БИОХИМИЯ, 2020, том 85, вып. 2, с. 174–196

УДК 543.94

Изотермические методы амплификации нуклеиновых кислот и их применение в биоанализе

Обзор

© 2020 О.Л. Бодулев, И.Ю. Сахаров *

Московский государственный университет им. М.В. Ломоносова, химический факультет, 119991 Москва, Россия; электронная почта: sakharovivan@gmail.com

Поступила в редакцию 13.08.2019
После доработки 01.11.2019
Принята к публикации 01.11.2019

DOI: 10.31857/S0320972520020037

КЛЮЧЕВЫЕ СЛОВА: нуклеиновые кислоты, амплификация, изотермическая, биоанализ, аптамеры.

Аннотация

В последние годы бурно развиваются методы изотермической амплификации нуклеиновых кислот как альтернатива полимеразной цепной реакции (ПЦР). Их использование позволяет проводить амплификацию нуклеиновых кислот при постоянной температуре в отличие от ПЦР, для которой требуется циклическое изменение температуры. Кроме того, при использовании изотермических методов амплификация может проводиться непосредственно в живых клетках. В настоящем обзоре в краткой форме изложены принципы известных изотермических методов амплификации, а также продемонстрирована их высокая эффективность при конструировании новых высокочувствительных методов анализа как нуклеиновых кислот, так и ферментов, ответственных за их модификацию. Более того, приведены данные об успешном использовании изотермических методов амплификации в анализе клеток и биомолекул, определение которых проводится с применением ДНК/РНК-аптамеров.

Сноски

* Адресат для корреспонденции.

Финансирование

Работа выполнена при поддержке Российского научного фонда (грант 17-14-01042).

Конфликт интересов

Авторы заявляют об отсутствии конфликта интересов.

Соблюдение этических норм

Настоящая статья не содержит описания каких-либо исследований с участием людей или использованием животных в качестве объектов.

Список литературы

1. Manzanares-Palenzuela, C.L., de-los-Santos-Alvarez, N., Lobo-Castanon, M.J., and Lopez-Ruiz, B. (2015) Multiplex electrochemical DNA platform for femtomolar-level quantification of genetically modified soybean, Biosens. Bioelectron., 68, 259–265, doi: 10.1016/j.bios.2015.01.007.

2. Cavanaugh, S.E., and Bathrick, A.S. (2018) Direct PCR amplification of forensic touch and other challenging DNA samples: a review, Foressic Sci. Int. Genet., 32, 40–49, doi: 10.1016/j.fsigen.2017.10.005.

3. Higuchi, R., Dollinger, G., Walsh, P.S., and Griffith, R. (1992) Simultaneous amplification and detection of specific DNA-sequences, Biotechnology (NY), 10, 413–417.

4. Алексеев Я.И., Белов Ю.В., Варламов Д.А., Коновалов С.В., Курочкин В.Е., Маракушин Н.Ф., Петров А.И., Петряков А.О., Румянцев Д.А., Скоблилов Е.Ю., Соколов В.Н., Фесенко В.А., Чернышев А.В. (2006) Приборы для диагностики биологических объектов на основе метода полимеразной цепной реакции в реальном времени (ПЦР-РВ), Научное приборостроение, 16, 132–136.

5. 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, doi: 10.1007/s10096-004-1100-1.

6. Notomi, T., Okayama, H., Masubuchi, H., Yonekawa, T., Watanabe, K., Amino, N., and Hase, T. (2000) Loop-mediated isothermal amplification of DNA, Nucleic Acids Res., 28, E63, doi: 10.1093/nar/28.12.e63.

7. Yan, L., Zhou, J., Zheng, Y., Gamson, A.S., Roembke, B.T., Nakayama, S., and Sintim, H.O. (2014) Isothermal amplified detection of DNA and RNA, Mol. Biosyst., 10, 970–1003, doi: 10.1039/c3mb70304e.

8. Mori, Y., Kitao, M., Tomita, N., and Notomi, T. (2004) Real-time turbidimetry of LAMP reaction for quantifying template DNA, J. Biochem. Biophys. Methods, 59, 145–157, doi: 10.1016/j.jbbm.2003.12.005.

9. Tomita, N., Mori, Y., Kanda, H., and Notomi, T. (2008) Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products, Nat. Protoc., 3, 877–882, doi: 10.1038/nprot.2008.57.

10. Pang, B., Yao, S., Xu, K., Wang, J., Song, X.L., Mu, Y., Zhao, C., and Li, J. (2019) A novel visual-mixed-dye for LAMP and its application in the detection of foodborne pathogens, Anal. Biochem., 574, 1–6, doi: 10.1016/j.ab.2019.03.002.

