Dual regulation of neuronal morphogenesis by a δ-catenin-cortactin complex and Rho

Journal of Cell Biology

Volumn 162, Issue 1, 2003, Pages 99-111

  Martinez, Maria Cruz ^a   Ochiishi, Tomoyo ^a   Majewski, Michael ^a   Kosik, Kenneth S ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

catenin; Cortactin; Dendretic branching; Rho; Tyrosine phosphorylation

Indexed keywords

CATENIN; CORTACTIN; DELTA CATENIN; NEURITE PROMOTING FACTOR; PROLINE DERIVATIVE; PROTEIN TYROSINE KINASE; RHO FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; DENDRITE; MORPHOGENESIS; NERVE CELL; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT;

NON-PROGRAMMATIC;

AMINO ACID SEQUENCE; ANIMALS; ARMADILLO DOMAIN PROTEINS; BRAIN; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL SIZE; CORTACTIN; CYTOSKELETAL PROTEINS; DENDRITES; FETUS; GENETIC VECTORS; MICROFILAMENT PROTEINS; NEURITES; PC12 CELLS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROLINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; RHOA GTP-BINDING PROTEIN; SRC-FAMILY KINASES; TYROSINE;

ANIMALIA; ARMADILLO;

EID: 0037810840     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200211025     Document Type: Article

References (53)

