Skip to main content
Log in

Modern Methods for Assessment of microRNAs

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

The review discusses modern methods for the quantitative and semi-quantitative analysis of miRNAs, which are small non-coding RNAs affecting numerous biological processes such as development, differentiation, metabolism, and immune response. miRNAs are considered as promising biomarkers in the diagnosis of various diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

Abbreviations

CEAM:

cyclic enzymatic amplification method

CRISPR/Cas:

clustered regularly interspaced palindromic repeats/CRISPR associated protein

CHA:

catalytic hairpin assembly

EXPAR:

exponential amplification reaction

HCR:

hybridization chain reaction

HRCA:

hyperbranched rolling circle amplification

ICSDP:

isothermal circular-strand-displacement polymerization

LAMP:

loop-mediated isothermal amplification

PCR:

polymerase chain reaction

RCA:

rolling circle amplification

SEXPAR:

symmetric exponential amplification reaction

References

  1. Bodulev, O. L., and Sakharov, I. Y. (2020) Isothermal nucleic acid amplification techniques and their use in bioanalysis, Biochemistry (Moscow), 85, 147-166, https://doi.org/10.1134/S0006297920020030.

    Article  CAS  Google Scholar 

  2. Pritchard, C. C., Cheng, H. H., and Tewari, M. (2012) MicroRNA profiling: Approaches and considerations, Nat. Rev. Genet., 13, 358-369, https://doi.org/10.1038/nrg3198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. De Planell-Saguer, M., and Rodicio, M. C. (2011) Analytical aspects of microRNA in diagnostics: A review, Anal. Chim. Acta, 699, 134-152, https://doi.org/10.1016/j.aca.2011.05.025.

    Article  CAS  PubMed  Google Scholar 

  4. Ragan, C., Zuker, M., and Ragan, M. A. (2011) Quantitative prediction of miRNA-mRNA interaction based on equilibrium concentrations, PLoS Comput. Biol., 7, e1001090, https://doi.org/10.1371/journal.pcbi.1001090.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Kozomara, A., Birgaoanu, M., and Griffiths-Jones, S. (2019) miRBase: From microRNA sequences to function, Nucleic Acids Res., 47, D155-D162, https://doi.org/10.1093/nar/gky1141.

    Article  CAS  PubMed  Google Scholar 

  6. Plotnikova, O., Baranova, A., and Skoblov, M. (2019) Comprehensive analysis of human microRNA–mRNA interactome, Front. Genet., 10, 933, https://doi.org/10.3389/fgene.2019.00933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Krol, J., Loedige, I., and Filipowicz, W. (2010) The widespread regulation of microRNA biogenesis, function and decay, Nat. Rev. Genet., 11, 597-610, https://doi.org/10.1038/nrg2843.

    Article  CAS  PubMed  Google Scholar 

  8. Katoh, T., Sakaguchi, Y., Miyauchi, K., Suzuki, T., Kashiwabara, S. I., et al. (2009) Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly (A) polymerase GLD-2, Genes Dev., 23, 433-438, https://doi.org/10.1101/gad.1761509.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14, Cell, 75, 843-854, https://doi.org/10.1016/0092-8674(93)90529-Y.

    Article  CAS  PubMed  Google Scholar 

  10. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions, Cell, 136, 215-233, https://doi.org/10.1016/j.cell.2009.01.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Liang, Y., Ridzon, D., Wong, L., and Chen, C. (2007) Characterization of microRNA expression profiles in normal human tissues, BMC Genom., 8, 1-20, https://doi.org/10.1186/1471-2164-8-166.

    Article  CAS  Google Scholar 

  12. Wienholds, E., Kloosterman, W. P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., et al. (2005) MicroRNA expression in zebrafish embryonic development, Science, 309, 310-311, https://doi.org/10.1126/science.1114519.

    Article  CAS  PubMed  Google Scholar 

  13. Alvarez-Garcia, I., and Miska, E. A. (2005) MicroRNA functions in animal development and human disease, Development, 132, 4653-4662, https://doi.org/10.1242/dev.02073.

    Article  CAS  PubMed  Google Scholar 

  14. Lu, J., Getz, G., Miska, E.A., Alvarez-Saavedra, E., Lamb, J., et al. (2005) MicroRNA expression profiles classify human cancers, Nature, 435, 834-838, https://doi.org/10.1038/nature03702.

    Article  CAS  PubMed  Google Scholar 

  15. Lee, J. S., Ahn, Y. H., Won, H. S., Sun, D. S., Kim, Y. H., et al. (2017) Prognostic role of the microRNA-200 family in various carcinomas: a systematic review and meta-analysis, BioMed Res. Int., 2017, https://doi.org/10.1155/2017/1928021.

    Google Scholar 

  16. Zhang, L., Wu, H., Zhao, M., and Lu, Q. (2020) Identifying the differentially expressed microRNAs in autoimmunity: a systemic review and meta-analysis, Autoimmunity, 53, 122-136, https://doi.org/10.1080/08916934.2019.1710135.

    Article  CAS  PubMed  Google Scholar 

  17. He, M., Zhang, H. N., Tang, Z. C., Gao, S. G. (2021) Diagnostic and therapeutic potential of exosomal microRNAs for neurodegenerative diseases, J. Neural Transplant. Plast., 2021, https://doi.org/10.1155/2021/8884642.

    Google Scholar 

  18. Ono, K., Kuwabara, Y., and Han, J. (2011) MicroRNAs and cardiovascular diseases, FEBS J., 278, 1619-1633, https://doi.org/10.1111/j.1742-4658.2011.08090.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., et al. (2004) Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation, Genome Biol., 5, 1-11, https://doi.org/10.1186/gb-2004-5-3-r13.

    Article  Google Scholar 

  20. Wightman, B., Ha, I., Ruvkun, G. (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans, Cell, 75, 855-862, https://doi.org/10.1016/0092-8674(93)90530-4.

