Structured States of Disordered Proteins from Genomic Sequences

Cell

Volumn 167, Issue 1, 2016, Pages 158-170.e12

  Toth Petroczy, Agnes ^a   Palmedo, Perry ^a,b,c   Ingraham, John ^a   Hopf, Thomas A ^a   Berger, Bonnie ^c,d   Sander, Chris ^a   Marks, Debora S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

bioinformatics; computational biology; conformational flexibility; disorder; EVfold; Evolutionary couplings; maximum entropy; statistical physics; structure prediction

Indexed keywords

AMYLOID; INTRINSICALLY DISORDERED PROTEIN; PROTEOME;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENOMICS; HUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN POLYMERIZATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; ZINC FINGER MOTIF; CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; GENETICS; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

DIRECTED MOLECULAR EVOLUTION; GENOMICS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEOME;

EID: 84988649813     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.09.010     Document Type: Article

References (72)

1. Alexander, P.A., He, Y., Chen, Y., Orban, J., Bryan, P.N., A minimal sequence code for switching protein structure and function. Proc. Natl. Acad. Sci. USA 106 (2009), 21149–21154.
2. Bah, A., Vernon, R.M., Siddiqui, Z., Krzeminski, M., Muhandiram, R., Zhao, C., Sonenberg, N., Kay, L.E., Forman-Kay, J.D., Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch. Nature 519 (2015), 106–109.
3. Baker, J.M., Hudson, R.P., Kanelis, V., Choy, W.Y., Thibodeau, P.H., Thomas, P.J., Forman-Kay, J.D., CFTR regulatory region interacts with NBD1 predominantly via multiple transient helices. Nat. Struct. Mol. Biol. 14 (2007), 738–745.
4. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E., The Protein Data Bank. Nucleic Acids Res. 28 (2000), 235–242.
5. Brown, C.J., Johnson, A.K., Daughdrill, G.W., Comparing models of evolution for ordered and disordered proteins. Mol. Biol. Evol. 27 (2010), 609–621.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998), 905–921.
7. Cerf, C., Lippens, G., Ramakrishnan, V., Muyldermans, S., Segers, A., Wyns, L., Wodak, S.J., Hallenga, K., Homo- and heteronuclear two-dimensional NMR studies of the globular domain of histone H1: full assignment, tertiary structure, and comparison with the globular domain of histone H5. Biochemistry 33 (1994), 11079–11086.
8. Dancheck, B., Nairn, A.C., Peti, W., Detailed structural characterization of unbound protein phosphatase 1 inhibitors. Biochemistry 47 (2008), 12346–12356.
9. Daugherty, M.D., Liu, B., Frankel, A.D., Structural basis for cooperative RNA binding and export complex assembly by HIV Rev. Nat. Struct. Mol. Biol. 17 (2010), 1337–1342.
10. Dealwis, C.G., Chen, L., Brennan, C., Mandecki, W., Abad-Zapatero, C., 3-D structure of the D153G mutant of Escherichia coli alkaline phosphatase: an enzyme with weaker magnesium binding and increased catalytic activity. Protein Eng. 8 (1995), 865–871.
11. Dikic, I., Wakatsuki, S., Walters, K.J., Ubiquitin-binding domains - from structures to functions. Nat. Rev. Mol. Cell Biol. 10 (2009), 659–671.
12. Dosztányi, Z., Csizmok, V., Tompa, P., Simon, I., IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21 (2005), 3433–3434.
13. Ekeberg, M., Lövkvist, C., Lan, Y., Weigt, M., Aurell, E., Improved contact prediction in proteins: using pseudolikelihoods to infer Potts models. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 87, 2013, 012707.
