Mapping the Structure of Folding Cores in TIM Barrel Proteins by Hydrogen Exchange Mass Spectrometry: The Roles of Motif and Sequence for the Indole-3-glycerol Phosphate Synthase from Sulfolobus solfataricus

Journal of Molecular Biology

Volumn 368, Issue 2, 2007, Pages 582-594

  Gu, Zhenyu ^a   Zitzewitz, Jill A ^a   Matthews, C Robert ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

equilibrium intermediate; hydrophobic clusters; modular assembly; protein folding; thermodynamics of folding reactions

Indexed keywords

AMIDE; HYDROGEN; INDOLE 3 GLYCEROL PHOSPHATE SYNTHASE; ISOLEUCINE; LEUCINE; PEPSIN A; PROTEIN; PROTON; TRYPTOPHAN SYNTHASE; UREA; VALINE;

AMINO ACID SEQUENCE; ARTICLE; CORRELATION ANALYSIS; DENATURATION; DEUTERIUM HYDROGEN EXCHANGE; ELECTROSPRAY; HYDROPHOBICITY; KINETICS; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SULFOLOBUS SOLFATARICUS; THERMODYNAMICS;

SULFOLOBUS SOLFATARICUS;

EID: 33947593231     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.02.027     Document Type: Article

References (41)

