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C. elegans midbodies are released, phagocytosed and undergo LC3-dependent degradation independent of macroautophagy

Fazeli, Gholamreza, Trinkwalder, Michaela, Irmisch, Linda, Wehman, Ann Marie·2016·Journal of Cell Science
DOI 10.1242/jcs.190223PMC PMC5087666
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Abstract

In animals, the midbody coordinates the end of cytokinesis when daughter cells separate through abscission. The midbody was thought to be sequestered by macroautophagy, but recent evidence suggests that midbodies are primarily released and phagocytosed. It was unknown, however, whether autophagy proteins play a role in midbody phagosome degradation. Using a protein degradation assay, we show that midbodies are released in Caenorhabditis elegans. Released midbodies are known to be internalized by actin-driven phagocytosis, which we show requires the RAB-5 GTPase to localize the class III phosphoinositide 3-kinase (PI3K) complex at the cortex. Autophagy-associated proteins, including the Beclin 1 homolog BEC-1 and the Atg8/LC3-family members LGG-1 and LGG-2, localize around the midbody phagosome and are required for midbody degradation. In contrast, proteins required specifically for macroautophagy, such as UNC-51 and EPG-8 (homologous to ULK1/Atg1 and Atg14, respectively) are not required for midbody degradation. These data suggest that the C. elegans midbody is degraded by LC3-associated phagocytosis (LAP), not macroautophagy. Our findings reconcile the two prevailing models on the role of phagocytic and autophagy proteins, establishing a new non-canonical role for autophagy proteins in midbody degradation.

