Cytoplasmic RNA: A case of the tail wagging the dog

Nature Reviews Molecular Cell Biology

Volumn 14, Issue 10, 2013, Pages 643-653

  Norbury, Chris J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HEXOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; MESSENGER RNA; MICRORNA; NUCLEAR RNA; POLYADENYLIC ACID; POLYNUCLEOTIDE ADENYLYLTRANSFERASE;

ARTICLE; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION; HUMAN; NERVE CELL; NONHUMAN; OOCYTE; PRIORITY JOURNAL; RNA STABILITY; RNA TRANSLATION; RNA TRANSPORT;

CYTOPLASM; MICRORNAS; NUCLEOTIDYLTRANSFERASES; POLYADENYLATION; PROTEIN BIOSYNTHESIS; RNA; RNA STABILITY; RNA, MESSENGER;

CANIS FAMILIARIS; EUKARYOTA;

EID: 84886404826     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3645     Document Type: Article

References (102)

1. Aravind, L. & Koonin, E. V. DNA polymerase β-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res. 27, 1609-1618 (1999).
2. Ingle, C. A. & Kushner, S. R. Development of an in vitro mRNA decay system for Escherichia coli: poly(A) polymerase I is necessary to trigger degradation. Proc. Natl Acad. Sci. USA 93, 12926-12931 (1996).
3. Schmidt, M. J. & Norbury, C. J. Polyadenylation and beyond: emerging roles for noncanonical poly(A) polymerases. Wiley Interdiscip. Rev. RNA 1, 142-151 (2010).
4. Kadaba, S. et al. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. 18, 1227-1240 (2004).
5. Wyers, F. et al. Cryptic Pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 121, 725-737 (2005).
6. LaCava, J. et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121, 713-724 (2005).
7. Vanacova, S. et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 3, e189 (2005).
8. Lunde, B. M., Magler, I. & Meinhart, A. Crystal structures of the Cid1 poly (U) polymerase reveal the mechanism for UTP selectivity. Nucleic Acids Res. 40, 9815-9824 (2012).
9. Yates, L. A. et al. Structural basis for the activity of a cytoplasmic RNA terminal uridylyl transferase. Nature Struct. Mol. Biol. 19, 782-787 (2012).
10. Munoz-Tello, P., Gabus, C. & Thore, S. Functional implications from the Cid1 poly(U) polymerase crystal structure. Structure 20, 977-986 (2012).
11. Aphasizhev, R. & Aphasizheva, I. Uridine insertion/ deletion editing in trypanosomes: a playground for RNA-guided information transfer. Wiley Interdiscip. Rev. RNA 2, 669-685 (2011).
12. Chang, J. H. & Tong, L. Mitochondrial poly(A) polymerase and polyadenylation. Biochim. Biophys. Acta 1819, 992-997 (2012).
13. Nagaike, T., Suzuki, T. & Ueda, T. Polyadenylation in mammalian mitochondria: insights from recent studies. Biochim. Biophys. Acta 1779, 266-269 (2008).
14. Marzluff, W. F., Wagner, E. J. & Duronio, R. J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nature Rev. Genet. 9, 843-854 (2008).
15. Parker, R. RNA degradation in Saccharomyces cerevisae. Genetics 191, 671-702 (2012).
16. Yamashita, A. et al. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nature Struct. Mol. Biol. 12, 1054-1063 (2005).
17. van Hoof, A., Frischmeyer, P. A., Dietz, H. C. & Parker, R. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295, 2262-2264 (2002).
18. Frischmeyer, P. A. et al. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295, 2258-2261 (2002).
19. Chen, C. Y. & 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).
20. Schoenberg, D. R. & Maquat, L. E. Regulation of cytoplasmic mRNA decay. Nature Rev. Genet. 13, 246-259 (2012).
21. 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).
22. 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).
23. Chen, J., Chiang, Y. C. & Denis, C. L. CCR4, a 3′-5′ poly(A) RNA and ssDNA exonuclease, is the catalytic component of the cytoplasmic deadenylase. EMBO J. 21, 1414-1426 (2002).
