XRN1: A Major 5' to 3' Exoribonuclease in Eukaryotic Cells

Enzymes

Volumn 31, Issue , 2012, Pages 97-114

  Geisler, Sarah ^a   Coller, Jeff ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Ribonuclease; RNA degradation; RNA stability; RNA turnover; XRN1

Indexed keywords

EUKARYOTA;

EID: 84866890839     PISSN: 18746047     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-404740-2.00005-7     Document Type: Chapter

References (87)

1. Ghosh S., Jacobson A. RNA decay modulates gene expression and controls its fidelity. Wiley Interdiscip Rev RNA 2010, 1:351-361.
2. Schoenberg D.R., Maquat L.E. Regulation of cytoplasmic mRNA decay. Nat Rev Genet 2012, 13:246-259.
3. Nicholson A, Ribonucleases (series: nucleic acids and molecular biology), Recherche. 2006; vol 26.
4. Stevens A. 5'-Exoribonuclease 1: Xrn1. Methods Enzymol 2001, 342:251-259.
5. Jones C.I., Zabolotskaya M.V., Newbury S.F. The 5' → 3' exoribonuclease XRN1/Pacman and its functions in cellular processes and development. Wiley Interdiscip Rev RNA 2012, 3:455-468.
6. Furuichi Y., LaFiandra A., Shatkin A.J. 5'-Terminal structure and mRNA stability. Nature 1977, 266:235-239.
7. Shimotohno K., Kodama Y., Hashimoto J., Miura K.I. Importance of 5'-terminal blocking structure to stabilize mRNA in eukaryotic protein synthesis. Proc Natl Acad Sci U S A 1977, 74:2734-2738.
8. Stevens A. An exoribonuclease from Saccharomyces cerevisiae: effect of modifications of 5' end groups on the hydrolysis of substrates to 5'mononucleotides. Biochem Biophys Res Commun 1978, 81:656-661.
9. Stevens A. Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yields 5'-mononucleotides by a 5' → 3' mode of hydrolysis. J Biol Chem 1980, 255:3080-3085.
10. Larimer F.W., Hsu C.L., Maupin M.K., Stevens A. Characterization of the XRN1 gene encoding a 5' → 3' exoribonuclease: sequence data and analysis of disparate protein and mRNA levels of gene-disrupted yeast cells. Gene 1992, 120:51-57.
11. Hsu C.L., Stevens A. Yeast cells lacking 5' → 3' exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5' cap structure. Mol Cell Biol 1993, 13:4826-4835.
12. Decker C.J., Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev 1993, 7:1632-1643.
13. Muhlrad D., Decker C.J., Parker R. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5' → 3' digestion of the transcript. Genes Dev 1994, 8:855-866.
14. Beelman C.A., Stevens A., Caponigro G., LaGrandeur T.E., Hatfield L., Fortner D.M., et al. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 1996, 382:642-646.
15. Dunckley T., Parker R. The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 1999, 18:5411-5422.
16. Isken O., Maquat L.E. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev 2007, 21:1833-1856.
17. Baker K.E., Parker R. Nonsense-mediated mRNA decay: terminating erroneous gene expression. Curr Opin Cell Biol 2004, 16:293-299.
18. Muhlrad D., Parker R. Premature translational termination triggers mRNA decapping. Nature 1994, 370:578-581.
19. Huntzinger E., Kashima I., Fauser M., Saulière J., Izaurralde E. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 2008, 14:2609-2617.
20. Eberle A.B., Lykke-Andersen S., Muhlemann O., Jensen T.H. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 2009, 16:49-55.
21. Doma M.K., Parker R. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 2006, 440:561-564.
22. Filipowicz W. RNAi: the nuts and bolts of the RISC machine. Cell 2005, 122:17-20.
23. Eulalio A., Huntzinger E., Izaurralde E. Getting to the root of miRNA-mediated gene silencing. Cell 2008, 132:9-14.
24. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
25. Olsen P.H., Ambros V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 1999, 216:671-680.
26. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
27. Lim L.P., et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
28. Behm-Ansmant I., et al. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 2006, 20:1885-1898.
