Vorinostat inhibits brain metastatic colonization in a model of triple-negative breast cancer and induces DNA double-strand breaks

Clinical Cancer Research

Volumn 15, Issue 19, 2009, Pages 6148-6157

  Palmieri, Diane ^a,e   Lockman, Paul R ^b   Thomas, Fancy C ^b   Hua, Emily ^a   Herring, Jeanne ^c   Hargrave, Elizabeth ^a   Johnson, Matthew ^a   Flores, Natasha ^a   Qian, Yongzhen ^c   Vega Valle, Eleazar ^c   Taskar, Kunal S ^b   Rudraraju, Vinay ^b   Mittapalli, Rajendar K ^b   Gaasch, Julie A ^b   Bohn, Kaci A ^b   Thorsheim, Helen R ^b   Liewehr, David J ^a   Davis, Sean ^a   Reilly, John F ^d   Walker, Robert ^a   Bronder, Julie L ^a   Feigenbaum, Lionel ^c   Steinberg, Seth M ^a   Camphausen, Kevin ^a   Meltzer, Paul S ^a   Richon, Victoria M ^d   Smith, Quentin R ^b   Steeg, Patricia S ^a   more..

^a NATIONAL CANCER INSTITUTE   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

^e NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H4; RAD52 PROTEIN; VORINOSTAT;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BRAIN METASTASIS; BREAST CANCER; CANCER MODEL; CANCER SIZE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG MECHANISM; DRUG PENETRATION; DRUG UPTAKE; FEMALE; GENE EXPRESSION REGULATION; MICROMETASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; BREAST NEOPLASMS; CARCINOMA; DNA BREAKS, DOUBLE-STRANDED; ENZYME INHIBITORS; FEMALE; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; MICE; MICE, INBRED BALB C; MICE, NUDE; RATS; RATS, SPRAGUE-DAWLEY; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 70349671463     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-09-1039     Document Type: Article

References (38)

