Adaptor Proteins Intersectin 1 and 2 Bind Similar Proline-Rich Ligands but Are Differentially Recognized by SH2 Domain-Containing Proteins

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Novokhatska, Olga ^a   Dergai, Mykola ^a   Tsyba, Liudmyla ^a   Skrypkina, Inessa ^a   Filonenko, Valeriy ^a   Moreau, Jacques ^b   Rynditch, Alla ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

^b INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; INTERSECTIN; ISOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA; PROLINE RICH PROTEIN; PROTEIN CRK; PROTEIN FGR; PROTEIN ITSN1; PROTEIN ITSN2; PROTEIN KINASE FYN; PROTEIN SH2; PROTEIN SH3; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; HELA CELL; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID SEQUENCE; BINDING SITES; CELL LINE, TUMOR; CLATHRIN; ENDOCYTOSIS; EPIDERMAL GROWTH FACTOR; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROLINE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 84880808602     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070546     Document Type: Article

References (50)

1. Dacks JB, Field MC, (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J Cell Sci 120: 2977-2985.
2. Henne MW, Boucrot E, Meinecke M, Evergren E, Vallis Y, et al. (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Sci 328: 1281-1284.
3. Sengar AS, Wang W, Bishay J, Cohen S, Egan SE, (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J 18: 1159-1171.
4. Pucharcos C, Casas C, Nadal M, Estivill X, de la Luna S, (2001) The human intersectin genes and their spliced variants are differentially expressed. Biochim Biophys Acta 1521: 1-11.
5. Tsyba L, Nikolaienko O, Dergai O, Dergai M, Novokhatska O, et al. (2011) Intersectin multidomain adaptor proteins: Regulation of functional diversity. Gene 473: 67-75.
6. O'Bryan JP, (2010) INTERSECTINg Pathways in Cell Biology. Sci Signal 3: re10.
7. Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT, et al. (2000) Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am J Pathol 157: 277-286.
8. Cataldo AM, Petanceska S, Peterhoff CM, Terio NB, Epstein CJ, et al. (2003) App gene dosage modulates endosomal abnormalities of Alzheimer's disease in a segmental trisomy 16 mouse model of down syndrome. J Neurosci 23: 6788-6792.
9. Pucharcos C, Fuentes JJ, Casas C, de la Luna S, Alcantara S, et al. (1999) Alu-splice cloning of human Intersectin (ITSN), a putative multivalent binding protein expressed in proliferating and differentiating neurons and overexpressed in Down syndrome. Eur J Hum Genet 7: 704-712.
10. Fuentes JJ, Dierssen M, Pucharcos C, Fillat C, Casas C,et al. (1999) Application of Alu-splice PCR on chromosome 21: DSCR1 and Intersectin. J Neural Transm Suppl 57: 337-352.
11. Wilmot B, McWeeney SK, Nixon RR, Montine TJ, Laut J, et al. (2008) Translational gene mapping of cognitive decline. Neurobiol Aging 29: 524-541.
12. Hunter MP, Nelson M, Kurzer M, Wang X, Kryscio RJ, et al. (2011) Intersectin 1 contributes to phenotypes in vivo: implications for Down Syndrome. Neuroreport 22: 767-772.
13. Scappini E, Koh TW, Martin NP, O'Bryan JP, (2007) Intersectin enhances huntingtin aggregation and neurodegeneration through activation of c-Jun-NH2-terminal kinase (JNK). Hum Mol Genet 16: 1862-1871.
14. Specht K, Harbeck N, Smida J, Annecke K, Reich U, et al. (2009) Expression profiling identifies genes that predict recurrence of breast cancer after adjuvant CMF-based chemotherapy. Breast Cancer Res Treat 118: 45-56.
15. McGavin M, Badour K, Hardy LA, Kubiseski TJ, Zhang J, et al. (2001) The intersectin 2 adaptor links Wiskott Aldrich syndrome protein (WASp)-mediated actin polymerization to T cell antigen receptor endocytosis. J Exp Med 194: 1777-1787.
16. Lim CS, Seet BT, Ingham RJ, Gish G, Matskova L, et al. (2007) The K15 protein of Kaposi's sarcoma-associated herpesvirus recruits the endocytic regulator intersectin 2 through a selective SH3 domain interaction. Biochem 46: 9874-9885.
17. Asbach B, Ludwig C, Saksela K, Wagner R, (2012) Comprehensive analysis of interactions between the Src-associated protein in mitosis of 68 kDa and the human Src-homology 3 proteome. PLoS ONE 7: e38540.
18. Klein I, Predescu D, Sharma T, Knezevic I, Malik A, et al. (2009) Intersectin-2L regulates caveola endocytosis secondary to Cdc42-mediated actin polymerization. J Biol Chem 284: 25953-25961.
19. Rodriguez-Fraticelli AE, Vergarajauregui S, Eastburn DJ, Datta A, Alonso MA, et al. (2010) The Cdc42 GEF Intersectin 2 controls mitotic spindle orientation to form the lumen during epithelial morphogenesis. J Cell Biol 189: 725-738.
20. Novokhatska O, Dergai M, Houssin N, Tsyba L, Moreau J, et al. (2011) Intersectin 2 nucleotide exchange factor regulates Cdc42 activity during Xenopus early development. Biochem Biophys Res Commun 408: 663-668.
