Cordycepin interferes with 3' end formation in yeast independently of its potential to terminate RNA chain elongation

RNA

Volumn 15, Issue 5, 2009, Pages 837-849

  Holbein, Sandra ^a   Wengi, Agnieszka ^a   Decourty, Laurence ^b   Freimoser, Florian M ^c   Jacquier, Alain ^b   Dichtl, Bernhard ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b INSTITUT PASTEUR   (France)

^c ETH ZURICH   (Switzerland)

Author keywords

3 end formation; ATP; Cordycepin; Poly(A); RNA; Saccharomyces cerevisiae; Transcription

Indexed keywords

CORDYCEPIN; DNA DIRECTED DNA POLYMERASE ALPHA; MESSENGER RNA; POLYADENYLIC ACID;

ARTICLE; CELL GROWTH; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCUS; GROWTH INHIBITION; HUMAN; PRIORITY JOURNAL; RNA METABOLISM; RNA SYNTHESIS; SACCHAROMYCES CEREVISIAE;

DEOXYADENOSINES; GENE EXPRESSION; GENOME, FUNGAL; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 65249104997     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1458909     Document Type: Article

References (60)

1. Ahn, Y.J., Park, S.J., Lee, S.G., Shin, S.C., and Choi, D.H. 2000. Cordycepin: Selective growth inhibitor derived from liquid culture of Cordyceps militaris against Clostridium spp. J. Agric. Food Chem. 48: 2744-2748.
2. Amberg, D.C., Goldstein, A.L., and Cole, C.N. 1992. Isolation and characterization of RAT1: An essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes & Dev. 6: 1173-1189.
3. Amiott, E.A. and Jaehning, J.A. 2006. Mitochondrial transcription is regulated via an ATP "sensing" mechanism that couples RNA abundance to respiration. Mol. Cell 22: 329-338.
4. Arigo, J.T., Eyler, D.E., Carroll, K.L., and Corden, J.L. 2006. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23: 841-851.
5. Ashe, M.P., De Long, S.K., and Sachs, A.B. 2000. Glucose depletion rapidly inhibits translation initiation in yeast. Mol. Biol. Cell 11:833-848.
6. Bloch, J.C., Perrin, F., and Lacroute, F. 1978. Yeast temperature- sensitive mutants specifically impaired in processing of poly(A)- containing RNAs. Mol. Gen. Genet. 165: 123-127.
7. Boeck, R., Tarun Jr., S., Rieger, M., Deardorff, J.A., Muller-Auer, S., and Sachs, A.B. 1996. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J. Biol. Chem. 271: 432-38.
8. Brown, C.E. and Sachs, A.B. 1998. Poly(A) tail length control in Saccharomyces cerevisiae occurs by message-specific deadenylation. Mol. Cell. Biol. 18: 6548-6559.
9. Brown, C.E., Tarun Jr., S.Z., Boeck, R., and Sachs, A.B. 1996. PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 5744-5753.
10. Brown, J.T., Bai, X., and Johnson, A.W. 2000. The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6:449-457.
11. Cunningham, K.G., Manson, W., Spring, F.S., and Hutchinson, S.A. 1950. Cordycepin, a metabolic product isolated from cultures of Cordyceps militaris (Linn.) Link. Nature 166: 949.
12. Daugeron, M.C., Mauxion, F., and Seraphin, B. 2001. The yeast POP2 gene encodes a nuclease involved in mRNA deadenylation. Nucleic Acids Res. 29: 2448-2455.
13. Decourty, L., Saveanu, C., Zemam, K., Hantraye, F., Frachon, E., Rousselle, J.C., Fromont-Racine, M., and Jacquier, A. 2008. Linking functionally related genes by sensitive and quantitative characterization of genetic interaction profiles. Proc. Natl. Acad. Sci. 105: 5821-5826.
14. Desmoucelles, C., Pinson, B., Saint-Marc, C., and Daignan- Fornier, B. 2002. Screening the yeast "disruptome" for mutants affecting resistance to the immunosuppressive drug, mycophenolic acid. J. Biol. Chem. 277: 27036-27044.
15. Dichtl, B., Blank, D., Ohnacker, M., Friedlein, A., Roeder, D., Langen, H., and Keller, W. 2002a. A role for SSU72 in balancing RNA polymerase II transcription elongation and termination. Mol. Cell 10: 1139-1150.
16. Dichtl, B., Blank, D., Sadowski, M., Hubner, W., Weiser, S., and Keller, W. 2002b. Yhh1p/Cft1p directly links poly(A) site recognition and RNA polymerase II transcription termination. EMBO J. 21: 4125-135.
17. Fischer, T., Strasser, K., Racz, A., Rodriguez-Navarro, S., Oppizzi, M., Ihrig, P., Lechner, J., and Hurt, E. 2002. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J. 21: 5843-5852.
