Polysaccharide-Targeting Lipid Nanoparticles to Kill Gram-Negative Bacteria.

antibiotic resistance bacteria lipid nanoparticles model membranes neutron reflectometry polysaccharide

Journal

Small (Weinheim an der Bergstrasse, Germany)
ISSN: 1613-6829
Titre abrégé: Small
Pays: Germany
ID NLM: 101235338

Informations de publication

Date de publication:
05 Oct 2023
Historique:
revised: 16 08 2023
received: 15 06 2023
medline: 6 10 2023
pubmed: 6 10 2023
entrez: 5 10 2023
Statut: aheadofprint

Résumé

The rapid increase and spread of Gram-negative bacteria resistant to many or all existing treatments threaten a return to the preantibiotic era. The presence of bacterial polysaccharides that impede the penetration of many antimicrobials and protect them from the innate immune system contributes to resistance and pathogenicity. No currently approved antibiotics target the polysaccharide regions of microbes. Here, describe monolaurin-based niosomes, the first lipid nanoparticles that can eliminate bacterial polysaccharides from hypervirulent Klebsiella pneumoniae, are described. Their combination with polymyxin B shows no cytotoxicity in vitro and is highly effective in combating K. pneumoniae infection in vivo. Comprehensive mechanistic studies have revealed that antimicrobial activity proceeds via a multimodal mechanism. Initially, lipid nanoparticles disrupt polysaccharides, then outer and inner membranes are destabilized and destroyed by polymyxin B, resulting in synergistic cell lysis. This novel lipidic nanoparticle system shows tremendous promise as a highly effective antimicrobial treatment targeting multidrug-resistant Gram-negative pathogens.

Identifiants

pubmed: 37798622
doi: 10.1002/smll.202305052
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2305052

Subventions

Organisme : National Health and Medical Research Council
ID : APP1144652
Organisme : National Health and Medical Research Council
ID : APP2002921

Informations de copyright

© 2023 The Authors. Small published by Wiley-VCH GmbH.

