Optimization of Gonyautoxin1/4-Binding G-Quadruplex Aptamers by Label-Free Surface-Enhanced Raman Spectroscopy
Abstract
:1. Introduction
2. Results and Discussion
2.1. Analysis of the SERS Spectrum of Wild-Type Aptamer GO18
2.2. Interaction between Wild-Type Aptamer GO18 and GTX1/4
2.2.1. SERS
2.2.2. DCOS
2.2.3. MD Simulations
2.3. Guide Mutation and Truncation Optimization of Aptamers
2.3.1. Optimization of Mutation
2.3.2. Optimization of Truncation
3. Materials and Methods
3.1. Reagents
3.2. Preparation of Ag IMNPs
3.3. SERS Detection
3.4. MD Simulation
3.5. Circular Dichroism
3.6. Determination of Affinity of MST
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Tuerk, C.; Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 1990, 249, 505–510. [Google Scholar] [CrossRef] [PubMed]
- Ellington, A.D.; Szostak, J.K. In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346, 818–822. [Google Scholar] [CrossRef] [PubMed]
- Djordjevic, M. SELEX experiments: New prospects, applications and data analysis in inferring regulatory pathways. Biomol. Eng. 2007, 24, 179–189. [Google Scholar] [CrossRef] [PubMed]
- Gao, S.; Zheng, X.; Jiao, B.; Wang, L. Post-SELEX optimization of aptamers. Anal. Bioanal. Chem. 2016, 408, 4567–4573. [Google Scholar] [CrossRef] [PubMed]
- Huppert, J.L. Four-stranded nucleic acids: Structure, function and targeting of G-quadruplexes. Chem. Soc. Rev. 2008, 37, 1375–1384. [Google Scholar] [CrossRef]
- Rhodes, D.; Lipps, H.J. G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 2015, 43, 8627–8637. [Google Scholar] [CrossRef]
- Burge, S.; Parkinson, G.N.; Hazel, P.; Todd, A.K.; Neidle, S. Quadruplex DNA: Sequence, topology and structure. Nucleic Acids Res. 2006, 34, 5402–5415. [Google Scholar] [CrossRef]
- Huppert, J.L.; Balasubramanian, S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res. 2005, 33, 2908–2916. [Google Scholar] [CrossRef]
- Biffi, G.; Tannahill, D.; Mccafferty, J.; Balasubramanian, S. Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem. 2013, 5, 182–186. [Google Scholar] [CrossRef]
- Siddiqui-Jain, A.; Grand, C.L.; Bearss, D.J.; Hurley, L.H. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl. Acad. Sci. USA 2002, 99, 11593–11598. [Google Scholar] [CrossRef] [Green Version]
- Balasubramanian, S.; Hurley, L.H.; Neidle, S. Targeting G-quadruplexes in gene promoters: A novel anticancer strategy? Nat. Rev. Drug Discov. 2011, 10, 261–275. [Google Scholar] [CrossRef] [PubMed]
- Kwok, C.K.; Merrick, C.J. G-Quadruplexes: Prediction, characterization, and biological application. Trends Biotechnol. 2017, 35, 997–1013. [Google Scholar] [CrossRef] [PubMed]
- Cammas, A.; Millevoi, S. RNA G-quadruplexes: Emerging mechanisms in disease. Nucleic Acids Res. 2017, 45, 1584–1595. [Google Scholar] [CrossRef] [PubMed]
- Rosenberg, J.E.; Bambury, R.M.; Van Allen, E.M.; Drabkin, H.A.; Lara, P.N.; Harzstark, A.L.; Wagle, N.; Figlin, R.A.; Smith, G.W.; Garraway, L.A.; et al. A phase II trial of AS1411 (a novel nucleolin-targeted DNA aptamer) in metastatic renal cell carcinoma. Investig. New Drugs 2014, 32, 178–187. [Google Scholar] [CrossRef]
- Qin, Y.; Rezler, E.M.; Gokhale, V.; Sun, D.; Hurley, L.H. Characterization of the G-quadruplexes in the duplex nuclease hypersensitive element of the PDGF-A promoter and modulation of PDGF-A promoter activity by TMPyP4. Nucleic Acids Res. 2007, 35, 7698–7713. [Google Scholar] [CrossRef]
