Abi2-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory

Molecular and Cellular Biology

Volumn 24, Issue 24, 2004, Pages 10905-10922

  Grove, Matthew ^a   Demyanenko, Galina ^b   Echarri, Asier ^a   Zipfel, Patricia A ^a   Quiroz, Marisol E ^a   Rodriguiz, Ramona M ^a   Playford, Martin ^a   Martensen, Shelby A ^a   Robinson, Matthew R ^a   Wetsel, William C ^a   Maness, Patricia F ^b   Pendergast, Ann Marie ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABI2 PROTEIN; ACTIN; ADAPTOR PROTEIN; COMPLEMENTARY DNA; GUANOSINE TRIPHOSPHATASE; RAC PROTEIN; RNA; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; COGNITION; DENDRITIC SPINE; EMBRYO; EPITHELIUM CELL; EYE DEVELOPMENT; HIPPOCAMPUS; HISTOLOGY; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; LEARNING; LENS; MEMORY; MORPHOLOGY; MOUSE; NEOCORTEX; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PLASMID; POLYMERIZATION; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ADHERENS JUNCTIONS; ANIMALS; CELL LINE; CELL MOVEMENT; DENDRITES; DENDRITIC SPINES; DOGS; EMBRYO; FIBROBLASTS; GENE DELETION; HELA CELLS; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; HOMOZYGOTE; HUMANS; LEARNING; LENS, CRYSTALLINE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHOGENESIS; NEOCORTEX; RNA INTERFERENCE; RNA, SMALL INTERFERING;

ANIMALIA; MURINAE;

EID: 10044236688     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.24.10905-10922.2004     Document Type: Article

References (82)

