Structural Basis for the Interaction of the Adaptor Protein Grb14 with Activated Ras

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Qamra, Rohini ^a   Hubbard, Stevan R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN GRB14; PROTEIN SH2; RAP1 PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DOWN REGULATION; HUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS P21(RAS); SRC HOMOLOGY DOMAINS;

EID: 84881510335     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072473     Document Type: Article

References (36)

1. Holt LJ, Siddle K, (2005) Grb10 and Grb14: enigmatic regulators of insulin action- and more? Biochem J 388: 393-406. doi:10.1042/BJ20050216. PubMed: 15901248.
2. Cooney GJ, Lyons RJ, Crew AJ, Jensen TE, Molero JC, et al. (2004) Improved glucose homeostasis and enhanced insulin signalling in Grb14-deficient mice. EMBO J 23: 582-593. doi:10.1038/sj.emboj.7600082. PubMed: 14749734.
3. Smith FM, Holt LJ, Garfield AS, Charalambous M, Koumanov F, et al. (2007) Mice with a disruption of the imprinted Grb10 gene exhibit altered body composition, glucose homeostasis, and insulin signaling during postnatal life. Mol Cell Biol 27: 5871-5886. doi:10.1128/MCB.02087-06. PubMed: 17562854.
4. Holt LJ, Lyons RJ, Ryan AS, Beale SM, Ward A, et al. (2009) Dual ablation of Grb10 and Grb14 in mice reveals their combined role in regulation of insulin signaling and glucose homeostasis. Mol Endocrinol 23: 1406-1414. doi:10.1210/me.2008-0386. PubMed: 19541746.
5. Shiura H, Miyoshi N, Konishi A, Wakisaka-Saito N, Suzuki R, et al. (2005) Meg1/Grb10 overexpression causes postnatal growth retardation and insulin resistance via negative modulation of the IGF1R and IR cascades. Biochem Biophys Res Commun 329: 909-916. doi:10.1016/j.bbrc.2005.02.047. PubMed: 15752742.
6. Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, et al. (2003) Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc Natl Acad Sci U S A 100: 8292-8297. doi:10.1073/pnas.1532175100. PubMed: 12829789.
7. Cariou B, Capitaine N, Le Marcis V, Vega N, Béréziat V, et al. (2004) Increased adipose tissue expression of Grb14 in several models of insulin resistance. FASEB J 18: 965-967. PubMed: 15059968.
8. Garfield AS, Cowley M, Smith FM, Moorwood K, Stewart-Cox JE, et al. (2011) Distinct physiological and behavioural functions for parental alleles of imprinted Grb10. Nature 469: 534-538. doi:10.1038/nature09651. PubMed: 21270893.
9. Blagitko N, Mergenthaler S, Schulz U, Wollmann HA, Craigen W, et al. (2000) Human GRB10 is imprinted and expressed from the paternal and maternal allele in a highly tissue- and isoform-specific fashion. Hum Mol Genet 9: 1587-1595. doi:10.1093/hmg/9.11.1587. PubMed: 10861285.
10. Béréziat V, Kasus-Jacobi A, Perdereau D, Cariou B, Girard J, et al. (2002) Inhibition of insulin receptor catalytic activity by the molecular adapter Grb14. J Biol Chem 277: 4845-4852. doi:10.1074/jbc.M106574200. PubMed: 11726652.
11. Depetris RS, Hu J, Gimpelevich I, Holt LJ, Daly RJ, et al. (2005) Structural basis for inhibition of the insulin receptor by the adaptor protein Grb14. Mol Cell 20: 325-333. doi:10.1016/j.molcel.2005.09.001. PubMed: 16246733.
12. Depetris RS, Wu J, Hubbard SR, (2009) Structural and functional studies of the Ras-associating and pleckstrin-homology domains of Grb10 and Grb14. Nat Struct Mol Biol 16: 833-839. doi:10.1038/nsmb.1642. PubMed: 19648926.
13. Young A, Lyons J, Miller AL, Phan VT, Alarcón IR, et al. (2009) Ras signaling and therapies. Adv Cancer Res 102: 1-17. doi:10.1016/S0065-230X(09)02001-6. PubMed: 19595305.
14. Lafuente EM, van Puijenbroek AA, Krause M, Carman CV, Freeman GJ, et al. (2004) RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell 7: 585-595. doi:10.1016/j.devcel.2004.07.021. PubMed: 15469846.
15. Krause M, Leslie JD, Stewart M, Lafuente EM, Valderrama F, et al. (2004) Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev Cell 7: 571-583. doi:10.1016/j.devcel.2004.07.024. PubMed: 15469845.
