Functional analysis of mmel from methanol utilizer methylophilus methylotrophus, a subtype IIC restriction-modification enzyme related to type I enzymes

Applied and Environmental Microbiology

Volumn 75, Issue 1, 2009, Pages 212-223

  Nakonieczna, Joanna ^a   Kaczorowski, Tadeusz ^a,e   Obarska Kosinska, Agnieszka ^b,c   Bujnicki, Janusz M ^b,d  

^a UNIVERSITY OF GDA SK   (Poland)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^c INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^d ADAM MICKIEWICZ UNIVERSITY   (Poland)

^e MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; BINDING MOTIFS; BIOINFORMATIC TOOLS; COFACTOR; DO-MAINS; ENZYMATIC ACTIVITIES; FUNCTIONAL DOMAINS; METHANOL UTILIZERS; METHYL GROUP DONORS; METHYL TRANSFERASES; NUCLEOTIDE SEQUENCES; PARTICULAR FEATURES; RECOGNITION SITES; SEQUENCE MOTIFS; SERIAL ANALYSIS OF GENE EXPRESSIONS; SPECIFIC SITES; TARGET RECOGNITIONS; TERMINAL PORTIONS; TRANSCRIPT PROFILING;

AMINATION; AMINES; AMINO ACIDS; BINDING SITES; CATALYSTS; DNA; DNA SEQUENCES; ENZYME ACTIVITY; GENE EXPRESSION; GENES; HYDROCARBONS; METHANOL; NUCLEIC ACIDS; ORGANIC ACIDS; PORT TERMINALS; PROTEINS; SIGNAL INTERFERENCE;

ENZYMES;

AMINO ACID; BACTERIUM; CATALYSIS; ENZYME ACTIVITY; MUTATION;

DNA; ENDODEOXYRIBONUCLEASE MMEI; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; DNA METHYLATION; ENZYMOLOGY; GENETICS; METABOLISM; METHYLOPHILUS METHYLOTROPHUS; MISSENSE MUTATION; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA; DNA METHYLATION; METHYLOPHILUS METHYLOTROPHUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 58149347788     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01322-08     Document Type: Article

