Origins of peptide selectivity and phosphoinositide binding revealed by structures of Disabled-1 PTB domain complexes

Structure

Volumn 11, Issue 5, 2003, Pages 569-579

  Stolt, Peggy C ^a   Jeon, Hyesung ^a   Song, Hyun Kyu ^b   Herz, Joachim ^c   Eck, Michael J ^b   Blacklow, Stephen C ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

ApoER2; Disabled; Lipoprotein receptor; Phosphoinositide; Reelin signaling; X ray crystallography

Indexed keywords

APOLIPOPROTEIN E; LIPOPROTEIN RECEPTOR; PHOSPHATIDYLINOSITIDE; PHOSPHOTYROSINE; REELIN; TYROSINE; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

ARTICLE; BINDING SITE; BRAIN DEVELOPMENT; CELL MEMBRANE; CELL MIGRATION; COMPLEX FORMATION; CRYSTAL STRUCTURE; NEOCORTEX; NERVE CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

MAMMALIA;

EID: 0037986355     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(03)00068-6     Document Type: Article

References (47)

1. Gertler F.B., Bennett R.L., Clark M.J., Hoffmann F.M. Drosophila abl tyrosine kinase in embryonic CNS axons. a role in axonogenesis is revealed through dosage-sensitive interactions with disabled Cell. 58:1989;103-113.
2. Gertler F.B., Hill K.K., Clark M.J., Hoffmann F.M. Dosage-sensitive modifiers of Drosophila abl tyrosine kinase function. prospero, a regulator of axonal outgrowth, and disabled, a novel tyrosine kinase substrate Genes Dev. 7:1993;441-453.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. Gotthardt M., Trommsdorff M., Nevitt M.F., Shelton J., Richardson J.A., Stockinger W., Nimpf J., Herz J. Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem. 275:2000;25616-25624.
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. Blaikie P., Immanuel D., Wu J., Li N., Yajnik V., Margolis B. A region in Shc distinct from the SH2 domain can bind tyrosine-phosphorylated growth factor receptors. J. Biol. Chem. 269:1994;32031-32034.
13. Kavanaugh W.M., Williams L.T. An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science. 266:1994;1862-1865.
14. Kavanaugh W.M., Turck C.W., Williams L.T. PTB domain binding to signaling proteins through a sequence motif containing phosphotyrosine. Science. 268:1995;1177-1179.
15. Howell B.W., Lanier L.M., Frank R., Gertler F.B., Cooper J.A. The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids. Mol. Cell. Biol. 19:1999;5179-5188.
16. Harlan J.E., Hajduk P.J., Yoon H.S., Fesik S.W. Pleckstrin homology domains bind to phosphatidylinositol 4,5-bisphosphate. Nature. 371:1994;168-170.
17. Hyvonen M., Macias M.J., Nilges M., Oschkinat H., Saraste M., Wilmanns M. Structure of the binding site for inositol phosphates in a PH domain. EMBO J. 14:1995;4676-4685.
18. Lemmon M.A., Ferguson K.M., Sigler P.B., Schlessinger J. Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc. Natl. Acad. Sci. USA. 92:1995;10472-10476.
19. Mishra S.K., Keyel P.A., Hawryluk M.J., Agostinelli N.R., Watkins S.C., Traub L.M. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21:2002;4915-4926.
20. Zhang Z., Lee C.H., Mandiyan V., Borg J.P., Margolis B., Schlessinger J., Kuriyan J. Sequence-specific recognition of the internalization motif of the Alzheimer's amyloid precursor protein by the X11 PTB domain. EMBO J. 16:1997;6141-6150.
21. Farooq A., Plotnikova O., Zeng L., Zhou M.M. Phosphotyrosine binding domains of Shc and insulin receptor substrate 1 recognize the NPXpY motif in a thermodynamically distinct manner. J. Biol. Chem. 274:1999;6114-6121.
22. Zwahlen C., Li S.C., Kay L.E., Pawson T., Forman-Kay J.D. Multiple modes of peptide recognition by the PTB domain of the cell fate determinant Numb. EMBO J. 19:2000;1505-1515.
