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Ultrastructural Imaging of Salmonella–Host Interactions Using Super‐Resolution Correlative Light‐Electron Microscopy of Bi

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Ultrastructural Imaging of Salmonella–Host Interactions Using Super‐Resolution Correlative Light‐Electron Microscopy of Bi Ultrastructural imaging of Salmonella-Host interactions using super-resolution correlative light-electron microscopy of bioorthogonal pathogens Citation for published version (APA): van Elsland, D. M., Pujals, S., Bakkum, T., Bos, E., Oikonomeas-Koppasis, N., Berlin, I., Neefjes, J., Meijer, A. H., Koster, A. J., Albertazzi, L., & van Kasteren, S. I. (2018). Ultrastructural imaging of Salmonella-Host interactions using super-resolution correlative light-electron microscopy of bioorthogonal pathogens. ChemBioChem, 19(16), 1766-1770. https://doi.org/10.1002/cbic.201800230 DOI: 10.1002/cbic.201800230 Document status and date: Published: 16/08/2018 Document Version: Publisher’s PDF, also known as Version of Record (includes final page, issue and volume numbers) Please check the document version of this publication: • A submitted manuscript is the version of the article upon submission and before peer-review. There can be important differences between the submitted version and the official published version of record. People interested in the research are advised to contact the author for the final version of the publication, or visit the DOI to the publisher's website. • The final author version and the galley proof are versions of the publication after peer review. • The final published version features the final layout of the paper including the volume, issue and page numbers. Link to publication General rights Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights. • Users may download and print one copy of any publication from the public portal for the purpose of private study or research. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying the publication in the public portal. If the publication is distributed under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license above, please follow below link for the End User Agreement: www.tue.nl/taverne Take down policy If you believe that this document breaches copyright please contact us at: [email protected] providing details and we will investigate your claim. Download date: 24. Sep. 2021 DOI:10.1002/cbic.201800230 Full Papers Ultrastructural Imaging of Salmonella–Host Interactions Using Super-resolution Correlative Light-Electron Microscopy of Bioorthogonal Pathogens Daphne M. van Elsland+,[a, b] Sílvia Pujals+,[c] ThomasBakkum+,[a] Erik Bos,[d] Nikolaos Oikonomeas-Koppasis,[a] Ilana Berlin,[b] Jacques Neefjes,[b] AnnemarieH.Meijer,[e] Abraham J. Koster,*[d] LorenzoAlbertazzi,*[c, f] and SanderI.van Kasteren*[a] The imaging of intracellular pathogens inside host cells is com- duce fluorophores compatible with stochastic opticalrecon- plicated by the low resolution and sensitivity of fluorescence struction microscopy (STORM) and placing this in acorrelative microscopy and by the lack of ultrastructural information to light electron microscopy (CLEM) workflow,the pathogen can visualizethe pathogens. Herein, we present anew methodto be imaged within its host cell context Typhimurium with ares- visualizethese pathogens during infectionthat circumvents olution of 20 nm. This STORM-CLEM approachthus presentsa these problems: by using ametabolic hijacking approachto new approachtounderstand these pathogens during infec- bioorthogonally label the intracellular pathogen Salmonella Ty- tion. phimurium and by using thesebioorthogonal groups to intro- Introduction The rise of antibiotic resistance is one of the major threats to lose analogues,[4] intracellular pathogens have been visualized global health.One class of pathogens proving particularly trou- selectively within host-cell phagosomes. Bioorthogonal non- blesomeinthis regard is intracellular bacteria. These thwart canonical amino acid tagging (BONCAT[5])—the incorporation immune detection by residingand replicating inside host-cell of bioorthogonal amino acids into atarget cell proteome—has phagosomes.[1] Through secretion of factorsthat manipulate also proven valuableinthis context, for example, to image phagosomal maturation, they ensure their intracellular survival, bacterialprotein synthesis or retrieve pathogenic proteins despite an extensive arsenal of defence mechanisms deployed secreted into the host cytosol by Yersinia enterocolitica,[6] Sal- by the mammalian host.[2] It is, therefore, of utmost importance monella Typhimurium,[7] Escherichia coli,[8] and Mycobacterium to understand bacterium–host interactionsatthe cellular and smegmatis.