Phosphotyrosine-dependent interaction of SHC and insulin receptor substrate 1 with the NPEY motif of the insulin receptor via a novel non-SH2 domain

Molecular and Cellular Biology

Volumn 15, Issue 5, 1995, Pages 2500-2508

  Gustafson, Thomas A ^a   Weimin, H E ^a   Craparo, Ann ^a   Schaub, Charles D ^a   O'Neill, Thomas J ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; INSULIN; INSULIN RECEPTOR; PHOSPHOTYROSINE; PROTEIN TYROSINE KINASE;

ARTICLE; AUTOPHOSPHORYLATION; BINDING SITE; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY;

SACCHAROMYCES CEREVISIAE;

EID: 0028912999     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.15.5.2500     Document Type: Article

References (65)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore. J. G. Seidman, J. A. Smith, and K. Struhl. (ed.). 1987-1993. Current protocols in molecular biology. John Wiley & Sons. New York.
2. Backer, J. M., M. G. Myers, X. J. Sun, D. J. Chin. S. E. Shoelson, M. Miralpeix, and M. F. White. 1993. Association of IRS-1 with the insulin receptor and the phosphatidylinositol 3′-kinase. J. Biol. Chem. 268:8204-8212.
3. Barford, D., A. J. Flint, and N. K. Tonks. 1994. Crystal structure of human protein tyrosine phosphatase 1B. Science 263:1397-1404.
4. Batzer, A. G., D. Rotin, J. M. Urena, E. Y. Skolnik, and J. Schlessinger. 1994. Hierarchy of binding sites for GRB-2 and SHC on the epidermal growth factor receptor. Mol. Cell. Biol. 14:5192-5201.
5. Becker, D. M., and L. Guarente. 1991. High-efficiency transformation of yeast by electroporation. Methods Enzymol. 194:182-187.
6. Blaikie, P., D. Immanuel, J. Wu, N. Li, V. Yajnik, and B. Margolis. 1994. A region of SHC distinct from the SH2 domain can bind tyrosine-phosphorylated growth factor receptors. J. Biol. Chem. 269:32031-32034.
7. Breeden, L., and K. Nasmyth. 1985. Regulation of the yeast HO gene. Cold Spring Harbor Symp. Quant. Biol. 50:643-650.
8. Breeden, L., and K. Nasmyth. 1987. Cell cycle control of the yeast HO gene: cis- and trans-acting regulators. Cell 48:389-397.
9. Campbell, K. S., E. Ogris, B. Burke, W. Su, K. R. Auger. B. J. Druker, B. S. Schaffhausen, T. M. Roberts, and D. C. Pallas. 1994. Polyoma middle tumor antigen interacts with SHC protein via the NPTY (Asn-Pro-Thr-Tyr) motif in middle tumor antigen. Proc. Natl. Acad. Sci. USA 91:6344-6348.
10. Cantley, L. C., K. R. Auger, C. Carpenter, B. Duckworth, A. Graziani, R. Kapeller, and S. Soltoff. 1991. Oncogenes and signal transduction. Cell 64:281-302.
11. Coughlin. S. R., J. A. Ecsobedo, and L. T. Williams. 1989. Role of phosphatidylinositol kinase in PDGF receptor signal transduction. Science 243:1191-1194.
12. Craparo, A., T. J. O'Neill, and T. A. Gustafson. Unpublished data.
13. Dilworth, S. M., C. E. P. Brewster, M. D. Jones, L. Lanfrancone, G. Pelicci, and P. G. Pelicci. 1994. Transformation by polyoma middle-T antigen involves the binding and phosphorylation of SHC. Nature (London) 367:87-90.
14. Ellis, L., E. Clauser, D. O. Morgan, M. Edery, R. A. Roth, and W. J. Rutter. 1986. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell 45:721-732.
15. Golemis, E. A., and R. Brent. 1992. Fused protein domains inhibit DNA binding by LexA. Mol. Cell. Biol. 12:3006-3014.
