Cited by 1,683

The DOI matches its Crossref record; 6 of the 6 references it cites were found in a registry or an index.

Autophagosomes form at ER–mitochondria contact sites

Hamasaki, Maho, Furuta, Nobumichi, Matsuda, Atsushi, Nezu, Akiko, Yamamoto, Akitsugu, Fujita, Naonobu, Oomori, Hiroko, Noda, Takeshi, Haraguchi, Tokuko, Hiraoka, Yasushi, Amano, Atsuo, Yoshimori, Tamotsu·2013·Nature

Abstract

Autophagy is a tightly regulated intracellular bulk degradation/recycling system that has fundamental roles in cellular homeostasis. Autophagy is initiated by isolation membranes, which form and elongate as they engulf portions of the cytoplasm and organelles. Eventually isolation membranes close to form double membrane-bound autophagosomes and fuse with lysosomes to degrade their contents. The physiological role of autophagy has been determined since its discovery, but the origin of autophagosomal membranes has remained unclear. At present, there is much controversy about the organelle from which the membranes originate--the endoplasmic reticulum (ER), mitochondria and plasma membrane. Here we show that autophagosomes form at the ER-mitochondria contact site in mammalian cells. Imaging data reveal that the pre-autophagosome/autophagosome marker ATG14 (also known as ATG14L) relocalizes to the ER-mitochondria contact site after starvation, and the autophagosome-formation marker ATG5 also localizes at the site until formation is complete. Subcellular fractionation showed that ATG14 co-fractionates in the mitochondria-associated ER membrane fraction under starvation conditions. Disruption of the ER-mitochondria contact site prevents the formation of ATG14 puncta. The ER-resident SNARE protein syntaxin 17 (STX17) binds ATG14 and recruits it to the ER-mitochondria contact site. These results provide new insight into organelle biogenesis by demonstrating that the ER-mitochondria co…

Overview

Integrity signals

Registry

Crossref · 10.1038/nature11910

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 28

  1. Mizushima, N., Yoshimori, T. & Ohsumi, Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107–132 (2011) · DOI · Paper page
  2. Tooze, S. A. & Yoshimori, T. The origin of the autophagosomal membrane. Nature Cell Biol. 12, 831–835 (2010) · DOI
  3. Vance, J. E. Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265, 7248–7256 (1990) · DOI
  4. Rizzuto, R. et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280, 1763–1766 (1998) · DOI · Paper page
  5. Hayashi, T., Rizzuto, R., Hajnoczky, G. & Su, T.-P. MAM: more than just a housekeeper. Trends Cell Biol. 19, 81–88 (2009) · DOI · Paper page
  6. Matsunaga, K. et al. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 190, 511–521 (2010) · DOI · Paper page
  7. Hayashi-Nishino, M. et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nature Cell Biol. 11, 1433–1437 (2009) · DOI
  8. Ylä-Anttila, P., Vihinen, H., Jokitalo, E. & Eskelinen, E.-L. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180–1185 (2009) · DOI
  9. Axe, E. L. et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685–701 (2008) · DOI · Paper page
  10. Hayashi, T. & Su, T.-P. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca2+ signaling and cell survival. Cell 131, 596–610 (2007) · DOI · Paper page
  11. Simmen, T. et al. PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J. 24, 717–729 (2005) · DOI
  12. Künkele, K. P. et al. The preprotein translocation channel of the outer membrane of mitochondria. Cell 93, 1009–1019 (1998) · DOI
  13. Mizushima, N. et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657–668 (2001) · DOI · Paper page
  14. Szabadkai, G. et al. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J. Cell Biol. 175, 901–911 (2006) · DOI · Paper page
  15. Hailey, D. W. et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141, 656–667 (2010) · DOI
  16. Furuta, N., Fujita, N., Noda, T., Yoshimori, T. & Amano, A. Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes. Mol. Biol. Cell 21, 1001–1010 (2010) · DOI
  17. Steegmaier, M., Oorschot, V., Klumperman, J. & Scheller, R. H. Syntaxin 17 is abundant in steroidogenic cells and implicated in smooth endoplasmic reticulum membrane dynamics. Mol. Biol. Cell 11, 2719–2731 (2000) · DOI
  18. Fujita, N. et al. An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol. Biol. Cell 19, 4651–4659 (2008) · DOI
  19. Bjørkøy, G. et al. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol. 452, 181–197 (2009) · DOI · Paper page
  20. Yamamoto, A. & Masaki, R. Pre-embedding nanogold silver and gold intensification. Methods Mol. Biol. 657, 225–235 (2010) · DOI
  21. Kageyama, S. et al. The LC3 recruitment mechanism is separate from Atg9L1-dependent membrane formation in the autophagic response against Salmonella. Mol. Biol. Cell 22, 2290–2300 (2011) · DOI · Paper page
  22. Saitoh, T. et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc. Natl Acad. Sci. USA 106, 20842–20846 (2009) · DOI · Paper page
  23. Kawai, S., Yamauchi, M., Wakisaka, S., Ooshima, T. & Amano, A. Zinc-finger transcription factor odd-skipped related 2 is one of the regulators in osteoblast proliferation and bone formation. J. Bone Miner. Res. 22, 1362–1372 (2007) · DOI
  24. Nakagawa, I. et al. Autophagy defends cells against invading group A Streptococcus. Science 306, 1037–1040 (2004) · DOI
  25. Fujita, N. et al. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19, 2092–2100 (2008) · DOI
  26. Slot, J. W. & Geuze, H. J. Cryosectioning and immunolabeling. Nature Protocols 2, 2480–2491 (2007) · DOI
  27. Griffiths, G., McDowall, A., Back, R. & Dubochet, J. On the preparation of cryosections for immunocytochemistry. J. Ultrastruct. Res. 89, 65–78 (1984) · DOI
  28. Boulanger, J., Kervrann, C. & Bouthemy, P. A simulation and estimation framework for intracellular dynamics and trafficking in video-microscopy and fluorescence imagery. Med. Image Anal. 13, 132–142 (2009) · DOI

Cited by

Sorted by citations

Metadata

Authors
Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., Amano, A., & Yoshimori, T.
Venue
Nature
Published
2013-03
Volume
495
Issue
7441
Pages
389-393
ISSN
  • 0028-0836
  • 1476-4687
Cited by
1,683
References
6
Language
en

About these checks

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.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review