Targeting histone deacetylase in thyroid cancer

Expert Opinion on Therapeutic Targets

Volumn 17, Issue 2, 2013, Pages 179-193

  Russo, Diego ^a   Durante, Cosimo ^b   Bulotta, Stefania ^a   Puppin, Cinzia ^c   Puxeddu, Efisio ^d   Filetti, Sebastiano ^b   Damante, Giuseppe ^c  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF UDINE   (Italy)

^d UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Epigenetics; Histone acetylation; Histone deacetylase inhibitors; Thyroid cancer

Indexed keywords

ABEXINOSTAT; BELINOSTAT; BUTYRIC ACID; DACINOSTAT; ENTINOSTAT; GIVINOSTAT; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; MOCETINOSTAT; PANOBINOSTAT; PIVALOYLOXYMETHYL BUTYRATE; ROMIDEPSIN; TRICHOSTATIN A; TUBACIN; VALPROIC ACID; VORINOSTAT;

CANCER CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; NONHUMAN; REVIEW; THYROID CANCER; TUMOR GROWTH;

ACETYLATION; ANIMALS; ANTINEOPLASTIC AGENTS; EPIGENESIS, GENETIC; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; HUMANS; THYROID NEOPLASMS;

EID: 84872250456     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2013.740013     Document Type: Review

References (106)

