This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Burkard, K. T. D.
Right arrow Articles by Butler, J. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Burkard, K. T. D.
Right arrow Articles by Butler, J. S.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, January 2000, p. 604-616, Vol. 20, No. 2
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

A Nuclear 3'-5' Exonuclease Involved in mRNA Degradation Interacts with Poly(A) Polymerase and the hnRNA Protein Npl3p

Karina T. D. Burkard and J. Scott Butler*

Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York 14618

Received 26 July 1999/Returned for modification 20 September 1999/Accepted 7 October 1999

Inactivation of poly(A) polymerase (encoded by PAP1) in Saccharomyces cerevisiae cells carrying the temperature-sensitive, lethal pap1-1 mutation results in reduced levels of poly(A)+ mRNAs. Genetic selection for suppressors of pap1-1 yielded two recessive, cold-sensitive alleles of the gene RRP6. These suppressors, rrp6-1 and rrp6-2, as well as a deletion of RRP6, allow growth of pap1-1 strains at high temperature and partially restore the levels of poly(A)+ mRNA in a manner distinct from the cytoplasmic mRNA turnover pathway and without slowing a rate-limiting step in mRNA decay. Subcellular localization of an Rrp6p-green fluorescent protein fusion shows that the enzyme residues in the nucleus. Phylogenetic analysis and the nature of the rrp6-1 mutation suggest the existence of a highly conserved 3'-5' exonuclease core domain within Rrp6p. As predicted, recombinant Rrp6p catalyzes the hydrolysis of a synthetic radiolabeled RNA in a manner consistent with a 3'-5' exonucleolytic mechanism. Genetic and biochemical experiments indicate that Rrp6p interacts with poly(A) polymerase and with Npl3p, a poly(A)+ mRNA binding protein implicated in pre-mRNA processing and mRNA nuclear export. These findings suggest that Rrp6p may interact with the mRNA polyadenylation system and thereby play a role in a nuclear pathway for the degradation of aberrantly processed precursor mRNAs.


* Corresponding author. Mailing address: Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, 601 Elmwood Ave., Box 672, Rochester, NY 14618. Phone: (716) 275-7921. Fax: (716) 473-9573. E-mail: btlr{at}uhura.cc.rochester.edu.


