Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells

Journal of Cell Biology

Volumn 182, Issue 1, 2008, Pages 89-101

  Zheng, Dinghai ^a   Ezzeddine, Nader ^a   Chen, Chyi Ying A ^a   Zhu, Wenmiao ^a   He, Xiangwei ^b   Shyu, Ann Bin ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAF1 DEADENYLASE; CCR4 DEADENYLASE; ENZYME; MESSENGER RNA; PAN2 DEADENYLASE; PAN3 DEADENYLASE;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL CULTURE; CONTROLLED STUDY; DEADENYLATION; EMBRYO; ENZYME ANALYSIS; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; RNA PROCESSING; RNA TRANSLATION; WESTERN BLOTTING;

ANIMALS; CYTOPLASMIC STRUCTURES; HUMANS; MICE; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; NIH 3T3 CELLS; POLY A; POLYADENYLATION; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEINS; PUROMYCIN; RECEPTORS, CCR4; RNA STABILITY; RNA, MESSENGER;

MAMMALIA;

EID: 47549087539     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200801196     Document Type: Article

References (62)

1. Albert, T.K., M. Lemaire, N.L. van Berkum, R. Gentz, M.A. Collart, and H.T.M. Timmers. 2000. Isolation and characterization of human orthologs of yeast CCR4-NOT complex subunits. Nucleic Acids Res. 28:809-817.
2. Andrei, M.A., D.I. Ingelfinger, R. Heintzmann, T. Achsel, R. Rivera-Pomar, and R. Luhrmann. 2005. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA. 11:717-727.
3. Barbee, S.A., P.S. Estes, A.-M. Cziko, J. Hillebrand, R.A. Luedeman, J. Coller, N. Johnson, I.C. Howlett, C. Geng, R. Ueda, et al. 2006. Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron. 52:997-1009.
4. Beelman, C.A., A. Stevens, G. Caponigro, T.E. LaGrandeur, L. Hatfield, D.M. Fortner, and R. Parker. 1996. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature. 382:642-646.
5. Behm-Ansmant, I., J. Rehwinkel, T. Doerks, A. Stark, P. Bork, and E. Izaurralde. 2006. mRNA degradation by miRNAs and GW182 requires both CCR4: NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20:1885-1898.
6. Bianchin, C., F. Mauxion, S. Sentis, B. Seraphin, and L. Corbo. 2005. Conservation of the deadenylase activity of proteins of the Caf1 family in human. RNA. 11:487-494.
7. Boeck, R., S. Tarun Jr., M. Rieger, J.A. Deardorff, S. Muller-Auer, and A.B. Sachs. 1996. The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J. Biol. Chem. 271:432-438.
8. Brengues, M., D. Teixeira, and R. Parker. 2005. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science. 310:486-489.
9. Brown, C.E., S.Z. Tarun Jr., R. Boeck, and A.B. Sachs. 1996. PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:5744-5753.
10. Chang, T.-C., A. Yamashita, C.-Y.A. Chen, Y. Yamashita, W. Zhu, S. Durdan, A. Kahvejian, N. Sonenberg, and A.-B. Shyu. 2004. 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.
11. Chen, C.Y., and A.B. Shyu. 1994. Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements. Mol. Cell. Biol. 14:8471-8482.
12. Chen, C.Y., and A.-B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
13. Chen, C.-Y.A., and A.-B. Shyu. 2003. Rapid deadenylation triggered by a non-sense codon precedes decay of the RNA body in a mammalian cytoplasmic nonsense-mediated decay pathway. Mol. Cell. Biol. 23:4805-4813.
14. Chen, C.-Y.A., Y. Yamashita, T.-C. Chang, A. Yamashita, W. Zhu, Z. Zhong, and A.-B. Shyu. 2007. Versatile applications of transcriptional pulsing to study mRNA turnover in mammalian cells. RNA. 13:1775-1786.
15. Coller, J., and R. Parker. 2005. General translational repression by activators of mRNA decapping. Cell. 122:875-886.
