Hyperthermophilic DNA methyltransferase M.PabI from the archaeon Pyrococcus abyssi

Applied and Environmental Microbiology

Volumn 72, Issue 8, 2006, Pages 5367-5375

  Watanabe, Miki ^a   Yuzawa, Harumi ^a   Handa, Naofumi ^a   Kobayashi, Ichizo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONCENTRATION (PROCESS); ENZYME KINETICS; ESCHERICHIA COLI; GENETIC ENGINEERING; PH; SODIUM CHLORIDE;

DNA ENGINEERING; GENE COMPLEX; METHYLATION; MODIFICATION ENZYMES;

DNA SEQUENCES;

CALCIUM ION; DNA; DNA METHYLTRANSFERASE; MAGNESIUM ION; MANGANESE; SODIUM CHLORIDE; ZINC ION;

DNA FINGERPRINTING; ENZYME; GENOME; POLYMORPHISM; THERMOPHILIC BACTERIUM;

ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENOME; DNA METHYLATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBUNIT; ESCHERICHIA COLI; NONHUMAN; PYROCOCCUS ABYSSI; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMOPHILIC BACTERIUM; THERMOSTABILITY; THIN LAYER CHROMATOGRAPHY;

AMINO ACID SEQUENCE; DNA METHYLATION; DNA RESTRICTION ENZYMES; ESCHERICHIA COLI; HEAT; KINETICS; PYROCOCCUS ABYSSI; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC);

ARCHAEA; ESCHERICHIA COLI; PYROCOCCUS; PYROCOCCUS ABYSSI;

EID: 33747367212     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00433-06     Document Type: Article

References (64)