Molecular and Cellular Biology, January 2000, p. 604-616, Vol. 20, No. 2
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Roth, K. M., Byam, J., Fang, F., Butler, J. S. (2009). Regulation of NAB2 mRNA 3'-end formation requires the core exosome and the Trf4p component of the TRAMP complex. RNA 15: 1045-1058 [Abstract] [Full Text]  
  • Lykke-Andersen, S., Brodersen, D. E., Jensen, T. H. (2009). Origins and activities of the eukaryotic exosome. J. Cell Sci. 122: 1487-1494 [Abstract] [Full Text]  
  • Graham, A. C., Kiss, D. L., Andrulis, E. D. (2009). Core Exosome-independent Roles for Rrp6 in Cell Cycle Progression. Mol. Biol. Cell 20: 2242-2253 [Abstract] [Full Text]  
  • Schneider, C., Leung, E., Brown, J., Tollervey, D. (2009). The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37: 1127-1140 [Abstract] [Full Text]  
  • Callahan, K. P., Butler, J. S. (2008). Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Res 36: 6645-6655 [Abstract] [Full Text]  
  • Hurt, J. A., Silver, P. A. (2008). mRNA nuclear export and human disease. DMM 1: 103-108 [Abstract] [Full Text]  
  • Navarro, M. V. A. S., Oliveira, C. C., Zanchin, N. I. T., Guimaraes, B. G. (2008). Insights into the Mechanism of Progressive RNA Degradation by the Archaeal Exosome. J. Biol. Chem. 283: 14120-14131 [Abstract] [Full Text]  
  • Hoskins, J., Butler, J. S. (2008). RNA-Based 5-Fluorouracil Toxicity Requires the Pseudouridylation Activity of Cbf5p. Genetics 179: 323-330 [Abstract] [Full Text]  
  • Bernstein, J., Patterson, D. N., Wilson, G. M., Toth, E. A. (2008). Characterization of the Essential Activities of Saccharomyces cerevisiae Mtr4p, a 3'->5' Helicase Partner of the Nuclear Exosome. J. Biol. Chem. 283: 4930-4942 [Abstract] [Full Text]  
  • Stead, J. A., Costello, J. L., Livingstone, M. J., Mitchell, P. (2007). The PMC2NT domain of the catalytic exosome subunit Rrp6p provides the interface for binding with its cofactor Rrp47p, a nucleic acid-binding protein. Nucleic Acids Res 0: gkm614v2-12 [Abstract] [Full Text]  
  • Abruzzi, K., Denome, S., Olsen, J. R., Assenholt, J., Haaning, L. L., Jensen, T. H., Rosbash, M. (2007). A Novel Plasmid-Based Microarray Screen Identifies Suppressors of rrp6{Delta} in Saccharomyces cerevisiae. Mol. Cell. Biol. 27: 1044-1055 [Abstract] [Full Text]  
  • Graham, A. C., Kiss, D. L., Andrulis, E. D. (2006). Differential Distribution of Exosome Subunits at the Nuclear Lamina and in Cytoplasmic Foci. Mol. Biol. Cell 17: 1399-1409 [Abstract] [Full Text]  
  • Schilders, G., Raijmakers, R., Raats, J. M. H., Pruijn, G. J. M. (2005). MPP6 is an exosome-associated RNA-binding protein involved in 5.8S rRNA maturation. Nucleic Acids Res 33: 6795-6804 [Abstract] [Full Text]  
  • Milligan, L., Torchet, C., Allmang, C., Shipman, T., Tollervey, D. (2005). A Nuclear Surveillance Pathway for mRNAs with Defective Polyadenylation. Mol. Cell. Biol. 25: 9996-10004 [Abstract] [Full Text]  
  • FANG, F., PHILLIPS, S., BUTLER, J. S. (2005). Rat1p and Rai1p function with the nuclear exosome in the processing and degradation of rRNA precursors. RNA 11: 1571-1578 [Abstract] [Full Text]  
  • Kuai, L., Das, B., Sherman, F. (2005). A nuclear degradation pathway controls the abundance of normal mRNAs in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102: 13962-13967 [Abstract] [Full Text]  
  • Roth, K. M., Wolf, M. K., Rossi, M., Butler, J. S. (2005). The Nuclear Exosome Contributes to Autogenous Control of NAB2 mRNA Levels. Mol. Cell. Biol. 25: 1577-1585 [Abstract] [Full Text]  
  • Dunn, E. F., Hammell, C. M., Hodge, C. A., Cole, C. N. (2005). Yeast poly(A)-binding protein, Pab1, and PAN, a poly(A) nuclease complex recruited by Pab1, connect mRNA biogenesis to export. Genes Dev. 19: 90-103 [Abstract] [Full Text]  
  • Hieronymus, H., Yu, M. C., Silver, P. A. (2004). Genome-wide mRNA surveillance is coupled to mRNA export. Genes Dev. 18: 2652-2662 [Abstract] [Full Text]  
