Evidence map›Paper›PMID 37932397›Full record

ArticleNature methods2023

Genetically encoded multimeric tags for subcellular protein localization in cryo-EM.

Herman K H Fung, Yuki Hayashi, Veijo T Salo, Anastasiia Babenko, Ievgeniia Zagoriy, Andreas Brunner, Jan Ellenberg, Christoph W Müller, Sara Cuylen-Haering, Julia Mahamid

Open access · hybridAbstract read
In one paragraph

Article in Nature methods, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 32 papers.

0numbers the graph read from it
0cells of the map it votes in
32citing papers in PubMed
15.5field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

32 citing papers in PubMed, 56 citations in OpenAlex.

  1. Review
  2. Article
  3. Review
  4. Heterogeneity, dynamics and organelle interactions of lipid droplets.Nature reviews. Molecular cell biology · 2026
    Review
  5. Chemical reviews · 2026
    Review
  6. Review
  7. Review
  8. Cloneable contrast across all biological length scales.Journal of structural biology · 2026
    Article
  9. Article
  10. Article
  11. Article
  12. Article
  13. Review
  14. Article
  15. Molecular tags for electron cryo-tomography.Emerging topics in life sciences · 2025
    Review
  16. Review
  17. bioRxiv : the preprint server for biology · 2025
    Article
  18. Review
  19. Structural glycobiology - from enzymes to organelles.Biochemical Society transactions · 2025
    Review
  20. Review
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

10 authors at 4 institutions in 2 countries.

Herman K H Fung *Structural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.ORCID 0000-0001-9568-1782
Yuki Hayashi *Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany.ORCID 0000-0002-6991-2142
Veijo T Salo *Structural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.
Anastasiia BabenkoStructural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.
Ievgeniia ZagoriyStructural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.ORCID 0000-0003-2523-5132
Andreas BrunnerCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany.
Jan EllenbergCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany.ORCID 0000-0001-5909-701X
Christoph W MüllerStructural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany.ORCID 0000-0003-2176-8337
Sara Cuylen-HaeringCell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany. sara.cuylen-haering@embl.de.ORCID 0000-0002-1193-4648
Julia MahamidStructural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany. julia.mahamid@embl.de.ORCID 0000-0001-6968-041X
European Molecular Biology Laboratory · DEEuropean Bioinformatics Institute · GBEuropean Molecular Biology Laboratory · DEHeidelberg University · DE

Funding

Deutsche Forschungsgemeinschaft (German Research Foundation) 402723784Deutsche Forschungsgemeinschaft (German Research Foundation) 419120233EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 Marie Skłodowska-Curie Actions (H2020 Excellent Science - Marie Skłodowska-Curie Actions) 101028297Human Frontier Science Program (HFSP) CDA00045/2019
6 · The paper itself

Abstract

Cryo-electron tomography (cryo-ET) allows for label-free high-resolution imaging of macromolecular assemblies in their native cellular context. However, the localization of macromolecules of interest in tomographic volumes can be challenging. Here we present a ligand-inducible labeling strategy for intracellular proteins based on fluorescent, 25-nm-sized, genetically encoded multimeric particles (GEMs). The particles exhibit recognizable structural signatures, enabling their automated detection in cryo-ET data by convolutional neural networks. The coupling of GEMs to green fluorescent protein-tagged macromolecules of interest is triggered by addition of a small-molecule ligand, allowing for time-controlled labeling to minimize disturbance to native protein function. We demonstrate the applicability of GEMs for subcellular-level localization of endogenous and overexpressed proteins across different organelles in human cells using cryo-correlative fluorescence and cryo-ET imaging. We describe means for quantifying labeling specificity and efficiency, and for systematic optimization for rare and abundant protein targets, with emphasis on assessing the potential effects of labeling on protein function.

Indexed as

Neural Networks, ComputerOrganellesCryoelectron MicroscopyElectron Microscope TomographyHumansLigandsLigands

Identifiers

PMID37932397
PMCPMC10703698
OpenAlexW4388424988

What OpenQuestion holds

Textmetadata
LicenceCC BY
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.