- Kang, H.J.; Park, H.J. Novel molecular mechanism for actinomycin D activity as an oncogenic promoter G-quadruplex binder. Biochemistry 2009, 48, 7392–7398. [Google Scholar] [CrossRef]
- Tauchi, T.; Shin-Ya, K.; Sashida, G.; Sumi, M.; Okabe, S.; Ohyashiki, J.H.; Ohyashiki, K. Telomerase inhibition with a novel G-quadruplex-interactive agent, telomestatin: In vitro and in vivo studies in acute leukemia. Oncogene 2006, 25, 5719–5725. [Google Scholar] [CrossRef]
- Ruttkay-Nedecky, B.; Kudr, J.; Nejdl, L.; Maskova, D.; Kizek, R.; Adam, V. G-quadruplexes as sensing probes. Molecules 2013, 18, 14760–14779. [Google Scholar] [CrossRef]
- Liu, Z.; Li, W.; Nie, Z.; Peng, F.; Huang, Y.; Yao, S. Randomly arrayed G-quadruplexes for label-free and real-time assay of enzyme activity. Chem. Commun. 2014, 50, 6875–6878. [Google Scholar] [CrossRef]
- Wang, H.; Li, Y.; Zhao, K.; Chen, S.; Wang, Q.; Lin, B.; Nie, Z.; Yao, S. G-quadruplex-based fluorometric biosensor for label-free and homogenous detection of protein acetylation-related enzymes activities. Biosens. Bioelectron. 2017, 91, 400–407. [Google Scholar] [CrossRef]
- Warner, K.D.; Chen, M.C.; Song, W.; Strack, R.L.; Thorn, A.; Jaffrey, S.R.; Ferre-D’amare, A.R. Structural basis for activity of highly efficient RNA mimics of green fluorescent protein. Nat. Struct. Mol. Biol. 2014, 21, 658–663. [Google Scholar] [CrossRef] [PubMed]
- Feng, G.; Luo, C.; Yi, H.; Yuan, L.; Lin, B.; Luo, X.; Hu, X.; Wang, H.; Lei, C.; Nie, Z.; et al. DNA mimics of red fluorescent proteins (RFP) based on G-quadruplex-confined synthetic RFP chromophores. Nucleic Acids Res. 2017, 45, 10380–10392. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Yang, D.; Schluesener, H.J.; Zhang, Z. Advances in SELEX and application of aptamers in the central nervous system. Biomol. Eng. 2007, 24, 583–592. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, V.T.; Kwon, Y.S.; Kim, J.H.; Gu, M.B. Multiple GO-SELEX for efficient screening of flexible aptamers. Chem. Commun. 2014, 50, 10513–10516. [Google Scholar] [CrossRef]
- Ahmad Raston, N.H.; Gu, M.B. Highly amplified detection of visceral adipose tissue-derived serpin (vaspin) using a cognate aptamer duo. Biosens. Bioelectron. 2015, 70, 261–267. [Google Scholar] [CrossRef] [PubMed]
- Gao, S.; Hu, B.; Zheng, X.; Cao, Y.; Liu, D.; Sun, M.; Jiao, B.; Wang, L. Gonyautoxin 1/4 aptamers with high-affinity and high-specificity: From efficient selection to aptasensor application. Biosens. Bioelectron. 2016, 79, 938–944. [Google Scholar] [CrossRef]
- Gao, S.; Zheng, X.; Tang, Y.; Cheng, Y.; Hu, X.; Wu, J. Development of a novel fluorescently-labeled aptamer structure-switching assay for sensitive and rapid detection of gliotoxin. Anal. Chem. 2019, 91, 1610–1618. [Google Scholar] [CrossRef]
- Darmostuk, M.; Rimpelova, S.; Gbelcova, H.; Ruml, T. Current approaches in SELEX: An update to aptamer selection technology. Biotechnol. Adv. 2015, 33, 1141–1161. [Google Scholar] [CrossRef]
- Bullock, T.L.; Sherlin, L.D.; Perona, J.J. Tertiary core rearrangements in a tight bindingtransfer RNA aptamer. Nat. Struct. Mol. Biol. 2000, 7, 497–504. [Google Scholar] [CrossRef]
- Wang, R.E.; Wu, H.; Niu, Y.; Cai, J. Improving the stability of aptamers by chemical modification. Curr. Med. Chem. 2011, 18, 4126–4138. [Google Scholar] [CrossRef]
