About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 525241, 15 pages
http://dx.doi.org/10.1155/2010/525241
Review Article

Gene Expression in Trypanosomatid Parasites

1Unidad de Biomedicina, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Av. De los Barrios 1, Col. Los Reyes Iztacala, Tlalnepantla, Edo. de México, CP 54090, Mexico
2Departmento de Biomedicina Molecular, Centro de Investigación y de Estudios Avanzados del IPN, Apartado Postal 14-740, 07360 México, D.F., Mexico

Received 19 August 2009; Accepted 4 November 2009

Academic Editor: Luis I. Terrazas

Copyright © 2010 Santiago Martínez-Calvillo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Desjeux, “Leishmaniasis: current situation and new perspectives,” Comparative Immunology, Microbiology and Infectious Diseases, vol. 27, no. 5, pp. 305–318, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. E. Handman, “Cell biology of Leishmania,” Advances in Parasitology, vol. 44, pp. 1–39, 1999. View at Scopus
  3. K. R. Matthews, “The developmental cell biology of Trypanosoma brucei,” Journal of Cell Science, vol. 118, no. 2, pp. 283–290, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. W. De Souza, “Basic cell biology of Trypanosoma cruzi,” Current Pharmaceutical Design, vol. 8, no. 4, pp. 269–285, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Vanhamme and E. Pays, “Control of gene expression in trypanosomes,” Microbiological Reviews, vol. 59, no. 2, pp. 223–240, 1995. View at Scopus
  6. C. E. Clayton, “Life without transcriptional control? From fly to man and back again,” EMBO Journal, vol. 21, no. 8, pp. 1881–1888, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. D. A. Campbell, S. Thomas, and N. R. Sturm, “Transcription in kinetoplastid protozoa: why be normal?” Microbes and Infection, vol. 5, no. 13, pp. 1231–1240, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Das, M. Banday, and V. Bellofatto, “RNA polymerase transcription machinery in trypanosomes,” Eukaryotic Cell, vol. 7, no. 3, pp. 429–434, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. L. Vanhamme, “Trypanosome RNA polymerases and transcription factors: sensible trypanocidal drug targets?” Current Drug Targets, vol. 9, no. 11, pp. 979–996, 2008. View at Scopus
  10. K. D. Stuart, A. Schnaufer, N. L. Ernst, and A. K. Panigrahi, “Complex management: RNA editing in trypanosomes,” Trends in Biochemical Sciences, vol. 30, no. 2, pp. 97–105, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. P. Wincker, C. Ravel, C. Blaineau, et al., “The Leishmania genome comprises 36 chromosomes conserved across widely divergent human pathogenic species,” Nucleic Acids Research, vol. 24, no. 9, pp. 1688–1694, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. A. C. Ivens, C. S. Peacock, E. A. Worthey, et al., “The genome of the kinetoplastid parasite, Leishmania major,” Science, vol. 309, no. 5733, pp. 436–442, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. D. B. Weatherly, C. Boehlke, and R. L. Tarleton, “Chromosome level assembly of the hybrid Trypanosoma cruzi genome,” BMC Genomics, vol. 10, article 255, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. N. M. El-Sayed, P. J. Myler, D. C. Bartholomeu, et al., “The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease,” Science, vol. 309, no. 5733, pp. 409–415, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. S. E. Melville, V. Leech, M. Navarro, and G. A. M Cross, “The molecular karyotype of the megabase chromosomes of Trypanosoma brucei stock 427,” Molecular and Biochemical Parasitology, vol. 111, no. 2, pp. 261–273, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Berriman, E. Ghedin, C. Hertz-Fowler, et al., “The genome of the African trypanosome Trypanosoma brucei,” Science, vol. 309, no. 5733, pp. 416–422, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. P. J. Myler, L. Audleman, T. Devos, et al., “Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 6, pp. 2902–2906, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. N. E. Padilla-Mejía, L. E. Florencio-Martínez, E. E. Figueroa-Angulo, et al., “Gene organization and sequence analyses of transfer RNA genes in trypanosomatid parasites,” BMC Genomics, vol. 10, article 232, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. J. S. Cordingley, “Nucleotide sequence of the 5S ribosomal RNA gene repeat of Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 17, no. 3, pp. 321–330, 1985. View at Scopus
  20. R. Hernandez-Rivas, S. Martinez-Calvillo, M. Romero, and R. Hernandez, “Trypanosoma cruzi 5S rRNA genes: molecular cloning, srtucture and chromosomal organization,” FEMS Microbiology Letters, vol. 92, no. 1, pp. 63–67, 1992. View at Publisher · View at Google Scholar · View at Scopus
  21. N. M. El-Sayed, P. J. Myler, G. Blandin, et al., “Comparative genomics of trypanosomatid parasitic protozoa,” Science, vol. 309, no. 5733, pp. 404–409, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. G. Mair, H. Shi, H. Li, et al., “A new twist in trypanosome RNA metabolism: cis-splicing of pre-mRNA,” RNA, vol. 6, no. 2, pp. 163–169, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. T. H. P. Tan, R. Pach, A. Crausaz, A. Ivens, and A. Schneider, “tRNAs in Trypanosoma brucei: genomic organization, expression, and mitochondrial import,” Molecular and Cellular Biology, vol. 22, no. 11, pp. 3707–3717, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Bastien, C. Blaineau, and M. Pages, “Leishmania: sex, lies and karyotype,” Parasitology Today, vol. 8, no. 5, pp. 174–177, 1992. View at Scopus