References (67)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Aravind, L., K. S. Makarova, and E. V. Koonin. 2000. Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res. 28:3417-3432.
3. Backman, K., M. Ptashne, and W. Gilbert. 1976. Construction of plasmids carrying the cI gene of bacteriophage lambda. Proc. Natl. Acad. Sci. USA 73:4174-4178.
4. Bourniquel, A. A., and T. A. Bickle. 2002. Complex restriction enzymes: NTP-driven molecular motors. Biochimie 84:1047-1059.
5. Boyd, A. C., I. G. Charles, J. W. Keyte, and W. J. Brammar. 1986. Isolation and computer-aided characterization of MmeI, a type II restriction endonuclease from Methylophilus methylotrophus. Nucleic Acids Res. 14:5255-5274.
6. Bujnicki, J. M. 1999. Comparison of protein structures reveals monophyletic origin of the Ado Met-dependent methyl transferase family and mechanistic convergence rather than recent differentiation of N4-cytosine and N6-adenine DNA methylation. In Silico Biol. 1:175-182.
7. Bujnicki, J. M. 2000. Phylogeny of the restriction endonuclease-like superfamily inferred from comparison of protein structures. J. Mol. Evol. 50:39-44.
8. Bujnicki, J. M. 2003. Crystallographic and bioinformatic studies on restriction endonucleases: inference of evolutionary relationships in the "midnight zone" of homology. Curr. Protein Pept. Sci. 4:327-337.
9. Bujnicki, J. M., and M. Radlinska. 1999. Molecular evolution of DNA-(cytosine-N4) methyl transferases: evidence for their polyphyletic origin. Nucleic Acids Res. 27:4501-4509.
10. Bujnicki, J. M., and L. Rychlewski. 2001. Grouping together highly diverged PD-(D/E)XK nucleases and identification of novel superfamily members using structure-guided alignment of sequence profiles. J. Mol. Microbiol. Biotechnol. 3:69-72.
11. Case, D. A., T. A. Darden, T. E. Cheatham III, C. L. Simmerling, J. Wang, R. E. Duke, R. Luo, K. M. Merz, B. Wang, D. A. Pearlman, M. Crowley, S. Brozell, V. Tsui, H. Gohlke, J. Mongan, V. Hornak, G. Cui, P. Beroza, C. Schafmeister, J. W. Caldwell, W. S. Ross, and P. A. Kollman. 2004. AMBER 8. University of California, San Francisco.
12. Chmiel, A. A., J. M. Bujnicki, and K. J. Skowronek. 2005. A homology model of restriction endonuclease Sfil in complex with DNA. BMC Struct. Biol. 5:2.
13. Daemen, F. J., and J. F. Riordan. 1974. Essential arginyl residues in Escherichia coli alkaline phosphatase. Biochemistry 13:2865-2871.
14. Davies, G. P., I. Martin, S. S, Sturrock, A. Cronshaw, N. E, Murray, and D. T. Dryden. 1999. On the structure and operation of type I DNA restriction enzymes. J. Mol. Biol. 290:565-579.
15. Dunn, J. J., S. R. MeCorkle, L. A. Praissman, G. Hind, D. Van Der Lelie, W. F. Bahou, D. V. Gnatenko, and M. K. Krause. 2002. Genomic signature tags (GSTs): a system for profiling genomic DNA. Genome Res. 12:1756-1765.
16. Edgar. R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
17. Emmersen, J., A. M. Heidenblut, A. L. Høgh, S. A. Hahn, K. G. Welinder, and K. L, Nielsen. 2007. Discarding duplicate ditags in long SAGE analysis may introduce significant error. BMC Bioinformatics 8:92.
18. Fomenkov, A., J. P. Xiao, D. Dila, E. Raleigh, and S. Y. Xu. 1994. The 'endo-blue method" for direct cloning of restriction endonuclease genes in E. coli. Nucleic Acids Res. 22:2399-2403.
19. Fritz, A., W. Kuster, and J. Alves. 1998. Asn141 is essential for DNA recognition by Eco RI restriction endonuclease. FEBS Lett. 438:66-70.
20. Grazulis, S., E. Manakova, M. Roessle, M. Bochtler, G. Tamulaitiene, R. Huber, and V. Siksnys. 2005. Structure of the metal-independent restriction enzyme Bfil reveals fusion of a specific DNA-binding domain with a nonspecific nuclease. Proc. Natl. Acad. Sci. USA 102:15797-15802.
21. Jaroszewski, L., L. Rychlewski, Z. Li, W. Li, and A. Godzik. 2005. FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33: W284-W288.
22. Kelleher, J. E., A. S. Daniel, and N. E. Murray. 1991. Mutations that confer de novo activity upon a maintenance methyltransferase. J. Mol. Biol. 221: 431-440.
23. Kim, Y. C., J. C. Grable, R. Love, P. J. Greene, and J. M. Rosenberg. 1990. Refinement of Eco RI endonuclease crystal structure: a revised protein chain tracing. Science 249:1307-1309.
24. Kneale, G. G. 1994. A symmetrical model for the domain structure of type I DNA methyl transferases. J. Mol. Biol. 243:1-5.
