The therapeutic potential of class I selective histone deacetylase inhibitors in ovarian cancer

Frontiers in Oncology

Volumn 4 MAY, Issue , 2014, Pages

  Khabele, Dineo ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

Epigenetic therapy; Histone deacetylase inhibitors; Histone deacetylases; Ovarian cancer; Targeted therapy

Indexed keywords

BELINOSTAT; BENZAMIDE; CARBOPLATIN; DEPSIPEPTIDE; ENTINOSTAT; GEMCITABINE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; PACLITAXEL; PROTEIN P21; ROMIDEPSIN; VALPROIC ACID; VORINOSTAT;

ANTINEOPLASTIC ACTIVITY; CARCINOGENICITY; DEACETYLATION; DNA DAMAGE; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OVARY CANCER; PERITONEUM CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; T CELL LYMPHOMA; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; UTERINE TUBE DISEASE;

EID: 84904636264     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00111     Document Type: Review

References (100)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin (2014) 64(1):9-29. doi: 10.3322/caac.21208
2. Kurman RJ, Shih Ie M. Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer - shifting the paradigm. Hum Pathol (2011) 42(7):918-31. doi:10.1016/j.humpath.2011.03.003
3. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature (2011) 474(7353):609-15. doi:10.1038/nature10166
4. Alsop K, Fereday S, Meldrum C, Defazio A, Emmanuel C, George J, et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J Clin Oncol (2012) 30(21):2654-63. doi:10.1200/JCO.2011.39.8545
5. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet (2010) 376(9737):245-51. doi:10.1016/S0140-6736(10)60893-8
6. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med (2009) 361(2):123-34. doi:10.1056/NEJMoa0900212
7. Fong PC, Yap TA, Boss DS, Carden CP, Mergui-Roelvink M, Gourley C, et al. Poly(ADP)-ribose polymerase inhibition: frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol (2010) 28(15):2512-9. doi:10.1200/JCO.2009.26.9589
8. Muggia F. Platinum compounds 30 years after the introduction of cisplatin: implications for the treatment of ovarian cancer. Gynecol Oncol (2009) 112(1):275-81. doi:10.1016/j.ygyno.2008.09.034
9. Yap TA, Carden CP, Kaye SB. Beyond chemotherapy: targeted therapies in ovarian cancer. Nat Rev Cancer (2009) 9(3):167-81. doi:10.1038/nrc2583
10. Cannistra SA. Cancer of the ovary. N Engl J Med (2004) 351(24):2519-29. doi:10.1056/NEJMra041842
11. Ozols RF. Update of the NCCN ovarian cancer practice guidelines. Oncology (Williston Park) (1997) 11(11A):95-105.
12. Covens A, Carey M, Bryson P, Verma S, Fung Kee Fung M, Johnston M. Systematic review of first-line chemotherapy for newly diagnosed postoperative patients with stage II, III, or IV epithelial ovarian cancer. Gynecol Oncol (2002) 85(1):71-80. doi:10.1006/gyno.2001.6552
13. Katsumata N, Yasuda M, Isonishi S, Takahashi F, Michimae H, Kimura E, et al. Long-term results of dose-dense paclitaxel and carboplatin versus conventional paclitaxel and carboplatin for treatment of advanced epithelial ovarian, fallopian tube, or primary peritoneal cancer (JGOG 3016): a randomised, controlled, open-label trial. Lancet Oncol (2013) 14(10):1020-6. doi:10.1016/S1470-2045(13)70363-2
14. Armstrong DK, Bundy B, Wenzel L, Huang HQ, Baergen R, Lele S, et al. Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med (2006) 354(1):34-43. doi:10.1056/NEJMoa052985
15. West AC, Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. J Clin Invest (2014) 124(1):30-9. doi:10.1172/JCI69738
16. Frew AJ, Johnstone RW, Bolden JE. Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett (2009) 280(2):125-33. doi:10.1016/j.canlet.2009.02.042
17. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet (2009) 10(1):32-42. doi:10.1038/nrg2485
18. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, Sun ZW, et al. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell (2008) 30(1):61-72. doi:10.1016/j.molcel.2008.02.030
19. Conti C, Leo E, Eichler GS, Sordet O, Martin MM, Fan A, et al. Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res (2010) 70(11):4470-80. doi:10.1158/0008-5472.CAN-09-3028
20. Bhaskara S, Knutson SK, Jiang G, Chandrasekharan MB, Wilson AJ, Zheng S, et al. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell (2010) 18(5):436-47. doi:10.1016/j.ccr.2010.10.022
21. Wilson AJ, Velcich A, Arango D, Kurland AR, Shenoy SM, Pezo RC, et al. Novel detection and differential utilization of a c-myc transcriptional block in colon cancer chemoprevention. Cancer Res (2002) 62(21):6006-10.
