Glucosylated hydroxymethyluracil, DNA base J, prevents transcriptional readthrough in Leishmania

Cell

Volumn 150, Issue 5, 2012, Pages 909-921

  Van Luenen, Henri G A M ^a   Farris, Carol ^b,c   Jan, Sabrina ^a   Genest, Paul Andre ^a   Tripathi, Pankaj ^a   Velds, Arno ^a   Kerkhoven, Ron M ^a   Nieuwland, Marja ^a   Haydock, Andrew ^b   Ramasamy, Gowthaman ^b   Vainio, Saara ^a   Heidebrecht, Tatjana ^a   Perrakis, Anastassis ^a   Pagie, Ludo ^a   Van Steensel, Bas ^a   Myler, Peter J ^b,c   Borst, Piet ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLURACIL; BETA DEXTRO GLUCOSYL HYDROXYMETHYLURACIL; BROXURIDINE; J BINDING PROTEIN 2; RNA BINDING PROTEIN; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CELL DEATH; CHROMOSOME STRUCTURE; CLONING; CULTURE MEDIUM; LEISHMANIA MAJOR; LEISHMANIA TARENTOLAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCRIPTION TERMINATION; WILD TYPE;

EID: 84865683794     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.07.030     Document Type: Article

References (76)

1. N. Agabian Trans splicing of nuclear pre-mRNAs Cell 61 1990 1157 1160
2. C.D. Armour, J.C. Castle, R. Chen, T. Babak, P. Loerch, S. Jackson, J.K. Shah, J. Dey, C.A. Rohl, J.M. Johnson, and C.K. Raymond Digital transcriptome profiling using selective hexamer priming for cDNA synthesis Nat. Methods 6 2009 647 649
3. C. Beisel, and R. Paro Silencing chromatin: comparing modes and mechanisms Nat. Rev. Genet. 12 2011 123 135
4. S.I. Belli, S. Monnerat, C. Schaff, S. Masina, T. Noll, P.J. Myler, K. Stuart, and N. Fasel Sense and antisense transcripts in the histone H1 (HIS-1) locus of Leishmania major Int. J. Parasitol. 33 2003 965 975
5. M. Berriman, E. Ghedin, C. Hertz-Fowler, G. Blandin, H. Renauld, D.C. Bartholomeu, N.J. Lennard, E. Caler, N.E. Hamlin, and B. Haas The genome of the African trypanosome Trypanosoma brucei Science 309 2005 416 422
6. J.C. Boothroyd, and G.A.M. Cross Transcripts coding for variant surface glycoproteins of Trypanosoma brucei have a short, identical exon at their 5′ end Gene 20 1982 281 289
7. P. Borst, and C. Weissmann Replication of viral RNA, 8. Studies on the enzymatic mechanism of replication of MS2 RNA Proc. Natl. Acad. Sci. USA 54 1965 982 987
8. P. Borst, and R. Sabatini Base J: discovery, biosynthesis, and possible functions Annu. Rev. Microbiol. 62 2008 235 251
9. L.J. Cliffe, R. Kieft, T. Southern, S.R. Birkeland, M. Marshall, K. Sweeney, and R. Sabatini JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes Nucleic Acids Res. 37 2009 1452 1462
10. L.J. Cliffe, T.N. Siegel, M. Marshall, G.A. Cross, and R. Sabatini Two thymidine hydroxylases differentially regulate the formation of glucosylated DNA at regions flanking polymerase II polycistronic transcription units throughout the genome of Trypanosoma brucei Nucleic Acids Res. 38 2010 3923 3935
11. M. Cross, R. Kieft, R. Sabatini, M. Wilm, M. de Kort, G.A. van der Marel, J.H. van Boom, F. van Leeuwen, and P. Borst The modified base J is the target for a novel DNA-binding protein in kinetoplastid protozoans EMBO J. 18 1999 6573 6581
12. M. Cross, R. Kieft, R. Sabatini, A. Dirks-Mulder, I. Chaves, and P. Borst J-binding protein increases the level and retention of the unusual base J in trypanosome DNA Mol. Microbiol. 46 2002 37 47