16. Gotoh, N., A. Tojo, K. Muroya, Y. Hashimoto, S. Hattori. S. Nakamura, T. Takenawa, Y. Yazaki, and M. Shibuya. 1994. Epidermal growth factor-receptor mutant lacking the autophosphorylation sites induces phosphorylation of SHC protein and SHC-GRB2/ASH association and retains mitogenic activity. Proc. Natl. Acad. Sci. USA 91:167-171.
17. Guthrie, C., and G. R. Fink. 1992. Guide to yeast genetics and molecular biology. Methods Enzymol. 194:1-774.
18. Gyuris, J., E. Golemis, H. Chertkov, and R. Brent. 1993. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 75:791-803.
19. Kahn, C. R., M. F. While, S. E. Shoelson, J. M. Backer. E. Araki, B. Cheatham, P. Csermely, F. Folli, B. J. Goldstein, P. Hiertas, P. L. Rothenberg, M. J. A. Saad, K. Siddle, X.-J. Sun, P. Wilden, K. Yamada, and S. A. Kahn. 1993. The insulin receptor and its substrate: molecular determinants of early events in insulin action. Recent Prog. Horm. Res. 48:291-339.
20. Kaplan, D. R., D. K. Morrison, G. Wong, F. McCormick, and L. T. Williams. 1990. PDGF β-receptor stimulates tyrosine phosphorylation of GAP and association of GAP with a signalling complex. Cell 61:125-133.
21. Kavanaugh, W. M., and L. T. Williams. 1994. An alternative to SH2 domains for binding to tyrosine-phosphorylated receptors. Science 266:1862-1865.
22. Kazlauskas, A., and J. Cooper. 1989. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58:1121-1133.
23. Keegan, A. D., K. Nelms, M. White, L.-M. Wang, J. H. Pierce, and W. E. Paul. 1994. An IL-4 receptor region containing an insulin receptor motif is important for IL-4-mediated IRS-1 phosphorylation and cell growth. Cell 76:811-820.
24. Koch, C. A., D. Anderson, M. F. Moran, C. Ellis, and T. Pawson. 1991. SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252:668-674.
25. Kovacina, K. S., and R. A. Roth. 1993. Identification of SHC as a substrate of the insulin receptor kinase distinct from the GAP-associated 62kDa tyrosine phosphoprotein. Biochem. Biophys. Res. Commun. 192:1303-1311.
26. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
27. Lechleider, R. J., R. M. Freeman, and B. G. Neel. 1993. Tyrosyl phosphorylation and growth factor receptor association of the human corkscrew homologue, SH-PTP2. J. Biol. Chem. 268:13434-13438.
28. Lioubin, M. N., G. M. Myles, K. Carlberg, D. Bowtell, and L. R. Rohschneider. 1994. Shc, Grb2, Sos, and a 150-kilodalton tyrosine-phosphorylated protein form complexes with Fms in hematopoietic cells. Mol. Cell. Biol. 14:5682-5691.
29. Liu, L., J. E. Damen, R. L. Cutler, and G. Krystal. 1994. Multiple cytokines stimulate the binding of a common 145-kilodalton protein to SHC at the GRB-2 recognition site of SHC. Mol. Cell. Biol. 14:6926-6935.
30. Margolis, B., S. G. Rhee, S. Felder, M. Mervic, R. Lyall, A. Levitzki, A. Ullrich, A. Zilberstein, and J. Schlessinger. 1989. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signalling. Cell 57:1101-1107.
31. Matsuguchi, T., R. Salgia, M. Hallek. M. Eder, B. Druker, T. J. Ernst, and J. D. Griffin. 1994. SHC phosphorylation in myeloid cells is regulated by granulocyte macrophage colony-stimulating factor, interleukin-3, and steel factor and is constitutively increased by p210 bcr/abl. J. Biol. Chem. 269: 5016-5021.
32. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
33. Myers, M. G., Jr., L. M. Wang, X. J. Sun, Y. Zhang, L. Yenush, J. Schlessinger, J. H. Pierce, and M. F. White. 1994. Role of IRS-1-GRB-2 complexes in insulin signaling. Mol. Cell. Biol. 14:3577-3587.
