Deadenylation-independent stage-specific mRNA degradation in Leishmania

Nucleic Acids Research

Volumn 36, Issue 5, 2008, Pages 1634-1644

  Haile, Simon ^a   Dupé, Aurélien ^a   Papadopoulou, Barbara ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE H;

3' UNTRANSLATED REGION; ADENYLATION; AMASTIGOTE; ARTICLE; CONTROLLED STUDY; EUKARYOTE; GENE EXPRESSION REGULATION; LEISHMANIA DONOVANI; LIFE CYCLE; METABOLIC REGULATION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROMASTIGOTE; PROTOZOAL GENETICS; RNA CAPPING; RNA DEGRADATION; RNA STRUCTURE; SIGNAL TRANSDUCTION; U RICH ELEMENT;

3' UNTRANSLATED REGIONS; ANIMALS; ANTIGENS, PROTOZOAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LEISHMANIA INFANTUM; POLY A; RNA CAPS; RNA STABILITY; RNA, MESSENGER; URIDINE;

EUKARYOTA; HEXAPODA; MAMMALIA; TRYPANOSOMATIDAE;

EID: 41149170097     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn019     Document Type: Article

References (61)

1. Cohen-Freue,G., Holzer,T.R., Forney,J.D. and McMaster,W.R. (2007) Global gene expression in Leishmania. Int. J. Parasitol., 37, 1077-1086.
2. Brems,S., Guilbride,D.L., Gundlesdodjir-Planck,D., Busold,C., Luu,V.D., Schanne,M., Hoheisel,J. and Clayton,C. (2005) The transcriptomes of Trypanosoma brucei Lister 427 and TREU927 bloodstream and procyclic trypomastigotes. Mol. Biochem. Parasitol., 139, 163-172.
3. Minning,T.A., Bua,J., Garcia,G.A., McGraw,R.A. and Tarleton,R.L. (2003) Microarray profiling of gene expression during trypomastigote to amastigote transition in Trypanosoma cruzi. Mol. Biochem. Parasitol. 131, 55-64.
4. Atwood,J.A.,3rd, Weatherly,D.B., Minning,T.A., Bundy,B., Cavola,C., Opperdoes,F.R., Orlando,R. and Tarleton,R.L. (2005) The Trypanosoma cruzi proteome. Science, 309, 473-476.
5. Berriman,M., Ghedin,E., Hertz-Fowler,C., Blandin,G., Renauld,H., Bartholomeu,D.C., Lennard,N.J., Caler,E., Hamlin,N.E et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science, 309, 416-422.
6. EI-Sayed,N.M., Myler,P.J., Blandin,G., Berriman,M., Crabtree,J., Aggarwal,G., Caler,E., Renauld,H., Worthey,E.A. et al. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309, 404-409.
7. Ivens,A.C., Peacock,C.S., Worthey,E.A., Murphy,L., Aggarwal,G., Berriman,M., Sisk,E., Rajandream,M.A., Adlem,E. et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science, 309, 436-442.
8. 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.
9. 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.
10. Martinez-Calvillo,S., Nguyen,D., Stuart,K. and Myler,P.J. (2004) Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot. Cell, 3, 506-517.
11. Clayton,C. and Shapira,M. (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol. Biochem. Parasitol. 156, 93-101.
12. Haile,S. and Papadopoulou,B. (2007) Developmental regulation gene expression in trypanosomatid parasitic protozoa. Curr. Opin. Microbiol., 10, 569-577.
13. Parker,R. and Song,H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol., 11, 121-127.
14. Mitchell,P. and Tallervey,D. (2000) mRNA stability in eukaryotes. Curr. Opin. Genet. Dev., 10, 193-198.
15. Heyer,W.D., Johnson,A.W., Reinhart,U. and Kolodner,R.D. (1995) Regulation and intracellular localization of Saccharomyces cerevisiae strand exchange protein 1 (Sep1/Xrn1/Kem1), a multifunctional exonuclease. Mol. Cell. Biol., 15, 2728-2736.
16. Johnson,A.W. (1997) Rat1p and Xrn1p are functionally interchangeable exoribonucleases that are restricted to and required in the nucleus and cytoplasm, respectively. Mol. Cell. Biol., 17, 6122-6130.
17. Amberg,D.C., Goldstein,A.L. and Cole,C.N. (1992) Isolation and characterization of RAT1: An essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev., 6, 1173-1189.
