The DNA recognition subunit of the type IB restriction-modification enzyme EcoAI tolerates circular permutions of its polypeptide chain

Journal of Molecular Biology

Volumn 284, Issue 4, 1998, Pages 937-948

  Janscak, Pavel ^a   Bickle, Thomas A ^a  

^a NONE

Author keywords

Circularly permuted protein; DNA binding; HsdS polypeptide; Restriction modification; Subunit complex

Indexed keywords

BACTERIAL DNA; DNA METHYLTRANSFERASE; MUTANT PROTEIN; RESTRICTION ENDONUCLEASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CODON; CONTROLLED STUDY; ENZYME SUBUNIT; ESCHERICHIA COLI; GEL ELECTROPHORESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FOLDING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0032509099     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2250     Document Type: Article

References (49)

1. Abadjieva A., Patel J., Webb M., Zinkevich V., Firman K. A deletion mutant of the type IC restriction endonuclease Eco R124I expressing a novel DNA specificity. Nucl. Acids Res. 21:1993;4435-4443.
2. Bickle T. A., Krüger D. H. The biology of DNA restriction. Microbiol. Rev. 57:1993;434-450.
3. Burckhardt J., Weisemann J., Yuan R. Characterization of the DNA methylase activity of the restriction enzyme from Escherichia coli K. J. Biol. Chem. 256:1981;4024-4032.
4. Chang A. C. Y., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1978;1141-1156.
5. Cowan G. M., Gann A. A. F., Murray N. E. Conservation of complex DNA recognition domains between families of restriction enzymes. Cell. 56:1989;103-109.
6. Dreier J., MacWilliams M. P., Bickle T. A. DNA cleavage by the type IC restriction-modification enzyme Eco R124II. J. Mol. Biol. 264:1996;722-733.
7. Dryden D. T. F., Cooper L. P., Murray N. E. Purification and characterization of the methyltransferase from the type I restriction and modification system ofEscherichia coli K12. J. Biol. Chem. 268:1993;13228-13236.
8. Dryden D. T. F., Sturrock S. S., Winter M. Structural modelling of a type I DNA methyltransferase. Nature Struct. Biol. 2:1995;632-635.
9. Endlich B., Linn S. The DNA restriction endonuclease of Escherichia coli B. I. Studies of the DNA translocation and the ATPase activities. J. Biol. Chem. 260:1985;5720-5728.
10. Eskin B., Linn S. The deoxyribonucleic acid modification and restriction enzymes of Escherichia coli B. III. Studies of the restriction adenosine triphosphatase. J. Biol. Chem. 247:1972;6192-6196.
11. Fuller-Pace F. V., Bullas L. R., Delius H., Murray N. E. Genetic recombination can generate altered restriction specificity. Proc. Natl Acad. Sci. USA. 81:1984;6095-6099.
12. Fuller-Pace F. V., Cowan G. M., Murray N. E. Eco A and Eco E: alternatives to the Eco K family of type I restriction and modification systems of Escherichia coli. J. Mol. Biol. 186:1985;65-75.
13. Goldenberg D. P., Creighton T. E. Circular and circularly permuted forms of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 165:1983;407-413.
14. Gough J. A., Murray N. E. Sequence diversity among related genes for recognition of specific targets in DNA molecules. J. Mol. Biol. 166:1983;1-19.
15. Graf R., Schachman H. K. Random circular permutation of genes and expressed polypeptide chains: application of the method to the catalytic chains of aspartate transcarbamoylase. Proc. Natl Acad. Sci. USA. 93:1996;11591-11596.
16. Gubler M., Bickle T. A. Increased protein flexibility leads to promiscuous protein-DNA interactions in type IC restriction-modification systems. EMBO J. 10:1991;951-957.
17. Gubler M., Braguglia D., Meyer J., Piekarowicz A., Bickle T. A. Recombination of constant and variable modules alters DNA sequence recognition by type IC restriction-modification enzymes. EMBO J. 11:1992;233-240.
18. Hahn M., Piotukh K., Borriss R., Heinemann U. Native-like in vivo folding of a circularly permuted jellyroll protein shown by crystal structure analysis. Proc. Natl Acad. Sci. USA. 91:1994;10417-10421.
19. Jacob F., Wollman E. L. Etude génétique d'un bactériophage tempéré d'Escherichia coli. I. Le système génétique du bactériophage l. Ann. Inst. Pasteur. 87:1954;653-673.
20. Janscak P., Abadjieva A., Firman K. The type I restriction endonuclease R. Eco R124I: over-production and biochemical properties. J. Mol. Biol. 257:1996;977-991.
21. Johnson J. L., Raushel F. M. Influence of primary sequence transpositions on the folding pathways of ribonuclease T1. Biochemistry. 35:1996;10223-10233.
22. Kannan P., Cowan G. M., Daniel A. S., Gann A. A. F., Murray N. E. Conservation of organization in the specificity polypeptides of two families of type I restriction enzymes. J. Mol. Biol. 209:1989;335-344.