25. Kosinski, J., M. Feder, and J. M. Bujnicki. 2005. The PD-(D/E)XK super-family revisited: identification of new members among proteins involved in DNA metabolism and functional predictions for domains of (hitherto) unknown function. BMC Bioinformatics 6:172.
26. Kosinski, J., I. A. Cymerman, M. Feder, M. A. Kurowski, J. M. Sasin, and J. M. Bujnicki. 2003. A "FRankenstein's monster" approach to comparative modeling: merging the finest fragments of Fold-Recognition models and iterative model refinement aided by 3D structure evaluation. Proteins 53(Suppl. 6):369-379.
27. Kosinski, J., M. J. Gajda, I. A. Cymerman, M. A. Kurowski, M. Pawlowski, M. Boniecki, A. Obarska, G. Papaj, P. Sroczynska-Obuchowicz, K. L. Tkaczuk, P. Sniezynska, J. M. Sasin, A. Augustyn, J. M. Bujnicki, and M. Feder. 2005. FRankenstein becomes a cyborg: the automatic recombination and realignment of fold recognition models in CASP6. Proteins 61(Suppl. 7): 106-113.
28. Kosinski, J., E. Kubareva, and J. M. Bujnicki. 2007. A model of restriction endonuclease MvaI in complex with DNA: a template for interpretation of experimental data and a guide for specificity engineering. Proteins 68:324-336.
29. Kozbial, P. Z., and A. R. Mushegian. 2005. Natural history of S-adenosyl methionine-binding proteins. BMC Struct. Biol. 5:19.
30. Kurowski, M. A., and J. M. Bujnicki. 2003. Gene Silico protein structure prediction meta-server. Nucleic Acids Res. 31:3305-3307.
31. Kurpiewski, M. R., L. E. Engler, L. A. Wozniak, A. Kobylanska, M. Koziolkiewicz, W. J. Stec, and L. Jen-Jacobson. 2004. Mechanisms of coupling between DNA recognition specificity and catalysis in Eco RI endonuclease. Structure 12:1775-1788.
32. Lundstrom, J., L. Rychlewski, J. M. Bujnicki, and A. Elofsson. 2001. Peons: a neural-network-based consensus predictor that improves fold recognition. Protein Sci. 10:2354-2362.
33. Luscombe, N. M., R, A. Laskowski, and J. M. Thornton. 2001. Amino acid-base interactions: a three dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res. 29:2860-2874.
34. Malone, T., R. M. Blumenthal, and X. Cheng. 1995. Structure-guided analysis reveals nine sequence motif's conserved among DNA amino-methyl- transferases, and suggests a catalytic mechanism for these enzymes. J. Mol. Biol. 253:618-632.
35. Mantovani, J., N. Holic, K. Martinez, O. Danos, and J. Perea. 2006. A high throughput method for genome-wide analysis of retroviral integration. Nucleic Acids Res. 34:el34.
36. McGuffin, L. J., and D. T. Jones. 2003. Improvement of the Gen THREADER method for genomic fold recognition. Bioinformatics 19:874-881.
37. Meisel, A., T. A. Bickle, D. H. Kruger, and C. Schroeder. 1992. Type III restriction enzymes need two inversely oriented recognition sites for DNA cleavage. Nature 355:467-469.
38. Miyazono, K., M. Watanabe, J. Kosinski, K. Ishikawa, M. Kamo, T. Sawasaki, K. Nagata, J. M. Bujnicki, Y. Endo, M. Tanokura, and I. Kobayashi. 2007. Novel protein fold discovered in the PabI family of restriction enzymes. Nucleic Acids Res. 35:1908-1918.
39. Morgan, R. D., T. Bhatia, T. Davis, and L. Lovasco. 2004. Rccombinant type II restriction endonucleases, MmeI and related endonucleases and methods for producing the same. Patent WO 2004007670.
40. Nakonieczna, J., J. W. Zmijewski, B. Banecki, and A. J. Podhajska. 2007. Binding of MmeI restriction-modification enzyme to its specific recognition sequence is stimulated by S-adenosyl-L-methionine. Mol. Biotechnol. 37: 127-135.
41. Niv, M. Y., D. R. Ripoll, J. A. Vila, A. Liwo, E. S. Vanamee, A. K. Aggarwal, H. Weinstein, and H. A. Seheraga. 2007. Topology of type II REases revisited; structural classes and the common conserved core. Nucleic Acids Res. 35:2227-2237.
42. Obarska, A., A. Blundell, M. Feder, S. Vejsadova, E. Sisakova, M. Weiserova, J. M. Bujnicki, and K. Firman. 2006. Structural model for the multi-subunit type IC restriction-modification DNA methyltransferase M. EcoR124I in complex with DNA. Nucleic Acids Res. 34:1992-2005.
43. Orlowski, J., and J. M. Bujnicki. 2008. Structural and evolutionary classification of type II restriction enzymes based on theoretical and experimental analyses. Nucleic Acids Res. 36:3552-3569.
44. Pawlowski, M., M. J. Gajda, R. Matlak, and J. M. Bujnicki. 2008. Meta MQAP: a meta-server for the quality assessment of protein models BMC Bioinformatics 9:403.
