The role of the 5′-3′ exoribonuclease XRNA in transcriptome-wide mRNA degradation

RNA

Volumn 17, Issue 11, 2011, Pages 2039-2047

  Manful, Theresa ^a   Fadda, Abeer ^a   Clayton, Christine ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

mRNA decay; Polycistronic; RNASeq; Trypanosoma; Xrn1

Indexed keywords

EXORIBONUCLEASE; MESSENGER RNA; RIBOSOME PROTEIN; RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; XRNA ENZYME; 5' EXORIBONUCLEASE; 5'-EXORIBONUCLEASE; PROTOZOAL RNA;

ADENYLATION; ARTICLE; GENE DOSAGE; GENE SEQUENCE; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; RNA DEGRADATION; TRYPANOSOMA; ENZYMOLOGY; GENETICS; METABOLISM; OPEN READING FRAME; RNA STABILITY; TRYPANOSOMA BRUCEI;

PROTISTA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EXORIBONUCLEASES; OPEN READING FRAMES; RNA STABILITY; RNA, MESSENGER; RNA, PROTOZOAN; TRANSCRIPTOME; TRYPANOSOMA BRUCEI BRUCEI;

EID: 80054730384     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2837311     Document Type: Article

References (63)

1. Agarwal A, Koppstein D, Rozowsky J, Sboner A, Habegger L, Hillier L, Sasidharan R, Reinke V, Waterston R, Gerstein M. 2010. Comparison and calibration of transcriptome data from RNA-Seq and tiling arrays. BMC Genomics 11: 383. doi: 10.1186/1471-2164-11-383.
2. Archer S, Inchaustegui D, de Queiroz R, Clayton C. 2011. The cell-cycle regulated transcriptome of an early-branching eukaryote. PLoS ONE 6: e18425. doi: 10.1371/journal.pone.0018425.
3. Bernstein J, Khodursky A, Lin P, Lin-Chao S, Cohen S. 2002. Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays. Proc Natl Acad Sci 99: 9697-9702. (Pubitemid 34831110)
4. Carver T, Berriman M, Tivey A, Patel C, Böhme U, Barrell B, Parkhill J, Rajandream M. 2008. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24: 2672-2676. (Pubitemid 352722607)
5. Clayton CE. 2002. Life without transcriptional control? From fly to man and back again. EMBO J 21: 1881-1888. (Pubitemid 34437185)
6. Clayton C, Estevez A. 2010. The exosomes of trypanosomes and other protists. In RNA exosome (ed. T. Jensen), pp. 39-49. Landes Bioscience, Austin.
7. Clayton C, Shapira M. 2007. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101. (Pubitemid 47600362)
8. Colasante C, Robles A, Li C-H, Schwede A, Benz C, Voncken F, Guilbride DL, Clayton C. 2007. Regulated expression of glycosomal phosphoglycerate kinase in Trypanosoma brucei. Mol Biochem Parasitol 151: 193-204. (Pubitemid 46054215)
9. Fernández-Moya S, Estévez A. 2010. Posttranscriptional control and the role of RNA-binding proteins in gene regulation in trypanosomatid protozoan parasites. WIREs RNA 1: 34-46.
10. Figueiredo L, Janzen C, Cross G. 2008. A histone methyltransferase modulates antigenic variation in African trypanosomes. PLoS Biol 6: e161. doi: 10.1371/journal.pbio.0060161.
11. Gibson WC, Swinkels BW, Borst P. 1988. Post-transcriptional control of the differential expression of phosphoglycerate kinase genes in Trypanosoma brucei. J Mol Biol 201: 315-325.
12. Grigull J, Mnaimneh S, Pootoolal J, Robinson M, Hughes T. 2004. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol Cell Biol 24: 5534-5547. (Pubitemid 38738184)
13. Gunzl A, Bruderer T, Laufer G, Schimanski B, Tu LC, Chung HM, Lee PT, Lee MG. 2003. RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryot Cell 2: 542-551. (Pubitemid 36774702)
14. Haanstra J, Stewart M, Luu V-D, van Tuijl A, Westerhoff H, Clayton C, Bakker B. 2008. Control and regulation of gene expression: quantitative analysis of the expression of phosphoglycerate kinase in bloodstream form Trypanosoma brucei. J Biol Chem 283: 2495-2507.
15. He F, Li X, Spatrick P, Casillo R, Dong S, Jacobson A. 2003. Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol Cell 12: 1439-1452. (Pubitemid 38037013)
16. Hughes K, Wand M, Foulston L, Young R, Harley K, Terry S, Ersfeld K, Rudenko G. 2007. A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO J 26: 2400-2410. (Pubitemid 46685860)
