Efficiency and specificity of RNA interference generated by intra- and intermolecular double stranded RNA in Trypanosoma brucei

Molecular and Biochemical Parasitology

Volumn 129, Issue 1, 2003, Pages 11-21

  Durand Dubief, Mickaël ^a   Kohl, Linda ^a   Bastin, Philippe ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Flagellum; Phenotype; RNA interference; Trypanosoma

Indexed keywords

DOUBLE STRANDED RNA; PROTOZOAL PROTEIN; RNA;

ARTICLE; CELL MOTILITY; CONTROLLED STUDY; FLAGELLUM; GENE EXPRESSION; GENETIC CODE; IMMUNOFLUORESCENCE; INVERTED REPEAT; MOLECULE; MONITORING; NONHUMAN; OBSERVATION; PHENOTYPE; PRIORITY JOURNAL; PRODUCTIVITY; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTOZOON; RNA DEGRADATION; TRYPANOSOMA BRUCEI;

EUKARYOTA; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0038173771     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-6851(03)00071-9     Document Type: Article

References (79)

1. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 391:1998;806-811.
2. van der Krol A.R., Mur L.A., Beld M., Mol J.N., Stuitje A.R. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell. 2:1990;291-299.
3. Cogoni C., Irelan J.T., Schumacher M., Schmidhauser T.J., Selker E.U., Macino G. Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J. 15:1996;3153-3163.
4. Ruiz F., Vayssie L., Klotz C., Sperling L., Madeddu L. Homology-dependent gene silencing in Paramecium. Mol. Biol. Cell. 9:1998;931-943.
5. Ngo H., Tschudi C., Gull K., Ullu E. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA. 95:1998;14687-14692.
6. Galvani A., Sperling L. RNA interference by feeding in Paramecium. Trends Genet. 18:2002;11-12.
7. Martens H., Novotny J., Oberstrass J., Steck T.L., Postlethwait P., Nellen W. RNAi in Dictyostelium: the role of RNA-directed RNA polymerases and double-stranded RNase. Mol. Biol. Cell. 13:2002;445-453.
8. Kennerdell J.R., Carthew R.W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell. 95:1998;1017-1026.
9. Waterhouse P.M., Graham M.W., Wang M.B. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc. Natl. Acad. Sci. USA. 95:1998;13959-13964.
10. Wianny F., Zernicka-Goetz M. Specific interference with gene function by double-stranded RNA in early mouse development. Nat. Cell Biol. 2:2000;70-75.
11. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 411:2001;494-498.
12. Zamore P.D., Tuschl T., Sharp P.A., Bartel D.P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21-23 nucleotide intervals. Cell. 101:2000;25-33.
13. Tuschl T. RNA interference and small interfering RNAs. Chembiochem. Eur. J. Chem. Biol. 2:2001;239-245.
14. Cogoni C. Homology-dependent gene silencing mechanisms in fungi. Annu. Rev. Microbiol. 55:2001;381-406.
15. Plasterk R.H. RNA silencing: the genome's immune system. Science. 296:2002;1263-1265.
16. Bernstein E., Caudy A.A., Hammond S.M., Hannon G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature. 409:2001;363-366.
17. Hamilton A.J., Baulcombe D.C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science. 286:1999;950-952.
18. Hutvagner G., Zamore P.D. RNAi: nature abhors a double-strand. Curr. Opin. Genet. Dev. 12:2002;225-232.
19. Elbashir S.M., Lendeckel W., Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15:2001;188-200.
20. Djikeng A., Shi H., Tschudi C., Ullu E. RNA interference in Trypanosoma brucei: cloning of small interfering RNAs provides evidence for retroposon-derived 24-26-nucleotide RNAs. RNA. 7:2001;1522-1530.
21. Caplen N.J., Parrish S., Imani F., Fire A., Morgan R.A. Specific inhibition of gene expression by small double-stranded RNAs in invertebrate and vertebrate systems. Proc. Natl. Acad. Sci. USA. 98:2001;9742-9747.
22. Cogoni C., Macino G. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature. 399:1999;166-169.
23. Smardon A., Spoerke J.M., Stacey S.C., Klein M.E., Mackin N., Maine E.M. EGO-1 is related to RNA-directed RNA polymerase and functions in germ-line development and RNA interference in C. elegans. Curr. Biol. 10:2000;169-178.
24. Mourrain P., Beclin C., Elmayan T., Feuerbach F., Godon C., Morel J.B.et al. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell. 101:2000;533-542.
25. Dalmay T., Hamilton A., Rudd S., Angell S., Baulcombe D.C. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell. 101:2000;543-553.
