Saccharomyces cerevisiae Ngl3p is an active 3′-5′ exonuclease with a specificity towards poly-A RNA reminiscent of cellular deadenylases

Nucleic Acids Research

Volumn 40, Issue 2, 2012, Pages 837-846

  Feddersen, Ane ^a   Dedic, Emil ^a   Poulsen, Esben G ^a   Schmid, Manfred ^b   Van, Lan Bich ^a   Jensen, Torben Heick ^b   Brodersen, Ditlev E ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b NONE   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; EXONUCLEASE; GENOMIC DNA; MESSENGER RNA; PHOSPHATASE; POLYADENYLATED RNA; PROTEIN NGL3P; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; DEADENYLATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME STABILITY; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE DELETION; IN VITRO STUDY; NGL3P GENE; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA DEGRADATION; RNA PROCESSING; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84855882664     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr782     Document Type: Article

References (38)

1. Goldstrohm, A. C. and Wickens, M. (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol., 9, 337-344.
2. Parker, R. and Song, H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol., 11, 121-127.
3. Houseley, J. and Tollervey, D. (2009) The many pathways of RNA degradation. Cell, 136, 763-776.
4. Garneau, N. L., Wilusz, J. and Wilusz, C. J. (2007) The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol., 8, 113-126.
5. Chen, J., Chiang, Y. C. and Denis, C. L. (2002) CCR4, a 30-50 poly (A) RNA and ssDNA exonuclease, is the catalytic component of the cytoplasmic deadenylase. EMBO J., 21, 1414-1426.
6. 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.
7. Chen, J., Rappsilber, J., Chiang, Y. C., Russell, P., Mann, M. and Denis, C. L. (2001) Purification and characterization of the 1.0 MDa CCR4-NOT complex identifies two novel components of the complex. J. Mol. Biol., 314, 683-694.
8. Tucker, M., Valencia-Sanchez, M. A., Staples, R. R., Chen, J., Denis, C. L. and Parker, R. (2001) The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell, 104, 377-386.
9. Boeck, R., Tarun, S. Jr, 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, 432-438.
10. Brown, C. E., Tarun, S. Z. Jr, 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.
11. Sachs, A. B. and Deardorff, J. A. (1992) Translation initiation requires the PAB-dependent poly (A) ribonuclease in yeast. Cell, 70, 961-973.
12. Astrom, J., Astrom, A. and Virtanen, A. (1992) Properties of a HeLa cell 3' exonuclease specific for degrading poly (A) tails of mammalian mRNA. J. Biol. Chem., 267, 18154-18159.
13. Korner, C. G. and Wahle, E. (1997) Poly (A) tail shortening by a mammalian poly (A)-specific 3'-exoribonuclease. J. Biol. Chem., 272, 10448-10456.
14. Wang, H., Morita, M., Yang, X., Suzuki, T., Yang, W., Wang, J., Ito, K., Wang, Q., Zhao, C., Bartlam, M. et al. (2010) Crystal structure of the human CNOT6L nuclease domain reveals strict poly (A) substrate specificity. EMBO J., 29, 2566-2576.
15. Bianchin, C., Mauxion, F., Sentis, S., Seraphin, B. and Corbo, L. (2005) Conservation of the deadenylase activity of proteins of the Caf1 family in human. RNA, 11, 487-494.
16. 2+ in the active site. RNA, 15, 850-861.
17. Jonstrup, A. T., Andersen, K. R., Van, L. B. and Brodersen, D. E. (2007) The 1.4-A crystal structure of the S. pombe Pop2p deadenylase subunit unveils the configuration of an active enzyme. Nucleic Acids Res., 35, 3153-3164.
18. Thore, S., Mauxion, F., Seraphin, B. and Suck, D. (2003) X-ray structure and activity of the yeast Pop2 protein: a nuclease subunit of the mRNA deadenylase complex. EMBO Rep., 4, 1150-1155.