34. Nishiyama, M., and J. R. Wands. 1992. Cloning and increased expression of an insulin receptor substrate-1-like gene in human hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 183:280-285.
35. Obermeier, A., R. Lammers, K.-H. Weismuller, G. Jung, J. Schlessinger, and A. Ullrich. 1993. Identification of Trk binding sites for SHC and phosphatidylinositol 3′-kinase and formation of a multimeric signaling complex. J. Biol. Chem. 268:22963-22966.
36. Okabayashi, Y., Y. Kido, T. Okutani, Y. Sugimoto, K. Sakaguchi, and M. Kasuga. 1994. Tyrosines 1148 and 1173 of activated epidermal growth factor receptors are binding sites of SHC in intact cells. J. Biol. Chem. 269:18674-18678.
37. O'Neill, T. J., A. Craparo, and T. A. Gustafson. 1994. Characterization of an interaction between IRS-1 and the insulin receptor using the two-hybrid system. Mol. Cell. Biol. 14:6433-6442.
38. Pawson, T., and J. Schlessinger. 1993. SH2 and SH3 domains. Curr. Biol. 3:434-442.
39. Pelicci, G., L. Lanfrancone, F. Grignani, J. McGlade, F. Cavallo, G. Forni, I. Nicoletti, F. Grignani, T. Pawson, and P. G. Pelicci. 1992. A novel transforming protein (she) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93-104.
40. Prigent, S. A., and W. J. Gullick. 1994. Identification of c-erbB-3 binding sites for phosphatidylinositol 3′-kinase and SHC using an EGR receptor/c-erb-3 chimera. EMBO J. 13:2831-2841.
41. ras. Mol. Cell. Biol. 14:1575-1581.
42. Pronk, G. J., J. McGlade, G. Pelicci, T. Pawson, and J. L. Bos. 1993. Insulin-induced phosphorylation of the 46- and 52-kDa She proteins. J. Biol. Chem. 268:5748-5753.
43. Ravichandran. K. S., and S. J. Burakoff. 1994. The adapter protein SHC interacts with the interleukin-2 (IL-2) receptor upon IL-2 stimulation. J. Biol. Chem. 269:1599-1602.
44. Ravichandran, K. S., K. K. Lee, L. C. Songyang, L. C. Cantley, P. Burn, and S. J. Burakoff. 1993. Interaction of SHC with the ζ chain of the T cell receptor upon T cell activation. Science 262:902-905.
45. Sasaoka, T., B. Draznin, J. W. Leitner, W. J. Langlois, and J. M. Olefsky. 1994. She is the predominant signaling molecular coupling insulin receptors to activation of guanine nucleotide releasing factor and p21ras-GTP formation. J. Biol. Chem. 269:10734-10738.
46. Schiestl, R. H., and R. D. Gietz. 1989. High efficiency transformation of intact yeast cells using single-stranded nucleic acids as a carrier. Curr. Genet. 16:339-346.
47. Shoelson, S. E., S. Chatterjee, M. Chaudhuri, and M. F. White. 1992. YMXM motifs of IRS-1 define substrate specificity of the insulin receptor kinase. Proc. Natl. Acad. Sci. USA 89:2027-2031.
48. Skolnik, E. Y., C. H. Lee, A. Batzer, L. M. Vicentini, M. Zhou. R. Daly, M. J. Myers, Jr., J. M. Backer, A. Ullrich, M. F. White, and J. Schlessinger. 1993. The SH2/SH3 domain-containing protein GRB2 interacts with tyrosinephosphorylated IRS1 and She: implications for insulin control of ras signalling. EMBO J. 12:1929-1936.
49. Soler, C., C. V. Alvarez, L. Beguinot, and G. Carpenter. 1994. Potent SHC tyrosine phosphorylation by epidermal growth factor at low receptor density or in the absence of receptor autophosphorylation sites. Oncogene 9:2207-2215.
50. Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, B. G. Neel, R. B. Birge, J. E. Fajardo, M. M. Chou, H. Hanafusa, B. Schaffhausen, and L. C. Cantley. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
