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Mitochondria Supply Membranes for Autophagosome Biogenesis during Starvation

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Hailey, Dale W., Rambold, Angelika S., Satpute-Krishnan, Prasanna, Mitra, Kasturi, Sougrat, Rachid, Kim, Peter K., Lippincott-Schwartz, Jennifer·2010·Cell

Abstract

Starvation-induced autophagosomes engulf cytosol and/or organelles and deliver them to lysosomes for degradation, thereby re-supplying depleted nutrients. Despite advances in understanding the molecular basis of this process, the membrane origin of autophagosomes remains unclear. Here, we demonstrate that, in starved cells, autophagosomes are derived from the outer membranes of mitochondria. In time-lapse movies, the early autophagosomal marker, mApg5, transiently localizes to punctae on the surface of mitochondria, followed by the late autophagosomal marker, LC3. A unique tail-anchored outer mitochondrial membrane protein, but not other outer nor inner mitochondrial membrane proteins, labels autophagosomes and diffuses into newly forming autophagosomes from mitochondria. The fluorescent lipid, NBD-PS (which converts to PE in mitochondria) transfers from mitochondria to autophagosomes in starved cells. In addition, when mitochondria/ER connections are perturbed by loss of mitofusin2, starvation-induced autophagosomes do not form. Mitochondria thus play a central role in starvation-induced autophagy, serving as membrane source of autophagosomes.