18. Allmang,C., Kufel,J., Chanfreau,G., Mitchell,P., Petfalski,E. and Tollervey,D. (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. Embo J., 18, 5399-5410.
19. Bousquet-Antonelli,C., Presutti,C, and Tollervey,D. (2000) Identification of a regulated pathway for nuclear pre-mRNA turnover. Cell, 102, 765-775.
20. Chen,C.Y., Gherzi,R., Ong,S.E., Chan,E.L., Raijmakers,R., Pruijn,G.J., Stoecklin,G., Moroni,C., Mann,M. et al. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell, 107 451-464.
21. Mukherjee,D., Gao,M., O'Connor,J.P., Raijmakers,R., Pruijn,G., Lutz,C.S. and Wilusz,J. (2002) The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. Embo J., 21 165-174.
22. Stoecklin,G., Mayo,T. and Anderson,P. (2006) ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep., 7, 72-77.
23. 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.
24. Irmer,H. and Clayton,C. (2001) Degradation of the unstable EP1 mRNA in Trypanosoma brucei involves initial destruction of the 3′-untranslated region. Nucleic Acids Res., 29, 4707-4715.
25. Estevez,A.M., Kempf,T. and Clayton,C. (2001) The exosome of Trypanosoma brucei. Embo J., 20, 3831-3839.
26. 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.
27. Haile,S., Cristodero,M., Clayton,C. and Estevez,A.M. (2007) The subcellular localisation of trypanosome RRP6 and its association with the exosome. Mol. Biochem. Parasitol., 151, 52-58.
28. Li,C.H., Irmer,H., Gudjonsdottir-Planck,D., Freese,S., Sahm,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.
29. 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.
30. Colasante,C., Robles,A., Li,C.H., Schwede,A., Benz,C., Voncken,F., Guilbride,D.L. and Clayton,C. (2007) Regulated expression of glycosomal phosphoglycerate kinase in Trypanosoma brucei. Mol. Biochem. Parasitol., 151, 193-204.
31. 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(9), 1291-1307.
32. Boucher,N., Wu,Y., Dumas,C., Dubé,M., Sereno,D., Breton,M. and Papadopoulou,B. (2002) A common mechanism of stage-regulated gene expression in Leshmania mediated by a conserved 3′-untranslated region element. J. Biol. Chem., 277, 19511-19520.
33. 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.
34. D'Orso,I., De Gaudenzi,J.G. and Frasch,A.C. (2003) RNA-binding proteins and mRNA turnover in trypanosomes. Trends Parasitol., 19, 151-155.
35. Drozdz,M. and Clayton,C. (1999) Structure of a regulatory 3′ untranslated. region from Trypanosoma brucei. RNA, 5, 1632 1644.
36. Hotz,H.R., Hartmann,C., Huober,K., Hug,M. and Clayton,C. (1997) Mechanisms of developmental regulation in Trypanosoma brucei: A polypyrimidine tract in the 3′-untranslated region of a surface protein mRNA affects RNA abundance and translation. Nucleic Acids Res., 25, 3017-3026.
37. Di Noia,J.M., D'Orso,I., Sanchez,D.O. and Frasch,A.C. (2000) 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. J. Biol. Chem., 275, 10218-10227.
38. D'Orso,I. and Frasch,A.C. (2001) Functionally different AU- and G-rich cis-elements confer developmentally regulated mRNA stability in Trypanosoma cruzi by interaction with specific RNA-binding proteins. J. Biol. Chem., 276, 15783-15793.
39. Quijada,L., Guerra-Giraldez,C., Drozdz,M., Hartmann,C., Irmer,H., Ben-Dov,C., Cristodero,M., Ding,M. and 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 Res., 30, 4414-424.
40. Mayho,M., Fenn,K., Craddy,P., Crosthwaite,S. and Matthews,K. (2006) Post-transcriptional control of nuclear-encoded cytochrome oxidase subunits in Trypanosoma brucei: Evidence for genome-wide conservation of life-cycle stage-specific regulatory elements. Nucleic Acids Res., 34, 5312-5324.
41. Chen,C.Y., Xu,N. and Shyu,A.B. (1995) 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. Mol. Cell. Biol., 15, 5777-5788.
