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Research Article

Antibacterial mechanism and transcriptomic analysis of a near-infrared triggered upconversion nanoparticles@AgBiS2 for synergetic bacteria-infected therapy

Shi Chen1,§, Zhaoyou Chu2,§, Limian Cao1,§, Lingling Xu2( ), Qianqian Jin2, Nian Liu1, Benjin Chen2, Ming Fang1, Wanni Wang2, Haisheng Qian2( ), Min Shao1( )
Department of Critical Care Medicine, The First Affiliated Hospital of Anhui Medical University, Hefei 230032, China
School of Biomedical Engineering, Research and Engineering Center of Biomedical Materials, Anhui Provincial Institute of Translational Medicine, Anhui Medical University, Hefei 230032, China

§ Shi Chen, Zhaoyou Chu, and Limian Cao contributed equally to this work.

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Graphical Abstract

Upconversion nanoparticles@AgBiS2 were successfully prepared, which showed enhanced photothermal conversion performance and good reactive oxygen species production ability for combined photothermal–photodynamic therapy of methicillin-resistant Staphylococcus aureus (MRSA) infection.

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) has become a rising clinical problem as its occurrence has increased due to the overuse and misuse of antibiotics. In this work, upconversion nanoparticles@AgBiS2 core–shell were produced with enhanced photothermal transformation efficiency and ability to produce reactive oxygen species for synergistic photodynamic photothermal and photodynamic antibacterial performance. The nanoparticles exhibit good antibacterial effects in vitro and satisfactory therapeutic performance on healing MRSA-infected wounds in vivo experiments. RNA-sequencing technique has been used to investigate and reveal that photothermal–photodynamic therapy using the nanoparticles can interfere with metabolic processes such as galactose metabolism in MRSA bacteria, destroy the transport system on the surface of MRSA, and affect quorum sensing to hinder the formation of biofilms to achieve effective antibacterial efficacy. It was demonstrated that this work presents an alternative near-infrared photoactive multimodal nanostructure for antibacterial applications.

Keywords

photothermal therapyphotodynamic therapyanti-methicillin-resistant Staphylococcus aureus (MRSA)RNA-sequencingtranscriptomic analysis

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References

1

Grundmann, H.; Aires-de-Sousa, M.; Boyce, J.; Tiemersma, E. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 2006, 368, 874–885.
Crossref Google Scholar
2

Wang, W. S.; Li, B. L.; Yang, H. L.; Lin, Z. F.; Chen, L. L.; Li, Z.; Ge, J. Y.; Zhang, T.; Xia, H.; Li, L. H. et al. Efficient elimination of multidrug-resistant bacteria using copper sulfide nanozymes anchored to graphene oxide nanosheets. Nano Res. 2020, 13, 2156–2164.
Crossref Google Scholar
3

Turner, N. A.; Sharma-Kuinkel, B. K.; Maskarinec, S. A.; Eichenberger, E. M.; Shah, P. P.; Carugati, M.; Holland, T. L.; Fowler, V. G. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat. Rev. Microbiol. 2019, 17, 203–218.
Crossref Google Scholar
4

Timsit, J. F.; Bassetti, M.; Cremer, O.; Daikos, G.; de Waele, J.; Kallil, A.; Kipnis, E.; Kollef, M.; Laupland, K.; Paiva, J. A. et al. Rationalizing antimicrobial therapy in the ICU: A narrative review. Intensive Care Med. 2019, 45, 172–189.
Crossref Google Scholar
5

Kim, H. J.; Choi, Q.; Kwon, G. C.; Koo, S. H. Molecular epidemiology and virulence factors of methicillin-resistant Staphylococcus aureus isolated from patients with bacteremia. J. Clin. Lab. Anal. 2020, 34, e23077.
Crossref Google Scholar
6

Sit, P. S.; Teh, C. S. J.; Idris, N.; Ponnampalavanar, S. Methicillin-resistant Staphylococcus aureus (MRSA) bacteremia: Correlations between clinical, phenotypic, genotypic characteristics and mortality in a tertiary teaching hospital in Malaysia. Infect. Genet. Evol. 2018, 59, 132–141.
Crossref Google Scholar
7

Styers, D.; Sheehan, D. J.; Hogan, P.; Sahm, D. F. Laboratory-based surveillance of current antimicrobial resistance patterns and trends among Staphylococcus aureus: 2005 status in the United States. Ann. Clin. Microbiol. Antimicrob. 2006, 5, 2.
Crossref Google Scholar
8