  • Kuai, L., Fang, F., Butler, J. S., Sherman, F. (2004). Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101: 8581-8586 [Abstract] [Full Text]  
  • Kadaba, S., Krueger, A., Trice, T., Krecic, A. M., Hinnebusch, A. G., Anderson, J. (2004). Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 18: 1227-1240 [Abstract] [Full Text]  
  • CHEKANOVA, J. A., BELOSTOTSKY, D. A. (2003). Evidence that poly(A) binding protein has an evolutionarily conserved function in facilitating mRNA biogenesis and export. RNA 9: 1476-1490 [Abstract] [Full Text]  
  • Kufel, J., Allmang, C., Verdone, L., Beggs, J., Tollervey, D. (2003). A complex pathway for 3' processing of the yeast U3 snoRNA. Nucleic Acids Res 31: 6788-6797 [Abstract] [Full Text]  
  • Mitchell, P., Petfalski, E., Houalla, R., Podtelejnikov, A., Mann, M., Tollervey, D. (2003). Rrp47p Is an Exosome-Associated Protein Required for the 3' Processing of Stable RNAs. Mol. Cell. Biol. 23: 6982-6992 [Abstract] [Full Text]  
  • PHILLIPS, S., BUTLER, J. S. (2003). Contribution of domain structure to the RNA 3' end processing and degradation functions of the nuclear exosome subunit Rrp6p. RNA 9: 1098-1107 [Abstract] [Full Text]  
  • Das, B., Butler, J. S., Sherman, F. (2003). Degradation of Normal mRNA in the Nucleus of Saccharomyces cerevisiae. Mol. Cell. Biol. 23: 5502-5515 [Abstract] [Full Text]  
  • Zheng, X., Kelley, K., Elnakat, H., Yan, W., Dorn, T., Ratnam, M. (2003). mRNA Instability in the Nucleus Due to a Novel Open Reading Frame Element Is a Major Determinant of the Narrow Tissue Specificity of Folate Receptor {alpha}. Mol. Cell. Biol. 23: 2202-2212 [Abstract] [Full Text]  
  • Libri, D., Dower, K., Boulay, J., Thomsen, R., Rosbash, M., Jensen, T. H. (2002). Interactions between mRNA Export Commitment, 3'-End Quality Control, and Nuclear Degradation. Mol. Cell. Biol. 22: 8254-8266 [Abstract] [Full Text]  
  • Oliveira, C. C., Gonzales, F. A., Zanchin, N. I. T. (2002). Temperature-sensitive mutants of the exosome subunit Rrp43p show a deficiency in mRNA degradation and no longer interact with the exosome. Nucleic Acids Res 30: 4186-4198 [Abstract] [Full Text]  
  • van Hoof, A., Frischmeyer, P. A., Dietz, H. C., Parker, R. (2002). Exosome-Mediated Recognition and Degradation of mRNAs Lacking a Termination Codon. Science 295: 2262-2264 [Abstract] [Full Text]  
  • Chekanova, J. A., Dutko, J. A., Mian, I. S., Belostotsky, D. A. (2002). Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3'->5' exonuclease containing S1 and KH RNA-binding domains. Nucleic Acids Res 30: 695-700 [Abstract] [Full Text]  
  • Beckley, S. A., Liu, P., Stover, M. L., Gunderson, S. I., Lichtler, A. C., Rowe, D. W. (2001). Reduction of Target Gene Expression by a Modified U1 snRNA. Mol. Cell. Biol. 21: 2815-2825 [Abstract] [Full Text]  
  • Zuo, Y., Deutscher, M. P. (2001). Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res 29: 1017-1026 [Abstract] [Full Text]  
  • Das, B., Guo, Z., Russo, P., Chartrand, P., Sherman, F. (2000). The Role of Nuclear Cap Binding Protein Cbc1p of Yeast in mRNA Termination and Degradation. Mol. Cell. Biol. 20: 2827-2838 [Abstract] [Full Text]  
  • Allmang, C., Mitchell, P., Petfalski, E., Tollervey, D. (2000). Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res 28: 1684-1691 [Abstract] [Full Text]  
  • Chekanova, J. A., Shaw, R. J., Wills, M. A., Belostotsky, D. A. (2000). Poly(A) Tail-dependent Exonuclease AtRrp41p from Arabidopsis thaliana Rescues 5.8 S rRNA Processing and mRNA Decay Defects of the Yeast ski6 Mutant and Is Found in an Exosome-sized Complex in Plant and Yeast Cells. J. Biol. Chem. 275: 33158-33166 [Abstract] [Full Text]  
  • Brouwer, R., Allmang, C., Raijmakers, R., van Aarssen, Y., Egberts, W. V., Petfalski, E., van Venrooij, W. J., Tollervey, D., Pruijn, G. J. M. (2001). Three Novel Components of the Human Exosome. J. Biol. Chem. 276: 6177-6184 [Abstract] [Full Text]