High-throughput fabrication of antimicrobial phage microgels and example applications in food decontamination

Lei Tian, Kyle Jackson, Leon He, Shadman Khan, Mathura Thirugnanasampanthar, Mellissa Gomez, Fereshteh Bayat, Tohid F. Didar, Zeinab Hosseinidoust

Published: 2024-02-27 DOI: 10.1038/s41596-024-00964-6

antimicrobial phage microgels

food decontamination

high-throughput fabrication

phage biofunctionality

selective targeting

AI 解读

Publisher Correction: A practical guide to large-scale docking

Thrombin generation test based on a 96-channel pipettor for evaluation of FXIa procoagulant activity in pharmaceuticals

Universal platform for the generation of thermostabilized GPCRs that crystallize in LCP

Probing the free-state solution behavior of drugs and their tendencies to self-aggregate into nano-entities

Fabrication and use of silicon hollow-needle arrays to achieve tissue nanotransfection in mouse tissue in vivo

Use of stable isotope-tagged thymidine and multi-isotope imaging mass spectrometry (MIMS) for quantification of human cardiomyocyte division

Graphene- and metal-induced energy transfer for single-molecule imaging and live-cell nanoscopy with (sub)-nanometer axial resolution

Analyzing somatic mutations by single-cell whole-genome sequencing

Transcriptome-wide measurement of poly(A) tail length and composition at subnanogram total RNA sensitivity by PAIso-seq

3D human induced pluripotent stem cell–derived bioengineered skeletal muscles for tissue, disease and therapy modeling

查看全部

Sections

Figures

References

Introduction
Materials
Procedure
Troubleshooting
Timing
Anticipated results
Acknowledgements

