Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons

Current Biology

Volumn 14, Issue 7, 2004, Pages 606-610

  Ballif, Bryan A ^a,c   Arnaud, Lionel ^a,d   Arthur, William T ^a   Guris, Deborah ^b   Imamoto, Akira ^b   Cooper, Jonathan A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SERONO PHARMACEUTICAL RES INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CRK LIKE PROTEIN; DAB1 PROTEIN, MOUSE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; NUCLEAR PROTEIN; RAP1 PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AFFINITY CHROMATOGRAPHY; ANIMAL; ARTICLE; BACULOVIRUS; CELL CULTURE; COMPARATIVE STUDY; DRUG EFFECT; ENZYME ACTIVATION; GENE VECTOR; GENETIC TRANSFECTION; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MOUSE; NERVE CELL; PHOSPHORYLATION; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SERODIAGNOSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BACULOVIRIDAE; BLOTTING, WESTERN; CELL ADHESION MOLECULES, NEURONAL; CELLS, CULTURED; CHROMATOGRAPHY, AFFINITY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; EXTRACELLULAR MATRIX PROTEINS; GENETIC VECTORS; GUANINE NUCLEOTIDE-RELEASING FACTOR 2; MASS SPECTROMETRY; MICE; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; PHOSPHORYLATION; PRECIPITIN TESTS; RAP1 GTP-BINDING PROTEINS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; TRANSFECTION;

ANIMALIA; UNIDENTIFIED BACULOVIRUS; VERTEBRATA;

EID: 1842715852     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2004.03.038     Document Type: Article

References (46)

1. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24:2001;1005-1039.
2. Gupta A., Tsai L.H., Wynshaw-Boris A. Life is a journey. a genetic look at neocortical development Nat. Rev. Genet. 3:2002;342-355.
3. Howell B.W., Herrick T.M., Hildebrand J.D., Zhang Y., Cooper J.A. Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr. Biol. 10:2000;877-885.
4. Arnaud L., Ballif B.A., Forster E., Cooper J.A. Fyn tyrosine kinase is a critical regulator of Disabled-1 during brain development. Curr. Biol. 13:2003;9-17.
5. Bock H.H., Herz J. Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13:2003;18-26.
6. Feller S.M. Crk family adaptors-signalling complex formation and biological roles. Oncogene. 20:2001;6348-6371.
7. Ichiba T., Hashimoto Y., Nakaya M., Kuraishi Y., Tanaka S., Kurata T., Mochizuki N., Matsuda M. Activation of C3G guanine nucleotide exchange factor for Rap1 by phosphorylation of tyrosine 504. J. Biol. Chem. 274:1999;14376- 14381.
8. Gotoh T., Hattori S., Nakamura S., Kitayama H., Noda M., Takai Y., Kaibuchi K., Matsui H., Hatase O., Takahashi H.et al. Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol. Cell. Biol. 15:1995;6746-6753.
9. Tanaka S., Morishita T., Hashimoto Y., Hattori S., Nakamura S., Shibuya M., Matuoka K., Takenawa T., Kurata T., Nagashima K.et al. C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA. 91:1994;3443-3447.
10. Knudsen B.S., Feller S.M., Hanafusa H. Four proline-rich sequences of the guanine-nucleotide exchange factor C3G bind with unique specificity to the first Src homology 3 domain of Crk. J. Biol. Chem. 269:1994;32781-32787.
11. Stork P.J. Does Rap1 deserve a bad Rap? Trends Biochem. Sci. 28:2003;267-275.
12. Caron E. Cellular functions of the Rap1 GTP-binding protein. a pattern emerges J. Cell Sci. 116:2003;435-440.
13. Voss A.K., Gruss P., Thomas T. The guanine nucleotide exchange factor C3G is necessary for the formation of focal adhesions and vascular maturation. Development. 130:2003;355-367.
14. Ohba Y., Ikuta K., Ogura A., Matsuda J., Mochizuki N., Nagashima K., Kurokawa K., Mayer B.J., Maki K., Miyazaki J.et al. Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20:2001;3333-3341.
15. Herrick T.M., Cooper J.A. A hypomorphic allele of dab1 reveals regional differences in reelin-Dab1 signaling during brain development. Development. 129:2002;787-796.
16. Howell B.W., Herrick T.M., Cooper J.A. Reelin-induced tyrosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13:1999;643-648.
17. Feller S.M., Knudsen B., Hanafusa H. c-Abl kinase regulates the protein binding activity of c-Crk. EMBO J. 13:1994;2341-2351.
18. Rosen M.K., Yamazaki T., Gish G.D., Kay C.M., Pawson T., Kay L.E. Direct demonstration of an intramolecular SH2-phosphotyrosine interaction in the Crk protein. Nature. 374:1995;477-479.
19. Abassi Y.A., Vuori K. Tyrosine 221 in Crk regulates adhesion-dependent membrane localization of Crk and Rac and activation of Rac signaling. EMBO J. 21:2002;4571-4582.
20. Senechal K., Heaney C., Druker B., Sawyers C.L. Structural requirements for function of the Crkl adapter protein in fibroblasts and hematopoietic cells. Mol. Cell. Biol. 18:1998;5082-5090.
21. Okada S., Matsuda M., Anafi M., Pawson T., Pessin J.E. Insulin regulates the dynamic balance between Ras and Rap1 signaling by coordinating the assembly states of the Grb2-SOS and CrkII-C3G complexes. EMBO J. 17:1998;2554-2565.
22. Pawson T., Scott J.D. Signaling through scaffold, anchoring, and adaptor proteins. Science. 278:1997;2075-2080.
23. Keshvara L., Benhayon D., Magdaleno S., Curran T. Identification of reelin-induced sites of tyrosyl phosphorylation on disabled 1. J. Biol. Chem. 276:2001;16008-16014.
24. Songyang Z., Shoelson S.E., Chaudhuri M., Gish G., Pawson T., Haser W.G., King F., Roberts T., Ratnofsky S., Lechleider R.J.et al. SH2 domains recognize specific phosphopeptide sequences. Cell. 72:1993;767-778.
25. de Jong R., van Wijk A., Heisterkamp N., Groffen J. C3G is tyrosine-phosphorylated after integrin-mediated cell adhesion in normal but not in Bcr/Abl expressing cells. Oncogene. 17:1998;2805-2810.
26. Ling L., Zhu T., Lobie P.E. Src-CrkII-C3G-dependent activation of Rap1 switches growth hormone-stimulated p44/42 MAP kinase and JNK/SAPK activities. J. Biol. Chem. 278:2003;27301-27311.
27. Franke B., Akkerman J.W., Bos J.L. Rapid Ca2+-mediated activation of Rap1 in human platelets. EMBO J. 16:1997;252-259.
28. del Pozo M.A., Price L.S., Alderson N.B., Ren X.D., Schwartz M.A. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2000;2008-2014.
29. Cook S.J., Rubinfeld B., Albert I., McCormick F. RapV12 antagonizes Ras-dependent activation of ERK1 and ERK2 by LPA and EGF in Rat-1 fibroblasts. EMBO J. 12:1993;3475-3485.
30. Vossler M.R., Yao H., York R.D., Pan M.G., Rim C.S., Stork P.J. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell. 89:1997;73-82.
31. Ballif B.A., Arnaud L., Cooper J.A. Tyrosine phosphorylation of disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Brain Res. Mol. Brain Res. 117:2003;152-159.
32. Li L., Okura M., Imamoto A. Focal adhesions require catalytic activity of Src family kinases to mediate integrin-matrix adhesion. Mol. Cell. Biol. 22:2002;1203-1217.
33. Li L., Guris D.L., Okura M., Imamoto A. Translocation of CrkL to focal adhesions mediates integrin-induced migration downstream of Src family kinases. Mol. Cell. Biol. 23:2003;2883-2892.
34. Bos J.L., de Rooij J., Reedquist K.A. Rap1 signalling. adhering to new models Nat. Rev. Mol. Cell Biol. 2:2001;369-377.
35. Uemura N., Griffin J.D. The adapter protein Crkl links Cbl to C3G after integrin ligation and enhances cell migration. J. Biol. Chem. 274:1999;37525-37532.
36. Dulabon L., Olson E.C., Taglienti M.G., Eisenhuth S., McGrath B., Walsh C.A., Kreidberg J.A., Anton E.S. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron. 27:2000;33-44.
37. Hack I., Bancila M., Loulier K., Carroll P., Cremer H. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat. Neurosci. 5:2002;939-945.
38. Ogawa M., Miyata T., Nakajima K., Yagyu K., Seike M., Ikenaka K., Yamamoto H., Mikoshiba K. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron. 14:1995;899-912.
39. Hoffarth R.M., Johnston J.G., Krushel L.A., van der Kooy D. The mouse mutation reeler causes increased adhesion within a subpopulation of early postmitotic cortical neurons. J. Neurosci. 15:1995;4838-4850.
40. Kato M., Dobyns W.B. Lissencephaly and the molecular basis of neuronal migration. Hum. Mol. Genet. 12:2003;R89-R96.
41. Toyo-oka K., Shionoya A., Gambello M.J., Cardoso C., Leventer R., Ward H.L., Ayala R., Tsai L.H., Dobyns W., Ledbetter D.et al. 14-3-3epsilon is important for neuronal migration by binding to NUDEL. a molecular explanation for Miller-Dieker syndrome Nat. Genet. 34:2003;274-285.
42. Guris D.L., Fantes J., Tara D., Druker B.J., Imamoto A. Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat. Genet. 27:2001;293-298.
43. Assadi A.H., Zhang G., Beffert U., McNeil R.S., Renfro A.L., Niu S., Quattrocchi C.C., Antalffy B.A., Sheldon M., Armstrong D.D.et al. Interaction of reelin signaling and Lis1 in brain development. Nat. Genet. 35:2003;270-276.
44. Pramatarova A., Ochalski P.G., Chen K., Gropman A., Myers S., Min K.T., Howell B.W. Nck beta interacts with tyrosine-phosphorylated disabled 1 and redistributes in Reelin-stimulated neurons. Mol. Cell. Biol. 23:2003;7210-7221.
45. Bock H.H., Jossin Y., Liu P., Forster E., May P., Goffinet A.M., Herz J. Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to Reelin signaling and is required for normal cortical lamination. J. Biol. Chem. 278:2003;38772-38779.
46. Mayer B.J., Hirai H., Sakai R. Evidence that SH2 domains promote processive phosphorylation by protein-tyrosine kinases. Curr. Biol. 5:1995;296-305.