NUCLEIC ACID RECOGNITION BY OB-FOLD PROTEINS

Department of Chemistry and Biochemistry, University of Colorado at Boulder, Boulder, Colorado 80309-0215; email: ude.odaroloc@laboeht

Department of Chemistry and Biochemistry, University of Colorado at Boulder, Boulder, Colorado 80309-0215;email: ude.odaroloc@mryrf

Department of Chemistry and Biochemistry, University of Colorado at Boulder, Boulder, Colorado 80309-0215;email: ude.odaroloc@ekttuw.harobed

Abstract

The OB-fold domain is a compact structural motif frequently used for nucleic acid recognition. Structural comparison of all OB-fold/nucleic acid complexes solved to date confirms the low degree of sequence similarity among members of this family while highlighting several structural sequence determinants common to most of these OB-folds. Loops connecting the secondary structural elements in the OB-fold core are extremely variable in length and in functional detail. However, certain features of ligand binding are conserved among OB-fold complexes, including the location of the binding surface, the polarity of the nucleic acid with respect to the OB-fold, and particular nucleic acid—protein interactions commonly used for recognition of single-stranded and unusually structured nucleic acids. Intriguingly, the observation of shared nucleic acid polarity may shed light on the longstanding question concerning OB-fold origins, indicating that it is unlikely that members of this family arose via convergent evolution.

Keywords: single stranded, protein fold, structural alignment

Abstract

Footnotes

NOTE ADDED IN PROOF

Following the preparation of this review, the high-resolution structure of the conserved C-terminal domain of BRCA-2 complexed with DSS1 in the presence and absence of ssDNA was reported (Yang H, Jeffrey PD, Miller J, Kinnucan E, Sun Y, et al. 2002. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297:1837—48) (1MJE, 1MIU, 1IYJ). This protein contains a tandem array of three OB-folds, two of which are seen to interact with ssDNA. The DNA-binding interface is similar to that of RPA, and the ssDNA binds in the standard polarity defined here.