51. Songyang, Z., S. E. Shoelson, J. McGlade, P. Olivier, T. Pawson, X. R. Bustelo, M. Barbacid, H. Sabe. H. Hanafusa, T. Yi, R. Ren, D. Baltimore, S. Ratnofsky, R. A. Feldman, and L. C. Cantley. 1994. Specific motifs recognized by the SH2 domains of Csk, 3BP2, Fps/Fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14:2777-2785.
52. Stephens, R. M., D. M. Loeb, T. D. Copeland, T. Pawson, L. A. Greene, and D. R. Kaplan. 1994. Trk receptors use redundant signal transduction pathways involving SHC and PLC-γ1 to mediate NGF responses. Neuron 12: 691-705.
53. Stuckey, J. A., H. L. Schubert, E. B. Fauman, Z.-Y. Zhang, J. E. Dixon, and M. A. Saper. 1994. Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 A and the complex with tungstate. Nature (London) 370:571-575.
54. Su, X.-D., N. Taddei, M. Stefani, G. Ramponi, and P. Norlund. 1994. The crystal structure of a low-molecular-weight phosphotyrosine protein phosphatase. Nature (London) 370:575-578.
55. Sun, X. J., D. L. Crimmins, M. G. Myers, Jr., M. Miralpeix, and M. F. White. 1993. Pleiotropic insulin signals are engaged by multisite phosphorylation of IRS-1. Mol. Cell. Biol. 13:7418-7428.
56. Sun, X. J., M. Miralpeix, M. G. Myers, E. M. Glasheen, J. M. Backer, C. R. Kahn, and M. F. White. 1992. Expression and function of IRS-1 in insulin signal transmission. J. Biol. Chem. 267:22662-22672.
57. Ullrich, A., and J. Schlessinger. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61:203-212.
58. Van Horn, D. J., M. G. Myers, and J. M. Backer. 1994. Direct activation of the phosphatidylinositol 3′-kinase by the insulin receptor. J. Biol. Chem. 269:29-32.
59. Wang, L. M., A. D. Keegan, W. Li, G. E. Lienhard, S. Pacini, J. S. Gutkind, M. G. Myers, X. J. Sun, M. F. White, S. A. Aaronson, W. E. Paul, and J. H. Pierce. 1993. Common elements in interleukin 4 and insulin signaling pathways in factor-dependent hematopoietic cells. Proc. Natl. Acad. Sci. USA 90:4032-4036.
60. Wang, L.-M., M. G. Myers, X.-J. Sun, S. A. Aaronson, M. White, and J. H. Pierce. 1993. IRS-1: essential for IL-4-stimulated mitogenesis in hematopoietic cells. Science 261:1591-1594.
61. Welham, M. J., V. Duronio, K. B. Leslie, D. Bowtell, and J. W. Schrader. 1994. Multiple hemopoietins, with the exception of interleukin-4, induce modification of SHC and mSos1, but not their translocation. J. Biol. Chem. 269:21165-21176.
62. Yokote, K., S. Mori, K. Hansen, JL McGlade, T. Pawson, K. H. Heldin, and L. Claesson-Welsh. 1994. Direct interaction between Shc and the platelet-derived growth factor (5-receptor. J. Biol. Chem. 269:15337-15343.
63. Yonezawa, K., A. Ando, Y. Kaburagi, R. Yamamoto-Honda, T. Kitamura, K. Hara, M. Nakafuku, Y. Okabayashi, T. Kadowaki, Y. Kaziro, and M. Kasuga. 1994. Signal transduction pathways from insulin receptors to ras: analysis by mutant insulin receptors. J. Biol. Chem. 269:4634-4640.
64. Zervos, A. S., J. Gyuris, and R. Brent. 1993. Mxi1, a protein that specifically interacts with max to bind myc-max recognition sites. Cell 72:223-232.
65. Zhu, X., K.-L. Suen, M. Barbacid, J. B. Bolen, and J. Fargnoli. 1994. Interleukin-2-induced phosphorylation of SHC proteins correlates with factor-dependent T cell proliferation. J. Biol. Chem. 269:5518-5522.