Hi-Fi SELEX: A high-fidelity digital-PCR based therapeutic aptamer discovery platform

Biotechnology and Bioengineering

Volumn 112, Issue 8, 2015, Pages 1506-1522

  Ouellet, Eric ^a,b   Foley, Jonathan H ^b   Conway, Edward M ^b   Haynes, Charles ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Aptamer; DNA; Oligonucleotide; RNA; SELEX; Therapeutic

Indexed keywords

BINDING ENERGY; DEHALOGENATION; DIGITAL LIBRARIES; DISSOCIATION; DNA; FIXED PLATFORMS; NUCLEIC ACIDS; OLIGONUCLEOTIDES; RNA;

APTAMERS; EQUILIBRIUM DISSOCIATION CONSTANT; FUNCTIONAL DIVERSITY; SELEX; STOICHIOMETRIC CONVERSION; SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENTS; THERAPEUTIC; THERAPEUTIC ACTIVITY;

POLYMERASE CHAIN REACTION;

APTAMER; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 9A; COMPLEMENT FACTOR D; RNA; SINGLE STRANDED DNA; THROMBIN; PROTEIN BINDING;

ADSORPTION; ARTICLE; COMBINATORIAL CHEMISTRY; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DNA LIBRARY; HIGH FIDELITY SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENT; HUMAN; IONIC STRENGTH; ISOTHERMAL TITRATION CALORIMETRY; MICROWELL PLATE; MOLECULAR LIBRARY; NUCLEOPHILICITY; POLYMERASE CHAIN REACTION; RNA LIBRARY; STEREOSPECIFICITY; STOICHIOMETRY; DRUG DEVELOPMENT; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES; SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENT APTAMER TECHNIQUE;

APTAMERS, NUCLEOTIDE; COMPLEMENT FACTOR D; DRUG DISCOVERY; FACTOR IXA; FACTOR X; HUMANS; POLYMERASE CHAIN REACTION; PROTEIN BINDING; SELEX APTAMER TECHNIQUE; THROMBIN;

EID: 84932195434     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.25581     Document Type: Article

References (78)

