Active interaction mapping reveals the hierarchical organization of autophagy
Open accessAbstract
We have developed a general progressive procedure, Active Interaction Mapping, to guide assembly of the hierarchy of functions encoding any biological system. Using this process, we assemble an ontology of functions comprising autophagy, a central recycling process implicated in numerous diseases. A first-generation model, built from existing gene networks in Saccharomyces, captures most known autophagy components in broad relation to vesicle transport, cell cycle, and stress response. Systematic analysis identifies synthetic-lethal interactions as most informative for further experiments; consequently, we saturate the model with 156,364 such measurements across autophagy-activating conditions. These targeted interactions provide more information about autophagy than all previous datasets, producing a second-generation ontology of 220 functions. Approximately half are previously unknown; we confirm roles for Gyp1 at the phagophore-assembly site, Atg24 in cargo engulfment, Atg26 in cytoplasm-to-vacuole targeting, and Ssd1, Did4, and others in selective and non-selective autophagy. The procedure and autophagy hierarchy are at http://atgo.ucsd.edu/.
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One approach to combining multiple network datasets treats them as different features annotated to each edge in a single unified network, with features combined to estimate a single interaction likelihood score for each node pair using supervised machine learning or Bayesian inference.
“One approach is to treat the multiple datasets as different “features” annotated to each edge in a single unified network; these multiple features are combined to estimate a single interaction likelihood score for each node pair using supervised machine learning (Kramer et al., 2017) or Bayesian inference (Franceschini et al., 2013; Wong et al., 2004).”
From Mapping the multiscale structure of biological systems (2021) · cites this paper as Kramer et al., 2017
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Biological Functions of Autophagy Genes: A Disease Perspective
Levine, B., & Kroemer, G. (2019) · Cell · doi:10.1016/j.cell.2018.09.048 · Cited by 2,832 · see citing works
Mapping the Genetic Landscape of Human Cells
Horlbeck, M. A., Xu, A., Wang, M., Bennett, N. K., Park, C. Y., Bogdanoff, D., Adamson, B., Chow, E. D., Kampmann, M., Peterson, T. R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.010 · Cited by 319 · see citing works
Global Genetic Networks and the Genotype-to-Phenotype Relationship
Costanzo, M., Kuzmin, E., van Leeuwen, J., Mair, B., Moffat, J., Boone, C., & Andrews, B. (2019) · Cell · doi:10.1016/j.cell.2019.01.033 · Cited by 241 · see citing works
Interpretation of cancer mutations using a multiscale map of protein systems
Zheng, F., Kelly, M. R., Ramms, D. J., Heintschel, M. L., Tao, K., Tutuncuoglu, B., Lee, J. J., Ono, K., Foussard, H., Chen, M., et al. (2021) · Science · doi:10.1126/science.abf3067 · Cited by 81 · see citing works
Self-citationMapping the multiscale structure of biological systems
Schaffer, L. V., & Ideker, T. (2021) · Cell Systems · doi:10.1016/j.cels.2021.05.012 · Cited by 75 · see citing works
Self-citationAutophagic clearance of proteasomes in yeast requires the conserved sorting nexin Snx4
Nemec, A. A., Howell, L. A., Peterson, A. K., Murray, M. A., & Tomko, R. J. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.817999 · Cited by 70 · see citing works
Environmental robustness of the global yeast genetic interaction network
Costanzo, M., Hou, J., Messier, V., Nelson, J., Rahman, M., VanderSluis, B., Wang, W., Pons, C., Ross, C., Ušaj, M., et al. (2021) · Science · doi:10.1126/science.abf8424 · Cited by 73 · see citing works
Autophagy in the context of the cellular membrane-trafficking system: the enigma of Atg9 vesicles
Noda, T. (2017) · Biochemical Society Transactions · doi:10.1042/bst20170128 · Cited by 65 · see citing works
Ma, M., Kumar, S., Purushothaman, L. K., Babst, M., Ungermann, C., Chi, R. J., & Burd, C. G. (2018) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-12-0743 · Cited by 45 · see citing works
Price, A., Manzoni, C., Cookson, M. R., & Lewis, P. A. (2018) · Cell and Tissue Research · doi:10.1007/s00441-017-2759-9 · Cited by 40 · see citing works
Jonathan Flint, C., & Ideker, T. E. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008519 · Cited by 34 · see citing works
Self-citationLoos, B., Klionsky, D. J., du Toit, A., & Hofmeyr, J. S. (2019) · Autophagy · doi:10.1080/15548627.2019.1687211 · Cited by 31 · see citing works
Jones, E. J., Matthews, Z. J., Gul, L., Sudhakar, P., Treveil, A., Divekar, D. P., Buck, J., Wrzesiński, T., Jefferson, M. A., Armstrong, S. D., et al. (2019) · Disease Models & Mechanisms · doi:10.1242/dmm.037069 · Cited by 25 · see citing works