  25. J. Henriksson, L. Aslund, and U. Pettersson, “Karyotype variability in Trypanosoma cruzi,” Parasitology Today, vol. 12, no. 3, pp. 108–114, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. S. M. Sunkin, P. Kiser, P. J. Myler, and K. Stuart, “The size difference between Leishmania major Friedlin chromosome one homologues is localized to sub-telomeric repeats at one chromosomal end,” Molecular and Biochemical Parasitology, vol. 109, no. 1, pp. 1–15, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. P. J. Johnson, J. M. Kooter, and P. Borst, “Inactivation of transcription by UV irradiation of T. brucei provides evidence for a multicistronic transcription unit including a VSG gene,” Cell, vol. 51, no. 2, pp. 273–281, 1987. View at Scopus
  28. J. C. Mottram, W. J. Murphy, and N. Agabian, “A transcriptional analysis of the Trypanosoma brucei hsp83 gene cluster,” Molecular and Biochemical Parasitology, vol. 37, no. 1, pp. 115–128, 1989. View at Scopus
  29. S. Martinez-Calvillo, S. Yan, D. Nguyen, M. Fox, K. Stuart, and P. J. Myler, “Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region,” Molecular Cell, vol. 11, no. 5, pp. 1291–1299, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Parsons, R. G. Nelson, K. P. Watkins, and N. Agabian, “Trypanosome mRNAs share a common 5 spliced leader sequence,” Cell, vol. 38, no. 1, pp. 309–316, 1984. View at Scopus
  31. J. M. Kooter and P. Borst, “Alpha-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes,” Nucleic Acids Research, vol. 12, no. 24, pp. 9457–9472, 1984. View at Scopus
  32. X.-H. Liang, A. Haritan, S. Uliel, and S. Michaeli, “trans and cis splicing in trypanosomatids: mechanism, factors, and regulation,” Eukaryotic Cell, vol. 2, no. 5, pp. 830–840, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. H. S. Hummel, R. D. Gillespie, and J. Swindle, “Mutational analysis of 3 splice site selection during trans-splicing,” Journal of Biological Chemistry, vol. 275, no. 45, pp. 35522–35531, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. C. Benz, D. Nilsson, B. Andersson, C. Clayton, and D. L. Guilbride, “Messenger RNA processing sites in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 143, no. 2, pp. 125–134, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. T. N. Siegel, K. S. W. Tan, and G. A. M. Cross, “Systematic study of sequence motifs for RNA trans splicing in Trypanosoma brucei,” Molecular and Cellular Biology, vol. 25, no. 21, pp. 9586–9594, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. J. H. LeBowitz, H. Q. Smith, L. Rusche, and S. M. Beverley, “Coupling of poly(A) site selection and trans-splicing in Leishmania,” Genes and Development, vol. 7, no. 6, pp. 996–1007, 1993. View at Scopus
  37. S. Haile and B. Papadopoulou, “Developmental regulation of gene expression in trypanosomatid parasitic protozoa,” Current Opinion in Microbiology, vol. 10, no. 6, pp. 569–577, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. S. Martinez-Calvillo, D. Nguyen, K. Stuart, and P. J. Myler, “Transcription initiation and termination on Leishmania major chromosome 3,” Eukaryotic Cell, vol. 3, no. 2, pp. 506–517, 2004. View at Publisher · View at Google Scholar
  39. T. N. Siegel, D. R. Hekstra, L. E. Kemp, et al., “Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei,” Genes and Development, vol. 23, no. 9, pp. 1063–1076, 2009. View at Publisher · View at Google Scholar · View at PubMed
  40. S. Thomas, A. Green, N. R. Sturm, D. A. Campbell, and P. J. Myler, “Histone acetylations mark origins of polycistronic transcription in Leishmania major,” BMC Genomics, vol. 10, article 152, 2009. View at Publisher · View at Google Scholar · View at PubMed
  41. P. Respuela, M. Ferella, A. Rada-Iglesias, and L. Aslund, “Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi,” Journal of Biological Chemistry, vol. 283, no. 23, pp. 15884–15892, 2008. View at Publisher · View at Google Scholar · View at PubMed
  42. N. Boucher, Y. Wu, C. Dumas, et al., “A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3-untranslated region element,” Journal of Biological Chemistry, vol. 277, no. 22, pp. 19511–19520, 2002. View at Publisher · View at Google Scholar · View at PubMed
  43. L. Quijada, C. Guerra-Giraldez, M. Drozdz, et al., “Expression of the human RNA-binding protein HuR in Trypanosoma brucei increases the abundance of mRNAs containing AU-rich regulatory elements,” Nucleic Acids Research, vol. 30, no. 20, pp. 4414–4424, 2002.
  44. A. Furger, N. Schurch, U. Kurath, and I. Roditi, “Elements in the 3 untranslated region of procyclin mRNA regulate expression in insect forms of Trypanosoma brucei by modulating RNA stability and translation,” Molecular and Cellular Biology, vol. 17, no. 8, pp. 4372–4380, 1997.
  45. H.-R. Hotz, C. Hartmann, K. Huober, M. Hug, and C. Clayton, “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 Research, vol. 25, no. 15, pp. 3017–3025, 1997. View at Publisher · View at Google Scholar
  46. M. Gale Jr., V. Carter, and M. Parsons, “Translational control mediates the developmental regulation of the Trypanosoma brucei Nrk protein kinase,” Journal of Biological Chemistry, vol. 269, no. 50, pp. 31659–31665, 1994.
