Ultra-sensitive colorimetric detection of SARS-CoV-2 by novel gold nanoparticle (AuNP)-assisted loop-mediated isothermal amplification (LAMP) and freezing methods.
False positivity identification
Gold nanoparticle
Loop-mediated isothermal amplification
SARS-CoV-2
Journal
Mikrochimica acta
ISSN: 1436-5073
Titre abrégé: Mikrochim Acta
Pays: Austria
ID NLM: 7808782
Informations de publication
Date de publication:
24 May 2024
24 May 2024
Historique:
received:
20
02
2024
accepted:
06
05
2024
medline:
25
5
2024
pubmed:
25
5
2024
entrez:
24
5
2024
Statut:
epublish
Résumé
Loop-mediated isothermal amplification (LAMP) is a molecular diagnosis technology with the advantages of isothermal reaction conditions and high sensitivity. However, the LAMP reactions are prone to producing false-positive results and thus are usually less reliable. This study demonstrates a gold nanoparticle (AuNP)-assisted colorimetric LAMP technique for diagnosing SARS-CoV-2, which aims to overcome the false-positive results. The AuNPs were functionalized with E gene probes, specifically tailored to bind to the amplified E-gene LAMP product, using the freezing method. Varied salt concentration and AuNP/probe combinations were tested for the highest visual performance. The experiments were conducted on synthetic SARS-CoV-2 RNA (Omicron variant), as well as on clinical samples. The assay showed an exceptional sensitivity of 8.05 fg of LAMP amplicon mixture (0.537 fg/µL). The average reaction time was ~ 30 min. In conclusion, AuNP-assisted LAMP detection will not identify any potential unspecific amplification, which helps to improve the efficiency and reliability of LAMP assays in point-of-care applications. The freezing method to functionalize the AuNPs with probes simplifies the assay, which can be utilized in further diagnostic studies.
Identifiants
pubmed: 38789855
doi: 10.1007/s00604-024-06422-0
pii: 10.1007/s00604-024-06422-0
doi:
Substances chimiques
Gold
7440-57-5
RNA, Viral
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
339Subventions
Organisme : Institute for Research and Medical Consultations, Imam Abdulrahman Bin Faisal University
ID : 2020-IRMC-S-3
Organisme : Institute for Research and Medical Consultations, Imam Abdulrahman Bin Faisal University
ID : 2020-IRMC-S-4
Organisme : Institute for Research and Medical Consultations, Imam Abdulrahman Bin Faisal University
ID : COVID19-2020-026-IRMC
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Rabaan AA, Smajlović S, Tombuloglu H, Ćordić S, Hajdarević A, Kudić N et al (2023) SARS-CoV-2 infection and multi-organ system damage: a review. Biomol Biomed 23(1):37–52
pubmed: 36124445
pmcid: 9901898
COVID - Coronavirus Statistics - Worldometer (2023) Available from: https://www.worldometers.info/coronavirus/ . Accessed 29 July 2023
Dorta-Gorrín A, Navas-Méndez J, Gozalo-Margüello M, Miralles L, García-Hevia L (2023) Detection of SARS-CoV-2 based on nucleic acid amplification tests (NAATs) and its integration into nanomedicine and microfluidic devices as point-of-care testing (POCT). Int J Mol Sci 24(12):10233
pubmed: 37373381
pmcid: 10299269
doi: 10.3390/ijms241210233
Filchakova O, Dossym D, Ilyas A, Kuanysheva T, Abdizhamil A, Bukasov R (2022) Review of COVID-19 testing and diagnostic methods. Talanta 244:123409
pubmed: 35390680
pmcid: 8970625
