Coupling of an Au@AgPt nanozyme array with an micrococcal nuclease-specific responsiveness strategy for colorimetric/SERS sensing of <i>Staphylococcus aureus</i> in patients with sepsis

Xueqin Huang; Yingqi Yang; Hanlin Zhou; Liping Hu; Annan Yang; Hua Jin; Biying Zheng; Jiang Pi; Jun Xu; Pinghua Sun; Huai-Hong Cai; Xujing Liang; Bin Pan; Junxia Zheng; Haibo Zhou

doi:10.1016/j.jpha.2024.101085

Volume 15 Issue 2

Feb. 2025

Turn off MathJax

Article Contents

Article Navigation > Journal of Pharmaceutical Analysis > 2025 > 15(2): 101085

Xueqin Huang, Yingqi Yang, Hanlin Zhou, Liping Hu, Annan Yang, Hua Jin, Biying Zheng, Jiang Pi, Jun Xu, Pinghua Sun, Huai-Hong Cai, Xujing Liang, Bin Pan, Junxia Zheng, Haibo Zhou. Coupling of an Au@AgPt nanozyme array with an micrococcal nuclease-specific responsiveness strategy for colorimetric/SERS sensing of Staphylococcus aureus in patients with sepsis[J]. Journal of Pharmaceutical Analysis, 2025, 15(2): 101085. doi: 10.1016/j.jpha.2024.101085

Citation:

Xueqin Huang, Yingqi Yang, Hanlin Zhou, Liping Hu, Annan Yang, Hua Jin, Biying Zheng, Jiang Pi, Jun Xu, Pinghua Sun, Huai-Hong Cai, Xujing Liang, Bin Pan, Junxia Zheng, Haibo Zhou. Coupling of an Au@AgPt nanozyme array with an micrococcal nuclease-specific responsiveness strategy for colorimetric/SERS sensing of Staphylococcus aureus in patients with sepsis[J]. Journal of Pharmaceutical Analysis, 2025, 15(2): 101085. doi: 10.1016/j.jpha.2024.101085

Citation:

Xueqin Huang, Yingqi Yang, Hanlin Zhou, Liping Hu, Annan Yang, Hua Jin, Biying Zheng, Jiang Pi, Jun Xu, Pinghua Sun, Huai-Hong Cai, Xujing Liang, Bin Pan, Junxia Zheng, Haibo Zhou. Coupling of an Au@AgPt nanozyme array with an micrococcal nuclease-specific responsiveness strategy for colorimetric/SERS sensing of Staphylococcus aureus in patients with sepsis[J]. Journal of Pharmaceutical Analysis, 2025, 15(2): 101085. doi: 10.1016/j.jpha.2024.101085

PDF( 5401 KB)

Coupling of an Au@AgPt nanozyme array with an micrococcal nuclease-specific responsiveness strategy for colorimetric/SERS sensing of Staphylococcus aureus in patients with sepsis

doi: 10.1016/j.jpha.2024.101085

a. College of Pharmacy, The Second Clinical Medical College (Shenzhen People's Hospital), The Fifth Affiliated Hospital, Jinan University, Guangzhou, 510632, China;
b. Research Center of Nano Technology and Application Engineering, The First Dongguan Affiliated Hospital, School of Medical Technology, Guangdong Medical University, Dongguan, Guangdong, 523000, China;
c. School of Pharmacy, Shihezi University, Shihezi, Xinjiang, 832003, China;
d. College of Chemistry and Materials Science, Jinan University, Guangzhou, 510632, China;
e. The First Affiliated Hospital of Jinan University, Jinan University, Guangzhou, 510632, China;
f. School of Biomedical and Pharmaceutical Sciences, Guangdong University of Technology, Guangzhou, 510006, China

Funds:

This work is financially supported by the National Natural Science Foundation of China (Grant Nos.: 82373833, 22177039, and 82304438), the National Key Research and Development Program of China (Grant No.: 2021YFC2300400), and Guangdong Basic and Applied Basic Research Foundation, China (Grant Nos.: 2024A1515012204, 2022A1515010300, and 2022A1515110618).

