Retromer Ensures the Degradation of Autophagic Cargo by Maintaining Lysosome Function in Drosophila

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Volumn 16, Issue 10, 2015, Pages 1088-1107

  Maruzs, Tamás ^a,b   Lorincz, Péter ^a   Szatmári, Zsuzsanna ^a   Széplaki, Szilvia ^a   Sándor, Zoltán ^a   Lakatos, Zsolt ^a   Puska, Gina ^a   Juhász, Gábor ^a,b   Sass, Miklós ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Autophagy; Drosophila; Endocytosis; Lysosomal storage diseases; Lysosome; Retromer

Indexed keywords

DIMER; RETROMER; UNCLASSIFIED DRUG; CARRIER PROTEIN; SORTING NEXIN; VESICULAR TRANSPORT PROTEIN;

ADIPOCYTE; AMPHISOME; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL VACUOLE; CYTOPLASM; FAT BODY; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; TRANS GOLGI NETWORK;

ANIMALS; AUTOPHAGY; CARRIER PROTEINS; CYTOPLASM; DROSOPHILA; ENDOCYTOSIS; ENDOSOMES; FAT BODY; LYSOSOMES; PROTEIN TRANSPORT; SORTING NEXINS; TRANS-GOLGI NETWORK; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 84941600807     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12309     Document Type: Article

References (75)