22. Kobayashi Y, Ohtsuki M, Murakami T, Kobayashi T, Sutheesophon K, Kitayama H, et al. Histone deacetylase inhibitor FK228 suppresses the Ras-MAP kinase signaling pathway by upregulating Rap1 and induces apoptosis in malignant melanoma. Oncogene (2006) 25(4):512-24.
23. Chang HC, Liu LT, Hung WC. Involvement of histone deacetylation in ras-induced down-regulation of the metastasis suppressor RECK. Cell Signal (2004) 16(6):675-9. doi:10.1016/j.cellsig.2003.11.001
24. Pan L, Lu J, Wang X, Han L, Zhang Y, Han S, et al. Histone deacetylase inhibitor trichostatin a potentiates doxorubicin-induced apoptosis by up-regulating PTEN expression. Cancer (2007) 109(8):1676-88. doi:10.1002/cncr.22585
25. Spange S, Wagner T, Heinzel T, Kramer OH. Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int J Biochem Cell Biol (2009) 41(1):185-98. doi:10.1016/j.biocel.2008.08.027
26. Eot-Houllier G, Fulcrand G, Magnaghi-Jaulin L, Jaulin C. Histone deacetylase inhibitors and genomic instability. Cancer Lett (2009) 274(2):169-76. doi:10.1016/j.canlet.2008.06.005
27. Glozak MA, Sengupta N, Zhang X, Seto E. Acetylation and deacetylation of non-histone proteins. Gene (2005) 363:15-23. doi:10.1016/j.gene.2005.09.010
28. Taunton J, Hassig CA, Schreiber SL. A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science (1996) 272(5260):408-11. doi:10.1126/science.272.5260.408
29. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov (2006) 5(9):769-84. doi:10.1038/nrd2133
30. Guenther MG, Yu J, Kao GD, Yen TJ, Lazar MA. Assembly of the SMRT-histone deacetylase 3 repression complex requires the TCP-1 ring complex. Genes Dev (2002) 16(24):3130-5. doi:10.1101/gad.1037502
31. Guenther MG, Barak O, Lazar MA. The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol (2001) 21(18):6091-101. doi:10.1128/MCB.21.18.6091-6101.2001
32. Yang WM, Tsai SC, Wen YD, Fejer G, Seto E. Functional domains of histone deacetylase-3. J Biol Chem (2002) 277(11):9447-54. doi:10.1074/jbc.M105993200
33. Escaffit F, Vaute O, Chevillard-Briet M, Segui B, Takami Y, Nakayama T, et al. Cleavage and cytoplasmic relocalization of histone deacetylase 3 are important for apoptosis progression. Mol Cell Biol (2007) 27(2):554-67. doi:10.1128/MCB.00869-06
34. Glaser KB, Li J, Staver MJ, Wei RQ, Albert DH, Davidsen SK. Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochem Biophys Res Commun (2003) 310(2):529-36. doi:10.1016/j.bbrc.2003.09.043
35. Wilson AJ, Byun DS, Popova N, Murray LB, L'Italien K, Sowa Y, et al. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem (2006) 281(19):13548-58. doi:10.1074/jbc.M510023200
36. Khabele D, Son DS, Parl AK, Goldberg GL, Augenlicht LH, Mariadason JM, et al. Drug-induced inactivation or gene silencing of class I histone deacetylases suppresses ovarian cancer cell growth: implications for therapy. Cancer Biol Ther (2007) 6(5):795-801. doi:10.4161/cbt.6.5.4007
37. Weichert W, Denkert C, Noske A, Darb-Esfahani S, Dietel M, Kalloger SE, et al. Expression of class I histone deacetylases indicates poor prognosis in endometrioid subtypes of ovarian and endometrial carcinomas. Neoplasia (2008) 10(9):1021-7.