  47. M. Mayho, K. Fenn, P. Craddy, S. Crosthwaite, and K. Matthews, “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 Research, vol. 34, no. 18, pp. 5312–5324, 2006. View at Publisher · View at Google Scholar · View at PubMed
  48. S. C. Nardelli, A. R. Ávila, A. Freund, et al., “Small-subunit rRNA processome proteins are translationally regulated during differentiation of Trypanosoma cruzi,” Eukaryotic Cell, vol. 6, no. 2, pp. 337–345, 2007. View at Publisher · View at Google Scholar · View at PubMed
  49. T. I. Lee and R. A. Young, “Transcription of eukaryotic protein-coding genes,” Annual Review of Genetics, vol. 34, pp. 77–137, 2000. View at Publisher · View at Google Scholar · View at PubMed
  50. T. Juven-Gershon, J.-Y. Hsu, J. W. Theisen, and J. T. Kadonaga, “The RNA polymerase II core promoter—the gateway to transcription,” Current Opinion in Cell Biology, vol. 20, no. 3, pp. 253–259, 2008. View at Publisher · View at Google Scholar · View at PubMed
  51. R. M. Saito, M. G. Elgort, and D. A. Campbell, “A conserved upstream element is essential for transcription of the Leishmania tarentolae mini-exon gene,” EMBO Journal, vol. 13, no. 22, pp. 5460–5469, 1994.
  52. A. Günzl, E. Ullu, M. Dörner, et al., “Transcription of the Trypanosoma brucei spliced leader RNA gene is dependent only on the presence of upstream regulatory elements,” Molecular and Biochemical Parasitology, vol. 85, no. 1, pp. 67–76, 1997. View at Publisher · View at Google Scholar
  53. H. Luo and V. Bellofatto, “Characterization of two protein activities that interact at the promoter of the trypanosomatid spliced leader RNA,” Journal of Biological Chemistry, vol. 272, no. 52, pp. 33344–33352, 1997. View at Publisher · View at Google Scholar
  54. C. Yang, E. Bolotin, T. Jiang, F. M. Sladek, and E. Martinez, “Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters,” Gene, vol. 389, no. 1, pp. 52–65, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. R. Anish, M. B. Hossain, R. H. Jacobson, and S. Takada, “Characterization of transcription from TATA-less promoters: identification of a new core promoter element XCPE2 and analysis of factor requirements,” PLoS ONE, vol. 4, no. 4, article e5103, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. P. Carninci, A. Sandelin, B. Lenhard, et al., “Genome-wide analysis of mammalian promoter architecture and evolution,” Nature Genetics, vol. 38, no. 6, pp. 626–635, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. M. C. Frith, E. Valen, A. Krogh, Y. Hayashizaki, P. Carninci, and A. Sandelin, “A code for transcription initiation in mammalian genomes,” Genome Research, vol. 18, no. 1, pp. 1–12, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  58. Y. Tokusumi, Y. Ma, X. Song, R. H. Jacobson, and S. Takada, “The new core promoter element XCPE1 (X core promoter element 1) directs activator-, mediator-, and TATA-binding protein-dependent but TFIID-independent RNA polymerase II transcription from TATA-less promoters,” Molecular and Cellular Biology, vol. 27, no. 5, pp. 1844–1858, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. N. D. Trinklein, S. F. Aldred, S. J. Hartman, D. I. Schroeder, R. P. Otillar, and R. M. Myers, “An abundance of bidirectional promoters in the human genome,” Genome Research, vol. 14, no. 1, pp. 62–66, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. J. L. Huppert and S. Balasubramanian, “G-quadruplexes in promoters throughout the human genome,” Nucleic Acids Research, vol. 35, no. 2, pp. 406–413, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. E. P. Geiduschek and G. A. Kassavetis, “The RNA polymerase III transcription apparatus,” Journal of Molecular Biology, vol. 310, no. 1, pp. 1–26, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. I. M. Willis, “RNA polymerase III. Genes, factors and transcriptional specificity,” European Journal of Biochemistry, vol. 212, no. 1, pp. 1–11, 1993. View at Scopus
  63. M. R. Paule and R. J. White, “Survey and summary: transcription by RNA polymerases I and III,” Nucleic Acids Research, vol. 28, no. 6, pp. 1283–1298, 2000. View at Scopus
  64. V. Nakaar, A. O. Dare, D. Hong, E. Ullu, and C. Tschudi, “Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in trypanosomes,” Molecular and Cellular Biology, vol. 14, no. 10, pp. 6736–6742, 1994. View at Scopus
  65. H. Ben-Shlomo, A. Levitan, O. Beja, and S. Michaeli, “The trypanosomatid leptomonas collosoma 7SL RNA gene. Analysis of elements controlling its expression,” Nucleic Acids Research, vol. 25, no. 24, pp. 4977–4984, 1997. View at Publisher · View at Google Scholar · View at Scopus
  66. V. Nakaar, A. Gunzl, E. Ullu, and C. Tschudi, “Structure of the Trypanosoma brucei U6 snRNA gene promoter,” Molecular and Biochemical Parasitology, vol. 88, no. 1-2, pp. 13–23, 1997. View at Publisher · View at Google Scholar · View at Scopus
  67. S. D. Bell and J. D. Barry, “Trypanosome nuclear factors which bind to internal promoter elements of tRNA genes,” Nucleic Acids Research, vol. 23, no. 16, pp. 3103–3110, 1995. View at Scopus
  68. M. J. Lenardo, D. M. Dorfman, L. V. Reddy, and J. E. Donelson, “Characterization of the Trypanosoma brucei 5S ribosomal RNA gene and transcript: the 5S rRNA is a spliced-leader-independent species,” Gene, vol. 35, no. 1-2, pp. 131–141, 1985. View at Scopus
  69. J. C. B. M. Zomerdijk, R. Kieft, P. G. Shiels, and P. Borst, “Alpha-amanitin-resistant transcription units in trypanosomes: a comparison of promoter sequences for a VSG gene expression site and for the ribosomal RNA genes,” Nucleic Acids Research, vol. 19, no. 19, pp. 5153–5158, 1991.
