The role of DNA damage and repair in decitabine-mediated apoptosis in multiple myeloma

Oncotarget

Volumn 5, Issue 10, 2014, Pages 3115-3129

  Maes, Ken ^a   Smedt, Eva De ^a   Lemaire, Miguel ^a   De Raeve, Hendrik ^b   Menu, Eline ^a   Van Valckenborgh, Els ^a   McClue, Steve ^c   Vanderkerken, Karin ^a   De Bruyne, Elke ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^c JOHNSON AND JOHNSON   (United States)

Author keywords

DNA damage; DNA methyltransferase inhibitor; DNA repair; Histone deacetylase inhibitor; Multiple myeloma

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BRCA1 PROTEIN; BRCA2 PROTEIN; CASPASE 3; CASPASE 8; CASPASE 9; HISTONE DEACETYLASE INHIBITOR; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN MCL 1; PROTEIN P27; QUISINOSTAT; RAD51 PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; ANTINEOPLASTIC AGENT; AZACITIDINE; HYDROXAMIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER SURVIVAL; CELL CYCLE; CELL CYCLE CHECKPOINT; DNA DAMAGE; DNA REPAIR; DRUG CYTOTOXICITY; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PROTEIN CLEAVAGE; RAD51 GENE; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HOMOLOGOUS RECOMBINATION; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; AZACITIDINE; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA REPAIR; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HOMOLOGOUS RECOMBINATION; HUMANS; HYDROXAMIC ACIDS; MICE; MICE, INBRED C57BL; MULTIPLE MYELOMA; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84902082388     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1821     Document Type: Article

References (70)

1. Mahindra A, Hideshima T and Anderson KC. Multiple myeloma: biology of the disease. Blood Rev. 2011; 24 Suppl 1: S5-11.
2. Engelhardt M, Terpos E, Kleber M, Gay F, Wasch R, Morgan G, Cavo M, van de Donk N, Beilhack A, Bruno B, Johnsen HE, Hajek R, Driessen C, et al. European Myeloma Network recommendations on the evaluation and treatment of newly diagnosed patients with multiple myeloma. Haematologica. 2014; 99: 232-242.
3. Facon T, Mary JY, Hulin C, Benboubker L, Attal M, Pegourie B, Renaud M, Harousseau JL, Guillerm G, Chaleteix C, Dib M, Voillat L, Maisonneuve H, et al. Melphalan and prednisone plus thalidomide versus melphalan and prednisone alone or reduced-intensity autologous stem cell transplantation in elderly patients with multiple myeloma (IFM 99-06): a randomised trial. Lancet. 2007; 370: 1209-1218.
4. Harousseau JL, Attal M, Avet-Loiseau H, Marit G, Caillot D, Mohty M, Lenain P, Hulin C, Facon T, Casassus P, Michallet M, Maisonneuve H, Benboubker L, et al. Bortezomib plus dexamethasone is superior to vincristine plus doxorubicin plus dexamethasone as induction treatment prior to autologous stem-cell transplantation in newly diagnosed multiple myeloma: results of the IFM 2005-01 phase III trial. J Clin Oncol. 2010; 28: 4621-4629.
5. Leleu X, Attal M, Arnulf B, Moreau P, Traulle C, Marit G, Mathiot C, Petillon MO, Macro M, Roussel M, Pegourie B, Kolb B, Stoppa AM, et al. Pomalidomide plus low-dose dexamethasone is active and well tolerated in bortezomib and lenalidomide-refractory multiple myeloma: Intergroupe Francophone du Myelome 2009-02. Blood. 2013; 121: 1968-1975.
6. Roussel M, Facon T, Moreau P, Harousseau JL and Attal M. Firstline treatment and maintenance in newly diagnosed multiple myeloma patients. Recent Results Cancer Res. 2011; 183: 189-206.
7. Sonneveld P, Schmidt-Wolf IG, van der Holt B, El Jarari L, Bertsch U, Salwender H, Zweegman S, Vellenga E, Broyl A, Blau IW, Weisel KC, Wittebol S, Bos GM, et al. Bortezomib induction and maintenance treatment in patients with newly diagnosed multiple myeloma: results of the randomized phase III HOVON-65/ GMMG-HD4 trial. J Clin Oncol. 2012; 30: 2946-2955.
