Regulatory elements involved in the post-transcriptional control of stage-specific gene expression in trypanosoma cruzi - A review

Memorias do Instituto Oswaldo Cruz

Volumn 106, Issue 3, 2011, Pages 257-266

  Araújo, Patricia R ^a   Teixeira, Santuza M ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Gene expression; Mrna; Post transcriptional control; Trypanosoma cruzi

Indexed keywords

PROTOZOA; TRYPANOSOMA CRUZI;

EID: 79957942595     PISSN: 00740276     EISSN: 16788060     Source Type: Journal    
DOI: 10.1590/S0074-02762011000300002     Document Type: Review

References (95)

1. Abuin G, Freitas-Junior LH, Colli W, Alves MJ, Schenkman S 1999. 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 274: 13041-13047.
2. Alves LR, Avila AR, Correa A, Holetz FB, Mansur FC, Manque PA, de Menezes JP, Buck GA, Krieger MA, Goldenberg S 2010. Proteomic analysis reveals the dynamic association of proteins with translated mRNAs in Trypanosoma cruzi. Gene 452: 72-78.
3. Araújo PR, Burle-Caldas GA, Silva-Pereira RA, Bartholomeu DC, Darocha WD, Teixeira SM 2011. Development of a dual reporter system to identify regulatory cis-acting elements in untranslated regions of Trypanosoma cruzi mRNAs. Parasitol Int 60: 161-169.
4. Atayde VD, Neira I, Cortez M, Ferreira D, Freymüller E, Yoshida N 2004. Molecular basis of non-virulence of Trypanosoma cruzi clone CL-14. Int J Parasitol 34: 851-860.
5. Atwood JA 3rd, Weatherly DB, Minning TA, Bundy B, Cavola C, Opperdoes FR, Orlando R, Tarleton RL 2005. The Trypanosoma cruzi proteome. Science 309: 473-476.
6. Avila AR, Yamada-Ogatta SF, da Silva Monteiro V, Krieger MA, Nakamura CV, de Souza W, Goldenberg S 2001. Cloning and characterization of the metacyclogenin gene, which is specifically expressed during Trypanosoma cruzi metacyclogenesis. Mol Biochem Parasitol 117: 169-177.
7. Bartholomeu DC, Cerqueira GC, Leão AC, daRocha WD, Pais FS, Macedo C, Djikeng A, Teixeira SM, El-Sayed NM 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.
8. Bartholomeu DC, Silva RA, Galvão LM, el-Sayed NM, Donelson JE, Teixeira SM 2002. Trypanosoma cruzi: RNA structure and post-transcriptional control of tubulin gene expression. Exp Parasitol 102: 123-133.
9. Batista JA, Teixeira SM, Donelson JE, Kirchhoff LV, de Sá CM 1994. Characterization of a Trypanosoma cruzi poly(A)-binding protein and its genes. Mol Biochem Parasitol 67: 301-312.
10. Benz C, Nilsson D, Andersson B, Clayton C, Guilbride DL 2005. Messenger RNA processing sites in Trypanosoma brucei. Mol Biochem Parasitol 143: 125-134.
11. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Böhme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, Davies RM, Doggett J, Djikeng A, Feldblyum T, Field MC, Fraser A, Goodhead I, Hance Z, Harper D, Harris BR, Hauser H, Hostetler J, Ivens A, Jagels K, Johnson D, Johnson J, Jones K, Kerhornou AX, Koo H, Larke N, Landfear S, Larkin C, Leech V, Line A, Lord A, Macleod A, Mooney PJ, Moule S, Martin DM, Morgan GW, Mungall K, Norbertczak H, Ormond D, Pai G, Peacock CS, Peterson J, Quail MA, Rabbinowitsch E, Rajandream MA, Reitter C, Salzberg SL, Sanders M, Schobel S, Sharp S, Simmonds M, Simpson AJ, Tallon L, Turner CM, Tait A, Tivey AR, Van Aken S, Walker D, Wanless D, Wang S, White B, White O, Whitehead S, Woodward J, Wortman J, Adams MD, Embley TM, Gull K, Ullu E, Barry JD, Fairlamb AH, Opperdoes F, Barrell BG, Donelson JE, Hall N, Fraser CM, Melville SE, El-Sayed NM 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422.
12. Brandão A, Jiang T 2009. The composition of untranslated regions in Trypanosoma cruzi genes. Parasitol Int 58: 215-219.
