Linkage of N-cadherin to multiple cytoskeletal elements revealed by a proteomic approach in hippocampal neurons

Neurochemistry International

Volumn 61, Issue 2, 2012, Pages 240-250

  Tanaka, Hidekazu ^a   Takafuji, Kazuaki ^a   Taguchi, Akihiko ^b   Wiriyasermkul, Pattama ^a   Ohgaki, Ryuichi ^a   Nagamori, Shushi ^a   Suh, Pann Ghill ^c   Kanai, Yoshikatsu ^a  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^b INSTITUTE OF BIOMEDICAL RESEARCH AND INNOVATION   (Japan)

^c Ulsan National Institute of Science and Technology   (South Korea)

Author keywords

Adhesion; Cadherin; Cytoskeleton; Hippocampus; Plasticity; Synapse

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM) INHIBITOR; ALPHA ACTININ 4; ALPHA CATENIN; BETA CATENIN; DESMOPLAKIN; DYNEIN ADENOSINE TRIPHOSPHATASE; F ACTIN; INTEGRIN; MOLECULAR SCAFFOLD; NERVE CELL ADHESION MOLECULE; PLAKOGLOBIN; PLAKOPHILIN; SPECTRIN; TRITON X 100;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; HIPPOCAMPUS; IMMUNOPRECIPITATION; LINKAGE ANALYSIS; MEMBRANE DEPOLARIZATION; MICROTUBULE; MOLECULAR WEIGHT; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN TRANSPORT; PROTEOMICS; RAT; SYNAPSE;

ACTINS; ANIMALS; BLOTTING, WESTERN; CADHERINS; CATENINS; CHROMATOGRAPHY, LIQUID; CYTOSKELETON; FEMALE; HIPPOCAMPUS; IMMUNOPRECIPITATION; INTERMEDIATE FILAMENT PROTEINS; MASS SPECTROMETRY; MICE; MICROTUBULES; NEURONAL PLASTICITY; NEURONS; PREGNANCY; PROTEOMICS; RATS; SYNAPSES; SYNAPTOSOMES; TRYPSIN;

EID: 84863467083     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.05.008     Document Type: Article

References (78)