8. Usmani SZ, Crowley J, Hoering A, Mitchell A, Waheed S, Nair B, AlSayed Y, Vanrhee F and Barlogie B. Improvement in long-term outcomes with successive Total Therapy trials for multiple myeloma: are patients now being cured? Leukemia. 2013; 27: 226-232.
9. Sharma S, Kelly TK and Jones PA. Epigenetics in cancer. Carcinogenesis. 2010; 31: 27-36.
10. Maes K, Menu E, Van Valckenborgh E, Van Riet I, Vanderkerken K and De Bruyne E. Epigenetic modulating agents as a new therapeutic approach in multiple myeloma. Cancers. 2013; 5: 430-461.
11. Stresemann C and Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer. 2008; 123: 8-13.
12. Lord CJ and Ashworth A. The DNA damage response and cancer therapy. Nature. 2012; 481: 287-294.
13. Gourzones-Dmitriev C, Kassambara A, Sahota S, Reme T, Moreaux J, Bourquard P, Hose D, Pasero P, Constantinou A and Klein B. DNA repair pathways in human multiple myeloma: role in oncogenesis and potential targets for treatment. Cell Cycle. 2013; 12: 2760-2773.
14. Yang C, Betti C, Singh S, Toor A and Vaughan A. Impaired NHEJ function in multiple myeloma. Mutat Res. 2009; 660: 66-73.
15. Shammas MA, Shmookler Reis RJ, Koley H, Batchu RB, Li C and Munshi NC. Dysfunctional homologous recombination mediates genomic instability and progression in myeloma. Blood. 2009; 113: 2290-2297.
16. Nakano T, Katafuchi A, Matsubara M, Terato H, Tsuboi T, Masuda T, Tatsumoto T, Pack SP, Makino K, Croteau DL, Van Houten B, Iijima K, Tauchi H, et al. Homologous recombination but not nucleotide excision repair plays a pivotal role in tolerance of DNA-protein cross-links in mammalian cells. J Biol Chem. 2009; 284: 27065-27076.
17. Orta ML, Calderon-Montano JM, Dominguez I, Pastor N, Burgos-Moron E, Lopez-Lazaro M, Cortes F, Mateos S and Helleday T. 5-Aza-2'-deoxycytidine causes replication lesions that require Fanconi anemia-dependent homologous recombination for repair. Nucleic Acids Res. 2013; 41: 5827-5836.
18. Dimopoulos M, Siegel DS, Lonial S, Qi J, Hajek R, Facon T, Rosinol L, Williams C, Blacklock H, Goldschmidt H, Hungria V, Spencer A, Palumbo A, et al. Vorinostat or placebo in combination with bortezomib in patients with multiple myeloma (VANTAGE 088): a multicentre, randomised, double-blind study. Lancet Oncol. 2013; 14: 1129-1140.
19. Richardson PG, Schlossman RL, Alsina M, Weber DM, Coutre SE, Gasparetto C, Mukhopadhyay S, Ondovik MS, Khan M, Paley CS and Lonial S. PANORAMA 2: panobinostat in combination with bortezomib and dexamethasone in patients with relapsed and bortezomib-refractory myeloma. Blood. 2013; 122: 2331-2337.
20. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, Botrugno OA, Parazzoli D, Oldani A, Minucci S and Foiani M. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature. 2011; 471: 74-79.
21. Boumber Y and Issa JP. Epigenetics in cancer: what's the future? Oncology (Williston Park). 2011; 25: 220-226, 228.
22. Mercurio C, Minucci S and Pelicci PG. Histone deacetylases and epigenetic therapies of hematological malignancies. Pharmacol Res. 2010; 62: 18-34.
23. Heller G, Schmidt WM, Ziegler B, Holzer S, Mullauer L, Bilban M, Zielinski CC, Drach J and Zochbauer-Muller S. Genome-wide transcriptional response to 5-aza-2'-deoxycytidine and trichostatin a in multiple myeloma cells. Cancer Res. 2008; 68: 44-54.
24. Steele N, Finn P, Brown R and Plumb JA. Combined inhibition of DNA methylation and histone acetylation enhances gene re-expression and drug sensitivity in vivo. Br J Cancer. 2009; 100: 758-763.
25. Brodska B and Holoubek A. Generation of reactive oxygen species during apoptosis induced by DNA-damaging agents and/or histone deacetylase inhibitors. Oxid Med Cell Longev. 2011; 2011: 253529-253535.
