Abstract
A sensing methodology that combines Au, tobacco mosaic virus (TMV), and folic acid for selective, sensitive, and colorimetric detection of tumor cells based on the peroxidase-like activity was reported in this study. Gold nanowires with a high aspect ratio were synthesized using TMV as a template. Au@TMV nanowire (AT) complex was obtained with diameter of 4 nm and length between 200 and 300 nm. In addition, since TMV was biocompatible and had many amino and carboxyl groups on its surface, AT was conjugated by folate to form a folic acid (FA)–conjugated AT composite (ATF) and tested by FTIR measurements. Furthermore, the peroxidase-like properties were studied and the optimal conditions for mimic enzyme activity were optimized. Finally, HeLa and other tumor cells expressed excessive receptors of folate on the surface, which can specifically bind to folic acid. As the specific binding of ATF with HeLa cells, the peroxidase properties of ATF were used for detection of cancer cells (Scheme 1). The cancer cells were detected not only qualitatively but also quantitatively. In this study, as low as 2000 cancer cells/mL could be detected using the current method.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad F, Ashraf N, Ashraf T, Zhou RB, Yin DC (2019) Biological synthesis of metallic nanoparticles (MNPs) by plants and microbes: their cellular uptake, biocompatibility, and biomedical applications. Appl Microbiol Biotechnol 103(7):2913–2935. https://doi.org/10.1007/s00253-019-09675-5
Alonso JM, Gorzny ML, Bittner AM (2013) The physics of tobacco mosaic virus and virus-based devices in biotechnology. Trends Biotechnol. 31(9):530–538. https://doi.org/10.1016/j.tibtech.2013.05.013
Asati A, Santra S, Kaittanis C, Nath S, Perez JM (2009) Oxidase - like activity of polymer - coated cerium oxide nanoparticles. Angew ChemInt Ed 48(13):2308–2312. https://doi.org/10.1002/anie.200805279
Bonanni A, Del Valle M (2010) Use of nanomaterials for impedimetric DNA sensors: a review. Anal Chim Acta 678(1):7–17. https://doi.org/10.1016/j.aca.2010.08.022
Bruckman MA, Kaur G, Lee LA, Xie F, Sepulveda J, Breitenkamp R, Zhang X, Joralemon M, Russell TP, Emrick T (2008) Surface modification of tobacco mosaic virus with “click” chemistry. ChemBioChem 9(4):519–523. https://doi.org/10.1002/cbic.200700559
Bruckman MA, Czapar AE, VanMeter A, Randolph LN, Steinmetz NF (2016) Tobacco mosaic virus-based protein nanoparticles and nanorods for chemotherapy delivery targeting breast cancer. J Control Release 231:103–113. https://doi.org/10.1016/j.jconrel.2016.02.045
Chattopadhyay K, Mazumdar S (2000) Structural and conformational stability of horseradish peroxidase: effect of temperature and pH. Biochemistry 39(1):263–270. https://doi.org/10.1021/bi990729o
Chen H, Crum M, Chavan D, Vu B, Kourentzi K, Willson RC (2018) Nanoparticle-based proximity ligation assay for ultrasensitive, quantitative detection of protein biomarkers. ACS Appl Mater Interfaces 10(38):31845–31849. https://doi.org/10.1021/acsami.8b01377
Cheung A, Bax HJ, Josephs DH, Ilieva KM, Pellizzari G, Opzoomer J, Bloomfield J, Fittall M, Grigoriadis A, Figini M (2016) Targeting folate receptor alpha for cancer treatment. Oncotarget 7(32):52553. https://doi.org/10.18632/oncotarget.9651
Fu F-F, Zhou B-Q, Ouyang Z-J, Wu Y-L, Zhu J-Y, Shen M-W, Xia J-D, Shi X-Y (2019) Multifunctional cholesterol-modified dendrimers for targeted drug delivery to cancer cells expressing folate receptors. Chin J Polym Sci 37(02):36–42+104-109. https://doi.org/10.1007/s10118-019-2172-9
Gao L, Zhuang J, Nie L, Zhang J, Zhang Y, Gu N, Wang T, Feng J, Yang D, Perrett S (2007) Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nat Nanotechnol 2(9):577. https://doi.org/10.1038/nnano.2007.260