Received Date: May 01, 2024
Accepted Date: Aug. 22, 2024
Rev Recd Date: Aug. 18, 2024
Publish Date: Aug. 27, 2024

Abstract

Abstract

Rapid and ultrasensitive detection of pathogen-associated biomarkers is vital for the early diagnosis and therapy of bacterial infections. Herein, we developed a close-packed and ordered Au@AgPt array coupled with a cascade triggering strategy for surface-enhanced Raman scattering (SERS) and colorimetric identification of the Staphylococcus aureus biomarker micrococcal nuclease (MNase) in serum samples. The trimetallic Au@AgPt nanozymes can catalyze the oxidation of 3,3’,5,5’-tetramethylbenzidine (TMB) molecules to SERS-enhanced oxidized TMB (oxTMB), accompanied by the color change from colorless to blue. In the presence of S. aureus, the secreted MNase preferentially cut the nucleobase AT-rich regions of DNA sequences on magnetic beads (MBs) to release alkaline phosphatase (ALP), which subsequently mediated the oxTMB reduction for inducing the colorimetric/SERS signal fade away. Using this “on-to-off” triggering strategy, the target S. aureus can be recorded in a wide linear range with a limit of detection of 38 CFU/mL in the colorimetric mode and 6 CFU/mL in the SERS mode. Meanwhile, the MNase-mediated strategy characterized by high specificity and sensitivity successfully discriminated between patients with sepsis (n = 7) and healthy participants (n = 3), as well as monitored the prognostic progression of the disease (n = 2). Overall, benefiting from highly active and dense “hot spot” substrate, MNase-mediated cascade response strategy, and colorimetric/SERS dual-signal output, this methodology will offer a promising avenue for the early diagnosis of S. aureus infection.
- Au@AgPt nanoarrays,
- Surface-enhanced Raman scattering,
- Colorimetry,
- Cascade response strategy,
- MNase

FullText(HTML)

References(44)

