Targeting DNA repair in chronic lymphocytic leukemia cells with a novel acyclic nucleotide analogue, GS-9219

Clinical Cancer Research

Volumn 15, Issue 11, 2009, Pages 3760-3769

  Tsai, Cheng Yu ^a,b   Ray, Adrian S ^c   Tumas, Daniel B ^b   Keating, Michael J ^a   Reiser, Hans ^c   Plunkett, William ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c GILEAD SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

9 (2 PHOSPHONYLMETHOXYETHYL)GUANINE; ATM PROTEIN; DNA DEPENDENT PROTEIN KINASE; GS 9219; GUANINE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN P53; PUMA PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; CHRONIC LYMPHATIC LEUKEMIA; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DNA SYNTHESIS; DRUG DNA INTERACTION; DRUG MECHANISM; DRUG METABOLISM; DRUG STRUCTURE; ENZYME ACTIVATION; EXCISION REPAIR; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ALANINE; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL SURVIVAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DNA DAMAGE; DNA REPAIR; DNA, NEOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; GUANINE; HUMANS; IMMUNOBLOTTING; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; ORGANOPHOSPHORUS COMPOUNDS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; PURINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; ULTRAVIOLET RAYS;

EID: 66649100502     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-08-2848     Document Type: Article

References (51)

