1887

Abstract

All known type I restriction and modification (R–M) systems of and belong to one of four discrete families: type IA, IB, IC or ID. The classification of type I systems from a wide range of other genera is mainly based on complementation and molecular evidence derived from the comparison of the amino acid similarity of the corresponding subunits. This affiliation was seldom based on the strictest requirement for membership of a family, which depends on relatedness as demonstrated by complementation tests. This paper presents data indicating that the type I NgoAV R–M system from , despite the very high identity of HsdM and HsdR subunits with members of the type IC family, does not show complementation with type IC R–M systems. Sequence analysis of the HsdS subunit of several different potential type IC R–M systems shows that the presence of different tetra-amino-acid sequence repeats, e.g. TAEL, LEAT, SEAL, TSEL, is characteristic for type IC R–M systems encoded by distantly related bacteria. The other regions of the HsdS subunits potentially responsible for subunit interaction are also different between a group of distantly related bacteria, but show high similarity within these bacteria. Complementation between the NgoAV R–M system and members of the EcoR124 R–M family can be restored by changing the tetra-amino-acid repeat within the HsdS subunit. The authors propose that the type IC family of R–M systems could consist of several complementation subgroups whose specificity would depend on differences in the conserved regions of the HsdS polypeptide.

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2003-11-01
2019-12-15
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References

  1. Abadjieva, A., Patel, J., Webb, M., Zinkevich, V. & Firman, K. ( 1993; ). A deletion mutant of the Type IC restriction endonuclease EcoR1241 expressing a novel DNA specificity. Nucleic Acids Res 25, 4435–4443.
    [Google Scholar]
  2. Abadjieva, A., Webb, M., Patel, J., Zinkevich, V. & Firman, K. ( 1994; ). Deletions within the DNA recognition subunit of M.EcoR124I that identify a region involved in protein-protein interactions between HsdS and HsdM. J Mol Biol 241, 35–43.[CrossRef]
    [Google Scholar]
  3. Argos, P. ( 1985; ). Evidence for a repeating domain in Type I restriction enzymes. EMBO J 4, 1351–1355.
    [Google Scholar]
  4. Bannister, D. & Glover, S. W. ( 1968; ). Restriction and modification of bacteriophages by R+ strains of Escherichia coli K12. Biochem Biophys Res Commun 30, 735–738.[CrossRef]
    [Google Scholar]
  5. Barcus, V. A. & Murray, N. E. ( 1995; ). Barriers to recombination: restriction. In Population Genetics of Bacteria, pp. 31–58. Edited by S. Baumberg, J. P. W. Young, E. M. H. Wellington & J. R. Saunders. Cambridge: Cambridge University Press.
  6. Barcus, V. A., Titheradge, A. J. & Murray, N. E. ( 1995; ). The diversity of alleles at the hsd locus in natural populations of Escherichia coli. Genetics 140, 1187–1197.
    [Google Scholar]
  7. Bickle, T. A. ( 1987; ). DNA restriction and modification systems. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, pp. 692–696. Edited by J. L. Ingraham, K. B. Low, B. Magasanik, F. C. Neidhardt, M. Schaechter & H. E. Umbarger. Washington, DC: American Society for Microbiology.
  8. Bickle, T. A. & Kruger, D. H. ( 1993; ). Biology of DNA restriction. Microbiol Rev 57, 434–450.
    [Google Scholar]
  9. Boyer, H. W. & Roulland-Dussoix, D. ( 1969; ). A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41, 459–472.[CrossRef]
    [Google Scholar]
  10. Cooper, L. P. & Dryden, D. T. ( 1994; ). The domains of a Type I DNA methyltransferase. Interactions and role in recognition of DNA methylation. J Mol Biol 236, 1011–1021.[CrossRef]
    [Google Scholar]
  11. Dryden, D. T., Cooper, L. P. & Murray, N. E. ( 1993; ). Purification and characterization of the methyltransferase from the type 1 restriction and modification system of Escherichia coli K12. J Biol Chem 268, 13228–13236.
    [Google Scholar]
  12. Dryden, D. T., Davies, G. D., Martin, I., Powell, L. M., Murray, N. E., Ellis, D. J., Berge, T., Edwardson, J. M. & Henderson, R. M. ( 1999; ). The assembly of the EcoKI Type I DNA restriction/modification enzyme and its interaction with DNA. Biochem Soc Trans 27, 691–696.