Fernandez-nieves, A., Wyss, H. M., Mattsson, J. & Weitz, D. A. Microgel Suspensions https://doi.org/10.1002/9783527632992 (Wiley, 2011).
Jones, C. G. in Forensic Microscopy for Skeletal Tissues (ed. Bell, L. S.) 1–20 (Springer, 2012).
The promise of phages. Nat. Biotechnol. 41, 583–583 (2023).
Souza, G. R. et al. Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol. 5, 291–296 (2010).
Chiang, C. Y. et al. Weaving genetically engineered functionality into mechanically robust virus fibers. Adv. Mater. 19, 826–832 (2007).
Chung, W. J. et al. Biomimetic self-templating supramolecular structures. Nature 478, 364–368 (2011).
Chen, S. et al. Identification of highly selective covalent inhibitors by phage display. Nat. Biotechnol. 39, 490–498 (2021).
Tian, L. et al. Bacteriophage‐built gels as platforms for biomedical applications. Can. J. Chem. Eng. 100, 2191–2203 (2022).
Jackson, K., Peivandi, A., Fogal, M., Tian, L. & Hosseinidoust, Z. Filamentous phages as building blocks for bioactive hydrogels. ACS Appl. Bio. Mater. 4, 2262–2273 (2021).
Salmond, G. P. C. & Fineran, P. C. A century of the phage: past, present and future. Nat. Rev. Microbiol. 13, 777–786 (2015).
Antimicrobial resistanceWorld Health Organization http://www.who.int/en/news-room/fact-sheets/detail/antimicrobial-resistance (2021).
Smith, G. P. & Petrenko, V. A. Phage display. Chem. Rev. 97, 391–410 (1997).
Smith, G. P., Petrenko, V. A. & Matthews, L. J. Cross-linked filamentous phage as an affinity matrix. J. Immunol. Methods 215, 151–161 (1998).
Jung, S. M., Qi, J., Oh, D., Belcher, A. & Kong, J. M13 virus aerogels as a scaffold for functional inorganic materials. Adv. Funct. Mater. 27, 1603203 (2017).
Peivandi, A., Tian, L., Mahabir, R. & Hosseinidoust, Z. Hierarchically structured, self-healing, fluorescent, bioactive hydrogels with self-organizing bundles of phage nanofilaments. Chem. Mater. 31, 5442–5449 (2019).
Peivandi, A. et al. Inducing microscale structural order in phage nanofilament hydrogels with globular proteins. ACS Biomater. Sci. Eng. 8, 340–347 (2022).
Chen, P. Y. et al. Assembly of viral hydrogels for three-dimensional conducting nanocomposites. Adv. Mater. 26, 5101–5107 (2014).
Oh, J. W. et al. Biomimetic virus-based colourimetric sensors. Nat. Commun. 5, 3043 (2014).
Ohmura, J. F. et al. Highly adjustable 3D nano-architectures and chemistries: via assembled 1D biological templates. Nanoscale 11, 1091–1101 (2019).
Lee, J. H. et al. Production of tunable nanomaterials using hierarchically assembled bacteriophages. Nat. Protoc. 12, 1999–2013 (2017).
Lee, J. H. et al. Phage-based structural color sensors and their pattern recognition sensing system. ACS Nano 11, 3632–3641 (2017).
Chen, L., Zhao, X., Lin, Y., Su, Z. & Wang, Q. Dual stimuli-responsive supramolecular hydrogel of bionanoparticles and hyaluronan. Polym. Chem. 5, 6754–6760 (2014).
Sawada, T., Yanagimachi, M. & Serizawa, T. Controlled release of antibody proteins from liquid crystalline hydrogels composed of genetically engineered filamentous viruses. Mater. Chem. Front. 1, 146–151 (2017).
Li, Y. et al. Selectively suppressing tumor angiogenesis for targeted breast cancer therapy by genetically engineered phage. Adv. Mater. 32, e2001260 (2020).
Yun, Y. H., Goetz, D. J., Yellen, P. & Chen, W. Hyaluronan microspheres for sustained gene delivery and site-specific targeting. Biomaterials 25, 147–157 (2004).
Tian, L. et al. Self-assembling nanofibrous bacteriophage microgels as sprayable antimicrobials targeting multidrug-resistant bacteria. Nat. Commun. 13, 7158 (2022).
Mao, A. S. et al. Deterministic encapsulation of single cells in thin tunable microgels for niche modelling and therapeutic delivery. Nat. Mater. 16, 236–243 (2017).
Zhu, C., Tian, L., Liao, J., Zhang, X. & Gu, Z. Fabrication of bioinspired hierarchical functional structures by using honeycomb films as templates. Adv. Funct. Mater. 28, 1–8 (2018).
Årdal, C. et al. Antibiotic development—economic, regulatory and societal challenges. Nat. Rev. Microbiol. 18, 267–274 (2020).
Emergency cases treated with investigational phage bank. Adaptive Phage Therapeutics https://aphage.com/science/case-studies/ (2023).
Maitz, J., Merlino, J., Rizzo, S., McKew, G. & Maitz, P. Burn wound infections microbiome and novel approaches using therapeutic microorganisms in burn wound infection control. Adv. Drug Deliv. Rev. 196, 114769 (2023).
Awwad, S. et al. Principles of pharmacology in the eye. Br. J. Pharmacol. 174, 4205–4223 (2017).
Jóhannesson, G., Stefánsson, E. & Loftsson, T. Microspheres and nanotechnology for drug delivery. Dev. Ophthalmol. 55, 93–103 (2016).
Rahman, R., Scharff, R. L. & Wu, F. Foodborne disease outbreaks in flour and flour-based food products from microbial pathogens in the United States, and their health economic burden. Risk Anal. https://doi.org/10.1111/risa.14132 (2023).
Prasad, A. et al. Advancing in situ food monitoring through a smart lab‐in‐a‐package system demonstrated by the detection of salmonella in whole chicken. Adv. Mater. https://doi.org/10.1002/adma.202302641 (2023).