    Article  CAS  PubMed  Google Scholar 

  21. Válóczi, A., Hornyik, C., Varga, N., Burgyán, J., Kauppinen, S., et al. (2004) Sensitive and specific detection of microRNAs by northern blot analysis using LNA-modified oligonucleotide probes, Nucleic Acids Res., 32, e175, https://doi.org/10.1093/nar/gnh171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Várallyay, E., Burgyán, J., and Havelda, Z. (2008) MicroRNA detection by northern blotting using locked nucleic acid probes, Nat. Protoc., 3, 190-196, https://doi.org/10.1038/nprot.2007.528.

    Article  CAS  PubMed  Google Scholar 

  23. Pall, G. S., Codony-Servat, C., Byrne, J., Ritchie, L., and Hamilton, A. (2007) Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot, Nucleic Acids Res., 35, e60, https://doi.org/10.1093/nar/gkm112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ramkissoon, S. H., Mainwaring, L. A., Sloand, E. M., Young, N. S., and Kajigaya, S. (2006) Nonisotopic detection of microRNA using digoxigenin labeled RNA probes, Mol. Cell. Probes, 20, 1-4, https://doi.org/10.1016/j.mcp.2005.07.004.

    Article  CAS  PubMed  Google Scholar 

  25. Kim, S. W., Li, Z., Moore, P. S., Monaghan, A. P., Chang, Y., et al. (2010) A sensitive non-radioactive northern blot method to detect small RNAs, Nucleic Acids Res., 38, e98, https://doi.org/10.1093/nar/gkp1235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Johnson, B. N., and Mutharasan, R. (2014) Biosensor-based microRNA detection: techniques, design, performance, and challenges, Analyst, 139, 1576-1588, https://doi.org/10.1039/C3AN01677C.

    Article  CAS  PubMed  Google Scholar 

  27. Dong, H., Lei, J., Ding, L., Wen, Y., Ju, H., et al. (2013) MicroRNA: function, detection, and bioanalysis, Chem. Rev., 113, 6207-6233, https://doi.org/10.1021/cr300362f.

    Article  CAS  PubMed  Google Scholar 

  28. Shimomura, A., Shiino, S., Kawauchi, J., Takizawa, S., Sakamoto, H., et al. (2016) Novel combination of serum microRNA for detecting breast cancer in the early stage, Cancer Sci., 107, 326-334, https://doi.org/10.1111/cas.12880.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gungormez, C., Aktas, H. G., Dilsiz, N., and Borazan, E. (2019) Novel miRNAs as potential biomarkers in stage II colon cancer: microarray analysis, Mol. Biol. Rep., 46, 4175-4183, https://doi.org/10.1007/s11033-019-04868-7.

    Article  CAS  PubMed  Google Scholar 

  30. Li, W., and Ruan, K. (2009) MicroRNA detection by microarray, Anal. Bioanal. Chem., 394, 1117-1124, https://doi.org/10.1007/s00216-008-2570-2.

    Article  CAS  PubMed  Google Scholar 

  31. Ueno, T., and Funatsu, T. (2014) Label-free quantification of microRNAs using ligase-assisted sandwich hybridization on a DNA microarray, PLoS One, 9, e90920, https://doi.org/10.1371/journal.pone.0090920.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wang, H., Ach, R. A., and Curry, B. O. (2007) Direct and sensitive miRNA profiling from low-input total RNA, RNA, 13, 151-159, https://doi.org/10.1261/rna.234507.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Castoldi, M., Schmidt, S., Benes, V., Noerholm, M., Kulozik, A. E., et al. (2006) A sensitive array for microRNA expression profiling (miChip) based on locked nucleic acids (LNA), RNA, 12, 913-920, https://doi.org/10.1261/rna.2332406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Liu, C. G., Calin, G. A., Volinia, S., and Croce, C. M. (2008) MicroRNA expression profiling using microarrays, Nat. Protoc., 3, 563-578, https://doi.org/10.1038/nprot.2008.14.

    Article  CAS  PubMed  Google Scholar 

  35. Tian, R., Ning, W., Chen, M., Zhang, C., Li, Q., et al. (2019) High performance electrochemical biosensor based on 3D nitrogen-doped reduced graphene oxide electrode and tetrahedral DNA nanostructure, Talanta, 194, 273-281, https://doi.org/10.1016/j.talanta.2018.09.110.

    Article  CAS  PubMed  Google Scholar 

  36. Kutluk, H., Bruch, R., Urban, G. A., and Dincer, C. (2020) Impact of assay format on miRNA sensing: Electrochemical microfluidic biosensor for miRNA-197 detection, Biosens. Bioelectron., 148, 111824, https://doi.org/10.1016/j.bios.2019.111824.

    Article  CAS  PubMed  Google Scholar 

  37. Smith, D. A., Simpson, K., Cicero, M. L., Newbury, L. J., Nicholas, P., et al. (2021) Detection of urinary microRNA biomarkers using diazo sulfonamide-modified screen-printed carbon electrodes, RSC Adv., 11, 18832-18839, https://doi.org/10.1039/D0RA09874D.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Bodulev, O. L., and Sakharov, I. Y. (2019) Chemiluminescent determination of microRNA-141 using target-dependent activation of the peroxidase-mimicking DNAzyme, Anal. Lett., 52, 813-824, https://doi.org/10.1080/00032719.2018.1498506.

    Article  CAS  Google Scholar 

  39. Lai, M., and Slaughter, G. (2019) Label-free MicroRNA optical biosensors, Nanomaterials, 9, 1573, https://doi.org/10.3390/nano9111573.