13. Brener Z, Andrade ZA, Barral-Neto M 2000. Trypanosoma cruzi e doença de Chagas, 2nd ed., Guanabara Koogan, Rio de Janeiro, 431 pp.
14. Briones MR, Egima CM, Schenkman S 1995. Trypanosoma cruzi trans-sialidase gene lacking C-terminal repeats and expressed in epimastigote forms. Mol Biochem Parasitol 70: 9-17.
15. Buscaglia CA, Campo VA, Frasch AC, Di Noia JM 2006. Trypanosoma cruzi surface mucins: host-dependent coat diversity. Nat Rev Microbiol 4: 229-236.
16. Campos PC, Bartholomeu DC, DaRocha WD, Cerqueira GC, Teixeira SM 2008. Sequences involved in mRNA processing in Trypanosoma cruzi. Int J Parasitol 38: 1383-1389.
17. Cano MI, Gruber A, Vazquez M, Cortés A, Levin MJ, González A, Degrave W, Rondinelli E, Zingales B, Ramirez JL, Alonso C, Requena JM, Franco da Silveira J 1995. Molecular karyotype of clone CL Brener chosen for the Trypanosoma cruzi genome project. Mol Biochem Parasitol 71: 273-278.
18. Caro F, Bercovich N, Atorrasagasti C, Levin MJ, Vázquez MP 2006. Trypanosoma cruzi: analysis of the complete PUF RNA-binding protein family. Exp Parasitol 113: 112-124.
19. Cassola A, De Gaudenzi JG, Frasch AC 2007. Recruitment of mRNAs to cytoplasmic ribonucleoprotein granules in trypanosomes. Mol Microbiol 65: 655-670.
20. 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.
21. Cléry A, Blatter M, Allain FH 2008. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol 18: 290-298.
22. Coughlin BC, Teixeira SM, Kirchhoff LV, Donelson JE 2000. 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 275: 12051-12060.
23. Cremona ML, Sánchez DO, Frasch AC, Campetella O 1995. A single tyrosine differentiates active and inactive Trypanosoma cruzi trans-sialidases. Gene 160: 123-128.
24. Cribb P, Esteban L, Trochine A, Girardini J, Serra E 2010. Trypanosoma cruzi TBP shows preference for C/G-rich DNA sequences in vitro. Exp Parasitol 124: 346-349.
25. Cribb P, Serra E 2009. One- and two-hybrid analysis of the interactions between components of the Trypanosoma cruzi spliced leader RNA gene promoter binding complex. Int J Parasitol 39: 525-532.
26. da Silva RA, Bartholomeu DC, Teixeira SM 2006. Control mechanisms of tubulin gene expression in Trypanosoma cruzi. Int J Parasitol 36: 87-96.
27. Dallagiovanna B, Correa A, Probst CM, Holetz F, Smircich P, de Aguiar AM, Mansur F, da Silva CV, Mortara RA, Garat B, Buck GA, Goldenberg S, Krieger MA 2008. Functional genomic characterization of mRNAs associated with TcPUF6, a pumilio-like protein from Trypanosoma cruzi. J Biol Chem 283: 8266-8273.
28. Dallagiovanna B, Pérez L, Sotelo-Silveira J, Smircich P, Duhagon MA, Garat B 2005. Trypanosoma cruzi: molecular characterization of TcPUF6, a Pumilio protein. Exp Parasitol 109: 260-264.
29. 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.
30. de Carvalho EF, de Castro FT, Rondinelli E, Soares CM, Carvalho JF 1990. HSP 70 gene expression in Trypanosoma cruzi is regulated at different levels. J Cell Physiol 143: 439-444.
31. De Gaudenzi JG, D'Orso I, Frasch AC 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.
32. Di Noia JM, D'Orso I, Sánchez 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. Doniger T, Katz R, Wachtel C, Michaeli S, Unger R 2010. A comparative genome-wide study of ncRNAs in trypanosomatids. BMC Genomics 11: 615.
34. D'Orso I, Frasch AC 2001. TcUBP-1, a developmentally regulated U-rich RNA-binding protein involved in selective mRNA destabilization in trypanosomes. J Biol Chem 276: 34801-34809.
35. D'Orso I, Frasch AC 2002. TcUBP-1, an mRNA destabilizing factor from trypanosomes, homodimerizes and interacts with novel AU-rich element- and poly(A)-binding proteins forming a ribonucleoprotein complex. J Biol Chem 277: 50520-50528.
