Equilibrium and Kinetic Folding of Rabbit Muscle Triosephosphate Isomerase by Hydrogen Exchange Mass Spectrometry

Journal of Molecular Biology

Volumn 336, Issue 5, 2004, Pages 1251-1263

  Pan, Hai ^a,b   Raza, Ashraf S ^a   Smith, David L ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b AMGEN INC   (United States)

Author keywords

Hydrogen exchange; Mass spectrometry; Protein unfolding and refolding; TIM; Triosephosphate isomerase

Indexed keywords

AMIDE; DEUTERIUM; GUANIDINE; HYDROGEN; ISOTOPE; MUSCLE ENZYME; POLYPEPTIDE; TRIOSEPHOSPHATE ISOMERASE; UREA; WATER;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DENATURATION; DILUTION; ELECTROSPRAY MASS SPECTROMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOTOPE LABELING; KINETICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STABILITY; RABBIT;

ORYCTOLAGUS CUNICULUS;

EID: 1242294469     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.12.076     Document Type: Article

References (32)

1. Farber G.K., Petsko G.A. The evolution of alpha/beta barrel enzymes. Trends Biochem. Sci. 15:1990;228-234.
2. Banner D.W., Bloomer A.C., Petsko G.A., Phillips D.C., Pogson C.I., Wilson I. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 angstrom resolution using amino acid sequence data. Nature. 255:1975;609-614.
3. Miranker A., Robinson C.V., Radford S.E., Aplin R.T., Dobson C.M. Detection of transient protein folding populations by mass spectrometry. Science. 262:1993;896-900.
4. Zhang Z., Smith D.L. Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci. 2:1993;522-531.
5. Englander J.J., Rogero J.R., Englander S.W. Protein hydrogen exchange studied by the fragment separation method. Anal. Biochem. 147:1985;234-244.
6. Gokhale R.S., Ray S.S., Balaram H., Balaram P. Unfolding of Plasmodium falciparum triosephosphate isomerase in urea and guanidinium chloride: evidence for a novel disulfide exchange reaction in a covalently cross-linked mutant. Biochemistry. 38:1999;423-431.
7. Rietveld A.W., Ferreira S.T. Kinetics and energetics of subunit dissociation/unfolding of TIM: the importance of oligomerization for conformational persistence and chemical stability of proteins. Biochemistry. 37:1998;933-937.
8. Pan, H. (2002). Characterization of folding intermediates of TIM barrel proteins by hydrogen exchange and mass spectrometry. PhD thesis, University of Nebraska.
9. Brandts J.F., Halvorson H.R., Brennan M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry. 14:1975;4953-4963.
10. Juminaga D., Wedemeyer W.J., Scheraga H.A. Proline isomerization in bovine pancreatic ribonuclease A. 1. Unfolding conditions. Biochemistry. 37:1998;11614-11620.
11. Wang L., Pan H., Smith D.L. Hydrogen exchange-mass spectrometry: optimization of digestion conditions. Mol. Cell. Proteomics. 1:2002;132-138.
12. Deng Y., Smith D.L. Rate and equilibrium constants for protein unfolding and refolding determined by hydrogen exchange-mass spectrometry. Anal. Biochem. 276:1999;150-160.
13. Deng Y., Smith D.L. Hydrogen exchange demonstrates three domains in aldolase unfold sequentially. J. Mol. Biol. 294:1999;247-258.
14. Sepulveda-Becerra M.A., Ferreira S.T., Strasser R.J., Garzon-Rodriguez W., Beltran C., Gomez-Puyou A., Darszon A. Refolding of triosephosphate isomerase in low-water media investigated by fluorescence resonance energy transfer. Biochemistry. 35:1996;15915-15922.
15. Mainfroid V., Terpstra P., Beauregard M., Frere J.M., Mande S.C., Hol W.G., et al. Three hTIM mutants that provide new insights on why TIM is a dimer. J. Mol. Biol. 257:1996;441-456.
