Down-regulation of deoxycytidine kinase in human leukemic cell lines resistant to cladribine and clofarabine and increased ribonucleotide reductase activity contributes to fludarabine resistance

Biochemical Pharmacology

Volumn 65, Issue 2, 2003, Pages 237-247

  Månsson, Emma ^a   Flordal, Emma ^a   Liliemark, Jan ^a   Spasokoukotskaja, Tatiana ^b   Elford, Howard ^c   Lagercrantz, Svetlana ^a   Eriksson, Staffan ^d   Albertioni, Freidoun ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c Molecules for Health Inc   (United States)

^d SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Cladribine; Clofarabine; Deoxycytidine kinase; Fludarabine; Ribonucleotide reductase

Indexed keywords

3,4 DIHYDROXYBENZOHYDROXAMIC ACID; 5' NUCLEOTIDASE; CLADRIBINE; CLOFARABINE; DEOXYCYTIDINE KINASE; FLUDARABINE; GUANOSINE DERIVATIVE; NUCLEOSIDE ANALOG; PRODRUG; PURINE DERIVATIVE; RIBONUCLEOTIDE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; DRUG ACTIVATION; DRUG CYTOTOXICITY; DRUG RESISTANCE; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME REGULATION; EXPOSURE; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHATIC LEUKEMIA; PRIORITY JOURNAL; T LYMPHOBLAST;

ADENINE NUCLEOTIDES; ANTINEOPLASTIC AGENTS; ARABINONUCLEOSIDES; CELL LINE; CLADRIBINE; CYTOGENETICS; DEOXYCYTIDINE KINASE; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; HUMANS; LEUKEMIA; PHENOTYPE; PHOSPHORYLATION; RIBONUCLEOTIDE REDUCTASES; VIDARABINE;

EID: 0037437762     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(02)01484-3     Document Type: Article

References (49)

