Trypanosomatid comparative genomics: Contributions to the study of parasite biology and different parasitic diseases

Genetics and Molecular Biology

Volumn 35, Issue 1, 2012, Pages 1-17

  Teixeira, Santuza M ^a   de Paiva, Rita Márcia Cardoso ^a   Kangussu Marcolino, Monica M ^b   DaRocha, Wanderson D ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

Author keywords

Genome; Leishmania major; RNAseq; Trypanosoma brucei; Trypanosoma cruzi

Indexed keywords

ANTIPARASITIC AGENT; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; RNA POLYMERASE II; TRYPTOPHAN;

AFRICAN TRYPANOSOMIASIS; CHAGAS DISEASE; DISEASE CARRIER; DNA SEQUENCE; FUNCTIONAL GENOMICS; GENE DOSAGE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC DISTANCE; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOME ANALYSIS; GENOMICS; HUMAN; KINETOPLASTIDA; LEISHMANIA MAJOR; LEISHMANIASIS; LIFE CYCLE; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NONHUMAN; PARASITE CONTROL; PARASITE IDENTIFICATION; PARASITE TRANSMISSION; PARASITE VECTOR; PARASITE VIRULENCE; PREVALENCE; REVIEW; RNA INTERFERENCE; RNA SEQUENCE; TRANSCRIPTION REGULATION; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

HEXAPODA; LEISHMANIA MAJOR; PROTOZOA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

EID: 84858242418     PISSN: 14154757     EISSN: 16784685     Source Type: Journal    
DOI: 10.1590/S1415-47572012005000008     Document Type: Review

References (135)

1. Aksoy S, Lalor TM, Martin J, Van der Ploeg LH and Richards FF (1987) Multiple copies of a retroposon interrupt spliced leader RNA genes in the African trypanosome, Trypanosoma gambiense. EMBO J 6:3819-3826.
2. Alves LR, Avila AR, Correa A, Holetz FB, Mansur FC, Manque PA, de Menezes JP, Buck GA, Krieger MA and Goldenberg S (2010) Proteomic analysis reveals the dynamic association of proteins with translated mRNAs in Trypanosoma cruzi. Gene 452:72-78.
3. Araujo PR, Burle-Caldas GA, Silva-Pereira RA, Bartholomeu DC, DaRocha WD and 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. Arner E, Kindlund E, Nilsson D, Farzana F, Ferella M, Tammi MT and Andersson B (2007) Database of Trypanosoma cruzi repeated genes: 20,000 additional gene variants. BMC Genomics 8:e391.
5. Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, Carrington M, Depledge DP, Fischer S, Gajria B, Gao X, et al. (2010) TriTrypDB: A functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38:D457-D462.
6. Augusto-Pinto L, Teixeira SM, Pena SD and Machado CR (2003) Single-nucleotide polymorphisms of the Trypanosoma cruzi MSH2 gene support the existence of three phylogenetic lineages presenting differences in mismatch-repair efficiency. Genetics 164:117-126.
7. Baida RC, Santos MR, Carmo MS, Yoshida N, Ferreira D, Ferreira AT, El Sayed NM, Andersson B and da Silveira JF (2006) Molecular characterization of serine-, alanine-, and proline-rich proteins of Trypanosoma cruzi and their possible role in host cell infection. Infect Immun 74:1537-1546.
8. Bartholomeu DC, Cerqueira GC, Leão AC, DaRocha WD, Pais FS, Macedo C, Djikeng A, Teixeira SM and 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.
9. Bates PA (2007) Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol 37:1097-1106.
10. Benabdellah K, González-Rey E and González A (2007) Alternative trans-splicing of the Trypanosoma cruzi LYT1 gene transcript results in compartmental and functional switch for the encoded protein. Mol Microbiol 65:1559-1567.
11. Benz C, Nilsson D, Andersson B, Clayton C and Guilbride DL (2005) Messenger RNA processing sites in Trypanosoma brucei. Mol Biochem Parasitol 143:125-134.
12. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422.
13. Blackwell JM and Melville SE (1999) Status of protozoan genome analysis: Trypanosomatids. Parasitology 118 (Suppl):S11-14.