38. Mariadason JM. HDACs and HDAC inhibitors in colon cancer. Epigenetics (2008) 3(1):28-37. doi:10.4161/epi.3.1.5736
39. Marsoni S, Damia G, Camboni G. A work in progress: the clinical development of histone deacetylase inhibitors. Epigenetics (2008) 3(3):164-71. doi:10.4161/epi.3.3.6253
40. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene (2007) 26(37):5541-52. doi:10.1038/sj.onc.1210620
41. Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist (2007) 12(10):1247-52. doi:10.1634/theoncologist.12-10-1247
42. Mann BS, Johnson JR, He K, Sridhara R, Abraham S, Booth BP, et al. Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res (2007) 13(8):2318-22. doi:10.1158/1078-0432.CCR-06-2672
43. Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, et al. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol (2009) 27(32):5410-7. doi:10.1200/JCO.2008.21.6150
44. Piekarz RL, Frye R, Prince HM, Kirschbaum MH, Zain J, Allen SL, et al. Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood (2011) 117(22):5827-34. doi:10.1182/blood-2010-10-312603
45. Dizon DS, Blessing JA, Penson RT, Drake RD, Walker JL, Johnston CM, et al. A phase II evaluation of belinostat and carboplatin in the treatment of recurrent or persistent platinum-resistant ovarian, fallopian tube, or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol (2012) 125(2):367-71. doi:10.1016/j.ygyno.2012.02.019
46. Dizon DS, Damstrup L, Finkler NJ, Lassen U, Celano P, Glasspool R, et al. Phase II activity of belinostat (PXD-101), carboplatin, and paclitaxel in women with previously treated ovarian cancer. Int J Gynecol Cancer (2012) 22(6):979-86. doi:10.1097/IGC.0b013e31825736fd
47. Mendivil AA, Micha JP, Brown JV III, Rettenmaier MA, Abaid LN, Lopez KL, et al. Increased incidence of severe gastrointestinal events with first-line paclitaxel, carboplatin, and vorinostat chemotherapy for advanced-stage epithelial ovarian, primary peritoneal, and fallopian tube cancer. Int J Gynecol Cancer (2013) 23(3):533-9. doi:10.1097/IGC.0b013e31828566f1
48. Modesitt SC, Sill M, Hoffman JS, Bender DP. A phase II study of vorinostat in the treatment of persistent or recurrent epithelial ovarian or primary peritoneal carcinoma: a Gynecologic Oncology Group study. Gynecol Oncol (2008) 109(2):182-6. doi:10.1016/j.ygyno.2008.01.009
49. Bradner JE, West N, Grachan ML, Greenberg EF, Haggarty SJ, Warnow T, et al. Chemical phylogenetics of histone deacetylases. Nat Chem Biol (2010) 6(3):238-43. doi:10.1038/nchembio.313
50. Wilson AJ, Holson E, Wagner F, Zhang YL, Fass DM, Haggarty SJ, et al. The DNA damage mark pH2AX differentiates the cytotoxic effects of small molecule HDAC inhibitors in ovarian cancer cells. Cancer Biol Ther (2011) 12(6):484-93. doi:10.4161/cbt.12.6.15956
51. Furumai R, Matsuyama A, Kobashi N, Lee KH, Nishiyama M, Nakajima H, et al. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res (2002) 62(17):4916-21.