1. Ajikumar PK, Ng JK, Tang YC, Lee JY, Stephanopoulos G, Too HP. 2007. Carboxyl-terminated dendrimer-coated bioactive interface for protein microarray: high-sensitivity detection of antigen in complex biological samples. Langmuir 23(10):5670-5677.
2. Arend WP, Mehta G, Antonioli AH, Takahashi M, Takahashi K, Stahl GL, Holers VM, Banda NK. 2013. Roles of Adipocytes and Fibroblasts in Activation of the Alternative Pathway of Complement in Inflammatory Arthritis in Mice. J Immunol 190(12):6423-6433.
3. Avci-Adali M, Paul A, Wilhelm N, Ziemer G, Wendel HP. 2009. Upgrading SELEX technology by using lambda exonuclease digestion for single-stranded DNA generation. Molecules 15(1):1-11.
4. Ayel E, Escudé C. 2010. In vitro selection of oligonucleotides that bind double-stranded DNA in the presence of triplex-stabilizing agents. Nucl Acids Res 38(5):e31.
5. Baker M. 2012. Digital PCR hits its stride. Nat Methods 9(6):541-544.
6. Berezovski M, Drabovich A, Krylova SM, Musheev M, Okhonin V, Petrov A, Krylov SN. 2005. Nonequilibrium Capillary Electrophoresis of Equilibrium Mixtures: A Universal Tool for Development of Aptamers. J Am Chem Soc 127(9):3165-3171.
7. Berezovski MV, Musheev MU, Drabovich AP, Jitkova JV, Krylov SN. 2006. Non-SELEX: selection of aptamers without intermediate amplification of candidate oligonucleotides. Nat Protocols 1(3):1359-1369.
8. Bock LC, Griffin LC, Latham JA, Vermaas EH, Toole JJ. 1992. Selection of single-stranded DNA molecules that bind and inhibit human thrombin. Nature 355(6360):564-566.
9. Britten RJ, Kohne DE. 1968. Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science 161(3841):529-540.
10. Burke DH, Scates L, Andrews K, Gold L. 1996. Bent Pseudoknots and Novel RNA Inhibitors of Type 1 Human Immunodeficiency Virus (HIV-1) Reverse Transcriptase. J Mol Biol 264(4):650-666.
11. Cattani-Scholz A, Pedone D, Blobner F, Abstreiter G, Schwartz J, Tornow M, Andruzzi L. 2009. PNA-PEG modified silicon platforms as functional bio-interfaces for applications in DNA microarrays and biosensors. Biomacromolecules 10(3):489-496.
12. Chen C-hB, Chernis GA, Hoang VQ, Landgraf R. 2003. Inhibition of heregulin signaling by an aptamer that preferentially binds to the oligomeric form of human epidermal growth factor receptor-3. Proc Natl Acad Sci 100(16):9226-9231.
13. Chen A, Kozak D, Battersby BJ, Forrest RM, Scholler N, Urban N, Trau M. 2009. Antifouling surface layers for improved signal-to-noise of particle-based immunoassays. Langmuir 25(23):13510-13515.
14. Cho M, Soo Oh S, Nie J, Stewart R, Eisenstein M, Chambers J, Marth JD, Walker F, Thomson JA, Soh HT. 2013. Quantitative selection and parallel characterization of aptamers. Proc Natl Acad Sci 110(46):p 18460-18465.
15. Cho M, Xiao Y, Nie J, Stewart R, Csordas AT, Oh SS, Thomson JA, Soh HT. 2010. Quantitative selection of DNA aptamers through microfluidic selection and high-throughput sequencing. Proc Natl Acad Sci 107(35):15373-15378.
16. Civit L, Fragoso A, O'Sullivan CK. 2012. Evaluation of techniques for generation of single-stranded DNA for quantitative detection. Anal Biochem 431(2):132-138.
17. Croy JE, Fast JL, Grimm NE, Wuttke DS. 2008. Deciphering the mechanism of thermodynamic accommodation of telomeric oligonucleotide sequences by the Schizosaccharomyces pombe protection of telomeres 1 (Pot1pN) protein. Biochemistry 47(15):4345-4358.
18. Dey AK, Griffiths C, Lea SM, James W. 2005. Structural characterization of an anti-gp120 RNA aptamer that neutralizes R5 strains of HIV-1. RNA 11(6):873-884.