1. Anastasiadis, P.Z., and A.B. Reynolds. 2001. Regulation of Rho GTPases by p120-catenin. Curr. Opin. Cell Biol. 13:604-610.
2. Anastasiadis, P.Z., S.Y. Moon, M.A. Thoreson, D.J. Mariner, H.C. Crawford, Y. Zheng, and A.B. Reynolds. 2000. Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2:637-644.
3. Arthur, W.T., L.A. Petch, and K. Burridge. 2000. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10:719-722.
4. Banzai, Y., H. Miki, H. Yamaguchi, and T. Takenawa. 2000. Essential role of neural Wiskott-Aldrich Syndrome protein in neurite extension in PC12 cells and rat hippocampal primary culture cells. J Biol. Chem. 275:11987-11992.
5. Boquet, P. 1999. Bacterial toxins inhibiting or activating small GTP-binding proteins. Ann. NY Acad. Sci. 886:83-90.
6. Brouns, M.R., S.F. Matheson, and J. Settleman. 2001. p190 RhoGAP is the principal Src substrate in brain and regulates axon outgrowth, guidance and fasciculation. Nat. Cell Biol. 3:361-367.
7. Dailey, M.E., and S.J. Smith. 1996. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16:2983-2994.
8. Desmond, N.L., and W.B. Levy. 1984. Dendritic caliber and the 3/2 power relationship ofdentate granule cells. J. Comp. Neurol. 227:589-596.
9. Du, Y., S.A. Weed, W.C. Xiong, T.D. Marshall, and J.T. Parsons. 1998. Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol. Cell. Biol. 18:5838-5851.
10. Dudek, S.M., K.G. Birukov, X. Zhan, and J.G. Garcia. 2002. Novel interaction of cortactin with endothelial cell myosin light chain kinase. Biochem. Biophys. Res. Commun. 298:511-519.
11. Fujita, H., H. Katoh, Y. Ishikawa, K. Mori, and M. Negishi. 2002. Rapostlin is a novel effector of Rnd2 GTPase inducing neurite branching. J. Biol. Chem. 277:45428-45434
12. Gao, F.B., J.E. Brenman, L.Y. Jan, and Y.N. Jan. 1999. Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13:2549-2561.
13. Garcia, J.G., A.D. Verin, K. Schaphorst, R. Siddiqui, C.E. Patterson, C. Csortos, and V. Natarajan. 1999. Regulation of endothelial cell myosin light chain kinase by Rho, cortactin, and p60(src). Am. J. Physiol. 276:L989-L998.
14. Hattan, D., E. Nesti, T.G. Cachero, and A.D. Morielli. 2002. Tyrosine phosphorylation of Kv1.2 modulates its interaction with the actin binding protein cortactin. J. Biol. Chem. 277:38596-38606
15. Ho, C., J. Zhou, M. Medina, T. Goto, M. Jacobson, P.G. Bhide, and K.S. Kosik. 2000. delta-catenin is a nervous system-specific adherens junction protein which undergoes dynamic relocalization during development. J. Comp. Neurol. 420:261-276.
16. Huang, C., Y. Ni, T. Wang, Y. Gao, C.C. Haudenschild, and X. Zhan. 1997. Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediared tyrosine phosphorylation. J. Biol. Chem. 272:13911-13915.
17. Ide, N., Y. Hata, M. Deguchi, K. Hirao, I. Yao, and Y. Takai. 1999. Interaction of S-SCAM with neural plakophilin-related Armadillo-repeat protein/delta-catenin. Biochem. Biophys. Res. Commun. 256:456-461.
18. Jalink, K., E.J. van Corven, T. Hengeveld, N. Morii, S. Narumiya, and W.H. Moolenaar. 1994. Inhibition of lysophosphatidate- and thrombin-induced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126:801-810.
19. Kanner, S.B., A.B. Reynolds, R.R. Vines, and J.T. Parsons. 1990. Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc. Natl. Acad. Sci. USA. 87:3328-3332.
20. Kanner, S.B., A.B. Reynolds, and J.T. Parsons. 1991. Tyrosine phosphorylation of a 120-kilodalton pp60src substrate upon epidermal growth factor and platelet-derived growth factor receptor stimulation and in polyomavirus middle-T-antigen-transformed cells. Mol. Cell. Biol. 11:713-720.
21. Katoh, H., J. Aoki, Y. Yamaguchi, Y. Kitano, A. Ichikawa, and M. Negishi. 1998. Constitutively active Galpha12, Galpha13, and Galphaq induce Rho-dependent neurite retraction through different signaling pathways. J. Biol. Chem. 273:28700-28707.
22. Kim, K., A. Sirota, Y.H. Chen Yh, S.B. Jones, R. Dudek, G.W. Lanford, C. Thakore, and Q. Lu. 2002. Dendrite-like process formation and cytoskeletal remodeling regulated by delta-carenin expression. Exp. Cell Res. 275:171-184.
23. Kinnunen, T., M. Kaksonen, J. Saarinen, N. Kalkkinen, H.B. Peng, and H. Rauvala. 1998. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite ourgrowth. J. Biol. Chem. 273:10702-10708.
24. Kozma, R., S. Sarner, S. Ahmed, and L. Lim. 1997. Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17:1201-1211.
25. Larkum, M.E., J.J. Zhu, and B. Sakmann. 1999. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature. 398:338-341.
26. Lehmann, M., A. Fournier, I. Selles-Navarro, P. Dergham, A. Sebok, N. Leclerc, G. Tigyi, and L. McKerracher. 1999. Inactivation of Rho signaling pathway promotes CNS axon regeneration. J. Neurosci. 19:7537-7547.
