Polymyxin B inhibits pro-inflammatory effects of E. coli outer membrane vesicles whilst increasing immune cell uptake and clearance.
Journal
The Journal of antibiotics
ISSN: 1881-1469
Titre abrégé: J Antibiot (Tokyo)
Pays: England
ID NLM: 0151115
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
06
12
2022
accepted:
20
03
2023
revised:
13
03
2023
medline:
30
5
2023
pubmed:
5
4
2023
entrez:
4
4
2023
Statut:
ppublish
Résumé
Polymyxin B (PMB) is a peptide based antibiotic that binds the lipid A moiety of lipopolysaccharide (LPS) with a resultant bactericidal effect. The interaction of PMB with LPS presented on outer membrane vesicles (OMVs) is not fully known, however, a sacrificial role of OMVs in protecting bacterial cells by sequestering PMB has been described. Here we assess the ability of PMB to neutralize the immune-stimulatory properties of OMVs whilst modulating the uptake of OMVs in human immune cells. We show for the first time that PMB increases immune cell uptake of Escherichia coli derived OMVs whilst inhibiting TNF and IL-1β production. Therefore, we present a potential new role for PMB in the neutralization of OMVs via LPS masking and increased immune cell uptake.
Identifiants
pubmed: 37016014
doi: 10.1038/s41429-023-00615-0
pii: 10.1038/s41429-023-00615-0
doi:
Substances chimiques
Polymyxin B
J2VZ07J96K
Lipopolysaccharides
0
Anti-Bacterial Agents
0
Peptides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
360-364Informations de copyright
© 2023. The Author(s), under exclusive licence to the Japan Antibiotics Research Association.
Références
Mohapatra SS, Dwibedy SK, Padhy I. Polymyxins, the last-resort antibiotics: mode of action, resistance emergence, and potential solutions. J Biosci. 2021;46:85.
doi: 10.1007/s12038-021-00209-8
pubmed: 34475315
pmcid: 8387214
Liu X, Chen Y, Yang H, Li J, Yu J, Yu Z, et al. Acute toxicity is a dose-limiting factor for intravenous polymyxin B: a safety and pharmacokinetic study in healthy Chinese subjects. J Infect. 2021;82:207–15.
doi: 10.1016/j.jinf.2021.01.006
pubmed: 33453286
Zavascki AP, Goldani LZ, Li J, Nation RL. Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J Antimicrob Chemother. 2007;60:1206–15.
doi: 10.1093/jac/dkm357
pubmed: 17878146
Wang PP, Bao P, Sun GX. The relationship between biofilm and outer membrane vesicles: a novel therapy overview. FEMS Microbiol Lett. 2015;362:1–6.
doi: 10.1093/femsle/fnu003
pubmed: 25790486
Svennerholm K, Park KS, Wikström J, Lässer C, Crescitelli R, Shelke GV, et al. Escherichia coli outer membrane vesicles can contribute to sepsis induced cardiac dysfunction. Sci Rep. 2017;7:1–11.
doi: 10.1038/s41598-017-16363-9
Marchant P, Carreno A, Vivanco E, Silva A, Nevermann J, Otero C, et al. “One for All”: functional transfer of OMV-mediated polymyxin B resistance from salmonella enterica sv. Typhi ΔtolR and ΔdegS to susceptible bacteria. Front Microbiol. 2021;12:672467.
doi: 10.3389/fmicb.2021.672467
pubmed: 34025627
pmcid: 8131662
Kim SW, Park SB, Im SP, Lee JS, Jung JW, Gong TW, et al. Outer membrane vesicles from β-lactam-resistant Escherichia coli enable the survival of β-lactam-susceptible E. coli in the presence of β-lactam antibiotics. Sci Rep. 2018;8:5402.
doi: 10.1038/s41598-018-23656-0
pubmed: 29599474
pmcid: 5876404
Jan AT. Outer membrane vesicles (OMVs) of gram-negative bacteria: a perspective update. Front Microbiol. 2017;8:1053.
doi: 10.3389/fmicb.2017.01053
pubmed: 28649237
pmcid: 5465292
Park J, Kim M, Shin B, Kang M, Yang J, Lee TK, et al. A novel decoy strategy for polymyxin resistance in Acinetobacter baumannii. Elife. 2021;10:e66988.
