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PMID: 9475724 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae.

Genetics ·Vol. 148 ·No. 1 ·1998-01-00 ·Pages 99-112

Helliwell SB, Howald I, Barbet N, Hall MN

Abstract

The Saccharomyces cerevisiae genes TOR1 and TOR2 encode phosphatidylinositol kinase homologs. TOR2 has two essential functions. One function overlaps with TOR1 and mediates protein synthesis and cell cycle progression. The second essential function of TOR2 is unique to TOR2 and mediates the cell-cycle-dependent organization of the actin cytoskeleton. We have isolated temperature-sensitive mutants that are defective for either one or both of the two TOR2 functions. The three classes of mutants were as follows. Class A mutants, lacking only the TOR2-unique function, are defective in actin cytoskeleton organization and arrest within two to three generations as small-budded cells in the G2/M phase of the cell cycle. Class B mutants, lacking only the TOR-shared function, and class C mutants, lacking both functions, exhibit a rapid loss of protein synthesis and a G1 arrest within one generation. To define further the two functions of TOR2, we isolated multicopy suppressors that rescue the class A or B mutants. Overexpression of MSS4, PKC1, PLC1, RHO2, ROM2, or SUR1 suppressed the growth defect of a class A mutant. Surprisingly, overexpression of PLC1 and MSS4 also suppressed the growth defect of a class B mutant. These genes encode proteins that are involved in phosphoinositide metabolism and signaling. Thus, the two functions (readouts) of TOR2 appear to involve two related signaling pathways controlling cell growth.

