A 43-nucleotide U-rich element in 3′-untranslated region of large number of Trypanosoma cruzi transcripts is important for mRNA Abundance in intracellular amastigotes

Journal of Biological Chemistry

Volumn 287, Issue 23, 2012, Pages 19058-19069

  Li, Zhu Hong ^a   De Gaudenzi, Javier G ^c   Alvarez, Vanina E ^c   Mendiondo, Nicolás ^c   Wang, Haiming ^a   Kissinger, Jessica C ^a,b   Frasch, Alberto C ^c   Docampo, Roberto ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b Consejo Nacional de Investigaciones Científicas Y Técnicas ^*  (United States)

^c INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CHAGAS DISEASE; CO-IMMUNOPRECIPITATION EXPERIMENTS; COPY NUMBER; DIFFERENTIAL DISPLAY; GENE FAMILIES; GREEN FLUORESCENT PROTEIN; IN-VIVO; MRNA ABUNDANCES; NORTHERN BLOTS; PARASITE-; POST-TRANSCRIPTIONAL MECHANISMS; PROTEIN KINASE; REGULATION OF TRANSCRIPTION; REPORTER GENE; RIBONUCLEOPROTEIN COMPLEX; RNA-BINDING PROTEIN; RT-PCR ANALYSIS; TRANSCRIPT LEVEL; TRYPANOSOMA CRUZI; UNIDENTIFIED SEQUENCES; UNTRANSLATED REGIONS;

DISEASE CONTROL; GENES; POLYMERASE CHAIN REACTION; RNA; TRANSCRIPTION;

ENZYME ACTIVITY;

43 NUCLEOTIDE U RICH MRNA ELEMENT; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MUCIN ASSOCIATED PROTEIN; PROTEIN; PROTEIN KINASE; PROTEINASE; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SIALIDASE; SURFACE PROTEASE GP63; UBP1 PROTEIN; UNCLASSIFIED DRUG; URIDINE;

3' UNTRANSLATED REGION; AMASTIGOTE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DIFFERENTIAL DISPLAY RT PCR; EPIMASTIGOTE; GENE DOSAGE; GENOME ANALYSIS; IMMUNOPRECIPITATION; MULTIGENE FAMILY; MUTATION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN RNA BINDING; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; TRYPANOSOMA CRUZI;

3' UNTRANSLATED REGIONS; GENOME, PROTOZOAN; RNA, PROTOZOAN; RNA-BINDING PROTEINS; TRYPANOSOMA CRUZI;

TRYPANOSOMA CRUZI;

EID: 84861728364     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338699     Document Type: Article

References (52)

