Uncoupled binding and folding of immune signaling-related intrinsically disordered proteins

Progress in Biophysics and Molecular Biology

Volumn 106, Issue 3, 2011, Pages 525-536

  Sigalov, Alexander B ^a  

^a SignaBlok Inc   (United States)

Author keywords

Immune signaling; Intrinsically disordered proteins; Protein disorder; SCHOOL concept; Scissors cut paradox; Uncoupled folding and binding

Indexed keywords

PROTEIN;

CHEMISTRY; GENETICS; IMMUNE SYSTEM; METABOLISM; PATHOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; REVIEW; SIGNAL TRANSDUCTION;

IMMUNE SYSTEM; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEINS; SIGNAL TRANSDUCTION;

EID: 80053120529     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2011.08.005     Document Type: Review

References (87)

1. Aivazian D., Stern L.J. Phosphorylation of T cell receptor zeta is regulated by a lipid dependent folding transition. Nat. Struct. Biol. 2000, 7:1023-1026.
2. Archakov A.I., Govorun V.M., Dubanov A.V., Ivanov Y.D., Veselovsky A.V., Lewi P., Janssen P. Protein-protein interactions as a target for drugs in proteomics. Proteomics 2003, 3:380-391.
3. Arkin M. Protein-protein interactions and cancer: small molecules going in for the kill. Curr. Opin. Chem. Biol. 2005, 9:317-324.
4. Bourhis J.M., Receveur-Brechot V., Oglesbee M., Zhang X., Buccellato M., Darbon H., Canard B., Finet S., Longhi S. The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded. Protein Sci. 2005, 14:1975-1992.
5. Danielsson J., Liljedahl L., Barany-Wallje E., Sonderby P., Kristensen L.H., Martinez-Yamout M.A., Dyson H.J., Wright P.E., Poulsen F.M., Maler L., Graslund A., Kragelund B.B. The intrinsically disordered RNR inhibitor Sml1 is a dynamic dimer. Biochemistry 2008, 47:13428-13437.
6. Duchardt E., Sigalov A.B., Aivazian D., Stern L.J., Schwalbe H. Structure Induction of the T-Cell Receptor zeta-chain upon lipid binding investigated by NMR spectroscopy. Chembiochem 2007, 8:820-827.
7. Dunker A.K., Brown C.J., Lawson J.D., Iakoucheva L.M., Obradovic Z. Intrinsic disorder and protein function. Biochemistry 2002, 41:6573-6582.
8. Dunker A.K., Brown C.J., Obradovic Z. Identification and functions of usefully disordered proteins. Adv. Protein Chem. 2002, 62:25-49.
9. Dunker A.K., Lawson J.D., Brown C.J., Williams R.M., Romero P., Oh J.S., Oldfield C.J., Campen A.M., Ratliff C.M., Hipps K.W., Ausio J., Nissen M.S., Reeves R., Kang C., Kissinger C.R., Bailey R.W., Griswold M.D., Chiu W., Garner E.C., Obradovic Z. Intrinsically disordered protein. J. Mol. Graph Model. 2001, 19:26-59.
10. Dunker A.K., Silman I., Uversky V.N., Sussman J.L. Function and structure of inherently disordered proteins. Curr. Opin. Struct. Biol. 2008, 18:756-764.
11. Dyson H.J., Wright P.E. Coupling of folding and binding for unstructured proteins. Curr. Opin. Struct. Biol. 2002, 12:54-60.
12. Dyson H.J., Wright P.E. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 2004, 104:3607-3622.
13. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 2005, 6:197-208.
14. Ekiel I., Sulea T., Jansen G., Kowalik M., Minailiuc O., Cheng J., Harcus D., Cygler M., Whiteway M., Wu C. Binding the atypical RA domain of Ste50p to the unfolded Opy2p cytoplasmic tail is essential for the high-osmolarity glycerol pathway. Mol. Biol. Cell 2009, 20:5117-5126. 2793289.
15. Fernandes R.A., Yu C., Carmo A.M., Evans E.J., van der Merwe P.A., Davis S.J. What controls T cell receptor phosphorylation?. Cell 2010, 142:668-669.
16. Fletcher C.M., McGuire A.M., Gingras A.C., Li H., Matsuo H., Sonenberg N., Wagner G. 4E binding proteins inhibit the translation factor eIF4E without folded structure. Biochemistry 1998, 37:9-15.
17. Fletcher C.M., Wagner G. The interaction of eIF4E with 4E-BP1 is an induced fit to a completely disordered protein. Protein Sci. 1998, 7:1639-1642.
18. Fong J.H., Shoemaker B.A., Garbuzynskiy S.O., Lobanov M.Y., Galzitskaya O.V., Panchenko A.R. Intrinsic disorder in protein interactions: insights from a comprehensive structural analysis. PLoS Comput. Biol. 2009, 5. e1000316.
