The putative HORMA domain protein Atg101 dimerizes and is required for starvation-induced and selective autophagy in drosophila

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Hegedus, Krisztina ^a   Nagy, Péter ^a   Gáspári, Zoltán ^b   Juhász, Gábor ^a  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ATG 13 PROTEIN; ATG 16 PROTEIN; ATG 18 PROTEIN; ATG 8A PROTEIN; ATG101 PROTEIN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; PROTEIN; PROTEIN MAD2; RAGC PROTEIN; UNCLASSIFIED DRUG; ATG101 PROTEIN, DROSOPHILA; ATG13 PROTEIN, DROSOPHILA; CARRIER PROTEIN; DROSOPHILA PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CLONE; CELL GROWTH; CELL ULTRASTRUCTURE; CONFORMATION; CONTROLLED STUDY; DIMERIZATION; DROSOPHILA; FAT BODY; GENE OVEREXPRESSION; HORMA DOMAIN; LYSOSOME; NONHUMAN; PROTEIN DOMAIN; SELECTIVE AUTOPHAGY; STARVATION; ANIMAL; CELL VACUOLE; CHEMISTRY; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN TERTIARY STRUCTURE;

ANIMALS; AUTOPHAGY; CARRIER PROTEINS; DIMERIZATION; DROSOPHILA; DROSOPHILA PROTEINS; LYSOSOMES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; VACUOLES;

EID: 84901792768     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/470482     Document Type: Article

References (49)

