Regulation of transcription termination by glucosylated hydroxymethyluracil, base J, in Leishmania major and Trypanosoma brucei

Nucleic Acids Research

Volumn 42, Issue 15, 2014, Pages 9717-9729

  Reynolds, David ^a   Cliffe, Laura ^a   Förstner, Konrad U ^b   Hon, Chung Chau ^c,d   Siegel, T Nicolai ^b   Sabatini, Robert ^a  

^a University of Georgia   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c INSTITUT PASTEUR   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BASE J; BROXURIDINE; COMPLEMENTARY RNA; UNCLASSIFIED DRUG; URACIL DERIVATIVE; 5-((GLUCOPYRANOSYLOXY)METHYL)URACIL; GLUCOSIDE; PROTOZOAL RNA; RNA POLYMERASE II; URACIL;

ARTICLE; CONTROLLED STUDY; ENZYME REGULATION; GENE CLUSTER; GENE DELETION; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC ASSOCIATION; LEISHMANIA MAJOR; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; TRYPANOSOMA BRUCEI; UPREGULATION; ANALOGS AND DERIVATIVES; CELL LINE; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; TRYPANOSOMA BRUCEI BRUCEI;

CELL LINE; GENE EXPRESSION REGULATION; GLUCOSIDES; LEISHMANIA MAJOR; RNA POLYMERASE II; RNA, PROTOZOAN; TRANSCRIPTION TERMINATION, GENETIC; TRYPANOSOMA BRUCEI BRUCEI; URACIL;

EID: 84925398641     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku714     Document Type: Article

References (56)

1. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D.C., Lennard, N.J., Caler, E., Hamlin, N.E., Haas, B. et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science, 309, 416-422.
2. Jackson, A.P., Sanders, M., Berry, A., McQuillan, J., Aslett, M.A., Quail, M.A., Chukualim, B., Capewell, P., MacLeod, A., Melville, S.E. et al. (2010) The genome sequence of Trypanosoma brucei gambiense, causative agent of chronic human african trypanosomiasis. PLoS Negl. Trop. Dis., 4, e658.
3. El-Sayed, N.M., Myler, P.J., Blandin, G., Berriman, M., Crabtree, J., Aggarwal, G., Caler, E., Renauld, H., Worthey, E.A., Hertz-Fowler, C. et al. (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science, 309, 404-409.
4. Martinez-Calvillo, S., Yan, S., Nguyen, D., Fox, M., Stuart, K. and Myler, P.J. (2003) Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol. Cell, 11, 1291-1299.
5. Siegel, T.N., Hekstra, D.R., Kemp, L.E., Figueiredo, L.M., Lowell, J.E., Fenyo, D., Wang, X., Dewell, S. and Cross, G.A. (2009) Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev., 23, 1063-1076.
6. Thomas, S., Green, A., Sturm, N.R., Campbell, D.A. and Myler, P.J. (2009) Histone acetylations mark origins of polycistronic transcription in Leishmania major. BMC Genomics, 10, 152.
7. Kolev, N.G., Franklin, J.B., 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.
8. Boothroyd, J.C. and Cross, G.A. (1982) Transcripts coding for variant surface glycoproteins of Trypanosoma brucei have a short, identical exon at their 5' end. Gene, 20, 281-289.
9. Van der Ploeg, L.H., Liu, A.Y., Michels, P.A., De Lange, T.D., Borst, P., Majumder, H.K., Weber, H., Veeneman, G.H. and Van Boom, J. (1982) RNA splicing is required to make the messenger RNA for a variant surface antigen in trypanosomes. Nucleic Acids Res., 10, 3591-3604.
10. De Lange, T., Liu, A.Y., Van der Ploeg, L.H., Borst, P., Tromp, M.C. and Van Boom, J.H. (1983) Tandem repetition of the 5' mini-exon of variant surface glycoprotein genes: a multiple promoter for VSG gene transcription? Cell, 34, 891-900.
11. Nelson, R.G., Parsons, M., Barr, P.J., Stuart, K., Selkirk, M. and Agabian, N. (1983) Sequences homologous to the variant antigen mRNA spliced leader are located in tandem repeats and variable orphons in Trypanosoma brucei. Cell, 34, 901-909.
12. Sutton, R.E. and Boothroyd, J.C. (1986) Evidence for Trans splicing in trypanosomes. Cell, 47, 527-535.
13. Agabian, N. (1990) Trans splicing of nuclear pre-mRNAs. Cell, 61, 1157-1160.
14. Gromak, N., West, S. and Proudfoot, N.J. (2006) Pause sites promote transcriptional termination of mammalian RNA polymerase II. Mol. Cell. Biol., 26, 3986-3996.
15. LeBowitz, J.H., Smith, H.Q., Rusche, L. and Beverley, S.M. (1993) Coupling of poly(A) site selection and trans-splicing in Leishmania. Genes Dev., 7, 996-1007.
16. Clayton, C.E. (2002) Life without transcriptional control? From fly to man and back again. EMBO J., 21, 1881-1888.
17. Campbell, D.A., Thomas, S. and Sturm, N.R. (2003) Transcription in kinetoplastid protozoa: why be normal? Microbes Infect., 5, 1231-1240.
18. Cliffe, L.J., Siegel, T.N., Marshall, M., Cross, G.A. and Sabatini, R. (2010) 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, 3923-3935.
19. 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.
20. van Leeuwen, F., Taylor, M.C., Mondragon, A., Moreau, H., Gibson, W., Kieft, R. and Borst, P. (1998) beta-D-glucosyl-hydroxymethyluracil is a conserved DNA modification in kinetoplastid protozoans and is abundant in their telomeres. Proc. Natl Acad. Sci. U.S.A., 95, 2366-2371.
21. Dooijes, D., Chaves, I., Kieft, R., Dirks-Mulder, A., Martin, W. and Borst, P. (2000) Base J originally found in kinetoplastid is also a minor constituent of nuclear DNA of Euglena gracilis. Nucleic Acids Res., 28, 3017-3021.
22. Gommers-Ampt, J.H., Van Leeuwen, F., de Beer, A.L., Vliegenthart, J.F., Dizdaroglu, M., Kowalak, J.A., Crain, P.F. and Borst, P. (1993) beta-D-glucosyl-hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T. brucei. Cell, 75, 1129-1136.
23. van Leeuwen, F., Kieft, R., Cross, M. and Borst, P. (2000) Tandemly repeated DNA is a target for the partial replacement of thymine by beta-D-glucosal-hydroxymethyluracil in Trypanosoma brucei. Mol. Biochem. Parasitol., 109, 133-145.
24. van Leeuwen, F., Wijsman, E.R., Kieft, R., van der Marel, G.A., van Boom, J.H. and Borst, P. (1997) Localization of the modified base J in telomeric VSG gene expression sites of Trypanosoma brucei. Genes Dev., 11, 3232-3241.
25. van Leeuwen, F., Wijsman, E.R., Kuyl-Yeheskiely, E., van der Marel, G.A., van Boom, J.H. and Borst, P. (1996) The telomeric GGGTTA repeats of Trypanosoma brucei contain the hypermodified base J in both strands. Nucleic Acids Res., 24, 2476-2482.
26. Ekanayake, D.K., Minning, T., Weatherly, B., Gunasekera, K., Nilsson, D., Tarleton, R., Ochsenreiter, T. and Sabatini, R. (2011) Epigenetic regulation of transcription and virulence in Trypanosoma cruzi by O-linked thymine glucosylation of DNA. Mol. Cell. Biol., 31, 1690-1700.
27. van Luenen, H.G., Farris, C., Jan, S., Genest, P.A., Tripathi, P., Velds, A., Kerkhoven, R.M., Nieuwland, M., Haydock, A., Ramasamy, G. et al. (2012) Glucosylated hydroxymethyluracil, DNA base J, prevents transcriptional readthrough in Leishmania. Cell, 150, 909-921.
28. Borst, P. and Sabatini, R. (2008) Base J: discovery, biosynthesis, and possible functions. Annu. Rev. Microbiol., 62, 235-251.
29. Cliffe, L.J., Hirsch, G., Wang, J., Ekanayake, D., Bullard, W., Hu, M., Wang, Y. and Sabatini, R. (2012) JBP1 and JBP2 proteins are Fe2+/2-oxoglutarate-dependent dioxygenases regulating hydroxylation of thymidine residues in trypanosome DNA. J. Biol. Chem., 287, 19886-19895.
30. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L. et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 324, 930-935.
31. Iyer, L.M., Tahiliani, M., Rao, A. and Aravind, L. (2009) Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle, 8, 1698-1710.
32. Kieft, R., Brand, V., Ekanayake, D.K., Sweeney, K., DiPaolo, C., Reznikoff, W.S. and Sabatini, R. (2007) JBP2, a SWI2/SNF2-like protein, regulates de novo telomeric DNA glycosylation in bloodstream form Trypanosoma brucei. Mol. Biochem. Parasitol., 156, 24-31.
33. Cross, M., Kieft, R., Sabatini, R., Dirks-Mulder, A., Chaves, I. and Borst, P. (2002) J binding protein increases the level and retention of the unusual base J in trypanosome DNA. Mol. Microbiol., 46, 37-47.
34. Cliffe, L.J., Kieft, R., Southern, T., Birkeland, S.R., Marshall, M., Sweeney, K. and Sabatini, R. (2009) JBP1 and JBP2 are two distinct thymidine hydroxylases involved in J biosynthesis in genomic DNA of African trypanosomes. Nucleic Acids Res., 37, 1452-1462.
35. Genest, P.A., ter Riet, B., Dumas, C., Papadopoulou, B., van Luenen, H.G. and Borst, P. (2005) Formation of linear inverted repeat amplicons following targeting of an essential gene in Leishmania. Nucleic Acids Res., 33, 1699-1709.
36. Ekanayake, D. and Sabatini, R. (2011) Epigenetic regulation of Pol II transcription initiation in Trypanosoma cruzi: modulation of nucleosome abundance, histone modification and polymerase occupancy by O-linked thymine DNA glucosylation. Eukaryot. Cell, 10, 1465-1472.
37. Michishita, E., Nakabayashi, K., Suzuki, T., Kaul, S.C., Ogino, H., Fujii, M., Mitsui, Y. and Ayusawa, D. (1999) 5-Bromodeoxyuridine induces senescence-like phenomena in mammalian cells regardless of cell type or species. J. Biochem., 126, 1052-1059.
38. Miki, K., Shimizu, M., Fujii, M., Takayama, S., Hossain, M.N. and Ayusawa, D. (2010) 5-bromodeoxyuridine induces transcription of repressed genes with disruption of nucleosome positioning. FEBS J., 277, 4539-4548.
39. Duque, A. and Rakic, P. (2011) Different effects of bromodeoxyuridine and [3H]thymidine incorporation into DNA on cell proliferation, position, and fate. J. Neurosci., 31, 15205-15217.
40. DiPaolo, C., Kieft, R., Cross, M. and Sabatini, R. (2005) Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein. Mol. Cell, 17, 441-451.
41. Kapler, G.M., Coburn, C.M. and Beverley, S.M. (1990) Stable transfection of the human parasite Leishmania major delineates a 30-kilobase region sufficient for extrachromosomal replication and expression. Mol. Cell. Biol., 10, 1084-1094.
42. Bernards, A., Van der Ploeg, L.H., Frasch, A.C., Borst, P., Boothroyd, J.C., Coleman, S. and Cross, G.A. (1981) Activation of trypanosome surface glycoprotein genes involves a duplicationtransposition leading to an altered 3' end. Cell, 27, 497-505.
43. Langmead, B. and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods, 9, 357-359.
44. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R. and Genome Project Data Processing, S. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
45. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
46. Abuin, G., Freitas-Junior, L.H.G., Colli, W., Alves, M.J.M. and Schenkman, S. (1999) Expression of trans-sialidase and 85-kDa glycoprotein genes in Trypanosoma cruzi is differentially regulated at the post-transcriptional level by labile protein factors. J. Biol. Chem., 274, 13041-13047.
47. Roditi, I., Schwarz, H., Pearson, T.W., Beecroft, R.P., Liu, M.K., Richardson, J.P., Bühring, H.J., Pleiss, J., Bülow, R. and Williams, R.O. (1989) Procyclin gene expression and loss of the variant surface glycoprotein during differentiation of Trypanosoma brucei. J. Cell Biol., 108, 737-746.
48. Al Husini, N., Kudla, P. and Ansari, A. (2013) A role for CF1A 3' end processing complex in promoter-associated transcription. PLoS Genet., 9, e1003722.
49. Fujii, M., Ito, H., Hasegawa, T., Suzuki, T., Adachi, N. and Ayusawa, D. (2002) 5-Bromo-2'-deoxyuridine efficiently suppresses division potential of the yeast Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem., 66, 906-909.
50. Tschudi, C., Fau, S.H. and Ullu, E. (2012) Small interfering RNA-producing loci in the ancient parasitic eukaryote Trypanosoma brucei. BMC Genomics, 13, 427.
51. Suzuki, T., Michishita, E., Ogino, H., Fujii, M. and Ayusawa, D. (2002) Synergistic induction of the senescence-associated genes by 5-bromodeoxyuridine and AT-binding ligands in HeLa cells. Exp. Cell Res., 276, 174-184.
52. Suzuki, T., Yaginuma, M., Oishi, T., Michishita, E., Ogino, H., Fujii, M. and Ayusawa, D. (2001) 5-Bromodeoxyuridine suppresses position effect variegation of transgenes in HeLa cells. Exp. Cell Res., 266, 53-63.
53. Hobson, D.J., Wei, W., Steinmetz, L.M. and Svejstrup, J.Q. (2012) RNA polymerase II collision interrupts convergent transcription. Mol. Cell, 48, 365-374.
54. Zheng, L.L., Wen, Y.Z., Yang, J.H., Liao, J.Y., Shao, P., Xu, H., Zhou, H., Wen, J.Z., Lun, Z.R., Ayala, F.J. et al. (2013) Comparative transcriptome analysis of small noncoding RNAs in different stages of Trypanosoma brucei. RNA, 19, 863-875.
55. Ngô, H., Tschudi, C., Gull, K. and Ullu, E. (1998) Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl Acad. Sci. U.S.A., 95, 14687-14692.
56. Kelly, S., Kramer, S., Schwede, A., Maini, P.K., Gull, K. and Carrington, M. (2012) Genome organization is a major component of gene expression control in response to stress and during the cell division cycle in trypanosomes. Open Biol., 2, 120033.