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Progress in Chemistry 2020, Vol. 32 Issue (5): 562-580 DOI: 10.7536/PC190914 Previous Articles   Next Articles

• Review •

Nanopore-Based Biomolecular Detection

Zihan Lin1,3, Huang Chen1, Jiawei Dong1, Daohui Zhao2,**(), Libo Li1,**()   

  1. 1. School of Chemistry and Chemical Engineering, South China University of Technology, Guangzhou 510640, China
    2. College of Chemistry and Chemical Engineering, Hubei University, Wuhan 430062, China
    3. Chucai College, Hubei University, Wuhan 430062, China
  • Received: Revised: Online: Published:
  • Contact: Daohui Zhao, Libo Li
  • About author:
    ** e-mail: (Daohui Zhao);
    (Libo Li)
  • Supported by:
    National Natural Science Foundation of China(21908046); State Key Laboratory of Pulp and Paper Engineering(SCUT201828); Hubei Natural Science Foundation(2019CFB293); Guangdong Natural Science Foundation(2019A1515011121); Guangzhou Technology Project(201804010219); Fundamental Research Funds for the Central Universities()
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Nanopore-based single molecular detection technology is a sensing technology that combines the advantages of simple operation, high sensitivity, fast speed, and no labeling. It is widely used in protein detection, gene sequencing, and marker detection. The cost, sensitivity and accuracy are the main challenges in developing such technology, and to develop new nanopore materials is the key to solve them. From the perspective of selecting and designing nanopore materials, the application status of three different nanopores: biological nanopore, solid-state nanopore and novel two-dimensional(2D) material nanopore in biomolecule detection are reviewed. Meanwhile, the differences between biological nanopores and solid-state nanopores are compared in details. The article also emphasizes the experimental and simulation research progress of 2D material nanopores in biomolecule detection. Finally, the future development of nanopore-based detection technology is also discussed.

