Autophagy in Saccharomyces cerevisiae requires the monomeric GTP-binding proteins, Arl1 and Ypt6

Autophagy

Volumn 12, Issue 10, 2016, Pages 1721-1737

  Yang, Shu ^a   Rosenwald, Anne G ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

Arl1; Atg9; autophagy; GARP; membrane trafficking; temperature; yeast; Ypt6

Indexed keywords

ARL1 PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; YPT6 PROTEIN; ARL1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN; YPT6 PROTEIN, S CEREVISIAE;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; ENDOSOME; HIGH TEMPERATURE; NONHUMAN; PROTEIN FAMILY; SACCHAROMYCES CEREVISIAE; TEMPERATURE STRESS; TRANS GOLGI NETWORK; BIOLOGICAL MODEL; CYTOLOGY; GENETICS; GOLGI COMPLEX; METABOLISM; MUTATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TEMPERATURE;

AUTOPHAGOSOMES; AUTOPHAGY; GOLGI APPARATUS; MODELS, BIOLOGICAL; MONOMERIC GTP-BINDING PROTEINS; MUTATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TEMPERATURE; VESICULAR TRANSPORT PROTEINS;

EID: 84980047767     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1196316     Document Type: Article

References (70)

1. D.Glick, S.Barth, K.F.Macleod. Autophagy:cellular and molecular mechanisms. J Pathol 2010; 221:3-12; PMID:20225336; http://dx.doi.org/10.1002/path.2697
2. Z.Yang, D.J.Klionsky. Eaten alive:a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
3. A.Orvedahl, B.Levine. Eating the enemy within:autophagy in infectious diseases. Cell Death Differ 2009; 16:57-69; PMID:18772897; http://dx.doi.org/10.1038/cdd.2008.130
4. D.J.Klionsky, J.M.Cregg, W.A.Dunn, Jr., S.D.Emr, Y.Sakai, I.V.Sandoval, et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell 2003; 5:539-45; PMID:14536056; http://dx.doi.org/10.1016/S1534-5807(03)00296-X
5. D.J.Klionsky, R.Cueva, D.S.Yaver. Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J Cell Biol 1992; 119:287-99; PMID:1400574; http://dx.doi.org/10.1083/jcb.119.2.287
6. M.U.Hutchins, D.J.Klionsky. Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J Biol Chem 2001; 276:20491-8; PMID:11264288; http://dx.doi.org/10.1074/jbc.M101150200
7. M.Yuga, K.Gomi, D.J.Klionsky, T.Shintani. Aspartyl aminopeptidase is imported from the cytoplasm to the vacuole by selective autophagy in Saccharomyces cerevisiae. J Biol Chem 2011; 286:13704-13; PMID:21343297; http://dx.doi.org/10.1074/jbc.M110.173906
8. M.A.Lynch-Day, D.J.Klionsky. The Cvt pathway as a model for selective autophagy. FEBS Lett 2010; 584:1359-66; PMID:20146925; http://dx.doi.org/10.1016/j.febslet.2010.02.013
9. M.J.Ragusa, R.E.Stanley, J.H.Hurley. Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 2012; 151:1501-12; PMID:23219485; http://dx.doi.org/10.1016/j.cell.2012.11.028
10. D.J.Klionsky, A.M.Cuervo, P.O.Seglen. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3:181-206; PMID:17224625; http://dx.doi.org/10.4161/auto.3678
11. S.Yang, A.G.Rosenwald. The roles of monomeric GTP-binding proteins in macroautophagy in Saccharomyces cerevisiae. Int J Mol Sci 2014; 15:18084-101; PMID:25302616; http://dx.doi.org/10.3390/ijms151018084
