b Zhejiang Institute, China University of Geosciences Wuhan, Hangzhou 311305, China;
c Hubei Key Laboratory of Bioinorganic Chemistry & Materia Medica, School of Chemistry and Chemical Engineering, Huazhong University of Science and Technology, Wuhan 430074, China
Biomolecules play a great role in the process of life regulation. Itis of great significance to develop new methods for detecting and quantifying various biomolecules which are closely associated with human health with high sensitivity, selectivity, low-cost and simplicity [1, 2]. Single target detection assays might increase the possibility of "false positives" outcomes , leading to the wrong results in clinical diagnosis, because many diseases are often not determined by only one biomolecule . In order to overcome the drawbacks of single target detection assays, multiple targets detection assays open the new gate for enhancing the reliability of pathological assessment and thoroughly understanding the biomolecular mechanism of cell function. Moreover, comparedtosingle target detection assays, multiple targets detection assays possess the advantages of higher throughput, fewer sampling errors, easier internal control and so on [6, 7]. As a result, multiplexing technologies for multiplex targets detection have recently been developed for the disease diagnosis, treatment as well as drug discovery .
Nanomaterial-based biosensor field has made a great progress. Nanomaterials can be divided into four types according to their shapes : zero-dimensional materials (e.g., spherical nanomaterials), one-dimensional materials (e.g., nanotubes, nanowires, and nanochannels), two-dimensional materials (e.g., grapheme, and carbon nitride nanosheets) and three-dimensional materials (e.g., nanoprisms and nanoflowers). Due to their special electrochemical properties, stable structure, biological compatibility, high catalytic performance, and large specific surface area [10, 11], nanomaterials have been widely used in electrochemical detection of biomolecules, such as graphene oxide (GO) and nanochannels [12-15]. Gold nanoparticles [16, 17], carbon nanotubes (CNTs) and carbon nitride nanosheets that are highly effective nanomaterial quenchers have been widely reported and exhibit ultra-high adsorption capacity and high fluorescence quenching ability for the detection of multiple biomolecules [18-21].
By taking advantages of the unique photochemical and electrochemical properties of nanomaterials, herein, we discuss recent representative works for the determination of multiple biomolecules utilizing the nanomaterials (Fig. 1). Nanomaterials that we discuss below are classified into two sections on the basis of the materials used in the probes: one-dimensional materials (1DMs) and two-dimensional materials (2DMs).
|Fig. 1. Schematic of one-dimensional and two-dimensional nanomaterials for the detection of multiple biomolecules.|
2. 1DMs detection 2.1. 1DMs electrochemical detection
Polyethylene terephthalate (PET) based nanochannels with the diameter range of 20–100 nm and the length range of 10–20 nm are classified as 1DMs and play a crucial role in substance transport. Here we summarize the use of PET-based nanochannels for the electrochemical detection of multiple biomolecules that control the process of life regulation.
Artificial stimuli-responsive nanochannels that simulate the gating characteristics of biological ion channels to control the flow of ions across cell membranes have captured tremendous attention . Nevertheless, a large number of environmental factors in the reaction system have an influence on the ion current. Our group utilized double signals (fluorescence as well as ionic current) to directly verify the blockage of PET-based nanochannels . Moreover, by analyzing the fluorescence and ion current signals of the PET-based nanochannels , the opening and closing of the PET-based nanochannels was indicated through an intermediate state similar to the onion, and this was consistent with the calculation result of the MD simulation. In the presence of glucose (Glu), the surface of the PET-based nanochannels modified with 4-aminophenylboronic acid (PBA) specifically bound to Glu, resulting in clogging of the PET-based nanochannels and achieving the purpose of Glu detection (Fig. 2). Utilizing the reaction between AIE molecule (TPEDB) and Glu which could form oligomer, we can clearly observe the decrease of ion current and the enhancement of fluorescence signal upon the presence of Glu. The probe exhibited high sensitivity and good selectivity for the detection of Glu. In order to verify the ability of the strategy toward the clinical application (40 urine samples including 10 normal urine samples, 15 diabetic pre-treatment urine samples, and 15 diabetic patients treated urine samples have been examined). The results of the strategy were consistent with those of the standard methods that were used in hospitals, which also verifies the feasibility of this strategy. In addition, the dual-signal-responsive PET-based nanochannels had high antiinterference ability in complex practical applications, and can discriminate obviously Glu from interference, such as Vc and H2O2. By taking advantage of the oligomerization on the basis of AIE molecules , the strategy demonstrates great potential to monitor drugs in complex environments. Although PBA is not a biomolecule, the PET-based nanochannel provides a new idea for the detection of many biomolecules by replacing PBA with other biomolecules.
