The PTB domain of ShcA couples receptor activation to the cytoskeletal regulator IQGAP1

EMBO Journal

Volumn 29, Issue 5, 2010, Pages 884-896

  Smith, Matthew J ^a   Hardy, W Rod ^b   Li, Guang Yao ^a   Goudreault, Marilyn ^b   Hersch, Steven ^a   Metalnikov, Pavel ^b   Starostine, Andrei ^b   Pawson, Tony ^b,c   Ikura, Mitsuhiko ^a,c  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

ErbB2; IQGAP1; Lamellipodia; PTB domain; ShcA

Indexed keywords

ADAPTOR PROTEIN; BINDING PROTEIN; CELL SURFACE RECEPTOR; CYTOSKELETON PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOTYROSINE; PROTEIN SHCA; RAS PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; HUMAN; HUMAN CELL; LAMELLIPODIUM; MASS SPECTROMETRY; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANIMALS; CALORIMETRY; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; DOGS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RAS GTPASE-ACTIVATING PROTEINS; RATS; SHC SIGNALING ADAPTOR PROTEINS;

EID: 77649337246     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.399     Document Type: Article

References (94)

1. Bargmann CI, Weinberg RA (1988) Increased tyrosine kinase activity associated with the protein encoded by the activated neu oncogene. Proc Natl Acad Sci USA 85: 5394-5398
2. Bashour AM, Fullerton AT, Hart MJ, Bloom GS (1997) IQGAP1, a Rac-and Cdc42-binding protein, directly binds and cross-links microfilaments. J Cell Biol 137: 1555-1566
3. Bates ME, Busse WW, Bertics PJ (1998) Interleukin 5 signals through Shc and Grb2 in human eosinophils. Am J Respir Cell Mol Biol 18: 75-83
4. Bensenor LB, Kan HM, Wang N, Wallrabe H, Davidson LA, Cai Y, Schafer DA, Bloom GS (2007) IQGAP1 regulates cell motility by linking growth factor signaling to actin assembly. J Cell Sci 120: 658-669
5. Blagoev B, Ong SE, Kratchmarova I, Mann M (2004) Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat Biotechnol 22: 1139-1145
6. 15N NMR by enhanced heteronuclear spectroscopy. Chem Phys Lett 69: 185-189
7. Bourguignon LY, Gilad E, Rothman K, Peyrollier K (2005) Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression. J Biol Chem 280: 11961-11972
8. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr JP (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: poly-ethylenimine. Proc Natl Acad Sci USA 92: 7297-7301
9. Charest A, Wagner J, Jacob S, McGlade CJ, Tremblay ML (1996) Phosphotyrosine-independent binding of SHC to the NPLH sequence of murine protein-tyrosine phosphatase-PEST. Evidence for extended phosphotyrosine binding/phosphotyrosine interaction domain recognition specificity. J Biol Chem 271: 8424-8429
10. Clark EA, Golub TR, Lander ES, Hynes RO (2000) Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406: 532-535
11. Collins LR, Ricketts WA, Yeh L, Cheresh D (1999) Bifurcation of cell migratory and proliferative signaling by the adaptor protein Shc. J Cell Biol 147: 1561-1568
12. Cowan KJ, Law DA, Phillips DR (2000) Identification of shc as the primary protein binding to the tyrosine-phosphorylated beta 3 subunit of alpha IIbbeta 3 during outside-in integrin platelet signaling. J Biol Chem 275: 36423-36429
13. Dankort D, Maslikowski B, Warner N, Kanno N, Kim H, Wang Z, Moran MF, Oshima RG, Cardiff RD, Muller WJ (2001) Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB2)-induced mammary tumorigenesis: implications for human breast cancer. Mol Cell Biol 21: 1540-1551
14. Dankort DL, Wang Z, Blackmore V, Moran MF, Muller WJ (1997) Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation. Mol Cell Biol 17: 5410-5425
15. 4 integrin cytoplasmic domain mediates Shc signaling to extracellular signal-regulated kinase and antagonizes formation of hemi-desmosomes. J Biol Chem 276: 1494-1502
