Nucleolar localization of RNA binding proteins induced by Actinomycin D and heat shock in Trypanosoma cruzi

PLoS ONE

Volumn 6, Issue 5, 2011, 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

DACTINOMYCIN; MESSENGER RNA; POLYADENYLIC ACID; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE DELETION; GENETIC TRANSCRIPTION; HEAT SHOCK; NONHUMAN; NUCLEOLUS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RNA METABOLISM; TRYPANOSOMA CRUZI; DRUG EFFECT; METABOLISM;

EUKARYOTA; TRYPANOSOMA CRUZI;

CELL NUCLEOLUS; DACTINOMYCIN; PROTEIN TRANSPORT; RNA-BINDING PROTEINS; TRYPANOSOMA CRUZI;

EID: 79956367094     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019920     Document Type: Article

References (66)

1. Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, et al. (2003) The trypanosomiases. Lancet 362: 1469-1480.
2. Kedzierski L Leishmaniasis Vaccine: Where are We Today? J Glob Infect Dis 2: 177-185.
3. Tyler KM, Engman DM, (2001) The life cycle of Trypanosoma cruzi revisited. Int J Parasitol 31: 472-481.
4. Clayton C, Shapira M, (2007) Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156: 93-101.
5. Lee MG, Van der Ploeg LH, (1997) Transcription of protein-coding genes in trypanosomes by RNA polymerase I. Annu Rev Microbiol 51: 463-489.
6. Anderson P, Kedersha N, (2006) RNA granules. J Cell Biol 172: 803-808.
7. 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.
8. Cassola A, De Gaudenzi JG, Frasch AC, (2007) Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol Microbiol 65: 655-670.
9. 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.
10. 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.
11. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI, (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8: 574-585.
12. 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.
13. Olson MO, (2004) Sensing cellular stress: another new function for the nucleolus? Sci STKE 2004: pe10.
14. 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.
15. Fox AH, Lam YW, Leung AK, Lyon CE, Andersen J, et al. (2002) Paraspeckles: a novel nuclear domain. Curr Biol 12: 13-25.
16. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, et al. (2005) Nucleolar proteome dynamics. Nature 433: 77-83.
17. Brown JW, Shaw PJ, Shaw P, Marshall DF, (2005) Arabidopsis nucleolar protein database (AtNoPDB). Nucleic Acids Res 33: D633-636.
18. Lopez-Velazquez G, Hernandez R, Lopez-Villasenor I, Reyes-Vivas H, Segura-Valdez Mde L, et al. (2005) Electron microscopy analysis of the nucleolus of Trypanosoma cruzi. Microsc Microanal 11: 293-299.
19. Nepomuceno-Mejia T, Lara-Martinez R, Cevallos AM, Lopez-Villasenor I, Jimenez-Garcia LF, et al. The Trypanosoma cruzi nucleolus: a morphometrical analysis of cultured epimastigotes in the exponential and stationary phases. FEMS Microbiol Lett 313: 41-46.
20. Barth S, Shalem B, Hury A, Tkacz ID, Liang XH, et al. (2008) Elucidating the role of C/D snoRNA in rRNA processing and modification in Trypanosoma brucei. Eukaryot Cell 7: 86-101.
21. Elias MCQB, Marques-Porto R, Freymuller E, Schenkman S, (2001) Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Molecular and Biochemical Parasitology 112: 79-90.
22. Gluenz E, Taylor MC, Kelly JM, (2007) The Trypanosoma cruzi metacyclic-specific protein Met-III associates with the nucleolus and contains independent amino and carboxyl terminal targeting elements. Int J Parasitol 37: 617-625.
23. Zhong XY, Wang P, Han J, Rosenfeld MG, Fu XD, (2009) SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol Cell 35: 1-10.
