A Heterocatalytic Metal-Organic Framework to Stimulate Dispersal and Macrophage Combat with Infectious Biofilms

Renfei Wu; Tianrong Yu; Sidi Liu; Rui Shi; Guimei Jiang; Yijin Ren; Henny C. Van Der Mei; Henk J. Busscher; Jian Liu

doi:10.1021/acsnano.2c09008

A Heterocatalytic Metal-Organic Framework to Stimulate Dispersal and Macrophage Combat with Infectious Biofilms

Renfei Wu, Tianrong Yu, Sidi Liu, Rui Shi, Guimei Jiang, Yijin Ren, Henny C. Van Der Mei^*, Henk J. Busscher^*, Jian Liu^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Eradication of infectious biofilms is becoming increasingly difficult due to the growing number of antibiotic-resistant strains. This necessitates development of nonantibiotic-based, antimicrobial approaches. To this end, we designed a heterocatalytic metal-organic framework composed of zirconium 1,4-dicarboxybenzene (UiO-66) with immobilized Pt nanoparticles (Pt-NP/UiO-66). Pt-NP/UiO-66 enhanced singlet-oxygen generation compared with Pt nanoparticles or UiO-66, particularly in an acidic environment. Singlet-oxygen generation degraded phosphodiester bonds present in eDNA gluing biofilms together and therewith dispersed biofilms. Remaining biofilms possessed a more open structure. Concurrently, Pt-NP/UiO-66 stimulated macrophages to adapt a more M1-like, "fighting"phenotype, moving faster toward their target bacteria and showing increased bacterial killing. As a combined effect of biofilm dispersal and macrophage polarization, a subcutaneous Staphylococcus aureus biofilm in mice was more readily eradicated by Pt-NP/UiO-66 than by Pt nanoparticles or UiO-66. Therewith, heterocatalytic Pt-NP/UiO-66 metal-organic frameworks constitute a nonantibiotic-based strategy to weaken protective matrices and disperse infectious biofilms, while strengthening macrophages in bacterial killing.

Original language	English
Pages (from-to)	2328-2340
Number of pages	13
Journal	Acs Nano
Volume	17
Issue number	3
Early online date	24-Jan-2023
DOIs	https://doi.org/10.1021/acsnano.2c09008
Publication status	Published - 2023

Keywords

antibacterial
extracellular DNA
immunomodulation
Metal organic framework
wound healing

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A Heterocatalytic Metal–Organic Framework to Stimulate Dispersal and Macrophage Combat with Infectious BiofilmsFinal publisher's version, 9.75 MBLicence: CC BY

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@article{dde959a6d661401f944bd8fecad72550,

title = "A Heterocatalytic Metal-Organic Framework to Stimulate Dispersal and Macrophage Combat with Infectious Biofilms",

abstract = "Eradication of infectious biofilms is becoming increasingly difficult due to the growing number of antibiotic-resistant strains. This necessitates development of nonantibiotic-based, antimicrobial approaches. To this end, we designed a heterocatalytic metal-organic framework composed of zirconium 1,4-dicarboxybenzene (UiO-66) with immobilized Pt nanoparticles (Pt-NP/UiO-66). Pt-NP/UiO-66 enhanced singlet-oxygen generation compared with Pt nanoparticles or UiO-66, particularly in an acidic environment. Singlet-oxygen generation degraded phosphodiester bonds present in eDNA gluing biofilms together and therewith dispersed biofilms. Remaining biofilms possessed a more open structure. Concurrently, Pt-NP/UiO-66 stimulated macrophages to adapt a more M1-like, {"}fighting{"}phenotype, moving faster toward their target bacteria and showing increased bacterial killing. As a combined effect of biofilm dispersal and macrophage polarization, a subcutaneous Staphylococcus aureus biofilm in mice was more readily eradicated by Pt-NP/UiO-66 than by Pt nanoparticles or UiO-66. Therewith, heterocatalytic Pt-NP/UiO-66 metal-organic frameworks constitute a nonantibiotic-based strategy to weaken protective matrices and disperse infectious biofilms, while strengthening macrophages in bacterial killing.",

keywords = "antibacterial, extracellular DNA, immunomodulation, Metal organic framework, wound healing",

author = "Renfei Wu and Tianrong Yu and Sidi Liu and Rui Shi and Guimei Jiang and Yijin Ren and {Van Der Mei}, {Henny C.} and Busscher, {Henk J.} and Jian Liu",

note = "Funding Information: This work was financially supported by National Key Research and Development Program of China (2017YFE0131700), the National Natural Science Foundation of China (21874096), the 111 Project, Joint International Research Laboratory of Carbon-Based Materials and Devices, the Collaborative Innovation Center of Suzhou Nano Science and Technology, Suzhou Key Laboratory of Nanotechnology and Biomedicine, and UMCG, Groningen, The Netherlands. Publisher Copyright: {\textcopyright} 2023 The Authors. Published by American Chemical Society.",

year = "2023",

doi = "10.1021/acsnano.2c09008",

language = "English",

volume = "17",

pages = "2328--2340",

journal = "Acs Nano",

issn = "1936-0851",

publisher = "AMER CHEMICAL SOC",

number = "3",

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TY - JOUR

T1 - A Heterocatalytic Metal-Organic Framework to Stimulate Dispersal and Macrophage Combat with Infectious Biofilms