52. Wang C, Henkes LM, Doughty LB, He M, Wang D, Meyer-Almes FJ, et al. Thailandepsins: bacterial products with potent histone deacetylase inhibitory activities and broad-spectrum antiproliferative activities. J Nat Prod (2011) 74(10):2031-8. doi:10.1021/np200324x
53. Wilson AJ, Cheng YQ, Khabele D. Thailandepsins are new small molecule class I HDAC inhibitors with potent cytotoxic activity in ovarian cancer cells: a preclinical study of epigenetic ovarian cancer therapy. J Ovarian Res (2012) 5(1):12. doi:10.1186/1757-2215-5-12
54. Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol (2004) 338(1):17-31. doi:10.1016/j.jmb.2004.02.006
55. 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(9):970-7. doi:10.1016/j.dnarep.2011.07.003
56. 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(49):19482-7. doi:10.1073/pnas.0707828104
57. Ladd B, Ackroyd JJ, Hicks JK, Canman CE, Flanagan SA, Shewach DS. Inhibition of homologous recombination with vorinostat synergistically enhances ganciclovir cytotoxicity. DNA Repair (Amst) (2013) 12(12):1114-21. doi:10.1016/j.dnarep.2013.10.008
58. Konstantinopoulos PA, Wilson AJ, Saskowski J, Wass E, Khabele D. Suberoylanilide hydroxamic acid (SAHA) enhances olaparib activity by targeting homologous recombination DNA repair in ovarian cancer. Gynecol Oncol (2014). doi:10.1016/j.ygyno.2014.03.007
59. Mackay HJ, Hirte H, Colgan T, Covens A, MacAlpine K, Grenci P, et al. Phase II trial of the histone deacetylase inhibitor belinostat in women with platinum resistant epithelial ovarian cancer and micropapillary (LMP) ovarian tumours. Eur J Cancer (2010) 46(9):1573-9. doi:10.1016/j.ejca.2010.02.047
60. Son DS, Wilson AJ, Parl AK, Khabele D. The effects of the histone deacetylase inhibitor romidepsin (FK228) are enhanced by aspirin (ASA) in COX-1 positive ovarian cancer cells through augmentation of p21. Cancer Biol Ther (2010) 9(11):928-35. doi:10.4161/cbt.9.11.11873
61. Batty N, Malouf GG, Issa JP. Histone deacetylase inhibitors as anti-neoplastic agents. Cancer Lett (2009) 280(2):192-200. doi:10.1016/j.canlet.2009.03.013
62. Kim IA, No M, Lee JM, Shin JH, Oh JS, Choi EJ, et al. Epigenetic modulation of radiation response in human cancer cells with activated EGFR or HER-2 signaling: potential role of histone deacetylase 6. Radiother Oncol (2009) 92(1):125-32. doi:10.1016/j.radonc.2009.03.008
63. 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) 8:9. doi:10.4161/cbt.8.9.8143
64. Cuneo KC, Fu A, Osusky K, Huamani J, Hallahan DE, Geng L. Histone deacetylase inhibitor NVP-LAQ824 sensitizes human nonsmall cell lung cancer to the cytotoxic effects of ionizing radiation. Anticancer Drugs (2007) 18(7):793-800. doi:10.1097/CAD.0b013e3280b10d57
65. Geng L, Cuneo KC, Fu A, Tu T, Atadja PW, Hallahan DE. Histone deacetylase (HDAC) inhibitor LBH589 increases duration of gamma-H2AX foci and confines HDAC4 to the cytoplasm in irradiated non-small cell lung cancer. Cancer Res (2006) 66(23):11298-304. doi:10.1158/0008-5472.CAN-06-0049
66. Marchion DC, Bicaku E, Turner JG, Schmitt ML, Morelli DR, Munster PN. HDAC2 regulates chromatin plasticity and enhances DNA vulnerability. Mol Cancer Ther (2009) 8(4):794-801. doi:10.1158/1535-7163.MCT-08-0985
67. Ozaki K, Kishikawa F, Tanaka M, Sakamoto T, Tanimura S, Kohno M. Histone deacetylase inhibitors enhance the chemosensitivity of tumor cells with cross-resistance to a wide range of DNA-damaging drugs. Cancer Sci (2008) 99(2):376-84. doi:10.1111/j.1349-7006.2007.00669.x