  70. D. R. Sherman, L. Janz, M. Hug, and C. Clayton, “Anatomy of the parp gene promoter of Trypanosoma brucei,” EMBO Journal, vol. 10, no. 11, pp. 3379–3386, 1991.
  71. G. Laufer, G. Schaaf, S. Bollgonn, and A. Gunzl, “In vitro analysis of α-amanitin-resistant transcription from the rRNA, procyclic acidic repetitive protein, and variant surface glycoprotein gene promoters in Trypanosoma brucei,” Molecular and Cellular Biology, vol. 19, no. 8, pp. 5466–5473, 1999.
  72. J. Russell and J. C. B. M. Zomerdijk, “RNA-polymerase-I-directed rDNA transcription, life and works,” Trends in Biochemical Sciences, vol. 30, no. 2, pp. 87–96, 2005. View at Publisher · View at Google Scholar · View at PubMed
  73. G. Hasan, M. J. Turner, and J. S. Cordingley, “Ribosomal RNA genes of Trypanosoma brucei: mapping the regions specifying the six small ribosomal RNAs,” Gene, vol. 27, no. 1, pp. 75–86, 1984. View at Publisher · View at Google Scholar
  74. D. F. Spencer, J. C. Collings, M. N. Schnare, and M. W. Gray, “Multiple spacer sequences in the nuclear large subunit ribosomal RNA gene of Crithidia fasciculata,” The EMBO Journal, vol. 6, pp. 1063–1071, 1987.
  75. R. Hernandez, F. Diaz-de Leon, and M. Castaneda, “Molecular cloning and partial characterization of ribosomal RNA genes from Trypanosoma cruzi,” Molecular and Biochemical Parasitology, vol. 27, no. 2-3, pp. 275–279, 1988.
  76. S. Martinez-Calvillo, S. M. Sunkin, S.-F. Yan, M. Fox, K. Stuart, and P. J. Myler, “Genomic organization and functional characterization of the Leishmania major Friedlin ribosomal RNA gene locus,” Molecular and Biochemical Parasitology, vol. 116, no. 2, pp. 147–157, 2001. View at Publisher · View at Google Scholar
  77. L. Janz and C. Clayton, “The PARP and rRNA promoters of Trypanosoma brucei are composed of dissimilar sequence elements that are functionally interchangeable,” Molecular and Cellular Biology, vol. 14, no. 9, pp. 5804–5811, 1994.
  78. S. R. B. Uliana, W. Fischer, V. A. Stempliuk, and L. M. Floeter-Winter, “Structural and functional characterization of the Leishmania amazonensis ribosomal RNA promoter,” Molecular and Biochemical Parasitology, vol. 76, no. 1-2, pp. 245–255, 1996.
  79. L. S. Gay, M. E. Wilson, and J. E. Donelson, “The promoter for the ribosomal RNA genes of Leishmania chagasi,” Molecular and Biochemical Parasitology, vol. 77, no. 2, pp. 193–200, 1996. View at Publisher · View at Google Scholar
  80. S. Yan, M. J. Lodes, M. Fox, P. J. Myler, and K. Stuart, “Characterization of the Leishmania donovani ribosomal RNA promoter,” Molecular and Biochemical Parasitology, vol. 103, no. 2, pp. 197–210, 1999. View at Publisher · View at Google Scholar
  81. S. Martinez-Calvillo and R. Hernandez, “Trypanosoma cruzi ribosomal DNA: mapping of a putative distal promoter,” Gene, vol. 142, no. 2, pp. 243–247, 1994. View at Publisher · View at Google Scholar
  82. E. Figueroa-Angulo, S. Martinez-Calvillo, I. Lopez-Villasenor, and R. Hernandez, “Evidence supporting a major promoter in the Trypanosoma cruzi rRNA gene,” FEMS Microbiology Letters, vol. 225, no. 2, pp. 221–225, 2003. View at Publisher · View at Google Scholar
  83. B. S. Stolf, R. P. Souto, A. Pedroso, and B. Zingales, “Two types of ribosomal RNA genes in hybrid Trypanosoma cruzi strains,” Molecular and Biochemical Parasitology, vol. 126, no. 1, pp. 73–80, 2003. View at Publisher · View at Google Scholar
  84. E. Figueroa-Angulo, A. Maria Cevallos, A. Zentella, I. Lopez-Villasenor, and R. Hernandez, “Potential regulatory elements in the Trypanosoma cruzi rRNA gene promoter,” Biochimica et Biophysica Acta, vol. 1759, no. 10, pp. 497–501, 2006. View at Publisher · View at Google Scholar · View at PubMed
  85. J. C. B. M. Zomerdijk, R. Kieft, and P. Borst, “Efficient production of functional mRNA mediated by RNA polymerase I in Trypanosoma brucei,” Nature, vol. 353, no. 6346, pp. 772–775, 1991. View at Publisher · View at Google Scholar · View at PubMed
  86. G. Rudenko, H.-M. M. Chung, V. P. Pham, and L. H. T. Van der Ploeg, “RNA polymerase I can mediate expression of CAT and neo protein-coding genes in Trypanosoma brucei,” EMBO Journal, vol. 10, no. 11, pp. 3387–3397, 1991.