29. Eulalio A., et al. Deadenylation is a widespread effect of miRNA regulation. RNA 2009, 15:21-32.
30. Giraldez A.J., et al. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79.
31. Wu L., Fan J., Belasco J.G. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci U S A 2006, 103:4034-4039.
32. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
33. Bazzini A.A., Lee M.T., Giraldez A.J. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 2012, 336:233-237.
34. Djuranovic S., Nahvi A., Green R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 2012, 336:237-240.
35. Bagga S., et al. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 2005, 122:553-563.
36. Valencia-Sanchez M.A., et al. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 2006, 20:515-524.
37. Newbury S., Woollard A. The 5'-3' exoribonuclease xrn-1 is essential for ventral epithelial enclosure during C. elegans embryogenesis. RNA 2004, 10:59-65.
38. Dorner S., Eulalio A., Huntzinger E., Izaurralde E. Delving into the diversity of silencing pathways 2007, 723-729.
39. Orban T.I., Izaurralde E. Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 2005, 11:459-469.
40. Souret F.F., Kastenmayer J.P., Green P.J. AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 2004, 15:173-183.
41. Eulalio A., Behm-Ansmant I., Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007, 8:9-22.
42. Franks T.M., Lykke-Andersen J. The control of mRNA decapping and P-body formation. Mol Cell 2008, 32:605-615.
43. Parker R., Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell 2007, 25:635-646.
44. Hu W., Sweet T.J., Chamnongpol S., Baker K.E., Coller J. Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 2009, 461:225-229.
45. Beelman C.A., Parker R. Differential effects of translational inhibition in cis and in trans on the decay of the unstable yeast MFA2 mRNA. J Biol Chem 1994, 269:9687-9692.
46. Mangus D.A., Jacobson A. Linking mRNA turnover and translation: assessing the polyribosomal association of mRNA decay factors and degradative intermediates. Methods 1999, 17:28-37.
47. Bashkirov V.I., Scherthan H., Solinger J.A., Buerstedde J.M., Heyer W.D. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates. J Cell Biol 1997, 136:761-773.
48. Eystathioy T., Chan E.K.L., Tenenbaum S.A., Keene J.D., Griffith K., Fritzler M.J. A phosphorylated cytoplasmic autoantigen, GW182, associates with a unique population of human mRNAs within novel cytoplasmic speckles. Mol Biol Cell 2002, 13:1338-1351.
49. Eulalio A., Tritschler F., Izaurralde E. The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA 2009, 15:1433-1442.
50. Sheth U., Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 2003, 300:805-808.
51. Cougot N., Babajko S., Seraphin B. Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 2004, 165:31-40.
52. Leung A.K., Calabrese J.M., Sharp P.A. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc Natl Acad Sci U S A 2006, 103:18125-18130.
53. Sweet T.J., Boyer B., Hu W., Baker K.E., Coller J. Microtubule disruption stimulates P-body formation. RNA 2007, 13:493-502.
54. Decker C.J., Teixeira D., Parker R. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J Cell Biol 2007, 179:437-449.
55. Eulalio A., Behm-Ansmant I., Schweizer D., Izaurralde E. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 2007, 27:3970-3981.
56. Chu C.Y., Rana T.M. Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol 2006, 4:e210.
57. Wang Y., Liu C.L., Storey J.D., Tibshirani R.J., Herschlag D., Brown P.O. Precision and functional specificity in mRNA decay. Proc Natl Acad Sci U S A 2002, 99:5860-5865.
58. Berretta J., Morillon A. Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep 2009, 10:973-982.
59. Geisler S., Lojek L., Khalil A.M., Baker K.E., Coller J. Decapping of long noncoding RNAs regulates inducible genes. Mol Cell 2012, 45:279-291.
60. Thompson D.M., Parker R. Cytoplasmic decay of intergenic transcripts in Saccharomyces cerevisiae. Mol Cell Biol 2007, 27:92-101.