14. Blackwell JM, Fakiola M, Ibrahim ME, Jamieson SE, Jeronimo SB, Miller EN, Mishra A, Mohamed HS, Peacock CS, Raju M, et al. (2009) Genetics and visceral leishmaniasis: Of mice and man. Parasite Immunol 31:254-266.
15. Boucher N, McNicoll F, Dumas C and Papadopoulou B (2002) RNA polymerase I-mediated transcription of a reporter gene integrated into different loci of Leishmania. Mol Biochem Parasitol 119:153-158.
16. Branche C, Ochaya S, Aslund L and Andersson B (2006) Comparative karyotyping as a tool for genome structure analysis of Trypanosoma cruzi. Mol Biochem Parasitol 147:30-38.
17. Brandão A, Urmenyi T, Rondinelli E, Gonzalez A, de Miranda AB and Degrave W (1997) Identification of transcribed sequences (ESTs) in the Trypanosoma cruzi genome project. Mem Inst Oswaldo Cruz 92:863-866.
18. Brener Z (1973) Biology of Trypanosoma cruzi. Annu Rev Microbiol 27:347-382.
19. Bringaud F, Berriman M and Hertz-Fowler C (2009) Trypanosomatid genomes contain several subfamilies of ingirelated retroposons. Eukaryot Cell 8:1532-1542.
20. Brisse S, Dujardin JC and Tibayrenc M (2000) Identification of six Trypanosoma cruzi lineages by sequence-characterised amplified region markers. Mol Biochem Parasitol 111:95-105.
21. Buscaglia CA and Di Noia JM (2003) Trypanosoma cruzi clonal diversity and the epidemiology of Chagas' disease. Microbes Infect 5:419-427.
22. Campos PC, Bartholomeu DC, DaRocha WD, Cerqueira GC and Teixeira SM (2008) Sequences involved in mRNA processing in Trypanosoma cruzi. Int J Parasitol 38:1383-1389.
23. Cano MI, Gruber A, Vazquez M, Cortés A, Levin MJ, González A, Degrave W, Rondinelli E, Zingales B, Ramirez JL, et al. (1995) Molecular karyotype of clone CL Brener chosen for the Trypanosoma cruzi genome project. Mol Biochem Parasitol 71:273-278.
24. Cerqueira GC, DaRocha WD, Campos PC, Zouain CS and Teixeira SM (2005) Analysis of expressed sequence tags from Trypanosoma cruzi amastigotes. Mem Inst Oswaldo Cruz 100:385-389.
25. Cerqueira GC, Bartholomeu DC, DaRocha WD, Hou L, Freitas-Silva DM, Machado CR, El-Sayed NM and Teixeira SM (2008) Sequence diversity and evolution of multigene families in Trypanosoma cruzi. Mol Biochem Parasitol 157:65-72.
26. Clayton CE (2002) Life without transcriptional control? From fly to man and back again. EMBO J 21:1881-1888.
27. Cribb P and 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.
28. Cribb P, Esteban L, Trochine A, Girardini J and Serra E (2010) Trypanosoma cruzi TBP shows preference for C/G-rich DNA sequences in vitro. Exp Parasitol 124:346-349.
29. DaRocha WD, Otsu K, Teixeira SM and 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 Freitas JM, Augusto-Pinto L, Pimenta JR, Bastos-Rodrigues L, Gonçalves VF, Teixeira SM, Chiari E, Junqueira AC, Fernandes O, Macedo AM, et al. (2006) Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathog 2:e24.
31. De Greef C and Hamers R (1994) The serum resistance-associated (SRA) gene of Trypanosoma brucei rhodesiense encodes a variant surface glycoprotein-like protein. Mol Biochem Parasitol 68:277-284.
32. De Greef C, Chimfwembe E, Kihang'a Wabacha J, Bajyana Songa E and Hamers R (1992) Only the serum-resistant bloodstream forms of Trypanosoma brucei rhodesiense express the serum resistance associated (SRA) protein. Ann Soc Belg Med Trop 72(Suppl 1):13-21.
33. Denise H, Poot J, Jimenez M, Ambit A, Hermman DC, Vermeulen AN, Coombs GH and Mottram JC (2006) Studies on the CPA cysteine peptidase in the Leishmania infantum genome strain JPCM5. BMC Mol Biol 7:42.