26. Brodska B, Otevrelova P and Holoubek A. Decitabine-induced apoptosis is derived by Puma and Noxa induction in chronic myeloid leukemia cell line as well as in PBL and is potentiated by SAHA. Mol Cell Biochem. 2011; 350: 71-80.
27. Chen MY, Liao WS, Lu Z, Bornmann WG, Hennessey V, Washington MN, Rosner GL, Yu Y, Ahmed AA and Bast RC, Jr. Decitabine and suberoylanilide hydroxamic acid (SAHA) inhibit growth of ovarian cancer cell lines and xenografts while inducing expression of imprinted tumor suppressor genes, apoptosis, G2/M arrest, and autophagy. Cancer. 2011; 117: 4424-4438.
28. Nishioka C, Ikezoe T, Yang J, Udaka K and Yokoyama A. Simultaneous inhibition of DNA methyltransferase and histone deacetylase induces p53-independent apoptosis via down-regulation of Mcl-1 in acute myelogenous leukemia cells. Leuk Res. 2011; 35: 932-939.
29. De Bruyne E, Bos TJ, Schuit F, Van Valckenborgh E, Menu E, Thorrez L, Atadja P, Jernberg-Wiklund H and Vanderkerken K. IGF-1 suppresses Bim expression in multiple myeloma via epigenetic and posttranslational mechanisms. Blood. 2010; 115: 2430-2440.
30. Asosingh K, Radl J, Van Riet I, Van Camp B and Vanderkerken K. The 5TMM series: a useful in vivo mouse model of human multiple myeloma. Hematol J. 2000; 1: 351-356.
31. Deleu S, Lemaire M, Arts J, Menu E, Van Valckenborgh E, King P, Vande Broek I, De Raeve H, Van Camp B, Croucher P and Vanderkerken K. The effects of JNJ-26481585, a novel hydroxamate-based histone deacetylase inhibitor, on the development of multiple myeloma in the 5T2MM and 5T33MM murine models. Leukemia. 2009; 23: 1894-1903.
32. Besson A, Dowdy SF and Roberts JM. CDK inhibitors: cell cycle regulators and beyond. Dev Cell. 2008; 14: 159-169.
33. Huang F, Motlekar NA, Burgwin CM, Napper AD, Diamond SL and Mazin AV. Identification of specific inhibitors of human RAD51 recombinase using high-throughput screening. ACS Chem Biol. 2011; 6: 628-635.
34. Huang F, Mazina OM, Zentner IJ, Cocklin S and Mazin AV. Inhibition of homologous recombination in human cells by targeting RAD51 recombinase. J Med Chem. 2012; 55: 3011-3020.
35. Donawho CK, Luo Y, Luo Y, Penning TD, Bauch JL, Bouska JJ, Bontcheva-Diaz VD, Cox BF, DeWeese TL, Dillehay LE, Ferguson DC, Ghoreishi-Haack NS, Grimm DR, et al. ABT-888, an orally active poly(ADP-ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin Cancer Res. 2007; 13: 2728-2737.
36. Moreaux J, Reme T, Leonard W, Veyrune JL, Requirand G, Goldschmidt H, Hose D and Klein B. Development of gene expression-based score to predict sensitivity of multiple myeloma cells to DNA methylation inhibitors. Mol Cancer Ther. 2012; 11: 2685-2692.
37. Kim JH, Sim SH, Ha HJ, Ko JJ, Lee K and Bae J. MCL-1ES, a novel variant of MCL-1, associates with MCL-1L and induces mitochondrial cell death. FEBS Lett. 2009; 583: 2758-2764.
38. Le Gouill S, Podar K, Harousseau JL and Anderson KC. Mcl-1 regulation and its role in multiple myeloma. Cell Cycle. 2004; 3: 1259-1262.
39. Kiziltepe T, Hideshima T, Catley L, Raje N, Yasui H, Shiraishi N, Okawa Y, Ikeda H, Vallet S, Pozzi S, Ishitsuka K, Ocio EM, Chauhan D, et al. 5-Azacytidine, a DNA methyltransferase inhibitor, induces ATR-mediated DNA double-strand break responses, apoptosis, and synergistic cytotoxicity with doxorubicin and bortezomib against multiple myeloma cells. Mol Cancer Ther. 2007; 6: 1718-1727.