1. Klionsky DJ, Codogno P. The mechanism and physiological function of macroautophagy. J Innate Immun 2013;5:427-433.
2. Lamb CA, Dooley HC, Tooze SA. Endocytosis and autophagy: shared machinery for degradation. BioEssays 2013;35:34-45.
3. Hsu VW, Bai M, Li J. Getting active: protein sorting in endocytic recycling. Nat Rev Mol Cell Biol 2012;13:323-328.
4. Gordon PB, Seglen PO. Prelysosomal convergence of autophagic and endocytic pathways. Biochem Biophys Res Commun 1988;151:40-47.
5. Fader CM, Colombo MI. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 2009;16:70-78.
6. Maxfield FR. Role of endosomes and lysosomes in human disease. Cold Spring Harb Perspect Biol 2014;6:a016931.
7. Seaman MN. The retromer complex - endosomal protein recycling and beyond. J Cell Sci 2012;125:4693-4702.
8. Seaman MN, McCaffery JM, Emr SD. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol 1998;142:665-681.
9. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJG, Evans PR, McMahon HT. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 2004;303:495-499.
10. Koumandou VL, Klute MJ, Herman EK, Nunez-Miguel R, Dacks JB, Field MC. Evolutionary reconstruction of the retromer complex and its function in Trypanosoma brucei. J Cell Sci 2011;124:1496-1509.
11. Cullen PJ. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 2008;9:574-582.
12. Knævelsrud H, Søreng K, Raiborg C, Håberg K, Rasmuson F, Brech A, Liestøl K, Rusten TE, Stenmark H, Neufeld TP, Carlsson SR, Simonsen A. Membrane remodeling by the PX-BAR protein SNX18 promotes autophagosome formation. J Cell Biol 2013;202:331-349.
13. Rojas R, Kametaka S, Haft CR, Bonifacino JS. Interchangeable but essential functions of SNX1 and SNX2 in the association of retromer with endosomes and the trafficking of mannose 6-phosphate receptors. Mol Cell Biol 2007;27:1112-1124.
14. Wassmer T, Attar N, Bujny MV, Oakley J, Traer CJ, Cullen PJ. A loss-of-function screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J Cell Sci 2007;120:45-54.
15. Wassmer T, Attar N, Harterink M, van Weering JR, Traer CJ, Oakley J, Goud B, Stephens DJ, Verkade P, Korswagen HC, Cullen PJ. The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network. Dev Cell 2009;17:110-122.
16. Cullen PJ, Korswagen HC. Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 2012;14:29-37.
17. Zhang P, Wu Y, Belenkaya TY, Lin X. SNX3 controls Wingless/Wnt secretion through regulating retromer-dependent recycling of Wntless. Cell Res 2011;21:1677-1690.
18. Harterink M, Port F, Lorenowicz MJ, McGough IJ, Silhankova M, Betist MC, van Weering JR, van Heesbeen RG, Middelkoop TC, Basler K, Cullen PJ, Korswagen HC. A SNX3-dependent retromer pathway mediates retrograde transport of the Wnt sorting receptor Wntless and is required for Wnt secretion. Nat Cell Biol 2011;13:914-923.
19. Temkin P, Lauffer B, Jäger S, Cimermancic P, Krogan NJ, von Zastrow M. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 2011;13:715-721.
20. Arighi CN, Hartnell LM, Aguilar RC, Haft CR, Bonifacino JS. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J Cell Biol 2004;165:123-133.
21. Bonifacino JS. The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 2004;5:23-32.
22. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the β2-adrenergic receptor. Nature 1999;401:286-290.
23. Franch-Marro X, Wendler F, Guidato S, Griffith J, Baena-Lopez A, Itasaki N, Maurice MM, Vincent JP. Wingless secretion requires endosome-to-Golgi retrieval of Wntless/Evi/Sprinter by the retromer complex. Nat Cell Biol 2008;10:170-177.
24. Pocha SM, Wassmer T, Niehage C, Hoflack B, Knust E. Retromer controls epithelial cell polarity by trafficking the apical determinant Crumbs. Curr Biol 2011;21:1111-1117.
25. Steinberg F, Gallon M, Winfield M, Thomas EC, Bell AJ, Heesom KJ, Tavaré JM, Cullen PJ. A global analysis of SNX27-retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat Cell Biol 2013;15:461-471.
26. Korolchuk VI, Schutz MM, Gomez-Llorente C, Rocha J, Lansu NR, Collins SM, Wairkar YP, Robinson IM, O'Kane CJ. Drosophila Vps35 function is necessary for normal endocytic trafficking and actin cytoskeleton organisation. J Cell Sci 2007;120:4367-4376.
27. Zavodszky E, Seaman MN, Moreau K, Jimenez-Sanchez M, Breusegem SY, Harbour ME, Rubinsztein DC. Mutation in VPS35 associated with Parkinson's disease impairs WASH complex association and inhibits autophagy. Nat Commun 2014;5:3828.