doi: 10.1016/j.talanta.2022.123409
Alhamid G, Tombuloglu H, Motabagani D, Motabagani D, Rabaan AA, Unver K et al (2022) Colorimetric and fluorometric reverse transcription loop-mediated isothermal amplification (RT-LAMP) assay for diagnosis of SARS-CoV-2. Funct Integr Genomics 22(6):1391–1401
pubmed: 36089609
pmcid: 9464610
doi: 10.1007/s10142-022-00900-5
Tombuloglu H, Sabit H, Al-Khallaf H, Kabanja JH, Alsaeed M, Al-Saleh N et al (2022) Multiplex real-time RT-PCR method for the diagnosis of SARS-CoV-2 by targeting viral N, RdRP and human RP genes. Sci Rep 12(1):2853
pubmed: 35181721
pmcid: 8857243
doi: 10.1038/s41598-022-06977-z
James AS, Alawneh JI (2020) COVID-19 infection diagnosis: potential impact of isothermal amplification technology to reduce community transmission of SARS-CoV-2. Diagnostics 10(6):399
pubmed: 32545412
pmcid: 7345291
doi: 10.3390/diagnostics10060399
Khan P, Aufdembrink LM, Engelhart AE (2020) Isothermal SARS-CoV-2 diagnostics: Tools for enabling distributed pandemic testing as a means of supporting safe reopenings. ACS Synth Biol 9(11):2861–2880
pubmed: 32966744
doi: 10.1021/acssynbio.0c00359
Dierks S, Bader O, Schwanbeck J, Groß U, Weig MS, Mese K et al (2021) Diagnosing SARS-CoV-2 with antigen testing, transcription-mediated amplification and real-time PCR. J Clin Med 10(11):2404
pubmed: 34072381
pmcid: 8199284
doi: 10.3390/jcm10112404
Amaral C, Antunes W, Moe E, Duarte AG, Lima LMP, Santos C et al (2021) A molecular test based on RT-LAMP for rapid, sensitive and inexpensive colorimetric detection of SARS-CoV-2 in clinical samples. Sci Rep 11(1):16430
pubmed: 34385527
pmcid: 8361189
doi: 10.1038/s41598-021-95799-6
Kashir J, Yaqinuddin A (2020) Loop mediated isothermal amplification (LAMP) assays as a rapid diagnostic for COVID-19. Med Hypotheses 141:109786
pubmed: 32361529
pmcid: 7182526
doi: 10.1016/j.mehy.2020.109786
Alhamid G, Tombuloglu H, Rabaan AA, Al-Suhaimi E (2022) SARS-CoV-2 detection methods: a comprehensive review. Saudi J Biol Sci 29(11):103465
pubmed: 36186678
pmcid: 9512523
doi: 10.1016/j.sjbs.2022.103465
Alsaeed M, Alhamid G, Tombuloglu H, Kabanja JH, Karagoz A, Tombuloglu G et al (2024) Ultrasensitive and fast detection of SARS-CoV-2 using RT-LAMP without pH-dependent dye. Funct Integr Genomics 24(1):16
pubmed: 38242999
doi: 10.1007/s10142-024-01297-z
Choi G, Moehling TJ, Meagher RJ (2023) Advances in RT-LAMP for COVID-19 testing and diagnosis. Expert Rev Mol Diagn 23(1):9–28
pubmed: 36695788
doi: 10.1080/14737159.2023.2169071
Tanner NA, Zhang Y, Evans TC (2015) Visual detection of isothermal nucleic acid amplification using pH-sensitive dyes. Biotechniques 58(2):59–68
pubmed: 25652028
doi: 10.2144/000114253
Goto M, Honda E, Ogura A, Nomoto A, Hanaki KI (2009) Colorimetric detection of loop-mediated isothermal amplification reaction by using hydroxy naphthol blue. Biotechniques 46(3):167–172
pubmed: 19317660
doi: 10.2144/000113072
Tessaro L, Aquino A, Panzenhagen P, Ochioni AC, Mutz YS, Raymundo-Pereira PA et al (2022) Development and application of an SPR nanobiosensor based on AuNPs for the detection of SARS-CoV-2 on food surfaces. Biosensors 12(12):1101
pubmed: 36551068
pmcid: 9776341
doi: 10.3390/bios12121101