40. Jiemjit A, Fandy TE, Carraway H, Bailey KA, Baylin S, Herman JG and Gore SD. p21(WAF1/CIP1) induction by 5-azacytosine nucleosides requires DNA damage. Oncogene. 2008; 27: 3615-3623.
41. Lavelle D, DeSimone J, Hankewych M, Kousnetzova T and Chen YH. Decitabine induces cell cycle arrest at the G1 phase via p21(WAF1) and the G2/M phase via the p38 MAP kinase pathway. Leuk Res. 2003; 27: 999-1007.
42. Shin DY, Sung Kang H, Kim GY, Kim WJ, Yoo YH and Choi YH. Decitabine, a DNA methyltransferases inhibitor, induces cell cycle arrest at G2/M phase through p53-independent pathway in human cancer cells. Biomed Pharmacother. 2013; 67: 305-311.
43. Cuadrado M, Gutierrez-Martinez P, Swat A, Nebreda AR and Fernandez-Capetillo O. p27Kip1 stabilization is essential for the maintenance of cell cycle arrest in response to DNA damage. Cancer Res. 2009; 69: 8726-8732.
44. Carrano A, Eytan E, Hershko A and Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol. 1999; 1: 193-199.
45. Roe JS, Kim HR, Hwang IY, Cho EJ and Youn HD. von Hippel-Lindau protein promotes Skp2 destabilization on DNA damage. Oncogene. 2011; 30: 3127-3138.
46. Sugihara E, Kanai M, Saito S, Nitta T, Toyoshima H, Nakayama K, Nakayama KI, Fukasawa K, Schwab M, Saya H and Miwa M. Suppression of centrosome amplification after DNA damage depends on p27 accumulation. Cancer Res. 2006; 66: 4020-4029.
47. Palii SS, Van Emburgh BO, Sankpal UT, Brown KD and Robertson KD. DNA methylation inhibitor 5-Aza-2'-deoxycytidine induces reversible genome-wide DNA damage that is distinctly influenced by DNA methyltransferases 1 and 3B. Mol Cell Biol. 2008; 28: 752-771.
48. Walters DK, Wu X, Tschumper RC, Arendt BK, Huddleston PM, Henderson KJ, Dispenzieri A and Jelinek DF. Evidence for ongoing DNA damage in multiple myeloma cells as revealed by constitutive phosphorylation of H2AX. Leukemia. 2011; 25: 1344-1353.
49. Chen G, Wang Y, Huang H, Lin F, Wu D, Sun A, Chang H and Feng Y. Combination of DNA methylation inhibitor 5-azacytidine and arsenic trioxide has synergistic activity in myeloma. Eur J Haematol. 2009; 82: 176-183.
50. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM and Buggy JJ. HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci U S A. 2007; 104: 19482-19487.
51. Chen X, Wong P, Radany EH, Stark JM, Laulier C and Wong JY. Suberoylanilide hydroxamic acid as a radiosensitizer through modulation of RAD51 protein and inhibition of homology-directed repair in multiple myeloma. Mol Cancer Res. 2012; 10: 1052-1064.
52. Lee CK, Wang S, Huang X, Ryder J and Liu B. HDAC inhibition synergistically enhances alkylator-induced DNA damage responses and apoptosis in multiple myeloma cells. Cancer Lett. 2010; 296: 233-240.
53. Sanchez E, Shen J, Steinberg J, Li M, Wang C, Bonavida B, Chen H, Li ZW and Berenson JR. The histone deacetylase inhibitor LBH589 enhances the anti-myeloma effects of chemotherapy in vitro and in vivo. Leuk Res. 2010; 35: 373-379.
54. Neri P, Ren L, Gratton K, Stebner E, Johnson J, Klimowicz A, Duggan P, Tassone P, Mansoor A, Stewart DA, Lonial S, Boise LH and Bahlis NJ. Bortezomib-induced "BRCAness" sensitizes multiple myeloma cells to PARP inhibitors. Blood. 2011; 118: 6368-6379.
55. Clark CC, Weitzel JN and O'Connor TR. Enhancement of synthetic lethality via combinations of ABT-888, a PARP inhibitor, and carboplatin in vitro and in vivo using BRCA1 and BRCA2 isogenic models. Mol Cancer Ther. 2012; 11: 1948-1958.
