Elements in the 3′ Untranslated Region of Procyclin mRNA Regulate Expression in Insect Forms of Trypanosoma brucei by Modulating RNA Stability and Translation

REFERENCES

• Bayne, R. A. L., E. A. Kilbride, F. A. Lainson, L. Tetley, and J. D. Barry. 1993. A major surface antigen of procyclic stage Trypanosoma congolense. Mol. Biochem. Parasitol. 61:295–310.
   PubMedGoogle Scholar
• Beecroft, R. P., I. Roditi, and T. W. Pearson. 1993. Identification and characterization of a major surface glycoprotein from procyclic stage Trypanosoma congolense. Mol. Biochem. Parasitol. 61:285–294.
   PubMedGoogle Scholar
• Belasco, J., and G. Brawerman. 1993. Control of messenger RNA stability. Academic Press, New York, N.Y.
   Google Scholar
• Berberof, M., A. Pays, and E. Pays. 1991. Asimilar gene is shared byboth the variant surface glycoprotein and procyclin gene transcription units of Trypanosoma brucei. Mol. Cell. Biol. 11:1473–1479.
   PubMedGoogle Scholar
• Berberof, M., L. Vanhamme, P. Tebabi, A. Pays, D. Jefferies, S. Welburn, and E. Pays. 1995. The 3′-terminal region of the mRNAs for VSG and procyclin can confer stage-specificity to gene expression in Trypanosoma brucei. EMBO J. 14:2925–2934.
   PubMed Web of Science ®Google Scholar
• Berberof, M., A. Pays, S. Lips, P. Tebabi, and E. Pays. 1996. Characterization of a transcription terminator of the procyclin PARP A unit of Trypanosoma brucei. Mol. Cell. Biol. 16:914–924.
   PubMedGoogle Scholar
• Bindler, R., J. A. Horowitz, J. P. Basilion, D. M. Koeller, R. D. Klausner, and J. B. Harford. 1994. Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J. 13:1969–1980.
   PubMedGoogle Scholar
• Brun, R., and M. Schoenenberger. 1979. Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289–292.
   PubMed Web of Science ®Google Scholar
• Clayton, C. E., and M. R. Mowatt. 1989. The procyclic acidic repetitive proteins of Trypanosoma brucei: purification and post-translational modification. J. Biol. Chem. 264:15088–15093.
   PubMedGoogle Scholar
• Cross, G. A. M., and J. C. Manning. 1973. Cultivation ofTrypanosoma brucei ssp. in semi-defined and defined media. Parasitology 67:315–331.
   PubMedGoogle Scholar
• Dahakunar, A., and R. P. Wharton. 1996. The nanos gradient in Drosophila is generated by translational regulation. Genes Dev. 10:2610–2620.
   PubMedGoogle Scholar
• Dalby, B., and D. M. Glover. 1993. Discrete sequence elements control posterior pole accumulation and translational repression of maternal cyclin B RNA in Drosophila. EMBO J. 12:1219–1227.
   PubMed Web of Science ®Google Scholar
• Dorn, P. L., R. A. Aman, and J. C. Boothroyd. 1991. Inhibition of protein synthesis results in a super-induction of procyclin (PARP) RNA levels. Mol. Biochem. Parasitol. 44:133–139.
   PubMedGoogle Scholar
• Dubnau, J., and G. Struhl. 1996. RNA recognition and translational regulation by a homeodomain protein. Nature 379:694–699.
   PubMed Web of Science ®Google Scholar
• Ferguson, M. A., P. Murray, H. Rutherford, and M. J. McConville. 1993. A simple purification of procyclic acidic repetitive protein and demonstration of a sialylated glycosyl-phosphatidylinositol membrane anchor. Biochem. J. 291:51–55.
   PubMedGoogle Scholar
• Field, M. C., A. K. Menon, and G. A. M. Cross. 1991. A glycosylphosphati-dylinositol protein anchor from procyclic stage Trypanosoma brucei: lipid structure and biosynthesis. EMBO J. 10:2731–2739.
   PubMedGoogle Scholar
• Gavis, E. R., and R. Lehmann. 1994. Translational regulation of nanos by RNA localization. Nature 369:315–318.
   PubMed Web of Science ®Google Scholar
• Gavis, E. R., L. Lunsford, S. E. Bergsten, and R. Lehmann. 1996. A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122:2791–2800.
   PubMedGoogle Scholar
• Graham, S. V., and J. D. Barry. 1996. Polysomal, procyclin mRNAs accumulate in bloodstream forms of monomorphic and pleomorphic trypano-somes treated with protein synthesis inhibitors. Mol. Biochem. Parasitol. 80:179–191.
