Characterization and expression of the Escherichia coli Mrr restriction system
10.1128/jb.173.16.5207-5219.1991
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

The mrr gene of Escherichia coli K-12 is involved in the acceptance of foreign DNA which is modified. The introduction of plasmids carrying the HincII, HpaI, and TaqI R and M genes is severely restricted in E. coli strains that are Mrr+. A 2-kb EcoRI fragment from the plasmid pBg3 (B. Sain and N. E. Murray, Mol. Gen. Genet. 180:35-46, 1980) was cloned. The resulting plasmid restores Mrr function to mrr strains of E. coli. The boundaries of the mrr gene were determined from an analysis of subclones, and plasmids with a functional mrr gene produce a polypeptide of 33.5 kDa. The nucleotide sequence of the entire fragment was determined; in addition to mrr, it includes two open reading frames, one of which encodes part of the hsdR. By using Southern blot analysis, E. coli RR1 and HB101 were found to lack the region containing mrr. The acceptance of various cloned methylases in E. coli containing the cloned mrr gene was tested. Plasmid constructs containing the AccI, CviRI, HincII, Hinfl (HhaII), HpaI, NlaIII, PstI, and TaqI N6-adenine methylases and SssI and HhaI C5-cytosine methylases were found to be restricted. Plasmid constructs containing 16 other adenine methylases and 12 cytosine methylases were not restricted. No simple consensus sequence causing restriction has been determined. The Mrr protein has been overproduced, an antibody has been prepared, and the expression of mrr under various conditions has been examined. The use of mrr strains of E. coli is suggested for the cloning of N6-adenine and C5-cytosine methyl-containing DNA.

Bibliography

Waite-Rees, P. A., Keating, C. J., Moran, L. S., Slatko, B. E., Hornstra, L. J., & Benner, J. S. (1991). Characterization and expression of the Escherichia coli Mrr restriction system. Journal of Bacteriology, 173(16), 5207–5219.

Authors 6
  1. P A Waite-Rees (first)
  2. C J Keating (additional)
  3. L S Moran (additional)
  4. B E Slatko (additional)
  5. L J Hornstra (additional)
  6. J S Benner (additional)
References 72 Referenced 91
  1. Ansorge , W. , and S. Labeit . 1984 . Field gradients improve resolution on DNA sequencing gels . J. Biochem. Biophys. Methods 10 : 237 - 243 . (10.1016/0165-022X(84)90043-5) / J. Biochem. Biophys. Methods / Field gradients improve resolution on DNA sequencing gels by Ansorge W. (1984)
  2. Blumenthal , R. M. , S. A. Gregory , and J. S. Cooperider . 1985 . Cloning of a restriction-modification system from Proteus vulgaris and its use in analyzing a methylase-sensitive phenotype in Escherichia coli . J. Bacteriol. 164 : 501 - 509 . (10.1128/jb.164.2.501-509.1985) / J. Bacteriol. / Cloning of a restriction-modification system from Proteus vulgaris and its use in analyzing a methylase-sensitive phenotype in Escherichia coli by Blumenthal R. M. (1985)
  3. Bolivar , F. , and K. Backman . 1979 . Plasmids of Escherichia coli as cloning vectors . Methods Enzymol. 68 : 245 - 267 . (10.1016/0076-6879(79)68018-7) / Methods Enzymol. / Plasmids of Escherichia coli as cloning vectors by Bolivar F. (1979)
  4. Brooks , J. E. , J. S. Benner , D. F. Heiter , K. R. Silber , L. A. Sznyter , T. Jager-Quinton , L. S. Moran , B. E. Slatko , G. G. Wilson , and D. 0. Nwankwo . 1989 . Cloning the BamHI restriction modification system . Nucleic Acids Res. 17 : 979 - 997 . (10.1093/nar/17.3.979) / Nucleic Acids Res. / Cloning the BamHI restriction modification system by Brooks J. E. (1989)