19. Gagnon E., Xu C., Yang W., Chu H.H., Call M.E., Chou J.J., Wucherpfennig K.W. Response multilayered control of T cell receptor phosphorylation. Cell 2010, 142:669-671.
20. Gerlach H., Laumann V., Martens S., Becker C.F., Goody R.S., Geyer M. HIV-1 Nef membrane association depends on charge, curvature, composition and sequence. Nat. Chem. Biol. 2010, 6:46-53.
21. Hazy E., Tompa P. Limitations of induced folding in molecular recognition by intrinsically disordered proteins. Chemphyschem 2009, 10:1415-1419.
22. Hershberger S.J., Lee S.G., Chmielewski J. Scaffolds for blocking protein-protein interactions. Curr. Top. Med. Chem. 2007, 7:928-942.
23. Iakoucheva L.M., Brown C.J., Lawson J.D., Obradovic Z., Dunker A.K. Intrinsic disorder in cell-signaling and cancer-associated proteins. J. Mol. Biol. 2002, 323:573-584.
24. Katragadda M., Alderfer J.L., Yeagle P.L. Assembly of a polytopic membrane protein structure from the solution structures of overlapping peptide fragments of bacteriorhodopsin. Biophys. J. 2001, 81:1029-1036. 1301572.
25. Keegan A.D., Paul W.E. Multichain immune recognition receptors: similarities in structure and signaling pathways. Immunol. Today 1992, 13:63-68.
26. Keppler O.T., Tibroni N., Venzke S., Rauch S., Fackler O.T. Modulation of specific surface receptors and activation sensitization in primary resting CD4+ T lymphocytes by the Nef protein of HIV-1. J. Leukoc. Biol. 2006, 79:616-627.
27. Kim W.M., Sigalov A.B., Stern L.J. Pseudo-merohedral twinning and noncrystallographic symmetry in orthorhombic crystals of SIVmac239 Nef core domain bound to different-length TCRzeta fragments. Acta Crystallogr. D Biol. Crystallogr. 2010, 66:163-175.
28. Laczko I., Hollosi M., Vass E., Hegedus Z., Monostori E., Toth G.K. Conformational effect of phosphorylation on T cell receptor/CD3 zeta-chain sequences. Biochem. Biophys. Res. Commun. 1998, 242:474-479.
29. Landon Cleavage at aspartyl-prolyl bonds. Methods Enzymol. 1977, 47:145-149.
30. Lanza D.C., Silva J.C., Assmann E.M., Quaresma A.J., Bressan G.C., Torriani I.L., Kobarg J. Human FEZ1 has characteristics of a natively unfolded protein and dimerizes in solution. Proteins 2009, 74:104-121.
31. Loregian A., Palu G. Disruption of protein-protein interactions: towards new targets for chemotherapy. J. Cell Physiol. 2005, 204:750-762.
32. Meszaros B., Tompa P., Simon I., Dosztanyi Z. Molecular principles of the interactions of disordered proteins. J. Mol. Biol. 2007, 372:549-561.
33. Meyer H.W., Richter W., Rettig W., Stumpf M. Bilayer fragments and bilayered micelles (bicelles) of dimyristoylphosphatidylglycerol (DMPG) are induced by storage in distilled water at 4 °C. Colloids Surf. A: Physicochemical Eng. Aspects 2001, 183-185:495-504.
34. Minezaki Y., Homma K., Nishikawa K. Intrinsically disordered regions of human plasma membrane proteins preferentially occur in the cytoplasmic segment. J. Mol. Biol. 2007, 368:902-913.
35. Mittag T., Orlicky S., Choy W.Y., Tang X., Lin H., Sicheri F., Kay L.E., Tyers M., Forman-Kay J.D. Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:17772-17777. 2582940.
36. Ortega E. How do multichain immune recognition receptors signal? A structural hypothesis. Mol. Immunol. 1995, 32:941-945.
37. Patil A., Nakamura H. Disordered domains and high surface charge confer hubs with the ability to interact with multiple proteins in interaction networks. FEBS Lett. 2006, 580:2041-2045.
38. Paz A., Zeev-Ben-Mordehai T., Lundqvist M., Sherman E., Mylonas E., Weiner L., Haran G., Svergun D.I., Mulder F.A., Sussman J.L., Silman I. Biophysical characterization of the unstructured cytoplasmic domain of the human neuronal adhesion protein neuroligin 3. Biophys. J. 2008, 95:1928-1944. 2483779.
39. Pitcher L.A., van Oers N.S. T-cell receptor signal transmission: who gives an ITAM?. Trends Immunol. 2003, 24:554-560.
40. Popovic M., Bella J., Zlatev V., Hodnik V., Anderluh G., Barlow P.N., Pintar A., Pongor S. The interaction of Jagged-1 cytoplasmic tail with afadin PDZ domain is local, folding-independent, and tuned by phosphorylation. J. Mol. Recognit 2011, 24:245-253.
