miRNA Electrochemical Biosensors: Comparison
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Please note this is a comparison between Version 2 by Jessie Wu and Version 4 by Jessie Wu.

Electrochemical biosensors are devices that convert the biological signal generated by the specific binding of a recognition probe to a target to be measured into electrical signals such as voltage, current, and impedance. Electrochemical biosensors are suitable for point-of-care (POC) detection due to the ease of miniaturization, automation, integration, and mass production. In recent years, nanotechnology has brought great opportunities for development in the field of electrochemical biosensors. The large surface volume ratio of nanomaterials helps to improve the detection sensitivity of biosensors. The commonly used electrochemical detection methods mainly include voltammetry and impedance methods. 

  • hepatocellular carcinoma
  • microRNAs
  • electrochemistry
  • optics
  • electrochemiluminescence

1. Voltammetry

Voltammetry is based on the relationship between the electrode potential and the current through the electrolytic cell to obtain analytical results. With the development of bioanalytical techniques, voltammetry is now mostly performed using a three-electrode system consisting of a working electrode, a counter electrode, and a reference electrode. The test methods mainly include cyclic voltammetry (CV) [1], square wave voltammetry (SWV) [2], differential pulse voltammetry (DPV) [3], and other methods.
Pathological studies have shown that miRNA-122 acts to repress oncogenes involved in different HCC features, and downregulation of miRNA-122 can cause tumor metastasis and hepatocellular carcinoma progression [4]. Therefore, simple and sensitive detection of miRNA-122 is highly relevant for the early diagnosis of HCC. Gao et al. [5] proposed an electrochemical biosensor based on the ion barrier effect for the detection of miRNA-122. Prussian blue (PB) and gold nanoparticles (AuNPs) were first modified on the surface of a glassy carbon electrode (GCE) by a two-step electrodeposition method. The addition of Prussian blue was able to sensitize the GCE electrode to K+, resulting in a significant change in the voltammetric signal. KNO3 was chosen to provide K+. The modification of AuNPs enabled the GCE electrode to immobilize thiolated DNA probes by the self-assembly of Au-S bonds. An ionic barrier effect was produced when the DNA probe hybridized specifically with the target miRNA-122, preventing the diffusion of K+ from the solution to the electrode surface. In this way, the voltammetric signal at the electrode surface was suppressed, which achieved the quantitative detection of miRNA-122. The electrochemical response of the sensor was studied using DPV. The sensor has a response time of 60 min and can analyze miRNA-122 in the concentration range of 0.1 fmol/L–1.0 nmol/L with a detection limit of 0.021 fmol/L. This biosensor based on the ion barrier effect has the advantages of simple operation, low cost, sensitive response, high specificity, and high stability. In addition, the method shows better detection in real human serum samples and can be used to analyze complex biological samples. However, the detection time of this method is long, which is not conducive to the realization of point-of-care detection.
Losada et al. [6] designed an electrochemical biosensing platform based on microfluidic sensing technology that can perform eight multiple measurements of miRNA-122. The platform consisted of a glass substrate containing gold microelectrodes and a polydimethylsiloxane (PDMS) layer containing microfluidic channels. The capture probe modified with thiols was incubated in the microfluidic channel, and the probe was able to form a self-assembled monolayer (SAM) by immobilizing it on the electrode surface with Au-S bonds. After rinsing the channel with 0.5 M NaCl, miRNA-122 was injected into the microfluidic channel to hybridize with the capture probe. In this research, CV was used for electrochemical measurements, and the detection time required 30 min. The electrochemical sensing platform has a linear working concentration of 10−18−10−6 mol/L and a detection limit of 10−18 mol/L. This method has a wider linear detection range, lower detection limit, and shorter assay time for the detection of miRNA-122 compared to the method of Gao et al. [5]. In addition, microfluidic sensing technology makes the sensing platform miniaturized and more portable. It can also reduce costs and achieve high-throughput detection.
