Genetic screen in drosophila muscle identifies autophagy-mediated T-tubule remodeling and a Rab2 role in autophagy

eLife

Volumn 6, Issue , 2017, Pages

  Fujita, Naonobu ^a,b   Huang, Wilson ^a   Lin, Tzu Han ^a   Groulx, Jean Francois ^a   Jean, Steve ^a   Nguyen, Jen ^a   Kuchitsu, Yoshihiko ^b   Koyama Honda, Ikuko ^c   Mizushima, Noboru ^c   Fukuda, Mitsunori ^b   Kiger, Amy A ^a  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGOSOME; AUTOPHAGY; CHEMICAL BINDING; CLEARANCE; DROSOPHILA; LYSOSOME; MEDIATOR; MEMBRANE; NONHUMAN; TRANSVERSE TUBULAR SYSTEM; ANIMAL; ANTAGONISTS AND INHIBITORS; DROSOPHILA MELANOGASTER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEMBRANE FUSION; METABOLISM; MORPHOGENESIS; MUSCLE; PHAGOSOME; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ATG8A PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; ISOPROTEIN; RAB PROTEIN; RAB7 PROTEIN; SMALL INTERFERING RNA; SNARE PROTEIN; SYNAPTOBREVIN; SYNTAXIN; UNISNAP PROTEIN, DROSOPHILA; VAMP7 PROTEIN, DROSOPHILA;

ANIMALS; AUTOPHAGY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LYSOSOMES; MEMBRANE FUSION; MORPHOGENESIS; MUSCLES; PHAGOSOMES; PROTEIN ISOFORMS; PROTEIN TRANSPORT; QA-SNARE PROTEINS; R-SNARE PROTEINS; RAB GTP-BINDING PROTEINS; RAB2 GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SNARE PROTEINS;

EID: 85010633369     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.23367     Document Type: Article

References (87)

1. Ailion M, Hannemann M, Dalton S, Pappas A, Watanabe S, Hegermann J, Liu Q, Han HF, Gu M, Goulding MQ, Sasidharan N, Schuske K, Hullett P, Eimer S, Jorgensen EM. 2014. Two Rab2 interactors regulate dense-core vesicle maturation. Neuron 82:167-180. doi: 10.1016/j.neuron.2014.02.017
2. Aizawa M, Fukuda M. 2015. Small GTPase Rab2B and its specific binding protein Golgi-associated Rab2B Interactor-like 4 (GARI-L4) regulate Golgi Morphology. Journal of Biological Chemistry 290:22250-22261. doi: 10.1074/jbc.M115.669242
3. Al-Qusairi L, Laporte J. 2011. T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skeletal Muscle 1:26. doi: 10.1186/2044-5040-1-26
4. Balderhaar HJ, Ungermann C. 2013. CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion. Journal of Cell Science 126:1307-1316. doi: 10.1242/jcs.107805
5. Bashir R, Britton S, Strachan T, Keers S, Vafiadaki E, Lako M, Richard I, Marchand S, Bourg N, Argov Z, Sadeh M, Mahjneh I, Marconi G, Passos-Bueno MR, Moreira ES, Zatz M, Beckmann JS, Bushby K. 1998. A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2b. Nature Genetics 20:37-42. doi: 10.1038/1689
6. Berry DL, Baehrecke EH. 2007. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131:1137-1148. doi: 10.1016/j.cell.2007.10.048
7. Betz RC, Schoser BG, Kasper D, Ricker K, Ramírez A, Stein V, Torbergsen T, Lee YA, Nothen MM, Wienker TF, Malin JP, Propping P, Reis A, Mortier W, Jentsch TJ, Vorgerd M, Kubisch C. 2001. Mutations in CAV3 cause mechanical hyperirritability of skeletal muscle in rippling muscle disease. Nature Genetics 28:218-219. doi: 10.1038/90050
8. Bitoun M, Maugenre S, Jeannet PY, Lacène E, Ferrer X, Laforêt P, Martin JJ, Laporte J, Lochmuller H, Beggs AH, Fardeau M, Eymard B, Romero NB, Guicheney P. 2005. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nature Genetics 37:1207-1209. doi: 10.1038/ng1657
9. Brette F, Orchard C. 2003. T-tubule function in mammalian cardiac myocytes. Circulation Research 92:1182-1192. doi: 10.1161/01.RES.0000074908.17214.FD
10. Burkart C, Qiu F, Brendel S, Benes V, Hååg P, Labeit S, Leonard K, Bullard B. 2007. Modular proteins from the Drosophila sallimus (sls) gene and their expression in muscles with different extensibility. Journal of Molecular Biology 367:953-969. doi: 10.1016/j.jmb.2007.01.059
