Developmental regulation of gene expression in trypanosomatid parasitic protozoa

Current Opinion in Microbiology

Volumn 10, Issue 6, 2007, Pages 569-577

  Haile, Simon ^a,b   Papadopoulou, Barbara ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTE; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; LEISHMANIA BRAZILIENSIS; LEISHMANIA INFANTUM; LEISHMANIA MAJOR; NONHUMAN; REVIEW; RNA DEGRADATION; RNA SPLICING; RNA TRANSCRIPTION; RNA TRANSLATION; TRYPANOSOMA BRUCEI;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; PROTOZOAN PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, PROTOZOAN; TRYPANOSOMATINA;

EUKARYOTA; KINETOPLASTIDA; PROTOZOA; TRYPANOSOMATIDAE;

EID: 36549005184     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2007.10.001     Document Type: Review

References (60)

1. El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., Caler E., Renauld H., Worthey E.A., Hertz-Fowler C., et al. Comparative genomics of trypanosomatid parasitic protozoa. Science 309 (2005) 404-409. This study provides information about sequence comparison between Trypanosoma spp. and L. major genomes that highlighted large syntenic polycistronic gene clusters but also important differences in gene content and organization.
2. Smith D.F., Peacock C.S., and Cruz A.K. Comparative genomics: From genotype to disease phenotype in the leishmaniases. Int J Parasitol 37 (2007) 1173-1186
3. Peacock C.S., Seeger K., Harris D., Murphy L., Ruiz J.C., Quail M.A., Peters N., Adlem E., Tivey A., Aslett M., et al. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39 (2007) 839-847. This paper reports the sequencing of L. infantum and L. braziliensis and the comparison of these sequences with the published genome of L. major. This bioinformatic analysis revealed marked conservation of synteny and identified putative species-specific genes.
4. McNicoll F., Drummelsmith J., Muller M., Madore E., Boilard N., Ouellette M., and Papadopoulou B. A combined proteomic and transcriptomic approach to the study of stage differentiation in Leishmania infantum. Proteomics 6 (2006) 3567-3581. A comprehensive approach consisting of protein prefractionation, global proteomics and targeted DNA microarray analysis to the study of stage differentiation in Leishmania infantum showing that post-translational modifications might play an important role in the differentiation of the parasite.
5. Brems S., Guilbride D.L., Gundlesdodjir-Planck D., Busold C., Luu V.D., Schanne M., Hoheisel J., and Clayton C. The transcriptomes of Trypanosoma brucei Lister 427 and TREU927 bloodstream and procyclic trypomastigotes. Mol Biochem Parasitol 139 (2005) 163-172
6. Minning T.A., Bua J., Garcia G.A., McGraw R.A., and Tarleton R.L. Microarray profiling of gene expression during trypomastigote to amastigote transition in Trypanosoma cruzi. Mol Biochem Parasitol 131 (2003) 55-64
7. Cohen-Freue G., Holzer T.R., Forney J.D., and McMaster W.R. Global gene expression in Leishmania. Int J Parasitol 37 (2007) 1077-1086
8. Atwood III J.A., Weatherly D.B., Minning T.A., Bundy B., Cavola C., Opperdoes F.R., Orlando R., and Tarleton R.L. The Trypanosoma cruzi proteome. Science 309 (2005) 473-476
9. Martinez-Calvillo S., Yan S., Nguyen D., Fox M., Stuart K., and Myler P.J. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11 (2003) 1291-1299
10. Liang X.H., Haritan A., Uliel S., and Michaeli S. trans and cis splicing in trypanosomatids: mechanism, factors, and regulation. Eukaryot Cell 2 (2003) 830-840
11. Benz C., Nilsson D., Andersson B., Clayton C., and Guilbride D.L. Messenger RNA processing sites in Trypanosoma brucei. Mol Biochem Parasitol 143 (2005) 125-134