Références

World Health Organization, Antimicrobial resistance https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance, (accessed: November, 2021).
D. M. De Oliveira, B. M. Forde, T. J. Kidd, P. N. Harris, M. A. Schembri, S. A. Beatson, D. L. Paterson, M. J. Walker, Clin. Microbiol. Rev. 2020, 33, e00181.
M. A. Campos, M. A. Vargas, V. Regueiro, C. M. Llompart, S. Alberti, J. A. Bengoechea, Infect. Immun. 2004, 72, 7107.
M. K. Paczosa, J. Mecsas, Microbiol. Mol. Biol. Rev. 2016, 80, 629.
J. A. Bengoechea, J. Sa Pessoa, FEMS Microbiol. Rev. 2019, 43, 123.
S. Singh, J. J. Wilksch, R. A. Dunstan, A. Mularski, N. Wang, D. Hocking, L. Jebeli, H. Cao, A. Clements, A. W. Jenney, Microbiol. Spectr. 2022, 10, e01517.
V. N. Volozhantsev, M. A. Shpirt, I. A. Borzilov, V. E. Komisarova, M. V. Krasilnikova, S. A. Shashkov, V. V. Verevkin, A. Y. Knirel, Antibiotics 2020, 9, 732.
D. R. Drake, K. A. Brogden, D. V. Dawson, P. W. Wertz, J. Lipid Res. 2008, 49, 4.
C. L. Fischer, Antibiotics 2020, 9, 75.
H. Thormar, Lipids and Essential Oils as Antimicrobial Agents, John Wiley& Sons, Ltd, Chichester 2011, 25.
B. K. Yoon, J. A. Jackman, E. R. Valle-Gonzalez, N. J. Cho, Int. J. Mol. Sci. 2018, 19, 1114.
E. Porter, World J. Immunol. 2015, 5, 51.
H. Vorum, R. Brodersen, U. Kragh-Hansen, A. O. Pedersen, Biochim. Biophys. Acta. 1992, 1126, 135.
J. A. Jackman, B. K. Yoon, D. Li, N. J. Cho, Molecules 2016, 21, 305.
J. Y. B. Tan, B. K. Yoon, N. J. Cho, J. Lovric, M. Jug, J. A. Jackman, Int. J. Mol. Sci. 2021, 22, 9664.
A. Umerska, V. Cassisa, N. Matougui, M. L. Joly-Guillou, M. Eveillard, P. Saulnier, Eur. J. Pharm. Biopharm. 2016, 108, 100.
C. R. Thorn, N. Thomas, B. J. Boyd, C. A. Prestidge, Drug Deliv. Transl. Res. 2021, 11, 1598.
L. Xu, X. Wang, Y. Liu, G. Yang, R. J. Falconer, C.-X. Zhao, Adv. Nanobiomed. Res. 2021, 2, 2100109.
A. Sharma, U. S. Sharma, Int. J. Pharm. 1997, 154, 123.
Q. Zhang, W. Wu, J. Zhang, X. Xia, J. Drug Target 2020, 28, 271.
A. C. Pham, L. Hong, O. Montagnat, C. J. Nowell, T. H. Nguyen, B. J. Boyd, Mol. Pharm. 2016, 13, 280.
C. A. Brimacombe, J. T. Beatty, Bio. Protoc. 2013, 3, e934.
H. C. Neu, Am J Med 1990, 88, 2S.
D. L. Paterson, D. D. DePestel, Clin. Infect. Dis. 2009, 49, 291.
B. V. Peechakara, H. Basit, M. Gupta, Ampicillin, https://europepmc.org/article/nbk/nbk519569, (accessed: August, 2018).
M. J. Dorman, T. Feltwell, D. A. Goulding, J. Parkhill, F. L. Short, mBio 2018, 9, e01863.
L. A. Clifton, S. A. Holt, A. V. Hughes, E. L. Daulton, W. Arunmanee, F. Heinrich, S. Khalid, D. Jefferies, T. R. Charlton, J. R. Webster, C. J. Kinane, J. H. Lakey, Angew. Chem. Int. Ed. Engl. 2015, 54, 11952.
L. A. Clifton, M. W. Skoda, E. L. Daulton, A. V. Hughes, A. P. Le Brun, J. H. Lakey, S. A. Holt, J. R. Soc. Interface 2013, 10, 20130810.
X. Lai, M.-L. Han, Y. Ding, S. H. Chow, A. P. Le Brun, C.-M. Wu, P. J. Bergen, J.-H. Jiang, H.-Y. Hsu, B. W. Muir, Nat. Commun. 2022, 13, 343.
Y. Zhu, J. Lu, M. L. Han, X. Jiang, M. A. K. Azad, N. A. Patil, Y. W. Lin, J. Zhao, Y. Hu, H. H. Yu, K. Chen, J. D. Boyce, R. A. Dunstan, T. Lithgow, C. K. Barlow, W. Li, E. K. Schneider-Futschik, J. Wang, B. Gong, B. Sommer, D. J. Creek, J. Fu, L. Wang, F. Schreiber, T. Velkov, J. Li, Adv. Sci. 2020, 7, 2000704.
S. C. Nang, M. A. K. Azad, T. Velkov, Q. T. Zhou, J. Li, Pharmacol. Rev. 2021, 73, 679.
X. Lai, Y. Ding, C. M. Wu, X. Chen, J. H. Jiang, H. Y. Hsu, Y. Wang, A. P. Le Brun, J. Song, M. L. Han, J. Li, H. H. Shen, ACS Appl. Mater. Interfaces 2020, 12, 44485.
T. Jiang, Z. Zhang, Y. Zhang, H. Lv, J. Zhou, C. Li, L. Hou, Q. Zhang, Biomaterials 2012, 33, 9246.
Performance standards for antimicrobial susceptibility testing, 32th ed., Clinical and Laboratory Standards Institute, Malvern, Pennsylvania, USA 2022.
J. Meletiadis, S. Pournaras, E. Roilides, T. J. Walsh, Antimicrob. Agents Chemother. 2010, 54, 602.
S. Hammerschmidt, M. Rohde, Methods Mol. Biol. 2019, 1968, 13.
M. T. Anderson, L. A. Mitchell, L. Zhao, H. L. Mobley, mBio 2017, 8, 00740.
S. H. Chow, P. Deo, A. T. Y. Yeung, X. P. Kostoulias, Y. Jeon, M. L. Gao, A. Seidi, F. A. B. Olivier, S. Sridhar, C. Nethercott, D. Cameron, A. A. B. Robertson, R. Robert, C. R. Mackay, A. Traven, Z. B. Jin, C. Hale, G. Dougan, A. Y. Peleg, T. Naderer, J. Leukoc. Biol. 2020, 108, 967.
B. T. Tsuji, J. M. Pogue, A. P. Zavascki, M. Paul, G. L. Daikos, A. Forrest, D. R. Giacobbe, C. Viscoli, H. Giamarellou, I. Karaiskos, D. Kaye, J. W. Mouton, V. H. Tam, V. Thamlikitkul, R. G. Wunderink, J. Li, R. L. Nation, K. S. Kaye, Pharmacotherapy 2019, 39, 10.
C. B. Landersdorfer, J. Wang, V. Wirth, K. Chen, K. S. Kaye, B. T. Tsuji, J. Li, R. L. Nation, J. Antimicrob. Chemother. 2018, 73, 462.
A. M. Sandri, C. B. Landersdorfer, J. Jacob, M. M. Boniatti, M. G. Dalarosa, D. R. Falci, T. F. Behle, R. C. Bordinhão, J. Wang, A. Forrest, Clin. Infect. Dis. 2013, 57, 524.
M. James, A. Nelson, S. A. Holt, T. Saerbeck, W. A. Hamilton, F. Klose, Nucl. Instrum. Methods Phys. Res. A 2011, 632, 112.
A. R. J. Nelson, S. W. Prescott, J. Appl. Crystallogr. 2019, 52, 193.
S. A. Holt, A. P. Le Brun, C. F. Majkrzak, D. J. McGillivray, F. Heinrich, M. Lösche, J. H. Lakey, Soft Matter 2009, 5, 2576.
F. Heinrich, T. Ng, D. J. Vanderah, P. Shekhar, M. Mihailescu, H. Nanda, M. Losche, Langmuir 2009, 25, 4219.

