Severe heat shock induces nucleolar accumulation of mRNAs in Trypanosoma cruzi

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Názer, Ezequiel ^a   Verdún, Ramiro E ^b   Sánchez, Daniel O ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CYTOPLASM; ENVIRONMENTAL STRESS; EPIMASTIGOTE; GENETIC TRANSCRIPTION; HEAT SHOCK RESPONSE; IMMUNOFLUORESCENCE; NONHUMAN; POLYMERASE CHAIN REACTION; POPULATION DYNAMICS; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RNA METABOLISM; RNA SYNTHESIS; TRYPANOSOMA CRUZI;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEOLUS; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; POLY A; PROTOZOAN PROTEINS; RNA, MESSENGER; TRYPANOSOMA CRUZI;

EID: 84865416681     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043715     Document Type: Article

References (42)

1. Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, et al. (2003) The trypanosomiases. Lancet 362: 1469-1480.
2. Clayton C, Shapira M, (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
3. Martinez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, et al. (2003) Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11: 1291-1299.
4. Sutton RE, Boothroyd JC, (1986) Evidence for trans splicing in trypanosomes. Cell 47: 527-535.
5. Anderson P, Kedersha N, (2006) RNA granules. J Cell Biol 172: 803-808.
6. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, et al. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169: 871-884.
7. Cassola A, De Gaudenzi JG, Frasch AC, (2007) Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol Microbiol 65: 655-670.
8. Holetz FB, Correa A, Avila AR, Nakamura CV, Krieger MA, et al. (2007) Evidence of P-body-like structures in Trypanosoma cruzi. Biochem Biophys Res Commun 356: 1062-1067.
9. Kramer S, Queiroz R, Ellis L, Webb H, Hoheisel JD, et al. (2008) Heat shock causes a decrease in polysomes and the appearance of stress granules in trypanosomes independently of eIF2(alpha) phosphorylation at Thr169. J Cell Sci 121: 3002-3014.
10. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, et al. (2002) Directed proteomic analysis of the human nucleolus. Curr Biol 12: 1-11.
11. Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, et al. (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16: 260-269.
12. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, et al. (2006) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93-106.
13. Fang Y, Spector DL, (2007) Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr Biol 17: 818-823.
14. Kim SH, Koroleva OA, Lewandowska D, Pendle AF, Clark GP, et al. (2009) Aberrant mRNA transcripts and the nonsense-mediated decay proteins UPF2 and UPF3 are enriched in the Arabidopsis nucleolus. Plant Cell 21: 2045-2057.
15. Boyne JR, Whitehouse A, (2006) Nucleolar trafficking is essential for nuclear export of intronless herpesvirus mRNA. Proceedings of the National Academy of Sciences 103: 15190-15195.
16. Hiscox JA, (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5: 119-127.
17. Michienzi A, Cagnon L, Bahner I, Rossi JJ, (2000) Ribozyme-mediated inhibition of HIV 1 suggests nucleolar trafficking of HIV-1 RNA. Proc Natl Acad Sci U S A 97: 8955-8960.
18. Rubbi CP, Milner J, (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. Embo J 22: 6068-6077.
19. Olson MO, (2004) Sensing cellular stress: another new function for the nucleolus? Sci STKE 2004: pe10.
20. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI, (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8: 574-585.
21. Koroleva OA, Calder G, Pendle AF, Kim SH, Lewandowska D, et al. (2009) Dynamic behavior of Arabidopsis eIF4A-III, putative core protein of exon junction complex: fast relocation to nucleolus and splicing speckles under hypoxia. Plant Cell 21: 1592-1606.
22. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, et al. (2005) Nucleolar proteome dynamics. Nature 433: 77-83.
23. Saavedra C, Tung KS, Amberg DC, Hopper AK, Cole CN, (1996) Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev 10: 1608-1620.
24. Tani T, Derby RJ, Hiraoka Y, Spector DL, (1995) Nucleolar accumulation of poly (A)+ RNA in heat-shocked yeast cells: implication of nucleolar involvement in mRNA transport. Mol Biol Cell 6: 1515-1534.
25. Ideue T, Azad AK, Yoshida J-i, Matsusaka T, Yanagida M, et al. (2004) The nucleolus is involved in mRNA export from the nucleus in fission yeast. J Cell Sci 117: 2887-2895.
26. Nazer E, Verdun RE, Sanchez DO, (2011) Nucleolar Localization of RNA Binding Proteins Induced by Actinomycin D and Heat Shock in Trypanosoma cruzi. PLoS One 6: e19920.
27. Nazer E, Sanchez DO, (2011) Nucleolar accumulation of RNA binding proteins induced by Actinomycin D is functional in Trypanosoma cruzi and Leishmania mexicana but not in T. brucei. PLoS One 6: e24184.
28. Requena JM, Jimenez-Ruiz A, Soto M, Assiego R, Santaren JF, et al. (1992) Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Mol Biochem Parasitol 53: 201-211.
29. Urmenyi TP, De Castro FT, Carvalho JF, De Souza W, Rondinelli E, (1992) Transcriptional and post-transcriptional control of tubulin gene expression in Trypanosoma cruzi. DNA Cell Biol 11: 101-109.
30. Bartholomeu DC, Silva RA, Galvao LM, el-Sayed NM, Donelson JE, et al. (2002) Trypanosoma cruzi: RNA structure and post-transcriptional control of tubulin gene expression. Exp Parasitol 102: 123-133.
31. Rodrigues DC, Silva R, Rondinelli E, Urmenyi TP, (2010) Trypanosoma cruzi: modulation of HSP70 mRNA stability by untranslated regions during heat shock. Exp Parasitol 126: 245-253.
32. Di Noia JM, D'Orso I, Sanchez DO, Frasch AC, (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.
33. Urban I, Santurio LB, Chidichimo A, Yu H, Chen X, et al. (2011) Molecular diversity of the Trypanosoma cruzi TcSMUG family of mucin genes and proteins. Biochem J 438: 303-313.
34. Lee MG, (1998) The 3′ untranslated region of the hsp 70 genes maintains the level of steady state mRNA in Trypanosoma brucei upon heat shock. Nucleic Acids Res 26: 4025-4033.
35. Jager AV, De Gaudenzi JG, Cassola A, D'Orso I, Frasch AC, (2007) mRNA maturation by two-step trans-splicing/polyadenylation processing in trypanosomes. Proc Natl Acad Sci U S A 104: 2035-2042.
36. Kramer S, Marnef A, Standart N, Carrington M (2012) Inhibition of mRNA maturation in trypanosomes causes the formation of novel foci at the nuclear periphery containing cytoplasmic regulators of mRNA fate. J Cell Sci.
37. Cuevas IC, Frasch AC, D'Orso I, (2005) Insights into a CRM1-mediated RNA-nuclear export pathway in Trypanosoma cruzi. Mol Biochem Parasitol 139: 15-24.
38. Cassola A, Frasch AC, (2009) An RNA recognition motif mediates the nucleocytoplasmic transport of a trypanosome RNA-binding protein. J Biol Chem 284: 35015-35028.
39. DaRocha WD, Otsu K, Teixeira SM, Donelson JE, (2004) Tests of cytoplasmic RNA interference (RNAi) and construction of a tetracycline-inducible T7 promoter system in Trypanosoma cruzi. Mol Biochem Parasitol 133: 175-186.
40. Ullu E, Tschudi C, Chakraborty T, (2004) RNA interference in protozoan parasites. Cell Microbiol 6: 509-519.
41. Okura M, Fang J, Salto ML, Singer RS, Docampo R, et al. (2005) A lipid-modified phosphoinositide-specific phospholipase C (TcPI-PLC) is involved in differentiation of trypomastigotes to amastigotes of Trypanosoma cruzi. J Biol Chem 280: 16235-16243.
42. Cougot N, Babajko S, Seraphin B, (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165: 31-40.