- Zheng, X.; Hu, B.; Gao, S.X.; Liu, D.J.; Sun, M.J.; Jiao, B.H.; Wang, L.H. A saxitoxin-binding aptamer with higher affinity and inhibitory activity optimized by rational site-directed mutagenesis and truncation. Toxicon 2015, 101, 41–47. [Google Scholar] [CrossRef] [PubMed]
- Xu, G.; Zhao, J.; Liu, N.; Yang, M.; Zhao, Q.; Li, C.; Liu, M. Structure-guided post-SELEX optimization of an ochratoxin A aptamer. Nucleic Acids Res. 2019, 47, 5963–5972. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Chen, C.; Larcher, L.M.; Barrero, R.A.; Veedu, R.N. Three decades of nucleic acid aptamer technologies: Lessons learned, progress and opportunities on aptamer development. Biotechnol. Adv. 2019, 37, 28–50. [Google Scholar] [CrossRef] [PubMed]
- Kuai, H.; Zhao, Z.; Mo, L.; Liu, H.; Hu, X.; Fu, T.; Zhang, X.; Tan, W. Circular bivalent aptamers enable in vivo stability and recognition. J. Am. Chem. Soc. 2017, 139, 9128–9131. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Y.; Pan, X.; Chang, J.; Niu, W.; Hou, W.; Kuai, H.; Zhao, Z.; Liu, J.; Wang, M.; Tan, W. Supramolecularly engineered circular bivalent aptamer for enhanced functional protein delivery. J. Am. Chem. Soc. 2018, 140, 6780–6784. [Google Scholar] [CrossRef]
- Pan, X.; Yang, Y.; Li, L.; Li, X.; Li, Q.; Cui, C.; Wang, B.; Kuai, H.; Jiang, J.; Tan, W. A bispecific circular aptamer tethering a built-in universal molecular tag for functional protein delivery. Chem. Sci. 2020, 11, 9648–9654. [Google Scholar] [CrossRef]
- Seenisamy, J.; Bashyam, S.; Gokhale, V.; Vankayalapati, H.; Sun, D.; Siddiqui-Jain, A.; Streiner, N.; Shin-Ya, K.; White, E.; Wilson, W.D.; et al. Design and synthesis of an expanded porphyrin that has selectivity for the c-MYC G-quadruplex structure. J. Am. Chem. Soc. 2005, 127, 2944–2959. [Google Scholar] [CrossRef]
- Pagano, B.; Mattia, C.A.; Giancola, C. Applications of isothermal titration calorimetry in biophysical studies of G-quadruplexes. Int. J. Mol. Sci. 2009, 10, 2935–2957. [Google Scholar] [CrossRef]
- Biniuri, Y.; Albada, B.; Willner, I. Probing ATP/ATP-aptamer or ATP-aptamer mutant complexes by microscale thermophoresis and molecular dynamics simulations: Discovery of an ATP-aptamer sequence of superior binding properties. J. Phys. Chem. B 2018, 122, 9102–9109. [Google Scholar] [CrossRef]
- Cui, X.; Song, M.; Liu, Y.; Yuan, Y.; Huang, Q.; Cao, Y.; Lu, F. Identifying conformational changes of aptamer binding to theophylline: A combined biolayer interferometry, surface-enhanced Raman spectroscopy, and molecular dynamics study. Talanta 2020, 217, 121073–121079. [Google Scholar] [CrossRef]
- Song, M.; Li, G.; Zhang, Q.; Liu, J.; Huang, Q. De novo post-SELEX optimization of a G-quadruplex DNA aptamer binding to marine toxin gonyautoxin 1/4. Comput. Struct. Biotechnol. J. 2020, 18, 3425–3433. [Google Scholar] [CrossRef]
- Garcia-Rico, E.; Alvarez-Puebla, R.A.; Guerrini, L. Direct surface-enhanced Raman scattering (SERS) spectroscopy of nucleic acids: From fundamental studies to real-life applications. Chem. Soc. Rev. 2018, 47, 4909–4923. [Google Scholar] [CrossRef] [PubMed]
- Graham, D.; Faulds, K. Quantitative SERRS for DNA sequence analysis. Chem. Soc. Rev. 2008, 37, 1042–1051. [Google Scholar] [CrossRef]
- Bell, S.E.J.; Sirimuthu, N.M.S. Surface-Enhanced Raman Spectroscopy (SERS) for Sub-Micromolar Detection of DNA/RNA Mononucleotides. J. Am. Chem. Soc. 2006, 128, 15580–15581. [Google Scholar] [CrossRef] [PubMed]
