δ-catenin/NPRAP: A new member of the glycogen synthase kinase-3β signaling complex that promotes β-catenin turnover in neurons

Journal of Neuroscience Research

Volumn 88, Issue 11, 2010, Pages 2350-2363

  Bareiss, Sonja ^a   Kim, Kwonseop ^a,b   Lu, Qun ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b Chonnam National University   (South Korea)

Author keywords

catenin; catenin NPRAP; Glycogen synthase kinase 3 ; Proteasome; Ubiquitination

Indexed keywords

APC PROTEIN; BETA CATENIN; CATENIN; CYCLOHEXIMIDE; DELTA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; NPRAP PROTEIN; UNCLASSIFIED DRUG; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL STRAIN; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; HYPOTHESIS; IMMUNOREACTIVITY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN STABILITY; RAT; SIGNAL TRANSDUCTION; UBIQUITINATION; 3T3 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL LINE; GENETIC TRANSFECTION; HALF LIFE TIME; IMMUNOPRECIPITATION; MALE; METABOLISM; MOUSE; PC12 CELL LINE; PHYSIOLOGY; WESTERN BLOTTING;

3T3 CELLS; ANIMALS; BETA CATENIN; BLOTTING, WESTERN; CATENINS; CELL LINE; CELLS, CULTURED; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HALF-LIFE; IMMUNOPRECIPITATION; MALE; MICE; MICROSCOPY, FLUORESCENCE; NEURONS; PC12 CELLS; RATS; SIGNAL TRANSDUCTION; TRANSFECTION; UBIQUITINATION;

EID: 77955349622     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22414     Document Type: Article

