Transcriptome-wide analysis of trypanosome mRNA decay reveals complex degradation kinetics and suggests a role for co-transcriptional degradation in determining mRNA levels

Molecular Microbiology

Volumn 94, Issue 2, 2014, Pages 307-326

  Fadda, Abeer ^a,c   Ryten, Mark ^d   Droll, Dorothea ^c   Rojas, Federico ^e   Färber, Valentin ^b,c   Haanstra, Jurgen R ^f,g   Merce, Clemetine ^c   Bakker, Barbara M ^f,g   Matthews, Keith ^e   Clayton, Christine ^c  

^a SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

^b Fresenius Kabi Deutschland GmbH   (Germany)

^c GERMAN CANCER RESEARCH CENTER   (Germany)

^d University of Edinburgh ^*  (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^g VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EXORIBONUCLEASE; MESSENGER RNA; TRANSCRIPTOME;

ARTICLE; CONTROLLED STUDY; GENETIC REGULATION; HALF LIFE TIME; LIFE CYCLE STAGE; MICROBIAL KINETICS; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; RNA DEGRADATION; RNA PROCESSING; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRYPANOSOMA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; RNA STABILITY;

GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; RNA STABILITY; TRYPANOSOMA;

EID: 84916606564     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12764     Document Type: Article

References (85)