24. Eulalio, A., Behm-Ansmant, I. & Izaurralde, E. P bodies: at the crossroads of post-transcriptional pathways. Nature Rev. Mol. Cell Biol. 8, 9-22 (2007).
25. Parker, R. & Sheth, U. P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635-646 (2007).
26. Kruk, J. A., Dutta, A., Fu, J., Gilmour, D. S. & Reese, J. C. The multifunctional Ccr4-Not complex directly promotes transcription elongation. Genes Dev. 25, 581-593 (2011).
27. Gao, M., Wilusz, C. J., Peltz, S. W. & Wilusz, J. A novel mRNA-decapping activity in HeLa cytoplasmic extracts is regulated by AU-rich elements. EMBO J. 20, 1134-1143 (2001).
28. Vasudevan, S. & Peltz, S. W. Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol. Cell 7, 1191-1200 (2001).
29. Mukherjee, D. et al. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J. 21, 165-174 (2002).
30. Chritton, J. J. & Wickens, M. A role for the poly(A)- binding protein Pab1p in PUF protein-mediated repression. J. Biol. Chem. 286, 33268-33278 (2011).
31. Goldstrohm, A. C., Hook, B. A., Seay, D. J. & Wickens, M. PUF proteins bind Pop2p to regulate messenger RNAs. Nature Struct. Mol. Biol. 13, 533-539 (2006).
32. Beilharz, T. H. et al. microRNA-mediated messenger RNA deadenylation contributes to translational repression in mammalian cells. PLoS ONE 4, e6783 (2009).
33. Eulalio, A. et al. Deadenylation is a widespread effect of miRNA regulation. RNA 15, 21-32 (2009).
34. Braun, J. E., Huntzinger, E., Fauser, M. & Izaurralde, E. GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol. Cell 44, 120-133 (2011).
35. Zekri, L., Kuzuoglu-Ozturk, D. & Izaurralde, E. GW182 proteins cause PABP dissociation from silenced miRNA targets in the absence of deadenylation. EMBO J. 32, 1052-1065 (2013).
36. Goldstrohm, A. C. & Wickens, M. Multifunctional deadenylase complexes diversify mRNA control. Nature Rev. Mol. Cell Biol. 9, 337-344 (2008).
37. Lee, J. E. et al. The PARN deadenylase targets a discrete set of mRNAs for decay and regulates cell motility in mouse myoblasts. PLoS Genet. 8, e1002901 (2012).
38. Coller, J. & Parker, R. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73, 861-890 (2004).
39. Tharun, S. & Parker, R. Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs. Mol. Cell 8, 1075-1083 (2001).
40. Chowdhury, A., Mukhopadhyay, J. & Tharun, S. The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs. RNA13, 998-1016 (2007).
41. Tharun, S. et al. Yeast Sm-like proteins function in mRNA decapping and decay. Nature 404, 515-518 (2000).
42. Lykke-Andersen, S., Brodersen, D. E. & Jensen, T. H. Origins and activities of the eukaryotic exosome. J. Cell Sci. 122, 1487-1494 (2009).
43. Rissland, O. S. & Norbury, C. J. Decapping is preceded by 3′ uridylation in a novel pathway of bulk mRNA turnover. Nature Struct. Mol. Biol. 16, 616-624 (2009).
44. Hu, W., Sweet, T. J., Chamnongpol, S., Baker, K. E. & Coller, J. Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 461, 225-229 (2009).
45. McGrew, L. L., Dworkin-Rastl, E., Dworkin, M. B. & Richter, J. D. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 3, 803-815 (1989).
46. Weill, L., Belloc, E., Bava, F. A. & Mendez, R. Translational control by changes in poly(A) tail length: recycling mRNAs. Nature Struct. Mol. Biol. 19, 577-585 (2012).
47. Groisman, I. et al. CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division. Cell 103, 435-447 (2000).
48. Eliscovich, C., Peset, I., Vernos, I. & Mendez, R. Spindle-localized CPE-mediated translation controls meiotic chromosome segregation. Nature Cell Biol. 10, 858-865 (2008).
