The Paf1 complex subunit rtf1 buffers cells against the toxic effects of [PSI+] and defects in rkr1-dependent protein quality control in Saccharomyces cerevisiae

Genetics

Volumn 191, Issue 4, 2012, Pages 1107-1118

  Klucevsek, Kristin M ^a   Braun, Mary A ^a,b   Arndt, Karen M ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 104; MEMBRANE PROTEIN; PROTEIN PAF1; PROTEIN RKR1; PROTEIN RTF1; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOTRANSFORMATION; CONFOCAL MICROSCOPY; FUNGAL STRAIN; FUNGUS GROWTH; GENE DELETION; GENE INACTIVATION; GENE LOSS; HETEROZYGOTE; HISTONE MODIFICATION; IMMUNOFLUORESCENCE; MUTATIONAL ANALYSIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SUBUNIT; PROTEIN SYNTHESIS; QUALITY CONTROL; SACCHAROMYCES CEREVISIAE; TRANSPOSON; WESTERN BLOTTING;

DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, FUNGAL; GENES, LETHAL; GLUTATHIONE PEROXIDASE; HEAT-SHOCK PROTEINS; HISTONES; MUTAGENESIS, INSERTIONAL; NUCLEAR PROTEINS; PEPTIDE TERMINATION FACTORS; PHENOTYPE; PRIONS; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TATA-BOX BINDING PROTEIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84865068778     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.141713     Document Type: Article

References (69)

