Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila
Summary: Drosophila Toll-1 and all mammalian Toll-like receptors regulate innate immunity. However, the functions of the remaining eight Toll-related proteins in Drosophila are not fully understood. Here, we show that Drosophila Toll-9 is necessary and sufficient for a special form of compensatory p...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-05-01
|
| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124722005885 |
| _version_ | 1818211547729625088 |
|---|---|
| author | Alicia Shields Alla Amcheslavsky Elizabeth Brown Tom V. Lee Yingchao Nie Takahiro Tanji Y. Tony Ip Andreas Bergmann |
| author_facet | Alicia Shields Alla Amcheslavsky Elizabeth Brown Tom V. Lee Yingchao Nie Takahiro Tanji Y. Tony Ip Andreas Bergmann |
| author_sort | Alicia Shields |
| collection | DOAJ |
| description | Summary: Drosophila Toll-1 and all mammalian Toll-like receptors regulate innate immunity. However, the functions of the remaining eight Toll-related proteins in Drosophila are not fully understood. Here, we show that Drosophila Toll-9 is necessary and sufficient for a special form of compensatory proliferation after apoptotic cell loss (undead apoptosis-induced proliferation [AiP]). Mechanistically, for AiP, Toll-9 interacts with Toll-1 to activate the intracellular Toll-1 pathway for nuclear translocation of the NF-κB-like transcription factor Dorsal, which induces expression of the pro-apoptotic genes reaper and hid. This activity contributes to the feedback amplification loop that operates in undead cells. Given that Toll-9 also functions in loser cells during cell competition, we define a general role of Toll-9 in cellular stress situations leading to the expression of pro-apoptotic genes that trigger apoptosis and apoptosis-induced processes such as AiP. This work identifies conceptual similarities between cell competition and AiP. |
| first_indexed | 2024-12-12T05:34:14Z |
| format | Article |
| id | doaj.art-6a1fc7ad54e6466c9b1985c50dc6f126 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-12-12T05:34:14Z |
| publishDate | 2022-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-6a1fc7ad54e6466c9b1985c50dc6f1262022-12-22T00:36:13ZengElsevierCell Reports2211-12472022-05-01397110817Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in DrosophilaAlicia Shields0Alla Amcheslavsky1Elizabeth Brown2Tom V. Lee3Yingchao Nie4Takahiro Tanji5Y. Tony Ip6Andreas Bergmann7Department of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA 01605, USADepartment of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA 01605, USADepartment of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA 01605, USADepartment of Neurology, Baylor College of Medicine, Houston, TX 77030, USAProgram in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USAProgram in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USAProgram in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USADepartment of Molecular, Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA 01605, USA; Corresponding authorSummary: Drosophila Toll-1 and all mammalian Toll-like receptors regulate innate immunity. However, the functions of the remaining eight Toll-related proteins in Drosophila are not fully understood. Here, we show that Drosophila Toll-9 is necessary and sufficient for a special form of compensatory proliferation after apoptotic cell loss (undead apoptosis-induced proliferation [AiP]). Mechanistically, for AiP, Toll-9 interacts with Toll-1 to activate the intracellular Toll-1 pathway for nuclear translocation of the NF-κB-like transcription factor Dorsal, which induces expression of the pro-apoptotic genes reaper and hid. This activity contributes to the feedback amplification loop that operates in undead cells. Given that Toll-9 also functions in loser cells during cell competition, we define a general role of Toll-9 in cellular stress situations leading to the expression of pro-apoptotic genes that trigger apoptosis and apoptosis-induced processes such as AiP. This work identifies conceptual similarities between cell competition and AiP.http://www.sciencedirect.com/science/article/pii/S2211124722005885Toll-9apoptosis-induced proliferationundead cellsDrosophilaToll-1amplification loop |
| spellingShingle | Alicia Shields Alla Amcheslavsky Elizabeth Brown Tom V. Lee Yingchao Nie Takahiro Tanji Y. Tony Ip Andreas Bergmann Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila Cell Reports Toll-9 apoptosis-induced proliferation undead cells Drosophila Toll-1 amplification loop |
| title | Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila |
| title_full | Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila |
| title_fullStr | Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila |
| title_full_unstemmed | Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila |
| title_short | Toll-9 interacts with Toll-1 to mediate a feedback loop during apoptosis-induced proliferation in Drosophila |
| title_sort | toll 9 interacts with toll 1 to mediate a feedback loop during apoptosis induced proliferation in drosophila |
| topic | Toll-9 apoptosis-induced proliferation undead cells Drosophila Toll-1 amplification loop |
| url | http://www.sciencedirect.com/science/article/pii/S2211124722005885 |
| work_keys_str_mv | AT aliciashields toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT allaamcheslavsky toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT elizabethbrown toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT tomvlee toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT yingchaonie toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT takahirotanji toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT ytonyip toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila AT andreasbergmann toll9interactswithtoll1tomediateafeedbackloopduringapoptosisinducedproliferationindrosophila |