DDOT: A Swiss Army Knife for Investigating Data-Driven Biological Ontologies
Yu, M., Ma, J., Ono, K., Zheng, F., Fong, S. H., Gary, A., Chen, J., Demchak, B., Pratt, D. R., & Ideker, T. E. (2019) · Cell Systems · doi:10.1016/j.cels.2019.02.003 · Cited by 24 · see citing works
Self-citationWhat We Learned From Big Data for Autophagy Research
Jacomin, A., Gul, L., Sudhakar, P., Korcsmaros, T. D., & Nezis, I. P. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00092 · Cited by 16 · see citing works
Mapping the Genetic Interaction Network of PARP inhibitor ResponsePreprint
Simpson, D., Jia, L., Jing, Y., & Adamson, B. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.08.19.553986 · Cited by 13 · see citing works
Gyp1 has a dual function as Ypt1 GAP and interaction partner of Atg8 in selective autophagy
Mitter, A. L., Schlotterhose, P., & Krick, R. (2019) · Autophagy · doi:10.1080/15548627.2019.1569929 · Cited by 12 · see citing works
Using the hierarchy of biological ontologies to identify mechanisms in flat networks
Bechtel, W. (2017) · Biology & Philosophy · doi:10.1007/s10539-017-9579-x · Cited by 12 · see citing works
Systematic Gene-to-Phenotype Arrays: A High-Throughput Technique for Molecular Phenotyping
Jaeger, P. A., Ornelas, L., McElfresh, C., Wong, L. R., Hampton, R. Y., & Ideker, T. E. (2018) · Molecular Cell · doi:10.1016/j.molcel.2017.12.016 · Cited by 10 · see citing works
Self-citationVojtová, J., & Hasek, J. (2020) · Cells · doi:10.3390/cells9010138 · Cited by 7 · see citing works
Identifying Candida albicans Gene Networks Involved in Pathogenicity
Thomas, G. H., Bain, J. M., Budge, S., Brown, A. J. P., & Ames, R. M. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00375 · Cited by 6 · see citing works
Chica, N., Andersen, A. N., Orellana‐Muñoz, S., Garcia, I., Aurélie Nguéa, P., Nakken, S., Durán, P. A., Håkensbakken, L., Schultz, S. W., Rødningen, E., et al. (2026) · Nature Cell Biology · doi:10.1038/s41556-025-01837-0 · Cited by 4 · see citing works
Bozorgmehr, J. H. (2024) · Molecular Genetics and Genomics · doi:10.1007/s00438-023-02090-6 · Cited by 4 · see citing works
Jones, E. J., Matthews, Z. J., Gul, L., Sudhakar, P., Treveil, A., Divekar, D., Buck, J., Wrzesinski, T., Jefferson, M., Armstrong, S. D., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/410027 · Cited by 4 · see citing works
Kumar, A., Hosseinnia, A., Gagarinova, A. G., Phanse, S., Kim, S., Aly, K. A., Zilles, S., & Babu, M. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz673 · Cited by 3 · see citing works
Screening for Genes Involved in Autophagy
Lu, K., & Li, H. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-981-16-2830-6_16 · Cited by 1 · see citing works
Bozorgmehr, J. H. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.28.542624
Bozorgmehr, J. H. (2023) · Research Square · doi:10.21203/rs.3.rs-2996044/v1
Bozorgmehr, J. H. (2024) · Research Square · doi:10.21203/rs.3.rs-2996044/v2
Using Biological Networks to Guide Biomedical Prediction
Zhao, X., Kong, J., Pu, K., Churas, C., Parker, J. A., & Ideker, T. E. (2026) · Methods in molecular biology · doi:10.1007/978-1-0716-5408-8_3
Self-citation
- Authors
- Kramer, M. H., Farré, J.-C., Mitra, K., Yu, M. K., Ono, K., Demchak, B., Licon, K., Flagg, M., Balakrishnan, R., Cherry, J. M., Subramani, S., & Ideker, T.
- Affiliations
- University of California San Diego (US)
- Stanford University (US)
- Corresponding author
- Subramani, Suresh
- Ideker, Trey
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 65
- Issue
- 4
- Pages
- 761-774.e5
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC5439305
- OpenAlex
- W2581669044
- Cited by
- 31
- References
- 93
- Citations by year
- 2026: 2 · 2024: 2 · 2023: 3 · 2021: 4 · 2020: 2 · 2019: 8 · 2018: 7 · 2017: 3
- FWCI
- 4.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (F30-HG007618, P50-GM085764, R01-DK41737, R01-ES014811, R01-GM084279, T32-GM007198, T32-GM008806, U41-HG001315, U41-HG002273)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Keywords
- autophagy, functional hierarchy, synthetic lethality, gene networks, vesicle trafficking, cell cycle, stress response, Ssd1, selective autophagy, Saccharomyces cerevisiae
- MeSH terms
- Autophagy-Related Proteins, Autophagy, Glucosyltransferases, Humans, Models, Genetic, Pichia, Saccharomyces cerevisiae, Gene Expression Regulation, Fungal, Systems Integration, GTPase-Activating Proteins, Genomics, Saccharomyces cerevisiae Proteins, Databases, Genetic, Systems Biology, Gene Regulatory Networks, Endosomal Sorting Complexes Required for Transport, Protein Interaction Maps
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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