Plasticity and steric strain in a parallel β-helix: Rational mutations in the P22 tailspike protein

Proteins: Structure, Function and Genetics

Volumn 39, Issue 1, 2000, Pages 89-101

  Schuler, Benjamin ^a,d   Fürst, Frank ^b   Osterroth, Frank ^a   Steinbacher, Stefan ^c   Huber, Robert ^c   Seckler, Robert ^b  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF POTSDAM   (Germany)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Active site; Backbone dihedral angles; Parallel beta helix; Protein folding; Protein stability; Temperature sensitive mutants

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACTERIOPHAGE P22; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SALMONELLA; TEMPERATURE SENSITIVE MUTANT;

BACTERIOPHAGE P22; BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; GLYCOSIDE HYDROLASES; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; THERMODYNAMICS; VIRAL TAIL PROTEINS;

BACTERIA (MICROORGANISMS); SALMONELLA;

EID: 17344380271     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(20000401)39:1<89::AID-PROT10>3.0.CO;2-Q     Document Type: Article

References (59)

1. Yoder MD, Keen NT, Jurnak F. New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science 1994;260:1503-1507.
2. Levitt M, Chothia C. Structural patterns in globular proteins. Nature 1976;261:552-558.
3. Richardson JS. The anatomy and taxonomy of protein structure. Adv Protein Chem 1981;34:167-339.
4. Sprang SR. On a (β-) roll. Trends Biochem Sci 1993;18:313-314.
5. Baumann U, Wu S, Flathery KM, McKay DB. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 1993;12:3357-3364.
6. Steinbacher S, Seckler R, Miller S, Steipe B, Huber R, Reinemer P. Crystal structure of P22 tailspike-protein, interdigitated subunits in a thermostable trimer. Science 1994;265:383-386.
7. Steinbacher S, Miller S, Baxa U, Budisa N, Weintraub A, Seckler R, Huber R. Phage P22 tailspike protein: crystal structure of the head-binding domain at 2.3 Å, fully refined structure of the endorhamnosidase at 1.56 Å resolution, and the molecular basis of O-antigen recognition and cleavage. J Mol Biol 1997;267:865-880.
8. Pickersgill R, Jenkins J, Harris G, Nasser W, Robert-Baudouy J. The structure of Bacillus subtilis pectate lyase in complex with calcium. Nature Struct Biol 1994;1:717-723.
9. Lietzke SE, Keen NT, Yoder MD, Jurnak F. The three-dimensional structure of pectate lyase E, a plant virulence factor from Erwinia chrysanthemi. Plant Physiol 1994;106:849-862.
10. Raetz CRH, Roderick SL. A left-handed parallel β helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 1995;270:997-1000.
11. Kisker C, Schindelin H, Alber BE, Ferry JG, Rees DC. A left-handed β-helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila. EMBO J 1996;15:2323-2330.
12. Emsley P, Charles IG, Fairweather NF, Isaacs NW. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 1996; 381:90-92.
13. Mayans O, Scott M, Connerton I, Gravesen T, Benen J, Visser J, Pickersgill R, Jenkins J. Two crystal structures of pectin lyase A from Aspergillus reveal a pH driven conformational change and striking divergence in the substrate-binding clefts of pectin and pectate lyases. Structure 1997;5:677-689.
14. Petersen TN, Kauppinen S, Larsen S. The crystal structure of rhamnogalacturonase A from Aspergillus aculeatus: a right-handed parallel β helix. Structure 1997;5:533-544.
15. Beaman TW, Binder DA, Blanchard JS, Roderick SL. Three-dimensional structure of tetrahydrodipicolinate N-succinyltransferase. Biochemistry 1997;36:489-494.
16. Vitali J, Schick B, Kester HCM, Visser J, Jurnak F. The three-dimensional structure of Aspergillus niger pectin lyase b at 1.7-Å resolution. Plant Physiol 1998;116:69-80.
17. Pickersgill R, Smith D, Worboys K, Jenkins J. Crystal structure of polygalacturonase from Erwinia carotovora ssp. Carotovora. J Biol Chem 1998;38:24660-24664.
18. Beaman TW, Sugantino M, Roderick SL. Structure of the hexapeptide xenobiotic acetyltransferase from Pseudomonas aeruginosa. Biochemistry 1998;12:6689-6696.
19. Yoder MD, Jurnak F. The parallel β helix and other coiled folds. FASEB J 1995;9:335-342.
20. Heffron S, Moe GR, Siebert V, Mengaud J, Cossart P, Vitali J, Jurnak F. Sequence profile of the parallel β helix in the pectate lyase superfamily. J Struct Biol 1998;122:223-235.
21. Steinbacher S, Baxa U, Miller S, Weintraub A, Seckler R, Huber R. Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci USA 1996;93:10584-10588.
22. Goldenberg DP, Berget PB, King J. Maturation of the tail spike endorhamnosidase of bacteriophage P22. J Biol Chem 1982;257: 7864-7871.
23. Goldenberg D, King J. Trimeric intermediate in the in vivo folding and assembly of the tail spike endorhamnosidase of bacteriophage P22. Proc Natl Acad Sci USA 1982;79:3403-3407.
24. Fuchs A, Seiderer C, Seckler R. In vitro folding pathway of the P22 tailspike protein. Biochemistry 1991;30:6598-6604.
25. Danner M, Seckler R. Mechanism of phage P22 tailspike protein folding mutations. Protein Sci 1993;2:1869-1881.
26. Betts SD, Haase-Pettingell C, King J. Mutational effects on inclusion body formation. Adv Prot Chem 1997;50:243-264.
27. Haase-Pettingell CA, King J. Formation of aggregates from a thermolabile in vivo folding intermediate in P22 tailspike maturation. A model for inclusion body formation. J Biol Chem 1988;263: 4977-4983.