1. Abe, K., O. Chisaka, F. van Roy, and M. Takeichi. 2004. Stability of dendritic spines and synaptic contacts is controlled by βN-catenin. Nat. Neurosci. 7:357-363.
2. Bassnett, S., H. Missey, and I. Vucemilo. 1999. Molecular architecture of the lens fiber cell basal membrane complex. J. Cell Sci. 112:2155-2165.
3. Biesova, Z., C. Piccoli, and W. T. Wong. 1997. Isolation and characterization of e3B1, an eps8 binding protein that regulates cell growth. Oncogene 14:233-241.
4. Blagg, S. L., M. Stewart, C. Sambles, and R. H. Insall. 2003. PIR121 regulates pseudopod dynamics and SCAR activity in Dictyostelium. Curr. Biol. 13:1480-1487.
5. Chelly, J., and J. L. Mandel. 2001. Monogenic causes of X-linked mental retardation. Nat. Rev. Genetics 2:669-680.
6. Contractor, A., C. Rogers, C. Maron, M. Henkemeyer, G. T. Swanson, and S. F. Heinemann. 2002. trans-synaptic Eph receptor-Ephrin signaling in hippocampal mossy fiber LTP. Science 296:1864-1869.
7. Cort,s, F., D. Dagget, R. J. Bryson-Richardson, C. Neyt, J. Maule, P. Gautier, G. E. Hollway, D. Keenan, and P. Currie. 2003. Cadherin-mediated differential cell adhesion controls slow muscle cell migration in the developing zebrafish myotome. Dev. Cell 5:865-876.
8. Courtney, K. D., M. Grove, H. Vandongen, A. Vandongen, A. S. LaMantia, and A. M. Pendergast. 2000. Localization and phosphorylation of Abl-interactor proteins, Abi-1 and Abi-2, in the developing nervous system. Mol. Cell. Neurosci. 16:244-257.
9. Cowan, C. A., and M. Henkemeyer. 2001. The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413:174-179.
10. Dai, Z., and A. M. Pendergast. 1995. Abi-2, a novel SH3-containing protein interacts with the c-Abl tyrosine kinase and modulates c-Abl transforming activity. Genes Dev. 9:2569-2582.
11. Demyanenko, G. P., A. Y. Tsai, and P. F. Maness. 1999. Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J. Neurosci. 19:4907-4920.
12. Echarri, A., M. J. Lai, M. R. Robinson, and A. M. Pendergast. 2004. Abl interactor 1 (Abi-1) Wave-binding and SNARE domains regulate its nucleocytoplasmic shuttling, lamellipodium localization, and Wave-1 levels. Mol. Cell. Biol. 24:4979-4993.
13. Eden, S., R. Rohatgi, A. V. Podtelejnikov, M. Mann, and M. W. Kirschner. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790-793.
14. Ehrlich, J. S., M. D. Hansen, and W. J. Nelson. 2002. Spatio-temporal regulation of Rac1 localization and lamellipodia dynamics during epithelial cell-cell adhesion. Dev. Cell 3:259-270.
15. Ethell, I. M., F. Irie, M. S. Kalo, J. R. Couchman, E. B. Pasquale, and Y. Yamaguchi. 2001. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31:1001-1013.
16. Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature 420:629-635.
17. Fan, P. D., and S. P. Goff. 2000. Abl interactor 1 binds to Sos and inhibits epidermal growth factor- and v-Abl-induced activation of extracellular signal-regulated kinases. Mol. Cell. Biol. 20:7591-7601.
18. Fukata, M., and K. Kaibuchi. 2001. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat. Rev. Mol. Cell Biol. 2:887-897.
19. Gavard, J., M. Lambert, I. Grosheva, V. Marthiens, T. Irinopoulou, J.-F. Riou, A. Bershadsky, and R.-M. Mege. 2003. Lamellipodium extension and cadherin adhesion: two cell responses to cadherin activation relying on distinct signaling pathways. J. Cell Sci. 117:257-270.
20. Govek, E.-E., S. E. Newey, C. J. Akerman, J. R. Cross, L. Van der Veken, and L. Van Aelst. 2004. The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat. Neurosci. 7:364-372.
21. Grunwald, I. C., M. Korte, G. Adelmann, A. Plueck, K. Kullander, R. H. Adams, M. Frotscher, T. Bonhoeffer, and R. Klein. 2004. Hippocampal plasticity requires postsynaptic ephrinBs. Nat. Neurosci. 7:33-40.
22. Hahne, P., A. Sechi, S. Benesch, and J. V. Small. 2001. Scar/WAVE is localized at the tips of protruding lamellipodia in living cells. FEBS Lett. 492:215-220.
23. Henkemeyer, M., O. S. Itkis, M. Ngo, P. W. Hickmott, and I. M. Ethell. 2003. Multiple Eph receptor tyrosine kinases shape dendritic spines in the hippocampus. J. Cell Biol. 163:1313-1326.
24. Hering, H., and M. Sheng. 2001. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2:880-888.
25. Innocenti, M., P. Tenca, E. Frittoli, M. Faretta, A. Tocchetti, P. P. Di Fiore, and G. Scita. 2002. Mechanisms through which Sos-1 coordinates the activation of Ras and Rac. J. Cell Biol. 156:125-136.
26. Innocenti, M., A. Zucconi, A. Disanza, E. Frittoli, L. B. Areces, A. Steffen, T. E. B. Stradal, P. P. Di Fiore, M.-F. Carlier, and G. Scita. 2004. Abi1 is essential for the formation and activation of a WAVE2 signalling complex. Nat. Cell Biol. 6:319-327.
27. Irie, F., and Y. Yamaguchi. 2002. Eph receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat. Neurosci. 5:1117-1118.