   PubMedGoogle Scholar
• Hehl, A., E. Vassella, R. Braun, and I. Roditi. 1994. A conserved stem-loop structure in the 3′ untranslated region of procyclin mRNAs regulates expression in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA 91:370–374.
   PubMed Web of Science ®Google Scholar
• Hehl, A., T. W. Pearson, J. D. Barry, R. Braun, and I. Roditi. 1995. Expression of GARP, a major surface glycoprotein of Trypanosoma congolense, on the surface of Trypanosoma brucei: characterisation and use as a surface marker. Mol. Biochem. Parasitol. 70:45–58.
   PubMedGoogle Scholar
• Hotz, H.-R., P. Lorenz, R. Fischer, S. Krieger, and C. Clayton. 1995. Role of 3′ -untranslated regions in the regulation of hexose transporter mRNAs in Trypanosoma brucei. Mol. Biochem. Parasitol. 75:1–14.
   PubMedGoogle Scholar
• Huang, J., and L. H. T. Van der Ploeg. 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.
   PubMedGoogle Scholar
• Hug, M., H. R. Hotz, C. Hartmann, and C. Clayton. 1994. Hierarchies of RNA processing signals in a trypanosome surface antigen mRNA precursor. Mol. Cell. Biol. 14:7428–7435.
   PubMedGoogle Scholar
• Jefferies, D., P. Tebabi, and E. Pays. 1991. Transient activity assays of the Trypanosoma brucei VSG gene promoter: control of gene expression at the posttranscriptional level. Mol. Cell. Biol. 11:338–343.
   PubMedGoogle Scholar
• Kim-Ha, J., K. Kerr, and P. M. Macdonald. 1995. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 81:403–412.
   PubMed Web of Science ®Google Scholar
• Koenig, E., H. Delius, M. Carrington, R. O. Williams, and I. Roditi. 1989. Duplication and transcription of procyclin genes in Trypanosoma brucei. Nucleic Acids Res. 17:8727–8739.
   PubMedGoogle Scholar
• Koenig-Martin, E., M. Yamage, and I. Roditi. 1992. A procyclin-associated gene in Trypanosoma brucei encodes a polypeptide related to ESAG 6 and 7. Mol. Biochem. Parasitol. 55:135–146.
   PubMedGoogle Scholar
• Kruys, V., and G. Huez. 1994. Translational control ofcytokine expression by 3′ UA-rich sequences. Biochimie 76:862–866.
   PubMedGoogle Scholar
• Lee, K., M. A. Farjardo, and R. E. Braun. 1996. A testis cytoplasmic RNA-binding protein has the properties of a translational repressor. Mol. Cell. Biol. 16:3023–3024.
   PubMedGoogle Scholar
• Matthews, K. R., and K. Gull. 1994. Cycles within cycles: the interplay between differentiation and cell division in Trypanosoma brucei. Parasitol. Today 10:473–476.
   PubMedGoogle Scholar
• Mowatt, M. R., and C. E. Clayton. 1987. Developmental regulationofa novel repetitive protein of Trypanosoma brucei. Mol. Cell. Biol. 7:2833–2844.
   Google Scholar
• Mowatt, M. R., and C. E. Clayton. 1988. Polymorphisms in the procyclic acidic repetitive protein (PARP) gene family of Trypanosoma brucei. Mol. Cell. Biol. 8:4055–4062.
   PubMedGoogle Scholar
• Mowatt, M. R., G. S. Wisdom, and C. E. Clayton. 1989. Variation of tandem repeats in the developmentally regulated procyclic acidic repetitive proteins of Trypanosoma brucei. Mol. Cell. Biol. 9:1332–1335.
   PubMedGoogle Scholar
• Ostareck-Lederer, A., D. H. Ostareck, N. Standart, and B. J. Thiele. 1994. Translationofthe 15-lipoxygenase mRNAis inhibited bya protein that binds to a repeated sequence in the 3′ untranslated region. EMBO J. 13:1476–1481.
   PubMed Web of Science ®Google Scholar
• Pays, E., H. Coquelet, P. Tebabi, A. Pays, D. Jefferies, M. Steinert, E. König, R. O. Williams, and I. Roditi. 1990. Trypanosoma brucei: constitutive activity of the VSG and procyclin gene promotors. EMBO J. 9:3145–3151.
   PubMedGoogle Scholar
• Pays, E., J. Hanocq-Quertier, F. Hanocq, S. van Assel, D. Nolan, and S. Rolin. 1993. Abrupt RNA changes preceding the first cell division during the differentiation of Trypanosoma brucei bloodstream forms into procyclic forms in vitro. Mol. Biochem. Parasitol. 61:107–114.