1. K. Abe, and M. Takeichi NMDA-receptor activation induces calpain-mediated beta-catenin cleavages for triggering gene expression Neuron 53 2007 387 397
2. S.X. Bamji, B. Rico, N. Kimes, and L.F. Reichardt BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions J. Cell Biol. 174 2006 289 299
3. S.X. Bamji, K. Shimazu, N. Kimes, J. Huelsken, W. Birchmeier, B. Lu, and L.F. Reichardt Role of beta-catenin in synaptic vesicle localization and presynaptic assembly Neuron 40 2003 719 731
4. D.L. Benson, and H. Tanaka N-cadherin redistribution during synaptogenesis in hippocampal neurons J. Neurosci. 18 1998 6892 6904
5. C. Bierkamp, H. Schwarz, O. Huber, and R. Kemler Desmosomal localization of beta-catenin in the skin of plakoglobin null-mutant mice Development 126 1999 371 381
6. S. Boguslavsky, I. Grosheva, E. Landau, M. Shtutman, M. Cohen, K. Arnold, E. Feinstein, B. Geiger, and A. Bershadsky P120 catenin regulates lamellipodial dynamics and cell adhesion in cooperation with cortactin Proc. Natl. Acad. Sci. USA 104 2007 10882 10887
7. O. Bozdagi, W. Shan, H. Tanaka, D.L. Benson, and G.W. Huntley Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation Neuron 28 2000 245 259
8. O. Bozdagi, M. Valcin, K. Poskanzer, H. Tanaka, and D.L. Benson Temporally distinct demands for classic cadherins in synapse formation and maturation Mol. Cell. Neurosci. 27 2004 509 521
9. O. Bozdagi, X.B. Wang, J.S. Nikitczuk, T.R. Anderson, E.B. Bloss, G.L. Radice, Q. Zhou, D.L. Benson, and G.W. Huntley Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin J. Neurosci. 30 2010 9984 9989
10. D.A. Brown, and J.K. Rose Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface Cell 68 1992 533 544
11. A. Chausovsky, A.D. Bershadsky, and G.G. Borisy Cadherin-mediated regulation of microtubule dynamics Nat. Cell Biol. 2 2000 797 804
12. X. Chen, S. Kojima, G.G. Borisy, and K.J. Green P120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions J. Cell Biol. 163 2003 547 557
13. N.A. Chitaev, A.Z. Averbakh, R.B. Troyanovsky, and S.M. Troyanovsky Molecular organization of the desmoglein-plakoglobin complex J. Cell Sci. 111 Pt 14 1998 1941 1949
14. K. Cho, T.G. Vaught, H. Ji, D. Gu, C. Papasakelariou-Yared, N. Horstmann, J.M. Jennings, M. Lee, L.M. Sevilla, M. Kloc, A.B. Reynolds, F.M. Watt, R.G. Brennan, A.P. Kowalczyk, and P.D. McCrea Xenopus Kazrin interacts with ARVCF-catenin, spectrin and p190B RhoGAP, and modulates RhoA activity and epithelial integrity J. Cell Sci. 123 2010 4128 4144
15. C.W. Cotman, G. Banker, L. Churchill, and D. Taylor Isolation of postsynaptic densities from rat brain J. Cell Biol. 63 1974 441 455
16. L.P. Elia, M. Yamamoto, K. Zang, and L.F. Reichardt P120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins Neuron 51 2006 43 56
17. A.M. Fannon, and D.R. Colman A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins Neuron 17 1996 423 434
18. M. Fischer, S. Kaech, U. Wagner, H. Brinkhaus, and A. Matus Glutamate receptors regulate actin-based plasticity in dendritic spines Nat. Neurosci. 3 2000 887 894
19. C.M. Franz, and A.J. Ridley P120 catenin associates with microtubules: inverse relationship between microtubule binding and Rho GTPase regulation J. Biol. Chem. 279 2004 6588 6594
20. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo Neuron 38 2003 447 460
21. J. Gu, B.L. Firestein, and J.Q. Zheng Microtubules in dendritic spine development J. Neurosci. 28 2008 12120 12124