[9] However,these labellingapproaches either re- molecular levels. Bioorthogonal chemistry has proventobea quire the mutant tRNA/tRNAsynthetase pair specific for the major breakthrough technique to study these host–pathogen bioorthogonal methionine, phenylalanine, or norleucine ana- interactions. Through hijacking the biosynthetic machinery of loguestobeintroduced into the pathogen to achieve incorpo- the cell wall with biorthogonalanalogues of d-Ala[3] or treha- ration of the desired groups or suffer from low sensitivity.[10] [a] Dr.D.M.van Elsland,+ T. Bakkum,+ N. Oikonomeas-Koppasis, E-mail:[email protected] Dr.S.I.van Kasteren [e] Dr.A.H.Meijer Leiden Institute of Chemistryand Institute of BiologyLeiden, Leiden University The Institute for ChemicalImmunology,Leiden University Sylviusweg 72,2333 BE, Leiden (The Netherlands) Einsteinweg55, 2333 CC Leiden (The Netherlands) [f] Dr.L.Albertazzi E-mail:[email protected] DepartmentofBiomedical Engineeringand + [b] Dr.D.M.van Elsland, Dr.I.Berlin, Dr.J.Neefjes Institute of ComplexMolecular Systems Department of Celland Chemical Biologyand Eindhoven UniversityofTechnology the Institute for Chemical Immunology 5600MBEindhoven (The Netherlands) Leiden University Medical Center LUMC [+] These authorscontributed equally to this work. Einthovenweg 22, 2333 ZC, Leiden (The Netherlands) Supporting Information and the ORCID identification numbers for the [c] Dr.S.Pujals,+ Dr.L.Albertazzi authors of this article can be found under https://doi.org/10.1002/ Department of Nanoscopy for Nanomedicine cbic.201800230. Institute of Bioengineering of Catalonia(IBEC) Barcelona Institute of Science and Technology 2018 The Authors. Published by Wiley-VCH Verlag GmbH&Co. KGaA. 08028 Barcelona(Spain) This is an open access article under the terms of the Creative Commons At- E-mail:[email protected] tributionNon-Commercial NoDerivs License, which permitsuse and distri- bution in any medium, provided the original work is properly cited, the use [d] Dr.E.Bos, Dr.A.J.Koster is non-commercial and no modifications or adaptations are made. Department of Electron Microscopy,LeidenUniversity Medical Center LUMC Einthovenweg 22, 2333 ZC, Leiden (The Netherlands) ChemBioChem 2018, 19,1766 –1770 1766 2018 The Authors. PublishedbyWiley-VCH Verlag GmbH &Co. KGaA, Weinheim Full Papers This has limited their use to bacterial strains for whichthese bacterialproteome after uptake by phagocytes without affect- techniques are available. ing bacterial growth and infectivity.Weoptimized the incorpo- In an effort to image the subcellular location of bacteria in ration of homopropargylglycine (Hpg) in vitro by using an in- host phagocytes,werecently reported an approachthat al- gel fluorescence assay (Figure S1 in the Supporting Informa- lowed visualization of bacteria within the ultrastructural con- tion) and observed detectable incorporation after pulsing with text of the hostcells. We imaged BONCAT-labelled E. coli by Hpg (0.04–4 mm)for 30 min. Thiswas confirmed by flow cy- using correlative light and electron microscopy (CLEM).[11] After tometry(Figures1Aand S2). BONCATofaDsRed-expressing sectioning frozen cell samples down to athickness of 75 nm strain of Salmonella[19] showed no effect on DsRed expression followed by an on-section copper-catalysedHuisgen cycloaddi- levelsinthe presenceofHpg up to aconcentrationof0.4 mm tion (ccHc) reaction,[12] we imaged the resulting bioorthogonal (Figure S2). Outgrowthexperiments—for whichgrowth rates labels by using confocal microscopy.Subsequenttransmission were determined after Hpg pulses (Figure S3)—showed that electron microscopy (TEM) of the same sectionallowed the growth rates recovered to 90 %within 1h(after 30 min Hpg Æ placementofthe fluorescent signal within its ultrastructural pulse). Recovery was longer (up to 3h)with longer Hpg context of the phagocytose. pulses. If this approach could be extended to pathogenic species, it would provide apowerful tool to study the interaction of host phagocytes with intracellular pathogens. However, for the ap- proach to be of use forunmodified strains, two major con- straintsrelating to both BONCATand CLEM have to be over- come. The first is the reliance on mutant tRNA/tRNA synthases for the incorporation of the bioorthogonal amino acids, com- poundedbythe low overall signal in BONCAT-CLEM (stemming from the thinness of the samples). We hypothesized that meta- bolic hijacking approaches reported for E. coli auxotrophic strains[13] would need to be extended and optimized to allow sufficient label incorporation with nonauxotrophic bacterial species, thusensuring their detection by CLEM.The second limitation is relatedtothe CLEM imaging itself:whereas the resolution of the electron micrograph is of the order of
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