Molecular analysis of restriction endonuclease EcoRII from Escherichia coli reveals precise regulation of its enzymatic activity by autoinhibition

Molecular Microbiology

Volumn 72, Issue 4, 2009, Pages 1011-1021

  Szczepek, Michal ^a   MacKeldanz, Petra ^a   Möncke Buchner, Elisabeth ^a   Alves, Jürgen ^b   Krüger, Detlev H ^a   Reuter, Monika ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; RESTRICTION ENDONUCLEASE; RESTRICTION ENDONUCLEASE ECORII; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA CLEAVAGE; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; MOLECULAR INTERACTION; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; CIRCULAR DICHROISM; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 65549118293     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06702.x     Document Type: Article

References (40)

1. Andrade, M.A., Chacon, P., Merelo, J.J. Moran, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng 6 : 383 390. (Pubitemid 23197398)
2. Arber, W. (1979) Promotion and limitation of genetic exchange. Science 205 : 361 365. (Pubitemid 9243916)
3. Arber, W. (2000) Genetic variation: molecular mechanisms and impact on microbial evolution. FEMS Microbiol Rev 24 : 1 7. (Pubitemid 30047111)
4. Bickle, T.A. Kruger, D.H. (1993) Biology of DNA restriction. Microbiol Rev 57 : 434 450. (Pubitemid 23170101)
5. Gemmen, G.J., Millin, R. Smith, D.E. (2006) DNA looping by two-site restriction endonucleases: heterogeneous probability distributions for loop size and unbinding force. Nucleic Acids Res 34 : 2864 2877. (Pubitemid 44540415)
6. Grazulis, S., Manakova, E., Roessle, M., Bochtler, M., Tamulaitiene, G., Huber, R. Siksnys, V. (2005) Structure of the metal-independent restriction enzyme BfiI reveals fusion of a specific DNA-binding domain with a nonspecific nuclease. Proc Natl Acad Sci USA 102 : 15797 15802. (Pubitemid 41552822)
7. Hoskisson, P.A. Smith, M.C. (2007) Hypervariation and phase variation in the bacteriophage 'resistome'. Curr Opin Microbiol 10 : 396 400. (Pubitemid 47404948)
8. Kaus-Drobek, M., Czapinska, H., Sokolowska, M., Tamulaitis, G., Szczepanowski, R.H., Urbanke, C., et al. (2007) Restriction endonuclease MvaI is a monomer that recognizes its target sequence asymmetrically. Nucleic Acids Res 35 : 2035 2046. (Pubitemid 47061669)
9. Kobayashi, I. (2001) Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res 29 : 3742 3756. (Pubitemid 32910516)
10. Kruger, D.H., Barcak, G.J., Reuter, M. Smith, H.O. (1988) EcoRII can be activated to cleave refractory DNA recognition sites. Nucleic Acids Res 16 : 3997 4008.
11. Kupper, D., Reuter, M., Mackeldanz, P., Meisel, A., Alves, J., Schroeder, C. Kruger, D.H. (1995) Hyperexpressed EcoRII renatured from inclusion bodies and native enzyme both exhibit essential cooperativity with two DNA sites. Protein Expr Purif 6 : 1 9.
12. Li, P., Martins, I.R., Amarasinghe, G.K. Rosen, M.K. (2008) Internal dynamics control activation and activity of the autoinhibited Vav DH domain. Nat Struct Mol Biol 15 : 613 618.
13. Ma, E., MacRae, I.J., Kirsch, J.F. Doudna, J.A. (2008) Autoinhibition of human dicer by its internal helicase domain. J Mol Biol 380 : 237 243.
14. McDonald, I.K. Thornton, J.M. (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238 : 777 793. (Pubitemid 24168633)
15. Mucke, M., Lurz, R., Mackeldanz, P., Behlke, J., Kruger, D.H. Reuter, M. (2000) Imaging DNA loops induced by restriction endonuclease EcoRII. A single amino acid substitution uncouples target recognition from cooperative DNA interaction and cleavage. J Biol Chem 275 : 30631 30637.
16. Mucke, M., Grelle, G., Behlke, J., Kraft, R., Kruger, D.H. Reuter, M. (2002a) EcoRII: a restriction enzyme evolving recombination functions? EMBO J 21 : 5262 5268.
17. Mucke, M., Pingoud, V., Grelle, G., Kraft, R., Kruger, D.H. Reuter, M. (2002b) Asymmetric photocross-linking pattern of restriction endonuclease EcoRII to the DNA recognition sequence. J Biol Chem 277 : 14288 14293.
18. Mucke, M., Kruger, D.H. Reuter, M. (2003) Diversity of type II restriction endonucleases that require two DNA recognition sites. Nucleic Acids Res 31 : 6079 6084. (Pubitemid 37442335)
19. Nunes-Duby, S.E., Kwon, H.J., Tirumalai, R.S., Ellenberger, T. Landy, A. (1998) Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26 : 391 406. (Pubitemid 28291560)