16. Davidson D, Veillette A (2001) PTP-PEST, a scaffold protein tyrosine phosphatase, negatively regulates lymphocyte activation by targeting a unique set of substrates. EMBO J 20: 3414-3426
17. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293
18. Dong PX, Jia N, Xu ZJ, Liu YT, Li DJ, Feng YJ (2008) Silencing of IQGAP1 by shRNA inhibits the invasion of ovarian carcinoma HO-8910PM cells in vitro. J Exp Clin Cancer Res 27: 77
19. Dorsch M, Hock H, Diamantstein T (1994) Tyrosine phosphoryla-tion of Shc is induced by IL-3, IL-5 and GM-CSF. Biochem Biophys Res Commun 200: 562-568
20. Farooq A, Zeng L, Yan KS, Ravichandran KS, Zhou MM (2003) Coupling of folding and binding in the PTB domain of the signaling protein Shc. Structure 11: 905-913
21. Finlayson CA, Chappell J, Leitner JW, Goalstone ML, Garrity M, Nawaz S, Ciaraldi TP, Draznin B (2003) Enhanced insulin signaling via Shc in human breast cancer. Metabolism 52: 1606-1611
22. Forman-Kay JD, Pawson T (1999) Diversity in protein recognition by PTB domains. Curr Opin Struct Biol 9: 690-695
23. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, Iwamatsu A, Perez F, Kaibuchi K (2002) Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109: 873-885
24. Fukushima A, Hatanaka Y, Chang JW, Takamatsu M, Singh N, Iwashima M (2006) Lck couples Shc to TCR signaling. Cell Signal 18: 1182-1189
25. Ganju P, O'Bryan JP, Der C, Winter J, James IF (1998) Differential regulation of SHC proteins by nerve growth factor in sensory neurons and PC12 cells. Eur J Neurosci 10: 1995-2008
26. Gotoh N, Tojo A, Shibuya M (1996) A novel pathway from phos-phorylation of tyrosine residues 239/240 of Shc, contributing to suppress apoptosis by IL-3. EMBO J 15: 6197-6204
27. Gotoh N, Toyoda M, Shibuya M (1997) Tyrosine phosphorylation sites at amino acids 239 and 240 of Shc are involved in epidermal growth factor-induced mitogenic signaling that is distinct from Ras/mitogen-activated protein kinase activation. Mol Cell Biol 17: 1824-1831
28. Groysman M, Hornstein I, Alcover A, Katzav S (2002) Vav1 and Ly-GDI two regulators of Rho GTPases, function cooperatively as signal transducers in T cell antigen receptor-induced pathways. J Biol Chem 277: 50121-50130
29. Grzesiek S, Bax A (1993) Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins. J Biomol NMR 3: 185-204
30. Hardy WR, Li L, Wang Z, Sedy J, Fawcett J, Frank E, Kucera J, Pawson T (2007) Combinatorial ShcA docking interactions support diversity in tissue morphogenesis. Science 317: 251-256
31. Hennige AM, Lammers R, Arlt D, Hoppner W, Strack V, Niederfellner G, Seif FJ, Haring HU, Kellerer M (2000) Ret oncogene signal transduction via a IRS-2/PI 3-kinase/PKB and a SHC/Grb-2 dependent pathway: possible implication for transforming activity in NIH3T3 cells. Mol Cell Endocrinol 167: 69-76
32. 2+/ calmodulin and Cdc42 signaling. J Biol Chem 274: 464-470
33. Hunt AE, Lali FV, Lord JD, Nelson BH, Miyazaki T, Tracey KJ, Foxwell BM (1999) Role of interleukin (IL)-2 receptor beta-chain subdomains and Shc in p38 mitogen-activated protein (MAP) kinase and p54 MAP kinase (stress-activated protein kinase/c-Jun N-terminal kinase) activation. IL-2-driven proliferation is independent of p38 and p54 MAP kinase activation. J Biol Chem 274: 7591-7597
34. Ikura M, Kay LE, Bax A (1990) A novel approach for sequential assignment of 1H, 13C, and 15N spectra of proteins: hetero-nuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29: 4659-4667
35. Jadeski L, Mataraza JM, Jeong HW, Li Z, Sacks DB (2008) IQGAP1 stimulates proliferation and enhances tumorigenesis of human breast epithelial cells. J Biol Chem 283: 1008-1017
36. Johnson BA (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol Biol 278: 313-352
