The C2 domain of Tollip, a Toll-like receptor signalling regulator, exhibits broad preference for phosphoinositides

Biochemical Journal

Volumn 435, Issue 3, 2011, Pages 597-608

  Ankem, Gayatri ^a   Mitra, Sharmistha ^a   Sun, Furong ^a   Moreno, Anna C ^a   Chutvirasakul, Boonta ^a,b   Azurmendi, Hugo F ^a   Li, Liwu ^a   Capelluto, Daniel G S ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b SRINAKHARINWIROT UNIVERSITY   (Thailand)

Author keywords

C2 domain; Calcium; Nuclear magnetic resonance (NMR); Phosphoinositide; Toll interacting protein (Tollip); Toll like receptor (TLR)

Indexed keywords

CALCIUM ION; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; LIPOSOME; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SYNAPTOTAGMIN; TOLL LIKE RECEPTOR; TOLLIP; UNCLASSIFIED DRUG;

ARTICLE; CLONING; ENZYME ACTIVATION; ENZYME BINDING; ENZYME CONFORMATION; ENZYME STRUCTURE; FLUORESCENCE SPECTROSCOPY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; IMMUNE RESPONSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; TOLLIP C2 STRUCTURE;

CALCIUM; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETICS; MUTATION; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

EID: 79954486751     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20102160     Document Type: Article

References (47)

