4,535
Views
36
CrossRef citations to date
0
Altmetric
Research Paper

Raft-like lipid microdomains drive autophagy initiation via AMBRA1-ERLIN1 molecular association within MAMs

, , ORCID Icon, , , , , , , , , ORCID Icon, , ORCID Icon, ORCID Icon & show all
Pages 2528-2548 | Received 20 Dec 2019, Accepted 05 Oct 2020, Published online: 23 Oct 2020

References

  • Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER- mitochondria contact sites. Nature. 2013;495:389–393.
  • Ktistakis NT, Tooze SA. Digesting the expanding mechanisms of autophagy. Trends Cell Biol. 2016;26:624–635.
  • Csordás G, Renken C, Várnai P, et al. Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol. 2006;174:915–921.
  • Tagaya M, Arasaki K. Regulation of mitochondrial dynamics and autophagy by the mitochondria- associated membrane. Adv Exp Med Biol. 2017;997:33–47.
  • Shimizu S. Organelle zones in mitochondria. J Biochem. 2019;165:1–7.
  • Rizzuto R, Pinton P, Carrington W, et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2± responses. Science. 1998;280:1763–1766.
  • Sassano ML, van Vliet AR, Agostinis P. Mitochondria-associated membranes as networking platforms and regulators of cancer cell fate. Front Oncol. 2017;7:1–16.
  • Xie Y, Kang R, Sun X, et al. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy. 2015;11:28–45.
  • Chan EY, Longatti A, McKnight NC, et al. Kinase- inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol. 2009;29:157–171.
  • Tang Z, Takahashi Y, Wang HG. ATG2 regulation of phagophore expansion at mitochondria-associated ER membranes. Autophagy. 2019;15:2165–2166.
  • Grimmel M, Backhaus C, Proikas-Cezanne T. WIPI-mediated autophagy and longevity. Cells. 2015;4:202–217.
  • Garofalo T, Matarrese P, Manganelli V, et al. Evidence for the involvement of lipid rafts localized at the ER-mitochondria associated membranes in autophagosome formation. Autophagy. 2016;12:917–935.
  • Fimia GM, Stoykova A, Romagnoli A, et al. Ambra1 regulates autophagy and development of the nervous system. Nature. 2007;447:1121–1125.
  • Nazio F, Strappazzon F, Antonioli M, et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol. 2013;15:406–416.
  • Di Rienzo M, Antonioli M, Fusco C, et al. Autophagy induction in atrophic muscle cells requires ULK1 activation by TRIM32 through unanchored K63-linked polyubiquitin chains. Sci Adv. 2019;5:eaau8857.
  • Antonioli M, Albiero F, Nazio F, et al. AMBRA1 interplay with cullin E3 ubiquitin ligases regulates autophagy dynamics. Dev Cell. 2014;31:734–746.
  • Di Bartolomeo S, Corazzari M, Nazio F, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol. 2010;191:155–168.
  • Sorice M, Longo A, Garofalo T, et al. Role of GM3 enriched microdomains in signal transduction regulation in T lymphocytes. Glycoconjugate J. 2004;20:63–70.
  • Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327:46–50.
  • Hayashi T, Fujimoto M. Detergent-resistant microdomains determine the localization of sigma-1 receptors to the endoplasmic reticulum-mitochondria junction. Mol Pharmacol. 2010;77:517–528.
  • Garofalo T, Giammarioli AM, Misasi R, et al. Lipid microdomains contribute to apoptosis-associated modifications of mitochondria in T cells. Cell Death Differ. 2005;12:1378–1389.
  • Sorice M, Garofalo T, Misasi R, et al. Ganglioside GD3 as a raft component in cell death regulation. Anticancer Agents Med Chem. 2012;12:376–382.
  • Area-Gomez E, Del Carmen Lara Castillo M, Tambini MD, et al. Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J. 2012;31:4106–4123.
  • Poston CN, Duong E, Cao Y, et al. Proteomic analysis of lipid raft-enriched membranes isolated from internal organelles. Biochem Biophys Res Commun. 2011;415:355–360.