Chen, C. J.; Huang, Y. C. New epidemiology of Staphylococcus aureus infection in Asia. Clin. Microbiol. Infect. 2014, 20, 605–623.
Crossref Google Scholar
9

Munthe, C.; Nijsingh, N. Cutting red tape to manage public health threats: An ethical dilemma of expediting antibiotic drug innovation. Bioethics 2019, 33, 785–791.
Crossref Google Scholar
10

Brown, E. D.; Wright, G. D. Antibacterial drug discovery in the resistance era. Nature 2016, 529, 336–343.
Crossref Google Scholar
11

Ding, Y. M.; Wang, Z., Zhang, Z. Y.; Zhao, Y. C.; Yang, S. Y.; Zhang, Y. L.; Yao, S. C.; Wang, S. B.; Huang, T.; Zhang, Y. et al. Oxygen vacancy-engineered BaTiO3 nanoparticles for synergistic cancer photothermal, photodynamic, and catalytic therapy. Nano Res. 2022, 15, 7304–7312.
Crossref Google Scholar
12

Zhao, Y.; Chen, L.; Wang, Y. N.; Song, X. Y.; Li, K. Y., Yan, X. F.; Yu, L. M.; He, Z. Y. Nanomaterial-based strategies in antimicrobial applications: Progress and perspectives. Nano Res. 2021, 14, 4417–4441.
Crossref Google Scholar
13

Xu, W. J.; Wang, J. X.; Jin, L. J.; Zhu, Y. Q.; Yang, X. Z. A tumor acidity-driven transformable polymeric nanoassembly with deep tumor penetration and membrane-anchoring capability for targeted photodynamic therapy. Biomaterials 2021, 276, 121024.
Crossref Google Scholar
14

Fang, F. C. Antimicrobial reactive oxygen and nitrogen species: Concepts and controversies. Nat. Rev. Microbiol. 2004, 2, 820–832.
Crossref Google Scholar
15

Ezraty, B.; Gennaris, A.; Barras, F.; Collet, J. F. Oxidative stress, protein damage and repair in bacteria. Nat. Rev. Microbiol. 2017, 15, 385–396.
Crossref Google Scholar
16

Zhao, Y.; Guo, Q. Q.; Dai, X. M.; Wei, X. S.; Yu, Y. J.; Chen, X. L.; Li, C. X.; Cao, Z. Q.; Zhang, X. G. A biomimetic non-antibiotic approach to eradicate drug-resistant infections. Adv. Mater. 2019, 31, 1806024.
Crossref Google Scholar
17

Huang, Y.; Gao, Q.; Li, X.; Gao, Y. F.; Han, H. J.; Jin, Q.; Yao, K.; Ji, J. Ofloxacin loaded MoS2 nanoflakes for synergistic mild-temperature photothermal/antibiotic therapy with reduced drug resistance of bacteria. Nano Res. 2020, 13, 2340–2350.
Crossref Google Scholar
18

Chen, Q.; Hu, Q. Y.; Dukhovlinova, E.; Chen, G. J.; Ahn, S.; Wang, C.; Ogunnaike, E. A.; Ligler, F. S.; Dotti, G.; Gu, Z. Photothermal therapy promotes tumor infiltration and antitumor activity of CAR T cells. Adv. Mater. 2019, 31, 1900192.
Crossref Google Scholar
19

Zhu, Y. L.; Wang, Z.; Zhao, R. X.; Zhou, Y. H.; Feng, L. L.; Cai, S. L.; Yang, P. P. Pt decorated Ti3C2Tx MXene with NIR-II light amplified nanozyme catalytic activity for efficient phototheranostics. ACS Nano 2022, 16, 3105–3118.
Crossref Google Scholar
20

Wang, W. N.; Zhang, C. Y.; Zhang, M. F.; Pei, P.; Zhou, W.; Zha, Z. B.; Shao, M.; Qian, H. S. Precisely photothermal controlled releasing of antibacterial agent from Bi2S3 hollow microspheres triggered by NIR light for water sterilization. Chem. Eng. J. 2020, 381, 122630.
Crossref Google Scholar
21

Wang, W. N.; Pei, P.; Chu, Z. Y.; Chen, B. J.; Qian, H. S.; Zha, Z. B.; Zhou, W.; Liu, T.; Shao, M.; Wang, H. Bi2S3 coated Au nanorods for enhanced photodynamic and photothermal antibacterial activities under NIR light. Chem. Eng. J. 2020, 397, 125488.
Crossref Google Scholar
22