1. Alm, R. A., L. S. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
2. Bheemanaik, S., S. Chandrashekaran, V. Nagaraja, and D. N. Rao. 2003. Kinetic and catalytic properties of dimeric KpnI DNA methyltransferase. J. Biol. Chem. 278:7863-7874.
3. 2a. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
4. Breslauer, K. J., R. Frank, H. Blocker, and L. A. Marky. 1986. Predicting DNA duplex stability from the base sequence. Proc. Natl. Acad. Sci. USA 83:3746-3750.
5. Bujnicki, J. M. 2001. Understanding the evolution of restriction- modification systems: clues from sequence and structure comparisons. Acta Biochim. Pol. 48:935-967.
6. Calisto, B. M., O. Q. Pich, J. Pinol, I. Fita, E. Querol, and X. Carpena. 2005. Crystal structure of a putative type I restriction-modification S subunit from Mycoplasma genitalium. J. Mol. Biol. 351:749-762.
7. Casadaban, M. J., and S. N. Cohen. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138:179-207.
8. Cheng, X., and R. J. Roberts. 2001. AdoMet-dependent methylation, DNA methyltransferases and base flipping. Nucleic Acids Res. 29:3784-3795.
9. Chinen, A., I. Uchiyama, and I. Kobayashi. 2000. Comparison between Pyrococcus horikoshii and Pyrococcus abyssi genome sequences reveals linkage of restriction-modification genes with large genome polymorphisms. Gene 259:109-121.
10. Cohen, G. N., V. Barbe, D. Flament, M. Galperin, R. Heilig, O. Lecompte, O. Poch, D. Prieur, J. Querellou, R. Ripp, J. C. Thierry, J. Van der Oost, J. Weissenbach, Y. Zivanovic, and P. Forterre. 2003. An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol. Microbiol. 47:1495-1512.
11. Fabry, S., and R. Hensel. 1987. Purification and characterization of D-glyceraldehyde-3-phosphate dehydrogenase from the thermophilic archaebacterium Methanothermus fervidus. Eur. J. Biochem. 165:147-155.
12. BAD promoter. J. Bacteriol. 177:4121-4130.
13. Handa, N., A. Ichige, K. Kusano, and I. Kohayashi. 2000. Cellular responses to postsegregational killing by restriction-modification genes. J. Bacteriol. 182:2218-2229.
14. Handa, N., Y. Nakayama, M. Sadykov, and I. Kohayashi. 2001. Experimental genome evolution: large-scale genome rearrangements associated with resistance to replacement of a chromosomal restriction-modification gene complex. Mol. Microbiol. 40:932-940.
15. Ichige, A., and I. Kobayashi. 2005. Stability of EcoRI restriction-modification enzymes in vivo differentiates the EcoRI restriction-modification system from other postsegregational cell killing systems. J. Bacteriol. 187:6612-6621.
16. Ishikawa, K., M. Watanabe, T. Kuroita, I. Uchiyama, J. M. Bujnicki, B. Kawakami, M. Tanokura, and I. Kobayashi. 2005. Discovery of a novel restriction endonuclease by genome comparison and application of a wheat-germ-based cell-free translation assay: PabI (5′GTA/C) from the hyperthermophilic archaeon Pyrococcus abyssi. Nucleic Acids Res. 33:e112.
17. Jeltsch, A., and A. Pingoud. 1996. Horizontal gene transfer contributes to the wide distribution and evolution of type II restriction-modification systems. J. Mol. Evol. 42:91-96.
18. Kawarabayasi, Y., Y. Hino, H. Horikawa, S. Yamazaki, Y. Haikawa, K. Jin-no, M. Takahashi, M. Sekine, S. Baba, A. Ankai, H. Kosugi, A. Hosoyama, S. Fukui, Y. Nagai, K. Nishijima, H. Nakazawa, M. Takamiya, S. Masuda, T. Funahashi, T. Tanaka, Y. Kudoh, J. Yamazaki, N. Kushida, A. Oguchi, K. Aoki, K. Kubota, Y. Nakamura, N. Nomura, Y. Sako, and H. Kikuchi. 1999. Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 6:83-101, 145-152.
19. Kawarabayasi, Y., M. Sawada, H. Horikawa, Y. Haikawa, Y. Hino, S. Yamamoto, M. Sekine, S. Baba, H. Kosugi, A. Hosoyama, Y. Nagai, M. Sakai, K. Ogura, R. Otsuka, H. Nakazawa, M. Takamiya, Y. Ohfuku, T. Funahashi, T. Tanaka, Y. Kudoh, J. Yamazaki, N. Kushida, A. Oguchi, K. Aoki, and H. Kikuchi. 1998. Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res. 5:55-76.
20. Kim, J. S., A. DeGiovanni, J. Jancarik, P. D. Adams, H. Yokota, R. Kim, and S. H. Kim. 2005. Crystal structure of DNA sequence specificity subunit of a type I restriction-modification enzyme and its functional implications. Proc. Natl. Acad. Sci. USA 102:3248-3253.
21. Klimasauskas, S., S. Kumar, R. J. Roberts, and X. Cheng. 1994. HhaI methyltransferase flips its target base out of the DNA helix. Cell 76:357-369.