19. Mol, C. D., Hosfield, D. J. and Tainer, J. A. (2000) Abasic site recognition by two apurinic/apyrimidinic endonuclease families in DNA base excision repair: the 3' ends justify the means. Mutat. Res., 460, 211-229.
20. Mol, C. D., Kuo, C. F., Thayer, M. M., Cunningham, R. P. and Tainer, J. A. (1995) Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature, 374, 381-386.
21. 2+-dependent endonucleases. Trends Biochem. Sci., 25, 272-273.
22. Matsuo, Y., Yamada, A., Tsukamoto, K., Tamura, H., Ikezawa, H., Nakamura, H. and Nishikawa, K. (1996) A distant evolutionary relationship between bacterial sphingomyelinase and mammalian DNase I. Protein Sci., 5, 2459-2467.
23. Whisstock, J. C., Romero, S., Gurung, R., Nandurkar, H., Ooms, L. M., Bottomley, S. P. and Mitchell, C. A. (2000) The inositol polyphosphate 5-phosphatases and the apurinic/apyrimidinic base excision repair endonucleases share a common mechanism for catalysis. J. Biol. Chem., 275, 37055-37061.
24. 2+-dependent endonuclease-related proteins in higher eukaryotes, and characterization of orthologs of yCCR4 with a conserved leucine-rich repeat essential for hCAF1/hPOP2 binding. BMC Genomics, 2, 9.
25. 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.
26. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S. and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature, 425, 686-691.
27. Faber, A. W., Van Dijk, M., Raue, H. A. and Vos, J. C. (2002) Ngl2p is a Ccr4p-like RNA nuclease essential for the final step in 30-end processing of 5.8S rRNA in Saccharomyces cerevisiae. RNA, 8, 1095-1101.
28. Thomson, E. and Tollervey, D. (2010) The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell. Biol., 30, 976-984.
29. Reinders, J., Zahedi, R. P., Pfanner, N., Meisinger, C. and Sickmann, A. (2006) Toward the complete yeast mitochondrial proteome: multidimensional separation techniques for mitochondrial proteomics. J. Proteome. Res., 5, 1543-1554.
30. Assenholt, J., Mouaikel, J., Andersen, K. R., Brodersen, D. E., Libri, D. and Jensen, T. H. (2008) Exonucleolysis is required for nuclear mRNA quality control in yeast THO mutants. RNA, 14, 2305-2313.
31. Andersen, K. R., Jensen, T. H. and Brodersen, D. E. (2008) Take the "A" tail-quality control of ribosomal and transfer RNA. Biochim. Biophys. Acta, 1779, 532-537.
32. Steitz, T. A. and Steitz, J. A. (1993) A general two-metal-ion mechanism for catalytic RNA. Proc. Natl Acad. Sci. USA, 90, 6498-6502.
33. Tholey, G., Ledig, M., Mandel, P., Sargentini, L., Frivold, A. H., Leroy, M., Grippo, A. A. and Wedler, F. C. (1988) Concentrations of physiologically important metal ions in glial cells cultured from chick cerebral cortex. Neurochem. Res., 13, 45-50.
34. Wienken, C. J., Baaske, P., Rothbauer, U., Braun, D. and Duhr, S. (2010) Protein-binding assays in biological liquids using microscale thermophoresis. Nat. Commun., 1, 100.
35. Mol, C. D., Izumi, T., Mitra, S. and Tainer, J. A. (2000) DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected]. Nature, 403, 451-456.
36. Beernink, P. T., Segelke, B. W., Hadi, M. Z., Erzberger, J. P., Wilson, D. M. 3rd and Rupp, B. (2001) Two divalent metal ions in the active site of a new crystal form of human apurinic/apyrimidinic endonuclease, Ape1: implications for the catalytic mechanism. J. Mol. Biol., 307, 1023-1034.
37. Vanacova, S., Wolf, J., Martin, G., Blank, D., Dettwiler, S., Friedlein, A., Langen, H., Keith, G. and Keller, W. (2005) A new yeast poly (A) polymerase complex involved in RNA quality control. PLoS Biol., 3, e189.
38. Goldstrohm, A. C., Hook, B. A. and Wickens, M. (2008) Regulated deadenylation in vitro. Methods Enzymol., 448, 77-106.