References

[1]	T.L. Burke, M.E. Rupp, P.D. Fey, Staphylococcus epidermidis, Trends Microbiol. 31 (2023) 763-764.
[2]	J.M. Kwiecinski, A.R. Horswill, Staphylococcus aureus bloodstream infections: Pathogenesis and regulatory mechanisms, Curr. Opin. Microbiol. 53 (2020) 51-60.
[3]	S.S. Samani, A. Khojastehnezhad, M. Ramezani, et al., Ultrasensitive detection of micrococcal nuclease activity and Staphylococcus aureus contamination using optical biosensor technology-a review, Talanta 226 (2021), 122168.
[4]	J. Allan, R.M. Fraser, T. Owen-Hughes, et al., Micrococcal nuclease does not substantially bias nucleosome mapping, J. Mol. Biol. 417 (2012) 152-164.
[5]	Y. He, L. Xiong, X. Xing, et al., An ultra-high sensitive platform for fluorescence detection of micrococcal nuclease based on graphene oxide, Biosens. Bioelectron. 42 (2013) 467-473.
[6]	S.P. Yazdankhah, L. Soelveroed, S. Simonsen, et al., Development and evaluation of an immunomagnetic separation-ELISA for the detection of Staphylococcus aureus thermostable nuclease in composite milk, Vet. Microbiol. 67 (1999) 113-125.
[7]	E.A. Ottesen, J.W. Hong, S.R. Quake, et al., Microfluidic digital PCR enables multigene analysis of individual environmental bacteria, Science 314 (2006) 1464-1467.
[8]	D. Kang, M.M. Ali, K. Zhang, et al., Rapid detection of single bacteria in unprocessed blood using Integrated Comprehensive Droplet Digital Detection, Nat. Commun. 5 (2014), 5427.
[9]	J. Zhou, R. Fu, F. Tian, et al., Dual enzyme-induced Au-Ag alloy nanorods as colorful chromogenic substrates for sensitive detection of Staphylococcus aureus, ACS Appl. Bio Mater. 3 (2020) 6103-6109.
[10]	Y. Chen, L. Wang, W. Jiang, Micrococcal nuclease detection based on peptide-bridged energy transfer between quantum dots and dye-labeled DNA, Talanta 97 (2012) 533-538.
[11]	X. Huang, Z. Zhang, L. Chen, et al., Multifunctional Au nano-bridged nanogap probes as ICP-MS/SERS dual-signal tags and signal amplifiers for bacteria discriminating, quantitative detecting and photothermal bactericidal activity, Biosens. Bioelectron. 212 (2022), 114414.
[12]	X. Huang, B. Sheng, H. Tian, et al., Real-time SERS monitoring anticancer drug release along with SERS/MR imaging for pH-sensitive chemo-phototherapy, Acta Pharm. Sin. B 13 (2023) 1303-1317.
[13]	X. Huang, Q. Chen, Y. Ma, et al., Chiral Au nanostars for SERS sensing of enantiomers discrimination, multibacteria recognition and photothermal antibacterial application, Chem. Eng. J. 479 (2024), 147528.
[14]	J.Y. Kim, D. Han, G.M. Crouch, et al., Capture of single silver nanoparticles in nanopore arrays detected by simultaneous amperometry and surface-enhanced Raman scattering, Anal. Chem. 91 (2019) 4568-4576.
[15]	S. Xiang, C. Ge, S. Li, et al., In situ detection of endotoxin in bacteriostatic process by SERS chip integrated array microchambers within bioscaffold nanostructures and SERS tags, ACS Appl. Mater. Interfaces 12 (2020) 28985-28992.
[16]	L. Zhang, R. Hao, D. Zhang, et al., Shape-controlled hierarchical flowerlike Au nanostructure microarrays by electrochemical growth for surface-enhanced Raman spectroscopy application, Anal. Chem. 92 (2020) 9838-9846.
[17]	X. Zhou, H. Huang, Y. Yang, et al., Dendritic alloy shell Au@AgPt yolk sensor with excellent dual SERS enhancement and catalytic performance for in situ SERS monitoring reaction, Sens. Actuat. B Chem. 394 (2023), 134385.
[18]	J. Li, W. Liu, X. Wu, et al., Mechanism of pH-switchable peroxidase and catalase-like activities of gold, silver, platinum and palladium, Biomaterials 48 (2015) 37-44.
[19]	Y. Lin, J. Ren, X. Qu, Nano-gold as artificial enzymes: Hidden talents, Adv. Mater. Deerfield Beach Fla 26 (2014) 4200-4217.
[20]	J. Liu, L. Meng, Z. Fei, et al., On the origin of the synergy between the Pt nanoparticles and MnO₂ nanosheets in Wonton-like 3D nanozyme oxidase mimics, Biosens. Bioelectron. 121 (2018) 159-165.
[21]	C. Wang, Y. Gao, S. Hu, et al., MnO₂ coated Au nanoparticles advance SERS detection of cellular glutathione, Biosens. Bioelectron. 215 (2022), 114388.
[22]	Y. Li, P. Li, Y. Chen, et al., Interfacial deposition of Ag nanozyme on metal-polyphenol nanosphere for SERS detection of cellular glutathione, Biosens. Bioelectron. 228 (2023), 115200.
[23]	L. Wang, Y. Chen, Y. Ji, et al., Cheap and portable paper chip with terrific oxidase-like activity and SERS enhancement performance for SERS-colorimetric bimodal detection of intracellular glutathione, Biosens. Bioelectron. 244 (2024), 115817.
