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Alpha-Hemolysin Nanopore Allows Discrimination of the Microcystins Variants† Cite This: RSC Adv.,2019,9, 14683 Ad B Bc Janilson J

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Alpha-Hemolysin Nanopore Allows Discrimination of the Microcystins Variants† Cite This: RSC Adv.,2019,9, 14683 Ad B Bc Janilson J RSC Advances PAPER View Article Online View Journal | View Issue Alpha-hemolysin nanopore allows discrimination of the microcystins variants† Cite this: RSC Adv.,2019,9, 14683 ad b bc Janilson J. S. Junior,´ Thereza A. Soares, Laercio´ Pol-Fachin, Dijanah C. Machado,a Victor H. Rusu,b Juliana P. Aguiarad ad and Claudio´ G. Rodrigues * Microcystins (MCs) are a class of cyclic heptapeptides with more than 100 variants produced by cyanobacteria present in surface waters. MCs are potent hepatotoxic agents responsible for fatal poisoning in animals and humans. Several techniques are employed in the detection of MCs, however, there is a shortage of methods capable of discriminating variants of MCs. In this work we demonstrate that the a-hemolysin (aHL) nanopore can detect and discriminate the variants (LR, YR and RR) of MCs in aqueous solution. The discrimination process is based on the analysis of the residence times of each variant of MCs within the unitary nanopore, as well as, on the amplitudes of the blockages in the ionic current flowing through it. Simulations of molecular dynamics and calculation of the electrostatic Creative Commons Attribution-NonCommercial 3.0 Unported Licence. potential revealed that the variants of MCs present different charge distribution and correlated with the three patterns on the amplitudes of the blockages in the ionic current. Additionally, molecular docking Received 18th December 2018 analysis indicates different patterns of interaction of the variants of MCs with two specific regions of the Accepted 1st April 2019 nanopore. We conclude that aHL nanopore can discriminate variants of microcystins by a mechanism DOI: 10.1039/c8ra10384d based mainly on electrostatic interaction. Finally, we propose the use of nanopore-based technology as rsc.li/rsc-advances a promising method for analyzing microcystins in aqueous solutions. resulting in variants with different toxicity proles.3 Currently This article is licensed under a Introduction over 100 variants of MCs have been described which differ from Microcystins (MCs) are constituted by cyclic heptapeptides con- each other with respect to the identity of the two variable residues taining several non-proteinogenic amino acids, and represent and chemical modications in the other amino acids.4 The Open Access Article. Published on 10 May 2019. Downloaded 9/26/2021 10:56:29 AM. a class of exotoxins produced by cyanobacteria species commonly variant Microcystin-LR (MC-LR, 995 Da) containing the residues present in surface waters of tropical regions in the northern and Leu2 and Arg4 is the most common and toxic of MCs.1,4 southern hemispheres.1,2 MCs general sequence is cyclo-(D-Ala1- MCs are potent hepatotoxic and nephrotoxic agents, which X2-D-MeAsp3-Z4-Adda5-D-Glu6-Mdha7) where the numbers have been associated to liver, digestive and skin diseases, indicate the position of a given amino acid in the sequence neurological impairment and death.5 It has been associated (Fig. 1). The modied residues MeAsp (Masp), Adda and Mdha with most of the poisoning incidents worldwide.6 In February corresponds to D-erythro-beta methylisoaspartic acid, 1996, one of the largest toxic diseases caused by MCs in humans (2S,3S,8S,9S)-3-amino-9-methoxy-2,6,8-trimethyl-10-phenyldeca- occurred in Caruaru in the Northeast of Brazil, resulting in the (4E,6E)-dienoic acid and methyldehydroalanine, respectively. deaths of 60 patients.7 MCs exert their toxicity via irreversible Positions X2 and Z4 are occupied by variable L-amino acids, aDepartamento de Biof´ısica e Radiobiologia, Universidade Federal de Pernambuco, Avenida Prof. Moraes Rego, s/n, Cidade Universitaria,´ Recife, Pernambuco, 50670-901, Brazil. E-mail: [email protected]; Fax: +55 81 2126 8560; Tel: +55 81 2126 8535 bDepartamento de Qu´ımica Fundamental, Universidade Federal de Pernambuco, Cidade Universitaria´ 50740-560, Recife, PE, Brazil cCentro de Pesquisas Aggeu Magalhaes,˜ Fundaçao˜ Oswaldo Cruz, Cidade Universitaria´ 50740-465, Recife, PE, Brazil dPrograma de Pos-graduaç´ ao˜ em Inovaçao˜ Terapˆeutica, Universidade Federal de Pernambuco, Brazil Fig. 1 Structure of microcystin-LR. Variants differ with respect to the † The authors dedicate this work to Dr Oleg Vladimirovich Krasilnikov (in identity of L-amino acids in position 2 and 4. Numbers represent the memoriam). position of the amino acid residue. This journal is © The Royal Society of Chemistry 2019 RSC Adv.,2019,9, 14683–14691 | 14683 View Article Online RSC Advances Paper inhibition of protein phosphatases 1 and 2A, affecting mainly Results and discussion liver cells, which can lead to death.8 Additionally, long-term exposure to low concentrations of MCs has been implicated in aHL nanopores exhibited uniform single-channel conductance tumour growth promotion.9 The World Health Organization state of long duration at both negative and positive trans- À (WHO) recommends an upper limit of 