11. Troger, V., Niemann, K., Gartig, C., and Kuhlmeier, D. (2015) Isothermal amplification and quantification of nucleic acids and its use in microsystems, J. Nanomed. Nanotechnol., 6, 282–298, doi: 10.4172/2157-7439.1000282.

12. Najian, A.B.N., Foo, P.C., Ismail, N., Kim-Fatt, L., and Yean, C.Y. (2019) Probe-specific loop-mediated isothermal amplification magnetogenosensor assay for rapid and specific detection of pathogenic Leptospira, Mol. Cell. Probes, 44, 63–68, doi: 10.1016/j.mcp.2019.03.001.

13. Shchit, I.Yu., Ignatov, K.B., Kudryavtseva, T.Yu., Shishkova, N.A., Mironova, R.I., Marinin, L.I., Mokrievich, A.N., Kramarov, V.M., Biketov, S.F., and Dyatlov, I.A. (2017) The use of loop-mediated isothermal DNA amplification for the detection and identification of the anthrax pathogen, Mol. Genet. Microbiol. Virol., 32, 100–108, doi: 10.3103/S0891416817020094.

14. Poschl, B., Waneesorn, J., Thekisoe, O., Chutipongvivate, S., and Panagiotis, K. (2010) Comparative diagnosis of malaria infections by microscopy, nested PCR, and LAMP in northern Thailand, Am. J. Tropical Med. Hygiene, 83, 56–60, doi: 10.4269/ajtmh.2010.09-0630.

15. Gao, X., Sun, B., and Guan, Y. (2019) Pullulan reduces the non-specific amplification of loop-mediated isothermal amplification (LAMP), Anal. Bioanal. Chem., 411, 1211–1218, doi: 10.1007/s00216-018-1552-2.

15а. Yang, Q., Domesle, K.J., and Ge, B. (2018) Loop-mediated isothermal amplification for Salmonella detection in food and feed: current applications and future directions, Foodborne Pathogens and Disease, 15, 309–331, doi: 10.1089/fpd.2018.2445.

15б. Maruyama, F., Kenzaka, T., Yamaguchi, N., Tani, K., and Nasu, M. (2003) Detection of bacteria carrying the stx2 gene by in situ loop-mediated isothermal amplification, Appl. Environ. Microbiol., 69, 5023–5028, doi: 10.1128/aem.69.8.5023-5028.2003.

16. Щит И.Ю., Игнатов К.Б., Бикетов С.Ф. (2018) Cравнительный анализ методов LAMP и ПЦР-РВ для обнаружения возбудителей сапа и мелиоидоза, Клинич. лаб. диагностика, 63, 378–384.

17. Макарова Ю.А., Зотиков А.А., Белякова Г.А., Алексеев Б.Я., Шкурников М.Ю. (2018) Изотермическая петлевая амплификация: эффективный метод экспресс-диагностики в онкологии, Онкоурология, 14, 88–99, doi: 10.17650/1726-9776-2018-14-2-88-99.

18. Wong, Y.P., Othman, S., Lau, Y.L., Radu, S., and Chee, H.Y. (2018) Loop mediated isothermal amplification (LAMP): a versatile technique for detection of microorganisms, J. Appl. Microbiol., 124, 626–643, doi: 10.1111/jam.13647.

19. Compton, J. (1991) Nucleic acid sequence-based amplification, Nature, 350, 91–92, doi: 10.1038/350091a0.

20. Kievits, T., van Gemen, B., van Strijp, D., Schukkink, R., Dircks, M., Adriaanse, H., Malek, L., Sooknanan, R., and Lens, P. (1991) NASBA isothermal enzymatic in vitro nucleic acid amplification optimized for the diagnosis of HIV-1 infection, J. Virol. Methods, 35, 273–286.

21. Mader, A., Riehle, U., Brandstetter, T., Stickeler, E., and Ruehe, J. (2012) Universal nucleic acid sequence-based amplification for simultaneous amplification of messengerRNAs and microRNAs, Anal. Chim. Acta, 754, 1–7, doi: 10.1016/j.aca.2012.09.045.

22. Ma, Y., Dai, X., Hong, T., Munk, G.B., and Libera, M. (2017) A NASBA on microgel-tethered molecular-beacon microarray for real-time microbial molecular diagnostics, Analyst, 142, 147–155, doi: 10.1039/c6an02192a.

23. Lu, X., Shi, X., Wu, G., Wu, T., Qin, R., and Wang, Y. (2017) Visual detection and differentiation of Classic Swine Fever Virus strains using nucleic acid sequence-based amplification (NASBA) and G-quadruplex DNAzyme assay, Scientific Reports, 7, 44211, doi: 10.1038/srep44211.