1. Kawai, T. and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384
2. Barton, G. M. and Kagan, J. C. (2009) A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9, 535-542
3. Bowie, A. and O'Neill, L. A. (2000) The interleukin-1 receptor/Toll-like receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. J. Leukoc. Biol. 67, 508-514
4. Frantz, S., Ertl, G. and Bauersachs, J. (2007) Mechanisms of disease: Toll-like receptors in cardiovascular disease. Nat. Clin. Pract. 4, 444-454
5. Gan, L. and Li, L. (2006) Regulations and roles of the interleukin-1 receptor associated kinases (IRAKs) in innate and adaptive immunity. Immunol. Res. 35, 295-302
6. Burns, K., Clatworthy, J., Martin, L., Martinon, F., Plumpton, C., Maschera, B., Lewis, A., Ray, K., Tschopp, J. and Volpe, F. (2000) Tollip, a new component of the IL-1RI pathway, links IRAK to the IL-1 receptor. Nat. Cell Biol. 2, 346-351
7. Zhang, G. and Ghosh, S. (2002) Negative regulation of toll-like receptor-mediated signaling by Tollip. J. Biol. Chem. 277, 7059-7065
8. Katoh, Y., Shiba, Y., Mitsuhashi, H., Yanagida, Y., Takatsu, H. and Nakayama, K. (2004) Tollip and Tom1 form a complex and recruit ubiquitin-conjugated proteins onto early endosomes. J. Biol. Chem. 279, 24435-24443
9. Yamakami, M., Yoshimori, T. and Yokosawa, H. (2003) Tom1, a VHS domaincontaining protein, interacts with tollip, ubiquitin, and clathrin. J. Biol. Chem. 278, 52865-52872
10. Brissoni, B., Agostini, L., Kropf, M., Martinon, F., Swoboda, V., Lippens, S., Everett, H., Aebi, N., Janssens, S., Meylan, E. et al. (2006) Intracellular trafficking of interleukin-1 receptor I requires Tollip. Curr. Biol. 16, 2265-2270
11. Ciarrocchi, A., D'Angelo, R., Cordiglieri, C., Rispoli, A., Santi, S., Riccio, M., Carone, S., Mancia, A. L., Paci, S., Cipollini, E. et al. (2009) Tollip is a mediator of protein sumoylation. PLoS ONE 4, e4404
12. Li, T., Hu, J. and Li, L. (2004) Characterization of Tollip protein upon lipopolysaccharide challenge. Mol. Immunol. 41, 85-92
13. Shih, S. C., Prag, G., Francis, S. A., Sutanto, M. A., Hurley, J. H. and Hicke, L. (2003) A ubiquitin-binding motif required for intramolecular monoubiquitylation, the CUE domain. EMBO J. 22, 1273-1281 (Pubitemid 36362691)
14. Prag, G., Misra, S., Jones, E. A., Ghirlando, R., Davies, B. A., Horazdovsky, B. F. and Hurley, J. H. (2003) Mechanism of ubiquitin recognition by the CUE domain of Vps9p. Cell 113, 609-620
15. Kang, R. S., Daniels, C. M., Francis, S. A., Shih, S. C., Salerno, W. J., Hicke, L. and Radhakrishnan, I. (2003) Solution structure of a CUE-ubiquitin complex reveals a conserved mode of ubiquitin binding. Cell 113, 621-630 (Pubitemid 36694187)
16. 13C resonance assignments and secondary structure of the Tollip CUE domain. Mol. Cells 30, 581-585
17. Stahelin, R. V. (2009) Lipid binding domains: more than simple lipid effectors. J. Lipid Res. 50, S299-S304
18. Cho, W. and Stahelin, R. V. (2006) Membrane binding and subcellular targeting of C2 domains. Biochim. Biophys. Acta 1761, 838-849
19. 2+ signaling pathways display functional and mechanistic diversity. Biochemistry 40, 3089-3100
20. 2+-independent C2 domains. J. Mol. Biol. 311, 837-849
21. Lindsay, A. J. and McCaffrey, M. W. (2004) The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane. J. Cell Sci. 117, 4365-4375
22. Melowic, H. R., Stahelin, R. V., Blatner, N. R., Tian, W., Hayashi, K., Altman, A. and Cho, W. (2007) Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase Cθ. J. Biol. Chem. 282, 21467-21476
23. 2+ binding to synaptotagmin 4. Nat. Struct. Mol. Biol. 11, 844-849
24. Fukuda, M., Kojima, T., Aruga, J., Niinobe, M. and Mikoshiba, K. (1995) Functional diversity of C2 domains of synaptotagmin family. Mutational analysis of inositol high polyphosphate binding domain. J. Biol. Chem. 270, 26523-26527
25. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
26. Garrett, D. S., Powers, R., Gronenborn, A. M. and Clore, G. M. (1991) A common-sense approach to peak picking in 2-dimensional, 3-dimensional, and 4-dimensional spectra using automatic computer-analysis of contour diagrams. J. Magn. Reson. 95, 214-220
27. Whitmore, L. and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32, W668-W673
28. Sreerama, N. and Woody, R. W. (2004) Computation and analysis of protein circular dichroism spectra. Methods Enzymol. 383, 318-351
29. Cheever, M. L., Sato, T. K., de Beer, T., Kutateladze, T. G., Emr, S. D. and Overduin, M. (2001) Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3, 613-618
30. Kelly, S. M., Jess, T. J. and Price, N. C. (2005) How to study proteins by circular dichroism. Biochim. Biophys. Acta 1751, 119-139
31. Guan, R., Dai, H., Tomchick, D. R., Dulubova, I., Machius, M., Sudhof, T. C. and Rizo, J. (2007) Crystal structure of the RIM1α C2B domain at 1.7 Å resolution. Biochemistry 46, 8988-8998 (Pubitemid 47237374)
32. 2+ regulation of neurotransmitter release. EMBO J. 20, 1605-1619
33. Liu, L., Song, X., He, D., Komma, C., Kita, A., Virbasius, J. V., Huang, G., Bellamy, H. D., Miki, K., Czech, M. P. and Zhou, G. W. (2006) Crystal structure of the C2 domain of class II phosphatidylinositide 3-kinase Cα. J. Biol. Chem. 281, 4254-4260
34. 2-sensing domains with different affinities for membrane binding. J. Mol. Biol. 371, 608-621
35. Stahelin, R. V., Karathanassis, D., Bruzik, K. S., Waterfield, M. D., Bravo, J., Williams, R. L. and Cho, W. (2006) Structural and membrane binding analysis of the Phox homology domain of phosphoinositide 3-kinase-C2α. J. Biol. Chem. 281, 39396-39406
36. Abreu, M. T. (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat. Rev. Immunol. 10, 131-144
37. Di Paolo, G. and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (Pubitemid 44564702)
38. 2+-dependent electrostatic switch. Neuron 18, 133-142
39. 2+/phospholipid-binding fold. Cell 80, 929-938
40. 2+ bridges the C2 membrane-binding domain of protein kinase Cα directly to phosphatidylserine. EMBO J. 18, 6329-6338
41. Therrien, C., Di Fulvio, S., Pickles, S. and Sinnreich, M. (2009) Characterization of lipid binding specificities of dysferlin C2 domains reveals novel interactions with phosphoinositides. Biochemistry 48, 2377-2384
42. Zhang, D. and Aravind, L. (2010) Identification of novel families and classification of the C2 domain superfamily elucidate the origin and evolution of membrane targeting activities in eukaryotes. Gene 469, 18-30
43. Ananthanarayanan, B., Das, S., Rhee, S. G., Murray, D. and Cho, W. (2002) Membrane targeting of C2 domains of phospholipase C-δ isoforms. J. Biol. Chem. 277, 3568-3575
44. Das, S., Dixon, J. E. and Cho, W. (2003) Membrane-binding and activation mechanism of PTEN. Proc. Natl. Acad. Sci. U.S.A. 100, 7491-7496
45. Dunn, R., Klos, D. A., Adler, A. S. and Hicke, L. (2004) The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J. Cell Biol. 165, 135-144 (Pubitemid 38649183)
46. Wiesner, S., Ogunjimi, A. A., Wang, H. R., Rotin, D., Sicheri, F., Wrana, J. L. and Forman-Kay, J. D. (2007) Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain. Cell 130, 651-662
47. Montaville, P., Coudevylle, N., Radhakrishnan, A., Leonov, A., Zweckstetter, M. and Becker, S. (2008) The PIP2 binding mode of the C2 domains of rabphilin-3A. Protein Sci. 17, 1025-1034 (Pubitemid 351749208)