Huo, J. J.; Jia, Q. Y.; Huang, H.; Zhang, J.; Li, P.; Dong, X. C.; Huang, W. Emerging photothermal-derived multimodal synergistic therapy in combating bacterial infections. Chem. Soc. Rev. 2021, 50, 8762–8789.
Crossref Google Scholar
23

Wang, Y. H.; Song, S. Y.; Zhang, S. T.; Zhang, H. J. Stimuli-responsive nanotheranostics based on lanthanide-doped upconversion nanoparticles for cancer imaging and therapy: Current advances and future challenges. Nano Today 2019, 25, 38–67.
Crossref Google Scholar
24

Zhu, X. H.; Zhang, J.; Liu, J. L.; Zhang, Y. Recent progress of rare-earth doped upconversion nanoparticles: Synthesis, optimization, and applications. Adv. Sci. 2019, 6, 1901358.
Crossref Google Scholar
25

Fan, Y.; Liu, L.; Zhang, F. Exploiting lanthanide-doped upconversion nanoparticles with core/shell structures. Nano Today 2019, 25, 68–84.
Crossref Google Scholar
26

Tian, Q. Y.; Yao, W. J.; Wu, W.; Jiang, C. Z. NIR light-activated upconversion semiconductor photocatalysts. Nanoscale Horiz. 2019, 4, 10–25.
Crossref Google Scholar
27

Jafari, M.; Rezvanpour, A. Upconversion nano-particles from synthesis to cancer treatment: A review. Adv. Powder Technol. 2019, 30, 1731–1753.
Crossref Google Scholar
28

Wang, D. M.; Liu, B.; Quan, Z. W.; Li, C. X.; Hou, Z. Y.; Xing, B. G.; Lin, J. New advances on the marrying of UCNPs and photothermal agents for imaging-guided diagnosis and the therapy of tumors. J. Mater. Chem. B 2017, 5, 2209–2230.
Crossref Google Scholar
29

Hou, Z. Y.; Zhang, Y. X.; Deng, K. R.; Chen, Y. Y.; Li, X. J.; Deng, X. R.; Cheng, Z. Y.; Lian, H. Z.; Li, C. C.; Lin, J. UV-emitting upconversion-based TiO2 photosensitizing nanoplatform: Near-infrared light mediated in vivo photodynamic therapy via mitochondria-involved apoptosis pathway. ACS Nano 2015, 9, 2599.
Crossref Google Scholar
30

Hou, Z. Y.; Deng, K. R.; Li, C. X.; Deng, X. R.; Lian, H. Z.; Cheng, Z. Y.; Jin, D. Y.; Lin, J. 808 nm light-triggered and hyaluronic acid-targeted dual-photosensitizers nanoplatform by fully utilizing Nd3+-sensitized upconversion emission with enhanced anti-tumor efficacy. Biomaterials 2016, 101, 32–46.
Crossref Google Scholar
31

Fu, L. H.; Wan, Y. L.; Qi, C.; He, J.; Li, C. Y.; Yang, C.; Xu, H.; Lin, J.; Huang, P. Nanocatalytic theranostics with glutathione depletion and enhanced reactive oxygen species generation for efficient cancer therapy. Adv. Mater. 2021, 33, 2006892.
Crossref Google Scholar
32

Liu, Y. J.; Bhattarai, P.; Dai, Z. F.; Chen, X. Y. Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. Chem. Soc. Rev. 2019, 48, 2053–2108.
Crossref Google Scholar
33

Chen, T.; Su, L. C.; Lin, L. S.; Ge, X. G.; Bai, F. C.; Niu, M.; Wang, C. L.; Song, J. B.; Guo, S. L.; Yang, H. H. Mesoporous radiosensitized nanoprobe for enhanced NIR-II photoacoustic imaging-guided accurate radio-chemotherapy. Nano Res. 2022, 15, 4154–4163.
Crossref Google Scholar
34

He, T.; Jiang, C.; He, J.; Zhang, Y. F.; He, G.; Wu, J. Y. Z.; Lin, J.; Zhou, X.; Huang, P. Manganese-dioxide-coating-instructed plasmonic modulation of gold nanorods for activatable duplex-imaging-guided NIR-II photothermal–chemodynamic therapy. Adv. Mater. 2021, 33, 2008540.
Crossref Google Scholar
35

Cui, J. B.; Jiang, R.; Guo, C.; Bai, X. L.; Xu, S. Y.; Wang, L. Y. Fluorine grafted Cu7S4-Au heterodimers for multimodal imaging guided photothermal therapy with high penetration depth. J. Am. Chem. Soc. 2018, 140, 5890–5894.
Crossref Google Scholar
36