28. Danner M, Fuchs A, Miller S, Seckler R. Folding and assembly of phage P22 tailspike endorhamnosidase lacking the N-terminal, head-binding domain. Eur J Biochem 1993;215:653-661.
29. Yu M-H, King J. Single amino acid substitutions influence the folding pathway of phage P22 tail spike endorhamnosidase. Proc Natl Acad Sci USA 1984;81:6584-6588.
30. Yu M-H, King J. Surface amino acids as sites of temperature-sensitive folding mutations in the P22 tailspike protein. J Biol Chem 1988;263:1424-1431.
31. Villafane R, King J. Nature and distribution of temperature-sensitive folding mutations in the gene for the P22 tailspike polypeptide chain. J Mol Biol 1988;204:607-619.
32. Goldenberg D, King J. Temperature-sensitive mutants blocked in the folding or subunit assembly of the bacteriophage P22 tailspike protein. II. Active mutant proteins matured at 30°C. J Mol Biol 1981;145:633-651.
33. Haase-Pettingell C, King J. Prevalence of temperature sensitive folding mutations in the parallel beta coil domain of the phage P22 tailspike endorhamnosidase. J Mol Biol 1997;267:88-102.
34. Fane B, Villafane R, Mitraki A, King J. Identification of global suppressors for temperature-sensitive folding mutations in the P22 tailspike protein. J Biol Chem 1991;266:11640-11648.
35. Mitraki A, Fane B, Haase-Pettingell C, Sturtevant J, King J. Global suppression of protein folding defects and inclusion body formation. Science 1991;253:54-58.
36. Lee SC, Koh H, Yu MH. Molecular properties of global suppressors of temperature-sensitive folding mutations in P22 tailspike endorhamnosidase. J Biol Chem 1991;266:23191-23196.
37. Beißinger M, Lee SC, Steinbacher S, Reinemer P, Huber R, Yu M-H, Seckler R. Mutations that stabilize folding intermediates of phage P22 tailspike protein: folding in vivo and in vitro, stability, and structural context. J Mol Biol 1995;249:185-194.
38. Schuler B, Seckler R. P22 tailspike folding mutants revisited: effects on the thermodynamic stability of the isolated β-helix domain. J Mol Biol 1998;281:227-234.
39. Miller S, Schuler B, Seckler R. Phage P22 tailspike protein: Removal of head-binding domain unmasks effects of folding mutations on native-state thermal stability. Protein Sci 1998;7: 2223-2232.
40. Pace CN. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 1986;131: 266-280.
41. Baxa U, Steinbacher S, Miller S, Weintraub A, Huber R, Seckler R. Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide. Biophys J 1996;71:2040-2048.
42. Kunkel TA, Roberts JD, Zakour RA. Rapid and efficient site-directed mutagenesis without phenotypic selection. Methods Enzymol 1987;154:367-382.
43. Yuckenberg PD, Witney F, Geisselsoder J, McClary J. Site-directed in vitro mutagenesis using uracil-containing DNA and phagemid vectors. In: MacPherson MJ, editor. Directed mutagenesis, a practical approach. Oxford: IRL Press, 1991:27-48.
44. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci 1995;4:2411-2423.
45. Seckler R, Fuchs A, King J, Jaenicke R. Reconstitution of the thermostable trimeric phage P22 tailspike protein from denatured chains in vitro. J Biol Chem 1989;264:11750-11753.
46. Brunschier R, Danner M, Seckler R. Interactions of phage P22 Tailspike protein with GroE molecular chaperones during refolding in vitro. J Biol Chem 1993;268:2767-2772,
47. Leslie AGW. Recent changes to the MOSFLM package for processing film and image plate data. In: CCP4 & ESF-EACMB Newsletter on Protein Crystallography, SERC Laboratory, Daresbury, Warrington WA4 4AD, England, 1991.
48. Engh RA, Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog Sect A 1991;47:392-400.
49. Laskowski RA, MacArthur MW, Moss DS, Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 1993;26:283-291.
50. Baxa U, Steinbacher S, Weintraub A, Huber R, Seckler R. Mutations improving the folding of phage P22 tailspike protein affect its receptor binding activity. J Mol Biol 1999;293:693-701.
51. Klemm JD, Wozniak JA, Alber T, Goldenberg DP. Correlation between mutational destabilization of phage T4 lysozyme and increased unfolding rates. Biochemistry 1991;30:589-594.
52. Dunbrack RL Jr, Cohen FE. Bayesian statistical analysis of protein side-chain rotamer preferences. Protein Sci 1997;6:1661-1681.
53. Lee SC, Yu MH. Side-chain specificity at three temperature-sensitive folding mutation sites of P22 tailspike protein. Biochem Biophys Res Commun 1997;233:857-862.
54. Herzberg O, Moult J. Analysis of the steric strain in the polypeptide backbone of protein molecules. Proteins 1991;11:223-229.
55. Shoichet BK, Baase WA, Kuroki R, Matthews BW. A relationship between protein stability and protein function. Proc Natl Acad Sci USA 1995;92:452-456.
56. Stiles WE, Pranata J. Empirical evaluation of the influence of side chains on the conformational entropy of the polypeptide backbone. Proteins 1995;22:132-140.
57. D'Aquino JA, Gómez J, Hilser VJ, Lee KH, Amzel LM, Freire E. The magnitude of the backbone conformational entropy change in protein folding. Proteins 1996;25:143-156.
58. Fane B, King J. Intragenic suppressors of folding defects in the P22 tailspike protein. Genetics 1991;127:263-277.
59. Koradi R, Billeter M, Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 1996;14:51-55.