26. Sijen T., Fleenor J., Simmer F., Thijssen K.L., Parrish S., Timmons L.et al. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell. 107:2001;465-476.
27. Wu-Scharf D., Jeong B., Zhang C., Cerutti H. Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-Box RNA helicase. Science. 290:2000;1159-1163.
28. Dalmay T., Horsefield R., Braunstein T.H., Baulcombe D.C. SDE3 encodes an RNA helicase required for post-transcriptional gene silencing in Arabidopsis. EMBO J. 20:2001;2069-2078.
29. Tijsterman M., Ketting R.F., Okihara K.L., Sijen T., Plasterk R.H. RNA helicase MUT-14-dependent gene silencing triggered in C. elegans by short antisense RNAs. Science. 295:2002;694-697.
30. Tabara H., Sarkissian M., Kelly W.G., Fleenor J., Grishok A., Timmons L.et al. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell. 99:1999;123-132.
31. Fagard M., Boutet S., Morel J.B., Bellini C., Vaucheret H. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl. Acad. Sci. USA. 97:2000;11650-11654.
32. Catalanotto C., Azzalin G., Macino G., Cogoni C. Gene silencing in worms and fungi. Nature. 404:2000;245.
33. Hammond S.M., Caudy A.A., Hannon G.J. Post-transcriptional gene silencing by double-stranded RNA. Nat. Rev. Genet. 2:2001;110-119.
34. Kasschau K.D., Carrington J.C. A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell. 95:1998;461-470.
35. Ketting R.F., Haverkamp T.H., van Luenen H.G., Plasterk R.H. Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell. 99:1999;133-141.
36. Bass B.L. Double-stranded RNA as a template for gene silencing. Cell. 101:2000;235-238.
37. Grishok A., Pasquinelli A.E., Conte D., Li N., Parrish S., Ha I.et al. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell. 106:2001;23-234.
38. Hutvagner G., McLachlan J., Pasquinelli A.E., Balint E., Tuschl T., Zamore P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science. 293:2001;834-838.
39. Knight S.W., Bass B.L. A role for the RNase III enzyme DCR-1 in RNA interference and germ line development in Caenorhabditis elegans. Science. 293:2001;2269-2271.
40. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 15:2001;2654-2659.
41. Gonczy P., Echeverri G., Oegema K., Coulson A., Jones S.J., Copley R.R.et al. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature. 408:2000;331-336.
42. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature. 408:2000;325-330.
43. Timmons L., Fire A. Specific interference by ingested dsRNA. Nature. 395:1998;854.
44. Tavernarakis N., Wang S.L., Dorovkov M., Ryazanov A., Driscoll M. Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nat. Genet. 24:2000;180-183.
45. Bastin P., Ellis K., Kohl L., Gull K. Flagellum ontogeny studied via an inherited and regulated RNA interference system. J. Cell Sci. 113:2000;3321-3328.
46. Shi H., Djikeng A., Mark T., Wirtz E., Tschudi C., Ullu E. Genetic interference in Trypanosoma brucei by heritable and inducible double-stranded RNA. RNA. 6:2000;1069-1076.
47. Allikian MJ, Deckert-Cruz D, Rose MR, Landis GN, Tower J. Doxycycline-induced expression of sense and inverted-repeat constructs modulates phosphogluconate mutase (Pgm) gene expression in adult Drosophila melanogaster. Genome Biol 2002;3:RESEARCH0021.
48. Paddison P.J., Caudy A.A., Bernstein E., Hannon G.J., Conklin D.S. Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 16:2002;948-958.
49. Brummelkamp T.R., Bernards R., Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science. 296:2002;550-553.
50. Wang Z, Morris JC, Drew ME, Englund PT. Interference of Trypanosoma brucei gene expression by RNA Interference using an integratable vector with opposing T7 promoters. J Biol Chem 2000;275:40174-9.
51. LaCount D.J., Bruse S., Hill K.L., Donelson J.E. Double-stranded RNA interference in Trypanosoma brucei using head-to-head promoters. Mol. Biochem. Parasitol. 111:2000;67-76.
52. Parrish S., Fleenor J., Xu S., Mello C., Fire A. Functional anatomy of a dsRNA trigger. Differential requirement for the two trigger strands in RNA interference. Mol. Cell. 6:2000;1077-1087.
53. Yang D., Lu H., Erickson J.W. Evidence that processed small dsRNAs may mediate sequence-specific mRNA degradation during RNAi in Drosophila embryos. Curr. Biol. 10:2000;1191-1200.
54. Bringaud F., Robinson D.R., Barradeau S., Biteau N., Baltz D., Baltz T. Characterization and disruption of a new Trypanosoma brucei repetitive flagellum protein, using double-stranded RNA inhibition. Mol. Biochem. Parasitol. 111:2000;283-297.