Gao X, Hai X, Baigude H, Guan W, Liu Z (2016) Fabrication of functional hollow microspheres constructed from MOF shells: promising drug delivery systems with high loading capacity and targeted transport. Sci Rep 6:37705. https://doi.org/10.1038/srep37705
Glasgow J, Tullman-Ercek D (2014) Production and applications of engineered viral capsids. Appl Microbiol Biotechnol 98(13):5847–5858. https://doi.org/10.1007/s00253-014-5787-3
Gooding G Jr, Hebert T (1967) A simple technique for purification of tobacco mosaic virus in large quantities. Phytopathology 57(11):1285
Górzny MŁ, Walton AS, Evans SD (2010) Synthesis of high-surface-area platinum nanotubes using a viral template. Adv Funct Mater. 20(8):1295–1300. https://doi.org/10.1002/adfm.200902196
Guo J, Wang Y, Zhao M (2018a) 3D flower-like ferrous (II) phosphate nanostructures as peroxidase mimetics for sensitive colorimetric detection of hydrogen peroxide and glucose at nanomolar level. Talanta 182:230–240. https://doi.org/10.1016/j.talanta.2018.01.080
Guo J, Zhao X, Hu J, Lin Y, Wang Q (2018b) Tobacco mosaic virus with peroxidase-like activity for cancer cell detection through colorimetric assay. Mol Pharm 15(8):2946–2953. https://doi.org/10.1021/acs.molpharmaceut.7b00921
Henrick K, Thornton JM (1998) PQS: a protein quaternary structure file server. Trends Biochem Sci 23(9):358–361.https://doi.org/10.1016/S0968-0004(98)01253-5
Johnson KA, Goody RS (2011) The original Michaelis constant: translation of the 1913 Michaelis–Menten paper. Biochemistry 50(39):8264–8269. https://doi.org/10.1021/bi201284u
Josephy PD, Eling T, Mason RP (1982) The horseradish peroxidase-catalyzed oxidation of 3, 5, 3′, 5′-tetramethylbenzidine. Free radical and charge-transfer complex intermediates. J Biol Chem 257(7):3669–3675
Jv Y, Li B, Cao R (2010) Positively-charged gold nanoparticles as peroxidiase mimic and their application in hydrogen peroxide and glucose detection. Chem Commun (Camb) 46(42):8017–8019. https://doi.org/10.1039/c0cc02698k
Kang J, Yeom G, Jang H, Oh J, Park CJ, Kim MG (2019) Development of replication protein A-conjugated gold nanoparticles for highly sensitive detection of disease biomarkers. Anal Chem 91(15):10001–10007. https://doi.org/10.1021/acs.analchem.9b01827
Klug A (1999) The tobacco mosaic virus particle: structure and assembly. PhilosTransRSoc, B 354(1383):531–535. https://doi.org/10.1098/rstb.1999.0404
Knez M (2003) The tobacco mosaic virus (TMV) as biological template for nanostructuring. Dissertation. University of Stuttgart
Knez M, Bittner AM, Boes F, Wege C, Jeske H, Maiβ E, Kern K (2003) Biotemplate synthesis of 3-nm nickel and cobalt nanowires. Nano lett 3(8):1079–1082. https://doi.org/10.1021/nl0342545
Knez M, Sumser M, Bittner AM, Wege C, Jeske H, Martin TP, Kern K (2004) Spatially selective nucleation of metal clusters on the tobacco mosaic virus. Adv Funct Mater 14(2):116–124. https://doi.org/10.1002/adfm.200304376
Kohler N, Sun C, Wang J, Zhang M (2005) Methotrexate-modified superparamagnetic nanoparticles and their intracellular uptake into human cancer cells. J Chem Phys 21(19):8858–8864. https://doi.org/10.1021/la0503451
Li Y-Z, Li T-T, Chen W, Song Y-Y (2017) Co4N nanowires: noble-metal-free peroxidase mimetic with excellent salt-and temperature-resistant abilities. ACS Appl Mater Interfaces 9(35):29881–29888. https://doi.org/10.1021/acsami.7b09861
Liang M, Yan X (2019) Nanozymes: from new concepts, mechanisms, and standards to applications. Acc Chem Res. https://doi.org/10.1021/acs.accounts.9b00140
Lin Y, Ren J, Qu X (2014) Catalytically active nanomaterials: a promising candidate for artificial enzymes. Acc Chem Res 47(4):1097–1105. https://doi.org/10.1021/ar400250z
Luckanagul JA, Lee LA, You S, Yang X, Wang Q (2015) Plant virus incorporated hydrogels as scaffolds for tissue engineering possess low immunogenicity in vivo. J Biomed Mater Res A 103(3):887–895. https://doi.org/10.1002/jbm.a.35227
