Role of human nucleoside transporters in the uptake and cytotoxicity of azacitidine and decitabine

Nucleosides, Nucleotides and Nucleic Acids

Volumn 31, Issue 3, 2012, Pages 236-255

  Damaraju, Vijaya L ^a   Mowles, Delores ^a   Yao, Sylvia ^a   Ng, Amy ^a   Young, James D ^a   Cass, Carol E ^a   Tong, Zeen ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b CELGENE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; AZACITIDINE; GEMCITABINE; NUCLEOSIDE TRANSPORTER;

ARTICLE; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DOSE RESPONSE; DRUG UPTAKE; FEMALE; HUMAN; HUMAN CELL; IC 50; NONHUMAN; OOCYTE; SACCHAROMYCES CEREVISIAE; XENOPUS LAEVIS;

ANIMALS; AZACITIDINE; CARBON RADIOISOTOPES; DEOXYCYTIDINE; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; HUMANS; MEMBRANE TRANSPORT PROTEINS; OOCYTES; SACCHAROMYCES CEREVISIAE; TRITIUM; XENOPUS;

SACCHAROMYCES CEREVISIAE; XENOPUS LAEVIS;

EID: 84859707152     PISSN: 15257770     EISSN: 15322335     Source Type: Journal    
DOI: 10.1080/15257770.2011.652330     Document Type: Article

References (43)