1. Minning, T. A., Weatherly, D. B., Atwood, J., 3rd, Orlando, R., and Tarleton, R. L. (2009) The steady state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 10, 370
2. Clayton, C. E. (2002) Life without transcriptional control? From fly to man and back again. EMBO J. 21, 1881-1888
3. Haile, S., and Papadopoulou, B. (2007) Developmental regulation of gene expression in trypanosomatid parasitic protozoa. Curr. Opin. Microbiol. 10, 569-577 (Pubitemid 350180594)
4. Palenchar, J. B., and Bellofatto, V. (2006) Gene transcription in trypanosomes. Mol. Biochem. Parasitol. 146, 135-141 (Pubitemid 43356354)
5. 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 (Pubitemid 36411966)
6. Jäger, A. V., De Gaudenzi, J. G., Cassola, A., D'Orso, I., and Frasch, A. C. (2007) mRNA maturation by two-step trans-splicing/polyadenylation processing in trypanosomes. Proc. Natl. Acad. Sci. U.S.A. 104, 2035-2042 (Pubitemid 46391348)
7. Nardelli, S. C., Avila, A. R., Freund, A., Motta, M. C., Manhães, L., de Jesus, T. C., Schenkman, S., Fragoso, S. P., Krieger, M. A., Goldenberg, S., and Dallagiovanna, B. (2007) Small-subunit rRNA processome proteins are translationally regulated during differentiation of Trypanosoma cruzi. Eukaryot. Cell 6, 337-345
8. Cassola, A., De Gaudenzi, J. G., and Frasch, A. C. (2007) Recruitment of mRNAsto cytoplasmic ribonucleoprotein granules in trypanosomes. Mol. Microbiol. 65, 655-670 (Pubitemid 47077240)
9. Holetz, F. B., Correa, A., Avila, A. R., Nakamura, C. V., Krieger, M. A., and Goldenberg, S. (2007) Evidence of P-body-like structures in Trypanosoma cruzi. Biochem. Biophys. Res. Commun. 356, 1062-1067 (Pubitemid 46529399)
10. Kramer, S., and Carrington, M. (2011) Trans-acting proteins regulating mRNA maturation, stability, and translation in trypanosomatids. Trends Parasitol. 27, 23-30
11. Hendriks, E. F., and Matthews, K. R. (2007) in Trypanosomes: After The Genome (Barry, D., McCulloch, R., Mottram, J., and Acosta-Serrano, A., eds) pp. 209-238, Horizon Bioscience, Norfolk, UK
12. De Gaudenzi, J. G., Noé, G., Campo, V. A., Frasch, A. C., and Cassola, A. (2011) Gene expression regulation in trypanosomatids. Essays Biochem. 51, 31-46
13. Keene, J. D., and Tenenbaum, S. A. (2002) Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9, 1161-1167
14. Keene, J. D. (2001) Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc. Natl. Acad. Sci. U.S.A. 98, 7018-7024
15. Keene, J. D. (2007) RNA regulons. Coordination of post-transcriptional events. Nat. Rev. Genet 8, 533-543
16. Mansfield, K. D., and Keene, J. D. (2009) The ribonome. A dominant force in co-ordinating gene expression. Biol. Cell 101, 169-181
17. Ouellette, M., and Papadopoulou, B. (2009) Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J. Biol. 8, 100
18. 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 (Pubitemid 34967463)
19. Schmatz, D. M., and Murray, P. K. (1982) Cultivation of Trypanosoma cruzi in irradiated muscle cells. Improved synchronization and enhanced trypomastigote production. Parasitology 85, 115-125 (Pubitemid 13229732)
20. Moreno, S. N., Silva, J., Vercesi, A. E., and Docampo, R. (1994) Cytosolic-free calcium elevation in Trypanosoma cruzi is required for cell invasion. J. Exp. Med. 180, 1535-1540 (Pubitemid 24289627)
21. Bone, G. J., and Steinert, M. (1956) Isotopes incorporated in the nucleic acids of Trypanosoma mega. Nature 178, 308-309
22. Caler, E. V., Vaena de Avalos, S., Haynes, P. A., Andrews, N. W., and Burleigh, B. A. (1998) Oligopeptidase B-dependent signaling mediates host cell invasion by Trypanosoma cruzi. EMBO J. 17, 4975-4986 (Pubitemid 28408464)
23. Bailey, T. L., and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28-36
24. Bailey, T. L., and Gribskov, M. (1998) Combining evidence using p values. Application to sequence homology searches. Bioinformatics 14, 48-54 (Pubitemid 28395676)
25. Jäger, A. V., Muiá, R. P., and Campetella, O. (2008) Stage-specific expression of Trypanosoma cruzi trans-sialidase involves highly conserved 3′-untranslated regions. FEMS Microbiol. Lett. 283, 182-188 (Pubitemid 351678575)
26. de Diego, J. L., Katz, J. M., Marshall, P., Gutiérrez, B., Manning, J. E., Nussenzweig, V., and González, J. (2001) The ubiquitin-proteasome pathway plays an essential role in proteolysis during Trypanosoma cruzi remodeling. Biochemistry 40, 1053-1062 (Pubitemid 32108598)
27. De Gaudenzi, J. G., D'Orso, I., and Frasch, A. C. (2003) RNA recognition motif-type RNA-binding proteins in Trypanosoma cruzi form a family involved in the interaction with specific transcripts in vivo. J. Biol. Chem. 278, 18884-18894 (Pubitemid 36799271)
28. Noé, G., De Gaudenzi, J. G., and Frasch, A. C. (2008) Functionally related transcripts have common RNA motifs for specific RNA-binding proteins in trypanosomes. BMC Mol. Biol. 9, 107
