Alkylated EDTA potentiates antibacterial photodynamic activity of protoporphyrin.

Journal

Journal of nanobiotechnology
ISSN: 1477-3155
Titre abrégé: J Nanobiotechnology
Pays: England
ID NLM: 101152208

Informations de publication

Date de publication:
08 Apr 2024
Historique:
received: 08 12 2023
accepted: 20 02 2024
medline: 9 4 2024
pubmed: 9 4 2024
entrez: 8 4 2024
Statut: epublish

Résumé

Antibiotic resistance has garnered significant attention due to the scarcity of new antibiotics in development. Protoporphyrin IX (PpIX)-mediated photodynamic therapy shows promise as a novel antibacterial strategy, serving as an alternative to antibiotics. However, the poor solubility of PpIX and its tendency to aggregate greatly hinder its photodynamic efficacy. In this study, we demonstrate that alkylated EDTA derivatives (aEDTA), particularly C14-EDTA, can enhance the solubility of PpIX by facilitating its dispersion in aqueous solutions. The combination of C14-EDTA and PpIX exhibits potent antibacterial activity against Staphylococcus aureus (S. aureus) when exposed to LED light irradiation. Furthermore, this combination effectively eradicates S. aureus biofilms, which are known to be strongly resistant to antibiotics, and demonstrates high therapeutic efficacy in an animal model of infected ulcers. Mechanistic studies reveal that C14-EDTA can disrupt PpIX crystallization, increase bacterial membrane permeability and sequester divalent cations, thereby improving the accumulation of PpIX in bacteria. This, in turn, enhances reactive oxygen species (ROS) production and the antibacterial photodynamic activity. Overall, this effective strategy holds great promise in combating antibiotic-resistant strains.

Identifiants

DOI: 10.1186/s12951-024-02353-3 PMID: 38589895
pubmed: 38589895
doi: 10.1186/s12951-024-02353-3
pii: 10.1186/s12951-024-02353-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

161

Subventions

Organisme : National Key Research and Development Program of China
ID : 2021YFA1201200
Organisme : National Natural Science Foundation of China
ID : 51833008
Organisme : Key Research and Development Program of Zhejiang Province
ID : 2020C01123
Organisme : Fundamental Research Funds for the Central Universities
ID : 226-2023-00022
Organisme : Basic Public Welfare Research Program of Zhejiang Province
ID : LGC21B040001
Organisme : Natural Sciences and Engineering Research Council of Canada
ID : ALLRP 570723 - 21

Informations de copyright

© 2024. The Author(s).