Zhao, S.; Tian, R. R.; Shao, B. Q.; Feng, Y.; Yuan, S. W.; Dong, L. P.; Zhang, L.; Liu, K.; Wang, Z. X.; You, H. P. Designing of UCNPs@Bi@SiO2 hybrid theranostic nanoplatforms for simultaneous multimodal imaging and photothermal therapy. ACS Appl. Mater. Interfaces 2019, 11, 394–402.
Crossref Google Scholar
37

Zhang, C. Y.; Li, D. D.; Pei, P.; Wang, W. N.; Chen, B. J.; Chu, Z. Y.; Zha, Z.; Yang, X. Z.; Wang, J. B.; Qian, H. S. Rod-based urchin-like hollow microspheres of Bi2S3: Facile synthesis, photo-controlled drug release for photoacoustic imaging and chemo–photothermal therapy of tumor ablation. Biomaterials 2020, 237, 119835.
Crossref Google Scholar
38
ZhaoS.TianR. R.ShaoB. Q.FengY.YuanS. W.DongL. P.ZhangL.WangZ. X.YouH. P. UCNP-Bi2Se3 upconverting nanohybrid for upconversion luminescence and CT imaging and photothermal therapyChem. —Eur. J.2020261127113510.1002/chem.201904586

Zhao, S.; Tian, R. R.; Shao, B. Q.; Feng, Y.; Yuan, S. W.; Dong, L. P.; Zhang, L.; Wang, Z. X.; You, H. P. UCNP-Bi2Se3 upconverting nanohybrid for upconversion luminescence and CT imaging and photothermal therapy. Chem. —Eur. J. 2020, 26, 1127–1135.
Crossref Google Scholar
39

Lei, P. P.; An, R.; Zheng, X. H.; Zhang, P.; Du, K. M.; Zhang, M. L.; Dong, L. L.; Gao, X.; Feng, J.; Zhang, H. J. Ultrafast synthesis of ultrasmall polyethylenimine-protected AgBiS2 nanodots by “rookie method” for in vivo dual-modal CT/PA imaging and simultaneous photothermal therapy. Nanoscale 2018, 10, 16765–16774.
Crossref Google Scholar
40

Sun, M. D.; Yang, D.; Wang, C.; Bi, H. T.; Zhou, Y.; Wang, X. X.; Xu, J. T.; He, F.; Gai, S. L.; Yang, P. P. AgBiS2-TPP nanocomposite for mitochondrial targeting photodynamic therapy, photothermal therapy and bio-imaging under 808 nm NIR laser irradiation. Biomater. Sci. 2019, 7, 4769–4781.
Crossref Google Scholar
41

Ouyang, R. Z.; Cao, P. H.; Jia, P. P.; Wang, H.; Zong, T. Y.; Dai, C. Y.; Yuan, J.; Li, Y. H.; Sun, D.; Guo, N. et al. Bistratal Au@Bi2S3 nanobones for excellent NIR-triggered/multimodal imaging-guided synergistic therapy for liver cancer. Bioact. Mater. 2021, 6, 386–403.
Crossref Google Scholar
42

Chen, B. J.; Zhang, C. Y.; Wang, W. N.; Chu, Z. Y.; Zha, Z.; He, X. Y.; Zhou, W.; Liu, T.; Wang, H.; Qian, H. S. Ultrastable AgBiS2 hollow nanospheres with cancer cell-specific cytotoxicity for multimodal tumor therapy. ACS Nano 2020, 14, 14919–14928.
Crossref Google Scholar
43

Stark, R.; Grzelak, M.; Hadfield, J. RNA sequencing: The teenage years. Nat. Rev. Genet. 2019, 20, 631–656.
Crossref Google Scholar
44

Chu, Z. Y.; Tian, T.; Tao, Z. C., ; Yang, J.; Chen, B. J.; Chen, H.; Wang, W. N.; Yin, P. Q.; Xia, X. P.; Wang, H. et al. Upconversion nanoparticles@AgBiS2 core–shell nanoparticles with cancer-cell-specific cytotoxicity for combined photothermal and photodynamic therapy of cancers. Bioact. Mater. 2022, 17, 71–80.
Crossref Google Scholar
45