17. Irmer H, Clayton CE. 2001. Degradation of the EP1 mRNA in Trypanosoma brucei is initiated by destruction of the 3′-untranslated region. Nucleic Acids Res 29: 4707-4715. (Pubitemid 33095032)
18. Ivens AC. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
19. Jacobs Anderson JS, Parker RP. 1998. 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: 1497-1506.
20. Jensen B, Sivam D, Kifer C, Myler P, Parsons M. 2009. Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics 10: 482. doi: 10.1186/1471-2164-10-482.
21. Kabani S, Fenn K, Ross A, Ivens A, Smith T, Ghazal P, Matthews K. 2009. Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 10: 427. doi: 10.1186/1471-2164-10-427.
22. Kebaara B, Atkin A. 2009. Long 3′-UTRs target wild-type mRNAs for nonsense-mediated mRNA decay in Saccharomyces cerevisiae. Nucleic Acids Res 37: 2771-2778.
23. Kolev N, Franklin J, Carmi S, Shi H, Michaeli S, Tschudi C. 2010. The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 6: e1001090. doi: 10.1371/journal.ppat.1001090.
24. Kramer S, Carrington M. 2011. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol 27: 23-30.
25. Langmead B, Trapnell C, Pop M, Salzberg S. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25. doi: 10.1186/gb-2009-10-3-r25.
26. Li C-H, Irmer H, Gudjonsdottir-Planck D, Freese S, Salm H, Haile S, Estévez AM, Clayton CE. 2006. Roles of a Trypanosoma brucei 5′→3′ exoribonuclease homologue in mRNA degradation. RNA 12: 2171-2186. (Pubitemid 44865964)
27. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
28. Liu Q, Liang X, Uliel S, Belahcen M, Unger R, Michaeli S. 2004. Identification and functional characterization of Lsm proteins in Trypanosoma brucei. J Biol Chem 279: 18210-18219. (Pubitemid 38623234)
29. Martínez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ. 2003. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11: 1291-1299. (Pubitemid 36645147)
30. Martínez-Calvillo S, Nguyen D, Stuart K, Myler PJ. 2004. Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot Cell 3: 506-517. (Pubitemid 38497988)
31. Metzker M. 2010. Sequencing technologies: the next generation. Nat Rev Genet 11: 31-46.
32. Milone J, Wilusz J, Bellofatto V. 2004. Characterization of deadenylation in trypanosome extracts and its inhibition by poly(A)-binding protein Pab1p. RNA 10: 448-457. (Pubitemid 38241005)
33. Mortazavi A, Williams B, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. (Pubitemid 351911867)
34. Muhlrad D, Decker CJ, Parker R. 1994. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′→3′ digestion of the transcript. Genes Dev 8: 855-866.
35. Narsai R, Howell K, Millar A, O'Toole N, Small I, Whelan J. 2007. Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. Plant Cell 19: 3418-3436.
36. Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L, Baerlocher L, Roditi I, Ochsenreiter T. 2010. Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 6: e1001037. doi: 10.1371/journal.ppat.1001037.
37. Ouellette M, Papadopoulou B. 2009. Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J Biol 8: 100. doi: 10.1186/jbiol203.
38. Palenchar JB, Bellofatto V. 2006. Gene transcription in trypanosomes. Mol Biochem Parasitol 146: 135-141. (Pubitemid 43356354)
39. Parker R, Song H. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 11: 121-127. (Pubitemid 38146514)
40. Queiroz R, Benz C, Fellenberg K, Hoheisel JD, Clayton C. 2009. Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics 10: 495. doi: 10.1186/1471-2164-10-495.
41. Quijada L, Hartmann C, Guerra-Giraldez C, Drozdz M, Irmer H, Clayton CE. 2002. Expression of the human RNA-binding protein HuR in Trypanosoma brucei induces differentiation-related changes in the abundance of developmentally- regulated mRNAs. Nucleic Acids Res 30: 1-11.
42. Ramani A, Nelson A, Kapranov P, Bell I, Gingeras T, Fraser A. 2009. High resolution transcriptome maps for wild-type and nonsense-mediated decay-defective Caenorhabditis elegans. Genome Biol 10: R101. doi: 10.1186/gb-2009-10-9-r101.
43. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream M, Barrell B. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
44. Rymarquis LA, Souret FF, Green PJ. 2011. Evidence that XRN4, an Arabidopsis homolog of exoribonuclease XRN1, preferentially impacts transcripts with certain sequences or in particular functional categories. RNA 17: 501-511.
45. Schwede A, Ellis L, Luther J, Carrington M, Stoecklin G, Clayton C. 2008. A role for Caf1 in mRNA deadenylation and decay in trypanosomes and human cells. Nucleic Acids Res 36: 3374-3388. (Pubitemid 351863370)
46. Schwede A, Manful T, Jha B, Helbig C, Bercovich N, Stewart M, Clayton C. 2009. The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res 37: 5511-5528.
47. Sharova L, Sharov A, Nedorezov T, Piao Y, Shaik N, Ko M. 2009. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res 16: 45-58.
48. Shock J, Fischer K, DeRisi J. 2007. Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol 8: R134. doi: 10.1186/gb-2007-8-7-r134.
49. Siegel T, Hekstra D, Kemp L, Figueiredo L, Lowell J, Fenyo D, Wang X, Dewell S, Cross G. 2009. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 23: 1063-1076.
50. Siegel T, Hekstra D, Wang X, Dewell S, Cross G. 2010. Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res 38: 4946-4957.
51. Souret FF, Kastenmayer JP, Green PJ. 2004. AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol Cell 15: 173-183. (Pubitemid 38950965)
52. Steglich C, Lindell D, Futschik M, Rector T, Steen R, Chisholm S. 2010. Short RNA half-lives in the slow-growing marine cyanobacterium Prochlorococcus. Genome Biol 11: R54. doi: 10.1186/gb-2010-11-5-r54.
53. Stern MZ, Gupta SK, Salmon-Divon M, Haham T, Barda O, Levi S, Wachtel C, Nilsen TW, Michaeli S. 2009. Multiple roles for polypyrimidine tract binding (PTB) proteins in trypanosome RNA metabolism. RNA 15: 648-665.
54. Stevens A. 1980. Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yields 59-mononucleotides by a 5′→3′ mode of hydrolysis. J Biol Chem 255: 3080-3085. (Pubitemid 10089260)
55. Stoecklin G, Mayo T, Anderson P. 2006. ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep 7: 72-77.
56. 't Hoen P, Hirsch M, de Meijer E, de Menezes R, van Ommen G, den Dunnen J. 2011. mRNA degradation controls differentiation state-dependent differences in transcript and splice variant abundance. Nucleic Acids Res 39: 556-566.
57. van Duersen FJ, Shahi SK, Hartmann C, Guerra-Giraldez C, Matthew KR, Clayton CE. 2001. Characterisation of the growth and differentiation in vivo and in vitro of bloodstream-form Trypanosoma brucei strain TREU 927. Mol Biochem Parasitol 112: 163-172.
58. Vanhamme L, Postiaux S, Poelvoorde P, Pays E. 1999. Differential regulation of ESAG transcripts in Trypanosoma brucei. Mol Biochem Parasitol 102: 35-42. (Pubitemid 29342272)
59. Vijayasarathy S, Ernest I, Itzhaki JE, Sherman D, Mowatt MR, Michels PAM, Clayton CE. 1990. The genes encoding fructose bisphosphate aldolase in Trypanosoma brucei are interspersed with unrelated genes. Nucleic Acids Res 18: 2967-2975.
60. Wang Y, Liu CL, Storey JD, Tibshirani RJ, Herschlag D, Brown PO. 2002. Precision and functional specificity in mRNA decay. Proc Natl Acad Sci 99: 5860-5865. (Pubitemid 34493230)
61. Webb H, Burns R, Ellis L, Kimblin N, Carrington M. 2005. Developmentally regulated instability of the GPI-PLC mRNA is dependent on a short-lived protein factor. Nucleic Acids Res 33: 1503-1512. (Pubitemid 41418379)
62. Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M, Magnasco M, Darnell J Jr. 2003. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13: 1863-1872. (Pubitemid 36987192)
63. Zhang X, Cui J, Nilsson D, Gunasekera K, Chanfon A, Song X, Wang H, Xu Y, Ochsenreiter T. 2010. The Trypanosoma brucei MitoCarta and its regulation and splicing pattern during development. Nucleic Acids Res 38: 7378-7387.