1. Alberti, S., R. Halfmann, O. King, A. Kapila, and S. Lindquist, 2009 A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137: 146-158.
2. Amberg, D. C., D. J. Burke, and J. N. Strathern, 2006 Yeast immunofluorescence. CSH Protoc, pii.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman et al., 1988 Current Protocols in Molecular Biology. Green Publishing Associates and Wiley-Interscience, New York.
4. Batta, K., Z. Zhang, K. Yen, D. B. Goffman, and B. F. Pugh, 2011 Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev. 25: 2254-2265.
5. Beggs, J. D., 2005 Lsm proteins and RNA processing. Biochem. Soc. Trans. 33: 433-438.
6. Bengtson, M. H., and C. A. Joazeiro, 2010 Role of a ribosomeassociated E3 ubiquitin ligase in protein quality control. Nature 467: 470-473.
7. Bradley, M. E., and S. W. Liebman, 2003 Destabilizing interactions among [PSI(+)] and [PIN(+)] yeast prion variants. Genetics 165: 1675-1685.
8. Bradley, M. E., S. Bagriantsev, N. Vishveshwara, and S. W. Liebman, 2003 Guanidine reduces stop codon read-through caused by missense mutations in SUP35 or SUP45. Yeast 20: 625-632.
9. Braun, M. A., P. J. Costa, E. M. Crisucci, and K. M. Arndt, 2007 Identification of Rkr1, a nuclear RING domain protein with functional connections to chromatin modification in Saccharomyces cerevisiae. Mol. Cell. Biol. 27: 2800-2811.
10. Burns, N., B. Grimwade, P. B. Ross-Macdonald, E. Y. Choi, K. Finberg et al., 1994 Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev. 8: 1087-1105.
11. Chernoff, Y. O., S. L. Lindquist, B. Ono, S. G. Inge-Vechtomov, and S. W. Liebman, 1995 Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268: 880-884.
12. Chu, J., N. A. Hong, C. A. Masuda, B. V. Jenkins, K. A. Nelms et al., 2009 A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. Proc. Natl. Acad. Sci. USA 106: 2097-2103.
13. Cox, J. S., R. E. Chapman, and P. Walter, 1997 The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8: 1805-1814.
14. Crisucci, E. M., and K. M. Arndt, 2011 The roles of the Paf1 complex and associated histone modifications in regulating gene expression. Genet. Res. Int.,15.
15. Crow, E. T., and L. Li, 2011 Newly identified prions in budding yeast, and their possible functions. Semin. Cell Dev. Biol. 22: 452-459.
16. Derkatch, I. L., M. E. Bradley, J. Y. Hong, and S. W. Liebman, 2001 Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 106: 171-182.
17. Dover, J., J. Schneider, M. A. Tawiah-Boateng, A. Wood, K. Dean et al., 2002 Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J. Biol. Chem. 277: 28368-28371.
18. Farber, L. J., E. J. Kort, P. Wang, J. Chen, and B. T. Teh, 2010 The tumor suppressor parafibromin is required for posttranscriptional processing of histone mRNA. Mol. Carcinog. 49: 215-223.
19. Fasken, M. B., and A. H. Corbett, 2005 Process or perish: quality control in mRNA biogenesis. Nat. Struct. Mol. Biol. 12: 482-488.
20. Ferreira, P. C., F. Ness, S. R. Edwards, B. S. Cox, and M. F. Tuite, 2001 The elimination of the yeast [PSI+] prion by guanidine hydrochloride is the result of Hsp104 inactivation. Mol. Microbiol. 40: 1357-1369.
21. Fleischer, T. C., C. M. Weaver, K. J. McAfee, J. L. Jennings, and A. J. Link, 2006 Systematic identification and functional screens of uncharacterized proteins associated with eukaryotic ribosomal complexes. Genes Dev. 20: 1294-1307.
22. Frischmeyer, P. A., A. van Hoof, K. O'Donnell, A. L. Guerrerio, R. Parker et al., 2002 An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295: 2258-2261.
23. Grimminger-Marquardt, V., and H. A. Lashuel, 2010 Structure and function of the molecular chaperone Hsp104 from yeast. Biopolymers 93: 252-276.
24. Harlow, E., and D. Lane, 1988 Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Haslberger, T., B. Bukau, and A. Mogk, 2010 Towards a unifying mechanism for ClpB/Hsp104-mediated protein disaggregation and prion propagation. Biochem. Cell Biol. 88: 63-75.
26. Hoffman, C. S., and F. Winston, 1987 A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272.
27. Hwang, W. W., S. Venkatasubrahmanyam, A. G. Ianculescu, A. Tong, C. Boone et al., 2003 A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol. Cell 11: 261-266.
28. Ivanov, I., K. C. Lo, L. Hawthorn, J. K. Cowell, and Y. Ionov, 2007 Identifying candidate colon cancer tumor suppressor genes using inhibition of nonsense-mediated mRNA decay in colon cancer cells. Oncogene 26: 2873-2884.
29. Jaehning, J. A., 2010 The Paf1 complex: Platform or player in RNA polymerase II transcription? Biochim. Biophys. Acta 1799: 379-388.
30. Jung, G., and D. C. Masison, 2001 Guanidine hydrochloride inhibits Hsp104 activity in vivo: a possible explanation for its effect in curing yeast prions. Curr. Microbiol. 43: 7-10.
31. Kumar, A., S. A. des Etages, P. S. Coelho, G. S. Roeder, and M. Snyder, 2000 High-throughput methods for the large-scale analysis of gene function by transposon tagging. Methods Enzymol. 328: 550-574.
32. Li, B., M. Carey, and J. L. Workman, 2007 The role of chromatin during transcription. Cell 128: 707-719.
33. Mackay, R. G., C. W. Helsen, J. M. Tkach, and J. R. Glover, 2008 The C-terminal extension of Saccharomyces cerevisiae Hsp104 plays a role in oligomer assembly. Biochemistry 47: 1918-1927.
34. Masison, D. C., H. K. Edskes, M. L. Maddelein, K. L. Taylor, and R. B. Wickner, 2000 [URE3] and [PSI] are prions of yeast and evidence for new fungal prions. Curr. Issues Mol. Biol. 2: 51-59.
35. Mathur, V., J. Y. Hong, and S. W. Liebman, 2009 Ssa1 overexpression and [PIN(+)] variants cure [PSI(+)] by dilution of aggregates. J. Mol. Biol. 390: 155-167.
36. Mayer, A., M. Lidschreiber, M. Siebert, K. Leike, J. Soding et al., 2010 Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol. 17: 1272-1278.