29. Li, Z. H., Alvarez, V. E., De Gaudenzi, J. G., Sant'Anna, C., Frasch, A. C., Cazzulo, J. J., and Docampo, R. (2011) Hyperosmotic stress induces aquaporin-dependent cell shrinkage, polyphosphate synthesis, amino acid accumulation, and global gene expression changes in Trypanosoma cruzi. J. Biol. Chem. 286, 43959-43971
30. Campos, P. C., Bartholomeu, D. C., DaRocha, W. D., Cerqueira, G. C., and Teixeira, S. M. (2008) Sequences involved in mRNA processing in Trypanosoma cruzi. Int. J. Parasitol. 38, 1383-1389
31. Bartholomeu, D. C., Cerqueira, G. C., Leão, A. C., daRocha, W. D., Pais, F. S., Macedo, C., Djikeng, A., Teixeira, S. M., and El-Sayed, N. M. (2009) Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res. 37, 3407-3417
32. El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D., Aggarwal, G., Tran, A. N., Ghedin, E., Worthey, E. A., Delcher, A. L., Blandin, G., Westenberger, S. J., Caler, E., Cerqueira, G. C., Branche, C., Haas, B., Anupama, A., Arner, E., Aslund, L., Attipoe, P., Bontempi, E., Bringaud, F., Burton, P., Cadag, E., Campbell, D. A., Carrington, M., Crabtree, J., Darban, H., da Silveira, J. F., de Jong, P., Edwards, K., Englund, P. T., Fazelina, G., Feldblyum, T., Ferella, M., Frasch, A. C., Gull, K., Horn, D., Hou, L., Huang, Y., Kindlund, E., Klingbeil, M., Kluge, S., Koo, H., Lacerda, D., Levin, M. J., Lorenzi, H., Louie, T., Machado, C. R., McCulloch, R., McKenna, A., Mizuno, Y., Mottram, J. C., Nelson, S., Ochaya, S., Osoegawa, K., Pai, G., Parsons, M., Pentony, M., Pettersson, U., Pop, M., Ramirez, J. L., Rinta, J., Robertson, L., Salzberg, S. L., Sanchez, D. O., Seyler, A., Sharma, R., Shetty, J., Simpson, A. J., Sisk, E., Tammi, M. T., Tarleton, R., Teixeira, S., Van Aken, S., Vogt, C., Ward, P. N., Wickstead, B., Wortman, J., White, O., Fraser, C. M., Stuart, K. D., and Andersson, B. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409-415
33. Liang, P., and Pardee, A. B. (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967-971
34. Frasch, A. C. (2000) Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol. Today 16, 282-286
35. De Gaudenzi, J., Frasch, A. C., and Clayton, C. (2005) RNA-binding domain proteins in Kinetoplastids. A comparative analysis. Eukaryot. Cell 4, 2106-2114 (Pubitemid 41798316)
36. Stern, M. Z., Gupta, S. K., Salmon-Divon, M., Haham, T., Barda, O., Levi, S., Wachtel, C., Nilsen, T. W., and Michaeli, S. (2009) Multiple roles for polypyrimidine tract binding (PTB) proteins in trypanosomeRNAmetabolism. RNA 15, 648-665
37. Caput, D., Beutler, B., Hartog, K., Thayer, R., Brown-Shimer, S., and Cerami, A. (1986) Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. U.S.A. 83, 1670-1674 (Pubitemid 16018626)
38. Khabar, K. S. (2005) The AU-rich transcriptome. More than interferons and cytokines, and its role in disease. J. Interferon Cytokine Res. 25, 1-10
39. Chen, C. Y., and Shyu, A. B. (1995) AU-rich elements. Characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470
40. Barreau, C., Paillard, L., and Osborne, H. B. (2005) AU-rich elements and associated factors. Are there unifying principles? Nucleic Acids Res. 33, 7138-7150 (Pubitemid 43125082)
41. Bakheet, T., Frevel, M., Williams, B. R., Greer, W., and Khabar, K. S. (2001) ARED. Human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res. 29, 246-254 (Pubitemid 32054460)
42. Di Noia, J. M., D'Orso, I., Sánchez, 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 (Pubitemid 30202078)
43. 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
44. 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
45. Tomlinson, S., Vandekerckhove, F., Frevert, U., and Nussenzweig, V. (1995) The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH. Parasitology 110, 547-554
46. 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 (Pubitemid 44742495)
47. 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
48. Archer, S. K., Luu, V. D., de Queiroz, R. A., Brems, S., and Clayton, C. (2009) Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathog 5, e1000565
49. Mao, Y., Najafabadi, H. S., and Salavati, R. (2009) Genome-wide computational identification of functional RNA elements in Trypanosoma brucei. BMC Genomics 10, 355
50. Archer, S. K., Inchaustegui, D., Queiroz, R., and Clayton, C. (2011) The cell cycle regulated transcriptome of Trypanosoma brucei. PLoS One 6, e18425
51. Bringaud, F., Müller, 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 (Pubitemid 47510282)
52. Aslett, M., Aurrecoechea, C., Berriman, M., Brestelli, J., Brunk, B. P., Carrington, M., Depledge, D. P., Fischer, S., Gajria, B., Gao, X., Gardner, M. J., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Hertz-Fowler, C., Houston, R., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Logan, F. J., Miller, J. A., Mitra, S., Myler, P. J., Nayak, V., Pennington, C., Phan, I., Pinney, D. F., Ramasamy, G., Rogers, M. B., Roos, D. S., Ross, C., Sivam, D., Smith, D. F., Srinivasamoorthy, G., Stoeckert, C. J., Jr., Subramanian, S., Thibodeau, R., Tivey, A., Treatman, C., Velarde, G., and Wang, H. (2010) TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res. 38, D457-462