mRNA stability in eukaryotes

Current Opinion in Genetics and Development

Volumn 10, Issue 2, 2000, Pages 193-198

  Mitchell, Philip ^a   Tollervey, David ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA BINDING PROTEIN;

ADENYLATION; EUKARYOTE; HUMAN; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA CAPPING; RNA DEGRADATION; YEAST;

EUKARYOTA;

EID: 0034030583     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(00)00063-0     Document Type: Review

References (62)

1. Caponigro G., Parker R. Mechanisms and control of mRNA turnover in Saccharomyces cerevisiae. Microbiol Rev. 60:1996;233-249.
2. McCarthy J.E.G. Posttranscriptional control of gene expression in yeast. Microbiol Mol Biol Rev. 62:1998;1492-1553.
3. Decker C.J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 7:1993;1632-1643.
4. Herrick D., Parker R., Jacobson A. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 10:1990;2269-2284.
5. Tarun S.Z., Wells S.E., Deardorff J.A., Sachs A.B. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc Natl Acad Sci USA. 94:1997;9046-9051.
6. Pestova T.V., Hellen C.U. Ribosome recruitment and scanning: what's new? Trends Biochem Sci. 24:1999;85-87.
7. Tarun S.Z. Jr., Sachs A.B. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15:1996;7168-7177.
8. Wells S.E., Hillner P.E., Vale R.D., Sachs A.B. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell. 2:1998;135-140. This paper provides direct evidence that the interaction between Pab1p and eIF4G can bring the 5′ and 3′ ends of mRNAs together.
9. Imataka H., Gradi A., Sonenberg N. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:1998;7480-7489. The association of the poly(A)-binding protein with the translation initiation factor is shown to be conserved in humans and not just yeast specific.
10. Schwartz D.C., Parker R. Mutations in translation initiation factors lead to increased rates of deadenylation and decapping of mRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 19:1999;5247-5256. Mutations in a variety of translation initiation factors that reduce translation initiation rates also destabilise mRNAs but do not lead to decapping before deadenylation. Evidence is provided for the role of reduced translation initiation rates in stimulating deadenylation, and decapping after deadenylation.
11. Linz B., Koloteva N., Vasilescu S., McCarthy J.E. Disruption of ribosomal scanning on the 5′-untranslated region, and not restriction of translational initiation per se, modulates the stability of nonaberrant mRNAs in the yeast Saccharomyces cerevisiae. J Biol Chem. 272:1997;9131-9140.
12. Welch E.M., Jacobson A. An internal open reading frame triggers nonsense-mediated decay of the yeast SPT10 mRNA. EMBO J. 18:1999;6134-6145. The authors show that the nonsense-mediated decay pathway may function to limit the expression of a class of mRNAs.
13. Futcher B., Latter G.I., Monardo P., McLaughlin C.S., Garrels J.I. A sampling of the yeast proteome. Mol Cell Biol. 19:1999;7357-7368.
14. Caponigro G., Parker R. Multiple functions for the poly(A)-binding protein in mRNA decapping and deadenylation in yeast. Genes Dev. 9:1995;2421-2432.
15. Morrissey J.P., Deardorff J.A., Hebron C., Sachs A.B. Decapping of stabilized, polyadenylated mRNA in yeast pab1 mutants. Yeast. 15:1999;687-702.
16. Otero L.J., Ashe M.P., Sachs A.B. The yeast poly(A)-binding protein Pab1p stimulates in vitro poly(A)-dependent and cap-dependent translation by distinct mechanisms. EMBO J. 18:1999;3153-3163. Mutations in Pab1p can separate different functional interactions with the translation initiation machinery, which suggests that Pab1p interacts with factors in addition to eIF4G.
17. Anderson J.S.J., Parker R.P. The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J. 17:1998;1497-1506. In addition to the previously studied 5′ decay pathway, yeast mRNAs are degraded 3′→5′ by the exosome complex. This activity also requires a putative, ATP-dependent RNA helicase, Ski2p.
18. Allmang C., Kufel J., Chanfreau G., Mitchell P., Petfalski E., Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 18:1999;5399-5410. The yeast exosome complex is shown to have a large number of different RNA substrates.
19. van Hoof A., Parker R. The exosome: a proteasome for RNA? Cell. 99:1999;347-350. A useful review of the composition and potential mode of action of the exosome.
20. Korner C.G., Wahle E. Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease. J Biol Chem. 272:1997;10448-10456.
21. Ford L.P., Watson J., Keene J.D., Wilusz J. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev. 13:1999;188-201. This paper reports the development of a system to study activated, ARE-mediated mRNA degradation in vitro - a very useful step in understanding the mechanisms involved. Consistent with the in vivo data, elav proteins, including HuR, stabilised some transcripts.
