Re-evaluation of the mutagenic response to phosphorothioate nucleotides in human lymphoblastoid TK6 cells

Toxicological Sciences

Volumn 145, Issue 1, 2015, Pages 169-176

  Saleh, Amer F ^a   Priestley, Catherine C ^a   Gooderham, Nigel J ^b   Fellows, Mick D ^a  

^a ASTRAZENECA   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Mutagenesis; Nucleotide; Phosphorothioate; Thymidine kinase

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; DEOXYADENOSINE DERIVATIVE; NUCLEOTIDE DERIVATIVE; PHOSPHOROTHIOIC ACID; TRIFLURIDINE; MUTAGENIC AGENT; NUCLEOTIDE; ORGANOPHOSPHORUS COMPOUND;

ARTICLE; CELL CYCLE G1 PHASE; CELL KINETICS; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; G1 PHASE CELL CYCLE CHECKPOINT; GENOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOBLASTOID CELL; MALE; MUTAGENICITY; CELL LINE;

CELL LINE; HUMANS; MUTAGENS; NUCLEOTIDES; ORGANOPHOSPHORUS COMPOUNDS;

EID: 84929672162     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv043     Document Type: Article

References (38)

1. Agrawal, S., Temsamani, J., and Tang, J. Y. (1991). Pharmacokinetics, biodistribution, and stability of oligodeoxynucleotide phosphorothioates in mice. Proc. Natl Acad. Sci. U.S.A. 88, 7595-7599.
2. Anderson, D., Richardson, C. R., and Davies, P. J. (1981). The genotoxic potential of bases and nucleosides. Mutat. Res. 91, 265-272.
3. Brox, L., Ng, A., Pollock, E., and Belch, A. (1984). DNA strand breaks induced in human T-lymphocytes by the combination of deoxyadenosine and deoxycoformycin. Cancer Res. 44, 934-937.
4. Bynum, J. W. (1980). Characterization of adenosine-induced cytostasis in melanoma cells. Cancer Res. 40, 2147-2152.
5. Call, K. M., and Thilly, W. G. (1991). 5-Azacytidine inhibits the induction of transient TK-deficient cells by 5-bromodeoxyuridine. A novel hypothesis for the facilitation of hypermethylation by 5-bromodeoxyuridine. Mutat. Res. 248, 101-114.
6. Clements, J. (2000). The mouse lymphoma assay. Mutat. Res. 455, 97-110.
7. Clive, D., Flamm, W. G., Machesko, M. R., and Bernheim, N. J. (1972). A mutational assay system using the thymidine kinase locus in mouse lymphoma cells. Mutat. Res. 16, 77-87.
8. Cusack, N. J., Pearson, J. D., and Gordon, J. L. (1983). Stereoselectivity of ectonucleotidases on vascular endothelial cells. Biochem. J. 214, 975-981.
9. Deleavey, G. F., and Damha, M. J. (2012). Designing chemically modified oligonucleotides for targeted gene silencing. Chem. Biol. 19, 937-954.
10. Eckstein, F. (2000). Phosphorothioate oligodeoxynucleotides: What is their origin and what is unique about them? Antisense Nucleic Acid Drug Dev. 10, 117-121.
11. Fersht, A. R. (1979). Fidelity of replication of phage phi X174 DNA by DNA polymerase III holoenzyme: Spontaneous mutation by misincorporation. Proc. Natl Acad. Sci. U.S.A. 76, 4946-4950.
12. Fishman, P., Bar-Yehuda, S., Ohana, G., Pathak, S., Wasserman, L., Barer, F., and Multani, A. S. (2000). Adenosine acts as an inhibitor of lymphoma cell growth: A major role for the A3 adenosine receptor. Eur. J. Cancer 36, 1452-1458.
13. Geary, R. S., Leeds, J. M., Fitchett, J., Burckin, T., Truong, L., Spainhour, C., Creek, M., and Levin, A. A. (1997). Pharmacokinetics and metabolism in mice of a phosphorothioate oligonucleotide antisense inhibitor of C-raf-1 kinase expression. Drug Metab. Dispos. 25, 1272-1281.
14. Graham, M. J., Lee, R. G., Bell, T. A., 3rd, Fu, W., Mullick, A. E., Alexander, V. J., Singleton, W., Viney, N., Geary, R., Su, J., et al. (2013). Antisense oligonucleotide inhibition of apolipoprotein C-III reduces plasma triglycerides in rodents, nonhuman primates, and humans. Circ. Res. 112, 1479-1490.
15. Hakulinen, P., Yamamoto, A., Koyama, N., Kumita, W., Yasui, M., and Honma, M. (2011). Induction of TK mutations in human lymphoblastoid TK6 cells by the rat carcinogen 3-chloro-4 -(dichloromethyl)-5-hydroxy-2(5 H)-furanone (MX). Mutat. Res. 725, 43-49.
16. Henry, S. P., Monteith, D. K., Matson, J. E., Mathison, B. H., Loveday, K. S., Winegar, R. A., Matson, J. E., Lee, P. S., Riccio, E.S., Bakke, J. P., et al. (2002). Assessment of the genotoxic potential of ISIS 2302: A phosphorothioate oligodeoxynucleotide. Mutagenesis 17, 201-209.
17. Honma, M. (2005). Generation of loss of heterozygosity and its dependency on p53 status in human lymphoblastoid cells. Environ. Mol. Mutagen. 45, 162-176.
