A truncated form of K1Lsm4p and the absence of factors involved in mRNA decapping trigger apoptosis in yeast

Molecular Biology of the Cell

Volumn 14, Issue 2, 2003, Pages 721-729

  Mazzoni, Cristina ^a   Mancini, Patrizia ^a,b   Verdone, Loredana ^a   Madeo, Frank ^c   Serafini, Agnese ^a   Herker, Eva ^c   Falcone, Claudio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; DNA FRAGMENT; FUNGAL PROTEIN; MESSENGER RNA; MESSENGER RNA PRECURSOR; MUTANT PROTEIN; PROTEIN KLLSM4P; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; DHH1 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; PAT1 PROTEIN, S CEREVISIAE; RNA; RNA BINDING PROTEIN; RNA HELICASE; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL VIABILITY; CHROMATIN CONDENSATION; DELETION MUTANT; KLUYVEROMYCES; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN VARIANT; RNA CAPPING; RNA DECAPPING; RNA DEGRADATION; RNA SPLICING; RNA STABILITY; SACCHAROMYCES CEREVISIAE; ALLELE; CHEMISTRY; CHROMATIN; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENE DELETION; GENETICS; GENOTYPE; METABOLISM; NICK END LABELING; PROTEIN TERTIARY STRUCTURE; SERODIAGNOSIS;

KLUYVEROMYCES LACTIS; SACCHAROMYCES CEREVISIAE;

ALLELES; APOPTOSIS; CHROMATIN; DEAD-BOX RNA HELICASES; DNA FRAGMENTATION; DNA-BINDING PROTEINS; GENE DELETION; GENOTYPE; IN SITU NICK-END LABELING; KLUYVEROMYCES; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; PHENOTYPE; PRECIPITIN TESTS; PROTEIN STRUCTURE, TERTIARY; REACTIVE OXYGEN SPECIES; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RNA; RNA HELICASES; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 0037326056     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-05-0258     Document Type: Article

References (43)