1. Keating MJ, Chiorazzi N, Messmer B, et al. Biology and treatment of chronic lymphocytic leukemia. Hematology Am Soc Hematol Educ Program 2003;153-175
2. Deriano L, Guipaud O, Merle-Beral H, et al. Human chronic lymphocytic leukemia B cells can escape DNA damage-induced apoptosis through the nonhomologous end-joining DNA repair pathway. Blood 2005;105:4776-4783 (Pubitemid 40807303)
3. Sandoval A, Consoli U, Plunkett W. Fludarabine-mediated inhibition of nucleotide excision repair induces apoptosis in quiescent human lymphocytes. Clin Cancer Res 1996;2:1731-1741 (Pubitemid 26356359)
4. Huang P, Chubb S, Plunkett W. Termination of DNA synthesis by 9-β-D-arabinofuranosyl-2-fluoroadenine. A mechanism for cytotoxicity. J Biol Chem 1990;265:16617-16625 (Pubitemid 20324547)
5. Rao VA, Plunkett W. Activation of a p53-mediated apoptotic pathway in quiescent lymphocytes after the inhibition of DNA repair by fludarabine. Clin Cancer Res 2003;9:3204-3212 (Pubitemid 36993284)
6. Moufarij MA, Sampath D, Keating MJ, Plunkett W. Fludarabine increases oxaliplatin cytotoxicity in normal and chronic lymphocytic leukemia lymphocytes by suppressing interstrand DNA crosslink removal. Blood 2006;108:4187-4193 (Pubitemid 44913291)
7. Hallek M, Schmitt B, Wilhelm M, et al. Fludarabine plus cyclophosphamide is an efficient treatment for advanced chronic lymphocytic leukaemia (CLL): results of a phase II study of the German CLL Study Group. Br J Haematol 2001;114:342-348 (Pubitemid 32762233)
8. O'Brien SM, Kantarjian HM, Cortes J, et al. Results of the fludarabine and cyclophosphamide combination regimen in chronic lymphocytic leukemia. J Clin Oncol 2001;19:1414-1420 (Pubitemid 32202548)
9. Montillo M, Tedeschi A, O'Brien S, et al. Phase II study of cladribine and cyclophosphamide in patients with chronic lymphocytic leukemia and prolymphocytic leukemia. Cancer 2003;97:114-120 (Pubitemid 36033870)
10. Eichhorst BF, Busch R, Hopfinger G, et al. Fludarabine plus cyclophosphamide versus fludarabine alone in first-line therapy of younger patients with chronic lymphocytic leukemia. Blood 2006;107:885-891 (Pubitemid 43156283)
11. Catovsky D, Richards S, Matutes E, et al. Assessment of fludarabine plus cyclophosphamide for patients with chronic lymphocytic leukaemia (the LRF CLL4 Trial): a randomised controlled trial. Lancet 2007;370:230-239 (Pubitemid 47069536)
12. Flinn IW, Neuberg DS, Grever MR, et al. Phase III trial of fludarabine plus cyclophosphamide compared with fludarabine for patients with previously untreated chronic lymphocytic leukemia: U.S. Intergroup Trial E2997. J Clin Oncol 2007;25:793-798 (Pubitemid 350002879)
13. Reiser H, Wang J, Chong L, et al. GS-9219 - a novel acyclic nucleotide analogue with potent antineoplastic activity in dogs with spontaneous non-Hodgkin's lymphoma. Clin Cancer Res 2008;14:2824-2832
14. Rose WC, Crosswell AR, Bronson JJ, Martin JC. In vivo antitumor activity of 9-[(2-phosphonylmethoxy) ethyl]-guanine and related phosphonate nucleotide analogues. J Natl Cancer Inst 1990;82:510-512
15. Holy A. Antiviral acyclic nucleoside phosphonates structure activity studies. Antiviral Res 2006;71:248-253 (Pubitemid 44223782)
16. Cihlar T, Lin DC, Pritchard JB, Fuller MD, Mendel DB, Sweet DH. The antiviral nucleotide analogs cidofovir and adefovir are novel substrates for human and rat renal organic anion transporter 1. Mol Pharmacol 1999;56:570-580 (Pubitemid 29406884)
17. 6-cyclopropyl-2,6-diaminopurine: a novel prodrug of 9-(2-phosphonylmethoxyethyl)guanine with improved antitumor efficacy and selectivity in choriocarcinoma-bearing rats. Oncol Res 1999;11:195-203.
18. 6-cyclopropyl-2,6-diaminopurine (cpr-PMEDAP) as a prodrug of 9-(2-phosphonylmethoxyethyl)guanine (PMEG). Biochem Pharmacol 1999;58:709-714
19. McGuigan C, Tsang HW, Sutton PW, De Clercq E, Balzarini J. Synthesis and anti-HIV activity of some novel chain extended phosphoramidate derivatives of d4T (stavudine): esterase hydrolysis as a rapid predictive test for antiviral potency. Antivir Chem Chemother 1998;9:109-115 (Pubitemid 28160956)
20. Ho HT, Woods KL, Konrad SA, De Boeck H, Hitchcock MJ. Cellular metabolism and enzymatic phosphorylation of 9-(2-phosphonylmethoxyethyl) guanine (PMEG), a potent antiviral agent. Adv Exp Med Biol 1992;312:159-166
21. Kramata P, Votruba I, Otova B, Holy A. Different-inhibitory potencies of acyclic phosphonomethoxyalkyl nucleotide analogs toward DNA polymerases α, δ and ε Mol Pharmacol 1996;49:1005-1011
22. Kramata P, Downey KM, Paborsky LR. Incorporation and excision of 9-(2-phosphonylmethoxyethyl)guanine (PMEG) by DNA polymerase δ and ε in vitro. J Biol Chem 1998;273:21966-21971 (Pubitemid 28405376)
23. Kramata P, Downey KM. 9-(2-Phosphonylmethoxyethyl) derivatives of purine nucleotide analogs: a comparison of their metabolism and interaction with cellular DNA synthesis. Mol Pharmacol 1999;56:1262-1270
24. Yamauchi T, Nowak BJ, Keating MJ, Plunkett W. DNA repair initiated in chronic lymphocytic leukemia lymphocytes by 4-hydroperoxycyclophosphamide is inhibited by fludarabine and clofarabine. Clin Cancer Res 2001;7:3580-3589 (Pubitemid 33069998)
25. Olive PL, Banath JP, Durand RE. Detection of etoposide resistance by measuring DNA damage in individual Chinese hamster cells. J Natl Cancer Inst 1990;82:779-783 (Pubitemid 20159279)
26. Olive PL, Banath JP, Durand RE. Heterogeneity in radiation-induced DNA damage and repair in tumor and normal cells measured using the "comet" assay. Radiat Res 1990;122:86-94.
27. Chen R, Gandhi V, Plunkett W. A sequential blockade strategy for the design of combination therapies to overcome oncogene addiction in chronic myelogenous leukemia. Cancer Res 2006;66:10959-10966 (Pubitemid 44876995)
28. Gu J, Zhang L, Swisher SG, Liu J, Roth JA, Fang B. Induction of p53-regulated genes in lung cancer cells: implications of the mechanism for adenoviral p53-mediated apoptosis. Oncogene 2004;23:1300-1307 (Pubitemid 38297185)
29. Balakrishnan K, Nimmanapalli R, Ravandi F, Keating MJ, Gandhi V. Forodesine, an inhibitor of purine nucleoside phosphorylase, induces apoptosis in chronic lymphocytic leukemia cells. Blood 2006;108:2392-2398 (Pubitemid 44497524)
30. Ringborg ULB. Ultraviolet-induced DNA-repair synthesis in lymphocytes from patients with chronic lymphatic leukemia. Cancer Lett 1977;3:77-C81.
31. Van Den Neste E, Cardoen S, Husson B, et al. 2-Chloro-2′- deoxyadenosine inhibits DNA repair synthesis and potentiates UVC cytotoxicity in chronic lymphocytic leukemia B lymphocytes. Leukemia 2002;16:36-C43. (Pubitemid 34105597)
32. Abraham RT. PI 3-kinase related kinases: "big" players in stress-induced signaling pathways. DNA Repair (Amst) 2004;3:883-C7.
33. Jones GG, Reaper PM, Pettitt AR, Sherrington PD. The ATR-p53 pathway is suppressed in non-cycling normal and malignant lymphocytes. Oncogene 2004;23:1911-C21. (Pubitemid 38445417)
34. Banin S, Moyal L, Shieh S, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998;281:1674-C7. (Pubitemid 28435583)
35. Hickson I, Zhao Y, Richardson CJ, et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004;64:9152-C9. (Pubitemid 39665530)
36. Mackus WJ, Kater AP, Grummels A, et al. Chronic lymphocytic leukemia cells display p53-dependent drug-induced Puma up-regulation. Leukemia 2005;19:427-C34. (Pubitemid 40403321)
37. Wu Y, Mehew JW, Heckman CA, Arcinas M, Boxer LM. Negative regulation of bcl-2 expression by p53 in hematopoietic cells. Oncogene 2001;20:240-C51. (Pubitemid 32150269)
38. Perdiz D, Grof P, Mezzina M, Nikaido O, Moustacchi E, Sage E. Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis. J Biol Chem 2000;275:26732-C42.
39. Tew KD, Colvin M, Chabner BA. Alkylating agents. In: Chabner BA, Longo DL, editors. Cancer chemotherapy and biotherapy. Philadelphia: Lippincot-Raven; 1996. p. 297-C332.
40. Byrd JC, Gribben JG, Peterson BL, et al. Select high-risk genetic features predict earlier progression following chemoimmunotherapy with fludarabine and rituximab in chronic lymphocytic leukemia: justification for risk-adapted therapy. J Clin Oncol 2006;24:437-C43. (Pubitemid 46655595)
41. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 2003;3:155-C68.
42. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003;421:499-C506. (Pubitemid 36168436)
43. Lobrich M, Jeggo PA. Harmonising the response to DSBs: a new string in the ATM bow. DNA Repair (Amst) 2005;4:749-C59. (Pubitemid 40835847)
44. Austen B, Skowronska A, Baker C, et al. Mutation status of the residual ATM allele is an important determinant of the cellular response to chemotherapy and survival in patients with chronic lymphocytic leukemia containing an 11q deletion. J Clin Oncol 2007;25:5448-C57. (Pubitemid 350232222)
45. Wang S, Guo M, Ouyang H, et al. The catalytic subunit of DNA-dependent protein kinase selectively regulates p53-dependent apoptosis but not cell-cycle arrest. Proc Natl Acad Sci U S A 2000;97:1584-C8. (Pubitemid 30118485)
46. Del Gaizo Moore V, Brown JR, Certo M, Love TM, Novina CD, Letai A. Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737. J Clin Invest 2007;117:112-C21. (Pubitemid 46048458)
47. Nakano K, Vousden KH. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 2001;7:683-C94. (Pubitemid 32706359)
48. Oda E, Ohki R, Murasawa H, et al. Noxa, a BH3- only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 2000;288:1053-C8. (Pubitemid 30324238)
49. Sax JK, Fei P, Murphy ME, Bernhard E, Korsmeyer SJ, El-Deiry WS. BID regulation by p53 contributes to chemosensitivity. Nat Cell Biol 2002;4:842-C9. (Pubitemid 35331358)
50. Yee KS, Vousden KH. Contribution of membrane localization to the apoptotic activity of PUMA. Apoptosis 2008;13:87-C95.
51. Letai AG. Diagnosing and exploiting cancer's addiction to blocks in apoptosis. Nat Rev Cancer 2008;8:121-C32.