16. Cougot, N., S. Babajko, and B. Seraphin. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165:31-40.
17. Daugeron, M.-C., F. Mauxion, and B. Seraphin. 2001. The yeast POP2 gene encodes a nuclease involved in mRNA deadenylation. Nucleic Acids Res. 29:2448-2455.
18. Ding, L., and M. Han. 2007. GW182 family proteins are crucial for microRNA-mediated gene silencing. Trends Cell Biol. 17:411-416.
19. Dupressoir, A., A.-P. Morel, W. Barbot, M.-P. Loireau, L. Corbo, and T. Heidmann. 2001. 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. 2:9.
20. Eulalio, A., I. Behm-Ansmant, D. Schweizer, and E. Izaurralde. 2007a. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol. Cell. Biol. 27:3970-3981.
21. Eulalio, A., I. Behm-Ansmant, and E. Izaurralde. 2007b. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8:9-22.
22. Eystathioy, T., A. Jakymiw, E.K.L. Chan, B. Seraphin, N. Cougot, and M.J. Fritzler. 2003. The GW182 protein colocalizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA. 9:1171-1173.
23. Ferraiuolo, M.A., S. Basak, J. Dostie, E.L. Murray, D.R. Schoenberg, and N. Sonenberg. 2005. A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay. J. Cell Biol. 170:913-924.
24. Franks, T.M., and J. Lykke-Andersen. 2007. TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev. 21:719-735.
25. Garneau, N.L., J. Wilusz, and C.J. Wilusz. 2007. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 8:113-126.
26. Grosset, C., C.-Y.A. Chen, N. Xu, N. Sonenberg, H. Jacquemin-Sablon, and A.-B. Shyu. 2000. A mechanism for translationally coupled mRNA turnover: Interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell. 103:29-40.
27. Jackson, R.J., and N. Standart. 2007. How do microRNAs regulate gene expression? Sci. STKE. 2007:re1.
28. Kashima, I., A. Yamashita, N. Izumi, N. Kataoka, R. Morishita, S. Hoshino, M. Ohno, G. Dreyfuss, and S. Ohno. 2006. Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. Genes Dev. 20: 355-367.
29. Kedersha, N., and P. Anderson. 2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61-81.
30. Kedersha, N., S. Chen, N. Gilks, W. Li, I.J. Miller, J. Stahl, and P. Anderson. 2002. Evidence that ternary complex (eIF2-GTP-tRNAiMet)-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell. 13:195-210.
31. Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M.J. Fritzler, D. Scheuner, R.J. Kaufman, D.E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871-884.
32. Loflin, P., C.-Y.A. Chen, and A.-B. Shyu. 1999a. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes Dev. 13:1884-1897.
33. Loflin, P.T., C.-Y.A. Chen, N. Xu, and A.-B. Shyu. 1999b. Transcriptional pulsing approaches for analysis of mRNA turnover in mammalian cells. Methods. 17:11-20.
34. Lykke-Andersen, J. 2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22:8114-8121.
35. Mangus, D.A., M.C. Evans, N.S. Agrin, M. Smith, P. Gongidi, and A. Jacobson. 2004. Positive and negative regulation of Poly(A) nuclease. Mol. Cell. Biol. 24:5521-5533.
36. Maroney, P.A., Y. Yu, J. Fisher, and T.W. Nilsen. 2006. Evidence that micro-RNAs are associated with translating messenger RNAs in human cells. Nat. Struct. Mol. Biol. 13:1102-1107.
37. Meyer, S., C. Temme, and E. Wahle. 2004. Messenger RNA turnover in eukaryotes: pathways and enzymes. Crit. Rev. Biochem. Mol. Biol. 39: 197-216.
