3qlp Citations

Thrombin-aptamer recognition: a revealed ambiguity.

Nucleic Acids Res 39 7858-67 (2011)
Cited: 75 times
EuropePMC logo PMID: 21715374

Abstract

Aptamers are structured oligonucleotides that recognize molecular targets and can function as direct protein inhibitors. The best-known example is the thrombin-binding aptamer, TBA, a single-stranded 15-mer DNA that inhibits the activity of thrombin, the key enzyme of coagulation cascade. TBA folds as a G-quadruplex structure, as proved by its NMR structure. The X-ray structure of the complex between TBA and human α-thrombin was solved at 2.9-Å resolution, but did not provide details of the aptamer conformation and the interactions with the protein molecule. TBA is rapidly processed by nucleases. To improve the properties of TBA, a number of modified analogs have been produced. In particular, a modified TBA containing a 5'-5' polarity inversion site, mTBA, has higher stability and higher affinity toward thrombin with respect to TBA, although it has a lower inhibitory activity. We present the crystal structure of the thrombin-mTBA complex at 2.15-Å resolution; the resulting model eventually provides a clear picture of thrombin-aptamers interaction, and also highlights the structural bases of the different properties of TBA and mTBA. Our findings open the way for a rational design of modified aptamers with improved potency as anticoagulant drugs.

Reviews - 3qlp mentioned but not cited (4)

  1. Characterization of aptamer-protein complexes by X-ray crystallography and alternative approaches. Ruigrok VJ, Levisson M, Hekelaar J, Smidt H, Dijkstra BW, van der Oost J. Int J Mol Sci 13 10537-10552 (2012)
  2. On Characterizing the Interactions between Proteins and Guanine Quadruplex Structures of Nucleic Acids. McRae EKS, Booy EP, Padilla-Meier GP, McKenna SA. J Nucleic Acids 2017 9675348 (2017)
  3. Structural Biology for the Molecular Insight between Aptamers and Target Proteins. Zhang N, Chen Z, Chen Z, Liu D, Jiang H, Zhang ZK, Lu A, Zhang BT, Yu Y, Zhang G. Int J Mol Sci 22 4093 (2021)
  4. Exosite Binding in Thrombin: A Global Structural/Dynamic Overview of Complexes with Aptamers and Other Ligands. Troisi R, Balasco N, Autiero I, Vitagliano L, Sica F. Int J Mol Sci 22 10803 (2021)

Articles - 3qlp mentioned but not cited (6)

  1. High-resolution structures of two complexes between thrombin and thrombin-binding aptamer shed light on the role of cations in the aptamer inhibitory activity. Russo Krauss I, Merlino A, Randazzo A, Novellino E, Mazzarella L, Sica F. Nucleic Acids Res. 40 8119-8128 (2012)
  2. Thrombin-aptamer recognition: a revealed ambiguity. Russo Krauss I, Merlino A, Giancola C, Randazzo A, Mazzarella L, Sica F. Nucleic Acids Res. 39 7858-7867 (2011)
  3. Crystal structure of a DNA aptamer bound to PvLDH elucidates novel single-stranded DNA structural elements for folding and recognition. Choi SJ, Ban C. Sci Rep 6 34998 (2016)
  4. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  5. Energy Transfer as A Driving Force in Nucleic Acid⁻Protein Interactions. Zavyalova E, Kopylov A. Molecules 24 E1443 (2019)
  6. Putative Mechanisms Underlying High Inhibitory Activities of Bimodular DNA Aptamers to Thrombin. Zavyalova EG, Legatova VA, Alieva RS, Zalevsky AO, Tashlitsky VN, Arutyunyan AM, Kopylov AM. Biomolecules 9 (2019)


Reviews citing this publication (9)

