Epigenetic regulation in African trypanosomes: A new kid on the block

Nature Reviews Microbiology

Volumn 7, Issue 7, 2009, Pages 504-513

  Figueiredo, Luisa M ^a   Cross, George A M ^a   Janzen, Christian J ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; RIBOSOME RNA;

ACETYLATION; AFRICAN TRYPANOSOMIASIS; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DNA HISTONE INTERACTION; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; EUKARYOTE EVOLUTION; GENE EXPRESSION REGULATION; HISTONE CODE; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTIST LIFE CYCLE STAGE; REVIEW; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; TRYPANOSOMA BRUCEI; ANIMAL; CHROMATIN; GENETIC EPIGENESIS; GENETICS; HUMAN; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; TRYPANOSOMA;

EUKARYOTA;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; TRYPANOSOMA; TRYPANOSOMIASIS, AFRICAN;

EID: 67649397588     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2149     Document Type: Review

References (107)

1. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
2. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000).
3. World Health Organization. The world health report 2004 - changing history (WHO, Geneva, 2004).
4. Engstler, M. & Boshart, M. Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev. 18, 2798-2811 (2004).
5. Urwyler, S., Studer, E., Renggli, C. K. & Roditi, I. A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. Mol. Microbiol. 63, 218-228 (2007).
6. Welstead, G. G., Schorderet, P. & Boyer, L. A. The reprogramming language of pluripotency. Curr. Opin. Genet. Dev. 18, 123-129 (2008).
7. Rothenberg, E. V., Moore, J. E. & Yui, M. A. Launching the T-cell-lineage developmental programme. Nature Rev. Immunol. 8 9-21 (2008).
8. Palenchar, J. B. & Bellofatto, V. Gene transcription in trypanosomes. Mol. Biochem. Parasitol. 146, 135-141 (2006).
9. Clayton, C. E. Life without transcriptional control? From fly to man and back again. EMBO J. 21, 1881-1888 (2002).
10. Janzen, C. J. et al. Unusual histone modifications in Trypanosoma brucei. FEBS Lett. 580, 2306-2310 (2006).
11. Mandava, V. et al. Histone modifications in Trypanosoma brucei. Mol. Biochem. Parasitol. 156, 41-50 (2007).
12. Saha, A., Wittmeyer, J. & Cairns, B. R. Chromatin remodelling: The industrial revolution of DNA around histones. Nature Rev. Mol. Cell Biol. 7, 437-447 (2006).
13. Martens, J. A. & Winston, F. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13, 136-142 (2003).
14. Deuring, R. et al. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol. Cell 5, 355-365 (2000).
15. de la Serna, I. L., Ohkawa, Y. & Imbalzano, A. N. Chromatin remodelling in mammalian differentiation: Lessons from ATP-dependent remodellers. Nature Rev. Genet. 7, 461-473 (2006).
16. Hughes, K. et al. A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO J. 26, 2400-2410 (2007).
17. Dipaolo, C., Kieft, R., Cross, M. & Sabatini, R. Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein. Mol. Cell 17, 441-451 (2005).
18. Allis, C. D. et al. New nomenclature for chromatin-modifying enzymes. Cell 131, 633-636 (2007).
19. Ingram, A. K. & Horn, D. Histone deacetylases in Trypanosoma brucei two are essential and another is required for normal cell cycle progression. Mol. Microbiol. 45, 89-97 (2002).
20. Kawahara, T. et al. Two essential MYST-family proteins display distinct roles in histone H4K10 acetylation and telomeric silencing in trypanosomes. Mol. Microbiol. 69, 1054-1068 (2008).
21. Siegel, T. N. et al. Acetylation of histone H4K4 is cell cycle regulated and mediated by HAT3 in Trypanosoma brucei. Mol. Microbiol. 67, 762-771 (2008).
22. Alsford, S., Kawahara, T., Isamah, C. & Horn, D. A sirtuin in the African trypanosome is involved in both DNA repair and telomeric gene silencing but is not required for antigenic variation. Mol. Microbiol. 63, 724-736 (2007).
23. Garcia-Salcedo, J. A., Gijon, P., Nolan, D. P., Tebabi, P. & Pays, E. A chromosomal SIR2 homologue with both histone NAD-dependent ADP-ribosyltransferase and deacetylase activities is involved in DNA repair in Trypanosoma brucei. EMBO J. 22, 5851-5862 (2003).
24. Cloos, P. A., Christensen, J., Agger, K. & Helin, K. Erasing the methyl mark: Histone demethylases at the center of cellular differentiation and disease. Genes Dev. 22, 1115-1140 (2008).
25. Bedford, M. T. & Clarke, S. G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13 (2009).
26. Wysocka, J., Allis, C. D. & Coonrod, S. Histone arginine methylation and its dynamic regulation. Front. Biosci. 11, 344-355 (2006).
27. Pelletier, M., Pasternack, D. A. & Read, L. K. In vitro and in vivo analysis of the major type I protein arginine methyltransferase from Trypanosoma brucei. Mol. Biochem. Parasitol. 144, 206-217 (2005).
28. Pasternack, D. A., Sayegh, J., Clarke, S. & Read, L. K. Evolutionarily divergent type II protein arginine methyltransferase in Trypanosoma brucei. Eukaryot. Cell 6, 1665-1681 (2007).
29. Fisk, J. C. et al. A type III protein arginine methyltransferase from the protozoan parasite, Trypanosoma brucei. J. Biol. Chem. 284, 11590-11600 (2009).
30. Lowell, J. E. & Cross, G. A. A variant histone H3 is enriched at telomeres in Trypanosoma brucei. J. Cell Sci. 117, 5937-5947 (2004).
31. Lowell, J. E., Kaiser, F., Janzen, C. J. & Cross, G. A. Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei. J. Cell Sci. 118, 5721-5730 (2005).
32. Alsford, S. & Horn, D. Trypanosomatid histones. Mol. Microbiol. 53, 365-372 (2004).
33. Sullivan, W. J. Jr, Naguleswaran, A. & Angel, S. O. Histones and histone modifications in protozoan parasites. Cell. Microbiol. 8, 1850-1861 (2006).
34. Thatcher, T. H. & Gorovsky, M. A. Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res. 22, 174-179 (1994).
35. da Cunha, J. P., Nakayasu, E. S., de Almeida, I. C. & Schenkman, S. Post-translational modifications of Trypanosoma cruzi histone H4. Mol. Biochem. Parasitol. 150, 268-277 (2006).
36. Latham, J. A. & Dent, S. Y. Cross-regulation of histone modifications. Nature Struct. Mol. Biol. 14, 1017-1024 (2007).
37. Briggs, S. D. et al. Gene silencing: Trans-histone regulatory pathway in chromatin. Nature 418, 498 (2002).
38. Sun, Z. W. & Allis, C. D. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418, 104-108 (2002).
39. Mandava, V., Janzen, C. J. & Cross, G. A. Trypanosome H2Bv replaces H2B in nucleosomes enriched for H3 K4 and K76 trimethylation. Biochem. Biophys. Res. Commun. 368, 846-851 (2008).
40. Hyland, E. M. et al. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol. Cell. Biol. 25, 10060-10070 (2005).
41. Shilatifard, A. Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annu. Rev. Biochem. 75, 243-269 (2006).
42. Steger, D. J. et al. DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol. 28, 2825-2839 (2008).
43. San-Segundo, P. A. & Roeder, G. S. Role for the silencing protein Dot1 in meiotic checkpoint control. Mol. Biol. Cell 11, 3601-3615 (2000).
44. Huyen, Y. et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406-411 (2004).
45. Janzen, C. J., Hake, S. B., Lowell, J. E. & Cross, G. A. M. Selective di- or trimethylation of histone H3 lysine 76 by two DOT1 homologs is important for cell cycle regulation in Trypanosoma brucei. Mol. Cell 23, 497-507 (2006).
46. Grant, P. A. & Berger, S. L. Histone acetyltransferase complexes. Semin. Cell Dev. Biol. 10, 169-177 (1999).
47. Tachibana, M. et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779-1791 (2002).
48. Brownell, J. E. & Allis, C. D. Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr. Opin. Genet. Dev. 6, 176-184 (1996).
49. Sterner, D. E. & Berger, S. L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64 435-459 (2000).
50. Siegel, T. N. et al. Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev. 23, 1063-1076 (2009).
51. Schotta, G. et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18 1251-1262 (2004).
52. Schotta, G. et al. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22, 2048-2061 (2008).
53. Donati, G. et al. An NF-Y-dependent switch of positive and negative histone methyl marks on CCAAT promoters. PLoS ONE 3 e2066 (2008).