   PubMedGoogle Scholar
• Pelle, R., and N. B. Murphy. 1993. Stage-specific differential polyadenylation of miniexon derived RNA on African trypanosomes. Mol. Biochem. Parasitol. 59:277–286.
   PubMedGoogle Scholar
• Rivera-Pomar, R., D. Niessing, U. Schmidt-Ott, W. J. Gehring, and H. Jaeckle. 1996. RNA binding and translational suppression by bicoid. Nature 379:746–749.
   PubMed Web of Science ®Google Scholar
• Roditi, I. 1996. The VSG-procyclin switch. Parasitol. Today 12:47–49.
   PubMedGoogle Scholar
• Roditi, I., M. Carrington, and M. Turner. 1987. Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei. Nature 325:272–274.
   PubMedGoogle Scholar
• Roditi, I., H. Schwarz, T. W. Pearson, R. P. Beecroft, M. K. Liu, J. P. Richardson, H. H. Bühring, J. Pleiss, R. Blliow, R. O. Williams, and P. Overath. 1989. Procyclin gene expression and loss of variant surface glycoprotein during differentiation of Trypanosoma brucei. J. Cell Biol. 108:737–746.
   PubMedGoogle Scholar
• Rudenko, G., D. Bishop, K. Gottesdiener, and L. H. T. Van der Ploeg. 1989. Alpha-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei. EMBO J. 8:4259–4263.
   PubMedGoogle Scholar
• Ruepp, S., A. Furger, U. Kurath, C. Kunz Renggli, A. Hemphill, R. Brun, and I. Roditi. Different roles for the procyclins of Trypanosoma brucei established by sequential deletion of eight genes. J. Cell Biol., in press.
   Google Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Schurch, N., A. Hehl, E. Vassella, R. Braun, and I. Roditi. 1994. Accurate polyadenylation of procyclin mRNAs is determined by pyrimidine-rich elements in the intergenic regions. Mol. Cell. Biol. 14:3668–3675.
   PubMed Web of Science ®Google Scholar
• Schuürch, N. et al. Submitted for publication.
   Google Scholar
• Seebeck, T., P. A. Whittaker, M. A. Imboden, N. Hardman, and R. Braun. 1983. Tubulin genes of Trypanosoma brucei: a tightly clustered family of alternating genes. Proc. Natl. Acad. Sci. USA 80:4634–4638.
   PubMedGoogle Scholar
• ten Asbroek, A. L. M. A., M. Oullette, and P. Borst. 1990. Targeted insertion of the neomycin posphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 348:174–175.
   PubMedGoogle Scholar
• Vanhamme, L., M. Berberof, D. Le Ray, and E. Pays. 1995. Stimuli of differentiation regulate RNA elongation in the transcription units for the major stage-specific antigens of Trypanosoma brucei. Nucleic Acids Res. 23:1862–1869.
   PubMedGoogle Scholar
• Vanhamme, L., and E. Pays. 1995. Control of gene expression in trypano-somes. Microbiol. Rev. 59:223–240.
   PubMedGoogle Scholar
• Vassella, E., R. Braun, and I. Roditi. 1994. Control of polyadenylation and alternative splicing of transcripts from adjacent genes in a procyclin expression site: a dual role for polypyrimidine tracts in trypanosomes? Nucleic Acids Res. 22:1359–1364.
   PubMed Web of Science ®Google Scholar
• Vassella, E., and I. Roditi. Unpublished data.
   Google Scholar
• Wilson, T., and R. Treisman. 1988. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by AU-rich sequences. Nature 336:396–399.
   PubMed Web of Science ®Google Scholar
• Young, J. R., J. E. Donelson, P. A. O. Majiwa, S. Z. Shapiro, and R. O. Williams. 1982. Analysis of genomic rearrangements associated with two variable antigen genes of Trypanosoma brucei. Nucleic Acids Res. 10:803–819.
   PubMedGoogle Scholar
• Ziegelbauer, K., M. Quinten, H. Schwarz, T. W. Pearson, and P. Overath. 1990. Synchronous differentiation of Trypanosoma brucei from bloodstream to procyclic forms in vitro. Eur. J. Biochem. 192:373–378.
   PubMedGoogle Scholar
• Zomerdijk, J. C. B. M., M. Ouellette, A. L. M. A. ten Asbroek, R. Kieft, A. M. M. Bommer, C. E. Clayton, and P. Borst. 1990. The promoter for the variant surface glycoprotein gene expression site in Trypanosoma brucei. EMBO J. 9:2791–2801.
   PubMedGoogle Scholar
• Zuker, M., and P. Stiegler. 1981. Optimal computer folding of large RNA sequence using thermodynamics and auxiliary information. Nucleic Acids Res. 9:133–148.
   PubMed Web of Science ®Google Scholar