Thermally Induced Protein Unfolding Probed by Isotope-edited IR Spectroscopy

Overview

Journal J Phys Chem B

Publisher American Chemical Society

Specialty Chemistry

Date 2012 Aug 3

PMID 22853174

Citations 5

Authors

Lu Wang

James L Skinner

Affiliations

Soon will be listed here.

Abstract

Infrared (IR) spectroscopy has been widely utilized for the study of protein folding, unfolding, and misfolding processes. We have previously developed a theoretical method for calculating IR spectra of proteins in the amide I region. In this work, we apply this method, in combination with replica-exchange molecular dynamics simulations, to study the equilibrium thermal unfolding transition of the villin headpiece subdomain (HP36). Temperature-dependent IR spectra and spectral densities are calculated. The spectral densities correctly reflect the unfolding conformational changes in the simulation. With the help of isotope labeling, we are able to capture the feature that helix 2 of HP36 loses its secondary structure before global unfolding occurs, in agreement with experiment.

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References

Lessing J, Roy S, Reppert M, Baer M, Marx D, Jansen T . Identifying residual structure in intrinsically disordered systems: a 2D IR spectroscopic study of the GVGXPGVG peptide. J Am Chem Soc. 2012; 134(11):5032-5. DOI: 10.1021/ja2114135. View

Torres J, Kukol A, Goodman J, Arkin I . Site-specific examination of secondary structure and orientation determination in membrane proteins: the peptidic (13)C=(18)O group as a novel infrared probe. Biopolymers. 2001; 59(6):396-401. DOI: 10.1002/1097-0282(200111)59:6<396::AID-BIP1044>3.0.CO;2-Y. View

Lin C, Hu C, Hansmann U . Parallel tempering simulations of HP-36. Proteins. 2003; 52(3):436-45. DOI: 10.1002/prot.10351. View

Moran S, Woys A, Buchanan L, Bixby E, Decatur S, Zanni M . Two-dimensional IR spectroscopy and segmental 13C labeling reveals the domain structure of human γD-crystallin amyloid fibrils. Proc Natl Acad Sci U S A. 2012; 109(9):3329-34. PMC: 3295317. DOI: 10.1073/pnas.1117704109. View

Zhuang W, Cui R, Silva D, Huang X . Simulating the T-jump-triggered unfolding dynamics of trpzip2 peptide and its time-resolved IR and two-dimensional IR signals using the Markov state model approach. J Phys Chem B. 2011; 115(18):5415-24. DOI: 10.1021/jp109592b. View

Reddy A, Wang L, Lin Y, Ling Y, Chopra M, Zanni M . Solution structures of rat amylin peptide: simulation, theory, and experiment. Biophys J. 2010; 98(3):443-51. PMC: 2814214. DOI: 10.1016/j.bpj.2009.10.029. View

van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark A, Berendsen H . GROMACS: fast, flexible, and free. J Comput Chem. 2005; 26(16):1701-18. DOI: 10.1002/jcc.20291. View

Meng W, Shan B, Tang Y, Raleigh D . Native like structure in the unfolded state of the villin headpiece helical subdomain, an ultrafast folding protein. Protein Sci. 2009; 18(8):1692-701. PMC: 2776957. DOI: 10.1002/pro.152. View

Tang Y, Grey M, McKnight J, Palmer 3rd A, Raleigh D . Multistate folding of the villin headpiece domain. J Mol Biol. 2005; 355(5):1066-77. DOI: 10.1016/j.jmb.2005.10.066. View

10.

Sagle L, Zimmermann J, Dawson P, Romesberg F . Direct and high resolution characterization of cytochrome c equilibrium folding. J Am Chem Soc. 2006; 128(44):14232-3. DOI: 10.1021/ja065179d. View

11.

Smith A, Lessing J, Ganim Z, Peng C, Tokmakoff A, Roy S . Melting of a beta-hairpin peptide using isotope-edited 2D IR spectroscopy and simulations. J Phys Chem B. 2010; 114(34):10913-24. DOI: 10.1021/jp104017h. View

12.

Strasfeld D, Ling Y, Shim S, Zanni M . Tracking fiber formation in human islet amyloid polypeptide with automated 2D-IR spectroscopy. J Am Chem Soc. 2008; 130(21):6698-9. PMC: 3209517. DOI: 10.1021/ja801483n. View

13.

Dill K . Dominant forces in protein folding. Biochemistry. 1990; 29(31):7133-55. DOI: 10.1021/bi00483a001. View

14.

Falvo C, Zhuang W, Kim Y, Axelsen P, Hochstrasser R, Mukamel S . Frequency distribution of the amide-I vibration sorted by residues in amyloid fibrils revealed by 2D-IR measurements and simulations. J Phys Chem B. 2012; 116(10):3322-30. PMC: 3314731. DOI: 10.1021/jp2096423. View

15.

Brewer S, Vu D, Tang Y, Li Y, Franzen S, Raleigh D . Effect of modulating unfolded state structure on the folding kinetics of the villin headpiece subdomain. Proc Natl Acad Sci U S A. 2005; 102(46):16662-7. PMC: 1283803. DOI: 10.1073/pnas.0505432102. View

16.

Haris P, Chapman D . Does Fourier-transform infrared spectroscopy provide useful information on protein structures?. Trends Biochem Sci. 1992; 17(9):328-33. DOI: 10.1016/0968-0004(92)90305-s. View

17.

Wang M, Tang Y, Sato S, Vugmeyster L, McKnight C, Raleigh D . Dynamic NMR line-shape analysis demonstrates that the villin headpiece subdomain folds on the microsecond time scale. J Am Chem Soc. 2003; 125(20):6032-3. DOI: 10.1021/ja028752b. View

18.

Tang Y, Goger M, Raleigh D . NMR characterization of a peptide model provides evidence for significant structure in the unfolded state of the villin headpiece helical subdomain. Biochemistry. 2006; 45(22):6940-6. DOI: 10.1021/bi052484n. View

19.

Hayashi T, Zhuang W, Mukamel S . Electrostatic DFT map for the complete vibrational amide band of NMA. J Phys Chem A. 2006; 109(43):9747-59. DOI: 10.1021/jp052324l. View

20.

Wang L, Middleton C, Singh S, Reddy A, Woys A, Strasfeld D . 2DIR spectroscopy of human amylin fibrils reflects stable β-sheet structure. J Am Chem Soc. 2011; 133(40):16062-71. PMC: 3196637. DOI: 10.1021/ja204035k. View