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5 MESSENGER RNA (Full Edition)

13 mRNA degradation involves multiple activities

Key Terms
  • Degradation of yeast mRNA requires removal of the 5' cap and the 3' poly(A).
  • One yeast pathway involves exonucleolytic degradation from 5' – 3'.
  • Another yeast pathway uses a complex of several exonucleases that work in the 3' – 5' direction.
  • The deadenylase of animal cells may bind directly to the 5' cap.

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We know most about the degradation of mRNA in yeast. There are basically two pathways. Both start with removal of the poly(A) tail (for review see 1934). This is catalyzed by a specific deadenylase which probably functions as part of a large protein complex (1933). (The catalytic subunit is the exonuclease Ccr4 in yeast, and is the exonuclease PARN in vertebrates, which is related to RNAase D.) The enzyme action is processive — once it has started to degrade a particular mRNA substrate, it continues to whittle away that mRNA, base by base.

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Figure 5.24  
Deadenylation allows decapping to occur, which leads to endonucleolytic cleavage from the 5' end.

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The major degradation pathway is summarized in Figure 5.24. Deadenylation at the 3' end triggers decapping at the 5' end. The basis for this relationship is that the presence of the PABP (poly(A)-binding protein) on the poly(A) prevents the decapping enzyme from binding to the 5' end. PABP is released when the length of poly(A) falls below 10-15 residues. Decapping occurs by cleaving the methylated base off the 5' end to leave a monophosphate in the reaction:m7 GpppX... ? m7GDP + pX... The enzyme requires the 7-methyl group (for review see 5856).

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Each end of the mRNA influences events that occur at the other end. This is explained by the fact that the two ends of the mRNA are held together by the factors involved in protein synthesis (see Eukaryotes use a complex of many initiation factors). The effect of PABP on decapping allows the 3' end to have an effect in stabilizing the 5' end. There is also a connection between the structure at the 5' end and degradation at the 3' end. The deadenylase directly binds to the 5' cap, and this interaction is in fact needed for its exonucleolytic attack on the poly(A) (1435).

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What is the rationale for the connection between events occurring at both ends of an mRNA? Perhaps it is necessary to ensure that the mRNA is not left in a state (having the structure of one end but not the other) that might compete with active mRNA for the proteins that bind to the ends.

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Removal of the cap triggers the 5' – 3' degradation pathway in which the mRNA is degraded rapidly from the 5' end, by the 5' – 3' exonuclease XRN1 (1935). The decapping enzyme is concentrated in discrete cytoplasmic foci, which may be " processing bodies" where the mRNA is deadenylated and then degraded after it has been decapped (3999).

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Figure 5.25  
Deadenylation may lead directly to endonucleolytic cleavage and exonucleolytic cleavage from 3' end(s).

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In the second pathway, deadenylated yeast mRNAs can be degraded by the 3' – 5' exonuclease activity of the exosome , a complex of >9 exonucleases (426, 1936). The exosome is also involved in processing precursors for rRNAs. The aggregation of the individual exonucleases into the exosome complex may enable 3' – 5' exonucleolytic activities to be coordinately controlled. The exosome may also degrade fragments of mRNA released by endonucleolytic cleavage. Figure 5.25 shows that the 3' – 5' degradation pathway may actually involve combinations of endonucleolytic and exonucleolytic action. The exosome is also found in the nucleus, where it degrades unspliced precursors to mRNA (2190).

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Yeast mutants lacking either exonucleolytic pathway degrade their mRNAs more slowly, but the loss of both pathways is lethal (426; for review see 30).

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Last Revised on April 6, 2005

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reviews
  • 30 Jacobson, A. and Peltz, S. W. (1996).  Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells.  Annu. Rev. Biochem. 65, 693-739.  PubMed   Journal
  • 1934 Beelman, C. A. and Parker, R. (1995).  Degradation of mRNA in eukaryotes.  Cell 81, 179-183.  PubMed   Journal
  • 5856 Coller, J. and Parker, R. (2004).  Eukaryotic mRNA decapping.  Annu. Rev. Biochem. 73, 861-890.  PubMed  
reviews
  • 426 Mitchell, P. et al. (1997).  The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'-5' exoribonuclease activities.  Cell 91, 457-466.  PubMed   Journal
  • 1435 Gao, M., Fritz, D. T., Ford, L. P., and Wilusz, J. (2000).  Interaction between a poly(A)-specific ribonuclease and the 5' cap influences mRNA deadenylation rates in vitro.  Mol. Cell 5, 479-488.  PubMed   Journal
  • 1933 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 S. cerevisiae.  Cell 104, 377-386.  PubMed   Journal
  • 1935 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.  PubMed  
  • 1936 Allmang, C., Petfalski, E., Podtelejnikov, A., Mann, M., Tollervey, D., and Mitchell, P. (1999).  The yeast exosome and human PM-Scl are related complexes of 3'- 5' exonucleases.  Genes Dev. 13, 2148-2158.  PubMed   Journal
  • 2190 Bousquet-Antonelli, C., Presutti, C., and Tollervey, D. (2000).  Identification of a regulated pathway for nuclear pre-mRNA turnover.  Cell 102, 765-775.  PubMed   Journal
  • 3999 Sheth, U., and Parker, R. (2003).  Decapping and decay of messenger RNA occur in cytoplasmic processing bodies.  Science 300, 805-808.  PubMed  

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