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Lessons Learned.Pdf Biotechnology Advances 37 (2019) 28–50 Contents lists available at ScienceDirect Biotechnology Advances journal homepage: www.elsevier.com/locate/biotechadv Research review paper Three decades of nucleic acid aptamer technologies: Lessons learned, T progress and opportunities on aptamer development ⁎ Tao Wanga,b,c,1, Changying Chenc,1, Leon M. Larchera, Roberto A. Barreroa, Rakesh N. Veedua,b, a Centre for Comparative Genomics, Murdoch University, Perth 6150, Australia b Perron Institute for Neurological and Translational Science, Perth 6009, Australia c School of Nursing, Zhengzhou University & Nursing Department, The First Affiliated Hospital of Zheng Zhou University, Zhengzhou 450001, China ARTICLE INFO ABSTRACT Keywords: Aptamers are short single-stranded nucleic acid sequences capable of binding to target molecules in a way SELEX similar to antibodies. Due to various advantages such as prolonged shelf life, low batch to batch variation, low/ Aptamer no immunogenicity, freedom to incorporate chemical modification for enhanced stability and targeting capacity, SELEX library aptamers quickly found their potential in diverse applications ranging from therapy, drug delivery, diagnosis, Synthetic genetic polymers and functional genomics to bio-sensing. Aptamers are generated by a process called SELEX. However, the current Single-strand DNA preparation overall success rate of SELEX is far from being satisfactory, and still presents a major obstacle for aptamer-based PCR bias research and application. The need for an efficient selection strategy consisting of defined procedures todeal with a wide variety of targets is significantly important. In this work, by analyzing key aspects of SELEX in- cluding initial library design, target preparation, PCR optimization, and single strand DNA separation, we provide a comprehensive analysis of individual steps to facilitate researchers intending to develop personalized protocols to address many of the obstacles in SELEX. In addition, this review provides suggestions and opinions for future aptamer development procedures to address the concerns on key SELEX steps, and post-SELEX modifications. 1. Introduction quickly found their way in diverse applications ranging from therapy, drug delivery, diagnosis, and functional genomics to bio-sensing First introduced in 1990 (Ellington and Szostak, 1990; Tuerk and (AlShamaileh et al., 2017; Khan et al., 2018; Shigdar et al., 2013a; Gold, 1990), aptamers are short synthetic single-stranded (ss) nucleic Tapsin et al., 2018). acid sequences that can bind to a broad range of targets including metal Aptamers are generally developed in vitro by a very defined iterative ions, chemical compounds, proteins, cells and whole micro-organisms. procedure known as Systematic Evolution of Ligands by Exponential As a class of affinity ligands, aptamers display some advantages over enrichment (SELEX) (Tuerk and Gold, 1990). The originally reported traditional antibodies such as prolonged shelf life, low batch to batch SELEX procedures is, however, time and labor consuming. Over the past variation, low/no immunogenicity, and the flexibility to incorporate three decades, by adaption and integration of progresses in material chemical modifications for enhanced stability and targeting affinity sciences and analytical techniques, various SELEX variations have been (Wang et al., 2015). Consequently, over the past few decades, aptamers reported in an attempt to either reduce processing time (e.g. CE-SELEX Abbreviations: SELEX, Systematic Evolution of Ligands by Exponential enrichment; AEGIS, artificially expanded genetic information system; AFM, atomic force microscope; AON, antisense oligonucleotide; CMACS, continuous-flow magnetic activated chips; Ds, 7-(2-thienyl) imidazo [4, 5-b] pyridine; EMSA, electrophoretic mobility shift assay; ECEEM, equilibrium capillary electrophoresis of equilibrium mixtures; ePCR, Emulsion PCR; FACS, fluorescence-activated cell sorter; FITC, Fluorescein isothiocyanate; Flu-Mag, Fluorescence-Magnetic; LNA, locked nucleic acid; MARAS, Magnetic-Assisted Rapid Aptamer Selection; NA, Nucleic acid; NRR, non-homologous random recombination; NGS, next generation sequencing; P, 2-amino-8-(10-β-D-2-deoxyribofuranosyl)-imidazo[1,2-a]-1,3,5-triazin-4(8H)-one; PEG, polyethylene glycol; Px, 2-nitro-4- propynylpyrrole; RAPID, RNA aptamer Isolation via dual-cycles; SweepCE, Sweeping capillary electrophoresis; SOMAmer, Slow off-rate modified aptamer; ssDNA, single-stranded DNA; TECS, target expressed on the cell surface; Thioaptamers, Thiophosphate-modified aptamers;UV- LEDIF, ultraviolet light-emitting diode-induced native fluorescence; Z, 6-amino-5-nitro-3-(1'- β-D-2'-deoxyribofur-anosyl)-2(1H)-pyridone; μFFE, Micro Free Flow Electrophoresis; 2′-FANA, 2'-fluoroarabino nucleic acid ⁎ Corresponding author at: Centre for Comparative Genomics, Murdoch University, Building 390 Discovery Drive, Perth, Western Australia 6150, Australia E-mail address: [email protected] (R.N. Veedu). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.biotechadv.2018.11.001 Received 2 August 2018; Received in revised form 28 October 2018; Accepted 4 November 2018 Available online 05 November 2018 0734-9750/ © 2018 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). T. Wang et al. Biotechnology Advances 37 (2019) 28–50 (Yang and Bowser, 2013), Flu-Mag SELEX (Stoltenburg et al., 2005), in SELEX since very early stages of aptamer development (Ellington and silico SELEX (Rabal et al., 2016)), generate aptamers with novel designs Szostak, 1992), RNA libraries were preferentially used in the majority and functions (e.g. μFFE-SELEX (Jing and Bowser, 2011), Capture- of the early SELEX protocols - based on the belief that RNA could fold SELEX (Istamboulie et al., 2017)), or increase the process throughput into more functional motifs and result in higher affinity binders (Cheng (e.g. Sweep-CE-SELEX (Okhonin et al., 2004)). Today, some groups can et al., 2001). However, accumulating evidences suggest that ssDNA reduce the time for aptamer development from months required for exhibits comparable propensity for forming intricate tertiary structures conventional SELEX to several hours (Lokesh et al., 2017; Martin et al., with that of RNA. This finding is important for aptamer related work. 2015; Zhuo et al., 2017). Furthermore, a recently developed computer Evidently, in terms of aptamer development and subsequent applica- supported in silico assay promises to predict an aptamer structure even tion, DNA aptamers show advantages over their RNA counterparts before SELEX is conducted (Ahirwar et al., 2016). Stemming from this, (Lakhin et al., 2013). Firstly, DNA is more chemically and biologically aptamers such as the hydrophobic SOMAmers (Eid et al., 2015), stable, which makes both selection and application easier. This is thioaptamers (Volk and Lokesh, 2017), and X-Aptamers (Lokesh et al., especially true when microarray platforms are applied for high 2017) have been developed. NOX-A12, a nuclease resistant L-nucleic throughput SELEX; secondly, DNA-based SELEX is more cost and time- acid aptamer (Vater and Klussmann, 2015), recently entered Phase 1/2 effective, as an extra reverse transcription step essential for RNASELEX clinical trial for multiple oncology indications (ClinicalTrials.gov is not required; thirdly, from the perspective of commercialization, Identifier: NCT03168139). Progress in nucleic acid chemistry andse- DNA is easier to synthesize and is more robust than RNA in terms of lection strategies significantly contribute to the commercialization and shelf life (Lakhin et al., 2013). Accordingly, DNA libraries are being clinical translation of aptamers. However, it is worth mentioning that used more frequently in recent SELEX studies. By 2007, DNA re- the number of aptamers showing strong binding capacity and specificity presented half of the performed SELEX libraries. And more than 85% of is still limited (Baird, 2010). Improving the current SELEX procedure the reported aptamers in 2013 were developed using DNA. Today, DNA and developing more aptamers with high binding capacity and speci- aptamers represent almost all of the products provided by commercial ficity remains a major hurdle for aptamer related basic and applied aptamer developers (Darmostuk et al., 2015). As a special variation of studies, and the knowledge accumulated over the last three decades SELEX, genomic SELEX is very different from common SELEX by em- would be of significant benefit in developing the successful individual ploying genomic DNA (double strand), genome encoded RNA, and SELEX procedure. transcriptomic total RNA as starting libraries (Cheung et al., 2013). SELEX is a typical multidisciplinary procedure related to different Genomic SELEX is mainly for functional studies aiming to identify fields such as molecular biology, nucleic acid chemistry, material sci- regulatory domains in a genome such as DNA sequences recognized by ence, and bioinformatics to develop affinity ligands against a vast transcription factors, RNA fragments recognized by splicing factors, variety of targets (Blind and Blank, 2015). As such, a standard SELEX RNA polymerases, ribosomes or other components of the gene expres- protocol suitable for all experimental settings may not exist (Svobodova sion machinery (Vorobyeva et al., 2018). Since RNA especially non- et al., 2012). To identify aptamers for a specific
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