19. Dragan AI, Casas-Finet JR, Bishop ES, Strouse RJ, Schenerman MA, Geddes CD. 2010. Characterization of PicoGreen Interaction with dsDNA and the Origin of Its Fluorescence Enhancement upon Binding. Biophys J 99(9):3010-3019.
20. Dwight ZL, Palais R, Wittwer CT. 2012. UAnalyze: web-based high-resolution DNA melting analysis with comparison to thermodynamic predictions. IEEE/ACM Trans Comput Biol Bioinform 9(6):1805-1811.
21. Ellington AD, Szostak JW. 1990. In vitro selection of RNA molecules that bind specific ligands. Nature 346(6287):818-822.
22. Gong P, Grainger DW. 2007. Nonfouling surfaces: a review of principles and applications for microarray capture assay designs. Methods Mol Biol 381:59-92.
23. Gopinath SC. 2007. Methods developed for SELEX. Anal Bioanal Chem 387(1):171-182.
24. Heyries KA, Tropini C, VanInsberghe M, Doolin C, Petriv OI, Singhal A, Leung K, Hughesman CB, Hansen CL. 2011. Megapixel digital PCR. Nat Methods 8(8):649-651.
25. Hindson BJ, Ness KD, Masquelier DA, Belgrader P, Heredia NJ, Makarewicz AJ, Bright IJ, Lucero MY, Hiddessen AL, Legler TC, Legler TC, Kitano TK, Hodel MR, Petersen JF, Wyatt PW, Steenblock ER, Shah PH, Bousse LJ, Troup CB, Mellen JC, Wittmann DK, Erndt NG, Cauley TH, Koehler RT, So AP, Dube S, Rose KA, Montesclaros L, Wang SL, Stumbo DP, Hodges SP, Romine S, Milanovich FP, White HE, Regan JF, Karlin-Neumann GA, Hindson CM, Saxonov S, Colston BW. 2011. High-Throughput Droplet Digital PCR System for Absolute Quantitation of DNA Copy Number. Anal Chem 83(22):8604-8610.
26. Hünniger T, Wessels H, Fischer C, Paschke-Kratzin A, Fischer M. 2014. Just in time-selection: A rapid semiautomated SELEX of DNA aptamers using magnetic separation and Beaming. Anal Chem 86(21):10940-10947.
27. Irvine D, Tuerk C, Gold L. 1991. Selexion: Systematic evolution of ligands by exponential enrichment with integrated optimization by non-linear analysis. J Mol Biol 222(3):739-761.
28. Jacobsen MH, Koch T. US Patent, assignee. 2000. Method of photochemical immobilization of ligands using quinones. US Patent, patent 6, 033, 784.
29. Janssen KPF, Knez K, Pollet J, Roberts SJ, Schrooten J, Lammertyn J. 2011. Assay design considerations for use of affinity aptamer amplification in ultra-sensitive protein assays using capillary electrophoresis. Anal Methods 3(9):2156-2159.
30. Jensen MA, Straus N. 1993. Effect of PCR conditions on the formation of heteroduplex and single-stranded DNA products in the amplification of bacterial ribosomal DNA spacer regions. Genome Res 3(3):186-194.
31. Jensen SP, Rasmussen SE, Jakobsen MH. 1996. Photochemical Coupling of Peptides to Polystyrene MicroWell Plates. Innovations & Perspectives in Solid Phase Synthesis & Combinatorial Chemical Libraries 419-422.
32. Jha P, Bora PS, Bora NS. 2007. The role of complement system in ocular diseases including uveitis and macular degeneration. Mol Immunol 44(16):3901-3908.
33. Jolma A, Kivioja T, Toivonen J, Cheng L, Wei G, Enge M, Taipale M, Vaquerizas JM, Yan J, Sillanpää MJ. 2010. Multiplexed massively parallel SELEX for characterization of human transcription factor binding specificities. Genome Res 20(6):861-873.
34. Jones LA, Clancy LE, Rawlinson WD, White PA. 2006. High-affinity aptamers to subtype 3a hepatitis C virus polymerase display genotypic specificity. Antimicrob Agents Chemother 50(9):3019-3027.
35. Kavanagh D, Goodship THJ. 2011. Atypical hemolytic uremic syndrome, genetic basis, and clinical manifestations. ASH Education Program Book 2011(1):15-20.
36. Kikuchi K, Umehara T, Fukuda K, Hwang J, Kuno A, Hasegawa T, Nishikawa S. 2003. RNA Aptamers Targeted to Domain II of Hepatitis C Virus IRES That Bind to Its Apical Loop Region. J Biochem 133(3):263-270.