27. 2-mediated injury of human endothelial cells. J. Biol. Chem. 275:37187-37193.
28. Lu, Q., M. Paredes, M. Medina, J. Zhou, R. Cavallo, M. Peifer, L. Orecchio, and K.S. Kosik. 1999. delta-catenin, an adhesive junction-associated protein which promotes cell scattering. J. Cell Biol. 144:519-532.
29. Lu, Q., N.K. Mukhopadhyay, J.D. Griffin, M. Paredes, M. Medina, and K.S. Kosik. 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.
30. Magie, C.R., D. Pinto-Santini, and S.M. Parkhurst. 2002. Rho1 interacts with p120cm and alpha-catenin, and regulates cadherin-based adherens junction components in Drosophila. Development. 129:3771-3782.
31. May, R.C. 2001. The Arp2/3 complex: a central regulator of the actin cytoskeleton. Cell. Mol. Life Sci. 58:1607-1626.
32. Naisbitt, S., E. Kim, J.C. Tu, B. Xiao, C. Sala, J. Valtschanoff, R.J. Weinberg, P.F. Worley, and M. Sheng. 1999. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron. 23:569-582.
33. 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.
34. Narisawa-Saito, M., A.J. Silva, T. Yamaguchi, T. Hayashi, T. Yamamoto, and H. Nawa. 1999. Growth factor-mediated Fyn signaling regulates alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor expression in rodent neocortical neurons. Proc. Natl. Acad. Sci. USA. 96:2461-2466.
35. Neumann, H., R. Schweigreiter, T. Yamashita, K. Rosenkranz, H. Wekerle, and Y.A. Barde. 2002. Tumor necrosis factor inhibits neurite outgrowth and branching of hippocampal neurons by a rho-dependent mechanism. J. Neurosci. 22:854-862.
36. Nishiki, T., S. Narumiya, N. Morii, M. Yamamoto, M. Fujiwara, Y. Kamata, G. Sakaguchi, and S. Kozaki. 1990. ADP-ribosylation of the rho/rac proteins induces growth inhibition, neurite outgrowth and acetylcholine esterase in cultured PC-12 cells. Biochem. Biophys. Res. Commun. 167:265-272.
37. Nobes, C.D., I. Lauritzen, M.G. Mattei, S. Paris, A. Hall, and P. Chardin. 1998. A new member of the Rho family, Rnd1, promotes disassembly of actin filament structures and loss of cell adhesion. J. Cell Biol. 141:187-197.
38. Noren, N.K., B.P. Liu, K. Burridge, and B. Kreft. 2000. p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150:567-580.
39. Reynolds, A.B., L. Herbert, J.L. Cleveland, S.T. Berg, and J.R. Gaut. 1992. p120, a novel substrate of protein tyrosine kinase receptors and of p60v-src, is related to cadherin-binding factors beta-carenin, plakoglobin and armadillo. Oncogene. 7:2439-2445.
40. Reynolds, A.B., J.M. Daniel, Y.Y. Mo, J. Wu, and Z. Zhang. 1996. The novel catenin p120cas binds classical cadherins and induces an unusual morphological phenotype in NIH3T3 fibroblasts. Exp. Cell Res. 225:328-337.
41. Rook, M.S., M. Lu, and K.S. Kosik. 2000. CaMKIIalpha 3′ untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 20:6385-6393.
42. Sebok, A., N. Nusser, B. Debreceni, Z. Guo, M.F. Santos, J. Szeberenyi, and G. Tigyi. 1999. Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J. Neurochem. 73:949-960.
43. Tanaka, H., T. Yamashita, M. Asada, S. Mizutani, H. Yoshikawa, and M. Tohyama. 2002. Cytoplasmic p21(Cip1/WAF1) regulates neurite remodeling by inhibiting Rho kinase activity. J. Cell Biol. 158:321-329.
44. Tigyi, G., and R. Miledi. 1992. Lysophosphatidates bound to serum albumin activate membrane currents in Xenopus oocyres and neurite retraction in PC12 pheochromocytoma cells. J. Biol. Chem. 267:21360-21367.
45. Tigyi, G., D.J. Fischer, A. Sebok, C. Yang, D.L. Dyer, and R. Miledi. 1996. Lysophospharidic acid-induced neurite retraction in PC12 cells: control by phosphoinositide-Ca2+ signaling and Rho. J. Neurochem. 66:537-548.
46. Uruno, T., J. Liu, P. Zhang, Y. Fan, C. Egile, R. Li, S.C. Mueller, and X. Zhan. 2001. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3:259-266.
47. Weaver, A.M., A.V. Karginow, A.W. Kinley, S.A. Weed, Y. Li, J.T. Parsons, and J.A. Cooper. 2001. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11:370-374.
48. Weaver, A.M., J.E. Heuser, A.V. Karginov, W.L. Lee, J.T. Parsons, and J.A. Cooper. 2002. Interaction of cortactin and N-WASp with Arp2/3 complex. Curr. Biol. 12:1270-1278.
49. Weed, S.A., A.V. Karginov, D.A. Schafer, A.M. Weaver, A.W. Kinley, J.A. Cooper, and J.T. Parsons. 2000, Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J. Cell Biol. 151:29-40.
50. Weed, S.A., and J.T. Parsons. 2001. Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene. 20:6418-6434.
51. Wu, H., and J.T. Parsons. 1993. Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell Biol. 120:1417-1426.
52. Yamada, K.M., and B. Geiger. 1997. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9:76-85.
53. Zipkin, I.D., R.M. Kindt, and C.J. Kenyon. 1997. Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell. 90:883-894.