28. Juang, J. L., and F. M. Hoffmann. 1999. Drosophila abelson interacting protein (dAbi) is a positive regulator of abelson tyrosine kinase activity. Oncogene 18:5138-5147.
29. Kobielak, A., H. A. Pasolli, and E. Fuchs. 2004. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat. Cell Biol. 6:21-30.
30. Kovacs, E. M., M. Goodwin, R. G. Ali, A. D. Paterson, and A. S. Yap. 2002. Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr. Biol. 12:379-382.
31. Kunda, P., G. Craig, V. Dominguez, and B. Baum. 2003. Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 13:1867-1875.
32. Lo, W. K. 1988. Adherens junctions in the ocular lens of various species: ultrastructural analysis with an improved fixation. Cell Tissue Res. 254:31-40.
33. Matus, A. 2000. Actin-based plasticity in dendritic spines. Science 290:754-758.
34. McAvoy, J. W. 1980. Induction of the eye lens. Differentiation 17:137-149.
35. Meng, Y., Y. Zhang, V. Tregoubov, C. Janus, L. Cruz, M. Jackson, W. Y. Lu, J. F. MacDonald, J. Y. Wang, D. L. Falls, and Z. Jia. 2002. Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35:121-133.
36. Miyazaki, K., S. Matsuda, Y. Ichigotani, Y. Takenouchi, K. Hayashi, Y. Fukuda, Y. Nimura, and M. Hamaguchi. 2000. Isolation and characterization of a novel human gene (NESH) which encodes a putative signaling molecule similar to e3B1 protein. Biochim. Biophys. Acta 1493:237-241.
37. Moresco, E. M., A. J. Scheetz, W. G. Bornmann, A. J. Koleske, and R. M. Fitzsimonds. 2003. Abl family kinases modulate short-term synaptic plasticity. J. Neurophysiol. 89:1678-1687.
38. Morgenbesser, S. D., B. O. Williams, T. Jacks, and R. A. DePinho. 1994. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature 371:72-74.
39. Morgenbesser, S. D., N. Schreiber-Agus, M. Bidder, K. A. Mahon, P. A. Overbeek, J. Horner, and R. A. DePinho. 1995. Contrasting roles for c-Myc and L-Myc in the regulation of cellular growth and differentiation in vivo. EMBO J. 14:743-756.
40. Murai, K. K., L. N. Nguyen, F. Irie, Y. Yamaguchi, and E. B. Pasquale. 2003. Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6:153-160.
41. Nakayama, A. Y., M. B. Harms, and L. Luo. 2000. Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20:5329-5338.
42. Nishiguchi, S., H. Wood, H. Kondoh, R. Lovell-Badge, and V. Episkopou. 1998. Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev. 12:776-781.
43. Penzes, P., A. Beeser, J. Chernoff, M. R. Schiller, B. A. Eipper, R. E. Mains, and R. L. Huganir. 2003. Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37:263-274.
44. Piatigorsky, J. 1981. Lens differentiation in vertebrates: a review of cellular and molecular features. Differentiation. 19:134-153.
45. Plattner, R., L. Kadlec, K. A. DeMali, A. Kazlauskas, and A. M. Pendergast. 1999. c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 13:2400-2411.
46. Ramakers, G. J. A. 2002. Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 25:191-199.
47. Reddy, B. A., M. Kloc, and L. D. Etkin. 1992. The cloning and characterization of a localized maternal transcript in Xenopus laevis whose zygotic counterpart is detected in the CNS. Mech. Dev. 39:143-150.
48. Reya, T., A. W. Duncan, L. Ailles, J. Domen, D. C. Scherer, K. Willert, L. Hintz, R. Nusse, and I. L. Weissman. 2003. A role for Wnt signaling in self-renewal of haematopoietic stem cells. Nature 423:409-414.
49. 2+/calmodulin kinase IV-deficient mice. J. Neurosci. 20:RC107.
50. Rogers, S. L., U. Wiedemann, N. Stuurman, and R. D.Vale. 2003. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162:1079-1088.
51. Sahai, E., and C. J. Marshall. 2002. ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat. Cell Biol. 4:408-415.
52. Schenck, A., B. Bardoni, A. Moro, C. Bagni, and J.-L. Mandel. 2001. A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc. Natl. Acad. Sci. USA 98:8844-8849.
53. Schenck, A., B. Bardoni, C. Langmann, N. Harden, J. L. Mandel, and A. Giangrande. 2003. CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38:887-898.
54. Schöck, F., and N. Perrimon. 2002. Molecular mechanisms of epithelial morphogenesis. Annu. Rev. Cell. Dev. Biol. 18:463-493.
55. Schuz, A., and G. P. Demianenko. 1995. Constancy and variability in cortical structure. A study on synapses and dendritic spines in hedgehog and monkey. J. Hirnforsch. 36:113-122.
56. Scita, G., J. Nordstrom, R. Carbone, P. Tenca, G. Giardina, S. Gutkind, M. Bjarnegard, C. Betsholtz, and P. P. Di Fiore. 1999. EPS8 and E3B1 transduce signals from Ras to Rac. Nature 401:290-293.
