Implication of CA repeated tracts on post-transcriptional regulation in trypanosoma cruzi

Experimental Parasitology

Volumn 134, Issue 4, 2013, Pages 511-518

  Pastro, Lucía ^a,b   Smircich, Pablo ^a,b   Pérez Díaz, Leticia ^a   Duhagon, María Ana ^a,b   Garat, Beatriz ^a  

^a Facultad de Ciencias   (Uruguay)

^b Facultad de Ciencias   (Uruguay)

Author keywords

MRNA stability; MRNA steady state; Polydinucleotides; Reporter assay; RNA conformation; UTR

Indexed keywords

MESSENGER RNA; MUCINE ASSOCIATED PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; AMASTIGOTE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; DINUCLEOTIDE REPEAT; EPIMASTIGOTE; GENE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INSERTION; GENE STRUCTURE; GENETIC ANALYSIS; LIFE CYCLE; MULTIGENE FAMILY; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REPORTER GENE; STEADY STATE; TRANSCRIPTION REGULATION; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; UNTRANSLATED REGION;

MRNA STABILITY; MRNA STEADY STATE; POLYDINUCLEOTIDES; REPORTER ASSAY; RNA CONFORMATION; UTR;

CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DINUCLEOTIDE REPEATS; GENE EXPRESSION REGULATION; GENES, REPORTER; NUCLEIC ACID CONFORMATION; POLY A; POLY C; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, PROTOZOAN; TRYPANOSOMA CRUZI; UNTRANSLATED REGIONS;

TRYPANOSOMA CRUZI;

EID: 84879594068     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2013.04.004     Document Type: Article

References (55)