|Fig. 2. Schematic of the PET-based nanochannel based on the ionic current and fluorescence dual signal output for the detection of Glu and PBA.Copied with permission . Copyright 2016, American Chemical Society.|
In 2013, our group designed a nanostructure that had various target-binding sites for the detection of multiple oligonucleotide chains and ATP by observing amplified electrochemical signals (Fig. 3) . This nanostructure indirectly monitored the change of the received electrical signals by controlling the smart nanofluidic switch to achieve the purpose of detecting multiple targets [25, 26]. When the target DNAs were present, the target DNAs will hybridize with the capture DNA probes modified on the surface of the PET-based nanochannels [27-29], resulting in the PET-based nanochannels to be blocked. Then, we verified the presence of target DNA by observing changes in PET-based nanochannels' conductance. When the capture DNA probe contained an ATP aptamer sequence, ATP can be detected in high concentrations of interfering substances or serum samples through the change of the preformed supersandwich structures. Moreover, the detection limit of ATP can reach 1 nmol/L, and the detection of oligonucleotides can reach 10 fmol/L.
|Fig. 3. Illustration of the PET-based nanochannels on the basic of ionic current signal for detecting multiple DNAs and ATP. Copied with permission . Copyright 2013, Wiley Publishing Group.|
The biological pathways on the cell membrane are crucial for the regulation of life activities, controlling the entry and exit of small molecules and the transmission of neurotransmitters like the gatekeepers of the gate. Our group assembled a PET-based nanochannel and controlled the PET-based nanochannel switch by using 3D [30, 31], cross-linked DNA as an efficient gatekeeper (Fig. 4) . Three single-stranded DNAs were combined into a 3- point star motif by Waston-Crick base pairing, called Y-DNA. When the PET-based nanochannel modified with the capture probe was immersed in a solution containing Y-DNA, the two complementary DNAs hybridized to each other for forming a 3D structure since the apical DNA of the Y-DNA was complementary to the apical DNA of the capture probe. The insert and the capture probe contained an embedded aptamer sequence of ATP by a specific sequence design. Then in the presence of ATP or DNase I, the 3D nanostructure reopened the ion channel pathway, resulting in a shift in electrical signals. We can detect ATP and DNase I by observing the transition of electrical signals.
|Fig. 4. The detection mechanism for ATP and DNase I based on 3D, cross-linked DNA superstructures. Copied with permission . Copyright 2015, Wiley Publishing Group.|
2.2. 1DMs fluorescence detection
As a kind of classical 1DMs, carbon nanotubes are widely used for fluorescence detection due to their high fluorescence quenching ability.
Chen and coworkers have developed a multi-walled carbon nanotube (MWCNT) based on multicolor fluorescent nanobeacon for the determination of multiple DNA in the single solution with high sensitivity and selectivity [33-35]. Because the quenching capability of MWCNT, three DNA hairpin labled different dyes were adsorbed on the surface of MWCNT through π-π stacking interaction. In the presence of targets DNAs, target DNAs could hybridize with the corresponding probe, leading to the probe was away from the surface of MWCNT . Thus, gradual enhancement of fluorescence signals was observed with increasing the targets concentration. Importantly, the novel multicolor nanoprobes on the basis of MWCNTs were only modified with one fluorescence dye toward every target. Comparing to traditional MBs, the strategy was simple as well as low-cost. Furthermore, high sensitivity of the nanoprobe was exhibited by taking advantage of the adsorbability of MWCNTs and its ability to quench the fluorescence. In addition, Zhang et al. utilized a probe based on single-walled CNTs for the detection of thrombin and ATP (Fig. 5) . The aptamers modified with different kinds of fluorescence dyes were adsorbed on the CNTs respectively due to their strong π-π stacking interactions. Using the various fluorescence that emitted from different probes achieves the purpose of detecting thrombin and ATP. But they cannot do simultaneous detection of ATP and thrombin, and the sensitivity needs to be improved.
