Abstract—
The review provides an analysis of the literature data on the use of various modern molecular genetic methods for the indication and identification of Yersinia pestis strains with different properties and degrees of virulence, which is due to the diverse natural conditions in which they circulate. The methods are also considered from the perspective of their application at three levels of organizations forming the system of laboratory diagnostics of infectious diseases of the Russian Federation (territorial, regional, and federal) to solve the problem of maintaining the sanitary and epidemiological well-being of the country’s population. The main conditional groups of methods are considered: based on the analysis of the lengths of restriction fragments (ribo- and IS-typing, pulse gel electrophoresis); based on the analysis of specific fragments (DFR typing, VNTR typing); based on sequencing (MLST, CRISPR analysis, SNP analysis); PCR methods (including IPCR, SPA); isothermal amplification methods (LAMP, HDA, RPA, SEA, PCA, SHERLOCK); DNA microarray; methods using aptamer technology; bio- and nanosensors; DNA origami; and methods based on neural networks. As a result of the analysis, it can be concluded that there is rapid development of molecular diagnostics and genetics, which is aimed at increasing efficiency, multifactority, and simplification of application with no need for expensive equipment and highly qualified personnel for analysis. At all levels of the organizations forming the system of laboratory diagnostics of infectious diseases of the Russian Federation, it is possible to use methods based on PCR, isothermal amplification, SHERLOCK, biosensors, and small-sized sequencing devices. At the territorial level, at antiplague stations, the use of immuno-PCR and SPA for the indication of Y. pestis is promising. At the regional level, the introduction of technologies based on the use of aptamers and DNA microarray looks promising. At the federal level, the use of DNA origami methods and new technologies of whole genome sequencing is promising in the framework of advanced identification, molecular typing, and sequencing of the genomes of plague pathogen strains.
REFERENCES
Onishchenko, G.G., Smolenskii, V.Yu., Ezhlova, E.B., Demina, Yu.V., Toporkov, V.P., Toporkov, A.V., Lyapin, M.N., and Kutyrev, V.V., Conceptual foundations of biological safety. Part 1, Vestn. Ross. Akad. Med. Nauk, 2013, no. 10, pp. 4–13.
Onishchenko, G.G., Kutyrev, V.V., Krivulya, S.D., Fedorov, Yu.M., and Toporkov, V.P., Strategy for combating infectious diseases and sanitary protection of territories in modern conditions, Probl. Osobo Opasnykh Infekts., 2006, no. 2, pp. 5–9.
Eroshenko, G.A., Krasnov, Ya.M., Nosov, N.Yu., Kukleva, L.M., Nikiforov, K.A., Oglodin, E.G., and Kutyrev, V.V., Improving the subspecies classification of Yersinia pestis based on data from whole-genome sequencing of strains from Russia and neighboring countries, Probl. Osobo Opasnykh Infekts., 2015, no. 4, pp. 58–64. https://doi.org/10.21055/0370-1069-2015-4-58-64
Kutyrev, V.V., Eroshenko, G.A., Motin, V.L., Nosov, N.Y., Krasnov, J.M., Kukleva, L.M., Nikiforov, K.A., Al’khova, Z.V., Oglodin, E.G., and Guseva, N.P., Phylogeny and classification of Yersinia pestis through the lens of strains from the plague foci of Commonwealth of Independent States, Front. Microbiol., 2018, vol. 9, p. 1106. https://doi.org/10.3389/fmicb.2018.01106
Nikiforov, K.A., Morozov, O.A., Nosov, N.Yu., Kukleva, L.M., Yeroshenko, G.A., and Kutyrev, V.V., Population structure, taxonomy, and genetic features of Yersinia pestis strains of the Central Asian subspecies, Russ. J. Genet., 2018, vol. 54, no. 10, pp. 1142–1151. https://doi.org/10.1134/S1022795418100101
Cui, Y., Yu, C., Yan, Y., Li, D., Li, Y., Jombart, T., Weinert, L.A., Wang, Z., Guo, Z., Xu, L., Zhang, Y., Zheng, H., Qin, N., Xiao, X., Wu, M., Wang, X., Zhou, D., Qi, Z., Du, Z., Wu, H., Yang, X., Cao, H., Wang, H., Wang, J., Yao, S., Rakin, A., Li, Y., Falush, D., Balloux, F., Achtman, M., Song, Y., Wang, J., and Yang, R., Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis, Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 2, pp. 577–582. https://doi.org/10.1073/pnas.1205750110
Platonov, M.E., Evseeva, V.V., Dentovskaya, S.V., and Anisimov, A.P., Molecular typing of Yersinia pestis, Mol. Genet., Microbiol. Virol., 2013, vol. 28, no. 2, pp. 41–51.