21. Irie F, Yamaguchi Y, (2002) EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5: 1117-1118.
22. Nishimura T, Yamaguchi T, Tokunaga A, Hara A, Hamaguchi T, (2006) Role of Numb in dendritic spine development with a Cdc42 GEF intersectin and EphB2. Mol Biol Cell 17: 1273-1285.
23. Pechstein A, Shupliakov O, Haucke V, (2010) Intersectin 1: a versatile actor in the synaptic vesicle cycle. Biochem Soc Trans 38: 181-186.
24. Tsyba L, Gryaznova T, Dergai O, Dergai M, Skrypkina I, et al. (2008) Alternative splicing affecting the SH3A domain controls the binding properties of intersectin 1 in neurons. Biochem Biophys Res Commun 372: 929-934.
25. Nikolaienko O, Skrypkina I, Tsyba L, Fedyshyn Y, Morderer D, et al. (2009) Intersectin 1 forms a complex with adaptor protein Ruk/CIN85 in vivo independently of epidermal growth factor stimulation. Cell Signal 21: 753-759.
26. Pucharcos C, Estvill X, de la Luna S, (2000) Intersectin 2, a new multimodular protein involved in clathrin-mediated endocytosis. FEBS Lett 478: 43-51.
27. Aranda S, Alvarez M, Turro S, Laguna A, de la Luna S, (2008) Sprouty2-mediated inhibition of fibroblast growth factor signaling is modulated by the protein kinase DYRK1A. Mol Cell Biol 28: 5899-5911.
28. Dergai O, Novokhatska O, Dergai M, Skrypkina I, Tsyba L, et al. (2010) Intersectin 1 forms complexes with SGIP1 and Reps1 in clathrin-coated pits. Biochem Biophys Res Commun 402: 408-413.
29. Colaluca IN, Tosoni D, Nuciforo P, Senic-Matuglia F, Galimberti V, et al. (2008) NUMB controls p53 tumour suppressor activity. Nat 451: 76-80.
30. Santonico E, Panni S, Falconi M, Castagnoli L, Cesareni G, (2007) Binding to DPF-motif by the POB1 EH domain is responsible for POB1-Eps15 interaction. BMC Biochem 8: 29.
31. Dergai M, Skrypkina I, Dergai O, Tsyba L, Novokhatska O, et al. (2011) Identification and characterization of a novel mammalian isoform of the endocytic adaptor ITSN1. Gene 485: 120-129.
32. Obenauer JC, Cantley LC, Yaffe MB, (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31: 3635-3641.
33. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
34. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Cryst D66: 12-21.
35. Wong KA, Wilson J, Russo A, Wang L, Okur MN, et al. (2012) Intersectin (ITSN) family of scaffolds function as molecular hubs in protein interaction networks. PLoS One 7: e36023.
36. Morderer D, Nikolaienko O, Skrypkina I, Cherkas V, Tsyba L, et al. (2012) Endocytic adaptor protein intersectin 1 forms a complex with microtubule stabilizer STOP in neurons. Gene 505: 360-364.
37. Dergai O, Dergai M, Skrypkina I, Matskova L, Tsyba L, et al. (2013) The LMP2A protein of Epstein-Barr virus regulates phosphorylation of ITSN1 and Shb adaptors by tyrosine kinases. Cell Signal 25: 33-40.
38. Larson SF, Davidson AR, (2000) The identification of conserved interactions within the SH3 domain by alignment of sequences and structures. Prot Sci 9: 2170-2180.
39. Dergai M, Tsyba L, Dergai O, Zlatskii I, Skrypkina I, et al. (2010) Microexon-based regulation of ITSN1 and Src SH3 domains specificity relies on introduction of charged amino acids into the interaction interface. Biochem Biophys Res Commun 399: 307-312.
40. Lim WA, Richards FM, Fox RO, (1994) Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nat 372: 375-379.
41. Feng S, Chen JK, Yu H, Simon JA, Schreiber SL, (1994) Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Sci 266: 1241-1247.
42. Betts MJ, Russell RB (2003) Amino acid properties and consequences of subsitutions. In: Barnes MR, Gray IC, editors. Bioinformatics for Geneticists. Wiley. 289-314.
43. Primeau M, Ben Djoudi Ouadda A, Lamarche-Vane N, (2011) Cdc42 GTPase-activating protein (CdGAP) interacts with the SH3D domain of Intersectin through a novel basic-rich motif. FEBS Let 585: 847-853.
44. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, et al. (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40: D261-270.
45. Wang LH, Rothberg KG, Anderson RG, (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol 123: 1107-1117.
46. Ahmad KF, Lim WA, (2010) The minimal autoinhibited unit of the guanine nucleotide exchange factor intersectin. PLoS ONE 5: e11291.
47. Harkiolaki M, Gilbert RJC, Jones EY, Feller SM, (2006) The C-terminal SH3 domain of CRKL as a dynamic dimerization module transiently exposing a nuclear export signal. Structure 14: 1741-1753.
48. Nishida M, Nagata K, Hachimori Y, Horiuchi M, Ogura K, et al. (2001) Novel recognition mode between Vav and Grb2 SH3 domains. EMBO J 20: 2995-3007.
49. Huang PH, Mukasa A, Bonavia R, Flynn RA, Brewer ZE, et al. (2007) Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc Natl Acad Sci USA 104: 12867-12872.
50. Neduva V, Russell RB, (2005) Linear motifs: Evolutionary interaction switches. FEBS Lett 579: 3342-3345.