    Article  CAS  PubMed Central  Google Scholar 

  40. Xue, T., Liang, W., Li, Y., Sun, Y., Xiang, Y., et al. (2019) Ultrasensitive detection of miRNA with an antimonene-based surface plasmon resonance sensor, Nat. Commun., 10, 1-9, https://doi.org/10.1038/s41467-018-07947-8.

    Article  CAS  Google Scholar 

  41. Chen, C., Ridzon, D. A., Broomer, A. J., Zhou, Z., Lee, D. H., et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR, Nucleic Acids Res., 33, e179, https://doi.org/10.1093/nar/gni178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lao, T. D., and Le, T. A. H. (2020) Development of stem-loop real-time PCR technique for miRNA-141 expression analysis in nasopharyngeal carcinoma, Asian J. Pharm. Res. Health Care, 11, 30-36, https://doi.org/10.18311/ajprhc/2019/24990.

    Article  Google Scholar 

  43. Xu, Y. F., Hannafon, B. N., Khatri, U., Gin, A., and Ding, W. Q. (2019) The origin of exosomal miR-1246 in human cancer cells, RNA Biol., 16, 770-784, https://doi.org/10.1080/15476286.2019.1585738.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Zhang, L., Lin, J., Ye, Y., Oba, T., Gentile, E., et al. (2018) Serum microRNA-150 predicts prognosis for early-stage non-small cell lung cancer and promotes tumor cell proliferation by targeting tumor suppressor gene SRCIN1, Clin. Pharmacol. Ther., 103, 1061-1073, https://doi.org/10.1002/cpt.870.

    Article  CAS  PubMed  Google Scholar 

  45. Konoshenko, M. Y., Lekchnov, E. A., Bryzgunova, O. E., Zaporozhchenko, I. A., Yarmoschuk, S. V., et al. (2020) The panel of 12 cell-free microRNAs as potential biomarkers in prostate neoplasms, Diagnostics, 10, 38, https://doi.org/10.3390/diagnostics10010038.

    Article  CAS  PubMed Central  Google Scholar 

  46. Androvic, P., Valihrach, L., Elling, J., Sjoback, R., and Kubista, M. (2017) Two-tailed RT-qPCR: A novel method for highly accurate miRNA quantification, Nucleic Acids Res., 45, e144, https://doi.org/10.1093/nar/gkx588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Raabe, C. A., Tang, T. H., Brosius, J., and Rozhdestvensky, T. S. (2014) Biases in small RNA deep sequencing data, Nucleic Acids Res., 42, 1414-1426, https://doi.org/10.1093/nar/gkt1021.

    Article  CAS  PubMed  Google Scholar 

  48. Zhang, J., Li, Z., Wang, H., Wang, Y., Jia, H., and Yan, J. (2011) Ultrasensitive quantification of mature microRNAs by real-time PCR based on ligation of a ribonucleotide-modified DNA probe, Chem. Commun., 47, 9465-9467, https://doi.org/10.1039/C1CC13466C.

    Article  CAS  Google Scholar 

  49. Tian, H., Sun, Y., Liu, C., Duan, X., Tang, W., et al. (2016) Precise quantitation of microRNA in a single cell with droplet digital PCR based on ligation reaction, Anal. Chem., 88, 11384-11389, https://doi.org/10.1021/acs.analchem.6b01225.

    Article  CAS  PubMed  Google Scholar 

  50. Zhao, G., Jiang, T., Liu, Y., Huai, G., Lan, C., et al. (2018) Droplet digital PCR-based circulating microRNA detection serve as a promising diagnostic method for gastric cancer, BMC Cancer, 18, 1-10, https://doi.org/10.1186/s12885-018-4601-5.

    Article  CAS  Google Scholar 

  51. Cirillo, P. D., Margiotti, K., Mesoraca, A., and Giorlandino, C. (2020) Quantification of circulating microRNAs by droplet digital PCR for cancer detection, BMC Res. Notes, 13, 1-6, https://doi.org/10.1186/s13104-020-05190-3.

    Article  CAS  Google Scholar 

  52. Friedländer, M. R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., et al. (2008) Discovering microRNAs from deep sequencing data using miRDeep, Nat. Biotechnol., 26, 407-415, https://doi.org/10.1038/nbt1394.

    Article  CAS  PubMed  Google Scholar 

  53. Dave, V. P., Ngo, T. A., Pernestig, A. K., Tilevik, D., Kant, K., et al. (2019) MicroRNA amplification and detection technologies: opportunities and challenges for point of care diagnostics, Lab. Invest., 99, 452-469, https://doi.org/10.1038/s41374-018-0143-3.

    Article  CAS  PubMed  Google Scholar 

  54. Castoldi, M., Collier, P., Nolan, T., and Benes, V. (2013) Expression profiling of microRNAs by quantitative real-time PCR: the good, the bad, and the ugly, PCR Technology: Current Innovations, 307-319, Boca Raton, FL: CRC Press.

  55. Borst, A., Box, A. T. A., and Fluit, A. C. (2004) False-positive results and contamination in nucleic acid amplification assays: suggestions for a prevent and destroy strategy, Eur. J. Clin. Microbiol. Infect. Dis., 23, 289-299, https://doi.org/10.1007/s10096-004-1100-1.

    Article  CAS  PubMed  Google Scholar 

  56. García, P. B., Robledo, N. L., and Islas, A. L. (2004) Analysis of non-template-directed nucleotide addition and template switching by DNA polymerase, Biochemistry, 43, 16515-16524, https://doi.org/10.1021/bi0491853.