Zhang, Y., Luo, T., Yang, C, Yue, X., Guo, R., Wang, X., Buren, M., Song, Y., Yang, R., Cao, H., Cui, Y., and Dai, X., Phenotypic and molecular genetic characteristics of Yersinia pestis at an emerging natural plague focus, Junggar Basin, China, Am. J. Trop. Med. Hyg., 2018, vol. 98, no. 1, pp. 231–237. https://doi.org/10.4269/ajtmh.17-0195
Wang, P., Shi, L., Zhang, F., Guo, Y., Zhang, Z., Tan, H., Cui, Z., Ding, Y., Liang, Y., Liang, Y., Yu, D., Xu, J., Li, W., and Song, Z., Ten years of surveillance of the Yulong plague focus in China and the molecular typing and source tracing of the isolates, PLoS Neglected Trop. Dis., 2018, vol. 12, no. 3, p. e0006352. https://doi.org/10.1371/journal.pntd.0006352
Nour El-Din, H.T., Yassin, A.S., Ragab, Y.M., and Hashem, A.M., Phenotype-genotype characterization and antibiotic-resistance correlations among colonizing and infectious methicillin-resistant Staphylococcus aureus recovered from intensive care units, Infect. Drug Resist., 2021, vol. 14, pp. 1557–1571. https://doi.org/10.2147/IDR.S296000
Jolley, K.A. and Maiden, M.C., Using multilocus sequence typing to study bacterial variation: Prospects in the genomic era, Future Microbiol., 2014, vol. 9, no. 5, pp. 623–630. https://doi.org/10.2217/fmb.14.24
Grissa, I., Vergnaud, G., and Pourcel, C., Clustered regularly interspaced short palindromic repeats (CRIS-PRs) for the genotyping of bacterial pathogens, in Molecular Epidemiology of Microorganisms, Caugant, D., Ed., Methods in Molecular Biology, vol 551, Totowa, NJ: Humana. https://doi.org/10.1007/978-1-60327-999-4_9
Spyrou, M.A., Keller, M., Tukhbatova, R.I., Scheib, C.L., Nelson, E.A., Andrades Valtueña, A., Neumann, G.U., Walker, D., Alterauge, A., Carty, N., Cessford, C., Fetz, H., Gourvennec, M., Hartle, R., Henderson, M., von Heyking, K., Inskip, S.A., Kacki, S., Key, F.M., Knox, E.L., Later, C., Maheshwari-Aplin, P., Peters, J., Robb, J.E., Schreiber, J., Kivisild, T., Castex, D., Lösch, S., Harbeck, M., Herbig, A., Bos, K.I., and Krause, J., Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes, Nat. Commun., 2019, vol. 10, no. 1, p. 4470. https://doi.org/10.1038/s41467-019-12154-0
Chen, F., Ye, J., Liu, W., Chio, C., Wang, W., and Qin, W., Knockout of a highly GC-rich gene in Burkholderia pyrrocinia by recombineering with freeze-thawing transformation, Mol. Plant Pathol., 2021, vol. 22, no. 7, pp. 843–857. https://doi.org/10.1111/mpp.13058
Yang, S., Yuan, Z.J., Zhu, Y.H., Chen, X., and Wang, W., lncRNA PVT1 promotes cetuximab resistance of head and neck squamous cell carcinoma cells by inhibiting miR-124-3p, Head Neck, 2021, vol. 43, no. 9, pp. 2712–2723. https://doi.org/10.1002/hed.26742
Mortazavipour, M.M., Shahbazi, S., and Mahdian, R., Detection of paternal IVS-II-1 (G>A) (HBB: c.315+1G>A) mutation in cell-free fetal DNA using COLD-PCR assay, Hemoglobin, 2020, vol. 44, no. 3, pp. 168–173. https://doi.org/10.1080/03630269.2020.1768864