37. Johnson M, Sharma M, Henderson BR (2009) IQGAP1 regulation and roles in cancer. Cell Signal 21: 1471-1478
38. Khoury H, Dankort DL, Sadekova S, Naujokas MA, Muller WJ, Park M (2001) Distinct tyrosine autophosphorylation sites mediate induction of epithelial mesenchymal like transition by an activated ErbB2/Neu receptor. Oncogene 20: 788-799
39. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M (2005) Mechanism of divergent growth factor effects in mesench-ymal stem cell differentiation. Science 308: 1472-1477
40. Kurella VB, Richard JM, Parke CL, Lecour Jr LF, Bellamy HD, Worthylake DK (2009) Crystal structure of the GAP-related domain from IQGAP1. J Biol Chem 284: 14857-14865
41. Kuroda S, Fukata M, Kobayashi K, Nakafuku M, Nomura N, Iwamatsu A, Kaibuchi K (1996) Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J Biol Chem 271: 23363-23367
42. Kuroda S, Fukata M, Nakagawa M, Fujii K, Nakamura T, Ookubo T, Izawa I, Nagase T, Nomura N, Tani H, Shoji I, Matsuura Y, Yonehara S, Kaibuchi K (1998) Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 281: 832-835
43. Kuroda S, Fukata M, Nakagawa M, Kaibuchi K (1999) Cdc42, Rac1, and their effector IQGAP1 as molecular switches for cadherin-mediated cell-cell adhesion. Biochem Biophys Res Commun 262: 1-6
44. Kurokawa K, Itoh RE, Yoshizaki H, Nakamura YO, Matsuda M (2004) Coactivation of Rac1 and Cdc42 at lamellipodia and membrane ruffles induced by epidermal growth factor. Mol Biol Cell 15: 1003-1010
45. Lai KM, Olivier JP, Gish GD, Henkemeyer M, McGlade J, Pawson T (1995) A Drosophila shc gene product is implicated in signaling by the DER receptor tyrosine kinase. Mol Cell Biol 15: 4810-4818
46. Lai KM, Pawson T (2000) The ShcA phosphotyrosine docking protein sensitizes cardiovascular signaling in the mouse embryo. Genes Dev 14: 1132-1145
47. Le Clainche C, Schlaepfer D, Ferrari A, Klingauf M, Grohmanova K, Veligodskiy A, Didry D, Le D, Egile C, Carlier MF, Kroschewski R (2007) IQGAP1 stimulates actin assembly through the N-WASP-ARP2/3 pathway. J Biol Chem 282: 426-435
48. Li H, Koshiba S, Hayashi F, Tochio N, Tomizawa T, Kasai T, Yabuki T, Motoda Y, Harada T, Watanabe S, Inoue M, Hayashizaki Y, Tanaka A, Kigawa T, Yokoyama S (2008) Structure of the C-terminal phosphotyrosine interaction domain of Fe65L1 complexed with the cytoplasmic tail of amyloid precursor protein reveals a novel peptide-binding mode. J Biol Chem 283: 27165-27178
49. Li SC, Zwahlen C, Vincent SJ, McGlade CJ, Kay LE, Pawson T, Forman-Kay JD (1998) Structure of a Numb PTB domain-peptide complex suggests a basis for diverse binding specificity. Nat Struct Biol 5: 1075-1083
50. Lotti LV, Lanfrancone L, Migliaccio E, Zompetta C, Pelicci G, Salcini AE, Falini B, Pelicci PG, Torrisi MR (1996) Shc proteins are localized on endoplasmic reticulum membranes and are redistributed after tyrosine kinase receptor activation. Mol Cell Biol 16: 1946-1954
51. Luttrell LM, Daaka Y, Della Rocca GJ, Lefkowitz RJ (1997) G protein-coupled receptors mediate two functionally distinct pathways of tyrosine phosphorylation in rat 1a fibroblasts. Shc phosphorylation and receptor endocytosis correlate with activation of Erk kinases. J Biol Chem 272: 31648-31656
52. Mainiero F, Pepe A, Wary KK, Spinardi L, Mohammadi M, Schlessinger J, Giancotti FG (1995) Signal transduction by the alpha 6 beta 4 integrin: distinct beta 4 subunit sites mediate recruitment of Shc/Grb2 and association with the cytoskeleton of hemidesmosomes. EMBO J 14: 4470-4481
53. Margolis B, Borg JP, Straight S, Meyer D (1999) The function of PTB domain proteins. Kidney Int 56: 1230-1237
54. Marone R, Hess D, Dankort D, Muller WJ, Hynes NE, Badache A (2004) Memo mediates ErbB2-driven cell motility. Nat Cell Biol 6: 515-522
