The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy

Molecular Biology of the Cell

Volumn 27, Issue 20, 2016, Pages 3132-3142

  Hegedus, Krisztina ^a   Takats, Szabolcs ^a   Boda, Attila ^a   Jipa, Andras ^b   Nagy, Péter ^a   Varga, Kata ^b   Kovacs, Attila L ^a   Juhasz, Gabor ^a,b  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CCZ1 PROTEIN; CELL PROTEIN; MON1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; CCZ1 PROTEIN, S CEREVISIAE; DROSOPHILA PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MON1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN;

ADIPOCYTE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL FUSION; CELL MUTANT; CONTROLLED STUDY; DROSOPHILA; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; STARVATION; ANIMAL; CELL VACUOLE; ENDOSOME; METABOLISM; PHAGOSOME; PHYSIOLOGY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

ANIMALS; AUTOPHAGY; DROSOPHILA; DROSOPHILA PROTEINS; ENDOSOMES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; LYSOSOMES; PHAGOSOMES; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 84992060946     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E16-03-0205     Document Type: Article

References (54)

1. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000). Rab7: a key to lysosome biogenesis. Mol Biol Cell 11, 467-480.
2. Cabrera M, Nordmann M, Perz A, Schmedt D, Gerondopoulos A, Barr F, Piehler J, Engelbrecht-Vandre S, Ungermann C (2014). The Mon1-Ccz1 GEF activates the Rab7 GTPase Ypt7 via a longin-fold-Rab interface and association with PI3P-positive membranes. J Cell Sci 127, 1043-1051.
3. Chang YY, Neufeld TP (2009). An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell 20, 2004-2014.
4. Chen Y, Zhou F, Zou S, Yu S, Li S, Li D, Song J, Li H, He Z, Hu B, et al. (2014). A Vps21 endocytic module regulates autophagy. Mol Biol Cell 25, 3166-3177.
5. Cherry S, Jin EJ, Ozel MN, Lu Z, Agi E, Wang D, Jung WH, Epstein D, Mein-ertzhagen IA, Chan CC, et al. (2013). Charcot-Marie-Tooth 2B mutations in rab7 cause dosage-dependent neurodegeneration due to partial loss of function. Elife 2, e01064.
6. Cui Y, Zhao Q, Gao C, Ding Y, Zeng Y, Ueda T, Nakano A, Jiang L (2014). Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-vacuole traffcking and plant growth in Arabidopsis. Plant Cell 26, 2080-2097.
7. Diao J, Liu R, Rong Y, Zhao M, Zhang J, Lai Y, Zhou Q, Wilz LM, Li J, Vivona S, et al. (2015). ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature 520, 563-566.
8. Dilcher M, Kohler B, von Mollard GF (2001). Genetic interactions with the yeast Q-SNARE VTI1 reveal novel functions for the R-SNARE YKT6. J Biol Chem 276, 34537-34544.
9. Dooley HC, Razi M, Polson HE, Girardin SE, Wilson MI, Tooze SA (2014). WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell 55, 238-252.
10. Fader CM, Colombo MI (2009). Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16, 70-78.
11. Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerod L, Fisher EM, Isaacs A, Brech A, Stenmark H, Simonsen A (2007). Functional multivesic-ular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 179, 485-500.
12. Gerondopoulos A, Langemeyer L, Liang JR, Linford A, Barr FA (2012). BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr Biol 22, 2135-2139.
13. Gutierrez MG, Munafo DB, Beron W, Colombo MI (2004). Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117, 2687-2697.
14. Hennig KM, Colombani J, Neufeld TP (2006). TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. J Cell Biol 173, 963-974.
15. Hickey CM, Stroupe C, Wickner W (2009). The major role of the Rab Ypt7p in vacuole fusion is supporting HOPS membrane association. J Biol Chem 284, 16118-16125.
16. Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, Yoshimori T, Noda T, Ohsumi Y (2001). Autophagosome requires specifc early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 12, 3690-3702.
17. Itakura E, Kishi C, Inoue K, Mizushima N (2008). Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19, 5360-5372.
18. Itakura E, Kishi-Itakura C, Mizushima N (2012). The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 151, 1256-1269.
19. Jiang P, Nishimura T, Sakamaki Y, Itakura E, Hatta T, Natsume T, Mizushima N (2014). The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol Biol Cell 25, 1327-1337.
20. Juhasz G, Hill JH, Yan Y, Sass M, Baehrecke EH, Backer JM, Neufeld TP (2008). The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 181, 655-666.
21. Kim J, Dalton VM, Eggerton K P, Scott SV, Klionsky DJ (1999). Apg7p/Cvt2p is required for the cytoplasm-to-vacuole targeting, macroautophagy, and peroxisome degradation pathways. Mol Biol Cell 10, 1337-1351.
22. Kondo S, Ueda R (2013). Highly improved gene targeting by germline-specifc Cas9 expression in Drosophila. Genetics 195, 715-721.
23. Kucharczyk R, Kierzek AM, Slonimski P P, Rytka J (2001). The Ccz1 protein interacts with Ypt7 GTPase during fusion of multiple transport intermediates with the vacuole in S. cerevisiae. J Cell Sci 114, 3137-3145.