1. Ali, J., Tagoe, D., Munday, J., Donachie, A., Morrison, L., and de Koning, H. (2013) Pyrimidine biosynthesis is not an essential function for Trypanosoma brucei bloodstream forms. PLoS ONE 8: e58034.
2. Ali, J.A., Creek, D.J., Burgess, K., Allison, H.C., Field, M.C., Maser, P., and De Koning, H.P. (2012) Pyrimidine salvage in Trypanosoma brucei bloodstream forms and the trypanocidal action of halogenated pyrimidines. Mol Pharmacol 83: 439-453.
3. Alsford, S., Kawahara, T., Glover, L., and Horn, D. (2005) Tagging a T. brucei RRNA locus improves stable transfection efficiency and circumvents inducible expression position effects. Mol Biochem Parasitol 144: 142-148.
4. Anders, S., and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
5. Avliyakulov, N., Hines, J., and Ray, D. (2003) Sequence elements in both the intergenic space and the 3′ untranslated region of the Crithidia fasciculata KAP3 gene are required for cell cycle regulation of KAP3 mRNA. Eukaryot Cell 2: 671-677.
6. Bakker, B.M., Krauth-Siegel, R.L., Clayton, C., Matthews, K., Girolami, M., Westerhoff, H.V., etal. (2010) The silicon trypanosome. Parasitology 137: 1333-1341.
7. Bringaud, F., Riviere, L., and Coustou, V. (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 149: 1-9.
8. Brooks, D.R., Denise, H., Westrop, G.D., and Coombs, G.H. (2001) The stage-regulated expression of Leishmania mexicana CPB cysteine proteases is mediated by an intercistronic sequence element. J Biol Chem 276: 47061-47069.
9. Brown, B.S.V., Chi, T.B., and Williams, N. (2001) The Trypanosoma brucei mitochondrial ATP synthase is developmentally regulated at the level of transcript stability. Mol Biochem Parasitol 115: 177-187.
10. Chaudhuri, M., Sharan, R., and Hill, G. (2002) Trypanosome alternative oxidase is regulated post-transcriptionally at the level of RNA stability. J Eukaryot Microbiol 49: 263-269.
11. Chekanova, J.A., Gregory, B.D., Reverdatto, S.V., Chen, H., Kumar, R., Hooker, T., etal. (2007) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131: 1340-1353.
12. Churchman, L.S., and Weissman, J.S. (2011) Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469: 368-373.
13. Clayton, C. (2013) The regulation of trypanosome gene expression by RNA-binding proteins. PLoS Pathog 9: e1003680.
14. Clayton, C., and Estevez, A. (2010) The exosomes of trypanosomes and other protists. In RNA Exosome. Jensen, T. (ed.). Austin, TX: Landes Bioscience, pp. 39-49.
15. Colasante, C., Robles, A., Li, C.-H., Schwede, A., Benz, C., Voncken, F., etal. (2007) Regulated expression of glycosomal phosphoglycerate kinase in Trypanosoma brucei. Mol Biochem Parasitol 151: 193-204.
16. Cristodero, M., and Clayton, C. (2007) Trypanosome MTR4 in involved in ribosomal RNA processing. Nucleic Acids Res 35: 7023-7030.
17. Daniels, J., Gull, K., and Wickstead, B. (2010) Cell biology of the trypanosome genome. Microbiol Mol Biol Rev 74: 552-569.
18. Darzacq, X., Shav-Tal, Y., de Turris, V., Brody, Y., Shenoy, S., Phair, R., and Singer, R. (2007) In vivo dynamics of RNA polymerase II transcription. Nat Struct Mol Biol 14: 796-806.
19. Deneke, C., Lipowsky, R., and Valleriani, A. (2013) Complex degradation processes lead to non-exponential decay patterns and age-dependent decay rates of messenger RNA. PLoS ONE 8: e55442.
20. Dennis, J., Gay, D., and Roy Welsch, R. (1981) Algorithm 573: an adaptive nonlinear least-squares algorithm. ACM Trans Math Softw 7: 367-383.
21. Erben, E., Chakraborty, C., and Clayton, C. (2014) The CAF1-NOT complex of trypanosomes. Front Genet 4: 299.
22. Estévez, A. (2008) The RNA-binding protein TbDRBD3 regulates the stability of a specific subset of mRNAs in trypanosomes. Nucleic Acids Res 36: 4573-4586.
23. Etheridge, R.D., Clemens, D.M., Gershon, P.D., and Aphasizhev, R. (2009) Identification and characterization of nuclear non-canonical poly(A) polymerases from Trypanosoma brucei. Mol Biochem Parasitol 164: 66-73.
24. Fadda, A., Färber, V., Droll, D., and Clayton, C. (2013) The roles of 3′-exoribonucleases and the exosome in trypanosome mRNA degradation. RNA 19: 937-947.
25. Färber, V., Erben, E., Sharma, S., Stoecklin, G., and Clayton, C. (2013) Trypanosome CNOT10 is essential for the integrity of the NOT deadenylase complex and for degradation of many mRNAs. Nucleic Acids Res 41: 1211-1222.
26. Fernández-Moya, S., and Estévez, A. (2010) Posttranscriptional control and the role of RNA-binding proteins in gene regulation in trypanosomatid protozoan parasites. Wiley Interdiscip Rev RNA 1: 34-46.
27. Fluck, C., Salomone, J., Kurath, U., and Roditi, I. (2003) Cycloheximide-mediated accumulation of transcripts from a procyclin expression site depends on the intergenic region. Mol Biochem Parasitol 127: 93-97.
28. Grigull, J., Mnaimneh, S., Pootoolal, J., Robinson, M., and 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.
29. Gudipati, R.K., Xu, Z., Lebreton, A., Seraphin, B., Steinmetz, L.M., Jacquier, A., and Libri, D. (2012) Extensive degradation of RNA precursors by the exosome in wild-type cells. Mol Cell 48: 409-421.