  87. P. Borst, “Antigenic variation and allelic exclusion,” Cell, vol. 109, no. 1, pp. 5–8, 2002. View at Publisher · View at Google Scholar
  88. E. Pays, L. Vanhamme, and D. Perez-Morga, “Antigenic variation in Trypanosoma brucei: facts, challenges and mysteries,” Current Opinion in Microbiology, vol. 7, no. 4, pp. 369–374, 2004. View at Publisher · View at Google Scholar · View at PubMed
  89. L. Vanhamme, E. Pays, R. McCulloch, and J. D. Barry, “An update on antigenic variation in African trypanosomes,” Trends in Parasitology, vol. 17, no. 7, pp. 338–343, 2001. View at Publisher · View at Google Scholar
  90. J. D. Barry and R. McCulloch, “Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite,” Advances in Parasitology, vol. 49, pp. 1–70, 2001.
  91. D. Horn, “The molecular control of antigenic variation in Trypanosoma brucei,” Current Molecular Medicine, vol. 4, no. 6, pp. 563–576, 2004. View at Publisher · View at Google Scholar
  92. C. E. Boothroyd, O. Dreesen, T. Leonova, et al., “A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei,” Nature, vol. 459, no. 7244, pp. 278–281, 2009. View at Publisher · View at Google Scholar · View at PubMed
  93. I. Roditi, A. Furger, S. Ruepp, N. Schurch, and P. Butikofer, “Unravelling the procyclin coat of Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 91, no. 1, pp. 117–130, 1998. View at Publisher · View at Google Scholar
  94. M. Berriman, N. Hall, K. Sheader, et al., “The architecture of variant surface glycoprotein gene expression sites in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 122, no. 2, pp. 131–140, 2002. View at Publisher · View at Google Scholar
  95. E. Konig, H. Delius, M. Carrington, R. O. Williams, and I. Roditi, “Duplication and transcription of procyclin genes in Trypanosoma brucei,” Nucleic Acids Research, vol. 17, no. 21, pp. 8727–8739, 1989.
  96. S. D. Brown, J. Huang, and L. H. T. Van der Ploeg, “The promoter for the procyclic acidic repetitive protein (PARP) genes of Trypanosoma brucei shares features with RNA polymerase I promoters,” Molecular and Cellular Biology, vol. 12, no. 6, pp. 2644–2652, 1992. View at Scopus
  97. L. Vanhamme, A. Pays, P. Tebabi, S. Alexandre, and E. Pays, “Specific binding of proteins to the noncoding strand of a crucial element of the variant surface glycoprotein, procyclin, and ribosomal promoters of Trypanosoma brucei,” Molecular and Cellular Biology, vol. 15, no. 10, pp. 5598–5606, 1995. View at Scopus
  98. A. Günzl, T. Bruderer, G. Laufer, et al., “RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei,” Eukaryotic Cell, vol. 2, no. 3, pp. 542–551, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. P. Hu, S. Wu, Y. Sun, et al., “Characterization of human RNA polymerase III identifies orthologues for Saccharomyces cerevisiae RNA polymerase III subunits,” Molecular and Cellular Biology, vol. 22, no. 22, pp. 8044–8055, 2002. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Devaux, L. Lecordier, P. Uzureau, et al., “Characterization of RNA polymerase II subunits of Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 148, no. 1, pp. 60–68, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  101. S. Martinez-Calvillo, A. Saxena, A. Green, A. Leland, and P. J. Myler, “Characterization of the RNA polymerase II and III complexes in Leishmania major,” International Journal for Parasitology, vol. 37, no. 5, pp. 491–502, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  102. A. Das, H. Li, T. Liu, and V. Bellofatto, “Biochemical characterization of Trypanosoma brucei RNA polymerase II,” Molecular and Biochemical Parasitology, vol. 150, no. 2, pp. 201–210, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  103. R. Evers, A. Hammer, J. Köck, et al., “Trypanosoma brucei contains two RNA polymerase II largest subunit genes with an altered C-terminal domain,” Cell, vol. 56, no. 4, pp. 585–597, 1989. View at Scopus
  104. A. Gunzl, L. Vanhamme, and P. J. Myler, “Transcription in trypanosomes: a different means to the end,” in Trypanosomes: After the Genome, J. D. Barry, R. McCulloch, J. C. Mottram, and A. Acosta-Serrano, Eds., pp. 177–208, Horizon Bioscience, Wymonham, UK, 2007.
  105. R. Hernandez-Rivas, L. E. Florencio-Martinez, M. Martinez-Salazar, and S. Martinez-Calvillo, “Gene expression and transcriptional machinery in trypanosomatid and apicomplexa parasites,” in Advances in the Immunobiology of Parasitic Diseases, L. I. Terrazas, Ed., pp. 313–337, Research Signpost, Kerala, India, 2007.