42. D'Orso,I. and Frasch,A.C. (2001) TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes. J. Biol. Chem., 276, 34801-34809.
43. D'Orso,I. and Frasch,A.C. (21)02) TcUBP-1, an mRNA destabilizing factor from trypanosomes, homodimerizes and interacts witfi novel AU-rich element- and Poly(A)-binding proteins forming a ribonucleoprotein complex. J. Biol. Chem., 277, 50520-50528.
44. Hartmann,C., Benz,C., Brems,S., Ellis,L., Luu,V.D., Stewart,M., D'Orso,J., Busold,C., Fellenberg,K. et al. (2007) The small trypanosome RNA-binding proteins TbUBP1 and TbUBP2 influence expression of F-box protein mRNAs in bloodstream trypanosomes. Eukaryot. Cell 6(11), 1964-1978.
45. Derbise,A., Lesic,B., Dacheux,D., Ghigo,J.M. and Carniel,E. (2003) A rapid and simple method for inactivating chromosomal genes in Yersinia. FEMS Immunol. Med. Microbiol., 38, 113-116.
46. Sereno,D. and Lemesre,J.L. (1997) Axenically cultured amastigote forms as an in vitro model for investigation of antileishmanial agents. Antimicrob. Agents Chemother., 41, 972-976.
47. 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.
48. Salles,F.J., Richards,W.G. and Strickland,S. (1999) Assaying the polyadenylation state of mRNAs. Methods, 17, 38-45.
49. Rochette,A., McNicoll,F., Girard,J., Breton,M., Leblanc,E., Bergeron,M.G. and rapadopoulou,B. (2005) Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp. Mol. Biochem. parasitol., 140, 205-220.
50. Rafati,S., Hassani, N., Taslimi,Y., Movassagh,H., Rochette,A. and Papadopoulou,B. (2006) Amastin peptide-binding antibodies as biomarkers of active human visceral leishmaniasis. Clin. Vaccine Immunol., 13, 1104-1110.
51. Wu,Y., El Fakhry,Y., Sereno,D., Tamar,S. and Papadopoulou,B. (2000) A new developmentally regulated gene family in Leishmania amastigotes enooding a homolog of amastin surface proteins. Mol. Biochem. Parasitol., 110, 345-357.
52. Kundig,C., Haimeur,A., Legare,D., Papadopoulou,B. and Ouellette,M. (1999) Increased transport of pteridines compensates for mutations in the high affinity folate transporter and contributes to methotrexate resistance in the protozoan parasite Leishmania tarentolae. Embo J. 18, 2342-2351.
53. Bonisch,C., Temme,C., Moritz,B. and Wahle,E. (2007) Degradation of hsp70 and other mRNAs in Drosophila via the 5′ 3′ pathway and its regulation by heat shock. J. Biol. Chem., 282, 21818-21828.
54. Meijer,H.A., Bushell,M.,.Hill,K., Gant,T.W., Willis,A.E., Jones,P. and de Mooi,C.H. (2007) A novel method for poly(A) fractionation reveals a large population of mRNAs with a short poly(A) tail in mammalian cells. Nucleic Acids Res., 35, e132.
55. Kushner,S.R. (2002) mRNA decay in Escherichia cob comes of age. J. Bacteriol., 184, 4658-4665; discussion 4657.
56. LaCava,J., Houseley,J., Saveanu,C., Petfalski,E., Thompson,E., Jacquier,A. and Tollervey,D. (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell, 121, 713-724.
57. Wyers,F., Rougemaille,M., Badis,G., Rousselle,J.C., Dufour,M.E., Boulay,J., Regnault,B., Devaux,F., Namane,A. et al. (2005) Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell, 121, 725-737.
58. West S, Gromak,N., Norbury,C.J. and Proudfoot,N.J. (2006) Adenylation and exosome-mediated degradation of cotranscriptionally cleaved pre-messenger RNA in human cells. Mol. Cell, 21, 437-443.
59. Hagan,K.W., Ruiz-Echevarria,M.J., Quan,Y. and Peltz,S.W. (1995) Characterization of cis-acting sequences and decay intermediates involved in nonsense-mediated mRNA turnover. Mol. Cell. Biol., 15, 809-823.
60. Muhlrad,D. and Parker,R. (1994) Premature translational termination triggers mRNA decapping. Nature, 370, 578-581.
61. Liu,H and Kiledjian,M. (2007) An erythroid-enriched endoribonuclease (ErEN) involved in alpha-globin mRNA turnover. Protein Pept. Lett. 14, 131-136.