Atg6 is required for multiple vesicle trafficking pathways and hematopoiesis in Drosophila

Development (Cambridge)

Volumn 140, Issue 6, 2013, Pages 1321-1329

  Shravage, Bhupendra V ^a   Hill, Jahda H ^a,b,c   Powers, Christine M ^a   Wu, Louisa ^b   Baehrecke, Eric H ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Bldg 142   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Autophagy; Drosophila; Endocytosis; Protein secretion

Indexed keywords

BECLIN 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P62;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BLOOD CELL COUNT; CELL DIFFERENTIATION; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; DROSOPHILA; ENDOCYTOSIS; HEMATOPOIESIS; LARVAL DEVELOPMENT; LYMPH NODE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AUTOPHAGY; BIOLOGICAL TRANSPORT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; EPISTASIS, GENETIC; HEMATOPOIESIS; LARVA; PROTEIN TRANSPORT; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; TRANSPORT VESICLES; VESICULAR TRANSPORT PROTEINS;

EID: 84874531109     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.089490     Document Type: Article

References (61)

1. Aita, V. M., Liang, X. H., Murty, V. V., Pincus, D. L., Yu, W., Cayanis, E., Kalachikov, S., Gilliam, T. C. and Levine, B. (1999). Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics 59, 59-65.
2. Asha, H., Nagy, I., Kovacs, G., Stetson, D., Ando, I. and Dearolf, C. R. (2003). Analysis of Ras-induced overproliferation in Drosophila hemocytes. Genetics 163, 203-215.
3. Berry, D. L. and Baehrecke, E. H. (2007). Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 131, 1137-1148.
4. Biyasheva, A., Do, T. V., Lu, Y., Vaskova, M. and Andres, A. J. (2001). Glue secretion in the Drosophila salivary gland: a model for steroid-regulated exocytosis. Dev. Biol. 231, 234-251.
5. Bodenstein, D. (1965). The postembryonic development of Drosophila. In Biology of Drosophila (ed. M. Demerec), pp. 275-367. New York, NY: Hafner Publishing.
6. Budnik, V., Gorczyca, M. and Prokop, A. (2006). Selected methods for the anatomical study of Drosophila embryonic and larval neuromuscular junctions. Int. Rev. Neurobiol. 75, 323-365.
7. Denton, D., Shravage, B., Simin, R., Mills, K., Berry, D. L., Baehrecke, E. H. and Kumar, S. (2009). Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr. Biol. 19, 1741-1746.
8. Deretic, V. (2011). Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol. Rev. 240, 92-104.
9. Deretic, V., Jiang, S. and Dupont, N. (2012). Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol. 22, 397-406.
10. Ellson, C. D., Andrews, S., Stephens, L. R. and Hawkins, P. T. (2002). The PX domain: a new phosphoinositide-binding module. J. Cell Sci. 115, 1099-1105.
11. Fimia, G. M., Stoykova, A., Romagnoli, A., Giunta, L., Di Bartolomeo, S., Nardacci, R., Corazzari, M., Fuoco, C., Ucar, A., Schwartz, P. et al. (2007). Ambra1 regulates autophagy and development of the nervous system. Nature 447, 1121-1125.
12. Funderburk, S. F., Wang, Q. J. and Yue, Z. (2010). The Beclin 1-VPS34 complex -at the crossroads of autophagy and beyond. Trends Cell Biol. 20, 355-362.
13. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G. and Stenmark, H. (2000). Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588.
14. Harding, T. M., Morano, K. A., Scott, S. V. and Klionsky, D. J. (1995). Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 131, 591-602.
15. Henne, W. M., Buchkovich, N. J. and Emr, S. D. (2011). The ESCRT pathway. Dev. Cell 21, 77-91.
16. Herz, H. M., Chen, Z., Scherr, H., Lackey, M., Bolduc, C. and Bergmann, A. (2006). vps25 mosaics display non-autonomous cell survival and overgrowth, and autonomous apoptosis. Development 133, 1871-1880.
