Defining the sequence requirements for the positioning of base J in DNA using SMRT sequencing

Nucleic Acids Research

Volumn 43, Issue 4, 2015, Pages 2102-2115

  Genest, Paul Andre ^a   Baugh, Loren ^b   Taipale, Alex ^b   Zhao, Wanqi ^a   Jan, Sabrina ^a   Van Luenen, Henri G A M ^a   Korlach, Jonas ^c   Clark, Tyson ^c   Luong, Khai ^c   Boitano, Matthew ^c   Turner, Steve ^c   Myler, Peter J ^b,d   Borst, Piet ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c PACIFIC BIOSCIENCES   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5-((GLUCOPYRANOSYLOXY)METHYL)URACIL; DNA BINDING PROTEIN; GLUCOSIDE; J-SPECIFIC DNA-BINDING PROTEIN, PROTOZOA; PROTOZOAL PROTEIN; URACIL;

ANALOGS AND DERIVATIVES; DNA SEQUENCE; GENETICS; LEISHMANIA; METABOLISM; PLASMID;

DNA-BINDING PROTEINS; GLUCOSIDES; LEISHMANIA; PLASMIDS; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; URACIL;

EID: 84945174290     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv095     Document Type: Article

References (50)

1. Bernards, A., De Lange, T., Michels, P.A., Lui, A.Y., Huisman, M.J., Borst, P. (1984) Two models of activation of a single surface antigen gene of Trypanosoma brucei. Cell, 36, 163-170.
2. Pays, E., Delauw, M.F., Laurent, M., Steinert, M. (1984) Possible DNA modification in GC dinucleotides of Trypanosoma brucei telomeric sequences; relationship with antigen gene transcription. Nucleic Acids Res., 12, 5235-5247.
3. Gommers-Ampt, J.H., Van Leeuwen, F., De Beer, A.L., Vliegenthart, J.F., Dizdaroglu, M., Kowalak, J.A., Crain, P.F., Borst, P. (1993)-D-glucosyl-hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T. brucei. Cell, 75, 1129-1136.
4. Van Leeuwen, F., Taylor, M.C., Mondragon, A., Moreau, H., Gobson, W., Kieft, R., Borst, P. (1998)-D-glucosyl-hydroxymethyluracil is a conserved DNA modification in kinetoplastid protozoans and is abundant in their telomeres. Proc. Natl. Acad. Sci. USA, 95, 2366-2371.
5. Dooijes, D., Chaves, I., Kieft, R., Dirks-Mulder, A., Martin, W., Borst, P. (2000) Base J origanally found in Kinetoplastida is also a minor constituent of nuclear DNA of Euglena gracilis. Nucleic Acids Res., 28, 3017-3021.
6. Liu, S., Ji, D., Sabatini, R., Wang, Y. (2014) Quantitative mass spectrometry-based analysis of-D-glucosyl-5-hydroxymethyluracil in genomic DNA of Trypanosoma brucei. J. Am. Soc. Mass. Spectrom., 25, 1763-1770.
7. Van Leeuwen, F., Kieft, R., Cross, M., Borst, P. (2000) Tandemly repeated DNA is a target for the partial replacement of thymine by-D-glucosyl-hydoxymethyluracil in Trypanosoma brucei. Mol. Biochem. Parasitol., 109, 133-145.
8. Van Leeuwen, F., Kieft, R., Cross, M., Borst, P. (1998) Biosynthesis and function of the modified DNA base-D-glucosyl-hydroxymethyluracil in Trypanosoma brucei. Mol. Cell. Biol., 18, 5643-5651.
9. Borst, P., Sabatini, R. (2008) Base J: discovery, biosynthesis, and possible functions. Annu. Rev. Microbiol., 62, 235-251.
10. Ulbert, S., Cross, M., Boorstein, R., Teebor, G., Borst, P. (2002) Expression of the human DNA glycosylase hSMUG1 in Trypanosoma brucei causes DNA damage and interferes with J biosynthesis. Nucleic Acids Res., 30, 3919-3926.
11. Iyer, L.M., Zhang, D., Maxwell Burroughs, A., Aravind, L. (2013) Computational identification of novel biochemical systems involved in oxidation, glycosylation and other complex modifications of bases in DNA. Nucleic Acids Res., 41, 7635-7655.
12. Bullard, W., Lopes da Rosa-Spiegler, J., Liu, S., Wang, Y., Sabatini, R. (2014) Identification of the glucosyltransferase that converts hydroxymethyluracil to base J in the trypanosomatid genome. J. Biol. Chem., 289, 20273-20282.
