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Nucleotide shuffling and ssDNA recognition in Oxytricha nova telomere end-binding protein complexes.

Theobald DL, Schultz SC
EMBO J 22 4314-24 (2003)
Related entries: 1ph1, 1ph2, 1ph3, 1ph4, 1ph5, 1ph6, 1ph7, 1ph8, 1ph9, 1phj

Cited: 40 times
EuropePMC logo PMID: 12912928

Abstract

Sequence-specific protein recognition of single-stranded nucleic acids is critical for many fundamental cellular processes, such as DNA replication, DNA repair, transcription, translation, recombination, apoptosis and telomere maintenance. To explore the mechanisms of sequence-specific ssDNA recognition, we determined the crystal structures of 10 different non-cognate ssDNAs complexed with the Oxytricha nova telomere end-binding protein (OnTEBP) and evaluated their corresponding binding affinities (PDB ID codes 1PH1-1PH9 and 1PHJ). The thermodynamic and structural effects of these sequence perturbations could not have been predicted based solely upon the cognate structure. OnTEBP accommodates non-cognate nucleotides by both subtle adjustments and surprisingly large structural rearrangements in the ssDNA. In two complexes containing ssDNA intermediates that occur during telomere extension by telomerase, entire nucleotides are expelled from the complex. Concurrently, the sequence register of the ssDNA shifts to re-establish a more cognate-like pattern. This phenomenon, termed nucleotide shuffling, may be of general importance in protein recognition of single-stranded nucleic acids. This set of structural and thermodynamic data highlights a fundamental difference between protein recognition of ssDNA versus dsDNA.

Articles - 1pa6 mentioned but not cited (2)

  1. Crystallographic analysis of an RNA polymerase σ-subunit fragment complexed with -10 promoter element ssDNA: quadruplex formation as a possible tool for engineering crystal contacts in protein-ssDNA complexes. Feklistov A, Darst SA. Acta Crystallogr Sect F Struct Biol Cryst Commun 69 950-955 (2013)
  2. Dataset of normalized probability distributions of virtual bond lengths, bond angles, and dihedral angles for the coarse-grained single-stranded DNA structures. Qian JL, Sun LZ. Data Brief 42 108284 (2022)


Reviews citing this publication (7)

  1. Single-stranded DNA-binding proteins: multiple domains for multiple functions. Dickey TH, Altschuler SE, Wuttke DS. Structure 21 1074-1084 (2013)
  2. Telomerase and telomere-associated proteins: structural insights into mechanism and evolution. Lewis KA, Wuttke DS. Structure 20 28-39 (2012)
  3. Themes in ssDNA recognition by telomere-end protection proteins. Croy JE, Wuttke DS. Trends Biochem Sci 31 516-525 (2006)
  4. Structural identity of telomeric complexes. Giraud-Panis MJ, Pisano S, Poulet A, Le Du MH, Gilson E. FEBS Lett 584 3785-3799 (2010)
  5. Telomere DNA recognition in Saccharomycotina yeast: potential lessons for the co-evolution of ssDNA and dsDNA-binding proteins and their target sites. Steinberg-Neifach O, Lue NF. Front Genet 6 162 (2015)
  6. Structural anatomy of telomere OB proteins. Horvath MP. Crit Rev Biochem Mol Biol 46 409-435 (2011)
  7. Molecular Modeling Applied to Nucleic Acid-Based Molecule Development. Krüger A, Zimbres FM, Kronenberger T, Wrenger C. Biomolecules 8 E83 (2018)