1 mgL1 of MCs in membrane potentials.20 In 40 mV an unobstructed aHL nano- drinking water for human health protection.10 Eutrophication pore has a constant current of approximately 150 pA and and climatic changes has led to the rapid proliferation and conductance of 4 nS in KCl 4 M, pH 7.5, and the values of dominance of harmful blooms of cyanobacteria in freshwater these parameters are in agreement with several previous and marine ecosystems.11,12 Temperatures ranging between 15– reports.24,29,30 The addition of MC-LR, MC-RR or MC-YR to the 30 C can selective promote cyanobacterial proliferation as the trans side of nanopore induces reversible partial blockades of growth rates of these bacteria are optimal at relatively high the ionic current, and similarly to studies with other analytes, temperatures.13 MCs are a growing threat to the use of fresh- this clearly indicates that this nanopore is capable of detecting water ecosystems and reservoirs for drinking water, irrigation, MCs, so it works as a molecular counter31–33 (Fig. 2). and shing. Therefore, sh and water consumption can be an The prole of the microcystin-induced ionic current block- important route of microcystin exposure for humans.14 ages differ considerably from those reported in other studies The low concentration and large number of variants repre- using synthetic linear peptides with a number of amino acids sent a considerable challenge for the monitoring of MCs in similar to microcystins, suggesting that the nanopore is capable water bodies, to which several analytical methods have been of discriminating the analytes by the molecular congura- employed.15 Among the most sensitive techniques are high tion.34,35 Although the MCs variants differ in only a single amino performance liquid chromatography coupled with mass spec- acid (Fig. 2A), each variants exhibits a typical characteristic trometry (HPLC-MS), enzyme-linked immunosorbent assay blockages of the ionic current (Fig. 2B). Observe that the (ELISA) and phosphatase assay. Some of these techniques offer amplitude of the blockages of the ionic current caused by MC- Creative Commons Attribution-NonCommercial 3.0 Unported Licence. excellent sensitivity and speci city but at high cost, time- YR is larger compared to the other variants (Table 1, right consuming sample preparation procedures and lengthy anal- column). The MC-YR has blocked about 91.6% of the ionic ysis.16 Furthermore, the use of HPLC-MS for the detection and current, followed by 81.6% of the MC-RR and 70.1% of MC- identication of unknown MCs in environmental samples is LR, respectively. Then, the magnitude of the ionic current hampered mainly by the lack of analytical standards for many blockages amplitude in the nanopore depends on the MC MC variants.3,16 In addition, HPLC-MS requires highly skilled variant. As expected the percentage reduction in ionic current personal and expensive equipment. Protein phosphatase inhi- induced by microcystin is higher than that of acyclic peptides.34 bition assays are susceptible to high rates of false-positive In order to rationalize the molecular basis of specic results, and cannot distinguish between different MC vari- blockage types for each MCs by the aHL nanopore, molecular This article is licensed under a ants.3,17 Likewise, immunoassay techniques may present cross docking experiments were conducted. Such approach is the reactivity to MCs variants.17 Therefore, there is a critical demand most common method employed to model the interaction for the development of low-cost analytical devices for MC between a small molecule and a protein at the atomic level, Open Access Article. Published on 10 May 2019. Downloaded 9/26/2021 10:56:29 AM. monitoring in water, which features high sensitivity and spec- allowing the characterization of ligands behaviour in the icity, easiness to use and great portability. Nanopore based- binding site of target receptors, and generating novel informa- systems have been successfully employed in the stochastic tion to help elucidating biological and biotechnological biosensing18,19 Stochastic biosensing is an approach that relies processes.36 Molecular docking is conducted through two steps: on the observation of individual binding events between analyte (1) sampling conformations of the ligand in the active site of the molecules and a single bioreceptor.20 Recently, solid-state protein, which should be able to reproduce the experimental nanopore with a diameter of approximately 10 nm was used binding mode; and (2) ranking these conformations via to detect MC-LR via aptamer-conjugated with gold nano- a scoring function, which should also rank it highest among all particles.21 In here, we used a-hemolysin (aHL) nanopore with generated conformations.37 From our calculations, the lowest diameter approximately 1 nm to discrimination microcystins energy docked conformations for each of the three MCs indeed variants.22 Nanopore formed by Staphylococcus aureus a-hemo- tted the region of constriction of the aHL nanopore (Fig. 3B), lysin (aHL) is the most commonly protein nanopore employed in which the Arg residues in MCs would interact with Glu111 in the stochastic biosensing technology.23 Because these pores residues.
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