Probing the structural role of an αβ loop of maltose-binding protein by mutagenesis: Heat-shock induction by loop variants of the maltose-binding protein that form periplasmic inclusion bodies

Journal of Molecular Biology

Volumn 262, Issue 2, 1996, Pages 140-150

  Betton, Jean Michel ^a   Boscus, Didier ^a   Missiakas, Dominique ^b   Raina, Satish ^b   Hofnung, Maurice ^a  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Heat shock; Inclusion bodies; Loop; Maltose binding protein; Protein folding

Indexed keywords

CYTOPLASM PROTEIN; MALTOSE BINDING PROTEIN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BETA CHAIN; CELL INCLUSION; ESCHERICHIA COLI; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE;

ESCHERICHIA COLI;

EID: 0030595346     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0504     Document Type: Article

References (46)

1. Berstein, F. C., Koetzle, T., F., Williams, G. J. B., Meyer, E. F., Jr, Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. & Tasumi, M. (1977). The protein data bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542.
2. Betton, J. M. & Hofnung, M. (1994). In vivo assembly of active maltose binding protein from independently exported protein fragments. EMBO J. 13, 1226-1234.
3. Betton, J. M. & Hofnung, M. (1996). Folding of a mutant maltose binding protein of E. coli which forms inclusion bodies. J. Biol. Chem. 271, 8046-8052.
4. Brunet, A. P., Huang, E. S., Huffine, M.-E., Loeb, J. E., Weltman, R. J. & Hecht, M. H. (1993). The role of turns in the structure of an α-helical protein. Nature, 364, 355-358.
5. Castagnoli, L., Vetriani, C. & Cesarini, G. (1994). Linking an easily detectable phenotype to the folding of a common structural motif. J. Mol. Biol. 237, 378-387.
6. Chun, S.-Y., Strobel, S., Bassford, P. J. & Randall, L. L. (1993). Folding of maltose-binding protein. J. Biol. Chem. 268, 20855-20862.
7. Duplay, P., Szmelcman, S., Bedouelle, H. & Hofnung, M. (1987). Silent and functional changes in the periplasmic maltose-binding protein of Escherichia coli K12. J. Mol. Biol. 194, 663-673.
8. Dyson, H. J. & Wright, P. E. (1991). Defining solution conformations of small linear peptides. Annu. Rev. Biophys. Chem. 20, 519-538.
9. Edwards, M. S., Sternberg, M. J. E. & Thornton, J. M. (1987). Structural and sequence patterns in the loops of βαβ units. Protein Eng. 1, 173-181.
10. Haase-Pettingell, C. A. & King, J. (1988). Formation of aggregates from thermolabile in-vivo folding intermediate in P22 tailspike maturation. J. Biol. Chem. 263, 4977-4983.
11. Hartl, F.-U., Hlodan, R. & Langer, T. (1994). Molecular chaperones in protein folding: the art of avoiding sticky situations. Trends Biochem. Sci. 19, 20-25.
12. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
13. King, J., Fane, B., Haase-Pettingell, C., Mitraki, A., Villafane, R. & Yu, M.-H. (1990). Identification of amino acid sequences influencing intracellular folding pathways using temperature-sensitive folding mutations. Protein Folding: Deciphering the Second Half of the Genetic Code (Gierasch, L. M. & King, J., eds), pp. 225-240, American Association for the Advancement of Science, Washington, DC.
14. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
15. Kunkel, T. A. (1985). Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA, 82, 488-492.
16. LaBean, T. H. & Kauffman, S. A. (1993). Design of synthetic gene libraries encoding random sequence proteins with desired ensemble characteristics. Protein Sci. 2, 1249-1254.
17. Lipinska, B., Fayet, O., Baird, L. & Georgopoulos, C. (1989). Identification, characterization, and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J. Bacteriol. 171, 1574-1584.
18. E, an Escherichia coli heat-inducible s-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7, 2618-2628.
19. Miller, J. H. (1992). A Short Course in Bacterial Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Mitraki, A. & King, J. (1989). Protein folding intermediates and inclusion body formation. Bio/Technology, 7, 690-697.
21. Mowbray, S. L. & Cole, L. B. (1992). 1.7 Å X-ray structure of the periplasmic ribose receptor from Escherichia coli. J. Mol. Biol. 225, 155-175.