22. S. Heyraud, M. Jaquinod, C. Durmort, E. Dambroise, E. Concord, J.P. Schaal, P. Huber, and D. Gulino-Debrac Contribution of annexin 2 to the architecture of mature endothelial adherens junctions Mol. Cell. Biol. 28 2008 1657 1668
23. X. Hu, C. Viesselmann, S. Nam, E. Merriam, and E.W. Dent Activity-dependent dynamic microtubule invasion of dendritic spines J. Neurosci. 28 2008 13094 13105
24. T. Ichii, and M. Takeichi P120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner Genes Cells 12 2007 827 839
25. I. Israely, R.M. Costa, C.W. Xie, A.J. Silva, K.S. Kosik, and X. Liu Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction Curr. Biol. 14 2004 1657 1663
26. K. Jungling, V. Eulenburg, R. Moore, R. Kemler, V. Lessmann, and K. Gottmann N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons J. Neurosci. 26 2006 6968 6978
27. U. Kaufmann, J. Kirsch, A. Irintchev, A. Wernig, and A. Starzinski-Powitz The M-cadherin catenin complex interacts with microtubules in skeletal muscle cells: implications for the fusion of myoblasts J. Cell Sci. 112 Pt 1 1999 55 68
28. R. Kemler From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion Trends Genet. 9 1993 317 321
29. S.S. Kholmanskikh, H.B. Koeller, A. Wynshaw-Boris, T. Gomez, P.C. Letourneau, and M.E. Ross Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility Nat. Neurosci. 9 2006 50 57
30. K.A. Knudsen, A.P. Soler, K.R. Johnson, and M.J. Wheelock Interaction of alpha-actinin with the cadherin/catenin cell-cell adhesion complex via alpha-catenin J. Cell Biol. 130 1995 67 77
31. R. Koob, M. Zimmermann, W. Schoner, and D. Drenckhahn Colocalization and coprecipitation of ankyrin and Na+, K+-ATPase in kidney epithelial cells Eur. J. Cell Biol. 45 1988 230 237
32. A.P. Kowalczyk, E.A. Bornslaeger, J.E. Borgwardt, H.L. Palka, A.S. Dhaliwal, C.M. Corcoran, M.F. Denning, and K.J. Green The amino-terminal domain of desmoplakin binds to plakoglobin and clusters desmosomal cadherin-plakoglobin complexes J. Cell Biol. 139 1997 773 784
33. L.A. Ligon, and E.L. Holzbaur Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly Traffic 8 2007 808 819
34. L.A. Ligon, S. Karki, M. Tokito, and E.L. Holzbaur Dynein binds to beta-catenin and may tether microtubules at adherens junctions Nat. Cell Biol. 3 2001 913 917
35. B. Lin, E.A. Kramar, X. Bi, F.A. Brucher, C.M. Gall, and G. Lynch Theta stimulation polymerizes actin in dendritic spines of hippocampus J. Neurosci. 25 2005 2062 2069
36. J. Luo, Y. Wang, R.P. Yasuda, A.W. Dunah, and B.B. Wolfe The majority of N-methyl-d-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B) Mol. Pharmacol. 51 1997 79 86
37. T. Manabe, H. Togashi, N. Uchida, S.C. Suzuki, Y. Hayakawa, M. Yamamoto, H. Yoda, T. Miyakawa, M. Takeichi, and O. Chisaka Loss of cadherin-11 adhesion receptor enhances plastic changes in hippocampal synapses and modifies behavioral responses Mol. Cell. Neurosci. 15 2000 534 546
38. S. Mary, S. Charrasse, M. Meriane, F. Comunale, P. Travo, A. Blangy, and C. Gauthier-Rouviere Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism Mol. Biol. Cell 13 2002 285 301
39. M. Mathur, L. Goodwin, and P. Cowin Interactions of the cytoplasmic domain of the desmosomal cadherin Dsg1 with plakoglobin J. Biol. Chem. 269 1994 14075 14080
40. H. McNeill, M. Ozawa, R. Kemler, and W.J. Nelson Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity Cell 62 1990 309 316
41. P. Mendez, M. De Roo, L. Poglia, P. Klauser, and D. Muller N-cadherin mediates plasticity-induced long-term spine stabilization J. Cell Biol. 189 2010 589 600
42. W. Meng, Y. Mushika, T. Ichii, and M. Takeichi Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts Cell 135 2008 948 959
