Cloning of the Haemophilus influenzae Dam methyltransferase and analysis of its relationship to the Dam methyltransferase encoded by the HP1 phage

• Autorzy: Bujnicki J. M. , Radlinska M. , Zaleski P. , Piekarowicz A.
• Języki publikacji: EN

Abstrakty

EN

In this paper we report cloning and experimental characterization of the DNA ade­nine methyltransferase (dam) gene from Haemophilus influenzae and comparison of its product with the Dam protein from the lysogenic phage of H. influenzae, HP1. Mo­lecular modeling of M.HinDam and M.HP1Dam was carried out, providing a frame­work for a comparative analysis of these enzymes and their close homologs in the structural context. Both proteins share the common fold and essential cofactor-bind- ing and catalytic residues despite overall divergence. However, subtle but significant differences in the cofactor-binding pocket have been identified. Moreover, while M.HinDam seems to contact its target DNA sequence using a number of loops, most of them are missing from M.HP1Dam. Analysis of both MTases suggests that their cata­lytic activity was derived from a common ancestor, but similar sequence specificities arose by convergence.

Słowa kluczowe

EN

molecular evolution; DNA adenine methyltransferase; cloning; sequence specificity; protein structure; Haemophilus influenzae

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2001
• Tom: 48
• Numer: 4
• Opis fizyczny: p.969-983,fig.

Twórcy

autor

Bujnicki J. M.

• International Institute of Molecular and Cell Biology, ks.Trojdena 4, 02-109 Warsaw, Poland

autor

Radlinska M.

autor

Zaleski P.

autor

Piekarowicz A.

