AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Nano Research Article
Article Link
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Observing antimicrobial process with traceable gold nanoclusters

Kaiyuan Zheng1, Magdiel I. Setyawati2, David Tai Leong1( ), Jianping Xie1( )
Department of Chemical and Biomolecular Engineering, National University of Singapore, 4 Engineering Drive 4, Singapore 117585, Singapore
School of Materials Science and Engineering, Nanyang Technological University, 50 Nanyang Avenue, Singapore 639798, Singapore
Show Author Information

Graphical Abstract

Abstract

Understanding the interaction of nanomaterials with biological systems has always been of high concern and interest. An emerging type of nanomaterials, ultrasmall metal nanoclusters (NCs, < 2 nm in size), are promising in this aspect due to their well-defined molecular formulae and structures, as well as unique physical and chemical properties that are distinctly different from their larger counterparts (metal nanoparticles). For example, metal NCs possess intrinsic strong luminescence, which can be used for real-time tracking of their interactions with biological systems. Herein, luminescent gold (Au) NCs were used as traceable antimicrobial agents to study their interactions with the bacteria and to further understand their underlining antimicrobial mechanism. It is shown for the first time that the Au NCs would first attach on the bacterial membrane, penetrate, and subsequently accumulate inside the bacteria. Thereafter, the internalized Au NCs would induce reactive oxygen species (ROS) generation and damage the bacterial membrane, resulting in the leakage of bacterial contents, which can finally kill the bacteria. Traceable Au NCs (or other metal NCs) provide a promising platform to study the antimicrobial mechanisms as well as other fundamentals on the interfacing of functional nanomaterials with the biological systems, further increasing their acceptance in various biomedical applications.

Keywords

metal nanoclustersgold nanoclustersantimicrobial agentsluminescent probesbioimaging

Electronic Supplementary Material

Download File(s)
12274_2020_3146_MOESM1_ESM.pdf (2.7 MB)