[24]	Y. Huang, Y. Gu, X. Liu, et al., Reusable ring-like Fe₃O₄/Au nanozymes with enhanced peroxidase-like activities for colorimetric-SERS dual-mode sensing of biomolecules in human blood, Biosens. Bioelectron. 209 (2022), 114253.
[25]	Y. Wang, K. Jiang, J. Zhu, et al., A FRET-based carbon dot-MnO₂ nanosheet architecture for glutathione sensing in human whole blood samples, Chem. Commun. Camb. Engl. 51 (2015) 12748-12751.
[26]	T. Bai, L. Wang, M. Wang, et al., Strategic synthesis of trimetallic Au@Ag-Pt nanorattles for ultrasensitive colorimetric detection in lateral flow immunoassay, Biosens. Bioelectron. 208 (2022), 114218.
[27]	X. Huang, L. Chen, T. Sha, et al., In situ tyrosinase monitoring by wearable microneedle patch toward clinical melanoma screening, ACS Nano 17 (2023) 20073-20086.
[28]	X. Huang, H. Tian, L. Huang, et al., Well-ordered Au nanoarray for sensitive and reproducible detection of hepatocellular carcinoma-associated miRNA via CHA-assisted SERS/fluorescence dual-mode sensing, Anal. Chem. 95 (2023) 5955-5966.
[29]	T. Kang, J. Zhu, X. Luo, et al., Controlled self-assembly of a close-packed gold octahedra array for SERS sensing exosomal microRNAs, Anal. Chem. 93 (2021) 2519-2526.
[30]	S. Shanmukh, L. Jones, J. Driskell, et al., Rapid and sensitive detection of respiratory virus molecular signatures using a silver nanorod array SERS substrate, Nano Lett. 6 (2006) 2630-2636.
[31]	D. Dong, L.W. Yap, D.M. Smilgies, et al., Two-dimensional gold trisoctahedron nanoparticle superlattice sheets: Self-assembly, characterization and immunosensing applications, Nanoscale 10 (2018) 5065-5071.
[32]	S. Weng, D. Lin, S. Lai, et al., Highly sensitive and reliable detection of microRNA for clinically disease surveillance using SERS biosensor integrated with catalytic hairpin assembly amplification technology, Biosens. Bioelectron. 208 (2022), 114236.
[33]	B. Feng, X. Pan, T. Liu, et al., A broadband photoelectronic detector in a silicon nanopillar array with high detectivity enhanced by a monolayer graphene, Nano Lett. 21 (2021) 5655-5662.
[34]	J. Wang, J. Wu, Y. Zhang, et al., Colorimetric and SERS dual-mode sensing of mercury (II) based on controllable etching of Au@Ag core/shell nanoparticles, Sens. Actuat. B Chem. 330 (2021), 129364.
[35]	J. Wu, X. Zhou, P. Li, et al., Ultrasensitive and simultaneous SERS detection of multiplex microRNA using fractal gold nanotags for early diagnosis and prognosis of hepatocellular carcinoma, Anal. Chem. 93 (2021) 8799-8809.
[36]	L. Li, W.S. Chin, Rapid and sensitive SERS detection of melamine in milk using Ag nanocube array substrate coupled with multivariate analysis, Food Chem. 357 (2021), 129717.
[37]	L. Chen, X. Huang, X. Zeng, et al., Signal-on bimodal sensing glucose based on enzyme product-etching MnO₂ nanosheets for detachment of MoS₂ quantum dots, Chin. Chem. Lett. 32 (2021) 1967-1971.
[38]	X. Ma, S. Wen, X. Xue, et al., Controllable synthesis of SERS-active magnetic metal-organic framework-based nanocatalysts and their application in photoinduced enhanced catalytic oxidation, ACS Appl. Mater. Interfaces 10 (2018) 25726-25736.
[39]	S. Huang, Q. Xiao, Z. He, et al., A high sensitive and specific QDs FRET bioprobe for MNase, Chem. Commun. Camb. Engl. (2008) 5990-5992.
[40]	T. Qiu, D. Zhao, G. Zhou, et al., A positively charged QDs-based FRET probe for micrococcal nuclease detection, Anal. 135 (2010) 2394-2399.
[41]	Y. Peng, J. Jiang, R. Yu, Label-free and sensitive detection of micrococcal nuclease activity using DNA-scaffolded silver nanoclusters as a fluorescence indicator, Anal. Methods 6 (2014) 4090-4094.
[42]	D. Li, J. Qin, G. Yan, A phosphorescent sensor for detection of Micrococcal nuclease base on phosphorescent resonance energy transfer between quantum dots and DNA-ROX, Sens. Actuat. B Chem. 255 (2018) 529-535.
[43]	X. Huang, H. Cai, H. Zhou, et al., Cobalt oxide nanoparticle-synergized protein degradation and phototherapy for enhanced anticancer therapeutics, Acta Biomater. 121 (2021) 605-620.
[44]	X. Huang, L. Chen, Y. Lin, et al., Tumor targeting and penetrating biomimetic mesoporous polydopamine nanoparticles facilitate photothermal killing and autophagy blocking for synergistic tumor ablation, Acta Biomater. 136 (2021) 456-472.