24. Lin S, Fu XD, (2007) SR proteins and related factors in alternative splicing. Adv Exp Med Biol 623: 107-122.
25. Laird PW, ten Asbroek AL, Borst P, (1987) Controlled turnover and 3′ trimming of the trans splicing precursor of Trypanosoma brucei. Nucleic Acids Res 15: 10087-10103.
26. Durand-Dubief M, Bastin P, (2003) TbAGO1, an argonaute protein required for RNA interference, is involved in mitosis and chromosome segregation in Trypanosoma brucei. BMC Biol 1: 2.
27. Li Z, Wang CC, (2006) Changing roles of aurora-B kinase in two life cycle stages of Trypanosoma brucei. Eukaryot Cell 5: 1026-1035.
28. Elias MC, Marques-Porto R, Freymuller E, Schenkman S, (2001) Transcription rate modulation through the Trypanosoma cruzi life cycle occurs in parallel with changes in nuclear organisation. Mol Biochem Parasitol 112: 79-90.
29. McNally KP, Agabian N, (1992) Trypanosoma brucei spliced-leader RNA methylations are required for trans splicing in vivo. Mol Cell Biol 12: 4844-4851.
30. Schwede A, Manful T, Jha BA, Helbig C, Bercovich N, et al. (2009) The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res 37: 5511-5528.
31. Dossin F de M, Schenkman S, (2005) Actively transcribing RNA polymerase II concentrates on spliced leader genes in the nucleus of Trypanosoma cruzi. Eukaryot Cell 4: 960-970.
32. De Gaudenzi J, Frasch AC, Clayton C, (2005) RNA-binding domain proteins in Kinetoplastids: a comparative analysis. Eukaryot Cell 4: 2106-2114.
33. Batista JA, Teixeira SM, Donelson JE, Kirchhoff LV, de Sa CM, (1994) Characterization of a Trypanosoma cruzi poly(A)-binding protein and its genes. Mol Biochem Parasitol 67: 301-312.
34. Stern MZ, Gupta SK, Salmon-Divon M, Haham T, Barda O, et al. (2009) Multiple roles for polypyrimidine tract binding (PTB) proteins in trypanosome RNA metabolism. Rna 15: 648-665.
35. Foldynova-Trantirkova S, Paris Z, Sturm NR, Campbell DA, Lukes J, (2005) The Trypanosoma brucei La protein is a candidate poly(U) shield that impacts spliced leader RNA maturation and tRNA intron removal. Int J Parasitol 35: 359-366.
36. Avila ML, Bercovich N, Westergaard G, Levin MJ, Vazquez MP, (2007) Mapping of the protein-binding interface between splicing factors SF3b155 and p14 of Trypanosoma cruzi. Biochem Biophys Res Commun 364: 26-32.
37. Bercovich N, Levin MJ, Vazquez MP, (2009) The FIP-1 like polyadenylation factor in trypanosomes and the structural basis for its interaction with CPSF30. Biochem Biophys Res Commun 380: 850-855.
38. Wurst M, Robles A, Po J, Luu VD, Brems S, et al. (2009) An RNAi screen of the RRM-domain proteins of Trypanosoma brucei. Mol Biochem Parasitol 163: 61-65.
39. Martin F, Requena JM, Martin J, Alonso C, Lopez MC, (1993) Cytoplasmic-nuclear translocation of the Hsp70 protein during environmental stress in Trypanosoma cruzi. Biochem Biophys Res Commun 196: 1155-1162.
40. Metz A, Soret J, Vourc'h C, Tazi J, Jolly C, (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117: 4551-4558.
41. Pelham HR, (1984) Hsp70 accelerates the recovery of nucleolar morphology after heat shock. Embo J 3: 3095-3100.
42. Welch WJ, Feramisco JR, (1984) Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. J Biol Chem 259: 4501-4513.
43. Schwoebel ED, Ho TH, Moore MS, (2002) The mechanism of inhibition of Ran-dependent nuclear transport by cellular ATP depletion. J Cell Biol 157: 963-974.
44. Shulga N, Roberts P, Gu Z, Spitz L, Tabb MM, et al. (1996) In vivo nuclear transport kinetics in Saccharomyces cerevisiae: a role for heat shock protein 70 during targeting and translocation. J Cell Biol 135: 329-339.