18. Freimoser, F.M., Hurlimann, H.C., Jakob, C.A., Werner, T.P., and Amrhein, N. 2006. Systematic screening of polyphosphate (poly P) levels in yeast mutant cells reveals strong interdependence with primary metabolism. Genome Biol. 7: R109. doi: 10.1186/gb-2006- 7-11-r109.
19. Garas, M., Dichtl, B., and Keller, W. 2008. The role of the putative 3' end processing endonuclease Ysh1p in mRNA and snoRNA synthesis. RNA 14: 2671-2684.
20. Gollub, J., Ball, C.A., Binkley, G., Demeter, J., Finkelstein, D.B., Hebert, J.M., Hernandez- Boussard, T., Jin, H., Kaloper, M., Matese, J.C., et al. 2003. The Stanford Microarray Database: Data access and quality assessment tools. Nucleic Acids Res. 31:94-96.
21. Gudipati, R.K., Villa, T., Boulay, J., and Libri, D. 2008. Phosphory- lation of the RNA polymerase II C-terminal domain dictates transcription termination choice. Nat. Struct. Mol. Biol. 15: 786-794.
22. Halbeisen, R.E. and Gerber, A.P. 2009. Stress-dependent coordination of transcriptome and translatome in yeast. PLoS Biol. (in press).
23. Hillenmeyer, M.E., Fung, E., Wildenhain, J., Pierce, S.E., Hoon, S., Lee, W., Proctor, M., St Onge, R.P., Tyers, M., Koller, D., et al. 2008. The chemical genomic portrait of yeast: Uncovering a phenotype for all genes. Science 320: 362-365.
24. Hilleren, P. and Parker, R. 2001. Defects in the mRNA export factors Rat7p, Gle1p, Mex67p, and Rat8p cause hyperadenylation during 3' end formation of nascent transcripts. RNA 7: 753-764.
25. Holbein, S., Freimoser, F.M., Werner, T.P., Wengi, A., and Dichtl, B. 2008. Cordycepin- hypersensitive growth links elevated polyphos- phate levels to inhibition of poly(A) polymerase in Saccharomyces cerevisiae. Nucleic Acids Res. 36: 353-363.
26. Horowitz, B., Goldfinger, B.A., and Marmur, J. 1976. Effect of cordycepin triphosphate on the nuclear DNA-dependent RNA polymerases and poly(A) polymerase from the yeast, Saccharomy- ces cerevisiae. Arch. Biochem. Biophys. 172: 143-148.
27. Houseley, J., LaCava, J., and Tollervey, D. 2006. RNA- quality control by the exosome. Nat. Rev. Mol. Cell Biol. 7: 529-539.
28. Kiel, J.A., Veenhuis, M., and van der Klei, I.J. 2006. PEX genes in fungal genomes: Common, rare or redundant. Traffic 7: 1291-1303.
29. Konrad, M. 1988. Analysis and in vivo disruption of the gene coding for adenylate kinase (ADK1) in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 263: 19468-19474.
30. Kyburz, A., Sadowski, M., Dichtl, B., and Keller, W. 2003. The role of the yeast cleavage and polyadenylation factor subunit Ydh1p/Cft2p in pre -mRNA 3' end formation. Nucleic Acids Res. 31: 3936-3945.
31. Lecoq, K., Belloc, I., Desgranges, C., and Daignan-Fornier, B. 2001. Role of adenosine kinase in Saccharomyces cerevisiae: Identification of the ADO1 gene and study of the mutant phenotypes. Yeast 18:335-342.
32. Lykke- Andersen, S. and Jensen, T.H. 2007. Overlapping pathways dictate termination of RNA polymerase II transcription. Biochimie 89: 1177-1182.
33. Mandart, E. and Parker, R. 1995. Effects of mutations in the Saccharomyces cerevisiae RNA14, RNA15, and PAP1 genes on polyadenylation in vivo. Mol. Cell. Biol. 15: 6979-6986.
34. Maser, P., Sutterlin, C., Kralli, A., and Kaminsky, R. 1999. A nucleoside transporter from Trypanosoma brucei involved in drug resistance. Science 285: 242-244.
35. Meyer, S., Temme, C., and Wahle, E. 2004. Messenger RNA turnover in eukaryotes: Pathways and enzymes. Crit. Rev. Biochem. Mol. Biol. 39: 197-216.
36. Minvielle-Sebastia, L., Preker, P.J., and Keller, W. 1994. RNA14 and RNA15 proteins as components of a yeast pre-mRNA 3' end processing factor. Science 266: 1702-1705.
37. Mortimer, R.K. and Johnston, J.R. 1986. Genealogy of principal strains of the yeast genetic stock center. Genetics 113: 35-43.
38. Muhlrad, D., Decker, C.J., and Parker, R. 1994. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5' → 3' digestion of the transcript. Genes & Dev. 8: 855-866.