1. Klionsky D. J., Cregg J. M., Dunn W. A. Jr., Emr S. D., Sakai Y., Sandoval I. V., Sibirny A., Subramani S., Thumm M., Veenhuis M., Ohsumi Y., A unified nomenclature for yeast autophagy-related genes. Developmental Cell 2003 5 4 539 545 2-s2.0-10744225487 10.1016/S1534-5807(03)00296-X (Pubitemid 37243044)
2. Erdi B., Nagy P., Zvara A., Varga A., Pircs K., Menesi D., Puskas L. G., Juhasz G., Loss of the starvation-induced gene Rack1 leads to glycogen deficiency and impaired autophagic responses in Drosophila. Autophagy 2012 8 1124 1135
3. Mizushima N., The role of the Atg1/ULK1 complex in autophagy regulation. Current Opinion in Cell Biology 2010 22 2 132 139 2-s2.0-77951221542 10.1016/j.ceb.2009.12.004
4. Zoncu R., Bar-Peled L., Efeyan A., Wang S., Sancak Y., Sabatini D. M., mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase. Science 2011 334 6056 678 683 2-s2.0-80555143078 10.1126/science.1207056
5. Juhasz G., Interpretation of bafilomycin, pH neutralizing or protease inhibitor treatments in autophagic flux experiments: novel considerations. Autophagy 2012 8 1875 1876
6. Hosokawa N., Hara T., Kaizuka T., Kishi C., Takamura A., Miura Y., Iemura S.-I., Natsume T., Takehana K., Yamada N., Guan J.-L., Oshiro N., Mizushima N., Nutrient-dependent mTORCl association with the ULK1-Atg13-FIP200 complex required for autophagy. Molecular Biology of the Cell 2009 20 7 1981 1991 2-s2.0-65249119430 10.1091/mbc.E08-12-1248
7. Banreti A., Lukacsovich T., Csikos G., Erdelyi M., Sass M., PP2A regulates autophagy in two alternative ways in Drosophila. Autophagy 2012 8 623 636
8. Chang Y.-Y., Neufeld T. P., An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Molecular Biology of the Cell 2009 20 7 2004 2014 2-s2.0-65249155441 10.1091/mbc.E08-12-1250
9. Nagy P., Kárpáti M., Varga A., Pircs K., Venkei Z., Takáts S., Varga K., Erdi B., Hegedu′s K., Juhász G., Atg17/FIP200 localizes to perilysosomal Ref(2)P aggregates and promotes autophagy by activation of Atg1 in Drosophila. Autophagy 2014 10 453 467
10. Scott R. C., Juhász G., Neufeld T. P., Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Current Biology 2007 17 1 1 11 2-s2.0-33845874899 10.1016/j.cub.2006.10.053 (Pubitemid 46027564)
11. Ichimura Y., Kirisako T., Takao T., Satomi Y., Shimonishi Y., Ishihara N., Mizushima N., Tanida I., Kominami E., Ohsumi M., Noda T., Ohsumi Y., A ubiquitin-like system mediates protein lipidation. Nature 2000 408 6811 488 492 2-s2.0-0034707036 10.1038/35044114
12. Mizushima N., Yamamoto A., Matsui M., Yoshimori T., Ohsumi Y., In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Molecular Biology of the Cell 2004 15 3 1101 1111 2-s2.0-1542283812 10.1091/mbc.E03-09-0704 (Pubitemid 38316219)
13. Johansen T., Lamark T., Selective autophagy mediated by autophagic adapter proteins. Autophagy 2011 7 3 279 296 2-s2.0-79952355107 10.4161/auto.7.3.14487
14. Pankiv S., Clausen T. H., Lamark T., Brech A., Bruun J.-A., Outzen H., Øvervatn A., Bjørkøy G., Johansen T., p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. Journal of Biological Chemistry 2007 282 33 24131 24145 2-s2.0-34548259958 10.1074/jbc.M702824200 (Pubitemid 47328003)
15. Nezis I. P., Simonsen A., Sagona A. P., Finley K., Gaumer S., Contamine D., Rusten T. E., Stenmark H., Brech A., Ref(2)P, the Drosophila melanogaster homologue of mammalian p62, is required for the formation of protein aggregates in adult brain. Journal of Cell Biology 2008 180 6 1065 1071 2-s2.0-41549151641 10.1083/jcb.200711108 (Pubitemid 351468465)
16. Hosokawa N., Sasaki T., Iemura S.-I., Natsume T., Hara T., Mizushima N., Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 2009 5 7 973 979 2-s2.0-70349644856 10.4161/auto.5.7.9296
17. Mercer C. A., Kaliappan A., Dennis P. B., A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy 2009 5 5 649 662 2-s2.0-67549110195 10.4161/auto.5.5.8249
18. Liang Q., Yang P., Tian E., Han J., Zhang H., The C. elegans ATG101 homolog EPG-9 directly interacts with EPG-1/Atg13 and is essential for autophagy. Autophagy 2012 8 1426 1433
19. Takats S., Nagy P., Varga Á., Autophagosomal syntaxin17-dependent lysosomal degradation maintains neuronal function in Drosophila. The Journal of Cell Biology 2013 201 531 539
20. Nagy P., Varga A., Pircs K., Hegedus K., Juhasz G., Myc-driven overgrowth requires unfolded protein response-mediated induction of autophagy and antioxidant responses in drosophila melanogaster. PLOS Genetics 2013 9 e1003664
21. Juhász G., Érdi B., Sass M., Neufeld T. P., Atg7-dependent autophagy promotes neuronal health, stress tolerance, and longevity but is dispensable for metamorphosis in Drosophila. Genes and Development 2007 21 23 3061 3066 2-s2.0-36849021043 10.1101/gad.1600707 (Pubitemid 350223523)
22. Pircs K., Nagy P., Varga A., Venkei Z., Erdi B., Hegedus K., Juhasz G., Advantages and limitations of different p62-based assays for estimating autophagic activity in Drosophila. PloS ONE 2012 7 e44214
23. Juhasz G., Neufeld T. P., Experimental control and characterization of autophagy in drosophila. Methods in Molecular Biology 2008 445 125 133 2-s2.0-46049098633 10.1007/978-1-59745-157-4-8
24. Nagy P., Hegedus K., Pircs K., Varga A., Juhasz G., Different effects of Atg2 and Atg18 mutations on Atg8a and Atg9 trafficking during starvation in Drosophila. FEBS Letters 2014 588 408 413