11. Butler MH, David C, Ochoa GC, Freyberg Z, Daniell L, Grabs D, Cremona O, De Camilli P. 1997. Amphiphysin II (SH3P9; BIN1), a member of the amphiphysin/Rvs family, is concentrated in the cortical cytomatrix of axon initial segments and nodes of ranvier in brain and around T tubules in skeletal muscle. The Journal of Cell Biology 137:1355-1367. doi: 10.1083/jcb.137.6.1355
12. Carlsson SR, Simonsen A. 2015. Membrane dynamics in autophagosome biogenesis. Journal of Cell Science 128: 193-205. doi: 10.1242/jcs.141036
13. Chang TK, Shravage BV, Hayes SD, Powers CM, Simin RT, Wade Harper J, Baehrecke EH. 2013. Uba1 functions in Atg7- and Atg3-independent autophagy. Nature Cell Biology 15:1067-1078. doi: 10.1038/ncb2804
14. Chen GC, Lee JY, Tang HW, Debnath J, Thomas SM, Settleman J. 2008. Genetic interactions between Drosophila melanogaster Atg1 and paxillin reveal a role for paxillin in autophagosome formation. Autophagy 4: 37-45. doi: 10.4161/auto.5141
15. Chun DK, McEwen JM, Burbea M, Kaplan JM. 2008. UNC-108/Rab2 regulates postendocytic trafficking in Caenorhabditis elegans. Molecular Biology of the Cell 19:2682-2695. doi: 10.1091/mbc.E07-11-1120
16. Das G, Shravage BV, Baehrecke EH. 2012. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harbor Perspectives in Biology 4:a008813. doi: 10.1101/cshperspect.a008813
17. Demontis F, Piccirillo R, Goldberg AL, Perrimon N. 2013. Mechanisms of skeletal muscle aging: insights from Drosophila and mammalian models. Disease Models & Mechanisms 6:1339-1352. doi: 10.1242/dmm.012559
18. Dowling JJ, Low SE, Busta AS, Feldman EL. 2010. Zebrafish MTMR14 is required for excitation-contraction coupling, developmental motor function and the regulation of autophagy. Human Molecular Genetics 19:2668-2681. doi: 10.1093/hmg/ddq153
19. Durieux AC, Vassilopoulos S, Lainé J, Fraysse B, Briñas L, Prudhon B, Castells J, Freyssenet D, Bonne G, Guicheney P, Bitoun M. 2012. A centronuclear myopathy-dynamin 2 mutation impairs autophagy in mice. Traffic 13:869-879. doi: 10.1111/j.1600-0854.2012.01348.x
20. Eckly A, Heijnen H, Pertuy F, Geerts W, Proamer F, Rinckel JY, Léon C, Lanza F, Gachet C. 2014. Biogenesis of the demarcation membrane system (DMS) in megakaryocytes. Blood 123:921-930. doi: 10.1182/blood-2013-03-492330
21. Edwards SL, Charlie NK, Richmond JE, Hegermann J, Eimer S, Miller KG. 2009. Impaired dense core vesicle maturation in Caenorhabditis elegans mutants lacking Rab2. The Journal of Cell Biology 186:881-895. doi: 10.1083/jcb.200902095
22. Fukuda M, Kanno E, Mikoshiba K. 1999. Conserved N-terminal cysteine motif is essential for Homo-and heterodimer formation of synaptotagmins III, V, VI, and X. Journal of Biological Chemistry 274:31421-31427. doi: 10.1074/jbc.274.44.31421
23. Fukuda M. 2003. Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. Journal of Biological Chemistry 278:15373-15380. doi: 10.1074/jbc.M212341200
24. Gillingham AK, Sinka R, Torres IL, Lilley KS, Munro S. 2014. Toward a comprehensive map of the effectors of rab GTPases. Developmental Cell 31:358-373. doi: 10.1016/j.devcel.2014.10.007
25. Munafó DB, Berón W, Colombo MI. 2004. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. Journal of Cell Science 117:2687-2697. doi: 10.1242/jcs.01114
26. Hegedűs K, Takáts S, Boda A, Jipa A, Nagy P, Varga K, Kovács AL, Juhász G. 2016. The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy. Molecular Biology of the Cell 27:3132-3142. doi: 10.1091/mbc.E16-03-0205
27. Hnia K, Vaccari I, Bolino A, Laporte J. 2012. Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology. Trends in Molecular Medicine 18:317-327. doi: 10.1016/j.molmed.2012.04.004
28. Hyttinen JM, Niittykoski M, Salminen A, Kaarniranta K. 2013. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1833:503-510. doi: 10.1016/j. bbamcr.2012.11.018
29. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T, Kominami E, Yamane T, Tanaka K, Komatsu M. 2008. Structural basis for sorting mechanism of p62 in selective autophagy. Journal of Biological Chemistry 283:22847-22857. doi: 10.1074/jbc.M802182200
30. 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. doi: 10.1016/j.cell.2012.11.001
31. Itoh T, Kanno E, Uemura T, Waguri S, Fukuda M. 2011. OATL1, a novel autophagosome-resident Rab33B-GAP, regulates autophagosomal maturation. The Journal of Cell Biology 192:839-853. doi: 10.1083/jcb.201008107
32. Itoh T, Satoh M, Kanno E, Fukuda M. 2006. Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes to Cells 11:1023-1037. doi: 10.1111/j.1365-2443.2006.00997.x
33. Jean S, Kiger AA. 2012. Coordination between RAB GTPase and phosphoinositide regulation and functions. Nature Reviews Molecular Cell Biology 13:463-470. doi: 10.1038/nrm3379
34. Jean S, Cox S, Nassari S, Kiger AA. 2015. Starvation-induced MTMR13 and RAB21 activity regulates VAMP8 to promote autophagosome-lysosome fusion. EMBO reports 16:297-311. doi: 10.15252/embr.201439464
35. 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. Molecular Biology of the Cell 25:1327-1337. doi: 10.1091/mbc.E13-08-0447
36. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, Eskelinen EL. 2004. Role for Rab7 in maturation of late autophagic vacuoles. Journal of Cell Science 117:4837-4848. doi: 10.1242/jcs.01370
37. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. The EMBO Journal 19:5720-5728. doi: 10.1093/emboj/19.21.5720
38. Kajiho H, Kajiho Y, Frittoli E, Confalonieri S, Bertalot G, Viale G, Di Fiore PP, Oldani A, Garre M, Beznoussenko GV, Palamidessi A, Vecchi M, Chavrier P, Perez F, Scita G. 2016. RAB2A controls MT1-MMP endocytic and E-cadherin polarized Golgi trafficking to promote invasive breast cancer programs. EMBO Reports 17:1061-1080. doi: 10.15252/embr.201642032
39. Kimura KI, Truman JW. 1990. Postmetamorphic cell death in the nervous and muscular systems of Drosophila melanogaster. Journal of Neuroscience 10:403-401
40. Kimura S, Noda T, Yoshimori T. 2007. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3:452-460. doi: 10.4161/auto.4451
41. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, Noda T, Ohsumi Y. 1999. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. The Journal of Cell Biology 147:435-446. doi: 10.1083/jcb.147.2.435
42. Klopper TH, Kienle N, Fasshauer D, Munro S. 2012. Untangling the evolution of rab G proteins: implications of a comprehensive genomic analysis. BMC Biology 10:71. doi: 10.1186/1741-7007-10-71
43. Koyama-Honda I, Itakura E, Fujiwara TK, Mizushima N. 2013. Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy 9:1491-1499. doi: 10.4161/auto.25529
44. Kuleesha Y, Puah WC, Lin F, Wasser M. 2014. FMAj: a tool for high content analysis of muscle dynamics in Drosophila metamorphosis. BMC Bioinformatics 15 Suppl 16:S6. doi: 10.1186/1471-2105-15-S16-S6
45. Kuleesha Y, Puah WC, Wasser M. 2016. A model of muscle atrophy based on live microscopy of muscle remodelling in Drosophila metamorphosis. Royal Society Open Science 3:150517. doi: 10.1098/rsos.150517
46. Laporte J, Hu LJ, Kretz C, Mandel JL, Kioschis P, Coy JF, Klauck SM, Poustka A, Dahl N. 1996. A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nature Genetics 13:175-182. doi: 10.1038/ng0696-175
47. Lee CY, Cooksey BA, Baehrecke EH. 2002a. Steroid regulation of midgut cell death during Drosophila development. Developmental Biology 250:101-111. doi: 10.1006/dbio.2002.0784
48. Lee DM, Harris TJ. 2013. An Arf-GEF regulates antagonism between endocytosis and the cytoskeleton for Drosophila blastoderm development. Current Biology 23:2110-2120. doi: 10.1016/j.cub.2013.08.058
49. Lee DM, Harris TJ. 2014. Coordinating the cytoskeleton and endocytosis for regulated plasma membrane growth in the early Drosophila embryo. BioArchitecture 4:68-74. doi: 10.4161/bioa.28949
50. Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA, Ochoa GC, Farsad K, Wenk MR, De Camilli P. 2002b. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297:1193-1196. doi: 10.1126/science.1071362
51. Lek A, Evesson FJ, Sutton RB, North KN, Cooper ST. 2012. Ferlins: regulators of vesicle fusion for auditory neurotransmission, receptor trafficking and membrane repair. Traffic 13:185-194. doi: 10.1111/j.1600-0854.2011.01267.x
52. Liou W, Geuze HJ, Slot JW. 1996. Improving structural integrity of cryosections for immunogold labeling. Histochemistry and Cell Biology 106:41-58. doi: 10.1007/BF02473201
53. Liu J, Aoki M, Illa I, Wu C, Fardeau M, Angelini C, Serrano C, Urtizberea JA, Hentati F, Hamida MB, Bohlega S, 1998. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nature Genetics 20:31-36. doi: 10.1038/1682
54. Malicdan MC, Noguchi S, Nonaka I, Saftig P, Nishino I. 2008. Lysosomal myopathies: an excessive build-up in autophagosomes is too much to handle. Neuromuscular Disorders 18:521-529. doi: 10.1016/j.nmd.2008.04.010
55. Mangahas PM, Yu X, Miller KG, Zhou Z. 2008. The small GTPase Rab2 functions in the removal of apoptotic cells in Caenorhabditis elegans. The Journal of Cell Biology 180:357-373. doi: 10.1083/jcb.200708130
56. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M. 2009. Autophagy is required to maintain muscle mass. Cell Metabolism 10:507-515. doi: 10.1016/j.cmet.2009.10.008
57. Minetti C, Sotgia F, Bruno C, Scartezzini P, Broda P, Bado M, Masetti E, Mazzocco M, Egeo A, Donati MA, Volonte D, Galbiati F, Cordone G, Bricarelli FD, Lisanti MP, Zara F. 1998. Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Nature Genetics 18:365-368. doi: 10.1038/ng0498-365
58. Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T, Natsume T, Ohsumi Y, Yoshimori T. 2003. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. Journal of Cell Science 116:1679-1688. doi: 10.1242/jcs.00381
59. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. 2001. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. The Journal of Cell Biology 152:657-668. doi: 10.1083/jcb.152.4.657
60. Morita S, Kojima T, Kitamura T. 2000. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Therapy 7:1063-1066. doi: 10.1038/sj.gt.3301206
61. Morlot S, Roux A. 2013. Mechanics of dynamin-mediated membrane fission. Annual Review of Biophysics 42: 629-649. doi: 10.1146/annurev-biophys-050511-102247
62. Nicot AS, Toussaint A, Tosch V, Kretz C, Wallgren-Pettersson C, Iwarsson E, Kingston H, Garnier JM, Biancalana V, Oldfors A, Mandel JL, Laporte J. 2007. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nature Genetics 39:1134-1139. doi: 10.1038/ng2086
63. Pelissier A, Chauvin JP, Lecuit T. 2003. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Current Biology 13:1848-1857. doi: 10.1016/j.cub.2003.10.023
64. Peterson SJ, Krasnow MA. 2015. Subcellular trafficking of FGF controls tracheal invasion of Drosophila flight muscle. Cell 160:313-323. doi: 10.1016/j.cell.2014.11.043
65. Piccirillo R, Demontis F, Perrimon N, Goldberg AL. 2014. Mechanisms of muscle growth and atrophy in mammals and Drosophila. Developmental Dynamics 243:201-215. doi: 10.1002/dvdy.24036
66. 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. doi: 10.1371/journal.pone.0044214
67. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F. 2013. Genome engineering using the CRISPR-Cas9 system. Nature Protocols 8:2281-2308. doi: 10.1038/nprot.2013.143
68. Razzaq A, Robinson IM, McMahon HT, Skepper JN, Su Y, Zelhof AC, Jackson AP, Gay NJ, O’Kane CJ. 2001. Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes & Development 15:2967-2979. doi: 10.1101/gad.207801