68. Kim DH, Kim M, Kwon HJ. Histone deacetylase in carcinogenesis and its inhibitors as anti-cancer agents. J Biochem Mol Biol (2003) 36(1):110-9. doi:10.5483/BMBRep.2003.36.1.110
69. Wang D, Lippard SJ. Cisplatin-induced post-translational modification of histones H3 and H4. J Biol Chem (2004) 279(20):20622-5. doi:10.1074/jbc.M402547200
70. Cohen SM, Lippard SJ. Cisplatin: from DNA damage to cancer chemotherapy. Prog Nucleic Acid Res Mol Biol (2001) 67:93-130. doi:10.1016/S0079-6603(01)67026-0
71. Steele N, Finn P, Brown R, Plumb JA. Combined inhibition of DNA methylation and histone acetylation enhances gene re-expression and drug sensitivity in vivo. Br J Cancer (2009) 100(5):758-63. doi:10.1038/sj.bjc.6604932
72. Knutson SK, Chyla BJ, Amann JM, Bhaskara S, Huppert SS, Hiebert SW. Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J (2008) 27(7):1017-28. doi:10.1038/emboj.2008.51
73. Wilson AJ, Lalani AS, Wass E, Saskowski J, Khabele D. Romidepsin (FK228) combined with cisplatin stimulates DNA damage-induced cell death in ovarian cancer. Gynecol Oncol (2012) 127(3):579-86. doi:10.1016/j.ygyno.2012.09.016
74. Wilson AJ, Byun DS, Nasser S, Murray LB, Ayyanar K, Arango D, et al. HDAC4 promotes growth of colon cancer cells via repression of p21. Mol Biol Cell (2008) 19(10):4062-75. doi:10.1091/mbc.E08-02-0139
75. Huang W, Tan D, Wang X, Han S, Tan J, Zhao Y, et al. Histone deacetylase 3 represses p15(INK4b) and p21(WAF1/cip1) transcription by interacting with Sp1. Biochem Biophys Res Commun (2006) 339(1):165-71. doi:10.1016/j.bbrc.2005.11.010
76. Gelmetti V, Zhang J, Fanelli M, Minucci S, Pelicci PG, Lazar MA. Aberrant recruitment of the nuclear receptor corepressor-histone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol Cell Biol (1998) 18(12):7185-91.
77. Grignani F, De Matteis S, Nervi C, Tomassoni L, Gelmetti V, Cioce M, et al. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature (1998) 391(6669):815-8. doi:10.1038/35901
78. Atsumi A, Tomita A, Kiyoi H, Naoe T. Histone deacetylase 3 (HDAC3) is recruited to target promoters by PML-RARalpha as a component of the N-CoR co-repressor complex to repress transcription in vivo. Biochem Biophys Res Commun (2006) 345(4):1471-80. doi:10.1016/j.bbrc.2006.05.047
79. Summers AR, Fischer MA, Stengel KR, Zhao Y, Kaiser JF, Wells CE, et al. HDAC3 is essential for DNA replication in hematopoietic progenitor cells. J Clin Invest (2013) 123(7):3112-23. doi:10.1172/JCI60806
80. Wells CE, Bhaskara S, Stengel KR, Zhao Y, Sirbu B, Chagot B, et al. Inhibition of histone deacetylase 3 causes replication stress in cutaneous T cell lymphoma. PLoS One (2013) 8(7):e68915. doi:10.1371/journal.pone.0068915
81. Bolden JE, Shi W, Jankowski K, Kan CY, Cluse L, Martin BP, et al. HDAC inhibitors induce tumor-cell-selective pro-apoptotic transcriptional responses. Cell Death Dis (2013) 4:e519. doi:10.1038/cddis.2013.9
82. Alvero AB, Montagna MK, Craveiro V, Liu L, Mor G. Distinct subpopulations of epithelial ovarian cancer cells can differentially induce macrophages and T regulatory cells toward a pro-tumor phenotype. Am J Reprod Immunol (2012) 67(3):256-65. doi:10.1111/j.1600-0897.2011.01068.x
83. Krempski J, Karyampudi L, Behrens MD, Erskine CL, Hartmann L, Dong H, et al. Tumor-infiltrating programmed death receptor-1+ dendritic cells mediate immune suppression in ovarian cancer. J Immunol (2011) 186(12):6905-13. doi:10.4049/jimmunol.1100274
