Base J Originally Found in Kinetoplastida is Also a Minor Constituent of Nuclear DNA of Euglena Gracilis

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2000 Aug 10

PMID 10931915

Citations 31

Authors

D Dooijes

I Chaves

R Kieft

A Dirks-Mulder

W Martin

P Borst

Affiliations

Soon will be listed here.

Abstract

We have analyzed DNA of EUGLENA: gracilis for the presence of the unusual minor base beta-D-glucosyl-hydroxymethyluracil or J, thus far only found in kinetoplastid flagellates and in DIPLONEMA: Using antibodies specific for J and post-labeling of DNA digests followed by two-dimensional thin-layer chromatography of labeled nucleotides, we show that approximately 0.2 mole percent of EUGLENA: DNA consists of J, an amount similar to that found in DNA of Trypanosoma brucei. By staining permeabilized EUGLENA: cells with anti-J antibodies, we show that J is rather uniformly distributed in the EUGLENA: nucleus, and does not co-localize to a substantial extent with (GGGTTA)(n) repeats, the putative telomeric repeats of EUGLENA: Hence, most of J in EUGLENA: appears to be non-telomeric. Our results add to the existing evidence for a close phylogenetic relation between kinetoplastids and euglenids.

Citing Articles

Protein phosphatase PP1 regulation of RNA polymerase II transcription termination and allelic exclusion of VSG genes in trypanosomes.

Kieft R, Zhang Y, Yan H, Schmitz R, Sabatini R Nucleic Acids Res. 2024; 52(12):6866-6885.

PMID: 38783162 PMC: 11229358. DOI: 10.1093/nar/gkae392.

Genome-wide distribution of 5-hydroxymethyluracil and chromatin accessibility in the Breviolum minutum genome.

Marinov G, Chen X, Swaffer M, Xiang T, Grossman A, Greenleaf W Genome Biol. 2024; 25(1):115.

PMID: 38711126 PMC: 11071213. DOI: 10.1186/s13059-024-03261-3.

Leishmania PNUTS discriminates between PP1 catalytic subunits through an RVxF-ΦΦ-F motif and polymorphisms in the PP1 C-tail and catalytic domain.

Zhang Y, Sabatini R J Biol Chem. 2023; 299(12):105432.

PMID: 37926279 PMC: 10731240. DOI: 10.1016/j.jbc.2023.105432.

Genome-wide distribution of 5-hydroxymethyluracil and chromatin accessibility in the genome.

Marinov G, Chen X, Swaffer M, Xiang T, Grossman A, Greenleaf W bioRxiv. 2023; .

PMID: 37781619 PMC: 10541103. DOI: 10.1101/2023.09.18.558303.

Knockout of protein phosphatase 1 in Leishmania major reveals its role during RNA polymerase II transcription termination.

Kieft R, Zhang Y, Yan H, Schmitz R, Sabatini R Nucleic Acids Res. 2023; 51(12):6208-6226.

PMID: 37194692 PMC: 10325913. DOI: 10.1093/nar/gkad394.

References

Van Leeuwen F, Kieft R, Cross M, Borst P . Biosynthesis and function of the modified DNA base beta-D-glucosyl-hydroxymethyluracil in Trypanosoma brucei. Mol Cell Biol. 1998; 18(10):5643-51. PMC: 109150. DOI: 10.1128/MCB.18.10.5643. View

Borst P, VAN DER PLOEG M, van Hoek J, Tas J, James J . On the DNA content and ploidy of trypanosomes. Mol Biochem Parasitol. 1982; 6(1):13-23. DOI: 10.1016/0166-6851(82)90049-4. View

Chaves I, Zomerdijk J, Dirks-Mulder A, Dirks R, Raap A, Borst P . Subnuclear localization of the active variant surface glycoprotein gene expression site in Trypanosoma brucei. Proc Natl Acad Sci U S A. 1998; 95(21):12328-33. PMC: 22831. DOI: 10.1073/pnas.95.21.12328. View

Levasseur P, Meng Q, Bouck G . Tubulin genes in the algal protist Euglena gracilis. J Eukaryot Microbiol. 1994; 41(5):468-77. DOI: 10.1111/j.1550-7408.1994.tb06044.x. View

Van Leeuwen F, Wijsman E, van der Marel G, VAN Boom J, Borst P . The telomeric GGGTTA repeats of Trypanosoma brucei contain the hypermodified base J in both strands. Nucleic Acids Res. 1996; 24(13):2476-82. PMC: 145968. DOI: 10.1093/nar/24.13.2476. View