16. Morgan C.J., Wilkins D.K., Smith L.J., Kawata Y., Dobson C.M. A compact monomeric intermediate identified by NMR in the denaturation of dimeric triose phosphate isomerase. J. Mol. Biol. 300:2000;11-16.
17. Chanez-Cardenas M.E., Fernandez-Velasco D.A., Vazquez-Contreras E., Coria R., Saab-Rincon G., Perez-Montfort R. Unfolding of triosephosphate isomerase from Trypanosoma brucei: identification of intermediates and insight into the denaturation pathway using tryptophan mutants. Arch. Biochem. Biophys. 399:2002;117-129.
18. Zabori S., Rudolph R., Jaenicke R. Folding and association of triose phosphate isomerase from rabbit muscle. Z. Naturforsch. [C]. 35:1980;999-1004.
19. Fernandez-Velasco D.A., Sepulveda-Becerra M., Galina A., Darszon A., Tuena de Gomez-Puyou M., Gomez-Puyou A. Water requirements in monomer folding and dimerization of triosephosphate isomerase in reverse micelles. Intrinsic fluorescence of conformers related to reactivation. Biochemistry. 34:1995;361-369.
20. Lang D., Thoma R., Henn-Sax M., Sterner R., Wilmanns M. Structural evidence for evolution of the beta/alpha barrel scaffold by gene duplication and fusion. Science. 289:2000;1546-1550.
21. Hocker B., Beismann-Driemeyer S., Hettwer S., Lustig A., Sterner R. Dissection of a (beta alpha)8-barrel enzyme into two folded halves. Nature Struct. Biol. 8:2001;32-36.
22. Bertolaet B.L., Knowles J.R. Complementation of fragments of triosephosphate isomerase defined by exon boundaries. Biochemistry. 34:1995;5736-5743.
23. Crisanti M.M., Matthews C.R. Characterization of the slow steps in the folding of the alpha subunit of tryptophan synthase. Biochemistry. 20:1981;2700-2706.
24. Miles E.W., Yutani K., Ogasahara K. Guanidine hydrochloride induced unfolding of the alpha subunit of tryptophan synthase and of the two alpha proteolytic fragments: evidence for stepwise unfolding of the two alpha domains. Biochemistry. 21:1982;2586-2592.
25. Godzik A., Skolnick J., Kolinski A. Simulations of the folding pathway of triose phosphate isomerase-type alpha/beta barrel proteins. Proc. Natl Acad. Sci. USA. 89:1992;2629-2633.
26. Zitzewitz J.A., Matthews C.R. Molecular dissection of the folding mechanism of the alpha subunit of tryptophan synthase: an amino-terminal autonomous folding unit controls several rate-limiting steps in the folding of a single domain protein. Biochemistry. 38:1999;10205-10214.
27. Eder J., Kirschner K. Stable substructures of eightfold beta alpha-barrel proteins: fragment complementation of phosphoribosylanthranilate isomerase. Biochemistry. 31:1992;3617-3625.
28. Jasanoff A., Davis B., Fersht A.R. Detection of an intermediate in the folding of the (beta alpha)8-barrel N-(5′-phosphoribosyl)anthranilate isomerase from Escherichia coli. Biochemistry. 33:1994;6350-6355.
29. Zitzewitz J.A., Gualfetti P.J., Perkons I.A., Wasta S.A., Matthews C.R. Identifying the structural boundaries of independent folding domains in the alpha subunit of tryptophan synthase, a beta/alpha barrel protein. Protein Sci. 8:1999;1200-1209.
30. Deng Y., Smith D.L. Identification of unfolding domains in large proteins by their unfolding rates. Biochemistry. 37:1998;6256-6262.
31. Pan H., Smith D.L. Quaternary structure of aldolase leads to differences in its folding and unfolding intermediates. Biochemistry. 42:2003;5713-5721.
32. Chen J., Smith D.L. Unfolding and disassembly of the chaperonin GroEL occurs via a tetradecameric intermediate with a folded equatorial domain. Biochemistry. 39:2000;4250-4258.