|Fig. 5. The detection strategy for thrombin and ATP based on single-walled CNTs. Copied with permission . Copyright 2011, Elsevier.|
Qian et al. developed a light-up fluorescent sensor for the determination of multiple DNA targets on the basis of singlestrand DNA functionalized graphene quantum dots (GQDs) and CNTs platform (Fig. 6) [38-40]. The sensor was composed of three parts, dual-color GQDs acting as signal reporter, single strand serving as recognition unit and CNTs as super quencher. In order to detect two targets in the meanwhile, two fluorescence sensors were simply mixed with CNTs and the formation of the corresponding assembly quenches the fluorescence of the sensor . It has been demonstrated that the fluorescence of GQDs was efficiently quenched by CNTs. In the presence of DNA target 1 (T1) and DNA target 2 (T2), T1 and T2 can hybridize with P1 and P2 in the assembly (P1 + P2)/CNTs to generate double-stranded DNA assembly P1/T1 and P2/T2 via their corresponding base pairing. The formed double-stranded DNAs were released from the CNTs. Therefore, two fluorescences, such as blue and green fluorescence, were observed when two DNA targets were present. The probe had good biocompatibility that enabled it to be applied for determination of two DNA targets in vivo. In addition, the limit of detection was founded to be 4.2 nmol/L toward T1 and 3.6 nmol/L toward T2, respectively, demonstrating high sensitivity toward two targets, which was on account of the high efficiency of GQDs. The probe displayed excellent linear correspondence between fluorescence signal versus concentration of T1 over the range from 6.9 to 80.0 nmol/L. A good linearity exists between the fluorescence signal of the probe and T2 concentration ranging from 8.2 nmol/L to 100 nmol/L. The proposed probe provided the capability to detection of two targets in the meanwhile. The method with high selectivity and sensitivity has high applicability for detection of multiple DNAs in vivo.
|Fig. 6. Schematic of multiple DNA targets detection on the basic of GQDs and CNTs platform. Copied with permission . Copyright 2014, Wiley Publishing Group.|
3. 2DMs detection 3.1. 2DMs electrochemical detection
2DMs like GO have good electrochemical properties and are widely used for electrochemical detection. Manoj et al. have developed a multiple host platform for the detection of H2O2 as well as glucose (Fig. 7) . First, the aldehyde modified ionic liquid was attached on the surface of reduced GO via π-π stacking interaction. Subsequently, either Azure mediator or glucose oxidase (GOx) enzyme was immobilized to the surface of reduced GO . Electroactive organic dye Azu-A with high solubility in aqueous media was attached to the host IL by utilizing the chemical reaction [43, 44]. The strategy exhibited good linear correlation toward H2O2 in the range of 0.03–1 mmol/L. And the detection limit for H2O2 was 11.5 μmol/L. Furthermore, the activity of GOx enzyme was remained after the enzyme was attached to the platform. Under the optimal conditions, an electrochemical sensor for the detection of glucose was developed in the presence of GOx enzyme. The current signals of the sensor and glucose concentration exhibited good linearity ranging from 0 to 200 mmol/L. The limit of detection was estimated to be 17 μmol/L. Moreover, the electrochemical sensor was employed to detect H2O2 in the presence of Azu-A as well as glucose upon the presence of GOx in the real sample. This method with a lower detection limit is difficult to apply in actual detection due to its complicated operation.
|Fig. 7. The mechanism of the GO-based sensor for monitoring H2O2 and glucose. Copied with permission . Copyright 2018, Elsevier.|
By utilizing GO loading nile blue (NB) , methyl blue (MB), and ferrocene (Fc) as platform in conjunction with anti-cytokine antibodies including IL-6, IL-1β, and TNF-α, Wei et al. have developed a robust electrochemical immunosensor for monitoring three cytokines IL-6, IL-1β, and TNF-α at the same time (Fig. 8) [12, 46]. The surface was designed through attaching 4-carboxylic phenyl as well as 4-aminophenyl phosphorylcholine (PPC) with mixed layers to the surface of glassy carbon surfaces . Subsequently, the carboxylic acid terminated sensing interface was modified with the capture monoclonal antibody toward IL-6, IL-1β, and TNF-α via forming covalent bond resulting in the formation of a sandwich assay. In the presence of target cytokines, the distinctively electrochemical signal changes from the immunsensor were observed, respectively. Gradual increase of the electrochemical signal was achieved along with the concentration of cytokine. In order to resist nonspecific protein adsorption, PPC, which was a zwitterionic molecule, was employed. In addition, the sensitivity as well as selectivity was improved by using PPC. Furthermore, aryldiazonium salt chemistry was employed for surface coupling of reagents, leading to enhance the stability of sensor. Then the designed immunosensor was successfully applied for determination of three cytokines in the meanwhile, as well as was used to monitor the level of cytokines in serum. The inventive method enables the simultaneous detection of three cytokines, which can be applied to monitor multiple biomolecules in complex biological environments.