20. Pingoud, A., Fuxreiter, M., Pingoud, V. Wende, W. (2005) Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62 : 685 707. (Pubitemid 40500928)
21. Pingoud, V., Kubareva, E., Stengel, G., Friedhoff, P., Bujnicki, J.M., Urbanke, C., et al. (2002) Evolutionary relationship between different subgroups of restriction endonucleases. J Biol Chem 277 : 14306 14314.
22. Pufall, M.A. Graves, B.J. (2002) Autoinhibitory domains: modular effectors of cellular regulation. Annu Rev Cell Dev Biol 18 : 421 462. (Pubitemid 35387357)
23. Reichmann, D., Rahat, O., Albeck, S., Meged, R., Dym, O. Schreiber, G. (2005) The modular architecture of protein-protein binding interfaces. Proc Natl Acad Sci USA 102 : 57 62. (Pubitemid 40094428)
24. Reuter, M., Kupper, D., Meisel, A., Schroeder, C. Kruger, D.H. (1998) Cooperative binding properties of restriction endonuclease EcoRII with DNA recognition sites. J Biol Chem 273 : 8294 8300. (Pubitemid 28168887)
25. Reuter, M., Schneider-Mergener, J., Kupper, D., Meisel, A., Mackeldanz, P., Kruger, D.H. Schroeder, C. (1999) Regions of endonuclease EcoRII involved in DNA target recognition identified by membrane-bound peptide repertoires. J Biol Chem 274 : 5213 5221. (Pubitemid 129501544)
26. Richards, J.D., Johnson, K.A., Liu, H., McRobbie, A.M., McMahon, S., Oke, M., et al. (2008) Structure of the DNA repair helicase hel308 reveals DNA binding and autoinhibitory domains. J Biol Chem 283 : 5118 5126. (Pubitemid 50010796)
27. Roberts, R.J., Belfort, M., Bestor, T., Bhagwat, A.S., Bickle, T.A., Bitinaite, J., et al. (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31 : 1805 1812. (Pubitemid 36437486)
28. Roberts, R.J., Vincze, T., Posfai, J. Macelis, D. (2007) REBASE - enzymes and genes for DNA restriction and modification. Nucleic Acids Res 35 : D269 D270. (Pubitemid 46056212)
29. Schymkowitz, J., Borg, J., Stricher, F., Nys, R., Rousseau, F. Serrano, L. (2005) The FoldX web server: an online force field. Nucleic Acids Res 33 : W382 W388.
30. Smith, A.J., Szczelkun, M.D. Savery, N.J. (2007) Controlling the motor activity of a transcription-repair coupling factor: autoinhibition and the role of RNA polymerase. Nucleic Acids Res 35 : 1802 1811. (Pubitemid 47061651)
31. Szczepek, M., Brondani, V., Buchel, J., Serrano, L., Segal, D.J. Cathomen, T. (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25 : 786 793. (Pubitemid 47052189)
32. Takahashi, S., Matsuno, H., Furusawa, H. Okahata, Y. (2008) Direct monitoring of allosteric recognition of type IIE restriction endonuclease EcoRII. J Biol Chem 283 : 15023 15030.
33. Tamulaitis, G., Solonin, A.S. Siksnys, V. (2002) Alternative arrangements of catalytic residues at the active sites of restriction enzymes. FEBS Lett 518 : 17 22. (Pubitemid 34454956)
34. Tamulaitis, G., Sasnauskas, G., Mucke, M. Siksnys, V. (2006) Simultaneous binding of three recognition sites is necessary for a concerted plasmid DNA cleavage by EcoRII restriction endonuclease. J Mol Biol 358 : 406 419.
35. Topal, M.D. Conrad, M. (1993) Changing endonuclease EcoRII Tyr308 to Phe abolishes cleavage but not recognition: possible homology with the Int-family of recombinases. Nucleic Acids Res 21 : 2599 2603. (Pubitemid 23209155)
36. Wallace, A.C., Laskowski, R.A. Thornton, J.M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8 : 127 134.
37. Yamasaki, K., Kigawa, T., Inoue, M., Tateno, M., Yamasaki, T., Yabuki, T., et al. (2004) Solution structure of the B3 DNA binding domain of the Arabidopsis cold-responsive transcription factor RAV1. Plant Cell 16 : 3448 3459. (Pubitemid 41096018)
38. Yamasaki, K., Kigawa, T., Inoue, M., Watanabe, S., Tateno, M., Seki, M., et al. (2008) Structures and evolutionary origins of plant-specific transcription factor DNA-binding domains. Plant Physiol Biochem 46 : 394 401.
39. Zaremba, M., Sasnauskas, G., Urbanke, C. Siksnys, V. (2005) Conversion of the tetrameric restriction endonuclease Bse634I into a dimer: oligomeric structure-stability-function correlations. J Mol Biol 348 : 459 478. (Pubitemid 40462109)
40. Zhou, X.E., Wang, Y., Reuter, M., Mucke, M., Kruger, D.H., Meehan, E.J. Chen, L. (2004) Crystal structure of type IIE restriction endonuclease EcoRII reveals an autoinhibition mechanism by a novel effector-binding fold. J Mol Biol 335 : 307 319. (Pubitemid 37494981)