[en] Like other lysozymes, the bacteriophage lambda lysozyme is involved in the digestion of bacterial walls. This enzyme is remarkable in that its mechanism of action is different from the classical lysozyme's mechanism. From the point of view of protein evolution, it shows features of lysozymes from different classes. The crystal structure of the enzyme in which all tryptophan residues have been replaced by aza-tryptophan has been solved by X-ray crystallography at 2.3 Å using a combination of multiple isomorphous replacement, non-crystallographic symmetry averaging and density modification techniques. There are three molecules in the asymmetric unit. The characteristic structural elements of lysozymes are conserved: each molecule is organized in two domains connected by a helix and the essential catalytic residue (Glu19) is located in the depth of a cleft between the two domains. This cleft shows an open conformation in two of the independent molecules, while access to the cavity is much more restricted in the last one. A structural alignment with T4 lysozyme and hen egg white lysozyme allows us to superpose about 60 Cα atoms with a rms distance close to 2 Å. The best alignments concern the helix preceding the catalytic residue, some parts of the beta sheets and the helix joining the two domains. The results of sequence alignments with the V and C lysozymes, in which weak local similarities had been detected, are compared with the structural results.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Evrard, Christine ; Université Catholique de Louvain - UCL > Département de Chimie > CPMC - BIOP
Fastrez, Jacques; Université Catholique de Louvain - UCL > Département de Chimie > Laboratoire de Biochimie Physique et des Biopolymères - BIOP
Declercq, Jean-Paul; Université Catholique de Louvain - UCL > Département de Chimie > Laboratoire de Chimie Physique et de Cristallographie - CPMC
Language :
English
Title :
Crystal Structure of the Lysozyme from Bacteriophage Lambda and its Relationship with V and C-type Lysozymes
Argos P. A sensitive procedure to compare amino acid sequences. J. Mol. Biol. 193:1987;385-396
Bernstein 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. The Protein Data Bank a computer based archival file for macromolecular structures. J. Mol. Biol. 112:1977;535-542
Bienkowska-Szewczyk K., Lipinska B., Taylor A. The R gene product of bacteriophage λ is a murein transglycosylase. Mol. Gen. Genet. 184:1981;111-114
Blake C.C.F., Johnson L.N., Mair G.A., North A.C.T., Phillips D.C., Sarma V.R. Crystallographic studies of the activity of hen egg-white lysozyme. Proc. Roy. Soc. ser. B. 167:1967;378-388
Blake C.C.F., Cassels R., Dobson C.M., Poulsen F.M., Williams R.J.P., Wilson K.S. Structure and binding properties of hen lysozyme modified at tryptophan 62. J. Mol. Biol. 147:1981;73-95
Bowie J.U., Lüthy R., Eisenberg D. A method to identify protein sequences that fold into a known three-dimensional structure. Science. 253:1991;164-170
Brünger A.T. X-PLOR Version 3. 1, A System for X-ray Crystallography and NMR. 1992;Yale University Press, New Haven, CT
Brünger A.T. Free R value a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-475
The CCP4 Suite programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763
Cowtan K. DM, an automated procedure for phase improvement by density modification. Joint CCP4 ESF-EACBM Newsletter Protein Crystallog. 31:1994;24-28
Dayhoff M.O., Barker W.C., Hunt L.T. Established homologies in protein sequences. Methods Enzymol. 91:1983;524-545
Diamond R., Phillips D.C., Blake C.C.F., North A.C.T. Real-space refinement of the structure of hen egg white lysozyme. J. Mol. Biol. 82:1974;371-391
Engh R., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400
Evrard C., Declercq J.-P., Fastrez J. Crystallization and preliminary X-ray analysis of bacteriophage lambda lysozyme in which all tryptophans have been replaced by aza-tryptophans. Acta Crystallog. sect. D. 53:1997;217-219
Fastrez J. Phage lysozymes. Jollès P. Lysozymes: Model Enzymes in Biochemistry and Biology. 1996;35-64 Birkhaüuser Verlag, Basel
Garvey K.J., Saedi M.S., Ito J. Nucleotide sequence of Bacillus phage φ29 genes 14 and 15 homology of gene 15 with other phage lysozymes. Nucl. Acids Res. 14:1986;10001-10008
Hardy L.W., Poteete A.R. Reexamination of the role of Asp20 in catalysis by bacteriophage T4 lysozyme. Biochemistry. 30:1991;9457-9463
Imada M., Tsugita A. Amino-acid sequence of λ phage endolysin. Nature New Biol. 233:1971;230-231
Jespers L., Sonveaux E., Fastrez J. Is the bacteriophage lambda lysozyme an evolutionary link or a hybrid between the C and V-type lysozymes? Homology analysis and detection of the catalytic amino acid residues. J. Mol. Biol. 228:1992;529-538
Jollès P. Lysozymes: Model Enzymes in Biochemistry and Biology. 1996;Birkhäuser Verlag, Basel
Jones T.A., Zou J.-Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119