23. Yan K.S., Kuti M., Yan S., Mujtaba S., Farooq A., Goldfarb M.P., Zhou M.M. FRS2 PTB domain conformation regulates interactions with divergent neurotrophic receptors. J. Biol. Chem. 277:2002;17088-17094.
24. Zhou M.M., Ravichandran K.S., Olejniczak E.F., Petros A.M., Meadows R.P., Sattler M., Harlan J.E., Wade W.S., Burakoff S.J., Fesik S.W. Structure and ligand recognition of the phosphotyrosine binding domain of Shc. Nature. 378:1995;584-592.
25. Li S.C., Zwahlen C., Vincent S.J., McGlade C.J., Kay L.E., Pawson T., Forman-Kay J.D. Structure of a Numb PTB domain-peptide complex suggests a basis for diverse binding specificity. Nat. Struct. Biol. 5:1998;1075-1083.
26. Eck M.J., Dhe-Paganon S., Trub T., Nolte R.T., Shoelson S.E. Structure of the IRS-1 PTB domain bound to the juxtamembrane region of the insulin receptor. Cell. 85:1996;695-705.
27. Chang D.D., Hoang B.Q., Liu J., Springer T.A. Molecular basis for interaction between Icap1 alpha PTB domain and beta 1 integrin. J. Biol. Chem. 277:2002;8140-8145.
28. 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.
29. Bock H.H., Herz J. Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13:2003;18-26.
30. Xu X.X., Yang W., Jackowski S., Rock C.O. Cloning of a novel phosphoprotein regulated by colony-stimulating factor 1 shares a domain with the Drosophila disabled gene product. J. Biol. Chem. 270:1995;14184-14191.
31. He G., Gupta S., Yi M., Michaely P., Hobbs H.H., Cohen J.C. ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin, and AP-2. J. Biol. Chem. 277:2002;44044-44049.
32. Mishra S.K., Watkins S.C., Traub L.M. The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc. Natl. Acad. Sci. USA. 99:2002;16099-16104.
33. Ferguson K.M., Lemmon M.A., Schlessinger J., Sigler P.B. Structure of the high affinity complex of inositol trisphosphate with a phospholipase C pleckstrin homology domain. Cell. 83:1995;1037-1046.
34. Ravichandran K.S., Zhou M.M., Pratt J.C., Harlan J.E., Walk S.F., Fesik S.W., Burakoff S.J. Evidence for a requirement for both phospholipid and phosphotyrosine binding via the Shc phosphotyrosine-binding domain in vivo. Mol. Cell. Biol. 17:1997;5540-5549.
35. Rameh L.E., Arvidsson A., Carraway K.L. III, Couvillon A.D., Rathbun G., Crompton A., VanRenterghem B., Czech M.P., Ravichandran K.S., Burakoff S.J.et al. A comparative analysis of the phosphoinositide binding specificity of pleckstrin homology domains. J. Biol. Chem. 272:1997;22059-22066.
36. Dhe-Paganon S., Ottinger E.A., Nolte R.T., Eck M.J., Shoelson S.E. Crystal structure of the pleckstrin homology-phosphotyrosine binding (PH-PTB) targeting region of insulin receptor substrate 1. Proc. Natl. Acad. Sci. USA. 96:1999;8378-8383.
37. 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.
38. 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.
39. Minor W., Tomchick D., Otwinowski Z. Strategies for macromolecular synchrotron crystallography. Structure. 8:2000;R105-R110.
40. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55:1999;849-861.
41. Cowtan, K.D. (1994). An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31, 34-38.
42. Perrakis A., Morris R., Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6:1999;458-463.
43. Jones T.A., Zou J.-Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47:1991;110-119.
44. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S.et al. Crystallography and NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54:1998;905-921.
45. Sali A., Blundell T.L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:1993;779-815.
46. Nicholls A., Sharp K., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins Struct. Funct. Genet. 11:1991;281-296.
47. Kraulis P. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.