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Differential polyadenylation of ribosomal RNA during post-transcriptional processing in Leishmania

Published online by Cambridge University Press:  10 May 2005

S. DECUYPERE
Affiliation:
Department of Parasitology, Unit of Molecular Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp B-2000, Belgium Department of Biomedical Sciences, University of Antwerp, Antwerp B-2080, Belgium
J. VANDESOMPELE
Affiliation:
Centre for Medical Genetics, Ghent University Hospital 1K5, Ghent B-9000, Belgium
V. YARDLEY
Affiliation:
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London WC1E7HT, UK
S. DE DONCKER
Affiliation:
Department of Parasitology, Unit of Molecular Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp B-2000, Belgium
T. LAURENT
Affiliation:
Department of Parasitology, Unit of Molecular Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp B-2000, Belgium
S. RIJAL
Affiliation:
B.P. Koirala Institute of Health Sciences, Dharan, Nepal
A. LLANOS-CUENTAS
Affiliation:
Departamento de Bioquimica, Biologia Molecular y Farmacologia, Facultad de Ciencias y Filosofia and Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, Lima 100, Peru
F. CHAPPUIS
Affiliation:
Department of Community Medicine, Travel and Migration Medicine Unit, Hopitaux Universitaires de Geneve, Geneva, Switzerland
J. AREVALO
Affiliation:
Departamento de Bioquimica, Biologia Molecular y Farmacologia, Facultad de Ciencias y Filosofia and Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, Lima 100, Peru
J.-C. DUJARDIN
Affiliation:
Department of Parasitology, Unit of Molecular Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp B-2000, Belgium