45. Pingoud, A., M. Fuxreiter, V. Pingoud, and W. Wende. 2005. Type II restriction endonucleases: structure and mechanism. Cell. Mol. Life Sci. 62:685-707.
46. Pingoud, V., C. Conzelmann, S. Kinzebach, A. Sudina, V. Metelev, E. Kubareva, J. M. Bujnicki, R. Lurz, G. Luder, S. Y. Xu, and A. Pingoud. 2003. Psp GI, a type II restriction endonuclease from the extreme thermophile Pyrococcus sp.: structural and functional studies to investigate an evolutionary relationship with several mesophilic restriction enzymes. J. Mol. Biol. 329:913-929.
47. Pingoud, V., A. Sudina, H. Geyer, J. M. Bujnicki, R. Lurz, G. Luder, R. Morgan, E. Kubareva, and A. Pingoud. 2005. Specificity changes in the evolution of type II restriction endonucleases: a biochemical and bioinformatic analysis of restriction enzymes that recognize unrelated sequences. J. Biol. Chem. 280:4289-4298.
48. Pósfai, J., A. S. Bhagwat, and R. J. Roberts. 1988. Sequence motifs specific for cytosine methyl transferases. Gene 74:261-265.
49. 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 methyl transferases, homing endonucleases and their genes. Nucleic Acids Res. 31:1805-1812.
50. Roberts, R. J., T. Vincze, J. Posfai, and D. Macelis. 2007. REBASE- enzymes and genes for DNA restriction and modification. Nucleic Acids Res. 35:D269-D270.
51. Rosenberg, J. M. 1991. Structure and function of restriction endonucleases. Curr. Opin. Struct. Biol. 1:104-113.
52. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
53. Sasin, J. M., and J. M. Bujnicki. 2004. COLORADO3D, a web server for the visual analysis of protein structures. Nucleic Acids Res. 32:W586-W589.
54. Seeman, N. C., J. M. Rosenberg, and A. Rich. 1976. Sequence-specific recognition of double helical nucleic acids by proteins. Proc. Natl. Acad. Sci. USA 73:804-808.
55. Shiraki, T., S. Kondo, S. Katayama, K. Waki, T. Kasukawa, H. Kawaji, R. Kodzius, A. Watahiki, M. Nakamura, T. Arakawa, S. Fukuda, D. Sasaki, A. J. Podhajska, M. Harbers, J. Kawai, P. Carninci, and Y. Hayashizaki. 2003. Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc. Natl. Acad. Sci. USA 100:15776-15781.
56. Simons, K. T., C. Kooperberg, E. Huang, and D. Baker. 1997. Assembly of protein tertiary structures from fragments with similar local sequences using simulated annealing and Bayesian scoring functions. J. Mol. Biol. 268:209-225.
57. Soding, J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960.
58. Stahl, F., W. Wende, A. Jeltsch, and A. Pingoud. 1996. Introduction of asymmetry in the naturally symetric restriction endonuclease Eco RV to investigate inter subunit communication in the homodimeric protein. Proc. Natl. Acad. Sci. USA 93:6175-6180.
59. Tamulaitiene, G., S. Grazulis, A. Janulaitis, R. Janowski, G. Bujacz, and M. Jaskolski. 2004. Crystallization and preliminary crystallographic studies of a bifunctional restriction endonuclease Eco57I. Biochim. Biophys. Acta 1698: 251-254.
60. Tucholski, J., P. M. Skowron, and A. J. Podhajska. 1995. MmeI. a class-US restriction endonuclease: purification and characterization. Gene 157:87-92.
61. Tucholski, J., J. W. Zmijewski, and A. J. Podhajska. 1998. Two intertwined methylation activities of the MmeI restriction-modification class-US system from Methylophilus methylotrophus. Gene 223:293-302.
62. Vekulescu, V. E., L. Zhang, B. Vogelstein, and K. W. Kinzler. 1995. Serial analysis of gene expression. Science 270:484-487.
63. Venclovas. C., A. Timinskas, and V. Siksnys. 1994. Five-stranded beta-sheet sandwiched with two alpha-helices: a structural link between restriction endonucleases EcoRI and EcoRV. Proteins 20:279-282.
64. Wah, D. A., J. Bitinaite, I. Schildkraut, and A. K. Aggarwal. 1998. Structure of FokI has implications for DNA cleavage. Proc. Natl. Acad. Sci. USA 95:10564-10569.
65. Wallner, B., and A. Elofsson. 2003. Can correct protein models be identified? Protein Sci. 12:1073-1086.
66. Wallner, B., and A. Elofsson. 2006. Identification of correct regions in protein models using structural, alignment, and consensus information. Protein Sci. 15:900-913.
67. Winkler, F. K., D, W. Banner, C. Oefner, D. Tsernoglou, R. S. Brown, S. P. Heathman, R. K. Bryan, P. D. Martin, K. Petratos, and K. S. Wilson. 1993. The crystal structure of Eco RV endonuclease and of its complexes with cognate and non cognate DNA fragments. EMBO J. 12:1781-1795.