MeSH Terms
Cell Cycle Proteins Cell Division/genetics Fungal Proteins/biosynthesis,physiology G1 Phase G2 Phase Genes, Fungal/genetics Metaphase Mutation Phosphatidylinositol 3-Kinases Phosphotransferases (Alcohol Group Acceptor)/physiology Saccharomyces cerevisiae/cytology,genetics,growth & development Saccharomyces cerevisiae Proteins Signal Transduction/genetics
Chemicals
Cell Cycle Proteins Fungal Proteins Saccharomyces cerevisiae Proteins Phosphotransferases (Alcohol Group Acceptor) TOR2 protein, S cerevisiae
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Helliwell S B
Department of Biochemistry, Biozentrum, University of Basel, Switzerland.
Howald I
Barbet N
Hall M N
References (37)
37 references, click to expand
  1. RAPT1, a mammalian homolog of yeast Tor, interacts with the FKBP12/rapamycin complex.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12574-8 PMID: 7809080
  2. Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells.
    J Biol Chem. 1995 Jan 13;270(2):815-22 PMID: 7822316
  3. The CLS2 gene encodes a protein with multiple membrane-spanning domains that is important Ca2+ tolerance in yeast.
    Mol Gen Genet. 1995 Feb 6;246(3):269-81 PMID: 7854312
  4. TOR kinase domains are required for two distinct functions, only one of which is inhibited by rapamycin.
    Cell. 1995 Jul 14;82(1):121-30 PMID: 7606777
  5. Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast.
    Mol Biol Cell. 1995 May;6(5):525-39 PMID: 7663021
  6. Control of p70 s6 kinase by kinase activity of FRAP in vivo.
    Nature. 1995 Oct 5;377(6548):441-6 PMID: 7566123
  7. A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae.
    EMBO J. 1995 Dec 1;14(23):5931-8 PMID: 8846785
  8. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation.
    EMBO J. 1996 Feb 1;15(3):658-64 PMID: 8599949
  9. Activation of yeast protein kinase C by Rho1 GTPase.
    J Biol Chem. 1996 Apr 19;271(16):9193-6 PMID: 8621575
  10. Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding protein in Saccharomyces cerevisiae.
    EMBO J. 1996 May 1;15(9):2196-207 PMID: 8641285
  11. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases.
    Genes Dev. 1996 Aug 1;10(15):1904-16 PMID: 8756348
  12. TOR controls translation initiation and early G1 progression in yeast.
    Mol Biol Cell. 1996 Jan;7(1):25-42 PMID: 8741837
  13. Coordinated regulation of gene expression by the cell cycle transcription factor Swi4 and the protein kinase C MAP kinase pathway for yeast cell integrity.
    EMBO J. 1996 Sep 16;15(18):5001-13 PMID: 8890173
  14. TOR2 is required for organization of the actin cytoskeleton in yeast.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13780-5 PMID: 8943012
  15. The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2.
    Cell. 1997 Feb 21;88(4):531-42 PMID: 9038344
  16. TOR signalling and control of cell growth.
    Curr Opin Cell Biol. 1997 Dec;9(6):782-7 PMID: 9425342
  17. Phenotypic analysis of temperature-sensitive yeast actin mutants.
    Cell. 1985 Feb;40(2):405-16 PMID: 3967297
  18. Isolation of the NPR1 gene responsible for the reactivation of ammonia-sensitive amino-acid permeases in Saccharomyces cerevisiae. RNA analysis and gene dosage effects.
    Eur J Biochem. 1987 May 4;164(3):607-12 PMID: 3552673
  19. Fluorescence microscopy methods for yeast.
    Methods Cell Biol. 1989;31:357-435 PMID: 2476649
  20. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle.
    Cell. 1990 Jul 27;62(2):213-24 PMID: 2196995
  21. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast.
    Methods Enzymol. 1991;194:302-18 PMID: 2005795
  22. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast.
    Science. 1991 Aug 23;253(5022):905-9 PMID: 1715094
  23. Yeast mutant affected for viability upon nutrient starvation: characterization and cloning of the RVS161 gene.
    Yeast. 1991 Oct;7(7):727-43 PMID: 1776363
  24. Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect.
    J Cell Biol. 1992 Mar;116(5):1221-9 PMID: 1740473
  25. The putative phosphoinositide-specific phospholipase C gene, PLC1, of the yeast Saccharomyces cerevisiae is important for cell growth.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1804-8 PMID: 8383328
  26. Yeast mutants affected in viability upon starvation have a modified phospholipid composition.
    Yeast. 1993 Mar;9(3):267-77 PMID: 8488727
  27. Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression.
    Cell. 1993 May 7;73(3):585-96 PMID: 8387896
  28. A mutation in PLC1, a candidate phosphoinositide-specific phospholipase C gene from Saccharomyces cerevisiae, causes aberrant mitotic chromosome segregation.
    Mol Cell Biol. 1993 Jul;13(7):4351-64 PMID: 8391635
  29. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns.
    Mol Cell Biol. 1993 Aug;13(8):5070-84 PMID: 8336735
  30. Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Sep;13(9):5861-76 PMID: 8395015
  31. Dominant missense mutations in a novel yeast protein related to mammalian phosphatidylinositol 3-kinase and VPS34 abrogate rapamycin cytotoxicity.
    Mol Cell Biol. 1993 Oct;13(10):6012-23 PMID: 8413204
  32. The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae.
    J Cell Biol. 1993 Dec;123(6 Pt 2):1821-33 PMID: 8276900
  33. A novel gene, STT4, encodes a phosphatidylinositol 4-kinase in the PKC1 protein kinase pathway of Saccharomyces cerevisiae.
    J Biol Chem. 1994 Jan 14;269(2):1166-72 PMID: 8288577
  34. Genetic interactions among genes involved in the STT4-PKC1 pathway of Saccharomyces cerevisiae.
    Mol Gen Genet. 1994 Mar;242(6):631-40 PMID: 8152413
  35. TOR1 and TOR2 are structurally and functionally similar but not identical phosphatidylinositol kinase homologues in yeast.
    Mol Biol Cell. 1994 Jan;5(1):105-18 PMID: 8186460
  36. A mammalian protein targeted by G1-arresting rapamycin-receptor complex.
    Nature. 1994 Jun 30;369(6483):756-8 PMID: 8008069
  37. RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs.
    Cell. 1994 Jul 15;78(1):35-43 PMID: 7518356
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1998-01-00
Pages
99-112
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1459785
Subset
IM
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