The non-penicillin-binding module of the tripartite penicillin-binding protein 3 of Escherichia Coli is required for folding and/or stability of the penicillin-binding module and the membrane-anchoring module confers cell septation activity on the folded structure
[en] The ftsI-encoded multimodular class B penicillin-binding protein 3 (PBP3) is a key element of the cell septation machinery of Escherichia coli. Altered ftsI genes were overexpressed, and the gene products were analyzed with respect to the level of production, stability, penicillin affinity, and cell septation activity. In contrast to the serine beta-lactamases and low-molecular-mass PBPs which are autonomous folding entities, the S-259-to-V-577 penicillin-binding module of M-1-to-V-577 PBP3 lacks the amino acid sequence information for correct folding. The missing piece of information is provided by the associated G-57-to-E-258 non-penicillin-binding module which functions as a noncleaved, pseudointramolecular chaperone. Key elements of the folding information reside within the motif 1-containing R-60-to-W-110 polypeptide segment and within G-188-to-D-197 motif 3 of the n-PB module. The intermodule interaction is discussed in the light of the known three-dimensional structure (at 3.5-A [0.35-nm] resolution) of the analogous class B PBP2x of Streptococcus pneumoniae (S. Pares, N. Mouz, Y. Petillot, R. Hakenbeck, and O. Dideberg, Nature Struct. Biol. 3:284-289, 1996). Correct folding and adoption of a stable penicillin-binding conformation are necessary but not sufficient to confer cell septation activity to PBP3 in exponentially growing cells. The in vivo activity of PBP3 also depends on the M-1-to-E-56 amino-terminal module which encompasses the cytosol, the membrane, and the periplasm and which functions as a noncleaved pseudo-signal peptide.
Goffin, Colette ; Université de Liège - ULiège > Institut de Chimie > Centre d'ingénierie des protéines
Fraipont, Claudine ; Université de Liège - ULiège > Institut de Chimie > Centre d'ingénierie des protéines
Ayala, Juan; Universidad Autonoma (Madrid) > Consejo Superior de Investigaciones Cientificas > Centro de Biologia Molecular Severo Ochoa
Terrak, Mohammed ; Université de Liège - ULiège > Institut de Chimie > Centre d'ingénierie des protéines
Nguyen-Distèche, Martine ; Université de Liège - ULiège > Institut de Chimie > Centre d'ingénierie des protéines
Ghuysen, Jean-Marie ; Université de Liège - ULiège > Institut de Chimie > Centre d'ingénierie des protéines
Language :
English
Title :
The non-penicillin-binding module of the tripartite penicillin-binding protein 3 of Escherichia Coli is required for folding and/or stability of the penicillin-binding module and the membrane-anchoring module confers cell septation activity on the folded structure
Publication date :
September 1996
Journal title :
Journal of Bacteriology
ISSN :
0021-9193
eISSN :
1098-5530
Publisher :
American Society for Microbiology (ASM), Washington, United States - District of Columbia
Volume :
178
Issue :
18
Pages :
5402-5409
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRFC - Fonds de la Recherche Fondamentale Collective
Bartholomé-De Belder, J., M. Nguyen-Distèche, N. Houba-Hérin, J. M. Ghuysen, J. N. Maruyama, H. Hara, Y. Hirota, and M. Inouye. 1988. Over-expression, solubilization and refolding of a genetically-engineered derivative of the penicillin-binding protein 3 of E. coli K-12. Mol. Microbiol. 2:519-525.
Bramhill, D., M. El Sherbeini, B. Cunningham, D. Trusca, and D. L. Pompliano. 1995. Interaction of FtsZ with other cell division proteins, p. 25. In 42nd Workshop on Structure, Function and Controls in Microbial Division. Institute Juan March, Madrid.
Broome-Smith, J. K., P. J. Hedge, and B. G. Spratt. 1985. Production of thiol-penicillin-binding protein 3 of Escherichia coli using a two primer method of site-directed mutagenesis. EMBO J. 4:231-235.
Charlier, P., G. Buisson, O. Dideberg, J. Wierenga, W. Keck, G. Laible, and R. Hakenbeck. 1993. Crystallization of a genetically engineered water-soluble primary penicillin target enzyme. The high molecular mass PBP2x of Streptococcus pneumoniae. J. Mol. Biol. 232:1007-1009.
Dobson, C. M. 1995. Finding the right fold. Nature Struct. Biol. 2:513-518.
Eder, J., and A. R. Fersht. 1995. Micro review: pro-sequence-assisted protein folding. Mol. Microbiol. 16:609-615.
Englebert, S., A. El Kharroubi, G. Piras, B. Joris, J. Coyette, M. NguyenDistèche, and J. M. Ghuysen. 1993. Molecular design of the bi(multi?)functional penicillin-binding proteins, p. 319-333. In M. A. de Pedro, J. V. Höltje, and W. Löffelhardt (ed.), Bacterial growth and lysis: metabolism and structure of the bacterial sacculus. Plenum Publishing Co., New York.
