2,486
Views
28
CrossRef citations to date
0
Altmetric
Basic Research Papers

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

&
Pages 1721-1737 | Received 28 Sep 2015, Accepted 24 May 2016, Published online: 27 Jul 2016

References

  • Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol 2010; 221:3-12; PMID:20225336; http://dx.doi.org/10.1002/path.2697
  • Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814-22; PMID:20811353; http://dx.doi.org/10.1038/ncb0910-814
  • Orvedahl A, Levine B. 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
  • Klionsky DJ, Cregg JM, Dunn WA, Jr., Emr SD, Sakai Y, Sandoval IV, 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
  • Klionsky DJ, Cueva R, Yaver DS. 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
  • Hutchins MU, Klionsky DJ. 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
  • Yuga M, Gomi K, Klionsky DJ, Shintani T. 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
  • Lynch-Day MA, Klionsky DJ. 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
  • Ragusa MJ, Stanley RE, Hurley JH. 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
  • Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy 2007; 3:181-206; PMID:17224625; http://dx.doi.org/10.4161/auto.3678
  • Yang S, Rosenwald AG. 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
  • Wang J, Menon S, Yamasaki A, Chou HT, Walz T, Jiang Y, 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
  • Geng J, Nair U, Yasumura-Yorimitsu K, Klionsky DJ. 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
  • Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, 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
  • van der Vaart A, Griffith J, Reggiori F. 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
  • Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, 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
  • Rosenwald AG, Rhodes MA, Van Valkenburgh H, Palanivel V, Chapman G, Boman A, et al. ARL1 and membrane traffic in Saccharomyces cerevisiae. Yeast 2002; 19:1039-56; PMID:12210899; http://dx.doi.org/10.1002/yea.897
  • Lee FJ, Huang CF, Yu WL, Buu LM, Lin CY, Huang MC, 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
  • Li B, Warner JR. 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
  • Singer-Kruger B, Lasic M, Burger AM, Hausser A, Pipkorn R, Wang Y. Yeast and human Ysl2p/hMon2 interact with Gga adaptors and mediate their subcellular distribution. EMBO J 2008; 27:1423-35; PMID:18418388
  • Liu YW, Lee SW, Lee FJ. 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
  • Panic B, Whyte JR, Munro S. 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
  • Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, 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
  • Siniossoglou S, Pelham HR. 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
  • Lafourcade C, Galan JM, Gloor Y, Haguenauer-Tsapis R, Peter M. 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
  • Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, 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
  • Bugnicourt A, Mari M, Reggiori F, Haguenauer-Tsapis R, Galan JM. 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
  • Matsuura A, Tsukada M, Wada Y, Ohsumi Y. 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
  • Xie Z, Nair U, Klionsky DJ. 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
  • Noda T, Klionsky DJ. 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
  • Kahn RA, Clark J, Rulka C, Stearns T, Zhang CJ, Randazzo PA, 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
  • Dascher C, Balch WE. 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
  • Jones S, Jedd G, Kahn RA, Franzusoff A, Bartolini F, Segev N. Genetic interactions in yeast between Ypt GTPases and Arf guanine nucleotide exchangers. Genetics 1999; 152:1543-56; PMID:10430582
  • Lee MT, Mishra A, Lambright DG. 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
  • Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 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
  • Vida TA, Emr SD. 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
  • Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y. 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
  • Bonangelino CJ, Chavez EM, Bonifacino JS. 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
  • Bensen ES, Yeung BG, Payne GS. 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
  • Nair U, Thumm M, Klionsky DJ, Krick R. 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
  • Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. 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
  • Noda T, Kim J, Huang WP, Baba M, Tokunaga C, Ohsumi Y, 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
  • Reggiori F, Shintani T, Nair U, Klionsky DJ. 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
  • Mari M, Griffith J, Rieter E, Krishnappa L, Klionsky DJ, Reggiori F. 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
  • Shintani T, Suzuki K, Kamada Y, Noda T, Ohsumi Y. 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
  • Guan J, Stromhaug PE, George MD, Habibzadegah-Tari P, Bevan A, Dunn WA, 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
  • Reggiori F, Tucker KA, Stromhaug PE, Klionsky DJ. 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
  • Tooze SA, Yoshimori T. The origin of the autophagosomal membrane. Nat Cell Biol 2010; 12:831-5; PMID:20811355; http://dx.doi.org/10.1038/ncb0910-831
  • Reggiori F, Klionsky DJ. 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
  • Reggiori F, Wang CW, Stromhaug PE, Shintani T, Klionsky DJ. 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
  • Dulubova I, Yamaguchi T, Gao Y, Min SW, Huryeva I, Sudhof TC, et al. How Tlg2p/syntaxin 16 ‘snares’ Vps45. EMBO J 2002; 21:3620-31; PMID:12110575; http://dx.doi.org/10.1093/emboj/cdf381
  • Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen WL, 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
  • Yla-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL. 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
  • Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, 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
  • Geng J, Klionsky DJ. 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
  • Abeliovich H, Dunn WA, Jr., Kim J, Klionsky DJ. 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
  • Bonifacino JS, Hierro A. 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
  • Lynch-Day MA, Bhandari D, Menon S, Huang J, Cai H, Bartholomew CR, 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
  • Yen WL, Shintani T, Nair U, Cao Y, Richardson BC, Li Z, 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
  • Gietz D, St Jean A, Woods RA, Schiestl RH. 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
  • Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, Andre B, 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
  • He C, Song H, Yorimitsu T, Monastyrska I, Yen WL, Legakis JE, 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
  • Monastyrska I, He C, Geng J, Hoppe AD, Li Z, Klionsky DJ. 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
  • Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS. Golgi maturation visualized in living yeast. Nature 2006; 441:1002-6; PMID:16699524; http://dx.doi.org/10.1038/nature04717
  • Longtine MS, McKenzie A, 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, 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
  • Cross FR. '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-
  • Tanaka S, Miyazawa-Onami M, Iida T, Araki H. 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
  • Green SR, Moehle CM. Media and culture of yeast. Curr Protoc Cell Biol 2001; Chapter 1:Unit 1 6; PMID:18228294
  • Bradford MM. 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
  • Juhnke H, Krems B, Kotter P, Entian KD. 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