  5. Brooks , J. E. , R. M. Blumenthal , and T. R. Gingeras . 1983 . The isolation and characterization of the E. coli DNA adenine methylase (dam) gene . Nucleic Acids Res. 11 : 837 - 851 . (10.1093/nar/11.3.837) / Nucleic Acids Res. / The isolation and characterization of the E. coli DNA adenine methylase (dam) gene by Brooks J. E. (1983)
  6. Card , C. O. , G. G. Wilson , K. Weule , J. Hasapes , A. Kiss , and R. J. Roberts . 1990 . Cloning and characterization of the HpaII methylase gene . Nucleic Acids Res. 18 : 1377 - 1383 . (10.1093/nar/18.6.1377) / Nucleic Acids Res. / Cloning and characterization of the HpaII methylase gene by Card C. O. (1990)
  7. Caserta , M. , W. Zacharias , D. Nwankwo , G. G. Wilson , and R. D. Wells . 1987 . Cloning, sequencing, in vivo promoter mapping and expression in Escherichia coli of the gene for the HhaI methyltransferase . J. Biol. Chem. 262 : 4770 - 4777 . (10.1016/S0021-9258(18)61262-1) / J. Biol. Chem. / Cloning, sequencing, in vivo promoter mapping and expression in Escherichia coli of the gene for the HhaI methyltransferase by Caserta M. (1987)
  8. Chandrasegaran , S. , K. D. Lunnen , H. 0. Smith , and G. G. Wilson . 1988 . Cloning and sequencing the Hinfl restriction and modification genes . Gene 70 : 387 - 392 . (10.1016/0378-1119(88)90210-7) / Gene / Cloning and sequencing the Hinfl restriction and modification genes by Chandrasegaran S. (1988)
  9. Chang , A. , and S. Cohen . 1978 . Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid . J. Bacteriol. 134 : 1141 - 1156 . (10.1128/jb.134.3.1141-1156.1978) / J. Bacteriol. / Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid by Chang A. (1978)
  10. Chen , E. Y. , and P. H. Seeburg . 1985 . Supercoil sequencing: a fast and simple method for sequencing plasmid DNA . DNA 4 : 165 - 170 . (10.1089/dna.1985.4.165) / DNA / Supercoil sequencing: a fast and simple method for sequencing plasmid DNA by Chen E. Y. (1985)
  11. Cohen , S. N. , A. C. Y. Chang , and L. Hsu . 1972 . Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA . Proc. Natl. Acad. Sci. USA 69 : 2110 - 2114 . (10.1073/pnas.69.8.2110) / Proc. Natl. Acad. Sci. USA / Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA by Cohen S. N. (1972)
  12. Dayhoff , M. O. , W. C. Barker , and L. T. Hunt . 1983 . Establishing homologies in protein sequences . Methods Enzymol. 91 : 524 - 545 . (10.1016/S0076-6879(83)91049-2) / Methods Enzymol. / Establishing homologies in protein sequences by Dayhoff M. O. (1983)
  13. Dever , T. E. , M. J. Glynias , and W. C. Merrick . 1987 . GTPbinding domain: three consensus sequence elements with distinct spacing . Proc. Natl. Acad. Sci. USA 84 : 1814 - 1818 . (10.1073/pnas.84.7.1814) / Proc. Natl. Acad. Sci. USA / GTPbinding domain: three consensus sequence elements with distinct spacing by Dever T. E. (1987)
  14. Devereux , J. , P. Haeberli , and 0. Smithies . 1984 . A comprehensive set of sequence analysis programs for the VAX . Nucleic Acids Res. 12 : 387 - 395 . (10.1093/nar/12.1Part1.387) / Nucleic Acids Res. / A comprehensive set of sequence analysis programs for the VAX by Devereux J. (1984)
  15. Dila , D. , E. Sutherland , L. Moran , B. Slatko , and E. A. Raleigh . 1990 . Genetic and sequence organization of the mcrBC locus of Escherichia coli K-12 . J. Bacteriol. 172 : 4888 - 4900 . (10.1128/jb.172.9.4888-4900.1990) / J. Bacteriol. / Genetic and sequence organization of the mcrBC locus of Escherichia coli K-12 by Dila D. (1990)