17. Herz, H. M., Woodfield, S. E., Chen, Z., Bolduc, C. and Bergmann, A. (2009). Common and distinct genetic properties of ESCRT-II components in Drosophila. PLoS ONE 4, e4165.
18. Itakura, E., Kishi, C., Inoue, K. and Mizushima, N. (2008). Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 19, 5360-5372.
19. Juhász, G., Hill, J. H., Yan, Y., Sass, M., Baehrecke, E. H., Backer, J. M. and Neufeld, T. P. (2008). The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J. Cell Biol. 181, 655-666.
20. Kadandale, P., Stender, J. D., Glass, C. K. and Kiger, A. A. (2010). Conserved role for autophagy in Rho1-mediated cortical remodeling and blood cell recruitment. Proc. Natl. Acad. Sci. USA 107, 10502-10507.
21. Karantza-Wadsworth, V., Patel, S., Kravchuk, O., Chen, G., Mathew, R., Jin, S. and White, E. (2007). Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 21, 1621-1635.
22. Kihara, A., Kabeya, Y., Ohsumi, Y. and Yoshimori, T. (2001a). Beclin- phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2, 330-335.
23. Kihara, A., Noda, T., Ishihara, N. and Ohsumi, Y. (2001b). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152, 519-530.
24. Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T. and Ohsumi, Y. (1999). Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147, 435-446.
25. Lebestky, T., Chang, T., Hartenstein, V. and Banerjee, U. (2000). Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288, 146-149.
26. Liang, C., Lee, J. S., Inn, K. S., Gack, M. U., Li, Q., Roberts, E. A., Vergne, I., Deretic, V., Feng, P., Akazawa, C. et al. (2008). Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10, 776-787.
27. Lindmo, K. and Stenmark, H. (2006). Regulation of membrane traffic by phosphoinositide 3-kinases. J. Cell Sci. 119, 605-614.
28. Lindmo, K., Brech, A., Finley, K. D., Gaumer, S., Contamine, D., Rusten, T. E. and Stenmark, H. (2008). The PI 3-kinase regulator Vps15 is required for autophagic clearance of protein aggregates. Autophagy 4, 500-506.
29. Maroni, G. and Stamey, S. C. (1983). Use of blue food to select synchronous, late third instar larvae. Dros. Inf. Serv. 59, 142-143.
30. Mathew, R., Kongara, S., Beaudoin, B., Karp, C. M., Bray, K., Degenhardt, K., Chen, G., Jin, S. and White, E. (2007). Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev. 21, 1367-1381.
31. Mathew, R., Karp, C. M., Beaudoin, B., Vuong, N., Chen, G., Chen, H. Y., Bray, K., Reddy, A., Bhanot, G., Gelinas, C. et al. (2009). Autophagy suppresses tumorigenesis through elimination of p62. Cell 137, 1062-1075.
32. 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-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 11, 385-396.
33. Minakhina, S. and Steward, R. (2006). Melanotic mutants in Drosophila: pathways and phenotypes. Genetics 174, 253-263.
34. Mizushima, N. and Komatsu, M. (2011). Autophagy: renovation of cells and tissues. Cell 147, 728-741.
35. Muro, I., Berry, D. L., Huh, J. R., Chen, C. H., Huang, H., Yoo, S. J., Guo, M., Baehrecke, E. H. and Hay, B. A. (2006). The Drosophila caspase Ice is important for many apoptotic cell deaths and for spermatid individualization, a nonapoptotic process. Development 133, 3305-3315.
36. Nezis, I. P., Simonsen, A., Sagona, A. P., Finley, K., Gaumer, S., Contamine, D., Rusten, T. E., Stenmark, H. and 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.
37. Qiu, P., Pan, P. C. and Govind, S. (1998). A role for the Drosophila Toll/Cactus pathway in larval hematopoiesis. Development 125, 1909-1920.
38. Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E. L., Mizushima, N., Ohsumi, Y. et al. (2003). Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809-1820.
