Conserved structural and dynamics features in the denatured states of drosophila SUMO, human SUMO and ubiquitin proteins: Implications to sequence-folding paradigm

Proteins: Structure, Function and Bioinformatics

Volumn 76, Issue 2, 2009, Pages 387-402

  Kumar, Dinesh ^a   Chugh, Jeetender ^a   Sharma, Shilpy ^a   Hosur, Ramakrishna V ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Conformational sampling; Folding funnel; Protein folding; Residual structure; Sequencefolding paradigm; Structural propensities

Indexed keywords

STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; UBIQUITIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; DATA ANALYSIS; DENATURATION; DROSOPHILA; HYDROPHOBICITY; INFORMATION PROCESSING; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TEMPERATURE; THERMOREGULATION;

ANIMALS; DROSOPHILA PROTEINS; HUMANS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; STRUCTURE-ACTIVITY RELATIONSHIP; SUMO-1 PROTEIN; UBIQUITIN;

EID: 67650248992     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22354     Document Type: Article

References (81)

1. Chan HS, Dill KA. Protein folding in the landscape perspective: chevron plots and non-Arrhenius kinetics. Proteins 1998;30:2-33.
2. Dill KA, Chan HS. From Levinthal to pathways to funnels. Nat Struct Biol 1997;4:10-19.
3. Chugh J, Sharma S, Hosur RV. Pockets of short-range transient order and restricted topological heterogeneity in the guanidine-denatured state ensemble of GED of dynamin. Biochemistry 2007;46:11819-11832.
4. Kumar A, Srivastava S, Mishra RK, Mittal R, Hosur RV. Local structural preferences and dynamics restrictions in the urea-denatured state of SUMO-1: NMR characterization. Biophys J 2006;90:2498-2509.
5. Schwarzinger S, Wright PE, Dyson HJ. Molecular hinges in protein folding: the urea-denatured state of apomyoglobin. Biochemistry 2002;41:12681-12686.
6. Bhavesh NS, Panchal SC, Mittal R, Hosur RV. NMR identification of local structural preferences in HIV-1 protease tethered heterodimer in 6 M guanidine hydrochloride. FEBS Lett 2001;509:218-224.
7. Bhavesh NS, Sinha R, Mohan PM, Hosur RV. NMR elucidation of early folding hierarchy in HIV-1 protease. J Biol Chem 2003;278:19980-19985.
8. Bhavesh NS, Juneja J, Udgaonkar JB, Hosur RV. Native and nonnative conformational preferences in the urea-unfolded state of barstar. Protein Sci 2004;13:3085-3091.
9. Chatterjee A, Krishna Mohan PM, Prabhu A, Ghosh-Roy A, Hosur RV. Equilibrium unfolding of DLC8 monomer by urea and guanidine hydrochloride: distinctive global and residue level features. Biochimie 2007;89:117-134.
10. Wong KB, Freund SM, Fersht AR. Cold denaturation of barstar: 1H, 15N and 13C NMR assignment and characterisation of residual structure. J Mol Biol 1996;259:805-818.
11. Kmiecik S, Kolinski A. Folding pathway of the B1 domain of protein G explored by multiscale modeling. Biophys J 2008;94:726-736.
12. Klein-Seetharaman J, Oikawa M, Grimshaw SB, Wirmer J, Duchardt E, Ueda T, Imoto T, Smith LJ, Dobson CM, Schwalbe H. Long-range interactions within a nonnative protein. Science 2002;295:1719-1722.
13. Shortle D, Ackerman MS. Persistence of native-like topology in a denatured protein in 8 M urea. Science 2001;293:487-489.
14. Meekhof AE, Freund SM. Probing residual structure and backbone dynamics on the milli- to picosecond timescale in a urea-denatured fibronectin type III domain. J Mol Biol 1999;286:579-592.