  1. Nucleic Acid Ligands With Protein-like Side Chains: Modified Aptamers and Their Use as Diagnostic and Therapeutic Agents. Rohloff JC, Gelinas AD, Jarvis TC, Ochsner UA, Schneider DJ, Gold L, Janjic N. Mol Ther Nucleic Acids 3 e201 (2014)
  2. Embracing proteins: structural themes in aptamer-protein complexes. Gelinas AD, Davies DR, Janjic N. Curr. Opin. Struct. Biol. 36 122-132 (2016)
  3. An overview of biological macromolecule crystallization. Russo Krauss I, Merlino A, Vergara A, Sica F. Int J Mol Sci 14 11643-11691 (2013)
  4. MIPs and Aptamers for Recognition of Proteins in Biomimetic Sensing. Menger M, Yarman A, Erdőssy J, Yildiz HB, Gyurcsányi RE, Scheller FW. Biosensors (Basel) 6 (2016)
  5. Dimeric and Multimeric DNA Aptamers for Highly Effective Protein Recognition. Riccardi C, Napolitano E, Musumeci D, Montesarchio D. Molecules 25 E5227 (2020)
  6. Applications of synchrotron-based spectroscopic techniques in studying nucleic acids and nucleic acid-functionalized nanomaterials. Wu P, Yu Y, McGhee CE, Tan LH, Lu Y. Adv. Mater. Weinheim 26 7849-7872 (2014)
  7. The modulation of coagulation by aptamers: an up-to-date review. Hu PP, Zhang KH. Blood Coagul. Fibrinolysis 26 1-6 (2015)
  8. Structural Insights into Protein-Aptamer Recognitions Emerged from Experimental and Computational Studies. Troisi R, Balasco N, Autiero I, Vitagliano L, Sica F. Int J Mol Sci 24 16318 (2023)
  9. Structural motifs and intramolecular interactions in non-canonical G-quadruplexes. Jana J, Mohr S, Vianney YM, Weisz K. RSC Chem Biol 2 338-353 (2021)

Articles citing this publication (56)