84. Hagemann T, Lawrence T, McNeish I, Charles KA, Kulbe H, Thompson RG, et al. "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J Exp Med (2008) 205(6):1261-8. doi:10.1084/jem.20080108
85. Hagemann T, Robinson SC, Thompson RG, Charles K, Kulbe H, Balkwill FR. Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol Cancer Ther (2007) 6(7):1993-2002. doi:10.1158/1535-7163.MCT-07-0118
86. Robinson-Smith TM, Isaacsohn I, Mercer CA, Zhou M, Van Rooijen N, Husseinzadeh N, et al. Macrophages mediate inflammation-enhanced metastasis of ovarian tumors in mice. Cancer Res (2007) 67(12):5708-16. doi:10.1158/0008-5472.CAN-06-4375
87. Coussens LM, Zitvogel L, Palucka AK. Neutralizing tumor-promoting chronic inflammation: a magic bullet? Science (2013) 339(6117):286-91. doi:10.1126/science.1232227
88. Hagemann T, Wilson J, Kulbe H, Li NF, Leinster DA, Charles K, et al. Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK. J Immunol (2005) 175(2):1197-205. doi:10.4049/jimmunol.175.2.1197
89. Kulbe H, Chakravarty P, Leinster DA, Charles KA, Kwong J, Thompson RG, et al. A dynamic inflammatory cytokine network in the human ovarian cancer microenvironment. Cancer Res (2012) 72(1):66-75. doi:10.1158/0008-5472.CAN-11-2178
90. Hagemann T, Wilson J, Burke F, Kulbe H, Li NF, Pluddemann A, et al. Ovarian cancer cells polarize macrophages toward a tumor-associated phenotype. J Immunol (2006) 176(8):5023-32. doi:10.4049/jimmunol.176.8.5023
91. Mullican SE, Gaddis CA, Alenghat T, Nair MG, Giacomin PR, Everett LJ, et al. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev (2011) 25(23):2480-8. doi:10.1101/gad.175950.111
92. Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J, et al. Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci U S A (2012) 109(42):E2865-74. doi:10.1073/pnas.1121131109
93. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science (2001) 293(5535):1653-7. doi:10.1126/science.1062374
94. Ziesche E, Kettner-Buhrow D, Weber A, Wittwer T, Jurida L, Soelch J, et al. The coactivator role of histone deacetylase 3 in IL-1-signaling involves deacetylation of p65 NF-kappaB. Nucleic Acids Res (2013) 41(1):90-109. doi:10.1093/nar/gks916
95. Yan Q, Carmody RJ, Qu Z, Ruan Q, Jager J, Mullican SE, et al. Nuclear factor-kappaB binding motifs specify toll-like receptor-induced gene repression through an inducible repressosome. Proc Natl Acad Sci U S A (2012) 109(35):14140-5. doi:10.1073/pnas.1119842109
96. Delcuve GP, Khan DH, Davie JR. Targeting class I histone deacetylases in cancer therapy. Expert Opin Ther Targets (2013) 17(1):29-41. doi:10.1517/14728222.2013.729042
97. Li Y, Liu T, Ivan C, Huang J, Shen DY, Kavanagh JJ, et al. Enhanced cytotoxic effects of combined valproic acid and the aurora kinase inhibitor VE465 on gynecologic cancer cells. Front Oncol (2013) 3:58. doi:10.3389/fonc.2013.00058
98. Needham LA, Davidson AH, Bawden LJ, Belfield A, Bone EA, Brotherton DH, et al. Drug targeting to monocytes and macrophages using esterase-sensitive chemical motifs. J Pharmacol Exp Ther (2011) 339(1):132-42. doi:10.1124/jpet.111.183640
99. Santoro F, Botrugno OA, Dal Zuffo R, Pallavicini I, Matthews GM, Cluse L, et al. A dual role for Hdac1: oncosuppressor in tumorigenesis, oncogene in tumor maintenance. Blood (2013) 121(17):3459-68. doi:10.1182/blood-2012-10-461988
100. Heideman MR, Wilting RH, Yanover E, Velds A, de Jong J, Kerkhoven RM, et al. Dosage-dependent tumor suppression by histone deacetylases 1 and 2 through regulation of c-Myc collaborating genes and p53 function. Blood (2013) 121(11):2038-50. doi:10.1182/blood-2012-08-450916