37. Kizhakkedathu JN, Creagh AL, Shenoi RA, Rossi NAA, Brooks DE, Chan T, Lam J, Dandepally SR, Haynes CA. 2010. High Molecular Weight Polyglycerol-Based Multivalent Mannose Conjugates. Biomacromolecules 11(10):2567-2575.
38. Kong HY, Byun J. 2013. Nucleic Acid aptamers: new methods for selection, stabilization, and application in biomedical science. Biomol Ther (Seoul) 21(6):423-434.
39. Kulbachinskiy AV. 2007. Methods for selection of aptamers to protein targets. Biochemistry (Mosc) 72(13):1505-1518.
40. Lai BFL, Creagh AL, Janzen J, Haynes CA, Brooks DE, Kizhakkedathu JN. 2010. The induction of thrombus generation on nanostructured neutral polymer brush surfaces. Biomaterials 31(26):6710-6718.
41. Latulippe DR, Szeto K, Ozer A, Duarte FM, Kelly CV, Pagano JM, White BS, Shalloway D, Lis JT, Craighead HG. 2013. Multiplexed microcolumn-based process for efficient selection of RNA aptamers. Anal Chem 85(6):3417-3424.
42. Lee G, Yoo J, Leslie BJ, Ha T. 2011. Single-molecule analysis reveals three phases of DNA degradation by an exonuclease. Nat Chem Biol 7(6):367-374.
43. Levine HA, Nilsen-Hamilton M. 2007. A mathematical analysis of SELEX. Comput Biol Chem 31(1):11-35.
44. Little JW. 1967. An Exonuclease Induced by Bacteriophage λ: II. Nature of the enzymatic reaction. J Biol Chem 242(4):679-686.
45. Lou X, Qian J, Xiao Y, Viel L, Gerdon AE, Lagally ET, Atzberger P, Tarasow TM, Heeger AJ, Soh HT. 2009. Micromagnetic selection of aptamers in microfluidic channels. Proc Natl Acad Sci 106(9):2989-2994.
46. Lyon E, Millson A, Lowery MC, Woods R, Wittwer CT. 2001. Quantification of HER2/neu gene amplification by competitive PCR using fluorescent melting curve analysis. Clin Chem 47(5):844-851.
47. Mencin N, Šmuc T, Vraničar M, Mavri J, Hren M, Galeša K, Krkoč P, Ulrich H, Šolar B. 2014. Optimization of SELEX: Comparison of different methods for monitoring the progress of in vitro selection of aptamers. J Pharm Biomed Anal 91:151-159.
48. Mendonsa SD, Bowser MT. 2004. In vitro evolution of functional DNA using capillary electrophoresis. J Am Chem Soc 126(1):20-21.
49. Meyer S, Maufort JP, Nie J, Stewart R, McIntosh BE, Conti LR, Ahmad KM, Soh HT, Thomson JA. 2013. Development of an efficient targeted cell-SELEX procedure for DNA aptamer reagents. PLoS ONE 8(8):e71798.
50. Musheev MU, Krylov SN. 2006. Selection of aptamers by systematic evolution of ligands by exponential enrichment: addressing the polymerase chain reaction issue. Anal Chim Acta 564(1):91-96.
51. Ng EWM, Shima DT, Calias P, Cunningham ET, Guyer DR, Adamis AP. 2006. Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat Rev Drug Discov 5(2):123-132.
52. Ouellet E, Lagally ET, Cheung KC, Haynes CA. 2014. A simple method for eliminating fixed-region interference of aptamer binding during SELEX. Biotechnology 111(11):2265-2279.
53. Ozer A, White BS, Lis JT, Shalloway D. 2013. Density-dependent cooperative non-specific binding in solid-phase SELEX affinity selection. Nucleic Acids Res 41(14):7167-7175.
54. Palais RA, Wittwer CT. US Patent, assignee. 2011. Melting curve analysis with exponential background subtraction patent 8 068 992
55. Pollard J, Bell SD, Ellington AD. 2001. Design, Synthesis, and Amplification of DNA Pools for Construction of Combinatorial Pools and Libraries. In: Taylor GP, editor. Current Protocols in Molecular Biology. New York, NY: John Wiley & Sons, Inc. p 24.2.1-24.2.24.
56. Poncin-Epaillard F, Vrlinic T, Debarnot D, Mozetic M, Coudreuse A, Legeay G, El Moualij B, Zorzi W. 2012. Surface Treatment of Polymeric Materials Controlling the Adhesion of Biomolecules. J Funct Biomater 3(3):528-543.