  1. Structural basis for discriminatory recognition of Plasmodium lactate dehydrogenase by a DNA aptamer. Cheung YW, Kwok J, Law AW, Watt RM, Kotaka M, Tanner JA. Proc. Natl. Acad. Sci. U.S.A. 110 15967-15972 (2013)
  2. Selective recognition of parallel and anti-parallel thrombin-binding aptamer G-quadruplexes by different fluorescent dyes. Zhao D, Dong X, Jiang N, Zhang D, Liu C. Nucleic Acids Res. 42 11612-11621 (2014)
  3. Structural requirements for the procoagulant activity of nucleic acids. Gansler J, Jaax M, Leiting S, Appel B, Greinacher A, Fischer S, Preissner KT. PLoS ONE 7 e50399 (2012)
  4. Single molecule multiplexed nanopore protein screening in human serum using aptamer modified DNA carriers. Sze JYY, Ivanov AP, Cass AEG, Edel JB. Nat Commun 8 1552 (2017)
  5. Stability and bioactivity of thrombin binding aptamers modified with D-/L-isothymidine in the loop regions. Cai B, Yang X, Sun L, Fan X, Li L, Jin H, Wu Y, Guan Z, Zhang L, Zhang L, Yang Z. Org. Biomol. Chem. 12 8866-8876 (2014)
  6. Non-helical DNA Triplex Forms a Unique Aptamer Scaffold for High Affinity Recognition of Nerve Growth Factor. Jarvis TC, Davies DR, Hisaminato A, Resnicow DI, Gupta S, Waugh SM, Nagabukuro A, Wadatsu T, Hishigaki H, Gawande B, Zhang C, Wolk SK, Mayfield WS, Nakaishi Y, Burgin AB, Stewart LJ, Edwards TE, Gelinas AD, Schneider DJ, Janjic N. Structure 23 1293-1304 (2015)
  7. 5-Hydroxymethyl-2'-deoxyuridine residues in the thrombin binding aptamer: investigating anticoagulant activity by making a tiny chemical modification. Virgilio A, Petraccone L, Scuotto M, Vellecco V, Bucci M, Mayol L, Varra M, Esposito V, Galeone A. Chembiochem 15 2427-2434 (2014)
  8. Comparison of the 'chemical' and 'structural' approaches to the optimization of the thrombin-binding aptamer. Tatarinova O, Tsvetkov V, Basmanov D, Barinov N, Smirnov I, Timofeev E, Kaluzhny D, Chuvilin A, Klinov D, Varizhuk A, Pozmogova G. PLoS ONE 9 e89383 (2014)
  9. Duplex-quadruplex motifs in a peculiar structural organization cooperatively contribute to thrombin binding of a DNA aptamer. Russo Krauss I, Pica A, Merlino A, Mazzarella L, Sica F. Acta Crystallogr. D Biol. Crystallogr. 69 2403-2411 (2013)
  10. Analysis and Identification of Aptamer-Compound Interactions with a Maximum Relevance Minimum Redundancy and Nearest Neighbor Algorithm. Wang S, Zhang YH, Lu J, Cui W, Hu J, Cai YD. Biomed Res Int 2016 8351204 (2016)
  11. Differential scanning calorimetry to investigate G-quadruplexes structural stability. Pagano B, Randazzo A, Fotticchia I, Novellino E, Petraccone L, Giancola C. Methods 64 43-51 (2013)
  12. Prediction of aptamer-target interacting pairs with pseudo-amino acid composition. Li BQ, Zhang YC, Huang GH, Cui WR, Zhang N, Cai YD. PLoS ONE 9 e86729 (2014)
  13. Specific loop modifications of the thrombin-binding aptamer trigger the formation of parallel structures. Aviñó A, Portella G, Ferreira R, Gargallo R, Mazzini S, Gabelica V, Orozco M, Eritja R. FEBS J. 281 1085-1099 (2014)
  14. Dissecting the contribution of thrombin exosite I in the recognition of thrombin binding aptamer. Pica A, Russo Krauss I, Merlino A, Nagatoishi S, Sugimoto N, Sica F. FEBS J. 280 6581-6588 (2013)
  15. Site-specific replacement of the thymine methyl group by fluorine in thrombin binding aptamer significantly improves structural stability and anticoagulant activity. Virgilio A, Petraccone L, Vellecco V, Bucci M, Varra M, Irace C, Santamaria R, Pepe A, Mayol L, Esposito V, Galeone A. Nucleic Acids Res. 43 10602-10611 (2015)
  16. Through-bond effects in the ternary complexes of thrombin sandwiched by two DNA aptamers. Pica A, Russo Krauss I, Parente V, Tateishi-Karimata H, Nagatoishi S, Tsumoto K, Sugimoto N, Sica F. Nucleic Acids Res. 45 461-469 (2017)
  17. Assay of multiplex proteins from cell metabolism based on tunable aptamer and microchip electrophoresis. Lin X, Chen Q, Liu W, Yi L, Li H, Wang Z, Lin JM. Biosens Bioelectron 63 105-111 (2015)
  18. Interaction of water with the G-quadruplex loop contributes to the binding energy of G-quadruplex to protein. Nagatoishi S, Sugimoto N. Mol Biosyst 8 2766-2770 (2012)
