Atg27 tyrosine sorting motif is important for its trafficking and Atg9 localization

Verónica A. Segarra, Douglas R. Boettner, Sandra Lemmon

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

During autophagy, the transmembrane protein Atg27 facilitates transport of the major autophagy membrane protein Atg9 to the preautophagosomal structure (PAS). To better understand the function of Atg27 and its relationship with Atg9, Atg27 trafficking and localization were examined. Atg27 localized to endosomes and the vacuolar membrane, in addition to previously described PAS, Golgi and Atg9-positive structures. Atg27 vacuolar membrane localization was dependent on the adaptor AP-3, which mediates direct transport from the trans-Golgi to the vacuole. The four C-terminal amino acids (YSAV) of Atg27 comprise a tyrosine sorting motif. Mutation of the YSAV abrogated Atg27 transport to the vacuolar membrane and affected its distribution in TGN/endosomal compartments, while PAS localization was normal. Also, in atg27(ΔYSAV) or AP-3 mutants, accumulation of Atg9 in the vacuolar lumen was observed upon autophagy induction. Nevertheless, PAS localization of Atg9 was normal in atg27(ΔYSAV) cells. The vacuole lumen localization of Atg9 was dependent on transport through the multivesicular body, as Atg9 accumulated in the class E compartment and vacuole membrane in atg27(ΔYSAV) vps4Δ but not in ATG27 vps4Δ cells. We suggest that Atg27 has an additional role to retain Atg9 in endosomal reservoirs that can be mobilized during autophagy. The transmembrane protein Atg27 facilitates transport of the major autophagy membrane protein, Atg9, to the preautophagosomal structure (PAS). This new study demonstrates that Atg27 has a tyrosine-sorting motif in its cytoplasmic tail that mediates its localization to the vacuole membrane by the AP-3 adaptor pathway. Moreover, this motif is also important for preventing Atg9 delivery to the vacuole lumen via the MVB pathway, suggesting that Atg27 retains Atg9 in endosomal reservoirs for mobilization during autophagy.

Original languageEnglish (US)
Pages (from-to)365-378
Number of pages14
JournalTraffic
Volume16
Issue number4
DOIs
StatePublished - Apr 1 2015

Fingerprint

Autophagy
Sorting
Tyrosine
Vacuoles
Membranes
Membrane Proteins
Multivesicular Bodies
Endosomes
Proteins
Amino Acids
Mutation

Keywords

  • AP-3
  • Atg27
  • Atg9
  • Autophagy
  • Cytoplasm to vacuole transport
  • Endosome
  • Preautophagosomal structure
  • Trans-Golgi network
  • Tyrosine sorting motif
  • Vacuole

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Structural Biology
  • Molecular Biology
  • Genetics

Cite this

Atg27 tyrosine sorting motif is important for its trafficking and Atg9 localization. / Segarra, Verónica A.; Boettner, Douglas R.; Lemmon, Sandra.

In: Traffic, Vol. 16, No. 4, 01.04.2015, p. 365-378.

Research output: Contribution to journalArticle

Segarra, Verónica A. ; Boettner, Douglas R. ; Lemmon, Sandra. / Atg27 tyrosine sorting motif is important for its trafficking and Atg9 localization. In: Traffic. 2015 ; Vol. 16, No. 4. pp. 365-378.
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AB - During autophagy, the transmembrane protein Atg27 facilitates transport of the major autophagy membrane protein Atg9 to the preautophagosomal structure (PAS). To better understand the function of Atg27 and its relationship with Atg9, Atg27 trafficking and localization were examined. Atg27 localized to endosomes and the vacuolar membrane, in addition to previously described PAS, Golgi and Atg9-positive structures. Atg27 vacuolar membrane localization was dependent on the adaptor AP-3, which mediates direct transport from the trans-Golgi to the vacuole. The four C-terminal amino acids (YSAV) of Atg27 comprise a tyrosine sorting motif. Mutation of the YSAV abrogated Atg27 transport to the vacuolar membrane and affected its distribution in TGN/endosomal compartments, while PAS localization was normal. Also, in atg27(ΔYSAV) or AP-3 mutants, accumulation of Atg9 in the vacuolar lumen was observed upon autophagy induction. Nevertheless, PAS localization of Atg9 was normal in atg27(ΔYSAV) cells. The vacuole lumen localization of Atg9 was dependent on transport through the multivesicular body, as Atg9 accumulated in the class E compartment and vacuole membrane in atg27(ΔYSAV) vps4Δ but not in ATG27 vps4Δ cells. We suggest that Atg27 has an additional role to retain Atg9 in endosomal reservoirs that can be mobilized during autophagy. The transmembrane protein Atg27 facilitates transport of the major autophagy membrane protein, Atg9, to the preautophagosomal structure (PAS). This new study demonstrates that Atg27 has a tyrosine-sorting motif in its cytoplasmic tail that mediates its localization to the vacuole membrane by the AP-3 adaptor pathway. Moreover, this motif is also important for preventing Atg9 delivery to the vacuole lumen via the MVB pathway, suggesting that Atg27 retains Atg9 in endosomal reservoirs for mobilization during autophagy.

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