  16. Fleischman , R. A. , J. L. Campbell , and C. C. Richardson . 1976 . Modification and restriction of T-even bacteriophage. In vitro degradation of DNA containing 5-hydroxylmethylcytosine . J. Biol. Chem. 251 : 1561 - 1570 . (10.1016/S0021-9258(17)33685-2) / J. Biol. Chem. / Modification and restriction of T-even bacteriophage. In vitro degradation of DNA containing 5-hydroxylmethylcytosine by Fleischman R. A. (1976)
  17. Haltiner , M. , T. Kempe , and R. Tjian . 1985 . A novel strategy for constructing clustered point mutations . Nucleic Acids Res. 13 : 1015 - 1025 . (10.1093/nar/13.3.1015) / Nucleic Acids Res. / A novel strategy for constructing clustered point mutations by Haltiner M. (1985)
  18. Hattman , S. 1980 . Specificity of the bacteriophage Mu mom+- controlled DNA modification . J. Virol. 34 : 277 - 279 . (10.1128/jvi.34.1.277-279.1980) / J. Virol. / Specificity of the bacteriophage Mu mom+- controlled DNA modification by Hattman S. (1980)
  19. Hattori , M. , and Y. Sakaki . 1986 . Dideoxy sequencing method using denatured plasmid templates . Anal. Biochem. 152 : 232 - 238 . (10.1016/0003-2697(86)90403-3) / Anal. Biochem. / Dideoxy sequencing method using denatured plasmid templates by Hattori M. (1986)
  20. .Heitman J. Unpublished data.
  21. Heitman , J. , and P. Model . 1987 . Site-specific methylases induce the SOS DNA repair response in Escherichia coli . J. Bacteriol. 169 : 3243 - 3250 . (10.1128/jb.169.7.3243-3250.1987) / J. Bacteriol. / Site-specific methylases induce the SOS DNA repair response in Escherichia coli by Heitman J. (1987)
  22. Howard , K. A. , C. Card , J. S. Benner , H. L. Callahan , R. Maunus , K. Silber , G. Wilson , and J. E. Brooks . 1986 . Cloning the DdeI restriction-modification system using a two-step method . Nucleic Acids Res. 14 : 7939 - 7951 . (10.1093/nar/14.20.7939) / Nucleic Acids Res. / Cloning the DdeI restriction-modification system using a two-step method by Howard K. A. (1986)
  23. Janulaitis , A. , P. Povilionis , and K. Sanauskas . 1982 . Cloning of the modification methylase gene of Bacillus centrisporus in Escherichia coli . Gene 20 : 197 - 204 . (10.1016/0378-1119(82)90038-5) / Gene / Cloning of the modification methylase gene of Bacillus centrisporus in Escherichia coli by Janulaitis A. (1982)
  24. KelHeher , J. E. , and E. A. Raleigh . 1991 . A novel activity in Escherichia coli K-12 that directs restriction of DNA modified at CG dinucleotides . J. Bacteriol. 173 : 5220 - 5223 . (10.1128/jb.173.16.5220-5223.1991) / J. Bacteriol. / A novel activity in Escherichia coli K-12 that directs restriction of DNA modified at CG dinucleotides by KelHeher J. E. (1991)
  25. Keller , C. , N. Corcoran , and R. J. Roberts . 1984 . Computer programs for handling nucleic acid sequences . Nucleic Acids Res. 12 : 379 - 386 . (10.1093/nar/12.1Part1.379) / Nucleic Acids Res. / Computer programs for handling nucleic acid sequences by Keller C. (1984)
  26. Kohara , Y. , K. Akiyama , and K. Isono . 1987 . The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library . Cell 50 : 495 - 508 . (10.1016/0092-8674(87)90503-4) / Cell / The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library by Kohara Y. (1987)