22. Wang Z., Day N., Trifillis P., Kiledjian M. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol Cell Biol. 19:1999;4552-4560.
23. Korner C.G., Wormington M., Muckenthaler M., Schneider S., Dehlin E., Wahle E. The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. EMBO J. 17:1998;5427-5437. Evidence is provided for the in vivo function of DAN as a deadenylase.
24. Brown C.E., Sachs A.B. Poly(A) tail length control in Saccharomyces cerevisiae occurs by message-specific deadenylation. Mol Cell Biol. 18:1998;6548-6559.
25. Allmang C., Petfalski E., Podtelejnikov A., Mann M., Tollervey D., Mitchell P. The yeast exosome and human PM-Scl are related complexes of 3′→5′ exonucleases. Genes Dev. 13:1999;2148-2158. The yeast nuclear exosome complex has at least 11 components (10 in the cytoplasm), 10 of which are shown or predicted to be 3′→5′ exonucleases. The human PM-Scl complex is predicted to be the structural and functional homologue.
26. LaGrandeur T.E., Parker R. Isolation and characterization of Dcp1p, the yeast mRNA decapping enzyme. EMBO J. 17:1998;1487-1496. Despite the large numbers of cofactors needed for mRNA decapping in vivo, Dcp1p is necessary and sufficient for decapping in vitro.
27. Dunckley T., Parker R. The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J. 18:1999;5411-5422. Dcp2p is predicted to be diphosphatase and can be isolated in association with the decapping enzyme, Dcp1p.
28. Boeck R., Lapeyre B., Brown C.E., Sachs A.B. Capped mRNA degradation intermediates accumulate in the yeast spb8-2 mutant. Mol Cell Biol. 18:1998;5062-5072. Spb8p/Lsm1p is required for mRNA decapping. The authors provide evidence that decapping involves more than simple access of the decapping enzyme to the cap structure and requires the Lsm complex.
29. Achsel T., Brahms H., Kastner B., Bachi A., Wilm M., Lührmann R. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18:1999;5789-5802. Lsm proteins form a ring-like structure, which is strikingly similar to the structure of the canonical Sm proteins. RNA substrates are assumed to pass through the centre of the ring, and the complex probably functions in many aspects of RNA processing.
30. Mayes A.E., Verdone L., Legrain P., Beggs J.D. Characterization of Sm like proteins in yeast and their association with U6 snRNA. EMBO J. 18:1999;4321-4331. Seven Lsm proteins associate with the U6 snRNA which, unlike the other spliceosomal snRNAs, does not bind to the canonical Sm proteins. The Lsm complex is involved in the association of U6 with U4 and U5. A related complex may be involved in restructuring other RNAs, including mRNAs destined for decapping.
31. Salgado-Garrido J., Bragado-Nilsson E., Kandels-Lewis S., Seraphin B. Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J. 18:1999;3451-3462. This paper presents a phylogeny of the Sm protein families.
32. Hatfield L., Beelman C.A., Stevens A., Parker R. Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol Cell Biol. 16:1996;5830-5838.
33. Zuk D., Jacobson A. A single amino acid substitution in yeast eIF 5A results in mRNA stabilization. EMBO J. 17:1998;2914-2925. Evidence is provided that, like decapping, subsequent exonuclease degradation requires cofactors in vivo.
34. Chen C.Y., Shyu A.B. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci. 20:1995;465-470.
35. Peng S.S., Chen C.Y., Xu N., Shyu A.B. RNA stabilization by the AU rich element binding protein, HuR, an ELAV protein. EMBO J. 17:1998;3461-3470. Overexpressed HuR protein stabilises some ARE-containing mRNAs. The rate of deadenylation is not greatly affected but the deadenylated mRNA is stabilised.
36. Peng S.S., Chen C.Y., Shyu A.B. Functional characterization of a non-AUUUA AU-rich element from the c- jun proto-oncogene mRNA: evidence for a novel class of AU-rich elements. Mol Cell Biol. 16:1996;1490-1499.
37. Fan X.C., Steitz J.A. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:1998;3448-3460. This paper reports that, contrary to initial expectations, HuR overexpression by transient transfection stabilises ARE-containing mRNAs, rather than activating their degradation.
38. Loflin P., Chen C.Y., Shyu A.B. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes Dev. 13:1999;1884-1897. The presence of the hnRNP D protein in the cytoplasm is correlated with the destabilisation of ARE-containing mRNAs. These findings suggest that HuR and hnRNP D have antagonistic roles in destabilisation.
39. Kiledjian M., DeMaria C.T., Brewer G., Novick K. Identification of AUF1 (heterogeneous nuclear ribonucleoprotein D) as a component of the alpha-globin mRNA stability complex. Mol Cell Biol. 17:1997;4870-4876.
40. Fan X.C., Myer V.E., Steitz J.A. AU-rich elements target small nuclear RNAs as well as mRNAs for rapid degradation. Genes Dev. 11:1997;2557-2568.
41. Dreyfuss G., Matunis M.J., Pinol-Roma S., Burd C.G. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 62:1993;289-321.