13. T. De Lange, A.Y. Liu, L.H. Van der Ploeg, P. Borst, M.C. Tromp, and J.H. Van Boom Tandem repetition of the 5′ mini-exon of variant surface glycoprotein genes: a multiple promoter for VSG gene transcription? Cell 34 1983 891 900
14. T. De Lange, T.M. Berkvens, H.J. Veerman, A.C. Frasch, J.D. Barry, and P. Borst Comparison of the genes coding for the common 5′ terminal sequence of messenger RNAs in three trypanosome species Nucleic Acids Res. 12 1984 4431 4443
15. C. DiPaolo, R. Kieft, M. Cross, and R. Sabatini Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein Mol. Cell 17 2005 441 451
16. D. Dooijes, I. Chaves, R. Kieft, A. Dirks-Mulder, W. Martin, and P. Borst Base J originally found in kinetoplastida is also a minor constituent of nuclear DNA of Euglena gracilis Nucleic Acids Res. 28 2000 3017 3021
17. Fde.M. Dossin, A. Dufour, E. Dusch, J.L. Siqueira-Neto, C.B. Moraes, G.S. Yang, M.I. Cano, A. Genovesio, and L.H. Freitas-Junior Automated nuclear analysis of Leishmania major telomeric clusters reveals changes in their organization during the parasite's life cycle PLoS ONE 3 2008 e2313
18. R. Edgar, M. Domrachev, and A.E. Lash Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Nucleic Acids Res. 30 2002 207 210
19. D.K. Ekanayake, T. Minning, B. Weatherly, K. Gunasekera, D. Nilsson, R. Tarleton, T. Ochsenreiter, and R. Sabatini Epigenetic regulation of transcription and virulence in Trypanosoma cruzi by O-linked thymine glucosylation of DNA Mol. Cell. Biol. 31 2011 1690 1700
20. N.M. El-Sayed, P.J. Myler, D.C. Bartholomeu, D. Nilsson, G. Aggarwal, A.N. Tran, E. Ghedin, E.A. Worthey, A.L. Delcher, and G. Blandin The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease Science 309 2005 409 415
21. N.M. El-Sayed, P.J. Myler, G. Blandin, M. Berriman, J. Crabtree, G. Aggarwal, E. Caler, H. Renauld, E.A. Worthey, and C. Hertz-Fowler Comparative genomics of trypanosomatid parasitic protozoa Science 309 2005 404 409
22. B.A. Flusberg, D.R. Webster, J.H. Lee, K.J. Travers, E.C. Olivares, T.A. Clark, J. Korlach, and S.W. Turner Direct detection of DNA methylation during single-molecule, real-time sequencing Nat. Methods 7 2010 461 465
23. M. Fujii, K. Miki, S. Takayama, and D. Ayusawa Identification of genes that affect sensitivity to 5-bromodeoxyuridine in the yeast Saccharomyces cerevisiae Mol. Genet. Genomics 283 2010 461 468
24. P.A. Genest, B. ter Riet, C. Dumas, B. Papadopoulou, H.G.A.M. van Luenen, and P. Borst Formation of linear inverted repeat amplicons following targeting of an essential gene in Leishmania Nucleic Acids Res. 33 2005 1699 1709
25. P.A. Genest, B. Ter Riet, T. Cijsouw, H.G. van Luenen, and P. Borst Telomeric localization of the modified DNA base J in the genome of the protozoan parasite Leishmania Nucleic Acids Res. 35 2007 2116 2124
26. J.H. Gommers-Ampt, F. Van Leeuwen, A.L. de Beer, J.F. Vliegenthart, M. Dizdaroglu, J.A. Kowalak, P.F. Crain, and P. Borst β-D-glucosyl- hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T. brucei Cell 75 1993 1129 1136