  27. Lacks , S. , and B. Greenberg . 1977 . Complementary specificity of restriction endonucleases of Diplococcus pneumoniae with respect to DNA methylation . J. Mol. Biol. 114 : 153 - 168 . (10.1016/0022-2836(77)90289-3) / J. Mol. Biol. / Complementary specificity of restriction endonucleases of Diplococcus pneumoniae with respect to DNA methylation by Lacks S. (1977)
  28. Looney , M. C. , L. S. Moran , W. E. Jack , G. R. Feehery , J. S. Benner , B. E. Slatko , and G. G. Wilson . 1989 . Nucleotide sequence of the FokI restriction-modification system: separate strand-specificity domains in the methyltransferase . Gene 80 : 193 - 208 . (10.1016/0378-1119(89)90284-9) / Gene / Nucleotide sequence of the FokI restriction-modification system: separate strand-specificity domains in the methyltransferase by Looney M. C. (1989)
  29. Lunnen , K. D. , J. M. Barsomian , R. R. Camp , C. 0. Card , S. Chen , R. Croft , M. C. Looney , M. M. Meda , L. S. Moran , D. 0. Nwankwo , B. E. Slatko , E. M. Van Cott , and G. G. Wilson . 1988 . Cloning type-II restriction modification genes . Gene 74 : 25 - 32 . (10.1016/0378-1119(88)90242-9) / Gene / Cloning type-II restriction modification genes by Lunnen K. D. (1988)
  30. MacNeil , D. J. 1988 . Characterization of a unique methylspecific restriction system in Streptomyces avermitilis . J. Bacteriol. 170 : 5607 - 5612 . (10.1128/jb.170.12.5607-5612.1988) / J. Bacteriol. / Characterization of a unique methylspecific restriction system in Streptomyces avermitilis by MacNeil D. J. (1988)
  31. Maniatis T. E. F. Fritsch and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  32. Marinus , M. G. , and J. A. Poteete . 1984 . Correlation of DNA adenine methylase activity with spontaneous mutability in Escherichia coli K-12 . Gene 28 : 123 - 125 . (10.1016/0378-1119(84)90095-7) / Gene / Correlation of DNA adenine methylase activity with spontaneous mutability in Escherichia coli K-12 by Marinus M. G. (1984)
  33. Matsudaira , P. 1987 . Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes . J. Biol. Chem. 262 : 10035 - 10038 . (10.1016/S0021-9258(18)61070-1) / J. Biol. Chem. / Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes by Matsudaira P. (1987)
  34. McClelland , M. 1988 . Recognition sequences of type II restriction systems are constrained by the G + C content of host genomes . Nucleic Acids Res. 16 : 2283 - 2294 . (10.1093/nar/16.5.2283) / Nucleic Acids Res. / Recognition sequences of type II restriction systems are constrained by the G + C content of host genomes by McClelland M. (1988)
  35. Nelson R. M. Unpublished data.
  36. Nwankwo , D. , and G. Wilson . 1987 . Cloning of two type II methylase genes that recognize asymmetric nucleotide sequences : FokI and HgaI. Mol. Gen. Genet. 209 : 570 - 574 . (10.1007/BF00331164) / FokI and HgaI. Mol. Gen. Genet. / Cloning of two type II methylase genes that recognize asymmetric nucleotide sequences by Nwankwo D. (1987)
  37. Nwankwo , D. O. , and G. G. Wilson . 1988 . Cloning and expression of the MspI restriction and modification genes . Gene 74 : 1 - 8 . (10.1016/0378-1119(88)90475-1) / Gene / Cloning and expression of the MspI restriction and modification genes by Nwankwo D. O. (1988)
  38. Olsson , A. , T. Moks , M. Muhlen , and A. B. Gaal . 1984 . Uniformly spaced banding pattern in DNA sequencing gels by use of field-strength gradient . J. Biochem. Biophys. Methods 10 : 83 - 90 . (10.1016/0165-022X(84)90053-8) / J. Biochem. Biophys. Methods / Uniformly spaced banding pattern in DNA sequencing gels by use of field-strength gradient by Olsson A. (1984)