Kane, S.R., Shah, S.R., and Alfaro, T.M., Development of a rapid viability polymerase chain reaction method for detection of Yersinia pestis, J. Microbiol. Methods, 2019, vol. 162, pp. 21–27. https://doi.org/10.1016/j.mimet.2019.05.005
Siggillino, A., Ulivi, P., Pasini, L., Reda, M.S., Chiadini, E., Tofanetti, F.R., Baglivo, S., Metro, G., Crinó, L., Delmonte, A., Minotti, V., Roila, F., and Ludovini, V., Detection of EGFR mutations in plasma cell-free tumor DNA of TKI-treated advanced-NSCLC patients by three methodologies: Scorpion-ARMS, PNAClamp, and Digital PCR, Diagnostics (Basel), 2020, vol. 10, no. 12, p. 1062. https://doi.org/10.3390/diagnostics10121062
Schneider, R., Lamien-Meda, A., Auer, H., Wiedermann-Schmidt, U., Chiodini, P.L., and Walochnik, J., Validation of a novel FRET real-time PCR assay for simultaneous quantitative detection and discrimination of human Plasmodium parasites, PLoS One, 2021, vol. 16, no. 6, p. e0252887. https://doi.org/10.1371/journal.pone.0252887
Sherrill-Mix, S., Hwang, Y., Roche, A.M., Glascock, A., Weiss, S.R., Li, Y., Haddad, L., Deraska, P., Monahan, C., Kromer, A., Graham-Wooten, J., Taylor, L.J., Abella, B.S., Ganguly, A., Collman, R.G., Van Duyne, G.D., and Bushman, F.D., Detection of SARS-CoV-2 RNA using RT-LAMP and molecular beacons, Genome Biol., 2021, vol. 22, no. 1, p. 169. https://doi.org/10.1186/s13059-021-02387-y
Nikiforov, K.A., Kukleva, L.M., Sitmbetov, D.A., Osina, N.A., Eroshenko, G.A., and Kutyrev, V.V., Construction of the reagent panel “GenPest-subspecies/Altai-RGF,” Probl. Osobo Opasnykh Infekts., 2021, no. 4, pp. 90–95. https://doi.org/10.21055/0370-1069-2021-4-90-95
Thomas, M.C., Janzen, T.W., Huscyzynsky, G., Mathews, A., and Amoako, K.K., Development of a novel multiplexed qPCR and Pyrosequencing method for the detection of human pathogenic yersiniae, Int. J. Food. Microbiol., 2017, vol. 257, pp. 247–253. https://doi.org/10.1016/j.ijfoodmicro.2017.06.019
Newton, C.R., Graham, A., Heptinstall, L.E., Powell, S.J., Summers, C., Kalsheker, N., Smith, J.C., and Markham, A.F., Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS), Nucleic Acids Res., 1989, vol. 17, no. 7, pp. 2503–2516. https://doi.org/10.1093/nar/17.7.2503
Cai, L., Kong, F., Jelfs, P., Gilbert, G.L., and Sintchenko, V., Rolling circle amplification and multiplex allele-specific PCR for rapid de-tection of katG and inhA gene mutations in Mycobacterium tuberculosis, Int. J. Med. Microbiol., 2009, vol. 299, no. 8, pp. 574–581. https://doi.org/10.1016/j.ijmm.2009.05.006
Vogler, A.J., Driebe, E.M., Lee, J., Auerbach, R.K., Allender, C.J., Stanley, M., Kubota, K., Andersen, G.L., Radnedge, L., Worsham, P.L., Keim, P., and Wagner, D.M., Assays for the rapid and specific identification of North American Yersinia pestis and the common laboratory strain CO92, Biotechniques, 2008, vol. 44, no. 2, pp. 203–204, 207. https://doi.org/10.2144/000112815