  • Rowland AA, Voeltz GK. Endoplasmic reticulum-mito- chondria contacts: function of the junction. Nat Rev Mol Cell Biol. 2012;13:607–625.
  • Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol. 2013;14:759–774.
  • Lynes EM, Bui M, Yap MC, et al. Palmitoylated TMX and calnexin target to the mitochondria-associated membrane. EMBO J. 2012;31(2):457–470.
  • Reali V, Mehdawy B, Nardacci R, et al. Reticulon protein-1C is a key component of MAMs. Biochim Biophys Acta. 2015;1853:733–745.
  • Browman DT, Resek ME, Zajchowski LD, et al. ERLIN1 and Erlin-2 are novel members of the prohibitin family of proteins that define lipid-raft-like domains of the ER. J Cell Sci. 2006;119:3149–4160.
  • Pednekar D, Wang Y, Fedotova TV, et al. Clustered hydrophobic amino acids in amphipathic helices mediate erlin1/2 complex assembly. Biochem Biophys Res Commun. 2011;415:135–140.
  • Hoegg MB, Browman DT, Resek ME, et al. Distinct regions within the erlins are required for oligomerization and association with high molecular weight complexes. Biol Chem. 2009;284:7766–7776.
  • Wright FA, Wojcikiewicz RJ. Chapter 4—inositol 1,4,5- trisphosphate receptor ubiquitination. Prog Mol Biol Transl Sci. 2016;141:141–159.
  • Wright FA, Bonzerato CG, Sliter DA, et al. The erlin2 T65I mutation inhibits erlin1/2 complex-mediated inositol 1,4,5-trisphosphate receptor ubiquitination and phosphatidylinositol 3-phosphate binding. J Biol Chem. 2018;40:15706–15714.
  • Pearce MM, Wormer DB, Wilkens S, et al. An endoplasmic reticulum (ER) membrane complex composed of SPFH1 and SPFH2 mediates the ER- associated degradation of inositol 1,4,5-trisphosphate receptors. J Biol Chem. 2009;284:10433–10445.
  • Nijtmans LG, de Jong L, Artal Sanz M, et al. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 2000;19:2444–2451.
  • Huber MD, Vesely PW, Datta K, et al. Erlins restrict SREBP activation in the ER and regulate cellular cholesterol homeostasis. J Biol Chem. 2013;203:427–436.
  • Wang G, Zhang X, Lee JS, et al. Endoplasmic reticulum factor erlin2 regulates cytosolic lipid con- tent in cancer cells. Biochem J. 2012;446:415–425.
  • Guardia-Laguarta C, Area-Gomez E, Rüb C, et al. α-Synuclein is localized to mitochondria-associated ER membranes. J Neurosci. 2014;34:249–259.
  • de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456:605–610.
  • Cosson P, Marchetti A, Ravazzola M, et al. Mitofusin-2 independent juxtaposition of endoplasmic reticulum and mitochondria: an ultrastructural study. PLoS ONE. 2012;7:e46293.
  • McLelland GL, Fon EA. MFN2 retrotranslocation boosts mitophagy by uncoupling mitochondria from the ER. Autophagy. 2018;14:1658–1660.
  • Vettori A, Bergamin G, Moro E, et al. Developmental defects and neuromuscular alterations due to mitofusin 2 gene (MFN2) silencing in zebrafish: a new model for Charcot-Marie-Tooth type 2A neuropathy. Neuromuscul Disord. 2011;21:58–67.
  • Debattisti V, Pendin D, Ziviani E, et al. Reduction of endoplasmic reticulum stress attenuates the defects caused by Drosophila mitofusin depletion. J Cell Biol. 2014;204:303–312.
  • Antonioli M, Ciccosanti F, Dengjel J, et al. Methods to study the BECN1 interactome in the course of autophagic responses. Methods Enzymol. 2017;587:429–445.
  • Itakura E, Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy. 2010;6:764–776.
  • Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007;3:452–460.