In recent years, the signal amplification strategy based on 3D DNA walkers has shown great potential for the ultrasensitive detection of microRNAs (miRNAs). Yang et al. [7] designed an “on-super off” dual-mode photoelectrochemical (PEC) and ratiometric electrochemical (EC) biosensor based on this strategy for the detection of miRNA-224. The sensor applied methylene blue (MB) and ferrocene (Fc) to induce signal quenching and enhancement. CdS quantum dots (QDs) were used here as photoactive electrode materials due to their photoelectric conversion efficiency. The signal “on” state was achieved by immobilizing MB-labeled hairpin DNA (MB-DNA) through Cd-S bonding, which sensitized the CdS QDs and generated significant PEC signals. Hairpin MB-DNA was turned on after the introduction of DNA probes labeled with Ag nanocubes (Ag-DNA). Several ferrocene-labeled DNA (Fc-DNA) generated by amplification of the 3D DNA walker, Ag-DNA, and MB-DNA hybridized to form a “Y” shaped hairpin structure. This structure keeps the MB away from the CdS QDs and the Fc close to the CdS QDs, which results in a reduced PEC signal and achieves a signal “super-off” state. In addition, miRNA-224 detection was also accomplished on the ratiometric EC biosensor using SWV. As the concentration of miRNA-224 increased, the oxidized peak current of MB decreased, and the oxidized peak current of Fc increased. Quantification of miRNA-224 was achieved by evaluating the value of IMB/IFc. The sensor has a linear detection range of 0.1–1000 fM with a detection limit of 0.019 fM in PEC and a detection range of 0.52–500 fM with a detection limit of 0.061 fM in ratiometric EC. CdS quantum dots exhibited excellent optoelectronic performance in the detection of miRNA-224 by this biosensor. The signal enhancing and quenching could be easily controlled by changing the structure of DNA, and the signal amplification strategy based on the 3D DNA walker significantly improved the sensitivity of detecting miRNAs.
Homogeneous electrochemical biosensors are low-cost, simple to immobilize, and the detection process occurs in a homogeneous solution. Wu et al. [8] designed a homogeneous electrochemical biosensor based on MnO2 nanosheets with dual enzyme activity for the detection of miRNA let-7a. In the absence of miRNA let-7a, the nucleic acid probe was tightly adsorbed on the surface of the 2D MnO2 nanosheets, and the catalytic activity of the MnO2 nanosheets was significantly inhibited. This led to the presence of a large amount of MB in the solution, which produced a very high DPV current peak. After the addition of miRNA let-7a, the phosphate group triggered the nucleobase pair shielding effect, and the probe was detached from the surface of MnO2 nanosheets after hybridization with miRNA let-7a. At this time, the surface-active sites of the MnO2 nanosheets were significantly increased and were able to fully react with MB. As a result, a large amount of MB was eliminated, leading to a significant decrease in the DPV response. The linear detection range of this homogeneous electrochemical biosensor was 0.4–140 nM, and the detection limit was 0.25 nM. Although this homogeneous electrochemical biosensor was simple to prepare, the detection sensitivity was limited.
Azab et al. [9] prepared an miRNA let-7a biosensor with a sandwich structure based on nanomaterials. Chrysin and carbon nanotubes (CNTs) were, respectively, modified on the carbon paste electrode (CPE), which could improve the antioxidant property of the electrode and optimize the conductivity and biocompatibility of the electrode. Then AuNPs were employed to modify the electrode surface, enhancing both the active surface area of the electrode and the stability of the immobilized capture probe. The electrochemical response was monitored by DPV, and the optimal time for hybridization of this sensor is 30 min. The current response increased with increasing miRNA let-7a concentration in the range of 1.0 zM to 11 nM, and the limit of detection was 1.0 zM. The introduction of nanomaterials such as CNTs and AuNPs has been instrumental in improving the sensitivity of the biosensor. In addition, the prepared biosensor has good applicability for miRNA let-7a detection in real serum samples. The biosensor has an excellent detection limit, which is highly favorable for early detection of clinical HCC.
Cai et al. [10] reported an AuNP-modified graphene field effect transistor (FET) biosensor for the sensitive detection of miRNA let-7b. This FET biosensor was prepared by first dropwise addition of a reduced graphene oxide (R-GO) suspension on the FET surface, followed by modification of AuNPs on top of it. The PNA probes possess an electrically neutral backbone, which contributes to enhanced hybridization efficiency and reduced background noise in comparison to traditional DNA probes. This neutral nature of PNA probes mitigates the repulsive effects that can arise during the hybridization process [11]. In this research, after immobilizing the PNA probe on the surface of AuNPs through Au-S bonds, the excess active site was blocked using ethanolamine solution to minimize potential nonspecific binding. When the PNA probe hybridizes with miRNA let-7b, a distinct voltammetric response signal is generated due to the binding event. It was found that the developed FET biosensor could achieve detection limits as low as 10 fM in the linear range of 1 fM–100 pM. In addition, this highly sensitive and selective method was also successfully used for the detection of miRNA let-7b in serum samples. The PNA probe is highly promising for miRNA detection, and this PNA probe-based FET biosensor has the potential to be used as a point-of-care tool.