22. Kobayashi, I. 2001. Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 29:3742-3756.
23. Kobayashi, I. 2004. Genetic addiction: a principle of gene symbiosis in a genome, p. 105-144. In B. E. Funnell and G. J. Phillips (ed.), Plasmid biology. ASM Press, Washington, D.C.
24. Kobayashi, I. 2004. Restriction-modification systems as minimal forms of life, p. 19-62. In A. Pingoud (ed.), Restriction endonucleases. Springer-Verlag, Berlin, Germany.
25. Kobayashi, I., A. Nobusato, N. Kobayashi-Takahashi, and I. Uchiyama. 1999. Shaping the genome-restriction-modification systems as mobile genetic elements. Curr. Opin. Genet. Dev. 9:649-656.
26. Komori, K., N. Fujita, K. Ichiyanagi, H. Shinagawa, K. Morikawa, and Y. Ishino. 1999. P1-PfuI and P1-PfuI1, intein-coded homing endonucleases from Pyrococcus furiosus. I. Purification and identification of the homing-type endonuclease activities. Nucleic Acids Res. 27:4167-4174.
27. Labahn, J., J. Granzin, G. Schluckebier, D. P. Robinson, W. E. Jack, I. Schildkraut, and W. Saenger. 1994. Three-dimensional structure of the adenine-specific DNA methyltransferase M.TaqI in complex with the cofactor S-adenosylmethionine. Proc. Natl. Acad. Sci. USA 91:10957-10961.
28. Malone, T., R. M. Blumenthal, and X. Cheng. 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.
29. Malygin, E. G., V. V. Zinoviev, A. A. Evdokimov, W. M. Lindstrom, Jr., N. O. Reich, and S. Hattman. 2003. DNA (cytosine-N4-)- and -(adenine-N6-)- methyltransferases have different kinetic mechanisms but the same reaction route. A comparison of M.BamHI and T4 Dam. J. Biol. Chem. 278:15713-15719.
30. Marguet, E., and P. Forterre. 1998. Protection of DNA by salts against thermodegradation at temperatures typical for hyperthermophiles. Extremophiles 2:115-122.
31. Marks, P., J. McGeehan, G. Wilson, N. Errington, and G. Kneale. 2003. Purification and characterisation of a novel DNA methyltransferase, M.AhdI. Nucleic Acids Res. 31:2803-2810.
32. Marshak, A., and H. J. Vogel. 1951. Microdetermination of purines and pyrimidines in biological materials. J. Biol. Chem. 189:597-605.
33. McClelland, M. 1981. Purification and characterization of two new modification methylases: MClai from Caryophanon latum L and MTaqI from Thermus aquaticus YTI. Nucleic Acids Res. 9:6795-6804.
34. Mills, K. V., J. S. Manning, A. M. Garcia, and L. A. Wuerdeman. 2004. Protein splicing of a Pyrococcus abyssi intein with a C-terminal glutamine. J. Biol. Chem. 279:20685-20691.
35. Morgan, R., J.-P. Xiao, and S.-Y. Xu. 1998. Characterization of an extremely thermostable restriction enzyme, PspGI, from a Pyrococcus strain and cloning of the PspGI restriction-modification system in Escherichia coli. Appl. Environ. Microbiol. 64:3669-3673.
36. Mruk, I., M. Cichowicz, and T. Kaczorowski. 2003. Characterization of the LlaCI methyltransferase from Laclococcus lactis subsp. cremoris W15 provides new insights into the biology of type II restriction-modification systems. Microbiology 149:3331-3341.
37. Naito, T., K. Kusano, and I. Kobayashi. 1995. Selfish behavior of restriction-modification systems. Science 267:897-899.
38. Nobusato, A., I. Uchiyama, and I. Kobayashi. 2000. Diversity of restriction-modification gene homologues in Helicobacter pylori. Gene 259:89-98.
39. Nobusato, A., I. Uchiyama, S. Ohashi, and I. Kobayashi. 2000. Insertion with long target duplication: a mechanism for gene mobility suggested from comparison of two related bacterial genomes. Gene 259:99-108.
40. Parks, L. W., and F. Schlenk. 1958. The stability and hydrolysis of S-adeno-sylmethionine; isolation of S-ribosylmethionine. J. Biol. Chem. 230:295-305.
41. Pues, H., N. Bleimling, B. Holz, J. Wolcke, and E. Weinhold. 1999. Functional roles of the conserved aromatic amino acid residues at position 108 (motif IV) and position 196 (motif VIII) in base flipping and catalysis by the N6-adenine DNA methyltransferase from Thermus aquaticus. Biochemistry 38:1426-1434.
42. Purcarea, C., V. Simon, D. Prieur, and G. Herve. 1996. Purification and characterization of carbamoyl-phosphate synthetase from the deep-sea hyperthermophilic archaebacterium Pyrococcus abyssi. Eur. J. Biochem. 236: 189-199.
43. Record, M. T., Jr., T. M. Lohman, and P. de Haseth. 1976. Ion effects on ligand-nucleic acid interaction. J. Mol. Biol. 107:145-158.