References

[1]
A. E. Nel,; L. Mädler,; D. Velegol,; T. Xia,; E. M. V. Hoek,; P. Somasundaran,; F. Klaessig,; V. Castranova,; M. Thompson, Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 2009, 8, 543-557.
Google Scholar
[2]
A. M. Alkilany,; S. E. Lohse,; C. J. Murphy, The gold standard: Gold nanoparticle libraries to understand the nano-bio interface. Acc. Chem. Res. 2012, 46, 650-661.
Google Scholar
[3]
C. Y. Tay,; M. I. Setyawati,; J. P. Xie,; W. J. Parak,; D. T. Leong, Back to basics: Exploiting the innate physico-chemical characteristics of nanomaterials for biomedical applications. Adv. Funct. Mater. 2014, 24, 5936-5955.
Google Scholar
[4]
M. I. Setyawati,; C. Y. Tay,; D. Docter,; R. H. Stauber,; D. T. Leong, Understanding and exploiting nanoparticles' intimacy with the blood vessel and blood. Chem. Soc. Rev. 2015, 44, 8174-8199.
Google Scholar
[5]
F. Peng,; M. I. Setyawati,; J. K. Tee,; X. G. Ding,; J. P. Wang,; M. E. Nga,; H. K. Ho,; D. T. Leong, Nanoparticles promote in vivo breast cancer cell intravasation and extravasation by inducing endothelial leakiness. Nat. Nanotechnol. 2019, 14, 279-286.
Google Scholar
[6]
M. I. Setyawati,; C. Y. Tay,; B. H. Bay,; D. T. Leong, Gold nanoparticles induced endothelial leakiness depends on particle size and endothelial cell origin. ACS Nano 2017, 11, 5020-5030.
Google Scholar
[7]
J. Y. Zhu,; C. Sevencan,; M. K. Zhang,; R. S. A. McCoy,; X. G. Ding,; J. J Ye,; J. P. Xie,; K. Ariga,; J. Feng,; B. H. Bay, et al. Increasing the potential interacting area of nanomedicine enhances its homotypic cancer targeting efficacy. ACS Nano 2020, 14, 3259-3271.
Google Scholar
[8]
X. G. Ding,; F. Peng,; J. Zhou,; W. B. Gong,; G. Slaven,; K. P. Loh,; C. T. Lim,; D. T. Leong, Defect engineered bioactive transition metals dichalcogenides quantum dots. Nat. Commun. 2019, 10, 41.
Google Scholar
[9]
R. C. Jin,; C. J. Zeng,; M. Zhou,; Y. X. Chen, Atomically precise colloidal metal nanoclusters and nanoparticles: Fundamentals and opportunities. Chem. Rev. 2016, 116, 10346-10413.
Google Scholar
[10]
P. D. Jadzinsky,; G. Calero,; C. J. Ackerson,; D. A. Bushnell,; R. D. Kornberg, Structure of a thiol monolayer-protected gold nanoparticle at 1.1 Å resolution. Science 2007, 318, 430-433.
Google Scholar
[11]
A. Desireddy,; B. E. Conn,; J. S. Guo,; B. Yoon,; R. N. Barnett,; B. M. Monahan,; K. Kirschbaum,; W. P. Griffith,; R. L. Whetten,; U. Landman, et al. Ultrastable silver nanoparticles. Nature 2013, 501, 399-402.
Google Scholar
[12]
I. Chakraborty,; T. Pradeep, Atomically precise clusters of noble metals: Emerging link between atoms and nanoparticles. Chem. Rev. 2017, 117, 8208-8271.
Google Scholar
[13]
X. Kang,; M. Z. Zhu, Tailoring the photoluminescence of atomically precise nanoclusters. Chem. Soc. Rev. 2019, 48, 2422-2457.
Google Scholar
[14]
S. Choi,; R. M. Dickson,; J. H. Yu, Developing luminescent silver nanodots for biological applications. Chem. Soc. Rev. 2012, 41, 1867-1891.
Google Scholar
[15]
Y. Tao,; M. Q. Li,; J. S. Ren,; X. G. Qu, Metal nanoclusters: Novel probes for diagnostic and therapeutic applications. Chem. Soc. Rev. 2015, 44, 8636-8663.
Google Scholar
[16]
Z. T. Luo,; K. Y. Zheng,; J. P. Xie, Engineering ultrasmall water- soluble gold and silver nanoclusters for biomedical applications. Chem. Commun. 2014, 50, 5143-5155.
Google Scholar
[17]
K. Y. Zheng,; J. P. Xie, Engineering ultrasmall metal nanoclusters as promising theranostic agents. Trends Chem. 2020, 2, 665-679.
Google Scholar
[18]
K. Y. Zheng,; M. I. Setyawati,; D. T. Leong,; J. P. Xie, Antimicrobial gold nanoclusters. ACS Nano 2017, 11, 6904-6910.
Google Scholar
[19]
K. Y. Zheng,; J. P. Xie, Composition-dependent antimicrobial ability of full-spectrum AuxAg25-x alloy nanoclusters. ACS Nano 2020, 14, 11533-11541.
Google Scholar
[20]
Z. E. Huma,; I. Javed,; Z. Z. Zhang,; H. Bilal,; Y. X. Sun,; S. Z. Hussain,; T. P. Davis,; D. E. Otzen,; C. B. Landersdorfer,; F. Ding, et al. Nanosilver mitigates biofilm formation via FapC amyloidosis inhibition. Small 2020, 16, 1906674.
