Small trypanosome RNA-binding proteins TbUBP1 and TbUBP2 influence expression of F-box protein mRNAs in bloodstream trypanosomes

Eukaryotic Cell

Volumn 6, Issue 11, 2007, Pages 1964-1978

  Hartmann, Claudia ^a   Benz, Corinna ^a   Brems, Stefanie ^b   Ellis, Louise ^c   Luu, Van Duc ^a   Stewart, Mhairi ^a,e   D'Orso, Iván ^d   Busold, Christian ^b   Fellenberg, Kurt ^b   Frasch, Alberto C C ^d   Carrington, Mark ^c   Hoheisel, Jörg ^b   Clayton, Christine E ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c Department of Biochemistry ^*  (United Kingdom)

^d INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F BOX PROTEIN; MESSENGER RNA; PROTOZOAL PROTEIN; PROTOZOAL RNA; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ANIMAL; ARTICLE; CELL FRACTIONATION; CELL PROLIFERATION; CYTOLOGY; DNA RESPONSIVE ELEMENT; GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT; RNA STABILITY; TRYPANOSOMA BRUCEI;

3' UNTRANSLATED REGIONS; ANIMALS; CELL PROLIFERATION; F-BOX PROTEINS; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; LIFE CYCLE STAGES; PROTEIN BINDING; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; RESPONSE ELEMENTS; RNA STABILITY; RNA, MESSENGER; RNA, PROTOZOAN; RNA-BINDING PROTEINS; SUBCELLULAR FRACTIONS; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 36849018485     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00279-07     Document Type: Article

References (57)