|Fig. 8. Schematic illustration of the electrochemical sensor based on GO for the simultaneous detection of three cytokines IL-6, IL-1β, and TNF-α. Copied with permission . Copyright 2018, American Chemical Society.|
3.2. 2DMs fluorescence detection
Telomerases and microRNAs (miRNAs) are key biomarkers [48-50], which are associated with tumors. Monitoring telomerase activity and miRNA is contributed to improve specificity as well as reliability. Recently, a fluorescent probe platform for the determination of telomerase and miRNA-21 has been developed by our group on the basis of GO (Fig. 9) . The probe (GOFA) consisted of GO, template strand (TS) primer and telomerase/miR-21 modified with fluorescent. Due to π-π stacking interaction of GO , TS primer and the probe toward telomerase/miRNA-21 were adsorbed on GO, leading to the quenching of fluorescence. Nevertheless, the double-stranded oligonucleotide strand will be desorbed from the surface of GO on account of hybridization between the extended TS primer as well as telomerase, miRNA-21 and miRNA-21 probe upon addition of telomerase and miRNA-21. As a consequence, bright green as well as red fluorescence enhancement took place. GOFA was capable of detecting telomerase activity and miRNA-21 with low signal background, high sensitivity as well as easy of operation. In addition, GOFA can be prepared to monitor telomerase activity and miRNA-21 in tissue samples from living cells and cancer patients. The proposed strategy have shown huge potential in enhancing the efficiency of tumor treatment. Simultaneous detection of telomerase and miRNA that are important tumor markers is of great significance for the diagnosis and treatment of tumors.
|Fig. 9. Schematic design of the fluorescent sensor on the basic of GO for detecting telomerases and miRNAs. Copied with permission . Copyright 2019, Elsevier.|
A probe was constructed by Hu et al. based on graphitic carbon nitride (g-C3N4) for simultaneously monitoring multiple DNAs in homogenous solution . Due to the efficient quenching efficiency of g-C3N4, the multicolor DNA probes were adsorbed on g-C3N4, resulting in fluorescence quenching. When multiple DNA targets were hybridized with multicolor DNA probes, the single-stranded DNA modified with the fluorescent dye would detach from g-C3N4, and emit different fluorescence. The method can be used for the disease diagnosis and treatment with high sensitive and selective. A GO based biosensor was constructed by Cui et al. for simultaneously detecting multiple miRNAs in complex biological samples with high sensitivity, excellent selectivity, and low signal background .
Recently, our group combined the telomerase extension reaction and miRNA-induced rolling circle amplification [54-56], and then GO as well as nicking enzyme-aided signal amplification was employed for detecting the telomerase activity and miRNA-21 in urine samples [57, 58]. In particular, when telomerase was present, the primers of the TS were extended. The reaction product which contained the tandem sequence TTAGGG and miRNA were capable of hybridizing to multiplex telomerase molecular beacons (T-MBs) as well as miRNA molecular beacons (M-MBs) (Fig. 10) , leading to form a recognition site for the nicking enzyme. Subsequently, a nicking enzyme-aided recycle was employed to amplifying the fluorescence signal. Therefore, an increase of fluorescence signal at 520 nm was observed. Additionally, GO was developed to provide adsorption sites for the spare T-MBs and M-MBs, enabling lowing the background noise. For the detection of miRNA, the circulating probe was served as a template, and the target miRNA was prepared as a primer to commence a rolling circle amplification reaction under the action of phi29 DNA polymerase. The single-stranded DNA (ssDNA) which was from the rolling circle amplification reaction has a variety of duplicated sequences which were capable of hybridizing to M-MBs. Upon the M-MBs were attached to the product which was generated by the rolling circle amplification reaction, the recognition site for the nicking enzyme was established. When the nicking enzyme is present, the M-MBs will be cleaved and detached from the ssDNA. Then, the signal amplification occurred with the assistant of nicking enzyme. As a consequence, fluorescent signal at 610 nm increased drastically. When both telomerase and miRNA are present in the system, rolling circle amplification products as well as telomerase amplification took place simultaneously, producing multiple ssDNA with multiple repetitions. Subsequently, the two repeat sequences formed by telomerase amplification and rolling circle amplification products were hybridized with T-MBs and M-MBs. And double bands were formed at 520 nm and 610 nm. Thereafter, Nt. CviPII was digested and both the hybridized telomerase messenger and the hybridized miRNA messenger were simultaneously detached, which also allowed the intact telomerase messenger and miRNA messenger to bind to the repeat. Thus, the nicking enzyme enabled detection of oligonucleotide strands and proteins and increased their detection signals.