Google Scholar
[21]
Q. L. Feng,; J. Wu,; G. Q. Chen,; F. Z. Cui,; T. N. Kim,; J. O. Kim, A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 2000, 52, 662-668.
Google Scholar
[22]
S. E. Crawford,; M. J. Hartmann,; J. E. Millstone, Surface chemistry-mediated near-infrared emission of small coinage metal nanoparticles. Acc. Chem. Res. 2019, 52, 695-703.
Google Scholar
[23]
G. L. Wang,; T. Huang,; R. W. Murray,; L. Menard,; R. G. Nuzzo, Near-IR luminescence of monolayer-protected metal clusters. J. Am. Chem. Soc. 2005, 127, 812-813.
Google Scholar
[24]
Z. H. Tang,; D. A. Robinson,; N. Bokossa,; B. Xu,; S. M. Wang,; G. L. Wang, Mixed dithiolate durene-DT and monothiolate phenylethanethiolate protected Au130 nanoparticles with discrete core and core-ligand energy states. J. Am. Chem. Soc. 2011, 133, 16037-16044.
Google Scholar
[25]
H. L. Liu,; G. S. Hong,; Z. T. Luo,; J. C. Chen,; J. L. Chang,; M. Gong,; H. He,; J. Yang,; X. Yuan,; L. L. Li, et al. Atomic-precision gold clusters for NIR-II imaging. Adv. Mater. 2019, 31, 1901015.
Google Scholar
[26]
A. Retnakumari,; S. Setua,; D. Menon,; P. Ravindran,; H. Muhammed,; T. Pradeep,; S. Nair,; M. Koyakutty, Molecular-receptor-specific, non-toxic, near-infrared-emitting Au cluster-protein nanoconjugates for targeted cancer imaging. Nanotechnology 2010, 21, 055103.
Google Scholar
[27]
L. Shang,; N. Azadfar,; F. Stockmar,; W. Send,; V. Trouillet,; M. Bruns,; D. Gerthsen,; G. U. Nienhaus, One-pot synthesis of near-infrared fluorescent gold clusters for cellular fluorescence lifetime imaging. Small 2011, 7, 2614-2620.
Google Scholar
[28]
X. Wu,; X. X. He,; K. M. Wang,; C. Xie,; B. Zhou,; Z. H. Qing, Ultrasmall near-infrared gold nanoclusters for tumor fluorescence imaging in vivo. Nanoscale 2010, 2, 2244-2249.
Google Scholar
[29]
Y. Chen,; D. M. Montana,; H. Wei,; J. M. Cordero,; M. Schneider,; X. Le Guével,; O. Chen,; O. T. Bruns,; M. G. Bawendi, Shortwave infrared in vivo imaging with gold nanoclusters. Nano Lett. 2017, 17, 6330-6334.
Google Scholar
[30]
J. B. Liu,; M. X. Yu,; X. H. Ning,; C. Zhou,; S. Y. Yang,; J. Zheng, PEGylation and zwitterionization: Pros and cons in the renal clearance and tumor targeting of near-IR-emitting gold nanoparticles. Angew. Chem., Int. Ed. 2013, 52, 12572-12576.
Google Scholar
[31]
J. B. Liu,; M. X. Yu,; C. Zhou,; S. Y. Yang,; X. H. Ning,; J. Zheng, Passive tumor targeting of renal-clearable luminescent gold nanoparticles: Long tumor retention and fast normal tissue clearance. J. Am. Chem. Soc. 2013, 135, 4978-4981.
Google Scholar
[32]
S. Mustalahti,; P. Myllyperkio,; S. Malola,; T. Lahtinen,; K. Salorinne,; J. Koivisto,; H. Häkkinen,; M. Pettersson, Molecule-like photodynamics of Au102(pMBA)44 nanocluster. ACS Nano 2015, 9, 2328-2335.
Google Scholar
[33]
Y. Pan,; A. Leifert,; D. Ruau,; S. Neuss,; J. Bornemann,; G. Schmid,; W. Brandau,; U. Simon,; W. Jahnen-Dechent, Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 2009, 5, 2067-2076.
Google Scholar
[34]
M. Tsoli,; H. Kuhn,; W. Brandau,; H. Esche,; G. Schmid, Cellular uptake and toxicity of Au55 clusters. Small 2005, 1, 841-844.
Google Scholar
[35]
Z. T. Luo,; X. Yuan,; Y. Yu,; Q. B. Zhang,; D. T. Leong,; J. Y. Lee,; J. P. Xie, From aggregation-induced emission of Au(I)-thiolate complexes to ultrabright Au(0)@Au(I)-thiolate core-shell nanoclusters. J. Am. Chem. Soc. 2012, 134, 16662-16670.
Google Scholar
[36]
O. A. Wong,; C. L. Heinecke,; A. R. Simone,; R. L. Whetten,; C. J. Ackerson, Ligand symmetry-equivalence on thiolate protected gold nanoclusters determined by NMR spectroscopy. Nanoscale 2012, 4, 4099-4102.
Google Scholar
[37]
Y. Levi-Kalisman,; P. D. Jadzinsky,; N. Kalisman,; H. Tsunoyama,; T. Tsukuda,; D. A. Bushnell,; R. D. Kornberg, Synthesis and characterization of Au102(p-MBA)44 nanoparticles. J. Am. Chem. Soc. 2011, 133, 2976-2982.
Google Scholar
[38]
K. Y. Zheng,; M. I. Setyawati,; D. T. Leong,; J. P. Xie, Surface ligand chemistry of gold nanoclusters determines their antimicrobial ability. Chem. Mater. 2018, 30, 2800-2808.