30. Gunasekera, K., Wuthrich, D., Braga-Lagache, S., Heller, M., and Ochsenreiter, T. (2012) Proteome remodelling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry. BMC Genomics 13: 556.
31. Haanstra, J., Stewart, M., Luu, V.-D., van Tuijl, A., Westerhoff, H., Clayton, C., and 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.
32. Haile, S., Estévez, A.M., and Clayton, C. (2003) A role for the exosome in the initiation of degradation of unstable mRNAs. RNA 9: 1491-1501.
33. Haimovich, G., Medina, D.A., Causse, S.Z., Garber, M., Millan-Zambrano, G., Barkai, O., etal. (2013) Gene expression is circular: factors for mRNA degradation also foster mRNA synthesis. Cell 153: 1000-1011.
34. Harigaya, Y., and Parker, R. (2012) Global analysis of mRNA decay intermediates in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 109: 11764-11769.
35. Hoops, S., Sahle, S., Gauges, R., Lee, C., Pahle, J., Simus, N., etal. (2006) COPASI - a COmplex PAthway SImulator. Bioinformatics 22: 3067-3074.
36. Hotz, H.-R., Hartmann, C., Huober, K., Hug, M., and Clayton, C.E. (1997) Mechanisms of developmental regulation in Trypanosoma brucei: a polypyrimidine tract in the 3′-untranslated region of a trypanosome surface protein mRNA affects RNA abundance and translation. Nucleic Acids Res 25: 3017-3025.
37. Houalla, R., Devaux, F., Fatica, A., Kufel, J., Barrass, D., Torchet, C., and Tollervey, D. (2006) Microarray detection of novel nuclear RNA substrates for the exosome. Yeast 23: 439-454.
38. Huang, J., and van der Ploeg, L. (1991) Maturation of polycistronic pre-mRNA in Trypanosoma brucei: analysis of trans splicing and poly(A) addition at nascent RNA transcripts from the hsp70 locus. Mol Cell Biol 11: 3180-3190.
39. Irmer, H., and Clayton, C.E. (2001) Degradation of the EP1 mRNA in Trypanosoma brucei is initiated by destruction of the 3′-untranslated region. Nucleic Acids Res 29: 4707-4715.
40. Jha, B., Fadda, A., Merce, C., Mugo, E., Droll, D., and Clayton, C. (2014) Depletion of the trypanosome pumilio domain protein PUF2 causes transcriptome changes related to coding region length. Eukaryot Cell 13: 664-674.
41. Kapotas, N., and Bellofatto, V. (1993) Differential response to RNA trans-splicing signals within the phosphoglycerate kinase gene cluster in Trypanosoma brucei. Nucleic Acids Res 21: 4067-4072.
42. Kelly, S., Kramer, S., Schwede, A., Maini, P., Gull, K., and Carrington, M. (2012) Genome organization is a major component of gene expression control in response to stress and during the cell division cycle in trypanosomes. Open Biol 2: 120033.
43. Kilchert, C., and Vasiljeva, L. (2013) mRNA quality control goes transcriptional. Biochem Soc Trans 41: 1666-1672.
44. Kiss, D.L., and Andrulis, E.D. (2010) Genome-wide analysis reveals distinct substrate specificities of Rrp6, Dis3, and core exosome subunits. RNA 16: 781-791.
45. Kolev, N., Franklin, J., Carmi, S., Shi, H., Michaeli, S., and Tschudi, C. (2010) The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 6: e1001090.
46. Kramer, S., and Carrington, M. (2011) Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol 27: 23-30.
47. Kramer, S., Queiroz, R., Ellis, L., Webb, H., Hoheisel, J., Clayton, C., and Carrington, M. (2008) Stress granules and the heat shock response in Trypanosoma brucei. J Cell Sci 121: 3002-3014.
48. Lamour, N., Riviere, L., Coustou, V., Coombs, G.H., Barrett, M.P., and Bringaud, F. (2005) Proline metabolism in procyclic Trypanosoma brucei is down-regulated in the presence of glucose. J Biol Chem 280: 11902-11910.
49. Lee, J.H., Jung, H.S., and Gunzl, A. (2009) Transcriptionally active TFIIH of the early-diverged eukaryote Trypanosoma brucei harbors two novel core subunits but not a cyclin-activating kinase complex. Nucleic Acids Res 37: 3811-3820.
50. Li, C.-H., Irmer, H., Gudjonsdottir-Planck, D., Freese, S., Salm, H., Haile, S., etal. (2006) Roles of a Trypanosoma brucei 5′->3′ exoribonuclease homologue in mRNA degradation. RNA 12: 2171-2186.
51. Manful, T., Fadda, A., and Clayton, C. (2011) The role of the 5′-3′ exoribonuclease XRNA in transcriptome-wide mRNA degradation. RNA 17: 2039-2047.
52. Mao, Y., Shateri Najafabadi, H., and Salavati, R. (2009) Genome-wide computational identification of functional RNA elements in Trypanosoma brucei. BMC Genomics 10: 355.
53. Mayho, M., Fenn, K., Craddy, P., Crosthwaite, S., and Matthews, K. (2006) Post-transcriptional control of nuclear-encoded cytochrome oxidase subunits in Trypanosoma brucei: evidence for genome-wide conservation of life-cycle stage-specific regulatory elements. Nucleic Acids Res 34: 5312-5324.
54. Michaeli, S. (2011) Trans-splicing in trypanosomes: machinery and its impact on the parasite transcriptome. Future Microbiol 6: 459-474.
55. Mnaimneh, S., Davierwala, A.P., Haynes, J., Moffat, J., Peng, W.T., Zhang, W., etal. (2004) Exploration of essential gene functions via titratable promoter alleles. Cell 118: 31-44.
56. Munchel, S., Shultzaberger, R., Takizawa, N., and Weis, K. (2011) Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol Biol Cell 22: 2787-2795.
