Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover

Nature Structural and Molecular Biology

Volumn 12, Issue 12, 2005, Pages 1054-1063

  Yamashita, Akio ^a   Chang, Tsung Cheng ^a   Yamashita, Yukiko ^a   Zhu, Wenmiao ^a   Zhong, Zhenping ^a   Chen, Chyi Ying A ^a   Shyu, Ann Bin ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLOBIN; MESSENGER RNA; NUCLEASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; FIBROBLAST; KINETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; STOP CODON; WILD TYPE;

ANIMALS; CELL NUCLEUS; CYTOPLASM; ENDORIBONUCLEASES; EXORIBONUCLEASES; FIBROBLASTS; GLOBINS; HUMANS; MICE; NIH 3T3 CELLS; RNA INTERFERENCE; RNA STABILITY; RNA, MESSENGER;

ANIMALIA; MAMMALIA;

EID: 28544450636     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1016     Document Type: Article

References (47)

1. Mitchell, P. & Tollervey, D. mRNA stability in eukaryotes. Curr. Opin. Genet. Dev. 10, 193-198 (2000).
2. Wilusz, C.J., Wormington, M. & Peltz, S.W. The cap-to-tail guide to mRNA turnover. Nat. Rev. Mol. Cell Biol. 2, 237-246 (2001).
3. Fritz, D.T., Bergman, N., Kilpatrick, W.J., Wilusz, C.J. & Wilusz, J. Messenger RNA decay in mammalian cells: the exonuclease perspective. Cell Biochem. Biophys. 41, 265-278 (2004).
4. Meyer, S., Temme, C. & Wahle, E. Messenger RNA turnover in eukaryotes: Pathways and enzymes. Crit. Rev. Biochem. Mol. Biol. 39, 197-216 (2004).
5. Parker, R. & Song, H. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11, 121-127 (2004).
6. Daugeron, M.-C., Mauxion, F. & Seraphin, B. The yeast POP2 gene encodes a nuclease involved in mRNA deadenylation. Nucleic Acids Res. 29, 2448-2455 (2001).
7. Boeck, R. et al. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J. Biol. Chem. 271, 432-438 (1996).
8. Brown, C., Tarun, S., Jr. Boeck, R. & Sachs, A. PAN3 encodes a subunit of the Pablp-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 5744-5753 (1996).
9. Tucker, M. et al. The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104, 377-386 (2001).
10. Gao, M., Fritz, D.T., Ford, L.P. & Wilusz, J. Interaction between a poly(A)-specific ribonuclease and the 5′ cap influences mRNA deadenylation rates in vitro. Mol. Cell 5, 479-488 (2000).
11. Dehlin, E., Wormington, M., Korner, C.G. & Wahle, E. Cap-dependent deadenylation of mRNA. EMBO J. 19, 1079-1086 (2000).
12. Körner, C.G. & Wahle, E. Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease. J. Biol. Chem. 272, 10448-10456 (1997).
13. Muhlrad, D. & Parker, R. Premature translational termination triggers mRNA decapping. Nature 370, 578-581 (1994).
14. Cao, D. & Parker, R. Computational modeling and experimental analysis of nonsense-mediated decay in yeast. Cell 113, 533-545 (2003).
15. Mitchell, P. & Tollervey, D. An NMD pathway in yeast involving accelerated deadenylation and exosome-mediated 3′ → 5′ degradation. Mol. Cell 11, 1405-1413 (2003).
16. Chen, C.-Y.A. & Shyu, A.-B. Rapid deadenylation triggered by a nonsense codon precedes decay of the RNA body in a mammalian cytoplasmic nonsense-mediated decay pathway. Mol. Cell. Biol. 23, 4805-4813 (2003).
17. Couttet, P. & Grange, T. Premature termination codons enhance mRNA decapping in human cells. Nucleic Acids Res. 32, 488-494 (2004).
18. Chang, T.-C. et al. UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant. Genes Dev. 18, 2010-2023 (2004).
19. Shyu, A.-B., Greenberg, M.E. & Belasco, J.G. The c-fos mRNA is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev. 3, 60-72 (1989).
20. Winzen, R. et al. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18, 4969-4980 (1999).
21. Xu, N., Loflin, P., Chen, C.-Y.A. & Shyu, A.-B. A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res. 26, 558-565 (1998).