57. Qian J, Lou X, Zhang Y, Xiao Y, Soh HT. 2009. Generation of Highly Specific Aptamers via Micromagnetic Selection. Anal Chem 81(13):5490-5495.
58. Robertson DL, Joyce GF. 1990. Selection in vitro of an RNA enzyme that specifically cleaves single-stranded DNA. Nature 344(6265):467-468.
59. Rouah-Martin E, Mehta J, van Dorst B, de Saeger S, Dubruel P, Maes B, Lemiere F, Goormaghtigh E, Daems D, Herrebout W, et al. 2012. Aptamer-Based Molecular Recognition of Lysergamine, Metergoline and Small Ergot Alkaloids. Int J Mol Sci 13(12):17138-17159.
60. Rusconi CP, Roberts JD, Pitoc GA, Nimjee SM, White RR, Quick G, Jr, Scardino E, Fay WP, Sullenger BA. 2004. Antidote-mediated control of an anticoagulant aptamer in vivo. Nat Biotech 22(11):1423-1428.
61. Schlapak R, Pammer P, Armitage D, Zhu R, Hinterdorfer P, Vaupel M, Frühwirth T, Howorka S. 2005. Glass Surfaces Grafted with High-Density Poly(ethylene glycol) as Substrates for DNA Oligonucleotide Microarrays. Langmuir 22(1):277-285.
62. Schütze T, Wilhelm B, Greiner N, Braun H, Peter F, Mörl M, Erdmann VA, Lehrach H, Konthur Z, Menger M, et al. 2011. Probing the SELEX Process with Next-Generation Sequencing. PLoS ONE 6(12):e29604.
63. Sriprakash KS, Lundh N, Huh MM-O, Radding CM. 1975. The specificity of lambda exonuclease. Interactions with single-stranded DNA. J Biol Chem 250(14):5438-5445.
64. Stoltenburg R, Nikolaus N, Strehlitz B. 2012. Capture-SELEX: Selection of DNA Aptamers for Aminoglycoside Antibiotics. J Anal Method Chem 2012:14.
65. Stoltenburg R, Reinemann C, Strehlitz B. 2005. FluMag-SELEX as an advantageous method for DNA aptamer selection. Anal Bioanal Chem 383(1):83-91.
66. Stoltenburg R, Reinemann C, Strehlitz B. 2007. SELEX - A (r) evolutionary method to generate high-affinity nucleic acid ligands. Biomol Eng 24(4):381-403.
67. Tasset DM, Kubik MF, Steiner W. 1997. Oligonucleotide inhibitors of human thrombin that bind distinct epitopes. J Mol Biol 272(5):688-698.
68. Thompson JR, Marcelino LA, Polz MF. 2002. Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Nucl Acids Res 30(9):2083-2088.
69. Thurman JM, Holers VM. 2006. The Central Role of the Alternative Complement Pathway in Human Disease. J Immunol 176(3):1305-1310.
70. Tuerk C, Gold L. 1990. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249(4968):505-510.
71. Vanbrabant J, Leirs K, Vanschoenbeek K, Lammertyn J, Michiels L. 2014. ReMelting curve analysis as a tool for enrichment monitoring in the SELEX process. Analyst 139(3):589-595.
72. Vant-Hull B, Payano-Baez A, Davis RH, Gold L. 1998. The mathematics of SELEX against complex targets. J Mol Biol 278(3):579-597.
73. Wang C, Yang G, Luo Z, Ding H. 2009. In vitro selection of high-affinity DNA aptamers for streptavidin. Acta Biochim Biophys Sin 41(4):335-340.
74. Wang J, Rudzinski JF, Gong Q, Soh HT, Atzberger PJ. 2012. Influence of target concentration and background binding on in vitro selection of affinity reagents. PLoS ONE 7(8):e43940.
75. Weng C-H, Huang C-J, Lee G-B. 2012. Screening of aptamers on microfluidic systems for clinical applications. Sensors 12(7):9514-9529.
76. Wilson R, Bourne C, Chaudhuri RR, Gregory R, Kenny J, Cossins A. 2014. Single-step selection of bivalent aptamers validated by comparison with SELEX using high-throughput sequencing. PLoS ONE 9(6):e100572.
77. Yufa R, Krylova SM, Bruce C, Bagg EA, Schofield CJ, Krylov SN. 2014. Emulsion PCR significantly improves nonequilibrium capillary electrophoresis of equilibrium mixtures-based aptamer selection: Allowing for efficient and rapid selection of aptamer to unmodified ABH2 protein. Anal Chem 87(2):1411-1419.
78. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31(13):3406-3415.