Improved volume CLEM revealed that aberrant phagophores and RB1CC1/FIP200-containing clusters appear surround SQSTM1/p62 aggregates in Atg9a-deficient cells

References

• Melia TJ, Lystad AH, Simonsen A. Autophagosome biogenesis: From membrane growth to closure. J Cell Biol. 2020 Jun 1;219(6).
   PubMed Web of Science ®Google Scholar
• Nakatogawa H. Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol. 2020 Aug;21(8):439–19.
   PubMed Web of Science ®Google Scholar
• Nishimura T, Tooze SA. Emerging roles of ATG proteins and membrane lipids in autophagosome formation. Cell Discov. 2020;6(1):32.
   PubMed Web of Science ®Google Scholar
• Itakura E, Kishi-Itakura C, Koyama-Honda I, et al. Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J Cell Sci. 2012 Mar 15;125(Pt 6):1488–99.
   PubMed Web of Science ®Google Scholar
• Kakuta S, Yamaguchi J, Suzuki C, et al. Small GTPase Rab1B is associated with ATG9A vesicles and regulates autophagosome formation. FASEB J. 2017 Sep;31(9):3757–3773.
   PubMed Web of Science ®Google Scholar
• Puri C, Renna M, Bento CF, et al. ATG16L1 meets ATG9 in recycling endosomes: additional roles for the plasma membrane and endocytosis in autophagosome biogenesis. Autophagy. 2014 Jan;10(1):182–4.
   PubMed Web of Science ®Google Scholar
• Sawa-Makarska J, Baumann V, Coudevylle N, et al. Reconstitution of autophagosome nucleation defines Atg9 vesicles as seeds for membrane formation. Science. 2020 Sep 4;369(6508).
   PubMed Web of Science ®Google Scholar
• Guardia CM, Christenson ET, Zhou W, et al. The structure of human ATG9A and its interplay with the lipid bilayer. Autophagy. 2020 Dec;16(12):2292–2293.
   PubMed Web of Science ®Google Scholar
• Maeda S, Yamamoto H, Kinch LN, et al. Structure, lipid scrambling activity and role in autophagosome formation of ATG9A. Nat Struct Mol Biol. 2020 Dec;27(12):1194–1201.
   PubMed Web of Science ®Google Scholar
• Matoba K, Kotani T, Tsutsumi A, et al. Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion. Nat Struct Mol Biol. 2020 Dec;27(12):1185–1193.
   PubMed Web of Science ®Google Scholar
• Orsi A, Razi M, Dooley HC, et al. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell. 2012 May;23(10):1860–73.
   PubMed Web of Science ®Google Scholar
• Runwal G, Stamatakou E, Siddiqi FH, et al. LC3-positive structures are prominent in autophagy-deficient cells. Sci Rep. 2019 Jul 12;9(1):10147.
   PubMedGoogle Scholar
• Peddie CJ, Collinson LM. Exploring the third dimension: volume electron microscopy comes of age. Micron. 2014 Jun;61:9–19.
   PubMed Web of Science ®Google Scholar
• Miranda K, Girard-Dias W, Attias M, et al. Three dimensional reconstruction by electron microscopy in the life sciences: An introduction for cell and tissue biologists. Mol Reprod Dev. 2015 Jul-Aug;82(7–8):530–47.
   PubMed Web of Science ®Google Scholar
• Titze B, Genoud C. Volume scanning electron microscopy for imaging biological ultrastructure. Biol Cell. 2016 Nov;108(11):307–323.
   PubMed Web of Science ®Google Scholar
• Ando T BS, Brending N, Colin-York H, et al. The 2018 correlative microscopy techniques roadmap. . J Phys D Appl Phys. 2018;51(44):443001.
   PubMed Web of Science ®Google Scholar
• de Boer P, Hoogenboom JP, Giepmans BN. Correlated light and electron microscopy: ultrastructure lights up! Nat Methods. 2015 Jun;12(6):503–13.
   PubMed Web of Science ®Google Scholar
• Guerin CJ, Lippens S. Correlative light and volume electron microscopy (vCLEM): How community participation can advance developing technologies. J Microsc. 2021 Nov;284(2):97–102.
   PubMed Web of Science ®Google Scholar
• Lippens S, Jokitalo E. 3D CLEM: Correlating Volume Light and Electron Microscopy. In: Collinson L, Verkade P, eds. Correlative Imaging: Focusing on the Future. Hoboken, NJ: John Wiley & Sons Ltd.; 2019:67–79.
   Google Scholar
• Heymann JA, Hayles M, Gestmann I, et al. Site-specific 3D imaging of cells and tissues with a dual beam microscope. J Struct Biol. 2006 Jul;155(1):63–73.
   PubMed Web of Science ®Google Scholar
• Kizilyaprak C, Bittermann AG, Daraspe J, et al. FIB-SEM tomography in biology. Methods Mol Biol. 2014;1117:541–58.
   PubMedGoogle Scholar
• Zhou X, Huang L. DNA transfection mediated by cationic liposomes containing lipopolylysine: characterization and mechanism of action. Biochim Biophys Acta. 1994 Jan 19;1189(2):195–203.
   PubMed Web of Science ®Google Scholar
• Jonker C, de Heus C, Faber L, et al. An adapted protocol to overcome endosomal damage caused by polyethylenimine (PEI) mediated transfections. Matters. 2017.
   Google Scholar
• Kageyama S, Gudmundsson SR, Sou YS, et al. p62/SQSTM1-droplet serves as a platform for autophagosome formation and anti-oxidative stress response. Nat Commun. 2021 Jan 4;12(1):16.