Sano, T., Smith, C.L., and Cantor, C.R., Immuno-PCR: Very sensitive antigen detection by means of specific antibody-DNA conjugates, Science, 1992, vol. 258, no. 5079, pp. 120–122. https://doi.org/10.1126/science.1439758
Jayathilake, C. and Nemoto, N., cDNA Display-mediated immuno-PCR (cD-IPCR): An ultrasensitive immunoassay for biomolecular detection, Methods Mol. Biol., 2021, vol. 2261, pp. 307–321. https://doi.org/10.1007/978-1-0716-1186-9_19
Malou, N., Tran, T.N., Nappez, C., Signoli, M., Le Forestier, C., Castex, D., Drancourt, M., and Raoult, D., Immuno-PCR—A new tool for paleomicrobiology: The plague paradigm, PLoS One, 2012, vol. 7, no. 2, p. e31744. https://doi.org/10.1371/journal.pone.0031744
Adessi, C., Matton, G., Ayala, G., Turcatti, G., Mermod, J.J., Mayer, P., and Kawashima, E., Solid phase DNA amplification: Characterisation of primer attachment and amplification mechanisms, Nucleic Acids Res., 2000, vol. 28, no. 20, p. E87. https://doi.org/10.1093/nar/28.20.e87
Notomi, T., Okayama, H., Masubuchi, H., Yonekawa, T., Watanabe, K., Amino, N., and Hase, T., Loop-mediated isothermal amplification of DNA, Nucleic Acids Res., 2000, vol. 28, no. 12, p. E63. https://doi.org/10.1093/nar/28.12.e63
Singh, R., Pal, V., Tripathi, N.K., and Goel, A.K., Development of a pair of real-time loop mediated isothermal amplification assays for detection of Yersinia pestis, the causative agent of plague, Mol. Cell Probes, 2020, vol. 54, p. 101670. https://doi.org/10.1016/j.mcp.2020.101670
Jin, J., Duan, L., Fu, J., Chai, F., Zhou, Q., Wang, Y., Shao, X., Wang, L., Yan, M., Su, X., Zhang, Y., Pan, J., and Chen, J., A real-time LAMP-based dual-sample microfluidic chip for rapid and simultaneous detection of multiple waterborne pathogenic bacteria from coastal waters, Anal. Methods, 2021, vol. 13, no. 24, pp. 2710–2721. https://doi.org/10.1039/d1ay00492a
Liu, W., Dong, D., Yang, Z., Zou, D., Chen, Z., Yuan, J., and Huang, L., Polymerase Spiral Reaction (PSR): A novel isothermal nucleic acid amplification method, Sci. Rep., 2015, vol. 5, p. 12723. https://doi.org/10.1038/srep12723
Mayboroda, O., Gonzalez Benito, A., Sabaté del Rio, J., Svobodova, M., Julich, S., Tomaso, H., O’Sullivan, C.K., and Katakis, I., Isothermal solid-phase amplification system for detection of Yersinia pestis, Anal. Bioanal Chem., 2016, vol. 408, no. 3, pp. 671–676. https://doi.org/10.1007/s00216-015-9177-1
Shi, L., Yang, G., Zhang, Z., Xia, L., Liang, Y., Tan, H., He, J., Xu, J., Song, Z., Li, W., and Wang, P., Reemergence of human plague in Yunnan, China in 2016, PLoS One, 2018, vol. 13, no. 6, p. e0198067. https://doi.org/10.1371/journal.pone.0198067
Zasada, A.A., Zacharczuk, K., Formińska, K., Wiatrzyk, A., Ziółkowski, R., and Malinowska, E., Isothermal DNA amplification combined with lateral flow dipsticks for detection of biothreat agents, Anal. Biochem., 2018, vol. 560, pp. 60–66. https://doi.org/10.1016/j.ab.2018.09.008
Kortli, S., Jauset-Rubio, M., Tomaso, H., Abbas, M.N., Bashammakh, A.S., El-Shahawi, M.S., Alyoubi, A.O., Ben-Ali, M., and O’Sullivan, C.K., Yersinia pestis detection using biotinylated dNTPs for signal enhancement in lateral flow assays, Anal. Chim. Acta, 2020, vol.1112, pp. 54–61. https://doi.org/10.1016/j.aca.2020.03.059
Müller, K., Daßen, S., Holowachuk, S., Zwirglmaier, K., Stehr, J., Buersgens, F., Ullerich, L., and Stoecker, K., Pulse-controlled amplification—A new powerful tool for on-site diagnostics under resource limited conditions, PLoS Neglected Trop. Dis., 2021, vol. 15, no. 1, p. e0009114. https://doi.org/10.1371/journal.pntd.0009114
Cunningham, C.H., Hennelly, C.M., Lin, J.T., Uba-lee, R., Boyce, R.M., Mulogo, E.M., Hathaway, N., Thwai, K.L., Phanzu, F., Kalonji, A., Mwandagalirwa, K., Tshefu, A., Juliano, J.J., and Parr, J.B., A novel CRISPR-based malaria diagnostic capable of Plasmodium detection, species differentiation, and drug-resistance genotyping, EBioMedicine, 2021, vol. 68, p. 103415. https://doi.org/10.1016/j.ebiom.2021.103415
Schermer, B., Fabretti, F., Damagnez, M., Di Cristanziano, V., Heger, E., Arjune, S., Tanner, N.A., Imhof, T., Koch, M., Ladha, A., Joung, J., Gootenberg, J.S., Abudayyeh, O.O., Burst, V., Zhang, F., Klein, F., Benzing, T., and Müller, R.U., Rapid SARS-CoV-2 testing in primary material based on a novel multiplex RT-LAMP assay, PLoS One, 2020, vol. 15, no. 11, p. e0238612. https://doi.org/10.1371/journal.pone.0238612
Savvateeva, E.N., Dementieva, E.I., Tsybulskaya, M.V., Osipova, T.V., Ryabykh, T.P., Turygin, A.Yu., Yurasov, R.A., Zasedatelev, A.S., and Rubina, A.Yu., Biological microchip for simultaneous quantitative immunoassay of tumor markers in human serum, Bull. Exp. Biol. Med., 2009, no. 6, vol. 147, pp. 737−741.
Jiang, D., Tian, Y., Zhang, Y., Lu, X., Xiao, D., and Zhou, C., One-step fast and label-free imaging array for multiplexed detection of trace avian influenza viruses, Anal. Chim. Acta, 2021, vol. 1171, p. 338645. https://doi.org/10.1016/j.aca.2021.338645
Srinivasan, V., Stedtfeld, R.D., Tourlousse, D.M., Baushke, S.W., Xin, Y., Miller, S.M., Pham, T., Rouillard, J.M., Gulari, E., Tiedje, J.M., and Hashsham, S.A., Diagnostic microarray for 14 water and foodborne pathogens using a flatbed scanner, J. Microbiol. Methods, 2017, vol. 139, pp. 15–21. https://doi.org/10.1016/j.mimet.2017.04.009
Nikiforov, K.A., Utkin, D.V., Makashova, M.A., Kukleva, L.M., Eroshenko, G.A., and Kutyrev, V.V., Construction of a multiplex PCR system with hybridization-fluorescent recording of results on a solid substrate for indication and identification of plague pathogen strains, Biotekhnologiya, 2020, vol. 36, no. 3, pp. 46–56. https://doi.org/10.21519/0234-2758-2020-36-3-46-56
Famulok, M., Allosteric aptamers and aptazymes as probes for screening approaches, Curr. Opin. Mol. Ther., 2005, vol. 7, no. 2, pp. 137‒143.
Ellington, A.D. and Szostak, J.W., In vitro selection of RNA molecules that bind specific ligands, Nature, 1990, vol. 346, no. 6287, pp. 818‒822. https://doi.org/10.1038/346818a0
Jeddi, I. and Saiz, L., Computational design of single-stranded DNA hairpin aptamers immobilized on a biosensor substrate, Sci. Rep., 2021, vol. 11, no. 1, p 10984. https://doi.org/10.1038/s41598-021-88796-2
Duanghathaipornsuk, S., Reaver, N.G.F., Cameron, B.D., and Kim, D.S., Adsorption kinetics of glycated hemoglobin on aptamer microarrays with antifouling surface modification, Langmuir, 2021, vol. 37, no. 15, pp. 4647–4657. https://doi.org/10.1021/acs.langmuir.1c00446
Jalali, T., Salehi-Vaziri, M., Pouriayevali, M.H., and Gargari, S.L.M., Aptamer based diagnosis of Crimean-Congo hemorrhagic fever from clinical specimens, Sci. Rep., 2021, vol. 11, no. 1, p. 12639. https://doi.org/10.1038/s41598-021-91826-8
Qlark, L.C., Jr., Monitor and control of blood and tissue oxygen tensions, ASAIO J., 1956, vol. 2, no. 1, pp. 41–48.
Hong, C.A., Park, J.C., Na, H., Jeon, H., and Nam, Y.S., Short DNA-catalyzed formation of quantum dot-DNA hydrogel for enzyme-free femtomolar specific DNA assay, Biosens. Bioelectron., 2021, vol. 182, p. 113110. https://doi.org/10.1016/j.bios.2021.113110
Born, F., Braun, P., Scholz, H.C., and Grass, G., Specific detection of Yersinia pestis based on receptor binding proteins of phages, Pathogens, 2020, vol. 9, no. 8, p. 611. https://doi.org/10.3390/pathogens9080611
Liu, X., Wang, L., Zhao, J., Zhu, Y., Yang, J., and Yang, F., Enhanced binding efficiency of microcantilever biosensor for the detection of Yersinia, Sensors (Basel), 2019, vol. 19, no. 15, p. 3326. https://doi.org/10.3390/s19153326
Seeman, N.C., Nucleic acid junctions and lattices, J. Theor. Biol., 1982, vol. 99, no. 2, pp. 237–247. https://doi.org/10.1016/0022-5193(82)90002-9
Rothemund, P.W., Folding DNA to create nanoscale shapes and patterns, Nature, 2006, vol. 440, no. 7082, pp. 297–302. https://doi.org/10.1038/nature04586
Raveendran, M., Lee, A.J., Sharma, R., Wälti, C., and Actis, P., Rational design of DNA nanostructures for single molecule biosensing, Nat. Commun., 2020, vol. 11, no. 1, p. 4384. https://doi.org/10.1038/s41467-020-18132-1
Ochmann, S.E., Vietz, C., Trofymchuk, K., Acuna, G.P., Lalkens, B., and Tinnefeld, P., Optical nanoantenna for single molecule-based detection of Zika virus nucleic acids without molecular multiplication, Anal. Chem., 2017, vol. 89, no. 23, pp. 13000–13007. https://doi.org/10.1021/acs.analchem.7b04082
Yang, B., Zhang, Z., Yang, C., Wang, Y., Orr, M.C., Hongbin, W., and Zhang, A.B., Identification of species by combining molecular and morphological data using convolutional neural networks, Syst. Biol., 2022, vol. 71, no. 3, pp. 690–705. https://doi.org/10.1093/sysbio/syab076
Funding
This work was supported by ongoing institutional funding. No additional grants to carry out or direct this particular research were obtained.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
This work does not contain any studies involving human and animal subjects.
CONFLICT OF INTEREST
The author of this work declares that he has no conflicts of interest.
Additional information
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nikiforov, K.A. Modern Molecular Genetic Methods and Prospects for Their Use for Indication and Identification of Yersinia pestis Strains. Biochem. Moscow Suppl. Ser. B 17, 6–16 (2023). https://doi.org/10.1134/S1990750823600140
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1990750823600140