Contents

1 Introduction

2 Basic principles and molecular simulation methods of nanopore-based single molecule detection technology

2.1 The basic principle of nanopore detection

2.2 Molecular dynamics simulation

3 Application of nanopores in biomolecular detection

3.1 Application of biological nanopore in biomolecule detection

3.2 Application of solid-state nanopores in biomolecule detection

3.3 Comparison of biological nanopores and solid-state nanopores

4 Biomolecular detection with two-dimensional(2D) material nanopore

4.1 Introduction to 2D materials

4.2 Experimental study of 2D nanopore in biomolecule detection

4.3 Simulation study of 2D nanopore in biomolecule detection

5 Conclusion and outlook

Key words: nanopore, single molecule detection, protein detection, DNA sequencing, ion current
Fig. 1 Development of next-generation sequencing technologies during 2004~2015[5]. Reproduced with permission from copyright(2017) Nature Publishing Group
Table 1 Comparison of available sequencing platforms[5]
Company Detection length Application range Website
454/Roche 400 bp(single end) Bacterial and viral genomes, multiplex PCR products, verification of point mutations, target detection of somatic mutations http://www.454.com/
Illumina 150~300 bp(paired end) Complex genomes(human, mouse and plant) and a wide range of gene applications, RNA sequences, hybrid or multiplex PCR products, somatic mutation detection, forensics, noninvasive prenatal diagnosis http://www.illumina.com/
ABI SOLiD 75 bp(single end) or 50 bp(paired end) Complex genomes(human, mouse and plant) and a wide range of gene applications, RNA sequences, hybrid or multiplex PCR products, somatic mutation detection http://www.thermofisher.com/
Pacific Biosciences Up to 40 kb(single end or circular consensus) Complex genomes(human, mouse and plant), microbial and infectious disease genes, transcriptional fusion detection, methylation detection http://www.pacb.com/
Ion Torrent 200~400 bp(single end) Multiplex PCR products, microbial and infectious disease genes, somatic mutation detection, point mutation verification http://www.thermofisher.com/
Oxford Nanopore Variable(1D or 2D reads) Pathogen monitoring, targeted mutations, metagenomics, bacterial and viral genes http://nanoporetech.com/
Qiagen GenReader 107 bp(single end) Targeted mutation detection, liquid biopsy in cancer http://www.genereaderngs.com/
Fig. 2 Schematic diagram of ionic current blockage method[26]
Table 2 The sensing principles of three electronic sensing technologies[19]. Reproduced with permission from copyright(2014), Royal Society of Chemistry
Detection technology Detection principle Advantage ref
By removing ions in the nanopore, the resistance of the nanopore ρL/πr 2(ρ, solution resistivity; L, pore length, and r, radius) is increased. The electric signal is obtained by changing the ion current of the Ag/AgCl electrode at the top and bottom of the nanopore. The experimental device is simple, requiring only a single molecular size nanopore. Although the current depends on the concentration of the electrolyte, a relatively large current can be observed. 26
The tunneling current(It ) is detected during the perforation of the test object. The conductivity of the target single molecule is measured by the nanogap electrode embedded in the nanopore. High spatial resolution is obtained by tunneling current, and DNA sensing based on single base recognition has been confirmed. 29
The potential change in the nanopore caused by the analyte molecule with charge q can be detected as the modulation of the gate voltage(ΔVg =Δq/C) by using a MOSFET device embedded in the nanopore. The embedded MOSFET has high-speed performance and fast operation is feasible. The bottom-up process can be integrated by using the nanowire FET and graphene nanoribbon. 30
Fig. 3 Development of nanopore-based single-molecule detection technologies[42]. Reproduced with permission from copyright(2016) Nature Publishing Group
Table 3 Details of commonly utilized biological nanopores
Nanopore pore size/nm Analyte ref
α-HL 1.4 Metal ions, organic small molecules, RNA, ssDNA, amino acids, unfolded proteins,
polymers, gold nanoparticles		 [7AHL] 45
MspA 1.2 ssDNA、dsDNA [1UUN] 51
Aerolysin 1~1.7 peptide, protein, DNA, RNA, organic small molecule [5JZT] 49, 52~61
OmpG ~2 Protein, antibody [2F1C] 62
FhuA ~2.4 Protein, Protein-ssDNA, polymer [1BY3] 63
Phi29 3.6 ssDNA, dsDNA, Thioester antibody [1FOU] 64
SP1 ~3 ssDNA [1TRO] 65
ClyA 3.3~4.2 ssDNA, protein [2WCD] 66
VDAC 2.5~3 Tubulin, organic small molecule, dsDNA [2JK4] 67
Fig. 4 Applications of biological nanopores for the detection of nucleotides.(a~c) Detection of oligonucleotides(polydeoxyadenines(dAn), n=2, 3, 4, 5, 10) with an aerolysin pore[49]. (a) Schematic illustration of a short oligonucleotide passing through an aerolysin nanopore.(b) Representative current traces recorded without dAn and with the addition of dAn. The red triangles denote typical blockades shown in the insets.(c) Histogram for the blockade events associated with dAn with Gaussian fits.(d~f) Detection of dsDNA with phi29 nanopore[68].(d) Illustration of dsDNA translocating through a phi29 nanopore.(e) Schematic and 2D sequence of 35 bp dsDNA. Typical current trace showing the translocation of 35 bp dsDNA showing single-level events.(f) Schematic and 2D sequences of double crossover DNA(DX-DNA). Typical current trace showing the translocation of DX-DNA showing double-level events. Reproduced with permission from copyright(2016) Nature Publishing Group
Fig. 5 Applications of biological nanopores in detecting proteins. Indirect detection of protein molecules with α-HL. Comparison of current modulations measured for the initial peptide substrate and its cleaved products can be performed to determine trypsin activities[80]. Reproduced with permission from copyright(2016) American Chemical Society
Table 4 Characteristics of solid-state nanopores
Material Minimum pore size Analyte ref
