocyte spectrin is comprised of many homologous triple helical segments. Nature 1984, 311:177-180.
50. Sytnyk V., Leshchyns'ka I., Nikonenko A.G., Schachner M. NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J. Cell Biol. 2006, 174:1071-1085.
51. Toyo-oka K., Shionoya A., Gambello M.J., Cardoso C., Leventer R., Ward H.L., Ayala R., Tsai L.H., Dobyns W., Ledbetter D., Hirotsune S., Wynshaw-Boris A. 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat. Genet. 2003, 34:274-285.
52. Wang B., Yang H., Liu Y.C., Jelinek T., Zhang L., Ruoslahti E., Fu H. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 1999, 38:12499-12504.
53. Wang K.K., Posmantur R., Nath R., McGinnis K., Whitton M., Talanian R.V., Glantz S.B., Morrow J.S. Simultaneous degradation of alphaII- and betaII-spectrin by caspase 3 (CPP32) in apoptotic cells. J. Biol. Chem. 1998, 273:22490-22497.
54. Wayman G.A., Lee Y.S., Tokumitsu H., Silva A., Soderling T.R. Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 2008, 59:914-931.
55. Wechsler A., Teichberg V.I. Brain spectrin binding to the NMDA receptor is regulated by phosphorylation, calcium and calmodulin. EMBO J. 1998, 17:3931-3939.
56. Yaffe M.B., Rittinger K., Volinia S., Caron P.R., Aitken A., Leffers H., Gamblin S.J., Smerdon S.J., Cantley L.C. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 1997, 91:961-971.
57. Yang Y., Lacas-Gervais S., Morest D.K., Solimena M., Rasband M.N. BetaIV spectrins are essential for membrane stability and the molecular organization of nodes of Ranvier. J. Neurosci. 2004, 24:7230-7240.