Rapid decay of unstable Leishmania mRNAs bearing a conserved retroposon signature 3'-UTR motif is initiated by a site-specific endonucleolytic cleavage without prior deadenylation

Nucleic Acids Research

Volumn 38, Issue 17, 2010, Pages 5867-5883

  Müller, Michaela ^a,b   Padmanabhan, Prasad K ^a   Rochette, Annie ^a   Mukherjee, Debdutta ^a   Smith, Martin ^a   Dumas, Carole ^a   Papadopoulou, Barbara ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; MESSENGER RNA; POLYADENYLIC ACID; URACIL; 3' UNTRANSLATED REGION; COMPLEMENTARY RNA; RETROPOSON; RIBONUCLEASE;

3' UNTRANSLATED REGION; ADENYLATION; ARTICLE; CONTROLLED STUDY; EUKARYOTE; GENE DELETION; IN VIVO STUDY; LEISHMANIA; LEISHMANIA BRAZILIENSIS; LEISHMANIA INFANTUM; LEISHMANIA MAJOR; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN MOTIF; RETROPOSON; RNA CLEAVAGE; RNA DEGRADATION; RNA STABILITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS;

EUKARYOTA;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; CONSERVED SEQUENCE; ENDORIBONUCLEASES; LEISHMANIA MAJOR; MOLECULAR SEQUENCE DATA; RETROELEMENTS; RNA STABILITY; RNA, ANTISENSE; RNA, MESSENGER;

EID: 77954359825     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq349     Document Type: Article

References (65)

