βα-Hairpin clamps brace βαβ modules and can make substantive contributions to the stability of TIM barrel proteins

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Yang, Xiaoyan ^a   Kathuria, Sagar V ^a   Vadrevu, Ramakrishna ^a,b   Matthews, C Robert ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; TIM BARREL PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; ESCHERICHIA COLI; NONHUMAN; PREDICTION; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SULFOLOBUS SOLFATARICUS; CHEMISTRY; CIRCULAR DICHROISM; CONFORMATION; HYDROGEN BOND; KINETICS; METABOLISM; METHODOLOGY; PH; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SULFOLOBUS; THERMODYNAMICS;

ALGORITHMS; BACTERIAL PROTEINS; CIRCULAR DICHROISM; ESCHERICHIA COLI; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR CONFORMATION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SULFOLOBUS; THERMODYNAMICS;

EID: 70349705579     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007179     Document Type: Article

References (47)

1. Nagano N, Orengo CA, Thornton JM (2002) One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol 321: 741-765.
2. Zitzewitz JA, Gualfetti PJ, Perkons IA, Wasta SA, Matthews CR (1999) Identifying the structural boundaries of independent folding domains in the a subunit of tryptophan synthase, a b/a barrel protein. Protein Sci 8: 1200-1209.
3. Gerstein M (1997) A structural census of genomes: comparing bacterial, eukaryotic, and archaeal genomes in terms of protein structure. J Mol Biol 274: 562-576.
4. Frenkel ZM, Trifonov EN (2005) Closed loops of TIM barrel protein fold. J Biomol Struct Dyn 22: 643-656.
5. FarzadFard F, Gharaei N, Pezeshk H, Marashi S-A (2008) [beta]-Sheet capping: Signals that initiate and terminate [beta]-sheet formation. Journal of Structural Biology 161: 101-110.
6. Yang X, Vadrevu R, Wu Y, Matthews CR (2007) Long-range side-chain-main-chain interactions play crucial roles in stabilizing the (betaalpha)8 barrel motif of the alpha subunit of tryptophan synthase. Protein Sci 16: 1398-1409.
7. Baker EN, Hubbard RE (1984) Hydrogen bonding in globular proteins. Prog Biophys Mol Biol 44: 97-179.
8. Stickle DF, Presta LG, Dill KA, Rose GD (1992) Hydrogen bonding in globular proteins. J Mol Biol 226: 1143-1159.
9. Presta LG, Rose GD (1988) Helix signals in proteins. Science 240: 1632-1641.
10. Aurora R, Rose GD (1998) Helix capping. Protein Sci 7: 21-38.
11. Horovitz A, Serrano L, Avron B, Bycroft M, Fersht AR (1990) Strength and cooperativity of contributions of surface salt bridges to protein stability. J Mol Biol 216: 1031-1044.
12. Serrano L, Kellis JT, Jr., Cann P, Matouschek A, Fersht AR (1992) The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability. J Mol Biol 224: 783-804.
13. Myers JK, Pace CN (1996) Hydrogen bonding stabilizes globular proteins. Biophys J 71: 2033-2039.
14. Ibarra-Molero B, Zitzewitz JA, Matthews CR (2004) Salt-bridges can stabilize but do not accelerate the folding of the homodimeric coiled-coil peptide GCN4-p1. J Mol Biol 336: 989-996.
15. Gromiha MM, Pujadas G, Magyar C, Selvaraj S, Simon I (2004) Locating the stabilizing residues in (alpha/beta)8 barrel proteins based on hydrophobicity, long-range interactions, and sequence conservation. Proteins 55: 316-329.
16. Matthews CR, Crisanti MM (1981) Urea-induced unfolding of the alpha subunit of tryptophan synthase: evidence for a multistate process. Biochemistry 20: 784-792.
17. Forsyth WR, Matthews CR (2002) Folding mechanism of indole-3-glycerol phosphate synthase from Sulfolobus solfataricus: a test of the conservation of folding mechanisms hypothesis in (beta(alpha))(8) barrels. J Mol Biol 320: 1119-1133.
18. Sanchez del Pino MM, Fersht AR (1997) Nonsequential unfolding of the alpha/beta barrel protein indole-3-glycerol-phosphate synthase. Biochemistry 36: 5560-5565.
19. Matthews CR (1987) Effect of point mutations on the folding of globular proteins. Methods Enzymol 154: 498-511.
20. Branden C, Tooze J (1999) Introduction to Protein Structure. New York: Garland Science Publishing. 302 p.