34. Depledge DP, Evans KJ, Ivens AC, Aziz N, Maroof A, Kaye PM and Smith DF (2009) Comparative expression profiling of Leishmania: Modulation in gene expression between species and in different host genetic backgrounds. PLoS Negl Trop Dis 3:e476.
35. Desjeux P (1996) Leishmaniasis. Public health aspects and control. Clin Dermatol 14:417-423.
36. Di Noia JM, Sánchez DO and Frasch AC (1995) The protozoan Trypanosoma cruzi has a family of genes resembling the mucin genes of mammalian cells. J Biol Chem 270:24146- 24149.
37. Diehl S, Diehl F, El-Sayed NM, Clayton C and Hoheisel JD (2002) Analysis of stage-specific gene expression in the bloodstream and the procyclic form of Trypanosoma brucei using a genomic DNA-microarray. Mol Biochem Parasitol 123:115-123.
38. El-Sayed NM and Donelson JE (1997) A survey of the Trypanosoma brucei rhodesiense genome using shotgun sequencing. Mol Biochem Parasitol 84:167-178.
39. El-Sayed NM, Alarcon CM, Beck JC, Sheffield VC and Donelson JE (1995) cDNA expressed sequence tags of Trypanosoma brucei rhodesiense provide new insights into the biology of the parasite. Mol Biochem Parasitol 73:75-90.
40. El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, Aggarwal G, Caler E, Renauld H, Worthey EA, Hertz-Fowler C, et al. (2005a) Comparative genomics of trypanosomatid parasitic protozoa. Science 309:404-409.
41. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, et al. (2005b) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415.
42. Fernandes AP, Costa MM, Coelho EA, Michalick MS, de Freitas E, Melo MN, Luiz T.W, Resende DM, Hermont V, Abrantes CF, et al. (2008) Protective immunity against challenge with Leishmania (Leishmania) chagasi in beagle dogs vaccinated with recombinant A2 protein. Vaccine 26:5888-5895.
43. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE and Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806-811.
44. Franzén O, Ochaya S, Sherwood E, Lewis MD, Llewellyn MS, Miles MA and Andersson B (2011) Shotgun sequencing analysis of Trypanosoma cruzi I Sylvio X10/1 and comparison with T. cruzi VI CL Brener. PLoS Negl Trop Dis 5:e984.
45. Girard A and Hannon GJ (2008) Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18:136-148.
46. Gunzl A, Bruderer T, Laufer G, Schimanski B, Tu LC, Chung HM, Lee PT and Lee MG (2003) RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryot Cell 2:542-551.
47. Haag J, O'hUigin C and Overath P (1998) The molecular phylogeny of trypanosomes: Evidence for an early divergence of the Salivaria. Mol Biochem Parasitol 91:37-49.
48. Hajduk SL, Harris ME and Pollard VW (1993) RNA editing in kinetoplastid mitochondria. FASEB J 7:54-63.
49. Henriksson J, Porcel B, Rydåker M, Ruiz A, Sabaj V, Galanti N, Cazzulo JJ, Frasch AC and Pettersson U (1995) Chromosome specific markers reveal conserved linkage groups in spite of extensive chromosomal size variation in Trypanosoma cruzi. Mol Biochem Parasitol 73:63-74.
50. Holzer TR, McMaster WR and Forney JD (2006) Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. Mol Biochem Parasitol 146:198-218.
51. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, et al. (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442.
52. Jackson AP (2010) The evolution of amastin surface glycoproteins in trypanosomatid parasites. Mol Biol Evol 27:33-45.
53. Jackson AP, Sanders M, Berry A, McQuillan J, Aslett MA, Quail MA, Chukualim B, Capewell P, MacLeod A, Melville SE, et al. (2010) The genome sequence of Trypanosoma brucei gambiense, causative agent of chronic human African trypanosomiasis. PLoS Negl Trop Dis 4:e658.
54. Kabani S, Fenn K, Ross A, Ivens A, Smith TK, Ghazal P and Matthews K (2009) Genome-wide expression profiling of in vivo-derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei. BMC Genomics 10:e427.