23. Kneale G. G. A symmetrical model for the domain structure of Type I DNA methyltransferases. J. Mol. Biol. 243:1994;1-5.
24. Koebnik R., Kramer L. Membrane assembly of circularly permuted variants of the E. coli outer membrane protein OmpA. J. Mol. Biol. 250:1995;617-626.
25. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
26. Luger K., Hommel U., Herold M., Hofsteenge J., Kirschner K. Correct folding of circularly permuted variants of a beta alpha barrel enzyme in vivo. Science. 243:1989;206-210.
27. MacWilliams M. P., Bickle T. A. Generation of new DNA binding specificity by truncation of the type IC Eco DXXI hsdS gene. EMBO J. 15:1996;4775-4783.
28. Meister J., MacWilliams M., Hubner P., Jutte H., Skrzypek E., Piekarowicz A., Bickle T. A. Macroevolution by transposition: drastic modification of DNA recognition by the type I restriction enzyme following Tn5 transposition. EMBO J. 12:1993;4585-4591.
29. Mernagh D. R., Reynolds L. A., Kneale G. G. DNA binding and subunit interactions in the type I methyltransferase M. EcoR124I. Nucl. Acids Res. 25:1997;987-991.
30. Nagaraja V., Shepherd J. C. W., Bickle T. A. A hybrid recognition sequence in a recombinant restriction enzyme and the evolution of DNA sequence specificity. Nature. 316:1985;371-372.
31. Patel J., Taylor I., Dutta C. F., Kneale G., Firman K. High-level expression of the cloned genes encoding the subunits of and intact DNA methyltransferase, M. EcoR124. Gene. 112:1992;21-27.
32. Pieper U., Hayakawa K., Li Z., Herzberg O. Circularly permuted beta-lactamase from Staphylococcus aureus PC1. Biochemistry. 36:1997;8767-8774.
33. Powell L. M., Dryden D. T. F., Willcock D. F., Pain R. H., Murray N. E. DNA recognition by the EcoK methyltransferase. The influence of DNA methylation and the cofactor S -adenosyl-L -methionine. J. Mol. Biol. 234:1993;60-71.
34. Redaschi N., Bickle T. A. DNA restriction and modification systems. Neidhardt F. C., Curtiss R. III, Ingraham J. L., Brooks Low K. B., Magasanik B., Reznikoff W. S., Riley R., Schaechter M., Umbarger H. E. Escherichia coli and Salmonella:Cellular and Molecular Biology. 1996;773-781 ASM Press, Washington.
35. Studier F. W., Bandyopadhyay P. K. Model for how type I restriction enzymes select cleavage sites in DNA. Proc. Natl Acad. Sci. USA. 85:1988;4677-4681.
36. Studier F. W., Rosenberg A. H., Dunn J. J., Dubendorff J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:1990;60-89.
37. Suri B., Bickle T. A. Eco A: the first member of a new family of type I restriction modification systems. Gene organization and enzymatic activities. J. Mol. Biol. 186:1985;77-85.
38. Suri B., Shepherd J. C. W., Bickle T. A. The Eco A restriction and modification system of Escherichia coli 15T-: enzyme structure and DNA recognition sequence. EMBO J. 3:1984;575-579.
39. Szczelkun M. D., Dillingham M. S., Janscak P., Firman K., Halford S. E. Repercussions of DNA tracking by the type IC restriction endonuclease Eco R124I on linear, circular and catenated substrates. EMBO J. 15:1996;6335-6347.
40. Taylor I., Patel J., Firman K., Kneale G. Purification and biochemical characterisation of the Eco R124 type I modification methylase. Nucl. Acids Res. 20:1992;179-186.
41. Taylor I., Watts D., Kneale G. Substrate recognition and selectivity in the type IC DNA modification methylase M. EcoR124I. Nucl. Acids Res. 21:1993;4929-4935.
42. Thorpe P. H., Ternent D., Murray N. E. The specificity of StySKI, a type I restriction enzyme, implies a structure with rotational symmetry. Nucl. Acids Res. 25:1997;1694-1700.
43. Tyndall C., Meister J., Bickle T. A. The Escherichia coli prr region encodes a functional type IC DNA restriction system closely integrated with an anticodon nuclease gene. J. Mol. Biol. 237:1994;266-274.
44. Webb M., Taylor I. A., Firman K., Kneale G. G. Probing the domain structure of the type IC DNA methyltransferase M. EcoR124I by limited proteolysis. J. Mol. Biol. 250:1995;181-190.
45. Willcock D. F., Dryden D. T. F., Murray N. E. A mutational analysis of the two motifs common to adenine methyltransferases. EMBO J. 13:1994;3902-3908.
46. Woodcock D. M., Crowther P. J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S. S., Michael M. Z., Graham M. W. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucl. Acids Res. 17:1989;3469-3478.
47. Yang Y. R., Schachman H. K. Aspartate transcarbamoylase containing circularly permuted catalytic polypeptide chains. Proc. Natl Acad. Sci. USA. 90:1993;11980-11984.
48. Yuan R., Heywood J., Meselson M. ATP hydrolysis by restriction endonuclease from E. coli K. Nature New Biol. 240:1972;42-43.
49. Yuan R., Hamilton D. L., Burckhardt J. DNA translocation by the restriction enzyme from E. coli K. Cell. 20:1980;237-244.