1. Alibu, V. P., L. Storm, S. Haile, C. Clayton, and D. Horn. 2004. A doubly inducible system for RNA interference and rapid RNAi plasmid construction in Trypanosoma brucei. Mol. Biochem. Parasitol. 139:75-82.
2. Barreau, C., L. Paillard, and H. Osborne. 2006. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33:7138-7150.
3. Benz, C., and C. Clayton. The cyclin F box protein CFB2 is required for cytokinesis of bloodstream-form Trypanosoma brucei. Mol. Biochem. Parasitol., in press.
4. Benz, C., D. Nilsson, B. Andersson, C. Clayton, and D. L. Guilbride. 2005. Messenger RNA processing sites in Trypanosoma brucei. Mol. Biochem. Parasitol. 143:125-134.
5. Berriman, M. E. A. 2005. The genome of the African trypanosome, Trypanosoma brucei. Science 309:416-422.
6. Biebinger, S., L. E. Wirtz, and C. E. Clayton. 1997. Vectors for inducible overexpression of potentially toxic gene products in bloodstream and procyclic Trypanosoma brucei. Mol. Biochem. Parasitol. 85:99-112.
7. Brems, S., D. L. Guilbride, D. Gundlesdodjir-Planck, C. Busold, V. D. Luu, M. Schanne, J. Hoheisel, and C. Clayton. 2005. The transcriptomes of Trypanosoma brucei Lister 427 and TREU927 bloodstream and procyclic trypomastigotes. Mol. Biochem. Parasitol. 139:163-172.
8. Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell Mol. Life Sci. 58:266-277.
9. Cassola, A., J. De Gaudenzi, and A. Frasch. 2007. Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol. Microbiol. 65:655-670.
10. Clayton, C. E. 2002. Developmental regulation without transcriptional control? From fly to man and back again. EMBO J. 21:1881-1888.
11. Colasante, C., V. P. Alibu, S. Kirchberger, J. Tjaden, C. Clayton, and F. Voncken. 2006. Characterisation and dcvelopmentally regulated localization of the mitochondrial carrier protein homologue MCP6 from Trypanosoma brucei. Eukaryot. Cell 5:1194-1205.
12. Colasante, C., A. Robles, C.-H. Li, A. Schwede, C. Benz, F. Voncken, D. L. Guilbride, and C. Clayton. 2007. Regulated expression of glycosomal phosphoglycerate kinase in Trypanosoma brucei. Mol. Biochem. Parasitol. 151:193-204.
13. De Gaudenzi, J. G., I. D'Orso, and A. C. C. Frasch. 2003. RNA recognition motif-type RNA-binding proteins in Trypanosoma cruzi form a family involved in the interaction with specific transcripts in vivo. J. Biol. Chem. 21:18884-18894.
14. De Gaudenzi, J. G., A. C. C. Frasch, and C. Clayton. 2006. RNA-binding domain proteins in Kinetoplastids: a comparative analysis. Eukaryot. Cell 4:2106-2114.
15. Diehl, S., F. Diehl, N. M. El-Sayed, C. E. Clayton, and J. D. Hoheisel. 2002. Analysis of stage-specific gene expression in the bloodstream and the procyclic form of Trypanosoma brucei using a genomic DNA microarray. Mol. Biochem. Parasitol. 123:115-123.
16. Di Noia, J. M., I. D'Orso, D. O. Sanchez, and A. C. C. Frasch. 2000. AU-rich elements in the 3′-untranslated region of a new mucin-type gene family of Trypanosoma cruzi confers mRNA instability and modulates translation efficiency. J. Biol. Chem. 275:10218-10227.
17. Djikeng, A., C. Agufa, J. E. Donelson, and P. A. Majiwa. 1998. Generation of expressed sequence tags as physical landmarks in the genome of Trypanosoma brucei. Gene 221:93-106.
18. D'Orso, I., and A. C. C. Frasch. 2001. TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes. J. Biol. Chem. 276:34801-34809.
19. D'Orso, I., and A. C. C. Frasch. 2002. TcUBP-1, an mRNA destabilizing factor from trypanosomes, homodimerizes and interacts with novel AU-rich element- and poly(A)-binding proteins forming a ribonucleoprotein complex. J. Biol. Chem. 277:50520-50528.
20. Drozdz, M., L. Quijada, and C. E. Clayton. 2002. RNA interference in trypanosomes transfected with sense and antisense plasmids. Mol. Biochem. Parasitol. 121:149-152.
21. Durand-Dubief, M., L. Kohl, and P. Bastin. 2003. Efficiency and specificity of RNA interference generated by intra- and intermolecular double-stranded RNA in Trypanosoma brucei. Mol. Biochem. Parasitol. 129:11-21.
22. Duttagupta, R., B. Tian, C. Wilusz, D. Khounh, P. Soteropoulos, M. Ouyang, J. Dougherty, and S. Peltz. 2005. Global analysis of Pub1p targets reveals a coordinate control of gene expression through modulation of binding and stability. Mol. Cell. Biol. 25:5499-5513.
23. El-Sayed, N. M., E. Ghedin, J. Song, A. MacLeod, F. Bringaud, C. Larkin, D. Wanless, J. Peterson, L. Hou, S. Taylor, A. Tweedie, N. Biteau, H. G. Khalak, X. Lin, T. Mason, L. Hannick, E. Caler, G. Blandin, D. Bartholomeu, A. J. Simpson, S. Kaul, H. Zhao, G. Pai, A. Van, S. T. Utterback, B. Haas, H. L. Koo, L. Umayam, B. Suh, C. Gerrard, V. Leech, R. Qi, S. Zhou, D. Schwartz, T. Feldblyum, S. Salzberg, A. Tait, C. M. Turner, E. Ullu, O. White, S. Melville, M. D. Adams, C. M. Fraser, and J. E. Donelson. 2003. The sequence and analysis of Trypanosoma brucei chromosome II. Nucleic Acids Res. 31:4856-4863.
24. Estévez, A., T. Kein pi, and C. E. Clayton. 2001. The exosome of Trypanosoma brucei. EMBO J. 20:3831-3839.
25. Estévez, A. M., B. Lehner, C. M. Sanderson, T. Ruppert, and C. Clayton. 2003. The roles of inter-subunit interactions in exosome stability. J. Biol. Chem. 278:34943-34951.
26. Fellenberg, K., N. C. Hauser, B. Brors, J. D. Hoheisel, and M. Vingron. 2002. Microarray data warehouse allowing for the statistical analysis of experiment annotations. Bioinformatics 18:423-433.
27. Fellenberg, K., N. C. Hauser, B. Brors, A. Neutzner, J. D. Hoheisel, and M. Vingron. 2001. Correspondence analysis applied to microarray data. Proc. Natl. Acad. Sci. USA 98:10781-10786.