43. F. Miskevich, Y. Zhu, B. Ranscht, and J.R. Sanes Expression of multiple cadherins and catenins in the chick optic tectum Mol. Cell. Neurosci. 12 1998 240 255
44. J.S. Morrow, C.D. Cianci, T. Ardito, A.S. Mann, and M. Kashgarian Ankyrin links fodrin to the alpha subunit of Na, K-ATPase in Madin-Darby canine kidney cells and in intact renal tubule cells J. Cell Biol. 108 1989 455 465
45. S. Murase, E. Mosser, and E.M. Schuman Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function Neuron 35 2002 91 105
46. I.S. Nathke, L. Hinck, J.R. Swedlow, J. Papkoff, and W.J. Nelson Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells J. Cell Biol. 125 1994 1341 1352
47. W.J. Nelson, E.M. Shore, A.Z. Wang, and R.W. Hammerton Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney epithelial cells J. Cell Biol. 110 1990 349 357
48. W.J. Nelson, and P.J. Veshnock Ankyrin binding to (Na+ + K+)ATPase and implications for the organization of membrane domains in polarized cells Nature 328 1987 533 536
49. J.E. Nieset, A.R. Redfield, F. Jin, K.A. Knudsen, K.R. Johnson, and M.J. Wheelock Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin J. Cell Sci. 110 Pt 8 1997 1013 1022
50. K. Okamoto, T. Nagai, A. Miyawaki, and Y. Hayashi Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity Nat. Neurosci. 7 2004 1104 1112
51. K. Okamura, H. Tanaka, Y. Yagita, Y. Saeki, A. Taguchi, Y. Hiraoka, L.H. Zeng, D.R. Colman, and N. Miki Cadherin activity is required for activity-induced spine remodeling J. Cell Biol. 167 2004 961 972
52. T. Okuda, L.M. Yu, L.A. Cingolani, R. Kemler, and Y. Goda Beta-Catenin regulates excitatory postsynaptic strength at hippocampal synapses Proc. Natl. Acad. Sci. USA 104 2007 13479 13484
53. C.A. Otey, F.M. Pavalko, and K. Burridge An interaction between alpha-actinin and the beta 1 integrin subunit in vitro J. Cell Biol. 111 1990 721 729
54. G.R. Phillips, J.K. Huang, Y. Wang, H. Tanaka, L. Shapiro, W. Zhang, W.S. Shan, K. Arndt, M. Frank, R.E. Gordon, M.A. Gawinowicz, Y. Zhao, and D.R. Colman The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution Neuron 32 2001 63 77
55. D. Pradhan, C.R. Lombardo, S. Roe, D.L. Rimm, and J.S. Morrow Alpha -Catenin binds directly to spectrin and facilitates spectrin-membrane assembly in vivo J. Biol. Chem. 276 2001 4175 4181
56. P.A. Sacco, T.M. McGranahan, M.J. Wheelock, and K.R. Johnson Identification of plakoglobin domains required for association with N-cadherin and alpha-catenin J. Biol. Chem. 270 1995 20201 20206
57. L. Saglietti, C. Dequidt, K. Kamieniarz, M.C. Rousset, P. Valnegri, O. Thoumine, F. Beretta, L. Fagni, D. Choquet, C. Sala, M. Sheng, and M. Passafaro Extracellular interactions between GluR2 and N-cadherin in spine regulation Neuron 54 2007 461 477
58. D. Salomon, P.A. Sacco, S.G. Roy, I. Simcha, K.R. Johnson, M.J. Wheelock, and A. Ben-Ze'ev Regulation of beta-catenin levels and localization by overexpression of plakoglobin and inhibition of the ubiquitin-proteasome system J. Cell Biol. 139 1997 1325 1335
59. A. Schmidt, H.W. Heid, S. Schafer, U.A. Nuber, R. Zimbelmann, and W.W. Franke Desmosomes and cytoskeletal architecture in epithelial differentiation: cell type-specific plaque components and intermediate filament anchorage Eur. J. Cell Biol. 65 1994 229 245
60. C. Schrick, A. Fischer, D.P. Srivastava, N.C. Tronson, P. Penzes, and J. Radulovic N-cadherin regulates cytoskeletally associated IQGAP1/ERK signaling and memory formation Neuron 55 2007 786 798