  19. Aptamers: new arrows to target dendritic cells. Ganji A, Varasteh A, Sankian M. J Drug Target 24 1-12 (2016)
  20. Artificial specific binders directly recovered from chemically modified nucleic acid libraries. Kasahara Y, Kuwahara M. J Nucleic Acids 2012 156482 (2012)
  21. Different duplex/quadruplex junctions determine the properties of anti-thrombin aptamers with mixed folding. Russo Krauss I, Spiridonova V, Pica A, Napolitano V, Sica F. Nucleic Acids Res. 44 983-991 (2016)
  22. Position-specific modification with imidazolyl group on10-23 DNAzyme realized catalytic activity enhancement. Li Z, Liu Y, Liu G, Zhu J, Zheng Z, Zhou Y, He J. Bioorg. Med. Chem. 22 4010-4017 (2014)
  23. A regular thymine tetrad and a peculiar supramolecular assembly in the first crystal structure of an all-LNA G-quadruplex. Russo Krauss I, Parkinson GN, Merlino A, Mattia CA, Randazzo A, Novellino E, Mazzarella L, Sica F. Acta Crystallogr. D Biol. Crystallogr. 70 362-370 (2014)
  24. A family of DNA aptamers with varied duplex region length that forms complexes with thrombin and prothrombin. Spiridonova VA, Barinova KV, Glinkina KA, Melnichuk AV, Gainutdynov AA, Safenkova IV, Dzantiev BB. FEBS Lett. 589 2043-2049 (2015)
  25. Development of an Efficient G-Quadruplex-Stabilised Thrombin-Binding Aptamer Containing a Three-Carbon Spacer Molecule. Aaldering LJ, Poongavanam V, Langkjaer N, Murugan NA, Jørgensen PT, Wengel J, Veedu RN. Chembiochem 18 755-763 (2017)
  26. Stability Is Not Everything: The Case of the Cyclisation of a Thrombin-Binding Aptamer. Riccardi C, Meyer A, Vasseur JJ, Russo Krauss I, Paduano L, Oliva R, Petraccone L, Morvan F, Montesarchio D. Chembiochem 20 1789-1794 (2019)
  27. Anomeric DNA quadruplexes. Kolganova NA, Varizhuk AM, Novikov RA, Florentiev VL, Pozmogova GE, Borisova OF, Shchyolkina AK, Smirnov IP, Kaluzhny DN, Timofeev EN. Artif DNA PNA XNA 5 e28422 (2014)
  28. Aptamer-based fiber sensor for thrombin detection. Coelho L, Marques Martins de Almeida JM, Santos JL, da Silva Jorge PA, Martins MC, Viegas D, Queirós RB. J Biomed Opt 21 87005 (2016)
  29. Expanding the recognition interface of the thrombin-binding aptamer HD1 through modification of residues T3 and T12. Smirnov I, Kolganova N, Troisi R, Sica F, Timofeev E. Mol Ther Nucleic Acids 23 863-871 (2021)
  30. Human Rev1 relies on insert-2 to promote selective binding and accurate replication of stabilized G-quadruplex motifs. Ketkar A, Smith L, Johnson C, Richey A, Berry M, Hartman JH, Maddukuri L, Reed MR, Gunderson JEC, Leung JWC, Eoff RL. Nucleic Acids Res 49 2065-2084 (2021)
  31. Crystal structures of thrombin in complex with chemically modified thrombin DNA aptamers reveal the origins of enhanced affinity. Dolot R, Lam CH, Sierant M, Zhao Q, Liu FW, Nawrot B, Egli M, Yang X. Nucleic Acids Res. 46 4819-4830 (2018)
  32. Engineering base-excised aptamers for highly specific recognition of adenosine. Li Y, Liu B, Huang Z, Liu J. Chem Sci 11 2735-2743 (2020)
  33. Volumetric contributions of loop regions of G-quadruplex DNA to the formation of the tertiary structure. Takahashi S, Sugimoto N. Biophys. Chem. 231 146-154 (2017)
  34. Crosslinked duplex DNA nanogels that target specified proteins. Iwasaki Y, Kondo JI, Kuzuya A, Moriyama R. Sci Technol Adv Mater 17 285-292 (2016)
  35. Congresses G-ruption: the third international meeting on G-quadruplex and G-assembly. Yatsunyk LA, Bryan TM, Johnson FB. Biochimie 94 2475-2483 (2012)
  36. Rapid identification of specific DNA aptamers precisely targeting CD33 positive leukemia cells through a paired cell-based approach. Yang C, Wang Y, Ge MH, Fu YJ, Hao R, Islam K, Huang P, Chen F, Sun J, Hong F, Naranmandura H. Biomater Sci 7 938-950 (2019)
  37. Several structural motifs cooperate in determining the highly effective anti-thrombin activity of NU172 aptamer. Troisi R, Napolitano V, Spiridonova V, Russo Krauss I, Sica F. Nucleic Acids Res. 46 12177-12185 (2018)