  106. J.-P. Ruan, G. K. Arhin, E. Ullu, and C. Tschudi, “Functional characterization of a Trypanosoma brucei TATA-binding protein-related factor points to a universal regulator of transcription in trypanosomes,” Molecular and Cellular Biology, vol. 24, no. 21, pp. 9610–9618, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  107. B. Schimanski, T. N. Nguyen, and A. Gunzl, “Characterization of a multisubunit transcription factor complex essential for spliced-leader RNA gene transcription in Trypanosoma brucei,” Molecular and Cellular Biology, vol. 25, no. 16, pp. 7303–7313, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  108. A. Das, Q. Zhang, J. B. Palenchar, B. Chatterjee, G. A. M. Cross, and V. Bellofatto, “Trypanosomal TBP functions with the multisubunit transcription factor tSNAP to direct spliced-leader RNA gene expression,” Molecular and Cellular Biology, vol. 25, no. 16, pp. 7314–7322, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  109. J. B. Palenchar, W. Liu, P. M. Palenchar, and V. Bellofatto, “A divergent transcription factor TFIIB in trypanosomes is required for RNA polymerase II-dependent spliced leader RNA transcription and cell viability,” Eukaryotic Cell, vol. 5, no. 2, pp. 293–300, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  110. B. Schimanski, J. Brandenburg, T. N. Nguyen, M. J. Caimano, and A. Gunzl, “A TFIIB-like protein is indispensable for spliced leader RNA gene transcription in Trypanosoma brucei,” Nucleic Acids Research, vol. 34, no. 6, pp. 1676–1684, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. A. Das and V. Bellofatto, “RNA polymerase II-dependent transcription in trypanosomes is associated with a SNAP complex-like transcription factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 1, pp. 80–85, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. L. Lecordier, S. Devaux, P. Uzureau, et al., “Characterization of a TFIIH homologue from Trypanosoma brucei,” Molecular Microbiology, vol. 64, no. 5, pp. 1164–1181, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. J. H. Lee, T. N. Nguyen, B. Schimanski, and A. Gunzl, “Spliced leader RNA gene transcription in Trypanosoma brucei requires transcription factor TFIIH,” Eukaryotic Cell, vol. 6, no. 4, pp. 641–649, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. J. H. Lee, H. S. Jung, and A. Gunzl, “Transcriptionally active TFIIH of the early-diverged eukaryote Trypanosoma brucei harbors two novel core subunits but not a cyclin-activating kinase complex,” Nucleic Acids Research, vol. 37, no. 11, pp. 3811–3820, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  115. H. Luo, G. Gilinger, D. Mukherjee, and V. Bellofatto, “Transcription initiation at the TATA-less spliced leader RNA gene promoter requires at least two DNA-binding proteins and a tripartite architecture that includes an initiator element,” Journal of Biological Chemistry, vol. 274, no. 45, pp. 31947–31954, 1999. View at Publisher · View at Google Scholar · View at Scopus
  116. T. N. Nguyen, B. Schimanski, A. Zahn, B. Klumpp, and A. Gunzl, “Purification of an eight subunit RNA polymerase I complex in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 149, no. 1, pp. 27–37, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  117. D. Walgraffe, S. Devaux, L. Lecordier, et al., “Characterization of subunits of the RNA polymerase I complex in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 139, no. 2, pp. 249–260, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  118. T. N. Nguyen, B. Schimanski, and A. Gunzl, “Active RNA polymerase I of Trypanosoma brucei harbors a novel subunit essential for transcription,” Molecular and Cellular Biology, vol. 27, no. 17, pp. 6254–6263, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  119. X. Penate, D. Lopez-Farfan, D. Landeira, A. Wentland, I. Vidal, and M. Navarro, “RNA pol II subunit RPB7 is required for RNA pol I-mediated transcription in Trypanosoma brucei,” EMBO Reports, vol. 10, no. 3, pp. 252–257, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  120. J. Brandenburg, B. Schimanski, E. Nogoceke, et al., “Multifunctional class I transcription in Trypanosoma brucei depends on a novel protein complex,” EMBO Journal, vol. 26, no. 23, pp. 4856–4866, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  121. N. R. Sturm, M. C. Yu, and D. A. Campbell, “Transcription termination and 3′-end processing of the spliced leader RNA in kinetoplastids,” Molecular and Cellular Biology, vol. 19, no. 2, pp. 1595–1604, 1999. View at Scopus
  122. E. A. Worthey, S. Martinez-Calvillo, A. Schnaufer, et al., “Leishmania major chromosome 3 contains two long convergent polycistronic gene clusters separated by a tRNA gene,” Nucleic Acids Research, vol. 31, no. 14, pp. 4201–4210, 2003. View at Publisher · View at Google Scholar · View at Scopus
  123. E. M. Prescott and N. J. Proudfoot, “Transcriptional collision between convergent genes in budding yeast,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 13, pp. 8796–8801, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  124. E. P. Geiduschek and G. P. Tocchini-Valentini, “Transcription by RNA polymerase III,” Annual Review of Biochemistry, vol. 57, pp. 873–914, 1988. View at Scopus
  125. H. Matsuzaki, G. A. Kassavetis, and E. P. Geiduschek, “Analysis of RNA chain elongation and termination by Saccharomyces cerevisiae RNA polymerase III,” Journal of Molecular Biology, vol. 235, no. 4, pp. 1173–1192, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  126. P. Braglia, R. Percudani, and G. Dieci, “Sequence context effects on oligo(dT) termination signal recognition by Saccharomyces cerevisiae RNA polymerase III,” Journal of Biological Chemistry, vol. 280, no. 20, pp. 19551–19562, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  127. A. Gunzl, C. Tschudi, V. Nakaar, and E. Ullu, “Accurate transcription of the Trypanosoma brucei U2 small nuclear RNA gene in a homologous extract,” Journal of Biological Chemistry, vol. 270, no. 29, pp. 17287–17291, 1995. View at Publisher · View at Google Scholar · View at Scopus