References (69)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. 1997. Beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804.
2. Abu-Elneel K, Ochiishi T, Medina M, Remedi M, Gastaldi L, Caceres A, Kosik K. 2008. A delta-catenin signaling pathway leading to dendritic protrusions. J Biol Chem 283:32781-32791.
3. Alvarez A, Toro R, Caceres A, Maccioni RB. 1999. Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett 459:421-426. (Pubitemid 29467380)
4. Arikkath J, Israely I, Tao Y, Mei L, Xin L, Reichardt L. 2008. Erbin controls dendritic morphogenesis by regulatin localization of δ-catenin. J Neurosci 28:7047-7056.
5. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. 1996. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382:638-642.
6. Bingol B.Schuman EM. 2005. Synaptic protein degradation by the ubiquitin proteasome system. Curr Opin Neurobiol 15:536-541. (Pubitemid 41394397)
7. Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW. 2000. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28:245-259.
8. Cadigan KM, Nusse R. 1997. Wnt signaling: a common theme in animal development. Genes Dev 11:3286-3305.
9. Fuentealba RA, Farias G, Scheu J, Bronfman M, Marzolo MP, Inestrosa NC. 2004. Signal transduction during amyloid-beta-peptide neurotoxicity: role in Alzheimer disease. Brain Res Brain Res Rev 47:275-289. (Pubitemid 39574325)
10. Georgakopoulos A, Marambaud P, Efthimiopoulos S, Shioi J, Cui W, Li HC, Schutte M, Gordon R, Holstein GR, Martinelli G, Mehta P, Friedrich VL Jr, Robakis NK. 1999. Presenilin-1 forms complexes with the cadherin/catenin cell-cell adhesion system and is recruited to intercellular and synaptic contacts. Mol Cell 4:893-902.
11. Goslin K, Asmussen H, Banker G. 1998. Rat hippocampal neurons in low density culture. Boston: MIT. p 339-370.
12. Grimes CA, Jope RS. 2001. CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J Neurochem 78:1219-1232.
13. Grosheva I, Shtutman M, Elbaum M, Bershadsky AD. 2001. p120 Catenin affects cell motility via modulation of activity of Rho-family GTPases: a link between cell-cell contact formation and regulation of cell locomotion. J Cell Sci 114:695-707. (Pubitemid 32237142)
14. Ha NC, Tonozuka T, Stamos JL, Choi HJ, Weis WI. 2004. Mechanism of phosphorylation-dependent binding of APC to beta-catenin and its role in beta-catenin degradation. Mol Cell 15:511-521.
15. Hart MJ, de los SR, Albert IN, Rubinfeld B, Polakis P. 1998. Downregulation of beta-catenin by human axin and its association with the APC tumor suppressor, beta-catenin and GSK3 beta. Curr Biol 8:573-581.
16. Hatzfeld M, Nachtsheim C. 1996. Cloning and characterization of a new armadillo family member, p0071, associated with the junctional plaque: evidence for a subfamily of closely related proteins. J Cell Sci 109:2767-2778.
17. Ho C, Zhou J, Medina M, Goto T, Jacobson M, Bhide PG, Kosik KS. 2000. Delta-catenin is a nervous system-specific adherens junction protein which undergoes dynamic relocalization during development. J Comp Neurol 420:261-276. (Pubitemid 30185982)
18. Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R. 1996. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev 59:3-10.
19. Ide N, Hata Y, Deguchi M, Hirao K, Yao I, Takai Y. 1999. Interaction of S-SCAM with neural plakophilin-related armadillo-repeat protein/ delta-catenin. Biochem Biophys Res Commun 256:456-461.
20. Israely I, Costa RM, Xie CW, Silva AJ, Kosik KS, Liu X. 2004. Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction. Curr Biol 14:1657-1663.
21. Jones SB, Lanford GW, Chen YH, Morabito M, Kim K, Lu Q. 2002. Glutamate-induced delta-catenin redistribution and dissociation from postsynaptic receptor complexes. Neuroscience 115:1009-1021.
22. Kaether C, Haass C, Steiner H. 2006. Assembly, trafficking and function of gamma-secretase. Neurodegen Dis 3:275-283.
23. Kang DE, Soriano S, Frosch MP, Collins T, Naruse S, Sisodia SS, Leibowitz G, Levine F, Koo EH. 1999. Presenilin 1 facilitates the constitutive turnover of beta-catenin: differential activity of Alzheimer's disease-linked PS1 mutants in the beta-catenin-signaling pathway. J Neurosci 19:4229-4237. (Pubitemid 29241077)