Abstract

The protozoan parasite Leishmania belongs to the most ancient eukaryotic lineages and this is reflected in several distinctive biological features, such as eukaryotic polycistronic transcription and RNA trans-splicing. The disclosure of this organism's unusual characteristics leads to a better understanding of the origin and nature of fundamental biological processes in eukaryotes. Here we report another unusual phenomenon as we demonstrate that precursor ribosomal RNA can be extensively polyadenylated during post-transcriptional processing[dagger]. Furthermore, we demonstrate that the degree of precursor rRNA polyadenylation is variable in different strains and in the different life-stages of a strain.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Burchmore, R. J. and Barrett, M. P. ( 2001). Life in vacuoles--nutrient acquisition by Leishmania amastigotes. International journal for Parasitology 31, 13111320.CrossRefGoogle Scholar
Carpousis, A. J., Vanzo, N. F. and Raynal, L. C. ( 1999). mRNA degradation. A tale of poly(A) and multiprotein machines. Trends in Genetics 15, 2428.Google Scholar
Colgan, D. F. and Manley, J. L. ( 1997). Mechanism and regulation of mRNA polyadenylation. Genes and Development 11, 27552766.CrossRefGoogle Scholar
Deutscher, M. P. ( 2003). Degradation of stable RNA in bacteria. The Journal of Biological Chemistry 278, 4504145044.CrossRefGoogle Scholar
Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D. and Siebert, P. D. ( 1996). Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences, USA 93, 60256030.CrossRefGoogle Scholar
Fleischmann, J. and Liu, H. ( 2001). Polyadenylation of ribosomal RNA by Candida albicans. Gene 265, 7176.CrossRefGoogle Scholar
Fleischmann, J., Liu, H. and Wu, C. P. ( 2004). Polyadenylation of ribosomal RNA by Candida albicans also involves the small subunit. BMC. Molecular Biology 5, 1722.CrossRefGoogle Scholar
Fromont-Racine, M., Senger, B., Saveanu, C. and Fasiolo, F. ( 2003). Ribosome assembly in eukaryotes. Gene 313, 1742.CrossRefGoogle Scholar
Hernandez, R., Diaz-De Leon, F. and Castaneda, M. ( 1988). Molecular cloning and partial characterization of ribosomal RNA genes from Trypanosoma cruzi. Molecular and Biochemical Parasitology 27, 275279.CrossRefGoogle Scholar
Hernandez-Rivas, R., Martinez-Calvillo, S., Romero, M. and Hernandez, R. ( 1992). Trypanosoma cruzi 5S rRNA genes: molecular cloning, structure and chromosomal organization. FEMS Microbiology Letters 71, 6367.CrossRefGoogle Scholar
Hirose, Y. and Manley, J. L. ( 1998). RNA polymerase II is an essential mRNA polyadenylation factor. Nature, London 395, 9396.CrossRefGoogle Scholar
Jensen, B. C., Brekken, D. L., Randall, A. C., Kifer, C. T. and Parsons, M. ( 2005). Species specificity in ribosome biogenesis: a nonconserved phosphoprotein is required for formation of the large ribosomal subunit in Trypanosoma brucei. Eukaryotic Cell 4, 3035.CrossRefGoogle Scholar
Kadaba, S., Krueger, A., Trice, T., Krecic, A. M., Hinnebusch, A. G. and Anderson, J. ( 2004). Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes and Development 18, 12271240.CrossRefGoogle Scholar
Kuai, L., Fang, F., Butler, J. S. and Sherman, F. ( 2004). Polyadenylation of rRNA in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 101, 85818586.CrossRefGoogle Scholar
Lebowitz, J. H., Smith, H. Q., Rusche, L. and Beverley, S. M. ( 1993). Coupling of poly(A) site selection and trans-splicing in Leishmania. Genes and Development 7, 9961007.CrossRefGoogle Scholar
Li, Z., Pandit, S. and Deutscher, M. P. ( 1998). Polyadenylation of stable RNA precursors in vivo. Proceedings of the National Academy of Sciences, USA 95, 1215812162.CrossRefGoogle Scholar
Martinez-Calvillo, S., Sunkin, S. M., Yan, S., Fox, M., Stuart, K. and Myler, P. J. ( 2001). Genomic organization and functional characterization of the Leishmania major Friedlin ribosomal RNA gene locus. Molecular and Biochemical Parasitology 116, 147157.CrossRefGoogle Scholar
Mazareb, S., Fu, Z. Y. and Zilberstein, D. ( 1999). Developmental regulation of proline transport in Leishmania donovani. Experimental Parasitology 91, 341348.CrossRefGoogle Scholar
McConville, M. J. and Ralton, J. E. ( 1997). Developmentally regulated changes in the cell surface architecture of Leishmania parasites. Behring Institute Mitteilungen 99, 3443.Google Scholar
Motulsky, H. ( 1995). Intuitive Biostatistics, Oxford University Press, New York.
Paule, M. R. and White, R. J. ( 2000). Survey and summary: transcription by RNA polymerases I and III. Nucleic Acids Research 28, 12831298.CrossRefGoogle Scholar
Proudfoot, N. and O'Sullivan, J. ( 2002). Polyadenylation: a tail of two complexes. Current Biology 12, R855R857.CrossRefGoogle Scholar
Reeder, R. H. ( 1990). rRNA synthesis in the nucleolus. Trends in Genetics 6, 390395.CrossRefGoogle Scholar
Salles, F. J., Richards, W. G. and Strickland, S. ( 1999). Assaying the polyadenylation state of mRNAs. Methods 17, 3845.CrossRefGoogle Scholar
Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. and Peattie, D. A. ( 1989). Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243, 7577.CrossRefGoogle Scholar
Sollner-Webb, B. and Mougey, E. B. ( 1991). News from the nucleolus: rRNA gene expression. Trends in Biochemical Sciences 16, 5862.CrossRefGoogle Scholar
Spencer, D. F., Collings, J. C., Schnare, M. N. and Gray, M. W. ( 1987). Multiple Spacer sequences in the nuclear large subunit ribosomal RNA gene of Crithidia fasciculata. The EMBOJ Journal 6, 10631071.Google Scholar
Tintaya, K. W., Ying, X., Dedet, J. P., Rijal, S., De-Bolle, X. and Dujardin, J. C. ( 2004). Antigen genes for molecular epidemiology of leishmaniasis: polymorphism of cysteine proteinase B and surface metalloprotease glycoprotein 63 in the Leishmania donovani complex. Journal of Infectious Diseases 189, 10351043.CrossRefGoogle Scholar
Tobie, E. J., Von Brand, T. and Mehlman, B. ( 1950). Cultural and physiological observations on Trypanosoma rhodesiense and Trypanosoma gambiense. The Journal of Parasitology 36, 4854.CrossRefGoogle Scholar
Victoir, K., De Doncker, S., Cabrera, L., Alvarez, E., Arevalo, J., Llanos-Cuentas, A., Le Ray, D. and Dujardin, J. C. ( 2003). Direct identification of Leishmania species in biopsies from patients with American tegumentary leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 8087.CrossRefGoogle Scholar
White, T. C. and Borst, P. ( 1987). RNA end-labeling and RNA ligase activities can produce a circular rRNA in whole cell extracts from trypanosomes. Nucleic Acids Research 15, 32753290.CrossRefGoogle Scholar
White, T. C., Rudenko, G. and Borst, P. ( 1986). Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs. Nucleic Acids Research 14, 94719489.CrossRefGoogle Scholar
Zhao, J., Hyman, L. and Moore, C. ( 1999). Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiology and Molecular Biology Reviews 63, 405445.Google Scholar