69. Ribeiro I, Yuan L, Tanentzapf G, Dowling JJ, Kiger A. 2011. Phosphoinositide regulation of integrin trafficking required for muscle attachment and maintenance. PLoS Genetics 7:e1001295. doi: 10.1371/journal.pgen.1001295
70. Rubinsztein DC, Mariño G, Kroemer G. 2011. Autophagy and aging. Cell 146:682-695.doi:10.1016/j.cell.2011.07.030
71. Saitoh T, Nakayama M, Nakano H, Yagita H, Yamamoto N, Yamaoka S. 2003. TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation. Journal of Biological Chemistry 278:36005-36012. doi: 10.1074/jbc.M304266200
72. Saraste J. 2016. Spatial and functional aspects of ER-Golgi Rabs and Tethers. Frontiers in Cell and Developmental Biology 4:28. doi: 10.3389/fcell.2016.00028
73. Shen HM, Mizushima N. 2014. At the end of the autophagic road: an emerging understanding of lysosomal functions in autophagy. Trends in Biochemical Sciences 39:61-71. doi: 10.1016/j.tibs.2013.12.001
74. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nature Reviews Molecular Cell Biology 10: 513-525. doi: 10.1038/nrm2728
75. Tabata K, Matsunaga K, Sakane A, Sasaki T, Noda T, Yoshimori T. 2010. Rubicon and PLEKHM1 negatively regulate the endocytic/autophagic pathway via a novel Rab7-binding domain. Molecular Biology of the Cell 21: 4162-4172. doi: 10.1091/mbc.E10-06-0495
76. Takekura H, Flucher BE, Franzini-Armstrong C. 2001. Sequential docking, molecular differentiation, and positioning of T-Tubule/SR junctions in developing mouse skeletal muscle. Developmental Biology 239:204-214. doi: 10.1006/dbio.2001.0437
77. Takeshima H, Hoshijima M, Song LS. 2015. Ca2+ microdomains organized by junctophilins. Cell Calcium 58:349-356. doi: 10.1016/j.ceca.2015.01.007
78. Takáts S, Nagy P, Varga Á, Pircs K, Kárpáti M, Varga K, Kovács AL, Hegedűs K, Juhász G. 2013. Autophagosomal Syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. The Journal of Cell Biology 201:531-539. doi: 10.1083/jcb.201211160
79. Takáts S, Pircs K, Nagy P, Varga Á, Kárpáti M, Hegedűs K, Kramer H, Kovács AL, Sass M, Juhász G. 2014. Interaction of the HOPS complex with Syntaxin 17 mediates autophagosome clearance in Drosophila. Molecular Biology of the Cell 25:1338-1354. doi: 10.1091/mbc.E13-08-0449
80. Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF, Lisanti MP. 1996. Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. The Journal of Biological Chemistry 271:2255-2261. doi: 10.1074/jbc.271.4.2255
81. Tian Y, Li Z, Hu W, Ren H, Tian E, Zhao Y, Lu Q, Huang X, Yang P, Li X, Wang X, Kovács AL, Yu L, Zhang H. 2010. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 141:1042-1055. doi: 10.1016/j.cell.2010.04.034
82. Tokuyasu KT. 1980. Immunochemistry on ultrathin frozen sections. The Histochemical Journal 12:381-403. doi: 10.1007/BF01011956
83. Tsuboyama K, Koyama-Honda I, Sakamaki Y, Koike M, Morishita H, Mizushima N. 2016. The ATG conjugation systems are important for degradation of the inner autophagosomal membrane. Science 354:1036-1041. doi: 10.1126/science.aaf6136
84. Wasser M, Bte Osman Z, Chia W. 2007. EAST and Chromator control the destruction and remodeling of muscles during Drosophila metamorphosis. Developmental Biology 307:380-393. doi: 10.1016/j.ydbio.2007.05.001
85. Weisleder N, Brotto M, Komazaki S, Pan Z, Zhao X, Nosek T, Parness J, Takeshima H, Ma J. 2006. Muscle aging is associated with compromised Ca2+ spark signaling and segregated intracellular Ca2+ release. The Journal of Cell Biology 174:639-645. doi: 10.1083/jcb.200604166
86. Zirin J, Nieuwenhuis J, Perrimon N. 2013. Role of autophagy in glycogen breakdown and its relevance to chloroquine myopathy. PLoS Biology 11:e1001708. doi: 10.1371/journal.pbio.1001708
87. Zitserman D, Roegiers F. 2011. Live-cell imaging of sensory organ precursor cells in intact Drosophila pupae. Journal of Visualized Experiments 51: 2706. doi: 10.3791/2706