Local structural preferences and dynamics restrictions in the urea-denatured state of SUMO-1: NMR characterization

Biophysical Journal

Volumn 90, Issue 7, 2006, Pages 2498-2509

  Kumar, Ashutosh ^a   Srivastava, Sudha ^a   Mishra, Ram Kumar ^a   Mittal, Rohit ^a   Hosur, Ramakrishna V ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; FUNCTIONAL GROUP; HYDROGEN; PROLINE DERIVATIVE; PROTON; SUMO 1 PROTEIN; UBIQUITIN; UREA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; EXPERIMENTATION; MOLECULAR DYNAMICS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; SPECTRUM; STRUCTURE ANALYSIS;

EID: 33646187492     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.071746     Document Type: Article

References (87)

1. Religa, T. L., J. S. Markson, U. Mayor, S. M. Freund, and A. R. Fersht. 2005. Solution structure of a protein denatured state and folding intermediate. Nature. 437:1053-1056.
2. Bhavesh, N. S., R. Sinha, P. M. Mohan, and R. V. Hosur. 2003. NMR elucidation of early folding hierarchy in HIV-1 protease. J. Biol. Chem. 278:19980-19985.
3. Plotkin, S. S., and J. N. Onuchic. 2002. Understanding protein folding with energy landscape theory. Part I: Basic concepts. Q. Rev. Biophys. 35:111-167.
4. Plotkin, S. S., and J. N. Onuchic. 2002. Understanding protein folding with energy landscape theory. Part II: Quantitative aspects. Q. Rev. Biophys. 35:205-286.
5. Chan, H. S., and K. A. Dill. 1998. Protein folding in the landscape perspective: chevron plots and non-Arrhenius kinetics. Proteins. 30:2-33.
6. Dill, K. A., and H. S. Chan. 1997. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4:10-19.
7. Onuchic, J. N., H. Nymeyer, A. E. Garcia, J. Chahine, and N. D. Socci. 2000. The energy landscape theory of protein folding: insights into folding mechanisms and scenarios. Adv. Protein Chem. 53:87-152.
8. Bhavesh, N. S., S. C. Panchal, R. Mittal, and R. V. Hosur. 2001. NMR identification of local structural preferences in HIV-1 protease tethered heterodimer in 6 M guanidine hydrochloride. FEBS Lett. 509:218-224.
9. Bhavesh, N. S., J. Juneja, J. B. Udgaonkar, and R. V. Hosur. 2004. Native and nonnative conformational preferences in the urea-unfolded state of barstar. Protein Sci. 13:3085-3091.
10. Chatterjee, A., P. Mridula, R. K. Mishra, R. Mittal, and R. V. Hosur. 2005. Folding regulates autoprocessing of HIV-1 protease precursor. J. Biol. Chem. 280:11369-11378.
11. Schwalbe, H., K. M. Fiebig, M. Buck, J. A. Jones, S. B. Grimshaw, A. Spencer, S. J. Glaser, L. J. Smith, and C. M. Dobson. 1997. Structural and dynamical properties of a denatured protein. Heteronuclear 3D NMR experiments and theoretical simulations of lysozyme in 8 M urea. Biochemistry. 36:8977-8991.
12. Shortle, D., and M. S. Ackerman. 2001. Persistence of native-like topology in a denatured protein in 8 M urea. Science. 293:487-489.
13. Griko, Y., N. Sreerama, P. Osumi-Davis, R. W. Woody, and A. Y. Woody. 2001. Thermal and urea-induced unfolding in T7 RNA polymerase: calorimetry, circular dichroism and fluorescence study. Protein Sci. 10:845-853.
14. Li, Y., F. Picart, and D. P. Raleigh. 2005. Direct characterization of the folded, unfolded and urea-denatured states of the C-terminal domain of the ribosomal protein L9. J. Mol. Biol. 349:839-846.
15. Zhang, X., Y. Xu, J. Zhang, J. Wu, and Y. Shi. 2005. Structural and dynamic characterization of the acid-unfolded state of hUBF HMG Box 1 provides clues for the early events in protein folding. Biochemistry. 44:8117-8125.
16. Baum, J., C. M. Dobson, P. A. Evans, and C. Hanley. 1989. Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig α-lactalbumin. Biochemistry. 28:7-13.
17. Eliezer, D., J. Yao, H. J. Dyson, and P. E. Wright. 1998. Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding. Nat. Struct. Biol. 5:148-155.