13. Sekar, A., Merritt, C., Baugh, L., Stuart, K., Myler, P.J. (2014) Tb927.10.6900 encodes the glucosyltransferase involved in synthesis of base J in Trypanosoma brucei. Mol. Biochem. Parasitol., 196, 9-11.
14. Yu, Z., Genest, P.A., Ter Riet, B., Sweeney, K., DiPaolo, C., Kieft, R., Christodoulou, E., Perrakis, A., Simmons, J., Hausinger, R. et al. (2007) The protein that binds to DNA base J in trypanosomatids has features of a thymidine hydroxylase. Nucleic Acids Res., 35, 2107-2115.
15. Tahiliani, M., Koh, K., Shen, Y., Pastor, W., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L., Liu, D., Aravind, L. et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 324, 930-935.
16. Cross, M., Kieft, R., Sabatini, R., Wilm, M., De Kort, M., Van der Marel, G.A., Van Boom, J.H., Van Leeuwen, F., Borst, P. (1999) The modified base J is the target for a novel DNA-binding protein in kinetoplastid protozoans. EMBO J., 18, 6573-6581.
17. Sabatini, R., Meeuwenoord, N., van Boom, J., Borst, P. (2002) Recognition of base J in duplex DNA by J-binding protein. J. Biol. Chem., 277, 958-966.
18. Sabatini, R., Meeuwenoord, N., van Boom, J., Borst, P. (2002) Site-specific interactions of JBP with base and sugar moieties in duplex J-DNA. Evidence for both major and minor groove contacts. J. Biol. Chem., 277, 28150-28156.
19. Heidebrecht, T., Christodoulou, E., Chalmers, M., Jan, S., Ter Riet, B., Grover, R., Joosten, R., Littler, D., van Luenen, H., Griffin, P. et al. (2011) The structural basis for recognition of base J containing DNA by a novel DNA binding domain in JBP1. Nucleic Acids Res., 39, 5715-5728.
20. Grover, R., Pond, S., Cui, Q., Subramaniam, P., Case, D., Millar, D., Wentworth, P. (2007) O-Glycoside orientation is an essential aspect of base J recognition by the kinetoplastid DNA-binding protein JBP1. Angew. Chem. Int. Ed., 46, 2839-2843.
21. Cliffe, L., Hirsch, G., Wang, J., Ekanayake, D., Bullard, W., Hu, M., Wang, Y., Sabatini, R. (2012) JBP1 and JBP2 proteins are Fe2oxoglutarate-dependent dioxygenases regulating hydroxylation of thymidine residues in trypanosome DNA. J. Biol. Chem., 287, 19886-19895.
22. DiPaolo, C., Kieft, R., Cross, M., Sabatini, R. (2005) Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein. Mol. Cell, 17, 441-451.
23. Cross, M., Kieft, R., Sabatini, R., Dirks-Mulder, A., Chaves, I., Borst, P. (2002) J-binding protein increases the level and retention of the unusual base J in trypanosome DNA. Mol. Microbiol., 46, 37-47.
24. Ekanayake, D., Minning, T., Weatherly, B., Gunasekera, K., Nilsson, D., Tarleton, R., Ochsenreiter, T., 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.
25. Genest, P.A., Ter Riet, B., Dumas, C., Papadopoulou, B., Van Luenen, H.G.A.M., Borst, P. (2005) Formation of linear inverted repeat amplicons following targeting of an essential gene in Leishmania. Nucleic Acids Res., 33, 1699-1709.
26. Kieft, R., Brand, V., Ekanayake, D., Sweeney, K., DiPaolo, C., Reznikoff, W., 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.
27. Vainio, S., Genest, P.A., Ter Riet, B., Van Luenen, H.G.A.M., Borst, P. (2009) 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, 157-161.
28. Genest, P.A., Ter Riet, B., Cijsouw, T., van Luenen, H., Borst, P. (2007) Telomeric localization of the modified DNA base J in the genome of the protozoan parasite Leishmania. Nucleic Acids Res., 35, 2116-2124.
29. Cliffe, L., Siegel, T.N., Marshall, M., Cross, G., 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.