55. Mataraza JM, Briggs MW, Li Z, Entwistle A, Ridley AJ, Sacks DB (2003) IQGAP1 promotes cell motility and invasion. J Biol Chem 278: 41237-41245
56. Mataraza JM, Li Z, Jeong HW, Brown MD, Sacks DB (2007) Multiple proteins mediate IQGAP1-stimulated cell migration. Cell Signal 19: 1857-1865
57. 1 Integrin interactions regulate breast cancer cell adhesion and motility. Exp Cell Res 252: 439-448
58. Meakin SO, MacDonald JI, Gryz EA, Kubu CJ, Verdi JM (1999) The signaling adapter FRS-2 competes with Shc for binding to the nerve growth factor receptor TrkA. A model for discriminating proliferation and differentiation. J Biol Chem 274: 9861-9870
59. Meyer RD, Sacks DB, Rahimi N (2008) IQGAP1-dependent signaling pathway regulates endothelial cell proliferation and angiogenesis. PLoS ONE 3: e3848
60. Motegi A, Fujimoto J, Kotani M, Sakuraba H, Yamamoto T (2004) ALK receptor tyrosine kinase promotes cell growth and neurite outgrowth. J Cell Sci 117: 3319-3329
61. Natarajan K, Berk BC (2006) Crosstalk coregulation mechanisms of G protein-coupled receptors and receptor tyrosine kinases. Methods Mol Biol 332: 51-77
62. Noritake J, Fukata M, Sato K, Nakagawa M, Watanabe T, Izumi N, Wang S, Fukata Y, Kaibuchi K (2004) Positive role of IQGAP1, an effector of Rac1, in actin-meshwork formation at sites of cell-cell contact. Mol Biol Cell 15: 1065-1076
63. Pandey A, Podtelejnikov AV, Blagoev B, Bustelo XR, Mann M, Lodish HF (2000) Analysis of receptor signaling pathways by mass spectrometry: identification of vav-2 as a substrate of the epidermal and platelet-derived growth factor receptors. Proc Natl Acad Sci USA 97: 179-184 (Pubitemid 30055804)
64. Patrussi L, Savino MT, Pellegrini M, Paccani SR, Migliaccio E, Plyte S, Lanfrancone L, Pelicci PG, Baldari CT (2005) Cooperation and selectivity of the two Grb2 binding sites of p52Shc in T-cell antigen receptor signaling to Ras family GTPases and Myc-dependent survival. Oncogene 24: 2218-2228
65. Patrussi L, Ulivieri C, Lucherini OM, Paccani SR, Gamberucci A, Lanfrancone L, Pelicci PG, Baldari CT (2007) p52Shc is required for CXCR4-dependent signaling and chemotaxis in T cells. Blood 11 0: 1730-1738
66. Pratt JC, van den Brink MR, Igras VE, Walk SF, Ravichandran KS, Burakoff SJ (1999) Requirement for Shc in TCR-mediated activation of a T cell hybridoma. J Immunol 163: 2586-2591
67. Psatha MI, Razi M, Koffer A, Moss SE, Sacks DB, Bolsover SR (2006) Targeting of calcium: calmodulin signals to the cytoskeleton by IQGAP1. Cell Calcium 41: 593-605
68. Ravichandran KS (2001) Signaling via Shc family adapter proteins. Oncogene 20: 6322-6330
69. Ravichandran KS, Lee KK, Songyang Z, Cantley LC, Burn P, Burakoff SJ (1993) Interaction of Shc with the zeta chain of the T cell receptor upon T cell activation. Science 262: 902-905
70. Ravichandran KS, Lorenz U, Shoelson SE, Burakoff SJ (1995) Interaction of Shc with Grb2 regulates association of Grb2 with mSOS. Mol Cell Biol 15: 593-600
71. Ren JG, Li Z, Crimmins DL, Sacks DB (2005) Self-association of IQGAP1: characterization and functional sequelae. J Biol Chem 280: 34548-34557
72. Ricketts WA, Rose DW, Shoelson S, Olefsky JM (1996) Functional roles of the Shc phosphotyrosine binding and Src homology 2 domains in insulin and epidermal growth factor signaling. J Biol Chem 271: 26165-26169
73. Roy M, Li Z, Sacks DB (2004) IQGAP1 binds ERK2 and modulates its activity. J Biol Chem 279: 17329-17337
74. Roy M, Li Z, Sacks DB (2005) IQGAP1 is a scaffold for mitogen-activated protein kinase signaling. Mol Cell Biol 25: 7940-7952
75. Sacks DB (2006) The role of scaffold proteins in MEK/ERK signalling. Biochem Soc Trans 34: 833-836