24. Zeng, W., Yao, W., Wang, Y., Li, Y., Bermann, S.M., Ren, Y., Shi, C., Song, X., Huang, Q., Zheng, S., and Wang, Q. (2017) Molecular detection of genotype II grass carp reovirus based on nucleic acid sequence-based amplification combined with enzyme-linked immunosorbent assay (NASBA-ELISA), J. Virol. Methods, 243, 92–97, doi: 10.1016/j.jviromet.2017.02.001.

25. Honsvall, B.K., and Robertson, L.J. (2017) From research lab to standard environmental analysis tool: will NASBA make the leap? Water Res., 109, 389–397, doi: 10.1016/j.watres.2016.11.052.

26. Vincent, M., Xu, Y., and Kong, H. (2004) Helicase-dependent isothermal DNA amplification, EMBO Reports, 5, 795–800, doi: 10.1038/sj.embor.7400200.

27. Zhao, Y., Chen, F., Li, Q., Wang, L., and Fan, C. (2015) Isothermal amplification of nucleic acids, Chem. Rev., 115, 12491–12545, doi: 10.1021/acs.chemrev.5b00428.

28. Barreda-Garcia, S., Miranda-Castro, R., de-los-Santos-Alvarez, N., Miranda-Ordieres, A.J., and Lobo-Castanon, M.J. (2018) Helicase-dependent isothermal amplification: a novel tool in the development of molecular-based analytical systems for rapid pathogen detection, Anal. Bioanal. Chem., 410, 679–693, doi: 10.1007/s00216-017-0620-3.

29. Mahalanabis, M., Do, J., ALMuayad, H., Zhang, J.Y., and Klapperich, C.M. (2011) An integrated disposable device for DNA extraction and helicase dependent amplification, Biomed. Microdevices, 13, 353–359, doi: 10.1007/s10544-009-9391-8.

30. Ao, W., Aldous, S., Woodruff, E., Hicke, B., Rea, L., Kreiswirth, B., and Jenison, R. (2012) Rapid detection of rpoB gene mutations conferring rifampin resistance in Mycobacterium tuberculosis, J. Clin. Microbiol., 50, 2433–2440, doi: 10.1128/JCM.00208-12.

31. Tang, R., Yang, H., Gong, Y., You, M., Liu, Z., Choi, J.R., Wen, T., Qu, Z., Mei, Q., and Xu, F. (2017) A fully disposable and integrated paper-based device for nucleic acid extraction, amplification and detection, Lab on a Chip, 17, 1270–1279, doi: 10.1039/c6lc01586g.

32. Barreda-Garcia, S., Miranda-Castro, R., de-Los-Santos-Alvarez, N., Miranda-Ordieres, A.J., and Lobo-Castanon, M.J. (2017) Solid-phase helicase dependent amplification and electrochemical detection of Salmonella on highly stable oligonucleotide-modified ITO electrodes, Chem. Commun., 53, 9721–9724, doi: 10.1039/c7cc05128j.

33. Schwenkbier, L., Pollok, S., Rudloff, A., Sailer, S., Cialla-May, D., Weber, K., and Popp, J. (2015) Non-instrumented DNA isolation, amplification and microarray-based hybridization for a rapid on-site detection of devastating Phytophthora kernoviae, Analyst, 140, 6610–6618, doi: 10.1039/c5an00855g.

34. Toldra, A., Jauset-Rubio, M., Andree, K.B., Fernandez-Tejedor, M., Diogene, J., Katakis, I., O’Sullivan, C.K., and Campas, M. (2018) Detection and quantification of the toxic marine microalgae Karlodinium veneficum and Karlodinium armiger using recombinase polymerase amplification and enzyme-linked oligonucleotide assay, Anal. Chim. Acta, 1039, 140–148, doi: 10.1016/j.aca.2018.07.057.

35. Ma, F., Liu, M., Tang, B., and Zhang, C.Y. (2017) Sensi-tive quantification of microRNAs by isothermal helicase-dependent amplification, Anal. Chem., 89, 6183–6188, doi: 10.1021/acs.analchem.7b01113.

36. 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, doi: 10.1002/anie.201712217.

37. 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, doi: 10.1073/pnas.0730811100.

38. Wang, H., Wang, H., Duan, X., Wang, X., Sun, Y., and Li, Z. (2017) Sensitive detection of mRNA by using specific cleavage-mediated isothermal exponential amplification reaction, Sens. Actuat. B: Chemical, 252, 215–221, doi: 10.1016/j.snb.2017.06.008.

39. Li, R.D., Yin, B.C., and Ye, B.C. (2016) Ultrasensitive, colorimetric detection of microRNAs based on isothermal exponential amplification reaction-assisted gold nanoparticle amplification, Biosens. Bioelectron., 15, 1011–1016, doi: 10.1016/j.bios.2016.07.042.