Bibliografia

• 1.Malone,T., Blumenthal, R.M. & Cheng, X. (1995) Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J. Mol. Biol. 253, 618-632.
• 2.Fauman,E.B., Blumenthal, R.M. & Cheng, X. (1999) Structure and evolution of AdoMet-dependent Mtases; in: S-Adenosylmethionine-dependent Methyltransferases: Structures and Functions (Cheng, X., etal, eds.) pp. 1-38, World Scientific Inc., Singapore.
• 3.Labahn,J., Granzin, J., Schluckebier, G., Robinson, D.P., Jack, W.E., Schildkraut, I. & Saenger, W. (1994) Three-dimensional structure of the adenine-specific DNA methyltransferase M. TaqI in complex with the cofactor S-adenosylmethionine. Proc. Natl. Acad. Sci. U.S.A. 91, 10957-10961.
• 4.Bujnicki,J.M. (2001) Understanding the evolution of restriction-modification systems: clues from sequence and structure comparisons. Acta Biochim. Polon. 48, 935-967.
• 5.Tran,P.H., Korszun, Z.R., Cerritelli, S., Springhorn, S.S. & Lacks, S.A. (1998) Crystal structure of the DpnM DNA adenine methyltransferase from the DpnII restriction system of Streptococcus pneumoniae bound to S-adenosylmethionine. Structure 6, 1563-1575.
• 6.Modrich,P. (1991) Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25, 229-253.
• 7.Modrich,P. (1989) Methyl-directed DNA mismatch correction. J. Biol. Chem. 264, 6597-6600.
• 8.Oka, A., Sugimoto, K., Takanami, M. & Hirota, Y. (1980) Replication origin of the Escherichia coli K-12 chromosome: The size and structure of the minimum DNA segment carrying the information for autonomous replication. Mol. Gen. Genet. 178, 9-20.
• 9.Crooke,E. (1995) DNA synthesis initiated at oriC: In vitro replication reactions. Methods Enzymol. 262, 500-506.
• 10.Bogan,J.A. & Helmstetter, C.E. (1997) DNA sequestration and transcription in the oriC region of Escherichia coli. Mol. Microbiol. 26, 889-896.
• 11.Palmer,B.R. & Marinus, M.G. (1994) The dam and dcm strains of Escherichia coli — a review. Gene 143, 1-12.
• 12.Scherzer, E., Auer, B. & Schweiger, M. (1987) Identification, purification, and characterization of Escherichia coli virus T1 DNA methyltransferase. J. Biol. Chem. 262, 15225- 15231.
• 13.Heithoff,D.M., Sinsheimer, R.L., Low, D.A. & Mahan, M.J. (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284, 967-970.
• 14.Fleischmann,R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., Bult, C.J., Tomb, J.F., Dougherty, B.A., Merrick, J.M., McKenney, K., Sutton, G., FitzHugh, W., Fields, C., Gocayne, J.D., Scott, J., Shirley, R., Liu, L.I., Glodek, A., Kelley, J.M., Weidman, J.F., Phillips, C.A., Spriggs, T., Hedblom, E., Cotton, M.D., Utterback, T., Hanna, M.C., Nguyen, D.T., Saudek, D.M., Brandon, R.C., Fine, L.D., Fritchman, J.L., Fuhrmann, J.L., Geoghagen, N.S., Gnehm, C.L., McDonald, L.A., Small, K.V., Fraser, C.M., Smith, H.O. & Venter, J.C. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496-512.
• 15.Stuy, J.H. (1974) Origin and direction of Haemophilus bacteriophage HP1 DNA replication. J. Virol. 13, 757-759.
• 16.Piekarowicz, A. & Bujnicki, J.M. (1999) Cloning of the Dam methyltransferase gene from Haemophilus influenzae bacteriophage HP1. Acta Microbiol. Pol. 48, 123-129.
• 17.Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual; 2nd edn., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
• 18.Barcak,G.J., Chandler, M.S., Redfield, R.J. & Tomb, J.F. (1991) Genetic systems in Haemophilus influenzae. Methods Enzymol. 204, 321-342.
• 19.Mayer,M.P. (1995) A new set of useful cloning and expression vectors derived from pBlueScript. Gene 163, 41-46.
• 20.Renbaum,P. & Razin, A. (1995) Interaction of M. SssI and M. HhaI with single-base mismatched oligodeoxynucleotide duplexes. Gene 157, 177-179.
• 21.Altschul,S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
• 22.Bujnicki,J.M., Elofsson, A., Fischer, D. & Rychlewski, L. (2001) Structure prediction Meta Server. Bioinformatics 17, 750-751.
• 23.Sali, A. & Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815.
• 24.Hooft,R.W., Vriend, G., Sander, C. & Abola, E.E. (1996) Errors in protein structures. Nature 381, 272.
• 25.Eisenberg,D., Luthy, R. & Bowie, J.U. (1997) VERIFY3D: Assessment of protein models with three-dimensional profiles. Methods Enzymol. 277, 396-404.
• 26.McClelland,M., Nelson, M. & Raschke, E. (1994) Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Res. 22, 3640-3659.
• 27.Radlinska,M. & Bujnicki, J.M. (2001) Cloning of enterohemorrhagic Escherichia coli phage VT-2 Dam methyltransferase. Acta Microbiol. Pol. 50, 161-167.
• 28.Fischer,D. & Eisenberg, D. (1996) Protein fold recognition using sequence-derived predictions. Protein Sei. 5, 947-955.
• 29.Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
• 30.Bugl,H., Fauman, E.B., Staker, B.L., Zheng, F., Kushner, S.R., Saper, M.A., Bardwell, J.C. & Jakob, U. (2000) RNA methylation under heat shock control. Mol. Cell6, 349-360.
• 31.Goedecke,K., Pignot, M., Goody, R.S., Scheidig, A.J. & Weinhold, E. (2001) Structure of the N6-adenine DNA methyltransferase M. TaqI in complex with DNA and a cofactor analog. Nat. Struct. Biol. 8, 121-125.
• 32.Karplus,P.A. & Schulz, G.E. (1985) Prediction of chain flexibility in proteins. Naturwissenschaften 72, 212-213.
• 33.Lustig,B. & Jernigan, R.L. (1995) Consistencies of individual DNA base-amino acid interactions in structures and sequences. Nucleic Acids Res. 23, 4707-4711.
• 34.Chothia,C. & Lesk, A.M. (1986) The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823-826.
• 35.Bujnicki,J.M. (1999) Comparison of protein structures reveals monophyletic origin of the AdoMet-dependent methyltransferase family and mechanistic convergence rather than recent differentiation of N4-cytosine and N6-adenine DNA methylation. In Silico Biol. 1, 175-182. http://www.bioinfo.de/isb/1999/01/0016/
• 36.Plunkett,G., Rose, D.J., Durfee, T.J. & Blattner, F.R. (1999) Sequence of Shiga toxin 2 phage 933W from Escherichia coliO157:H7: Shiga toxin as a phage late-gene product. J. Bacteriol. 181, 1767-1778.
• 37.Pontarollo,R.A., Rioux, C.R. & Potter, A.A. (1997) Cloning and characterization of bacteriophage-like DNA from Haemophilus somnus homologous to phages P2 and HP1. J. Bacteriol. 179, 1872-1879.
• 38.Campbell,A. (1994) Comparative molecular biology of lambdoid phages. Annu. Rev. Microbiol. 48, 193-222.
• 39.Holland,J. & Domingo, E. (1998) Origin and evolution of viruses. Virus Genes 16, 13-21.
• 40.Piekarowicz,A., Brzezinski, R., Smorawinska, M., Kauc, L., Skowronek, K., Lenarczyk, M., Golembiewska, M. & Siwinska, M. (1986) Major spontaneous genomic rearrengements in Haemophilus influenzae S2 and HP1c1 bacteriophages. Gene 49, 111-118.
• 41.Hendrix,R.W., Smith, M.C., Burns, R.N., Ford, M.E. & Hatfull, G.F. (1999) Evolutionary relationships among diverse bacteriophages and prophages: All the world 's a phage. Proc. Natl. Acad. Sci. U.S.A. 96, 2192-2197.
• 42.Fujioka,M. (1992) Mammalian small molecule methyltransferases: Their structural and functional features. Int. J. Biochem. 24, 1917- 1924.
• 43.Jeltsch, A., Christ, F., Fatemi, M. & Roth, M. (1999) On the substrate specificity of DNA methyltransferases. Adenine-N6 DNA methyltransferases also modify cytosine residues at position N4. J. Biol. Chem. 274, 19538- 19544.
• 44.Sheikhnejad, G., Brank, A., Christman, J.K., Goddard, A., Alvarez, E., Ford, H.J., Marquez, V.E., Marasco, C.J., Sufrin, J.R., O'Gara, M. & Cheng, X. (1999) Mechanism of inhibition of DNA (cytosine C5)-methyltransferases by oligodeoxyribonucleotides containing 5,6-dihydro-5-azacytosine. J. Mol. Biol. 285, 2021-2034.
• 45.Ho,D.K., Wu, J.C., Santi, D.V. & Floss, H.G. (1991) Stereochemical studies of the C-methylation of deoxycytidine catalyzed by HhaI methylase and the N-methylation of deoxyadenosine catalyzed by EcoRI methylase. Arch. Biochem. Biophys. 284, 264-269.
• 46.Yang,A.S., Shen, J.C., Zingg, J.M., Mi, S. & Jones, P.A. (1995) HhaI and HpaII DNA methyltransferases bind DNA mismatches, methylate uracil and block DNA repair. Nucleic Acids Res. 23, 1380-1387.
• 47.Richardson, A.R. & Stojiljkovic, I. (2001) Mismatch repair and the regulation of phase variation in Neisseria meningitidis. Mol. Microbiol. 40, 645-655.