42. Fan X.C., Steitz J.A. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc Natl Acad Sci USA. 95:1998;15293-15298. The authors propose that HuR binds ARE-containing mRNAs in the nucleus and is exported to form part of the cytoplasmic mRNP particle.
43. Gebauer F., Corona D.F., Preiss T., Becker P.B., Hentze M.W. Translational control of dosage compensation in Drosophila by sex-lethal: cooperative silencing via the 5′ and 3′ UTRs of msl-2 mRNA is independent of the poly(A) tail. EMBO J. 18:1999;6146-6154.
44. Handa N., Nureki O., Kurimoto K., Kim I., Sakamoto H., Shimura Y., Muto Y., Yokoyama S. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature. 398:1999;579-585.
45. Gebauer F., Merendino L., Hentze M.W., Valcárcel J. Novel functions for 'nuclear factors' in the cytoplasm: the Sex-lethal paradigm. Semin Cell Dev Biol. 8:1997;561-566.
46. Schiavi S.C., Wellington C.L., Shyu A.B., Chen C.Y., Greenberg M.E., Belasco J.G. Multiple elements in the c-fos protein-coding region facilitate mRNA deadenylation and decay by a mechanism coupled to translation. J Biol Chem. 269:1994;3441-3448.
47. Culbertson M.R. RNA surveillance. Unforeseen consequences for gene expression, inherited genetic disorders and cancer. Trends Genet. 15:1999;74-80.
48. Czaplinski K., Ruiz-Echevarria M.J., Gonzalez C.I., Peltz S.W. Should we kill the messenger? The role of the surveillance complex in translation termination and mRNA turnover. Bioessays. 21:1999;685-696.
49. Hillern P., Parker R. Mechanisms of RNA surveillance in eukaryotes. Annu Rev Genet. 33:1999;. in press.
50. Hilleren P., Parker R. mRNA surveillance in eukaryotes: kinetic proofreading of proper translation termination as assessed by mRNP domain organization? RNA. 5:1999;711-719. The presence of correctly located splice junctions and/or polyadenylation sites is proposed to enhance termination efficiency. This leads to termination before ATP hydrolysis by Upf1p, thus avoiding activation of RNA surveillance and potential nonsense-mediated degradation.
51. Ruiz-Echevarria M.J., Yasenchak J.M., Han X., Dinman J.D., Peltz S.W. The upf3 protein is a component of the surveillance complex that monitors both translation and mRNA turnover and affects viral propagation. Proc Natl Acad Sci USA. 95:1998;8721-8726.
52. Czaplinski K., Ruiz-Echevarria M.J., Paushkin S.V., Han X., Weng Y., Perlick H.A., Dietz H.C., Ter-Avanesyan M.D., Peltz S.W. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12:1998;1665-1677. Upf1p interacts with the translation termination factors. This work provides a potential explanation for link between the context of the termination site and the initiation of mRNA surveillance.
53. Oliveira C.C., McCarthy J.E. The relationship between eukaryotic translation and mRNA stability. A short upstream open reading frame strongly inhibits translational initiation and greatly accelerates mRNA degradation in the yeast Saccharomyces cerevisiae. J Biol Chem. 270:1995;8936-8943.
54. Ruiz-Echevarria M.J., Gonzalez C.I., Peltz S.W. Identifying the right stop: determining how the surveillance complex recognizes and degrades an aberrant mRNA. EMBO J. 17:1998;575-589. The context of the termination codon is important for triggering RNA surveillance, which searches for signals that trigger, or suppress, the nonsense-mediated degradation pathway.
55. Vilela C., Ramirez C.V., Linz B., Rodrigues-Pousada C., McCarthy J.E. Post-termination ribosome interactions with the 5′ UTR modulate yeast mRNA stability. EMBO J. 18:1999;3139-3152. The context of the termination codon strongly influences the fate of the ribosome after termination, and therefore mRNA stability.
56. Czaplinski K., Weng Y., Hagan K.W., Peltz S.W. Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA. 1:1995;610-623.
57. Weng Y., Czaplinski K., Peltz S.W. ATP is a cofactor of the Upf1 protein that modulates its translation termination and RNA binding activities. RNA. 4:1998;205-214.
58. Zhang S., Williams C.J., Hagan K., Peltz S.W. Mutations in VPS16 and MRT1 stabilize mRNAs by activating an inhibitor of the decapping enzyme. Mol Cell Biol. 19:1999;7568-7576.
59. Gao M., Fritz D.T., Ford L.P., Wilusz J. Interaction between a Poly(A)-specific ribonuclease and the 5′ cap influences deadenylation rates in an in vitro mRNA stability system. Mol Cell. 2000;. in press. Efficient deadenylation by DAN is dependent upon interaction with the 5′ cap of the mRNA. ARE-binding proteins can confer cap-dependent deadenylation by DAN.
60. 7G and exhibit cap-dependent deadenylation.
61. van Hoof A., Lennertz P., Parker R. Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. EMBO J. 2000;. in press.
62. Uetz P., Giot L., Cagney G., Mansfield T.A., Judson R.S., Knight J.R., Lockshon D., Narayan V., Srinivasan M., Pochart P.et al. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature. 403:2000;623-627.