41. Radhakrishnan I., Perez-Alvarado G.C., Dyson H.J., Wright P.E. Conformational preferences in the Ser133-phosphorylated and non-phosphorylated forms of the kinase inducible transactivation domain of CREB. FEBS Lett. 1998, 430:317-322.
42. Radhakrishnan I., Perez-Alvarado G.C., Parker D., Dyson H.J., Montminy M.R., Wright P.E. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions. Cell 1997, 91:741-752.
43. Receveur-Brechot V., Bourhis J.M., Uversky V.N., Canard B., Longhi S. Assessing protein disorder and induced folding. Proteins 2006, 62:24-45.
44. Reth M. Antigen receptor tail clue. Nature 1989, 338:383-384.
45. Richards J.P., Bachinger H.P., Goodman R.H., Brennan R.G. Analysis of the structural properties of cAMP-responsive element-binding protein (CREB) and phosphorylated CREB. J. Biol. Chem. 1996, 271:13716-13723.
46. Robinson J.A. Design of protein-protein interaction inhibitors based on protein epitope mimetics. Chembiochem 2009, 10:971-973.
47. Schaefer T.M., Bell I., Fallert B.A., Reinhart T.A. The T-cell receptor zeta chain contains two homologous domains with which simian immunodeficiency virus Nef interacts and mediates down-modulation. J. Virol. 2000, 74:3273-3283.
48. Schamel W.W., Arechaga I., Risueno R.M., van Santen H.M., Cabezas P., Risco C., Valpuesta J.M., Alarcon B. Coexistence of multivalent and monovalent TCRs explains high sensitivity and wide range of response. J. Exp. Med. 2005, 202:493-503.
49. Schrager J.A., Marsh J.W. HIV-1 Nef increases T cell activation in a stimulus-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:8167-8172.
50. Sickmeier M., Hamilton J.A., LeGall T., Vacic V., Cortese M.S., Tantos A., Szabo B., Tompa P., Chen J., Uversky V.N., Obradovic Z., Dunker A.K. DisProt: the database of disordered proteins. Nucleic Acids Res. 2007, 35:D786-D793. 1751543.
51. Sigalov A., Aivazian D., Stern L. Homooligomerization of the cytoplasmic domain of the T cell receptor zeta chain and of other proteins containing the immunoreceptor tyrosine-based activation motif. Biochemistry 2004, 43:2049-2061.
52. Sigalov A.B. Multichain immune recognition receptor signaling: different players, same game?. Trends Immunol. 2004, 25:583-589.
53. Sigalov A.B. New therapeutic strategies targeting transmembrane signal transduction in the immune system. Cell Adh Migr 2010, 4:255-267.
54. Sigalov A.B. The SCHOOL of nature. I. Transmembrane signaling. Self Nonself 2010, 1:4-39.
55. Sigalov A.B. The SCHOOL of nature: II. Protein order, disorder and oligomericity in transmembrane signaling. Self Nonself 2010, 1:89-102. 3065667.
56. Sigalov A.B. The SCHOOL of nature: III. From mechanistic understanding to novel therapies. Self Nonself 2010, 1:192-224. 3047783.
57. Sigalov A.B. The SCHOOL of nature: IV. Learning from viruses. Self Nonself 2010, 1:282-298. 3062383.
58. Sigalov A.B. Unusual biophysics of immune signaling-related intrinsically disordered proteins. Self Nonself 2010, 1:271-281. 3062382.
59. Sigalov A.B. Cells diversify transmembrane signaling through the controlled chaos of protein disorder. Self Nonself 2011, 2.
60. Sigalov A.B., Aivazian D.A., Uversky V.N., Stern L.J. Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling subunits. Biochemistry 2006, 45:15731-15739.
61. Sigalov A.B., Hendricks G.M. Membrane binding mode of intrinsically disordered cytoplasmic domains of T cell receptor signaling subunits depends on lipid composition. Biochem. Biophys. Res. Commun. 2009, 389:388-393.
62. Sigalov A.B., Kim W.M., Saline M., Stern L.J. The intrinsically disordered cytoplasmic domain of the T cell receptor zeta chain binds to the Nef protein of simian immunodeficiency virus without a disorder-to-order transition. Biochemistry 2008, 47:12942-12944.
63. Sigalov A.B., Uversky V.N. Differential occurrence of protein intrinsic disorder in the cytoplasmic signaling domains of cell receptors. Self Nonself 2011, 2:55-72.
64. Sigalov A.B., Zhuravleva A.V., Orekhov V.Y. Binding of intrinsically disordered proteins is not necessarily accompanied by a structural transition to a folded form. Biochimie 2007, 89:419-421.