Wang, Z. J.; Zhou, J. W.; Zhang, Y. H.; Zhu, W. Y.; Li, Y. Accessing highly efficient photothermal conversion with stable open-shell aromatic nitric acid radicals. Angew. Chem., Int. Ed. 2022, 61, e202113653.
Crossref Google Scholar
46
Li, W.; Fan, Y. Z.; Lin, J.; Yu, P.; Wang, Z. G.; Ning, C. Y. Near-infrared light-activatable bismuth-based nanomaterials for antibacterial and antitumor treatment. Adv. Ther., in press, https://doi.org/10.1002/adtp.202200027.
47

Irwansyah, I.; Li, Y. Q.; Shi, W. X.; Qi, D. P.; Leow, W. R.; Tang, M. B. Y.; Li, S. Z.; Chen, X. D. Gram-positive antimicrobial activity of amino acid-based hydrogels. Adv. Mater. 2015, 27, 648–654.
Crossref Google Scholar
48

Crowe, M.; O’Sullivan, M.; Cassetti, O.; O’Sullivan, A. Estimation and consumption pattern of free sugar intake in 3-year-old Irish preschool children. Eur. J. Nutr. 2020, 59, 2065–2074.
Crossref Google Scholar
49

Holden, H. M.; Rayment, I.; Thoden, J. B. Structure and function of enzymes of the leloir pathway for galactose metabolism. J. Biol. Chem. 2003, 278, 43885–43888.
Crossref Google Scholar
50

Althammer, M.; Regl, C.; Herburger, K.; Blöchl, C.; Voglas, E.; Huber, C. G.; Tenhaken, R. Overexpression of UDP-sugar pyrophosphorylase leads to higher sensitivity towards galactose, providing new insights into the mechanisms of galactose toxicity in plants. Plant J. 2022, 109, 1416–1426.
Crossref Google Scholar
51

Boulanger, E. F.; Sabag-Daigle, A.; Thirugnanasambantham, P.; Gopalan, V.; Ahmer, B. M. M. Sugar-phosphate toxicities. Microbiol. Mol. Biol. Rev. 2021, 85, e0012321.
Crossref Google Scholar
52

Ficicioglu, C.; Hussa, C.; Gallagher, P. R.; Thomas, N.; Yager, C. Monitoring of biochemical status in children with duarte galactosemia: Utility of galactose, galactitol, galactonate, and galactose 1-phosphate. Clin. Chem. 2010, 56, 1177–1182.
Crossref Google Scholar
53

Holden, H. M.; Thoden, J. B.; Timson, D. J.; Reece, R. J. Galactokinase: Structure, function, and role in type II galactosemia. Cell. Mol. Life Sci. 2004, 61, 2471–2484.
Crossref Google Scholar
54

Fath, M. J.; Kolter, R. ABC transporters: Bacterial exporters. Microbiol. Rev. 1993, 57, 995–1017.
Crossref Google Scholar
55

Locher, K. P.; Lee, A. T.; Rees, D. C. The E. coli BtuCD structure:A framework for ABC transporter architecture and mechanism. Science 2002, 296, 1091–1098.
Crossref Google Scholar
56

Huda, N.; Lee, E. W.; Chen, J.; Morita, Y.; Kuroda, T.; Mizushima, T.; Tsuchiya, T. Molecular cloning and characterization of an ABC multidrug efflux pump, VcaM, in Non-O1 Vibrio cholerae. Antimicrob. Agents Chemother. 2003, 47, 2413–2417.
Crossref Google Scholar
57

Orelle, C.; Mathieu, K.; Jault, J. M. Multidrug ABC transporters in bacteria. Res. Microbiol. 2019, 170, 381–391.
Crossref Google Scholar
58

Barbosa, T. M.; Levy, S. B. The impact of antibiotic use on resistance development and persistence. Drug Resist. Updat. 2000, 3, 303–311.
Crossref Google Scholar
59

Høiby, N.; Bjarnsholt, T.; Givskov, M.; Molin, S.; Ciofu, O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 2010, 35, 322–332.
Crossref Google Scholar
60

Waters, C. M.; Bassler, B. L. Quorum sensing: Cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 2005, 21, 319–346.
Crossref Google Scholar
Nano Research
Volume 15 Issue 10,
October 2022
Pages 9298-9308
DOI: 10.1007/s12274-022-4815-3
Cite this article:
Chen S, Chu Z, Cao L, et al. Antibacterial mechanism and transcriptomic analysis of a near-infrared triggered upconversion nanoparticles@AgBiS2 for synergetic bacteria-infected therapy. Nano Research, 2022, 15(10): 9298-9308. https://doi.org/10.1007/s12274-022-4815-3
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Received: 15 June 2022
Revised: 22 July 2022
Accepted: 25 July 2022
Published: 26 August 2022
© Tsinghua University Press 2022
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