    [Google Scholar]
  13. Fuller-Pace, F. V. & Murray, N. E. ( 1986; ). Two DNA recognition domains of the specificity polypeptides of a family of Type I restriction enzymes. Proc Natl Acad Sci U S A 83, 9368–9372.[CrossRef]
    [Google Scholar]
  14. Fuller-Pace, F. V., Cowan, G. M. & Murray, N. E. ( 1985; ). EcoA and EcoE: alternatives to the EcoK family of Type I restriction and modification systems of Escherichia coli. J Mol Biol 186, 65–75.[CrossRef]
    [Google Scholar]
  15. Gough, J. A. & Murray, N. E. ( 1983; ). Sequence diversity among related genes for recognition of specific targets in DNA molecules. J Mol Biol 166, 1–19.[CrossRef]
    [Google Scholar]
  16. Gubler, M. & Bickle, T. A. ( 1991; ). Increased protein flexibility leads to promiscuous protein-DNA interactions in Type IC restriction-modification systems. EMBO J 10, 951–957.
    [Google Scholar]
  17. Gubler, M., Braguglia, D., Meyer, J., Piekarowicz, A. & Bickle, T. A. ( 1992; ). Recombination of constant and variable modules alters DNA sequence recognition by Type IC restriction-modification enzymes. EMBO J 11, 233–240.
    [Google Scholar]
  18. Hubacek, J., Holubova, I. & Weiserova, M. ( 1998; ). The effect of recA mutation on the expression of EcoKI and EcoR124I hsd genes cloned in a multicopy plasmid. Folia Microbiol 43, 353–359.[CrossRef]
    [Google Scholar]
  19. Kannan, P., Cowan, G. M., Daniel, A. S., Gann, A. A. & Murray, N. E. ( 1989; ). Conservation of organization in the specificity polypeptides of two families of Type I restriction enzymes. J Mol Biol 209, 335–344.[CrossRef]
    [Google Scholar]
  20. Kneale, G. G. ( 1994; ). A symmetrical model for the domain structure of Type I DNA methyltransferases. J Mol Biol 14, 1–5.
    [Google Scholar]
  21. Kulik, E. M. & Bickle, T. A. ( 1996; ). Regulation of the activity of the Type IC EcoR124I restriction enzyme. J Mol Biol 264, 891–906.[CrossRef]
    [Google Scholar]
  22. MacWilliams, M. P. & Bickle, T. A. ( 1996; ). Generation of new DNA binding specificity by truncation of the Type IC EcoDXXI hsdS gene. EMBO J 15, 4775–4783.
    [Google Scholar]
  23. Mayer, M. P. ( 1995; ). A new set of useful cloning and expression vectors derived from pBlueScript. Gene 163, 41–46.[CrossRef]
    [Google Scholar]
  24. Meister, J., MacWilliams, M., Hubner, P., Jutte, H., Skrzypek, E., Piekarowicz, A. & Bickle, T. A. ( 1993; ). Macroevolution by transposition: drastic modification of DNA recognition by a Type I restriction enzyme following Tn5 transposition. EMBO J 12, 4585–4591.
    [Google Scholar]
  25. Murray, N. E. ( 2000; ). Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol Mol Biol Rev 64, 412–434.[CrossRef]
    [Google Scholar]
  26. Murray, N. E., Gough, J. A., Suri, B. & Bickle, T. A. ( 1982; ). Structural homologies among Type I restriction-modification systems. EMBO J 1, 535–539.
    [Google Scholar]
  27. Noyer-Weidner, M. & Trautner, T. ( 1993; ). Methylation of DNA in procaryotes. In DNA Methylation: Molecular Biology and Biological Significance, pp. 39–108. Edited by J. P. Jost & H. P. Saluz. Basel: Birkhauster Verlag.
  28. Piekarowicz, A., Goguen, J. D. & Skrzypek, E. ( 1985; ). The EcoDXXI restriction and modification system of Escherichia coli ET7. Purification, subunit structure and properties of the restriction endonuclease. Eur J Biochem 152, 387–393.[CrossRef]
    [Google Scholar]
  29. Piekarowicz, A., Klyz, A., Kwiatek, A. & Stein, D. C. ( 2001; ). Analysis of Type I restriction modification systems in the Neisseriaceae: genetic organization and properties of the gene products. Mol Microbiol 41, 1199–1210.
    [Google Scholar]
  30. Pingoud, A. & Jeltsch, A. ( 2001; ). Structure and function of Type II restriction endonucleases. Nucleic Acids Res 29, 3705–3727.[CrossRef]
    [Google Scholar]
  31. Price, C. & Bickle, T. A. ( 1988; ). Evolution of DNA sequence specificity in Type I restriction enzymes. Biochem Soc Trans 16, 942–943.
    [Google Scholar]
  32. Price, C., Pripfl, T. & Bickle, T. A. ( 1987; ). EcoR124 and EcoR124/3: the first members of a new family of Type I restriction and modification systems. Eur J Biochem 167, 111–115.[CrossRef]
    [Google Scholar]
  33. Price, C., Lingner, J., Bickle, T. A., Firman, K. & Glover, S. W. ( 1989; ). Basis for changes in DNA recognition by the EcoR124 & EcoR124/3 Type I DNA restriction and modification enzymes. J Mol Biol 205, 115–125.[CrossRef]
    [Google Scholar]
  34. Redaschi, N. & Bickle, T. A. ( 1996; ). DNA restriction and modification systems. In Escherichia coli and Salmonella, 2nd edn. pp. 773–781. Edited by F. C. Neidhardt and others. Washington, DC: American Society for Microbiology.