65. Sillerud L.O., Larson R.S. Design and structure of peptide and peptidomimetic antagonists of protein-protein interaction. Curr. Protein Pept. Sci. 2005, 6:151-169.
66. Simmons A., Aluvihare V., McMichael A. Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 2001, 14:763-777.
67. Simon S.M., Sousa F.J., Mohana-Borges R., Walker G.C. Regulation of Escherichia coli SOS mutagenesis by dimeric intrinsically disordered umuD gene products. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1152-1157.
68. Simons K.T., Bonneau R., Ruczinski I., Baker D. Ab initio protein structure prediction of CASP III targets using ROSETTA. Proteins 1999, (Suppl. 3):171-176.
69. Simons K.T., Kooperberg C., Huang E., Baker D. Assembly of protein tertiary structures from fragments with similar local sequences using simulated annealing and Bayesian scoring functions. J. Mol. Biol. 1997, 268:209-225.
70. Simons K.T., Ruczinski I., Kooperberg C., Fox B.A., Bystroff C., Baker D. Improved recognition of native-like protein structures using a combination of sequence-dependent and sequence-independent features of proteins. Proteins 1999, 34:82-95.
71. Simons K.T., Strauss C., Baker D. Prospects for ab initio protein structural genomics. J. Mol. Biol. 2001, 306:1191-1199.
72. Singh V.K., Pacheco I., Uversky V.N., Smith S.P., MacLeod R.J., Jia Z. Intrinsically disordered human C/EBP homologous protein regulates biological activity of colon cancer cells during calcium stress. J. Mol. Biol. 2008, 380:313-326.
73. Slupsky C.M., Gentile L.N., McIntosh L.P. Assigning the NMR spectra of aromatic amino acids in proteins: analysis of two Ets pointed domains. Biochem. Cell Biol. 1998, 76:379-390.
74. Sugase K., Dyson H.J., Wright P.E. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 2007, 447:1021-1025.
75. Tomoo K., Matsushita Y., Fujisaki H., Abiko F., Shen X., Taniguchi T., Miyagawa H., Kitamura K., Miura K., Ishida T. Structural basis for mRNA Cap-Binding regulation of eukaryotic initiation factor 4E by 4E-binding protein, studied by spectroscopic, X-ray crystal structural, and molecular dynamics simulation methods. Biochim. Biophys. Acta 2005, 1753:191-208.
76. Tompa P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 2005, 579:3346-3354.
77. Tyukhtenko S., Deshmukh L., Kumar V., Lary J., Cole J., Lemmon V., Vinogradova O. Characterization of the neuron-specific L1-CAM cytoplasmic tail: naturally disordered in solution it exercises different binding modes for different adaptor proteins. Biochemistry 2008, 47:4160-4168. 2426742.
78. Uversky V.N., Dunker A.K. Biochemistry. Controlled chaos. Science 2008, 322:1340-1341.
79. Uversky V.N., Gillespie J.R., Fink A.L. Why are " natively unfolded" proteins unstructured under physiologic conditions?. Proteins 2000, 41:415-427.
80. Veselovsky A.V., Archakov A.I. Inhibitors of protein-protein interactions as potential drugs. Curr. Computer-Aided Drug Des. 2007, 3:51-58.
81. Weissenhorn W., Eck M.J., Harrison S.C., Wiley D.C. Phosphorylated T cell receptor zeta-chain and ZAP70 tandem SH2 domains form a 1:3 complex in vitro. Eur. J. Biochem. 1996, 238:440-445.
82. Wood K., Paz A., Dijkstra K., Scheek R.M., Otten R., Silman I., Sussman J.L., Mulder F.A. Backbone and side chain NMR assignments for the intrinsically disordered cytoplasmic domain of human neuroligin-3. Biomol. NMR Assign 2011.
83. Wright P.E., Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 1999, 293:321-331.
84. Wu J., Cherwinski H., Spies T., Phillips J.H., Lanier L.L. DAP10 and DAP12 form distinct, but functionally cooperative, receptor complexes in natural killer cells. J. Exp. Med. 2000, 192:1059-1068.
85. Xu C., Gagnon E., Call M.E., Schnell J.R., Schwieters C.D., Carman C.V., Chou J.J., Wucherpfennig K.W. Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif. Cell 2008, 135:702-713.
86. Zhou P., Lugovskoy A.A., McCarty J.S., Li P., Wagner G. Solution structure of DFF40 and DFF45 N-terminal domain complex and mutual chaperone activity of DFF40 and DFF45. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6051-6055.
87. Zuiderweg E.R. Mapping protein-protein interactions in solution by NMR spectroscopy. Biochemistry 2002, 41:1-7.