doi: 10.7554/eLife.66988
pubmed: 34180396
pmcid: 8324293
Manning AJ, Kuehn MJ. Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol. 2011;11:258.
doi: 10.1186/1471-2180-11-258
pubmed: 22133164
pmcid: 3248377
Maluta RP, Logue CM, Casas MRT, Meng T, Guastalli EAL, Rojas TCG, et al. Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS ONE. 2014;9:e105016.
doi: 10.1371/journal.pone.0105016
pubmed: 25115913
pmcid: 4130637
Mehat JW, van Vliet AHM, La Ragione RM. The Avian Pathogenic Escherichia coli (APEC) pathotype is comprised of multiple distinct, independent genotypes. Avian Pathol. 2021;50:402–16.
doi: 10.1080/03079457.2021.1915960
pubmed: 34047644
Ronco T, Stegger M, Olsen RH, Sekse C, Nordstoga AB, Pohjanvirta T, et al. Spread of avian pathogenic Escherichia coli ST117 O78: H4 in Nordic broiler production. BMC Genomics. 2017;18:1–8.
doi: 10.1186/s12864-016-3415-6
Ronco T, Stegger M, Andersen PS, Pedersen K, Li L, Thøfner IC, et al. Draft genome sequences of two avian pathogenic Escherichia coli strains of clinical importance, E44 and E51. Genome Announc. 2016;4:0–1.
doi: 10.1128/genomeA.00768-16
O’Donoghue EJ, Sirisaengtaksin N, Browning DF, Bielska E, Hadis M, Fernandez-Trillo F, et al. Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog. 2017;13:e1006760.
doi: 10.1371/journal.ppat.1006760
pubmed: 29186191
pmcid: 5724897
McInerney MP, Roberts KD, Thompson PE, Li J, Nation RL, Velkov T, et al. Quantitation of polymyxin–lipopolysaccharide interactions using an image-based fluorescent probe. J Pharm Sci. 2016;105:1006–10.
doi: 10.1016/j.xphs.2015.10.028
pubmed: 26869441
pmcid: 5149457
Manioglu S, Modaresi SM, Ritzmann N, Thoma J, Overall SA, Harms A, et al. Antibiotic polymyxin arranges lipopolysaccharide into crystalline structures to solidify the bacterial membrane. Nat Commun. 2022;13:6195.
doi: 10.1038/s41467-022-33838-0
pubmed: 36271003
pmcid: 9587031
Goode A, Yeh V, Bonev BB. Interactions of polymyxin B with lipopolysaccharide-containing membranes. Faraday Discuss. 2021;232:317–29.
doi: 10.1039/D1FD00036E
pubmed: 34550139
pmcid: 8704168
Kagi T, Naganuma R, Inoue A, Noguchi T, Hamano S, Sekiguchi Y, et al. The polypeptide antibiotic polymyxin B acts as a pro-inflammatory irritant by preferentially targeting macrophages. J Antibiot. 2022;75:29–39.
doi: 10.1038/s41429-021-00490-7
Fathalla AM, Chow SH, Naderer T, Zhou QT, Velkov T, Azad M, et al. Polymyxin-induced cell death of human macrophage-like THP-1 and neutrophil-like HL-60 cells associated with the activation of apoptotic pathways. Antimicrob Agents Chemother. 2020;64:e00013–20.
doi: 10.1128/AAC.00013-20
pubmed: 32660985
pmcid: 7449205
Shah B, Sullivan CJ, Lonergan NE, Stanley S, Soult MC, Britt LD. Circulating bacterial membrane vesicles cause sepsis in rats. Shock. 2012;37:621–8.
doi: 10.1097/SHK.0b013e318250de5d
pubmed: 22395242
Avedissian SN, Liu J, Rhodes NJ, Lee A, Pais GM, Hauser AR, et al. A review of the clinical pharmacokinetics of polymyxin b. Antibiotics. 2019;8:1–11.
doi: 10.3390/antibiotics8010031
Li X, Liu C, Mao Z, Qi S, Song R, Zhou F. Effectiveness of polymyxin B-immobilized hemoperfusion against sepsis and septic shock: a systematic review and meta-analysis. J Crit Care. 2021;63:187–95.
doi: 10.1016/j.jcrc.2020.09.007
pubmed: 33012579