  128. P. Jansa and I. Grummt, “Mechanism of transcription termination: PTRF interacts with the largest subunit of RNA polymerase I and dissociates paused transcription complexes from yeast and mouse,” Molecular and General Genetics, vol. 262, no. 3, pp. 508–514, 1999. View at Publisher · View at Google Scholar · View at Scopus
  129. J. M. Requena, M. Soto, L. Quijada, G. Carrillo, and C. Alonso, “A region containing repeated elements is associated with transcriptional termination of Leishmania infantum ribosomal RNA genes,” Molecular and Biochemical Parasitology, vol. 84, no. 1, pp. 101–110, 1997. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Berberof, A. Pays, S. Lips, P. Tebabi, and E. Pays, “Characterization of a transcription terminator of the procyclin PARP A unit of Trypanosoma brucei,” Molecular and Cellular Biology, vol. 16, no. 3, pp. 914–924, 1996. View at Scopus
  131. S. Haenni, E. Studer, G. S. Burkard, and I. Roditi, “Bidirectional silencing of RNA polymerase I transcription by a strand switch region in Trypanosoma brucei,” Nucleic Acids Research, vol. 37, no. 15, pp. 5007–5018, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  132. F. Bringaud, E. Ghedin, N. M. A. El-Sayed, and B. Papadopoulou, “Role of transposable elements in trypanosomatids,” Microbes and Infection, vol. 10, no. 6, pp. 575–581, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  133. M. Olivares, J. L. Garcia-Perez, M. Carmen Thomas, S. R. Heras, and M. C. Lopez, “The non-LTR (long terminal repeat) retrotransposon L1Tc from Trypanosoma cruzi codes for a protein with RNase H activity,” Journal of Biological Chemistry, vol. 277, no. 31, pp. 28025–28030, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  134. S. R. Heras, M. C. Lopez, M. Olivares, and M. C. Thomas, “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 Research, vol. 35, no. 7, pp. 2199–2214, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  135. S. Aksoy, T. M. Lalor, J. Martin, L. H. Van der Ploeg, and F. F. Richards, “Multiple copies of a retroposon interrupt spliced leader RNA genes in the African trypanosome, Trypanosoma gambiense,” EMBO Journal, vol. 6, no. 12, pp. 3819–3826, 1987. View at Scopus
  136. K. L. Patrick, P. M. Luz, J.-P. Ruan, H. Shi, E. Ullu, and C. Tschudi, “Genomic rearrangements and transcriptional analysis of the spliced leader-associated retrotransposon in RNA interference-deficient Trypanosoma brucei,” Molecular Microbiology, vol. 67, no. 2, pp. 435–447, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  137. E. Ghedin, F. Bringaud, J. Peterson, et al., “Gene synteny and evolution of genome architecture in trypanosomatids,” Molecular and Biochemical Parasitology, vol. 134, no. 2, pp. 183–191, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  138. F. Bringaud, M. Müller, G. C. Cerqueira, et al., “Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania,” PLoS Pathogens, vol. 3, no. 9, pp. 1291–1307, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  139. J. M. Requena, C. Folgueira, M. C. Lopez, and M. C. Thomas, “The SIDER2 elements, interspersed repeated sequences that populate the Leishmania genomes, constitute subfamilies showing chromosomal proximity relationship,” BMC Genomics, vol. 9, article 263, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  140. M. Smith, F. Bringaud, and B. Papadopoulou, “Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome,” BMC Genomics, vol. 10, article 240, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  141. I. K. Jordan, I. B. Rogozin, G. V. Glazko, and E. V. Koonin, “Origin of a substantial fraction of human regulatory sequences from transposable elements,” Trends in Genetics, vol. 19, no. 2, pp. 68–72, 2003. View at Publisher · View at Google Scholar · View at Scopus
  142. G. Bourque, B. Leong, V. B. Vega, et al., “Evolution of the mammalian transcription factor binding repertoire via transposable elements,” Genome Research, vol. 18, no. 11, pp. 1752–1762, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  143. G. Felsenfeld and M. Groudine, “Controlling the double helix,” Nature, vol. 421, no. 6921, pp. 448–453, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  144. Y.-J. Park and K. Luger, “Histone chaperones in nucleosome eviction and histone exchange,” Current Opinion in Structural Biology, vol. 18, no. 3, pp. 282–289, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  145. W. Stunkel, I. Kober, and K. H. Seifart, “A nucleosome positioned in the distal promoter region activates transcription of the human U6 gene,” Molecular and Cellular Biology, vol. 17, no. 8, pp. 4397–4405, 1997. View at Scopus
  146. T. Kouzarides, “Chromatin modifications and their function,” Cell, vol. 128, no. 4, pp. 693–705, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  147. S. Henikoff, “Nucleosome destabilization in the epigenetic regulation of gene expression,” Nature Reviews Genetics, vol. 9, no. 1, pp. 15–26, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  148. S. I. Belli, “Chromatin remodelling during the life cycle of trypanosomatids,” International Journal for Parasitology, vol. 30, no. 6, pp. 679–687, 2000. View at Publisher · View at Google Scholar · View at Scopus
  149. D. Horn, “Nuclear gene transcription and chromatin in Trypanosoma brucei,” International Journal for Parasitology, vol. 31, no. 11, pp. 1157–1165, 2001. View at Publisher · View at Google Scholar · View at Scopus
  150. S. Masina, H. Zangger, D. Rivier, and N. Fasel, “Histone H1 regulates chromatin condensation in Leishmania parasites,” Experimental Parasitology, vol. 116, no. 1, pp. 83–87, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  151. H. Hecker, B. Betschart, K. Bender, M. Burri, and W. Schlimme, “The chromatin of trypanosomes,” International Journal for Parasitology, vol. 24, no. 6, pp. 809–819, 1994. View at Publisher · View at Google Scholar · View at Scopus
  152. I. Espinoza, G. C. Toro, U. Hellman, and N. Galanti, “Histone H1 and core histones in Leishmania and Crithidia: comparison with Trypanosoma,” Experimental Cell Research, vol. 224, no. 1, pp. 1–7, 1996. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  153. S. Astolfi Filho, C. Martins de Sá, and E. S. Gander, “On the chromatin structure of Trypanosoma cruzi,” Molecular and Biochemical Parasitology, vol. 1, pp. 45–53, 1980.