18. Matsuura, H., S. Shimotakahara, C. Sakuma, M. Tashiro, H. Shindo, K. Mochizuki, A. Yamagishi, M. Kojima, and K. Takahashi. 2004. Thermal unfolding of ribonuclease T1 studied by multi-dimensional NMR spectroscopy. Biol. Chem. 385:1157-1164.
19. Feio, M. J., J. A. Navarro, M. S. Teixeira, D. Harrison, B. G. Karlsson, and M. A. De la Rosa. 2004. A thermal unfolding study of plastocyanin from the thermophilic cyanobacterium Phormidium laminosum. Biochemistry. 43:14784-14791.
20. Englander, S. W. 2000. Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29:213-238.
21. Onuchic, J. N., and P. G. Wolynes. 2004. Theory of protein folding. Curr. Opin. Struct. Biol. 14:70-75.
22. Otzen, D. E. 2002. Protein unfolding in detergents: effect of micelle structure, ionic strength, pH, and temperature. Biophys. J. 83:2219-2230.
23. Kamal, J. K., M. Nazeerunnisa, and D. V. Behere. 2002. Thermal unfolding of soybean peroxidase. Appropriate high denaturant concentrations induce cooperativity allowing the correct measurement of thermodynamic parameters. J. Biol. Chem. 277:40717-40721.
24. Kamal, J. K., and D. V. Behere. 2002. Thermal and conformational stability of seed coat soybean peroxidase. Biochemistry. 41:9034-9042.
25. Baldwin, R. L. 1995. On-pathway versus off-pathway folding intermediates. Fold. Des. 1:R1-R8.
26. Bhuyan, A. K., and J. B. Udgaonkar. 1999. Observation of multistate kinetics during the slow folding and unfolding of barstar. Biochemistry. 38:9158-9168.
27. Dunker, A. K., C. J. Brown, J. D. Lawson, L. M. Iakoucheva, and Z. Obradovic. 2002. Intrinsic disorder and protein function. Biochemistry. 41:6573-6582.
28. Uversky, V. N. 2002. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11:739-756.
29. Pohlschroder, M., K. Dilks, N. J. Hand, and R. W. Rose. 2004. Translocation of proteins across archaeal cytoplasmic membranes. FEMS Microbiol. Rev. 28:3.
30. Stefani, M. 2004. Protein misfolding and aggregation: new examples in medicine and biology of the dark side of the protein world. Biochim. Biophys. Acta. 1739:5-25.
31. Ross, C. A., and M. A. Poirier. 2004. Protein aggregation and neurodegenerative disease. Nat. Med. 10(Suppl):S10-S17.
32. Dobson, C. M. 2001. Protein folding and its links with human disease. Biochem. Soc. Symp. 1-26.
33. Hodsdon, M. E., and C. Frieden. 2001. Intestinal fatty acid binding protein: the folding mechanism as determined by NMR studies. Biochemistry. 40:732-742.
34. Lietzow, M. A., M. Jamin, H. J. Jane Dyson, and P. E. Wright. 2002. Mapping long-range contacts in a highly unfolded protein. J. Mol. Biol. 322:655-662.
35. Neri, D., M. Billeter, G. Wider, and K. Wuthrich. 1992. NMR determination of residual structure in a urea-denatured protein, the 434-repressor. Science. 257:1559-1563.
36. Schwarzinger, S., P. E. Wright, and H. J. Dyson. 2002. Molecular hinges in protein folding: the urea-denatured state of apomyoglobin. Biochemistry. 41:12681-12686.
37. Arcus, V. L., S. Vuilleumier, S. M. Freund, M. Bycroft, and A. R. Fersht. 1995. 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. 254:305-321.
38. Wong, K. B., J. Clarke, C. J. Bond, J. L. Neira, S. M. Freund, A. R. Fersht, and V. Daggett. 2000. Towards a complete description of the structural and dynamic properties of the denatured state of barnase and the role of residual structure in folding. J. Mol. Biol. 296:1257-1282.
39. Serrano, L., A. Matouschek, and A. R. Fersht. 1992. The folding of an enzyme. VI. The folding pathway of barnase: comparison with theoretical models. J. Mol. Biol. 224:847-859.
40. Hamada, D., and Y. Goto. 1997. The equilibrium intermediate of β-lactoglobulin with non-native a-helical structure. J. Mol. Biol. 269:479-487.
41. Mohana-Borges, R., N. K. Goto, G. J. Kroon, H. J. Dyson, and P. E. Wright. 2004. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 340:1131-1142.