- Barhoumi, A.; Zhang, D.; Tam, F.; Halas, N.J. Surface-enhanced Raman spectroscopy of DNA. J. Am. Chem. Soc. 2008, 130, 5523–5529. [Google Scholar] [CrossRef] [PubMed]
- Mahajan, S.; Richardson, J.; Brown, T.; Bartlett, P.N. SERS-melting: A new method for discriminating mutations in DNA sequences. J. Am. Chem. Soc. 2008, 130, 15589–15601. [Google Scholar] [CrossRef]
- Rusciano, G.; De Luca, A.C.; Pesce, G.; Sasso, A.; Oliviero, G.; Amato, J.; Borbone, N.; D’errico, S.; Piccialli, V.; Piccialli, G.; et al. Label-free probing of G-quadruplex formation by surface-enhanced Raman scattering. Anal. Chem. 2011, 83, 6849–6855. [Google Scholar] [CrossRef]
- Papadopoulou, E.; Bell, S.E. Label-free detection of single-base mismatches in DNA by surface-enhanced Raman spectroscopy. Angew. Chem. Int. Ed. Engl. 2011, 50, 9058–9061. [Google Scholar] [CrossRef]
- Xu, L.J.; Lei, Z.C.; Li, J.; Zong, C.; Yang, C.J.; Ren, B. Label-free surface-enhanced Raman spectroscopy detection of DNA with single-base sensitivity. J. Am. Chem. Soc. 2015, 137, 5149–5154. [Google Scholar] [CrossRef]
- Guerrini, L.; Krpetic, Z.; Van Lierop, D.; Alvarez-Puebla, R.A.; Graham, D. Direct surface-enhanced Raman scattering analysis of DNA duplexes. Angew. Chem. Int. Ed. Engl. 2015, 54, 1144–1148. [Google Scholar] [CrossRef]
- Miljanic, S.; Ratkaj, M.; Matkovic, M.; Piantanida, I.; Gratteri, P.; Bazzicalupi, C. Assessment of human telomeric G-quadruplex structures using surface-enhanced Raman spectroscopy. Anal. Bioanal. Chem. 2017, 409, 2285–2295. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Han, X.; Yan, Y.; Cao, Y.; Xiang, X.; Wang, S.; Zhao, B.; Guo, X. Label-free detection of tetramolecular i-motifs by surface-enhanced Raman spectroscopy. Anal. Chem. 2018, 90, 2996–3000. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Han, X.; Zhou, S.; Yan, Y.; Xiang, X.; Zhao, B.; Guo, X. Structural features of DNA G-Quadruplexes revealed by surface-enhanced Raman spectroscopy. J. Phys. Chem. Lett. 2018, 9, 3245–3252. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Gao, T.; Xu, G.; Xiang, X.; Han, X.; Zhao, B.; Guo, X. The base pair contents and sequences of DNA double helixes differentiated by surface-enhanced Raman spectroscopy. J. Phys. Chem. Lett. 2019, 10, 3013–3018. [Google Scholar] [CrossRef] [PubMed]
- Andrinolo, D.O.; Michea, L.F.; Lagos, N. Toxic effects, pharmacokinetics and clearance of saxitoxin, a component of paralytic shellfish poison (PSP), in cats. Toxicon 1999, 37, 447–464. [Google Scholar] [CrossRef]
- Wiese, M.; D’agostino, P.M.; Mihali, T.K.; Moffitt, M.C.; Neilan, B.A. Neurotoxic alkaloids: Saxitoxin and its analogs. Mar. Drugs 2010, 8, 2185–2211. [Google Scholar] [CrossRef]
- Benevides, J.M.; Overman, S.A.; Thomas, G.J. Raman, polarized Raman and ultraviolet resonance Raman spectroscopy of nucleic acids and their complexes. J. Raman Spectrosc. 2005, 36, 279–299. [Google Scholar] [CrossRef]
- Deng, H.; Bloomfield, V.A.; Benevides, J.M.; Thomas, G.J. Dependence of the Raman signature of genomic B-DNA on nucleotide base sequence. Biopolymers 1999, 50, 656–666. [Google Scholar] [CrossRef]
- Krafft, C.; Benevides, J.M.; Thomas, G.J. Secondary structure polymorphism in Oxytricha nova telomeric DNA. Nucleic Acids Res. 2002, 30, 3981–3991. [Google Scholar] [CrossRef]
- Friedman, S.J.; Terentis, A.C. Analysis of G-quadruplex conformations using Raman and polarized Raman spectroscopy. J. Raman Spectrosc. 2016, 47, 259–268. [Google Scholar] [CrossRef]