30. Van Luenen, H.G.A.M., 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 read-through in Leishmania. Cell, 150, 909-921.
31. Reynolds, D., Cliffe, L., Förstner, K.U., Hon, C.-C., Siegel, T.N., Sabatini, R. (2014) Regulation of transcription termination by glucosylated hydroxymethyluracil, base J, in Leishmania major and Trypanosoma brucei. Nucleic Acids Res., 42, 9717-9729.
32. Van Leeuwen, F., Wijsman, E.R., Kuyl-Yeheskiely, E., Van der Marel, G.A., Van Boom, J.H., Borst, P. (1996) The telomeric GGGTTA repeats of Trypanosoma brucei contain the hypermodified base J in both strands. Nucleic Acids Res., 24, 2476-2482.
33. Cliffe, L., Kieft, R., Southern, T., Birkeland, S., Marshall, M., Sweeney, K., 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.
34. Eid, J., Fehr, A., Gray, J., Luong, K., Lyle, J., Otto, G., Peluso, P., Rank, D., Baybayan, P., Bettman, B. et al. (2009) Real-time DNA sequencing from single polymerase molecules. Science, 323, 133-138.
35. Flusberg, B., Webster, D., Lee, J., Travers, K., Olivares, E., Clark, T., Korlach, J., Turner, S. (2010) Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods, 7, 461-465.
36. Song, C., Clark, T., Lu, X., Kislyuk, A., Dai, Q., Turner, S., He, C., Korlach, J. (2012) Sensitive and specific single-molecule sequencing of 5-hydroxymethylcytosine. Nat. Methods, 9, 75-77.
37. Clark, T., Spittle, K., Turner, S., Korlach, J. (2011) Direct detection and sequencing of damaged DNA bases. Genome Integrity, 2, 10.
38. Brun, R., Schonenberger, M. (1979) Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop., 36, 289-292.
39. Papadopoulou, B., Roy, G., Ouelette, M. (1992) A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J., 11, 3601-3608.
40. Van Leeuwen, F., Wijsman, E.R., Kieft, R., Van der Marel, G.A., Van Boom, J.H., Borst, P. (1997) Localization of the modified base J in telomeric VSG gene expression sites of Trypanosoma brucei. Genes Dev., 11, 3232-3241.
41. Clarke, J. (2009) Continuous base identification for single-molecule nanopore DNA sequencing. Nat. Nanotechnol., 4, 265-270.
42. Lundquist, P.M. (2008) Parallel confocal detection of single molecules in real time. Opt. Lett., 33, 1026-1028.
43. Crooks, G.E., Hon, G., Chandonia, J.-M., Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
44. Heidebrecht, T., Fish, A., von Castelmur, E., Johnson, K.A., Zaccai, G., Borst, P., Perrakis, A. (2012) Binding of the J-binding protein to DNA containing glucosylated hmU (base J) or 5-hmC: evidence for a rapid conformational change upon DNA binding. J. Am. Chem. Soc., 134, 13357-13365.
45. Toaldo, C., Kieft, R., Dirks-Mulder, A., Sabatini, R., van Luenen, H., Borst, P. (2005) A minor fraction of base J in kinetoplastid nuclear DNA is bound by the J-binding protein 1. Mol. Biochem. Parasitol., 143, 111-115.
46. Henderson, A., Wu, Y., Huang, Y.C., Chavez, E.A., Platt, J., Johnson, F.B., Brosh, R.M., Sen, D., Lansdorp, P.M. (2014) Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res., 42, 860-869.
47. Patel, D., Phan, A., Kuryavyi, V. (2007) Human telomere, oncogenic promoter and 5-Ç-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res., 35, 7429-7455.
48. Bochman, M., Paeschke, K., Zakian, V. (2012) DNA secondary structures: stability and function of G-quadruplex structures. Nat. Rev. Genet., 13, 770-780.
49. Taylor, J.P. (2013) Neurodegenerative diseases: G-quadruplex poses quadruple threat. Nature, 507, 175-177.
50. Bernards, A., Michels, P.A., Lincke, C.R., Borst, P. (1983) Growth of chromosome ends in multiplying trypanosomes. Nature, 303, 592-597.