24. Lee G, Liang C, Park G, Jang C, Jung JU, Chung J (2011). UVRAG is re-quired for organ rotation by regulating Notch endocytosis in Drosophila. Dev Biol 356, 588-597.
25. Liang C, Feng P, Ku B, Dotan I, Canaani D, Oh BH, Jung JU (2006). Autoph-agic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 8, 688-699.
26. Lindmo K, Stenmark H (2006). Regulation of membrane traffc by phos-phoinositide 3-kinases. J Cell Sci 119, 605-614.
27. Lu H, Bilder D (2005). Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol 7, 1232-1239.
28. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, Maejima I, Shirahama-Noda K, Ichimura T, Isobe T, et al. (2009). Two Beclin 1-bind-ing proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 11, 385-396.
29. Mauvezin C, Ayala C, Braden CR, Kim J, Neufeld TP (2014). Assays to monitor autophagy in Drosophila. Methods 68, 134-139.
30. Mauvezin C, Nagy P, Juhasz G, Neufeld TP (2015). Autophagosome-lysosome fusion is independent of V-ATPase-mediated acidifcation. Nat Commun 6, 7007.
31. McEwan DG, Popovic D, Gubas A, Terawaki S, Suzuki H, Stadel D, Coxon F P, Miranda de Stegmann D, Bhogaraju S, Maddi K, et al. (2015). PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins. Mol Cell 57, 39-54.
32. Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008). Autophagy fghts disease through cellular self-digestion. Nature 451, 1069-1075.
33. Nagy P, Varga A, Kovacs AL, Takats S, Juhasz G (2015). How and why to study autophagy in Drosophila: it's more than just a garbage chute. Methods 75, 151-161.
34. Nezis I P, Simonsen A, Sagona AP, Finley K, Gaumer S, Contamine D, Rusten TE, Stenmark H, Brech A (2008). Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. J Cell Biol 180, 1065-1071.
35. Nordmann M, Cabrera M, Perz A, Brocker C, Ostrowicz C, Engelbrecht-Vandre S, Ungermann C (2010). The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 20, 1654-1659.
36. Obara K, Sekito T, Ohsumi Y (2006). Assortment of phosphatidylinositol 3-kinase complexes-Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae. Mol Biol Cell 17, 1527-1539.
37. Ohashi Y, Munro S (2010). Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol Biol Cell 21, 3998-4008.
38. Pereira-Leal JB, Seabra MC (2001). Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313, 889-901.
39. Pircs K, Nagy P, Varga A, Venkei Z, Erdi B, Hegedus K, Juhasz G (2012). Advantages and limitations of different p62-based assays for estimating autophagic activity in Drosophila. PLoS One 7, e44214.
40. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010). Identifcation of the switch in early-to-late endosome transition. Cell 141, 497-508.
41. Pulipparacharuvil S, Akbar MA, Ray S, Sevrioukov EA, Haberman AS, Rohrer J, Kramer H (2005). Drosophila Vps16A is required for traffcking to lysosomes and biogenesis of pigment granules. J Cell Sci 118, 3663-3673.
42. Ravikumar B, Imarisio S, Sarkar S, O'Kane CJ, Rubinsztein DC (2008). Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fy models of Huntington disease. J Cell Sci 121, 1649-1660.
43. Rieder SE, Emr SD (1997). A novel RING fnger protein complex essential for a late step in protein transport to the yeast vacuole. Mol Biol Cell 8, 2307-2327.
44. Rusten TE, Vaccari T, Lindmo K, Rodahl LM, Nezis I P, Sem-Jacobsen C, Wendler F, Vincent JP, Brech A, Bilder D, et al. (2007). ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 17, 1817-1825.
45. Sevrioukov EA, He J P, Moghrabi N, Sunio A, Kramer H (1999). A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Mol Cell 4, 479-486.
46. Stenmark H (2009). Rab GTPases as coordinators of vesicle traffc. Nat Rev Mol Cell Biol 10, 513-525.
47. Stroupe C, Collins KM, Fratti RA, Wickner W (2006). Purifcation of active HOPS complex reveals its affnities for phosphoinositides and the SNARE Vam7p. EMBO J 25, 1579-1589.
48. Takats S, Nagy P, Varga A, Pircs K, Karpati M, Varga K, Kovacs AL, Hegedus K, Juhasz G (2013). Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. J Cell Biol 201, 531-539.
49. Takats S, Pircs K, Nagy P, Varga A, Karpati M, Hegedus K, Kramer H, Kovacs AL, Sass M, Juhasz G (2014). Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Mol Biol Cell 25, 1338-1354.
50. Tanaka T, Nakamura A (2008). The endocytic pathway acts downstream of Oskar in Drosophila germ plasm assembly. Development 135, 1107-1117.
51. Wang CW, Stromhaug PE, Shima J, Klionsky DJ (2002). The Ccz1-Mon1 protein complex is required for the late step of multiple vacuole delivery pathways. J Biol Chem 277, 47917-47927.
52. Wucherpfennig T, Wilsch-Brauninger M, Gonzalez-Gaitan M (2003). Role of Drosophila Rab5 during endosomal traffcking at the synapse and evoked neurotransmitter release. J Cell Biol 161, 609-624.
53. Yousefan J, Troost T, Grawe F, Sasamura T, Fortini M, Klein T (2013). Dmon1 controls recruitment of Rab7 to maturing endosomes in Drosophila. J Cell Sci 126, 1583-1594.
54. Zeigerer A, Gilleron J, Bogorad RL, Marsico G, Nonaka H, Seifert S, Epstein-Barash H, Kuchimanchi S, Peng CG, Ruda VM, et al. (2012). Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485, 465-470.