22. Dupressoir, A. et al. Identification of four families of yCCR4- and Mg2+-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 [online] 2, 9 (2001)(doi:10.1186/1471-2164-2-9).
23. Albert, T.K. et al. Isolation and characterization of human orthologs of yeast CCR4-NOT complex subunits. Nucleic Acids Res. 28, 809-817 (2000).
24. Chen, C.-Y.A., Xu, N., Zhu, W. & Shyu, A.-B. Functional dissection of hnRNP D suggests that nuclear import is required before hnRNP D can modulate mRNA turnover in the cytoplasm. RNA 10, 669-680 (2004).
25. Shyu, A.B. & Wilkinson, M.F. The double lives of shuttling mRNA binding proteins. Cell 102, 135-138 (2000).
26. Kudo, N. et al. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96, 9112-9117 (1999).
27. Kudo, N. et al. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 242, 540-547 (1998).
28. Mendell, J.T., Medghalchi, S.M., Lake, R.G., Noensie, E.N. & Dietz, H.C. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 20, 8944-8957 (2000).
29. 2+-mediated cleavage. J. Biol. Chem. 277, 5982-5987 (2002).
30. Baggs, J.E. & Green, C.B. Nocturnin, a deadenylase in Xenopus laevis retina: A mechanism for posttranscriptional control of circadian-related mRNA. Curr. Biol. 13, 189-198 (2003).
31. Martinez, J., Ren, Y.-G., Nilsson, P., Ehrenberg, M. & Virtanen, A. The mRNA cap structure stimulates rate of poly(A) removal and amplifies processivity of degradation. J. Biol. Chem. 276, 27923-27929 (2001).
32. Loflin, P.T., Chen, C.-Y.A., Xu, N. & Shyu, A.-B. Transcriptional pulsing approaches for analysis of mRNA turnover in mammalian cells. Methods 17, 11-20 (1999).
33. Loflin, P.T., Chen, C.-Y.A. & 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, 1884-1897 (1999).
34. Fischer, N. & Weis, K. The DEAD box protein Dhhl stimulates the decapping enzyme Dcpl. EMBO J. 21, 2788-2797 (2002).
35. Coller, J.M., Tucker, M., Sheth, U., Valencia-Sanchez, M.A. & Parker, R. The DEAD box helicase, Dhh1p, functions in mRNA decapping and interacts with both the decapping and deadenylase complexes. RNA 7, 1717-1727 (2001).
36. Cougot, N., Babajko, S. & Seraphin, B. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165, 31-40 (2004).
37. Uchida, N., Hoshino, S. & Katada, T. Identification of a human -cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J. Biol. Chem. 279, 1383-1391 (2004).
38. Khanna, R. & Kiledjian, M. Poly(A)-binding-protein-mediated regulation of hDcp2 decapping in vitro. EMBO J. 23, 1968-1976 (2004).
39. Tucker, M., Staples, R.R., Valencia-Sanchez, M.A., Muhlrad, D. & Parker, R. Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 21, 1427-1436 (2002).
40. Andrei, M.A. et al. A role for elF4E and elF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11, 717-727 (2005).
41. Viswanathan, P., Ohn, T., Chiang, Y.-C., Chen, J. & Denis, C.L. Mouse CAF1 can function as a processive deadenylase/3′-5′-exonuclease in vitro but in yeast the deadenylase function of CAF1 is not required for mRNA poly(A) removal. J. Biol. Chem. 279, 23988-23995 (2004).
42. Temme, C., Zaessinger, S., Meyer, S., Simonelig, M. & Wahle, E. A complex containing the CCR4 and CAF1 proteins is involved in mRNA deadenylation in Drosophila. EMBO J. 23, 2862-2871 (2004).
43. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y. & Ohno, S. Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15, 2215-2228 (2001).
44. Chen, C.Y. & Shyu, A.B. Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements. Mol. Cell. Biol. 14, 8471-8482 (1994).
45. Shyu, A.-B., Garcia-Sanz, J.A. & Mullner, E. Analysis of mRNA decay in mammalian cells, in The Immunology Methods Manual (ed. Lefkovits, I.) 450-62 (Academic Press, London, 1996).
46. Shyu, A.-B., Belasco, J.G. & Greenberg, M.G. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 5, 221-232 (1991).
47. 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, 3461-3470 (1998).