|Fig. 10. Illustration of the GO-based sensor for simultaneous quantification of telomerase and miRNA. Copied with permission . Copyright 2017, American Chemical Society.|
He et al. designed a multicolor fluorescent DNA nanoparticle based on GO for the rapid , and selective determination of target DNAs in the single solution. Due to the efficient quenching capability of GO (Fig. 11) [61, 62], the fluorescent single-stranded DNA probes exhibited a low background fluorescence. However, when the target was present, bright fluorescence was observed upon the formation of double helix, resulting in high signal to noise ratio. In particularly, the great large surface of GO endowed quenching multiple DNA probes which were modified with various types of fluorescent dyes in the meanwhile. That contributed to form a multicolor sensor for simultaneous determination of multiple target DNAs. The biosensing approach provided great potential for the detection of various biomolecules in the meanwhile and in the homogenous solution. This novel strategy has a low fluorescence background and is highly resistant to interference when detecting multiple DNAs in vivo. In addition, a GO-based biological sensor was developed by Wu and coworkers for the simultaneous determination of ochratoxin A and fumonisin B1 .
|Fig. 11. The mechanism of multicolor probes based on GO for the detection of multiplex DNAs. Copied with permission . Copyright 2010, Wiley Publishing Group.|
A GO-DNA nanoplatform was developed by Yu et al. for the determination of multiplex miRNAs . Different DNA probes were covalently linked to the surface of GO (Fig. 12). Each probe consisted of two parts, one specific sequence which was used to detect the target miRNA, another one with a fixed strand which was a complementary strand to the common anchor sequence. Owing to the fluorescence quenching capability of GO, the fluorescence of the probe was effectively quenched upon grafting to GO. In the presence of target miRNAs, miRNAs could hybridize with probes via complementary base-pairing reactions and formed DNA duplex. Therefore, probes were released from the GO, leading to fluorescence recovery. The fluorescence intensity of nanoplatform gradually increased as the concentration of targets increased from 0 to 1000 nmol/L. The limit of detection towards miRNA-21, 125b and let 7a was founded to 181 pmol/L, 136 pmol/L and 210 pmol/L, respectively, demonstrating high sensitivities for various miRNAs targets. Finally, the nanoplatform was employed to simultaneously monitor miRNA in living cells. This method has a lower detection limit for detecting multiple miRNAs, which will open a new gate for the simultaneous detection of other multiple biomolecules.
|Fig. 12. The detection strategy for miRNA-let 7a, miRNA-125b, and miRNA-21 based on GO. Copied with permission . Copyright 2018, Royal Society of Chemistry.|
Nanomaterials have been attracted much attention for application in sensing on account of extraordinary physical as well as chemical properties. By taking advantage of the high catalytic performance of nanomaterials, electrochemical sensors have been developed. Furthermore, fluorescence probe toward multiple biomolecules have been constructed by utilizing the unique photochemistry properties, such as the quenching capability of nanomaterials. Additionally, the sensitivity of these probes has also been improved because of the great surface area of nanomaterial compared to traditional material. In this review, the recent development for the homogenous determination of multiple biomolecules is summarized by applying nanomaterials including 1DMs and 2DMs.
Although nanomaterials have made a great progress in the detection of various biomolecules, there are several aspects that need to be refined in future research. In the development of detection technology, simultaneous detection of more than three biomolecules is yet to be designed. During the same detection system, the correlation between different biomolecules remains to be reinforced. The modification of nanomaterials will improve the physical and chemical properties of nanomaterials and increase the loading efficiency of nanomaterials. Thus, a lot of simple nanomaterial modification methods should be developed in future research work.Acknowledgments
This work is supported by the National Natural Science Foundation of China (Nos. 21525523, 21722507, 21574048, 21874121), the National Basic Research Program of China (973 Program, No. 2015CB932600), the National Key R & D Program of China (Nos. 2017YFA020800, 2016YFF0100800), Natural Science Foundation of Zhejiang Province of China (No. LY18B050002).
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