28. Guerra-Giraldez, C., L. Quijada, and C. E. Clayton. 2002. Compartmentation of enzymes in a microbody, the glycosome, is essential in Trypanosoma brucei. J. Cell Sci. 115:2651.
29. Haile, S., M. Cristodero, C. Clayton, and A. Estévez. 2007. The subcellular localization of trypanosome RRP6 and its association with the exosome. Mol. Biochem. Parasitol. 151:52-58.
30. Haile, S., A. M. Estévez, and C. Clayton. 2003. A role for the exosome in the initiation of degradation of unstable mRNAs. RNA 9:1491-1501.
31. Hall, N., M. Berriman, N. J. Lennard, B. R. Harris, C. Hertz-Fowler, E. N. Bart-Delabesse, C. S. Gerrard, R. J. Atkin, A. J. Barron, S. Bowman, S. P. Bray-Allen, F. Bringaud, L. N. Clark, C. H. Corton, A. Cronin, R. Davies, J. Doggett, A. Fraser, E. Gruter, S. Hall, A. D. Harper, M. P. Kay, V. Leech, R. Mayes, C. Price, M. A. Quail, E. Rabbinowitsch, C. Reitter, K. Rutherford, J. Sasse, S. Sharp, R. Shownkeen, A. MacLeod, S. Taylor, A. Tweedie, C. M. Turner, A. Tait, K. Gull, B. Barrell, and S. E. Melville. 2003. The DNA sequence of chromosome I of an African trypanosome: gene content, chromosome organisation, recombination, and polymorphism. Nucleic Acids Res. 31:4864-4873.
32. 31a. Hartmann, C., and C. Clayton. Regulation of a transmembrane protein gene family by the small RNA binding proteins TbUBP1 and TbUBP2. Mol. Biochem. Parasitol., in press.
33. Hendriks, E. F., A. Abdul-Razak, and K. R. Matthews. 2003. TbCPSF30 depletion by RNA interference disrupts polycistronic RNA processing in Trypanosoma brucei. J. Biol. Chem. 278:26870-26878.
34. Holetz, F., A. Correa, A. Avila, C. Nakamura, M. Krieger, and S. Goldenberg. 2007. Evidence of P-body-like structures in Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 356:1062-1067.
35. Hotz, H.-R., C. Hartmann, K. Huober, M. Hug, and C. E. Clayton. 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.
36. Jäger, A., J. De Gaudenzi, A. Cassola, I. D'Orso, and A. Frasch. 2007. mRNA maturation by two-step trans-splicing/polyadenylation processing in trypanosomes. Proc. Natl. Acad. Sci. USA 104:2035-2042.
37. Jones, A., A. Faldas, A. Foucher, E. Hunt, A. Tait, J. Wastling, and C. Turner. 2006. Visualisation and analysis of proteomic data from the procyclic form of Trypanosoma brucei. Proteomics 6:259-267.
38. Liang, X., A. Haritan, S. Uliel, and S. Michaeli. 2003. Trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot. Cell 2:830-840.
39. Liang, X.-H., Q. Liu, L. Liu, C. Tschudi, and S. Michaeli. 2006. Analysis of spliceosomal complexes in Trypanosoma brucei and silencing of two splicing factors Prp31 and Prp43. Mol. Biochem. Parasitol. 145:29-39.
40. Liao, B., Y. Hu, and G. Brewer. 2007. Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat. Struct. Mol. Biol. 14:511-519.
41. Luu, V. D., S. Brems, J. Hoheisel, R. Burchmore, D. Guilbride, and C. Clayton. 2006. Functional analysis of Trypanosoma brucei PUF1. Mol. Biochem. Parasitol. 150:340-349.
42. Martinez-Calvillo, S., D. Nguyen, K. Stuart, and P. J. Myler. 2004. Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot. Cell 3:506-517.
43. Martinez-Calvillo, S., S. Yan, D. Nguyen, M. Fox, K. Stuart, and P. J. Myler. 2003. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol. Cell 11:1291-1299.
44. Mili, S., and J. A. Steitz. 2004. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10:1692-1694.
45. Myler, P. J., L. Audleman, T. deVos, G. Hixson, P. Riser, C. Lemley, C. Magness, E. Rickel, E. Sisk, S. Sunkin, S. Swartzell, T. Westlake, P. Bastien, G. Fu, A. Ivens, and K. Stuart. 1999. Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes. Proc. Natl. Acad. Sci. USA 96:2902-2906.
46. Park, S., D. G. Myszka, M. Yu, S. J. Littler, and I. A. Laird-Offringa. 2000. HuD RNA recognition motifs play distinct roles in the formation of a stable compex with AU-rich RNA. Mol. Cell. Biol. 20:4765-4772.
47. Parker, R., and U. Sheth. 2007. P bodies and the control of mRNA translation and degradation. Mol. Cell 25:635-646.
48. Quijada, L., C. Hartmann, C. Guerra-Giraldez, M. Drozdz, H. Irmer, and C. E. Clayton. 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.
49. Raineri, I., D. Wegmueller, B. Gross, U. Certa, and C. Moroni. 2004. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res. 32:1279-1288.
50. Sarkar, B., Q. Xi, C. He, and R. J. Schneider. 2003. Selective degradation of AU-rich mRNAs promoted by the p37 AUF1 protein isoform. Mol. Cell. Biol. 23:6685-6693.
51. Segal, S., T. Dunckley, and R. Parker. 2006. Sbp1p affects translational repression and dccapping in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:5120-5130.
52. Shen, S., G. K. Arhin, E. Ullu, and C. Tschudi. 2001. In vivo epitope tagging of Trypanosoma brucei genes using a one step PCR-based strategy. Mol. Biochem. Parasitol. 113:171-173.
53. Shi, H., A. Djikeng, T. Mark, E. Wirtz, C. Tschudi, and E. Ullu. 2000. Genetic interference in Trypanosoma brucei by heritable and inducible double-stranded RNA. RNA 6:1069-1076.
54. Tyers, M., and P. Jorgensen. 2000. Proteolysis and the cell cycle; with this RING I do thee destroy. Curr. Opin. Genet. Dev. 10:54-64.
55. van Deursen, F. J., S. H. Shahi, T. C. M. R., C. Hartmann, C. Guerra-Giraldez, K. R. Matthews, and C. E. Clayton. 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.
56. Volpon, L., I. D'Orso, C. R. Young, A. C. Frasch, and K. Gehring. 2005. NMR structural study of TcUBP1, a single RRM domain protein from Trypanosoma cruzi: contribution of a beta hairpin to RNA binding. Biochemistry 44:3708-3717.
57. Wang, X., and T. M. Tanaka Hall. 2001. Structural basis for the recognition of AU-rich element RNA by the HuD protein. Nat. Struct. Biol. 8:141-145.