    Article  CAS  PubMed  Google Scholar 

  57. Lomidze, L., Williford, T. H., Musier-Forsyth, K., and Kankia, B. (2018) Isothermal amplification of long DNA segments by quadruplex priming amplification, Anal. Methods, 10, 2972-2979, https://doi.org/10.1039/C8AY00843D.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Jonstrup, S. P., Koch, J., and Kjems, J. (2006) A microRNA detection system based on padlock probes and rolling circle amplification, RNA, 12, 1747-1752, https://doi.org/10.1261/rna.110706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Wu, X., Zhu, S., Huang, P., and Chen, Y. (2016) Highly specific quantification of microRNA by coupling probe–rolling circle amplification and Förster resonance energy transfer, Anal. Biochem., 502, 16-23, https://doi.org/10.1016/j.ab.2016.03.001.

    Article  CAS  PubMed  Google Scholar 

  60. Li, R., Liu, Q., Jin, Y., and Li, B. (2020) Sensitive colorimetric determination of microRNA let-7a through rolling circle amplification and a peroxidase-mimicking system composed of trimeric G-triplex and hemin DNAzyme, Microchim. Acta, 187, 1-8, https://doi.org/10.1007/s00604-019-4093-2.

    Article  CAS  Google Scholar 

  61. Kumara, G. S. R., Pandith, A., and Seo, Y. J. (2020) Highly fluorescent morpholine naphthalimide deoxyuridine nucleotide for the detection of miRNA 24-3P through rolling circle amplification, Analyst, 145, 4777-4781, https://doi.org/10.1039/D0AN00723D.

    Article  Google Scholar 

  62. Zhou, Y., Huang, Q., Gao, J., Lu, J., Shen, X., et al. (2010) A dumbbell probe-mediated rolling circle amplification strategy for highly sensitive microRNA detection, Nucleic Acids Res., 38, e156, https://doi.org/10.1093/nar/gkq556.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Li, R., Wang, Y., Wang, P., and Lu, J. (2017) A dual discrimination mode for improved specificity towards let-7a detection via a single-base mutated padlock probe-based exponential rolling circle amplification, Luminescence, 32, 1574-1581, https://doi.org/10.1002/bio.3362.

    Article  CAS  PubMed  Google Scholar 

  64. Liu, H., Li, L., Duan, L., Wang, X., Xie, Y., Tong, L., et al. (2013) High specific and ultrasensitive isothermal detection of microRNA by padlock probe-based exponential rolling circle amplification, Anal. Chem., 85, 7941-7947, https://doi.org/10.1021/ac401715k.

    Article  CAS  PubMed  Google Scholar 

  65. Chen, S., Zhao, J., Xu, C., Sakharov, I. Y., and Zhao, S. (2021) Absolute quantification of microRNAs in a single cell with chemiluminescence detection based on rolling circle amplification on a microchip platform, Anal. Chem., 93, 9218-9225, https://doi.org/10.1021/acs.analchem.1c01463.

    Article  CAS  PubMed  Google Scholar 

  66. Zhang, X., Liu, Y., Yang, Y., Huang, J., Wang, H., et al. (2018) Ligation-promoted hyperbranched rolling circle amplification enables ultrasensitive detection of microRNA in clinical specimens, Sens. Actuators B Chem., 277, 634-639, https://doi.org/10.1016/j.snb.2018.09.058.

    Article  CAS  Google Scholar 

  67. Bodulev, O. L., and Sakharov, I. Y. (2022) Microtiter-plate chemiluminescence method for the determination of MicroRNA-141 based on the application of catalytic hairpin assembly and a streptavidin–polyperoxidase conjugate, J. Anal. Chem., 77, 450-457, https://doi.org/10.1134/S1061934822040050.

    Article  CAS  Google Scholar 

  68. Eslamizadeh, S.., Heidari, M., Agah, S., Faghihloo, E., Ghazi, H., et al. (2018) The role of microRNA signature as diagnostic biomarkers in different clinical stages of colorectal cancer, Cell J., 20, 220, https://doi.org/10.22074/cellj.2018.5366.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Zhang, S., Liu, C., Zou, X., Geng, X., Zhou, X., et al. (2021) MicroRNA panel in serum reveals novel diagnostic biomarkers for prostate cancer, PeerJ, 9, e11441, https://doi.org/10.7717/peerj.11441.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Zyrina, N. V., and Antipova, V. N. (2021) Nonspecific synthesis in the reactions of isothermal nucleic acid amplification, Biochemistry (Moscow), 86, 887-897, https://doi.org/10.1134/S0006297921070099.

    Article  CAS  Google Scholar 

  71. Van Ness, J., Van Ness, L. K., and Galas, D. J. (2003) Isothermal reactions for the amplification of oligonucleotides, Proc. Natl. Acad. Sci. USA, 100, 4504-4509, https://doi.org/10.1073/pnas.0730811100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Jia, H., Li, Z., Liu, C., and Cheng, Y. (2010) Ultrasensitive detection of microRNAs by exponential isothermal amplification, Angew. Chem. Int. Ed., 49, 5498-5501, https://doi.org/10.1002/anie.201001375.

    Article  CAS  Google Scholar 

  73. Wu, H., Wu, J., Liu, Y., Wang, H., and Zou, P. (2019) Fluorometric determination of microRNA using arched probe-mediated isothermal exponential amplification combined with DNA-templated silver nanoclusters, Microchim. Acta, 186, 1-8, https://doi.org/10.1007/s00604-019-3836-4.

    Article  CAS  Google Scholar 

  74. Reid, M. S., Le, X. C., and Zhang, H. (2018) Exponential isothermal amplification of nucleic acids and assays for proteins, cells, small molecules, and enzyme activities: An EXPAR example, Angew. Chem. Int. Ed., 57, 11856-11866, https://doi.org/10.1002/anie.201712217.

    Article  CAS  Google Scholar 

  75. Chen, J., An, T., Ma, Y., Situ, B., Chen, D., et al. (2018) Isothermal amplification on a structure-switchable symmetric toehold dumbbell-template: A strategy enabling MicroRNA analysis at the single-cell level with ultrahigh specificity and accuracy, Anal. Chem., 90, 859-865, https://doi.org/10.1021/acs.analchem.7b03713.

    Article  CAS  PubMed  Google Scholar 

  76. Li, C., Li, Z., Jia, H., and Yan, J. (2011) One-step ultrasensitive detection of microRNAs with loop-mediated isothermal amplification (LAMP), Chem. Commun., 47, 2595-2597, https://doi.org/10.1039/C0CC03957H.

    Article  CAS  Google Scholar 

  77. Tran, D. H., and Phung, H. T. T. (2020) Detecting Fasciola hepatica and Fasciola gigantica microRNAs with loop-mediated isothermal amplification (LAMP), J. Parasit. Dis., 44, 364-373, https://doi.org/10.1007/s12639-019-01164-w.

    Article  PubMed  Google Scholar 

  78. Du, W., Lv, M., Li, J., Yu, R., and Jiang, J. (2016) A ligation-based loop-mediated isothermal amplification (ligation-LAMP) strategy for highly selective microRNA detection, Chem. Commun., 52, 12721-12724, https://doi.org/10.1039/C6CC06160E.

    Article  CAS  Google Scholar 

  79. Liu, L., Deng, D., Wu, D., Hou, W., Wang, L., et al. (2021) Duplex-specific nuclease-based electrochemical biosensor for the detection of microRNAs by conversion of homogeneous assay into surface-tethered electrochemical analysis, Anal. Chim. Acta, 1149, 338199, https://doi.org/10.1016/j.aca.2021.338199.

    Article  CAS  PubMed  Google Scholar 

  80. Yin, B. C., Liu, Y. Q., and Ye, B. C. (2012) One-step, multiplexed fluorescence detection of microRNAs based on duplex-specific nuclease signal amplification, J. Am. Chem. Soc., 134, 5064-5067, https://doi.org/10.1021/ja300721s.

    Article  CAS  PubMed  Google Scholar 

  81. Ma, X., Xu, H., Qian, K., Kandawa-Schulz, M., Miao, W., et al. (2020) Electrochemical detection of microRNAs based on AuNPs/CNNS nanocomposite with Duplex-specific nuclease assisted target recycling to improve the sensitivity, Talanta, 208, 120441, https://doi.org/10.1016/j.talanta.2019.120441.

    Article  CAS  PubMed  Google Scholar 

  82. Sang, Y., Xu, Y., Xu, L., Cheng, W., Li, X., et al. (2017) Colorimetric and visual determination of microRNA via cycling signal amplification using T7 exonuclease, Microchim. Acta, 184, 2465-2471, https://doi.org/10.1007/s00604-017-2238-8.

    Article  CAS  Google Scholar 

  83. Zheng, Y., Chen, J., Li, Y., Xu, Y., Chen, L., et al. (2021) Dual-probe fluorescent biosensor based on T7 exonuclease-assisted target recycling amplification for simultaneous sensitive detection of microRNA-21 and microRNA-155, Anal. Bioanal. Chem., 413, 1605-1614, https://doi.org/10.1007/s00216-020-03121-6.

    Article  CAS  PubMed  Google Scholar 

  84. Wang, M., Fu, Z., Li, B., Zhou, Y., Yin, H., et al. (2014) One-step, ultrasensitive, and electrochemical assay of microRNAs based on T7 exonuclease assisted cyclic enzymatic amplification, Anal. Chem., 86, 5606-5610, https://doi.org/10.1021/ac5010376.

    Article  CAS  PubMed  Google Scholar 

  85. Zhang, P., Zhuo, Y., Chang, Y., Yuan, R., and Chai, Y. (2015) Electrochemiluminescent graphene quantum dots as a sensing platform: A dual amplification for microRNA assay, Anal. Chem., 87, 10385-10391, https://doi.org/10.1021/acs.analchem.5b02495.

    Article  CAS  PubMed  Google Scholar 

  86. Chen, Z., Xie, Y., Huang, W., Qin, C., Yu, A., et al. (2019) Exonuclease-assisted target recycling for ultrasensitive electrochemical detection of microRNA at vertically aligned carbon nanotubes, Nanoscale, 11, 11262-11269, https://doi.org/10.1039/c9nr02543j.

    Article  CAS  PubMed  Google Scholar 

  87. Liu, M. X., Liang, S., Tang, Y., Tian, J., Zhao, Y., et al. (2018) Rapid and label-free fluorescence bioassay for microRNA based on exonuclease III-assisted cycle amplification, RSC Adv., 8, 15967-15972, https://doi.org/10.1039/c8ra01605d.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Tang, Y., Liu, M., Zhao, Z., Li, Q., Liang, X., et al. (2019) Fluorometric determination of microRNA-122 by using ExoIII-aided recycling amplification and polythymine induced formation of copper nanoparticles, Microchim. Acta, 186, 133, https://doi.org/10.1007/s00604-019-3237-8.

    Article  CAS  Google Scholar 

  89. Yan, X. M., Wang, Y. Q., Chen, Y., Chen, Z. P., and Yu, R. Q. (2020) Detection of microRNAs by the combination of exonuclease-III assisted target recycling amplification and repeated-fishing strategy, Anal. Chim. Acta, 1131, 1-8, https://doi.org/10.1016/j.aca.2020.07.025.

    Article  CAS  PubMed  Google Scholar 

  90. Miao, P., Wang, B., Yu, Z., Zhao, J., and Tang, Y. (2015) Ultrasensitive electrochemical detection of microRNA with star trigon structure and endonuclease mediated signal amplification, Biosens. Bioelectron., 63, 365-370, https://doi.org/10.1016/j.bios.2014.07.075.

    Article  CAS  PubMed  Google Scholar 

  91. Huang, Y., Wang, W., Wu, T., Xu, L. P., Wen, Y., et al. (2016) A three-line lateral flow biosensor for logic detection of microRNA based on Y-shaped junction DNA and target recycling amplification, Anal. Bioanal. Chem., 408, 8195-8202, https://doi.org/10.1007/s00216-016-9925-x.

