Mutations improving the folding of phage P22 tailspike protein affect its receptor binding activity

Journal of Molecular Biology

Volumn 293, Issue 3, 1999, Pages 693-701

  Baxa, Ulrich ^a   Steinbacher, Stefan ^b   Weintraub, Andrej ^c   Huber, Robert ^b   Seckler, Robert ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Endoglycosidase; Parallel helix; Protein folding; Protein carbohydrate recognition; Structure function relationship

Indexed keywords

BACTERIAL ANTIGEN; GLYCOSIDASE; MUTANT PROTEIN; POLYSACCHARIDE; STRUCTURAL PROTEIN;

ARTICLE; BACTERIOPHAGE P22; BINDING AFFINITY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; RECEPTOR BINDING; SALMONELLA; THERMOSTABILITY;

BACTERIA (MICROORGANISMS); SALMONELLA; UNIDENTIFIED BACTERIOPHAGE;

EID: 0032754530     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3165     Document Type: Article

References (41)

1. 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. 71:1996;2040-2048.
2. Beißinger M., Lee S. C., 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. 249:1995;185-194.
3. Brünger A. T. X-PLOR, Version 3.1: A system for crystallography and NMR. 1992;Yale University Press, New Haven.
4. Chrunyk B. A., Evans J., Lillquist J., Young P., Wetzel R. Inclusion body formation and protein stability in sequence variants of interleukin-1β J. Biol. Chem. 268:1993;18053-18061.
5. Acta Crystallog. sect. D. 50:1994;760-763.
6. Danner M., Seckler R. Mechanism of phage P22 tailspike protein folding mutations. Protein Sci. 2:1993;1869-1881.
7. 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. 215:1993;653-661.
8. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
9. Eriksson U., Svenson S. B., Lönngren J., Lindberg A. A. Salmonella phage glycanases: substrate specificity of the phage P22 endo-rhamnosidase. J. Gen. Virol. 43:1979;503-511.
10. Fane B., King J. Intragenic suppressors of folding defects in the P22 tailspike protein. Genetics. 127:1991;263-277.
11. Fane B., Villafane R., Mitraki A., King J. Identification of global suppressors for temperature-sensitive folding mutations of the P22 tailspike protein. J. Biol. Chem. 266:1991;11640-11648.
12. Fuchs A., Seiderer C., Seckler R. In vitro folding pathway of phage P22 tailspike protein. Biochemistry. 30:1991;6598-6604.
13. 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. 79:1982;3403-3407.
14. Goldenberg D. P., Berget P. B., King J. Maturation of the tail spike endorhamnosidase of Salmonella phage P22. J. Biol. Chem. 257:1982;7864-7871.
15. Haase-Pettingel C., King J. Formation of aggregates from a thermolabile in vivo folding intermediate in P22 tailspike maturation. J. Biol. Chem. 263:1988;4977-4983.
16. Hibler D. W., Stolowich N. J., Reynolds M. A., Gerlt J. A., Wilde J. A., Bolton P. H. Site-directed mutants of staphylococcal nuclease. Detection and localization by 1H NMR spectroscopy of conformational changes accompanying substitutions for glutamic acid-43. Biochemistry. 26:1987;6278-6286.
17. Israel V. A model for the adsorption of phage P22 to Salmonella typhimurium. J. Gen. Virol. 40:1978;669-673.
18. Iwashita S., Kanegasaki S. Enzymatic and molecular properties of base-plate parts of bacteriophage P22. Eur. J. Biochem. 65:1976;87-94.
19. Jones T. A. A graphics model building & refinement system for macromolecules. J. Appl. Crystallog. 11:1978;268-272.
20. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
21. Lee S. C., Hyeyeong K., Yu M.-H. Molecular properties of global suppressors of temperature-sensitive folding mutations in P22 tailspike endorhamnosidase. J. Biol. Chem. 266:1991;23191-23196.
22. Leslie A. G. W. Recent changes to the MOSFLM package for processing film and image plate data. CCP4 & ESF-EACMB Newsletters on Protein Crystallography. 1991;SERC Laboratory, Daresbury, Warrington.
23. Mammen M., Dahmann G., Whitesides G. M. Effective inhibitors of hemagglutination by influenza virus synthesized from polymers having active ester groups. Insight into mechanism of inhibition. J. Med. Chem. 38:1995;4179-4190.
24. Meiering E. M., Serrano L., Fersht A. R. Effect of active site residues in barnase on activity and stability. J. Mol. Biol. 225:1992;585-589.
25. 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. 7:1998a;2223-2232.
26. Miller S., Schuler B., Seckler R. A reversibly unfolding fragment of P22 tailspike protein with native structure: The isolated β-helix domain. Biochemistry. 37:1998b;9160-9168.
27. Mitraki A., Fane B., Haase-Pettingell C., Sturtevant J., King J. Global suppression of protein folding defects and inclusion body formation. Science. 253:1991;54-58.
28. Mitraki A., Danner M., King J., Seckler R. Temperature-sensitive mutations and second-site suppressor substitutions affect folding of the P22 tailspike protein in vitro. J. Biol. Chem. 268:1993;20071-20075.
29. Mortell K. H., Weatherman R. V., Kiessling L. L. Recognition specificity of neoglycopolymers prepared by ring-opening metathesis polymerization. J. Am. Chem. Soc. 118:1996;2297-2298.
30. Pakula A. A., Sauer R. T. Amino acid substitutions that increase the thermal stability of the lambda Cro protein. Proteins: Struct. Funct. Genet. 5:1989;202-210.
31. Poole L. B., Loveys D. A., Hale S. P., Gerlt J. A., Stanczyk S. M., Bolton P. H. Deletion of the omega-loop in the active site of staphylococcal nuclease. 1. Effect on catalysis and stability. Biochemistry. 30:1991;3621-3627.
32. Schuler B., Seckler R. P22 tailspike folding mutants revisited: effects on thermodynamic stability of the isolated β-helix domain. J. Mol. Biol. 281:1998;227-234.
33. Seckler R. Folding and function of repetitive structure in the homotrimeric phage P22 tailspike protein. J. Struct. Biol. 122:1998;216-222.
34. Shoichet B. K., Baase W. A., Kuroki R., Matthews B. W. A relationship between protein stability and protein function. Proc. Natl Acad. Sci. USA. 92:1995;452-456.
35. 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. 265:1994;383-386.
36. 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. 93:1996;10584-10588.
37. 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. 267:1997;865-880.
38. Svenson S. B., Lönngren J., Carlin N., Lindberg A. A. Salmonella bacteriophage glycanases: endorhamnosidases of Salmonella typhimurium bacteriophages. J. Virol. 32:1979;583-592.
39. Villafane R., King J. Nature and distribution of temperature-sensitive folding mutations in the gene for the P22 tailspike polypeptide chain. J. Mol. Biol. 204:1988;607-619.
40. Yu M.-H., King J. Single amino acid substitutions influencing the folding pathway of the phage P22 tail spike endorhamnosidase. Proc. Natl Acad. Sci. USA. 81:1984;6584-6588.
41. Yu M.-H., King J. Surface amino acids as sites of temperature-sensitive folding mutations in the P22 tailspike protein. J. Biol. Chem. 263:1988;1424-1431.