14. Ferreon, A.C., Ferreon, J.C., Wright, P.E., Deniz, A.A., Modulation of allostery by protein intrinsic disorder. Nature 498 (2013), 390–394.
15. Finn, R.D., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Mistry, J., Mitchell, A.L., Potter, S.C., Punta, M., Qureshi, M., Sangrador-Vegas, A., et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44:D1 (2016), D279–D285.
16. Frederick, K.K., Michaelis, V.K., Corzilius, B., Ong, T.C., Jacavone, A.C., Griffin, R.G., Lindquist, S., Sensitivity-enhanced NMR reveals alterations in protein structure by cellular milieus. Cell 163 (2015), 620–628.
17. Fuxreiter, M., Simon, I., Friedrich, P., Tompa, P., Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. J. Mol. Biol. 338 (2004), 1015–1026.
18. Guharoy, M., Pauwels, K., Tompa, P., SnapShot: Intrinsic Structural Disorder. Cell, 161, 2015 1230–1230 e1231.
19. Hansen, J.C., Lu, X., Ross, E.D., Woody, R.W., Intrinsic protein disorder, amino acid composition, and histone terminal domains. J. Biol. Chem. 281 (2006), 1853–1856.
20. Hopf, T.A., Colwell, L.J., Sheridan, R., Rost, B., Sander, C., Marks, D.S., Three-dimensional structures of membrane proteins from genomic sequencing. Cell 149 (2012), 1607–1621.
21. Hopf, T.A., Schärfe, C.P., Rodrigues, J.P., Green, A.G., Kohlbacher, O., Sander, C., Bonvin, A.M., Marks, D.S., Sequence co-evolution gives 3D contacts and structures of protein complexes. eLife, 3, 2014, e03430.
22. Hurley, T.D., Yang, J., Zhang, L., Goodwin, K.D., Zou, Q., Cortese, M., Dunker, A.K., DePaoli-Roach, A.A., Structural basis for regulation of protein phosphatase 1 by inhibitor-2. J. Biol. Chem. 282 (2007), 28874–28883.
23. Hyman, A.A., Weber, C.A., Jülicher, F., Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30 (2014), 39–58.
24. Jayaraman, B., Crosby, D.C., Homer, C., Ribeiro, I., Mavor, D., Frankel, A.D., RNA-directed remodeling of the HIV-1 protein Rev orchestrates assembly of the Rev-Rev response element complex. eLife, 3, 2014, e04120.
25. Johnson, L.S., Eddy, S.R., Portugaly, E., Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics, 11, 2010, 431.
26. Kato, H., van Ingen, H., Zhou, B.R., Feng, H., Bustin, M., Kay, L.E., Bai, Y., Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR. Proc. Natl. Acad. Sci. USA 108 (2011), 12283–12288.
27. Kato, M., Han, T.W., Xie, S., Shi, K., Du, X., Wu, L.C., Mirzaei, H., Goldsmith, E.J., Longgood, J., Pei, J., et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149 (2012), 753–767.
28. Knowles, T.P., Vendruscolo, M., Dobson, C.M., The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 15 (2014), 384–396.
29. Koglin, A., Mofid, M.R., Löhr, F., Schäfer, B., Rogov, V.V., Blum, M.M., Mittag, T., Marahiel, M.A., Bernhard, F., Dötsch, V., Conformational switches modulate protein interactions in peptide antibiotic synthetases. Science 312 (2006), 273–276.
30. Koshland, D.E. Jr., Enzyme flexibility and enzyme action. J. Cell. Comp. Physiol. 54 (1959), 245–258.
31. Kwon, I., Kato, M., Xiang, S., Wu, L., Theodoropoulos, P., Mirzaei, H., Han, T., Xie, S., Corden, J.L., McKnight, S.L., Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell 155 (2013), 1049–1060.
32. Livesay, D.R., Kreth, K.E., Fodor, A.A., A critical evaluation of correlated mutation algorithms and coevolution within allosteric mechanisms. Methods Mol. Biol. 796 (2012), 385–398.