18. Honma, M., Hayashi, M., and Sofuni, T. (1997). Cytotoxic and mutagenic responses to X-rays and chemical mutagens in normal and p53-mutated human lymphoblastoid cells. Mutat. Res. 374, 89-98.
19. Ishii, K., and Green, H. (1973). Lethality of adenosine for cultured mammalian cells by interference with pyrimidine biosynthesis. J. Cell Sci. 13, 429-439.
20. Kauffman, M. G., and Kelly, T. J. (1991). Cell cycle regulation of thymidine kinase: Residues near the carboxyl terminus are essential for the specific degradation of the enzyme at mitosis. Mol. Cell Biol. 11, 2538-2546.
21. Koziolkiewicz, M., Gendaszewska, E., Maszewska, M., Stein, C. A., and Stec, W. J. (2001). The mononucleotide-dependent, nonantisense mechanism of action of phosphodiester and phosphorothioate oligonucleotides depends upon the activity of an ecto-5'-nucleotidase. Blood 98, 995-1002.
22. Levy, J. A., Virolainen, M., and Defendi, V. (1968). Human lymphoblastoid lines from lymph node and spleen. Cancer 22, 517-524.
23. Liber, H. L., and Denault, C. M. (1991). Mutagenicity of 2-amino-N6-hydroxyadenine to TK6 human lymphoblast cells. Mutat. Res. 253, 91-95.
24. Liber, H. L., Call, K. M., and Little, J. B. (1987). Molecular and biochemical analyses of spontaneous and X-ray-induced mutants in human lymphoblastoid cells. Mutat. Res. 178, 143-153.
25. Liber, H. L., Call, K. M., Mascioli, D. A., and Thilly, W. G. (1985). Mutational and pseudomutational effects of 5-bromodeoxyuridine in human lymphoblasts. Mutat. Res. 151, 95-108.
26. Liber, H. L., Yandell, D. W., and Little, J. B. (1989). A comparison of mutation induction at the tk and hprt loci in human lymphoblastoid cells; quantitative differences are due to an additional class of mutations at the autosomal tk locus. Mutat. Res. 216, 9-17.
27. Mattano, S. S., Palella, T. D., and Mitchell, B. S. (1990). Mutations induced at the hypoxanthine-guanine phosphoribosyltransferase locus of human T-lymphoblasts by perturbations of purine deoxyribonucleoside triphosphate pools. Cancer Res. 50, 4566-4571.
28. Molloy, J., Doherty, A. T., Chocian, K., Hayes, J., and O'Donovan, M. (2010). Karyotypic analysis and stability with time in culture of TK6 and L5178Y cell lines. Mutagenesis 25, 645.
29. Murray, A. W., and Atkinson, M. R. (1968). Adenosine 5'-phosphorothioate. A nucleotide analog that is a substrate, competitive inhibitor, or regulator of some enzymes that interact with adenosine 5'-phosphate. Biochemistry 7, 4023-4029.
30. Oberly, T. J., Bewsey, B. J., and Probst, G. S. (1984). An evaluation of the L5178Y TK+/-mouse lymphoma forward mutation assay using 42 chemicals. Mutat. Res. 125, 291-306.
31. Reshat, R., Priestley, C. C., and Gooderham, N. J. (2012). Mutagenesis by an antisense oligonucleotide and its degradation product. Toxicol. Sci. 130, 319-327.
32. Ryan, T. J., Boddington, M. M., and Spriggs, A. I. (1965). Chromosomal abnormalities produced by folic acid antagonists. Br. J. Dermatol. 77, 541-55.
33. Skopek, T. R., Liber, H. L., Penman, B. W., and Thilly, W. G. (1978). Isolation of a human lymphoblastoid line heterozygous at the thymidine kinase locus: Possibility for a rapid human cell mutation assay. Biochem. Biophys. Res. Commun. 84, 411-416.
34. Suzuki, N., Nakagawa, F., Nukatsuka, M., and Fukushima, M. (2011). Trifluorothymidine exhibits potent antitumor activity via the induction of DNA double-strand breaks. Exp. Ther. Med. 2, 393-397.
35. Thaler, D. S., Liu, S., and Tombline, G. (1996). Extending the chemistry that supports genetic information transfer in vivo: Phosphorothioate DNA, phosphorothioate RNA, 2'-O-methyl RNA, and methylphosphonate DNA. Proc. Natl Acad. Sci. U.S.A. 93, 1352-1356.
36. Thomas, G. S., Cromwell, W. C., Ali, S., Chin, W., Flaim, J. D., and Davidson, M. (2013). Mipomersen, an apolipoprotein B synthesis inhibitor, reduces atherogenic lipoproteins in patients with severe hypercholesterolemia at high cardiovascular risk: A randomized, double-blind, placebo-controlled trial. J. Am. Coll. Cardiol. 62, 2178-2184.
37. Vaerman, J. L., Moureau, P., Deldime, F., Lewalle, P., Lammineur, C., Morschhauser, F., and Martiat, P. (1997). Antisense oligodeoxyribonucleotides suppress hematologic cell growth through stepwise release of deoxyribonucleotides. Blood 90, 331-339.
38. Zhan, L., Sakamoto, H., Sakuraba, M., Wu, D. S., Zhang, L. S., Suzuki, T., Hayashi, M., and Honma, M. (2004). Genotoxicity of microcystin-LR in human lymphoblastoid TK6 cells. Mutat. Res. 557, 1-6.