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  1. Rare missense variants in POT1 predispose to familial cutaneous malignant melanoma. Shi J, Yang XR, Ballew B, Rotunno M, Calista D, Fargnoli MC, Ghiorzo P, Bressac-de Paillerets B, Nagore E, Avril MF, Caporaso NE, McMaster ML, Cullen M, Wang Z, Zhang X, NCI DCEG Cancer Sequencing Working Group, NCI DCEG Cancer Genomics Research Laboratory, French Familial Melanoma Study Group, Bruno W, Pastorino L, Queirolo P, Banuls-Roca J, Garcia-Casado Z, Vaysse A, Mohamdi H, Riazalhosseini Y, Foglio M, Jouenne F, Hua X, Hyland PL, Yin J, Vallabhaneni H, Chai W, Minghetti P, Pellegrini C, Ravichandran S, Eggermont A, Lathrop M, Peris K, Scarra GB, Landi G, Savage SA, Sampson JN, He J, Yeager M, Goldin LR, Demenais F, Chanock SJ, Tucker MA, Goldstein AM, Liu Y, Landi MT. Nat Genet 46 482-486 (2014)
  2. Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. Thompson AA, Peersen OB. EMBO J 23 3462-3471 (2004)
  3. Human protection of telomeres 1 (POT1) is a negative regulator of telomerase activity in vitro. Kelleher C, Kurth I, Lingner J. Mol Cell Biol 25 808-818 (2005)
  4. DNA conformations and their sequence preferences. Svozil D, Kalina J, Omelka M, Schneider B. Nucleic Acids Res 36 3690-3706 (2008)
  5. Structural basis for telomeric single-stranded DNA recognition by yeast Cdc13. Mitton-Fry RM, Anderson EM, Theobald DL, Glustrom LW, Wuttke DS. J Mol Biol 338 241-255 (2004)
  6. Interferon-inducible protein 16: insight into the interaction with tumor suppressor p53. Liao JC, Lam R, Brazda V, Duan S, Ravichandran M, Ma J, Xiao T, Tempel W, Zuo X, Wang YX, Chirgadze NY, Arrowsmith CH. Structure 19 418-429 (2011)
  7. The telomere capping complex CST has an unusual stoichiometry, makes multipartite interaction with G-Tails, and unfolds higher-order G-tail structures. Lue NF, Zhou R, Chico L, Mao N, Steinberg-Neifach O, Ha T. PLoS Genet 9 e1003145 (2013)
  8. A new model for Schizosaccharomyces pombe telomere recognition: the telomeric single-stranded DNA-binding activity of Pot11-389. Croy JE, Podell ER, Wuttke DS. J Mol Biol 361 80-93 (2006)
  9. Cell cycle localization, dimerization, and binding domain architecture of the telomere protein cPot1. Wei C, Price CM. Mol Cell Biol 24 2091-2102 (2004)
  10. Letter Homology among telomeric end-protection proteins. Theobald DL, Cervantes RB, Lundblad V, Wuttke DS. Structure 11 1049-1050 (2003)
  11. 'Z-DNA like' fragments in RNA: a recurring structural motif with implications for folding, RNA/protein recognition and immune response. D'Ascenzo L, Leonarski F, Vicens Q, Auffinger P. Nucleic Acids Res 44 5944-5956 (2016)
  12. Identification of the determinants for the specific recognition of single-strand telomeric DNA by Cdc13. Eldridge AM, Halsey WA, Wuttke DS. Biochemistry 45 871-879 (2006)
  13. POT1 proteins in green algae and land plants: DNA-binding properties and evidence of co-evolution with telomeric DNA. Shakirov EV, Song X, Joseph JA, Shippen DE. Nucleic Acids Res 37 7455-7467 (2009)
  14. Nonspecific recognition is achieved in Pot1pC through the use of multiple binding modes. Dickey TH, McKercher MA, Wuttke DS. Structure 21 121-132 (2013)
  15. DNA binding provides a molecular strap activating the adenovirus proteinase. Gupta S, Mangel WF, McGrath WJ, Perek JL, Lee DW, Takamoto K, Chance MR. Mol Cell Proteomics 3 950-959 (2004)
  16. An intrastrand three-DNA-base interaction is a key specificity determinant of F transfer initiation and of F TraI relaxase DNA recognition and cleavage. Hekman K, Guja K, Larkin C, Schildbach JF. Nucleic Acids Res 36 4565-4572 (2008)
  17. Potential DNA binding and nuclease functions of ComEC domains characterized in silico. Baker JA, Simkovic F, Taylor HM, Rigden DJ. Proteins 84 1431-1442 (2016)
  18. Nonadditivity in the recognition of single-stranded DNA by the schizosaccharomyces pombe protection of telomeres 1 DNA-binding domain, Pot1-DBD. Croy JE, Altschuler SE, Grimm NE, Wuttke DS. Biochemistry 48 6864-6875 (2009)
  19. Automatic workflow for the classification of local DNA conformations. Čech P, Kukal J, Černý J, Schneider B, Svozil D. BMC Bioinformatics 14 205 (2013)
  20. Structural reorganization and the cooperative binding of single-stranded telomere DNA in Sterkiella nova. Buczek P, Horvath MP. J Biol Chem 281 40124-40134 (2006)
  21. Deciphering the mechanism of thermodynamic accommodation of telomeric oligonucleotide sequences by the Schizosaccharomyces pombe protection of telomeres 1 (Pot1pN) protein. Croy JE, Fast JL, Grimm NE, Wuttke DS. Biochemistry 47 4345-4358 (2008)
  22. Combinatorial recognition of a complex telomere repeat sequence by the Candida parapsilosis Cdc13AB heterodimer. Steinberg-Neifach O, Wellington K, Vazquez L, Lue NF. Nucleic Acids Res 43 2164-2176 (2015)
  23. Replication Protein A Utilizes Differential Engagement of Its DNA-Binding Domains to Bind Biologically Relevant ssDNAs in Diverse Binding Modes. Wieser TA, Wuttke DS. Biochemistry 61 2592-2606 (2022)
  24. Thermodynamic and electrostatic properties of ternary Oxytricha nova TEBP-DNA complex. Wojciechowski M, Fogolari F, Baginski M. J Struct Biol 152 169-184 (2005)
  25. Single-stranded telomere-binding protein employs a dual rheostat for binding affinity and specificity that drives function. Glustrom LW, Lyon KR, Paschini M, Reyes CM, Parsonnet NV, Toro TB, Lundblad V, Wuttke DS. Proc Natl Acad Sci U S A 115 10315-10320 (2018)
  26. Insights into the structure and function of Est3 from the Hansenula polymorpha telomerase. Shepelev NM, Mariasina SS, Mantsyzov AB, Malyavko AN, Efimov SV, Petrova OA, Rodina EV, Zvereva MI, Dontsova OA, Polshakov VI. Sci Rep 10 11109 (2020)
  27. A comparative study of protein-ssDNA interactions. Lin M, Malik FK, Guo JT. NAR Genom Bioinform 3 lqab006 (2021)
  28. Discrimination against RNA Backbones by a ssDNA Binding Protein. Lloyd NR, Wuttke DS. Structure 26 722-733.e2 (2018)
  29. Characterization of EndoTT, a novel single-stranded DNA-specific endonuclease from Thermoanaerobacter tengcongensis. Zhang S, Liu B, Yang H, Tian Y, Liu G, Li L, Tan H. Nucleic Acids Res 38 3709-3720 (2010)
  30. Nucleotides sequestered at different subsite loci within DNA-binding pockets of two OB-fold single-stranded DNA-binding proteins are unstacked to different extents. Nguyen HN, Zhao L, Gray CW, Gray DM, Xia T. Biopolymers 99 484-496 (2013)
  31. Role of conformational dynamics in sequence-specific autoantibody*ssDNA recognition. Bobeck MJ, Glick GD. Biopolymers 85 481-489 (2007)


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