12. J.Wang, S.Menon, A.Yamasaki, H.T.Chou, T.Walz, Y.Jiang, et al. Ypt1 recruits the Atg1 kinase to the preautophagosomal structure. Proc Natl Acad Sci U S A 2013; 110:9800-5; PMID:23716696; http://dx.doi.org/10.1073/pnas.1302337110
13. J.Geng, U.Nair, K.Yasumura-Yorimitsu, D.J.Klionsky. Post-Golgi Sec proteins are required for autophagy in Saccharomyces cerevisiae. Mol Biol Cell 2010; 21:2257-69; PMID:20444978; http://dx.doi.org/10.1091/mbc.E09-11-0969
14. T.Kirisako, M.Baba, N.Ishihara, K.Miyazawa, M.Ohsumi, T.Yoshimori, et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol 1999; 147:435-46; PMID:10525546; http://dx.doi.org/10.1083/jcb.147.2.435
15. A.van der Vaart, J.Griffith, F.Reggiori. Exit from the Golgi is required for the expansion of the autophagosomal phagophore in yeast Saccharomyces cerevisiae. Mol Biol Cell 2010; 21:2270-84; PMID:20444982; http://dx.doi.org/10.1091/mbc.E09-04-0345
16. N.Ishihara, M.Hamasaki, S.Yokota, K.Suzuki, Y.Kamada, A.Kihara, et al. Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 2001; 12:3690-702; PMID:11694599; http://dx.doi.org/10.1091/mbc.12.11.3690
17. A.G.Rosenwald, M.A.Rhodes, H.Van Valkenburgh, V.Palanivel, G.Chapman, A.Boman, et al. ARL1 and membrane traffic in Saccharomyces cerevisiae. Yeast 2002; 19:1039-56; PMID:12210899; http://dx.doi.org/10.1002/yea.897
18. F.J.Lee, C.F.Huang, W.L.Yu, L.M.Buu, C.Y.Lin, M.C.Huang, et al. Characterization of an ADP-ribosylation factor-like 1 protein in Saccharomyces cerevisiae. J Biol Chem 1997; 272:30998-1005; PMID:9388248; http://dx.doi.org/10.1074/jbc.272.49.30998
19. B.Li, J.R.Warner. Mutation of the Rab6 homologue of Saccharomyces cerevisiae, YPT6, inhibits both early Golgi function and ribosome biosynthesis. J Biol Chem 1996; 271:16813-9; PMID:8663225; http://dx.doi.org/10.1074/jbc.271.28.16813
20. B.Singer-Kruger, M.Lasic, A.M.Burger, A.Hausser, R.Pipkorn, Y.Wang. Yeast and human Ysl2p/hMon2 interact with Gga adaptors and mediate their subcellular distribution. EMBO J 2008; 27:1423-35; PMID:18418388
21. Y.W.Liu, S.W.Lee, F.J.Lee. Arl1p is involved in transport of the GPI-anchored protein Gas1p from the late Golgi to the plasma membrane. J Cell Sci 2006; 119:3845-55; PMID:16926193; http://dx.doi.org/10.1242/jcs.03148
22. B.Panic, J.R.Whyte, S.Munro. The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus. Curr Biol 2003; 13:405-10; PMID:12620189; http://dx.doi.org/10.1016/S0960-9822(03)00091-5
23. A.H.Tong, G.Lesage, G.D.Bader, H.Ding, H.Xu, X.Xin, et al. Global mapping of the yeast genetic interaction network. Science 2004; 303:808-13; PMID:14764870; http://dx.doi.org/10.1126/science.1091317
24. S.Siniossoglou, H.R.Pelham. An effector of Ypt6p binds the SNARE Tlg1p and mediates selective fusion of vesicles with late Golgi membranes. EMBO J 2001; 20:5991-8; PMID:11689439; http://dx.doi.org/10.1093/emboj/20.21.5991
25. C.Lafourcade, J.M.Galan, Y.Gloor, R.Haguenauer-Tsapis, M.Peter. The GTPase-activating enzyme Gyp1p is required for recycling of internalized membrane material by inactivation of the Rab/Ypt GTPase Ypt1p. Mol Cell Biol 2004; 24:3815-26; PMID:15082776; http://dx.doi.org/10.1128/MCB.24.9.3815-3826.2004