27. R.K. Grover, S.J. Pond, Q. Cui, P. Subramaniam, D.A. Case, D.P. Millar, and P. Wentworth Jr. O-glycoside orientation is an essential aspect of base J recognition by the kinetoplastid DNA-binding protein JBP1 Angew. Chem. Int. Ed. Engl. 46 2007 2839 2843
28. T. Heidebrecht, E. Christodoulou, M.J. Chalmers, S. Jan, B. Ter Riet, R.K. Grover, R.P. Joosten, D. Littler, H. van Luenen, and P.R. Griffin The structural basis for recognition of base J containing DNA by a novel DNA binding domain in JBP1 Nucleic Acids Res. 39 2011 5715 5728
29. A.C. Ivens, C.S. Peacock, E.A. Worthey, L. Murphy, G. Aggarwal, M. Berriman, E. Sisk, M.A. Rajandream, E. Adlem, and R. Aert The genome of the kinetoplastid parasite, Leishmania major Science 309 2005 436 442
30. L.M. Iyer, M. Tahiliani, A. Rao, and L. Aravind Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids Cell Cycle 8 2009 1698 1710
31. A.P. Jackson, M. Sanders, A. Berry, J. McQuillan, M.A. Aslett, M.A. Quail, B. Chukualim, P. Capewell, A. MacLeod, and S.E. Melville The genome sequence of Trypanosoma brucei gambiense, causative agent of chronic human african trypanosomiasis PLoS Negl. Trop. Dis. 4 2010 e658
32. J.M. Kooter, and P. Borst α-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes Nucleic Acids Res. 12 1984 9457 9472
33. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
34. L.F. Lye, K. Owens, H. Shi, S.M. Murta, A.C. Vieira, S.J. Turco, C. Tschudi, E. Ullu, and S.M. Beverley Retention and loss of RNA interference pathways in trypanosomatid protozoans PLoS Pathog. 6 2010 e1001161
35. S. Martínez-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 Mol. Cell 11 2003 1291 1299
36. S. Martínez-Calvillo, D. Nguyen, K. Stuart, and P.J. Myler Transcription initiation and termination on Leishmania major chromosome 3 Eukaryot. Cell 3 2004 506 517
37. K. Miki, M. Shimizu, M. Fujii, S. Takayama, M.N. Hossain, and D. Ayusawa 5-bromodeoxyuridine induces transcription of repressed genes with disruption of nucleosome positioning FEBS J. 277 2010 4539 4548
38. S. Monnerat, S. Martinez-Calvillo, E. Worthey, P.J. Myler, K.D. Stuart, and N. Fasel Genomic organization and gene expression in a chromosomal region of Leishmania major Mol. Biochem. Parasitol. 134 2004 233 243
39. P.J. Myler, L. Audleman, T. deVos, G. Hixson, P. Kiser, C. Lemley, C. Magness, E. Rickel, E. Sisk, and S. Sunkin Leishmania major Friedlin chromosome 1 has an unusual distribution of protein-coding genes Proc. Natl. Acad. Sci. USA 96 1999 2902 2906
40. P.J. Myler, E. Sisk, P.D. McDonagh, S. Martinez-Calvillo, A. Schnaufer, S.M. Sunkin, S. Yan, R. Madhubala, A. Ivens, and K. Stuart Genomic organization and gene function in Leishmania Biochem. Soc. Trans. 28 2000 527 531
41. R.G. Nelson, M. Parsons, P.J. Barr, K. Stuart, M. Selkirk, and N. Agabian Sequences homologous to the variant antigen mRNA spliced leader are located in tandem repeats and variable orphons in trypanosoma brucei Cell 34 1983 901 909
42. T. Otto, G. Dillon, W. Degrave, and M. Berriman RATT: Rapid Annotation Transfer Tool Nucleic Acids Res. 39 2011 e57
43. N.E. Padilla-Mejía, L.E. Florencio-Martínez, E.E. Figueroa-Angulo, R.G. Manning-Cela, R. Hernández-Rivas, P.J. Myler, and S. Martínez-Calvillo Gene organization and sequence analyses of transfer RNA genes in Trypanosomatid parasites BMC Genomics 10 2009 232