  38. Thermodynamic, Anticoagulant, and Antiproliferative Properties of Thrombin Binding Aptamer Containing Novel UNA Derivative. Kotkowiak W, Lisowiec-Wachnicka J, Grynda J, Kierzek R, Wengel J, Pasternak A. Mol Ther Nucleic Acids 10 304-316 (2018)
  39. Thrombin-Binding Aptamer with Inversion of Polarity Sites (IPS): Effect on DNAzyme Activity and Anticoagulant Properties. Kosman J, Juskowiak B. Int J Mol Sci 22 7902 (2021)
  40. A Comprehensive Analysis of the Thrombin Binding Aptamer Containing Functionalized Pyrrolo-2'-deoxycytidines. Kotkowiak W, Jahnz-Wechmann Z, Pasternak A. Pharmaceuticals (Basel) 14 1326 (2021)
  41. A terminal functionalization strategy reveals unusual binding abilities of anti-thrombin anticoagulant aptamers. Troisi R, Riccardi C, Pérez de Carvasal K, Smietana M, Morvan F, Del Vecchio P, Montesarchio D, Sica F. Mol Ther Nucleic Acids 30 585-594 (2022)
  42. Anabel: An Online Tool for the Real-Time Kinetic Analysis of Binding Events. Krämer SD, Wöhrle J, Rath C, Roth G. Bioinform Biol Insights 13 1177932218821383 (2019)
  43. Charge-Transfer Interactions Stabilize G-Quadruplex-Forming Thrombin Binding Aptamers and Can Improve Their Anticoagulant Activity. Pérez de Carvasal K, Riccardi C, Russo Krauss I, Cavasso D, Vasseur JJ, Smietana M, Morvan F, Montesarchio D. Int J Mol Sci 22 9510 (2021)
  44. Continuous Detection of Increasing Concentrations of Thrombin Employing a Label-Free Photonic Crystal Aptasensor. Martínez-Pérez P, Gómez-Gómez M, Angelova T, Griol A, Hurtado J, Bellieres L, García-Rupérez J. Micromachines (Basel) 11 (2020)
  45. Design, Synthesis and Characterization of Cyclic NU172 Analogues: A Biophysical and Biological Insight. Riccardi C, Meyer A, Vasseur JJ, Cavasso D, Russo Krauss I, Paduano L, Morvan F, Montesarchio D. Int J Mol Sci 21 (2020)
  46. Electrical Stimulus Controlled Binding/Unbinding of Human Thrombin-Aptamer Complex. Gosai A, Ma X, Balasubramanian G, Shrotriya P. Sci Rep 6 37449 (2016)
  47. Experimental and mathematical evidence that thrombin-binding aptamers form a 1 aptamer:2 protein complex. Mears KS, Markus DL, Ogunjimi O, Whelan RJ. Aptamers (Oxf) 2 64-73 (2018)
  48. Exploring New Potential Anticancer Activities of the G-Quadruplexes Formed by [(GTG2T(G3T)3] and Its Derivatives with an Abasic Site Replacing Single Thymidine. Virgilio A, Benigno D, Pecoraro A, Russo A, Russo G, Esposito V, Galeone A. Int J Mol Sci 22 7040 (2021)
  49. Improving the Biological Properties of Thrombin-Binding Aptamer by Incorporation of 8-Bromo-2'-Deoxyguanosine and 2'-Substituted RNA Analogues. Virgilio A, Benigno D, Aliberti C, Vellecco V, Bucci M, Esposito V, Galeone A. Int J Mol Sci 24 15529 (2023)
  50. Precise Microfluidic Luminescent Sensor Platform with Controlled Injection System. Kang B, Choi S, Kim K, Jung HS, Kwak MK. ACS Omega 6 23412-23420 (2021)
  51. Recognition Interface of the Thrombin Binding Aptamer Requires Antiparallel Topology of the Quadruplex Core. Svetlova J, Sardushkin M, Kolganova N, Timofeev E. Biomolecules 11 1332 (2021)
  52. Solution structure of a thrombin binding aptamer complex with a non-planar platinum(ii) compound. Zhu BC, He J, Xia XY, Jiang J, Liu W, Liu LY, Liang BB, Yao HG, Ke Z, Xia W, Mao ZW. Chem Sci 13 8371-8379 (2022)
  53. Structuring polarity-inverted TBA to G-quadruplex for selective recognition of planarity of natural isoquinoline alkaloids. Zhou Y, Yu Y, Gao L, Fei Y, Ye T, Li Q, Zhou X, Gan N, Shao Y. Analyst 143 4907-4914 (2018)
  54. The Influence of Chirality on the β-Amino-Acid Naphthalenediimides/G-Quadruplex DNA Interaction. Clowes SR, Ali Y, Astley OR, Răsădean DM, Pantoş GD. Molecules 28 7291 (2023)
  55. The role of DNA nanostructures in the catalytic properties of an allosterically regulated protease. Kosinski R, Perez JM, Schöneweiß EC, Ruiz-Blanco YB, Ponzo I, Bravo-Rodriguez K, Erkelenz M, Schlücker S, Uhlenbrock G, Sanchez-Garcia E, Saccà B. Sci Adv 8 eabk0425 (2022)
  56. Unraveling Determinants of Affinity Enhancement in Dimeric Aptamers for a Dimeric Protein. Manochehry S, McConnell EM, Li Y. Sci Rep 9 17824 (2019)