Preferential translation of Hsp83 in Leishmania requires a thermosensitive polypyrimidine-rich element in the 3′ UTR and involves scanning of the 5′ UTR

RNA

Volumn 16, Issue 2, 2010, Pages 364-374

  David, Maya ^a   Gabdank, Idan ^a   Ben David, Miriam ^a   Zilka, Alon ^a   Orr, Irit ^a   Barash, Danny ^a   Shapira, Michal ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

3 UTR; Hsp83; Leishmania; Polypyrimidine tract; Scanning of 5 UTR; Translation regulation

Indexed keywords

HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 83; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; LEISHMANIA; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYPYRIMIDINE RICH ELEMENT; PRIORITY JOURNAL; RNA FOLDING; RNA STRUCTURE; TEMPERATURE SENSITIVITY; TRANSLATION INITIATION; TRANSLATION REGULATION;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; DNA PRIMERS; GENES, REPORTER; HEAT-SHOCK PROTEINS; LEISHMANIA; LEISHMANIA MEXICANA; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; PROTOZOAN PROTEINS; RNA, MESSENGER; RNA, PROTOZOAN; TEMPERATURE;

MAMMALIA; TRYPANOSOMATIDAE;

EID: 75149175207     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1874710     Document Type: Article

References (48)

1. Ahmed R, Duncan RF. 2004. Translational regulation of Hsp90 mRNA. AUG-proximal 5′-untranslated region elements essential for preferential heat shock translation. J Biol Chem 279: 49919-49930.
2. Argaman M, Aly R, Shapira M. 1994. Expression of the heat shock protein 83 in Leishmania is regulated post transcriptionally. Mol Biochem Parasitol 64: 95-110.
3. Besse F, Lopez de Quinto S, Marchand V, Trucco A, Ephrussi A. 2009. Drosophila PTB promotes formation of high-order RNP particles and represses oskar translation. Genes & Dev 23: 195-207.
4. Boucher N, Wu Y, Dumas C, Dube M, Sereno D, Breton M, 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.
5. Bushell M, Stoneley M, Kong YW, Hamilton TL, Spriggs KA, Dobbyn HC, Qin X, Sarnow P, Willis AE. 2006. Polypyrimidine tract binding protein regulates IRES-mediated gene expression during apoptosis. Mol Cell 23: 401-412.
6. Chowdhury S, Ragaz C, Kreuger E, Narberhaus F. 2003. Temperature- controlled structural alterations of an RNA thermometer. J Biol Chem 278: 47915-47921.
7. Chowdhury S, Maris C, Allain FH, Narberhaus F. 2006. Molecular basis for temperature sensing by an RNA thermometer. EMBO J 25: 2487-2497.
8. Clayton C, Shapira M. 2007. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
9. Clerte C, Hall KB. 2009. The domains of polypyrimidine tract binding protein have distinct RNA structural preferences. Biochemistry 48: 2063-2074.
10. Duncan RF. 2008. Rapamycin conditionally inhibits Hsp90 but not Hsp70 mRNA translation in Drosophila: Implications for the mechanisms of HspmRNAtranslation. Cell Stress Chaperones 13: 143-155.
11. Folgueira C, Quijada L, Soto M, Abanades DR, Alonso C, Requena JM. 2005. The translational efficiencies of the two Leishmania infantum HSP70 mRNAs, differing in their 3′-untranslated regions, are affected by shifts in the temperature of growth through different mechanisms. J Biol Chem 280: 35172-35183.
12. Galban S, Kuwano Y, Pullmann R Jr, Martindale JL, Kim HH, Lal A, Abdelmohsen K, Yang X, Dang Y, Liu JO, et al. 2008. RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1α. Mol Cell Biol 28: 93-107.
13. Garlapati S, Dahan E, Shapira M. 1999. Effect of acidic pH on heat shock gene expression in Leishmania. Mol Biochem Parasitol 100: 95-101.
14. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963.
15. Hellen CU, Sarnow P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes & Dev 15: 1593-1612.
16. Hernandez G, Vazquez-Pianzola P, Sierra JM, Rivera-Pomar R. 2004. Internal ribosome entry site drives cap-independent translation of reaper and heat shock protein 70 mRNAs in Drosophila embryos. RNA 10: 1783-1797.
17. Hofacker IL. 2003. Vienna RNA secondary structure server. Nucleic Acids Res 31: 3429-3431.
18. Holcik M, Sonenberg N, Korneluk RG. 2000. Internal ribosome initiation of translation and the control of cell death. Trends Genet 16: 469-473.
19. Klemenz R, Hultmark D, Gehring WJ. 1985. Selective translation of heat shock mRNA in Drosophila melanogaster depends on sequence information in the leader. EMBO J 4: 2053-2060.
20. Laban A, Wirth DF. 1989. Transfection of Leishmania enriettii and expression of chloramphenicol acetyltransferase gene. Proc Natl Acad Sci 86: 9119-9123.
21. LeBowitz JH, Smith H, Beverley SM. 1993. Coupling of polyadenylation site selection and trans-splicing in Leishmania. Genes & Dev 7: 996-1007.