40. Liu, H., Zhang, L., Xu, Y., Chen, J., Wang, Y., Huang, Q., Che, X., Liu, Y., Da, Z., Zou, X., and Li, Z. (2019) Sandwich immunoassay coupled with isothermal exponential amplification reaction: an ultrasensitive approach for determination of tumor marker MUC1, Talanta, 204, 248–254, doi: 10.1016/j.talanta.2019.06.001.

41. Jia, H., Wang, Z., Wang, C., Chang, L., and Li, Z. (2014) Real-time fluorescence detection of Hg2+ ions with high sensitivity by exponentially isothermal oligonucleotide amplification, RSC Adv., 4, 9439–9444, doi: 10.1039/C3RA45986A.

42. Tian, L., and Weizmann, Y. (2013) Real-time detection of telomerase activity using the exponential isothermal amplification of telomere repeat assay, J. Am. Chem. Soc., 135, 1661–1664, doi: 10.1021/ja309198j.

43. Wang, L., Ren, M., Zhang, Q., Tang, B., and Zhang, C. (2017) Excision repair-initiated enzyme-assisted bicyclic cascade signal amplification for ultrasensitive detection of uracil-DNA glycosylase, Anal. Chem., 89, 4488–4494, doi: 10.1021/acs.analchem.6b04673.

44. Walker, G.T., Fraiser, M.S., Schram, J.L., Little, M.C., Nadeau, J.G., and Malinowski, D.P. (1992) Strand displacement amplification – an isothermal, in vitro DNA amplification technique, Nucleic Acids Res., 20, 1691–1696, doi: 10.1093/nar/20.7.1691.

45. Shi, C., Ge, Y., Gu, H., and Ma, C. (2011) Highly sensitive chemiluminescent point mutation detection by circular strand-displacement amplification reaction, Biosens. Bioelectron., 26, 4697–4701, doi: 10.1016/j.bios.2011.05.017.

46. Zhao, Y., Zhou, L., and Tang, Z. (2013) Cleavage-based signal amplification of RNA, Nat. Commun., 4, 1493, doi: 10.1038/ncomms2492.

47. Shi, C., Liu, Q., Ma, C., and Zhong, W. (2014) Exponential strand-displacement amplification for detection of microRNAs, Anal. Chem., 86, 336–339, doi: 10.1021/ac4038043.

48. Ren, R., Leng, C., and Zhang, S. (2010) Detection of DNA and indirect detection of tumor cells based on circular strand-replacement DNA polymerization on electrode, Chem. Commun., 46, 5758–5760, doi: 10.1039/C002466J.

49. Ding, C., Li, X., Ge, Y., and Zhang, S. (2010) Fluorescence detection of telomerase activity in cancer cells based on isothermal circular strand-displacement polymerization reaction, Anal. Chem., 82, 2850–2855, doi: 10.1021/ac902818w.

50. Zhu, C., Wen, Y., Li, D., Wang, L., Song, S., Fan, C., and Willner, I. (2009) Inhibition of the in vitro replication of DNA by an aptamer-protein complex in an autonomous DNA machine, Chemistry, 15, 11898–11903, doi: 10.1002/chem.200901275.

51. Li, Y., Zeng, Y., Mao, Y., Lei, C., and Zhang, S. (2014) Proximity-dependent isothermal cycle amplification for small-molecule detection based on surface enhanced Raman scattering, Biosens. Bioelectron., 51, 304–309, doi: 10.3390/bios9020057.

52. Li, J., Macdonald, J., and von Stetten, F. (2019) Review: a comprehensive summary of a decade development of the recombinase polymerase amplification, Analyst, 144, 31–67, doi: 10.1039/c8an01621f.

53. Kersting, S., Rausch, V., Bier, F.F., and von Nickisch-Rosenegk, M. (2014) Rapid detection of Plasmodium falciparum with isothermal recombinase polymerase amplification and lateral flow analysis, Malar. J., 13, 99, doi: 10.1186/1475-2875-13-99.

54. Lobato, I.M., and O’Sullivan, C.K. (2018) Recombinase polymerase amplification: basics, applications and recent advances, Trends Anal. Chem., 98, 19–35, doi: 10.1016/j.trac.2017.10.015.

55. Mayboroda, O., Gonzalez Benito, A., Sabate del Rio, J., Svobodova, M., Julich, S., Tomaso, H., O’Sullivan, C.K., and Katakis, I. (2016) Isothermal solid-phase amplification system for detection of Yersinia pestis, Anal. Bioanal. Chem., 408, 671–676, doi: 10.1007/s00216-015-9177-1.