57. Najafabadi, H.S., Lu, Z., MacPherson, C., Mehta, V., Adoue, V., Pastinen, T., and Salavati, R. (2013) Global identification of conserved post-transcriptional regulatory programs in trypanosomatids. Nucleic Acids Res 41: 8591-8600.
58. Nilsson, D., Gunasekera, K., Mani, J., Osteras, M., Farinelli, L., Baerlocher, L., etal. (2010) Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 6: e1001037.
59. Ouna, B., Nyambega, B., Manful, T., Helbig, C., Males, M., Fadda, A., and Clayton, C. (2012) Depletion of trypanosome CTR9 leads to gene expression defects. PLoS ONE 7: e34256.
60. Overath, P., and Engstler, M. (2004) Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol Microbiol 53: 735-744.
61. Palenchar, J.B., and Bellofatto, V. (2006) Gene transcription in trypanosomes. Mol Biochem Parasitol 146: 135-141.
62. Queiroz, R., Benz, C., Fellenberg, K., Hoheisel, J., and Clayton, C. (2009) Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics 10: 495.
63. Rabani, M., Levin, J., Fan, L., Adiconis, X., Raychowdhury, R., Garber, M., etal. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 29: 436-442.
64. Ramamoorthy, R., Swihart, K.G., McCoy, J.J., Wilson, M.E., and Donelson, J.E. (1995) Intergenic regions between tandem gp63 genes influence the differential expression of gp63 RNAs in Leishmania chagasi. J Biol Chem 270: 12133-12139.
65. Reese, J.C. (2013) The control of elongation by the yeast Ccr4-not complex. Biochim Biophys Acta 1829: 127-133.
66. Rettig, J., Wang, Y., Schneider, A., and Ochsenreiter, T. (2012) Dual targeting of isoleucyl-tRNA synthetase in Trypanosoma brucei is mediated through alternative trans-splicing. Nucleic Acids Res 40: 1299-1306.
67. Schmid, M., and Jensen, T.H. (2010) Nuclear quality control of RNA polymerase II transcripts. Wiley Interdiscip Rev RNA 1: 474-485.
68. Schmid, M., and Jensen, T.H. (2013) Transcription-associated quality control of mRNP. Biochim Biophys Acta 1829: 158-168.
69. Schneider, C., Kudla, G., Wlotzka, W., Tuck, A., and Tollervey, D. (2012) Transcriptome-wide analysis of exosome targets. Mol Cell 48: 422-433.
70. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., etal. (2011) Global quantification of mammalian gene expression control. Nature 473: 337-342.
71. Schwede, A., Ellis, L., Luther, J., Carrington, M., Stoecklin, G., and Clayton, C. (2008) A role for Caf1 in mRNA deadenylation and decay in trypanosomes and human cells. Nucleic Acids Res 36: 3374-3388.
72. Schwede, A., Manful, T., Jha, B., Helbig, C., Bercovich, N., Stewart, M., and Clayton, C. (2009) The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res 37: 5511-5528.
73. Shalem, O., Dahan, O., Levo, M., Martinez, M.F.R., Furman, I., Sega, E., and Pilpel, Y. (2008) Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Mol Syst Biol 4: 223.
74. Siegel, T., Tan, K., and Cross, G. (2005) Systematic study of sequence motifs for RNA trans splicing in Trypanosoma brucei. Mol Cell Biol 25: 9586-9594.
75. Siegel, T., Hekstra, D., Wang, X., Dewell, S., and 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.
76. Siegel, T., Gunasekera, K., Cross, G., and Ochsenreiter, T. (2011) Gene expression in Trypanosoma brucei: lessons from high-throughput RNA sequencing. Trends Parasitol 27: 434-441.
77. Singh, A., Minia, I., Droll, D., Fadda, A., Clayton, C., and Erben, E. (2014) Trypanosome MKT1 and the RNA-binding protein ZC3H11: interactions and potential roles in post-transcriptional regulatory networks. Nucleic Acids Res 42: 4652-4668.
78. Stern, M., Gupta, S., Salmon-Divon, M., Haham, T., Barda, O., Levi, S., etal. (2009) Multiple roles for polypyrimidine tract binding (PTB) proteins in trypanosome RNA metabolism. RNA 15: 648-665.
79. Sun, M., Schwalb, B., Schulz, D., Pirkl, N., Etzold, S., Larivière, L., etal. (2012) Comparative dynamic transcriptome analysis (cDTA) reveals mutual feedback between mRNA synthesis and degradation. Genome Res 22: 1350-1359.
80. Trcek, T., Larson, D.R., Moldon, A., Query, C.C., and Singer, R.H. (2011) Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell 147: 1484-1497.
81. Ullu, E., Matthews, K.R., and Tschudi, C. (1993) Temporal order of RNA-processing reactions in trypanosomes: rapid trans splicing precedes polyadenylation of newly synthesized tubulin transcripts. Mol Cell Biol 13: 720-725.
82. Urbaniak, M.D., Martin, D., and Ferguson, M.A. (2013) Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res 12: 2233-2244.
83. Vasquez, J.J., Hon, C.C., Vanselow, J.T., Schlosser, A., and Siegel, T.N. (2014) Comparative ribosome profiling reveals extensive translational complexity in different Trypanosoma brucei life cycle stages. Nucleic Acids Res 42: 3623-3637.
84. Webb, H., Burns, R., Ellis, L., Kimblin, N., and 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.
85. Zhang, X., Cui, J., Nilsson, D., Gunasekera, K., Chanfon, A., Song, X., etal. (2010) The Trypanosoma brucei MitoCarta and its regulation and splicing pattern during development. Nucleic Acids Res 38: 7378-7387.