15. Kazmirski SL, Wong KB, Freund SM, Tan YJ, Fersht AR, Daggett V. Protein folding from a highly disordered denatured state: the folding pathway of chymotrypsin inhibitor 2 at atomic resolution. Proc Natl Acad Sci USA 2001;98:4349-4354.
16. Frank MK, Clore GM, Gronenborn AM. Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy. Protein Sci 1995;4:2605-2615.
17. Sari N, Alexander P, Bryan PN, Orban J. Structure and dynamics of an acid-denatured protein G mutant. Biochemistry 2000;39:965-977.
18. Fersht AR. The sixth datta lecture. Protein folding and stability: the pathway of folding of barnase. FEBS Lett 1993;325:5-16.
19. Le Duff CS, Whittaker SBM, Radford SE, Moore GR. Characterisation of the conformational properties of urea-unfolded Im7: implications for the early stages of protein folding. J Mol Biol 2006;364:824-835.
20. Modig K, Jurgensen VW, Lindorff-Larsen K. Detection of initiation sites in protein folding of the four helix bundle ACBP by chemical shift analysis. FEBS Lett 2007;581:4965-4971.
21. Melchior F. SUMO-nonclassical ubiquitin. Annu Rev Cell Dev Biol 2000;16:591-626.
22. Seeler JS, Dejean A. SUMO: of branched proteins and nuclear bodies. Oncogene 2001;20:7243-7249.
23. arcon-Vargas D, Ronai Z. SUMO in cancer-wrestlers wanted. Cancer Biol Ther 2002;1:237-242.
24. Verger A, Perdomo J, Crossley M. Modification with SUMO. A role in transcriptional regulation. EMBO Rep 2003;4:137-142.
25. Saitoh H, Pu RT, Dasso M. SUMO-1: wrestling with a new ubiquitin-related modifier. Trends Biochem Sci 1997;22:374-376.
26. Orengo CA, Jones DT, Thornton JM. Protein superfamilies and domain superfolds. Nature 1994;372:631-634.
27. Paz Y, Elazar Z, Fass D. Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J Biol Chem 2000;275:25445-25450.
28. Bayer P, Arndt A, Metzger S, Mahajan R, Melchior F, Jaenicke R, Becker J. Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 1998;280:275-286.
29. Peti W, Smith LJ, Redfield C, Schwalbe H. Chemical shifts in denatured proteins: resonance assignments for denatured ubiquitin and comparisons with other denatured proteins. J Biomol NMR 2001;19:153-165.
30. Wirmer J, Peti W, Schwalbe H. Motional properties of unfolded ubiquitin: a model for a random coil protein. J Biomol NMR 2006;35:175-186.
31. Kitahara R, Zhao C, Saito K, Koshiba S, Ioune M, Kigawa T, Yokoyama S, Akasaka K. Basic folded and low-populated locally disordered conformers of SUMO-2 characterized by NMR spectroscopy at varying pressures. Biochemistry 2008;47:30-39.
32. 13C resonance assignment of folded and 8M urea denatured state of SUMO from Drosophila melanogaster. Biomol NMR Assign 2008;2:13-15.
33. Keller R. The computer aided resonance assignment tutorial. Goldau, Switzerland: CANTINA, Verlag; 2004.
34. Panchal SC, Bhavesh NS, Hosur RV. Improved 3D triple resonance experiments, HNN and HN(C)N, for HN and 15N sequential correlations in (13C, 15N) labeled proteins: application to unfolded proteins. J Biomol NMR 2001;20:135-147.
35. Bhavesh NS, Panchal SC, Hosur RV. An efficient high-throughput resonance assignment procedure for structural genomics and protein folding research by NMR. Biochemistry 2001;40:14727-14735.
36. Chugh J, Kumar D, Hosur RV. Tuning the HNN experiment: generation of serine-threonine check points. J Biomol NMR 2008;40:145-152.
37. Stonehouse J, Keeler J. A Convenient and accurate method for the measurement of the values of spin-spin coupling-constants. J Magn Reson A 1995;112:43-57.
38. Spyracopoulos L. A suite of Mathematica notebooks for the analysis of protein main chain 15N NMR relaxation data. J Biomol NMR 2006;36:215-224.
39. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, Gish G, Shoelson SE, Pawson T, Forman-Kay JD, Kay LE. Backbone dynamics of a free and a phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 1994;33:5984-6003.
40. Lefevre JF, Dayie KT, Peng JW, Wagner G. Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry 1996;35:2674-2686.
41. Rose GD, Geselowitz AR, Lesser GJ, Lee RH, Zehfus MH. Hydrophobicity of amino-acid residues in globular-proteins. Science 1985;229:834-838.
42. Wishart DS, Bigam CG, Holm A, Hodges RS, Sykes BD. 1H, 13C and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J Biomol NMR 1995;5:67-81.
43. Wishart DS, Sykes BD. Chemical shifts as a tool for structure determination. Methods Enzymol 1994;239:363-392.
44. Schwarzinger S, Kroon GJ, Foss TR, Chung J, Wright PE, Dyson HJ. Sequence-dependent correction of random coil NMR chemical shifts. J Am Chem Soc 2001;123:2970-2978.
45. Karplus M, Grant DM. A criterion for orbital hybridization and charge distribution in chemical bonds. Proc Natl Acad Sci USA 1959;45:1269-1273.
46. Smith LJ, Bolin KA, Schwalbe H, MacArthur MW, Thornton JM, Dobson CM. Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J Mol Biol 1996;255:494-506.
47. Serrano L. Comparison between the phi distribution of the amino acids in the protein database and NMR data indicates that amino acids have various phi propensities in the random coil conformation. J Mol Biol 1995;254:322-333.
48. Penkett CJ, Redfield C, Dodd I, Hubbard J, Mcbay DL, Mossakowska DE, Smith RAG, Dobson CM, Smith LJ. NMR analysis of main-chain conformational preferences in an unfolded fibronectinbinding protein. J Mol Biol 1997;274:152-159.
49. Baxter NJ, Williamson MP. Temperature dependence of 1H chemical shifts in proteins. J Biomol NMR 1997;9:359-369.
50. Merutka G, Dyson HJ, Wright PE. Random coil H-1 chemicalshifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series Ggxgg. J Biomol NMR 1995;5:14-24.
51. Sivaraman T, Kumar TK, Jayaraman G, Han CC, Yu C. Characterization of a partially structured state in an all-β-sheet protein. Biochem J 1997;321 (Part 2):457-464.
52. Tremmel P, Geyer A. An oligomeric ser-pro dipeptide mimetic assuming the polyproline II helix conformation. J Am Chem Soc 2002;124:8548-8549.
53. Dyson HJ, Wright PE. Insights into protein folding from NMR. Annu Rev Phys Chem 1996;47:369-395.
54. Peng JW, Wagner G. Mapping of the spectral densities of N-H bond motions in eglin c using heteronuclear relaxation experiments. Biochemistry 1992;31:8571-8586.
55. Farrow NA, Zhang O, Szabo A, Torchia DA, Kay LE. Spectral density function mapping using 15N relaxation data exclusively. J Biomol NMR 1995;6:153-162.
56. Kay LE, Torchia DA, Bax A. Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 1989;28:8972-8979.
57. Kneller JM, Min Lu, Bracken C. An effective method for the discrimination of motional anisotropy and chemical exchange. J Am Chem Soc 2001;124:1852-1853.
58. Cavanagh J, Fairbrother WJ, Palmer AG, Skelton NJ. Protein NMR spectroscopy. San Diego: Academic Press; 1996.
59. Bennion BJ, Daggett V. The molecular basis for the chemical denaturation of proteins by urea. Proc Natl Acad Sci USA 2003;100:5142-5147.
60. Eliezer D, Yao J, Dyson HJ, Wright PE. Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding. Nat Struct Biol 1998;5:148-155.
61. Eliezer D, Chung J, Dyson HJ, Wright PE. Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin. Biochemistry 2000;39:2894-2901.
62. Lumb KJ, Kim PS. Formation of a hydrophobic cluster in denatured bovine pancreatic trypsin inhibitor. J Mol Biol 1994;236:412-420.
63. Mok KH, Kuhn LT, Goez M, Day IJ, Lin JC, Andersen NH, Hore PJ. A pre-existing hydrophobic collapse in the unfolded state of an ultrafast folding protein. Nature 2007;447:106-109.
64. Mok YK, Alonso LG, Lima LMTR, Bycroft M, De Prat-Gay G. Folding of a dimeric b-barrel: residual structure in the urea denatured state of the human papillomavirus E2 DNA binding domain. Protein Sci 2000;9:799-811.
65. Yao J, Chung J, Eliezer D, Wright PE, Dyson HJ. NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding. Biochemistry 2001;40:3561-3571.
66. Chugha P, Oas TG. Backbone dynamics of the monomeric lambda repressor denatured state ensemble under nondenaturing conditions. Biochemistry 2007;46:1141-1151.
67. Arcus VL, Vuilleumier S, Freund SM, Bycroft M, Fersht AR. A comparison of the pH, urea, and temperature-denatured states of barnase by heteronuclear NMR: implications for the initiation of protein folding. J Mol Biol 1995;254:305-321.
68. Bofill R, Simpson ER, Platt GW, Crespo MD, Searle MS. Extending the folding nucleus of ubiquitin with an independently folding β-hairpin finger: hurdles to rapid folding arising from the stabilisation of local interactions. J Mol Biol 2005;349:205-221.
69. Brutscher B, Bruschweiler R, Ernst RR. Backbone dynamics and structural characterization of the partially folded A state of ubiquitin by 1H, 13C, and 15N nuclear magnetic resonance spectroscopy. Biochemistry 1997;36:13043-13053.
70. Cavagnero S, Nishimura C, Schwarzinger S, Dyson HJ, Wright PE. Conformational and dynamic characterization of the molten globule state of an apomyoglobin mutant with an altered folding pathway. Biochemistry 2001;40:14459-14467.
71. Fiebig KM, Schwalbe H, Buck M, Smith LJ, Dobson CM. Toward a description of the conformations of denatured states of proteins. Comparison of a random coil model with NMR measurements. J Phys Chem 1996;100:2661-2666.
72. Freund SM, Wong KB, Fersht AR. Initiation sites of protein folding by NMR analysis. Proc Natl Acad Sci USA 1996;93:10600-10603.
73. Neri D, Billeter M, Wider G, Wuthrich K. NMR determination of residual structure in a urea-denatured protein, the 434-repressor. Science 1992;257:1559-1563.
74. Religa TL, Markson JS, Mayor U, Freund SM, Fersht AR. Solution structure of a protein denatured state and folding intermediate. Nature 2005;437:1053-1056.
75. Smith LJ, Fiebig KM, Schwalbe H, Dobson CM. The concept of a random coil. Residual structure in peptides and denatured proteins. Fold Des 1996;1:R95-R106.
76. Went HM, Jackson SE. Ubiquitin folds through a highly polarized transition state. Protein Eng Des Sel 2005;18:229-237.
77. Harding MM, Williams DH, Woolfson DN. Characterization of a partially denatured state of a protein by two-dimensional NMR: reduction of the hydrophobic interactions in ubiquitin. Biochemistry 1991;30:3120-3128.
78. Stockman BJ, Euvrard A, Scahill TA. Heteronuclear three-dimensional NMR spectroscopy of a partially denatured protein: the Astate of human ubiquitin. J Biomol NMR 1993;3:285-296.
79. Gronenborn AM, Filpula DR, Essig NZ, Achari A, Whitlow M, Wingfield PT, Clore GM. A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science 1991;253:657-661.
80. Alm E, Baker D. Matching theory and experiment in protein folding. Curr Opin Struct Biol 1999;9:189-196.
81. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.