39. Muller, W.E., Seibert, G., Beyer, R., Breter, H.J., Maidhof, A., and Zahn, R.K. 1977. Effect of cordycepin on nucleic acid metabolism in L5178Y cells and on nucleic acid-synthesizing enzyme systems. Cancer Res. 37: 3824-3833.
40. Naula, N., Hilti, N., Schweingruber, A.M., and Schweingruber, M.E. 2003. Cordycepin in Schizosaccharomyces pombe: Effects on the wild type and phenotypes of mutants resistant to the drug. Curr. Genet. 43: 400-406.
41. Nonet, M., Scafe, C., Sexton, J., and Young, R. 1987. Eukaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol. Cell. Biol. 7: 1602-1611.
42. Ooi, S.L., Pan, X., Peyser, B.D., Ye, P., Meluh, P.B., Yuan, D.S., Irizarry, R.A., Bader, J.S., Spencer, F.A., and Boeke, J.D. 2006. Global synthetic-lethality analysis and yeast functional profiling. Trends Genet. 22: 56-63.
43. Parsons, A.B., Lopez, A., Givoni, I.E., Williams, D.E., Gray, C.A., Porter, J., Chua, G., Sopko, R., Brost, R.L., Ho, C.H., et al. 2006. Exploring the mode- of -action of bioactive compounds by chemical- genetic profiling in yeast. Cell 126: 611-625.
44. Patel, D. and Butler, J.S. 1992. Conditional defect in mRNA 3' end processing caused by a mutation in the gene for poly(A) poly- merase. Mol. Cell. Biol. 12: 3297-3304.
45. Paterson, R.R. 2008. Cordyceps: A traditional Chinese medicine and another fungal therapeutic biofactory? Phytochemistry 69: 1469-1495.
46. Rottenberg, M.E., Masocha, W., Ferella, M., Petitto-Assis, F., Goto, H., Kristensson, K., McCaffrey, R., and Wigzell, H. 2005. Treatment of African trypanosomiasis with cordycepin and aden- osine deaminase inhibitors in a mouse model. J. Infect. Dis. 192:1658-1665.
47. Schuldiner, M., Collins, S.R., Thompson, N.J., Denic, V., Bhamidipati, A., Punna, T., Ihmels, J., Andrews, B., Boone, C., Greenblatt, J.F., et al. 2005. Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
48. Segre, D., Deluna, A., Church, G.M., and Kishony, R. 2005. Modular epistasis in yeast metabolism. Nat. Genet. 37: 77-83.
49. Stack, J.H., Herman, P.K., Schu, P.V., and Emr, S.D. 1993. A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 12: 2195-2204.
50. Sugar, A.M. and McCaffrey, R.P. 1998. Antifungal activity of 3'- deoxyadenosine (cordycepin). Antimicrob. Agents Chemother. 42:1424-1427.
51. Thiebaut, M., Kisseleva-Romanova, E., Rougemaille, M., Boulay, J., and Libri, D. 2006. Transcription termination and nuclear degradation of cryptic unstable transcripts: A role for the Nrd1- Nab3 pathway in genome surveillance. Mol. Cell 23: 853-864.
52. Tu, J. and Carlson, M. 1995. REG1 binds to protein phosphatase type 1 and regulates glucose repression in Saccharomyces cerevisiae. 0EMBO J. 14: 5939-5946.
53. Tucker, M., Staples, R.R., Valencia-Sanchez, M.A., Muhlrad, D., and Parker, R. 2002. Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/ Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 21: 1427-1436.
54. Valay, J.G., Simon, M., Dubois, M.F., Bensaude, O., Facca, C., and Faye, G. 1995. The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpb1p CTD. J. Mol. Biol. 249: 535-544.
55. Vasiljeva, L., Kim, M., Mutschler, H., Buratowski, S., and Meinhart, A. 2008. The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat. Struct. Mol. Biol. 15: 795-804.
56. Wanders, R.J. and Waterham, H.R. 2006. Biochemistry of mammalian peroxisomes revisited. Annu. Rev. Biochem. 75: 295-332.
57. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J.D., Bussey, H., et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
58. Wyers, F., Rougemaille, M., Badis, G., Rousselle, J.C., Dufour, M.E., Boulay, J., Regnault, B., Devaux, F., Namane, A., Seraphin, B., et al. 2005. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121: 725-737.
59. Zhu, J.S., Halpern, G.M., and Jones, K. 1998a. The scientific rediscovery of a precious ancient Chinese herbal regimen: Cordyceps sinensis: Part II. J. Altern. Complement. Med. 4: 429-457.
60. Zhu, J.S., Halpern, G.M., and Jones, K. 1998b. The scientific rediscovery of an ancient Chinese herbal medicine: Cordyceps sinensis: part I. J. Altern. Complement. Med. 4: 289-303.