55. Kieft R, Capewell P, Turner CM, Veitch NJ, MacLeod A and Hajduk S (2010) Mechanism of Trypanosoma brucei gambiense (group 1) resistance to human trypanosome lytic factor. Proc Natl Acad Sci USA 107:16137-16141.
56. Koeller CM and Heise N (2011) The sphingolipid biosynthetic pathway is a potential target for chemotherapy against Chagas disease. Enzyme Res 2011:e648159.
57. Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S and Tschudi C (2010) The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 6:e1001090.
58. Lacomble S, Portman N and Gull K (2009) A protein-protein interaction map of the Trypanosoma brucei paraflagellar rod. PLoS One 4:e7685.
59. LaCount DJ, Bruse S, Hill KL and Donelson JE (2000) Double-stranded RNA interference in Trypanosoma brucei using head-to-head promoters. Mol Biochem Parasitol 111:67-76.
60. Lainson R, Ward RD and Shaw JJ (1977) Leishmania in phlebotomid sandflies: VI. Importance of hindgut development in distinguishing between parasites of the Leishmania mexicana and L. braziliensis complexes. Proc R Soc Lond B 199:309-320.
61. Laurentino EC, Ruiz JC, Fazelini G, Myler PJ, Degrave W, Ferreira MA, Ribeiro LMC and Cruz AK (2004) A survey of Leishmania braziliensis genome by shotgun sequencing. Mol Biochem Parasitol 13:81-86.
62. LeBowitz JH, Smith HQ, Rusche L and Beverley SM (1993) Coupling of poly(A) site selection and trans-splicing in Leishmania. Genes Dev 7:996-1007.
63. Leifso K, Cohen-Freue G, Dogra N, Murray A and McMaster WR (2007) Genomic and proteomic expression analysis of Leishmania promastigote and amastigote life stages: The Leishmania genome is constitutively expressed. Mol Biochem Parasitol 152:35-46.
64. Lepesheva GI, Villalta F and Waterman MR (2011) Targeting Trypanosoma cruzi sterol 14a -demethylase (CYP51). Adv Parasitol 75:65-87.
65. Levick MP, Blackwell JM, Connor V, Coulson RM, Miles A, Smith HE, Wan KL and Ajioka JW (1996) An expressed sequence tag analysis of a full-length, spliced-leader cDNA library from Leishmania major promastigotes. Mol Biochem Parasitol 76:345-348.
66. Liang XH, Haritan A, Uliel S and Michaeli S (2003) Trans and cis splicing in trypanosomatids: Mechanism, factors, and regulation. Eukaryot Cell 2:830-840.
67. Lima MT, Lenzi HL and Gattass CR (1995) Negative tissue parasitism in mice injected with a noninfective clone of Trypanosoma cruzi. Parasitol Res 81:6-12.
68. Lukes J, Jirkû M, Dolezel D, Kral'ová I, Hollar L and Maslov DA (1997) Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. J Mol Evol 44:521-527.
69. Lye LF, Owens K, Shi H, Murta SM, Vieira AC, Turco SJ, Tschudi C, Ullu E and Beverley SM (2010) Retention and loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathog 6:e1001161.
70. Lynn MA and McMaster RW(2008) Leishmania: Conserved evolution - Diverse diseases. Trends Parasitol 24:103-105.
71. Martínez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K and Myler PJ (2003) Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11:1291-1299.
72. Martínez-Calvillo S, Nguyen D, Stuart K and Myler PJ (2004) Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot Cell 3:506-517.
73. Martínez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martínez LE, Manning-Cela RG and Figueroa-Angulo EE (2010) Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010:525241.
74. Mathieu-Daudé F, Cheng R, Welsh J and McClelland M (1996) Screening of differentially amplified cDNA products from RNA arbitrarily primed PCR fingerprints using single strand conformation polymorphism (SSCP) gels. Nucleic Acids Res 24:1504-1507.
75. Matthews KR (2005) The developmental cell biology of Trypanosoma brucei. J Cell Sci 118:283-290.
76. Mauel J (2002) Vaccination against Leishmania infections. Curr Drug Targets Immune Endocr Metabol Disord 2:201-226.
77. McCall LI and Matlashewski G(2010) Localization and induction of the A2 virulence factor in Leishmania: Evidence that A2 is a stress response protein. Mol Microbiol 77:518-530.
