Prevalence, Specificity and Determinants of Lipid-Interacting PDZ Domains from an In-Cell Screen and In Vitro Binding Experiments

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Ivarsson, Ylva ^a,f   Wawrzyniak, Anna Maria ^a   Kashyap, Rudra ^a,b,c,d,e   Polanowska, Jolanta ^b,c,d,e   Betzi, Stéphane ^b,c,d,e   Lembo, Frédérique ^b,c,d,e   Vermeiren, Elke ^a   Chiheb, Driss ^a   Lenfant, Nicolas ^b,c,d,e   Morelli, Xavier ^b,c,d,e   Borg, Jean Paul ^b,c,d,e   Reboul, Jérôme ^b,c,d,e   Zimmermann, Pascale ^a,b,c,d,e  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b AIX MARSEILLE UNIVERSITY   (France)

^c INSTITUT PAOLI CALMETTES   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e CNRS   (France)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PDZ PROTEIN; PHOSPHATIDYLINOSITIDE;

ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID ANALYSIS; PDZ DOMAIN; PHOSPHORYLATION; PREDICTION; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CELL LINE, TUMOR; GENES, REPORTER; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; IMMUNOBLOTTING; KINETICS; LIGANDS; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PDZ DOMAINS; PEPTIDES; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE; SYNTENINS;

EID: 84873513075     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054581     Document Type: Article

References (60)