  154. P. Belnat, J. Paoletti, and G. Riou, “Subunit organization of chromatin from Trypanosoma cruzi sensitive and resistant to ethidium bromide,” Molecular and Biochemical Parasitology, vol. 2, no. 3-4, pp. 167–176, 1981. View at Scopus
  155. M. E. C. Moreira, H. A. Del Portillo, R. V. Milder, J. M. F. Balanco, and M. A. Barcinski, “Heat shock induction of apoptosis in promastigotes of the unicellular organism Leishmania (Leishmania) amazonensis,” Journal of Cellular Physiology, vol. 167, no. 2, pp. 305–313, 1996. View at Publisher · View at Google Scholar · View at Scopus
  156. H. Zangger, J. C. Mottram, and N. Fasel, “Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis?” Cell Death and Differentiation, vol. 9, no. 10, pp. 1126–1139, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  157. H. Hecker and E. S. Gander, “The compaction pattern of the chromatin of trypanosomes,” Biology of the Cell, vol. 53, no. 3, pp. 199–208, 1985. View at Scopus
  158. R. A. Hitchcock, S. Thomas, D. A. Campbell, and N. R. Sturm, “The promoter and transcribed regions of the Leishmania tarentolae spliced leader RNA gene array are devoid of nucleosomes,” BMC Microbiology, vol. 7, article 44, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  159. J. P. C. da Cunha, E. S. Nakayasu, I. C. de Almeida, and S. Schenkman, “Post-translational modifications of Trypanosoma cruzi histone H4,” Molecular and Biochemical Parasitology, vol. 150, no. 2, pp. 268–277, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  160. V. Mandava, J. P. Fernandez, H. Deng, C. J. Janzen, S. B. Hake, and G. A. M. Cross, “Histone modifications in Trypanosoma brucei,” Molecular and Biochemical Parasitology, vol. 156, no. 1, pp. 41–50, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  161. C. J. Janzen, J. P. Fernandez, H. Deng, R. Diaz, S. B. Hake, and G. A. M. Cross, “Unusual histone modifications in Trypanosoma brucei,” FEBS Letters, vol. 580, no. 9, pp. 2306–2310, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  162. T. Kawahara, T. N. Siegel, A. K. Ingram, S. Alsford, G. A. M. Cross, and D. Horn, “Two essential MYST-family proteins display distinct roles in histone H4K10 acetylation and telomeric silencing in trypanosomes,” Molecular Microbiology, vol. 69, no. 4, pp. 1054–1068, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  163. T. N. Siegel, T. Kawahara, J. A. DeGrasse, C. J. Janzen, D. Horn, and G. A. M. Cross, “Acetylation of histone H4K4 is cell cycle regulated and mediated by HAT3 in Trypanosoma brucei,” Molecular Microbiology, vol. 67, no. 4, pp. 762–771, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  164. X. De La Cruz, S. Lois, S. Sánchez-Molina, and M. A. Martínez-Balbás, “Do protein motifs read the histone code?” BioEssays, vol. 27, no. 2, pp. 164–175, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  165. G. V. Villanova, S. C. Nardelli, P. Cribb, et al., “Trypanosoma cruzi bromodomain factor 2 (BDF2) binds to acetylated histones and is accumulated after UV irradiation,” International Journal for Parasitology, vol. 39, no. 6, pp. 665–673, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  166. J. E. Lowell, F. Kaiser, C. J. Janzen, and G. A. M. Cross, “Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei,” Journal of Cell Science, vol. 118, no. 24, pp. 5721–5730, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  167. L. M. Figueiredo, G. A. M. Cross, and C. J. Janzen, “Epigenetic regulation in African trypanosomes: a new kid on the block,” Nature Reviews Microbiology, vol. 7, no. 7, pp. 504–513, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  168. P. B. Talbert and S. Henikoff, “Chromatin-based transcriptional punctuation,” Genes and Development, vol. 23, no. 9, pp. 1037–1041, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus