PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of narLink to Publisher's site
 
Nucleic Acids Res. 1997 December 15; 25(24): 5110–5118.
PMCID: PMC147149

The proofreading domain of Escherichia coli DNA polymerase I and other DNA and/or RNA exonuclease domains.

Abstract

Prior sequence analysis studies have suggested that bacterial ribonuclease (RNase) Ds comprise a complete domain that is found also in Homo sapiens polymyositis-scleroderma overlap syndrome 100 kDa autoantigen and Werner syndrome protein. This RNase D 3'-->5' exoribonuclease domain was predicted to have a structure and mechanism of action similar to the 3'-->5' exodeoxyibonuclease (proofreading) domain of DNA polymerases. Here, hidden Markov model (HMM) and phylogenetic studies have been used to identify and characterise other sequences that may possess this exonuclease domain. Results indicate that it is also present in the RNase T family; Borrelia burgdorferi P93 protein, an immunodominant antigen in Lyme disease; bacteriophage T4 dexA and Escherichia coli exonuclease I, processive 3'-->5' exodeoxyribonucleases that degrade single-stranded DNA; Bacillus subtilis dinG, a probable helicase involved in DNA repair and possibly replication, and peptide synthase 1; Saccharomyces cerevisiae Pab1p-dependent poly(A) nuclease PAN2 subunit, required for shortening mRNA poly(A) tails; Caenorhabditis elegans and Mus musculus CAF1, transcription factor CCR4-associated factor 1; Xenopus laevis XPMC2, prevention of mitotic catastrophe in fission yeast; Drosophila melanogaster egalitarian, oocyte specification and axis determination, and exuperantia, establishment of oocyte polarity; H.sapiens HEM45, expressed in tumour cell lines and uterus and regulated by oestrogen; and 31 open reading frames including one in Methanococcus jannaschii . Examination of a multiple sequence alignment and two three-dimensional structures of proofreading domains has allowed definition of the core sequence, structural and functional elements of this exonuclease domain.

Full Text

The Full Text of this article is available as a PDF (520K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Mummenbrauer T, Janus F, Müller B, Wiesmüller L, Deppert W, Grosse F. p53 Protein exhibits 3'-to-5' exonuclease activity. Cell. 1996 Jun 28;85(7):1089–1099. [PubMed]
  • Bernad A, Blanco L, Lázaro JM, Martín G, Salas M. A conserved 3'----5' exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell. 1989 Oct 6;59(1):219–228. [PubMed]
  • Delarue M, Poch O, Tordo N, Moras D, Argos P. An attempt to unify the structure of polymerases. Protein Eng. 1990 May;3(6):461–467. [PubMed]
  • Ito J, Braithwaite DK. Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res. 1991 Aug 11;19(15):4045–4057. [PMC free article] [PubMed]
  • Braithwaite DK, Ito J. Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res. 1993 Feb 25;21(4):787–802. [PMC free article] [PubMed]
  • Ollis DL, Brick P, Hamlin R, Xuong NG, Steitz TA. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature. 313(6005):762–766. [PubMed]
  • Freemont PS, Friedman JM, Beese LS, Sanderson MR, Steitz TA. Cocrystal structure of an editing complex of Klenow fragment with DNA. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8924–8928. [PubMed]
  • Derbyshire V, Freemont PS, Sanderson MR, Beese L, Friedman JM, Joyce CM, Steitz TA. Genetic and crystallographic studies of the 3',5'-exonucleolytic site of DNA polymerase I. Science. 1988 Apr 8;240(4849):199–201. [PubMed]
  • Beese LS, Steitz TA. Structural basis for the 3'-5' exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J. 1991 Jan;10(1):25–33. [PubMed]