    Article  CAS  PubMed  Google Scholar 

  92. Luo, L., Wang, L., Zeng, L., Wang, Y., Weng, Y., et al. (2020) A ratiometric electrochemical DNA biosensor for detection of exosomal microRNA, Talanta, 207, 120298, https://doi.org/10.1016/j.talanta.2019.120298.

    Article  CAS  PubMed  Google Scholar 

  93. Gong, S., Zhang, S., Lu, F., Pan, W., Li, N., and Tang, B. (2021) CRISPR/Cas-based in vitro diagnostic platforms for cancer biomarker detection, Anal. Chem., 93, 11899-11909, https://doi.org/10.1021/acs.analchem.1c02533.

    Article  CAS  PubMed  Google Scholar 

  94. Kim, S., Ji, S., and Koh, H. R. (2021) CRISPR as a diagnostic tool, Biomolecules, 11, 1162, https://doi.org/10.3390/biom11081162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Zhang, F. (2019) Development of CRISPR-Cas systems for genome editing and beyond, Q. Rev. Biophys., 52, 1-31, https://doi.org/10.1017/S0033583519000052.

    Article  Google Scholar 

  96. Shan, Y., Zhou, X., Huang, R., and Xing, D. (2019) High-fidelity and rapid quantification of miRNA combining crRNA programmability and CRISPR/Cas13a trans-cleavage activity, Anal. Chem., 91, 5278-5285, https://doi.org/10.1021/acs.analchem.9b00073.

    Article  CAS  PubMed  Google Scholar 

  97. Yuan, C., Tian, T., Sun, J., Hu, M., Wang, X., et al. (2020) Universal and naked-eye gene detection platform based on the clustered regularly interspaced short palindromic repeats/Cas12a/13a system, Anal. Chem., 92, 4029-4037, https://doi.org/10.1021/acs.analchem.9b05597.

    Article  CAS  PubMed  Google Scholar 

  98. Bruch, R., Johnston, M., Kling, A., Mattmüller, T., Baaske, J., et al. (2021) CRISPR-powered electrochemical microfluidic multiplexed biosensor for target amplification-free miRNA diagnostics, Biosens. Bioelectron., 177, 112887, https://doi.org/10.1016/j.bios.2020.112887.

    Article  CAS  PubMed  Google Scholar 

  99. Granados-Riveron, J. T., and Aquino-Jarquin, G. (2021) CRISPR/Cas13-based approaches for ultrasensitive and specific detection of microRNAs, Cells, 10, 1655, https://doi.org/10.3390/cells10071655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Sha, Y., Huang, R., Huang, M., Yue, H., Shan, Y., et al. (2021) Cascade CRISPR/Cas enables amplification-free microRNA sensing with fM-sensitivity and single-base-specificity, Chem. Commun., 57, 247-250, https://doi.org/10.1039/D0CC06412B.

    Article  CAS  Google Scholar 

  101. Zhang, G., Zhang, L., Tong, J., Zhao, X., and Ren, J. (2020) CRISPR-Cas12a enhanced rolling circle amplification method for ultrasensitive miRNA detection, Microchem. J., 158, 105239, https://doi.org/10.1016/j.microc.2020.105239.

    Article  CAS  Google Scholar 

  102. Zhou, T., Huang, R., Huang, M., Shen, J., Shan, Y., et al. (2020) CRISPR/Cas13a powered portable electrochemiluminescence chip for ultrasensitive and specific MiRNA detection, Adv. Sci., 7, 1903661, https://doi.org/10.1002/advs.201903661.

    Article  CAS  Google Scholar 

  103. Giuffrida, M. C., Zanoli, L. M., D’Agata, R., Finotti, A., Gambari, R., et al. (2015) Isothermal circular-strand-displacement polymerization of DNA and microRNA in digital microfluidic devices, Anal. Bioanal. Chem., 407, 1533-1543, https://doi.org/10.1007/s00216-014-8405-4.

    Article  CAS  PubMed  Google Scholar 

  104. Wang, B., You, Z., and Ren, D. (2019) Target-assisted FRET signal amplification for ultrasensitive detection of microRNA, Analyst, 144, 2304-2311, https://doi.org/10.1039/C8AN02266F.

    Article  CAS  PubMed  Google Scholar 

  105. Ma, W., Situ, B., Lv, W., Li, B., Yin, X., et al. (2016) Electrochemical determination of microRNAs based on isothermal strand-displacement polymerase reaction coupled with multienzyme functionalized magnetic micro-carriers, Biosens. Bioelectron., 80, 344-351, https://doi.org/10.1016/j.bios.2015.12.064.

    Article  CAS  PubMed  Google Scholar 

  106. Cai, S., Ye, J., Al-Maskri, A. A. A., Sun, L., and Zeng, S. (2019) A conformational switch-based aptasensor for the chemiluminescence detection of microRNA, Luminescence, 34, 823-829, https://doi.org/10.1002/bio.3677.

    Article  CAS  PubMed  Google Scholar 

  107. Solovjev, A. M., Galkin, I. I., Pletjushkina, O. Y., Medvedko, A. V., Zhao, S., et al. (2021) Isothermal chemiluminescent assay based on circular stand-displacement polymerization reaction amplification for cel-miRNA-39-3p determination in cell extracts, Int. J. Biol. Macromolecules, 182, 987-992, https://doi.org/10.1016/j.ijbiomac.2021.04.101.

    Article  CAS  Google Scholar 

  108. Ang, Y. S., and Yung, L.-Y. L. (2016) Rational design of hybridization chain reaction monomers for robust signal amplification, Chem. Commun., 52, 4219-4222, https://doi.org/10.1039/C5CC08907G.