Cavalier-Smith T . Kingdom protozoa and its 18 phyla. Microbiol Rev. 1993; 57(4):953-94. PMC: 372943. DOI: 10.1128/mr.57.4.953-994.1993. View

Van Leeuwen F, Taylor M, Mondragon A, Moreau H, Gibson W, Kieft R . 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. 1998; 95(5):2366-71. PMC: 19348. DOI: 10.1073/pnas.95.5.2366. View

Lutgerink J, Borst P . A novel DNA nucleotide in Trypanosoma brucei only present in the mammalian phase of the life-cycle. Nucleic Acids Res. 1991; 19(8):1745-51. PMC: 328099. DOI: 10.1093/nar/19.8.1745. View

Tessier L, van der Speck H, Gualberto J, Grienenberger J . The cox1 gene from Euglena gracilis: a protist mitochondrial gene without introns and genetic code modifications. Curr Genet. 1997; 31(3):208-13. DOI: 10.1007/s002940050197. View

10.

Borst P, Van Leeuwen F . beta-D-glucosyl-hydroxymethyluracil, a novel base in African trypanosomes and other Kinetoplastida. Mol Biochem Parasitol. 1998; 90(1):1-8. DOI: 10.1016/s0166-6851(97)00170-9. View

11.

Henze K, Badr A, Wettern M, Cerff R, Martin W . A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. Proc Natl Acad Sci U S A. 1995; 92(20):9122-6. PMC: 40936. DOI: 10.1073/pnas.92.20.9122. View

12.

Navazio L, Nardi M, Pancaldi S, Dainese P, Baldan B, Faye L . Functional conservation of calreticulin in Euglena gracilis. J Eukaryot Microbiol. 1998; 45(3):307-13. DOI: 10.1111/j.1550-7408.1998.tb04541.x. View

13.

Yasuhira S, Simpson L . Phylogenetic affinity of mitochondria of Euglena gracilis and kinetoplastids using cytochrome oxidase I and hsp60. J Mol Evol. 1997; 44(3):341-7. DOI: 10.1007/pl00006152. View

14.

Van Leeuwen F, Dirks-Mulder A, Dirks R, Borst P, Gibson W . The modified DNA base beta-D-glucosyl-hydroxymethyluracil is not found in the tsetse fly stages of Trypanosoma brucei. Mol Biochem Parasitol. 1998; 94(1):127-30. DOI: 10.1016/s0166-6851(98)00060-7. View

15.

Van Leeuwen F, de Beer A, Vliegenthart J, Dizdaroglu M, Kowalak J, Crain P . beta-D-glucosyl-hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T. brucei. Cell. 1993; 75(6):1129-36. DOI: 10.1016/0092-8674(93)90322-h. View

16.

Van Leeuwen F, de Kort M, van der Marel G, VAN Boom J, Borst P . The modified DNA base beta-D-glucosylhydroxymethyluracil confers resistance to micrococcal nuclease and is incompletely recovered by 32P-postlabeling. Anal Biochem. 1998; 258(2):223-9. DOI: 10.1006/abio.1998.2587. View

17.

Maslov D, Yasuhira S, Simpson L . Phylogenetic affinities of Diplonema within the Euglenozoa as inferred from the SSU rRNA gene and partial COI protein sequences. Protist. 2000; 150(1):33-42. DOI: 10.1016/S1434-4610(99)70007-6. View

18.

Martin W, Stoebe B, Goremykin V, Hapsmann S, Hasegawa M, Kowallik K . Gene transfer to the nucleus and the evolution of chloroplasts. Nature. 2001; 393(6681):162-5. DOI: 10.1038/30234. View

19.

Van Leeuwen F, Wijsman E, Kieft R, van der Marel G, VAN Boom J, Borst P . Localization of the modified base J in telomeric VSG gene expression sites of Trypanosoma brucei. Genes Dev. 1998; 11(23):3232-41. PMC: 316749. DOI: 10.1101/gad.11.23.3232. View

20.

Rawson J, Eckenrode V, Boerma C, Curtis S . DNA sequence organization in the alga Euglena gracilis. Biochim Biophys Acta. 1979; 563(1):1-16. DOI: 10.1016/0005-2787(79)90002-9. View