1. Piro L.D., Carrera C.J., Beutler E., Carson D.A. 2-Chlorodeoxyadenosine: an effective new agent for the treatment of chronic lymphocytic leukemia. Blood. 72:1988;1069-1073.
2. Kay A.C., Saven A., Carrera C.J., Carson D.A., Thurston D., Beutler E., Piro L.D. 2-Chlorodeoxyadenosine treatment of low-grade lymphomas. J. Clin. Oncol. 10:1992;371-377.
3. Kozuch P., Ibrahim N., Khuri F., Hoff P., Estey E., Gandhi V., Du M., Rios M.B., Plunkett W., Keating M., Kantarjian H. Phase I clinical and pharmacological study of clofarabine. Blood. 94:1999;127.
4. Lotfi K., Månsson E., Spasokoukotskaja T., Pettersson B., Liliemark J., Peterson C., Eriksson S., Albertioni F. Biochemical pharmacology and resistance to 2-chloro-2′-arabino-fluoro-2′-deoxyadenosine, a novel analogue of cladribine in human leukemic cells. Clin. Cancer Res. 5:1999;2438-2444.
5. Eriksson S., Kierdaszuk B., Munch-Petersen B., Oberg B., Johansson N.G. Comparison of the substrate specificities of human thymidine kinase 1 and 2 and deoxycytidine kinase toward antiviral and cytostatic nucleoside analogs. Biochem. Biophys. Res. Commun. 176:1991;586-592.
6. Arner E.S., Eriksson S. Mammalian deoxyribonucleoside kinases. Pharmacol. Ther. 67:1995;155-186.
7. Bai L., Yamaguchi M., Tatsumi M., Kon K., Brautigam M. Mechanisms responsible for resistance of sublines derived from leukemia cell lines to an antitumor agent 9-beta-D-arabinofuranosyl-2-fluoroadenine. J. Cancer Res. Clin. Oncol. 124:1998;367-373.
8. Jordan A., Reichard P. Ribonucleotide reductases. Ann. Rev. Biochem. 67:1998;71-98.
9. Schilsky R.L., Williams S.F., Ultmann J.E., Watson S. Sequential hydroxyurea-cytarabine chemotherapy for refractory non-Hodgkin's lymphoma. J. Clin. Oncol. 5:1987;419-425.
10. Elford H.L., van't Riet B. Inhibition of nucleoside diphosphate reductase by hydroxybenzohydroxamic acid derivatives. Pharmacol. Ther. 29:1985;239-254.
11. Bhalla K., Swerdlow P., Grant S. Effects of thymidine and hydroxyurea on the metabolism and cytotoxicity of 1-β-D-arabinofuranosylcytosine in highly resistant human leukemia cells. Blood. 78:1991;2937-2944.
12. Reichelova V., Albertioni F., Liliemark J. Determination of 2-chloro-2′-deoxyadenosine nucleotides in leukemic cells by ion-pair high-performance liquid chromatography. J. Chromatogr. B Biomed. Appl. 682:1996;115-123.
13. Plunkett W., Chubb S., Barlogie B. Simultaneous determination of 1-beta-D-arabinofuranosylcytosine 5′-triphosphate and 3-deazauridine 5′-triphosphate in human leukemia cells by high-performance liquid chromatography. J. Chromatogr. 221:1980;425-430.
14. Spasokoukotskaja T., Arner E.S., Brosjo O., Gunven P., Juliusson G., Liliemark J., Eriksson S. Expression of deoxycytidine kinase and phosphorylation of 2-chlorodeoxyadenosine in human normal and tumour cells and tissues. Eur. J. Cancer. 2:1995;202-208.
15. m (ecto-)-5′-nucleotidase gene expression in leukemic cells. Adv. Exp. Med. Biol. 370:1994;683-687.
16. Månsson E., Liliemark E., Söderhäll S., Gustafsson G., Eriksson S., Albertioni F. Real-time quantitative PCR assays for deoxycytidine kinase, deoxyguanosine kinase and 5′-nucleotidase mRNA measurement in cell lines and in patients with leukemia. Leukemia. 16:2002;386-392.
17. Albertioni F., Gruber A., Arestrom I., Vitols S. Multidrug resistance gene (mdr1) RNA levels in relation to P-glycoprotein content of leukemic cells from patients with acute leukemia. Med. Oncol. 12:1995;79-86.
18. Hatzis P., Al-Madhoon A.S., Jullig M., Petrakis T.G., Eriksson S., Talianidis I. The intracellular localization of deoxycytidine kinase. J. Biol. Chem. 273:1998;30239-30243.
19. Jullig M., Eriksson S. Mitochondrial and submitochondrial localization of human deoxyguanosine kinase. Eur. J. Biochem. 267:2000;5466-5472.
20. Lembo D., Gribaudo G., Hofer A., Riera L., Cornaglia M., Mondo A., Angeretti A., Gariglio M., Thelander L., Landolfo S. Expression of an altered ribonucleotide reductase activity associated with the replication of murine cytomegalovirus in quiescent fibroblasts. J. Virol. 74:2000;11557-11565.
21. Steeper J.R., Steuart C.D. A rapid assay for CDP reductase activity in mammalian cell extracts. Anal. Biochem. 34:1970;123-130.
22. Kallioniemi A., Kallioniemi O.P., Sudar D., Rutovitz D., Gray J.W., Waldman F., Pinkel D. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science. 258:1992;818-821.
23. Berglund M., Enblad G., Flordal E., Lui W.O., Backlin C., Thunberg U., Sundstrom C., Roos G., Allander S.V., Erlanson M., Rosenquist R., Larsson C., Lagercrantz S. Chromosomal imbalances in diffuse large B-cell lymphoma detected by comparative genomic hybridization. Mod. Pathol. 15:2002;807-816.
24. Goan Y.G., Zhou B., Hu E., Mi S., Yen Y. Overexpression of ribonucleotide reductase as a mechanism of resistance to 2,2-difluorodeoxycytidine in the human KB cancer cell line. Cancer Res. 59:1999;4204-4207.
25. Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., Takei Y., Nakamura Y. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature. 404:2000;42-49.
26. Guittet O., Hakansson P., Voevodskaya N., Fridd S., Graslund A., Arakawa H., Nakamura Y., Thelander L. Mammalian p53R2 protein forms an active ribonucleotide reductase in vitro with the R1 protein, which is expressed both in resting cells in response to DNA damage and in proliferating cells. J. Biol. Chem. 276:2001;40647-40651.
