Presynaptic CK2 promotes synapse organization and stability by targeting Ankyrin2

Journal of Cell Biology

Volumn 204, Issue 1, 2014, Pages 77-94

  Bulat, Victoria ^a,b   Rast, Melanie ^a,b   Pielage, Jan ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN2 PROTEIN; CASEIN KINASE II; CELL ADHESION MOLECULE; HOLOENZYME; PHOSPHATASE; PHOSPHOLIPID; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME STABILITY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MASS SPECTROMETRY; MOTONEURON; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REGULATORY MECHANISM; SYNAPSE; SYNAPTOSOME; WESTERN BLOTTING;

ANIMALS; ANKYRINS; CASEIN KINASE II; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; PHOSPHOLIPIDS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84891895993     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201305134     Document Type: Article

References (67)

1. Akten, B., E. Jauch, G.K. Genova, E.Y. Kim, I. Edery, T. Raabe, and F.R. Jackson. 2003. A role for CK2 in the Drosophila circadian oscillator. Nat. Neurosci. 6:251-257. http://dx.doi.org/10.1038/nn1007
2. Alvarez, V.A., and B.L. Sabatini. 2007. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 30:79-97. http://dx.doi.org/10.1146/annurev.neuro.30.051606.094222
3. Bednarek, E., and P. Caroni. 2011. β-Adducin is required for stable assembly of new synapses and improved memory upon environmental enrichment. Neuron. 69:1132-1146. http://dx.doi.org/10.1016/j.neuron.2011.02.034
4. Berger, J., K.A. Senti, G. Senti, T.P. Newsome, B. Asling, B.J. Dickson, and T. Suzuki. 2008. Systematic identification of genes that regulate neuronal wiring in the Drosophila visual system. PLoS Genet. 4:e1000085. http://dx.doi.org/10.1371/journal.pgen.1000085
5. Bischof, J., R.K. Maeda, M. Hediger, F. Karch, and K. Basler. 2007. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA. 104:3312-3317. http://dx.doi.org/10.1073/pnas.0611511104
6. Blanquet, P.R. 2000. Casein kinase 2 as a potentially important enzyme in the nervous system. Prog. Neurobiol. 60:211-246. http://dx.doi.org/10.1016/S0301-0082(99)00026-X
7. Brachet, A., C. Leterrier, M. Irondelle, M.-P. Fache, V. Racine, J.-B. Sibarita, D. Choquet, and B. Dargent. 2010. Ankyrin G restricts ion channel diffusion at the axonal initial segment before the establishment of the diffusion barrier. J. Cell Biol. 191:383-395. http://dx.doi.org/10.1083/jcb.201003042
8. Brechet, A., M.-P. Fache, A. Brachet, G. Ferracci, A. Baude, M. Irondelle, S. Pereira, C. Leterrier, and B. Dargent. 2008. Protein kinase CK2 contributes to the organization of sodium channels in axonal membranes by regulating their interactions with ankyrin G. J. Cell Biol. 183:1101-1114. http://dx.doi.org/10.1083/jcb.200805169
9. Buchou, T., M. Vernet, O. Blond, H.H. Jensen, H. Pointu, B.B. Olsen, C. Cochet, O.-G. Issinger, and B. Boldyreff. 2003. Disruption of the regulatory beta subunit of protein kinase CK2 in mice leads to a cell-autonomous defect and early embryonic lethality. Mol. Cell. Biol. 23:908-915. http://dx.doi.org/10.1128/MCB.23.3.908-915.2003
10. Budnik, V., Y.H. Koh, B. Guan, B. Hartmann, C. Hough, D. Woods, and M. Gorczyca. 1996. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron. 17:627-640. http://dx.doi.org/10.1016/S0896-6273(00)80196-8