Mu J, Wang Y, Zhao M, Zhang L (2012) Intrinsic peroxidase-like activity and catalase-like activity of Co 3 O 4 nanoparticles. Chem Commun 48(19):2540–2542. https://doi.org/10.1039/c2cc17013b
Musumeci D, Platella C, Riccardi C, Moccia F, Montesarchio D (2017) Fluorescence sensing using DNA aptamers in cancer research and clinical diagnostics. Cancers 9(12):1–43. https://doi.org/10.3390/cancers9120174
Narayanan KB, Han SS (2017) Icosahedral plant viral nanoparticles - bioinspired synthesis of nanomaterials/nanostructures. Adv Colloid Interf Sci 248:1–19. https://doi.org/10.1016/j.cis.2017.08.005
Nicell JA, Wright H (1997) A model of peroxidase activity with inhibition by hydrogen peroxide. Enzyme MicrobTechnol 21(4):302–310. https://doi.org/10.1016/S0141-0229(97)00001-X
Niemeyer CM, Mirkin CA (2006) Nanobiotechnology: concepts, applications and perspectives. Chemical Industry Press, Beijing
Paterlini-Brechot P, Benali NL (2007) Circulating tumor cells (CTC) detection: clinical impact and future directions. Cancer Lett 253(2):180–204. https://doi.org/10.1016/j.canlet.2006.12.014
Pattanayek R, Stubbs G (1992) Structure of the U2 strain of tobacco mosaic virus refined at 3.5 Å resolution using X-ray fiber diffraction. J Mol Biol 228(2):516–528. https://doi.org/10.1016/0022-2836(92)90839-C
Preechakasedkit P, Siangproh W, Khongchareonporn N, Ngamrojanavanich N, Chailapakul O (2018) Development of an automated wax-printed paper-based lateral flow device for alpha-fetoprotein enzyme-linked immunosorbent assay. Biosens Bioelectron 102:27–32. https://doi.org/10.1016/j.bios.2017.10.051
Rodríguez-Galván A, Martínez-Lorán E, Naveja JJ, Ornelas-Soto N, A. Basiuk V, Contreras-Torres FF (2017) In-situ metallization of thermally-treated tobacco mosaic virus using silver nanoparticles. J Nanosci Nanotechnol 17(7):4740–4747. https://doi.org/10.1166/jnn.2017.13714
Şener G, Denizli A (2019) Identification of several toxic metal ions using a colorimetric sensor array. In: Biomimetic sensing. Humana Press, New Jersey, pp 81–86. https://doi.org/10.1007/978-1-4939-9616-2_7
Shahjaman M, Rahman MR, Islam SMS, Mollah MNH (2019) A robust approach for identification of cancer biomarkers and candidate drugs. Medicina 55(6):269. https://doi.org/10.3390/medicina55060269
Shi W, Zhang X, He S, Huang Y (2011) CoFe2O4 magnetic nanoparticles as a peroxidase mimic mediated chemiluminescence for hydrogen peroxide and glucose. Chem Commun(Camb) 47(38):10785–10787. https://doi.org/10.1039/c1cc14300j
Shuai H-L, Huang K-J, Zhang W-J, Cao X, Jia M-P (2017) Sandwich-type microRNA biosensor based on magnesium oxide nanoflower and graphene oxide–gold nanoparticles hybrids coupling with enzyme signal amplification. SensActuators B 243:403–411. https://doi.org/10.1016/j.snb.2016.12.001
Song Y, Qu K, Zhao C, Ren J, Qu X (2010) Graphene oxide: intrinsic peroxidase catalytic activity and its application to glucose detection. Adv Mater 22(19):2206–2210. https://doi.org/10.1002/adma.200903783
Song Y, Chen Y, Feng L, Ren J, Qu X (2011) Selective and quantitative cancer cell detection using target-directed functionalized graphene and its synergetic peroxidase-like activity. Chem Commun (Camb) 47(15):4436–4438. https://doi.org/10.1039/c0cc05533f
Tao Y, Lin Y, Huang Z, Ren J, Qu X (2013) Incorporating graphene oxide and gold nanoclusters: a synergistic catalyst with surprisingly high peroxidase-like activity over a broad pH range and its application for cancer cell detection. Adv Mater 25(18):2594–2599. https://doi.org/10.1002/adma.201204419
Tsukamoto R, Muraoka M, Seki M, Tabata H, Yamashita I (2007) Synthesis of CoPt and FePt3 nanowires using the central channel of tobacco mosaic virus as a biotemplate. Chem Mater 19(10):2389–2391. https://doi.org/10.1021/cm062187k