12. Gopal S., Awadalla S., Gaasterland T., and Cross G.A. A computational investigation of kinetoplastid trans-splicing. Genome Biol 6 (2005) R95
13. Bringaud F., Muller M., Cerqueira G.C., Smith M., Rochette A., El-Sayed N.M., Papadopoulou B., and Ghedin E. Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog 3 9 (2007) 1291-1307. First evidence for genome-wide distribution and expansion of extinct degenerated retroposons (SIDERs) in Leishmania located predominantly within 3′UTRs and their role in regulating gene expression in this parasite.
14. Clayton C., and Shapira M. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol Biochem Parasitol 156 (2007) 93-101. Recent comprehensive review illustrating the diversity of post-transcriptional gene regulation mechanisms in trypanosomatids.
15. Colasante C., Robles A., Li C.H., Schwede A., Benz C., Voncken F., Guilbride D.L., and Clayton C. Regulated expression of glycosomal phosphoglycerate kinase in Trypanosoma brucei. Mol Biochem Parasitol 151 (2007) 193-204
16. Jager A.V., De Gaudenzi J.G., Cassola A., D'Orso I., and Frasch A.C. mRNA maturation by two-step trans-splicing/polyadenylation processing in trypanosomes. Proc Natl Acad Sci U S A 104 (2007) 2035-2042. This paper implicates differential post-transcriptional secondary splicing event in the regulation of cytoplasmic pre-mRNAs and mRNAs in T. cruzi, which might represent a novel post-transcriptional regulation in trypanosomes.
17. Campbell D.A., Thomas S., and Sturm N.R. Transcription in kinetoplastid protozoa: why be normal?. Microbes Infect 5 (2003) 1231-1240
18. Lustig Y., Sheiner L., Vagima Y., Goldshmidt H., Das A., Bellofatto V., and Michaeli S. Spliced-leader RNA silencing: a novel stress-induced mechanism in Trypanosoma brucei. EMBO Rep 8 (2007) 408-413. This study showed that SL-RNA transcription in T. brucei is dynamic, which might represent a novel form of global stress response that appears to be analogous to the unfolded protein response in other model organisms.
19. Taylor J.E., and Rudenko G. Switching trypanosome coats: what's in the wardrobe?. Trends Genet 22 (2006) 614-620
20. Pays E. Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol 21 (2005) 517-520
21. Clayton C.E. Life without transcriptional control? From fly to man and back again. EMBO J 21 (2002) 1881-1888
22. D'Orso I., De Gaudenzi J.G., and Frasch A.C. RNA-binding proteins and mRNA turnover in trypanosomes. Trends Parasitol 19 (2003) 151-155
23. Sonenberg N., and Dever T.E. Eukaryotic translation intiation factors and regulators. Curr Opin Struct Biol 13 (2003) 56-63
24. Yoffe Y., Zuberek J., Lerer A., Lewdorowicz M., Stepinski J., Altmann M., Darzynkiewicz E., and Shapira M. Binding specificities and potential roles of isoforms of eukaryotic intiation factor 4E in Leishmania. Eukaryot Cell 5 (2006) 1969-1979
25. Dhalia R., Reis C.R., Freire E.R., Rocha P.O., Katz R., Muniz J.R., Standart N., and de Melo Neto O.P. Translation initiation in Leishmania major: characterisation of mucltiple eIF4F subunit homologues. Mol Biochem Parasitol 140 (2005) 23-41
26. Stanton J.D., and Mensa-Wilmot K. AUG-proximal nucleotides regulate protein synthesis in Leishmania tropica. Mol Microbiol 61 (2006) 691-703
27. Lukes J, Paris Z, Regmi S, Breitling R, Mureev S, Kushnir S, Pyatkov KMJ, Alexandrov KA: Translational initiation in Leishmania tarentolae and Phytomonas serpens (Kinetoplastida) is strongly influenced by pre-ATG triplet and its 5′ sequence context. Mol Biochem Parasitol 2006, 148:125-132.