26. E.J.Brown, M.W.Albers, T.B.Shin, K.Ichikawa, C.T.Keith, W.S.Lane, et al. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 1994; 369:756-8; PMID:8008069; http://dx.doi.org/10.1038/369756a0
27. A.Bugnicourt, M.Mari, F.Reggiori, R.Haguenauer-Tsapis, J.M.Galan. Irs4p and Tax4p:two redundant EH domain proteins involved in autophagy. Traffic 2008; 9:755-69; PMID:18298591; http://dx.doi.org/10.1111/j.1600-0854.2008.00715.x
28. A.Matsuura, M.Tsukada, Y.Wada, Y.Ohsumi. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 1997; 192:245-50; PMID:9224897; http://dx.doi.org/10.1016/S0378-1119(97)00084-X
29. Z.Xie, U.Nair, D.J.Klionsky. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 2008; 19:3290-8; PMID:18508918; http://dx.doi.org/10.1091/mbc.E07-12-1292
30. T.Noda, D.J.Klionsky. The quantitative Pho8Delta60 assay of nonspecific autophagy. Methods Enzymol 2008; 451:33-42; PMID:19185711; http://dx.doi.org/10.1016/S0076-6879(08)03203-5
31. R.A.Kahn, J.Clark, C.Rulka, T.Stearns, C.J.Zhang, P.A.Randazzo, et al. Mutational analysis of Saccharomyces cerevisiae ARF1. J Biol Chem 1995; 270:143-50; PMID:7814365; http://dx.doi.org/10.1074/jbc.270.1.143
32. C.Dascher, W.E.Balch. Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J Biol Chem 1994; 269:1437-48; PMID:8288610
33. S.Jones, G.Jedd, R.A.Kahn, A.Franzusoff, F.Bartolini, N.Segev. Genetic interactions in yeast between Ypt GTPases and Arf guanine nucleotide exchangers. Genetics 1999; 152:1543-56; PMID:10430582
34. M.T.Lee, A.Mishra, D.G.Lambright. Structural mechanisms for regulation of membrane traffic by rab GTPases. Traffic 2009; 10:1377-89; PMID:19522756; http://dx.doi.org/10.1111/j.1600-0854.2009.00942.x
35. S.N.Ho, H.D.Hunt, R.M.Horton, J.K.Pullen, L.R.Pease. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989; 77:51-9; PMID:2744487; http://dx.doi.org/10.1016/0378-1119(89)90358-2
36. T.A.Vida, S.D.Emr. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 1995; 128:779-92; PMID:7533169; http://dx.doi.org/10.1083/jcb.128.5.779
37. K.Suzuki, T.Kirisako, Y.Kamada, N.Mizushima, T.Noda, Y.Ohsumi. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J 2001; 20:5971-81; PMID:11689437; http://dx.doi.org/10.1093/emboj/20.21.5971
38. C.J.Bonangelino, E.M.Chavez, J.S.Bonifacino. Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol Biol Cell 2002; 13:2486-501; PMID:12134085; http://dx.doi.org/10.1091/mbc.02-01-0005
39. E.S.Bensen, B.G.Yeung, G.S.Payne. Ric1p and the Ypt6p GTPase function in a common pathway required for localization of trans-Golgi network membrane proteins. Mol Biol Cell 2001; 12:13-26; PMID:11160819; http://dx.doi.org/10.1091/mbc.12.1.13
40. U.Nair, M.Thumm, D.J.Klionsky, R.Krick. GFP-Atg8 protease protection as a tool to monitor autophagosome biogenesis. Autophagy 2011; 7:1546-50; PMID:22108003; http://dx.doi.org/10.4161/auto.7.12.18424
41. K.Nishimura, T.Fukagawa, H.Takisawa, T.Kakimoto, M.Kanemaki. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods 2009; 6:917-22; PMID:19915560; http://dx.doi.org/10.1038/nmeth.1401
