FilamentID reveals the composition and function of metabolic enzyme polymers during gametogenesis
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Abstract
Gamete formation and subsequent offspring development often involve extended phases of suspended cellular development or even dormancy. How cells adapt to recover and resume growth remains poorly understood. Here, we visualized budding yeast cells undergoing meiosis by cryo-electron tomography (cryoET) and discovered elaborate filamentous assemblies decorating the nucleus, cytoplasm, and mitochondria. To determine filament composition, we developed a "filament identification" (FilamentID) workflow that combines multiscale cryoET/cryo-electron microscopy (cryoEM) analyses of partially lysed cells or organelles. FilamentID identified the mitochondrial filaments as being composed of the conserved aldehyde dehydrogenase Ald4 ALDH2 and the nucleoplasmic/cytoplasmic filaments as consisting of acetyl-coenzyme A (CoA) synthetase Acs1 ACSS2 . Structural characterization further revealed the mechanism underlying polymerization and enabled us to genetically perturb filament formation. Acs1 polymerization facilitates the recovery of chronologically aged spores and, more generally, the cell cycle re-entry of starved cells. FilamentID is broadly applicable to characterize filaments of unknown identity in diverse cellular contexts.
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Cites
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- Authors
- Hugener, J., Xu, J., Wettstein, R., Ioannidi, L., Velikov, D., Wollweber, F., Henggeler, A., Matos, J., & Pilhofer, M.
- Affiliations
- University of Vienna (AT)
- ETH Zurich (CH)
- Corresponding author
- Matos, Joao
- Pilhofer, Martin
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2024-06
- Volume
- 187
- Issue
- 13
- Pages
- 3303-3318.e18
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W4399854874
- Cited by
- 26
- References
- 4
- Citations by year
- 2026: 10 · 2025: 10 · 2024: 6
- FWCI
- 4.75
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- ETH Zürich Research Collection
- Funders
- European Research Council (101000232, 101002629)
- FWF (SFB F - 8807-B)
- Swiss National Science Foundation (176108)
- NOMIS Stiftung (101000232)
- ETH Zürich (31 17-2)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- meiosis, gametogenesis, Saccharomyces cerevisiae, aldehyde dehydrogenase, acetyl-CoA synthetase, ACS1, polymerization mechanism, cell cycle re-entry, starved cells, cryo-electron tomography, cryo-electron microscopy
- MeSH terms
- Aldehyde Dehydrogenase, Cell Nucleus, Coenzyme A Ligases, Cytoplasm, Gametogenesis, Meiosis, Mitochondria, Models, Molecular, Saccharomyces cerevisiae, Spores, Fungal, Cryoelectron Microscopy, Protein Structure, Quaternary, Saccharomyces cerevisiae Proteins, Electron Microscope Tomography
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