49. Kim, K. W., Wilson, T. L. & Kimble, J. GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proc. Natl Acad. Sci. USA 107, 17445-17450 (2010).
50. Schmid, M., Kuchler, B. & Eckmann, C. R. Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev. 23, 824-836 (2009).
51. Wang, L., Eckmann, C. R., Kadyk, L. C., Wickens, M. & Kimble, J. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419, 312-316 (2002).
52. Kwak, J. E. et al. GLD2 poly(A) polymerase is required for long-term memory. Proc. Natl Acad. Sci. USA 105, 14644-14649 (2008).
53. Benoit, P., Papin, C., Kwak, J. E., Wickens, M. & Simonelig, M. PAP- and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 135, 1969-1979 (2008).
54. Barnard, D. C., Ryan, K., Manley, J. L. & Richter, J. D. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 119, 641-651 (2004).
55. Lin, C. L., Evans, V., Shen, S., Xing, Y. & Richter, J. D. The nuclear experience of CPEB: implications for RNA processing and translational control. RNA 16, 338-348 (2010).
56. Bava, F. A. et al. CPEB1 coordinates alternative 3′-UTR formation with translational regulation. Nature 495, 121-125 (2013).
57. Kim, J. H. & Richter, J. D. Opposing polymerase- deadenylase activities regulate cytoplasmic polyadenylation. Mol. Cell 24, 173-183 (2006).
58. Stebbins-Boaz, B., Cao, Q., de Moor, C. H., Mendez, R. & Richter, J. D. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol. Cell 4, 1017-1027 (1999).
59. Morris, J. Z., Hong, A. & Lilly, M. A. & Lehmann, R. twin, a CCR4 homolog, regulates cyclin poly(A) tail length to permit Drosophila oogenesis. Development 132, 1165-1174 (2005).
60. Novoa, I., Gallego, J., Ferreira, P. G. & Mendez, R. Mitotic cell-cycle progression is regulated by CPEB1 and CPEB4-dependent translational control. Nature Cell Biol. 12, 447-456 (2010).
61. Udagawa, T. et al. Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol. Cell 47, 253-266 (2012).
62. Wu, L. et al. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII mRNA at synapses. Neuron 21, 1129-1139 (1998).
63. Groisman, I. et al. Control of cellular senescence by CPEB. Genes Dev. 20, 2701-2712 (2006).
64. Burns, D. M., D'Ambrogio, A., Nottrott, S. & Richter, J. D. CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature 473, 105-108 (2011).
65. Lubas, M. et al. Interaction profiling identifies the human nuclear exosome targeting complex. Mol. Cell 43, 624-637 (2011).
66. Shcherbik, N., Wang, M., Lapik, Y. R. Srivastava, L. & Pestov, D. G. Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 11, 106-111 (2010).
67. Berndt, H. et al. Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA 18, 958-972 (2012).
68. Nakanishi, T. et al. Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. Dev. Biol. 289, 115-126 (2006).
69. Nakanishi, T. et al. Disruption of mouse poly(A) polymerase mGLD-2 does not alter polyadenylation status in oocytes and somatic cells. Biochem. Biophys. Res. Commun. 364, 14-19 (2007).
70. Tay, J. & Richter, J. D. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev. Cell 1, 201-213 (2001).
71. Berger-Sweeney, J., Zearfoss, N. R. & Richter, J. D. Reduced extinction of hippocampal-dependent memories in CPEB knockout mice. Learn. Mem. 13, 4-7 (2006).
72. Huang, Y. S., Kan, M. C., Lin, C. L. & Richter, J. D. CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 25, 4865-4876 (2006).
73. Kojima, S., Sher-Chen, E. L. & Green, C. B. Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 26, 2724-2736 (2012).
74. Wang, Y. et al. Rhythmic expression of Nocturnin mRNA in multiple tissues of the mouse. BMC Dev. Biol. 1, 9 (2001).