42. Crowhurst, K. A., M. Tollinger, and J. D. Forman-Kay. 2002. Cooperative interactions and a non-native buried Trp in the unfolded state of an SH3 domain. J. Mol. Biol. 322:163-178.
43. Crowhurst, K. A., and J. D. Forman-Kay. 2003. Aromatic and methyl NOEs highlight hydrophobic clustering in the unfolded state of an SH3 domain. Biochemistry. 42:8687-8695.
44. Mok, K. H., and K. H. Han. 1999. NMR solution conformation of an antitoxic analogue of α-conotoxin GI: identification of a common nicotinic acetylcholine receptor α1-subunit binding surface for small ligands and α-conotoxins. Biochemistry. 38:11895-11904.
45. Parrot, I., P. C. Huang, and C. Khosla. 2002. Circular dichroism and nuclear magnetic resonance spectroscopic analysis of immunogenic gluten peptides and their analogs. J. Biol. Chem. 277:45572-45578.
46. Tremmel, P., and A. Geyer. 2002. An oligomeric Ser-Pro dipeptide mimetic assuming the polyproline II helix conformation. J. Am. Chem. Soc. 124:8548-8549.
47. Kelly, M. A., B. W. Chellgren, A. L. Rucker, J. M. Troutman, M. G. Fried, A. F. Miller, and T. P. Creamer. 2001. Host-guest study of left-handed polyproline II helix formation. Biochemistry. 40:14376-14383.
48. Moyna, G., H. J. Williams, R. J. Nachman, and A. I. Scott. 1999. Detection of nascent polyproline II helices in solution by NMR in synthetic insect kinin neuropeptide mimics containing the X-Pro-Pro-X motif. J. Pept. Res. 53:294-301.
49. Shi, Z., R. W. Woody, and N. R. Kallenbach. 2002. Is polyproline II a major backbone conformation in unfolded proteins? Adv. Protein Chem. 62:163-240.
50. Jha, A. K., A. Colubri, K. F. Freed, and T. R. Sosnick. 2005. Statistical coil model of the unfolded state: resolving the reconciliation problem. Proc. Natl. Acad. Sci. USA. 102:13099-13104.
51. Mahajan, R., C. Delphin, T. Guan, L. Gerace, and F. Melchior. 1997. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell. 88:97-107.
52. Bayer, P., A. Arndt, S. Metzger, R. Mahajan, F. Melchior, R. Jaenicke, and J. Becker. 1998. Structure determination of the small ubiquitin-related modifier SUMO-1. J. Mol. Biol. 280:275-286.
53. Jin, C., T. Shiyanova, Z. Shen, and X. Liao. 2001. Heteronuclear nuclear magnetic resonance assignments, structure and dynamics of SUMO-1, a human ubiquitin-like protein. Int. J. Biol. Macromol. 28:227-234.
54. Mishra, R. K., S. S. Jatiani, A. Kumar, V. R. Simhadri, R. V. Hosur, and R. Mittal. 2004. Dynamin interacts with members of the sumoylation machinery. J. Biol. Chem. 279:31445-31454.
55. Bhavesh, N. S., S. C. Panchal, and R. V. Hosur. 2001. An efficient high-throughput resonance assignment procedure for structural genomics and protein folding research by NMR. Biochemistry. 40:14727-14735.
56. 13C) labeled proteins: implications to structural genomics. Biochem. Biophys. Res. Commun. 293:427-432.
57. 15N) labeled proteins: application to unfolded proteins. J. Biomol. NMR. 20:135-147.
58. Permi, P., and A. Annila. 2004. Coherence transfer in proteins. Prog. Nucl. Magn. Reson. Spectrosc. 44:97-137.
59. Tugarinov, V., P. M. Hwang, and L. E. Kay. 2004. Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins. Annu. Rev. Biochem. 73:107-146.
60. 15N NMR relaxation. Biochemistry. 33:5984-6003.
61. Dyson, H. J., and P. E. Wright. 2004. Unfolded proteins and protein folding studied by NMR. Chem. Rev. 104:3607-3622.
62. Barbar, E. 1999. NMR characterization of partially folded and unfolded conformational ensembles of proteins. Biopolymers. 51:191-207.
63. Dyson, H. J., and P. E. Wright. 2001. Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Methods Enzymol. 339:258-270.
64. Dyson, H. J., and P. E. Wright. 2002. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance. Adv. Protein Chem. 62:311-340.