78. Miles MA, Souza A, Povoa M, Shaw JJ, Lainson R and Toye PJ (1978) Isozymic heterogeneity of Trypanosoma cruzi in the first autochthonous patients with Chagas' disease in Amazonian Brazil. Nature 272:819-821.
79. Mizbani A, Taslimi Y, Zahedifard F, Taheri T and Rafati S (2011) Effect of A2 gene on infectivity of the nonpathogenic parasite Leishmania tarentolae. Parasitol Res 109:793-799.
80. Momen H (1999) Taxonomy of Trypanosoma cruzi: A commentary on characterization and nomenclature. Mem Inst Oswaldo Cruz 94(Suppl 1):181-184.
81. Morris JC, Wang Z, Drew ME and Englund PT (2002) Glycolysis modulates trypanosome glycoprotein expression as revealed by an RNAi library. EMBO J 21:4429-4438.
82. Murray HW, Berman JD, Davies CR and Saravia NG (2005) Advances in leishmaniasis. Lancet 366:1561-1577.
83. Myler PJ, Audleman L, de Vos T, Hixson G, Kiser P, Lemley C, Magness C, Rickel E, Sisk E, Sunkin S, et al. (1999) Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes. Proc Natl Acad Sci USA 96:2902-2906.
84. Myung KS, Beetham JK, Wilson ME and Donelson JE (2002) Comparison of the post-transcriptional regulation of the mRNAs for the surface proteins PSA (GP46) and MSP (GP63) of Leishmania chagasi. J Biol Chem 277:16489-16497.
85. Ngo H, Tschudi C, Gull K and Ullu E (1998) Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc Natl Acad Sci USA 95:14687-14692.
86. Nilsson D, Gunasekera K, Mani J, Osteras M, Farinelli L, Baerlocher L, Roditi I and Ochsenreiter T (2010) Spliced leader trapping reveals widespread alternative splicing patterns in the highly dynamic transcriptome of Trypanosoma brucei. PLoS Pathog 6:e1001037.
87. Olin-Sandoval V, Moreno-Sánchez R and Saavedra E (2010) Targeting trypanothione metabolism in trypanosomatid human parasites. Curr Drug Targets 11:1614-1630.
88. Pays E, Salmon D, Morrison LJ, Marcello L and Barry JD (2007) Antigenic variation in Trypanosoma brucei. In: Barry JD, McCulloch R, Mottram J and Acosta-Serrano A (eds) Trypanosomes After the Genome. Horizon Bioscience, Wymondham, pp 339-372.
89. Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, Peters N, Adlem E, Tivey A, Aslett M, et al. (2007) Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet 39:839-847.
90. Pérez-Morga D, Vanhollebeke B, Paturiaux-Hanocq F, Nolan DP, Lins L, Homblé F, Vanhamme L, Tebabi P, Pays A, Poelvoorde P, et al. (2005) Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 309:469-472.
91. Porcel BM, Tran AN, Tammi M, Nyarady Z, Rydâker M, Urmenyi TP, Rondinelli E, Pettersson U, Andersson B and Aslund L (2000) Gene survey of the pathogenic protozoan Trypanosoma cruzi. Genome Res 10:1103-1107.
92. Portman N, Lacomble S, Thomas B, McKean PG and Gull K (2009) Combining RNA interference mutants and comparative proteomics to identify protein components and dependences in a eukaryotic flagellum. J Biol Chem 284:5610-5619.
93. Respuela P, Ferella M, Rada-Iglesias A and Aslund L (2008) Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi. J Biol Chem 283:15884-15892.
94. Robinson KA and Beverley SM (2003) Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol Biochem Parasitol 128:217-228.
95. Rochette A, Raymond F, Ubeda JM, Smith M, Messier N, Boisvert S, Rigault P, Corbeil J, Ouellette M and Papadopoulou B (2008) Genome-wide gene expression profiling analysis of Leishmania major and Leishmania infantum developmental stages reveals substantial differences between the two species. BMC Genomics 9:255.