28. Engstler M., and Boshart M. Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev 18 (2004) 2798-2811. This study shows that cold shock induces immediate and reversible expression of the insect stage-specific EP procyclin surface protein in bloodstream trypanosome forms via a post-transcriptional mechanism and that it sensitizes trypanosomes to chemical inducers of development. This sensitization is coincident with a developmentally regulated change in stage-specific EP surface protein trafficking.
29. Folgueira C., Quijada L., Soto M., Abanades D.R., Alonso C., and Requena J.M. The translational efficiencies of the two Leishmania infantum HSP70 mRNAs, differing in their 3′-untranslated regions, are affected by shifts in the temperature of growth through different mechanisms. J Biol Chem 280 (2005) 35172-35183
30. McNicoll F., Muller M., Cloutier S., Boilard N., Rochette A., Dubé M., and Papadopoulou B. Distinct 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J Biol Chem 280 (2005) 35238-35246. Indication that the 450 nt conserved 3′UTR element (belonging to SIDER1 retroposons) found also in the Leishmania amastin mRNAs mediates translational regulation in a stage-specific manner and that this regulation is induced principally upon heat stress.
31. Mayho M., Fenn K., Craddy P., Crosthwaite S., and Matthews K. 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 (2006) 5312-5324. Evidence for genome-wide conservation of U-rich regulatory elements among a large group of T. brucei procyclic-enriched transcripts.
32. Boucher N., Wu Y., Dumas C., Dubé M., Sereno D., Breton M., and Papadopoulou B. A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3′-untranslated region element. J Biol Chem 277 (2002) 19511-19520
33. Rochette A., McNicoll F., Girard J., Breton M., Leblanc E., Bergeron M.G., and Papadopoulou B. Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp. Mol Biochem Parasitol 140 (2005) 205-220
34. Wu Y., El Fakhry Y., Sereno D., Tamar S., and Papadopoulou B. A new developmentally regulated gene family in Leishmania amastigotes encoding a homolog of amastin surface proteins. Mol Biochem Parasitol 110 (2000) 345-357
35. De Gaudenzi J., Frasch A.C., and Clayton C. RNA-binding domain proteins in Kinetoplastids: a comparative analysis. Eukaryot Cell 4 (2005) 2106-2114
36. Luu V.D., Brems S., Hoheisel J.D., Burchmore R., Guilbride D.L., and Clayton C. Functional analysis of Trypanosoma brucei PUF1. Mol Biochem Parasitol 150 (2006) 340-349
37. Ivens A.C., Peacock C.S., Worthey E.A., Murphy L., Aggarwal G., Berriman M., Sisk E., Rajandream M.A., Adlem E., Aert R., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309 (2005) 436-442. This paper describes the complete genome sequence of Leishmania major.
38. Mittra B., and Ray D.S. Presence of a poly(A) binding protein and two proteins with cell cycle-dependent phosphorylation in Crithidia fasciculata mRNA cycling sequence binding protein II. Eukaryot Cell 3 (2004) 1185-1197
39. Pelletier M., and Read L.K. RBP16 is a multifunctional gene regulatory protein involved in editing and stabilization of specific mitochondrial mRNAs in Trypanosoma brucei. RNA 9 (2003) 457-468
40. Sbicego S., Alfonzo J.D., Estevez A.M., Rubio M.A., Kang X., Turck C.W., Peris M., and Simpson L. RBP38, a novel RNA-binding protein from trypanosomatid mitochondria, modulates RNA stability. Eukaryot Cell 2 (2003) 560-568
41. Purdy J.E., Donelson J.E., and Wilson M.E. Regulation of genes encoding the major surface protease of Leishmania chagasi via mRNA stability. Mol Biochem Parasitol 142 (2005) 88-97
42. Webb H., Burns R., Ellis L., Kimblin N., and Carrington M. Developmentally regulated instability of the GPI-PLC mRNA is dependent on a short-lived protein factor. Nucleic Acids Res 33 (2005) 1503-1512