28. Wen L, Tang FL, Hong Y, Luo SW, Wang CL, He W, Shen C, Jung JU, Xiong F, Lee DH, Zhang QG, Brann D, Kim TW, Yan R, Mei L, et al. VPS35 haploinsufficiency increases Alzheimer's disease neuropathology. J Cell Biol 2011;195:765-779.
29. Zimprich A, Benet-Pages A, Struhal W, Graf E, Eck SH, Offman MN, Haubenberger D, Spielberger S, Schulte EC, Lichtner P, Rossle SC, Klopp N, Wolf E, Seppi K, Pirker W, et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am J Hum Genet 2011;89:168-175.
30. Mamo A, Jules F, Dumaresq-Doiron K, Costantino S, Lefrancois S. The role of ceroid lipofuscinosis neuronal protein 5 (CLN5) in endosomal sorting. Mol Cell Biol 2012;32:1855-1866.
31. Burgess J, Del Bel LM, Ma CI, Barylko B, Polevoy G, Rollins J, Albanesi JP, Kramer H, Brill JA. Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. Development 2012;139:3040-3050.
32. Wang S, Tan KL, Agosto MA, Xiong B, Yamamoto S, Sandoval H, Jaiswal M, Bayat V, Zhang K, Charng WL, David G, Duraine L, Venkatachalam K, Wensel TG, Bellen HJ. The retromer complex is required for rhodopsin recycling and its loss leads to photoreceptor degeneration. PLoS Biol 2014;12:e1001847.
33. Rojas R, van Vlijmen T, Mardones GA, Prabhu Y, Rojas AL, Mohammed S, Heck AJ, Raposo G, van Der Sluijs P, Bonifacino JS. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 2008;183:513-526.
34. van Weering JR, Verkade P, Cullen PJ. SNX-BAR-Mediated Endosome Tubulation is Co-ordinated with Endosome Maturation. Traffic 2012;13:94-107.
35. Nagy P, Varga Á, Kovács AL, Takáts S, Juhász G. How and why to study autophagy in Drosophila: It's more than just a garbage chute. Methods 2015;75:151-161.
36. Nezis IP, Lamark T, Velentzas AD, Rusten TE, Bjørkøy G, Johansen T, Papassideri IS, Stravopodis DJ, Margaritis LH, Stenmark H. Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 2009;5:298-302.
37. Chang YY, Neufeld TP. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell 2009;20:2004-2014.
38. Nezis IP, Shravage BV, Sagona AP, Lamark T, Bjorkoy G, Johansen T, Rusten TE, Brech A, Baehrecke EH, Stenmark H. Autophagic degradation of dBruce controls DNA fragmentation in nurse cells during late Drosophila melanogaster oogenesis. J Cell Biol 2010;190:523-531.
39. 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.
40. Rusten TE, Lindmo K, Juhasz G, Sass M, Seglen PO, Brech A, Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell 2004;7:179-192.
41. Drosophila Ashburner M. A Laboratory Handbook. Cold Spring Harbor Laboratory Press; 1989.
42. Zhou B, Yun EY, Ray L, You J, Ip YT, Lin X. Retromer promotes immune quiescence by suppressing Spatzle-Toll pathway in Drosophila. J Cell Physiol 2014;229:512-520.
43. Dennes A, Cromme C, Suresh K, Kumar NS, Eble JA, Hahnenkamp A, Pohlmann R. The novel Drosophila lysosomal enzyme receptor protein mediates lysosomal sorting in mammalian cells and binds mammalian and Drosophila GGA adaptors. J Biol Chem 2005;280:12849-12857.
44. Hirst J, Sahlender DA, Choma M, Sinka R, Harbour ME, Parkinson M, Robinson MS. Spatial and functional relationship of GGAs and AP-1 in Drosophila and HeLa cells. Traffic 2009;10:1696-1710.
45. Eissenberg JC, Ilvarsonn AM, Sly WS, Waheed A, Krzyzanek V, Pohlmann R, Waschkau D, Kretzschmar D, Dennes AC. Drosophila GGA model: an ultimate gateway to GGA analysis. Traffic 2011;12:1821-1838.
46. Duvvuri M, Gong Y, Chatterji D, Krise JP. Weak base permeability characteristics influence the intracellular sequestration site in the multidrug-resistant human leukemic cell line HL-60. J Biol Chem 2004;279:32367-32372.
47. Kneen M, Farinas J, Li Y, Verkman A. Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys J 1998;74:1591-1599.
48. Finnigan GC, Hanson-Smith V, Houser BD, Park HJ, Stevens TH. The reconstructed ancestral subunit a functions as both V-ATPase isoforms Vph1p and Stv1p in Saccharomyces cerevisiae. Mol Biol Cell 2011;22:3176-3191.
49. Carnell M, Zech T, Calaminus SD, Ura S, Hagedorn M, Johnston SA, May RC, Soldati T, Machesky LM, Insall RH. Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis. J Cell Biol 2011;193:831-839.
50. Helfer E, Harbour ME, Henriot V, Lakisic G, Sousa-Blin C, Volceanov L, Seaman MN, Gautreau A. Endosomal recruitment of the WASH complex: active sequences and mutations impairing interaction with the retromer. Biol Cell 2013;105:191-207.
51. Figura Kv, Hasilik A. Lysosomal enzymes and their receptors. Annu Rev Biochem 1986;55:167-193.
52. Reczek D, Schwake M, Schroder J, Hughes H, Blanz J, Jin X, Brondyk W, Van Patten S, Edmunds T, Saftig P. LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell 2007;131:770-783.