55. Wang Z., Englund P.T. RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J. 20:2001;4674-4683.
56. Bastin P., Matthews K.R., Gull K. The paraflagellar rod of Kinetoplastida: solved and unsolved questions. Parasitol. Today. 12:1996;302-307.
57. Schlaeppi K., Deflorin J., Seebeck T. The major component of the paraflagellar rod of Trypanosoma brucei is a helical protein that is encoded by two identical, tandemly linked genes. J. Cell Biol. 109:1989;1695-1709.
58. Deflorin J., Rudolf M., Seebeck T. The major components of the paraflagellar rod of Trypanosoma brucei are two similar, but distinct proteins which are encoded by two different gene loci. J. Biol. Chem. 269:1994;28745-28751.
59. Santrich C., Moore L., Sherwin T., Bastin P., Brokaw C., Gull K.et al. A motility function for the paraflagellar rod of Leishmania parasites revealed by PFR-2 gene knockouts. Mol. Biochem. Parasitol. 90:1997;95-109.
60. Bastin P., Sherwin T., Gull K. Paraflagellar rod is vital for trypanosome motility. Nature. 391:1998;548.
61. Maga J.A., Sherwin T., Francis S., Gull K., LeBowitz J.H. Genetic dissection of the Leishmania paraflagellar rod, a unique flagellar cytoskeleton structure. J. Cell Sci. 112:1999;2753-2763.
62. Bastin P., Pullen T.J., Sherwin T., Gull K. Protein transport and flagellum assembly dynamics revealed by analysis of the paralysed trypanosome mutant snl-1. J. Cell Sci. 112:1999;3769-3777.
63. Kohl L., Sherwin T., Gull K. Assembly of the paraflagellar rod and the flagellum attachment zone complex during the Trypanosoma brucei cell cycle. J. Eukaryot. Microbiol. 46:1999;105-109.
64. Bastin P., Bagherzadeh Z., Matthews K.R., Gull K. A novel epitope tag system to study protein targeting and organelle biogenesis in Trypanosoma brucei. Mol. Biochem. Parasitol. 77:1996;235-239.
65. Beard C.A., Saborio J.L., Tewari D., Krieglstein K.G., Henschen A.H., Manning J.E. Evidence for two distinct major protein components, PAR 1 and PAR 2, in the paraflagellar rod of Trypanosoma cruzi. Complete nucleotide sequence of PAR. J. Biol. Chem. 267:1992;21656-21662.
66. Wirtz E., Leal S., Ochatt C., Cross G.A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:1999;89-101.
67. Beverley S.M., Clayton C.E. Transfection of Leishmania and Trypanosoma brucei by electroporation. Methods Mol. Biol. 21:1993;333-348.
68. Sherwin T., Schneider A., Sasse R., Seebeck T., Gull K. Distinct localization and cell cycle dependence of COOH terminally tyrosinolated alpha-tubulin in the microtubules of Trypanosoma brucei brucei. J. Cell Biol. 104:1987;439-446.
69. Wirtz E., Clayton C. Inducible gene expression in trypanosomes mediated by a prokaryotic repressor. Science. 268:1995;1179-1183.
70. Bastin P., Pullen T.J., Moreira-Leite F.F., Gull K. Inside and outside of the trypanosome flagellum:a multifunctional organelle. Microbes Infect. 2:2000;1865-1874.
71. Bastin P., MacRae T.H., Francis S.B., Matthews K.R., Gull K. Flagellar morphogenesis: protein targeting and assembly in the paraflagellar rod of trypanosomes. Mol. Cell Biol. 19:1999;8191-8200.
72. Bastin P., Gull K. Assembly and function of complex flagellar structures illustrated by the paraflagellar rod of trypanosomes. Protist. 150:1999;113-123.
73. Vaucheret H., Beclin C., Fagard M. Post-transcriptional gene silencing in plants. J. Cell Sci. 114:2001;3083-3091.
74. Beclin C., Boutet S., Waterhouse P., Vaucheret H. A branched pathway for transgene-induced RNA silencing in plants. Curr. Biol. 12:2002;684-688.
75. Galvani A., Sperling L. Transgene-mediated post-transcriptional gene silencing is inhibited by 3′ non-coding sequences in Paramecium. Nucleic Acids Res. 29:2001;4387-4394.
76. Tabara H., Grishok A., Mello C.C. RNAi in C. elegans: soaking in the genome sequence. Science. 282:1998;430-431.
77. Ismach R., Cianci C.M., Caulfield J.P., Langer P.J., Hein A., McMahon-Pratt D. Flagellar membrane and paraxial rod proteins of Leishmania: characterization employing monoclonal antibodies. J. Protozool. 36:1989;617-624.
78. Elbashir S.M., Martinez J., Patkaniowska A., Lendeckel W., Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 20:2001;6877-6888.
79. Boutla A., Delidakis C., Livadaras I., Tsagris M., Tabler M. Short 5′-phosphorylated double-stranded RNAs induce RNA interference in Drosophila. Curr. Biol. 11:2001;1776-1780.