Kleywegt G.J., Jones T.A. Halloween. . . masks and bones. Bailey S., Hubbard R., Waller D. From First Map to Final Model. 1994;59-66 SERC Daresbury Laboratory, UK
Kleywegt G.J., Jones T.A. Efficient rebuilding of protein structures. Acta Crystallog. sect. D. 52:1995;829-832
Kleywegt G.J., Jones T.A. Detecting folding motifs and similarities in protein structures. Methods Enzymol. 277:1997;525-545
Lüthy R., Bowie J.U., Eisenberg D. Assessment of protein models with three-dimensional profiles. Nature. 356:1992;83-85
Luzzati P.V. Traitement statistique des erreurs dans la détermination des structures cristallines. Acta Crystallog. 5:1952;802-810
Matthews B.W. Solvent content in protein crystals. J. Mol. Biol. 33:1968;491-497
Matthews B.W., Remington S.J., Grütter M.G., Anderson W.F. Relation between hen egg white lysozyme and bacteriophage T4 lysozyme evolutionary implications. J. Mol. Biol. 147:1981;545-558
Monzingo A.F., Marcotte E.M., Hart P.J., Robertus J.D. Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nature Struct. Biol. 3:1996;133-140
Mushegian A.R., Fullner K.J., Koonin E.V., Nester E.W. A family of lysozyme-like virulence factors in bacterial pathogens of plants and animals. Proc. Natl Acad. Sci. USA. 93:1996;7321-7326
Navaza J. On the fast rotation function. Acta Crystallog. sect. A. 43:1987;645-653
Nicholls A., Bharadway R., Honig B. GRASP graphical representation and analysis of surface properties. Biophys. J. 64:1993;166-170
Nitta K., Sugai S. The evolution of lysozyme and α-lactalbumin. Eur. J. Biochem. 182:1989;111-118
Otwinowski Z. Maximum likelihood refinement of heavy atom parameters. Wolf W., Evans P.R., Leslie A.G.W. Isomorphous Replacement and Anomalous Scattering. 1991;80-86 SERC Daresbury Laboratory, UK
Otwinowski Z. Oscillation data reduction programs. Sawyer L., Isaacs N., Bailey S.W. Data Collection and Processing. 1993;56-62 SERC Daresbury Laboratory, UK
Perry L.J., Wetzel R. Disulfide bond engineered into T4 lysozyme stabilization of the protein toward thermal inactivation. Science. 226:1984;555-557
Read R.J. Improved Fourier coefficients for maps using phases from partial structures with error. Acta Crystallog. sect. A. 42:1986;140-149
Remington S.J., Matthews B.W. A general method to assess similarity of protein structures, applications to T4 bacteriophage lysozyme. Proc. Natl Acad. Sci. USA. 75:1978;2180-2184
Rossmann M.G., Argos P. Exploring structural homology of proteins. J. Mol. Biol. 105:1976;75-95
Sanger F., Coulson A.R., Hong G.F., Hill D.F., Petersen G.B. Nucleotide sequence of bacteriophage λ DNA. J. Mol. Biol. 162:1982;729-773
Sheldrick G.M. SHELXS86. Program for the Solution of Crystal Structures. 1985;University of Göttingen, Germany
Soumillion P., Fastrez J. A large decrease in the heat-shock-induced proteolysis after tryptophan starvation leads to an increased expression of the phage lambda lysozyme in E. coli. Biochem. J. 286:1992;187-191
Soumillion P., Jespers L., Vervoort J., Fastrez J. Biosynthetic incorporation of 7-azatryptophan into the phage lambda lysozyme estimation of tryptophan accessibility, effect on enzymatic activity and protein stability. Protein Eng. 5:1995;451-456
Susskind M.M., Botstein D. Molecular genetics of bacteriophage P22. Microbiol. Rev. 42:1978;385-413
Taylor A., Das B.C., Van Heijenoort J. Bacterial-cell-wall peptidoglycan fragments produced by phage λ or Vi II endolysin and containing 1,6-anhydro-N-acetylmuramic acid. Eur. J. Biochem. 53:1975;47-54
Taylor W.R., Orengo C.A. Protein structure alignment. J. Mol. Biol. 208:1989;1-22
Thunnissen A.-M.W.H., Dijkstra A.J., Kalk K.H., Rozeboom H.J., Engel H., Keck W., Dijkstra B.W. Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography. Nature. 367:1994;750-753
Tickle I. Refinement of SIR heavy atoms parameters in Patterson versus reciprocal space. Wolf W., Evans P.R., Leslie A.G.W. Isomorphous Replacement and Anomalous Scattering. 1991;87-95 SERC Daresbury Laboratory, UK
Weaver L.H., Matthews B.W. Structure of bacteriophage T4 lysozyme refined at 1.7 Ångstroms resolution. J. Mol. Biol. 193:1987;189-199
Weaver L.H., Grütter M.G., Remington S.J., Gray T.M., Isaacs N.W., Matthews B.W. Comparison of goose-type, chicken-type and phage-type lysozymes illustrates the changes that occur in both amino acid sequence and three-dimensional structure during evolution. J. Mol. Evol. 21:1985;97-111
Weaver L.H., Rennell D., Poteete A.R., Matthews B.W. Structure of phage P22 gene 19 lysozyme inferred from its homology with phage T4 lysozyme. Implication for lysozyme evolution. J. Mol. Biol. 184:1985;739-741
Weaver L.H., Grütter M.G., Matthews B.W. The refined structures of goose lysozyme and its complex with a bound trisaccharide show that the goose-type lysozymes lack a catalytic aspartate residue. J. Mol. Biol. 245:1995;54-68
Wiggins B.A., Hilliker S. Genetic and DNA mapping of the late regulation and lysis genes of Salmonella bacteriophage P22 and coliphage λ J. Virol. 56:1985;1030-1033