11. Caroni, P., F. Donato, and D. Muller. 2012. Structural plasticity upon learning: regulation and functions. Nat. Rev. Neurosci. 13:478-490. http://dx.doi.org/10.1038/nrn3258
12. Charriaut-Marlangue, C., S. Otani, C. Creuzet, Y. Ben-Ari, and J. Loeb. 1991. Rapid activation of hippocampal casein kinase II during long-term potentiation. Proc. Natl. Acad. Sci. USA. 88:10232-10236. http://dx.doi.org/10.1073/pnas.88.22.10232
13. Cheusova, T., M.A. Khan, S.W. Schubert, A.-C. Gavin, T. Buchou, G. Jacob, H. Sticht, J. Allende, B. Boldyreff, H.R. Brenner, and S. Hashemolhosseini. 2006. Casein kinase 2-dependent serine phosphorylation of MuSK regulates acetylcholine receptor aggregation at the neuromuscular junction. Genes Dev. 20:1800-1816. http://dx.doi.org/10.1101/gad.375206
14. Chung, H.J., Y.H. Huang, L.-F. Lau, and R.L. Huganir. 2004. Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. J. Neurosci. 24:10248-10259. http://dx.doi.org/10.1523/JNEUROSCI.0546-04.2004
15. Cuesto, G., L. Enriquez-Barreto, C. Carames, M. Cantarero, X. Gasull, C. Sandi, A. Ferrus, A. Acebes, and M. Morales. 2011. Phosphoinositide-3-kinase activation controls synaptogenesis and spinogenesis in hippocampal neurons. J. Neurosci. 31:2721-2733. http://dx.doi.org/10.1523/JNEUROSCI.4477-10.2011
16. Dietzl, G., D. Chen, F. Schnorrer, K.C. Su, Y. Barinova, M. Fellner, B. Gasser, K. Kinsey, S. Oppel, S. Scheiblauer, et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature. 448:151-156. http://dx.doi.org/10.1038/nature05954
17. Di Paolo, G., and P. De Camilli. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature. 443:651-657. http://dx.doi.org/10.1038/nature05185
18. Eaton, B.A., and G.W. Davis. 2005. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron. 47:695-708. http://dx.doi.org/10.1016/j.neuron.2005.08.010
19. Eaton, B.A., R.D. Fetter, and G.W. Davis. 2002. Dynactin is necessary for synapse stabilization. Neuron. 34:729-741. http://dx.doi.org/10.1016/S0896-6273(02)00721-3
20. Enneking, E.-M., S.R. Kudumala, E. Moreno, R. Stephan, J. Boerner, T.A. Godenschwege, and J. Pielage. 2013. Transsynaptic coordination of synaptic growth, function, and stability by the L1-type CAM Neuroglian. PLoS Biol. 11:e1001537. http://dx.doi.org/10.1371/journal.pbio.1001537
21. Frere, S.G., B. Chang-Ileto, and G. Di Paolo. 2012. Role of phosphoinositides at the neuronal synapse. Subcell. Biochem. 59:131-175. http://dx.doi.org/10.1007/978-94-007-3015-1_5
22. Fu, M., X. Yu, J. Lu, and Y. Zuo. 2012. Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature. 483:92-95. http://dx.doi.org/10.1038/nature10844
23. Grillo, F.W., S. Song, L.M. Teles-Grilo Ruivo, L. Huang, G. Gao, G.W. Knott, B. Maco, V. Ferretti, D. Thompson, G.E. Little, and V. De Paola. 2013. Increased axonal bouton dynamics in the aging mouse cortex. Proc. Natl. Acad. Sci. USA. 110:E1514-E1523. http://dx.doi.org/10.1073/pnas.1218731110
24. Hafezparast, M., R. Klocke, C. Ruhrberg, A. Marquardt, A. Ahmad-Annuar, S. Bowen, G. Lalli, A.S. Witherden, H. Hummerich, S. Nicholson, et al. 2003. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science. 300:808-812. http://dx.doi.org/10.1126/science.1083129
25. Hannus, M., F. Feiguin, C.P. Heisenberg, and S. Eaton. 2002. Planar cell polarization requires Widerborst, a B' regulatory subunit of protein phosphatase 2A. Development. 129:3493-3503.