1. Vega M.C., Lorentzen E., Linden A., and Wilmanns M. Evolutionary markers in the (β/α)8-barrel fold. Curr. Opin. Chem. Biol. 7 (2003) 694-701
2. 8-barrel enzymes. Curr. Opin. Chem. Biol. 7 (2003) 252-264
3. Nagano N., Orengo C.A., and Thornton J.M. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321 (2002) 741-765
4. Wierenga R.K. The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Letters 492 (2001) 193-198
5. 8-barrel enzyme fold. Chem. Rev. 105 (2005) 4038-4055
6. Gualfetti P.J., Bilsel O., and Matthews C.R. The progressive development of structure and stability during the equilibrium folding of the α subunit of tryptophan synthase from Escherichia coli. Protein Sci. 8 (1999) 1623-1635
7. 8 barrels. J. Mol. Biol. 320 (2002) 1119-1133
8. Sanchez del Pino M.M., and Fersht A.R. Nonsequential unfolding of the α/β barrel protein indole-3-glycerol-phosphate synthase. Biochemistry 36 (1997) 5560-5565
9. 8-barrel N-(5′-phosphoribosyl)anthranilate isomerase from Escherichia coli. Biochemistry 33 (1994) 6350-6355
10. Bilsel O., Zitzewitz J.A., Bowers K.E., and Matthews C.R. Folding mechanism of the α-subunit of tryptophan synthase, an α/β barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry 38 (1999) 1018-1029
11. Higgins W., Fairwell T., and Miles E.W. An active proteolytic derivative of the α subunit of tryptophan synthase. Identification of the site of cleavage and characterization of the fragments. Biochemistry 18 (1979) 4827-4835
12. Miles E.W., Yutani K., and Ogasahara K. Guanidine hydrochloride induced unfolding of the α subunit of tryptophan synthase and of the two α proteolytic fragments: evidence for stepwise unfolding of the two α domains. Biochemistry 21 (1982) 2586-2592
13. Eder J., and Kirschner K. Stable substructures of eightfold βα-barrel proteins: fragment complementation of phosphoribosylanthranilate isomerase. Biochemistry 31 (1992) 3617-3625
14. Zitzewitz J.A., Gualfetti P.J., Perkons I.A., Wasta S.A., and Matthews C.R. Identifying the structural boundaries of independent folding domains in the α subunit of tryptophan synthase, a β/α barrel protein. Protein Sci. 8 (1999) 1200-1209
15. Akanuma S., and Yamagishi A. Identification and characterization of key substructures involved in the early folding events of a (β/α)8-barrel protein as studied by experimental and computational methods. J. Mol. Biol. 353 (2005) 1161-1170
16. Hocker B., Beismann-Driemeyer S., Hettwer S., Lustig A., and Sterner R. Dissection of a (βα)8-barrel enzyme into two folded halves. Nature Struct. Biol. 8 (2001) 32-36
17. Hocker B., Claren J., and Sterner R. Mimicking enzyme evolution by generating new (βα)8-barrels from (βα)4-half-barrels. Proc. Natl Acad. Sci. USA 101 (2004) 16448-16453
18. Rojsajjakul T., Wintrode P., Vadrevu R., Robert Matthews C., and Smith D.L. Multi-state unfolding of the α subunit of tryptophan synthase, a TIM barrel protein: insights into the secondary structure of the stable equilibrium intermediates by hydrogen exchange mass spectrometry. J. Mol. Biol. 341 (2004) 241-253
19. Pan H., and Smith D.L. Quaternary structure of aldolase leads to differences in its folding and unfolding intermediates. Biochemistry 42 (2003) 5713-5721
20. Pan H., Raza A.S., and Smith D.L. Equilibrium and kinetic folding of rabbit muscle triosephosphate isomerase by hydrogen exchange mass spectrometry. J. Mol. Biol. 336 (2004) 1251-1263
21. Silverman J.A., and Harbury P.B. The equilibrium unfolding pathway of a (β/α)8 barrel. J. Mol. Biol. 324 (2002) 1031-1040
22. Andreotti G., Tutino M.L., Sannia G., Marino G., and Cubellis M.V. Indole-3-glycerol-phosphate synthase from Sulfolobus solfataricus as a model for studying thermostable TIM-barrel enzymes. Biochim. Biophys. Acta 1208 (1994) 310-315
23. Krishna M.M., Hoang L., Lin Y., and Englander S.W. Hydrogen exchange methods to study protein folding. Methods 34 (2004) 51-64
24. Simler B.R., Levy Y., Onuchic J.N., and Matthews C.R. The folding energy landscape of the dimerization domain of Escherichia coli Trp repressor: a joint experimental and theoretical investigation. J. Mol. Biol. 363 (2006) 262-278
25. Schneider B., Knochel T., Darimont B., Hennig M., Dietrich S., Babinger K., et al. Role of the N-terminal extension of the (βα)8-barrel enzyme indole-3-glycerol phosphate synthase for its fold, stability, and catalytic activity. Biochemistry 44 (2005) 16405-16412
26. Miranker A., Robinson C.V., Radford S.E., Aplin R.T., and Dobson C.M. Detection of transient protein folding populations by mass spectrometry. Science 262 (1993) 896-900
27. 8 barrel proteins based on hydrophobicity, long-range interactions, and sequence conservation. Proteins: Struct. Funct. Genet. 55 (2004) 316-329
28. Wu Y., Vadrevu R., Kathuria S., Yang X., and Matthews C.R. A tightly-packed hydrophobic cluster directs the formation of an off-pathway sub-millisecond folding intermediate in the alpha subunit of tryptophan synthase, a TIM barrel protein. J. Mol. Biol. 366 (2006) 1624-1638
29. Wu Y., Vadrevu R., Yang X., and Matthews C.R. Specific structure appears at the N terminus in the sub-millisecond folding intermediate of the α subunit of tryptophan synthase, a TIM barrel protein. J. Mol. Biol. 351 (2005) 445-452
30. Branden C., and Tooze J. Introduction to Protein Structure. 2nd edit. (1999), Garland Publishing, Inc., New York
31. Bai Y., Sosnick T.R., Mayne L., and Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science 269 (1995) 192-197
32. Maity H., Maity M., and Englander S.W. How cytochrome c folds, and why: submolecular foldon units and their stepwise sequential stabilization. J. Mol. Biol. 343 (2004) 223-233
33. Krishna M.M., Maity H., Rumbley J.N., Lin Y., and Englander S.W. Order of steps in the cytochrome c folding pathway: evidence for a sequential stabilization mechanism. J. Mol. Biol. 359 (2006) 1410-1419
34. Weinkam P., Zong C., and Wolynes P.G. A funneled energy landscape for cytochrome c directly predicts the sequential folding route inferred from hydrogen exchange experiments. Proc. Natl Acad. Sci. USA 102 (2005) 12401-12406
35. Maity H., Maity M., Krishna M.M., Mayne L., and Englander S.W. Protein folding: the stepwise assembly of foldon units. Proc. Natl Acad. Sci. USA 102 (2005) 4741-4746
36. Chamberlain A.K., Handel T.M., and Marqusee S. Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nature Struct. Biol. 3 (1996) 782-787
37. Chu R., Pei W., Takei J., and Bai Y. Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 41 (2002) 7998-8003
38. Mandell J.G., Falick A.M., and Komives E.A. Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc. Natl Acad. Sci. USA 95 (1998) 14705-14710
39. Mandell J.G., Falick A.M., and Komives E.A. Measurement of amide hydrogen exchange by MALDI-TOF mass spectrometry. Anal. Chem. 70 (1998) 3987-3995
40. Hennig M., Darimont B.D., Jansonius J.N., and Kirschner K. The catalytic mechanism of indole-3-glycerol phosphate synthase: crystal structures of complexes of the enzyme from Sulfolobus solfataricus with substrate analogue, substrate, and product. J. Mol. Biol. 319 (2002) 757-766
41. Sobolev V., Eyal E., Gerzon S., Potapov V., Babor M., Prilusky J., and Edelman M. SPACE: a suite of tools for protein structure prediction and analysis based on complementarity and environment. Nucl. Acids Res. 33 (2005) W39-W43