- Palacky, J.; Vorlickova, M.; Kejnovska, I.; Mojzes, P. Polymorphism of human telomeric quadruplex structure controlled by DNA concentration: A Raman study. Nucleic Acids Res. 2013, 41, 1005–1016. [Google Scholar] [CrossRef] [PubMed]
- Jeddi, I.; Saiz, L. Three-dimensional modeling of single stranded DNA hairpins for aptamer-based biosensors. Sci. Rep. 2017, 7, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Bell, D.R.; Weber, J.K.; Yin, W.; Huynh, T.; Duan, W.; Zhou, R. In silico design and validation of high-affinity RNA aptamers targeting epithelial cellular adhesion molecule dimers. Proc. Natl. Acad. Sci. USA 2020, 117, 8486–8493. [Google Scholar] [CrossRef]
- O’hagan, M.P.; Haldar, S.; Morales, J.C.; Mulholland, A.J.; Carmengalan, M. Enhanced sampling molecular dynamics simulations correctly predict the diverse activities of a series of stiff-stilbene G-quadruplex DNA ligands. Chem. Sci. 2020, 12, 1415–1426. [Google Scholar] [CrossRef]
- Schlucker, S. Surface-enhanced Raman spectroscopy: Concepts and chemical applications. Angew. Chem. Int. Ed. Engl. 2014, 53, 4756–4795. [Google Scholar] [CrossRef] [PubMed]
- Cao, C.; Li, P.; Liao, H.; Wang, J.; Tang, X.; Yang, L. Cys-functionalized AuNP substrates for improved sensing of the marine toxin STX by dynamic surface-enhanced Raman spectroscopy. Anal. Bioanal. Chem. 2020, 412, 4609–4617. [Google Scholar] [CrossRef]
- Noda, I.; Ozaki, Y. Two-Dimensional Correlation Spectroscopy-Applications in Vibrational and Optical Spectroscopy; John Wiley & Sons, Ltd.: Chichester, UK, 2005; Volume 1, pp. 1–14. [Google Scholar]
- Lee, P.; Meisel, D. Adsorption and surface-enhanced Raman of dyes on silver and gold sols. J. Phys. Chem. 1982, 86, 3391–3395. [Google Scholar] [CrossRef]
- Wu, M.; Li, H.; Lv, D.; Lu, F. Dynamic-SERS spectroscopy for the in situ discrimination of xanthine analogues in ternary mixture. Anal. Bioanal. Chem. 2017, 409, 5569–5579. [Google Scholar] [CrossRef]
- Li, H.; Zhu, Q.; Chwee, T.; Wu, L.; Chai, Y.; Lu, F.; Yuan, Y. Detection of structurally similar adulterants in botanical dietary supplements by thin-layer chromatography and surface enhanced Raman spectroscopy combined with two-dimensional correlation spectroscopy. Anal. Chim. Acta 2015, 883, 22–31. [Google Scholar] [CrossRef]
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Liu, Y.; Jiang, C.; Song, M.; Cao, Y.; Huang, Q.; Lu, F. Optimization of Gonyautoxin1/4-Binding G-Quadruplex Aptamers by Label-Free Surface-Enhanced Raman Spectroscopy. Toxins 2022, 14, 622. https://doi.org/10.3390/toxins14090622
Liu Y, Jiang C, Song M, Cao Y, Huang Q, Lu F. Optimization of Gonyautoxin1/4-Binding G-Quadruplex Aptamers by Label-Free Surface-Enhanced Raman Spectroscopy. Toxins. 2022; 14(9):622. https://doi.org/10.3390/toxins14090622
Chicago/Turabian StyleLiu, Yan, Chengshun Jiang, Menghua Song, Yongbing Cao, Qiang Huang, and Feng Lu. 2022. "Optimization of Gonyautoxin1/4-Binding G-Quadruplex Aptamers by Label-Free Surface-Enhanced Raman Spectroscopy" Toxins 14, no. 9: 622. https://doi.org/10.3390/toxins14090622
APA StyleLiu, Y., Jiang, C., Song, M., Cao, Y., Huang, Q., & Lu, F. (2022). Optimization of Gonyautoxin1/4-Binding G-Quadruplex Aptamers by Label-Free Surface-Enhanced Raman Spectroscopy. Toxins, 14(9), 622. https://doi.org/10.3390/toxins14090622