24. Kim H, Han JR, Park J, Oh M, James SE, Chang S, Lu Q, Lee KY, Ki H, Song WJ, Kim K. 2008. Delta-catenin-induced dendritic morphogenesis. An essential role of p190RhoGEF interaction through Akt1-mediated phosphorylation. J Biol Chem 283:977-987.
25. Kim JS, Bareiss S, Kim KK, Tatum R, Han JR, Jin YH, Kim H, Lu Q, Kim K. 2006. Presenilin-1 inhibits delta-catenin-induced cellular branching and promotes delta-catenin processing and turnover. Biochem Biophys Res Commun 351:903-908.
26. Kim K, Sirota A, Chen YH, Jones SB, Dudek R, Lanford GW, Thakore C, Lu Q. 2002. Dendrite-like process formation and cytoskeletal remodeling regulated by delta-catenin expression. Exp Cell Res 275:171-184. (Pubitemid 34948360)
27. Kim WY, Zhou FQ, Zhou J, Yokota Y, Wang YM, Yoshimura T, Kaibuchi K, Woodgett JR, Anton ES, Snider WD. 2006. Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52:981-996.
28. Krylova O, Herreros J, Cleverley KE, Ehler E, Henriquez JP, Hughes SM, Salinas PC. 2002. WNT-3, expressed by motoneurons, regulates terminal arborization of neurotrophin-3-responsive spinal sensory neurons. Neuron 35:1043-1056.
29. Leroy K, Brion JP. 1999. Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J Chem Neuroanat 16:279-293. (Pubitemid 29296952)
30. Levesque G, Yu G, Nishimura M, Zhang DM, Levesque L, Yu H, Xu D, Liang Y, Rogaeva E, Ikeda M, Duthie M, Murgolo N, Wang L, VanderVere P, Bayne ML, Strader CD, Rommens JM, Fraser PE, St. George-Hyslop P. 1999. Presenilins interact with armadillo proteins including neural-specific plakophilin-related protein and beta-catenin. J Neurochem 72:999-1008.
31. Lu Q, Paredes M, Medina M, Zhou J, Cavallo R, Peifer M, Orecchio L, Kosik KS. 1999. Delta-catenin, an adhesive junction-associated protein which promotes cell scattering. J Cell Biol 144:519-532.
32. Lu Q, Mukhopadhyay NK, Griffin JD, Paredes M, Medina M, Kosik KS. 2002. Brain armadillo protein delta-catenin interacts with Abl tyrosine kinase and modulates cellular morphogenesis in response to growth factors. J Neurosci Res 67:618-624.
33. Martinez MC, Ochiishi T, Majewski M, Kosik KS. 2003. Dual regulation of neuronal morphogenesis by a delta-catenin-cortactin complex and Rho. J Cell Biol 162:99-111. (Pubitemid 36859538)
34. Medina M, Marinescu RC, Overhauser J, Kosik KS. 2000. Hemizygosity of delta-catenin (CTNND2) is associated with severe mental retardation in cri-du-chat syndrome. Genomics 63:157-164.
35. Meijer L, Flajolet M, Greengard P. 2004. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol Sci 25:471-480.
36. Molenaar M, van de WM, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destree O, Clevers H. 1996. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86:391-399.
37. Morrison EE, Askham J, Clissold P, Markham AF, Meredith DM. 1997. Expression of beta-catenin and the adenomatous polyposis coli tumour suppressor protein in mouse neocortical cells in vitro. Neurosci Lett 235:129-132. (Pubitemid 27501669)
38. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P. 1995. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A 92:3046-3050.
39. Munoz-Montano JR, Lim F, Moreno FJ, Avila J, az-Nido J. 1999. Glycogen synthase kinase-3 modulates neurite outgrowth in cultured neurons: possible implications for neurite pathology in Alzheimer's disease. J Alzheimers Dis 1:361-378.
40. Murase S, Mosser E, Schuman EM. 2002. Depolarization drives beta-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35:91-105. (Pubitemid 34804325)
41. Murayama O, Honda T, Mercken M, Murayama M, Yasutake K, Nihonmatsu N, Nakazato Y, Michel G, Song S, Sato K, Takahashi H, Takashima A. 1997. Different effects of Alzheimer-associated mutations of presenilin 1 on its processing. Neurosci Lett 229:61-64.
42. Paffenholz R, Franke WW. 1997. Identification and localization of a neurally expressed member of the plakoglobin/armadillo multigene family. Differentiation 61:293-304.
43. Peifer M, Polakis P. 2000. Wnt signaling in oncogenesis and embryogenesis - a look outside the nucleus. Science 287:1606-1609. (Pubitemid 30127755)
44. Peifer M, Berg S, Reynolds AB. 1994a. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789-791.
45. Peifer M, Pai LM, Casey M. 1994b. Phosphorylation of the Drosophila adherens junction protein armadillo: roles for wingless signal and zeste-white 3 kinase. Dev Biol 166:543-556.