1. Abuin G., Freitas-Junior L.H., Colli W., Alves M.J., Schenkman S. Expression of trans-sialidase and 85-kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post-transcriptional level by labile protein factors. J. Biol. Chem. 1999, 274:13041-13047.
2. Araujo P.R., Burle-Caldas G.A., Silva R.A., Bartolomeu D.C., Darocha W.D., Teixeira S.M. Development of a dual reporter system to identify regulatory cis-acting elements in untranslated regions of Trypanosoma cruzi mRNAs. Parasitol Int. 2011, 60:161-169.
3. Avila A.R., Yamada-Ogatta S.F., da Silva Monteiro V., Krieger M.A., Nakamura C.V., de Souza W., Goldenberg S. Cloning and characterization of the metacyclogenin gene, which is specifically expressed during Trypanosoma cruzi metacyclogenesis. Mol. Biochem. Parasitol. 2001, 117:169-177.
4. Baranovskaya S., Martin Y., Alonso S., Pisarchuk K.L., Falchetti M., Dai Y., Khaldoyanidi S., Krajewski S., Novikova I., Sidorenko Y.S., Perucho M., Malkhosyan S.R. Down-regulation of epidermal growth factor receptor by selective expansion of a 5'-end regulatory dinucleotide repeat in colon cancer with microsatellite instability. Clin. Cancer Res. 2009, 15:4531-4537.
5. Bartholomeu D.C., Cerqueira G.C., Leao A.C., daRocha W.D., Pais F.S., Macedo C., Djikeng A., Teixeira S.M., El-Sayed N.M. Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res. 2009, 37:3407-3417.
6. Bartholomeu D.C., Silva R.A., Galvao L.M., el-Sayed N.M., Donelson J.E., Teixeira S.M. Trypanosoma cruzi: RNA structure and post-transcriptional control of tubulin gene expression. Exp. Parasitol. 2002, 102:123-133.
7. Buisine M.P., Wacrenier A., Mariette C., Leteurtre E., Escande F., Aissi S., Ketele A., Leclercq A., Porchet N., Lesuffleur T. Frequent mutations of the CA simple sequence repeat in intron 1 of EGFR in mismatch repair-deficient colorectal cancers. World J. Gastroenterol. 2008, 14:1053-1059.
8. Buratti E., Dork T., Zuccato E., Pagani F., Romano M., Baralle F.E. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 2001, 20:1774-1784.
9. Campos P.C., Bartholomeu D.C., DaRocha W.D., Cerqueira G.C., Teixeira S.M. Sequences involved in mRNA processing in Trypanosoma cruzi. Int. J. Parasitol. 2008, 38:1383-1389.
10. Clayton C. Repetitive elements in parasitic protozoa. BMC Biol. 2010, 8:64.
11. Coderre J.A., Beverley S.M., Schimke R.T., Santi D.V. Overproduction of a bifunctional thymidylate synthetase-dihydrofolate reductase and DNA amplification in methotrexate-resistant Leishmania tropica. Proc. Natl. Acad. Sci. USA 1983, 80:2132-2136.
12. Contreras V.T., Araujo-Jorge T.C., Bonaldo M.C., Thomaz N., Barbosa H.S., Meirelles Mde N., Goldenberg S. Biological aspects of the Dm 28c clone of Trypanosoma cruzi after metacyclogenesis in chemically defined media. Mem. Inst. Oswaldo Cruz 1988, 83:123-133.
13. Contreras V.T., Morel C.M., Goldenberg S. Stage specific gene expression precedes morphological changes during Trypanosoma cruzi metacyclogenesis. Mol. Biochem. Parasitol. 1985, 14:83-96.
14. Coughlin B.C., Teixeira S.M., Kirchhoff L.V., Donelson J.E. Amastin mRNA abundance in Trypanosoma cruzi is controlled by a 3'-untranslated region position-dependent cis-element and an untranslated region-binding protein. J. Biol. Chem. 2000, 275:12051-12060.
15. Chagas C. Nova tripanozomiaze humana. Estudos sobre a morfologia e o ciclo evolutivo do Schizotrypanum cruzi, agente etiologico da nova entidade mórbida do homen. Mem. Inst. Oswaldo Cruz 1909, 1:159-219.
16. Chiribao M.L., Libisch M.G., Osinaga E., Parodi-Talice A., Robello C. Cloning, localization and differential expression of the Trypanosoma cruzi TcOGNT-2 glycosyl transferase. Gene 2012, 498:147-154.
17. D'Orso I., De Gaudenzi J.G., Frasch A.C. RNA-binding proteins and mRNA turnover in trypanosomes. Trends Parasitol. 2003, 19:151-155.
18. D'Orso I., Frasch A.C. 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. 2001, 276:15783-15793.
19. da Silva R.A., Bartholomeu D.C., Teixeira S.M. Control mechanisms of tubulin gene expression in Trypanosoma cruzi. Int. J. Parasitol. 2006, 36:87-96.
20. De Gaudenzi J.G., Noe G., Campo V.A., Frasch A.C., Cassola A. Gene expression regulation in trypanosomatids. Essays Biochem. 2011, 51:31-46.
21. Di Noia J.M., D'Orso I., Sanchez D.O., Frasch A.C. 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. 2000, 275:10218-10227.
22. Duhagon M.A., Dallagiovanna B., Garat B. Unusual features of poly[dT-dG].[dC-dA] stretches in CDS-flanking regions of Trypanosoma cruzi genome. Biochem. Biophys. Res. Commun. 2001, 287:98-103.
23. Duhagon M.A., Pastro L., Sotelo-Silveira J.R., Perez-Diaz L., Maugeri D., Nardelli S.C., Schenkman S., Williams N., Dallagiovanna B., Garat B. The Trypanosoma cruzi nucleic acid binding protein Tc38 presents changes in the intramitochondrial distribution during the cell cycle. BMC Microbiol. 2009, 9:34.
24. Duhagon M.A., Smircich P., Forteza D., Naya H., Williams N., Garat B. Comparative genomic analysis of dinucleotide repeats in Tritryps. Gene 2011, 487:29-37.