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Show all 9 references

Research works printed but not linked: 50

  1. Achleitner, 1999, Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact, Eur. J. Biochem., 264, 545, 10.1046/j.1432-1327.1999.00658.x · DOI · Paper page
  2. Axe, 2008, Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum, J. Cell Biol., 182, 685, 10.1083/jcb.200803137 · DOI · Paper page
  3. Bernales, 2006, Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response, PLoS Biol., 4, e423, 10.1371/journal.pbio.0040423 · DOI · Paper page
  4. Bjorkoy, 2005, p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death, J. Cell Biol., 171, 603, 10.1083/jcb.200507002 · DOI · Paper page
  5. Borgese, 2001, Targeting of a tail-anchored protein to endoplasmic reticulum and mitochondrial outer membrane by independent but competing pathways, Mol. Biol. Cell, 12, 2482, 10.1091/mbc.12.8.2482 · DOI
  6. Bozidis, 2008, Mitochondrial and secretory human cytomegalovirus UL37 proteins traffic into mitochondrion-associated membranes of human cells, J. Virol., 82, 2715, 10.1128/JVI.02456-07 · DOI
  7. Colell, 2007, GAPDH and autophagy preserve survival after apoptotic cytochrome c release in the absence of caspase activation, Cell, 129, 983, 10.1016/j.cell.2007.03.045 · DOI · Paper page
  8. D'Arrigo, 1993, The specific subcellular localization of two isoforms of cytochrome b5 suggests novel targeting pathways, J. Biol. Chem., 268, 2802, 10.1016/S0021-9258(18)53844-8 · doi:10.1016/s0021-9258(18)53844-8
  9. Doelling, 2002, The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana, J. Biol. Chem., 277, 33105, 10.1074/jbc.M204630200 · DOI · Paper page
  10. Furuya, 2005, The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function, Autophagy, 1, 46, 10.4161/auto.1.1.1542 · DOI · Paper page
  11. Hailey, 2009, Using photoactivatable proteins to monitor autophagysome lifetime, Methods Enzymol., 452, 25, 10.1016/S0076-6879(08)03603-3 · DOI
  12. Hayashi-Nishino, 2009, A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation, Nat. Cell Biol., 12, 1433, 10.1038/ncb1991 · DOI · Paper page
  13. Hoyvik, 1991, Inhibition of autophagic-lysosomal delivery and autophagic lactolysis by asparagine, J. Cell Biol., 113, 1305, 10.1083/jcb.113.6.1305 · DOI
  14. Juhasz, 2006, Autophagy: a forty-year search for a missing membrane source, PLoS Biol., 4, e36, 10.1371/journal.pbio.0040036 · DOI
  15. Kobayashi, 1991, Transport of exogenous fluorescent phosphatidylserine analogue to the Golgi apparatus in cultured fibroblasts, J. Cell Biol., 113, 235, 10.1083/jcb.113.2.235 · DOI
  16. Kuma, 2002, Formation of the approximately 350-kDa Apg12-Apg5.Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast, J. Biol. Chem., 277, 18619, 10.1074/jbc.M111889200 · DOI · Paper page
  17. Lederer, 1983, Two homologous cytochromes b5 in a single cell, Eur. J. Biochem., 132, 95, 10.1111/j.1432-1033.1983.tb07330.x · doi:10.1111/j.1432-1033.1983.tb07330.x
  18. Lee, 2008, A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy, Proc. Natl. Acad. Sci. USA, 105, 3374, 10.1073/pnas.0712145105 · DOI · Paper page
  19. Lorenz, 2006, Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization, Nat. Methods, 3, 205, 10.1038/nmeth857 · DOI
  20. Mijaljica, 2007, Different fates of mitochondria: alternative ways for degradation?, Autophagy, 3, 4, 10.4161/auto.3011 · DOI
  21. Mizushima, 2001, Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells, J. Cell Biol., 152, 657, 10.1083/jcb.152.4.657 · DOI · Paper page
  22. Mizushima, 2004, In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker, Mol. Biol. Cell, 15, 1101, 10.1091/mbc.e03-09-0704 · DOI · Paper page
  23. Nakatogawa, 2007, Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion, Cell, 130, 165, 10.1016/j.cell.2007.05.021 · DOI · Paper page
  24. Neuspiel, 2008, Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers, Curr. Biol., 18, 102, 10.1016/j.cub.2007.12.038 · DOI · Paper page
  25. Ogata, 2006, Autophagy is activated for cell survival after endoplasmic reticulum stress, Mol. Cell Biol., 26, 9220, 10.1128/MCB.01453-06 · DOI · Paper page
  26. Overbye, 2007, Proteomic analysis of membrane-associated proteins from rat liver autophagosomes, Autophagy, 3, 300, 10.4161/auto.3910 · DOI · Paper page
  27. Patterson, 2002, A photoactivatable GFP for selective photolabeling of proteins and cells, Science, 297, 1873, 10.1126/science.1074952 · DOI · Paper page
  28. Petiot, 2000, Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells, J. Biol. Chem., 275, 992, 10.1074/jbc.275.2.992 · DOI · Paper page