27. Juliusson G., Elmhorn-Rosenborg A., Liliemark J. Response to 2-chlorodeoxyadenosine in patients with B-cell chronic lymphocytic leukemia resistant to fludarabine. N. Engl. J. Med. 327:1992;1056-1061.
28. Rondelli D., Lauria F., Zinzani P.L., Raspadori D., Ventura M.A., Galieni P., Birtolo S., Forconi F., Algeri R., Tura S. 2-Chlorodeoxyadenosine in the treatment of relapsed/refractory chronic lymphoproliferative disorders. Eur. J. Haematol. 58:1997;46-50.
29. Parker W.B., Shaddix S.C., Chang C.H., White E.L., Rose L.M., Brockman R.W., Shortnacy A.T., Montgomery J.A., Secrist J.A. III, Bennett L.L. Jr. Effects of 2-chloro-9-(2-deoxy-2-fluoro-beta-D-arabinofuranosyl)adenine on K562 cellular metabolism and the inhibition of human ribonucleotide reductase and DNA polymerases by its 5′-triphosphate. Cancer Res. 51:1991;2386-2394.
30. Carson D.A., Wasson D.B., Esparza L.M., Carrera C.J., Kipps T.J., Cottam H.B. Oral antilymphocyte activity and induction of apoptosis by 2-chloro-2′-arabino-fluoro-2′-deoxyadenosine. Proc. Natl. Acad. Sci. U.S.A. 89:1992;2970-2974.
31. Xie K.C., Plunkett W. Deoxynucleotide pool depletion and sustained inhibition of ribonucleotide reductase and DNA synthesis after treatment of human lymphoblastoid cells with 2-chloro-9-(2-deoxy-2-fluoro-beta-D-arabinofuranosyl) adenine. Cancer Res. 56:1996;3030-3037.
32. Santana V.M., Mirro J. Jr., Harwood F.C., Cherrie J., Schell M., Kalwinsky D., Blakley R.L. A phase I clinical trial of 2-chlorodeoxyadenosine in pediatric patients with acute leukemia. J. Clin. Oncol. 9:1991;416-422.
33. Albertioni F., Lindemalm S., Reichelova V., Pettersson B., Eriksson S., Juliusson G., Liliemark J. Pharmacokinetics of cladribine in plasma and its 5-monophosphate and 5′-triphosphate in leukemic cells of patients with chronic lymphocytic leukemia. Clin. Cancer Res. 4:1998;653-658.
34. Owens J.K., Shewach D.S., Ullman B., Mitchell B.S. Resistance to 1-beta-D-arabinofuranosylcytosine in human T-lymphoblasts mediated by mutations within the deoxycytidine kinase gene. Cancer Res. 52:1992;2389-2393.
35. Månsson E., Spasokoukotskaja T., Sallstrom J., Eriksson S., Albertioni F. Molecular and biochemical mechanisms of fludarabine and cladribine resistance in a human promyelocytic cell line. Cancer Res. 59:1999;5956-5963.
36. Plunkett W., Saunders P.P. Metabolism and action of purine nucleoside analogs. Pharmacol. Ther. 49:1991;239-268.
37. Yen Y., Grill S.P., Dutschman G.E., Chang C.N., Zhou B.S., Cheng Y.C. Characterization of a hydroxyurea-resistant human KB cell line with supersensitivity to 6-thioguanine. Cancer Res. 54:1994;3686-3691.
38. Dumontet C., Fabianowska-Majewska K., Mantincic D., Callet Bauchu E., Tigaud I., Gandhi V., Lepoivre M., Peters G.J., Rolland M.O., Wyczechowska D., Fang X., Gazzo S., Voorn D.A., Vanier-Viornery A., MacKey J. Common resistance mechanisms to deoxynucleoside analogues in variants of the human erythroleukaemic line K562. Br. J. Haematol. 106:1999;78-85.
39. Meuth M., Green H. Alterations leading to increased ribonucleotide reductase in cells selected for resistance to deoxynucleosides. Cell. 3:1974;367-374.
40. Howell S.B., Gill S., Elford H.L. Modulation of cytarabine metabolism in the human promyelocytic leukemia cell line HL-60 by polyhydroxy-substituted benzohydroxamic acids. Cancer Treat Rep. 66:1982;1825-1829.
41. m 5′-nucleotidase in leukemic blasts is an independent prognostic factor in adults with acute myeloid leukemia. Blood. 98:2001;1922-1926.
42. Hunsucker S.A., Spychala J., Mitchell B.S. Human cytosolic 5′-nucleotidase I: characterization and role in nucleoside analog resistance. J. Biol. Chem. 276:2001;10498-10504.
43. Chitambar C.R., Wereley J.P., Heiman T., Antholine W.E., O'Brien W.J. Cellular adaptation to down-regulated iron transport into lymphoid leukaemic cells: effects on the expression of the gene for ribonucleotide reductase. Biochem. J. 345(Pt 3):2000;681-685.
44. Kong X.B., Tong W.P., Chou T.C. Induction of deoxycytidine kinase by 5-azacytidine in an HL-60 cell line resistant to arabinosylcytosine. Mol. Pharmacol. 39:1991;250-257.
45. Leegwater P.A., De Abreu R.A., Albertioni F. Analysis of DNA methylation of the 5′ region of the deoxycytidine kinase gene in CCRF-CEM-sensitive and cladribine (CdA) and 2-chloro-2′-arabino-fluoro-2′-deoxyadenosine (CAFdA)-resistant cells. Cancer Lett. 130:1998;169-173.
46. Wijnholds J., Mol C.A., van Deemter L., de Haas M., Scheffer G.L., Baas F., Beijnen J.H., Scheper R.J., Hatse S., De Clercq E., Balzarini J., Borst P. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc. Natl. Acad. Sci. U.S.A. 97:2000;7476-7481.
47. Leoni L.M., Chao Q., Cottam H.B., Genini D., Rosenbach M., Carrera C.J., Budihardjo I., Wang X., Carson D.A. Induction of an apoptotic program in cell-free extracts by 2-chloro-2′-deoxyadenosine 5′-triphosphate and cytochrome c. Proc. Natl. Acad. Sci. U.S.A. 95:1998;9567-9571.
48. Genini D., Adachi S., Chao Q., Rose D.W., Carrera C.J., Cottam H.B., Carson D.A., Leoni L.M. Deoxyadenosine analogs induce programmed cell death in chronic lymphocytic leukemia cells by damaging the DNA and by directly affecting the mitochondria. Blood. 96:2000;3537-3543.
49. Chandra J., Månsson E., Gogvadze V., Kaufmann S.H., Albertioni F., Orrenius S. Resistance of leukemic cells to 2-chlorodeoxyadenosine is due to a lack of calcium-dependent cytochrome c release. Blood. 99:2002;655-663.