Germ-elimination systems -
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values are shown for triplicate samples; data were representative of at least three independent experiments. To confirm a key property of PIAS, namely, the targeting of different microbes irrespective of species, we tested whether PIAS has a virucidal effect.
We targeted the viral pathogen SC and tested the antiviral effect of PIAS using various anti-spike antibodies because viral spikes form oligomers on the viral envelope for glycosylation and intermolecular interactions providing a variety of antigenicities. In addition, panitumumab anti-EGFR —IR conjugate Pan—IR served as a non-targeting conjugate.
PIAS using the SC-targeting conjugate SC—IR 1 potently inactivated the pathogen, resulting in cell survival similar to that of non-infected cells Fig.
PIAS using SC—IR 2 or 3 also inactivated SC Fig. Notably, PIAS showed an antiviral effect against SC, whereas the antibody conjugates had no neutralising activity against the pathogen in the test cases Fig.
No apparent effects were observed in cell samples treated with PIAS using the non-specific conjugate Pan—IR Fig. The virucidal effect was also evaluated by quantifying the viral RNA Fig.
In addition, SC-infected cells were subjected to immunostaining analysis 17 , indicating that almost all cells were infected with SC in i the untreated group and ii the group treated with PIAS using the non-specific conjugate Pan—IR, but not iii those in the group treated with PIAS using the SC-targeting conjugate SC—IR Fig.
Data normalised to the virus group are shown. SC-specific conjugates, SC—IR 1, 2, 3, and 4; non-specific conjugates, Pan—IR Conjugates, 0.
c Immunostaining analysis of virus-infected cells in which an antibody against the SC-nucleocapsid protein was used i—iii. SC treated with SC—IR 1 without NIR i ; SC subjected to PIAS using SC—IR 1 ii ; SC subjected to PIAS using Pan—IR iii.
SC and the nucleus are indicated in red and blue, respectively. d Virucidal effect of PIAS using T7—IR conjugates against T7 phage was evaluated according to the cell viability of Escherichia coli cells using the colony counting method. Control, non-infected and untreated; c.
not detected. Moreover, the bacterial virus bacteriophage T7 18 was inactivated by PIAS using a T7-targeting conjugate Fig. Finally, to confirm whether PIAS can specifically act on a target pathogen without affecting the normal host microflora in vivo, we used a rat model of MRSA-nasal colonisation Consistent with the in vitro results, PIAS eradicated the pathogen Fig.
Further analysis using a mouse model of MRSA intraperitoneal infection 20 showed that PIAS eliminated the pathogen Fig. No significant differences were observed in the normal intestinal microflora with PIAS treatment Fig. a — c Effect of PIAS on a methicillin-resistant Staphylococcus aureus MRSA , b non-target commensal bacteria, and c nasal tissues of cotton rats colonised by MRSA.
The illustrated image of PIAS against SA nasal colonisation is shown in a. NIR laser light was delivered from outside of the nares of cotton rats using laser fibres. b Arrowheads indicate MRSA colonies with haemolytic plaques.
c Histological analysis of untreated and PIAS-treated nasal tissues. A mouse undergoing PIAS treatment is shown. Box elements: centre lines, medians; box limits, upper and lower quartiles; whiskers, minimum and maximum values.
f , g Effect of PIAS on a mouse MRSA-thigh infection. f Homogenised thigh samples day 1; top images and colony counts.
g On day 7, visual analysis left , histochemical analysis middle , and bacterial culture right were performed on the thigh samples. Arrows and the illustrated image top left indicate abscesses.
HE-staining haematoxylin-eosin staining, c. Median and IQR values are shown. Additionally, PIAS was found to eliminate MRSA in the deep tissues of mice with MRSA-thigh infections 22 Fig.
However, in untreated mice, hyperaemia was observed in homogenised thigh samples on day 1 top images, Fig. This study demonstrated that PIAS can be used as an antimicrobial tool based on both its target precision and flexibility against a broad range of microbial pathogens regardless of their species or drug-resistance status.
PIAS enables the use of multiple conjugates against different epitopes, which can cover epitope variations and multiple target pathogens. Notably, the observed antimicrobial effects of PIAS were achieved even when using a commercial mAb that exhibited no neutralising activity.