36. Edwards TA, Pyle SE, Wharton RP, Aggarwal AK 2001. Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell 105: 281-289.
37. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B 2005a. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
38. El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, Aggarwal G, Caler E, Renauld H, Worthey EA, Hertz-Fowler C, Ghedin E, Peacock C, Bartholomeu DC, Haas BJ, Tran AN, Wortman JR, Alsmark UC, Angiuoli S, Anupama A, Badger J, Bringaud F, Cadag E, Carlton JM, Cerqueira GC, Creasy T, Delcher AL, Djikeng A, Embley TM, Hauser C, Ivens AC, Kummerfeld SK, Pereira-Leal JB, Nilsson D, Peterson J, Salzberg SL, Shallom J, Silva JC, Sundaram J, Westenberger S, White O, Melville SE, Donelson JE, Andersson B, Stuart KD, Hall N 2005b. Comparative genomics of trypanosomatid parasitic protozoa. Science 309: 404-409.
39. Espinosa JM, Portal D, Lobo GS, Pereira CA, Alonso GD, Gómez EB, Lan GH, Pomar RV, Flawiá MM, Torres HN 2003. Trypanosoma cruzi poly-zinc finger protein: a novel DNA/RNA-binding CCHC-zinc finger protein. Mol Biochem Parasitol 131: 35-44.
40. Folgueira C, Martínez-Bonet M, Requena JM 2010. The Leishmania infantum PUF proteins are targets of the humoral response during visceral leishmaniasis. BMC Res Notes 3: 13.
41. Folgueira C, Requena JM 2007. A postgenomic view of the heat shock proteins in kinetoplastids. FEMS Microbiol Rev 31: 359-377.
42. Frasch AC 2000. Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today 16: 282-286.
43. García EA, Ziliani M, Agüero F, Bernabó G, Sánchez DO, Tekiel V 2010. TcTASV: a novel protein family in Trypanosoma cruzi identified from a subtractive trypomastigote cDNA library. PLoS Negl Trop Dis 4: e841.
44. Gentil LG, Cordero EM, do Carmo MS, dos Santos MR, da Silveira JF 2009. Posttranscriptional mechanisms involved in the control of expression of the stage-specific GP82 surface glycoprotein in Trypanosoma cruzi. Acta Trop 109: 152-158.
45. Gingerich TJ, Feige JJ, LaMarre J 2004. AU-rich elements and the control of gene expression through regulated mRNA stability. Anim Health Res Rev 5: 49-63.
46. Gonzalez-Pino MJ, Rangel-Aldao R, Slezynger TC 1997. Cloning and sequence analysis of a Trypanosoma cruzi alpha-tubulin cDNA. Biol Res 30: 161-166.
47. Gull K 2001. Protist tubulins: new arrivals, evolutionary relationships and insights to cytoskeletal function. Curr Opin Microbiol 4: 427-432.
48. Hartmann C, Hotz HR, McAndrew M, Clayton C 1998. Effect of multiple downstream splice sites on polyadenylation in Trypanosoma brucei. Mol Biochem Parasitol 93: 149-152.
49. Hellman K, Prohaska K, Williams N 2007. Trypanosoma brucei RNA binding proteins p34 and p37 mediate NOPP44/46 cellular localization via the exportin 1 nuclear export pathway. Eukaryot Cell 6: 2206-2213.
50. Holetz FB, Alves LR, Probst CM, Dallagiovanna B, Marchini FK, Manque P, Buck G, Krieger MA, Correa A, Goldenberg S 2010. Protein and mRNA content of TcDHH1-containing mRNPs in Trypanosoma cruzi. FEBS J 277: 3415-3426.
51. Holetz FB, Correa A, Avila AR, Nakamura CV, Krieger MA, Goldenberg S 2007. Evidence of P-body-like structures in Trypanosoma cruzi. Biochem Biophys Res Commun 356: 1062-1067.
52. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J, Dobson DE, Duesterhoeft A, Fazelina G, Fosker N, Frasch AC, Fraser A, Fuchs M, Gabel C, Goble A, Goffeau A, Harris D, Hertz-Fowler C, Hilbert H, Horn D, Huang Y, Klages S, Knights A, Kube M, Larke N, Litvin L, Lord A, Louie T, Marra M, Masuy D, Matthews K, Michaeli S, Mottram JC, Müller-Auer S, Munden H, Nelson S, Norbertczak H, Oliver K, O'neil S, Pentony M, Pohl TM, Price C, Purnelle B, Quail MA, Rabbinowitsch E, Reinhardt R, Rieger M, Rinta J, Robben J, Robertson L, Ruiz JC, Rutter S, Saunders D, Schäfer M, Schein J, Schwartz DC, Seeger K, Seyler A, Sharp S, Shin H, Sivam D, Squares R, Squares S, Tosato V, Vogt C, Volckaert G, Wambutt R, Warren T, Wedler H, Woodward J, Zhou S, Zimmermann W, Smith DF, Blackwell JM, Stuart KD, Barrell B, Myler PJ 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309: 436-442.
53. Jäger AV, Muiá RP, Campetella O 2008. Stage-specific expression of Trypanosoma cruzi trans-sialidase involves highly conserved 3' untranslated regions. FEMS Microbiol Lett 283: 182-188.
54. Junqueira C, Caetano B, Bartholomeu DC, Melo MB, Ropert C, Rodrigues MM, Gazzinelli RT 2010. The endless race between Trypanosoma cruzi and host immunity: lessons for and beyond Chagas disease. Expert Rev Mol Med 12: e29.
55. Kohl L, Gull K 1998. Molecular architecture of the trypanosome cytoskeleton. Mol Biochem Parasitol 93: 1-9.
56. Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S, Tschudi C 2010. The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 6: e1001090.
57. Kramer S, Carrington M 2011. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol 27: 23-30.
58. Kulkarni M, Ozgur S, Stoecklin G 2010. On track with P-bodies. Biochem Soc Trans 38: 242-251.
59. Liang XH, Haritan A, Uliel S, Michaeli S 2003. Trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot Cell 2: 830-840.
60. López-Estraño C, Tschudi C, Ullu E 1998. Exonic sequences in the 5' untranslated region of alpha-tubulin mRNA modulate trans splicing in Trypanosoma brucei. Mol Cell Biol 18: 4620-4628.
61. Luu VD, Brems S, Hoheisel JD, Burchmore R, Guilbride DL, Clayton C 2006. Functional analysis of Trypanosoma brucei PUF1. Mol Biochem Parasitol 150: 340-349.
62. Maingon R, Gerke R, Rodriguez M, Urbina J, Hoenicka J, Negri S, Aguirre T, Nehlin J, Knapp T, Crampton J 1988. The tubulin genes of Trypanosoma cruzi. Eur J Biochem 171: 285-291.
63. Maris C, Dominguez C, Allain FH 2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272: 2118-2131.
64. Martínez-Calvillo S, Nguyen D, Stuart K, Myler PJ 2004. Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot Cell 3: 506-517.
65. Martínez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ 2003. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11: 1291-1299.
66. McNicoll F, Drummelsmith J, Müller M, Madore E, Boilard N, Ouellette M, Papadopoulou B 2006. A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics 6: 3567-3581.
67. Minning TA, Weatherly DB, Atwood J 3rd, Orlando R, Tarleton RL 2009. The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi. BMC Genomics 10: 370.
68. Mörking PA, Dallagiovanna BM, Foti L, Garat B, Picchi GF, Umaki AC, Probst CM, Krieger MA, Goldenberg S, Fragoso SP 2004. TcZFP1: a CCCH zinc finger protein of Trypanosoma cruzi that binds poly-C oligoribonucleotides in vitro. Biochem Biophys Res Commun 319: 169-177.
69. Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L, Baerlocher L, Roditi I, Ochsenreiter T 2010. Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 6: e1001037.
70. Noé G, De Gaudenzi JG, Frasch AC 2008. Functionally related transcripts have common RNA motifs for specific RNA-binding proteins in trypanosomes. BMC Mol Biol 9: 107.
71. Nogales E, Whittaker M, Milligan RA, Downing KH 1999. High-resolution model of the microtubule. Cell 96: 79-88.
72. Nozaki T, Cross GA 1995. Effects of 3' untranslated and intergenic regions on gene expression in Trypanosoma cruzi. Mol Biochem Parasitol 75: 55-67.
73. Pais FS, DaRocha WD, Almeida RM, Leclercq SY, Penido ML, Fragoso SP, Bartholomeu DC, Gazzinelli RT, Teixeira SM 2008. Molecular characterization of ribonucleoproteic antigens containing repeated amino acid sequences from Trypanosoma cruzi. Microbes Infect 10: 716-725.