1. Sorm, F.; Piskala, A.;Cihak,A.; Vesely, J. 5-Azacytidine, a new, highly effective cancerostatic. Experientia 1964, 20, 202-203.
2. Kantarjian, H.; Issa, J.P.; Rosenfeld, C.S.; Bennett, J.M.; Albitar, M.; DiPersio, J.; Klimek, V.; Slack, J.; de Castro, C.; Ravandi, F. et al. Decitabine improves patient outcomes in myelodysplastic syndromes: Results of a phase III randomized study. Cancer 2006, 106, 1794-1803.
3. Silverman, L.R.; Demakos, E.P.; Peterson, B.L.; Kornblith, A.B.; Holland, J.C.; Odchimar-Reissig, R.; Stone, R.M.; Nelson, D.; Powell, B.L.; DeCastro, C.M. et al. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B. J. Clin. Oncol. 2002, 20, 2429-2440. (Pubitemid 34525728)
4. Robak, T. New nucleoside analogs for patients with hematological malignancies. Expert. Opin. Investig. Drugs 2011, 20, 343-359.
5. Jones, P.A.; Taylor, S.M. Cellular differentiation, cytidine analogs and DNA methylation. Cell 1980, 20, 85-93. (Pubitemid 10117303)
6. Hollenbach, P.W.; Nguyen, A.N.; Brady, H.; Williams, M.; Ning, Y.; Richard, N.; Krushel, L.; Aukerman, S.L.; Heise, C.; MacBeth, K.J. A comparison of azacitidine and decitabine activities in acute myeloid leukemia cell lines. PLoS One 2010, 5, e9001.
7. Vesely, J.; Seifert, J.; Cihak, A.; Sorm, F. Biochemical changes associated with the development of resistance to 5-azacytidine in AKR leukemic mice. Int. J. Cancer 1966, 1, 31-39.
8. Hubeek, I.; Stam, R.W.; Peters, G.J.; Broekhuizen, R.; Meijerink, J.P.; van Wering, E.R.; Gibson, B.E.; Creutzig, U.; Zwaan, C.M.; Cloos, J. et al. The human equilibrative nucleoside transporter 1 mediates in vitro cytarabine sensitivity in childhood acute myeloid leukaemia. Br. J. Cancer 2005, 93, 1388-1394. (Pubitemid 41752866)
9. Huang, Y.; Anderle, P.; Bussey, K.J.; Barbacioru, C.; Shankavaram, U.; Dai, Z.; Reinhold, W.C.; Papp, A.; Weinstein, J.N.; Sadee, W. Membrane transporters and channels: Role of the transportome in cancer chemosensitivity and chemoresistance. Cancer Res. 2004, 64, 4294-4301. (Pubitemid 38802436)
10. Rius, M.; Keller, D.; Brom, M.; Hummel-Eisenbeiss, J.; Lyko, F.; Keppler, D. Vectorial transport of nucleoside analogs from the apical to the basolateral membrane in double-transfected cells expressing the human concentrative nucleoside transporter hCNT3 and the export pump ABCC4. Drug Metab. Dispos. 2009, 38, 1054-1063.
11. Rius, M.; Stresemann, C.; Keller, D.; Brom, M.; Schirrmacher, E.; Keppler, D.; Lyko, F. Human concentrative nucleoside transporter 1-mediated uptake of 5-azacytidine enhances DNA demethylation. Mol. Cancer Ther. 2009, 8, 225-231.
12. Baldwin, S.A.; Beal, P.R.; Yao, S.Y.; King, A.E.; Cass, C.E.; Young, J.D. The equilibrative nucleoside transporter family, SLC29. Pflugers Arch. 2004, 447, 735-743. (Pubitemid 38241459)
13. Gray, J.H.; Owen, R.P.; Giacomini, K.M. The concentrative nucleoside transporter family, SLC28. Pflugers Arch. 2004, 447, 728-734. (Pubitemid 38241458)
14. Baldwin, S.A.; Yao, S.Y.; Hyde, R.J.; Ng, A.M.; Foppolo, S.; Barnes, K.; Ritzel, M.W.; Cass, C.E.; Young, J.D. Functional characterization of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes. J. Biol. Chem. 2005, 280, 15880-15887. (Pubitemid 40616710)
15. Barnes, K.; Dobrzynski, H.; Foppolo, S.; Beal, P.R.; Ismat, F.; Scullion, E.R.; Sun, L.; Tellez, J.; Ritzel, M.W.; Claycomb, W.C. et al. Distribution and functional characterization of equilibrative nucleoside transporter-4, a novel cardiac adenosine transporter activated at acidic pH. Circ. Res. 2006, 99, 510-519. (Pubitemid 44337823)
16. Crawford, C.R.; Patel, D.H.; Naeve, C.; Belt, J.A. Cloning of the human equilibrative, nitrobenzylmercaptopurine riboside (NBMPR)-insensitive nucleoside transporter ei by functional expression in a transport-deficient cell line. J. Biol. Chem. 1998, 273, 5288-5293. (Pubitemid 28108694)