Wang J, Drelich AJ, Hopkins CM, Mecozzi S, Li L, Kwon G et al (2022) Gold nanoparticles in virus detection: Recent advances and potential considerations for SARS-CoV-2 testing development. WIREs Nanomed Nanobiotechnol 14(1):e1754
doi: 10.1002/wnan.1754
Alhamid G, Tombuloglu H, Al-Suhaimi E (2023) Development of loop-mediated isothermal amplification (LAMP) assays using five primers reduces the false-positive rate in COVID-19 diagnosis. Sci Rep 13(1):5066
pubmed: 36977756
pmcid: 10044074
doi: 10.1038/s41598-023-31760-z
Ruang-areerate T, Saengsawang N, Ruang-areerate P, Ratnarathorn N, Thita T, Leelayoova S et al (2022) Distance-based paper device using combined SYBR safe and gold nanoparticle probe LAMP assay to detect Leishmania among patients with HIV. Sci Rep 12(1):14558
pubmed: 36028548
pmcid: 9418321
doi: 10.1038/s41598-022-18765-w
Ge Y, Zhou Q, Zhao K, Chi Y, Liu B, Min X et al (2017) Detection of influenza viruses by coupling multiplex reverse-transcription loop-mediated isothermal amplification with cascade invasive reaction using nanoparticles as a sensor. Int J Nanomedicine 12:2645–2656
pubmed: 28435249
pmcid: 5388202
doi: 10.2147/IJN.S132670
Carlos FF, Veigas B, Matias AS, Doria G, Flores O, Baptista PV (2017) Allele specific LAMP- gold nanoparticle for characterization of single nucleotide polymorphisms. Biotechnol Rep 16:21–25
doi: 10.1016/j.btre.2017.10.003
Liu B, Liu J (2017) Freezing directed construction of bio/nano interfaces: reagentless conjugation, denser spherical nucleic acids, and better nanoflares. J Am Chem Soc 139(28):9471–9474
pubmed: 28661156
doi: 10.1021/jacs.7b04885
Baptista PV, Koziol-Montewka M, Paluch-Oles J, Doria G, Franco R (2006) Gold-nanoparticle-probe-based assay for rapid and direct detection of Mycobacterium tuberculosis DNA in clinical samples 52(7):1433–4
Liu B, Liu J (2019) Interface-driven hybrid materials based on DNA-functionalized gold nanoparticles. Matter 1(4):825–847
doi: 10.1016/j.matt.2019.08.008
Moitra P, Alafeef M, Dighe K, Frieman MB, Pan D (2020) Selective naked-eye detection of SARS-CoV-2 mediated by n gene targeted antisense oligonucleotide capped plasmonic nanoparticles. ACS Nano 14(6):7617–7627
pubmed: 32437124
doi: 10.1021/acsnano.0c03822
Ventura BD, Cennamo M, Minopoli A, Campanile R, Censi SB, Terracciano D et al (2020) Colorimetric test for fast detection of SARS-CoV-2 in nasal and throat swabs. ACS Sens 5(10):3043–3048
pubmed: 32989986
pmcid: 7534800
doi: 10.1021/acssensors.0c01742
Sanromán-Iglesias M, Lawrie CH, Liz-Marzán LM, Grzelczak M (2018) The role of chemically modified DNA in discrimination of single-point mutation through plasmon-based colorimetric assays. ACS Appl Nano Mater 1(7):3741–3746
doi: 10.1021/acsanm.8b00984
Zhang J, Jin J, Du Y, Zhou X, Liang H, Jiang W (2019) Enhancing the stability of single-stranded DNA on gold nanoparticles as molecular machines through salt and acid regulation. J Mater Chem B 7:5554–5562
pubmed: 31465072
doi: 10.1039/C9TB01238A
Iglesias MS, Grzelczak M (2020) Using gold nanoparticles to detect single-nucleotide polymorphisms: toward liquid biopsy. Beilstein J Nanotechnol 11:263–284
pubmed: 32082965
pmcid: 7006498
doi: 10.3762/bjnano.11.20
Hu M, Yuan C, Tian T, Wang X, Sun J, Xiong E et al (2020) Single-step, salt-aging-free, and thiol-free freezing construction of AuNP-based bioprobes for advancing CRISPR-based diagnostics. J Am Chem Soc 142(16):7506–7513
pubmed: 32223241