  39. Raleigh E. A. Unpublished data.
  40. Raleigh , E. A. , N. E. Murray , H. Revel , R. M. Blumenthal , D. Westaway , A. D. Reith , P. W. J. Rigby , J. Elhai , and D. Hanahan . 1988 . McrA and McrB restriction phenotypes of some E. coli strains and implications for gene cloning . Nucleic Acids Res. 16 : 1563 - 1575 . (10.1093/nar/16.4.1563) / Nucleic Acids Res. / McrA and McrB restriction phenotypes of some E. coli strains and implications for gene cloning by Raleigh E. A. (1988)
  41. Raleigh , E. A. , R. Trimarchi , and H. Revel . 1989 . Genetic and physical mapping of the mcrA (rglA) and mcrB (rglB) loci of Escherichia coli K-12 . Genetics 122 : 279 - 272 %. (10.1093/genetics/122.2.279) / Genetics / Genetic and physical mapping of the mcrA (rglA) and mcrB (rglB) loci of Escherichia coli K-12 by Raleigh E. A. (1989)
  42. Raleigh , E. A. , and G. Wilson . 1986 . Escherichia coli K-12 restricts DNA containing 5-methylcytosine . Proc. Natl. Acad. Sci. USA 83 : 9070 - 9074 . (10.1073/pnas.83.23.9070) / Proc. Natl. Acad. Sci. USA / Escherichia coli K-12 restricts DNA containing 5-methylcytosine by Raleigh E. A. (1986)
  43. Revel H. R. 1983. DNA modification: glucosylation p. 156-165. In C. K. Mathews E. M. Kutter G. Mosig and P. B. Berget (ed.) Bacteriophage T4. American Society for Microbiology Washington D.C.
  44. Rigby , P. W. J. , M. Dieckmann , C. Rhodes , and P. Berg . 1977 . Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase . J. Mol. Biol. 113 : 237 - 251 . (10.1016/0022-2836(77)90052-3) / J. Mol. Biol. / Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase by Rigby P. W. J. (1977)
  45. Ross , T. K. , E. C. Achberger , and H. D. Braymer . 1987 . Characterization of the Escherichia coli modified cytosine restriction (mcrB) gene . Gene 61 : 277 - 289 . (10.1016/0378-1119(87)90191-0) / Gene / Characterization of the Escherichia coli modified cytosine restriction (mcrB) gene by Ross T. K. (1987)
  46. Ross , T. K. , and H. D. Braymer . 1987 . Localization of a genetic region involved in McrB restriction in Escherichia coli K-12 . J. Bacteriol. 169 : 1757 - 1759 . (10.1128/jb.169.4.1757-1759.1987) / J. Bacteriol. / Localization of a genetic region involved in McrB restriction in Escherichia coli K-12 by Ross T. K. (1987)
  47. .Rudd K. E. Personal communication.
  48. Rudd , K. E. , W. Miller , J. Ostell , and D. A. Benson . 1990 . Alignment of Escherichia coli K12 DNA sequences to a genomic restriction map . Nucleic Acids Res. 18 : 313 - 321 . (10.1093/nar/18.2.313) / Nucleic Acids Res. / Alignment of Escherichia coli K12 DNA sequences to a genomic restriction map by Rudd K. E. (1990)
  49. Saiki , R. , D. Gelfand , S. Stoffel , S. Scharf , R. Higuchi , G. Horn , K. Mullis , and H. Erlich . 1988 . Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase . Science 239 : 487 - 491 . (10.1126/science.239.4839.487) / Science / Primer directed enzymatic amplification of DNA with a thermostable DNA polymerase by Saiki R. (1988)
  50. Sain , B. , and N. E. Murray . 1980 . The hsd (host specificity) genes of E. coli K-12 . Mol. Gen. Genet. 180 : 35 - 46 . (10.1007/BF00267350) / Mol. Gen. Genet. / The hsd (host specificity) genes of E. coli K-12 by Sain B. (1980)
  51. Sanger , F. , and A. R. Coulson . 1978 . The use of thin acrylamide gels for DNA sequencing . FEBS Lett. 87 : 107 - 110 . (10.1016/0014-5793(78)80145-8) / FEBS Lett. / The use of thin acrylamide gels for DNA sequencing by Sanger F. (1978)
  52. Sanger , F. , S. Nicklen , and A. R. Coulson . 1977 . DNA sequencing with chain-terminating inhibitors . Proc. Natl. Acad. Sci. USA 74 : 5463 - 5467 . (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA / DNA sequencing with chain-terminating inhibitors by Sanger F. (1977)
  53. Shields , S. L. , D. E. Burbank , R. Grabherr , and J. L. Van Etten . 1990 . Cloning and sequencing the cytosine methyltransferase gene M.CviJI from Chlorella virus IL-3A . Virology 176 : 16 - 24 . (10.1016/0042-6822(90)90225-G) / Virology / Cloning and sequencing the cytosine methyltransferase gene M.CviJI from Chlorella virus IL-3A by Shields S. L. (1990)