96. Roth C, Bringaud F, Layden RE, Baltz T and Eisen H (1989) Active late-appearing variable surface antigen genes in Trypanosoma equiperdum are constructed entirely from pseudogenes. Proc Natl Acad Sci USA 86:9375-9379.
97. Ruvalcaba-Trejo LI and Sturm NR (2011) The Trypanosoma cruzi Sylvio X10 strain maxicircle sequence: The third musketeer. BMC Genomics 12:58.
98. Sakthianandeswaren A, Foote SJ and Handman E (2009) The role of host genetics in leishmaniasis. Trends Parasitol 25:383-391.
99. Shi H, Djikeng A, Tschudi C and Ullu E (2004) Argonaute protein in the early divergent eukaryote Trypanosoma brucei: Control of small interfering RNA accumulation and retroposon transcript abundance. Mol Cell Biol 24:420-427.
100. Shi H, Djikeng A, Mark T, Wirtz E, Tschudi C and Ullu E (2000) Genetic interference in Trypanosoma brucei by heritable and inducible double-stranded RNA. RNA 6:1069-1076.
101. Shi H, Chamond N, Tschudi C and Ullu E (2004) Selection and characterization of RNA interference-deficient trypanosomes impaired in target mRNA degradation. Eukaryot Cell 3:1445-1453.
102. Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, Fenyo D, Wang X, Dewell S and Cross GA (2009) Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 23:1063-1076.
103. Siegel TN, Hekstra DR, Wang X, Dewell S and Cross GA (2010) Genome-wide analysis of mRNA abundance in two lifecycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites. Nucleic Acids Res 38:4946-4957.
104. Simpson AG, Stevens JR and Lukes J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22:168-174.
105. Smith DF, Peacock CS and Cruz AK (2007) Comparative genomics: From genotype to disease phenotype in the leishmaniases. Int J Parasitol 37:1173-1186.
106. Smith M, Blanchette M and Papadopoulou B (2008) Improving the prediction of mRNA extremities in the parasitic protozoan Leishmania. BMC Bioinformatics 9:158.
107. Souto RP, Fernandes O, Macedo AM, Campbell DA and Zingales B (1996) DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 83:141-152.
108. Stevens JR, Noyes HA, Dover GA and Gibson WC(1999) The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118:107-116.
109. Stuart K and Panigrahi AK (2002) RNA editing: Complexity and complications. Mol Microbiol 45:591-596.
110. Subramaniam C, Veazey P, Redmond S, Hayes-Sinclair J, Chambers E, Carrington M, Gull K, Matthews K, Horn D and Field MC (2006) Chromosome-wide analysis of gene function by RNA interference in the African trypanosome. Eukaryot Cell 5:1539-1549.
111. Teixeira SM, Kirchhoff LV and 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.
112. Thomas S, Green A, Sturm NR, Campbell DA and Myler PJ (2009) Histone acetylations mark origins of polycistronic transcription in Leishmania major. BMC Genomics 10:e152.
113. Turner CM and Barry JD (1989) High frequency of antigenic variation in Trypanosoma brucei rhodesiense infections. Parasitology 99:67-75.
114. Van der Ploeg LH, Valerio D, De Lange T, Bernards A, Borst P and Grosveld FG (1982) An analysis of cosmid clones of nuclear DNA from Trypanosoma brucei shows that the genes for variant surface glycoproteins are clustered in the genome. Nucleic Acids Res 10:5905-5923.
115. Vanhamme L, Paturiaux-Hanocq F, Poelvoorde P, Nolan DP, Lins L, van den Abbeele J, Pays A, Tebabi P, Van Xong H, Jacquet A, et al. (2003) Apolipoprotein L-I is the trypanosome lytic factor of human serum. Nature 422:83-87.
116. Vargas N, Pedroso A and 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.
117. Veitch NJ, Johnson PC, Trivedi U, Terry S, Wildridge D and MacLeod A (2010) Digital gene expression analysis of two life cycle stages of the human-infective parasite, Trypanosoma brucei gambiense, reveals differentially expressed clusters of co-regulated genes. BMC Genomics 11:e124.
118. Verdun RE, di Paolo N, Urmenyi TP, Rondinelli E, Frasch AC and Sanchez DO (1998) Gene discovery through expressed sequence Tag sequencing in Trypanosoma cruzi. Infect Immun 66:5393-5398.