   PubMed Web of Science ®Google Scholar
• Agudo-Canalejo J, Schultz SW, Chino H, et al. Wetting regulates autophagy of phase-separated compartments and the cytosol. Nature. 2021 Mar;591(7848):142–146.
   PubMed Web of Science ®Google Scholar
• Yamaguchi J, Suzuki C, Nanao T, et al. Atg9a deficiency causes axon-specific lesions including neuronal circuit dysgenesis. Autophagy. 2018;14(5):764–777.
   PubMed Web of Science ®Google Scholar
• Kishi-Itakura C, Koyama-Honda I, Itakura E, et al. Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells. J Cell Sci. 2014 Sep 15;127(Pt 18):4089–102.
   PubMed Web of Science ®Google Scholar
• Asano T, Komatsu M, Yamaguchi-Iwai Y, et al. Distinct mechanisms of ferritin delivery to lysosomes in iron-depleted and iron-replete cells. Mol Cell Biol. 2011 May;31(10):2040–52.
   PubMed Web of Science ®Google Scholar
• Ohnstad AE, Delgado JM, North BJ, et al. Receptor-mediated clustering of FIP200 bypasses the role of LC3 lipidation in autophagy. EMBO J. 2020 Dec 15;39(24):e104948.
   PubMed Web of Science ®Google Scholar
• Goodwin JM, Dowdle WE, DeJesus R, et al. Autophagy-Independent Lysosomal Targeting Regulated by ULK1/2-FIP200 and ATG9. Cell Rep. 2017 Sep 5;20(10):2341–2356.
   PubMed Web of Science ®Google Scholar
• Ohshima T, Yamamoto H, Sakamaki Y, et al. NCOA4 drives ferritin phase separation to facilitate macroferritinophagy and microferritinophagy. J Cell Biol. 2022 Oct 3;221(10).
   PubMedGoogle Scholar
• Karreman MA, Hyenne V, Schwab Y, et al. Intravital Correlative Microscopy: Imaging Life at the Nanoscale. Trends Cell Biol. 2016 Nov;26(11):848–863.
   PubMed Web of Science ®Google Scholar
• Thomas CI, Ryan MA, Scholl B, et al. Targeting Functionally Characterized Synaptic Architecture Using Inherent Fiducials and 3D Correlative Microscopy. Microsc Microanal. 2021 Feb;27(1):156–169.
   PubMed Web of Science ®Google Scholar
• Maco B, Holtmaat A, Cantoni M, et al. Correlative in vivo 2 photon and focused ion beam scanning electron microscopy of cortical neurons. PLoS One. 2013;8(2):e57405.
   PubMed Web of Science ®Google Scholar
• Russell MR, Lerner TR, Burden JJ, et al. 3D correlative light and electron microscopy of cultured cells using serial blockface scanning electron microscopy. J Cell Sci. 2017 Jan 1;130(1):278–291.
   PubMed Web of Science ®Google Scholar
• Kukulski W, Schorb M, Welsch S, et al. Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision. J Cell Biol. 2011 Jan 10;192(1):111–9.
   PubMed Web of Science ®Google Scholar
• Fermie J, Liv N, Ten Brink C, et al. Single organelle dynamics linked to 3D structure by correlative live-cell imaging and 3D electron microscopy. Traffic. 2018 May;19(5):354–369.
   PubMed Web of Science ®Google Scholar
• Hoffman DP, Shtengel G, Xu CS, et al. Correlative three-dimensional super-resolution and block-face electron microscopy of whole vitreously frozen cells. Science. 2020 Jan 17;367(6475).
   PubMed Web of Science ®Google Scholar
• Gudmundsson SR, Kallio KA, Vihinen H, et al. Morphology of Phagophore Precursors by Correlative Light-Electron Microscopy. Cells. 2022 Sep 30;11(19).
   PubMed Web of Science ®Google Scholar
• Olivas TJ, Wu Y, Yu S, et al. ATG9 vesicles comprise the seed membrane of mammalian autophagosomes. J Cell Biol. 2023 Jul 3;222(7).
   PubMed Web of Science ®Google Scholar
• Ghanbarpour A, Valverde DP, Melia TJ, et al. A model for a partnership of lipid transfer proteins and scramblases in membrane expansion and organelle biogenesis. Proc Natl Acad Sci U S A. 2021 Apr 20;118(16).
   PubMed Web of Science ®Google Scholar
• van Vliet AR, Chiduza GN, Maslen SL, et al. ATG9A and ATG2A form a heteromeric complex essential for autophagosome formation. Mol Cell. 2022 Nov 17;82(22):4324–4339 e8.
   PubMed Web of Science ®Google Scholar
• Yamada T, Carson AR, Caniggia I, et al. Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J Biol Chem. 2005 May 6;280(18):18283–90.
   PubMed Web of Science ®Google Scholar
• Ikeda R, Noshiro D, Morishita H, et al. Phosphorylation of phase-separated p62 bodies by ULK1 activates a redox-independent stress response. EMBO J. 2023 Jun 12:e113349.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Ueno T, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005 May 9;169(3):425–34.
   PubMed Web of Science ®Google Scholar
• Saitoh T, Fujita N, Hayashi T, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20842–6.
   PubMed Web of Science ®Google Scholar
• Nanao T, Koike M, Yamaguchi J, et al. Cellular localization and tissue distribution of endogenous DFCP1 protein. Biomed Res. 2015;36(2):121–33.
   PubMed Web of Science ®Google Scholar