56. Shunkwiler L, Ferris G and Kunos C. Inhibition of Poly(ADP-Ribose) Polymerase Enhances Radiochemosensitivity in Cancers Proficient in DNA Double-Strand Break Repair. Int J Mol Sci. 2013; 14: 3773-3785.
57. Chen A. PARP inhibitors: its role in treatment of cancer. Chin J Cancer. 2011; 30: 463-471.
58. De Lorenzo SB, Patel AG, Hurley RM and Kaufmann SH. The Elephant and the Blind Men: Making Sense of PARP Inhibitors in Homologous Recombination Deficient Tumor Cells. Front Oncol. 2013; 3: 228.
59. Pears CJ, Couto CA, Wang HY, Borer C, Kiely R and Lakin ND. The role of ADP-ribosylation in regulating DNA double-strand break repair. Cell Cycle. 2012; 11: 48-56.
60. Bryant HE, Petermann E, Schultz N, Jemth AS, Loseva O, Issaeva N, Johansson F, Fernandez S, McGlynn P and Helleday T. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. Embo J. 2009; 28: 2601-2615.
61. Couto CA, Wang HY, Green JC, Kiely R, Siddaway R, Borer C, Pears CJ and Lakin ND. PARP regulates nonhomologous end joining through retention of Ku at double-strand breaks. J Cell Biol. 2011; 194: 367-375.
62. Wang M, Wu W, Wu W, Rosidi B, Zhang L, Wang H and Iliakis G. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 2006; 34: 6170-6182.
63. Moreau P. Panobinostat to revert bortezomib resistance. Blood. 2013; 122: 2292-2293.
64. Moreau P, Facon T, Touzeau C, Benboubker L, Delain M, Badamo-Dotzis J, Phelps C, Doty C, Smit H, Fourneau N, Forslund A, Hellemans P and Leleu X. Phase 1b Dose Escalation Study Of Oral Quisinostat, a Histone Deacetylase Inhibitor (HDACi), In Combination With Velcade (Bortezomib) and Dexamethasone For Patients With Relapsed Multiple Myeloma (MM). Blood. 2013; 122: 1932.
65. Hose D, Reme T, Hielscher T, Moreaux J, Messner T, Seckinger A, Benner A, Shaughnessy JD, Jr., Barlogie B, Zhou Y, Hillengass J, Bertsch U, Neben K, et al. Proliferation is a central independent prognostic factor and target for personalized and risk-adapted treatment in multiple myeloma. Haematologica. 2011; 96: 87-95.
66. Jourdan M, Caraux A, Caron G, Robert N, Fiol G, Reme T, Bollore K, Vendrell JP, Le Gallou S, Mourcin F, De Vos J, Kassambara A, Duperray C, et al. Characterization of a transitional preplasmablast population in the process of human B cell to plasma cell differentiation. J Immunol. 2011; 187: 3931-3941.
67. Jourdan M, Caraux A, De Vos J, Fiol G, Larroque M, Cognot C, Bret C, Duperray C, Hose D and Klein B. An in vitro model of differentiation of memory B cells into plasmablasts and plasma cells including detailed phenotypic and molecular characterization. Blood. 2009; 114: 5173-5181.
68. Leung-Hagesteijn C, Erdmann N, Cheung G, Keats JJ, Stewart AK, Reece DE, Chung KC and Tiedemann RE. Xbp1s-negative tumor B cells and pre-plasmablasts mediate therapeutic proteasome inhibitor resistance in multiple myeloma. Cancer Cell. 2013; 24: 289-304.
69. Caraux A, Vincent L, Bouhya S, Quittet P, Moreaux J, Requirand G, Veyrune JL, Olivier G, Cartron G, Rossi JF and Klein B. Residual malignant and normal plasmacells shortly after high dose melphalan and stem cell transplantation. Highlight of a putative therapeutic window in Multiple Myeloma? Oncotarget. 2012; 3: 1335-1347.
70. Chaidos A, Barnes CP, Cowan G, May PC, Melo V, Hatjiharissi E, Papaioannou M, Harrington H, Doolittle H, Terpos E, Dimopoulos M, Abdalla S, Yarranton H, et al. Clinical drug resistance linked to interconvertible phenotypic and functional states of tumor-propagating cells in multiple myeloma. Blood. 2012; 121: 318-328.