Cooperative cold denaturation: The case of the C-terminal domain of ribosomal protein l9

Biochemistry

Volumn 52, Issue 14, 2013, Pages 2402-2409

  Luan, Bowu ^a   Shan, Bing ^a   Baiz, Carlos ^b   Tokmakoff, Andrei ^b   Raleigh, Daniel P ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; COLD DENATURATION; PRACTICAL IMPORTANCE; PROTEIN THERMODYNAMICS; RIBOSOMAL PROTEINS; SINGLE-DOMAIN PROTEINS; SMALL ANGLE X-RAY SCATTERING; THERAPEUTIC PROTEIN;

DENATURATION; FOURIER TRANSFORM INFRARED SPECTROSCOPY; THERMODYNAMICS;

PROTEINS;

CARBOXYL TERMINAL DOMAIN OF RIBOSOMAL PROTEIN L9; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; COLD; ENCAPSULATION; INFRARED SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN UNFOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSE MICELLE; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; CIRCULAR DICHROISM; COLD TEMPERATURE; GEOBACILLUS STEAROTHERMOPHILUS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POINT MUTATION; PROTEIN DENATURATION; PROTEIN STRUCTURE, TERTIARY; RIBOSOMAL PROTEINS; SCATTERING, SMALL ANGLE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THERMODYNAMICS; X-RAY DIFFRACTION;

EID: 84876008376     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3016789     Document Type: Article

References (40)