PIAS showed the target elimination of different microbes, including bacterial, fungal, and viral pathogens; other microbes, such as protozoan parasites without available drugs 23 , may also be targeted using PIAS. For PIAS to be effective in vivo, conjugates and NIR must reach the site of infection; however, the treatment can be limited to complex tissues and biofilms.
Conjugates should be administered into the target infection by intravenous or local injection. External NIR illumination can reach the target infection in complex tissues of patients with head-neck cancer, which was confirmed by our original photoimmunotherapy in clinical trials [ClinicalTrials.
Endoscopy with a NIR laser can also be used for internal illumination, including in the lumen of the gastrointestinal tract and in deeper tissues.
Since PIAS requires antibodies against target pathogens, the preparation of a library of conjugates against some of the main pathogens can be useful for future situations. PIAS may be applied to future emerging infections if antibodies are available; however, the usefulness of conventional antimicrobial drugs is evident, at least in the current situation 1.
With regards to the aspect of clinical application, PIAS can be applied to patients who have already been treated with antimicrobials in clinics or with conventional approaches in hospitals and in whom treatment has failed, rather than as the first-line treatment.
Considering that no panacea exists for antimicrobial strategies, choices must be made depending on the specific situation. In conclusion, we demonstrated that PIAS showed targeted elimination of different microbial pathogens, irrespective of their species or drug-resistance status.
Various strains of Staphylococcus aureus SA , including methicillin-sensitive SA MSSA, JKmsSA1 and JCM , methicillin-resistant SA MRSA, JKmrSA1, N and USA , mupirocin-resistant MRSA JKmmrSA1 resistant to mupirocin Furthermore, T7 NBRC and T4 NBRC phages were used.
Trypticase soy broth TSB , brain—heart infusion broth, L broth, mannitol salt agar with egg yolk, TSB agar supplemented with rabbit blood cells, and OPAII Staphylococcus agar were obtained from BD Biosciences Franklin Lakes, NJ, USA.
TSB containing 0. CROMagar was obtained from Kanto Chemical Co. Tokyo, Japan. In addition to cells in the exponential phase, microbial cells in the stationary phase are used; the stationary phase induces the development of persister cells that are recalcitrant to antibiotics To obtain microbial cells in the exponential phase, the cells were harvested at an OD of 0.
All experiments with a clinical isolate of SC were performed within a biological safety cabinet with prior approval from the biosafety committee of Yokohama City University. The anti-SA monoclonal antibody mAb against the SA peptidoglycan epitope clone Staph Anti-CA mAb clone MC3, murine IgG3 , which recognises the putative β-1,2-mannan epitope in the cell wall mannoproteins and phospholipomannans of CA, was purchased from ISCA Diagnostics Exeter, UK.
The anti-SC spike mAb was obtained from GeneTex GTX; Irvine, CA, USA. Anti-T7 phage mAb T7·Tag antibody, murine IgG2b directed against the 11 amino acid gene 10 leader peptide MetAlaSerMetThrGlyGlyGlnGlnMetGly of T7 phage was purchased from Merck KGaA Darmstadt, Germany.
Anti-human epidermal growth factor receptor 2 HER2 mAb trastuzumab Herceptin, humanised IgG1 was purchased from Chugai Pharmaceutical Tokyo, Japan.
IRDyeDX IR was purchased from LI-COR Biosciences Lincoln NE, USA. RPMI medium without phenol red was purchased from Thermo Fisher Scientific Waltham, MA, USA. IRconjugating mAb was synthesised as previously described Briefly, the mAb 1. The mixture was purified on a Sephadex G50 column PD; GE Healthcare, Little Chalfont, UK.
Conjugates containing approximately three IR molecules per mAb molecule were used. The fluorescence of IR was measured with a flow cytometry analyser MACSQant analyser; Miltenyi Biotec, Bergisch Gladbach, Germany and fluorescence microscopy IX73; Olympus, Tokyo, Japan with the following filter settings: —nm excitation filter and —nm emission filter.
To confirm the target specificity of mAb—IR conjugate, unconjugated mAb was added before mAb—IR treatments. Scanning electron microscopy SEM analyses were performed to detect mAb binding to the bacterial cells.
The mixture was dropped onto a nano-percolator to remove unbound antibodies and then washed with PBS. The samples were analysed using SEM SU; Hitachi, Tokyo, Japan.