44. F. Raymond, S. Boisvert, G. Roy, J.-F. Ritt, D. Legare, A. Isnard, M. Stanke, M. Olivier, M.J. Tremblay, and B. Papadopoulou Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species Nucleic Acids Res. 40 2012 1131 1147
45. P. Richard, and J.L. Manley Transcription termination by nuclear RNA polymerases Genes Dev. 23 2009 1247 1269
46. K.A. Robinson, and S.M. Beverley Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania Mol. Biochem. Parasitol. 128 2003 217 228
47. R. Sabatini, N. Meeuwenoord, J.H. van Boom, and P. Borst Recognition of base J in duplex DNA by J-binding protein J. Biol. Chem. 277 2002 958 966
48. P.J. Schatz Use of peptide libraries to map the substrate specificity of a peptide-modifying enzyme: a 13 residue consensus peptide specifies biotinylation in Escherichia coli Biotechnology (N.Y.) 11 1993 1138 1143
49. K.E. Shearwin, B.P. Callen, and J.B. Egan Transcriptional interference - a crash course Trends Genet. 21 2005 339 345
50. T.N. Siegel, D.R. Hekstra, L.E. Kemp, L.M. Figueiredo, J.E. Lowell, D. Fenyo, X. Wang, S. Dewell, and G.A. Cross Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei Genes Dev. 23 2009 1063 1076
51. A.G. Simpson, J.R. Stevens, and J. Lukes The evolution and diversity of kinetoplastid flagellates Trends Parasitol. 22 2006 168 174
52. J.R. Stevens Kinetoplastid phylogenetics, with special reference to the evolution of parasitic trypanosomes Parasite 15 2008 226 232
53. R.E. Sutton, and J.C. Boothroyd Evidence for trans splicing in trypanosomes Cell 47 1986 527 535
54. M. Tahiliani, K.P. Koh, Y. Shen, W.A. Pastor, H. Bandukwala, Y. Brudno, S. Agarwal, L.M. Iyer, D.R. Liu, L. Aravind, and A. Rao Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 Science 324 2009 930 935
55. 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 10 2009 152
56. C.B. Toaldo, R. Kieft, A. Dirks-Mulder, R. Sabatini, H.G. van Luenen, and P. Borst A minor fraction of base J in kinetoplastid nuclear DNA is bound by the J-binding protein 1 Mol. Biochem. Parasitol. 143 2005 111 115
57. E. Ullu, K.R. Matthews, and C. Tschudi Temporal order of RNA-processing reactions in trypanosomes: rapid trans splicing precedes polyadenylation of newly synthesized tubulin transcripts Mol. Cell. Biol. 13 1993 720 725
58. S. Vainio, P.A. Genest, B. ter Riet, H.G.A.M. van Luenen, and P. Borst Evidence that J-binding protein 2 is a thymidine hydroxylase catalyzing the first step in the biosynthesis of DNA base J Mol. Biochem. Parasitol. 164 2009 157 161
59. L.H.T. Van der Ploeg, A.Y.C. Liu, P.A.M. Michels, T. De Lange, P. Borst, H.K. Majumder, H. Weber, G.H. Veeneman, and J. Van Boom RNA splicing is required to make the messenger RNA for a variant surface antigen in trypanosomes Nucleic Acids Res. 10 1982 3591 3604
60. F. van Leeuwen, E.R. Wijsman, E. Kuyl-Yeheskiely, G.A. van der Marel, J.H. van Boom, and P. Borst The telomeric GGGTTA repeats of Trypanosoma brucei contain the hypermodified base J in both strands Nucleic Acids Res. 24 1996 2476 2482