33. Lorenzo, A., Razzaboni, B., Weir, G.C., Yankner, B.A., Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368 (1994), 756–760.
34. Love, J.J., Li, X., Chung, J., Dyson, H.J., Wright, P.E., The LEF-1 high-mobility group domain undergoes a disorder-to-order transition upon formation of a complex with cognate DNA. Biochemistry 43 (2004), 8725–8734.
35. Marks, D.S., Colwell, L.J., Sheridan, R., Hopf, T.A., Pagnani, A., Zecchina, R., Sander, C., Protein 3D structure computed from evolutionary sequence variation. PLoS ONE, 6, 2011, e28766.
36. Marsh, J.A., Forman-Kay, J.D., Ensemble modeling of protein disordered states: experimental restraint contributions and validation. Proteins 80 (2012), 556–572.
37. Mirecka, E.A., Shaykhalishahi, H., Gauhar, A., Akgül, Ş., Lecher, J., Willbold, D., Stoldt, M., Hoyer, W., Sequestration of a β-hairpin for control of α-synuclein aggregation. Angew. Chem. Int. Ed. Engl. 53 (2014), 4227–4230.
38. 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. USA 105 (2008), 17772–17777.
39. Monod, J., Changeux, J.P., Jacob, F., Allosteric proteins and cellular control systems. J. Mol. Biol. 6 (1963), 306–329.
40. Morcos, F., Pagnani, A., Lunt, B., Bertolino, A., Marks, D.S., Sander, C., Zecchina, R., Onuchic, J.N., Hwa, T., Weigt, M., Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc. Natl. Acad. Sci. USA 108 (2011), E1293–E1301.
41. Morcos, F., Jana, B., Hwa, T., Onuchic, J.N., Coevolutionary signals across protein lineages help capture multiple protein conformations. Proc. Natl. Acad. Sci. USA 110 (2013), 20533–20538.
42. Motlagh, H.N., Wrabl, J.O., Li, J., Hilser, V.J., The ensemble nature of allostery. Nature 508 (2014), 331–339.
43. Oates, M.E., Romero, P., Ishida, T., Ghalwash, M., Mizianty, M.J., Xue, B., Dosztányi, Z., Uversky, V.N., Obradovic, Z., Kurgan, L., et al. D²P²: database of disordered protein predictions. Nucleic Acids Res. 41 (2013), D508–D516.
44. Ovchinnikov, S., Kamisetty, H., Baker, D., Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information. eLife, 3, 2014, e02030.
45. Patel, A., Lee, H.O., Jawerth, L., Maharana, S., Jahnel, M., Hein, M.Y., Stoynov, S., Mahamid, J., Saha, S., Franzmann, T.M., et al. A Liquid-to-Solid Phase Transition of the ALS Protein FUS Accelerated by Disease Mutation. Cell 162 (2015), 1066–1077.
46. Pérez, F., Granger, B.E., IPython: a system for interactive scientific computing. Comput. Sci. Eng. 9 (2007), 21–29.
47. Perutz, M.F., Stereochemistry of cooperative effects in haemoglobin. Nature 228 (1970), 726–739.
48. Rao, J.N., Jao, C.C., Hegde, B.G., Langen, R., Ulmer, T.S., A combinatorial NMR and EPR approach for evaluating the structural ensemble of partially folded proteins. J. Am. Chem. Soc. 132 (2010), 8657–8668.
49. Roque, A., Ponte, I., Arrondo, J.L., Suau, P., Phosphorylation of the carboxy-terminal domain of histone H1: effects on secondary structure and DNA condensation. Nucleic Acids Res. 36 (2008), 4719–4726.
50. Russo, A.A., Jeffrey, P.D., Patten, A.K., Massagué, J., Pavletich, N.P., Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382 (1996), 325–331.
51. Saio, T., Guan, X., Rossi, P., Economou, A., Kalodimos, C.G., Structural basis for protein antiaggregation activity of the trigger factor chaperone. Science, 344, 2014, 1250494.
52. Sambashivan, S., Liu, Y., Sawaya, M.R., Gingery, M., Eisenberg, D., Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and native-like structure. Nature 437 (2005), 266–269.