44. Reich, N. O., and N. Mashhoon. 1991. Kinetic mechanism of the EcoR1 DNA methyltransferase. Biochemistry 30:2933-2939.
45. Roberts, R. J., M. Belfort, T. Bestor, A. S. Bhagwat, T. A. Bickle, J. Bitinaite, R. M. Blumenthal, S. Degtyarev, D. T. Dryden, K. Dybvig, K. Firman, E. S. Gromova, R. I. Gumport, S. E. Halford, S. Hattman, J. Heitman, D. P. Hornby, A. Janulaitis, A. Jeltsch, J. Josephsen, A. Kiss, T. R. Klaenhammer, I. Kobayashi, H. Kong, D. H. Kruger, S. Lacks, M. G. Marinus, M. Miyahara, R. D. Morgan, N. E. Murray, V. Nagaraja, A. Piekarowicz, A. Pingoud, E. Raleigh, D. N. Rao, N. Reich, V. E. Repin, E. U. Selker, P. C. Shaw, D. C. Stein, B. L. Stoddard, W. Szybalski, T. A. Trautner, J. L. Van Etten, J. M. Vitor, G. G. Wilson, and S. Y. Xu. 2003. A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res. 31:1805-1812.
46. Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis. 2005. REBASE-restriction enzymes and DNA methyltransferases. Nucleic Acids Res. 33: D230-D232.
47. Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis. 2003. REBASE: restriction enzymes and methyltransferases. Nucleic Acids Res. 31:418-420.
48. Rosenberg, A. H., B. N. Lade, D.-S. Chui, S.-W. Lin, J. J. Dunn, and F. W. Studier. 1987. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene 56:125-135.
49. Rubin, R. A., and P. Modrich. 1977. EcoRI methylase. Physical and catalytic properties of the homogeneous enzyme. J. Biol. Chem. 252:7265-7272.
50. Sadykov, M., Y. Asami H. Niki, N. Handa, M. Itaya, M. Tanokura, and I. Kobayashi. 2003. Multiplication of a restriction-modification gene complex. Mol. Microbiol. 48:417-427.
51. Sambrook, J., and D. W. Russell. 2001. Molecular cloning, a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. Sankpal, U. T., and D. N. Rao. 2002. Structure, function, and mechanism of HhaI DNA methyltransferases. Crit. Rev. Biochem. Mol. Biol. 37:167-197.
53. Schluckebier, G., M. Kozak, N. Bleimling, E. Weinhold, and W. Saenger. 1997. Differential binding of S-adenosylmethionine S-adenosylhomocysteine and sinefungin to the adenine-specific DNA methyltransferase M.TaqI. J. Mol. Biol. 265:56-67.
54. Schubert, H. L., J. D. Phillips, and C. P. Hill. 2003. Structures along the catalytic pathway of PrmC/HemK, an N5-glutamine AdoMet-dependent methyltransferase. Biochemistry 42:5592-5599.
55. Spies, M., Y. Kil, R. Masui, R. Kato, C. Kujo, T. Ohshima, S. Kuramitsu, and V. Lanzov. 2000. The RadA protein from a hyperthermophilic archaeon Pyrobaculum islandicum is a DNA-dependent ATPase that exhibits two disparate catalytic modes, with a transition temperature at 75 degrees C. Eur. J. Biochem. 267:1125-1137.
56. Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
57. Svadbina, I. V., N. V. Zelinskaya, N. P. Kovalevskaya, L. A. Zheleznaya, and N. I. Matvienko. 2004. Isolation and characterization of site-specific DNA-methyltransferases from Bacillus coagulans K. Biochemistry (Moscow) 69: 299-305.
58. Vieille, C., and G. J. Zeikus. 2001. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol. Mol. Biol. Rev. 65:1-43.
59. Vilkaitis, G., E. Merkiene, S. Serva, E. Weinhold, and S. Klimasauskas. 2001. The mechanism of DNA cytosine-5 methylation. Kinetic and mutational dissection of HhaI methyltransferase. J. Biol. Chem. 276:20924-20934.
60. Villa, A., L. Zecca, P. Fusi, S. Colombo, G. Tedeschi, and P. Tortora. 1993. Structural features responsible for kinetic thermal stability of a carboxypeptidase from the archaebacterium Sulfolobus solfataricus. Biochem. J. 295:827-831.
61. Wang, S., Y. Feng, Z. Zhang, B. Zheng, N. Li, S. Cao, I. Matsui, and Y. Kosugi. 2003. Heat effect on the structure and activity of the recombinant glutamate dehydrogenase from a hyperthermophilic archaeon Pyrococcus horikoshii. Arch. Biochem. Biophys. 411:56-62.
62. Xia, Y., K. E. Narva, and J. L. Van Etten. 1987. The cleavage site of the Rsa1 isoschizomer, CviII, is G ↓, TAC. Nucleic Acids Res. 15:10063.
63. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
64. Zinoviev, V. V., A. A. Evdokimov, Y. A. Gorhunov, E. G. Malygin, V. G. Kossykh, and S. Hattman. 1998. Phage T4 DNA [N6-adenine] methyltransferase: kinetic studies using oligonucleotides containing native or modified recognition sites. Biol. Chem. 379:481-488.