25. Altenhoff A. M., Schneider A., Gonnet G. H., Dessimoz C., OMA 2011: orthology inference among 1000 complete genomes. Nucleic Acids Research 2011 39 1 D289 D294 2-s2.0-78651316211 10.1093/nar/gkq1238
26. Roy A., Kucukural A., Zhang Y., I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 2010 5 4 725 738 2-s2.0-77954065271
27. Kelley L. A., Sternberg M. J. E., Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 2009 4 3 363 371 2-s2.0-63849246525 10.1038/nprot.2009.2
28. Holm L., Park J., DaliLite workbench for protein structure comparison. Bioinformatics 2000 16 6 566 567 2-s2.0-0033824470
29. Lupyan D., Leo-Macias A., Ortiz A. R., A new progressive-iterative algorithm for multiple structure alignment. Bioinformatics 2005 21 15 3255 3263 2-s2.0-25144458667 10.1093/bioinformatics/bti527 (Pubitemid 41418439)
30. Meszaros B., Dosztanyi Z., Simon I., Disordered binding regions and linear motifs-bridging the gap between two models of molecular recognition. PloS ONE 2012 7 e46829
31. Dosztányi Z., Csizmok V., Tompa P., Simon I., IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 2005 21 16 3433 3434 2-s2.0-24044538903 10.1093/bioinformatics/bti541 (Pubitemid 41222453)
32. Pettersen E. F., Goddard T. D., Huang C. C., Couch G. S., Greenblatt D. M., Meng E. C., Ferrin T. E., UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry 2004 25 13 1605 1612 2-s2.0-4444221565 10.1002/jcc.20084
33. Crooks G. E., Hon G., Chandonia J.-M., Brenner S. E., WebLogo: a sequence logo generator. Genome Research 2004 14 6 1188 1190 2-s2.0-2142738304 10.1101/gr.849004 (Pubitemid 38811555)
34. Subramaniam S., The Biology Workbench-a seamless database and analysis environment for the biologist. Proteins 1998 32 1 2 (Pubitemid 28313246)
35. Scott R. C., Schuldiner O., Neufeld T. P., Role and regulation of starvation-induced autophagy in the Drosophila fat body. Developmental Cell 2004 7 2 167 178 2-s2.0-4344563878 10.1016/j.devcel.2004.07.009 (Pubitemid 39145023)
36. Lu Q., Yang P., Huang X., Hu W., Guo B., Wu F., Lin L., Kovács A. L., Yu L., Zhang H., The WD40 repeat ptdIns(3)P-binding protein EPG-6 regulates progression of omegasomes to autophagosomes. Developmental Cell 2011 21 2 343 357 2-s2.0-80051474094 10.1016/j.devcel.2011.06.024
37. Velikkakath A. K. G., Nishimura T., Oita E., Ishihara N., Mizushima N., Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Molecular Biology of the Cell 2012 23 5 896 909 2-s2.0-84857844643 10.1091/mbc.E11-09-0785
38. Alemu E. A., Lamark T., Torgersen K. M., ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs. The Journal of Biological Chemistry 2012 287 39275 39290
39. Rogov V., Dotsch V., Johansen T., Kirkin V., Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Molecular Cell 2014 53 167 178
40. Komatsu M., Waguri S., Koike M., Sou Y.-S., Ueno T., Hara T., Mizushima N., Iwata J.-I., Ezaki J., Murata S., Hamazaki J., Nishito Y., Iemura S.-I., Natsume T., Yanagawa T., Uwayama J., Warabi E., Yoshida H., Ishii T., Kobayashi A., Yamamoto M., Yue Z., Uchiyama Y., Kominami E., Tanaka K., Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007 131 6 1149 1163 2-s2.0-36849089101 10.1016/j.cell.2007.10.035 (Pubitemid 350235021)
41. Bartlett B. J., Isakson P., Lewerenz J., Sanchez H., Kotzebue R. W., Cumming R., Harris G. L., Nezis I. P., Schubert D., Simonsen A., Finley K. D., p62, Ref(2)P and ubiquitinated proteins are conserved markers of neuronal aging, aggregate formation and progressive autophagic defects. Autophagy 2011 7 6 572 583 2-s2.0-79957916551 10.4161/auto.7.6.14943
42. Klionsky D. J., Abdalla F. C., Abeliovich H., Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012 8 445 544
43. Jung C. H., Seo M., Otto N. M., Kim D.-H., ULK1 inhibits the kinase activity of mTORC1 and cell proliferation. Autophagy 2011 7 10 1212 1221 2-s2.0-80053430528 10.4161/auto.7.10.16660
44. Jung C. H., Jun C. B., Ro S.-H., Kim Y.-M., Otto N. M., Cao J., Kundu M., Kim D.-H., ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Molecular Biology of the Cell 2009 20 7 1992 2003 2-s2.0-65249176304 10.1091/mbc.E08-12-1249
45. Jao C. C., Ragusa M. J., Stanley R. E., Hurley J. H., A HORMA domain in Atg13 mediates PI 3-kinase recruitment in autophagy. Proceedings of the National Academy of Sciences of the United States of America 2013 110 5486 5491
46. Mapelli M., Massimiliano L., Santaguida S., Musacchio A., The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell 2007 131 4 730 743 2-s2.0-36049044125 10.1016/j.cell.2007.08. 049 (Pubitemid 350087197)
47. Guruharsha K. G., Rual J.-F., Zhai B., Mintseris J., Vaidya P., Vaidya N., Beekman C., Wong C., Rhee D. Y., Cenaj O., McKillip E., Shah S., Stapleton M., Wan K. H., Yu C., Parsa B., Carlson J. W., Chen X., Kapadia B., Vijayraghavan K., Gygi S. P., Celniker S. E., Obar R. A., Artavanis-Tsakonas S., A protein complex network of Drosophila melanogaster. Cell 2011 147 3 690 703 2-s2.0-80155171417 10.1016/j.cell.2011.08.047
48. Nezis I. P., Selective autophagy in Drosophila. International Journal of Cell Biology 2012 2012 9 146767 10.1155/2012/146767
49. Fujita N., Morita E., Itoh T., Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. The Journal of Cell Biology 2013 203 115 128