119. Villanueva MS, Williams SP, Beard CB, Richards FF and Aksoy S (1991) A new member of a family of site-specific retrotransposons is present in the spliced leader RNA genes of Trypanosoma cruzi. Mol Cell Biol 11:6139-6148.
120. Voth BR, Kelly BL, Joshi PB, Ivens AC and McMaster WR (1998) Differentially expressed Leishmania major gp63 genes encode cell surface leishmanolysin with distinct signals for glycosylphosphatidylinositol attachment. Mol Biochem Parasitol 93:31-41.
121. Wang Z, Morris JC, Drew ME and Englund PT (2000) Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J Biol Chem 275:40174-40179.
122. Weatherly DB, Boehlke C and Tarleton RL (2009) Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 10:e255.
123. Westenberger SJ, Cerqueira GC, El-Sayed NM, Zingales B, Campbell DA and Sturm NR (2006) Trypanosoma cruzi mitochondrial maxicircles display species- and strain-specific variation and a conserved element in the non-coding region. BMC Genomics 7:e60.
124. Wheeler RJ (2010) The trypanolytic factor-mechanism, impacts and applications. Trends Parasitol 26:457-464.
125. Wincker P (1996) The Leishmania genome comprises 36 chromosomes conserved across widely divergent human pathogenic species. Nucleic Acids Res 24:1688-1694.
126. Wirtz E, Leal S, Ochatt C and Cross GA (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99:89-101.
127. Worthey EA, Martinez-Calvillo S, Schnaufer A, Aggarwal G, Cawthra J, Fazelinia G, Fong C, Fu G, Hassebrock M, Hixson G, et al. (2003) Leishmania major chromosome 3 contains two long convergent polycistronic gene clusters separated by a tRNA gene. Nucleic Acids Res 31:4201-4210.
128. Wright AD, Li S, Feng S, Martin DS and Lynn DH (1999) Phylogenetic position of the kinetoplastids, Cryptobia bullocki, Cryptobia catostomi, and Cryptobia salmositica and monophyly of the genus Trypanosoma inferred from small subunit ribosomal RNA sequences. Mol Biochem Parasitol 99:69-76.
129. Wright JR, Siegel TN and Cross GA (2010) Histone H3 trimethylated at lysine 4 is enriched at probable transcription start sites in Trypanosoma brucei. Mol Biochem Parasitol 172:141-144.
130. Yao C, Donelson JE and Wilson ME (2003) The major surface protease (MSP or GP63) of Leishmania sp. Biosynthesis, regulation of expression, and function. Mol Biochem Parasitol 132:1-16.
131. Zhang WW, Mendez S, Ghosh A, Myler P, Ivens A, Clos J, Sacks DL and Matlashewski G (2003) Comparison of the A2 gene locus in Leishmania donovani and Leishmania major and its control over cutaneous infection. J Biol Chem 278:35508-35515.
132. Zhou S, Kile A, Kvikstad E, Bechner M, Severin J, Forrest D, Runnheim R, Churas C, Anantharaman TS, Myler P, et al. (2004) Shotgun optical mapping of the entire Leishmania major Friedlin genome. Mol Biochem Parasitol 138:97-106.
133. Zingales B, Pereira ME, Almeida KA, Umezawa ES, Nehme NS, Oliveira RP, Macedo A and Souto RP (1997) Biological parameters and molecular markers of clone CL Brener - The reference organism of the Trypanosoma cruzi genome project. Mem Inst Oswaldo Cruz 92:811-814.
134. Zingales B, Souto RP, Mangia RH, Lisboa CV, Campbell DA, Coura JR, Jansen A and Fernandes O (1998) Molecular epidemiology of American trypanosomiasis in Brazil based on dimorphisms of rRNA and mini-exon gene sequences. Int J Parasitol 28:105-112.
135. Zingales B, Andrade SG, Briones MR, Campbell DA, Chiari E, Fernandes O, Guhl F, Lages-Silva E, Macedo AM, Machado CR, et al. (2009) A new consensus for Trypanosoma cruzi intraspecific nomenclature: Second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz 104:1051-1054.