  35. Roberts, R. J., Vincze, T., Posfai, J. & Macelis, D. ( 2003a; ). REBASE: restriction enzymes and methyltransferases. Nucleic Acids Res 31, 418–420.[CrossRef]
    [Google Scholar]
  36. Roberts, R. J., Belfort, M., Bestor, T. & 44 other authors ( 2003b; ). A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31, 1805–1812.[CrossRef]
    [Google Scholar]
  37. Roulland-Dussoix, D. & Boyer, H. W. ( 1969; ). The Escherichia coli B restriction endonuclease. Biochim Biophys Acta 195, 219–229.[CrossRef]
    [Google Scholar]
  38. Ryu, J., Rajadas, P. T. & Bullas, L. R. ( 1988; ). Complementation and hybridization evidence for additional families of type I DNA restriction and modification genes in Salmonella serotypes. J Bacteriol 170, 5785–5788.
    [Google Scholar]
  39. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  40. Schouler, C., Clier, F., Lerayer, A. L., Ehrlich, S. D. & Chopin, M. C. ( 1998a; ). A Type IC restriction-modification system in Lactococcus lactis. J Bacteriol 180, 407–411.
    [Google Scholar]
  41. Schouler, C., Gautier, M., Ehrlich, S. D. & Chopin, M. C. ( 1998b; ). Combinational variation of restriction modification specificities in Lactococcus lactis. Mol Microbiol 28, 169–178.
    [Google Scholar]
  42. Sharp, P. M., Kelleher, J. E., Daniel, A. S., Cowan, G. M. & Murray, N. E. ( 1992; ). Roles of selection and recombination in the evolution of Type I restriction-modification systems in enterobacteria. Proc Natl Acad Sci U S A 89, 9836–9840.[CrossRef]
    [Google Scholar]
  43. Sitaraman, R. & Dybvig, K. ( 1997; ). The hsd loci of Mycoplasma pulmonis: organization, rearrangements and expression of genes. Mol Microbiol 26, 109–120.[CrossRef]
    [Google Scholar]
  44. Skrzypek, E. & Piekarowicz, A. ( 1989; ). The EcoDXXI restriction and modification system: cloning the genes and homology to Type I restriction and modification systems. Plasmid 21, 195–204.[CrossRef]
    [Google Scholar]
  45. Suri, B. & Bickle, T. A. ( 1985; ). EcoA: the first member of a new family of Type I restriction modification systems. Gene organization and enzymatic activities. J Mol Biol 186, 77–85.[CrossRef]
    [Google Scholar]
  46. Taylor, I., Patel, J., Firman, K. & Kneale, G. ( 1992; ). Purification and biochemical characterisation of the EcoR124 Type I modification methylase. Nucleic Acids Res 20, 179–186.[CrossRef]
    [Google Scholar]
  47. Titheradge, A. J., Ternent, D. & Murray, N. E. ( 1996; ). A third family of allelic hsd genes in Salmonella enterica: sequence comparisons with related proteins identify conserved regions implicated in restriction of DNA. Mol Microbiol 22, 437–447.[CrossRef]
    [Google Scholar]
  48. Titheradge, A. J., King, J., Ryu, J. & Murray, N. E. ( 2001; ). Families of restriction enzymes: an analysis prompted by molecular and genetic data for Type ID restriction and modification systems. Nucleic Acids Res 29, 4195–4205.[CrossRef]
    [Google Scholar]
  49. Tyndall, C., Meister, J. & Bickle, T. A. ( 1994; ). The Escherichia coli prr region encodes a functional Type IC DNA restriction system closely integrated with an anticodon nuclease gene. J Mol Biol 237, 266–274.[CrossRef]
    [Google Scholar]
  50. Weiserova, M. & Firman, K. ( 1998; ). Isolation of a non-classical mutant of the DNA recognition subunit of the Type I restriction endonuclease R.EcoR124I. Biol Chem 379, 585–589.
    [Google Scholar]
  51. Weiserova, M., Janscak, P., Zinkevich, V. & Hubacek, J. ( 1994; ). Overproduction of the Hsd subunits leads to the loss of temperature-sensitive restriction and modification phenotype. Folia Microbiol 39, 452–458.[CrossRef]
    [Google Scholar]
  52. Weiserova, M., Dutta, C. F. & Firman, K. ( 2000; ). A novel mutant of the Type I restriction-modification enzyme EcoR124I is altered at a key stage of the subunit assembly pathway. J Mol Biol 304, 301–310.[CrossRef]
    [Google Scholar]
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