Suberoylanilide hydroxamic acid as a radiosensitizer through modulation of RAD51 protein and inhibition of homology-directed repair in multiple myeloma

Molecular Cancer Research

Volumn 10, Issue 8, 2012, Pages 1052-1064

  Chen, Xufeng ^a   Wong, Patty ^a   Radany, Eric H ^a   Stark, Jeremy M ^a   Laulier, Corentin ^a   Wong, Jeffrey Y C ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; RAD51 PROTEIN; RADIOSENSITIZING AGENT; VORINOSTAT;

ARTICLE; CELL CYCLE REGULATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DRUG MECHANISM; DRUG SELECTIVITY; HOMOLOGY DIRECTED REPAIR; HUMAN; HUMAN CELL; IONIZING RADIATION; MULTIPLE MYELOMA; MYELOMA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; RADIOSENSITIVITY; RADIOSENSITIZATION; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; CELL SURVIVAL; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MULTIPLE MYELOMA; RAD51 RECOMBINASE; RADIATION-SENSITIZING AGENTS; RECOMBINATIONAL DNA REPAIR;

EID: 84865305652     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-11-0587     Document Type: Article

References (51)

1. Barille-Nion S, Barlogie B, Bataille R, Bergsagel PL, Epstein J, Fenton RG, et al. Advances in biology and therapy of multiple myeloma. Hematology Am Soc Hematol Educ Program 2003;248-78.
2. Richards T, Weber D. Advances in treatment for relapses and refractory multiple myeloma. Med Oncol 2010;27 Suppl 1:S25-42.
3. Moehler T, Goldschmidt H. Therapy of relapsed and refractory multiple myeloma. Recent Results Cancer Res 2011;183:239-71.
4. Wong JY, Liu A, Schultheiss T, Popplewell L, Stein A, Rosenthal J, et al. Targeted total marrow irradiation using three-dimensional image-guided tomographic intensity-modulated radiation therapy: an alternative to standard total body irradiation. Biol Blood Marrow Transplant 2006;12:306-15.
5. Rosenthal J, Wong J, Stein A, Qian D, Hitt D, Naeem H, et al. Phase 1/2 trial of total marrow and lymph node irradiation to augment reduced-intensity transplantation for advanced hematologic malignancies. Blood 2011;117:309-15.
6. Wong JY, Rosenthal J, Liu A, Schultheiss T, Forman S, Somlo G. Image-guided total-marrow irradiation using helical tomotherapy in patients with multiple myeloma and acute leukemia undergoing hematopoietic cell transplantation. Int J Radiat Oncol Biol Phys 2009; 73:273-9.
7. Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol 2004;338:17-31.
8. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, Hideshima T, et al. Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications. Proc Natl Acad Sci U S A 2004;101:540-5.
9. Florenes VA, Skrede M, Jorgensen K, Nesland JM. Deacetylase inhibition in malignant melanomas: impact on cell cycle regulation and survival. Melanoma Res 2004;14:173-81.
10. Piekarz RL, Sackett DL, Bates SE. Histone deacetylase inhibitors and demethylating agents: clinical development of histone deacetylase inhibitors for cancer therapy. Cancer J 2007;13:30-9.
11. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 2009;27:5459-68.
12. Zhang F, Zhang T, Teng ZH, Zhang R, Wang JB, Mei QB. Sensitization to gamma-irradiation-induced cell cycle arrest and apoptosis by the histone deacetylase inhibitor trichostatin A in non-small cell lung cancer (NSCLC) cells. Cancer Biol Ther 2009;8:823-31.
13. Zhang Y, Adachi M, Zhao X, Kawamura R, Imai K. Histone deacetylase inhibitors FK228, N-(2-aminophenyl)-4-[N-(pyridin-3-yl-methoxycarbonyl) amino-methyl]benzamide and m-carboxycinnamic acid bis-hydroxamide augment radiation-induced cell death in gastrointestinal adenocarcinoma cells. Int J Cancer 2004;110: 301-8.
14. Munshi A, Kurland JF, Nishikawa T, Tanaka T, Hobbs ML, Tucker SL, et al. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 2005;11: 4912-22.
15. Chen X, Wong JY, Wong P, Radany EH. Low-dose valproic acid enhances radiosensitivity of prostate cancer through acetylated p53-dependent modulation of mitochondrial membrane potential and apoptosis. Mol Cancer Res 2011;9:448-61.
16. Duvic M, Talpur R, Ni X, Zhang C, Hazarika P, Kelly C, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 2007;109:31-9.
17. Chen L, Wilson D, Jayaram HN, Pankiewicz KW. Dual inhibitors of inosine monophosphate dehydrogenase and histone deacetylases for cancer treatment. J Med Chem 2007;50:6685-91.
18. Adimoolam S, Sirisawad M, Chen J, Thiemann P, Ford JM, Buggy JJ. HDAC inhibitor PCI-24781 decreases RAD51 expression and inhibits homologous recombination. Proc Natl Acad Sci U S A 2007;104: 19482-7.
19. Zhao H, Luoto KR, Meng AX, Bristow RG. The receptor tyrosine kinase inhibitor amuvatinib (MP470) sensitizes tumor cells to radio- and chemo-therapies in part by inhibiting homologous recombination. Radiother Oncol. 2011;101:59-65.
20. Gunn A, Bennardo N, Cheng A, Stark JM. Correct end use during end joining ofmultiple chromosomal double strand breaks is influenced by repair protein RAD50, DNA-dependent protein kinase DNA-PKcs, and transcription context. J Biol Chem 2011;286:42470-82.