Erdem et al. [12] developed a method for electrochemical analysis of miRNA-34a based on the Zip nucleic acid (ZNA) probe. ZNA probes were hybridized with target miRNA-34a in solution, and double-stranded products formed by hybridization were immobilized on the surface of magnetic beads (MBs) coated with streptavidin through biotin–streptavidin interaction. The double-stranded product was separated from the MBs by magnetic separation technique and then immobilized on the surface of pencil graphite electrodes (PGEs) for electrochemical measurements using DPV. The detection limit of this method was 0.87 µg/mL in the linear range of 2–8 µg/mL. In addition, the electrochemical analysis method based on the ZNA probe is also suitable for the detection of miRNA-34a in real samples. The innovative use of ZNA probes in this sensor overcomes the electrostatic repulsion between probes and their complementary sequences, thus improving hybridization efficiency. However, the biosensor detects miRNA-34a for up to 60 min, which is not conducive to achieving point-of-care detection. In the future, with the advantage of ZNA nucleic acids combined with rapid enrichment methods such as the AC electrokinetics (ACEK) effect, the detection performance of the sensor will be improved, and the detection time will be shortened.
Zeng et al. [13] explored the photocurrent properties of yolk-in-shell Au@CdS and yolk-shell Au@CdS and established a sensitive and feasible PEC biosensor for the quantitative detection of miRNA-21 based on yolk-in-shell Au@CdS. The biosensor used HRP-labeled ssDNA combined with MBs to form MB-ssDNA-HRP as the signal probe, yolk-in-shell Au@CdS as the photoactive substrate, and benzo-4-chlorohexadienone (4-CD) precipitation as the signal quencher. In the presence of miRNA-21, miRNA-21 and two hairpin DNAs (H1, H2) could generate a large amount of H1-H2 double-stranded (dsDNA) by catalytic hairpin assembly (CHA) reaction. dsDNA binding to Cas12a-crRNA triggered the cleavage of MB-ssDNA-HRP by Cas12a, which led to the detachment of HRP from the MB surface. After magnetic separation, HRP was able to catalyze 4-chloro-1-naphthol (4-CN) to generate 4-CD precipitates that covered the yolk-in-shell Au@CdS surface, resulting in a significant decrease in its photocurrent response. The linear detection range of this PEC biosensor for miRNA-21 was 0.01 pM-10 nM, with a detection limit of 4.2 fM. In addition, stronger synergistic effects, SPR, and thermal electron transfer were found for yolk-in-shell Au@CdS by FDTD simulation combined with photocurrent/photothermal testing. Yolk-in-shell Au@CdS functional nanomaterials have great potential for early screening and diagnosis of various cancers.
Ouyang et al. [14] constructed an electrochemical biosensor for miRNA-21 detection by combining nanomaterials and hybridization chain reaction (HCR). First, Ti3C2 was obtained by etching Ti3AlC2 with HF, and then Ti3C2 was covered with Bi2O3 nanoparticles to form Ti3C2@Bi2O3 with an accordion-like structure. GCE was modified with Ti3C2@Bi2O3 to enhance electrode conductivity and AuNPs to increase the active surface area. Then the thiol-modified capture probe (SH-CP) was immobilized on the electrode through Au-S bonds. The hairpin structure of the capture probe was opened when the target miRNA-21 was present, allowing miRNA-21 to hybridize specifically with the capture probe. The addition of primers H1 and H2 triggered the hybridization chain reaction, forming long double strands on the GCE surface. Many methylene blue (MB) molecules were embedded in the long double strand, which resulted in a significant DPV response of the biosensor at a potential of 0.19 V. This dual-signal amplification strategy based on nanomaterials and HCR can detect miRNA-21 in a wide linear range of 1 fM–100 pM with a detection limit as low as 0.16 fM. Compared with the qRT-PCR quantification technique, the biosensor detected miRNA-21 in the same linear range as qRT-PCR, but with a lower detection limit and higher sensitivity. In addition, the biosensor shows good applicability in human serum samples. However, the biosensor is dependent on primed DNA strands, which leads to higher costs and is not favorable for mass production.