Footnotes

LITERATURE CITED

References

1. Allison TJ, Wood TC, Briercheck DM, Rastinejad F, Richardson JP, Rule GSCrystal structure of the RNA-binding domain from transcription termination factor rho. Nat. Struct. Biol. 1998;5:352–56.[PubMed][Google Scholar]
2. Anderson EM, Halsey WH, Wuttke DSDelineation of the high-affinity single-stranded telomeric DNA-binding domain of S. cerevisiae Cdc13. Nucleic Acids Res. 2002;30:4305–13.[Google Scholar]
3. Anderson EM, Halsey WH, Wuttke DSSite-directed mutagenesis reveals the thermodynamic requirements for single-stranded DNA recognition by the telomere-binding protein Cdc13. Biochemistry. 2002;42 In press. [[PubMed][Google Scholar]
4. Antson AASingle stranded RNA binding proteins. Curr. Opin.Struct. Biol. 2000;10:87–94.[PubMed][Google Scholar]
5. Ban N, Nissen P, Hansen J, Moore PB, Steitz TAThe completeatomic structure of the large ribosomal subunit at 2.4 Å resolution. Science. 2000;289:905–20.[PubMed][Google Scholar]
6. Bastin-Shanower SA, Brill SJ. Functional analysis of the four DNA binding domains of replication protein A. The role of RPA2 in ssDNA binding. J. Biol. Chem. 2001;276:36446–53.
7. Battiste JL, Pestova TV, Hellen CUT, Wagner GThe eIF1A solution structure reveals a large RNA-binding surface important for scanning function. Mol. Cell. 2000;5:109–19.[PubMed][Google Scholar]
8. Berthet-Colominas C, Seignovert L, Härtlein M, Grotli M, Cusack S, Leberman RThe crystal structure of asparaginyl-tRNA synthetase from Thermus thermophilus and its complexes with ATP and asparaginyl-adenylate: the mechanism of discrimination between asparagine and aspartic acid. EMBO J. 1998;17:2947–60.[Google Scholar]
9. Bochkareva E, Belegu V, Korolev S, Bochkarev AStructure of the major single-stranded DNA-binding domain of replication protein A suggests a dynamic mechanism for DNA binding. 2001;20:612–18.
10. Bochkarev A, Bochkareva E, Frappier L, Edwards AMThe crystal structure of the complex of replication protein A subunits RPA32 and RPA14 reveals a mechanism for single-stranded DNA binding. EMBO J. 1999;18:4498–504.[Google Scholar]
11. Bochkareva E, Korolev S, Lees-Miller SP, Bochkarev AStructure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. EMBO J. 2002;21:1855–63.[Google Scholar]
12. Bochkarev A, Pfuetzner RA, Edwards AM, Frappier LStructure of the single-stranded-DNA-binding domain of replication protein A bound to DNA. Nature. 1997;385:176–81.[PubMed][Google Scholar]
13. Bogden CE, Fass D, Bergman N, Nichols MD, Berger JMThe structural basis for terminator recognition by the rho transcription termination factor. Mol. Cell. 1999;3:487–93.[PubMed][Google Scholar]
14. Brennan CA, Dombroski AJ, Platt TTranscription termination factor rho is an RNA-DNA helicase. Cell. 1987;48:945–52.[PubMed][Google Scholar]
15. Briercheck DM, Wood TC, Allison TJ, Richardson JP, Rule GSThe NMR structure of the RNA binding domain of E. coli rho factor suggests possible RNA-protein interactions. Nat. Struct. Biol. 1998;5:393–99.[PubMed][Google Scholar]
16. Brodersen DE, Clemons WM, Carter AP, Wimberly BT, Ramakrishnan VCrystal structure of the 30S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16S RNA. J. Mol. Biol. 2002;316:725–68.[PubMed][Google Scholar]
17. Bycroft M, Hubbard TJP, Proctor M, Freund SMV, Murzin AGThe solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell. 1997;88:235–42.[PubMed][Google Scholar]
18. Carter AP, Clemons WM. Brodersen DE, Morgan-Warren RJ, Hartsch T, et al. 2001. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science. 291:498–501.[PubMed]
19. Cavarelli J, Rees B, Ruff M, Thierry J-C, Moras DYeast tRNA^{recognition by its cognate class II aminoacyl-tRNA synthetase.}Nature. 1993;362:181–84.[PubMed][Google Scholar]
20. Chédin F, Seitz EM, Kowalczykowski SCNovel homologs of replication protein A in archaea: implications for the evolution of ssDNA-binding proteins. Trends Biochem. Sci. 1998;23:273–77.[PubMed][Google Scholar]
21. Classen S, Ruggles JA, Schultz SCCrystal structure of the N-terminal domain of Oxytricha nova telomere end-binding protein α subunit both uncomplexed and complexed with telomeric ssDNA. J. Mol. Biol. 2001;314:1113–25.[PubMed][Google Scholar]
22. Commans S, Plateau P, Blanquet S, Dardel FSolution structure of the anticodon-binding domain of Escherichia coli lysyl-tRNA synthetase and studies of its interaction with tRNA^.J. Mol. Biol. 1995;253:100–13.[PubMed][Google Scholar]
23. Diedrich G, Spahn CMT, Stelzl U, Schäfer MA, Wooten T, et al Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. EMBO J. 2000;19:5241–50.[Google Scholar]
24. Dolan JW, Marshall NF, Richardson JPTranscription termination factor rho has three distinct structural domains. J. Biol. Chem. 1990;265:5747–54.[PubMed][Google Scholar]