76. Salcini AE, McGlade J, Pelicci G, Nicoletti I, Pawson T, Pelicci PG (1994) Formation of Shc-Grb2 complexes is necessary to induce neoplastic transformation by overexpression of Shc proteins. Oncogene 9: 2827-2836
77. Sato K, Kimoto M, Kakumoto M, Horiuchi D, Iwasaki T, Tokmakov AA, Fukami Y (2000) Adaptor protein Shc undergoes transloca-tion and mediates up-regulation of the tyrosine kinase c-Src in EGF-stimulated A431 cells. Genes Cells 5: 749-764
78. Schafer B, Gschwind A, Ullrich A (2004) Multiple G-protein-coupled receptor signals converge on the epidermal growth factor receptor to promote migration and invasion. Oncogene 23: 991-999
79. Sini P, Cannas A, Koleske AJ, Di Fiore PP, Scita G (2004) Abl-dependent tyrosine phosphorylation of Sos-1 mediates growth-factor-induced Rac activation. Nat Cell Biol 6: 268-274
80. Sorkin A, McClure M, Huang F, Carter R (2000) Interaction of EGF receptor and grb2 in living cells visualized by fluorescence resonance energy transfer (FRET) microscopy. Curr Biol 10: 1395-1398
81. Stolt PC, Vardar D, Blacklow SC (2004) The dual-function disabled-1 PTB domain exhibits site independence in binding phospho-inositide and peptide ligands. Biochemistry 43: 10979-10987
82. Thomas D, Patterson SD, Bradshaw RA (1995) Src homologous and collagen (Shc) protein binds to F-actin and translocates to the cytoskeleton upon nerve growth factor stimulation in PC12 cells. J Biol Chem 270: 28924-28931
83. Uhlik MT, Temple B, Bencharit S, Kimple AJ, Siderovski DP, Johnson GL (2005) Structural and evolutionary division of phos-photyrosine binding (PTB) domains. J Mol Biol 345: 1-20
84. van der Geer P, Wiley S, Gish GD, Pawson T (1996) The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr Biol 6: 1435-1444
85. Velazquez L, Gish GD, van Der Geer P, Taylor L, Shulman J, Pawson T (2000) The shc adaptor protein forms interdependent phospho-tyrosine-mediated protein complexes in mast cells stimulated with interleukin 3. Blood 96: 132-138
86. Wang AC, Lodi PJ, Qin J, Vuister GW, Gronenborn AM, Clore GM (1994) An efficient triple-resonance experiment for proton-directed sequential backbone assignment of medium-sized proteins. J Magn Reson B 105: 196-198
87. Wary KK, Mainiero F, Isakoff SJ, Marcantonio EE, Giancotti FG (1996) The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87: 733-743
88. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K (2004) Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7: 871-883
89. Weyts FA, Li YS, van Leeuwen J, Weinans H, Chien S (2002) ERK activation and alpha v beta 3 integrin signaling through Shc recruitment in response to mechanical stimulation in human osteoblasts. J Cell Biochem 87: 85-92
90. Yamaoka-Tojo M, Ushio-Fukai M, Hilenski L, Dikalov SI, Chen YE, Tojo T, Fukai T, Fujimoto M, Patrushev NA, Wang N, Kontos CD, Bloom GS, Alexander RW (2004) IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species-dependent endothelial migration and proliferation. Circ Res 95: 276-283
91. Yan KS, Kuti M, Yan S, Mujtaba S, Farooq A, Goldfarb MP, Zhou MM (2002) FRS2 PTB domain conformation regulates interactions with divergent neurotrophic receptors. J Biol Chem 277: 17088-17094
92. Zhang B, Chernoff J, Zheng Y (1998) Interaction of Rac1 with GTPase-activating proteins and putative effectors. A comparison with Cdc42 and RhoA. J Biol Chem 273: 8776-8782
93. Zhou MM, Harlan JE, Wade WS, Crosby S, Ravichandran KS, Burakoff SJ, Fesik SW (1995a) Binding affinities of tyrosine-phosphorylated peptides to the COOH-terminal SH2 and NH2-terminal phosphotyrosine binding domains of Shc. J Biol Chem 270: 31119-31123
94. Zhou MM, Ravichandran KS, Olejniczak EF, Petros AM, Meadows RP, Sattler M, Harlan JE, Wade WS, Burakoff SJ, Fesik SW (1995b) Structure and ligand recognition of the phosphotyro-sine-binding domain of Shc. Nature 378: 584-592