Role of Human Nucleoside Transporters in the Uptake and Cytotoxicity of Azacitidine and Decitabine

REFERENCES

• Sorm , F. , Piskala , A. , Cihak , A. and Vesely , J. 1964 . 5-Azacytidine, a new, highly effective cancerostatic . Experientia , 20 : 202 – 203 .
   PubMedGoogle Scholar
• Kantarjian , H. , Issa , J. P. , Rosenfeld , C. S. , Bennett , J. M. , Albitar , M. , DiPersio , J. , Klimek , V. , Slack , J. , de Castro , C. Ravandi , F. 2006 . Decitabine improves patient outcomes in myelodysplastic syndromes: Results of a phase III randomized study . Cancer , 106 : 1794 – 1803 .
   PubMed Web of Science ®Google Scholar
• 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. 2002 . Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B . J. Clin. Oncol. , 20 : 2429 – 2440 .
   PubMed Web of Science ®Google Scholar
• Robak , T. 2011 . New nucleoside analogs for patients with hematological malignancies . Expert. Opin. Investig. Drugs , 20 : 343 – 359 .
   PubMed Web of Science ®Google Scholar
• Jones , P. A. and Taylor , S. M. 1980 . Cellular differentiation, cytidine analogs and DNA methylation . Cell , 20 : 85 – 93 .
   PubMed Web of Science ®Google Scholar
• Hollenbach , P. W. , Nguyen , A. N. , Brady , H. , Williams , M. , Ning , Y. , Richard , N. , Krushel , L. , Aukerman , S. L. , Heise , C. and MacBeth , K. J. 2010 . A comparison of azacitidine and decitabine activities in acute myeloid leukemia cell lines . PLoS One , 5 : e9001
   PubMed Web of Science ®Google Scholar
• Vesely , J. , Seifert , J. , Cihak , A. and Sorm , F. 1966 . Biochemical changes associated with the development of resistance to 5-azacytidine in AKR leukemic mice . Int. J. Cancer , 1 : 31 – 39 .
   PubMed Web of Science ®Google Scholar
• 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. 2005 . The human equilibrative nucleoside transporter 1 mediates in vitro cytarabine sensitivity in childhood acute myeloid leukaemia . Br. J. Cancer , 93 : 1388 – 1394 .
   PubMed Web of Science ®Google Scholar
• Huang , Y. , Anderle , P. , Bussey , K. J. , Barbacioru , C. , Shankavaram , U. , Dai , Z. , Reinhold , W. C. , Papp , A. , Weinstein , J. N. and Sadee , W. 2004 . Membrane transporters and channels: Role of the transportome in cancer chemosensitivity and chemoresistance . Cancer Res. , 64 : 4294 – 4301 .
   PubMed Web of Science ®Google Scholar
• Rius , M. , Keller , D. , Brom , M. , Hummel-Eisenbeiss , J. , Lyko , F. and Keppler , D. 2009 . 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. , 38 : 1054 – 1063 .
   Web of Science ®Google Scholar
• Rius , M. , Stresemann , C. , Keller , D. , Brom , M. , Schirrmacher , E. , Keppler , D. and Lyko , F. 2009 . Human concentrative nucleoside transporter 1-mediated uptake of 5-azacytidine enhances DNA demethylation . Mol. Cancer Ther. , 8 : 225 – 231 .
   PubMed Web of Science ®Google Scholar
• Baldwin , S. A. , Beal , P. R. , Yao , S. Y. , King , A. E. , Cass , C. E. and Young , J. D. 2004 . The equilibrative nucleoside transporter family, SLC29 . Pflugers Arch. , 447 : 735 – 743 .
   PubMed Web of Science ®Google Scholar
• Gray , J. H. , Owen , R. P. and Giacomini , K. M. 2004 . The concentrative nucleoside transporter family, SLC28 . Pflugers Arch. , 447 : 728 – 734 .
   PubMed Web of Science ®Google Scholar
• Baldwin , S. A. , Yao , S. Y. , Hyde , R. J. , Ng , A. M. , Foppolo , S. , Barnes , K. , Ritzel , M. W. , Cass , C. E. and Young , J. D. 2005 . Functional characterization of novel human and mouse equilibrative nucleoside transporters (hENT3 and mENT3) located in intracellular membranes . J. Biol. Chem. , 280 : 15880 – 15887 .
   PubMed Web of Science ®Google Scholar
• Barnes , K. , Dobrzynski , H. , Foppolo , S. , Beal , P. R. , Ismat , F. , Scullion , E. R. , Sun , L. , Tellez , J. , Ritzel , M. W. Claycomb , W. C. 2006 . Distribution and functional characterization of equilibrative nucleoside transporter-4, a novel cardiac adenosine transporter activated at acidic pH . Circ. Res. , 99 : 510 – 519 .