1. Lin N, Bellon J, Winer E. CNS metastases in breast cancer. J Clin Oncol 2004;22:3608-3617
2. Weil R, Palmieri D, Bronder J, Stark A, Steeg P. Breast cancer metastasis to the central nervous system. Am J Pathol 2005;167:913-920 (Pubitemid 41416243)
3. Bart J, Groen H, Hendrikse N, van der Graaf W, Vaalburg W, deVries E. The blood-brain barrier and oncology: new insights into function and modulation. Cancer Treat Rev 2000;26:449-462
4. Kniesel U, Wolburg H. Tight junctions of the blood-brain barrier. Cell Mol Neurobiol 1997;20: 57-76.
5. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res 2007;13:1663-1674 (Pubitemid 46952931)
6. Mahar Doan KM, Humphreys JE, Webster LO, et al. Passive permeability and P-glycoprotein- mediated efflux differentiate central nervous system (CNS) and non-CNS marketed drugs. J Pharmacol Exp Ther 2002;303: 1029-1037
7. Fidler I, Yano S, Zhang R, Fujimaki T, Bucana C. The seed and soil hypothesis: vascularisation and brain metastases. Lancet Oncol 2002; 3:53-57 (Pubitemid 34121146)
8. Palmieri D, Bronder JL, Herring JM, et al. Her-2 overexpression increases the metastatic outgrowth of breast cancer cells in the brain. Cancer Res 2007;67:4190-4198 (Pubitemid 46815065)
9. WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci U S A 2000;97:10014-10019
10. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007;26:5541-5552 (Pubitemid 47255934)
11. Richon V. Cancer biology: mechanism of antitumour action of vorinostat (suberoylanilide hydroxamic acid), a novel histone deacetylase inhibitor. Br J Cancer 2006;95: S2-6. (Pubitemid 44950782)
12. Eyupoglu IY, Hahnen E, Buslei R, et al. Suberoylanilide hydroxamic acid (SAHA) has potent anti-glioma properties in vitro, ex vivo and in vivo. J Neurochem 2005;93:992-999 (Pubitemid 40695758)
13. Yin D, Ong JM, Hu J, et al. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 2007; 13:1045-1052 (Pubitemid 46340384)
14. Cooper AL, Greenberg VL, Lancaster PS, van Nagell JR, Jr., Zimmer SG, Modesitt SC. In vitro and in vivo histone deacetylase inhibitor therapy with suberoylanilide hydroxamic acid (SAHA) and paclitaxel in ovarian cancer. Gynecol Oncol 2007;104:596-601.
15. Ugur HC, Ramakrishna N, Bello L, et al. Continuous intracranial administration of suberoylanilide hydroxamic acid (SAHA) inhibits tumor growth in an orthotopic glioma model. J Neurooncol 2007;83:267-275 (Pubitemid 46952237)
16. Mandula H, Parepally JM, Feng R, Smith QR. Role of site-specific binding to plasma albumin in drug availability to brain. J Pharmacol Exp Ther 2006;317:667-675
17. Parepally JM, Mandula H, Smith QR. Brain uptake of nonsteroidal anti-inflammatory drugs: ibuprofen, flurbiprofen, and indomethacin. Pharm Res 2006;23:873-881 (Pubitemid 43781395)
18. Konca K, Lankoff A, Banasik A, et al. A crossplatform public domain PC image-analysis program for the comet assay. Mutat Res 2003;534: 15-20. (Pubitemid 36015835)
19. Gril B, Palmieri D, Bronder JL, et al. Effect of lapatinibon the outgrowth of metastatic breast cancer cells to the brain. J Natl Cancer Inst 2008;100:1092-1103
20. Szuts D, Christov C, Kitching L, Krude T. Distinct populations of human PCNA are required for initiation of chromosomal DNA replication and concurrent DNA repair. Exp Cell Res 2005; 311:240-250 (Pubitemid 41636317)
21. Sedelnikova OA, Pilch DR, Redon C, Bonner WM. Histone H2AX in DNA damage and repair. Cancer Biol Ther 2003;2:233-235
22. Sung P. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J Biol Chem 1997;272: 28194-28197 (Pubitemid 27517755)
23. Bereczki D, Wei L, Acuff V, et al. Techniquedependent variations in cerebral microvessel blood volumes and hematocrits in the rat. J Appl Physiol 1992;73:918-924
24. Cisternino S, Rousselle C, Dagenais C, Scherrmann JM. Screening ofmultidrug-resistance sensitive drugs by in situ brain perfusion in Pglycoprotein- deficient mice. Pharm Res 2001; 18:183-190 (Pubitemid 32592598)
25. Hockly E, Richon V, Woodman B, et al. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington's disease. Proc Natl Acad Sci U S A 2003;100: 2041-2046 (Pubitemid 36254570)
26. Pajouhesh H, Lenz GR. Medicinal chemical properties of successful central nervous system drugs. NeuroRx 2005;2:541-553 (Pubitemid 41393264)
27. Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15: 220-231
28. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-239
29. Marchion D, Bicaku E, Daud A, Richon V, Sullivan D, Munster P. Sequence-specific potentiation of topoisomerase II inhibitors by the histone deacetylase inhibitor suberoylanilide hydroxamic acid. 2004;92:223-237
30. Munshi A, Tanaka T, Hobbs ML, Tucker SL, Richon VM, Meyn RE. Vorinostat, a histone deacetylase inhibitor, enhances the response of human tumor cells to ionizing radiation through prolongation of γ-H2AX foci. Mol Cancer Ther 2006;5:1967-1974 (Pubitemid 44336568)
31. Chinnaiyan P, Vallabhaneni G, Armstrong E, Huang SM, Harari PM. Modulation of radiation response by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 2005; 62:223-229 (Pubitemid 40591946)
32. New JH, Sugiyama T, Zaitseva E, Kowalczykowski SC. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 1998;391:407-410 (Pubitemid 28093518)
33. Song B, Sung P. Functional interactions among yeast Rad51 recombinase, Rad52 mediator, and replication protein A in DNA strand exchange. J Biol Chem 2000;275: 15895-15904 (Pubitemid 30366891)
34. Gaymes TJ, Padua RA, Pla M, et al. Histone deacetylase inhibitors (HDI) cause DNA damage in leukemia cells: a mechanism for leukemiaspecific HDI-dependent apoptosis. Mol Cancer Res 2006;4:563-573 (Pubitemid 44341366)
35. Luu TH, Morgan RJ, Leong L, et al. A phase II trial of vorinostat (suberoylanilide hydroxamic acid) in metastatic breast cancer: a California Cancer Consortium study. Clin Cancer Res 2008;14:7138-7142
36. Cameron D, Casey M, Press M, et al. A phase III randomized comparison of lapatinibplus capecitabine versus capecitabine alone in women with advanced breast cancer that has progressed on trastuzumab: updated efficacy and biomarker analyses. Breast Cancer Res Treat 2008;112: 533-543
37. Khalili P, Arakelian A, Chen G, Singh G, Rabbani SA. Effect of Herceptin on the development and progression of skeletal metastases in a xenograft model of human breast cancer. Oncogene 2005;24:6657-6666 (Pubitemid 41486796)
38. Baschnagel A, Russo A, Burgan WE, et al. Vorinostat enhances the radiosensitivity of a breast cancer brain metastatic cell line grown in vitro and as intracranial xenografts. Mol Cancer Ther 2009;8:1589-1595