PspGI, 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

Journal of Molecular Biology

Volumn 329, Issue 5, 2003, Pages 913-929

  Pingoud, Vera ^a   Conzelmann, Charlotte ^a   Kinzebach, Steffen ^a   Sudina, Anna ^b   Metelev, Valeri ^b   Kubareva, Elena ^b   Bujnicki, Janusz M ^c   Lurz, Rudi ^d   Lüder, Gerhild ^d   Xu, Shuang Yong ^e   Pingoud, Alfred ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

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

^d MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^e NEW ENGLAND BIOLABS   (United States)

Author keywords

Cross linking; DNA binding; DNA cleavage; Electron microscopy; Restriction modification systems

Indexed keywords

RESTRICTION ENDONUCLEASE; TYPE II SITE SPECIFIC DEOXYRIBONUCLEASE;

ARTICLE; CONTROLLED STUDY; CROSS LINKING; DNA CLEAVAGE; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME DENATURATION; ENZYME STABILITY; ENZYME STRUCTURE; EVOLUTION; GEL FILTRATION; MUTATION; NONHUMAN; PH; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PYROCOCCUS; TRANSMISSION ELECTRON MICROSCOPY;

ARCHAEA; PYROCOCCUS SP.;

EID: 0037531222     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00523-0     Document Type: Article

References (68)