Fraipont, C., M. Adam, M. Nguyen-Distèche, W. Keck, J. Van Beeumen, J. Ayala, B. Granier, H. Hara, and J. M. Ghuysen. 1994. Engineering and overexpression of periplasmic forms of the penicillin-binding protein 3 of E coli. Biochem. J. 298:189-195.
Frydman, J., E. Nimmesgern, K. Ohtsuka, and F. U. Hartl. 1994. Folding of nascent polypeptide chains in a high-molecular-mass assembly with molecular chaperones. Nature (London) 370:111-117.
Garcia del Portillo, F., M. A. de Pedro, and J. A. Ayala. 1991. Identification of a new mutation in E. coli that suppresses a pbpB(Ts) phenotype in the presence of PBP1b. FEMS Microbiol. Lett. 84:7-14.
Ghuysen, J. M. 1994. Molecular structures of penicillin-binding proteins and β-lactamases. Trends Microbiol. 2:372-380.
Ghuysen, J. M., J. M. Frère, M. Leyh-Bouille, M. Nguyen-Distèche, and J. Coyette. 1986. Active-site serine D-alanyl-D-alanine-cleaving peptidases-catalysed acyl transfer reactions. Procedures for studying the penicillin-binding proteins of bacterial plasma membranes. Biochem. J. 235:159-165.
Goloubinoff; P., A. R. Gatenby, and G. H. Lorimer. 1989. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature (London) 337:44-47.
Hedge, P. J., and B. G. Spratt. 1984. A gene fusion that localizes the penicillin-binding domain of penicillin-binding protein 3 of E. coli. FEBS Lett. 176:179-184.
Hlodan, R., P. Tempst. and F. U. Hartl. 1995. Binding of defined regions of a polypeptide to GroEL and its implication for chaperonin-medialed protein folding. Nature Struct. Biol. 2:587-595.
Höltje, J. V., T. Romeis, A. Ursinus, M. von Rechenberg, J. Lommatzsch, and K. Ehlert. 1995. Control of cell wall synthesis by means of multienzyme complexes, p. 23. In 42nd Workshop on Structure, Function and Controls in Microbial Division. Institute Juan March, Madrid.
Hunt, J. H., A. J. Weaver, S. L. Landry, L. Gierasch, and J. Deisenhofer. 1996. The crystal structure of the GroES co-chaperonin at 2.8 Å resolution. Nature (London) 379:37-45.
Matsuhashi, M. 1994. Utilization of lipid-linked precursors and the formation of peptidoglycan in the process of cell growth and division: membrane enzymes involved in the final steps of peptidoglycan synthesis and the mechanism of their regulation, p. 55-71. In J. M. Ghuysen and R. Hakenbeck (ed.), Bacterial cell wall. Elsevier Science Publishers, Amsterdam.
Mukherjee, A., and J. Lutkenhaus. 1994. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176:2754-2758.
Nagasawa, H., Y. Sakagami, A. Suzuki, H. Suzuki, H. Hara, and Y. Hirota. 1989. Determination of the cleavage site involved in C-terminal processing of penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 171:5890-5893.
Nakamura, M., I. N. Maruyama, M. Soma, J. Kato, H. Suzuki, and Y. Hirota. 1983. On the process of cell division in E. coli: nucleotide sequence of the gene for penicillin-binding protein 3. Mol. Gen. Genet. 191:1-9.
S. Pares, N. Mouz, Y. Pétillot, R. Hakenbeck, and O. Dideberg. 1996. X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme. Nature Struct. Biol. 3:284-289.
Romeis, T., and J. V. Höltje. 1994. Specific interaction of penicillin-binding protein 3 and 7/8 with the soluble lytic transglycosylase in E. coli. J. Biol. Chem. 269:21603-21607.
Sanchez, M., A. Valencia, M. J. Ferrandiz, C. Sander, and M. Vicente. 1994. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J. 13:4919-4925.
Shinde, U., and M. Inouye. 1993. Intramolecular chaperones and protein folding. Trends Biochem. Sci. 18:442-446.
Silen, J. L., C. N. McGrath, K. R. Smith, and D. A. Agard. 1988. Molecular analysis of the gene encoding α-lytic protease: evidence for a preprocnzyme. Gene 69:237-244.
Spratt, B. G., and K. D. Cromie. 1988. Penicillin-binding protein of gram-negative bacteria. Rev. Infect. Dis. 10:699-711.
Vanhove, M., X. Raquet, and J. M. Frère. 1995. Investigation of the folding pathway of the Teml β-lactamase. Proteins Struct. Fund. Genet. 22:110-118.