1. Myler,P.J., Audleman,L., deVos,T., Hixson,G., Kiser,P., Lemley,C., Magness,C., Rickel,E., Sisk,E., Sunkin,S. et al. (1999) Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes. Proc. Natl Acad. Sci. USA, 96, 2902-2906.
2. Martinez-Calvillo,S., Yan,S., Nguyen,D., Fox,M., Stuart,K. and Myler,P.J. (2003) Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol. Cell, 11, 1291-1299.
3. Liang,X.H., Haritan,A., Uliel,S. and Michaeli,S. (2003) trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot. Cell, 2, 830-840.
4. Clayton,C. and Shapira,M. (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol. Biochem. Parasitol., 156, 93-101.
5. Haile,S. and Papadopoulou,B. (2007) Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr. Opin. Microbiol., 10, 569-577.
6. Parker,R. and Song,H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol., 11, 121-127.
7. Houseley,J., LaCava,J. and Tollervey,D. (2006) RNA-quality control by the exosome. Nat. Rev. Mol. Cell. Biol., 7, 529-539.
8. Coller,J. and Parker,R. (2004) Eukaryotic mRNA decapping. Annu. Rev. Biochem., 73, 861-890.
9. Milone,J., Wilusz,J. and Bellofatto,V. (2002) Identification of mRNA decapping activities and an ARE-regulated 3′ to 5′ exonuclease activity in trypanosome extracts. Nucleic Acids Res., 30, 4040-4050.
10. Ivens,A.C., Peacock,C.S., Worthey,E.A., Murphy,L., Aggarwal,G., Berriman,M., Sisk,E., Rajandream,M.A., Adlem,E., Aert,R. et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science, 309, 436-442.
11. Schwede,A., Ellis,L., Luther,J., Carrington,M., Stoecklin,G. and Clayton,C. (2008) A role for Caf1 in mRNA deadenylation and decay in trypanosomes and human cells. Nucleic Acids Res., 36, 3374-3388.
12. Li,C.H., Irmer,H., Gudjonsdottir-Planck,D., Freese,S., Salm,H., Haile,S., Estevez,A.M. and Clayton,C. (2006) Roles of a Trypanosoma brucei 5′->3′ exoribonuclease homolog in mRNA degradation. RNA, 12, 2171-2186.
13. Cristodero,M., Bottcher,B., Diepholz,M., Scheffzek,K. and Clayton,C. (2008) The Leishmania tarentolae exosome: purification and structural analysis by electron microscopy. Mol. Biochem. Parasitol., 159, 24-29.
14. Estevez,A.M., Kempf,T. and Clayton,C. (2001) The exosome of Trypanosoma brucei. EMBO J., 20, 3831-3839.
15. Estevez,A.M., Lehner,B., Sanderson,C.M., Ruppert,T. and Clayton,C. (2003) The roles of intersubunit interactions in exosome stability. J. Biol. Chem., 278, 34943-34951.
16. Haile,S., Estevez,A.M. and Clayton,C. (2003) A role for the exosome in the in vivo degradation of unstable mRNAs. RNA, 9, 1491-1501.
17. Haile,S., Dupe,A. and Papadopoulou,B. (2008) Deadenylation-independent stage-specific mRNA degradation in Leishmania. Nucleic Acids Res., 36, 1634-1644.
18. Bringaud,F., Muller,M., Cerqueira,G.C., Smith,M., Rochette,A., El-Sayed,N.M., Papadopoulou,B. and Ghedin,E. (2007) Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog., 3, 1291-1307.
19. Bringaud,F., Ghedin,E., El-Sayed,N.M. and Papadopoulou,B. (2008) Role of transposable elements in trypanosomatids. Microbes. Infect., 10, 575-581.
20. Smith,M., Blanchette,M. and Papadopoulou,B. (2008) Improving the prediction of mRNA extremities in the parasitic protozoan Leishmania. BMC Bioinformatics, 9, 158.
21. Smith,M., Bringaud,F. and Papadopoulou,B. (2009) Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics, 10, 240.
22. Boucher,N., Wu,Y., Dumas,C., Dube,M., Sereno,D., Breton,M. and Papadopoulou,B. (2002) A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3′-untranslated region element. J. Biol. Chem., 277, 19511-19520.
23. McNicoll,F., Muller,M., Cloutier,S., Boilard,N., Rochette,A., Dube,M. and Papadopoulou,B. (2005) Distinct 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J. Biol. Chem., 280, 35238-35246.
24. Roy,G., Dumas,C., Sereno,D., Wu,Y., Singh,A.K., Tremblay,M.J., Ouellette,M.M.O. and Papadopoulou,B. (2000) Episomal and stable expression of reporter genes for quantifying Leishmania spp. infections in macrophages and in animal models. Mol. Biochem. Parasitol., 110, 195-206.
25. Papadopoulou,B., Roy,G. and Ouellette,M. (1992) A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J., 11, 3601-3608.
26. Schwede,A., Manful,T., Jha,B.A., Helbig,C., Bercovich,N., Stewart,M. and Clayton,C. (2009) The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res., 37, 5511-5528.
27. Badis,G., Saveanu,C., Fromont-Racine,M. and Jacquier,A. (2004) Targeted mRNA degradation by deadenylation-independent decapping. Mol. Cell, 15, 5-15.
28. Liu,H. and Kiledjian,M. (2007) An erythroid-enriched endoribonuclease (ErEN) involved in alpha-globin mRNA turnover. Protein Pept. Lett., 14, 131-136.
29. Muhlrad,D. and Parker,R. (2005) The yeast EDC1 mRNA undergoes deadenylation-independent decapping stimulated by Not2p, Not4p, and Not5p. EMBO J., 24, 1033-1045.
30. Schoenberg,D.R. and Cunningham,K.S. (1999) Characterization of mRNA endonucleases. Methods, 17, 60-73.
31. Grange,T. (2008) Sensitive detection of mRNA decay products by use of reverse-ligation-mediated PCR (RL-PCR). Methods Enzymol., 448, 445-466.
32. Couttet,P., Fromont-Racine,M., Steel,D., Pictet,R. and Grange,T. (1997) Messenger RNA deadenylylation precedes decapping in mammalian cells. Proc. Natl Acad. Sci. USA, 27, 5628-5633.
33. Monnerat,S., Martinez-Calvillo,S., Worthey,E., Myler,P.J., Stuart,K.D. and Fasel,N. (2004) Genomic organization and gene expression in a chromosomal region of Leishmania major. Mol. Biochem. Parasitol., 134, 233-243.
34. Papadopoulou,B., Roy,G. and Ouellette,M. (1994) Autonomous replication of bacterial DNA plasmid oligomers in Leishmania. Mol. Biochem. Parasitol., 65, 39-49.