26. Heriche, J.K., F. Lebrin, T. Rabilloud, D. Leroy, E.M. Chambaz, and Y. Goldberg. 1997. Regulation of protein phosphatase 2A by direct interaction with casein kinase 2alpha. Science. 276:952-955. http://dx.doi.org/10.1126/science.276.5314.952
27. Holtmaat, A., and K. Svoboda. 2009. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 10:647-658. http://dx.doi.org/10.1038/nrn2699
28. Hortsch, M., A.J. Bieber, N.H. Patel, and C.S. Goodman. 1990. Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron. 4:697-709. http://dx.doi.org/10.1016/0896-6273(90)90196-M
29. Huang, H.-D., T.-Y. Lee, S.-W. Tzeng, and J.-T. Horng. 2005. KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites. Nucleic Acids Res. 33(Web Server issue):W226-W229. http://dx.doi.org/10.1093/nar/gki471
30. Huillard, E., L. Ziercher, O. Blond, M. Wong, J.-C. Deloulme, S. Souchelnytskyi, J. Baudier, C. Cochet, and T. Buchou. 2010. Disruption of CK2beta in embryonic neural stem cells compromises proliferation and oligodendrogenesis in the mouse telencephalon. Mol. Cell. Biol. 30:2737-2749. http://dx.doi.org/10.1128/MCB.01566-09
31. Ikeda, Y., K.A. Dick, M.R. Weatherspoon, D. Gincel, K.R. Armbrust, J.C. Dalton, G. Stevanin, A. Durr, C. Zuhlke, K. Burk, et al. 2006. Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet. 38:184-190. http://dx.doi.org/10.1038/ng1728
32. Jauch, E., J. Melzig, M. Brkulj, and T. Raabe. 2002. In vivo functional analysis of Drosophila protein kinase casein kinase 2 (CK2) beta-subunit. Gene. 298:29-39. http://dx.doi.org/10.1016/S0378-1119(02)00921-6
33. Jenkins, S.M., and V. Bennett. 2001. Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155:739-746. http://dx.doi.org/10.1083/jcb.200109026
34. Khuong, T.M., R.L. Habets, J.R. Slabbaert, and P. Verstreken. 2010. WASP is activated by phosphatidylinositol-4,5-bisphosphate to restrict synapse growth in a pathway parallel to bone morphogenetic protein signaling. Proc. Natl. Acad. Sci. USA. 107:17379-17384. http://dx.doi.org/10.1073/pnas.1001794107
35. Klagges, B.R., G. Heimbeck, T.A. Godenschwege, A. Hofbauer, G.O. Pflugfelder, R. Reifegerste, D. Reisch, M. Schaupp, S. Buchner, and E. Buchner. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J. Neurosci. 16:3154-3165.