22. Lindquist S. 1980. Translational efficiency of heat induced messages in Drosophila melanogaster cells. J Mol Biol 137: 151-158.
23. Markham NR, Zuker M. 2005. DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res 33: W577-W581.
24. Markham NR, Zuker M. 2008. UNAFold: Software for nucleic acid folding and hybridization. Methods Mol Biol 453: 3-31.
25. Martinez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart KD, Myler PJ. 2003. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11: 1291-1299.
26. McGarry TJ, Lindquist S. 1985. The preferential translation of Drosophila hsp70 mRNA requires sequences in the untranslated leader. Cell 42: 903-911.
27. Mitchell SA, Spriggs KA, Bushell M, Evans JR, Stoneley M, Le Quesne JP, Spriggs RV, Willis AE. 2005. Identification of a motif that mediates polypyrimidine tract-binding protein-dependent internal ribosome entry. Genes & Dev 19: 1556-1571.
28. Morita MT, Tanaka Y, Kodama TS, Kyogoku Y, Yanagi H, Yura T. 1999. Translational induction of heat shock transcription factor σ32: Evidence for a built-in RNA thermosensor. Genes & Dev 13: 655-665.
29. Narberhaus F, Waldminghaus T, Chowdhury S. 2006. RNA thermometers. FEMS Microbiol Rev 30: 3-16.
30. Perez I, Lin CH, McAfee JG, Patton JG. 1997. Mutation of PTB binding sites causes misregulation of alternative 3′ splice site selection in vivo. RNA 3: 764-778.
31. Quijada L, Soto M, Alonso C, Requena JM. 1997. Analysis of post-transcriptional regulation operating on transcription products of the tandemly linked Leishmania infantum hsp70 genes. J Biol Chem 272: 4493-4499.
32. Quijada L, Soto M, Alonso C, Requena JM. 2000. Identification of a putative regulatory element in the 3′-untranslated region that controls expression of HSP70 in Leishmania infantum. Mol Biochem Parasitol 110: 79-91.
33. Reyes R, Izquierdo JM. 2007. The RNA-binding protein PTB exerts translational control on 3′-untranslated region of the mRNA for the ATP synthase β-subunit. Biochem Biophys Res Commun 357: 1107-1112.
34. Rosenzweig D, Smith D, Opperdoes F, Stern S, Olafson RW, Zilberstein D. 2008. Retooling Leishmania metabolism: From sand fly gut to human macrophage. FASEB J 22: 590-602.
35. Rubtsova MP, Sizova DV, Dmitriev SE, Ivanov DS, Prassolov VS, Shatsky IN. 2003. Distinctive properties of the 5′-untranslated region of human hsp70 mRNA. J Biol Chem 278: 22350-22356.
36. Shapira M, McEwen JG, Jaffe CL. 1988. Temperature effects on molecular processes which lead to stage differentiation in Leishmania. EMBO J 7: 2895-2901.
37. Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, Fenyo D, Wang X, Dewell S, Cross GA. 2009. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes & Dev 23: 1063-1076.
38. Singh R, Valcarcel J, Green MR. 1995. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science 268: 1173-1176.
39. Song Y, Tzima E, Ochs K, Bassili G, Trusheim H, Linder M, Preissner KT, Niepmann M. 2005. Evidence for an RNA chaperone function of polypyrimidine tract-binding protein in picornavirus translation. RNA 11: 1809-1824.
40. Spriggs KA, Bushell M, Mitchell SA, Willis AE. 2005. Internal ribosome entry segment-mediated translation during apoptosis: The role of IRES-trans-acting factors. Cell Death Differ 12: 585-591.
41. Stern MZ, Gupta SK, Salmon-Divon M, Haham T, Barda O, Levi S, Wachtel C, Nilsen TW, Michaeli S. 2009. Multiple roles for polypyrimidine tract binding (PTB) proteins in trypanosome RNA metabolism. RNA 15: 648-665.
42. Thomas R. 1951. On the existence of labile bonds in secondary structures of the nucleic acids' molecule. Experientia 7: 261-262.
43. Thomas R. 1993. The denaturation of DNA. Gene 135: 77-79.
44. Yoffe Y, Leger M, Zinoviev A, Zuberek J, Darzynkiewicz E, Wagner G, Shapira M. 2009. Evolutionary changes in the Leishmania eIF4F complex involve variations in the eIF4E-eIF4G interactions. Nucleic Acids Res 37: 3243-3253.
45. Yueh A, Schneider RJ. 2000. Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes & Dev 14: 414-421.
46. Zilka A, Garlapati S, Dahan E, Yaolsky V, Shapira M. 2001. Developmental regulation of heat shock protein 83 in Leishmania. 3′ processing and mRNA stability control transcript abundance, and translation is directed by a determinant in the 3′-untranslated region. J Biol Chem 276: 47922-47929.
47. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
48. Zuker M, Jacobson AB. 1998. Using reliability information to annotate RNA secondary structures. RNA 4: 669-679.