AU - Wu, Renfei

AU - Yu, Tianrong

AU - Liu, Sidi

AU - Shi, Rui

AU - Jiang, Guimei

AU - Ren, Yijin

AU - Van Der Mei, Henny C.

AU - Busscher, Henk J.

AU - Liu, Jian

N1 - Funding Information: This work was financially supported by National Key Research and Development Program of China (2017YFE0131700), the National Natural Science Foundation of China (21874096), the 111 Project, Joint International Research Laboratory of Carbon-Based Materials and Devices, the Collaborative Innovation Center of Suzhou Nano Science and Technology, Suzhou Key Laboratory of Nanotechnology and Biomedicine, and UMCG, Groningen, The Netherlands. Publisher Copyright: © 2023 The Authors. Published by American Chemical Society.

PY - 2023

Y1 - 2023

N2 - Eradication of infectious biofilms is becoming increasingly difficult due to the growing number of antibiotic-resistant strains. This necessitates development of nonantibiotic-based, antimicrobial approaches. To this end, we designed a heterocatalytic metal-organic framework composed of zirconium 1,4-dicarboxybenzene (UiO-66) with immobilized Pt nanoparticles (Pt-NP/UiO-66). Pt-NP/UiO-66 enhanced singlet-oxygen generation compared with Pt nanoparticles or UiO-66, particularly in an acidic environment. Singlet-oxygen generation degraded phosphodiester bonds present in eDNA gluing biofilms together and therewith dispersed biofilms. Remaining biofilms possessed a more open structure. Concurrently, Pt-NP/UiO-66 stimulated macrophages to adapt a more M1-like, "fighting"phenotype, moving faster toward their target bacteria and showing increased bacterial killing. As a combined effect of biofilm dispersal and macrophage polarization, a subcutaneous Staphylococcus aureus biofilm in mice was more readily eradicated by Pt-NP/UiO-66 than by Pt nanoparticles or UiO-66. Therewith, heterocatalytic Pt-NP/UiO-66 metal-organic frameworks constitute a nonantibiotic-based strategy to weaken protective matrices and disperse infectious biofilms, while strengthening macrophages in bacterial killing.

AB - Eradication of infectious biofilms is becoming increasingly difficult due to the growing number of antibiotic-resistant strains. This necessitates development of nonantibiotic-based, antimicrobial approaches. To this end, we designed a heterocatalytic metal-organic framework composed of zirconium 1,4-dicarboxybenzene (UiO-66) with immobilized Pt nanoparticles (Pt-NP/UiO-66). Pt-NP/UiO-66 enhanced singlet-oxygen generation compared with Pt nanoparticles or UiO-66, particularly in an acidic environment. Singlet-oxygen generation degraded phosphodiester bonds present in eDNA gluing biofilms together and therewith dispersed biofilms. Remaining biofilms possessed a more open structure. Concurrently, Pt-NP/UiO-66 stimulated macrophages to adapt a more M1-like, "fighting"phenotype, moving faster toward their target bacteria and showing increased bacterial killing. As a combined effect of biofilm dispersal and macrophage polarization, a subcutaneous Staphylococcus aureus biofilm in mice was more readily eradicated by Pt-NP/UiO-66 than by Pt nanoparticles or UiO-66. Therewith, heterocatalytic Pt-NP/UiO-66 metal-organic frameworks constitute a nonantibiotic-based strategy to weaken protective matrices and disperse infectious biofilms, while strengthening macrophages in bacterial killing.

KW - antibacterial

KW - extracellular DNA

KW - immunomodulation

KW - Metal organic framework

KW - wound healing

U2 - 10.1021/acsnano.2c09008

DO - 10.1021/acsnano.2c09008

M3 - Article

AN - SCOPUS:85146902777

SN - 1936-0851

VL - 17

SP - 2328

EP - 2340

JO - Acs Nano

JF - Acs Nano

IS - 3

ER -

A Heterocatalytic Metal-Organic Framework to Stimulate Dispersal and Macrophage Combat with Infectious Biofilms

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