Références

Murray CJL, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399:629–55.
doi: 10.1016/S0140-6736(21)02724-0
Kim H, Yoo YD, Lee GY. Identification of bacterial membrane selectivity of Romo1-derived antimicrobial peptide AMPR-22 via molecular dynamics. Int J Mol Sci. 2022;23:7404.
doi: 10.3390/ijms23137404 pubmed: 35806412 pmcid: 9266825
Selvakumar V, et al. Antibacterial efficacy of phytosynthesized multi-metal oxide nanoparticles against drug-resistant foodborne pathogens. J Nanomater. 2022;2022:6506796.
doi: 10.1155/2022/6506796
Martinez JL, Baquero F. Emergence and spread of antibiotic resistance: setting a parameter space. Upsala J Med Sci. 2014;119:68–77.
doi: 10.3109/03009734.2014.901444 pubmed: 24678768 pmcid: 4034563
Banerjee I, Mondal D, Martin J, Kane RS. Photoactivated antimicrobial activity of carbon nanotube-porphyrin conjugates. Langmuir. 2010;26:17369–74.
doi: 10.1021/la103298e pubmed: 20931992
Perni S, et al. The antimicrobial properties of light-activated polymers containing methylene blue and gold nanoparticles. Biomaterials. 2009;30:89–93.
doi: 10.1016/j.biomaterials.2008.09.020 pubmed: 18838166
Grinholc M, Szramka B, Olender K, Graczyk A. Bactericidal effect of photodynamic therapy against methicillin-resistant Staphylococcus aureus strain with the use of various porphyrin photosensitizers. Acta Biochim Pol. 2007;54:665–70.
doi: 10.18388/abp.2007_3240 pubmed: 17726547
Rai M, Yadav A, Gade A. Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv. 2009;27:76–83.
doi: 10.1016/j.biotechadv.2008.09.002 pubmed: 18854209
Wang XF, et al. Enhancing selective photosensitizer accumulation and oxygen supply for high-efficacy photodynamic therapy toward glioma by 5-aminolevulinic acid loaded nanoplatform. J Colloid Interface Sci. 2020;565:483–93.
doi: 10.1016/j.jcis.2020.01.020 pubmed: 31982715
Homayoni H, et al. Enhancement of protoporphyrin IX performance in aqueous solutions for photodynamic therapy. Photodiagn Photodyn Ther. 2015;12:258–66.
doi: 10.1016/j.pdpdt.2015.01.003
Grinholc M, Szramka B, Olender K, Graczyk A. Bactericidal effect of photodynamic therapy against methicillin-resistant Staphylococcus aureus strain with the use of various porphyrin photosensitizers. Acta Biochim Pol. 2007;54:665–70.
doi: 10.18388/abp.2007_3240 pubmed: 17726547
Liu Y, et al. Eradication of multidrug-resistant Staphylococcal infections by light-activatable micellar nanocarriers in a murine model. Adv Funct Mater. 2017;27:1701974.
doi: 10.1002/adfm.201701974
Ning LG, et al. Hydrothermal derived protoporphyrin IX nanoparticles for inactivation and imaging of bacteria strains. J Colloid Interface Sci. 2019;549:72–9.
doi: 10.1016/j.jcis.2019.04.050 pubmed: 31022525
Bumah VV, et al. The importance of porphyrins in blue light suppression of Streptococcus agalactiae. J Photochem Photobiol B. 2020;212:111996.
doi: 10.1016/j.jphotobiol.2020.111996 pubmed: 32863128
Caminos DA, Durantini EN. Photodynamic inactivation of Escherichia coli immobilized on agar surfaces by a tricationic porphyrin. Bioorg Med Chem. 2006;14:4253–9.
doi: 10.1016/j.bmc.2006.01.058 pubmed: 16481175
Choi S, Lee H, Chae H. Comparison of in vitro photodynamic antimicrobial activity of protoporphyrin IX between endoscopic white light and newly developed narrowband endoscopic light against Helicobacter pylori 26695. J Photochem Photobiol B. 2012;117:55–60.
doi: 10.1016/j.jphotobiol.2012.08.015 pubmed: 23079538
Basoglu H, Bilgin MD, Demir MM. Protoporphyrin IX-loaded magnetoliposomes as a potential drug delivery system for photodynamic therapy: fabrication, characterization and in vitro study. Photodiagn Photodyn Ther. 2016;13:81–90.
doi: 10.1016/j.pdpdt.2015.12.010
Finnegan S, Percival SL. EDTA: An antimicrobial and antibiofilm agent for use in wound care. Adv Wound Care. 2015;4:415–21.
doi: 10.1089/wound.2014.0577