1. Graziano, G. (2010) On the molecular origin of cold denaturation of globular proteins Phys. Chem. Chem. Phys. 12, 14245-14252
2. Yoshidome, T. and Kinoshita, M. (2009) Hydrophobicity at low temperatures and cold denaturation of a protein Phys. Rev. E 79, 030905 (R)
3. Dias, C. L. (2012) Unifying microscopic mechanism for pressure and cold denaturations of proteins Phys. Rev. Lett. 109, 048104
4. Dias, C. L., Ala-Nissila, T., Karttunen, M., Vattulainen, I., and Grant, M. (2008) Microscopic mechanism for cold denaturation Phys. Rev. Lett. 100, 118101
5. Davidovic, M., Mattea, C., Qvist, J., and Halle, B. (2009) Protein cold denaturation as seen from the solvent J. Am. Chem. Soc. 131, 1025-1036
6. Todgham, A. E., Hoaglund, E. A., and Hofmann, G. E. (2007) Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation of proteins in vivo J. Comp. Physiol., B 177, 857-866
7. Lazar, K. L., Patapoff, T. W., and Sharma, V. K. (2010) Cold denaturation of monoclonal antibodies mAbs 2, 42-52
8. Feller, G. (2010) Protein stability and enzyme activity at extreme biological temperatures J. Phys.: Condens. Matter 22, 323101
9. Pucciarelli, S., Parker, S. K., Detrich, H. W., III, and Melki, R. (2006) Characterization of the cytoplasmic chaperonin containing TCP-1 from the Antarctic fish Notothenia coriiceps Extremophiles 10, 537-549
10. Hayley, M., Chevaldina, T., and Heeley, D. H. (2011) Cold adaptation of tropomyosin Biochemistry 50, 6559-6566
11. Kolhe, P. and Badkar, A. (2011) Protein and solute distribution in drug substance containers during frozen storage and post-thawing: A tool to understand and define freezing-thawing parameters in biotechnology process development Biotechnol. Prog. 27, 494-504
12. Kim, H. Y., Cho, M. K., Riedel, D., Fernandez, C. O., and Zweckstetter, M. (2008) Dissociation of amyloid fibrils of α-synuclein in supercooled water Angew. Chem., Int. Ed. 47, 5046-5048
13. Tantos, A., Friedrich, P., and Tompa, P. (2009) Cold stability of intrinsically disordered proteins FEBS Lett. 583, 465-469
14. Babu, C. R., Hilser, V. J., and Wand, A. J. (2004) Direct access to the cooperative substructure of proteins and the protein ensemble via cold denaturation Nat. Struct. Mol. Biol. 11, 352-357
15. Whitten, S. T., Kurtz, A. J., Pometun, M. S., Wand, A. J., and Hilser, V. J. (2006) Revealing the nature of the native state ensemble through cold denaturation Biochemistry 45, 10163-10174
16. Pometun, M. S., Peterson, R. W., Babu, C. R., and Wand, A. J. (2006) Cold denaturation of encapsulated ubiquitin J. Am. Chem. Soc. 128, 10652-10653
17. Tian, J. H. and Garcia, A. E. (2011) Simulations of the confinement of ubiquitin in self-assembled reverse micelles J. Chem. Phys. 134, 225101
18. Van Horn, W. D., Simorellis, A. K., and Flynn, P. F. (2005) Low-temperature studies of encapsulated proteins J. Am. Chem. Soc. 127, 13553-13560
19. Kitahara, R., Okuno, A., Kato, M., Taniguchi, Y., Yokoyama, S., and Akasaka, K. (2006) Cold denaturation of ubiquitin at high pressure Magn. Reson. Chem. 44, S108-S113
20. Adrover, M., Esposito, V., Martorell, G., Pastore, A., and Temussi, P. A. (2010) Understanding cold denaturation: The case study of Yfh1 J. Am. Chem. Soc. 132, 16240-16246
21. Adrover, M., Martorell, G., Martin, S. R., Urosev, D., Konarev, P. V., Svergun, D. I., Daura, X., Temussi, P., and Pastore, A. (2012) The role of hydration in protein stability: Comparison of the cold and heat unfolded states of yfh1 J. Mol. Biol. 417, 413-424
22. Martin, S. R., Esposito, V., Rios, P. D. L., Pastore, A., and Temussi, P. A. (2008) Cold denaturation of yeast frataxin offers the clue to understand the effect of alcohols on protein stability J. Am. Chem. Soc. 130, 9963-9970
23. Pastore, A., Martin, S. R., Politou, A., Kondapalli, K. C., Stemmler, T., and Temussi, P. A. (2007) Unbiased cold denaturation: Low- and high-temperature unfolding of yeast frataxin under physiological conditions J. Am. Chem. Soc. 129, 5374-5375
24. Sato, S. and Raleigh, D. P. (2002) pH-dependent stability and folding kinetics of a protein with an unusual α-β topology: The C-terminal domain of the ribosomal protein L9 J. Mol. Biol. 318, 571-582
25. Sato, S., Kuhlman, B., Wu, W. J., and Raleigh, D. P. (1999) Folding of the multidomain ribosomal protein L9: The two domains fold independently with remarkably different rates Biochemistry 38, 5643-5650
26. Li, Y., Shan, B., and Raleigh, D. P. (2007) The cold denatured state is compact but expands at low temperatures: Hydrodynamic properties of the cold denatured state of the C-terminal domain of L9 J. Mol. Biol. 368, 256-262
27. Shan, B., McClendon, S., Rospigliosi, C., Eliezer, D., and Raleigh, D. P. (2010) The cold denatured state of the C-terminal domain of protein L9 is compact and contains both native and non-native structure J. Am. Chem. Soc. 132, 4669-4677
28. Li, Y., Gupta, R., Cho, J. H., and Raleigh, D. P. (2007) Mutational analysis of the folding transition state of the C-terminal domain of ribosomal protein L9: A protein with an unusual β-sheet topology Biochemistry 46, 1013-1021
29. 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
30. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278, 313-352
31. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J., and Svergun, D. I. (2003) PRIMUS: A Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36, 1277-1282
32. Guinier, A. and Fournet, G. (1955) Small Angle Scattering of X-rays, Wiley, New York.
33. Chan, H. S., Shimizu, S., and Kaya, H. (2004) Cooperativity principles in protein folding Methods Enzymol. 380, 350-379
34. Barrick, D. (2009) What have we learned from the studies of two-state folders, and what are the unanswered questions about two-state protein folding? Phys. Biol. 6, 015001
35. Makhatadze, G. I., Clore, G. M., and Gronenborn, A. M. (1995) Solvent isotope effect and protein stability Nat. Struct. Biol. 2, 852-855
36. 2O J. Phys. Chem. 69, 3132-3144
37. Baiz, C. R., Peng, C. S., Reppert, M. E., Jones, K. C., and Tokmakoff, A. (2012) Coherent two-dimensional infrared spectroscopy: Quantitative analysis of protein secondary structure in solution Analyst 137, 1793-1799
38. Volkov, V. and Hamm, P. (2004) A two-dimensional infrared study of localization, structure, and dynamics of a dipeptide in membrane environment Biophys. J. 87, 4213-4225
39. Choy, W. Y., Mulder, F. A., Crowhurst, K. A., Muhandiram, D. R., Millett, I. S., Doniach, S., Forman-Kay, J. D., and Kay, L. E. (2002) Distribution of molecular size within an unfolded state ensemble using small-angle X-ray scattering and pulse field gradient NMR techniques J. Mol. Biol. 316, 101-112
40. Simorellis, A. K., Van Horn, W. D., and Flynn, P. F. (2006) Dynamics of low temperature induced water shedding from AOT reverse micelles J. Am. Chem. Soc. 128, 5082-5090