75. Ibrahim, F., Rohr, J., Jeong, W. J., Hesson, J. & Cerutti, H. Untemplated oligoadenylation promotes degradation of RISC-cleaved transcripts. Science 314, 1893 (2006).
76. Katoh, T. et al. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 23, 433-438 (2009).
77. D'Ambrogio, A., Gu, W., Udagawa, T., Mello, C. C. & Richter, J. D. Specific miRNA stabilization by Gld2-catalyzed monoadenylation. Cell Rep. 2, 1537-1545 (2012).
78. Kwak, J. E., Wang, L., Ballantyne, S., Kimble, J. & Wickens, M. Mammalian GLD-2 homologs are poly(A) polymerases. Proc. Natl Acad. Sci. USA 101, 4407-4412 (2004).
79. Shen, B. & Goodman, H. M. Uridine addition after microRNA-directed cleavage. Science 306, 997 (2004).
80. Rissland, O. S. & Norbury, C. J. The Cid1 poly(U) polymerase. Biochim. Biophys. Acta 1779, 286-294 (2008).
81. Kwak, J. E. & Wickens, M. A family of poly(U) polymerases. RNA 13, 860-867 (2007).
82. Rissland, O. S., Mikulasova, A. & Norbury, C. J. Efficient RNA polyuridylation by noncanonical poly(A) polymerases. Mol. Cell. Biol. 27, 3612-3624 (2007).
83. Li, J., Yang, Z., Yu, B., Liu, J. & Chen, X. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr. Biol. 15, 1501-1507 (2005).
84. Ibrahim, F. et al. Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc. Natl Acad. Sci. USA 107, 3906-3911 (2010).
85. Jones, M. R. et al. Zcchc11 uridylates mature miRNAs to enhance neonatal IGF-1 expression, growth, and survival. PLoS Genet. 8, e1003105 (2012).
86. Jones, M. R. et al. Zcchc11-dependent uridylation of microRNA directs cytokine expression. Nature Cell Biol. 11, 1157-1163 (2009).
87. Heo, I. et al. Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell 151, 521-532 (2012).
88. Newman, M. A., Mani, V. & Hammond, S. M. Deep sequencing of microRNA precursors reveals extensive 3′ end modification. RNA 17, 1795-1803 (2011).
89. Hagan, J. P., Piskounova, E. & Gregory, R. I. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nature Struct. Mol. Biol. 16, 1021-1025 (2009).
90. Heo, I. et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 138, 696-708 (2009).
91. Lehrbach, N. J. et al. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nature Struct. Mol. Biol. 16, 1016-1027 (2009).
92. Chang, H. M., Triboulet, R., Thornton, J. E. & Gregory, R. I. A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 497, 244-248 (2013).
93. Thornton, J. E., Chang, H. M., Piskounova, E. & Gregory, R. I. Lin28-mediated control of let-7 microRNA expression by alternative TUTases Zcchc11 (TUT4) and Zcchc6 (TUT7). RNA 18, 1875-1885 (2012).
94. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
95. Morozov, I. Y. et al. mRNA 3′ tagging is induced by nonsense-mediated decay and promotes ribosome dissociation. Mol. Cell. Biol. 32, 2585-2595 (2012).
96. Morozov, I. Y., Jones, M. G., Razak, A. A., Rigden, D. J. & Caddick, M. X. CUCU modification of mRNA promotes decapping and transcript degradation in Aspergillus nidulans. Mol. Cell. Biol. 30, 460-469 (2010).
97. Malecki, M. et al. The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J. 32, 1842-1854 (2013).
98. Mullen, T. E. & Marzluff, W. F. Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev. 22, 50-65 (2008).
99. Meeks-Wagner, D. & Hartwell, L. H. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 44, 43-52 (1986).
100. Schmidt, M. J., West, S. & Norbury, C. J. The human cytoplasmic RNA terminal U-transferase ZCCHC11 targets histone mRNAs for degradation. RNA 17, 39-44 (2011).
101. Hoefig, K. P. et al. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-dependent decay. Nature Struct. Mol. Biol. 20, 73-81 (2013).
102. Song, M. G. & Kiledjian, M. 3′ terminal oligo U-tract-mediated stimulation of decapping. RNA 13, 2356-2365 (2007).