    Article  CAS  Google Scholar 

  109. Zhang, H., Liu, X., Zhang, C., Xu, Y., Su, J., et al. (2020) A DNA tetrahedral structure-mediated ultrasensitive fluorescent microarray platform for nucleic acid test, Sens. Actuators B Chem., 321, 128538, https://doi.org/10.1016/j.snb.2020.128538.

    Article  CAS  Google Scholar 

  110. Miao, P., Tang, Y., and Yin, J. (2015) MicroRNA detection based on analyte triggered nanoparticle localization on a tetrahedral DNA modified electrode followed by hybridization chain reaction dual amplification, Chem. Commun., 51, 15629-15632, https://doi.org/10.1039/C5CC05499K.

    Article  CAS  Google Scholar 

  111. Ge, Z., Lin, M., Wang, P., Pei, H., Yan, J., et al. (2014) Hybridization chain reaction amplification of microRNA detection with a tetrahedral DNA nanostructure-based electrochemical biosensor, Anal. Chem., 86, 2124-2130, https://doi.org/10.1021/ac4037262.

    Article  CAS  PubMed  Google Scholar 

  112. Liu, H., Bei, X., Xia, Q., Fu, Y., Zhang, S., et al. (2016) Enzyme-free electrochemical detection of microRNA-21 using immobilized hairpin probes and a target-triggered hybridization chain reaction amplification strategy, Microchim. Acta, 183, 297-304, https://doi.org/10.1007/s00604-015-1636-z.

    Article  CAS  Google Scholar 

  113. Guo, Q., Yu, Y., Zhang, H., Cai, C., and Shen, Q. (2020) Electrochemical sensing of exosomal microRNA based on hybridization chain reaction signal amplification with reduced false-positive signals, Anal. Chem., 92, 5302-5310, https://doi.org/10.1021/acs.analchem.9b05849.

    Article  CAS  PubMed  Google Scholar 

  114. Xiong, Z., Pan, R., Hu, Q., Yun, W., Li, N., et al. (2020) One-step triggered branched DNA nanostrucuture for ultra-sensitive electrochemical detection of microRNA, Microchem. J., 158, 105186, https://doi.org/10.1016/j.microc.2020.105186.

    Article  CAS  Google Scholar 

  115. Hosseinzadeh, E., Ravan, H., Mohammadi, A., and Pourghadamyari, H. (2020) Colorimetric detection of miRNA-21 by DNAzyme-coupled branched DNA constructs, Talanta, 216, 120913, https://doi.org/10.1016/j.talanta.2020.120913.

    Article  CAS  PubMed  Google Scholar 

  116. Li, Y., Huang, C. Z., and Li, Y. F. (2019) Ultrasensitive electrochemiluminescence detection of MicroRNA via one-step introduction of a target-triggered branched hybridization chain reaction circuit, Anal. Chem., 91, 9308-9314, https://doi.org/10.1021/acs.analchem.9b02580.

    Article  CAS  PubMed  Google Scholar 

  117. Shen, Z., He, L., Wang, W., Tan, L., and Gan, N. (2020) Highly sensitive and simultaneous detection of microRNAs in serum using stir-bar assisted magnetic DNA nanospheres-encoded probes, Biosens. Bioelectron., 148, 111831, https://doi.org/10.1016/j.bios.2019.111831.

    Article  CAS  PubMed  Google Scholar 

  118. Shuai, H. L., Huang, K. J., Xing, L. L., and Chen, Y. X. (2016) Ultrasensitive electrochemical sensing platform for microRNA based on tungsten oxide-graphene composites coupling with catalyzed hairpin assembly target recycling and enzyme signal amplification, Biosens. Bioelectron., 86, 337-345, https://doi.org/10.1016/j.bios.2016.06.057.

    Article  CAS  PubMed  Google Scholar 

  119. Ji, D., Mou, X., and Kwok, C. K. (2019) Label-free and ratiometric detection of microRNA based on target-induced catalytic hairpin assembly and two fluorescent dyes, Anal. Methods, 11, 4808-4813, https://doi.org/10.1039/C9AY01891C.

    Article  CAS  Google Scholar 

  120. Li, C., Huang, Y., and Yang, Y. (2021) Coupling of an antifouling and reusable nanoplatform with catalytic hairpin assembly for highly sensitive detection of nucleic acids using zeta potential as signal readout, Sens. Actuators B Chem., 326, 128845, https://doi.org/10.1016/j.snb.2020.128845.

    Article  CAS  Google Scholar 

  121. Jin, F., and Xu, D. (2021) A fluorescent microarray platform based on catalytic hairpin assembly for MicroRNAs detection, Anal. Chim. Acta, 1173, 338666, https://doi.org/10.1016/j.aca.2021.338666.

    Article  CAS  PubMed  Google Scholar 

  122. Jiang, Z., Wang, H., Zhang, X., Liu, C., and Li, Z. (2014) An enzyme-free signal amplification strategy for sensitive detection of microRNA via catalyzed hairpin assembly, Anal. Methods, 6, 9477-9482, https://doi.org/10.1039/C4AY02142H.

    Article  CAS  Google Scholar 

  123. Zhang, Y., Zhang, X., Situ, B., Wu, Y., Luo, S., et al. (2021) Rapid electrochemical biosensor for sensitive profiling of exosomal microRNA based on multifunctional DNA tetrahedron assisted catalytic hairpin assembly, Biosens. Bioelectron., 183, 113205, https://doi.org/10.1016/j.bios.2021.113205.

    Article  CAS  PubMed  Google Scholar 

  124. Zhang, R. Y., Luo, S. H., Lin, X. M., Hu, X. M., Zhang, Y., et al. (2021) A novel electrochemical biosensor for exosomal microRNA-181 detection based on a catalytic hairpin assembly circuit, Anal. Chim. Acta, 1157, 338396, https://doi.org/10.1016/j.aca.2021.338396.