61. van Dijk E.L., Chen C.L., d'Aubenton-Carafa Y., Gourvennec S., Kwapisz M., Roche V., et al. XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 2011, 475:114-117.
62. ENCODE Project Consortium, Birney E., Stamatoyannopoulos J.A., Dutta A., Guigó R., Gingeras T.R., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816.
63. Nagalakshmi U., Wang Z., Waern K., Shou C., Raha D., Gerstein M., et al. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320:1344-1349.
64. Xu Z., Wei W., Gagneur J., Perocchi F., Clauder-Münster S., Camblong J., et al. Bidirectional promoters generate pervasive transcription in yeast. Nature 2009, 457:1033-1037.
65. Ponting C.P., Belgard T.G. Transcribed dark matter: meaning or myth?. Hum Mol Genet 2010, 19:R162-R168.
66. Berretta J., Pinskaya M., Morillon A. A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev 2008, 22:615-626.
67. Guttman M., Amit I., Garber M., French C., Lin M.F., Feldser D., et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-227.
68. Hongay C.F., Grisafi P.L., Galitski T., Fink G.R. Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell 2006, 127:735-745.
69. Loewer S., Cabili M.N., Guttman M., Loh Y.-H., Thomas K., Park I.H., et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 2010, 42:1113-1117.
70. Luke B., Panza A., Redon S., Iglesias N., Li Z., Lingner J. The Rat1p 5' → 3' exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol Cell 2008, 32:465-477.
71. Ponting C.P., Oliver P.L., Reik W. Evolution and functions of long noncoding RNAs. Cell 2009, 136:629-641.
72. Niland C.N., Merry C.R., Khalil A.M. Emerging roles for long non-coding RNAs in cancer and neurological disorders. Front Genet 2012, 3:25.
73. Qureshi I.A., Mattick J.S., Mehler M.F. Long non-coding RNAs in nervous system function and disease. Brain Res 2010, 1338:20-35.
74. Tsai M.-C., Spitale R.C., Chang H.Y. Long intergenic noncoding RNAs: new links in cancer progression. Cancer Res 2011, 71:3-7.
75. Khalil A.M., Guttman M., Huarte M., Garber M., Raj A., Rivea Morales D., et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 2009, 106:11667-11672.
76. Martens J.A., Wu P.-Y.J., Winston F. Regulation of an intergenic transcript controls adjacent gene transcription in Saccharomyces cerevisiae. Genes Dev 2005, 19:2695-2704.
77. Toesca I., Nery C.R., Fernandez C.F., Sayani S., Chanfreau G.F. Cryptic transcription mediates repression of subtelomeric metal homeostasis genes. PLoS Genet 2011, 7:e1002163.
78. Marquardt S., Hazelbaker D.Z., Buratowski S. Distinct RNA degradation pathways and 3' extensions of yeast non-coding RNA species. Transcription 2011, 2:145-154.
79. Chernyakov I., Whipple J.M., Kotelawala L., Grayhack E.J., Phizicky E.M. Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5'-3' exonucleases Rat1 and Xrn1. Genes Dev 2008, 22:1369-1380.
80. Whipple J.M., Lane E.A., Chernyakov I., D'Silva S., Phizicky E.M. The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev 2011, 25:1173-1184.
81. Henry Y., Wood H., Morrissey J.P., Petfalski E., Kearsey S., Tollervey D. The 5' end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. EMBO J 1994, 13:2452-2463.
82. Geerlings T.H., Vos J.C., Raué H.A. The final step in the formation of 25S rRNA in Saccharomyces cerevisiae is performed by 5' → 3' exonucleases. RNA 2000, 6:1698-1703.
83. Petfalski E., Dandekar T., Henry Y., Tollervey D. Processing of the precursors to small nucleolar RNAs and rRNAs requires common components. Mol Cell Biol 1998, 18:1181-1189.
84. Liu H., Kiledjian M. Decapping the message: a beginning or an end. Biochem Soc Trans 2006, 34:35-38.
85. Wang Z., Kiledjian M. Functional link between the mammalian exosome and mRNA decapping. Cell 2001, 107:751-762.
86. Liu H., Kiledjian M. Scavenger decapping activity facilitates 5' → 3' mRNA decay. Mol Cell Biol 2005, 25:9764-9772.
87. Dichtl B., Stevens A., Tollervey D. Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J 1997, 16:7184-7195.