2. Impedance Method

Electrochemical impedance spectroscopy (EIS) is a sensitive and versatile electrochemical sensing technique that finds extensive applications in the analysis of microscopic interfacial features associated with biomolecules [15]. By probing the impedance spectroscopic response of electrochemical systems, EIS provides valuable insights into various physical properties such as diffusion rates, reaction rates, and microstructural features [16]. Currently, EIS serves a dual role in electrochemical biosensors. It can be used to characterize the sensor construction process, and also to quantitatively detect biomolecules [17].
La et al. [18] proposed a signal amplification strategy induced by the insulating effect to enable sensitive impedance measurements of miRNA-21. The DNA probe encapsulated on the surface of the Au electrode was able to capture the target miRNA-21 and a biotin-modified miRNA (biotin–miRNA) with the same nucleic acid sequence. After self-assembly by biotin–F monomers, the streptavidin (SA)–biotin–FNP network was formed by binding SA. Biotin–miRNA adsorbed onto the SA–biotin–FNP network through biotin–SA interactions, forming an insulating layer on the electrode surface that hinders electron transport and consequently amplifies the impedance response. When the target miRNA-21 was present, miRNA-21 and biotin–miRNA competed for hybridization to the capture probe. With the reduction of biotin–miRNA captured on the electrode, the adsorbed SA–biotin–FNP network was also reduced, resulting in a significant decrease in the impedance signal. The linear range of this detection strategy for miRNA-21 detection is 0.1–250 fM, with detection limits as low as 0.1 fM. The SA–biotin–FNP network used in this method is relatively easy to prepare and the sensor has good applicability in real samples. However, the detection time of this sensor is greater than 2 h, which is not conducive to achieving rapid point-of-care detection.
Eksin et al. [19] developed a paper-based electrochemical impedance biosensor for quantitative detection of miRNA-155. The paper-based sensor consisted of a microfluidic channel and a working area where the working electrode, counter electrode, and reference electrode were placed. AuNPs-PE was formed by depositing AuNPs onto PE through the chronocurrent method. The thiol-modified DNA probe was immobilized on AuNPs-PE via Au-S bonds. When miRNA-155 was present, KCl solution containing [Fe(CN)6]3−/4− was added dropwise, and miRNA-155 was quantified by measuring the change in charge transfer resistance (Rct). The linear detection range of the sensor was 0–1.5 μg/mL in PBS with a detection limit of 33.8 nM, and 0–4 μg/mL in the fetal bovine serum (FBS) medium with a detection limit of 93.4 nM. The biosensor shows good selectivity for non-complementary and mismatched miRNA sequences. The paper-based electrochemical biosensor can selectively detect miRNAs even in complex media such as serum with a detection time of only 15 min and good stability, which makes it very suitable for point-of-care (POC) detection applications.
Yarali et al. [20] developed an electrochemical biosensor for the detection of miRNA-155 and miRNA-21 associated with early cancer diagnosis using molybdenum disulfide (MoS2) modified paper-based electrodes for the first time. Block crystals and sheets of MoS2 were, respectively, fabricated and modified on the surface of paper-based electrodes to explore their performance in miRNA detection. The capture probe was modified on the MoS2-modified electrode, and different concentrations of target miRNA solutions were added dropwise for hybridization. The electrochemical response of the sensor was measured by EIS technology, and the entire miRNA detection process was completed within 30 min. The linear detection range of this biosensing platform is 1–200 ng/mL. In the PBS buffer, the LOD for miRNA-155 was calculated to be 17.0 ng/mL and the LOD for miRNA-21 was 9.2 ng/mL through linear fitting. In the FBS medium, the LOD of miRNA-155 was 1.0 ng/mL and the LOD of miRNA-21 was 17.0 ng/mL. The electrically active surface area of bulk MoS2 was larger compared to that of nanosheets, and thus the detection limit of the paper-based electrode modified by bulk MoS2 was lower. In addition, they are effective in distinguishing non-target sequences with single base mismatches. The biosensor has a low manufacturing cost and can perform highly sensitive and selective quantitative analysis of miRNAs at low sample volumes, offering great potential for the detection of miRNA biomarkers in human serum.

