Artículo

Quijada, L.; Guerra-Giraldez, C.; Drozdz, M.; Hartmann, C.; Irmer, H.; Ben-Dov, C.; Cristodero, M.; Ding, M.; Clayton, C. "Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements" (2002) Nucleic Acids Research. 30(20):4414-4424
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Abstract:

The salivarian trypanosome Trypanosoma brucei infects mammals and is transmitted by tsetse flies. The mammalian 'bloodstream form' trypanosome has a variant surface glycoprotein coat and relies on glycolysis while the procyclic form from tsetse flies has EP protein on the surface and has a more developed mitochondrion. We show here that the mRNA for the procyclic-specific cytosolic phosphoglycerate kinase PGKB, like that for EP proteins, contains a regulatory AU-rich element (ARE) that destabilises the mRNA in bloodstream forms. The human HuR protein binds to, and stabilises, mammalian mRNAs containing AREs. Expression of HuR in bloodstream-form trypanosomes resulted in growth arrest and in stabilisation of the EP, PGKB and pyruvate, phosphate dikinase mRNAs, while three bloodstream-specific mRNAs were reduced in abundance. The synthesis and abundance of unregulated mRNAs and proteins were unaffected. Our results suggest that regulation of mRNA stability by AREs arose early in eukaryotic evolution.

Registro:

Documento: Artículo
Título:Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements
Autor:Quijada, L.; Guerra-Giraldez, C.; Drozdz, M.; Hartmann, C.; Irmer, H.; Ben-Dov, C.; Cristodero, M.; Ding, M.; Clayton, C.
Filiación:ZMBH, Im Neuenheimer Feld 282, D-69120 Heidelberg, Germany
Centro de Biología Molecular 'SO', Lab. CX-203, Universidad Autónoma de Madrid, Cantoblanco, E-28049 Madrid, Spain
Friedrich Miescher Institute for Biomedical Research, PO Box 2543, 4002 Basel, Switzerland
Yale University School of Medicine, LLCI 8o1, 333 Cedar Street, New Haven, CT 06520-8022, United States
INGEBI, Vuelta de Obligado 2490, (1428) Buenos Aires, Argentina
Palabras clave:adenine; messenger RNA; phosphoglycerate kinase; protozoal protein; pyruvic acid; RNA binding protein; uracil; variant surface glycoprotein; article; controlled study; disease transmission; eukaryote; evolution; glycolysis; growth inhibition; mitochondrion; nonhuman; priority journal; protein expression; protein RNA binding; protein stability; RNA stability; RNA structure; RNA synthesis; Trypanosoma; Trypanosoma brucei; tsetse fly; 3' Untranslated Regions; Adenine; Animals; Antigens, Surface; Base Sequence; Gene Expression Regulation, Developmental; Humans; Molecular Sequence Data; Phosphoglycerate Kinase; Protozoan Proteins; Regulatory Sequences, Nucleic Acid; RNA Stability; RNA, Messenger; RNA, Protozoan; RNA-Binding Proteins; Trypanosoma brucei brucei; Uracil; Eukaryota; Glossina (proper); Mammalia; Protozoa; Trypanosoma; Trypanosoma brucei
Año:2002
Volumen:30
Número:20
Página de inicio:4414
Página de fin:4424
Título revista:Nucleic Acids Research
Título revista abreviado:Nucleic Acids Res.
ISSN:03051048
CODEN:NARHA
CAS:3' Untranslated Regions; Adenine, 73-24-5; Antigens, Surface; ELAV-like protein 1; Phosphoglycerate Kinase, EC 2.7.2.3; Protozoan Proteins; RNA, Messenger; RNA, Protozoan; RNA-Binding Proteins; Uracil, 66-22-8
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03051048_v30_n20_p4414_Quijada

Referencias:

  • Cross, G.A.M., Antigenic variation in trypanosomes: Secrets surface slowly (1997) Bioessays, 18, pp. 283-291
  • Matthews, K.R., Developments in the differentiation of Trypanosoma brucei (1999) Parasitol. Today, 15, pp. 76-80
  • Tyler, K.M., Matthews, K.R., Gull, K., The bloodstream differentiation-division of Trypanosoma brucei studied using mitochondrial markers (1997) Proc. R. Soc. London, 264, pp. 1481-1490
  • Tasker, M., Wilson, J., Sarkar, M., Hendriks, E., Matthews, K., A novel selection regime for differentiation defects demonstrates an essential role for the stumpy form in the life cycle of African trypanosomes (2000) Mol. Biol. Cell, 11, pp. 1905-1917
  • Roditi, I., Furger, A., Ruepp, S., Schurch, N., Butikofer, P., Unravelling the procyclin coat of Trypanosoma brucei (1998) Mol. Biochem. Parasitol, 91, pp. 117-130
  • Roditi, I., Clayton, C.E., An unambiguous nomenclature for the major surface glycoprotein genes of the procyclic form of Trypanosoma brucei (1999) Mal. Biochem. Parasitol, 103, pp. 99-100
  • Myler, P.J., Audleman, L., deVos, T., Hixson, G., Kiser, P., Lemley, C., Magness, C., Stuart, K., Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes (1999) Proc. Natl Acad. Sci. USA, 96, pp. 2902-2906
  • Clayton, C.E., Developmental regulation without transcriptional control? (2002) EMBO J, 21, pp. 1881-1888. , From fly to man and back again
  • Ullu, E., Matthews, K.R., Tschudi, C., Temporal order of RNA-processing reactions in trypanosomes: Rapid trans splicing precedes polyadenylation of newly synthesized tubulin transcripts (1993) Mol. Cell. Biol, 13, pp. 720-725
  • Matthews, K.R., Tschudi, C., Ullu, E., A common pyrimidine-rich motif governs trans-splicing and polyadenylation of tubulin polycistronic pre-mRNA in trypanosomes (1994) Genes Dev, 8, pp. 491-501
  • Blattner, J., Helfert, S., Michels, P., Clayton, C.E., Compartmentation of phosphoglycerate kinase in Trypanosoma brucei plays a critical role in parasite energy metabolism (1998) Proc. Natl Acad. Sci. USA, 95, pp. 11596-11600
  • Blattner, J., Clayton, C.E., The 3′-untranslated regions from the Trypanosoma brucei phosphoglycerate kinase genes mediate developmental regulation (1995) Gene, 162, pp. 153-156
  • Kapotas, N., Bellofatto, V., Differential response to RNA trans-splicing signals within the phosphoglycerate kinase gene cluster in Trypanosoma brucei (1993) Nucleic Acids Res, 21, pp. 4067-4072
  • Laufer, G., Günzl, A., In-vitro competition analysis of procyclin gene and variant surface glycoprotein gene expression site transcription in Trypanosoma brucei (2001) Mol. Biochem. Parasitol, 113, pp. 55-65
  • Horn, D., Cross, G.A.M., Position-dependent and promoter-specific regulation of gene expression in Trypanosoma brucei (1997) EMBO J, 16, pp. 7422-7431
  • Biebinger, S., Rettenmaier, S., Flaspohler, J., Hartmann, C., Peña-Diaz, J., Wirtz, L.E., Hotz, H.R., Clayton, C.E., The PARP promoter of Trypanosoma brucei is developmentally regulated in a chromosomal context (1996) Nucleic Acids Res, 24, pp. 1202-1211
  • Hotz, H.-R., Hartmann, C., Huober, K., Hug, M., Clayton, C.E., 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 (1997) Nucleic Acids Res, 25, pp. 3017-3025
  • Irmer, H., Clayton, C.E., Degradation of the EP1 mRNA in Trypanosoma brucei is initiated by destruction of the 3′-untranslated region (2001) Nucleic Acids Res, 29, pp. 4707-4715
  • Drozdz, M., Clayton, C.E., Structure of a regulatory 3′-untranslated region from Trypanosoma brucei (1999) RNA, 5, pp. 1632-1644
  • Schürch, N., Furger, A., Kurath, U., Roditi, I., Contribution of the procyclin 3′ untranslated region and coding region to the regulation of expression in bloodstream forms of Trypanosoma brucei (1997) Mol. Biochem. Parasitol, 89, pp. 109-121
  • Di Noia, J.M., D'Orso, I., Sánchez, D.O., Frasch, A.C.C., 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 (2000) J. Biol. Chem, 275, pp. 10218-10227
  • Chen, C.Y., Shyu, A.B., AU-rich elements: Characterization and importance in mRNA degradation (1995) Trends Biochem. Sci, 20, pp. 465-470
  • Mitchell, P., Tollervey, D., mRNA stability in eucaryotes (2000) Curr. Opin. Genet. Dev, 10, pp. 193-198
  • Chen, C.Y., Gherzi, R., Ong, S.E., Chan, E.L., Raijmakers, R., Pruijn, G.J., Stoecklin, G., Karin, M., AU binding proteins recruit the exosome to degrade ARE-containing mRNAs (2001) Cell, 107, pp. 451-464
  • Mukherjee, D., Gao, M., O'Connor, J.P., Raijmakers, R., Pruijn, G., Lutz, C.S., Wilusz, J., The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements (2002) EMBO J, 21, pp. 165-174
  • Zhao, Z., Chang, F.-C., Furneaux, H.M., The identification of an endonuclease that cleaves within an HuR binding site in mRNA (2000) Nucleic Acids Res, 28, pp. 2695-2701
  • Fan, X.C., Steitz, J.A., Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs (1998) EMBO J, 17, pp. 3448-3460