46. Peifer M, Sweeton D, Casey M, Wieschaus E. 1994c. wingless Signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of armadillo. Development 120:369-380. (Pubitemid 24042404)
47. Polakis P. 2000. Wnt signaling and cancer. Genes Dev 14:1837-1851.
48. Pollack AL, Barth AI, Altschuler Y, Nelson WJ, Mostov KE. 1997. Dynamics of beta-catenin interactions with APC protein regulate epithelial tubulogenesis. J Cell Biol 137:1651-1662.
49. Prager K, Wang-Eckhardt L, Fluhrer R, Killick R, Barth E, Hampel H, Haass C, Walter J. 2007. A structural switch of presenilin 1 by glycogen synthase kinase 3beta-mediated phosphorylation regulates the interaction with beta-catenin and its nuclear signaling. J Biol Chem 282:14083-14093.
50. Rubinfeld B, Souza B, Albert I, Munemitsu S, Polakis P. 1995. The APC protein and E-cadherin form similar but independent complexes with alpha-catenin, beta-catenin, and plakoglobin. J Biol Chem 270:5549-5555.
51. Rubinfeld B, Albert I, Porfiri E, Fiol C, Munemitsu S, Polakis P. 1996. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272:1023-1026.
52. Sakanaka C, Weiss JB, Williams LT. 1998. Bridging of beta-catenin and glycogen synthase kinase-3beta by axin and inhibition of beta-catenin-mediated transcription. Proc Natl Acad Sci U S A 95:3020-3023. (Pubitemid 28135847)
53. Shimomura A, Kohu K, Akiyama T, Senda T. 2005. Subcellular localization of the tumor suppressor protein APC in developing cultured neurons. Neurosci Lett 375:81-86.
54. Stambolic V, Woodgett JR. 1994. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem J 303:701-704.
55. Takahashi M, Yasutake K, Tomizawa K. 1999. Lithium inhibits neurite growth and tau protein kinase I/glycogen synthase kinase-3beta-dependent phosphorylation of juvenile tau in cultured hippocampal neurons. J Neurochem 73:2073-2083.
56. Takashima A, Noguchi K, Michel G, Mercken M, Hoshi M, Ishiguro K, Imahori K. 1996. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3 beta. Neurosci Lett 203:33-36.
57. Takashima A, Murayama M, Murayama O, Kohno T, Honda T, Yasutake K, Nihonmatsu N, Mercken M, Yamaguchi H, Sugihara S, Wolozin B. 1998. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc Natl Acad Sci U S A 95:9637-9641. (Pubitemid 28506284)
58. Tanahashi H, Tabira T. 1999. Isolation of human delta-catenin and its binding specificity with presenilin 1. Neuroreport 10:563-568.
59. Tatebayashi Y, Haque N, Tung YC, Iqbal K, Grundke-Iqbal I. 2004. Role of tau phosphorylation by glycogen synthase kinase-3beta in the regulation of organelle transport. J Cell Sci 117:1653-1663.
60. Twomey C, McCarthy JV. 2006. Presenilin-1 is an unprimed glycogen synthase kinase-3beta substrate. FEBS Lett 580:4015-4020.
61. Votin V, Nelson WJ, Barth AI. 2005. Neurite outgrowth involves adenomatous polyposis coli protein and beta-catenin. J Cell Sci 118:5699-5708.
62. Woodgett JR. 2001. Judging a protein by more than its name: GSK-3. Sci STKE 2001:RE12.
63. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. 1996. The axis-inducing activity, stability, and subcellular distribution of betacatenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10:1443-1454. (Pubitemid 26260702)
64. Yu G, Chen F, Levesque G, Nishimura M, Zhang DM, Levesque L, Rogaeva E, Xu D, Liang Y, Duthie M, St. George-Hyslop PH, Fraser PE. 1998. The presenilin 1 protein is a component of a high molecular weight intracellular complex that contains beta-catenin. J Biol Chem 273:16470-16475.
65. Yu X, Malenka RC. 2003. Beta-catenin is critical for dendritic morphogenesis. Nat Neurosci 6:1169-1177.
66. Zhang Z, Hartmann H, Do VM, Abramowski D, Sturchler-Pierrat C, Staufenbiel M, Sommer B, van de WM, Clevers H, Saftig P, De SB, He X, Yankner BA. 1998. Destabilization of beta-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 395:698-702.
67. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD. 2004. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897-912.
68. Zhou J, Liyanage U, Medina M, Ho C, Simmons AD, Lovett M, Kosik KS. 1997. Presenilin 1 interaction in the brain with a novel member of the armadillo family. Neuroreport 8:2085-2090. (Pubitemid 27314338)
69. Zumbrunn J, Kinoshita K, Hyman AA, Nathke IS. 2001. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr Biol 11:44-49. (Pubitemid 32062715)