42. T.Noda, J.Kim, W.P.Huang, M.Baba, C.Tokunaga, Y.Ohsumi, et al. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 2000; 148:465-80; PMID:10662773; http://dx.doi.org/10.1083/jcb.148.3.465
43. F.Reggiori, T.Shintani, U.Nair, D.J.Klionsky. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 2005; 1:101-9; PMID:16874040; http://dx.doi.org/10.4161/auto.1.2.1840
44. M.Mari, J.Griffith, E.Rieter, L.Krishnappa, D.J.Klionsky, F.Reggiori. An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J Cell Biol 2010; 190:1005-22; PMID:20855505; http://dx.doi.org/10.1083/jcb.200912089
45. T.Shintani, K.Suzuki, Y.Kamada, T.Noda, Y.Ohsumi. Apg2p functions in autophagosome formation on the perivacuolar structure. J Biol Chem 2001; 276:30452-60; PMID:11382761; http://dx.doi.org/10.1074/jbc.M102346200
46. J.Guan, P.E.Stromhaug, M.D.George, P.Habibzadegah-Tari, A.Bevan, W.A.Dunn, Jr., et al. Cvt18/Gsa12 is required for cytoplasm-to-vacuole transport, pexophagy, and autophagy in Saccharomyces cerevisiae and Pichia pastoris. Mol Biol Cell 2001; 12:3821-38; PMID:11739783; http://dx.doi.org/10.1091/mbc.12.12.3821
47. F.Reggiori, K.A.Tucker, P.E.Stromhaug, D.J.Klionsky. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell 2004; 6:79-90; PMID:14723849; http://dx.doi.org/10.1016/S1534-5807(03)00402-7
48. S.A.Tooze, T.Yoshimori. The origin of the autophagosomal membrane. Nat Cell Biol 2010; 12:831-5; PMID:20811355; http://dx.doi.org/10.1038/ncb0910-831
49. F.Reggiori, D.J.Klionsky. Atg9 sorting from mitochondria is impaired in early secretion and VFT-complex mutants in Saccharomyces cerevisiae. J Cell Sci 2006; 119:2903-11; PMID:16787937; http://dx.doi.org/10.1242/jcs.03047
50. F.Reggiori, C.W.Wang, P.E.Stromhaug, T.Shintani, D.J.Klionsky. Vps51 is part of the yeast Vps fifty-three tethering complex essential for retrograde traffic from the early endosome and Cvt vesicle completion. J Biol Chem 2003; 278:5009-20; PMID:12446664; http://dx.doi.org/10.1074/jbc.M210436200
51. I.Dulubova, T.Yamaguchi, Y.Gao, S.W.Min, I.Huryeva, T.C.Sudhof, et al. How Tlg2p/syntaxin 16 ‘snares’ Vps45. EMBO J 2002; 21:3620-31; PMID:12110575; http://dx.doi.org/10.1093/emboj/cdf381
52. U.Nair, A.Jotwani, J.Geng, N.Gammoh, D.Richerson, W.L.Yen, et al. SNARE proteins are required for macroautophagy. Cell 2011; 146:290-302; PMID:21784249; http://dx.doi.org/10.1016/j.cell.2011.06.022
53. P.Yla-Anttila, H.Vihinen, E.Jokitalo, E.L.Eskelinen. 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 2009; 5:1180-5; PMID:19855179; http://dx.doi.org/10.4161/auto.5.8.10274
54. D.W.Hailey, A.S.Rambold, P.Satpute-Krishnan, K.Mitra, R.Sougrat, P.K.Kim, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 2010; 141:656-67; PMID:20478256; http://dx.doi.org/10.1016/j.cell.2010.04.009
55. J.Geng, D.J.Klionsky. The Golgi as a potential membrane source for autophagy. Autophagy 2010; 6:950-1; PMID:20729630; http://dx.doi.org/10.4161/auto.6.7.13009