45. Marchetti MA, Tschudi C, Kwon H, Wolin SL, Ullu E, (2000) Import of proteins into the trypanosome nucleus and their distribution at karyokinesis. J Cell Sci 113 (Pt 5): 899-906.
46. Xie J, Lee JA, Kress TL, Mowry KL, Black DL, (2003) Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc Natl Acad Sci U S A 100: 8776-8781.
47. Misteli T, Caceres JF, Spector DL, (1997) The dynamics of a pre-mRNA splicing factor in living cells. Nature 387: 523-527.
48. Le H, Browning KS, Gallie DR, (2000) The phosphorylation state of poly(A)-binding protein specifies its binding to poly(A) RNA and its interaction with eukaryotic initiation factor (eIF) 4F, eIFiso4F, and eIF4B. J Biol Chem 275: 17452-17462.
49. Savaldi-Goldstein S, Sessa G, Fluhr R, (2000) The ethylene-inducible PK12 kinase mediates the phosphorylation of SR splicing factors. Plant J 21: 91-96.
50. Yeakley JM, Tronchere H, Olesen J, Dyck JA, Wang HY, et al. (1999) Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors. J Cell Biol 145: 447-455.
51. Cohen P, Holmes CF, Tsukitani Y, (1990) Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem Sci 15: 98-102.
52. Hidaka H, Kobayashi R, (1992) Pharmacology of protein kinase inhibitors. Annu Rev Pharmacol Toxicol 32: 377-397.
53. Misteli T, Spector DL, (1996) Serine/threonine phosphatase 1 modulates the subnuclear distribution of pre-mRNA splicing factors. Mol Biol Cell 7: 1559-1572.
54. Kruhlak MJ, Lever MA, Fischle W, Verdin E, Bazett-Jones DP, et al. (2000) Reduced mobility of the alternate splicing factor (ASF) through the nucleoplasm and steady state speckle compartments. J Cell Biol 150: 41-51.
55. Weingartner M, Binarova P, Drykova D, Schweighofer A, David JP, et al. (2001) Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell 13: 1929-1943.
56. Ali GS, Golovkin M, Reddy AS, (2003) Nuclear localization and in vivo dynamics of a plant-specific serine/arginine-rich protein. Plant J 36: 883-893.
57. Lindquist S, (1986) The heat-shock response. Annu Rev Biochem 55: 1151-1191.
58. Weighardt F, Cobianchi F, Cartegni L, Chiodi I, Villa A, et al. (1999) A novel hnRNP protein (HAP/SAF-B) enters a subset of hnRNP complexes and relocates in nuclear granules in response to heat shock. J Cell Sci 112: 1465-1476.
59. Biamonti G, Vourc'h C, (2010) Nuclear stress bodies. Cold Spring Harb Perspect Biol 2: a000695.
60. De Carvalho EF, De Castro FT, Rondinelli E, Carvalho JF, (1994) Physiological aspects of Trypanosoma cruzi gene regulation during heat-shock. Biol Res 27: 225-231.
61. Karni-Schmidt O, Zupnick A, Castillo M, Ahmed A, Matos T, et al. (2008) p53 is localized to a sub-nucleolar compartment after proteasomal inhibition in an energy-dependent manner. J Cell Sci 121: 4098-4105.
62. Tillemans V, Dispa L, Remacle C, Collinge M, Motte P, (2005) Functional distribution and dynamics of Arabidopsis SR splicing factors in living plant cells. Plant J 41: 567-582.
63. Cazalla D, Zhu J, Manche L, Huber E, Krainer AR, et al. (2002) Nuclear export and retention signals in the RS domain of SR proteins. Mol Cell Biol 22: 6871-6882.
64. Gama-Carvalho M, Krauss RD, Chiang L, Valcarcel J, Green MR, et al. (1997) Targeting of U2AF65 to sites of active splicing in the nucleus. J Cell Biol 137: 975-987.
65. Tillemans V, Leponce I, Rausin G, Dispa L, Motte P, (2006) Insights into Nuclear Organization in Plants as Revealed by the Dynamic Distribution of Arabidopsis SR Splicing Factors. Plant Cell 18: 3218-3234.
66. Kelly JM, Ward HM, Miles MA, Kendall G, (1992) A shuttle vector which facilitates the expression of transfected genes in Trypanosoma cruzi and Leishmania. Nucleic Acids Res 20: 3963-3969.