61. R.J. Shprintzen, R.B. Goldberg, M.L. Lewin, E.J. Sidoti, M.D. Berkman, R.V. Argamaso, and D. Young A new syndrome involving cleft palate, cardiac anomalies, typical facies, and learning disabilities: velo-cardio-facial syndrome Cleft Palate J. 15 1978 56 62
62. J.B. Silverman, S. Restituito, W. Lu, L. Lee-Edwards, L. Khatri, and E.B. Ziff Synaptic anchorage of AMPA receptors by cadherins through neural plakophilin-related arm protein AMPA receptor-binding protein complexes J. Neurosci. 27 2007 8505 8516
63. H. Sirotkin, H. O'Donnell, R. DasGupta, S. Halford, B. St Jore, A. Puech, S. Parimoo, B. Morrow, A. Skoultchi, S.M. Weissman, P. Scambler, and R. Kucherlapati Identification of a new human catenin gene family member (ARVCF) from the region deleted in velo-cardio-facial syndrome Genomics 41 1997 75 83
64. E.A. Smith, and E. Fuchs Defining the interactions between intermediate filaments and desmosomes J. Cell Biol. 141 1998 1229 1241
65. V. Soukoulis, S. Reddy, R.D. Pooley, Y. Feng, C.A. Walsh, and D.M. Bader Cytoplasmic LEK1 is a regulator of microtubule function through its interaction with the LIS1 pathway Proc. Natl. Acad. Sci. USA 102 2005 8549 8554
66. E.N. Star, D.J. Kwiatkowski, and V.N. Murthy Rapid turnover of actin in dendritic spines and its regulation by activity Nat. Neurosci. 5 2002 239 246
67. S.J. Stehbens, A.D. Paterson, M.S. Crampton, A.M. Shewan, C. Ferguson, A. Akhmanova, R.G. Parton, and A.S. Yap Dynamic microtubules regulate the local concentration of E-cadherin at cell-cell contacts J. Cell Sci. 119 2006 1801 1811
68. C.Y. Tai, S.P. Mysore, C. Chiu, and E.M. Schuman Activity-regulated N-cadherin endocytosis Neuron 54 2007 771 785
69. H. Tanaka, W. Shan, G.R. Phillips, K. Arndt, O. Bozdagi, L. Shapiro, G.W. Huntley, D.L. Benson, and D.R. Colman Molecular modification of N-cadherin in response to synaptic activity Neuron 25 2000 93 107
70. L. Tang, C.P. Hung, and E.M. Schuman A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation Neuron 20 1998 1165 1175
71. J. Teng, T. Rai, Y. Tanaka, Y. Takei, T. Nakata, M. Hirasawa, A.B. Kulkarni, and N. Hirokawa The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium Nat. Cell Biol. 7 2005 474 482
72. H. Togashi, K. Abe, A. Mizoguchi, K. Takaoka, O. Chisaka, and M. Takeichi Cadherin regulates dendritic spine morphogenesis Neuron 35 2002 77 89
73. N. Uchida, Y. Honjo, K.R. Johnson, M.J. Wheelock, and M. Takeichi The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones J. Cell Biol. 135 1996 767 779
74. C.M. Waterman-Storer, W.C. Salmon, and E.D. Salmon Feedback interactions between cell-cell adherens junctions and cytoskeletal dynamics in newt lung epithelial cells Mol. Biol. Cell 11 2000 2471 2483
75. T. Yagi, and M. Takeichi Cadherin superfamily genes: functions, genomic organization, and neurologic diversity Genes Dev. 14 2000 1169 1180
76. M. Yanagisawa, I.N. Kaverina, A. Wang, Y. Fujita, A.B. Reynolds, and P.Z. Anastasiadis A novel interaction between kinesin and p120 modulates p120 localization and function J. Biol. Chem. 279 2004 9512 9521
77. S. Yasuda, H. Tanaka, H. Sugiura, K. Okamura, T. Sakaguchi, U. Tran, T. Takemiya, A. Mizoguchi, Y. Yagita, T. Sakurai, E.M. De Robertis, and K. Yamagata Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2beta and p38 MAP kinases Neuron 56 2007 456 471
78. R. Zaidel-Bar, M.J. Joyce, A.M. Lynch, K. Witte, A. Audhya, and J. Hardin The F-BAR domain of SRGP-1 facilitates cell-cell adhesion during C. elegans morphogenesis J. Cell Biol. 191 2010 761 769