1. Bickle T.A., Kruger D.H. Biology of DNA restriction. Microbiol. Rev. 57:1993;434-450.
2. Heitman J. On the origins, structures and functions of restriction-modification enzymes. Genet. Eng. 15:1993;57-108.
3. Roberts R.J., Halford S.E. Type II restriction enzymes. Linn S.M., Lloyd R.S., Roberts R.J. Nucleases. 1993;35-88 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Roberts R.J., Macelis D. REBASE - restriction enzymes and methylases. Nucl. Acids Res. 29:2001;268-269.
5. Vitkute J., Maneliene Z., Janulaitis A. Two new thermostable type II restriction endonucleases from Thermus aquaticus: TatI and TauI, which recognize the novel nucleotide sequences 5′-W/GTACW-3′ and 5′-GCSG/C-3′ respectively. FEMS Microbiol. Letters. 204:2001;253-257.
6. Morgan R., Xiao J., Xu S. 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. 64:1998;3669-3673.
7. Kruger D.H., Kupper D., Meisel A., Tierlich M., Reuter M., Schroeder C. Restriction endonucleases functionally interacting with two DNA sites. Gene. 157:1995;165.
8. Kruger D.H., Barcak G.J., Reuter M., Smith H.O. EcoRII can be activated to cleave refractory DNA recognition sites. Nucl. Acids Res. 16:1988;3997-4008.
9. Kosykh V.G., Repik A.V., Kaliman A.V., Bur'ianov Ia I., Baev A.A. Primary structure of the gene of restriction endonuclease EcoRII. Dokl. Akad. Nauk. SSSR. 308:1989;1497-1499.
10. Karyagina A.S., Lunin V.G., Degtyarenko K.N., Uvarov V.Y., Nikolskaya I.I. Analysis of the nucleotide and derived amino acid sequences of the SsoII restriction endonuclease and methyltransferase. Gene. 124:1993;13-19.
11. Miyahara M., Ishiwata N., Yoshida Y. StyD4I restriction-modification system of Salmonella typhi D4: cloning and sequence analysis. Biol. Pharm. Bull. 20:1997;201-203.
12. Ibanez M., Alvarez I., Rodriguez-Pena J.M., Rotger R. A ColE1-type plasmid from Salmonella enteritidis encodes a DNA cytosine methyltransferase. Gene. 196:1997;145-158.
13. Den'mukhametov M.M., Zakharova M.V., Kravets A.N., Pertsev A.V., Sineva E.V., Repik A.V., et al. Characteristics of a plasmid bearing a gene of a restriction modification type II system - the SsoII isoschizomer. Mol. Biol. (Mosk). 31:1997;831-838.
14. Pingoud A., Jeltsch A. Structure and function of type II restriction endonucleases. Nucl. Acids Res. 29:2001;3705-3727.
15. Pingoud V., Kubareva E., Stengel G., Friedhoff P., Bujnicki J.M., Urbanke C., et al. Evolutionary relationship between different subgroups of restriction endonucleases. J. Biol. Chem. 277:2002;14306-14314.
16. Stein D.C., Chien R., Seifert H.S. Construction of a Neisseria gonorrhoeae MS11 derivative deficient in NgoMI restriction and modification. J. Bacteriol. 174:1992;4899-4906.
17. Janulaitis A., Stakenas P., Berlin Yu A. A new site-specific endodeoxyribonuclease from Citrobacter freundii. FEBS Letters. 161:1983;210-212.
18. Halford S.E., Bilcock D.T., Stanford N.P., Williams S.A., Milsom S.E., Gormley N.A., et al. Restriction endonuclease reactions requiring two recognition sites. Biochem. Soc. Trans. 27:1999;696-699.
19. Siksnys V., Skirgaila R., Sasnauskas G., Urbanke C., Cherny D., Grazulis S., Huber R. The Cfr10I restriction enzyme is functional as a tetramer. J. Mol. Biol. 291:1999;1105-1118.
20. Deibert M., Grazulis S., Sasnauskas G., Siksnys V., Huber R. Structure of the tetrameric restriction endonuclease NgoMIV in complex with cleaved DNA. Nature Struct. Biol. 7:2000;792-799.
21. Embleton M.L., Siksnys V., Halford S.E. DNA cleavage reactions by type II restriction enzymes that require two copies of their recognition sites. J. Mol. Biol. 311:2001;503-514.
22. Tamulaitis G., Solonin A.S., Siksnys V. Alternative arrangements of catalytic residues at the active sites of restriction enzymes. FEBS Letters. 518:2002;17-22.
23. Ellis K.J., Morrison J.F. Buffers of constant ionic strength for studying pH-dependent processes. Methods Enzymol. 87:1982;405-426.
24. Haq I., O'Brien R., Lagunavicius A., Siksnys V., Ladbury J.E. Specific DNA recognition by the type II restriction endonuclease MunI: the effect of pH. Biochemistry. 40:2001;14960-14967.
25. Bozic D., Grazulis S., Siksnys V., Huber R. Crystal structure of Citrobacter freundii restriction endonuclease Cfr10I at 2.15 Å resolution. J. Mol. Biol. 255:1996;176-186.
26. Wright D.J., King K., Modrich P. The negative charge of Glu-111 is required to activate the cleavage center of EcoRI endonuclease. J. Biol. Chem. 264:1989;11816-11821.
27. Selent U., Ruter T., Kohler E., Liedtke M., Thielking V., Alves J., et al. A site-directed mutagenesis study to identify amino acid residues involved in the catalytic function of the restriction endonuclease EcoRV. Biochemistry. 31:1992;4808-4815.
28. Lagunavicius A., Siksnys V. Site-directed mutagenesis of putative active site residues of MunI restriction endonuclease: replacement of catalytically essential carboxylate residues triggers DNA binding specificity. Biochemistry. 36:1997;11086-11092.
29. Pingoud A., Jeltsch A. Recognition and cleavage of DNA by type-II restriction endonucleases. Eur. J. Biochem. 246:1997;1-22.
30. Groll D.H., Jeltsch A., Selent U., Pingoud A. Does the restriction endonuclease EcoRV employ a two-metal-ion mechanism for DNA cleavage? Biochemistry. 36:1997;11389-11401.
31. Horton N.C., Otey C., Lusetti S., Sam M.D., Kohn J., Martin A.M., et al. Electrostatic contributions to site specific DNA cleavage by EcoRV endonuclease. Biochemistry. 41:2002;10754-10763.
32. Thielking V., Selent U., Kohler E., Wolfes H., Pieper U., Geiger R., et al. Site-directed mutagenesis studies with EcoRV restriction endonuclease to identify regions involved in recognition and catalysis. Biochemistry. 30:1991;6416-6422.
33. Nastri H.G., Evans P.D., Walker I.H., Riggs P.D. Catalytic and DNA binding properties of PvuII restriction endonuclease mutants. J. Biol. Chem. 272:1997;25761-25767.