1. SEER Stat Fact Sheets: Thyroid. Available from: http://seer.cancer.gov/ statfacts/html/thyro.html [Last accessed 19 July 2012]
2. Eheman C, Henley SJ Ballard-Barbash R, et al. Annual Report to the Nation on the status of cancer 1975-2008, featuring cancers associated with excess weight and lack of sufficient physical activity. Cancer 2012;118:2338-66
3. Hall SF, Walker H, Siemens R, et al. Increasing detection and increasing incidence in thyroid cancer. World J Surg 2009;33:2567-71
4. Enewold L, Zhu K, Ron E, et al. Rising thyroid cancer incidence in the United States by demographic and tumor characteristics, 1980-2005. Cancer Epidemiol Biomarkers Prev 2009;18:784-91
5. Cooper DS, Doherty GM, Haugen BR et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009;19:1167-214
6. Durante C, Haddy N, Baudin E, et al. Long-term outcome of 444 patients with distant metastases from papillary and follicular thyroid carcinoma: Benefits and limits of radioiodine therapy. J Clin Endocrinol Metab 2006;91:2892-9 (Pubitemid 44271732)
7. Schlumberger M, Lacroix L, Russo D et al. Defects in iodide metabolism in thyroid cancer and implications for the follow-up and treatment of patients. Nat Clin Pract Endocrinol Metab 2007;3:260-9
8. Arturi F, Russo D, Giuffrida D, et al. Sodium-Iodide symporter (NIS) gene expression in lymph node metastases of papillary thyroid carcinomas. Eur J Endocrinol 2000;143:623-7
9. Schlumberger M, Sherman SI. Approach to the patient with advanced differentiated thyroid cancer. Eur J Endocrinol 2012;166:5-11
10. Ellis LM, Hicklin DJ. Resistance to targeted therapies: Refining anticancer therapy in the era of molecular oncology. Clin Cancer Res 2009;15:7471-8
11. Pasquali D, Santoro A, Bufo P, et al. Upregulation of endocrine gland-derived vascular endothelial growth factor in papillary thyroid cancers displaying infiltrative patterns, lymph node metastases, and BRAF mutation. Thyroid 2011;21:391-9
12. Russo D, Damante G, Puxeddu E, et al. Epigenetics of thyroid cancer and novel therapeutic targets. J Mol Endocrinol 2011;46:R73-81
13. Kouzarides T. Chromatin modifications and their function. Cell 2007;128:693-705 (Pubitemid 46273577)
14. Chi P, Allis CD, Wang GG. Covalent histone modifications-miswritten misinterpreted and mis-erased in human cancers. Nat Rev Cancer 2010;10:457-9
15. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007;447(7143):407-12 (Pubitemid 46816746)
16. Yang XJ. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res 2004;32:959-76
17. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 2008;269:7-17
18. Glozak MA, Sengupta N, Zhang X Seto E. Acetylation and deacetylation of non-histone proteins. Gene 2005;363:15-23 (Pubitemid 41691888)
19. Turner BM. Histone acetylation and an epigenetic code. Bioassays 2000;22:836-45
20. Spiegel S, Milstien S, Grant S. Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene 2012;31(5):537-51
21. Rajendran P, Williams DE, Ho E Dashwood RH. Metabolism as a key to histone deacetylase inhibition. Crit Rev Biochem Mol Biol 2011;46(3):181-99
22. McKenna NJ, Xu J, Nawaz Z, et al. Nuclear receptor coactivators: multiple enzymes, multiple complexes, multiple functions. J Steroid Biochem Mol Biol 1999;69(1-6):3-12 (Pubitemid 29305520)
23. Wu Y, Koenig RJ. Gene regulation by thyroid hormone. Trends Endocrinol Metab 2000;11(6):207-11 (Pubitemid 30603165)
24. Miremadi A, Oestergaard MZ Pharoah PD, Caldas C. Cancer genetics of epigenetic genes. Hum Mol Genet 2007;16(Spec No 1):R28-49 (Pubitemid 47241841)
25. Ozdag H, Teschendorff AE, Ahmed AA et al. Differential expression of selected histone modifier genes in human solid cancers. BMC Genomics 2006;7:90
26. Seligson DB, Horvath S, Shi T, et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 2005;435:1262-6 (Pubitemid 40943093)
27. Mosashvilli D, Kahl P, Mertens C, et al. Global histone acetylation levels: Prognostic relevance in patients with renal cell carcinoma. Cancer Sci 2010;101:2664-9
28. Manzo F, Tambaro FP, Mai A Altucci L. Histone acetyltransferase inhibitors and preclinical studies. Exp Opin Ther Pat 2009;19(6):761-74
29. Dickinson M, Johnstone RW Prince HM. Histone deacetylase inhibitors: Potential targets responsible for their anti-cancer effect. Invest New Drugs 2010;28(Suppl 1):S3-20
30. Santo L, Hideshima T, Kung AL, et al. Preclinical activity, pharmacodynamic and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215 in combination with bortezomib in multiple myeloma. Blood 2012;119(11):2579-89
31. Hubbert C, Guardiola A, Shao R, et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002;417:455-8 (Pubitemid 34563539)