25. Dombroski AJ, Platt TStructure of rho factor: an RNA-binding domain and a separate region with strong similarity to proven ATP-binding domains. Proc. Natl. Acad. Sci. USA. 1988;85:2538–42.[Google Scholar]
26. Egebjerg J, Christiansen J, Garrett RAAttachment sites of primary binding proteins L1, L2 and L23 on 23S ribosomal RNA of Escherichia coli.J. Mol. Biol. 1991;222:251–64.[PubMed][Google Scholar]
27. Eiler S, Dock-Bregeon A-C, Moulinier L, Thierry J-C, Moras DSynthesis of aspartyl-tRNAⁱⁿEscherichia coli-a snapshot of the second step. EMBO J. 1999;18:6532–41.[Google Scholar]
28. Evans SK, Lundblad VEst1 and Cdc13 as comediators of telomerase access. Science. 1999;286:117–20.[PubMed][Google Scholar]
29. Froelich-Ammon SJ, Dickinson BA, Bevilacqua JM, Schultz SC, Cech TRModulation of telomerase activity by telomere DNA-binding proteins. Oxytricha. Genes Dev. 1998;12:1504–14.[Google Scholar]
30. Garvik B, Carson M, Hartwell LSingle-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. 1995;15:6128–38.
31. Golden BL, Hoffman DW, Ramakrishnan V, White SWRibosomal protein S17: characterization of the three-dimensional structure by ^{H NMR and}^{N NMR.}Biochemistry. 1993;32:12812–20.[PubMed][Google Scholar]
32. Goldgur Y, Mosyak L, Reshetnikova L, Ankilova V, Lavrik O, et al The crystal structure of phenylalanyl-tRNA synthetase from Thermus thermophilus complexed with cognate tRNA^.Structure. 1997;5:59–68.[PubMed][Google Scholar]
33. Gottschling DE, Zakian VATelo-mere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell. 1986;47:195–205.[PubMed][Google Scholar]
34. Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, et al High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 2001;107:679–88.[PubMed][Google Scholar]
35. Horvath MP, Schultz SCDNA G-quartets in a 1.86 Å resolution structure of an Oxytricha nova telomeric protein-DNA complex. J. Mol. Biol. 2001;310:367–77.[PubMed][Google Scholar]
36. Horvath MP, Schweiker VL, Bevilacqua JM, Ruggles JA, Schultz SCCrystal structure of the Oxytricha nova telomere end binding protein complexed with single strand DNA. Cell. 1998;95:963–74.[PubMed][Google Scholar]
37. Hubbard SJ, Thornton JM NACCESS, computer program. Dep. Biochem. Mol. Biol., University College; London: 1993. [PubMed][Google Scholar]
38. Hughes TR, Weilbaecher RG, Walterscheid M, Lundblad VIdentification of the single-strand telomeric DNA binding domain of the Saccharomyces cerevisiae Cdc13 protein. Proc. Natl. Acad. Sci. USA. 2000;97:6457–62.[Google Scholar]
39. Iftode C, Daniely Y, Borowiec JAReplication protein A (RPA): the eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 1999;34:141–80.[PubMed][Google Scholar]
40. Jacobs DM, Lipton AS, Isern NG, Daugh-drill GW, Lowry DF, et al Human replication protein A: Global fold of the N-terminal RPA-70 domain reveals a basic cleft and flexible C-terminal linker. J. Biol. NMR. 1999;14:321–31.[PubMed][Google Scholar]
41. Jaishree TN, Ramakrishnan V, White SWSolution structure of prokaryotic ribosomal protein S17 by high-resolution NMR spectroscopy. Biochemistry. 1996;35:2845–53.[PubMed][Google Scholar]
42. Kelly TJ, Simancek P, Brush GSIdentification and characterization of a single-stranded DNA-binding protein from the archaeon Methanococcus jannaschii. Proc. Natl. Acad. Sci. USA. 1998;95:14634–39.[Google Scholar]
43. Khaitovich P, Mankin AS, Green R, Lancaster L, Noller HFCharacterization of functionally active subribosomal particles from Thermus aquaticus. Proc. Natl. Acad. Sci. USA. 1999;96:85–90.[Google Scholar]
44. Kim C, Snyder RO, Wold MSBinding properties of replication protein A from human and yeast cells. Mol. Cell Biol. 1992;12:3050–59.[Google Scholar]
45. Kleywegt GJUse of non-crystal-lographic symmetry in protein structure refinement. Acta Crystallogr. D. 1996;52:842–57.[PubMed][Google Scholar]
46. Kleywegt GJValidation of protein models from C^α coordinates alone. J. Mol. Biol. 1997;273:371–75.[PubMed][Google Scholar]
47. Koradi R, Billeter M, Wüthrich KMOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 1996;14:51–55.[PubMed][Google Scholar]
48. Kraulis PJMOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 1991;24:946–50.[PubMed][Google Scholar]
49. Li W, Hoffman DWStructure and dynamics of translation initiation factor aIF-1A from the archaeon Methanococcus jannaschii determined by NMR spectroscopy. Protein Sci. 2001;10:2426–38.[Google Scholar]
50. Lin J-J, Zakian VAThe Saccharomyces CDC13 protein is a single-strand TG_1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo. Proc. Natl. Acad. Sci. USA. 1996;93:13760–65.[Google Scholar]
51. Lohman TM, Ferrari ME. Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu. Rev. Biochem. 1994;63:527–70.[PubMed]
52. McGlynn P, Lloyd RGModulation of RNA polymerase by (p)ppGpp reveals a RecG-dependent mechanism for replication fork progression. Cell. 2000;101:35–45.[PubMed][Google Scholar]