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Fig. 1. A subset of autophagy-related genes is required for midbody degradation. In embryos treated with atg-7 RNAi (n=9 embryos), lgg-1; lgg-2 double mutants (n=13), and bec-1 (n=4) or vps-34 (n=18) maternal-zygotic mutants. NMY-2::mCh persists longer than in controls (n=11, *P<0.01). The disappearance time in lgg-1 (n=9) or lgg-2 (n=8) single mutants, as well as in unc-51 (n=11 and 8 for e369 and e1189, respectively) or epg-8 maternal-zygotic mutants (n=9), was not significantly different than controls (P>0.05). Each point represents a single embryo and the mean±s.e.m. is also shown. Student's t-test with Bonferroni correction was used for statistical analysis.
Fig. 1. A subset of autophagy-related genes is required for midbody degradation. In embryos treated with atg-7 RNAi (n=9 embryos), lgg-1; lgg-2 double mutants (n=13), and bec-1 (n=4) or vps-34 (n=18) maternal-zygotic mutants. NMY-2::mCh persists longer than in controls (n=11, *P<0.01). The disappearance time in lgg-1 (n=9) or lgg-2 (n=8) single mutants, as well as in unc-51 (n=11 and 8 for e369 and e1189, respectively) or epg-8 maternal-zygotic mutants (n=9), was not significantly different than controls (P>0.05). Each point represents a single embryo and the mean±s.e.m. is also shown. Student's t-test with Bonferroni correction was used for statistical analysis.CC BY · PubMed Central
Fig. 2. Midbodies are released extracellularly and macroautophagy is not required for midbody internalization. (A) In control WEH51 embryos expressing mCh::PHPLCδ1 on membranes (PH, cyan), midbodies have lost NMY-2::GFP::ZF1 (yellow) fluorescence by the 15-cell stage (n=22/25 embryos). See also Movie 1. Midbody fluorescence (arrows) is retained in ced-2 and vps-34 mutants (n=12/12 and 11/13, respectively). Only one z-slice is shown. (B) Control midbodies (n=12), as well as midbodies from autophagy-deficient embryos treated with atg-7 RNAi (n=10), start losing NMY-2::GFP::ZF1 fluorescence on the AB midbody by 20 min after the six-cell stage, whereas the abscission mutant unc-59 lost fluorescence earlier (n=7, P<0.01). Midbodies that were not phagocytosed maintained fluorescence for at least 40 min after the six-cell stage (n=6 and 11 for bec-1 and ced-1, respectively). Results are mean±s.e.m. See also Fig. S1. (C) Midbodies internalize (arrows) in lgg-1; lgg-2 maternal-zygotic mutants (n=26) as in control embryos (n=28) expressing NMY-2::mCh (yellow) and GFP::PHPLCδ1 (cyan). Student's t-test with Bonferroni correction was used for statistical analysis.
Fig. 2. Midbodies are released extracellularly and macroautophagy is not required for midbody internalization. (A) In control WEH51 embryos expressing mCh::PHPLCδ1 on membranes (PH, cyan), midbodies have lost NMY-2::GFP::ZF1 (yellow) fluorescence by the 15-cell stage (n=22/25 embryos). See also Movie 1. Midbody fluorescence (arrows) is retained in ced-2 and vps-34 mutants (n=12/12 and 11/13, respectively). Only one z-slice is shown. (B) Control midbodies (n=12), as well as midbodies from autophagy-deficient embryos treated with atg-7 RNAi (n=10), start losing NMY-2::GFP::ZF1 fluorescence on the AB midbody by 20 min after the six-cell stage, whereas the abscission mutant unc-59 lost fluorescence earlier (n=7, P<0.01). Midbodies that were not phagocytosed maintained fluorescence for at least 40 min after the six-cell stage (n=6 and 11 for bec-1 and ced-1, respectively). Results are mean±s.e.m. See also Fig. S1. (C) Midbodies internalize (arrows) in lgg-1; lgg-2 maternal-zygotic mutants (n=26) as in control embryos (n=28) expressing NMY-2::mCh (yellow) and GFP::PHPLCδ1 (cyan). Student's t-test with Bonferroni correction was used for statistical analysis.CC BY · PubMed Central
Fig. 3. PI3K acts during phagocytosis to internalize the midbody. (A) In control BV113 embryos (left, n=13 embryos), actin accumulates around the P0 midbody before internalization. Actin does not accumulate in ced-2 (n=11) or bec-1 (n=5) mutants. NMY-2::GFP labels midbodies (yellow) and LifeAct::RFP labels F-actin (cyan). See also Fig. S2 and Movies 2–4. (B) LifeAct::RFP fluorescence intensity is significantly reduced around the P0 midbody in ced-2 (red) and bec-1 (green) mutants compared to control embryos (blue) (P<0.01). In controls, internalization occurs 7±4 min (mean±s.d.) after the four-cell stage (n=14). Graphed results are mean±s.e.m. Student's t-test with Bonferroni correction was used for statistical analysis.
Fig. 3. PI3K acts during phagocytosis to internalize the midbody. (A) In control BV113 embryos (left, n=13 embryos), actin accumulates around the P0 midbody before internalization. Actin does not accumulate in ced-2 (n=11) or bec-1 (n=5) mutants. NMY-2::GFP labels midbodies (yellow) and LifeAct::RFP labels F-actin (cyan). See also Fig. S2 and Movies 2–4. (B) LifeAct::RFP fluorescence intensity is significantly reduced around the P0 midbody in ced-2 (red) and bec-1 (green) mutants compared to control embryos (blue) (P<0.01). In controls, internalization occurs 7±4 min (mean±s.d.) after the four-cell stage (n=14). Graphed results are mean±s.e.m. Student's t-test with Bonferroni correction was used for statistical analysis.CC BY · PubMed Central
Fig. 4. RAB-5 and PI3K regulate trafficking of the phagocytic receptor CED-1 to the plasma membrane. (A) BEC-1::GFP (green) localizes to the plasma membrane before midbody internalization (white arrows) in controls (left, n=22/25 embryos). Mild treatment with rab-5 RNAi (right) prevents BEC-1::GFP localization to the plasma membrane (yellow arrows, n=14/15) and (B) prevents midbody internalization (n=15). NMY-2::GFP::ZF1 labels midbodies (yellow) and mCh::PHPLCδ1 labels cell membranes (PH, cyan). (C) CED-1 (green) localizes to the plasma membrane (white arrows) in control embryos (left, n=48/51), but fails to localize to the membrane (yellow arrows) in vps-34 mutants (middle, n=10/14) or embryos treated with rab-5 RNAi (right, n=63/68) and is only observed in cytoplasmic puncta. Antibody stainings were performed in triplicate.