32. Li G, Jiang H, Chang M, et al. HDAC6 alpha-tubulin deacetylase: A potential therapeutic target in neurodegenerative diseases. J Neurol Sci 2011;304(1-2):1-8
33. Aldana-Masangkay GI, Sakamoto KM. The role of HDAC6 in cancer. J Biomed Biotechnol 2011;2011:875824
34. www.clinicaltrials.gov 37. Wong ST. Emerging treatment combinations: integrating therapy into clinical practice. Am J Health Syst Pharm 2009;66(23 Suppl 6):S9-S14
35. Jagannath S, Dimopoulos MA, Lonial S. Combined proteasome and histone deacetylase inhibition: A promising synergy for patients with relapsed/refractory multiple myeloma. Leuk Res 2010;34:1111-18
36. Prince HM, Bishton MJ, Harrison SJ. Clinical studies of histone deacetylase inhibitors. Clin Cancer Res 2009;15:3958-69
37. Dovey OM, Foster CT, Cowley SM. Emphasizing the positive: A role for histone deacetylases in transcriptional activation. Cell Cycle 2010;9:2700-1
38. Shen F, Kirmani KZ, Xiao Z, et al. Nuclear protein isoforms: implications for cancer diagnosis and therapy. J Cell Biochem 2011;112:756-60
39. Gunderson FQ, Johnson TL. Acetylation by the transcriptional coactivator Gcn5 plays a novel role in co-transcriptional spliceosome assembly. PLoS Genet 2009;5:e1000682
40. Scroggins BT, Robzyk K, Wang D, et al. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 2007;25:151-9 (Pubitemid 46049066)
41. Yang MH, Nickerson S, Kim ET, et al. Regulation of RAS oncogenicity by acetylation. Proc Natl Acad Sci USA 2012;109(27):10843-8
42. Nakata S, Yoshida T, Horinaka M, et al. Histone deacetylase inhibitors upregulate death receptor 5/TRAIL-R2 and sensitize apoptosis induced by TRAIL/APO2-L in human malignant tumor cells. Oncogene 2004;23:6261-71 (Pubitemid 39215296)
43. Nebbioso A, Clarke N, Voltz E, et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat Med 2005;11:77-84 (Pubitemid 40215841)
44. Zhang XD, Gillespie SK, Borrow JM Hersey P. The histone deacetylase inhibitor suberic bishydroxamate regulates the expression of multiple apoptotic mediators and induces mitochondria-dependent apoptosis of melanoma cells. Mol Cancer Ther 2004;3:425-35 (Pubitemid 39193720)
45. Ocker M, Schneider-Stock R. Histone deacetylase inhibitors: Signalling towards p21cip1/waf1. Int J Biochem Cell Biol 2007;39:1367-74 (Pubitemid 47031035)
46. Sandor V, Senderowicz A, Mertins S et al. P21-dependent g(1)arrest with downregulation of cyclin D1 and upregulation of cyclin E by the histone deacetylase inhibitor FR901228. Br J Cancer 2000;83:817-25
47. Yu X, Guo ZS, Marcu MG, et al. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J Natl Cancer Inst 2002;94:504-13 (Pubitemid 34411289)
48. Oh ET, Park MT, Choi BH, et al. Novel histone deacetylase inhibitor CG200745 induces clonogenic cell death by modulating acetylation of p53 in cancer cells. Invest New Drugs 2012;30:435-42
49. Groenendyk J, Sreenivasaiah PK Kim do H, et al. Biology of endoplasmic reticulum stress in the heart. Circ Res 2010;107:1185-97
50. Kawaguchi Y, Kovacs JJ, McLaurin A et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003;115:727-38 (Pubitemid 38030301)
51. Hideshima T, Bradner JE, Wong J, et al. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc Natl Acad Sci USA 2005;102:8567-72 (Pubitemid 40862776)
52. Rosato RR, Almenara JA, Grant S. The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1. Cancer Res 2003;63:3637-45 (Pubitemid 36793047)
53. Robert T, Vanoli F, Chiolo I, et al. HDACs link the DNA damage response processing of double-strand breaks and autophagy. Nature 2011;471:74-9
54. Kramer OH, Baus D, Knauer SK, et al. Acetylation of Stat1 modulates NF-kappaB activity. Genes Dev 2006;20:473-85 (Pubitemid 43244401)
55. Brest P, Lassalle S, Hofman V, et al. MiR-129-5p is required for histone deacetylase inhibitor-induced cell death in thyroid cancer cells. Endocr Rel Cancer 2011;18:711-19
56. Barneda-Zahonero B, Parra M. Histone deacetylases and cancer. Mol Oncol 2012; Epub ahead of print
57. Johnstone RV. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 2002;1:287-9
58. Kondo T, Asa SL, Ezzat S. Epigenetic dysregulation in thyroid neoplasia. Endocrinol Metab Clin North Am 2008;37:389-400 (Pubitemid 351698083)
59. Schweppe RE, Klopper JP, Korch C et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 2008;93:4331-41 (Pubitemid 352789529)
60. Yuan GB, Kuang AR, Fan Q, et al. Combined effects of all-trans-retinoic acid and trichostatin A on the induction of differentiation of thyroid carcinoma cells. Chin J Cancer 2010;29:379-84
61. Kitazono M, Bates S, Fok P, et al. The histone deacetylase inhibitor FR901228 (depsipeptide) restores expression and function of pseudo-null p53. Cancer Biol Ther 2002;1:665-8