35. Mathews,D.H., Disney,M.D., Childs,J.L., Schroeder,S.J., Zuker,M. and Turner,D.H. (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl Acad. Sci. USA, 101, 7287-7292.
36. Rochette,A., Raymond,F., Ubeda,J.M., Smith,M., Messier,N., Boisvert,S., Rigault,P., Corbeil,J., Ouellette,M. and Papadopoulou,B. (2008) Genome-wide gene expression profiling analysis of Leishmania major and Leishmania infantum developmental stages reveals substantial differences between the two species. BMC Genomics, 9, 255.
37. Jensen,B.C., Sivam,D., Kifer,C.T., Myler,P.J. and Parsons,M. (2009) Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei. BMC Genomics, 10, 482.
38. Kabani,S., Fenn,K., Ross,A., Ivens,A., Smith,T.K., Ghazal,P. and Matthews,K. (2009) Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics, 10, 427.
39. Ouellette,M. and Papadopoulou,B. (2009) Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J. Biol., 8, 100.
40. Queiroz,R., Benz,C., Fellenberg,K., Hoheisel,J.D. and Clayton,C. (2009) Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics, 10, 495.
41. Gopalan,V., Vioque,A. and Altman,S. (2002) RNase P: variations and uses. J. Biol. Chem., 277, 6759-6762.
42. Xiao,S., Scott,F., Fierke,C.A. and Engelke,D.R. (2002) Eukaryotic ribonuclease P: a plurality of ribonucleoprotein enzymes. Annu. Rev. Biochem., 71, 165-189.
43. Yang,F. and Schoenberg,D.R. (2004) Endonuclease-mediated mRNA decay involves the selective targeting of PMR1 to polyribosome-bound substrate mRNA. Mol. Cell, 14, 435-445.
44. Tourriere,H., Gallouzi,I.E., Chebli,K., Capony,J.P., Mouaikel,J., van der Geer,P. and Tazi,J. (2001) RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol. Cell Biol., 21, 7747-7760.
45. Hollien,J. and Weissman,J.S. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science, 313, 104-107.
46. Gill,T., Aulds,J. and Schmitt,M. (2006) A specialized processing body that is temporally and asymmetrically regulated during the cell cycle in Saccharomyces cerevisiae. J. Cell Biol., 173, 35-45.
47. Jaskiewicz,L. and Filipowicz,W. (2008) Role of Dicer in posttranscriptional RNA silencing. Curr. Top. Microbiol. Immunol., 320, 77-97.
48. Lingel,A. and Izaurralde,E. (2004) RNAi: finding the elusive endonuclease. RNA, 10, 1675-1679.
49. Lebreton,A., Tomecki,R., Dziembowski,A. and Seraphin,B. (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature, 456, 993-996.
50. Schaeffer,D., Tsanova,B., Barbas,A., Reis,F.P., Dastidar,E.G., Sanchez-Rotunno,M., Arraiano,C.M. and van Hoof,A. (2009) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat. Struct. Mol. Biol., 16, 56-62.
51. Eberle,A.B., Lykke-Andersen,S., Muhlemann,O. and Jensen,T.H. (2009) SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat. Struct. Mol. Biol., 16, 49-55.
52. Bringaud,F., Ghedin,E., Blandin,G., Bartholomeu,D.C., Caler,E., Levin,M.J., Baltz,T. and El-Sayed,N.M. (2006) Evolution of non-LTR retrotransposons in the trypanosomatid genomes: Leishmania major has lost the active elements. Mol. Biochem. Parasitol., 145, 158-170.
53. Zingler,N., Weichenrieder,O. and Schumann,G.G. (2005) APE-type non-LTR retrotransposons: determinants involved in target site recognition. Cytogenet Genome Res., 110, 250-268.
54. Barnes,T., Kim,W.C., Mantha,A.K., Kim,S.E., Izumi,T., Mitra,S. and Lee,C.H. (2009) Identification of Apurinic/apyrimidinic endonuclease 1 (APE1) as the endoribonuclease that cleaves c-myc mRNA. Nucleic Acids Res., 37, 3946-3958.
55. Peacock,C.S., Seeger,K., Harris,D., Murphy,L., Ruiz,J.C., Quail,M.A., Peters,N., Adlem,E., Tivey,A., Aslett,M. et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat. Genet., 39, 839-847.
56. Robinson,K.A. and Beverley,S.M. (2003) Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol. Biochem. Parasitol., 128, 217-228.
57. Siomi,M.C., Saito,K. and Siomi,H. (2008) How selfish retrotransposons are silenced in Drosophila germline and somatic cells. FEBS Lett., 582, 2473-2478.
58. Belli,S.I., Monnerat,S., Schaff,C., Masina,S., Noll,T., Myler,P.J., Stuart,K. and Fasel,N. (2003) Sense and antisense transcripts in the histone H1 (HIS-1) locus of Leishmania major. Int. J. Parasitol., 33, 965-975.
59. Dumas,C., Chow,C., Muller,M. and Papadopoulou,B. (2006) A novel class of developmentally regulated noncoding RNAs in Leishmania. Eukaryot. Cell, 5, 2033-2046.
60. Kapler,G.M. and Beverley,S.M. (1989) Transcriptional mapping of the amplified region encoding the dihydrofolate reductase-thymidylate synthase of Leishmania major reveals a high density of transcripts, including overlapping and antisense RNAs. Mol. Cell Biol., 9, 3959-3972.
61. Brantl,S. (2007) Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr. Opin. Microbiol., 10, 102-109.
62. Matsui,K., Nishizawa,M., Ozaki,T., Kimura,T., Hashimoto,I., Yamada,M., Kaibori,M., Kamiyama,Y., Ito,S. and Okumura,T. (2008) Natural antisense transcript stabilizes inducible nitric oxide synthase messenger RNA in rat hepatocytes. Hepatology, 47, 686-697.
63. Opdyke,J., Kang,J. and Storz,G. (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J. Bacteriol., 186, 6698-6705.
64. Chen,D.Q., Kolli,B.K., Yadava,N., Lu,H.G., Gilman-Sachs,A., Peterson,D.A. and Chang,K.P. (2000) Episomal expression of specific sense and antisense mRNAs in Leishmania amazonensis: modulation of gp63 level in promastigotes and their infection of macrophages in vitro. Infect. Immun., 68, 80-86.
65. Zhang,W.W. and Matlashewski,G. (1997) Loss of virulence in Leishmania donovani deficient in an amastigote-specific protein, A2. Proc. Natl Acad. Sci. USA, 94, 8807-8811.