  54. Sladek , T. L. , J. A. Nowak , and J. Maniloff . 1986 . Mycoplasma restriction: identification of a new type of restriction specificity for DNA containing 5-methylcytosine . J. Bacteriol. 165 : 219 - 225 . (10.1128/jb.165.1.219-225.1986) / J. Bacteriol. / Mycoplasma restriction: identification of a new type of restriction specificity for DNA containing 5-methylcytosine by Sladek T. L. (1986)
  55. Slatko , B. E. , J. S. Benner , T. Jager-Quinton , L. S. Moran , T. G. Simcox , E. M. Van Cott , and G. G. Wilson . 1987 . Cloning, sequencing and expression of the TaqI restriction-modification system . Nucleic Acids Res. 15 : 9781 - 9796 . (10.1093/nar/15.23.9781) / Nucleic Acids Res. / Cloning, sequencing and expression of the TaqI restriction-modification system by Slatko B. E. (1987)
  56. Slatko , B. E. , R. Croft , L. S. Moran , and G. G. Wilson . 1988 . Cloning and analysis of the HaeIII and HaeII methyltransferase genes . Gene 74 : 45 - 50 . (10.1016/0378-1119(88)90248-X) / Gene / Cloning and analysis of the HaeIII and HaeII methyltransferase genes by Slatko B. E. (1988)
  57. Smith , G. E. , and M. D. Summers . 1980 . The bidirectional transfer of DNA and RNA to nitrocellulose or diazobenzyloxymethyl-paper . Anal. Biochem. 109 : 123 - 129 . (10.1016/0003-2697(80)90019-6) / Anal. Biochem. / The bidirectional transfer of DNA and RNA to nitrocellulose or diazobenzyloxymethyl-paper by Smith G. E. (1980)
  58. Southern , E. M. 1975 . Detection of specific sequences among DNA fragments separated by gel electrophoresis . J. Mol. Biol. 98 : 503 - 517 . (10.1016/S0022-2836(75)80083-0) / J. Mol. Biol. / Detection of specific sequences among DNA fragments separated by gel electrophoresis by Southern E. M. (1975)
  59. Stefan , C. , Y. H. Xia , and J. L. Van Etten . 1991 . Molecular cloning and characterization of the gene encoding the adenine methyltransferase M.CviRI from Chlorella virus XZ-6E . Nucleic Acids Res. 19 : 307 - 311 . (10.1093/nar/19.2.307) / Nucleic Acids Res. / Molecular cloning and characterization of the gene encoding the adenine methyltransferase M.CviRI from Chlorella virus XZ-6E by Stefan C. (1991)
  60. Studier , F. W. , and B. A. Moffatt . 1986 . Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes . J. Mol. Biol. 189 : 113 - 130 . (10.1016/0022-2836(86)90385-2) / J. Mol. Biol. / Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes by Studier F. W. (1986)
  61. Studier , F. W. , A. H. Rosenberg , J. J. Dunn , and J. W. Dubendorff . 1990 . Use of T7 RNA polymerase to direct expression of cloned genes . Methods Enzymol. 185 : 60 - 89 . (10.1016/0076-6879(90)85008-C) / Methods Enzymol. / Use of T7 RNA polymerase to direct expression of cloned genes by Studier F. W. (1990)
  62. Suggs , S. V. , R. B. Wallace , T. Hirose , E. H. Kawashima , and K. Itakura . 1981 . Use of synthetic oligonucleotides as hybridization probes: isolation of cloned sequences for human beta 2-microglobulin . Proc. Natl. Acad. Sci. USA 78 : 6613 - 6617 . (10.1073/pnas.78.11.6613) / Proc. Natl. Acad. Sci. USA / Use of synthetic oligonucleotides as hybridization probes: isolation of cloned sequences for human beta 2-microglobulin by Suggs S. V. (1981)
  63. Theriault , G. , P. H. Roy , K. A. Howard , J. E. Brooks , J. S. Benner , A. F. Waters , and T. R. Gingeras . 1985 . Nucleotide sequence of the PaeR7 restriction/modification system and partial characterization of its protein products . Nucleic Acids Res. 13 : 8441 - 8461 . (10.1093/nar/13.23.8441) / Nucleic Acids Res. / Nucleotide sequence of the PaeR7 restriction/modification system and partial characterization of its protein products by Theriault G. (1985)
  64. Van Cott , E. M. , and G. G. Wilson . 1988 . Cloning the FnuDI, Nae I, Nco I and Xba I restriction-modification systems . Gene 74 : 55 - 59 . (10.1016/0378-1119(88)90251-X) / Gene / Cloning the FnuDI, Nae I, Nco I and Xba I restriction-modification systems by Van Cott E. M. (1988)