Auteurs

Xiangfeng Lai (X)

Department of Materials Science and Engineering, Faculty of Engineering, Monash University, Clayton, Victoria, 3800, Australia.

Seong Hoong Chow (SH)

Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, 3800, Australia.

Anton P Le Brun (AP)

Australian Centre for Neutron Scattering, Australian Nuclear Science and Technology Organisation, Locked Bag 2001, Kirrawee DC, New South Wales, 2232, Australia.

Benjamin W Muir (BW)

CSIRO Manufacturing, Clayton, Victoria, 3168, Australia.

Phillip J Bergen (PJ)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Jacinta White (J)

CSIRO Manufacturing, Clayton, Victoria, 3168, Australia.

Heidi H Yu (HH)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Jiping Wang (J)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Jill Danne (J)

Monash Ramaciotti Centre for Cryo-Electron Microscopy, A Node of Microscopy Australia, Monash University, Clayton, Victoria, 3800, Australia.

Jhih-Hang Jiang (JH)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Francesca L Short (FL)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Mei-Ling Han (ML)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Richard A Strugnell (RA)

Department of Microbiology and Immunology at the Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Victoria, 3000, Australia.

Jiangning Song (J)

Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Clayton, Victoria, 3800, Australia.

Neil R Cameron (NR)

Department of Materials Science and Engineering, Faculty of Engineering, Monash University, Clayton, Victoria, 3800, Australia.

Anton Y Peleg (AY)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Jian Li (J)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Hsin-Hui Shen (HH)

Department of Materials Science and Engineering, Faculty of Engineering, Monash University, Clayton, Victoria, 3800, Australia.
Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Microbiology, Monash University, Clayton, Victoria, 3800, Australia.

Classifications MeSH