Tyrosine phosphorylated Disabled 1 recruits Crk family adapter proteins

Biochemical and Biophysical Research Communications

Volumn 318, Issue 1, 2004, Pages 204-212

  Huang, Yongcheng ^a   Magdaleno, Susan ^b   Hopkins, Rachel ^a   Slaughter, Clive ^b   Curran, Tom ^b   Keshvara, Lakhu ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Crk; Dab1; MALDI TOF; Reelin; SH2; Src; Tyrosine phosphorylation

Indexed keywords

ADAPTOR PROTEIN; BINDING PROTEIN; BRAIN EXTRACT; CRK PROTEIN; DISABLED 1 PROTEIN; PHOSPHOTYROSINE; SEPHAROSE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BINDING SITES; BINDING, COMPETITIVE; BRAIN; CELL LINE; GENE EXPRESSION; HUMANS; MICE; MUTATION; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-CRK; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SRC HOMOLOGY DOMAINS; SRC-FAMILY KINASES; TRANSFECTION; TYROSINE;

EID: 1942456593     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2004.04.023     Document Type: Article

References (40)

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. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 374:1995;719-723.
3. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 26:2000;93-96.
4. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., Curran T. Reelin is a ligand for lipoprotein receptors. Neuron. 24:1999;471-479.
5. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron. 24:1999;481-489.
6. Trommsdorff M., Borg J.P., Margolis B., Herz J. Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J. Biol. Chem. 273:1998;33556-33560.
7. Howell B.W., Herrick T.M., Cooper J.A. Reelin-induced tryosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13:1999;643-648.
8. Howell B.W., Hawkes R., Soriano P., Cooper J.A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature. 389:1997;733-737.
9. Sheldon M., Rice D.S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K., Howell B.W., Cooper J.A., Goldowitz D., Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature. 389:1997;730-733.
10. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., Herz J. Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell. 97:1999;689-701.
11. Howell B.W., Gertler F.B., Cooper J.A. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J. 16:1997;121-132.
12. 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.
13. 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.
14. Bock H.H., Herz J. Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13:2003;18-26.
15. 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.
16. Rice D.S., Sheldon M., D'Arcangelo G., Nakajima K., Goldowitz D., Curran T. Disabled-1 acts downstream of Reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development. 125:1998;3719-3729.
17. Keshvara L., Magdaleno S., Benhayon D., Curran T. Cyclin-dependent kinase 5 phosphorylates disabled 1 independently of Reelin signaling. J. Neurosci. 22:2002;4869-4877.
18. Buday L., Wunderlich L., Tamas P. The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal. 14:2002;723-731.
19. Henkemeyer M., Rossi D.J., Holmyard D.P., Puri M.C., Mbamalu G., Harpal K., Shih T.S., Jacks T., Pawson T. Vascular system defects and neuronal apoptosis in mice lacking ras GTPase-activating protein. Nature. 377:1995;695-701.
20. Bladt F., Aippersbach E., Gelkop S., Strasser G.A., Nash P., Tafuri A., Gertler F.B., Pawson T. The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol. Cell. Biol. 23:2003;4586-4597.
21. 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.
22. Feller S.M. Crk family adaptors-signalling complex formation and biological roles. Oncogene. 20:2001;6348-6371.
23. 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.
24. Mayer B.J., Hamaguchi M., Hanafusa H. A novel viral oncogene with structural similarity to phospholipase C. Nature. 332:1988;272-275.
25. ten Hoeve J., Morris C., Heisterkamp N., Groffen J. Isolation and chromosomal localization of CRKL, a human crk-like gene. Oncogene. 8:1993;2469-2474.
26. Sabe H., Shoelson S.E., Hanafusa H. Possible v-Crk-induced transformation through activation of Src kinases. J. Biol. Chem. 270:1995;31219-31224.
27. Sabe H., Okada M., Nakagawa H., Hanafusa H. Activation of c-Src in cells bearing v-Crk and its suppression by Csk. Mol. Cell. Biol. 12:1992;4706-4713.
28. Birge R.B., Fajardo J.E., Mayer B.J., Hanafusa H. Tyrosine-phosphorylated epidermal growth factor receptor and cellular p130 provide high affinity binding substrates to analyze Crk-phosphotyrosine-dependent interactions in vitro. J. Biol. Chem. 267:1992;10588-10595.
29. 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.
30. 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.
31. Beffert U., Morfini G., Bock H.H., Reyna H., Brady S.T., Herz J. Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J. Biol. Chem. 277:2002;49958-49964.
32. Akagi T., Shishido T., Murata K., Hanafusa H. v-Crk activates the phosphoinositide 3-kinase/AKT pathway in transformation. Proc. Natl. Acad. Sci. USA. 97:2000;7290-7295.
33. Arnaud L., Ballif B.A., Cooper J.A. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23:2003;9293-9302.
34. Reddien P.W., Horvitz H.R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2:2000;131-136.
35. 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.
36. Tanaka S., Hattori S., Kurata T., Nagashima K., Fukui Y., Nakamura S., Matsuda M. Both the SH2 and SH3 domains of human CRK protein are required for neuronal differentiation of PC12 cells. Mol. Cell. Biol. 13:1993;4409-4415.
37. Weinstein D.E., Dobrenis K., Birge R.B. Targeted expression of an oncogenic adaptor protein v-Crk potentiates axonal growth in dorsal root ganglia and motor neurons in vivo. Brain Res. Dev. Brain Res. 116:1999;29-39.
38. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron. 41:2004;71-84.
39. 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.
40. Imaizumi T., Araki K., Miura K., Araki M., Suzuki M., Terasaki H., Yamamura K. Mutant mice lacking Crk-II caused by the gene trap insertional mutagenesis: Crk-II is not essential for embryonic development. Biochem. Biophys. Res. Commun. 266:1999;569-574.