53. McGlynn P, Lloyd RGRescue of stalled replication forks by RecG:Simultaneous translocation on the leading and lagging strand templates supports an active DNA unwinding model of fork reversal and Holliday junction formation. Proc. Natl. Acad. Sci. USA. 2001;98:8227–34.[Google Scholar]
54. McGlynn P, Mahdi AA, Lloyd RGCharacterisation of the catalytically active form of RecG helicase. Nucleic Acids Res. 2000;28:2324–32.[Google Scholar]
55. Merritt EA, Bacon DJRaster3D: photorealistic molecular graphics. Methods Enzymol. 1997;277:505–24.[PubMed][Google Scholar]
56. Mitton-Fry RM, Anderson EM, Hughes TR, Lundblad V, Wuttke DSConserved structure for single-stranded telomeric DNA recognition. Science. 2002;296:145–47.[PubMed][Google Scholar]
57. Murzin AGOB (oligonucleotide/ oligosaccharide binding)-fold: common structural and functional solution for nonhomologous sequences. EMBO J. 1993;12:861–67.[Google Scholar]
58. Murzin AGHow far divergent evolution goes in proteins. Curr. Opin. Struct. Biol. 1998;8:380–87.[PubMed][Google Scholar]
59. Murzin AG, Brenner SE, Hubbard T, Chothia CSCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 1995;247:536–40.[PubMed][Google Scholar]
60. Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M, Tanaka IThe three-dimensional structure of the RNA-binding domain of ribosomal protein L2; a protein at the peptidyl transferase center of the ribosome. EMBO J. 1999;18:1459–67.[Google Scholar]
61. Nugent CI, Hughes TR, Lue NF, Lundblad VCdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science. 1996;274:249–52.[PubMed][Google Scholar]
62. Ogle JM, Brodersen DE, Clemons WM. Tarry MJ, Carter AP, Ramakrishnan V. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science. 292:897–902.[PubMed]
63. Peersen OB, Ruggles JA, Schultz SCDimeric structure of the Oxytricha novatelomere end-binding protein α-subunit bound to ssDNA. Nat. Struct. Biol. 2002;9:182–87.[PubMed][Google Scholar]
64. Pennock E, Buckley K, Lundblad VCdc13 delivers separate complexes to the telomere for end protection and replication. Cell. 2001;104:387–96.[PubMed][Google Scholar]
65. Price CM, Cech TRTelomeric DNA-protein interactions of Oxytricha macronuclear DNA. Genes Dev. 1987;1:783–93.[PubMed][Google Scholar]
66. Pütz J, Puglisi JD, Florentz C, Giegé RIdentity elements for specific amino-acylation of yeast tRNA^{by cognate aspartyl-tRNA synthetase.}Science. 1991;252:1696–99.[PubMed][Google Scholar]
67. Raghunathan S, Kozlov AG, Lohman TM, Waksman GStructure of the DNA binding domain of E. coli SSB bound to ssDNA. Nat. Struct. Biol. 2000;7:648–52.[PubMed][Google Scholar]
68. Raghunathan S, Ricard CS, Lohman TM, Waksman GCrystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwave-length x-ray diffraction on the selenomethionyl protein at 2.9-Å resolution. Proc. Natl. Acad. Sci. USA. 1997;94:6652–57.[Google Scholar]
69. Ruff M, Krishnaswamy S, Boeglin M, Poterszman A, Mitschler A, et al Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyltRNA synthetase complexed with tRNA^.Science. 1991;252:1682–89.[PubMed][Google Scholar]
70. Russell RB, Barton GJMultiple protein sequence alignment from tertiary structure comparison: assignment of global and residue confidence levels. Proteins. 1992;14:309–23.[PubMed][Google Scholar]
71. Sette M, van Tilborg P, Spurio R, Kaptein R, Paci M, et al The structure of the translational initiation factor IF1 from E. coli contains an oligomer-binding motif. EMBO J. 1997;16:1436–43.[Google Scholar]
72. Shamoo Y, Friedman AM, Parsons MR, Konigsberg WH, Steitz TACrystal structure of a replication fork single-stranded DNA binding protein (T4 gp32) complexed to DNA. Nature. 1995;376:362–66.[PubMed][Google Scholar]
73. Singleton MR, Scaife S, Wigley DBStructural analysis of DNA replication fork reversal by RecG. Cell. 2001;107:79–89.[PubMed][Google Scholar]
74. Suck DCommon fold, common function, common origin? Nat. Struct. Biol. 1997;4:161–65.[PubMed][Google Scholar]
75. Swofford DL PAUP^{4.0-Phylo-genetic Analysis Using Parsimony} (^{and Other Methods}). Sinauer Assoc.; Sunderland, MA: 2002. [PubMed]
76. Wang Y, von Hippel PH. Escherichia coli transcription termination factor rho. II. Binding of oligonucleotide cofactors. J. Biol. Chem. 1993;268:13947–55.[PubMed]
77. Webster G, Genschel J, Curth U, Urbanke C, Kang C, Hilgenfeld RA common core for binding single-stranded DNA: structural comparison of the single-stranded DNA-binding proteins (SSB) from E. coli and human mitochondria. FEBS Lett. 1997;411:313–16.[PubMed][Google Scholar]
78. Williamson JRInduced fit in RNA-protein recognition. Nat. Struct. Biol. 2000;7:834–37.[PubMed][Google Scholar]
79. Wimberly BT, Brodersen DE, Clemons WM. Morgan-Warren RJ, Carter AP, et al. 2000. Structure of the 30S ribosomal subunit. Nature. 407:327–39.[PubMed]
80. Wold MSReplication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 1997;66:61–92.[PubMed][Google Scholar]