  • Peng, S.S., Chen, C.Y., Xu, N., Shyu, A.B., RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein (1998) EMBO J, 17, pp. 3461-3479
  • Myer, V.E., Fan, X., Steitz, J.A., Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay (1997) EMBO J, 16, pp. 2130-2139
  • Ma, W.J., Cheng, S., Campbell, C., Wright, A., Furneaux, H., Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein (1996) J. Biol. Chem, 271, pp. 8144-8151
  • Antson, A.A., Single stranded RNA binding proteins (2000) Curr. Opin. Genet. Dev, 10, pp. 87-94
  • Wang, X., Tanaka Hall, T.M., Structural basis for the recognition of AU-rich element RNA by the HuD protein (2001) Nature Struct. Biol, 8, pp. 141-145
  • Peng, S.S., Chen, C.Y., Shyu, A.B., Functional characterization of a non-AUUUA AU-rich element from the c-jun proto-oncogene mRNA: Evidence for a novel class of AU-rich elements (1996) Mol. Cell. Biol, 16, pp. 1490-1499
  • Ford, L.P., Watson, J., Keene, J.D., Wilusz, J., ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system (1999) Genes Dev, 13, pp. 188-201
  • Vasudevan, S., Peltz, S.W., Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae (2001) Mol. Cell, 7, pp. 1191-1200
  • van Deursen, F.J., Shahi, S.H., Turner, C.M.R., Hartmann, C., Guerra-Giraldez, C., Matthews, K.R., Clayton, C.E., Characterisation of the growth and differentiation in vivo and in vitro of bloodstream-form Trypanosoma brucei strain TREU 927 (2001) Mol. Biochem. Parasitol, 112, pp. 163-172
  • Biebinger, S., Wirtz, L.E., Clayton, C.E., Vectors for inducible over-expression of potentially toxic gene products in bloodstream and procyclic Trypanosoma brucei (1997) Mol. Biochem. Parasitol, 85, pp. 99-112
  • Wirtz, L.E., Hartmann, C., Clayton, C.E., Gene expression mediated by bacteriophage T3 and T7 RNA polymerases in transgenic trypanosomes (1994) Nucleic Acids Res, 22, pp. 3887-3894
  • Hartmann, C., Hotz, H.-R., McAndrew, M., Clayton, C., Effect of multiple downstream splice sites on polyadenylation in Trypanosoma brucei (1998) Mol. Biochem. Parasitol, 93, pp. 149-152
  • Chung, S., Jiang, L., Cheng, S., Furneaux, H., Purification and properties of HuD, a neuronal RNA-binding protein (1996) J. Biol. Chem, 271, pp. 11518-11524
  • Michaeli, S., Podell, D., Agabian, N., Ullu, E., The 7SL RNA homologue of Trypanosoma brucei is closely related to mammalian 7SL RNA (1992) Mol. Biochem. Parasitol, 51, pp. 55-64
  • Clayton, C.E., Genetic manipulation of Kinetoplastida (1999) Parasitol. Today, 15, pp. 372-378
  • Sherwin, T., Gull, K., The cell division cycle of Trypanosoma brucei brucei: Timing of event markers and cytoskeletal modulations (1989) Phil. Trans. R. Soc. London, 323, pp. 573-588
  • Mutomba, M.C., Wang, C.C., Effects of aphidodocolin and hydroxyurea on the cell cycle and differentiation of Trypanosoma brucei bloodstream forms (1996) Mol. Biochem. Parasitol, 80, pp. 89-102
  • Dorn, P.L., Aman, R.A., Boothroyd, J.C., Inhibition of protein synthesis results in super-induction of procyclin (PARP) RNA levels (1991) Mol. Biochem. Parasitol, 44, pp. 133-140
  • Graham, S.V., Barry, J.D., Polysomal, procyclin mRNAs accumulate in bloodstream forms of monomorphic and pleomorphic trypanosomes treated with protein synthesis inhibitors (1996) Mol. Biochem. Parasitol, 80, pp. 179-192
  • Vanhamme, L., Postiaux, S., Poelvoorde, P., Pays, E., Differential regulation of ESAG transcripts in Trypanosoma brucei (1999) Mol. Biochem. Parasitol, 102, pp. 35-42
  • Diehl, S., Diehl, F., El-Sayed, N.M., Clayton, C.E., Hoheisel, J.D., Analysis of stage-specific gene expression in the bloodstream and the procyclic form of Trypanosoma brucei using a genomic DNA microarray (2002) Mol. Biochem. Parisitol, , in press
  • Bringaud, F., Baltz, D., Baltz, T., Functional and molecular characterization of a glycosomal PPi-dependent enzyme in trypanosomatids: Pyruvate phosphate dikinase (1998) J. Biol. Chem, 95, pp. 7963-7968
  • Boucher, N., Wu, Y., Dumas, C., Dube, M., Sereno, D., Breton, M., Papadopoulou, B., A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3′ UTR element (2002) J. Biol. Chem, 277, pp. 19511-19520
  • Chen, C.Y., Xu, N., Shyu, A.B., mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: Different deadenylation kinetics and uncoupling from translation (1995) Mol. Cell. Biol, 15, pp. 5777-5788
  • DeMaria, C.T., Brewer, G., AUF1 binding affinity to A+U-rich elements correlates with rapid mRNA degradation (1996) J. Biol. Chem, 271, pp. 12179-12184
  • D'Orso, I., Frasch, A.C.C., TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes (2001) J. Biol. Chem, 276, pp. 34801-34809
  • Hoek, M., Zanders, T., Cross, G.A.M., Trypanosoma brucei expression-site-associated-gene 8 protein interacts with a Pumilio family protein (2002) Mol. Biochem. Parasitol, 120, pp. 269-284
  • Hendriks, E.F., Robinson, D.R., Hinkins, M., Matthews, K.R., A novel CCCH protein which modulates differentiation of Trypanosoma brucei to its procyclic form (2001) EMBO J, 20, pp. 6700-6711