53. Schrag, J.D., Bergeron, J.J., Li, Y., Borisova, S., Hahn, M., Thomas, D.Y., Cygler, M., The Structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 8 (2001), 633–644.
54. Sickmeier, M., Hamilton, J.A., LeGall, T., Vacic, V., Cortese, M.S., Tantos, A., Szabo, B., Tompa, P., Chen, J., Uversky, V.N., et al. DisProt: the Database of Disordered Proteins. Nucleic Acids Res. 35 (2007), D786–D793.
55. Sohl, C.D., Szymanski, M.R., Mislak, A.C., Shumate, C.K., Amiralaei, S., Schinazi, R.F., Anderson, K.S., Yin, Y.W., Probing the structural and molecular basis of nucleotide selectivity by human mitochondrial DNA polymerase γ. Proc. Natl. Acad. Sci. USA 112 (2015), 8596–8601.
56. Sorenson, M.K., Ray, S.S., Darst, S.A., Crystal structure of the flagellar sigma/anti-sigma complex sigma(28)/FlgM reveals an intact sigma factor in an inactive conformation. Mol. Cell 14 (2004), 127–138.
57. Thompson, J., Baker, D., Incorporation of evolutionary information into Rosetta comparative modeling. Proteins 79 (2011), 2380–2388.
58. Tian, P., Boomsma, W., Wang, Y., Otzen, D.E., Jensen, M.H., Lindorff-Larsen, K., Structure of a functional amyloid protein subunit computed using sequence variation. J. Am. Chem. Soc. 137 (2015), 22–25.
59. Tokuriki, N., Tawfik, D.S., Protein dynamism and evolvability. Science 324 (2009), 203–207.
60. Tompa, P., Intrinsically unstructured proteins. Trends Biochem. Sci. 27 (2002), 527–533.
61. Tompa, P., Fuxreiter, M., Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem. Sci. 33 (2008), 2–8.
62. UniProt Consortium. UniProt: a hub for protein information. Nucleic Acids Res. 43 (2015), D204–D212.
63. Uversky, V.N., Dunker, A.K., Understanding protein non-folding. Biochim. Biophys. Acta 1804 (2010), 1231–1264.
64. Uversky, V.N., Li, J., Bower, K., Fink, A.L., Synergistic effects of pesticides and metals on the fibrillation of alpha-synuclein: implications for Parkinson's disease. Neurotoxicology 23 (2002), 527–536.
65. van der Lee, R., Buljan, M., Lang, B., Weatheritt, R.J., Daughdrill, G.W., Dunker, A.K., Fuxreiter, M., Gough, J., Gsponer, J., Jones, D.T., et al. Classification of intrinsically disordered regions and proteins. Chem. Rev. 114 (2014), 6589–6631.
66. Walters, K.J., Ufd1 exhibits dual ubiquitin binding modes. Structure 13 (2005), 943–944.
67. Weinreb, C., Riesselman, A.J., Ingraham, J.B., Gross, T., Sander, C., Marks, D.S., 3D RNA and Functional Interactions from Evolutionary Couplings. Cell 165 (2016), 963–975.
68. Wells, M., Tidow, H., Rutherford, T.J., Markwick, P., Jensen, M.R., Mylonas, E., Svergun, D.I., Blackledge, M., Fersht, A.R., Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain. Proc. Natl. Acad. Sci. USA 105 (2008), 5762–5767.
69. Williams, D.B., Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J. Cell Sci. 119 (2006), 615–623.
70. Wright, P.E., Dyson, H.J., Intrinsically disordered proteins in cellular signalling and regulation. Nat. Rev. Mol. Cell Biol. 16 (2015), 18–29.
71. Yachdav, G., Kloppmann, E., Kajan, L., Hecht, M., Goldberg, T., Hamp, T., Hönigschmid, P., Schafferhans, A., Roos, M., Bernhofer, M., et al. PredictProtein–an open resource for online prediction of protein structural and functional features. Nucleic Acids Res. 42 (2014), W337–W343.
72. Zhang, N., Wang, Q., Ehlinger, A., Randles, L., Lary, J.W., Kang, Y., Haririnia, A., Storaska, A.J., Cole, J.L., Fushman, D., Walters, K.J., Structure of the s5a:k48-linked diubiquitin complex and its interactions with rpn13. Mol. Cell 35 (2009), 280–290.