54. Ruthenburg, A. J., Li, H., Patel, D. J. & Allis, C. D. Multivalent engagement of chromatin modifications by linked binding modules. Nature Rev. Mol. Cell Biol. 8, 983-994 (2007).
55. Taverna, S. D., Li, H., Ruthenburg, A. J., Allis, C. D. & Patel, D. J. How chromatin-binding modules interpret histone modifications: Lessons from professional pocket pickers. Nature Struct. Mol. Biol. 14 1025-1040 (2007).
56. Colot, V. & Rossignol, J. L. Eukaryotic DNA methylation as an evolutionary device. Bioessays 21, 402-411 (1999).
57. Robertson, K. D. DNA methylation and human disease. Nature Rev. Genet. 6, 597-610 (2005).
58. Rojas, M. V. & Galanti, N. DNA methylation in Trypanosoma cruzi. FEBS Lett. 263, 113-116 (1990).
59. Militello, K. T. et al. African trypanosomes contain 5-methylcytosine in nuclear DNA. Eukaryot. Cell 7, 2012-2016 (2008).
60. Gommers-Ampt, J. H. et al. β-D-glucosyl-hydroxymethyluracil: A novel modified base present in the DNA of the parasitic protozoan T. brucei. Cell 75, 1129-1136 (1993).
61. Borst, P. & Sabatini, R. Base J: Discovery, biosynthesis, and possible functions. Annu. Rev. Microbiol. 62, 235-251 (2008).
62. Kieft, R. et al. JBP2, a SWI2/SNF2-like protein, regulates de novo telomeric DNA glycosylation in bloodstream form Trypanosoma brucei. Mol. Biochem. Parasitol. 156, 24-31 (2007).
63. Yu, Z. et al. The protein that binds to DNA base J in trypanosomatids has features of a thymidine hydroxylase. Nucleic Acids Res. 35, 2107-2115 (2007).
64. Cliffe, L. J. et al. JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes. Nucleic Acids Res. 37, 1452-1462 (2009).
65. Genest, P. A. et al. Formation of linear inverted repeat amplicons following targeting of an essential gene in Leishmania. Nucleic Acids Res. 33, 1699-1709 (2005).
66. McStay, B. & Grummt, I. The Epigenetics of rRNA genes: From molecular to chromosome biology. Annu. Rev. Cell Dev. Biol. 24, 131-157 (2008).
67. Berriman, M. et al. The genome of the African trypanosome Trypanosoma brucei. Science 309, 416-422 (2005).
68. Alsford, S., Kawahara, T., Glover, L. & Horn, D. Tagging a T. brucei RRNA locus improves stable transfection efficiency and circumvents inducible expression position effects. Mol. Biochem. Parasitol. 144, 142-148 (2005).
69. Waters, A. P., Syin, C. & McCutchan, T. F. Developmental regulation of stage-specific ribosome populations in Plasmodium. Nature 342 438-440 (1989).
70. Waters, A. P. et al. Species-specific regulation and switching of transcription between stage-specific ribosomal RNA genes in Plasmodium berghei. J. Biol. Chem. 272, 3583-3589 (1997).
71. McCracken, S. et al. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385, 357-361 (1997).
72. Kooter, J. M. & Borst, P. α-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes. Nucleic Acids Res. 12, 9457-9472 (1984).
73. Rudenko, G., Bishop, D., Gottesdiener, K. & Van der Ploeg, L. H. α-amanitin resistant transcription of protein coding genes in insect and bloodstream form Trypanosoma brucei. EMBO J. 8, 4259-4263 (1989).
74. Hertz-Fowler, C. et al. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE 3, e3527 (2008).
75. Navarro, M. & Gull, K. A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414, 759-763 (2001).
76. Landeira, D. & Navarro, M. Nuclear repositioning of the VSG promoter during developmental silencing in Trypanosoma brucei. J. Cell Biol. 176, 133-139 (2007).
77. Scherf, A. et al. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J. 17, 5418-5426 (1998).
78. Chess, A., Simon, I., Cedar, H. & Axel, R. Allelic inactivation regulates olfactory receptor gene expression. Cell 78, 823-834 (1994).
79. Brandenburg, J. et al. Multifunctional class I transcription in Trypanosoma brucei depends on a novel protein complex. EMBO J. 26, 4856-4866 (2007).
80. Grune, T. et al. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 12, 449-460 (2003).
81. Sandell, L. L., Gottschling, D. E. & Zakian, V. A. Transcription of a yeast telomere alleviates telomere position effect without affecting chromosome stability. Proc. Natl Acad. Sci. USA 91, 12061-12065 (1994).
