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TOR pp 73–84Cite as

Autophagy in Yeast: ATOR-Mediated Response to Nutrient Starvation

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Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 279))

Abstract

TOR plays a key role in cell growth and cell-cycle progression, but in addition recent studies have shown that TOR is also involved in the regulation of a number of molecular processes associated with nutrient deprivation, such as autophagy. In budding yeast, TOR negatively regulates activation of Apg1 protein kinase, which is essential for the induction of autophagy. This review describes recent research in this field and the mechanism by which TOR mediates induction of autophagy.

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References

  • Abeliovich H, Darsow T, Emr SD (1999) Cytoplasm to vacuole trafficking of amino-peptidase I requires a t-SNARE-Sec1p complex composed of Tlg2p and Vps45p. EMBO J. 18:6005–6016

    Article  PubMed  CAS  Google Scholar 

  • Abeliovich H, Dunn Jr. WA, Kim J, Klionsky DJ (2000) Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J. Cell Biol. 151:1025–1033

    Article  PubMed  CAS  Google Scholar 

  • Baba M, Takeshige K, Baba N, Ohsumi Y (1994) Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J. Cell Biol. 124:903–913

    Article  PubMed  CAS  Google Scholar 

  • Baba M, Ohsumi M, Scott SV, Klionsky DJ, Ohsumi Y (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J Cell Biol. 139:1687–1695

    Article  PubMed  CAS  Google Scholar 

  • Barbet NC, Schneider U, Helliwell SB, Stansfield I, Tuite MF, Hall MN (1996) TOR controls translation initiation and early Gl progression in yeast. Mol. Biol. Cell 7:25–42

    PubMed  CAS  Google Scholar 

  • Beck T, Schmidt A, Hall MN (1999) Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast. J Cell Biol. 146:1227–1238

    Article  PubMed  CAS  Google Scholar 

  • Beck T, Hall MN. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature. 402:689–692

    Article  PubMed  CAS  Google Scholar 

  • Bertram PG, Choi JH, Carvalho J, Ai Wandong, Zeng C, Chan TF Zheng XFS (2000) Tripartite regulation of Gln3 by TOR, Ure2p, and phosphatases. J. Biol. Chem. 275:35727–35733

    Article  PubMed  CAS  Google Scholar 

  • Cardenas ME, Cutler NS, Lorenz MC, Di Como CJ, Heitman J (1999) The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13, 3271–3279

    Article  PubMed  CAS  Google Scholar 

  • Chan TF, Bertram PG, Ai W, Zheng XFS (2001) Regulation of Apg14 expression by the GATA-type transcription factor Gln3p. J. Biol. Chem. 276:6463–6467

    Article  PubMed  CAS  Google Scholar 

  • Di Como CJ, Arndt KT (1996) Nutrients, via the TOR proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10:1904–1916

    Article  PubMed  Google Scholar 

  • Funakoshi T, Matsuura A, Noda T, Ohsumi Y (1997) Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae. Gene 192:207–13

    Article  PubMed  CAS  Google Scholar 

  • Hardwick J, Kuruvilla FG, Tong JK, Shamji AF, Schreiber SL. (1999) Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the TOR proteins. Proc. Natl. Acad. Sci. USA. 96:14866–14870

    Article  PubMed  CAS  Google Scholar 

  • Hinnebusch AG (1992) General and pathway-specific regulatory mechanisms controlling the synthesis of amino acid biosynthetic enzymes in Saccharomyces cerevisiae. In: Jones EW, Pringle JR, Broach JR (eds) The molecular and cellular biology of the yeast Saccharomyces vol. 2. Cold Spring Harbor Laboratory Press, pp 319–414

    Google Scholar 

  • Huang D, Farkas I, Roach PJ (1996) Pho85p, a cyclin-dependent protein kinase, and the Snf1p protein kinase act antagonistically to control glycogen accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4357–4365

    PubMed  CAS  Google Scholar 

  • Hutchins U, Klionsky DJ (2001) Vacuolar localization of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J. Biol. Chem. 2001 276:20491–20498

    Article  PubMed  CAS  Google Scholar 

  • Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y (2000) A ubiquitin-like system mediates protein lipidation. Nature 408:488–492

    Article  PubMed  CAS  Google Scholar 

  • Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, Yoshimori T, Noda T, Ohsumi Y (2001) Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol. Biol. Cell 12:3690–3702

    PubMed  CAS  Google Scholar 

  • Jiang Y, Broach J (1999) TOR proteins and protein phosphatase 2A reciprocally regulated Tap42 in controlling cell growth in yeast. EMBO J. 18, 2782–2792

    Article  PubMed  CAS  Google Scholar 

  • Johnston M, Carlson M (1992) Regulation of carbon and phosphate utilization. In: Jones EW, Pringle JR, Broach JR (eds) The molecular and cellular biology of the yeast Saccharomyces vol. 2. Cold Spring Harbor Laboratory Press, pp 193–281

    Google Scholar 

  • Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y (2000) TOR-mediated induction of autophagy via an Apg1 protein kinase complex. J. Cell Biol. 150:1507–1513

    Article  PubMed  CAS  Google Scholar 

  • Kametaka S, Okano T, Ohsumi M, Ohsumi Y (1998) Apg14p and Apg6/Vps30p form a protein complex essential for autophagy in the yeast, Saccharomyces cerevisiae. J. Biol. Chem. 273:22284–22291