38. Molin, L., and A. Puisieux. 2005. C. elegans homologue of the Caf1 gene, which encodes a subunit of the CCR4-NOT complex, is essential for embryonic and larval development and for meiotic progression. Gene. 358:73-81.
39. Muhlrad, D., and R. Parker. 1994. Premature translational termination triggers mRNA decapping. Nature. 370:578-581.
40. Nilsen, T.W. 2007. Mechanisms of miroRNA-mediated gene regulation in animal cells. Trends Genet. 23:243-249.
41. Parker, R., and H. Song. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11:121-127.
42. Parker, R., and U. Sheth. 2007. P bodies and the control of mRNA translation and degradation. Mol. Cell. 25:635-646.
43. Peng, S.-S., C.-Y.A. Chen, N. Xu, and A.-B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17:3461-3470.
44. Piccirillo, C., R. Khanna, and M. Kiledjian. 2003. Functional characterization of the mammalian mRNA decapping enzyme hDcp2. RNA. 9:1138-1147.
45. Pillai, R.S., S.N. Bhattacharyya, and W. Filipowicz. 2007. Repression of protein synthesis by miRNAs: how many mechanisms? Trends Cell Biol. 17:118-126.
46. Sheth, U., and R. Parker. 2003. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science. 300:805-808.
47. Sheth, U., and R. Parker. 2006. Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell. 125:1095-1109.
48. Shyu, A.-B., J.G. Belasco, and M.G. Greenberg. 1991. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev. 5:221-232.
49. Siddiqui, N., D.A. Mangus, T.-C. Chang, J.-M. Palermino, A.-B. Shyu, and K. Gehring. 2007. Poly(A) nuclease interacts with the C-terminal domain from poly(A)-binding protein. J. Biol. Chem. 282:25067-25075.
50. Stoecklin, G., T. Mayo, and P. Anderson. 2006. ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep. 7:72-77.
51. Teixeira, D., and R. Parker. 2007. Analysis of P-body assembly in Saccharomyces cerevisiae. Mol. Biol. Cell. 18:2274-2287.
52. Temme, C., S. Zaessinger, S. Meyer, M. Simonelig, and E. Wahle. 2004. A complex containing the CCR4 and CAF1 proteins is involved in mRNA deadenylation in Drosophila. EMBO J. 23:2862-2871.
53. Tucker, M., M.A. Valencia-Sanchez, R.R. Staples, J. Chen, C.L. Denis, and R. Parker. 2001. The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell. 104:377-386.
54. Tucker, M., R.R. Staples, M.A. Valencia-Sanchez, D. Muhlrad, and R. Parker. 2002. Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 21:1427-1436.
55. Uchida, N., S.-i. Hoshino, and T. Katada. 2004. Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J. Biol. Chem. 279:1383-1391.
56. van Dijk, E., N. Cougot, S. Meyer, S. Babajko, E. Wahle, and B. Seraphin. 2002. Human Dcp2: a catalytically active mRNA decapping enzyme located in specific cytoplasmic structures. EMBO J. 21:6915-6924.
57. Viswanathan, P., T. Ohn, Y.-C. Chiang, J. Chen, and C.L. Denis. 2004. 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.
58. Wang, Z., X. Jiao, A. Carr-Schmid, and M. Kiledjian. 2002. The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc. Natl. Acad. Sci. USA. 99:12663-12668.
59. Wu, L., J. Fan, and J.G. Belasco. 2006. MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. USA. 103:4034-4039.
60. Xu, N., P. Loflin, C.-Y.A. Chen, and A.-B. Shyu. 1998. A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res. 26:558-565.
61. Yamashita, A., T.C. Chang, Y. Yamashita, W. Zhu, Z. Zhong, C.Y. Chen, and A.B. Shyu. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat. Struct. Mol. Biol. 12:1054-1063.
62. Yang, W.-H., and D.B. Bloch. 2007. Probing the mRNA processing body using protein macroarrays and "autoantigenomics". RNA. 13:704-712.