Mtl1 O-mannosylation mediated by both Pmt1 and Pmt2 is important for cell survival under oxidative conditions and TOR blockade

Fungal Genetics and Biology

Volumn 49, Issue 11, 2012, Pages 903-914

  Petkova, Mima Ivanova ^a   Pujol Carrion, Nuria ^a   de la Torre Ruiz, Maria Angeles ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

Author keywords

Cell wall integrity (CWI); Mtl1; N glycosylation; O mannosylation; Oxidative stress; Pkc1; Pmt2; Rapamycin; Slt2; TOR

Indexed keywords

FUNGAL PROTEIN; MEMBRANE PROTEIN; MTL1 PROTEIN; PMT1 PROTEIN; PMT2 PROTEIN; PMT4 PROTEIN; RAPAMYCIN; ROM2 PROTEIN; SLT2 PROTEIN; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; BUD; CELL SURVIVAL; CELL WALL; CONTROLLED STUDY; CYTOPLASM; FUNGUS MUTANT; NONHUMAN; O MANNOSYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; UPREGULATION;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, FUNGAL; GLYCOSYLATION; MANNOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RAS PROTEINS; RECEPTORS, CELL SURFACE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 84867905955     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.08.005     Document Type: Article

References (55)

1. Arroyo J., Hutzler J., Bermejo C., Ragni E., García-Cantalejo J., Botías P., Piberger H., Schott A., Sanz B.S., Strahl S. Functional and genomic analyzes of blocked protein O-mannosylation in baker's yeast. Mol. Microbiol. 2011, 79:1529-1546.
2. Chen Y., Feldman D.E., Deng C., Brown J.A., De Giacomo A.F., Gaw A.F., Shi G., Le Q.T., Brown J.M., Koong A.C. Identification of mitogen-activated protein kinase signaling pathways that confer resistance to endoplasmic reticulum stress in Saccharomyces cerevisiae. Mol. Cancer Res. 2005, 3:669-677.
3. Crespo J.L., Hall M.N. Elucidating TOR signaling and rapamycin action: lessons from Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2002, 66:579-591.
4. de la Torre-Ruiz M.A., Torres J., Ariño J., Herrero E. Sit4 is required for proper modulation of the biological functions mediated by Pkc1 and the cell integrity pathway in Saccharomyces cerevisiae. J. Biol. Chem. 2002, 277:33468-33476.
5. de la Torre-Ruiz M.A., Mozo-Villarías A., Pujol N., Petkova M.I. How budding yeast sense and transduce the oxidative stress signal and the impact in cell growth and morphogenesis. Curr. Protein Pept. Sci. 2010, 11:669-679.
6. De Nobel H., Ruiz C., Martin H., Morris W., Brul S., Molina M., Klis F.M. Cell wall perturbation in yeast results in dual phosphorylation of the Slt2/Mpk1 MAP kinase and in an Slt2-mediated increase in FKS2-lacZ expression, glucanase resistance and thermotolerance. Microbiology 2000, 146:2121-2132.
7. Delley P.A., Hall M.N. Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J. Cell Biol. 1999, 147:163-174.
8. Fuchs B.B., Mylonakis E. Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot. Cell. 2009, 8:1616-1625.
9. Gallego C., Garí E., Colomina N., Herrero E., Aldea M. The Cln3 cyclin is down-regulated by translational repression and degradation during G1 arrest caused by nitrogen deprivation in budding yeast. EMBO J. 1997, 16:7196-7206.
10. Garí E., Piedrahita L., Aldea M., Herrero E. A set of vectors with tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 1997, 13:837-848.
11. Gentzsch M., Tanner W. The PMT gene family: protein O-glycosylation in Saccharomyces cerevisiae is vital. EMBO J. 1996, 15:5752-5759.
12. Gentzsch M., Tanner W. Protein-O-glycosylation in yeast: protein specific mannosyltransferases. Glycobiology 1997, 7:481-486.
13. Gietz D., St Jean A., Woods R.A., Schiestl R.H. Improved method for high efficiency transformation of intact yeast cells. Nucl. Acids Res. 1992, 20:1425.
14. Girrbach V., Strahl S. Members of the evolutionarily conserved PMT family of protein O-mannosyltransferases form distinct protein complexes among themselves. J. Biol. Chem. 2003, 278:12554-12562.
15. Goldstein A.L., McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 1999, 15:1541-1553.
16. Goërner W., Durchschlag E., Martinez-Pastor M.T., Estruch F., Ammerer G., Hamilton B., Ruis H., Schüller C. Nuclear localization of the C2H2 zing finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 1998, 12:586-597.
17. Gray J.V., Ogas J.P., Kamada Y., Stone M., Levin D.E., Herskowitz I. A role for the Pkc1 MAP kinase pathway of Saccharomyces cerevisiae in bud emergence and identification of a putative upstream regulator. EMBO J. 1997, 16:4924-4937.
18. Heinisch J.J., Lorberg A., Schmitz H.P., Jacoby J.J. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol. Microbiol. 1999, 32:671-680.
19. Helliwell S.B., Schmidt A., Ohya Y., Hall M.N. The Rho1 effector Pkc1, but not Bni1, mediates signalling from Tor2 to the actin cytoskeleton. Curr. Biol. 1998, 8:1211-1214.
20. Hutzler J., Schmid M., Bernard T., Henrissat B., Strahl S. Membrane association is a determinant for substrate recognition by PMT4 protein O-mannosyltransferases. Proc. Natl. Acad. Sci. USA 2007, 104:7827-7832.
21. Kaiser C., Michaelis S., Mitchell A. Methods in Yeast Genetics 1994, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Ketela T., Green R., Bussey H. Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J. Bacteriol. 1999, 181:3330-3340.