GRAS notice 755, Preparation containing two bacterial phages specific to Escherichia coli O157Food and Drug Administration https://www.fda.gov/media/117249/download (2018).
GRAS Notice 834, preparation containing bacterial phages specific to shiga-toxin producing Escherichia coliFood and Drug Administration https://www.fda.gov/media/133519/download (2019).
Chen, Y., Wang, Y., Paez-Espino, D., Polz, M. F. & Zhang, T. Prokaryotic viruses impact functional microorganisms in nutrient removal and carbon cycle in wastewater treatment plants. Nat. Commun. 12, 5398 (2021).
Bayat, F., Didar, T. F. & Hosseinidoust, Z. Emerging investigator series: bacteriophages as nano engineering tools for quality monitoring and pathogen detection in water and wastewater. Environ. Sci. Nano 8, 367–389 (2021).
Lewis, J. M. & Sagona, A. P. Armed phages are heading for clinical trials. Nat. Microbiol. https://doi.org/10.1038/s41564-023-01415-w (2023).
Headen, D. M., Aubry, G., Lu, H. & García, A. J. Microfluidic-based generation of size-controlled, biofunctionalized synthetic polymer microgels for cell encapsulation. Adv. Mater. 26, 3003–3008 (2014).
Eydelnant, I. A., Betty Li, B. & Wheeler, A. R. Microgels on-demand. Nat. Commun. 5, 3355 (2014).
Brugger, B. & Richtering, W. Magnetic, thermosensitive microgels as stimuli-responsive emulsifiers allowing for remote control of separability and stability of oil in water-emulsions. Adv. Mater. 19, 2973–2978 (2007).
An, H. Z., Helgeson, M. E. & Doyle, P. S. Nanoemulsion composite microgels for orthogonal encapsulation and release. Adv. Mater. 24, 3838–3844 (2012).
Schmitt, C. et al. Internal structure and colloidal behaviour of covalent whey protein microgels obtained by heat treatment. Soft Matter 6, 4876–4884 (2010).
Nicolai, T. Formation and functionality of self-assembled whey protein microgels. Colloids Surf. B Biointerfaces 137, 32–38 (2016).
Phan-Xuan, T. et al. On the crucial importance of the ph for the formation and self-stabilization of protein microgels and strands. Langmuir 27, 15092–15101 (2011).
Li, Y. et al. Rapid assembly of heterogeneous 3D cell microenvironments in a microgel array. Adv. Mater. 28, 3543–3548 (2016).
Yeh, J. et al. Micromolding of shape-controlled, harvestable cell-laden hydrogels. Biomaterials 27, 5391–5398 (2006).
Wang, J. et al. Antimicrobial peptides: promising alternatives in the post feeding antibiotic era. Med. Res. Rev. 39, 831–859 (2019).
Hou, K. et al. Microbiota in health and diseases. Signal Transduct. Target. Ther. 7, 135 (2022).
Burmeister, A. R. & Turner, P. E. Trading-off and trading-up in the world of bacteria–phage evolution. Curr. Biol. 30, R1120–R1124 (2020).
Daly, R., Sader, J. E. & Boland, J. J. Taming self-organization dynamics to dramatically control porous architectures. ACS Nano 10, 3087–3092 (2016).
Takehiro Nishikawa et al. Fabrication of honeycomb film of an amphiphilic copolymer at the air−water interface. Langmuir 18, 5734–5740 (2002).
Wang, W. et al. Deterministic reshaping of breath figure arrays by directional photomanipulation. ACS Appl. Mater. Interfaces 9, 4223–4230 (2017).
Zhang, A., Bai, H. & Li, L. Breath figure: a nature-inspired preparation method for ordered porous films. Chem. Rev. 115, 9801–9868 (2015).
Wang, X., Bukusoglu, E. & Abbott, N. L. A practical guide to the preparation of liquid crystal-templated microparticles. Chem. Mater. 29, 53–61 (2017).
Widawski, G. & Rawiso, M. Self-organized honeycomb morphology of star-polymer polystyrene films. Nature 369, 387–389 (1994).
Zhang, A. et al. Formation of breath figure arrays in methanol vapor assisted by surface active agents. ACS Appl. Mater. Interfaces 6, 8921–8927 (2014).
Zhao, B., Zhang, J., Wang, X. & Li, C. Water-assisted fabrication of honeycomb structure porous film from poly (l-lactide). J. Mater. Chem. 16, 509–513 (2006).
Liu, C., Lang, W., Shi, B. & Guo, Y. Fabrication of ordered honeycomb porous polyvinyl chloride (PVC) films by breath figures method. Mater. Lett. 107, 53–55 (2013).
Yabu, H., Tanaka, M., Ijiro, K. & Shimomura, M. Preparation of honeycomb-patterned polyimide films by self-organization. Langmuir 19, 6297–6300 (2003).
Sambrook, J. & Russell, D. W. Molecular Cloning: A Laboratory Manual 3rd edn https://doi.org/10.1177/0261018311403863 (Cold Spring Harbour Laboratory Press, 2001).
Chung, W. J., Lee, D. Y. & Yoo, S. Y. Chemical modulation of M13 bacteriophage and its functional opportunities for nanomedicine. Int. J. Nanomed. 9, 5825–5836 (2014).
Courchesne, N. M. D. et al. Assembly of a bacteriophage-based template for the organization of materials into nanoporous networks. Adv. Mater. 26, 3398–3404 (2014).
Tian, L., He, L., Jackson, K., Mahabir, R. & Hosseinidoust, Z. Bacteria repellent protein hydrogel decorated with tunable, isotropic, nano-on-micro hierarchical microbump array. Chem. Commun. 57, 10883–10886 (2021).
Migneault, I., Dartiguenave, C., Bertrand, M. J. & Waldron, K. C. Glutaraldehyde: behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking. Biotechniques 37, 790–802 (2004).

High-throughput fabrication of antimicrobial phage microgels and example applications in food decontamination

Supplementary information

推荐阅读