62. Copland JA, Marlow LA, Williams SF et al. Molecular diagnosis of a BRAF papillary thyroid carcinoma with multiple chromosome abnormalities and rare adrenal and hypothalamic metastases. Thyroid 2006;16:1293-302 (Pubitemid 46080173)
63. Imanishi R, Ohtsuru A, Iwamatsu M et al. A histone deacetylase inhibitor enhances killing of undifferentiated thyroid carcinoma cells by p53 gene therapy. J Clin Endocrinol Metab 2002;87(10):4821-4 (Pubitemid 35247082)
64. Marlow LA, Reynolds LA, Cleland AS et al. Reactivation of suppressed RhoB is a critical step for the inhibition of anaplastic thyroid cancer growth. Cancer Res 2009;69:1536-44
65. Mitsiades CS, Poulaki V, McMullan C et al. Novel histone deacetylase inhibitors in the treatment of thyroid cancer. Clin Cancer Res 2005;11:3958-65 (Pubitemid 40685618)
66. Clinckspoor I, Verlinden L Overbergh L, et al. 1,25-dihydroxyvitamin D3 and a superagonistic analog in combination with paclitaxel or suberoylanilide hydroxamic acid have potent antiproliferative effects on anaplastic thyroid cancer. J Steroid Biochem Mol Biol 2011;124:1-9
67. Luong MT, O'Kelly J, Braunstein GD et al. Antitumor activity of suberoylanilide hydroxamic acid against thyroid cancer cell lines in vitro and in vivo. Clin Cancer Res 2006;12(18):5570-7 (Pubitemid 44497275)
68. Borbone E, Berlingieri MT, De Bellis F et al. Histone deacetylase inhibitors induce thyroid cancer-specific apoptosis through proteasome-dependent inhibition of TRAIL degradation. Oncogene 2010;29:105-16
69. Kelly WK, O'Connor OA, Krug LM et al. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J Clin Oncol 2005;23:3923-31 (Pubitemid 46218695)
70. Woyach JA, Kloos RT, Ringel MD et al. Lack of therapeutic effect of the histone deacetylase inhibitor vorinostat in patients with metastatic radioiodine-refractory thyroid carcinoma. J Clin Endocrinol Metab 2009;94:164-70
71. Gottlicher M, Minucci S, Zhu P, et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001;20(24):6969-78 (Pubitemid 34062289)
72. Xiao X, Ning L, Chen H. Notch1 mediates growth suppression of papillary and follicular thyroid cancer cells by histone deacetylase inhibitors. Mol Cancer Ther 2009;8(2):350-6
73. Shen WT, Wong TS, Chung WY, et al. Valproic acid inhibits growth, induces apoptosis, and modulates apoptosis-regulatory and differentiation gene expression in human thyroid cancer cells. Surgery 2005;138:979-85 (Pubitemid 41797335)
74. Catalano MG, Fortunati N, Pugliese M et al. 2006 Valproic acid, a histone deacetylase inhibitor, enhances sensitivity to doxorubicin in anaplastic thyroid cancer cells. J Endocrinol 2006;191:465-72 (Pubitemid 44830622)
75. Kim TH, Yoo YH, Kang DY, et al. Efficacy on anaplastic thyroid carcinoma of valproic acid alone or in combination with doxorubicin, a synthetic chenodeoxycholic acid derivative, or lactacystin. Int J Oncol 2009;34(5):1353-62
76. Zhang Y, Li N, Caron C. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 2003;22(5):1168-79 (Pubitemid 36313600)
77. Matsuyama A, Shimazu T, Sumida Y et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 2002;21(24):6820-31 (Pubitemid 36014554)
78. Catalano MG, Poli R, Pugliese M, et al. Valproic acid enhances tubulin acetylation and apoptotic activity of paclitaxel on anaplastic thyroid cancer cell lines. Endocr Relat Cancer 2007;14(3):839-45 (Pubitemid 350074071)
79. Atadja P. Development of the pan-DAC inhibitor panobinostat (LBH589): Successes and challenges. Cancer Lett 2009;280(2):233-41
80. Catalano MG, Pugliese M, Gargantini E et al. Cytotoxic activity of the histone deacetylase inhibitor panobinostat (LBH589) in anaplastic thyroid cancer in vitro and in vivo. Int J Cancer 2012;130(3):694-704
81. Catalano MG, Fortunati N, Pugliese M et al. Histone deacetylase inhibition modulates e-cadherin expression and suppresses migration and invasion of anaplastic thyroid cancer cells. J Clin Endocrinol Metab 2012;97(7):E1150-9
82. Altmann A, Eisenhut M Bauder-Wust U, et al. Therapy of thyroid carcinoma with the histone deacetylase inhibitor MS-275. Eur J Nucl Med Mol Imaging 2010;37(12):2286-97
83. Wischnewski F, Pantel K Schwarzenbach H. 2006 Promoter demethylation and histone acetylation mediate gene expression of MAGE-A1, -A2, -A3, and -A12 in human cancer cells. Mol Cancer Res 2006;4:339-49 (Pubitemid 43837335)
84. Mitmaker EJ, Griff NJ, Grogan RH et al. Modulation of matrix metalloproteinase activity in human thyroid cancer cell lines using demethylating agents and histone deacetylase inhibitors. Surgery 2011;149:504-11