Citas:

---------- APA ----------
Quijada, L., Guerra-Giraldez, C., Drozdz, M., Hartmann, C., Irmer, H., Ben-Dov, C., Cristodero, M.,..., Clayton, C. (2002) . Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements. Nucleic Acids Research, 30(20), 4414-4424.
Recuperado de https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03051048_v30_n20_p4414_Quijada [ ]
---------- CHICAGO ----------
Quijada, L., Guerra-Giraldez, C., Drozdz, M., Hartmann, C., Irmer, H., Ben-Dov, C., et al. "Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements" . Nucleic Acids Research 30, no. 20 (2002) : 4414-4424.
Recuperado de https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03051048_v30_n20_p4414_Quijada [ ]
---------- MLA ----------
Quijada, L., Guerra-Giraldez, C., Drozdz, M., Hartmann, C., Irmer, H., Ben-Dov, C., et al. "Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements" . Nucleic Acids Research, vol. 30, no. 20, 2002, pp. 4414-4424.
Recuperado de https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03051048_v30_n20_p4414_Quijada [ ]
---------- VANCOUVER ----------
Quijada, L., Guerra-Giraldez, C., Drozdz, M., Hartmann, C., Irmer, H., Ben-Dov, C., et al. Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements. Nucleic Acids Res. 2002;30(20):4414-4424.
Available from: https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03051048_v30_n20_p4414_Quijada [ ]