17. Griffiths, M.; Beaumont, N.; Yao, S.Y.; Sundaram, M.; Boumah, C.E.; Davies, A.; Kwong, F.Y.; Coe, I.; Cass, C.E.; Young, J.D. et al. Cloning of a human nucleoside transporter implicated in the cellular uptake of adenosine and chemotherapeutic drugs. Nat. Med. 1997, 3, 89-93. (Pubitemid 27019148)
18. Griffiths, M.; Yao, S.Y.; Abidi, F.; Phillips, S.E.; Cass, C.E.; Young, J.D.; Baldwin, S.A. Molecular cloning and characterization of a nitrobenzylthioinosine-insensitive (ei) equilibrative nucleoside transporter from human placenta. Biochem. J. 1997, 328(Pt 3), 739-743. (Pubitemid 28005769)
19. Yao, S.Y.; Ng, A.M.; Vickers, M.F.; Sundaram, M.; Cass, C.E.; Baldwin, S.A.; Young, J.D. Functional andmolecular characterization of nucleobase transport by recombinant human and rat equilibrative nucleoside transporters 1 and 2. Chimeric constructs reveal a role for the ENT2 helix 5-6 region in nucleobase translocation. J. Biol. Chem. 2002, 277, 24938-24948. (Pubitemid 34951795)
20. Engel, K.; Zhou, M.; Wang, J. Identification and characterization of a novel monoamine transporter in the human brain. J. Biol. Chem. 2004, 279, 50042-50049. (Pubitemid 39577815)
21. Govindarajan, R.; Leung, G.P.; Zhou, M.; Tse, C.M.; Wang, J.; Unadkat, J.D. Facilitated mitochondrial import of antiviral and anticancer nucleoside drugs by human equilibrative nucleoside transporter-3. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296, G910-922.
22. Ritzel, M.W.; Ng, A.M.; Yao, S.Y.; Graham, K.; Loewen, S.K.; Smith, K.M.; Ritzel, R.G.; Mowles, D.A.; Carpenter, P.; Chen, X.Z. et al. Molecular identification and characterization of novel human and mouse concentrative Na+-nucleoside cotransporter proteins (hCNT3 and mCNT3) broadly selective for purine and pyrimidine nucleosides (system cib). J. Biol. Chem. 2001, 276, 2914-2927.
23. Ritzel, M.W.; Yao, S.Y.; Ng, A.M.; Mackey, J.R.; Cass, C.E.; Young, J.D. Molecular cloning, functional expression and chromosomal localization of a cDNA encoding a human Na+/nucleoside cotransporter (hCNT2) selective for purine nucleosides and uridine. Mol. Membr. Biol. 1998, 15, 203-211. (Pubitemid 29097592)
24. Mackey, J.R.; Mani, R.S.; Selner, M.; Mowles, D.; Young, J.D.; Belt, J.A.; Crawford, C.R.; Cass, C.E. Functional nucleoside transporters are required for gemcitabine influx and manifestation of toxicity in cancer cell lines. Cancer Res. 1998, 58, 4349-4357. (Pubitemid 28450036)
25. Farrell, J.J.; Elsaleh, H.; Garcia, M.; Lai, R.; Ammar, A.; Regine, W.F.; Abrams, R.; Benson, A.B.; Macdonald, J.; Cass, C.E. et al. Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology 2009, 136, 187-195.
26. Visser, F.; Vickers, M.F.; Ng, A.M.; Baldwin, S.A.; Young, J.D.; Cass, C.E. Mutation of residue 33 of human equilibrative nucleoside transporters 1 and 2 alters sensitivity to inhibition of transport by dilazep and dipyridamole. J. Biol. Chem. 2002, 277, 395-401. (Pubitemid 34952071)
27. Zhang, J.; Visser, F.; Vickers, M.F.; Lang, T.; Robins, M.J.; Nielsen, L.P.; Nowak, I.; Baldwin, S.A.; Young, J.D.; Cass, C.E. Uridine binding motifs of human concentrative nucleoside transporters 1 and 3 produced in Saccharomyces cerevisiae. Mol. Pharmacol. 2003, 64, 1512-1520. (Pubitemid 37532240)
28. Ullman, B.; Coons, T.; Rockwell, S.; McCartan, K. Genetic analysis of 2′,3′-dideoxycytidine incorporation into cultured human T lymphoblasts. J. Biol. Chem. 1988, 263, 12391-12396. (Pubitemid 19000418)
29. Lang, T.T.; Selner, M.; Young, J.D.; Cass, C.E. Acquisition of human concentrative nucleoside transporter 2 (hcnt2) activity by gene transfer confers sensitivity to fluoropyrimidine nucleosides in drug-resistant leukemia cells. Mol. Pharmacol. 2001, 60, 1143-1152. (Pubitemid 33027450)