36. Koch, I., H. Schwarz, D. Beuchle, B. Goellner, M. Langegger, and H. Aberle. 2008. Drosophila ankyrin 2 is required for synaptic stability. Neuron. 58:210-222. http://dx.doi.org/10.1016/j.neuron.2008.03.019
37. Lee, T., and L. Luo. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 22:451-461. http://dx.doi.org/10.1016/S0896-6273(00)80701-1
38. Lin, D.M., and C.S. Goodman. 1994. Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron. 13:507-523. http://dx.doi.org/10.1016/0896-6273(94)90022-1
39. Lin, J.-M., V.L. Kilman, K. Keegan, B. Paddock, M. Emery-Le, M. Rosbash, and R. Allada. 2002. A role for casein kinase 2alpha in the Drosophila circadian clock. Nature. 420:816-820. http://dx.doi.org/10.1038/nature01235
40. Litchfield, D.W. 2003. Protein kinase CK2: structure, regulation and role in cellular decisions of life and death. Biochem. J. 369:1-15. http://dx.doi.org/10.1042/BJ20021469
41. Lou, D.Y., I. Dominguez, P. Toselli, E. Landesman-Bollag, C. O'Brien, and D.C. Seldin. 2008. The alpha catalytic subunit of protein kinase CK2 is required for mouse embryonic development. Mol. Cell. Biol. 28:131-139. http://dx.doi.org/10.1128/MCB.01119-07
42. Martin-Pena, A., A. Acebes, J.-R. Rodriguez, A. Sorribes, G.G. de Polavieja, P. Fernandez-Funez, and A. Ferrus. 2006. Age-independent synaptogenesis by phosphoinositide 3 kinase. J. Neurosci. 26:10199-10208. http://dx.doi.org/10.1523/JNEUROSCI.1223-06.2006
43. Meggio, F., and L.A. Pinna. 2003. One-thousand-and-one substrates of protein kinase CK2? FASEB J. 17:349-368. http://dx.doi.org/10.1096/fj.02-0473rev
44. Murray, L.M., K. Talbot, and T.H. Gillingwater. 2010. Review: neuromuscular synaptic vulnerability in motor neurone disease: amyotrophic lateral sclerosis and spinal muscular atrophy. Neuropathol. Appl. Neurobiol. 36:133-156.
45. Niefind, K., J. Raaf, and O.-G. Issinger. 2009. Protein kinase CK2 in health and disease: Protein kinase CK2: from structures to insights. Cell. Mol. Life Sci. 66:1800-1816. http://dx.doi.org/10.1007/s00018-009-9149-8
46. Penner, C.G., Z. Wang, and D.W. Litchfield. 1997. Expression and localization of epitope-tagged protein kinase CK2. J. Cell. Biochem. 64:525-537. http://dx.doi.org/10.1002/(SICI)1097-4644(19970315)64:4<525::AID-JCB1>3.0.CO;2-T
47. Pielage, J., R.D. Fetter, and G.W. Davis. 2005. Presynaptic spectrin is essential for synapse stabilization. Curr. Biol. 15:918-928. http://dx.doi.org/10.1016/j.cub.2005.04.030
48. Pielage, J., L. Cheng, R.D. Fetter, P.M. Carlton, J.W. Sedat, and G.W. Davis. 2008. A presynaptic giant ankyrin stabilizes the NMJ through regulation of presynaptic microtubules and transsynaptic cell adhesion. Neuron. 58:195-209. http://dx.doi.org/10.1016/j.neuron.2008.02.017
49. Pielage, J., V. Bulat, J.B. Zuchero, R.D. Fetter, and G.W. Davis. 2011. Hts/Adducin controls synaptic elaboration and elimination. Neuron. 69:1114-1131. http://dx.doi.org/10.1016/j.neuron.2011.02.007
50. Raaf, J., N. Bischoff, K. Klopffleisch, E. Brunstein, B.B. Olsen, G. Vilk, D.W. Litchfield, O.-G. Issinger, and K. Niefind. 2011. Interaction between CK2α and CK2β, the subunits of protein kinase CK2: thermodynamic contributions of key residues on the CK2α surface. Biochemistry. 50:512-522. http://dx.doi.org/10.1021/bi1013563
51. Roos, J., T. Hummel, N. Ng, C. Klambt, and G.W. Davis. 2000. Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron. 26:371-382. http://dx.doi.org/10.1016/S0896-6273(00)81170-8