  • Beese LS, Derbyshire V, Steitz TA. Structure of DNA polymerase I Klenow fragment bound to duplex DNA. Science. 1993 Apr 16;260(5106):352–355. [PubMed]
  • Wang J, Yu P, Lin TC, Konigsberg WH, Steitz TA. Crystal structures of an NH2-terminal fragment of T4 DNA polymerase and its complexes with single-stranded DNA and with divalent metal ions. Biochemistry. 1996 Jun 25;35(25):8110–8119. [PubMed]
  • Joyce CM, Steitz TA. Function and structure relationships in DNA polymerases. Annu Rev Biochem. 1994;63:777–822. [PubMed]
  • Reuven NB, Deutscher MP. Multiple exoribonucleases are required for the 3' processing of Escherichia coli tRNA precursors in vivo. FASEB J. 1993 Jan;7(1):143–148. [PubMed]
  • Zhang JR, Deutscher MP. Transfer RNA is a substrate for RNase D in vivo. J Biol Chem. 1988 Dec 5;263(34):17909–17912. [PubMed]
  • Mian IS. Comparative sequence analysis of ribonucleases HII, III, II PH and D. Nucleic Acids Res. 1997 Aug 15;25(16):3187–3195. [PMC free article] [PubMed]
  • Mushegian AR, Bassett DE, Jr, Boguski MS, Bork P, Koonin EV. Positionally cloned human disease genes: patterns of evolutionary conservation and functional motifs. Proc Natl Acad Sci U S A. 1997 May 27;94(11):5831–5836. [PubMed]
  • Krogh A, Brown M, Mian IS, Sjölander K, Haussler D. Hidden Markov models in computational biology. Applications to protein modeling. J Mol Biol. 1994 Feb 4;235(5):1501–1531. [PubMed]
  • Baldi P, Chauvin Y, Hunkapiller T, McClure MA. Hidden Markov models of biological primary sequence information. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1059–1063. [PubMed]
  • Eddy SR. Hidden Markov models. Curr Opin Struct Biol. 1996 Jun;6(3):361–365. [PubMed]
  • Fujiwara Y, Asogawa M, Konagaya A. Stochastic motif extraction using hidden Markov model. Proc Int Conf Intell Syst Mol Biol. 1994;2:121–129. [PubMed]
  • Dalgaard JZ, Moser MJ, Hughey R, Mian IS. Statistical modeling, phylogenetic analysis and structure prediction of a protein splicing domain common to inteins and hedgehog proteins. J Comput Biol. 1997 Summer;4(2):193–214. [PubMed]
  • Bateman A, Chothia C. Fibronectin type III domains in yeast detected by a hidden Markov model. Curr Biol. 1996 Dec 1;6(12):1544–1547. [PubMed]
  • Bateman A, Eddy SR, Chothia C. Members of the immunoglobulin superfamily in bacteria. Protein Sci. 1996 Sep;5(9):1939–1941. [PubMed]
  • Hazes B. The (QxW)3 domain: a flexible lectin scaffold. Protein Sci. 1996 Aug;5(8):1490–1501. [PubMed]
  • Shub DA, Goodrich-Blair H, Eddy SR. Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends Biochem Sci. 1994 Oct;19(10):402–404. [PubMed]
  • Grundy WN, Bailey TL, Elkan CP, Baker ME. Hidden Markov model analysis of motifs in steroid dehydrogenases and their homologs. Biochem Biophys Res Commun. 1997 Feb 24;231(3):760–766. [PubMed]
  • Barton GJ, Sternberg MJ. Flexible protein sequence patterns. A sensitive method to detect weak structural similarities. J Mol Biol. 1990 Mar 20;212(2):389–402. [PubMed]
  • Gribskov M, McLachlan AD, Eisenberg D. Profile analysis: detection of distantly related proteins. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4355–4358. [PubMed]
  • Taylor WR. Identification of protein sequence homology by consensus template alignment. J Mol Biol. 1986 Mar 20;188(2):233–258. [PubMed]
  • Bowie JU, Lüthy R, Eisenberg D. A method to identify protein sequences that fold into a known three-dimensional structure. Science. 1991 Jul 12;253(5016):164–170. [PubMed]
  • Koonin EV, Deutscher MP. RNase T shares conserved sequence motifs with DNA proofreading exonucleases. Nucleic Acids Res. 1993 May 25;21(10):2521–2522. [PMC free article] [PubMed]