57. Scita, G., P. Tenca, L. B. Areces, A. Tocchetti, E. Frittoli, G. Giardina, I. Ponzanelli, P. Sini, M. Innocenti, and P. P. Di Fiore. 2001. An effector region in Eps8 is responsible for the activation of the Rac-specific GEF activity of Sos-1 and for the proper localization of the Rac-based actin-polymerizing machine. J. Cell Biol. 154:1031-1044.
58. Shi, Y., K. Alin, and S. P. Goff. 1995. Abl-interactor-1, a novel SH3 protein binding to the carboxy-terminal portion of the Abl protein, suppresses v-abl transforming activity. Genes Dev. 9:2583-2597.
59. Soderling, S. H., K. L. Binns, G. A. Wayman, S. M. Davee, S. H. Ong, T. Pawson, and J. D. Scott. 2002. The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat. Cell Biol. 4:970-975.
60. Soderling, S. H., L. K. Langeberg, J. A. Soderling, S. M. Davee, R. Simerly, J. Raber, and J. D. Scott. 2003. Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc. Natl. Acad. Sci. USA 100:1723-1728.
61. Soto, M. C., H. Qadota, K. Kasuya, M. Inoue, D. Tsuboi, C. C. Mello, and K. Kaibuchi. 2002. The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev. 16:620-632.
62. Steffen, A., K. Rottner, J. Ehinger, M. Innocenti, G. Scita, J. Wehland, and T. E. B. Stradal. 2004. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23:749-759.
63. Stradal, T., K. D. Courtney, K. Rottner, P. Hahne, J. V. Small, and A. M. Pendergast. 2001. The Abl interactor proteins localize to sites of actin polymerization at the tips of lamellipodia and filopodia. Curr. Biol. 11:891-895.
64. Straub, B. K., J. Boda, C. Kuhn, M. Schnoelzer, U. Korf, T. Kempf, H. Spring, M. Hatzfeld, and W. W. Franke. 2003. A novel cell-cell junction system: the cortex adherens mosaic of lens fiber cells. J. Cell Sci. 116:4985-4995.
65. Suetsugu, S., D. Yamazaki, S. Kurisu, and T. Takenawa. 2003. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev. Cell 5:595-609.
66. Svoboda, K., D. W. Tank, and W. Denk. 1996. Direct measurement of coupling between dendritic spines and shafts. Science 272:716-719.
67. Tani, K., S. Sato, T. Sukezane, H. Kojima, H. Hirose, H. Hanafusa, and T. Shishido. 2003. Abl interactor 1 promotes tyrosine 296 phosphorylation of mammalian enabled (Mena) by c-Abl kinase. J. Biol. Chem. 278:21685-21692.
68. Togashi, H., K. Abe, A. Mizoguchi, K. Takaoka, O. Chisaka, and M. Takeichi. 2002. Cadherin regulates dendritic spine morphogenesis. Neuron 35:77-89.
69. Vasioukhin, V., C. Bauer, M. Yin, and E. Fuchs. 2000. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100:209-219.
70. Vianna, M. R., L. A. Izquierdo, D. M. Barros, J. H. Medina, and I. Izquierdo. 1999. Intrahippocampal infusion of an inhibitor of protein kinase A separates short- from long-term memory. Behav. Pharmacol. 10:223-227.
71. Wallar, B. J., and A. S. Alberts. 2003. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 13:435-446.
72. Wang, B., T. Mysliwiec, D. Krainc, R. A. Jensen, G. Sonoda, J. R. Testa, E. A. Golemis, and G. D. Kruh. 1996. Identification of ArgBP1, an Arg protein tyrosine kinase binding protein that is the human homologue of a CNS-specific Xenopus gene. Oncogene 12:1921-1929.
73. Welch, M. D., and R. D. Mullins. 2002. Cellular control of actin nucleation. Annu. Rev. Cell. Dev. Biol. 18:247-288.
74. Westphal, R. S., S. H. Soderling, N. M. Alto, L. K. Langeberg, and J. D. Scott. 2000. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multikinase scaffold. EMBO J. 19:4589-4600.
75. Yamamoto, A., T. Suzuki, and Y. Sakaki. 2001. Isolation of hNap1BP which interacts with human Nap1 (NCKAP1) whose expression is down-regulated in Alzheimer's disease. Gene 271:159-169.
76. Yamazaki, D., S. Suetsugu, H. Miki, Y. Kataoka, S.-I. Nishikawa, T. Fujiwara, N. Yoshida, and T. Takenawa. 2003. WAVE2 is required for directed cell migration and cardiovascular development. Nature 424:452-456.
77. Yap, A. S., and E. M. Kovacs. 2003. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 160:11-16.
78. Yu, X., and R. C. Malenka. 2003. α-Catenin is critical for dendritic morphogenesis. Nat. Neurosci. 6:1169-1177.
79. Yuste, R., and T. Bonhoeffer. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24:1071-1089.
80. Zhang, H., D. J. Webb, H. Asmussen, and A. F. Horwitz. 2003. Synapse formation is regulated by the signaling adaptor GIT1. J. Cell Biol. 161:131-142.
81. Zhang, P., C. Wong, R. A. DePinho, J. W. Harper, and S. J. Elledge. 1998. Cooperation between the Cdk inhibitors p27(KIP1) and p57(KIP2) in the control of tissue growth and development. Genes Dev. 12:3162-3167.
82. Ziemnicka-Kotula, D., J. Xu, H. Gu, A. Potempska, K. S. Kim, E. C. Jenkins, E. Trenkner, and L. Kotula. 1998. Identification of a candidate human spectrin Src homology 3 domain-binding protein suggests a general mechanism of association of tyrosine kinases with the spectrin-based membrane skeleton. J. Biol. Chem. 273:13681-13692.