1. Good MC, Zalatan JG, Lim WA, (2011) Scaffold proteins: hubs for controlling the flow of cellular information. Science 332: 680-686.
2. Luck K, Charbonnier S, Trave G, (2012) The emerging contribution of sequence context to the specificity of protein interactions mediated by PDZ domains. FEBS Lett 586: 2648-2661.
3. te Velthuis AJ, Sakalis PA, Fowler DA, Bagowski CP, (2011) Genome-wide analysis of PDZ domain binding reveals inherent functional overlap within the PDZ interaction network. PLoS One 6: e16047.
4. Cho KO, Hunt CA, Kennedy MB, (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9: 929-942.
5. Kim E, Niethammer M, Rothschild A, Jan YN, Sheng M, (1995) Clustering of Shaker-type K+ channels by interaction with a family of membrane-associated guanylate kinases. Nature 378: 85-88.
6. Woods DF, Bryant PJ, (1993) ZO-1, DlgA and PSD-95/SAP90: homologous proteins in tight, septate and synaptic cell junctions. Mech Dev 44: 85-89.
7. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH, (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269: 1737-1740.
8. Niethammer M, Kim E, Sheng M, (1996) Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J Neurosci 16: 2157-2163.
9. Hillier BJ, Christopherson KS, Prehoda KE, Bredt DS, Lim WA, (1999) Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex. Science 284: 812-815.
10. Xu XZ, Choudhury A, Li X, Montell C, (1998) Coordination of an array of signaling proteins through homo- and heteromeric interactions between PDZ domains and target proteins. J Cell Biol 142: 545-555.
11. Ivarsson Y, (2012) Plasticity of PDZ domains in ligand recognition and signaling. FEBS Lett 586: 2638-2647.
12. Mortier E, Wuytens G, Leenaerts I, Hannes F, Heung MY, et al. (2005) Nuclear speckles and nucleoli targeting by PIP2-PDZ domain interactions. EMBO J 24: 2556-2565.
13. Zimmermann P, Meerschaert K, Reekmans G, Leenaerts I, Small JV, et al. (2002) PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol Cell 9: 1215-1225.
14. Balla T, Szentpetery Z, Kim YJ, (2009) Phosphoinositide signaling: new tools and insights. Physiology (Bethesda) 24: 231-244.
15. Di Paolo G, De Camilli P, (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657.
16. Barlow CA, Laishram RS, Anderson RA, (2010) Nuclear phosphoinositides: a signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol 20: 25-35.
17. Irvine RF, (2003) Nuclear lipid signalling. Nat Rev Mol Cell Biol 4: 349-360.
18. Kutateladze TG, (2010) Translation of the phosphoinositide code by PI effectors. Nat Chem Biol 6: 507-513.
19. Lambaerts K, Van Dyck S, Mortier E, Ivarsson Y, Degeest G, et al. (2012) Syntenin, a syndecan adaptor and an Arf6 phosphatidylinositol 4,5-bisphosphate effector, is essential for epiboly and gastrulation cell movements in zebrafish. J Cell Sci 125: 1129-1140.
20. Zimmermann P, Zhang Z, Degeest G, Mortier E, Leenaerts I, et al. (2005) Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev Cell 9: 377-388.
21. Wu H, Feng W, Chen J, Chan LN, Huang S, et al. (2007) PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol Cell 28: 886-898.
22. Chen Y, Sheng R, Kallberg M, Silkov A, Tun MP, et al. (2012) Genome-wide functional annotation of dual-specificity protein- and lipid-binding modules that regulate protein interactions. Mol Cell 46: 226-237.
23. Krojer T, Sawa J, Schafer E, Saibil HR, Ehrmann M, et al. (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453: 885-890.
24. Meerschaert K, Bruyneel E, De Wever O, Vanloo B, Boucherie C, et al. (2007) The tandem PDZ domains of syntenin promote cell invasion. Exp Cell Res 313: 1790-1804.
25. Pan L, Wu H, Shen C, Shi Y, Jin W, et al. (2007) Clustering and synaptic targeting of PICK1 requires direct interaction between the PDZ domain and lipid membranes. EMBO J 26: 4576-4587.
26. Meerschaert K, Tun MP, Remue E, De Ganck A, Boucherie C, et al. (2009) The PDZ2 domain of zonula occludens-1 and-2 is a phosphoinositide binding domain. Cell Mol Life Sci 66: 3951-3966.
27. Ivarsson Y, Wawrzyniak AM, Wuytens G, Kosloff M, Vermeiren E, et al. (2011) Cooperative phosphoinositide and peptide binding by PSD-95/discs large/ZO-1 (PDZ) domain of polychaetoid, Drosophila zonulin. J Biol Chem 286: 44669-44678.
28. Wawrzyniak AM, Vermeiren E, Zimmermann P, Ivarsson Y, (2012) Extensions of PSD-95/discs large/ZO-1 (PDZ) domains influence lipid binding and membrane targeting of syntenin-1. FEBS Lett 586: 1445-1451.
29. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, et al. (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19: 4577-4588.
30. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M, (1990) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62: 317-329.
31. Arcaro A, Wymann MP, (1993) Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J 296 (Pt 2): 297-301.