   PubMed Web of Science ®Google Scholar
• Crawford , C. R. , Patel , D. H. , Naeve , C. and Belt , J. A. 1998 . Cloning of the human equilibrative, nitrobenzylmercaptopurine riboside (NBMPR)-insensitive nucleoside transporter ei by functional expression in a transport-deficient cell line . J. Biol. Chem. , 273 : 5288 – 5293 .
   PubMed Web of Science ®Google Scholar
• 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. 1997 . Cloning of a human nucleoside transporter implicated in the cellular uptake of adenosine and chemotherapeutic drugs . Nat. Med. , 3 : 89 – 93 .
   PubMed Web of Science ®Google Scholar
• Griffiths , M. , Yao , S. Y. , Abidi , F. , Phillips , S. E. , Cass , C. E. , Young , J. D. and Baldwin , S. A. 1997 . Molecular cloning and characterization of a nitrobenzylthioinosine-insensitive (ei) equilibrative nucleoside transporter from human placenta . Biochem. J. , 328 ( Pt 3 ) : 739 – 743 .
   PubMed Web of Science ®Google Scholar
• Yao , S. Y. , Ng , A. M. , Vickers , M. F. , Sundaram , M. , Cass , C. E. , Baldwin , S. A. and Young , J. D. 2002 . Functional and molecular 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. , 277 : 24938 – 24948 .
   PubMed Web of Science ®Google Scholar
• Engel , K. , Zhou , M. and Wang , J. 2004 . Identification and characterization of a novel monoamine transporter in the human brain . J. Biol. Chem. , 279 : 50042 – 50049 .
   PubMed Web of Science ®Google Scholar
• Govindarajan , R. , Leung , G. P. , Zhou , M. , Tse , C. M. , Wang , J. and Unadkat , J. D. 2009 . Facilitated mitochondrial import of antiviral and anticancer nucleoside drugs by human equilibrative nucleoside transporter-3 . Am. J. Physiol. Gastrointest. Liver Physiol. , 296 : G910 – 922 .
   PubMed Web of Science ®Google Scholar
• 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. 2001 . 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. , 276 : 2914 – 2927 .
   PubMed Web of Science ®Google Scholar
• Ritzel , M. W. , Yao , S. Y. , Ng , A. M. , Mackey , J. R. , Cass , C. E. and Young , J. D. 1998 . 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. , 15 : 203 – 211 .
   PubMed Web of Science ®Google Scholar
• Mackey , J. R. , Mani , R. S. , Selner , M. , Mowles , D. , Young , J. D. , Belt , J. A. , Crawford , C. R. and Cass , C. E. 1998 . Functional nucleoside transporters are required for gemcitabine influx and manifestation of toxicity in cancer cell lines . Cancer Res. , 58 : 4349 – 4357 .
   PubMed Web of Science ®Google Scholar
• Farrell , J. J. , Elsaleh , H. , Garcia , M. , Lai , R. , Ammar , A. , Regine , W. F. , Abrams , R. , Benson , A. B. , Macdonald , J. Cass , C. E. 2009 . Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer . Gastroenterology , 136 : 187 – 195 .
   PubMed Web of Science ®Google Scholar
• Visser , F. , Vickers , M. F. , Ng , A. M. , Baldwin , S. A. , Young , J. D. and Cass , C. E. 2002 . 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. , 277 : 395 – 401 .
   PubMed Web of Science ®Google Scholar
• Zhang , J. , Visser , F. , Vickers , M. F. , Lang , T. , Robins , M. J. , Nielsen , L. P. , Nowak , I. , Baldwin , S. A. , Young , J. D. and Cass , C. E. 2003 . Uridine binding motifs of human concentrative nucleoside transporters 1 and 3 produced in Saccharomyces cerevisiae . Mol. Pharmacol. , 64 : 1512 – 1520 .
   PubMed Web of Science ®Google Scholar
• Ullman , B. , Coons , T. , Rockwell , S. and McCartan , K. 1988 . Genetic analysis of 2′,3′-dideoxycytidine incorporation into cultured human T lymphoblasts . J. Biol. Chem. , 263 : 12391 – 12396 .
   PubMed Web of Science ®Google Scholar
• Lang , T. T. , Selner , M. , Young , J. D. and Cass , C. E. 2001 . Acquisition of human concentrative nucleoside transporter 2 (hcnt2) activity by gene transfer confers sensitivity to fluoropyrimidine nucleosides in drug-resistant leukemia cells . Mol. Pharmacol. , 60 : 1143 – 1152 .
   PubMed Web of Science ®Google Scholar
• Lang , T. T. , Young , J. D. and Cass , C. E. 2004 . 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. , 65 : 925 – 933 .