43. Holetz F.B., Correa A., Avila A.R., Nakamura C.V., Krieger M.A., and Goldenberg S. Evidence of P-body-like structures in Trypanosoma cruzi. Biochem Biophys Res Commun 356 (2007) 1062-1067
44. Dumas C., Chow C., Muller M., and Papadopoulou B. A novel class of developmentally regulated noncoding RNAs in Leishmania. Eukaryot Cell 5 (2006) 2033-2046. This was the first report on the presence of cytosolic developmentally regulated non-coding RNAs in trypanosomatids that are expressed as sense and antisense transcripts in a regulated fashion.
45. Ullu E., Tschudi C., and Chakraborty T. RNA interference in protozoan parasites. Cell Microbiol 6 (2004) 509-519
46. Parsons M., Worthey E.A., Ward P.N., and Mottram J.C. Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genom 6 (2005) 127
47. Jones A., Faldas A., Foucher A., Hunt E., Tait A., Wastling J.M., and Turner C.M. Visualisation and analysis of proteomic data from the procyclic form of Trypanosoma brucei. Proteomics 6 (2006) 259-267
48. Li J., Ruyechan W.T., and Williams N. Stage-specific translational efficiency and protein stability regulate the developmental expression of p37, an RNA binding protein from Trypanosoma brucei. Biochem Biophys Res Commun 306 (2003) 918-923
49. Hall B.S., Smith E., Langer W., Jacobs L.A., Goulding D., and Field M.C. Developmental variation in Rab11-dependent trafficking in Trypanosoma brucei. Eukaryot Cell 4 (2005) 971-980
50. Hotz H.R., Hartmann C., Huober K., Hug M., and Clayton C. Mechanisms of developmental regulation in Trypanosoma brucei: a polypyrimidine tract in the 3′-untranslated region of a surface protein mRNA affects RNA abundance and translation. Nucleic Acids Res 25 (1997) 3017-3026
51. Quijada L., Guerra-Giraldez C., Drozdz M., Hartmann C., Irmer H., Ben-Dov C., Cristodero M., Ding M., and Clayton C. Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements. Nucleic Acids Res 30 (2002) 4414-4424
52. D'Orso I., and Frasch A.C. 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 (2002) 50520-50528
53. Di Noia J.M., D'Orso I., Sanchez D.O., and 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 275 (2000) 10218-10227
54. Hehl A., Vassella E., Braun R., and Roditi I. A conserved stem-loop structure in the 3′ untranslated region of procyclin mRNAs regulates expression in Trypanosoma brucei. Proc Natl Acad Sci U S A 91 (1994) 370-374
55. Coughlin B.C., Teixeira S.M., Kirchhoff L.V., and 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 275 (2000) 12051-12060
56. Mishra K.K., Holzer T.R., Moore L.L., and LeBowitz J.H. A negative regulatory element controls mRNA abundance of the Leishmania mexicana Paraflagellar rod gene PFR2. Eukaryot Cell 2 (2003) 1009-1017
57. Zilka A., Garlapati S., Dahan E., Yaolsky V., and Shapira M. Developmental regulation of heat shock protein 83 in Leishmania. 3′ processing and mRNA stability control transcript abundance, and translation id directed by a determinant in the 3′-untranslated region. J Biol Chem 276 (2001) 47922-47929
58. Quijada L., Soto M., Alonso C., and Requena J.M. Identification of a putative regulatory element in the 3′-untranslated region that controls expression of HSP70 in Leishmania infantum. Mol Biochem Parasitol 110 (2000) 79-91
59. Murray A., Fu C., Habibi G., and McMaster W.R. Regions in the 3′ untranslated region confer stage-specific expression to the Leishmania mexicana a600-4 gene. Mol Biochem Parasitol 153 (2007) 125-132
60. Heras S.R., Lopez M.C., Olivares M., and Thomas M.C. The L1Tc non-LTR retrotransposon of Trypanosoma cruzi contains an internal RNA-pol II-dependent promoter that strongly activates gene transcription and generates unspliced transcripts. Nucleic Acids Res 35 (2007) 2199-2214