Veitch NC (2004) Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry 65(3):249–259. https://doi.org/10.1016/j.phytochem.2003.10.022
Wang L, Wang S, Xu M, Hu X, Zhang H, Wang Y, Huang W (2013) A Au-functionalized ZnO nanowire gas sensor for detection of benzene and toluene. Phys Chem Chem Phys 15(40):17179–17186. https://doi.org/10.1039/C3CP52392F
Wang Q, Zou L, Yang X, Liu X, Nie W, Zheng Y, Cheng Q, Wang K (2019) Direct quantification of cancerous exosomes via surface plasmon resonance with dual gold nanoparticle-assisted signal amplification. Biosens Bioelectron 135:129–136. https://doi.org/10.1016/j.bios.2019.04.013
Wei H, Wang E (2008) Fe3O4 magnetic nanoparticles as peroxidase mimetics and their applications in H2O2 and glucose detection. Anal Chem 80(6):2250–2254. https://doi.org/10.1021/ac702203f
Wilson R (2008) The use of gold nanoparticles in diagnostics and detection. Chem Soc Rev 37(9):2028–2045. https://doi.org/10.1039/b712179m
Wnek M, Gorzny ML, Ward MB, Walti C, Davies AG, Brydson R, Evans SD, Stockley PG (2013) Fabrication and characterization of gold nano-wires templated on virus-like arrays of tobacco mosaic virus coat proteins. Nanotechnology 24(2):025605. https://doi.org/10.1088/0957-4484/24/2/025605
Wu G-W, He S-B, Peng H-P, Deng H-H, Liu A-L, Lin X-H, Xia X-H, Chen W (2014) Citrate-capped platinum nanoparticle as a smart probe for ultrasensitive mercury sensing. Anal Chem 86(21):10955–10960. https://doi.org/10.1021/ac503544w
Yang L, Zhang J, Ding JL (2011) Peptide isomerization induced by pH change regulates the S1 binding site in ficolins. Aust J Chem 64(7):887–893. https://doi.org/10.1071/CH11050
Yang C, Choi CH, Lee CS, Yi H (2013a) A facile synthesis-fabrication strategy for integration of catalytically active viral-palladium nanostructures into polymeric hydrogel microparticles via replica molding. ACS Nano 7(6):5032–5044. https://doi.org/10.1021/nn4005582
Yang X-j, Xu X-m, Xu j, Han Y-f (2013b) Iron oxychloride (FeOCl): an efficient Fenton-like catalyst for producing hydroxyl radicals in degradation of organic contaminants. J Am Chem Soc 135(43):16058–16061. https://doi.org/10.1021/ja409130c
Yu Y-y, Zhang L, Sun X-y, Li C-l, Qiu Y, Sun H-p, Tang D-q, Liu Y-w, Yin X-x (2015) A sensitive colorimetric strategy for monitoring cerebral β-amyloid peptides in AD based on dual-functionalized gold nanoplasmonic particles. Chem Commun 51(42):8880–8883. https://doi.org/10.1039/c5cc01855b
Zhang L, Hai X, Xia C, Chen X-W, Wang J-H (2017) Growth of CuO nanoneedles on graphene quantum dots as peroxidase mimics for sensitive colorimetric detection of hydrogen peroxide and glucose. Sensors Actuators B Chem 248:374–384. https://doi.org/10.1016/j.snb.2017.04.011
Zhang Y, Dong Y, Zhou J, Li X, Wang F (2018) Application of plant viruses as a biotemplate for nanomaterial fabrication. Molecules 23(9):2311. https://doi.org/10.3390/molecules23092311
Zopf D, Jatschka J, Dathe A, Jahr N, Fritzsche W, Stranik O (2016) Hyperspectral imaging of plasmon resonances in metallic nanoparticles. BiosensBioelectron 81:287–293. https://doi.org/10.1016/j.bios.2016.03.001
Acknowledgments
The authors would like to express special appreciation to scientist Yanhong Liu (Molecular Characterization of Foodborne Pathogens Research Unit, Eastern Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, Wyndmoor, PA 19038, USA) for polishing the manuscript.
Funding
This study was funded by National Natural Science Foundation of China (51678120).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 287 kb)
Rights and permissions
About this article
Cite this article
Qu, Y., Yang, Y., Du, R. et al. Peroxidase activities of gold nanowires synthesized by TMV as template and their application in detection of cancer cells. Appl Microbiol Biotechnol 104, 3947–3957 (2020). https://doi.org/10.1007/s00253-020-10520-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10520-3