  • Matarrese P, Garofalo T, Manganelli V, et al. Evidence for the involvement of GD3 ganglioside in autophagosome formation and maturation. Autophagy. 2014;10:750–765.
  • Levine TP, Patel S. Signalling at membrane contact sites: two membranes come together to handle second messengers. Curr Opin Cell Biol. 2016;39:77–83.
  • Betz C, Stracka D, Prescianotto-Baschong C, et al. Feature article: mTOR complex 2-Akt signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology. Proc Natl Acad Sci USA. 2013;110:12526–12534.
  • de Brito OM, Scorrano L. An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship. EMBO J. 2010;29:2715–2723.
  • Hayashi T, Rizzuto R, Hajnoczky G, et al. MAM: more than just a housekeeper. Trends Cell Biol. 2009;19:81–88.
  • Simmen T, Lynes EM, Gesson K, et al. Oxidative protein folding in the endoplasmic reticulum: tight links to the mitochondria-associated membrane (MAM). Biochim Biophys Acta. 2010;1798:1465–1473.
  • Vance JE. MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim Biophys Acta. 2014;1841:595–609.
  • Annunziata I, Sano R, d’Azzo A. Mitochondria-associated ER membranes (MAMs) and lysosomal storage diseases. Cell Death Dis. 2018;9:328.
  • Cheng X, Ma X, Ding X, et al. Pacer mediates the function of class III PI3K and HOPS complexes in autophagosome maturation by engaging Stx17. Mol Cell. 2017;65:1029:1043.e5.
  • Sano R, Annunziata I, Patterson A, et al. GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca(2+)-dependent mitochondrial apoptosis. Mol Cell. 2009;36:500–511.
  • Strappazzon F, Vietri-Rudan M, Campello S, et al. Mitochondrial BCL-2 inhibits AMBRA1-induced autophagy. EMBO J. 2011;30:1195–1208.
  • Sorice M, Matarrese P, Tinari A, et al. Raft component GD3 associates with tubulin following CD95/Fas ligation. FASEB J. 2009;23:3298–3308.
  • Sorice M, Matarrese P, Manganelli V, et al. Role of GD3-CLIPR-59 association in lymphoblastoid T cell apoptosis triggered by CD95/Fas. PLoS One. 2010;5:e8567.
  • Cebollero E, van der Vaart A, Zhao M, et al. Phosphatidylinositol-3-phosphate clearance plays a key role in autophagosome completion. Curr Biol. 2012;22:1545–1553.
  • Filadi R, Greotti E, Turacchio G, et al. Mitofusin 2 ablation increases endoplasmic reticulum-mitochondria coupling. Proc Natl Acad Sci U S A. 2015;112:E2174–E2181.
  • Ciarlo L, Vona R, Manganelli V, et al. Recruitment of mitofusin 2 into “lipid rafts” drives mitochondria fusion induced by Mdivi-1. Oncotarget. 2018;9:18869–18884.
  • Hailey DW, Rambold AS, Satpute-Krishnan P, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell. 2010;141:656–667.
  • Di Rita A, Peschiaroli A, Acunzo DP, et al. HUWE1 E3 ligase promotes PINK1/PARKIN-independent mitophagy by regulating AMBRA1 activation via IKKα. Nat Commun. 2018;9:3755.
  • Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140:313–326.
  • Wieckowski MR, Giorgi C, Lebiedzinska M, et al. Isolation of mitochondria-associated membranes and mitochondria from animal tissue and cells. Nat Protoc. 2009;4:1582–1590.
  • Stryer L. Fluorescence energy transfer as a spectroscopic ruler. Annu Rev Biochem. 1978;47:819–846.
  • Riemann D, Tcherkes A, Hansen GH, et al. Functional co-localization of monocyticaminopeptidase N/CD13 with the Fc gamma receptors CD32 and CD64. Biochem Biophys Res Commun. 2005;331:1408–1412.
  • De Leo A, Colavita F, Ciccosanti F, et al. Inhibition of autophagy in EBV-positive Burkitt’s lymphoma cells enhances EBV lytic genes expression and replication. Cell Death Dis. 2015;6:e1876.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.