SiN 3 nm RNA + drug 92
3.7 nm dsDNA + γ-PNA 93
3~20 nm RNAP + DNA 94
SiN/SiO2/SiN 20 nm histone nucleosome 95
HfO2/SiNx < 2 nm(HfO2) ssDNA 96
dsDNA
graphene/SiO2 22 nm(single layer) λ-DNA 97
graphene/SiNx 5 nm(1~2 layers) 10 kb-DNA 12
Al2O3/graphene/Al2O3 9 nm(graphene) dsDNA 98
dsDNA+protein
TiO2/graphene/SiN/SiO2 8 nm(3~15 layers) 15 kb-DNA 99
chemical modified graphene 5~15 nm ssDNA 100
MoS2/SiNx 5 nm(few-layer MoS2) λ-DNA 101
DNA Origami/SiN 15 nm(DNA origami) dsDNA 102
chemical modified SiN 40 nm(SiN) protein 103
25 nm(modified SiN)
chemical modified Au/SiN 20~25 nm(modified Au) His-tagged protein 104
IgG-antiboby
Fig. 6 Detection of various dsDNA structures with a 2.5 nm SiNx nanopore[111]. The picture shows the system diagram of DNA products and mismatched DNA products(left), typical current trace(middle), semi-logarithmic plot of residence time(right). Reproduced with permission from copyright(2015) American Chemical Society
Fig. 7 Schematic illustration of different kinds of typical ultrathin 2D nanomaterials[120]. Copyright 2015, American Chemical Society
Fig. 8 Schematic representation of DNA translocation through long channel nanopores and 2D nanopores[125]. Copyright 2016, Royal Society of Chemistry
Table 5 Experiments of biomolecule detection by 2D materials
Material Nano device Signal characteristics Biomolecular size Ion concentration ref
Graphene Nanopore(5~25 nm) Unfolded > partial folded > fully folded λ-dsDNA(16 μm long) 1 M KCl 97
Graphene Nanopore(5~10 nm) Low SNR, fully folded > unfolded dsDNA(15 kbp) 1 M KCl 99
Graphene Nanopore(5 nm) folded > unfolded dsDNA 3 M KCl 12
Graphene Nanopore(15~20 nm) precision:1 M LiCl > 1 M KCl ≈ 1 M NaCl dsDNA(48.5 kbp) 1 M KCl, 1 M
NaCl, 1 M LiCl		 131
Graphene Nanoribbon Blocking current + transverse current dsDNA(2.7 kbp) 1 M KCl 132
Graphene Nanopore folded > unfolded dsDNA 3 M KCl 100
Graphene Nanopore(2.5~5 nm) Aperture dependent dsDNA(10 kbp) 3 M KCl 133
Graphene Nanopore Conductivity + ionic current dsDNA(2.7 kbp) 1 M KCl 132
MoS2 Nanopore(5 nm) High SNR(> 10) dsDNA(48 kbp) 2 M KCl 101
MoS2 Nanopore(~2.8 nm) polyA30 > polyT30 > polyC30 > polyG30 dsDNA(48.5 kbp) 2 M KCl 14
h-BN Nanopore(12.3 nm) Unfolded > Partially folded dsDNA(10 kbp) 3 M KCl 13
Au Transistor Conductivity poly(GATC)x 134
Fig. 9 Experimental studies on DNA sequencing using graphene nanopores. (a) Dekker lab[97], the non-folded, partially folded and folded dsDNA could be identified by blockade current. Copyright(2010) American Chemical Society.(b) Golovchenko lab[12], the non-folded and folded dsDNA could be identified. Copyright(2010) Nature Publishing Group.(c) Drndic lab[99], the non-folded and folded dsDNA could be identified. Copyright(2010) American Chemical Society.(d) Bashir lab[98]. Copyright(2012) American Chemical Society
Fig. 10 (a) Schematic illustration of DNA sequencing using a MoS2 nanopore[101].(b) Optical image of a freshly exfoliated monolayer MoS2 flake.(c) Optical image after the chosen flake has been transferred to the desired location.(d) A typical trace(in blue) of λ-DNA translocation through a 20 nm MoS2 nanopore. The upper trace(in black) is an example of λ-DNA translocation through a SiN x nanopore.(e) Selected individual events with quantized current drops implying multiple conformations of λ-DNA within the nanopore, i.e., unfolded(1), partially folded(2), folded(3), and bumping event(4). Reproduced with permission from copyright(2014) American Chemical Society
Table 6 Theoretical simulations f biomolecule detection by 2D materials
Material Pore size
(nm)		 Simulation method Signal characteristics Molecular size Ion concentration ref
graphene 2.4 MD poly(G-C) > poly(A-T) 45 bases 1 M KCl 142
graphene 1.1~1.5 MD+BD poly(A)≈poly(G)< poly(T) < poly(C) 20 bases 1.7 M KCl 143
graphene 1.6~5.0 MD The SNR increases with the decrease of aperture 45 bases 1.0 M KCl 144
graphene 2.0~3.0 MD Conductivity is related to pore thickness 12 bases 1.0 M NaCl 129
graphene 2.4 MD The fluctuation of signal is related to the DNA structure 48 bases 1.0 M NaCl 145
graphene 1.5 MD Increasing the number of graphene layers can improve the accuracy 45 bases 1.0 M KCl 146
graphene 1.6 MD The charge regulates DNA perforation 20 bases 1.0 M KCl 147
graphene 2.1 MD Hybrid hole can improve the detection accuracy 20 bases 1.0 M NaCl 148
graphene 1.6 MD Ion current + perforation time 15 bases 1.0 M KCl 149
graphene 2.2 MD The perforation rate is related to the type of polypeptide and the number of graphene layers 48 residues 1.0 M KCl 150
graphene 10 MD IgG3 > IgG2 IgG 0.5 M NaCl 151
MoS2 2.3 MD+DFT SNR > 15 16 bases 1.0 M NaCl 130
MoS2 2.5 MD+DFT Pull force + ionic current 6 bases 5 mM KCl 152
h-BN 2.4 MD poly(A-T)40 <poly(G-C)40 40 bases 1.0 M KCl 153
graphene 1.5 SMD Pull force + ionic current Thioredoxin 2 M KCl 154
graphene 1.0 SMD G > A > T > C 11 bases 155
graphene 1.0 SMD G > A > T > C 12 bases 156
graphene 1.1 SMD Dependent on the structure of the hole 6 bases 157
graphene 1.6, 2.4 SMD Independent of pore size and shape 14 bases 1 M KCl 158
Fig. 11 (a) DNA translocation through a MoS2 nanopore.(b) Ionic current for different bases and combination of CG or AT bases through the MoS2 nanopore.(c) Signal-to-noise ratio of MoS2 nanopore for different biases and temperatures[130]. Copyright 2014 American Chemical Society
Fig. 12 Simulation system of DNA methylation detection with 2D material nanopores[161].(a) Schematic showing a CpG dinucleotide site in an mDNA molecule in complex with a MBD1 protein.(b) Schematic of the simulated nanopore device. Reproduced with permission from copyright(2017) Nature Publishing Group
Fig. 13 Schematic diagram of DNA translocation through graphene nanopore by SMD simulations, and the characteristic force peaks for different bases[155]. Reproduced with permission from copyright(2014) American Chemical Society
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Abstract

Nanopore-Based Biomolecular Detection