  65. Waite-Rees P. A. L. J. Hornstra L. S. Moran B. E. Slatko and J. S. Benner. Unpublished data.
  66. Waite-Rees P. A. D. Nwankwo L. S. Moran B. E. Slatko G. G. Wilson and J. S. Benner. Submitted for publication.
  67. Waite-Rees P. A. C. Polisson K. R. Silber L. S. Moran B. E. Slatko and J. S. Benner. Submitted for publication.
  68. Wallace , R. B. , M. J. Johnson , T. Hirose , T. Miyaki , E. H. Kawashima , and K. Itakura . 1981 . The use of synthetic oligonucleotides as hybridization probes. II. Hybridization of oligonucleotides of mixed sequence to rabbit beta-globin DNA . Nucleic Acids Res. 9 : 879 - 894 . (10.1093/nar/9.4.879) / Nucleic Acids Res. / The use of synthetic oligonucleotides as hybridization probes. II. Hybridization of oligonucleotides of mixed sequence to rabbit beta-globin DNA by Wallace R. B. (1981)
  69. Williams , S. A. , B. E. Slatko , L. S. Moran , and S. M. DeSimone . 1986 . Sequencing in the fast lane: a rapid protocol for [a-35S]- dATP dideoxy DNA sequencing . Biotechniques 4 : 138 - 147 . / Biotechniques / Sequencing in the fast lane: a rapid protocol for [a-35S]- dATP dideoxy DNA sequencing by Williams S. A. (1986)
  70. Wilson , G. G. 1988 . Type II restriction-modification systems . Trends Genet. 4 : 314 - 318 . (10.1016/0168-9525(88)90109-6) / Trends Genet. / Type II restriction-modification systems by Wilson G. G. (1988)
  71. Yanisch-Perron , C. , J. Vieira , and J. Messing . 1985 . Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl 8 and pUC19 vectors . Gene 33 : 103 - 119 . (10.1016/0378-1119(85)90120-9) / Gene / Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl 8 and pUC19 vectors by Yanisch-Perron C. (1985)
  72. Yuan R. and D. L. Hamilton. 1984. Type I and type II restriction-modification enzymes p. 11-37. In A. Razin H. H. Cedar and A. D. Riggs (ed.) DNA methylation biochemistry and biological significance. Springer-Verlag Inc. New York. (10.1007/978-1-4613-8519-6_2)
Dates
Type When
Created 8 years, 9 months ago (Nov. 4, 2016, 4:47 p.m.)
Deposited 4 years ago (July 29, 2021, 1:52 p.m.)
Indexed 1 month, 1 week ago (July 16, 2025, 9:30 a.m.)
Issued 34 years ago (Aug. 1, 1991)
Published 34 years ago (Aug. 1, 1991)
Published Print 34 years ago (Aug. 1, 1991)
Funders 0

None

@article{Waite_Rees_1991, title={Characterization and expression of the Escherichia coli Mrr restriction system}, volume={173}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.173.16.5207-5219.1991}, DOI={10.1128/jb.173.16.5207-5219.1991}, number={16}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Waite-Rees, P A and Keating, C J and Moran, L S and Slatko, B E and Hornstra, L J and Benner, J S}, year={1991}, month=aug, pages={5207–5219} }