23. Klis F.M., Boorsma A., De Groot P.W. Cell wall construction in Saccharomyces cerevisiae. Yeast 2006, 23:185-202.
24. Krause S.A., Gray J.V. The protein kinase C pathway is required for viability in quiescence in Saccharomyces cerevisiae. Curr. Biol. 2002, 12:588-593.
25. Lagorce A., Hauser N.C., Labourdette D., Rodriguez C., Martin-Yken H., Arroyo J., Hoheisel J.D., Francois J.M. Genome-wide analysis of the response to cell wall mutations in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278:20345-20357.
26. Lehle L., Strahl S., Tanner W. Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. 2006, 45:6802-6818.
27. Lengeler K.B., Tielker D., Ernst J.F. Protein-O-mannosyltransferases in virulence and development. Cell. Mol. Life Sci. 2008, 65:528-544.
28. Levin D.E. Cell wall integrity signalling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2005, 69:262-291.
29. Loewith R., Jacinto E., Wullschleger S., Lorberg A., Crespo J.L., Bonenfant D., Oppliger W., Jenoe P., Hall M.N. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell. 2002, 10:457-468.
30. Lommel M., Strahl S. Protein O-mannosylation: conserved from bacteria to humans. Glycobiology 2009, 19:816-828.
31. Lommel M., Bagnat M., Strahl S. Aberrant processing of the WSC family and Mid2p cell surface sensors results in cell death of Saccharomyces cerevisiae O-mannosylation mutants. Mol. Cell. Biol. 2004, 24:46-57.
32. Martín H., Rodríguez-Pachón J.M., Ruiz C., Nombela C., Molina M. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J. Biol. Chem. 2000, 275:1511-1519.
33. Martin D.E., Soulard A., Hall M.N. TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 2004, 119:969-979.
34. Motizuki M., Yokota S., Tsurugi K. Effect of low pH on organization of the actin cytoskeleton in Saccharomyces cerevisiae. Biochim. Biophys. Acta 2008, 1780:179-184.
35. Park J.I., Collinson E.J., Grant C.M., Dawes I.W. Rom2p, the Rho1 GTP/GDP exchange factor of Saccharomyces cerevisiae, can mediate stress responses via the Ras-cAMP pathway. J. Biol. Chem. 2005, 280:2529-2535.
36. Petkova M.I., Pujol-Carrion N., Arroyo J., García-Cantalejo J., de la Torre-Ruiz M.A. Mtl1 is required to activate general stress response through Tor1 and Ras2 inhibition under conditions of glucose starvation and oxidative stress. J. Biol. Chem. 2010, 285:19521-19531.
37. Petkova M.I., Pujol-Carrion N., de la Torre-Ruiz M.A. Signal flow between CWI/TOR and CWI/RAS in budding yeast under conditions of oxidative stress and glucose starvation. Commun. Integr. Biol. 2010, 3:555-557.
38. Philip B., Levin D.E. Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell. Biol. 2001, 21:271-280.
39. Rajavel M., Philip B., Buehrer B.M., Errede B., Levin D.E. Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:3969-3976.
40. Santangelo G.M. Glucose signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2006, 70:253-282.
41. Schmelzle T., Beck T., Martin D.E., Hall M.N. Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 2004, 24:338-351.
42. Serrano R., Martín H., Casamayor A., Ariño J. Signaling alkaline pH stress in Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway. J. Biol. Chem. 2006, 281:39785-39795.
43. Sobering A.K., Jung U.S., Lee K.S., Levin D.E. Yeast Rpi1 is a putative transcriptional regulator that contributes to preparation for stationary phase. Eukaryot. Cell 2002, 1:56-65.
44. Soulard A., Cremonesi A., Moes S., Schütz F., Jenö P., Hall M.N. The rapamycin-sensitive phosphoproteome reveals that TOR controls protein kinase A toward some some but not all substrates. Mol. Biol. Cell. 2010, 21:3475-3486.
45. Strahl-Bolsinger S., Immervoll T., Deutzmann R., Tanner W. PMT1 the gene for a key enzyme of protein O-glycosylation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1993, 90:8164-8168.
46. Strahl-Bolsinger S., Gentzsch M., Tanner W. Protein O-mannosylation. Biochim. Biophys. Acta 1999, 1426:297-307.
47. Tanner W., Lehle L. Protein glycosylation in yeast. Biochim. Biophys. Acta 1987, 906:81-99.
48. Torres J., Di Como C.J., Herrero E., de la Torre-Ruiz M.A. Regulation of the cell integrity pathway by rapamycin-sensitive TOR function in budding yeast. J. Biol. Chem. 2002, 277:43495-43504.
49. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000, 101:249-258.
50. Verna J., Lodder A., Lee K., Vagts A., Ballester R. A family of genes required for the maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1997, 94:13804-13809.
51. Vilella F., Herrero E., Torres J., de la Torre-Ruiz M.A. Pkc1 and the upstream elements of the cell integrity pathway in Saccharomyces cerevisiae, Rom2 and Mtl1, are required for cellular responses to oxidative stress. J. Biol. Chem. 2005, 280:9149-9159.
52. Wach A., Brachat A., Pohlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 1994, 10:1793-1808.
53. Willer T., Valero M.C., Tanner W., Cruces J., Strahl S. O-mannosyl glycans: from yeast to novel associations with human disease. Curr. Opin. Struct. Biol. 2003, 13:621-630.
54. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
55. Zurita-Martinez S.A., Cardenas M.E. Tor and cyclic AMP-protein kinase A: two parallel pathways regulating expression of genes required for cell growth. Eukaryot. Cell 2005, 4:63-71.