  • Li Z, Deutscher MP. The role of individual exoribonucleases in processing at the 3' end of Escherichia coli tRNA precursors. J Biol Chem. 1994 Feb 25;269(8):6064–6071. [PubMed]
  • Li Z, Deutscher MP. The tRNA processing enzyme RNase T is essential for maturation of 5S RNA. Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6883–6886. [PubMed]
  • Hughey R, Krogh A. Hidden Markov models for sequence analysis: extension and analysis of the basic method. Comput Appl Biosci. 1996 Apr;12(2):95–107. [PubMed]
  • Barnes MH, Spacciapoli P, Li DH, Brown NC. The 3'-5' exonuclease site of DNA polymerase III from gram-positive bacteria: definition of a novel motif structure. Gene. 1995 Nov 7;165(1):45–50. [PubMed]
  • Brown M, Hughey R, Krogh A, Mian IS, Sjölander K, Haussler D. Using Dirichlet mixture priors to derive hidden Markov models for protein families. Proc Int Conf Intell Syst Mol Biol. 1993;1:47–55. [PubMed]
  • Sjölander K, Karplus K, Brown M, Hughey R, Krogh A, Mian IS, Haussler D. Dirichlet mixtures: a method for improved detection of weak but significant protein sequence homology. Comput Appl Biosci. 1996 Aug;12(4):327–345. [PubMed]
  • Altschul SF. Amino acid substitution matrices from an information theoretic perspective. J Mol Biol. 1991 Jun 5;219(3):555–565. [PubMed]
  • Barrett C, Hughey R, Karplus K. Scoring hidden Markov models. Comput Appl Biosci. 1997 Apr;13(2):191–199. [PubMed]
  • Barton GJ. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 1993 Jan;6(1):37–40. [PubMed]
  • Kühn FJ, Knopf CW. Herpes simplex virus type 1 DNA polymerase. Mutational analysis of the 3'-5'-exonuclease domain. J Biol Chem. 1996 Nov 15;271(46):29245–29254. [PubMed]
  • Micklem DR. mRNA localisation during development. Dev Biol. 1995 Dec;172(2):377–395. [PubMed]
  • Mach JM, Lehmann R. An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev. 1997 Feb 15;11(4):423–435. [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Herbert A, Alfken J, Kim YG, Mian IS, Nishikura K, Rich A. A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8421–8426. [PubMed]
  • Dalgaard JZ, Klar AJ, Moser MJ, Holley WR, Chatterjee A, Mian IS. Statistical modeling and analysis of the LAGLIDADG family of site-specific endonucleases and identification of an intein that encodes a site-specific endonuclease of the HNH family. Nucleic Acids Res. 1997 Nov 15;25(22):4626–4638. [PMC free article] [PubMed]
  • Li Z, Zhan L, Deutscher MP. The role of individual cysteine residues in the activity of Escherichia coli RNase T. J Biol Chem. 1996 Jan 12;271(2):1127–1132. [PubMed]
  • Wong SW, Wahl AF, Yuan PM, Arai N, Pearson BE, Arai K, Korn D, Hunkapiller MW, Wang TS. Human DNA polymerase alpha gene expression is cell proliferation dependent and its primary structure is similar to both prokaryotic and eukaryotic replicative DNA polymerases. EMBO J. 1988 Jan;7(1):37–47. [PubMed]
  • Blasco MA, Blanco L, Parés E, Salas M, Bernad A. Structural and functional analysis of temperature-sensitive mutants of the phage phi 29 DNA polymerase. Nucleic Acids Res. 1990 Aug 25;18(16):4763–4770. [PMC free article] [PubMed]
  • Brown CE, Tarun SZ, Jr, Boeck R, Sachs AB. PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol Cell Biol. 1996 Oct;16(10):5744–5753. [PMC free article] [PubMed]
  • Boeck R, Tarun S, Jr, Rieger M, Deardorff JA, Müller-Auer S, Sachs AB. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J Biol Chem. 1996 Jan 5;271(1):432–438. [PubMed]
  • Lowell JE, Rudner DZ, Sachs AB. 3'-UTR-dependent deadenylation by the yeast poly(A) nuclease. Genes Dev. 1992 Nov;6(11):2088–2099. [PubMed]