21. Li PC, Lam E, Roos WP, Zdzienicka MZ, Kaina B, Efferth T. Artesunate derived from traditional Chinese medicine induces DNA damage and repair. Cancer Res 2008;68:4347-51.
22. Rothkamm K, Kruger I, Thompson LH, Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003;23:5706-15.
23. Fertil B, Dertinger H, Courdi A, Malaise EP. Mean inactivation dose: a useful concept for intercomparison of human cell survival curves. Radiat Res 1984;99:73-84.
24. Lauring J, Abukhdeir AM, Konishi H, Garay JP, Gustin JP, Wang Q, et al. The multiple myeloma associated MMSET gene contributes to cellular adhesion, clonogenic growth, and tumorigenicity. Blood 2008;111:856-64.
25. Gospodinov A, Tsaneva I, Anachkova B. RAD51 foci formation in response to DNA damage is modulated by TIP49. Int J Biochem Cell Biol 2009;41:925-33.
26. Sedelnikova OA, Pilch DR, Redon C, Bonner WM. Histone H2AX in DNA damage and repair. Cancer Biol Ther 2003;2:233-5.
27. Banath JP, Klokov D, MacPhail SH, Banuelos CA, Olive PL. Residual gammaH2AX foci as an indication of lethal DNA lesions. BMC Cancer 2010;10:4.
28. Taneja N, Davis M, Choy JS, Beckett MA, Singh R, Kron SJ, et al. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J Biol Chem 2004;279:2273-80.
29. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000;10:886-95.
30. Kinner A, Wu W, Staudt C, Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008;36:5678-94.
31. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 1997;88:265-75.
32. Yuan SS, Chang HL, Lee EY. Ionizing radiation-induced Rad51 nuclear focus formation is cell cycle-regulated and defective in both ATM(-/-) and c-Abl(-/-) cells. Mutat Res 2003;525:85-92.
33. Pagano M, Pepperkok R, Verde F, Ansorge W, Draetta G. Cyclin A is required at two points in the human cell cycle. EMBO J 1992;11: 961-71.
34. Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 2008;4:e1000110.
35. Allen C, Halbrook J, Nickoloff JA. Interactive competition between homologous recombination and non-homologous end joining. Mol Cancer Res 2003;1:913-20.
36. Mladenov E, Anachkova B, Tsaneva I. Sub-nuclear localization of Rad51 in response to DNA damage. Genes Cells 2006;11:513-24.
37. Bohm L. Inhibition of homologous recombination repair with Pentoxifylline targets G2 cells generated by radiotherapy and induces major enhancements of the toxicity of cisplatin and melphalan given after irradiation. Radiat Oncol 2006;1:12.
38. Quiros S, Roos WP, Kaina B. Rad51 and BRCA2-New molecular targets for sensitizing glioma cells to alkylating anticancer drugs. Plos One 2011;6:e27183.
39. Koprinarova M, Botev P, Russev G. Histone deacetylase inhibitor sodium butyrate enhances cellular radiosensitivity by inhibiting both DNA nonhomologous end joining and homologous recombination. DNA Repair (Amst) 2011;10:970-7.
40. Ward JF. The complexity of DNA damage: relevance to biological consequences. Int J Radiat Biol 1994;66:427-32.
41. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004;432:316-23.
42. Dikomey E, Brammer I, Johansen J, Bentzen SM, Overgaard J. Relationship between DNA double-strand breaks, cell killing, and fibrosis studied in confluent skin fibroblasts derived from breast cancer patients. Int J Radiat Oncol Biol Phys 2000;46:481-90.
43. Borgmann K, Dede M, Wrona A, Brammer I, Overgaard J, Dikomey E. For X-irradiated normal human fibroblasts, only half of cell inactivation results from chromosomal damage. Int J Radiat Oncol Biol Phys 2004;58:445-52.
44. Raderschall E, Stout K, Freier S, Suckow V, Schweiger S, Haaf T. Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res 2002;62:219-25.
45. Choudhury A, Zhao H, Jalali F, Al Rashid S, Ran J, Supiot S, et al. Targeting homologous recombination using imatinib results in enhanced tumor cell chemosensitivity and radiosensitivity. Mol Cancer Ther 2009;8:203-13.
46. Sak A, Stueben G, Groneberg M, Bocker W, Stuschke M. Targeting of Rad51-dependent homologous recombination: implications for the radiation sensitivity of human lung cancer cell lines. Br J Cancer 2005;92:1089-97.
47. Kim PM, Allen C, Wagener BM, Shen Z, Nickoloff JA. Overexpression of human RAD51 and RAD52 reduces double-strand break-induced homologous recombination in mammalian cells. Nucleic Acids Res 2001;29:4352-60.
48. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol 2004;24:9305-16.
49. van Veelen LR, Cervelli T, van de Rakt MW, Theil AF, Essers J, Kanaar R. Analysis of ionizing radiation-induced foci of DNA damage repair proteins. Mutat Res 2005;574:22-33.
50. Wang H, Boecker W, Wang X, Guan J, Thompson LH, Nickoloff JA, et al. Caffeine inhibits homology-directed repair of I-SceI-induced DNA double-strand breaks. Oncogene 2004;23:824-34.
51. Murakawa Y, Sonoda E, Barber LJ, Zeng W, Yokomori K, Kimura H, et al. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res 2007;67: 8536-43.