56. H.Abeliovich, W.A.Dunn, Jr., J.Kim, D.J.Klionsky. Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J Cell Biol 2000; 151:1025-34; PMID:11086004; http://dx.doi.org/10.1083/jcb.151.5.1025
57. J.S.Bonifacino, A.Hierro. Transport according to GARP:receiving retrograde cargo at the trans-Golgi network. Trends Cell Biol 2011; 21:159-67; PMID:21183348; http://dx.doi.org/10.1016/j.tcb.2010.11.003
58. M.A.Lynch-Day, D.Bhandari, S.Menon, J.Huang, H.Cai, C.R.Bartholomew, et al. Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc Natl Acad Sci U S A 2010; 107:7811-6; PMID:20375281; http://dx.doi.org/10.1073/pnas.1000063107
59. W.L.Yen, T.Shintani, U.Nair, Y.Cao, B.C.Richardson, Z.Li, et al. The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J Cell Biol 2010; 188:101-14; PMID:20065092; http://dx.doi.org/10.1083/jcb.200904075
60. D.Gietz, A.St Jean, R.A.Woods, R.H.Schiestl. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 1992; 20:1425; PMID:1561104; http://dx.doi.org/10.1093/nar/20.6.1425
61. E.A.Winzeler, D.D.Shoemaker, A.Astromoff, H.Liang, K.Anderson, B.Andre, et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999; 285:901-6; PMID:10436161; http://dx.doi.org/10.1126/science.285.5429.901
62. C.He, H.Song, T.Yorimitsu, I.Monastyrska, W.L.Yen, J.E.Legakis, et al. Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J Cell Biol 2006; 175:925-35; PMID:17178909; http://dx.doi.org/10.1083/jcb.200606084
63. I.Monastyrska, C.He, J.Geng, A.D.Hoppe, Z.Li, D.J.Klionsky. Arp2 links autophagic machinery with the actin cytoskeleton. Mol Biol Cell 2008; 19:1962-75; PMID:18287533; http://dx.doi.org/10.1091/mbc.E07-09-0892
64. E.Losev, C.A.Reinke, J.Jellen, D.E.Strongin, B.J.Bevis, B.S.Glick. Golgi maturation visualized in living yeast. Nature 2006; 441:1002-6; PMID:16699524; http://dx.doi.org/10.1038/nature04717
65. M.S.Longtine, A.McKenzie, 3rd, D.J.Demarini, N.G.Shah, A.Wach, A.Brachat, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998; 14:953-61; PMID:9717241; http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10%3c953::AID-YEA293%3e3.0.CO;2-U
66. F.R.Cross. 'Marker swap' plasmids:convenient tools for budding yeast molecular genetics. Yeast 1997; 13:647-53; PMID:9200814; http://dx.doi.org/10.1002/(SICI)1097-0061(19970615)13:7%3c647::AID-YEA115%3e3.0.CO;2-
67. S.Tanaka, M.Miyazawa-Onami, T.Iida, H.Araki. iAID:an improved auxin-inducible degron system for the construction of a ‘tight’ conditional mutant in the budding yeast Saccharomyces cerevisiae. Yeast 2015; 32:567-81; PMID:26081484; http://dx.doi.org/10.1002/yea.3080
68. S.R.Green, C.M.Moehle. Media and culture of yeast. Curr Protoc Cell Biol 2001; Chapter 1:Unit 1 6; PMID:18228294
69. M.M.Bradford. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-54; PMID:942051; http://dx.doi.org/10.1016/0003-2697(76)90527-3
70. H.Juhnke, B.Krems, P.Kotter, K.D.Entian. Mutants that show increased sensitivity to hydrogen peroxide reveal an important role for the pentose phosphate pathway in protection of yeast against oxidative stress. Mol Gen Genet 1996; 252:456-64; PMID:8879247; http://dx.doi.org/10.1007/BF02173011