34. Dorner L.F., Bitinaite J., Whitaker R.D., Schildkraut I. Genetic analysis of the base-specific contacts of BamHI restriction endonuclease. J. Mol. Biol. 285:1999;1515-1523.
35. Wenz C., Jeltsch A., Pingoud A. Probing the indirect readout of the restriction enzyme EcoRV. Mutational analysis of contacts to the DNA backbone. J. Biol. Chem. 271:1996;5565-5573.
36. Metelev V.G., Borisova O.A., Volkov E.M., Oretskaya T.S., Dolinnaya N.G. New chemically reactive dsDNAs containing single internucleotide monophosphoryldithio links: reactivity of 5′-mercapto-oligodeoxyribonucleotides. Nucl. Acids Res. 29:2001;4062-4069.
37. Roberts R.J., Macelis D. REBASE - restriction enzymes and methylases. Nucl. Acids Res. 29:2001;268-269.
38. Grazulis S., Deibert M., Rimseliene R., Skirgaila R., Sasnauskas G., Lagunavicius A., et al. Crystal structure of the Bse634I restriction endonuclease: comparison of two enzymes recognizing the same DNA sequence. Nucl. Acids Res. 30:2002;876-885.
39. Gerlt J.A., Babbitt P.C. Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu. Rev. Biochem. 70:2001;209-246.
40. Kovall R.A., Matthews B.W. Structural, functional, and evolutionary relationships between lambda-exonuclease and the type II restriction endonucleases. Proc. Natl Acad Sci. USA. 95:1998;7893-7897.
41. Ban C., Yang W. Structural basis for MutH activation in E. coli mismatch repair and relationship of MutH to restriction endonucleases. EMBO. J. 17:1998;1526-1534.
42. Tsutakawa S.E., Muto T., Kawate T., Jingami H., Kunishima N., Ariyoshi M., et al. Crystallographic and functional studies of very short patch repair endonuclease. Mol. Cell. 3:1999;621-628.
43. Hickman A.B., Li Y., Mathew S.V., May E.W., Craig N.L., Dyda F. Unexpected structural diversity in DNA recombination: the restriction endonuclease connection. Mol. Cell. 5:2000;1025-1034.
44. Hadden J.M., Convery M.A., Declais A.C., Lilley D.M., Phillips S.E. Crystal structure of the Holliday junction resolving enzyme T7 endonuclease I. Nature Struct. Biol. 8:2001;62-67.
45. Bond C.S., Kvaratskhelia M., Richard D., White M.F., Hunter W.N. Structure of Hjc, a Holliday junction resolvase, from Sulfolobus solfataricus. Proc. Natl Acad. Sci. USA. 98:2001;5509-5514.
46. Nishino T., Komori K., Tsuchiya D., Ishino Y., Morikawa K. Crystal structure of the archaeal holliday junction resolvase Hjc and implications for DNA recognition. Structure (Camb). 9:2001;197-204.
47. Bujnicki J.M., Radlinska M., Rychlewski L. Polyphyletic evolution of type II restriction enzymes revisited: two independent sources of second-hand folds revealed. Trends Biochem. Sci. 26:2001;9-11.
48. Sapranauskas R., Sasnauskas G., Lagunavicius A., Vilkaitis G., Lubys A., Siksnys V. Novel subtype of type IIs restriction enzymes. BfiI endonuclease exhibits similarities to the EDTA-resistant nuclease Nuc of Salmonella typhimurium. J. Biol. Chem. 275:2000;30878-30885.
49. Huai Q., Colandene J.D., Chen Y., Luo F., Zhao Y., Topal M.D., Ke H. Crystal structure of NaeI - an evolutionary bridge between DNA endonuclease and topoisomerase. EMBO J. 19:2000;3110-3118.
50. Bujnicki J.M. Phylogeny of the restriction endonuclease-like superfamily inferred from comparison of protein structures. J. Mol. Evol. 50:2000;39-44.
51. Bujnicki J.M. Understanding the evolution of restriction-modification systems: clues from sequence and structure comparisons. Acta Biochim. Pol. 48:2001;935-967.
52. Mucke M., Grelle G., Behlke J., Kraft R., Kruger D.H., Reuter M. EcoRII: a restriction enzyme evolving recombination functions? EMBO J. 21:2002;5262-5268.
53. Modrich P., Zabel D. EcoRI endonuclease. Physical and catalytic properties of the homogenous enzyme. J. Biol. Chem. 251:1976;5866-5874.
54. Langowski J., Urbanke C., Pingoud A., Maass G. Transient cleavage kinetics of the EcoRI restriction endonuclease measured in a pulsed quench-flow apparatus: enzyme concentration-dependent activity change. Nucl. Acids Res. 9:1981;3483-3490.
55. Scholz S., Sonnenbichler J., Schafer W., Hensel R. Di-myo-inositol-1,1′-phosphate: a new inositol phosphate isolated from Pyrococcus woesei. FEBS Letters. 306:1992;239-242.
56. Hethke C., Bergerat A., Hausner W., Forterre P., Thomm M. Cell-free transcription at 95 degrees: thermostability of transcriptional components and DNA topology requirements of Pyrococcus transcription. Genetics. 152:1999;1325-1333.
57. Bujnicki J.M., Rychlewski L. 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. 3:2001;69-72.
58. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25:1997;3389-3402.
59. Bujnicki J.M., Elofsson A., Fischer D., Rychlewski L. Structure prediction meta server. Bioinformatics. 17:2001;750-751.
60. Lundstrom J., Rychlewski L., Bujnicki J., Elofsson A. Pcons: a neural-network-based consensus predictor that improves fold recognition. Protein Sci. 10:2001;2354-2362.
61. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:1987;406-425.
62. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18:1997;2714-2723.
63. Eisenberg D., Luthy R., Bowie J.U. VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol. 277:1997;396-404.
64. Kirsch R.D., Joly E. An improved PCR-mutagenesis strategy for two-site mutagenesis or sequence swapping between related genes. Nucl. Acids Res. 26:1998;1848-1850.
65. Sheflyan G., Kubareva E.A., Kuznetsova S.A., Karyagina A.S., Nikolskaya I.I., Gromova E.S., Shabarova Z.A. Cross-linking of SsoII restriction endonuclease to cognate and non-cognate DNAs. FEBS Letters. 390:1996;307-310.
66. O'Farrell P.H. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250:1975;4007-4021.
67. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
68. Friedhoff P., Lurz R., Luder G., Pingoud A. Sau3AI, a monomeric type II restriction endonuclease that dimerizes on the DNA and thereby induces DNA loops. J. Biol. Chem. 276:2001;23581-23588.