61. F. van Leeuwen, E.R. Wijsman, R. Kieft, G.A. van der Marel, J.H. van Boom, and P. Borst Localization of the modified base J in telomeric VSG gene expression sites of Trypanosoma brucei Genes Dev. 11 1997 3232 3241
62. F. van Leeuwen, R. Kieft, M. Cross, and P. Borst Biosynthesis and function of the modified DNA base β-D-glucosyl-hydroxymethyluracil in Trypanosoma brucei Mol. Cell. Biol. 18 1998 5643 5651
63. F. van Leeuwen, M.C. Taylor, A. Mondragon, H. Moreau, W. Gibson, R. Kieft, and P. Borst β-D-glucosyl-hydroxymethyluracil is a conserved DNA modification in kinetoplastid protozoans and is abundant in their telomeres Proc. Natl. Acad. Sci. USA 95 1998 2366 2371
64. F. van Leeuwen, R. Kieft, M. Cross, and P. Borst Tandemly repeated DNA is a target for the partial replacement of thymine by β-D-glucosyl- hydroxymethyluracil in Trypanosoma brucei Mol. Biochem. Parasitol. 109 2000 133 145
65. C. Weissmann, and P. Borst Double-stranded ribonucleic acid formation in vitro by MS 2 phage-induced RNA synthetase Science 142 1963 1188 1191
66. E.A. Worthey, S. Martinez-Calvillo, A. Schnaufer, G. Aggarwal, J. Cawthra, G. Fazelinia, C. Fong, G. Fu, M. Hassebrock, and G. Hixson Leishmania major chromosome 3 contains two long convergent polycistronic gene clusters separated by a tRNA gene Nucleic Acids Res. 31 2003 4201 4210
67. J.R. Wright, T.N. Siegel, and G.A. Cross Histone H3 trimethylated at lysine 4 is enriched at probable transcription start sites in Trypanosoma brucei Mol. Biochem. Parasitol. 172 2010 141 144
68. Z. Yu, P.A. Genest, B. ter Riet, K. Sweeney, C. DiPaolo, R. Kieft, E. Christodoulou, A. Perrakis, J.M. Simmons, and R.P. Hausinger The protein that binds to DNA base J in trypanosomatids has features of a thymidine hydroxylase Nucleic Acids Res. 35 2007 2107 2115
69. Brun, R., and Schönenberger, M. (1979). Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop. 36, 289-292.
70. El-Sayed, N.M., Myler, P.J., Bartholomeu, D.C., Nilsson, D., Aggarwal, G., Tran, A.N., Ghedin, E., Worthey, E.A., Delcher, A.L., Blandin, G., et al. (2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409-415.
71. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
72. Luna-Vargas, M.P.A., Christodoulou, E., Alfieri, A., van Dijk, W.J., Stadnik, M., Hibbert, R.G., Sahtoe, D.D., Clerici, M., Marco, V.D., Littler, D., et al. (2011). Enabling high-throughput ligation-independent cloning and protein expression for the family of ubiquitin specific proteases. J. Struct. Biol. 175, 113-119.
73. Matthijnssens, J., Ciarlet, M., Rahman, M., Attoui, H., Bányai, K., Estes, M.K., Gentsch, J.R., Iturriza-Gómara, M., Kirkwood, C.D., Martella, V., et al. (2008). Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 153, 1621-1629.
74. Ozsolak, F., and Milos, P.M. (2011). RNA sequencing: advances, challenges and opportunities. Nat. Rev. Genet. 12, 87-98.
75. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A., and Barrell, B. (2000). Artemis: sequence visualization and annotation. Bioinformatics 16, 944-945.
76. Winter, E., Yamamoto, F., Almoguera, C., and Perucho, M. (1985). A method to detect and characterize point mutations in transcribed genes: amplification and overexpression of the mutant c-Ki-ras allele in human tumor cells. Proc. Natl. Acad. Sci. USA 82, 7575-7579.