65. Bhavesh, N. S., and R. V. Hosur. 2004. Exploring unstructured proteins. Proc. Indian Natl. Sci. Acad. 70A:579-596.
66. Chatterjee, A., A. Kumar, J. Chugh, S. Srivastava, N. S. Bhavesh, and R. V. Hosur. 2005. NMR of unfolded proteins. J. Chem. Sci. (Indian Acad. Sci.). 117:3-21.
67. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR. 5:67-81.
68. Wishart, D. S., and B. D. Sykes. 1994. Chemical shifts as a tool for structure determination. Methods Enzymol. 239:363-392.
69. Schwarzinger, S., G. J. Kroon, T. R. Foss, P. E. Wright, and H. J. Dyson. 2000. Random coil chemical shifts in acidic 8 M urea: implementation of random coil shift data in NMRView. J. Biomol. NMR. 18:43-48.
70. Schwarzinger, S., G. J. Kroon, T. R. Foss, J. Chung, P. E. Wright, and H. J. Dyson. 2001. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc. 123:2970-2978.
71. Penkett, C. J., C. Redfield, I. Dodd, J. Hubbard, D. L. McBay, D. E. Mossakowska, R. A. Smith, C. M. Dobson, and L. J. Smith. 1997. NMR analysis of main-chain conformational preferences in an unfolded fibronectin-binding protein. J. Mol. Biol. 274:152-159.
72. Baxter, N. J., and M. P. Williamson. 1997. Temperature dependence of 1H chemical shifts in proteins. J. Biomol. NMR. 9:359-369.
73. 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR. 5:14-24.
74. Wuthrich, K. 1986. NMR of Proteins and Nucleic Acids. John Wiley & Sons.
75. Kay, L. E. 2005. NMR studies of protein structure and dynamics. J. Magn. Reson. 173:193-207.
76. Palmer III, A. G. 1993. Dynamic properties of proteins from NMR spectroscopy. Curr. Opin. Biotechnol. 4:385-391.
77. Palmer III, A. G. 1997. Probing molecular motion by NMR. Curr. Opin. Struct. Biol. 7:732-737.
78. Palmer III, A. G. 2001. NMR probes of molecular dynamics: overview and comparison with other techniques. Annu. Rev. Biophys. Biomol. Struct. 30:129-155.
79. van Gunsteren, W. F., R. Burgi, C. Peter, and X. Daura. 2001. The key to solving the protein-folding problem lies in an accurate description of the denatured state. Angew. Chem. Int. Ed. Engl. 40:351-355.
80. Wintrode, P. L., T. Rojsajjakul, R. Vadrevu, C. R. Matthews, and D. L. Smith. 2005. An obligatory intermediate controls the folding of the α-subunit of tryptophan synthase, a TIM barrel protein. J. Mol. Biol. 347:911-919.
81. Daggett, V., and A. R. Fersht. 2003. Is there a unifying mechanism for protein folding? Trends Biochem. Sci. 28:18-25.
82. Daggett, V., A. Li, L. S. Itzhaki, D. E. Otzen, and A. R. Fersht. 1996. Structure of the transition state for folding of a protein derived from experiment and simulation. J. Mol. Biol. 257:430-440.
83. Gianni, S., N. R. Guydosh, F. Khan, T. D. Caldas, U. Mayor, G. W. White, M. L. DeMarco, V. Daggett, and A. R. Fersht. 2003. Unifying features in protein-folding mechanisms. Proc. Natl. Acad. Sci. USA. 100:13286-13291.
84. Kuwata, K., R. Shastry, H. Cheng, M. Hoshino, C. A. Batt, Y. Goto, and H. Roder. 2001. Structural and kinetic characterization of early folding events in β-lactoglobulin. Nat. Struct. Biol. 8:151-155.
85. Zerella, R., P. A. Evans, J. M. Ionides, L. C. Packman, B. W. Trotter, J. P. Mackay, and D. H. Williams. 1999. Autonomous folding of a peptide corresponding to the N-terminal β-hairpin from ubiquitin. Protein Sci. 8:1320-1331.
86. Zerella, R., P. Y. Chen, P. A. Evans, A. Raine, and D. H. Williams. 2000. Structural characterization of a mutant peptide derived from ubiquitin: implications for protein folding. Protein Sci. 9:2142-2150.
87. Jourdan, M., and M. S. Searle. 2000. Cooperative assembly of a nativelike ubiquitin structure through peptide fragment complexation: energetics of peptide association and folding. Biochemistry. 39:12355-12364.