53. Seaman MN. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J Cell Sci 2007;120:2378-2389.
54. Xu Y, Hortsman H, Seet L, Wong SH, Hong W. SNX3 regulates endosomal function through its PX-domain-mediated interaction with PtdIns (3) P. Nat Cell Biol 2001;3:658-666.
55. Takats S, Nagy P, Varga A, Pircs K, Karpati M, Varga K, Kovacs AL, Hegedus K, Juhasz G. Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. J Cell Biol 2013;201:531-539.
56. Takats S, Pircs K, Nagy P, Varga A, Karpati M, Hegedus K, Kramer H, Kovacs AL, Sass M, Juhasz G. Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Mol Biol Cell 2014;25:1338-1354.
57. Szatmari Z, Kis V, Lippai M, Hegedus K, Farago T, Lorincz P, Tanaka T, Juhasz G, Sass M. Rab11 facilitates cross-talk between autophagy and endosomal pathway through regulation of Hook localization. Mol Biol Cell 2014;25:522-531.
58. Rusten TE, Vaccari T, Lindmo K, Rodahl LM, Nezis IP, Sem-Jacobsen C, Wendler F, Vincent JP, Brech A, Bilder D, Stenmark H. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 2007;17:1817-1825.
59. Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerod L, Fisher EM, Isaacs A, Brech A, Stenmark H, Simonsen A. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 2007;179:485-500.
60. Lorincz P, Lakatos Z, Maruzs T, Szatmári Z, Kis V, Sass M. Atg6/UVRAG/Vps34-containing lipid kinase complex is required for receptor downregulation through endolysosomal degradation and epithelial polarity during Drosophila wing development. BioMed Res Int 2014;2014:851349.
61. Renna M, Schaffner C, Winslow AR, Menzies FM, Peden AA, Floto RA, Rubinsztein DC. Autophagic substrate clearance requires activity of the syntaxin-5 SNARE complex. J Cell Sci 2011;124:469-482.
62. Muhammad A, Flores I, Zhang H, Yu R, Staniszewski A, Planel E, Herman M, Ho L, Kreber R, Honig LS, Ganetzky B, Duff K, Arancio O, Small SA. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Proc Natl Acad Sci USA 2008;105:7327-7332.
63. Sevlever D, Jiang P, Yen SH. Cathepsin D is the main lysosomal enzyme involved in the degradation of alpha-synuclein and generation of its carboxy-terminally truncated species. Biochemistry 2008;47:9678-9687.
64. Follett J, Norwood SJ, Hamilton NA, Mohan M, Kovtun O, Tay S, Zhe Y, Wood SA, Mellick GD, Silburn PA, Collins BM, Bugarcic A, Teasdale RD. The Vps35 D620N mutation linked to Parkinson's disease disrupts the cargo sorting function of retromer. Traffic 2014;15:230-244.
65. McGough IJ, Steinberg F, Jia D, Barbuti PA, McMillan KJ, Heesom KJ, Whone AL, Caldwell MA, Billadeau DD, Rosen MK. Retromer binding to FAM21 and the WASH complex is perturbed by the Parkinson disease-linked VPS35 (D620N) mutation. Curr Biol 2014;24:1670-1676.
66. Munsie L, Milnerwood A, Seibler P, Beccano-Kelly D, Tatarnikov I, Khinda J, Volta M, Kadgien C, Cao L, Tapia L. Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson's disease VPS35 mutation p. D620N. Hum Mol Genet 2015;24:1691-1703.
67. Wang H-s, Toh J, Ho P, Tio M, Zhao Y, Tan E-K. In vivo evidence of pathogenicity of VPS35 mutations in the Drosophila. Mol Brain 2014;7:73.
68. Tsika E, Glauser L, Moser R, Fiser A, Daniel G, Sheerin U-M, Lees A, Troncoso JC, Lewis PA, Bandopadhyay R. Parkinson's disease-linked mutations in VPS35 induce dopaminergic neurodegeneration. Hum Mol Genet 2014;23:4621-4638.
69. Platt FM, Boland B, van der Spoel AC. The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 2012;199:723-734.
70. Cao Y, Espinola JA, Fossale E, Massey AC, Cuervo AM, MacDonald ME, Cotman SL. Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J Biol Chem 2006;281:20483-20493.
71. Lieberman AP, Puertollano R, Raben N, Slaugenhaupt S, Walkley SU, Ballabio A. Autophagy in lysosomal storage disorders. Autophagy 2012;8:719-730.
72. Marois E, Mahmoud A, Eaton S. The endocytic pathway and formation of the Wingless morphogen gradient. Development 2006;133:307-317.
73. Juhász G, Hill JH, Yan Y, Sass M, Baehrecke EH, Backer JM, Neufeld TP. The class III PI (3) K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 2008;181:655-666.
74. Nagy P, Varga Á, Pircs K, Hegedus K, Juhász G. Myc-driven overgrowth requires unfolded protein response-mediated induction of autophagy and antioxidant responses in Drosophila melanogaster. PLoS Genet 2013;9:e1003664.
75. Sinka R, Gillingham AK, Kondylis V, Munro S. Golgi coiled-coil proteins contain multiple binding sites for Rab family G proteins. J Cell Biol 2008;183:607-615.