PIAS-treated cells were subjected to SEM analysis. mAb—IR conjugates 0. Serially diluted samples were plated on agar plates for overnight culture to determine microbial viability. Two days after infection, the supernatant was collected and RNA was extracted using a QIAamp viral RNA Mini Kit Qiagen, Hilden, Germany.
Cell viability was measured in the form of ATP present in the culture supernatants after virus lysis. In addition, the antiviral effect of PIAS on SCs was evaluated by immunostaining.
The nuclei were stained with ProLong Gold Antifade Mountant with DAPI Thermo Fisher Scientific. Images were captured and measured using an imager BZ; Keyence, Tokyo, Japan. T7 and T4 phages 10 9 plaque-forming units p.
One sample was treated with NIR illumination, whereas the other was left untreated. Both samples were co-cultured with E. After co-culture, the samples were cultured on agar plates, and bacterial colonies were enumerated.
Notably, when phages 10 6 p. In contrast, no colonies were observed when phages 10 9 p. As an antiviral effect was clearly observed, we adopted this method in our study. Animal studies were performed in accordance with the guidelines established by the Animal Care Committee of the Jikei University School of Medicine.
All in vivo experiments were performed under isoflurane anaesthesia. The cotton rat nasal colonisation model 19 was used to determine the feasibility of the PIAS in vivo. Six- to ten-week-old cotton rats Sigmodon hispidus were obtained from the Animal Research Center of the University of Occupational and Environmental Health School of Medicine Fukuoka, Japan.
MRSA JKmrSA1 cells were instilled in both cotton rat nares. Anterior nares were harvested by dissecting the nose. Harvested nasal samples were collected in 1. Serially diluted samples were plated on agar plates for overnight culture to determine bacterial viability.
The absence of SA contamination was confirmed in all animals before use by nasal and rectal swab cultures.
A mouse model of intraperitoneal infection 20 was used. MRSA JKmrSA1 cells and treated with PIAS or antibiotics [vancomycin VCM , rifampicin RFP ]. SA—IR and VCM or RFP were administered intraperitoneally or orally, respectively.
Survival and adverse events were monitored via a once-daily assessment for 7 days. Faeces of PIAS and antibiotic VCM and RFP -treated mice and those of the non-treated mice were used for 16S-targeting metagenome analysis.
A mouse model of thigh infection 22 was used. One day after treatment, the mice were sacrificed with cervical dislocation, and the right thighs were dissected. Thigh samples were collected in PBS containing Tween 20 and homogenised manually.
The homogenised samples were cultured on OPAII Staphylococcus agar to evaluate the bactericidal effect of PIAS on the pathogen cells in the thigh. Thigh samples obtained 7 days after treatment were used to assess the pathology.
Macroscopic findings were confirmed histologically, as appropriate, with haematoxylin-eosin staining. Two paired-end reads were merged using the fastq-join programme based on overlapping sequences.
Filter-passed reads were further analysed after trimming off both the primer sequences. Taxonomic assignment of each operational taxonomic unit was performed by searching for similarities against the RDP and NCBI genome databases using the GLSEARCH programme.
values were calculated from a minimum of three samples. Calculations and statistical analyses were performed using GraphPad Prism software ver.
The Kaplan—Meier survival curve was assessed using the log-rank Mantel-Cox test. In metagenome analysis, ANOVA was performed for multiple group comparisons, and any significant differences were evaluated using the two-stage step-up method of Benjamini, Krieger, and Yekutieli Further information on research design is available in the Nature Research Reporting Summary linked to this article.
Data of this study are available from the corresponding authors upon reasonable request. The raw 16S metagenomic data have been deposited to DDBJ Sequence Read Archive accession number DRA in the DDBJ BioProject database.
Laxminarayan, R. et al. Access to effective antimicrobials: a worldwide challenge. Lancet , — Article PubMed Google Scholar. Levy, S. Antibacterial resistance worldwide: causes, challenges and responses. Article CAS PubMed Google Scholar.
Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in a systematic analysis. Kluytmans, J. Nasal carriage of Staphylococcus aureus : epidemiology, underlying mechanisms, and associated risks. Article CAS PubMed PubMed Central Google Scholar. Iwase, T. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization.
Nature , — Chambers, H. Waves of resistance: Staphylococcus aureus in the antibiotic era. coli, giardia, and Cryptosporidium, which are known to cause severe illnesses.
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