25. Gabellini N. A polymorphic GT repeat from the human cardiac Na+Ca2+ exchanger intron 2 activates splicing. Eur. J. Biochem. 2001, 268:1076-1083.
26. Gendrel C.G., Boulet A., Dutreix M. (CA/GT)(n) microsatellites affect homologous recombination during yeast meiosis. Genes Dev. 2000, 14:1261-1268.
27. Gentil L.G., Cordero E.M., do Carmo M.S., dos Santos M.R., Silveira J.F. Posttranscriptional mechanisms involved in the control of expression of the stage-specific GP82 surface glycoprotein in Trypanosoma cruzi. Acta Trop. 2009, 109:152-158.
28. Jager A.V., Muia R.P., Campetella O. Stage-specific expression of Trypanosoma cruzi trans-sialidase involves highly conserved 3' untranslated regions. FEMS Microbiol. Lett. 2008, 283:182-188.
29. Keene J.D. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8:533-543.
30. Kelly J.M., Ward H.M., Miles M.A., Kendall G. A shuttle vector which facilitates the expression of transfected genes in Trypanosoma cruzi and Leishmania. Nucleic Acids Res. 1992, 20:3963-3969.
31. Kramer S. Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol. Biochem. Parasitol. 2012, 181:61-72.
32. Kramer S., Carrington M. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol. 2011, 27:23-30.
33. Lee J.H., Jeon M.H., Seo Y.J., Lee Y.J., Ko J.H., Tsujimoto Y. CA repeats in the 3'-untranslated region of bcl-2 mRNA mediate constitutive decay of bcl-2 mRNA. J. Biol. Chem. 2004, 279:42758-42764.
34. Li Z.H., De Gaudenzi J.G., Alvarez V.E., Mendiondo N., Wang H., Kissinger J., Frasch A.C., Docampo R. A 43-nt U-rich element in the 3'untranslated region of a large number of Trypanosoma cruzi transcripts is important for mRNA abundance in intracellular amastigotes. J Biol Chem. 2012, 287:19058-19069.
35. Lin Z., Thomas N.J., Wang Y., Guo X., Seifart C., Shakoor H., Floros J. Deletions within a CA-repeat-rich region of intron 4 of the human SP-B gene affect mRNA splicing. Biochem. J. 2005, 389:403-412.
36. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
37. Majewski J., Ott J. GT repeats are associated with recombination on human chromosome 22. Genome Res. 2000, 10:1108-1114.
38. Martin-Farmer J., Janssen G.R. A downstream CA repeat sequence increases translation from leadered and unleadered mRNA in Escherichia coli. Mol. Microbiol. 1999, 31:1025-1038.
39. Martinez-Calvillo S., Vizuet-de-Rueda J.C., Florencio-Martinez L.E., Manning-Cela R.G., Figueroa-Angulo E.E. Gene expression in trypanosomatid parasites. J. Biomed. Biotechnol. 2010, 2010:525241.
40. Minning T.A., Weatherly D.B., Atwood J., Orlando R., Tarleton R.L. The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 2009, 10:370.
41. Noe G., De Gaudenzi J.G., Frasch A.C. Functionally related transcripts have common RNA motifs for specific RNA-binding proteins in trypanosomes. BMC Mol. Biol. 2008, 9:107.
42. Nozaki T., Cross G.A. Effects of 3' untranslated and intergenic regions on gene expression in Trypanosoma cruzi. Mol. Biochem. Parasitol. 1995, 75:55-67.
43. Perez-Diaz L., Duhagon M.A., Smircich P., Sotelo-Silveira J., Robello C., Krieger M.A., Goldenberg S., Williams N., Dallagiovanna B., Garat B. Trypanosoma cruzi: molecular characterization of an RNA binding protein differentially expressed in the parasite life cycle. Exp. Parasitol. 2007, 117:99-105.
44. Queiroz R., Benz C., Fellenberg K., Hoheisel J.D., Clayton C. Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics 2009, 10:495.
45. Rattenbacher B., Bohjanen P.R. Evaluating posttranscriptional regulation of cytokine genes. Methods Mol. Biol. 2012, 820:71-89.
46. Rockman M.V., Wray G.A. Abundant raw material for cis-regulatory evolution in humans. Mol. Biol. Evol. 2002, 19:1991-2004.
47. Rodrigues D.C., Silva R., Rondinelli E., Urmenyi T.P. Trypanosoma cruzi: modulation of HSP70 mRNA stability by untranslated regions during heat shock. Exp. Parasitol. 2010, 126:245-253.
48. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
49. Sinden R. DNA Structure and Function 1994, Academic Press, San Diego.
50. Songthamwat D., Kajihara K., Kikuchi M., Uemura H., Tran S.P., Yanagi T., Higo H., Hirayama K. Structure and expression of three gp82 gene subfamilies of Trypanosoma cruzi. Parasitol. Int. 2007, 56:273-280.
51. Suganuma K., Yamasaki S., Asada M., Kawazu S., Inoue N. The epimastigote stage-specific gene expression of CESP is tightly regulated by its 3' UTR. Mol. Biochem. Parasitol. 2012, 186:77-80.
52. Teixeira S.M., Russell D.G., Kirchhoff L.V., Donelson J.E. A differentially expressed gene family encoding "amastin", a surface protein of Trypanosoma cruzi amastigotes. J. Biol. Chem. 1994, 269:20509-20516.
53. Tyler K.M., Engman D.M. The life cycle of Trypanosoma cruzi revisited. Int. J. Parasitol. 2001, 31:472-481.
54. Weston D., La Flamme A.C., Van Voorhis W.C. Expression of Trypanosoma cruzi surface antigen FL-160 is controlled by elements in the 3' untranslated, the 3' intergenic, and the coding regions. Mol. Biochem. Parasitol. 1999, 102:53-66.
55. Zhao W., Blagev D., Pollack J.L., Erle D.J. Toward a systematic understanding of mRNA 3' untranslated regions. Proc. Am. Thorac. Soc. 2011, 8:163-166.