74. Palenchar JB, Bellofatto V 2006. Gene transcription in trypanosomes. Mol Biochem Parasitol 146: 135-141.
75. Pérez-Díaz L, Duhagon MA, Smircich P, Sotelo-Silveira J, Robello C, Krieger MA, Goldenberg S, Williams N, Dallagiovanna B, Garat B 2007. Trypanosoma cruzi: molecular characterization of an RNA binding protein differentially expressed in the parasite life cycle. Exp Parasitol 117: 99-105.
76. Quenault T, Lithgow T, Traven A 2011. PUF proteins: repression, activation and mRNA localization. Trends Cell Biol 21: 104-112.
77. Requena JM, Jimenez-Ruiz A, Soto M, Assiego R, Santarén JF, Lopez MC, Patarroyo ME, Alonso C 1992. Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Mol Biochem Parasitol 53: 201-211.
78. Rodrigues DC, Silva R, Rondinelli E, Urményi TP 2010. Trypanosoma cruzi: modulation of HSP70 mRNA stability by untranslated regions during heat shock. Exp Parasitol 126: 245-253.
79. Rondinelli E, de Moura-Neto RS, Silva R, de Almeida Soares CM, Carvalho JF, Torres de Castro F 1986. Control of tubulin gene expression during metacyclogenesis of Trypanosoma cruzi. FEBS Lett 208: 379-385.
80. Siegel TN, Hekstra DR, Wang X, Dewell S, Cross GA 2010. Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res 38: 4946-4957.
81. Smith M, Blanchette M, Papadopoulou B 2008. Improving the prediction of mRNA extremities in the parasitic protozoan Leishmania. BMC Bioinformatics 9: 158.
82. Soares CM, de Carvalho EF, Urményi TP, Carvalho JF, de Castro FT, Rondinelli E 1989. Alpha- and beta-tubulin mRNAs of Trypanosoma cruzi originate from a single multicistronic transcript. FEBS Lett 250: 497-502.
83. Songthamwat D, Kajihara K, Kikuchi M, Uemura H, Tran SP, Yanagi T, Higo H, Hirayama K 2007. Structure and expression of three gp82 gene subfamilies of Trypanosoma cruzi. Parasitol Int 56: 273-280.
84. Teixeira SM, daRocha WD 2003. Control of gene expression and genetic manipulation in the Trypanosomatidae. Genet Mol Res 2: 148-158.
85. Teixeira SM, Kirchhoff LV, Donelson JE 1995. Post-transcriptional elements regulating expression of mRNAs from the amastin/tuzin gene cluster of Trypanosoma cruzi. J Biol Chem 270: 22586-22594.
86. Teixeira SM, Russell DG, Kirchhoff LV, Donelson JE 1994. A differentially expressed gene family encoding "amastin", a surface protein of Trypanosoma cruzi amastigotes. J Biol Chem 269: 20509-20516.
87. Tibbetts RS, Jensen JL, Olson CL, Wang FD, Engman DM 1998. The DnaJ family of protein chaperones in Trypanosoma cruzi. Mol Biochem Parasitol 91: 319-326.
88. Urményi 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.
89. Vargas N, Pedroso A, Zingales B 2004. Chromosomal polymorphism, gene synteny and genome size in T. cruzi I and T. cruzi II groups. Mol Biochem Parasitol 138: 131-141.
90. Wang X, Zamore PD, Hall TM 2001. Crystal structure of a Pumilio homology domain. Mol Cell 7: 855-865.
91. Weatherly DB, Boehlke C, Tarleton RL 2009. Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10: 255.
92. Weston D, La Flamme AC, Van Voorhis WC 1999. 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 102: 53-66.
93. Wickens M, Bernstein DS, Kimble J, Parker R 2002. A PUF family portrait: 3'UTR regulation as a way of life. Trends Genet 18: 150-157.
94. Xu P, Wen L, Benegal G, Wang X, Buck GA 2001. Identification of a spliced leader RNA binding protein from Trypanosoma cruzi. Mol Biochem Parasitol 112: 39-49.
95. Yoshida N, Favoreto S Jr, Ferreira AT, Manque PM 2000. Signal transduction induced in Trypanosoma cruzi metacyclic trypomastigotes during the invasion of mammalian cells. Braz J Med Biol Res 33: 269-278.