   PubMed Web of Science ®Google Scholar
• Vickers , M. F. , Zhang , J. , Visser , F. , Tackaberry , T. , Robins , M. J. , Nielsen , L. P. , Nowak , I. , Baldwin , S. A. , Young , J. D. and Cass , C. E. 2004 . Uridine recognition motifs of human equilibrative nucleoside transporters 1 and 2 produced in Saccharomyces cerevisiae . Nucleosides Nucleotides Nucleic Acids , 23 : 361 – 373 .
   PubMed Web of Science ®Google Scholar
• Cheng , Y. and Prusoff , W. H. 1973 . Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction . Biochem. Pharmacol. , 22 : 3099 – 3108 .
   PubMed Web of Science ®Google Scholar
• Zhang , J. , Visser , F. , King , K. M. , Baldwin , S. A. , Young , J. D. and Cass , C. E. 2007 . The role of nucleoside transporters in cancer chemotherapy with nucleoside drugs . Cancer Metastasis Rev , 26 : 85 – 110 .
   PubMed Web of Science ®Google Scholar
• Damaraju , V. L. , Smith , K. M. , Mowles , D. , Nowak , I. , Karpinski , E. , Young , J. D. , Robins , M. J. and Cass , C. E. 2011 . Interaction of fused-pyrimidine nucleoside analogs with human concentrative nucleoside transporters: High-affinity inhibitors of human concentrative nucleoside transporter 1 . Biochem. Pharmacol. , 81 : 82 – 90 .
   PubMed Web of Science ®Google Scholar
• Vickers , M. F. , Kumar , R. , Visser , F. , Zhang , J. , Charania , J. , Raborn , R. T. , Baldwin , S. A. , Young , J. D. and Cass , C. E. 2002 . 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. , 80 : 639 – 644 .
   PubMed Web of Science ®Google Scholar
• Momparler , R. L. and Derse , D. 1979 . Kinetics of phosphorylation of 5-aza-2′-deoxyycytidine by deoxycytidine kinase . Biochem. Pharmacol. , 28 : 1443 – 1444 .
   PubMed Web of Science ®Google Scholar
• Lee , T. , Karon , M. and Momparler , R. L. 1974 . Kinetic studies on phosphorylation of 5-azacytidine with the purified uridine-cytidine kinase from calf thymus . Cancer Res. , 34 : 2482 – 2488 .
   PubMed Web of Science ®Google Scholar
• Damaraju , V. L. , Sawyer , M. B. , Mackey , J. R. , Young , J. D. and Cass , C. E. 2009 . Human nucleoside transporters: Biomarkers for response to nucleoside drugs . Nucleosides Nucleotides Nucleic Acids , 28 : 450 – 463 .
   PubMed Web of Science ®Google Scholar
• Cass , C. E. , King , K. M. , Montano , J. T. and Janowska-Wieczorek , A. 1992 . A comparison of the abilities of nitrobenzylthioinosine, dilazep, and dipyridamole to protect human hematopoietic cells from 7-deazaadenosine (tubercidin) . Cancer Res. , 52 : 5879 – 5886 .
   PubMed Web of Science ®Google Scholar
• Gati , W. P. , Paterson , A. R. , Belch , A. R. , Chlumecky , V. , Larratt , L. M. , Mant , M. J. and Turner , A. R. 1998 . Es nucleoside transporter content of acute leukemia cells: role in cell sensitivity to cytarabine (araC) . Leuk. Lymphoma , 32 : 45 – 54 .
   PubMed Web of Science ®Google Scholar
• Wiley , J. S. , Jones , S. P. , Sawyer , W. H. and Paterson , A. R. 1982 . “ Cytosine arabinoside influx and nucleoside transport sites in acute leukemia ” . In J. Clin. Invest. Vol. 69 , 479 – 489 .
   Google Scholar
• Marechal , R. , Mackey , J. R. , Lai , R. , Demetter , P. , Peeters , M. , Polus , M. , Cass , C. E. , Young , J. , Salmon , I. Deviere , J. 2009 . Human equilibrative nucleoside transporter 1 and human concentrative nucleoside transporter 3 predict survival after adjuvant gemcitabine therapy in resected pancreatic adenocarcinoma . Clin. Cancer Res. , 15 : 2913 – 2919 .
   PubMed Web of Science ®Google Scholar
• Spratlin , J. , Sangha , R. , Glubrecht , D. , Dabbagh , L. , Young , J. D. , Dumontet , C. , Cass , C. , Lai , R. and Mackey , J. R. 2004 . The absence of human equilibrative nucleoside transporter 1 is associated with reduced survival in patients with gemcitabine-treated pancreas adenocarcinoma . Clin. Cancer Res. , 10 : 6956 – 6961 .
   PubMed Web of Science ®Google Scholar