  • Draper MP, Salvadore C, Denis CL. Identification of a mouse protein whose homolog in Saccharomyces cerevisiae is a component of the CCR4 transcriptional regulatory complex. Mol Cell Biol. 1995 Jul;15(7):3487–3495. [PMC free article] [PubMed]
  • Strauss BS, Sagher D, Acharya S. Role of proofreading and mismatch repair in maintaining the stability of nucleotide repeats in DNA. Nucleic Acids Res. 1997 Feb 15;25(4):806–813. [PMC free article] [PubMed]
  • Kroutil LC, Register K, Bebenek K, Kunkel TA. Exonucleolytic proofreading during replication of repetitive DNA. Biochemistry. 1996 Jan 23;35(3):1046–1053. [PubMed]
  • Onel K, Koff A, Bennett RL, Unrau P, Holloman WK. The REC1 gene of Ustilago maydis, which encodes a 3'-->5' exonuclease, couples DNA repair and completion of DNA synthesis to a mitotic checkpoint. Genetics. 1996 May;143(1):165–174. [PubMed]
  • Belmont LD, Mitchison TJ. Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell. 1996 Feb 23;84(4):623–631. [PubMed]
  • Szankasi P, Smith GR. Requirement of S. pombe exonuclease II, a homologue of S. cerevisiae Sep1, for normal mitotic growth and viability. Curr Genet. 1996 Sep;30(4):284–293. [PubMed]
  • Bashkirov VI, Solinger JA, Heyer WD. Identification of functional domains in the Sep1 protein (= Kem1, Xrn1), which is required for transition through meiotic prophase in Saccharomyces cerevisiae. Chromosoma. 1995 Nov;104(3):215–222. [PubMed]
  • Dykhuizen DE, Polin DS, Dunn JJ, Wilske B, Preac-Mursic V, Dattwyler RJ, Luft BJ. Borrelia burgdorferi is clonal: implications for taxonomy and vaccine development. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10163–10167. [PubMed]
  • Tognoni A, Franchi E, Magistrelli C, Colombo E, Cosmina P, Grandi G. A putative new peptide synthase operon in Bacillus subtilis: partial characterization. Microbiology. 1995 Mar;141(Pt 3):645–648. [PubMed]
  • Gruber H, Kern G, Gauss P, Gold L. Effect of DNA sequence and structure on nuclease activity of the DexA protein of bacteriophage T4. J Bacteriol. 1988 Dec;170(12):5830–5836. [PMC free article] [PubMed]
  • Gauss P, Gayle M, Winter RB, Gold L. The bacteriophage T4 dexA gene: sequence and analysis of a gene conditionally required for DNA replication. Mol Gen Genet. 1987 Jan;206(1):24–34. [PubMed]
  • Koonin EV. Escherichia coli dinG gene encodes a putative DNA helicase related to a group of eukaryotic helicases including Rad3 protein. Nucleic Acids Res. 1993 Mar 25;21(6):1497–1497. [PMC free article] [PubMed]
  • Phillips GJ, Kushner SR. Determination of the nucleotide sequence for the exonuclease I structural gene (sbcB) of Escherichia coli K12. J Biol Chem. 1987 Jan 5;262(1):455–459. [PubMed]
  • Miesel L, Roth JR. Evidence that SbcB and RecF pathway functions contribute to RecBCD-dependent transductional recombination. J Bacteriol. 1996 Jun;178(11):3146–3155. [PMC free article] [PubMed]
  • Su JY, Maller JL. Cloning and expression of a Xenopus gene that prevents mitotic catastrophe in fission yeast. Mol Gen Genet. 1995 Feb 6;246(3):387–396. [PubMed]
  • Macdonald PM, Luk SK, Kilpatrick M. Protein encoded by the exuperantia gene is concentrated at sites of bicoid mRNA accumulation in Drosophila nurse cells but not in oocytes or embryos. Genes Dev. 1991 Dec;5(12B):2455–2466. [PubMed]
  • Luk SK, Kilpatrick M, Kerr K, Macdonald PM. Components acting in localization of bicoid mRNA are conserved among Drosophila species. Genetics. 1994 Jun;137(2):521–530. [PubMed]
  • Wang S, Hazelrigg T. Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. Nature. 1994 Jun 2;369(6479):400–403. [PubMed]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press