85. Lazar V, Bidart JM, Caillou B, et al. Expression of the Na+/I- symporter gene in human thyroid tumors: A comparison study with other thyroid-specific genes. J Clin Endocrinol Metab 1999;84:3228-34 (Pubitemid 30646949)
86. Gerard AC, Daumerie C, Mestdagh C et al. Correlation between the loss of thyroglobulin iodination and the expression of thyroid-specific proteins involved in iodine metabolism in thyroid carcinomas. J Clin Endocrinol Metab 2003;88:4977-83 (Pubitemid 37357552)
87. Arturi F, Russo D, Bidart JM, et al. Expression pattern of the pendrin and sodium/iodide symporter (NIS) gene in human thyroid carcinoma cell lines and human thyroid tumors. Eur J Endocrinol 2001;145:129-35 (Pubitemid 32707598)
88. Puxeddu E, Durante C, Avenia N, et al. Clinical implication of BRAF mutation in thyroid carcinoma. Trends Endocrinol Metab 2008;19:138-45 (Pubitemid 351621952)
89. Trapasso F, Iuliano R, Chiefari E, et al. Iodide symporter gene expression in normal and transformed rat thyroid cells. Eur J Endocrinol 1999;140:447-51 (Pubitemid 29254013)
90. Knauf JA, Fagin JA. Role of MAPK pathway oncoproteins in thyroid cancer pathogenesis and as drug targets. Curr Opin Cell Biol 2009;21:296-303
91. Furuya F, Shimura H, Suzuki H, et al. Histone deacetylase inhibitors restore radioiodide uptake and retention in poorly differentiated and anaplastic thyroid cancer cells by expression of the sodium/iodide symporter thyroperoxidase and thyroglobulin. Endocrinology 2004;145:2865-75 (Pubitemid 38686236)
92. Puppin C, D'Aurizio F, D'Elia AV, et al. Effects of histone acetylation on NIS promoter and expression of thyroid-specific transcription factors. Endocrinology 2005;146:3967-74 (Pubitemid 41175768)
93. Kitazono M, Robey R, Zhan Z, et al. Low concentrations of the histone deacetylase inhibitor, depsipeptide (FR901228), increase expression of the Na+/I- symporter and iodine accumulation in poorly differentiated thyroid carcinoma cells. J Clin Endocrinol Metab 2001;86:3430-5 (Pubitemid 32673517)
94. Fortunati N, Catalano MG, Arena K et al. Valproic acid induces the expression of the Na+/I- symporter and iodide uptake in poorly differentiated thyroid cancer cells. J Clin Endocrinol Metab 2004;89:1006-9 (Pubitemid 38269924)
95. Hou P, Bojdani E, Xing M. Induction of thyroid gene expression and radioiodine uptake in thyroid cancer cells by targeting major signaling pathways. J Clin Endocrinol Metab 2010;95:820-8
96. Liu Z, Xing M. Induction of sodium/iodide symporter (NIS) expression and radioiodine uptake in non-thyroid cancer cells. PLoS One 2012;7(2):e31729
97. Zhang M, Guo R, Xu H, et al. Retinoic acid and tributyrin induce in-vitro radioiodine uptake and inhibition of cell proliferation in a poorly differentiated follicular thyroid carcinoma. Nucl Med Commun 2011;32:605-10
98. Li W, Venkataraman GM, Ain KB. Protein synthesis inhibitors, in synergy with 5-Azacytidine, restore sodium/iodide symporter gene expression in human thyroid adenoma cell line, KAK-1 suggesting trans-active transcriptional repressor. J Clin Endocrinol Metab 2007;92:1080-7 (Pubitemid 46465686)
99. Provenzano MJ, Fitzgerald MP Krager K, Domann FE. Increased iodine uptake in thyroid carcinoma after treatment with sodium butyrate and decitabine (5-Aza-dC). Otolaryngol Head Neck Surg 2007;137:722-8 (Pubitemid 47632934)
100. Kramer OH, Gottlicher M, Heinzel T. Histone deacetylase as a therapeutic target. Trends Endocrinol Metab 2001;7:294-300 (Pubitemid 33714220)
101. Sherman EJ, Fury MG, Tuttle RM, et al. Phase II study of depsipeptide (DEP) in radioiodine (RAI)-refractory metastatic nonmedullary thyroid carcinoma. J Clin Oncol 2009;27(15S):6059
102. Kapiteijn E, Schneider TC, Morreau H et al. New treatment modalities in advanced thyroid cancer. Ann Oncol 2012;23:10-18
103. Puppin C, Passon N, Hershman JM et al. Cooperative effects of SAHA and VPA on expression of NIS mRNA and proliferation of thyroid cancer cells. J Mol Endocrinol 2012;48:217-27
104. Celano M, Calvagno MG, Bulotta S et al. Cytotoxic effects of Gemcitabine-loaded liposomes in human anaplastic thyroid carcinoma cells. BMC Cancer 2004;4:63
105. Celano M, Schenone S, Cosco D, et al. Cytotoxic effects of a novel pyrazolopyrimidine derivative entrapped in liposomes in anaplastic thyroid cancer cells in vitro and in xenograft tumors in vivo. Endocr Rel Cancer 2008;15:499-510 (Pubitemid 351880838)
106. Paolino D, Cosco D, Racanicchi L, et al. Gemcitabine-loaded PEGylated unilamellar liposomes vs GEMZAR-: Biodistribution, pharmacokinetic features and in vivo antitumor activity. J Control Rel 2010;144:144-50