Growth Arrest and Autophagy Are Required for Salivary Gland Cell Degradation in Drosophila
Open accessAbstract
Autophagy is a catabolic process that is negatively regulated by growth and has been implicated in cell death. We find that autophagy is induced following growth arrest and precedes developmental autophagic cell death of Drosophila salivary glands. Maintaining growth by expression of either activated Ras or positive regulators of the class I phosphoinositide 3-kinase (PI3K) pathway inhibits autophagy and blocks salivary gland cell degradation. Developmental degradation of salivary glands is also inhibited in autophagy gene (atg) mutants. Caspases are active in PI3K-expressing and atg mutant salivary glands, and combined inhibition of both autophagy and caspases increases suppression of gland degradation. Further, induction of autophagy is sufficient to induce premature cell death in a caspase-independent manner. Our results provide in vivo evidence that growth arrest, autophagy, and atg genes are required for physiological autophagic cell death and that multiple degradation pathways cooperate in the efficient clearance of cells during development.
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In a limited number of cases, autophagy has been established as the cause of cell death, although opposite results have been reported using analogous experimental settings.
“In a limited number of cases, autophagy has been established as the cause of cell death; 97,199,[658][659][660][661][662][663][664] although opposite results have been reported using analogous experimental settings.665”
From Guidelines for the use and interpretation of assays for monitoring autophagy (2012) · cites this paper as [658]
Complete removal of larval salivary glands during D. melanogaster metamorphosis requires both apoptotic and autophagic machinery.
“Along similar lines, the complete removal of larval salivary glands from D. melanogaster larvae undergoing metamorphosis requires the apoptotic as well as the autophagic machinery [830–832].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [830]
In D. melanogaster midgut and salivary gland developmental scenarios, autophagy-dependent cell death is preceded by growth arrest and controlled by ecdysone.
“In both these developmental scenarios, autophagy-dependent cell death is preceded by growth arrest and is controlled by ecdysone, a steroid hormone that is critically required in Drosophila to undergo the larva-to-pupa transition and subsequent metamorphosis into an adult fly [830, 833].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [830]
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Self-citationLi, Y.-B., Li, X.-R., Yang, T., Wang, J.-X., & Zhao, X.-F. (2016) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2016.10.004 · Cited by 62 · see citing works
UTX coordinates steroid hormone-mediated autophagy and cell death
Denton, D., Aung-Htut, M. T., Lorensuhewa, N., Nicolson, S., Zhu, W., Mills, K., Cakouros, D., Bergmann, A., & Kumar, S. (2013) · Nature Communications · doi:10.1038/ncomms3916 · Cited by 58 · see citing works
<i>Drosophila</i> Golgi membrane protein Ema promotes autophagosomal growth and function
Kim, S., Naylor, S. A., & DiAntonio, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1120320109 · Cited by 53 · see citing works
Autophagy activity contributes to programmed cell death in<i>Caenorhabditis elegans</i>
Wang, H., Lu, Q., Cheng, S., Wang, X., & Zhang, H. (2013) · Autophagy · doi:10.4161/auto.26152 · Cited by 39 · see citing works
The Proton-Coupled Monocarboxylate Transporter Hermes Is Necessary for Autophagy during Cell Death
Velentzas, P. D., Zhang, L., Das, G., Chang, T.-K., Nelson, C., Kobertz, W. R., & Baehrecke, E. H. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.09.015 · Cited by 31 · see citing works
Self-citationRal GTPase and the exocyst regulate autophagy in a tissue‐specific manner
Tracy, K., Velentzas, P. D., & Baehrecke, E. H. (2016) · The EMBO Reports · doi:10.15252/embr.201541283 · Cited by 22 · see citing works
Self-citationCharacterization of Autophagic Responses in Drosophila melanogaster
Xu, T., Kumar, S., & Denton, D. (2017) · Methods in Enzymology · doi:10.1016/bs.mie.2016.09.089 · Cited by 12 · see citing works
- Authors
- Berry, D. L., & Baehrecke, E. H.
- Affiliations
- Children's National (US)
- University of Massachusetts Chan Medical School (US)
- Corresponding author
- Baehrecke, Eric H.
- ORCID
- Baehrecke, Eric H.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-12
- Volume
- 131
- Issue
- 6
- Pages
- 1137-1148
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC2180345
- OpenAlex
- W2102601355
- Cited by
- 602
- References
- 49
- Citations by year
- 2026: 14 · 2025: 13 · 2024: 15 · 2023: 14 · 2022: 16 · 2021: 30 · 2020: 24 · 2019: 32 · 2018: 30 · 2017: 30 · 2016: 23 · 2015: 50 · 2014: 41 · 2013: 54 · 2012: 53
- FWCI
- 28.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2055 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (GM59136, R56GM059136, GM079431, R01GM059136, R01GM079431)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- autophagy, growth arrest, salivary glands, developmental cell death, caspases, PI3K signaling, Ras signaling, autophagy-related genes, caspase-independent cell death, Drosophila, tissue degradation
- MeSH terms
- Autophagy-Related Protein-1 Homolog, Animals, Autophagy, Cell Division, Drosophila, Mutation, Salivary Glands, Signal Transduction, Cell Death, Protein Serine-Threonine Kinases, Phosphatidylinositol 3-Kinases, Caspases, Drosophila Proteins
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