39. Rong, Y. S. and Golic, K. G. (2000). Gene targeting by homologous recombination in Drosophila. Science 288, 2013-2018.
40. Ruck, A., Attonito, J., Garces, K. T., Núnez, L., Palmisano, N. J., Rubel, Z., Bai, Z., Nguyen, K. C., Sun, L., Grant, B. D. et al. (2011). The Atg6/Vps30/Beclin 1 ortholog BEC-1 mediates endocytic retrograde transport in addition to autophagy in C. elegans. Autophagy 7, 386-400.
41. Scott, R. C., Schuldiner, O. and Neufeld, T. P. (2004). Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7, 167-178.
42. Scott, R. C., Juhász, G. and Neufeld, T. P. (2007). Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 17, 1-11.
43. Seaman, M. N., Marcusson, E. G., Cereghino, J. L. and Emr, S. D. (1997). Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137, 79-92.
44. Simonsen, A., Birkeland, H. C., Gillooly, D. J., Mizushima, N., Kuma, A., Yoshimori, T., Slagsvold, T., Brech, A. and Stenmark, H. (2004). Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes. J. Cell Sci. 117, 4239-4251.
45. Stenmark, H., Aasland, R. and Driscoll, P. C. (2002). The phosphatidylinositol 3- phosphate-binding FYVE finger. FEBS Lett. 513, 77-84.
46. Takahashi, Y., Coppola, D., Matsushita, N., Cualing, H. D., Sun, M., Sato, Y., Liang, C., Jung, J. U., Cheng, J. Q., Mulé, J. J. et al. (2007). Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat. Cell Biol. 9, 1142-1151.
47. Takamura, A., Komatsu, M., Hara, T., Sakamoto, A., Kishi, C., Waguri, S., Eishi, Y., Hino, O., Tanaka, K. and Mizushima, N. (2011). Autophagy deficient mice develop multiple liver tumors. Genes Dev. 25, 795-800.
48. Thompson, B. J., Mathieu, J., Sung, H. H., Loeser, E., Rørth, P. and Cohen, S. M. (2005). Tumor suppressor properties of the ESCRT-II complex component Vps25 in Drosophila. Dev. Cell 9, 711-720.
49. Thoresen, S. B., Pedersen, N. M., Liestøl, K. and Stenmark, H. (2010). A phosphatidylinositol 3-kinase class III sub-complex containing VPS15, VPS34, Beclin 1, UVRAG and BIF-1 regulates cytokinesis and degradative endocytic traffic. Exp. Cell Res. 316, 3368-3378.
50. Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M. and Wolf, D. H. (1994). Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349, 275-280.
51. Tsukada, M. and Ohsumi, Y. (1993). Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333, 169-174.
52. Vaccari, T. and Bilder, D. (2005). The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Dev. Cell 9, 687-698.
53. Vaccari, T., Rusten, T. E., Menut, L., Nezis, I. P., Brech, A., Stenmark, H. and Bilder, D. (2009). Comparative analysis of ESCRT-I, ESCRT-II and ESCRT-III function in Drosophila by efficient isolation of ESCRT mutants. J. Cell Sci. 122, 2413-2423.
54. White, E. and DiPaola, R. S. (2009). The double-edged sword of autophagy modulation in cancer. Clin. Cancer Res. 15, 5308-5316.
55. Wu, J., Randle, K. E. and Wu, L. P. (2007). ird1 is a Vps15 homologue important for antibacterial immune responses in Drosophila. Cell. Microbiol. 9, 1073-1085.
56. Wucherpfennig, T., Wilsch-Bräuninger, M. and González-Gaitán, M. (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161, 609-624.
57. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
58. Yang, Z., Huang, J., Geng, J., Nair, U. and Klionsky, D. J. (2006). Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. Mol. Biol. Cell 17, 5094-5104.
59. Yue, Z., Jin, S., Yang, C., Levine, A. J. and Heintz, N. (2003). Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. USA 100, 15077-15082.
60. Zhang, Y., Qi, H., Taylor, R., Xu, W., Liu, L. F. and Jin, S. (2007). The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3, 337-346.
61. Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N. and Yue, Z. (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476.