Google Scholar
[39]
Z. K. Wu,; R. C. Jin, On the ligand’s role in the fluorescence of gold nanoclusters. Nano Lett. 2010, 10, 2568-2573.
Google Scholar
[40]
M. S. Devadas,; J. Kim,; E. Sinn,; D. Lee,; T. Goodson III,; G. Ramakrishna, Unique ultrafast visible luminescence in monolayer- protected Au25 clusters. J. Phys. Chem. C 2010, 114, 22417-22423.
Google Scholar
[41]
N. Goswami,; Q. F. Yao,; Z. T. Luo,; J. G. Li,; T. K. Chen,; J. P. Xie, Luminescent metal nanoclusters with aggregation-induced emission. J. Phys. Chem. Lett. 2016, 7, 962-975.
Google Scholar
[42]
Y. Yu,; Z. T. Luo,; D. M. Chevrier,; D. T. Leong,; P. Zhang,; D. E. Jiang,; J. P. Xie, Identification of a highly luminescent Au22(SG)18 nanocluster. J. Am. Chem. Soc. 2014, 136, 1246-1249.
Google Scholar
[43]
X. F. Jia,; J. Li,; E. K. Wang, Cu nanoclusters with aggregation induced emission enhancement. Small 2013, 9, 3873-3879.
Google Scholar
[44]
X. Kang,; S. Wang,; Y. Song,; S. Jin,; G. Sun,; H. Yu,; M. Zhu, Bimetallic Au2Cu6 nanoclusters: Strong luminescence induced by the aggregation of copper(I) complexes with gold(0) species. Angew. Chem., Int. Ed. 2016, 128, 3675-3678.
Google Scholar
[45]
L. X. Yang,; L. Shang,; G. U. Nienhaus, Mechanistic aspects of fluorescent gold nanocluster internalization by live HeLa cells. Nanoscale 2013, 5, 1537-1543.
Google Scholar
[46]
B. D. Chithrani,; W. C. W. Chan, Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett. 2007, 7, 1542-1550.
Google Scholar
[47]
T. T. Yue,; X. R. Zhang, Cooperative effect in receptor-mediated endocytosis of multiple nanoparticles. ACS Nano 2012, 6, 3196-3205.
Google Scholar
[48]
X. Jiang,; C. Röcker,; M. Hafner,; S. Brandholt,; R. M. Dörlich,; G. U. Nienhaus, Endo-and exocytosis of zwitterionic quantum dot nanoparticles by live HeLa cells. ACS Nano 2010, 4, 6787-6797.
Google Scholar
[49]
B. L. Roth,; M. Poot,; S. T. Yue,; P. J. Millard, Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl. Environ. Microbiol. 1997, 63, 2421-2431.
Google Scholar
[50]
P. Lebaron,; P. Catala,; N. Parthuisot, Effectiveness of SYTOX green stain for bacterial viability assessment. Appl. Environ. Microbiol. 1998, 64, 2697-2700.
Google Scholar
[51]
M. Valko,; D. Leibfritz,; J. Moncol,; M. T. D. Cronin,; M. Mazur,; J. Telser, Free radicals and antioxidants in normal physiological functions and human disease. ‎Int. J. Biochem. Cell Biol. 2007, 39, 44-84.
Google Scholar
[52]
K. Apel,; H. Hirt, Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55, 373-399.
Google Scholar
[53]
C. P. Whitman, The 4-oxalocrotonate tautomerase family of enzymes: How nature makes new enzymes using a β-α-β structural motif. Arch. Biochem. Biophys. 2002, 402, 1-13.
Google Scholar
[54]
S. Fuchs,; J. Pané-Farré,; C. Kohler,; M. Hecker,; S. Engelmann, Anaerobic gene expression in Staphylococcus aureus. J. Bacteriol. 2007, 189, 4275-4289.
Google Scholar
[55]
J. M. McCord,; I. Fridovich, Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 1969, 244, 6049-6055.
Google Scholar
[56]
J. A. Fee, Regulation of sod genes in Escherichia coli: Relevance to superoxide dismutase function. Mol. Microbiol. 1991, 5, 2599-2610.
Google Scholar
[57]
K. Y. Zheng,; M. I. Setyawati,; T. P. Lim,; D. T. Leong,; J. P. Xie, Antimicrobial cluster bombs: Silver nanoclusters packed with daptomycin. ACS Nano 2016, 10, 7934-7942.
Google Scholar
Nano Research
Volume 14 Issue 4,
April 2021
Pages 1026-1033
DOI: 10.1007/s12274-020-3146-5
Cite this article:
Zheng K, Setyawati MI, Leong DT, et al. Observing antimicrobial process with traceable gold nanoclusters. Nano Research, 2021, 14(4): 1026-1033. https://doi.org/10.1007/s12274-020-3146-5
Topics:
Biological systemsGoldGold nanoclusters LuminescenceMedical applicationsMetal nanoparticlesNanoclustersNanostructured materials

913

Views

45

Crossref

N/A

Web of Science

46

Scopus

2

CSCD

Altmetrics
Received: 28 August 2020
Revised: 23 September 2020
Accepted: 24 September 2020
Published: 15 November 2020
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature
Return