1. Beelman, C.A., Stevens, A., Caponigro, G., LaGrandeur, T.E., Hatfield, L., Fortner, D.M., and Parker, R. (1996). An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 382, 642-646.
2. Bonnerot, C., Boeck, R., and Lapeyre, B. (2000). The two proteins Pat1p (Mrt1p) and Spb8p interact in vivo, are required for mRNA decay, and are functionally linked to Pab1p. Mol. Cell. Biol. 20, 5939-5946.
3. Boorstein, W.R., and Craig, E.A. (1990). Structure and regulation of the SSA4 HSP70 gene of Saccharomyces cerevisiae. J. Biol. Chem. 265, 18912-18921.
4. Bouveret, E., Rigaut, G., Shevchenko, A., Wilm, M., and Seraphin, B. (2000). A Sm-like protein complex that participates in mRNA degradation. EMBO J. 19, 1661-1671.
5. Coller, J.M., Tucker, M., Sheth, U., Valencia-Sanchez, M.A., and Parker, R. (2001). The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 7, 1717-1727.
6. Cooper, M., Johnston, L.H., and Beggs, J.D. (1995). Identification and characterization of Uss1p (Sdb23p): a novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J. 14, 2066-2075.
7. Cornillon, S., Foa, C., Davoust, J., Buonavista, N., Gross, J.D., and Golstein, P. (1994). Programmed cell death in Dictyostelium. J. Cell Sci. 107, 2691-2704.
8. Dunckley, T., and Parker, R. (1999). The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 18, 5411-5422.
9. Fischer, N., and Weis, K. (2002). The DEAD box protein Dhh1 stimulates the decapping enzyme Dcp1. EMBO J. 21, 2788-2797.
10. Frohlich, K.U., and Madeo, F. (2000). Apoptosis in yeast - a monocellular organism exhibits altruistic behavior. FEBS Lett. 473, 6-9.
11. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S.A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
12. Gross, A., Pilcher, K., Blachly-Dyson, E., Basso, E., Jockel, J., Bassik, M.C., Korsmeyer, S.J., and Forte, M. (2000). Biochemical and genetic analysis of the mitochondrial response of yeast to BAX and BCL-X(L). Mol. Cell. Biol. 20, 3125-3136.
13. Guhaniyogi, J., and Brewer, G. (2001). Regulation of mRNA stability in mammalian cells. Gene 265, 11-23.
14. Hatfield, L., Beelman, C.A., Stevens, A., and Parker, R. (1996). Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 5830-5838.
15. He, W., and Parker, R. (2000). Functions of Lsm proteins in mRNA degradation and splicing. Curr. Opin. Cell Biol. 12, 346-350.
16. He, W., and Parker, R. (2001). The yeast cytoplasmic LsmI/Pat1p complex protects mRNA 3′ termini from partial degradation. Genetics 158, 1445-1455.
17. Hughes, J.M.X., Konings, D.A.M., and Cesareni, G. (1987). The yeast homologue of U3 snRNA. EMBO J. 8, 2145-2155.
18. Huh, G.H., Damsz, B., Matsumoto, T.K., Reddy, M.P., Rus, A.M., Ibeas, J.I., Narasimhan, M.L., Bressan, R.A., and Hasegawa, P.M. (2002). Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J. 29, 649-659.
19. Kaiser, C.A., and Schekman, R. (1990). Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 61, 723-733.
20. Kissova, I., Polcic, P., Kempna, P., Zeman, I., Sabova, L., and Kolarov, J. (2000). The cytotoxic action of Bax on yeast cells does not require mitochondrial ADP/ATP carrier but may be related to its import to the mitochondria. FEBS Lett. 471, 113-118.
21. LaGrandeur, T.E., and Parker, R. (1998). Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme. EMBO J. 17, 1487-1496.
22. Lam, L.T., et al. (2001). Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol. 2, 0041.1-0041.11.
23. Laun, P., Pichova, A., Madeo, F., Fuchs, J., Ellinger, A., Kohlwein, S., Dawes, I., Frohlich, K.U., and Breitenbach, M. (2001). Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol. Microbiol. 39, 1166-1173.
24. Lazebnik, Y.A., Cole, S., Cooke, C.A., Nelson, W.G., and Earnshaw, W.C. (1993). Nuclear events of apoptosis in vitro in cell-free mitotic extracts: a model system for analysis of the active phase of apoptosis. J. Cell Biol. 123, 7-22.
25. Levine, A., Belenghi, B., Damari-Weisler, H., and Granot, D. (2001). Vesicle-associated membrane protein of Arabidopsis suppresses Bax-induced apoptosis in yeast downstream of oxidative burst. J. Biol. Chem. 276, 46284-46289.
26. Ligr, M., Madeo, F., Frohlich, E., Hilt, W., Frohlich, K.U., and Wolf, D.H. (1998). Mammalian Bax triggers apoptotic changes in yeast. FEBS Lett. 438, 61-65.
27. Ligr, M., Velten, I., Frohlich, E., Madeo, F., Ledig, M., Frohlich, K.U., Wolf, D.H., and Hilt, W. (2001). The proteasomal substrate Stm1 participates in apoptosis-like cell death in yeast. Mol. Biol. Cell 12, 2422-2432.
28. Madeo, F., Engelhardt, S., Herker, E., Lehmann, N., Maldener, C., Proksch, A., Wissing, S., and Frohlich, K.U. (2002a). Apoptosis in yeast: a new model system with applications in cell biology and medicine. Curr. Genet. 41, 208-216.
29. Madeo, F., Frohlich, E., and Frohlich, K.U. (1997). A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139, 729-734.
30. Madeo, F., Frohlich, E., Ligr, M., Gray, M., Sigrist, S.J., Wolf, D.H., and Frohlich, K.U. (1999). Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145, 757-767.
31. Madeo, F., et al. (2002b). A caspase-related protease regulates apoptosis in yeast. Mol Cell 9, 911-917.
32. Mayes, A.E., Verdone, L., Legrain, P., and Beggs, J.D. (1999). Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J. 18, 4321-4331.
33. Mazzoni, C., and Falcone, C. (2001). Isolation and study of K1LSM4, a Kluyveromyces lactis gene homologous to the essential gene LSM4 of Saccharomyces cerevisiae. Yeast 18, 1249-1256.
34. Narasimhan, M.L., Damsz, B., Coca, M.A., Ibeas, J.I., Yun, D.J., Pardo, J.M., Hasegawa, P.M., and Bressan, R.A. (2001). A plant defense response effector induces microbial apoptosis. Mol. Cell 8, 921-930.
35. Nissim-Rafinia, M., and Kerem, B. (2002). Splicing regulation as a potential genetic modifier. Trends Genet. 18, 123-127.
36. Reed, J.C., and Green, D.R. (2002). Remodeling for demolition: changes in mitochondrial ultrastructure during apoptosis. Mol Cell 9, 1-3.
37. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
38. Saavedra, C.A., Hammel, C.M., Heath, C.V., and Cole, C.N. (1997). Yeast heat shock mRNAs are exported through a distinct pathway defined by Rip1p. Genes Dev. 11, 2845-56.
39. Schmitt, M.E., Brown, T.A., and Trumpower, B.L. (1990). A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18, 3091-3092.
40. Schulz, J.B., Weller, M., and Klockgether, T. (1996). Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J. Neurosci. 16, 4696-4706.
41. Tharun, S., He, W., Mayes, A.E., Lennertz, P., Beggs, J.D., and Parker, R. (2000). Yeast Sm-like proteins function in mRNA decapping, and decay. Nature 404, 515-518.
42. Tharun, S., and Parker, R. (2001). Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs. Mol. Cell 8, 1075-1083.
43. Wyers, F., Minet, M., Dufour, M.E., Vo, L.T., and Lacroute, F. (2000). Deletion of the PAT1 gene affects translation initiation and suppresses a PAB1 gene deletion in yeast. Mol. Cell. Biol. 20, 3538-3549.