32. Vlahos CJ, Matter WF, Hui KY, Brown RF, (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269: 5241-5248.
33. Jefferies HB, Cooke FT, Jat P, Boucheron C, Koizumi T, et al. (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9: 164-170.
34. Chang BH, Gujral TS, Karp ES, BuKhalid R, Grantcharova VP, et al. (2011) A systematic family-wide investigation reveals that ~30% of mammalian PDZ domains engage in PDZ-PDZ interactions. Chem Biol 18: 1143-1152.
35. Narayan K, Lemmon MA, (2006) Determining selectivity of phosphoinositide-binding domains. Methods 39: 122-133.
36. van den Bout I, Divecha N, (2009) PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J Cell Sci 122: 3837-3850.
37. Lemmon MA, Falaska M, Schlessinger J, Ferguson KM, (1997) Regulatory recruitment of signalling molecules to the cell membrane by pleckstrinhomology domains. Trends Cell Biol 7: 237-242.
38. Varnai P, Balla T, (1998) Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143: 501-510.
39. Hammond GR, Fischer MJ, Anderson KE, Holdich J, Koteci A, et al. (2012) PI4P and PI(4,5)P2 are essential but independent lipid determinants of membrane identity. Science 337: 727-730.
40. Wiedemann C, Schafer T, Burger MM, (1996) Chromaffin granule-associated phosphatidylinositol 4-kinase activity is required for stimulated secretion. EMBO J 15: 2094-2101.
41. Varnai P, Thyagarajan B, Rohacs T, Balla T, (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175: 377-382.
42. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, et al. (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273: 20121-20127.
43. Mu FT, Callaghan JM, Steele-Mortimer O, Stenmark H, Parton RG, et al. (1995) EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J Biol Chem 270: 13503-13511.
44. Keller GA, Krisans S, Gould SJ, Sommer JM, Wang CC, et al. (1991) Evolutionary conservation of a microbody targeting signal that targets proteins to peroxisomes, glyoxysomes, and glycosomes. J Cell Biol 114: 893-904.
45. Komori M, Rasmussen SW, Kiel JA, Baerends RJ, Cregg JM, et al. (1997) The Hansenula polymorpha PEX14 gene encodes a novel peroxisomal membrane protein essential for peroxisome biogenesis. EMBO J 16: 44-53.
46. Jeynov B, Lay D, Schmidt F, Tahirovic S, Just WW, (2006) Phosphoinositide synthesis and degradation in isolated rat liver peroxisomes. FEBS Lett 580: 5917-5924.
47. Michalik J, Yeoman LC, Busch H, (1981) Nucleolar localization of protein B23 (37/5.1) by immunocytochemical techniques. Life Sci 28: 1371-1379.
48. Osborne SL, Thomas CL, Gschmeissner S, Schiavo G, (2001) Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J Cell Sci 114: 2501-2511.
49. Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, et al. (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13: 677-688.
50. van Wijk E, van der Zwaag B, Peters T, Zimmermann U, Te Brinke H, et al. (2006) The DFNB31 gene product whirlin connects to the Usher protein network in the cochlea and retina by direct association with USH2A and VLGR1. Hum Mol Genet 15: 751-765.
51. Cohen AR, Woods DF, Marfatia SM, Walther Z, Chishti AH, et al. (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol 142: 129-138.
52. Chi CN, Engstrom A, Gianni S, Larsson M, Jemth P, (2006) Two conserved residues govern the salt and pH dependencies of the binding reaction of a PDZ domain. J Biol Chem 281: 36811-36818.
53. Schmid AC, Wise HM, Mitchell CA, Nussbaum R, Woscholski R, (2004) Type II phosphoinositide 5-phosphatases have unique sensitivities towards fatty acid composition and head group phosphorylation. FEBS Lett 576: 9-13.
54. Zhang X, Jefferson AB, Auethavekiat V, Majerus PW, (1995) The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase. Proc Natl Acad Sci U S A 92: 4853-4856.
55. Park WS, Heo WD, Whalen JH, O'Rourke NA, Bryan HM, et al. (2008) Comprehensive identification of PIP3-regulated PH domains from C. elegans to H. sapiens by model prediction and live imaging. Mol Cell 30: 381-392.
56. Wang CK, Pan L, Chen J, Zhang M, (2010) Extensions of PDZ domains as important structural and functional elements. Protein Cell 1: 737-751.
57. Yan J, Wen W, Xu W, Long JF, Adams ME, et al. (2005) Structure of the split PH domain and distinct lipid-binding properties of the PH-PDZ supramodule of alpha-syntrophin. EMBO J 24: 3985-3995.
58. Zimmermann P, Tomatis D, Rosas M, Grootjans J, Leenaerts I, et al. (2001) Characterization of syntenin, a syndecan-binding PDZ protein, as a component of cell adhesion sites and microfilaments. Mol Biol Cell 12: 339-350.
59. Lenfant N, Polanowska J, Bamps S, Omi S, Borg JP, et al. (2010) A genome-wide study of PDZ-domain interactions in C. elegans reveals a high frequency of non-canonical binding. BMC Genomics 11: 671.
60. Jackson SE, Fersht AR, (1991) Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30: 10428-10435.