56. Ng, B.Y., Xiao, W., West, N.P., Wee, E.J., Wang, Y., and Trau, M. (2015) Rapid, single-cell electrochemical detection of Mycobacterium tuberculosis using colloidal gold nanoparticles, Anal. Chem., 87, 10613–10618, doi: 10.1021/acs.analchem.5b03121.

57. Tsaloglou, M.N., Nemiroski, A., Camci-Unal, G., Christodouleas, D.C., Murray, L.P., Connelly, J.T., and Whitesides, G.M. (2017) Handheld isothermal amplification and electrochemical detection of DNA in resource-limited settings, Anal. Biochem., 543, 116–121, doi: 10.1016/j.ab.2017.11.025.

58. Yang, B., Kong, J., and Fang, X. (2019) Bandage-like wearable flexible microfluidic recombinase polymerase amplification sensor for the rapid visual detection of nucleic acids, Talanta, 204, 685–692, doi: 10.1016/j.talanta.2019.06.031.

59. Fire, A., and Xu, S.Q. (1995) Rolling replication of short DNA circles, Proc. Nat. Acad. Sci. USA, 92, 4641–4645, doi: 10.1073/pnas.92.10.4641.

60. Goo, N.-I., and Kim, D.-E. (2016) Rolling circle amplification as isothermal gene amplification in molecular diagnostics, BioChip J., 10, 262–271, doi: 10.1007/s13206-016-0402-6.

61. Nilsson, M., Barbany, G., Antson, D.O., Gertow, K., and Landegren, U. (2000) Enhanced detection and distinction of RNA by enzymatic probe ligation, Nat. Biotechnol., 18, 791–793, doi: 10.1038/77367.

62. Marciniak, J., Kummel, A.C., Esener, S.C., Heller, M.J., and Messmer, B.T. (2008) Coupled rolling circle amplification loop-mediated amplification for rapid detection of short DNA sequences, Biotechniques, 45, 275–280, doi: 10.2144/000112910.

63. Li, X.H., Zhang, X.L., Wu, J., Lin, N., Sun, W.M., Chen, M., Ou, Q.S., and Lin, Z.Y. (2019) Hyperbranched rolling circle amplification (HRCA)-based fluorescence biosensor for ultrasensitive and specific detection of single-nucleotide polymorphism genotyping associated with the therapy of chronic hepatitis B virus infection, Talanta, 191, 277–282, doi: 10.1016/j.talanta.2018.08.064.

64. Schopf, E., Liu, Y., Deng, J.C., Yang, S., Cheng, G., and Chen, Y. (2011) Mycobacterium tuberculosis detection via rolling circle amplification, Anal. Methods, 3, 267–273, doi: 10.1039/C0AY00529K.

65. Cheng, Y., Zhang, X., Li, Z., Jiao, X., Wang, Y., and Zhang, Y. (2009) Highly sensitive determination of microRNA using target-primed and branched rolling-circle amplification, Angew. Chem. Int. Ed. Engl., 48, 3268–3272, doi: 10.1002/anie.200805665.

66. Deng, R., Tang, L., Tian, Q., Wang, Y., Lin, L., and Li, J. (2014) Toehold-initiated rolling circle amplification for visualizing individual microRNAs in situ in single cells, Angew. Chem. Int. Ed. Engl., 53, 2389–2393, doi: 10.1002/anie.201309388.

67. Mashimo, Y., Mie, M., Suzuki, S., and Kobatake, E. (2017) Detection of small RNA molecules by a combination of branched rolling circle amplification and bioluminescent pyrophosphate assay, Anal. Bioanal. Chem., 401, 221–227, doi: 10.1007/s00216-011-5083-3.

68. Cui, W., Wang, L., Xu, X., Wang, Y., and Jiang, W. (2017) A loop-mediated cascade amplification strategy for highly sensitive detection of DNA methyltransferase activity, Sens. Actuat. B: Chemical, 244, 599–605, doi: 10.1016/j.snb.2017.01.013.

69. Qing, T., He, D., He, X., Wang, K., Xu, F., Wen, L., Shangguan, J., Mao, Z., and Lei, Y. (2016) Nucleic acid tool enzymes-aided signal amplification strategy for biochemical analysis: status and challenges, Anal. Bioanal. Chem., 408, 2793–2811, doi: 10.1007/s00216-015-9240-y.

70. Dean, F.B., Nelson, J.R., Giesler, T.L., and Lasken, R.S. (2001) Rapid amplification of plasmid and phage DNA using Phi29 DNA polymerase and multiply-primed rolling circle amplification, Genome Res., 11, 1095–1099, doi: 10.1101/gr.180501.