  29. Petit, 1992, 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria, Eur. J. Biochem., 209, 267, 10.1111/j.1432-1033.1992.tb17285.x · DOI · Paper page
  30. Reef, 2006, A short mitochondrial form of p19ARF induces autophagy and caspase-independent cell death, Mol. Cell, 22, 463, 10.1016/j.molcel.2006.04.014 · DOI
  31. Reggiori, 2009, The EmERgence of autophagosomes, Dev. Cell, 17, 747, 10.1016/j.devcel.2009.12.004 · DOI
  32. Sakaki, 2008, Protein kinase Ctheta is required for autophagy in response to stress in the endoplasmic reticulum, J. Biol. Chem., 283, 15370, 10.1074/jbc.M710209200 · DOI · Paper page
  33. Schmidt, 2004, A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells, Curr. Biol., 14, 1002, 10.1016/j.cub.2004.05.044 · DOI
  34. Scott, 1996, Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole, Proc. Natl. Acad. Sci. USA, 93, 12304, 10.1073/pnas.93.22.12304 · DOI · Paper page
  35. Sneve, 2005, Comigration of two autophagosome-associated dehydrogenases on two-dimensional polyacrylamide gels, Autophagy, 1, 157, 10.4161/auto.1.3.2037 · doi:10.4161/auto.1.3.2037
  36. Tadini-Buoninsegni, 2008, Effects of high-affinity inhibitors on partial reactions, charge movements, and conformational States of the Ca2+ transport ATPase (sarco-endoplasmic reticulum Ca2+ ATPase), Mol. Pharmacol., 73, 1134, 10.1124/mol.107.043745 · doi:10.1124/mol.107.043745
  37. Takagaki, 1983, The membrane-embedded segment of cytochrome b5 as studied by cross-linking with photoactivatable phospholipids, J. Biol. Chem., 258, 9128, 10.1016/S0021-9258(17)44640-0 · doi:10.1016/s0021-9258(17)44640-0
  38. Takahashi, 2007, Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis, Nat. Cell Biol., 9, 1142, 10.1038/ncb1634 · DOI · Paper page
  39. Takahashi, 2007, Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis, Nat. Cell Biol., 9, 1142, 10.1038/ncb1634 · DOI · Paper page
  40. Tasdemir, 2008, Methods for assessing autophagy and autophagic cell death, Methods Mol. Biol., 445, 29, 10.1007/978-1-59745-157-4_3 · DOI · Paper page
  41. Thomas, 1989, Curvature and composition-dependent lipid asymmetry in phosphatidylcholine vesicles containing phosphatidylethanolamine and gangliosides, Biochim. Biophys. Acta, 978, 85, 10.1016/0005-2736(89)90502-6 · doi:10.1016/0005-2736(89)90502-6
  42. Tsukada, 1993, Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae, FEBS Lett., 333, 169, 10.1016/0014-5793(93)80398-E · DOI · Paper page
  43. van Meer, 2008, Membrane lipids: where they are and how they behave, Nat. Rev. Mol. Cell Biol., 9, 112, 10.1038/nrm2330 · DOI · Paper page
  44. Vance, 2008, Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids, J. Lipid Res., 49, 1377, 10.1194/jlr.R700020-JLR200 · DOI · Paper page
  45. Vance, 2004, Phospholipid biosynthesis in mammalian cells, Biochem. Cell Biol., 82, 113, 10.1139/o03-073 · DOI · Paper page
  46. Vergeres, 1995, Cytochrome b5, its functions, structure and membrane topology, Biochimie, 77, 604, 10.1016/0300-9084(96)88176-4 · DOI
  47. Xie, 2007, Autophagosome formation: core machinery and adaptations, Nat. Cell Biol., 9, 1102, 10.1038/ncb1007-1102 · DOI · Paper page
  48. Ylä-Anttila, 2009, 3D tomotgraphy redeals connections between the phagophore and endoplasmic reticulum, Autophagy, 5, 1180, 10.4161/auto.5.8.10274 · DOI · Paper page
  49. Young, 2006, Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes, J. Cell Sci., 119, 3888, 10.1242/jcs.03172 · DOI · Paper page
  50. Yousefi, 2006, Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis, Nat. Cell Biol., 8, 1124, 10.1038/ncb1482 · DOI · Paper page

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Metadata

Authors
Hailey, D. W., Rambold, A. S., Satpute-Krishnan, P., Mitra, K., Sougrat, R., Kim, P. K., & Lippincott-Schwartz, J.
Venue
Cell
Publisher
Elsevier BV
Published
2010-05
Volume
141
Issue
4
Pages
656-667
ISSN
0092-8674 (ISSN-L)
OpenAlex
W2132763961
Cited by
1,429
References
9
FWCI
88.69
Type
journal article
Language
en
Open access
bronze
Licence

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CoChat. (2026). Citation check: Mitochondria Supply Membranes for Autophagosome Biogenesis during Starvation. https://app.cochat.ai/papers/10.1016/j.cell.2010.04.009
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Hailey, D. W., Rambold, A. S., Satpute-Krishnan, P., Mitra, K., Sougrat, R., Kim, P. K., & Lippincott-Schwartz, J. (2010). Mitochondria Supply Membranes for Autophagosome Biogenesis during Starvation. Cell. https://doi.org/10.1016/j.cell.2010.04.009

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