3. Other Methods

In addition to the studies mentioned above, several other near-commercial miRNA biosensors have been developed. Jin et al. [21] combined magnetic nanobeads with metal–organic frameworks loaded with glucose oxidase (MOFs@GOX) and constructed a novel self-powered electrochemical sensor based on a photocatalytic zinc–air battery (ZAB-SPES) for the detection of miRNA let-7a. ZAB-SPES has a high-power density of 22.8 μW/cm2, which is 2–3 times higher than that of commonly used photofuel cells. Gao et al. [22] reported a flexible graphene field effect transistor (Gr-FET) biosensor. The biosensor was able to achieve an miRNA detection limit as low as 10 fM within 20 min. Gr-FET-based biosensors will have prospective applications in wearable electronic devices for health monitoring and disease diagnosis. Xu et al. [23] integrated EBFCs on a flexible paper tape carrier to establish an ingenious sensor technology for the detection of tumor markers in complex samples. Multivariate detection was realized by receiving real-time instantaneous current values via a smartphone. This smartphone-based paper tape sensor platform provides an opportunity for early cancer diagnosis and lays the foundation for the construction of flexible wearable platforms.
Table 1 summarizes the characteristics of these electrochemical biosensors for the detection of HCC-associated miRNAs. The main characteristics include receptor type, electrode material, electrochemical method, linear detection range, detection limit, sensitivity, and response time. It was found that the above electrochemical biosensors had wide detection limits and high sensitivity. However, most of the sensors have poor immunity to interference and still have a long response time, which is not conducive to rapid bedside detection.
Table 1. Electrochemical biosensors for the detection of hepatocellular carcinoma-associated miRNAs.
Analyte Receptor Electrode Electrochemical

Method		 Linearity Range LOD Sensitivity Assay Time Ref.
miRNA-122 DNA probe GCE DPV 0.1 fmol/L–1.0 nmol/L 0.021 fmol/L — 60 min [5]
miRNA-122 DNA probe Au CV 10−18–10−6 mol/L 10−18 mol/L — 30 min [6]
miRNA-224 DNA probe ITO SWV 0.52–500 fM 0.061 fM — — [7]
miRNA-let 7a DNA probe MnO2 DPV 0.4–140 nM 0.25 nM — — [8]
miRNA-let 7a DNA probe CPE DPV 1.0 zM–11 nM 1.0 zM — 30 min [9]
miRNA-let 7b PNA probe AuNPs Voltammetry 1 fM–100 pM 10 fM — 30 min [10]
miRNA-34a ZNA probe PGE DPV 2–8 μg/mL 0.87 μg/mL — 60 min [12]
miRNA-21 DNA probe Au@CdS Photocurrent 0.01 pM–10 nM 4.2 fM — — [13]
miRNA-21 DNA probe GCE DPV 1 fM–100 pM 0.16 fM — 30 min [14]
miRNA-21 — Au EIS 0.1–250 fM 0.1 fM — >2 h [18]
miRNA-155 DNA probe AuNPs-PE EIS 0–1.5 μg/mL 33.8 nM — 15 min [19]
miRNA-21

miRNA-155		 DNA probe MoS2-PE EIS 0.025–0.75 μg/mL

0.05–0.15 μg/mL		 9.2 ng/mL

17.0 ng/mL		 1372.4 kOhm.mL.μg−1.cm−2

1361 kOhm.mL.μg−1.cm−2		 30 min [20]
 

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