    Article  CAS  PubMed  Google Scholar 

  125. Jiang, Y. S., Bhadra, S., Li, B., and Ellington, A. D. (2014) Mismatches improve the performance of strand-displacement nucleic acid circuits, Angew. Chem. Int. Ed., 126, 1876-1879, https://doi.org/10.1002/ange.201307418.

    Article  Google Scholar 

  126. Bodulev, O. L., Zhao, S., and Sakharov, I. Y. (2021) Improving the sensitivity of the miRNA assay coupled with the mismatched catalytic hairpin assembly reaction by optimization of hairpin annealing conditions, Anal. Chem., 93, 6824-6830, https://doi.org/10.1021/acs.analchem.1c00820.

    Article  CAS  PubMed  Google Scholar 

  127. Tian, W., Li, P., He, W., Liu, C., and Li, Z. (2019) Rolling circle extension-actuated loop-mediated isothermal amplification (RCA-LAMP) for ultrasensitive detection of microRNAs, Biosens. Bioelectron., 128, 17-22, https://doi.org/10.1016/j.bios.2018.12.041.

    Article  CAS  PubMed  Google Scholar 

  128. Zhou, C., Huang, R., Zhou, X., and Xing, D. (2020) Sensitive and specific microRNA detection by RNA dependent DNA ligation and rolling circle optical signal amplification, Talanta, 216, 120954, https://doi.org/10.1016/j.talanta.2020.120954.

    Article  CAS  PubMed  Google Scholar 

  129. Zhuang, J., Lai, W., Chen, G., and Tang, D. (2014) A rolling circle amplification-based DNA machine for miRNA screening coupling catalytic hairpin assembly with DNAzyme formation, Chem. Commun., 50, 2935-2938, https://doi.org/10.1039/C3CC49873E.

    Article  CAS  Google Scholar 

  130. Fan, T., Mao, Y., Liu, F., Zhang, W., Lin, J. S., et al. (2019) Label-free fluorescence detection of circulating microRNAs based on duplex-specific nuclease-assisted target recycling coupled with rolling circle amplification, Talanta, 200, 480-486, https://doi.org/10.1016/j.talanta.2019.01.038.

    Article  CAS  PubMed  Google Scholar 

  131. Wang, S., Lu, S., Zhao, J., Ye, J., Huang, J., and Yang, X. (2019) An electric potential modulated cascade of catalyzed hairpin assembly and rolling chain amplification for microRNA detection, Biosens. Bioelectron., 126, 565-571, https://doi.org/10.1016/j.bios.2018.09.088.

    Article  CAS  PubMed  Google Scholar 

  132. Huang, M., Huang, R., Yue, H., Shan, Y., and Xing, D. (2020) Ultrasensitive and high-specific microRNA detection using hyper-branching rolling circle amplified CRISPR/Cas13a biosensor, Sens. Actuators B Chem., 325, 128799, https://doi.org/10.1016/j.snb.2020.128799.

    Article  CAS  Google Scholar 

  133. Liu, H., Tian, T., Zhang, Y., Ding, L., Yu, J., et al. (2017) Sensitive and rapid detection of microRNAs using hairpin probes-mediated exponential isothermal amplification, Biosens. Bioelectron., 89, 710-714, https://doi.org/10.1016/j.bios.2016.10.099.

    Article  CAS  PubMed  Google Scholar 

  134. Fu, P., Xu, M., Xing, S., Zhao, Y., and Zhao, C. (2021) Dual cascade isothermal amplification reaction based glucometer sensors for point-of-care diagnostics of cancer-related microRNAs, Analyst, 146, 3242-3250, https://doi.org/10.1039/D1AN00037C.

    Article  CAS  PubMed  Google Scholar 

  135. Song, W., Zhang, F., Song, P., Zhang, Z., He, P., et al. (2021) Untrasensitive photoelectrochemical sensor for microRNA detection with DNA walker amplification and cation exchange reaction, Sens. Actuators B Chem., 327, 128900, https://doi.org/10.1016/j.snb.2020.128900.

    Article  CAS  Google Scholar 

  136. Yuan, Y. H., Chi, B. Z., Wen, S. H., Liang, R. P., Li, Z. M., et al. (2018) Ratiometric electrochemical assay for sensitive detecting microRNA based on dual-amplification mechanism of duplex-specific nuclease and hybridization chain reaction, Biosens. Bioelectron., 102, 211-216, https://doi.org/10.1016/j.bios.2017.11.030.

    Article  CAS  PubMed  Google Scholar 

  137. Bodulev, O. L., Burkin, K. M., Efremov, E. E., and Sakharov, I. Y. (2020) One-pot microplate-based chemiluminescent assay coupled with catalytic hairpin assembly amplification for DNA detection, Anal. Bioanal. Chem., 412, 5105-5111, https://doi.org/10.1007/s00216-020-02438-6.

    Article  CAS  PubMed  Google Scholar 

  138. Kolosova, A. Y., and Sakharov, I. Y. (2019) Triple amplification strategy for the improved efficiency of a microplate-based assay for the chemiluminescent detection of DNA, Anal. Lett., 52, 1352-1362, https://doi.org/10.1080/00032719.2018.1539091.

    Article  CAS  Google Scholar 

Download references

Funding

The work was supported by the Russian Foundation for Basic Research (project no. 21-54-53007).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ivan Yu. Sakharov.

Ethics declarations

The authors declare no conflicts of interest. The article does not contain description of studies with participation of animals or humans performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bodulev, O.L., Sakharov, I.Y. Modern Methods for Assessment of microRNAs. Biochemistry Moscow 87, 425–442 (2022). https://doi.org/10.1134/S0006297922050042

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297922050042

Keywords

Navigation