82. Freitas-Junior, L. H. et al. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121, 25-36 (2005).
83. Figueiredo, L. M., Janzen, C. J. & Cross, G. A. A histone methyltransferase modulates antigenic variation in African trypanosomes. PLoS Biol 6, e161 (2008).
84. Li, B., Espinal, A. & Cross, G. A. M. Trypanosome telomeres are protected by a homologue of mammalian TRF2. Mol. Cell. Biol. 25 5011-5021 (2005).
85. Yang, X., Figueiredo, L. M., Espinal, A., Okubo, E. & Li, B. RAP1 is essential for silencing telomeric Variant Surface Glycoprotein genes in Trypanosoma brucei. Cell 137, 99-109 (2009).
86. Margueron, R., Trojer, P. & Reinberg, D. The key to development: interpreting the histone code? Curr. Opin.t Genet. Dev. 15, 163-176 (2005).
87. Schlimme, W., Burri, M., Bender, K., Betschart, B. & Hecker, H. Trypanosoma brucei brucei: Differences in the nuclear chromatin of bloodstream forms and procyclic culture forms. Parasitology 107 237-247 (1993).
88. Burri, M., Schlimme, W., Betschart, B. & Hecker, H. Characterization of the histones of Trypanosoma brucei brucei bloodstream forms. Acta Trop. 58, 291-305 (1994).
89. Rout, M. P. & Field, M. C. Isolation and characterization of subnuclear compartments from Trypanosoma brucei. Identification of a major repetitive nuclear lamina component. J. Biol. Chem. 276, 38261-38271 (2001).
90. Ziegelbauer, K., Quinten, M., Schwarz, H., Pearson, T. W. & Overath, P. Synchronous differentiation of Trypanosoma brucei from bloodstream to procyclic forms in vitro. Eur. J. Biochem. 192, 373-378 (1990).
91. Ogbadoyi, E., Ersfeld, K., Robinson, D., Sherwin, T. & Gull, K. Architecture of the Trypanosoma brucei nucleus during interphase and mitosis. Chromosoma 108, 501-513 (2000).
92. Hammarton, T. C. Cell cycle regulation in Trypanosoma brucei. Mol. Biochem. Parasitol. 153, 1-8 (2007).
93. Hirumi, H. & Hirumi, K. Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J. Parasitol. 75, 985-989 (1989).
94. Carruthers, V. B. & Cross, G. A. High-efficiency clonal growth of bloodstream- and insect-form Trypanosoma brucei on agarose plates. Proc. Natl Acad. Sci. USA 89, 8818-8821 (1992).
95. LaCount, D. J., Bruse, S., Hill, K. L. & Donelson, J. E. Double-stranded RNA interference in Trypanosoma brucei using head-to-head promoters. Mol. Biochem. Parasitol. 111, 67-76 (2000).
96. Wang, Z., Morris, J. C., Drew, M. E. & Englund, P. T. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275, 40174-40179 (2000).
97. Scahill, M. D., Pastar, I. & Cross, G. A. CRE recombinase-based positive-negative selection systems for genetic manipulation in Trypanosoma brucei. Mol. Biochem. Parasitol. 157, 73-82 (2008).
98. Pays, E. Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol. 21, 517-520 (2005).
99. Scherf, A., Lopez-Rubio, J. J. & Riviere, L. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62, 445-470 (2008).
100. Buck, L. & Axel, R. A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 65, 175-187 (1991).
101. Voss, T. S. et al. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439, 1004-1008 (2006).
102. Lopez-Rubio, J. J. et al. 5′ flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol. Microbiol. 66 1296-1305 (2007).
103. Nguyen, M. Q., Zhou, Z., Marks, C. A., Ryba, N. J. & Belluscio, L. Prominent roles for odorant receptor coding sequences in allelic exclusion. Cell 131, 1009-1017 (2007).
104. Frank, M. et al. Strict pairing of var promoters and introns is required for var gene silencing in the malaria parasite Plasmodium falciparum. J. Biol. Chem. 281, 9942-9952 (2006).
105. Klose, R. J. & Zhang, Y. Regulation of histone methylation by demethylimination and demethylation. Nature Rev. Mol. Cell Biol. 8, 307-318 (2007).
106. Amiguet-Vercher, A. et al. Loss of the mono-allelic control of the VSG expression sites during the development of Trypanosoma brucei in the bloodstream. Mol. Microbiol. 51, 1577-1588 (2004).
107. Dean, S., Marchetti, R., Kirk, K. & Matthews, K. R. A surface transporter family conveys the trypanosome differentiation signal. Nature 459, 213-217 (2009).