71. Li, Y., Kim, H.J., Zheng, C., Chow, W.H.A., Lim, J., Keenan, B., Pan, X., Lemieux, B., and Kong, H. (2008) Primase-based whole genome amplification, Nucleic Acids Res., 36, e79, doi: 10.1093/nar/gkn377.

72. Miao, P., Tang, Y., Wang, B., Yin, J., and Ning, L. (2015) Signal amplification by enzymatic tools for nucleic acids, Trends Anal. Chem., 67, 1–15, doi: 10.1016/j.trac.2014.12.006.

73. Mol, C.D., Kuo, C.F., Thayer, M.M., Cunningham, R.P., and Tainer, J.A. (1995) Structure and function of the multifunctional DNA-repair enzyme exonuclease III, Nature, 374, 381–386, doi: 10.1038/374381a0.

74. Zuo, X., Xia, F., Xiao, Y., and Plaxco, K.W. (2010) Sensitive and selective amplified fluorescence DNA detection based on exonuclease III-aided target recycling, J. Am. Chem. Soc., 132, 1816–1818, doi: 10.1021/ja909551b.

75. Yan, M., Bai, W., Zhu, C., Huang, Y., Yan, J., and Chen, A. (2016) Design of nuclease-based target recycling signal amplification in aptasensors, Biosens. Bioelectron., 77, 613–623, doi: 10.1016/j.bios.2015.10.015.

76. Yang, W., Tian, J., Ma, Y., Wang, L., Zhao, Y., and Zhao, S. (2015) A label-free fluorescent probe based on DNA-templated silver nanoclusters and exonuclease III-assisted recycling amplification detection of nucleic acid, Anal. Chim. Acta, 900, 90–96, doi: 10.1016/j.aca.2015.10.015.

77. Xu, L., Shen, X., Li, B., Zhu, C., and Zhou, X. (2017) G-Quadruplex based Exo III-assisted signal amplification aptasensor for the colorimetric detection of adenosine, Anal. Chim. Acta, 980, 58–64, doi: 10.1016/j.aca.2017.05.015.

78. Gao, Y., and Li, B. (2013) G-Quadruplex DNAzyme-based chemiluminescence biosensing strategy for ultrasensitive DNA detection: combination of exonuclease III-assisted signal amplification and carbon nanotubes-assisted background reducing, Anal. Chem., 85, 11494–11500, doi: 10.1021/ac402728d.

79. Gan, X., Zhao, H., Chen, S., and Quan, X. (2015) Electrochemical DNA sensor for specific detection of picomolar Hg (II) based on exonuclease III-assisted recycling signal amplification, Analyst, 140, 2029–2036, doi: 10.1039/C5AN00082C.

80. Yang, Z., Sismour, A.M., and Benner, S.A. (2007) Nucleoside α-thiotriphosphates, polymerases and the exonuclease III analysis of oligonucleotides containing phosphorothioate linkages, Nucleic Acids Res., 35, 3118–3127, doi: 10.1093/nar/gkm168.

81. Xu, Q., Cao, A., Zhang, L.-F., and Zhang, C.-Y. (2012) Rapid and label-free monitoring of exonuclease III-assisted target recycling amplification, Anal. Chem., 84, 10845–10851, doi: 10.1021/ac303095z.

82. Wang, Y., Wu, Y., Wang, Y., Zhou, B., and Wu, S. (2015) A sensitive immobilization-free electrochemical assay for T4PNK activity based on exonuclease III-assisted recycling, RSC Adv., 5, 75348–75353, doi: 10.1039/C5RA12849H.

83. Li, W., Liu, X., Hou, T., Li, H., and Li, F. (2015) Ultrasensitive homogeneous electrochemical strategy for DNA methyltransferase activity assay based on autonomous exonuclease III-assisted isothermal cycling signal amplification, Biosens. Bioelectron., 70, 304–309, doi: 10.1016/j.bios.2015.03.060.

84. Min, X., Xia, L., Zhuang, Y., Wang, X., Du, J., Zhang, X., Lou, X., and Xia, F. (2017) An AIEgens and exonuclease III aided quadratic amplification assay for detecting and cellular imaging of telomerase activity, Sci. Bull., 62, 997–1003, doi: 10.1016/j.scib.2017.06.008.

85. Yan, L., Nakayama, S., and Sintim, H.O. (2013) Probe design rules and effective enzymes for endonuclease-based detection of nucleic acids, Bioorg. Med. Chem., 21, 6181–6185, doi: 10.1016/j.bmc.2013.04.009.

86. Liu, S., Zhang, C., Ming, J., Wang, C., Liu, T., and Li, F. (2013) Amplified detection of DNA by an analyte-induced Y-shaped junction probe assembly followed with a nicking endonuclease-mediated autocatalytic recycling process, Chem. Commun., 49, 7947–7949, doi: 10.1039/c3cc45211e.

87. Chen, M., Gan, N., Li, T., Wang, Y., Xu, Q., and Chen, Y. (2017) An electrochemical aptasensor for multiplex antibiotics detection using Y-shaped DNA-based metal ions encoded probes with NMOF substrate and CSRP target-triggered amplification strategy, Anal. Chim. Acta, 968, 30–39, doi: 10.1016/j.aca.2017.03.024.

88. Wang, Q., Yang, L., Yang, X., Wang, K., He, L., Zhu, J., and Su, T. (2012) An electrochemical DNA biosensor based on the “Y” junction structure and restriction endonuclease-aided target recycling strategy, Chem. Commun., 48, 2982–2984, doi: 10.1039/c2cc17679c.

89. Huang, Y., Wang, W., Wu, T., Xu, L.-P., Wen, Y., and Zhang, X. (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, doi: 10.1007/s00216-016-9925-x.

90. Zhao, Z., Chen, S., Wang, J., Su, J., Xu, J., Mathur, S., Fan, C., and Song, S. (2017) Nuclease-free target recycling signal amplification for ultrasensitive multiplexing DNA biosensing, Biosens. Bioelectron., 94, 605–608, doi: 10.1016/j.bios.2017.03.051.

91. Kiesling, T., Cox, K., Davidson, E.A., Dretchen, K., Grater, G., Hibbard, S., and Danielsen, M. (2007) Sequence specific detection of DNA using nicking endonuclease signal amplification (NESA), Nucleic Acids Res., 35, e117, doi: 10.1093/nar/gkm654.

92. Lin, Z., Yang, W., Zhang, G., Liu, Q., Qiu, B., Cai, Z., and Chen, G. (2011) An ultrasensitive colorimeter assay strategy for p53 mutation assisted by nicking endonuclease signal amplification, Chem. Commun., 47, 9069–9071, doi: 10.1039/C1CC13146J.

93. Chen, J., Zhang, J., Li, J., Fu, F., Yang, H.H., and Chen, G. (2010) An ultrahighly sensitive and selective electrochemical DNA sensor via nicking endonuclease assisted current change amplification, Chem. Commun., 46, 5939–5941, doi: 10.1039/c0cc00748j.

94. Vijayan, A.N., Liu, Z., Zhao, H., and Zhang, P. (2019) Nicking enzyme-assisted signal-amplifiable Hg2+ detection using upconversion nanoparticles, Anal. Chim. Acta, 1072, 75–80, doi: 10.1016/j.aca.2019.05.001.

95. Xie, L.S., Li, T.H., Hu, F.T., Jiang, Q.L., Wang, Q.Q., and Gan, N. (2019) A novel microfluidic chip and antibody-aptamer based multianalysis method for simultaneous determination of several tumor markers with polymerization nicking reactions for homogenous signal amplification, Microchem. J., 147, 454–462, doi: 10.1016/j.microc.2019.03.028.

96. Guo, Q., Yang, X., Wang, K., Tan, W., Li, W., Tang, H., and Li, H. (2009) Sensitive fluorescence detection of nucleic acids based on isothermal circular strand-displacement polymerization reaction, Nucleic Acids Res., 37, e20, doi: 10.1093/nar/gkn1024.

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

98. Gao, F., Du, L., Zhang, Y., Tang, D., and Du, Y. (2015) Molecular beacon mediated circular strand displacement strategy for constructing a ratiometric electrochemical deoxyribonucleic acid sensor, Anal. Chim. Acta, 883, 67–73, doi: 10.1016/j.aca.2015.04.058.

99. Wang, T., Zhang, Z., Li, Y., and Xie, G. (2015) Amplified electrochemical detection of mecA gene in methicillin-resistant Staphylococcus aureus based on target recycling amplification and isothermal strand-displacement polymerization reaction, Sens. Actuat. B: Chemical, 221, 148–154, doi: 10.1016/j.snb.2015.06.057.

100. Dirks, R.M., and Pierce, N.A. (2004) Triggered amplification by hybridization chain reaction, Proc. Natl. Acad. Sci. USA, 101, 15275–15278, doi: 10.1073/pnas.0407024101.

101. Xuan, F., and Hsing, I.M. (2014) Triggering hairpin-free chain-branching growth of fluorescent DNA dendrimers for nonlinear hybridization chain reaction, J. Am. Chem. Soc., 136, 9810–9813, doi: 10.1021/ja502904s.

102. Bi, S., Chen, M., Jia, X., Dong, Y., and Wang, Z. (2015) Hyperbranched hybridization chain reaction for triggered signal amplification and concatenated logic circuits, Angew. Chem. Int. Ed., 54, 8144–8148, doi: 10.1002/anie.201501457.

103. Yang, X., Yuebo, Yu, Y., and Gao, Z. (2014) A highly sensitive plasmonic DNA assay based on triangular silver nanoprism etching, ACS Nano, 85, 4902–4907, doi: 10.1021/nn5008786.

104. 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, doi: 10.1039/C5CC05499K.

105. Wu, Z., Liu, G.-Q., Yang, X.-L., and Jiang, J.-H. (2015) Electrostatic nucleic acid nanoassembly enables hybridization chain reaction in living cells for ultrasensitive mRNA imaging, J. Am. Chem. Soc., 137, 6829–6836, doi: 10.1021/jacs.5b01778.

106. Guo, J., Wang, J., Zhao, J., Guo, Z., and Zhang, Y. (2016) Ultrasensitive multiplexed immunoassay for tumor biomarkers based on DNA hybridization chain reaction amplifying signal, ACS Appl. Materials Interfaces, 8, 6898–6904, doi: 10.1021/acsami.6b00756.

107. Jie, G., and Jie, G. (2016) Sensitive electrochemiluminescence detection of cancer cells based on a CdSe/ZnS quantum dot nanocluster by multibranched hybridization chain reaction on gold nanoparticles, RSC Adv., 6, 24780–24785, doi: 10.1039/C6RA00750C.

108. Choi, H.M.T., Chang, J.Y., Trinh, L.A., Padilla, J.E., Fraser, S.E., and Pierce, N.F. (2010) Programmable in situ amplification for multiplexed imaging of mRNA expression, Nat. Biotechnol., 28, 1208–1214, doi: 10.1038/nbt.1692.

109. Bertoli, G., Cava, C., and Castiglioni, I. (2015) MicroRNAs: new biomarkers for diagnosis prognosis, therapy prediction and therapeutic tools for breast cancer, Theranostics, 5, 1122–1143, doi: 10.7150/thno.11543.

110. Zhang, J., Zhang, W., and Gu, Y. (2018) Enzyme-free isothermal target-recycled amplification combined with PAGE for direct detection of microRNA-21, Anal. Biochem., 550, 117–122, doi: 10.1016/j.ab.2018.04.024.

111. 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, doi: 10.1016/j.bios.2016.06.057.

112. 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, doi: 10.1039/C4AY02142H.

113. Dong, G., Dai, J., Jin, L., Shi, H., Wang, F., Zhou, C., Zheng, B., Guo, Y., and Dan Xiao, D. (2019) A rapid room-temperature DNA amplification and detection strategy based on nicking endonuclease and catalyzed hairpin assembly, Anal. Methods, 11, 2537–2541, doi: 10.1039/C9AY00507B.

114. Xu, J., Guo, J., Maina, S.W., Yang, Y., Hu, Y., Li, X., Qiu, J., and Xin, Z. (2018) An aptasensor for Staphylococcus aureus based on nicking enzyme amplification reaction and rolling circle amplification, Anal. Biochem., 549, 136–142, doi: 10.1016/j.ab.2018.03.013.

115. Chen, D., Zhang, M., Ma, M., Hai, H., Li, J., and Shan, Y. (2019) A novel electrochemical DNA biosensor for transgenic soybean detection based on triple signal amplification, Anal. Chim. Acta, 1078, 24–31, doi: 10.1016/j.aca.2019.05.074.

116. Song, H., Yang, Z., Jiang, M., Zhang, G., Gao, Y., and Shen, Z., Wu, Z.-S., and Lou, Y. (2019) Target-catalyzed hairpin structure-mediated padlock cyclization for ultrasensitive rolling circle amplification, Talanta, 204, 29–35, doi: 10.1016/j.talanta.2019.05.057.

117. Chen, J., and Zhou, S. (2016) Label-free DNA Y junction for bisphenol A monitoring using exonuclease III-based signal protection strategy, Biosens. Bioelectron., 77, 277–283, doi: 10.1016/j.bios.2015.09.042.

118. Sun, J., Jiang, W., Zhu, J., Li, W., and Wang, L. (2015) Label-free fluorescence dual-amplified detection of adenosine based on exonuclease III-assisted DNA cycling and hybridization chain reaction, Biosens. Bioelectron., 70, 15–20, doi: 10.1016/j.bios.2015.03.014.

119. Bi, S., Li, L., and Cui, Y. (2012) Exonuclease-assisted cascaded recycling amplification for label-free detection of DNA, Chem. Commun., 48, 1018–1020, doi: 10.1039/c1cc16684k.

120. D’Agata, R., and Spoto, G. (2019) Advanced methods for microRNA biosensing: a problem-solving perspective, Anal. Bioanal. Chem., 411, 4425–4444, doi: 10.1007/s00216-019-01621-8.