16. Holt LJ, Daly RJ, (2005) Adapter protein connections: the MRL and Grb7 protein families. Growth Factors 23: 193-201. doi:10.1080/08977190500196267. PubMed: 16243711.
17. Wynne JP, Wu J, Su W, Mor A, Patsoukis N, et al. (2012) Rap1-interacting adapter molecule (RIAM) associates with the plasma membrane via a proximity detector. J Cell Biol 199: 317-329. doi:10.1083/jcb.201201157. PubMed: 23045549.
18. Huang L, Hofer F, Martin GS, Kim SH, (1998) Structural basis for the interaction of Ras with RalGDS. Nat Struct Biol 5: 422-426. doi:10.1038/nsb0698-422. PubMed: 9628477.
19. Chang YC, Zhang H, Brennan ML, Wu J, (2012) Crystal structure of Lamellipodin implicates diverse functions in actin polymerization and Ras signaling. Protein Cell 4: 211-219. PubMed: 2348348223150166.
20. Nassar N, Horn G, Herrmann C, Scherer A, McCormick F, et al. (1995) The 2.2 A crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature 375: 554-560. doi:10.1038/375554a0. PubMed: 7791872.
21. Lemmon MA, Ferguson KM, (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 350: 1-18. doi:10.1042/0264-6021:3500001. PubMed: 10926821.
22. Chang YC, Zhang H, Brennan ML, Wu J, (2012) Crystal structure of Lamellipodin implicates diverse functions in actin polymerization and Ras signaling. Protein Cell.
23. Pacold ME, Suire S, Perisic O, Lara-Gonzalez S, Davis CT, et al. (2000) Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Cell 103: 931-943. doi:10.1016/S0092-8674(00)00196-3. PubMed: 11136978.
24. Bunney TD, Harris R, Gandarillas NL, Josephs MB, Roe SM, et al. (2006) Structural and mechanistic insights into ras association domains of phospholipase C epsilon. Mol Cell 21: 495-507. doi:10.1016/j.molcel.2006.01.008. PubMed: 16483931.
25. Stieglitz B, Bee C, Schwarz D, Yildiz O, Moshnikova A, et al. (2008) Novel type of Ras effector interaction established between tumour suppressor NORE1A and Ras switch II. EMBO J 27: 1995-2005. doi:10.1038/emboj.2008.125. PubMed: 18596699.
26. Nassar N, Horn G, Herrmann C, Block C, Janknecht R, et al. (1996) Ras/Rap effector specificity determined by charge reversal. Nat Struct Biol 3: 723-729. doi:10.1038/nsb0896-723. PubMed: 8756332.
27. Wigley DB, Lyall A, Hart KW, Holbrook JJ, (1987) The greater strength of arginine: carboxylate over lysine carboxylate ion pairs implications for the design of novel enzymes and drugs. Biochem Biophys Res Commun 149: 927-929. doi:10.1016/0006-291X(87)90497-9. PubMed: 3122748.
28. Filchtinski D, Sharabi O, Rüppel A, Vetter IR, Herrmann C, et al. (2010) What makes Ras an efficient molecular switch: a computational, biophysical, and structural study of Ras-GDP interactions with mutants of Raf. J Mol Biol 399: 422-435. doi:10.1016/j.jmb.2010.03.046. PubMed: 20361980.
29. Rudolph MG, Linnemann T, Grunewald P, Wittinghofer A, Vetter IR, et al. (2001) Thermodynamics of Ras/effector and Cdc42/effector interactions probed by isothermal titration calorimetry. J Biol Chem 276: 23914-23921. doi:10.1074/jbc.M011600200. PubMed: 11292826.
30. Kiel C, Selzer T, Shaul Y, Schreiber G, Herrmann C, (2004) Electrostatically optimized Ras-binding Ral guanine dissociation stimulator mutants increase the rate of association by stabilizing the encounter complex. Proc Natl Acad Sci U S A 101: 9223-9228. doi:10.1073/pnas.0401160101. PubMed: 15197281.
31. Wright LP, Philips MR, (2006) Thematic review series: lipid posttranslational modifications. CAAX Modif Membr Target Ras J Lipids Res 47: 883-891.
32. Otwinowski Z, Minor W, (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326. doi:10.1016/S0076-6879(97)76066-X.
33. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ, (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D 61: 458-464. doi:10.1107/S0907444905001617. PubMed: 15805601.
34. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60: 2126-2132. doi:10.1107/S0907444904019158. PubMed: 15572765.
35. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255. doi:10.1107/S0907444996012255. PubMed: 15299926.
36. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797. doi:10.1016/j.jmb.2007.05.022. PubMed: 17681537.