Leive L. Release of lipopolysaccharide by EDTA treatment of E, coli. Biochem Biophys Res Commun. 1965;21:290–6.
doi: 10.1016/0006-291X(65)90191-9 pubmed: 4159978
Yoshizumi A, et al. Efficacies of calcium-EDTA in combination with imipenem in a murine model of sepsis caused by Escherichia coli with NDM-1 beta-lactamase. J Infect Chemother. 2013;19:992–5.
doi: 10.1007/s10156-012-0528-y pubmed: 23233082
Li X, et al. Synergistic in vitro effects of indocyanine green and ethylenediamine tetraacetate-mediated antimicrobial photodynamic therapy combined with antibiotics for resistant bacterial biofilms in diabetic foot infection. Photodiagn Photodyn Ther. 2019;25:300–8.
doi: 10.1016/j.pdpdt.2019.01.010
Jalil A, et al. Self-emulsifying drug delivery systems comprising chlorhexidine and alkyl-EDTA: A novel approach for augmented antimicrobial activity. J Mol Liq. 2019;295: 111649.
doi: 10.1016/j.molliq.2019.111649
Gonzalez-Lopez S, Camejo-Aguilar D, Sanchez-Sanchez P, Bolanos-Carmona V. Effect of CHX on the decalcifying effect of 10% citric acid, 20% citric acid, or 17% EDTA. J Endod. 2006;32:781–4.
doi: 10.1016/j.joen.2006.02.006 pubmed: 16861082
Jaeger DA, Peacock MF, Bohle DS. A surfactant transition metal chelate. Langmuir. 2003;19:4859–62.
doi: 10.1021/la026894d
Jo S, Kim T, Iyer VG, Im W. CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem. 2008;29:1859–65.
doi: 10.1002/jcc.20945 pubmed: 18351591
Huang J, MacKerell AD Jr. CHARMM36 all-atom additive protein force field: validation based on comparison to NMR data. J Comput Chem. 2013;34:2135–45.
doi: 10.1002/jcc.23354 pubmed: 23832629 pmcid: 3800559
Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH. The MARTINI force field: coarse grained model for biomolecular simulations. J Phys Chem B. 2007;111:7812–24.
doi: 10.1021/jp071097f pubmed: 17569554
de Jong DH, et al. Atomistic and coarse grain topologies for the cofactors associated with the photosystem II core complex. J Phys Chem B. 2015;119:7791–803.
doi: 10.1021/acs.jpcb.5b00809 pubmed: 26053327
Morales-de-Echegaray AV, et al. Rapid uptake and photodynamic inactivation of Staphylococci by Ga(III)-protoporphyrin IX. Acs Infect Dis. 2018;4:1564–73.
doi: 10.1021/acsinfecdis.8b00125 pubmed: 30175917 pmcid: 6724182
Gois MM, et al. Susceptibility of Staphylococcus aureus to porphyrin-mediated photodynamic antimicrobial chemotherapy: an in vitro study. J Lasers Med Sci. 2010;25:391–5.
doi: 10.1007/s10103-009-0705-0
Passerini L, Lam K, Costerton JW, King EG. Biofilms on indwelling vascular catheters. Crit Care Med. 1992;20:665–73.
doi: 10.1097/00003246-199205000-00020 pubmed: 1572192
Luppens SBI, Reij MW, van der Heijden RWL, Rombouts FM, Abee T. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Appl Environ Microbiol. 2002;68:4194–200.
doi: 10.1128/AEM.68.9.4194-4200.2002 pubmed: 12200265 pmcid: 124130

Auteurs

Ying Piao (Y)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China.

Sebastian Himbert (S)

Department of Physics and Astronomy, McMaster University, Hamilton, ON, L8S 3Z5, Canada. himberts@mcmaster.ca.

Zifan Li (Z)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China.

Jun Liu (J)

Suncor AgroScience, Mississauga, ON, L5K 1A8, Canada.

Zhihao Zhao (Z)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China.

Huahai Yu (H)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China.

Shuangshuang Liu (S)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China.

Shiqun Shao (S)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China. shiqun.shao@zju.edu.cn.

Michael Fefer (M)

Suncor AgroScience, Mississauga, ON, L5K 1A8, Canada.

Maikel C Rheinstädter (MC)

Department of Physics and Astronomy, McMaster University, Hamilton, ON, L8S 3Z5, Canada. rheinstadter@mcmaster.ca.

Youqing Shen (Y)

Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou, 310058, China. shenyq@zju.edu.cn.

Classifications MeSH