52. Salvi, M., S. Sarno, O. Marin, F. Meggio, E. Itarte, and L.A. Pinna. 2006. Discrimination between the activity of protein kinase CK2 holoenzyme and its catalytic subunits. FEBS Lett. 580:3948-3952. http://dx.doi.org/10.1016/j.febslet.2006.06.031
53. Sanz-Clemente, A., J.A. Matta, J.T.R. Isaac, and K.W. Roche. 2010. Casein kinase 2 regulates the NR2 subunit composition of synaptic NMDA receptors. Neuron. 67:984-996. http://dx.doi.org/10.1016/j.neuron.2010.08.011
54. Sarno, S., H. Reddy, F. Meggio, M. Ruzzene, S.P. Davies, A. Donella- Deana, D. Shugar, and L.A. Pinna. 2001. Selectivity of 4,5,6,7-tetrabromobenzotriazole, an ATP site-directed inhibitor of protein kinase CK2 ('casein kinase-2'). FEBS Lett. 496:44-48. http://dx.doi.org/10.1016/S0014-5793(01)02404-8
55. Saxena, S., and P. Caroni. 2007. Mechanisms of axon degeneration: from development to disease. Prog. Neurobiol. 83:174-191. http://dx.doi.org/10.1016/j.pneurobio.2007.07.007
56. Saxena, A., R. Padmanabha, and C.V. Glover. 1987. Isolation and sequencing of cDNA clones encoding alpha and beta subunits of Drosophila melanogaster casein kinase II. Mol. Cell. Biol. 7:3409-3417.
57. Schuldiner, O., D. Berdnik, J.M. Levy, J.S. Wu, D. Luginbuhl, A.C. Gontang, and L. Luo. 2008. piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev. Cell. 14:227-238. http://dx.doi.org/10.1016/j.devcel.2007.11.001
58. Schuster, C.M., G.W. Davis, R.D. Fetter, and C.S. Goodman. 1996. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron. 17:641-654. http://dx.doi.org/10.1016/S0896-6273(00)80197-X
59. Seldin, D.C., D.Y. Lou, P. Toselli, E. Landesman-Bollag, and I. Dominguez. 2008. Gene targeting of CK2 catalytic subunits. Mol. Cell. Biochem. 316:141-147. http://dx.doi.org/10.1007/s11010-008-9811-8
60. Trembley, J.H., G. Wang, G. Unger, J. Slaton, and K. Ahmed. 2009. Protein kinase CK2 in health and disease: CK2: a key player in cancer biology. Cell. Mol. Life Sci. 66:1858-1867.
61. Viquez, N.M., P. Fuger, V. Valakh, R.W. Daniels, T.M. Rasse, and A. DiAntonio. 2009. PP2A and GSK-3beta act antagonistically to regulate active zone development. J. Neurosci. 29:11484-11494. http://dx.doi.org/10.1523/JNEUROSCI.5584-08.2009
62. Wagh, D.A., T.M. Rasse, E. Asan, A. Hofbauer, I. Schwenkert, H. Durrbeck, S. Buchner, M.C. Dabauvalle, M. Schmidt, G. Qin, et al. 2006. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron. 49:833-844. http://dx.doi.org/10.1016/j.neuron.2006.02.008
63. Wodarz, A., U. Hinz, M. Engelbert, and E. Knust. 1995. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell. 82:67-76. http://dx.doi.org/10.1016/0092-8674(95)90053-5
64. Wong, E.V., A.W. Schaefer, G. Landreth, and V. Lemmon. 1996. Casein kinase II phosphorylates the neural cell adhesion molecule L1. J. Neurochem. 66:779-786. http://dx.doi.org/10.1046/j.1471-4159.1996.66020779.x
65. Xu, T., and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 117:1223-1237.
66. Xu, T., X. Yu, A.J. Perlik, W.F. Tobin, J.A. Zweig, K. Tennant, T. Jones, and Y. Zuo. 2009. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature. 462:915-919. http://dx.doi.org/10.1038/nature08389
67. Yang, G., F. Pan, and W.-B. Gan. 2009. Stably maintained dendritic spines are associated with lifelong memories. Nature. 462:920-924. http://dx.doi.org/10.1038/nature08577