30. Lang, T.T.; Young, J.D.; Cass, C.E. Interactions of nucleoside analogs, caffeine, and nicotine with human concentrative nucleoside transporters 1 and 2 stably produced in a transport-defective human cell line. Mol. Pharmacol. 2004, 65, 925-933. (Pubitemid 38420498)
31. Vickers, M.F.; Zhang, J.; Visser, F.; Tackaberry, T.; Robins, M.J.; Nielsen, L.P.;Nowak, I.; Baldwin, S.A.; Young, J.D.; Cass, C.E. Uridine recognition motifs of human equilibrative nucleoside transporters 1 and 2 produced in Saccharomyces cerevisiae. Nucleosides Nucleotides Nucleic Acids 2004, 23, 361-373. (Pubitemid 38351985)
32. Cheng, Y.; Prusoff, W.H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22, 3099-3108.
33. Zhang, J.; Visser, F.; King, K.M.; Baldwin, S.A.; Young, J.D.; Cass, C.E. The role of nucleoside transporters in cancer chemotherapy with nucleoside drugs. Cancer Metastasis Rev. 2007, 26, 85-110. (Pubitemid 46452184)
34. Damaraju, V.L.; Smith, K.M.; Mowles, D.; Nowak, I.; Karpinski, E.; Young, J.D.; Robins, M.J.; Cass, C.E. Interaction of fused-pyrimidine nucleoside analogs with human concentrative nucleoside transporters: High-affinity inhibitors of human concentrative nucleoside transporter 1. Biochem. Pharmacol. 2011, 81, 82-90.
35. Vickers, M.F.; Kumar, R.; Visser, F.; Zhang, J.; Charania, J.; Raborn, R.T.; Baldwin, S.A.; Young, J.D.; Cass, C.E. Comparison of the interaction of uridine, cytidine, and other pyrimidine nucleoside analogues with recombinant human equilibrative nucleoside transporter 2 (hENT2) produced in Saccharomyces cerevisiae. Biochem. Cell. Biol. 2002, 80, 639-644. (Pubitemid 36124822)
36. Momparler, R.L.; Derse, D. Kinetics of phosphorylation of 5-aza-2′-deoxyycytidine by deoxycytidine kinase. Biochem. Pharmacol. 1979, 28, 1443-1444. (Pubitemid 9174327)
37. Lee, T.; Karon, M.; Momparler, R.L. Kinetic studies on phosphorylation of 5-azacytidine with the purified uridine-cytidine kinase from calf thymus. Cancer Res. 1974, 34, 2482-2488.
38. Damaraju, V.L.; Sawyer, M.B.; Mackey, J.R.; Young, J.D.; Cass, C.E. Human nucleoside transporters: Biomarkers for response to nucleoside drugs. Nucleosides Nucleotides Nucleic Acids 2009, 28, 450-463.
39. Cass, C.E.; King, K.M.; Montano, J.T.; Janowska-Wieczorek, A. A comparison of the abilities of nitrobenzylthioinosine, dilazep, and dipyridamole to protect human hematopoietic cells from 7-deazaadenosine (tubercidin). Cancer Res. 1992, 52, 5879-5886.
40. Gati, W.P.; Paterson, A.R.; Belch, A.R.; Chlumecky, V.; Larratt, L.M.; Mant, M.J.; Turner, A.R. Es nucleoside transporter content of acute leukemia cells: role in cell sensitivity to cytarabine (araC). Leuk. Lymphoma 1998, 32, 45-54. (Pubitemid 29086382)
41. Wiley, J.S.; Jones, S.P.; Sawyer, W.H.; Paterson, A.R. Cytosine arabinoside influx and nucleoside transport sites in acute leukemia. J. Clin. Invest. 1982, 69, 479-489. (Pubitemid 12177627)
42. Marechal, R.; Mackey, J.R.; Lai, R.; Demetter, P.; Peeters, M.; Polus, M.; Cass, C.E.; Young, J.; Salmon, I.; Deviere, J. et al. Human equilibrative nucleoside transporter 1 and human concentrative nucleoside transporter 3 predict survival after adjuvant gemcitabine therapy in resected pancreatic adenocarcinoma. Clin. Cancer Res. 2009, 15, 2913-2919.
43. Spratlin, J.; Sangha, R.; Glubrecht, D.; Dabbagh, L.; Young, J.D.; Dumontet, C.; Cass, C.; Lai, R.; Mackey, J.R. The absence of human equilibrative nucleoside transporter 1 is associated with reduced survival in patients with gemcitabine-treated pancreas adenocarcinoma. Clin. Cancer Res. 2004, 10, 6956-6961. (Pubitemid 39383046)