    Article  PubMed  CAS  Google Scholar 

  • Kihara A, Noda T, Ishihara N, Ohsumi Y (2001) Two distinct Vps34 phosphatidyl-inositol 3-kinase complex function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152:519–530

    Article  PubMed  CAS  Google Scholar 

  • Kim J, Kamada Y, Stromhaug PE Hefner-Gravink A, Baba M, Scott SV, Ohsumi Y, Dunn Jr. WA Klionsky DJ (2001) Cvt9/Gsa9 functions in sequestering selective cy-tosolic cargo destined for the vacuole. J. Cell Biol. 153:381–396

    Article  PubMed  CAS  Google Scholar 

  • 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/Aut7 in yeast. J Cell Biol. 147:435–446

    Article  PubMed  CAS  Google Scholar 

  • Kirisako T, Ichimura Y. Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y (2000) The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J. Cell Biol. 151:263–275

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ (1998) Nonclassical protein sorting to the yeast vacuole. J. Biol. Chem. 273:10807–10810

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ, Ohsumi Y (1999) Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell. Dev. Biol. 15:1–32

    Article  PubMed  CAS  Google Scholar 

  • Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf DH Thumm M (1998) Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J. 17:3597–3607

    Article  PubMed  CAS  Google Scholar 

  • Magasanik B (1992) Regulation of nitrogen utilization. In: Jones EW, Pringle JR, Broach JR (eds) The molecular and cellular biology of the yeast Saccharomyces vol. 2. Cold Spring Harbor Laboratory Press, pp 283–317

    Google Scholar 

  • Matsuura A, Tsukada M, Wada Y, Ohsumi Y (1997) Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192:245–250

    Article  PubMed  CAS  Google Scholar 

  • Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y (1998) A protein conjugation system essential for autophagy. Nature 395:395–398

    Article  PubMed  CAS  Google Scholar 

  • Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, Marton MJ (2001) Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21:4347–4368

    Article  PubMed  CAS  Google Scholar 

  • Noda T, Matsuura A, Wada Y, Ohsumi Y (1995) Novel system for monitoring autophagy in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun.. 210:126–132

    Article  PubMed  CAS  Google Scholar 

  • Noda T, Ohsumi Y (1998) TOR, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem. 273:3963–3966

    Article  PubMed  CAS  Google Scholar 

  • Rabitsch KP, Toth A, Galova M, Schleiffer A, Schaffher G, Aigner E, Rupp C, Penkner AM, Moreno-Borchart AAC, Primig M, Esposito RE, Klein F, Knop M, Nasmyth K (2001) A screen for genes required for meiosis and spore formation based on whole-genome expression. Current Biol. 11:1001–1009

    Article  CAS  Google Scholar 

  • Schmidt A, Beck T, Roller A, Kunz J, Hall MN (1998) The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J. 17, 6924–6931

    Article  PubMed  CAS  Google Scholar 

  • Scott SV, Hefner-Gravink A, Morano KA, Noda T, Ohsumi Y, Klionsky DJ (1996) Cy-toplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl. Acad. Sci. USA. 93:12304–12308

    Article  PubMed  CAS  Google Scholar 

  • Scott SV, Nice III DC, Nau JJ Weisman LS, Kamada Y, Keizer-Gunnink I, Funakoshi T, Veenhuis M, Ohsumi Y, Klionsky DJ (2000) Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J. Biol. Chem. 275:25840–25849

    Article  PubMed  CAS  Google Scholar 

  • Takeshige K, Baba, M, Tsuboi S, Noda T, Ohsumi Y (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 119:301–311

    Article  PubMed  CAS  Google Scholar 

  • Talloczy Z, Jiang W, Virgin IV H, Leib DA, Scheuner D, Kaufman RJ, Eskellinen EL Levine B (2002) Regulation of starvation- and virus-induced autophagy by the eIF2α kinase signaling pathway. Proc. Natl. Acad. Sci. USA. 99:190–195

    Article  PubMed  CAS  Google Scholar 

  • Thomas G, Hall MN (1997) TOR signalling and control of cell growth. Curr. Opi. in Cell Biol. 9, 782–787

    Article  CAS  Google Scholar 

  • Thumm M, Egner R, Koch B, Schlumpberger M, Straub M, Veenhuis M, Wolf DH (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349:275–280

    Article  PubMed  CAS  Google Scholar 

  • Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333:169–174

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Wilson WA, Fujino MA, Roach PJ (2001) Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol. Cell. Biol. 21:5742–5752

    Article  PubMed  CAS  Google Scholar 

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© 2004 Springer-Verlag Berlin Heidelberg

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Kamada, Y., Sekito, T., Ohsumi, Y. (2004). Autophagy in Yeast: ATOR-Mediated Response to Nutrient Starvation. In: Thomas, G., Sabatini, D.M., Hall, M.N. (eds) TOR. Current Topics in Microbiology and Immunology, vol 279. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-18930-2_5

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  • DOI: https://doi.org/10.1007/978-3-642-18930-2_5

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-62360-8

  • Online ISBN: 978-3-642-18930-2

  • eBook Packages: Springer Book Archive

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