21. Schneider B, Knochel T, Darimont B, Hennig M, Dietrich S, et al. (2005) Role of the N-terminal extension of the (betaalpha)8-barrel enzyme indole-3-glycerol phosphate synthase for its fold, stability, and catalytic activity. Biochemistry 44: 16405-16412.
22. Wilmanns M, Priestle JP, Niermann T, Jansonius JN (1992) Three-dimensional structure of the bifunctional enzyme phosphoribosylanthranilate isomerase: indoleglycerolphosphate synthase from Escherichia coli refined at 2.0 A resolution. J Mol Biol 223: 477-507.
23. Hyde CC, Ahmed SA, Padlan EA, Miles EW, Davies DR (1988) Three-dimensional structure of the tryptophan synthase alpha 2 beta 2 multienzyme complex from Salmonella typhimurium. J Biol Chem 263: 17857-17871.
24. Wierenga RK (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett 492: 193-198.
25. Radzicka A, Wolfenden R (1988) Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry 27: 1664-1670.
26. Vadrevu R, Wu Y, Matthews CR (2008) NMR analysis of partially folded states and persistent structure in the alpha subunit of tryptophan synthase: implications for the equilibrium folding mechanism of a 29-kDa TIM barrel protein. J Mol Biol 377: 294-306.
27. Wu Y, Vadrevu R, Kathuria S, Yang X, Matthews CR (2007) 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: 1624-1638.
28. Gu Z, Zitzewitz JA, Matthews CR (2007) 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. J Mol Biol 368: 582-594.
29. Gao J, Bosco DA, Powers ET, Kelly JW (2009) Localized thermodynamic coupling between hydrogen bonding and microenvironment polarity substantially stabilizes proteins. Nat Struct Mol Biol 16: 684-690.
30. Kunin V, Chan B, Sitbon E, Lithwick G, Pietrokovski S (2001) Consistency analysis of similarity between multiple alignments: prediction of protein function and fold structure from analysis of local sequence motifs. J Mol Biol 307: 939-949.
31. Rohl CA, Strauss CE, Chivian D, Baker D (2004) Modeling structurally variable regions in homologous proteins with rosetta. Proteins 55: 656-677.
32. Brylinski M, Skolnick J (2009) FINDSITE: a threading-based approach to ligand homology modeling. PLoS Comput Biol 5: e1000405. doi:10.1371/ journal.-pcbi.1000405.
33. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
34. Gerlt JA, Babbitt PC (2009) Enzyme (re)design: lessons from natural evolution and computation. Curr Opin Chem Biol 13: 10-18.
35. Jurgens C, Strom A, Wegener D, Hettwer S, Wilmanns M, et al. (2000) Directed evolution of a (beta alpha)8-barrel enzyme to catalyze related reactions in two different metabolic pathways. Proc Natl Acad Sci U S A 97: 9925-9930.
36. Gerlt JA, Raushel FM (2003) Evolution of function in (beta/ alpha)8-barrel enzymes. Curr Opin Chem Biol 7: 252-264.
37. Wieczorek SJ, Kalivoda KA, Clifton JG, Ringe D, Petsko GA, et al. (1999) Evolution of enzymatic activities in the enolase superfamily: Identification of a "new" general acid catalyst in the active site of D-galactonate dehydratase from Escherichia coli. Journal of the American Chemical Society 121: 4540-4541.
38. Rothlisberger D, Khersonsky O, Wollacott AM, Jiang L, DeChancie J, et al. (2008) Kemp elimination catalysts by computational enzyme design. Nature 453: 190-195.
39. Altamirano MM, Blackburn JM, Aguayo C, Fersht AR (2000) Directed evolution of new catalytic activity using the alpha/beta-barrel scaffold. Nature 403: 617-622.
40. Bilsel O, Zitzewitz JA, Bowers KE, Matthews CR (1999) Folding mechanism of the alpha-subunit of tryptophan synthase, an alpha/beta barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry 38: 1018-1029.
41. Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247: 536-540.
42. Mizuguchi K, Deane CM, Blundell TL, Overington JP (1998) HOMSTRAD: a database of protein structure alignments for homologous families. Protein Sci 7: 2469-2471.
43. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
44. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
45. McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238: 777-793.
46. Delano WL (2002) The PyMOL Molecular Graphics System: DeLano Scientific.
47. 2 Test. Supplement to the Journal of the Royal Statistical Society 1: 217-235.