Fig. 4. RAB-5 and PI3K regulate trafficking of the phagocytic receptor CED-1 to the plasma membrane. (A) BEC-1::GFP (green) localizes to the plasma membrane before midbody internalization (white arrows) in controls (left, n=22/25 embryos). Mild treatment with rab-5 RNAi (right) prevents BEC-1::GFP localization to the plasma membrane (yellow arrows, n=14/15) and (B) prevents midbody internalization (n=15). NMY-2::GFP::ZF1 labels midbodies (yellow) and mCh::PHPLCδ1 labels cell membranes (PH, cyan). (C) CED-1 (green) localizes to the plasma membrane (white arrows) in control embryos (left, n=48/51), but fails to localize to the membrane (yellow arrows) in vps-34 mutants (middle, n=10/14) or embryos treated with rab-5 RNAi (right, n=63/68) and is only observed in cytoplasmic puncta. Antibody stainings were performed in triplicate.CC BY · PubMed Central
Fig. 5. Beclin 1 and LC3 homologs localize to the midbody phagosome. (A) BEC-1::GFP (green) staining surrounds midbodies (TSG-101, red) after internalization (n=5/22 embryos). Antibody staining was performed in triplicate. (B) mCh::LGG-2 (red) localizes on midbodies (NMY-2::GFP, green, n=12/14) and persists after acidification. Scale bars: 1 μm (A,B). See also Fig. S3. (C) mCh::LGG-2 is significantly enriched on midbody phagosomes after internalization (n=4 before internalization, n=5 after internalization, *P<0.05 compared to midbodies before internalization). mCh::LGG-2 enrichment does not occur in vps-34 mutants [n=6 released (solid blue circles), n=4 internalized midbodies (open blue circles)]. Results are mean±s.e.m. Student's t-test with Bonferroni correction was used for statistical analysis.
Fig. 5. Beclin 1 and LC3 homologs localize to the midbody phagosome. (A) BEC-1::GFP (green) staining surrounds midbodies (TSG-101, red) after internalization (n=5/22 embryos). Antibody staining was performed in triplicate. (B) mCh::LGG-2 (red) localizes on midbodies (NMY-2::GFP, green, n=12/14) and persists after acidification. Scale bars: 1 μm (A,B). See also Fig. S3. (C) mCh::LGG-2 is significantly enriched on midbody phagosomes after internalization (n=4 before internalization, n=5 after internalization, *P<0.05 compared to midbodies before internalization). mCh::LGG-2 enrichment does not occur in vps-34 mutants [n=6 released (solid blue circles), n=4 internalized midbodies (open blue circles)]. Results are mean±s.e.m. Student's t-test with Bonferroni correction was used for statistical analysis.CC BY · PubMed Central
Fig. 6. Midbodies are degraded by LC3-associated phagocytosis. (A) GFP-tagged NMY-2 with (blue, n=11 embryos) or without the ZF1 domain (green, n=7) starts to lose fluorescence by 15 min after AB midbody internalization (P<0.01), but mCherry-tagged NMY-2 (red, n=5) fluorescence persists longer. See also Fig. S4. (B) The disappearance of NMY-2::GFP::ZF1 was significantly delayed by NH4Cl treatment (n=9, P<0.05), but not by atg-7 RNAi (n=12, P>0.05) compared to controls (n=18). (C) NMY-2::mCh fluorescence is more stable in the P0 midbody in lgg-1; lgg-2 mutants (red, n=6) than in control WEH02 embryos (green, n=6) or unc-51 mutants (blue, n=10) (P<0.01). Results are mean±s.e.m. Student's t-test with Bonferroni correction was used for statistical analysis.
Fig. 6. Midbodies are degraded by LC3-associated phagocytosis. (A) GFP-tagged NMY-2 with (blue, n=11 embryos) or without the ZF1 domain (green, n=7) starts to lose fluorescence by 15 min after AB midbody internalization (P<0.01), but mCherry-tagged NMY-2 (red, n=5) fluorescence persists longer. See also Fig. S4. (B) The disappearance of NMY-2::GFP::ZF1 was significantly delayed by NH4Cl treatment (n=9, P<0.05), but not by atg-7 RNAi (n=12, P>0.05) compared to controls (n=18). (C) NMY-2::mCh fluorescence is more stable in the P0 midbody in lgg-1; lgg-2 mutants (red, n=6) than in control WEH02 embryos (green, n=6) or unc-51 mutants (blue, n=10) (P<0.01). Results are mean±s.e.m. Student's t-test with Bonferroni correction was used for statistical analysis.CC BY · PubMed Central
Fig. 7. Model of midbody fate. The contractile ring closes the membrane (dark gray) to form the intercellular bridge containing microtubules (blue) and the midbody (green). Abscission starts on one side of the midbody and the remnant is released after cuts on both sides requiring the septin UNC-59 and the ESCRT-I component TSG-101. Actin enrichment (red) depending on RAB-5, PI3K, CED-1 and CED-10 drives phagocytic cup formation and the midbody is engulfed. The midbody phagosome matures through PI3K activity and acquires lipidated LGG-1 and LGG-2 (blue) before fusing with lysosomes (orange) for degradation. Each line represents a membrane bilayer.
Fig. 7. Model of midbody fate. The contractile ring closes the membrane (dark gray) to form the intercellular bridge containing microtubules (blue) and the midbody (green). Abscission starts on one side of the midbody and the remnant is released after cuts on both sides requiring the septin UNC-59 and the ESCRT-I component TSG-101. Actin enrichment (red) depending on RAB-5, PI3K, CED-1 and CED-10 drives phagocytic cup formation and the midbody is engulfed. The midbody phagosome matures through PI3K activity and acquires lipidated LGG-1 and LGG-2 (blue) before fusing with lysosomes (orange) for degradation. Each line represents a membrane bilayer.CC BY · PubMed Central

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Metadata

Authors
Fazeli, G., Trinkwalder, M., Irmisch, L., & Wehman, A. M.
Affiliations
Rudolf Virchow Center for Experimental Biomedicine, University of Würzburg , Würzburg 97080 , Germany
ORCID
Wehman, Ann Marie
Venue
Journal of Cell Science
Publisher
The Company of Biologists
Published
2016-10-15
Volume
129
Issue
20
Pages
3721-3731
ISSN
  • 1477-9137
  • 0021-9533
DOI
10.1242/jcs.190223
PMC
PMC5087666
Cited by
50
References
8
Language
en
Licence
creativecommons.org/licenses/by/3.0 (vor, 1422 d)

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