37. Mueller, C. L., S. E. Porter, M. G. Hoffman, and J. A. Jaehning, 2004 The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol. Cell 14: 447-456.
38. Mumberg, D., R. Muller, and M. Funk, 1995 Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119-122.
39. Mutiu, A. I., S. M. Hoke, J. Genereaux, G. Liang, and C. J. Brandl, 2007 The role of histone ubiquitylation and deubiquitylation in gene expression as determined by the analysis of an HTB1 (K123R) Saccharomyces cerevisiae strain. Mol. Genet. Genomics 277: 491-506.
40. Nagaike, T., C. Logan, I. Hotta, O. Rozenblatt-Rosen, M. Meyerson et al., 2011 Transcriptional activators enhance polyadenylation of mRNA precursors. Mol. Cell 41: 409-418.
41. Nagalakshmi, U., Z. Wang, K. Waern, C. Shou, D. Raha et al., 2008 The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349.
42. Ng, H. H., S. Dole, and K. Struhl, 2003 The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J. Biol. Chem. 278: 33625-33628.
43. Nordick, K., M. G. Hoffman, J. L. Betz, and J. A. Jaehning, 2008 Direct interactions between the Paf1 complex and a cleavage and polyadenylation factor are revealed by dissociation of Paf1 from RNA polymerase II. Eukaryot. Cell 7: 1158-1167.
44. Parsell, D. A., A. S. Kowal, M. A. Singer, and S. Lindquist, 1994 Protein disaggregation mediated by heat-shock protein Hsp104. Nature 372: 475-478.
45. Paushkin, S. V., V. V. Kushnirov, V. N. Smirnov, and M. D. Ter-Avanesyan, 1996 Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J. 15: 3127-3134.
46. Penheiter, K., T. Washburn, S. Porter, M. Hoffman, and J. Jaehning, 2005 A posttranscriptional role for the yeast Paf1-RNA poly-merase II complex is revealed by identification of primary targets. Mol. Cell 20: 213-223.
47. Rose, M. D., F. Winston, and P. Hieter, 1991 Methods in Yeast Genetics: A Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Rubel, A. A., A. F. Saifitdinova, A. G. Lada, A. A. Nizhnikov, S. G. Inge-Vechtomov et al., 2008 Yeast chaperone Hspl04 regulates gene expression on the posttranscriptional level. Mol. Biol. (Mosk.) 42: 123-130 (in Russian).
49. Scherer, S., and R. W. Davis, 1979 Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc. Natl. Acad. Sci. USA 76: 4951-4955.
50. Schneider-Poetsch, T., J. Ju, D. E. Eyler, Y. Dang, S. Bhat et al., 2010 Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6: 209-217.
51. Schwimmer, C., and D. C. Masison, 2002 Antagonistic interactions between yeast [PSI(+)] and [URE3] prions and curing of [URE3] by Hsp70 protein chaperone Ssa1p but not by Ssa2p. Mol. Cell. Biol. 22: 3590-3598.
52. Sheldon, K. E., D. M. Mauger, and K. M. Arndt, 2005 A requirement for the Saccharomyces cerevisiae Paf1 complex in snoRNA 39 end formation. Mol. Cell 20: 225-236.
53. Shorter, J., and S. Lindquist, 2006 Destruction or potentiation of different prions catalyzed by similar Hsp104 remodeling activities. Mol. Cell 23: 425-438.
54. Stolinski, L. A., D. M. Eisenmann, and K.M. Arndt, 1997 Identification of RTF1, a novel gene important for TATA site selection by TATA box-binding protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 17: 4490-4500.
55. Strawn, L. A., C. A. Lin, E. M. Tank, M. M. Osman, S. A. Simpson et al., 2009 Mutants of the Paf1 complex alter phenotypic expression of the yeast prion [PSI+]. Mol. Biol. Cell 20: 2229-2241.
56. Sun, Z. W., and C. D. Allis, 2002 Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
57. Tomson, B. N., C. P. Davis, M. H. Warner, and K. M. Arndt, 2011 Identification of a role for histone H2B ubiquitylation in noncoding RNA 39-end formation through mutational analysis of Rtf1 in Saccharomyces cerevisiae. Genetics 188: 273-289.
58. True, H. L., I. Berlin, and S. L. Lindquist, 2004 Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431: 184-187.
59. van Hoof, A., P. A. Frischmeyer, H. C. Dietz, and R. Parker, 2002 Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295: 2262-2264.
60. Wagner, E., and J. Lykke-Andersen, 2002 mRNA surveillance: the perfect persist. J. Cell Sci. 115: 3033-3038.
61. Warner, M. H., K. L. Roinick, and K. M. Arndt, 2007 Rtf1 is a multifunctional component of the Paf1 complex that regulates gene expression by directing cotranscriptional histone modification. Mol. Cell. Biol. 27: 6103-6115.
62. Wickner, R. B., H. K. Edskes, and F. Shewmaker, 2006 How to find a prion: [URE3], [PSI+] and [beta]. Methods 39: 3-8.
63. Wilson, M. A., S. Meaux, R. Parker, and A. van Hoof, 2005 Genetic interactions between [PSI+] and nonstop mRNA decay affect phenotypic variation. Proc. Natl. Acad. Sci. USA 102: 10244-10249.
64. Wilson, M. A., S. Meaux, and A. van Hoof, 2007 A genomic screen in yeast reveals novel aspects of nonstop mRNA metabolism. Genetics 177: 773-784.
65. Winston, F., C. Dollard, and S. L. Ricupero-Hovasse, 1995 Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55.
66. Wood, A., J. Schneider, J. Dover, M. Johnston, and A. Shilatifard, 2003 The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 278: 34739-34742.
67. Yoshihisa, T., and Y. Anraku, 1989 Nucleotide sequence of AMS1, the structure gene of vacuolar alpha-mannosidase of Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 163: 908-915.
68. Zheng, S., J. J. Wyrick, and J. C. Reese, 2010 Novel trans-tail regulation of H2B ubiquitylation and H3K4 methylation by the N terminus of histone H2A. Mol. Cell. Biol. 30: 3635-3645.
69. Zhou, P., I. L. Derkatch, and S. W. Liebman, 2001 The relationship between visible intracellular aggregates that appear after overexpression of Sup35 and the yeast prion-like elements [PSI (+)] and [PIN(+)]. Mol. Microbiol. 39: 37-46.