22. Oh, B.-H., Pandit, J., Kang, C-H., Nikaido, K., Gokcen, S., Ames, G. F.-L. & Kim, S.-H. (1993). Three-dimensional structures of the periplasmic lysine/arginine/ornithine-binding protein. J. Biol. Chem. 268, 11348-11355.
23. Oh, B.-H., Kang, C-H., De Bondt, H., Kim, S.-H., Nikaido, K., Joshi, A. K. & Ames, G. F.-L. (1994). The bacterial periplasmic histidine-binding protein. J. Biol. Chem. 269, 4135-4143.
24. Pflugrath, J. W. & Quiocho, F. A. (1988). The 2 Å resolution structure of the sulfate-binding protein involved in active transport in Salmonella typhimurium. J. Mol. Biol. 200, 163-180.
25. Predki, P. F., Agrawal, V., Brünger, A. T. & Regan, L. (1996). Amino acid substitutions in a surface turn modulate protein stability. Nature Struct. Biol. 3, 54-58.
26. Quiocho, F. (1991). Atomic structures and function of periplasmic receptors for active transport and chemotaxis. Curr. Opin. Struct. Biol. 1, 922-933.
27. Quiocho, F. A. & Vyas, N. K. (1984). Novel stereospecificity of the L-arabinose-binding protein. Nature, 310, 381-386.
28. 24) heat shock sigma factor of Escherichia coli. EMBO J. 14, 1043-1055.
29. E, in Escherichia coli. EMBO J. 14, 1032-1042.
30. Sack, J. S., Trackhanov, S. G., Tsigannik, I. H. & Quiocho, F. A. (1989). Structure of the L-leucine-binding protein refined at 2.4 Å resolution and comparaison with the leu/ile/val-binding protein structure. J. Mol. Biol. 206, 192-207.
31. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Schatz, P. J. & Beckwith, J. (1990). Genetic analysis of protein export in Escherichia coli. Annu. Rev. Genet. 24, 215-248.
33. Schimmel, P. R. & Flory, P. J. (1968). Conformational energies and configurational statistics of copolypeptides containing L-proline. J. Mol. Biol. 34, 105-120.
34. Sharff, A. J., Rodseth, L. E., Spurlino, J. C. & Qiocho, F. A. (1992). Crystallographic evidence of a large ligand-induced hinge-twist motion between the two domains of the maltodextrin binding protein involved in active transport and chemotaxis. Biochemistry, 31, 10657-10663.
35. Song, T. & Park, C. (1995). Effect of folding on the export of ribose-binding protein studied with the genetically isolated suppressors for the signal sequence mutation. J. Mol. Biol. 253, 304-312.
36. Spurlino, J. C., Lu, G. Y. & Quiocho, F. A. (1991). The 2.3-Å resolution structure of the maltose-or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. J. Biol. Chem. 266, 5202-5219.
37. Strauch, K. L., Johnson, K. & Beckwith, J. (1989). Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171, 2689-2696.
38. Swindells, M. B., MacArthur, M. W. & Thornton, J. M. (1995). Intrinsic φ, ψ propensities of amino acids, derived from the coil regions of known structures. Nature Struct. Biol. 2, 596-603.
39. Tame, J. R. H., Murshudov, G. N., Dodson, E. J., Neil, T. K., Dodson, G. G., Higgins, C. F. & Wilkinson, A. J. (1994). The structural basis of sequence-independent peptide binding by Oppa protein. Science, 264, 1578-1581.
40. Thorn, J. R. & Randall, L. L. (1988). Role of the leader peptide of maltose-binding protein in two steps of the export process. J. Bacteriol. 170, 5654-5661.
41. Vyas, N. K., Vyas, M. N. & Quiocho, F. A. (1988). Sugar and signal-transducer binding sites of the Escherichia coli galactose chemoreceptor protein. Science, 242, 1290-1295.
42. Vyas, N. K., Vyas, M. N. & Quiocho, F. A. (1991). Comparaison of the periplasmic receptors for L-arabinose, D-glucose/D-galactose, and D-ribose. J. Biol. Chem. 266, 5226-5237.
43. Wells, J. A., Vasser, M. & Powers, D. B. (1985). Cassette mutagenesis: an efficient method for generation of multiple mutations at defined sites. Gene, 34, 315-323.
44. Wilmot, C. M. & Thornton, J. M. (1990). β-Turns and their distortions: a proposed new nomeclature. Protein Eng. 3, 479-493.
45. Wintjens, R. T., Rooman, M. J. & Wodak, S. J. (1996). Automatic classification and analysis of αα-turn motifs in proteins. J. Mol. Biol. 255, 235-253.
46. Zoller, M. J. & Smith, M. (1987). Oligonucleotide-directed mutagenesis: a simple method using two oligonucleotide primers and a single-stranded DNA template. Methods Enzymol. 154, 329-350.