doi: 10.1021/jacs.0c00217
Jaroenram W, Arunrut N, Kiatpathomchai W (2012) Rapid and sensitive detection of shrimp yellow head virus using loop-mediated isothermal amplification and a colorogenic nanogold hybridization probe. J Virol Methods 186(1–2):36–42
pubmed: 22960564
doi: 10.1016/j.jviromet.2012.08.013
Ye X, Fang X, Li X, Kong J (2018) Gold nanoparticle-mediated nucleic acid isothermal amplification with enhanced specificity. Anal Chim Acta 1043:150–157
pubmed: 30392663
doi: 10.1016/j.aca.2018.09.016
Qiu G, Gai Z, Tao Y, Schmitt J, Kullak-Ublick GA, Wang J (2020) Dual-functional plasmonic photothermal biosensors for highly accurate severe acute respiratory syndrome coronavirus 2 detection. ACS Nano 14(5):5268–5277
pubmed: 32281785
doi: 10.1021/acsnano.0c02439
Yano TA, Kajisa T, Ono M, Miyasaka Y, Hasegawa Y, Saito A, ... & Yasui, T (2022) Ultrasensitive detection of SARS-CoV-2 nucleocapsid protein using large gold nanoparticle-enhanced surface plasmon resonance. Sci Rep 12(1):1060
Karakuş E, Erdemir E, Demirbilek N, Liv L (2021) Colorimetric and electrochemical detection of SARS-CoV-2 spike antigen with a gold nanoparticle-based biosensor. Anal Chim Acta 1182:338939
pubmed: 34602210
pmcid: 8357269
doi: 10.1016/j.aca.2021.338939
Behrouzi K, Lin L (2022) Gold nanoparticle based plasmonic sensing for the detection of SARS-CoV-2 nucleocapsid proteins. Biosens Bioelectron 195:113669
pubmed: 34607117
doi: 10.1016/j.bios.2021.113669
Aithal S, Mishriki S, Gupta R, Sahu RP et al (2022) SARS-CoV-2 detection with aptamer-functionalized gold nanoparticles. Talanta 236:122841
pubmed: 34635231
doi: 10.1016/j.talanta.2021.122841
Zou L, Ling L (2018) Ultrasensitive detection of HIV DNA with polymerase chain reaction–dynamic light scattering. Anal Chem 90(22):13373–13377
pubmed: 30345744
doi: 10.1021/acs.analchem.8b03052
Kooti S, Kadivarian S, Abiri R et al (2023) Modified gold nanoparticle colorimetric probe-based biosensor for direct and rapid detection of Mycobacterium tuberculosis in sputum specimens. World J Microbiol Biotechnol 39:118
pubmed: 36918442
doi: 10.1007/s11274-023-03564-w
Suebsing R, Prombun P, Srisala J, Kiatpathomchai W (2013) Retracted: Loop-mediated isothermal amplification combined with colorimetric nanogold for detection of the microsporidian Enterocytozoon hepatopenaei in penaeid shrimp. J Appl Microbiol 114(5):1254–1263
pubmed: 23387348
doi: 10.1111/jam.12160
Gao Y, Deng X, Wen W, Zhang X, Wang S (2017) Ultrasensitive paper based nucleic acid detection realized by three-dimensional DNA-AuNPs network amplification. Biosens Bioelectron 92:529–535
pubmed: 27836603
doi: 10.1016/j.bios.2016.10.068
Choi JR, Liu Z, Hu J, Tang R, Gong Y, Feng S et al (2016) Polydimethylsiloxane-paper hybrid lateral flow assay for highly sensitive point-of-care nucleic acid testing. Anal Chem 88(12):6254–6264
pubmed: 27012657
doi: 10.1021/acs.analchem.6b00195
Weerathunge P, Ramanathan R, Torok VA, Hodgson K et al (2019) Ultrasensitive colorimetric detection of murine norovirus using NanoZyme aptasensor. Anal Chem 91(5):3270–3276
pubmed: 30642158
doi: 10.1021/acs.analchem.8b03300
Ma L, Yin L, Li X, Chen S, Peng L et al (2022) A smartphone-based visual biosensor for CRISPR-Cas powered SARS-CoV-2 diagnostics. Biosens Bioelectron 195:113646
pubmed: 34624801
doi: 10.1016/j.bios.2021.113646