Epigenetics in medullary thyroid cancer: From pathogenesis to targeted therapy

Recent Patents on Anti-Cancer Drug Discovery

Volumn 11, Issue 3, 2016, Pages 275-282

  Vitale, Giovanni ^a,b   Dicitore, Alessandra ^b   Messina, Erika ^c   Sciammarella, Concetta ^d   Faggiano, Antongiulio ^e   Colao, Annamaria ^f  

^a UNIVERSITY OF MILAN   (Italy)

^b ISTITUTO AUXOLOGICO ITALIANO   (Italy)

^c UNIVERSITY OF MESSINA   (Italy)

^d IOS and COLEMAN Srl   (Italy)

^e NATIONAL CANCER INSTITUTE   (Italy)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

DNA methylation; Epigenetic therapy; Epigenetics; Histone modifications; Medullary thyroid cancer; MicroRNA

Indexed keywords

CALCITONIN; CHROMOGRANIN A; MICRORNA; NOTCH1 RECEPTOR; UNTRANSLATED RNA; ANTINEOPLASTIC AGENT; TUMOR MARKER;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GROWTH; CONGENITAL MALFORMATION; DNA METHYLATION; EPIGENETICS; GENE MUTATION; GENE SILENCING; GENETIC SUSCEPTIBILITY; HISTONE MODIFICATION; HUMAN; MOLECULARLY TARGETED THERAPY; PATHOGENESIS; PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; SOMATIC MUTATION; SYSTEMATIC REVIEW; THYROID MEDULLARY CARCINOMA; ANIMAL; CARCINOMA, NEUROENDOCRINE; DRUG DESIGN; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; PATHOLOGY; THYROID NEOPLASMS;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; CARCINOMA, NEUROENDOCRINE; DRUG DESIGN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR TARGETED THERAPY; THYROID NEOPLASMS;

EID: 84983770591     PISSN: 15748928     EISSN: 22123970     Source Type: Journal    
DOI: 10.2174/1574892811666160614115356     Document Type: Article

References (95)

1. Vitale G, Caraglia M, Ciccarelli A, Lupoli G, Abbruzzese A, Tagliaferri P et al. Current approaches and perspectives in the therapy of medullary thyroid carcinoma. Cancer 2001; 91(9): 1797-808.
2. Manfredi GI, Dicitore A, Gaudenzi G, Caraglia M, Persani L, Vitale G. PI3K/Akt/mTOR signaling in medullary thyroid cancer: A promising molecular target for cancer therapy. Endocrine 2015; 48(2): 363-70.
3. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis 2010; 31(1): 27-36.
4. Gentilini D, Mari D, Castaldi D, Remondini D, Ogliari G, Ostan R, et al. Role of epigenetics in human aging and longevity: Genomewide DNA methylation profile in centenarians and centenarians' offspring. Age (Dordr) 2013; 35(5): 1961-73.
5. Kanwal R. Gupta S Epigenetic modifications in cancer. Clin Genet 2012; 81(4): 303-11.
6. Hudson J, Duncavage E, Tamburrino A, Salerno P, Xi L, Raffeld M, et al. Overexpression of miR-10a and miR-375 and downregulation of YAP1 in medullary thyroid carcinoma. Exp Mol Pathol 2013; 95(1): 62-7.
7. Schnekenburger M, Dicato M, Diederich M. Epigenetic modulators from “The Big Blue”: A treasure to fight against cancer. Cancer Lett 2014; 351(2): 182-97.
8. Hamm CA, Costa FF. Epigenomes as therapeutic targets. Pharmacol Ther 2015; 151: 72-86.
9. Cooper DN, Mort M, Stenson PD, Ball EV, Chuzhanova NA. Methylation-mediated deamination of 5-methylcytosine appears to give rise to mutations causing human inherited disease in CpNpG trinucleotides, as well as in CpG dinucleotides. Hum Genomics 2010; 4(6): 406-10.
10. Schübeler D. Function and information content of DNA methylation. Nature 2015; 517(7534): 321-6.
11. Lübbert M, Jones PA. Epigenetic Therapy of Cancer, 1st ed. Springer: New York 2014.
12. Subramaniam D, Thombre R, Dhar A, Anant S. DNA methyltransferases: A novel target for prevention and therapy. Front Oncol 2014; 1: 4: 80.
13. Josena KS, Chitale D, Narra V, Chen KM, Sawhney R, Worsham MJ. DNA Methylation in thyroid tumorigenesis. Cancers 2011; 3(2): 1732-43.
14. Faam B, Ghaffari MA, Ghadiri A, Azizi F. Epigenetic modifications in human thyroid cancer. Biomed Rep 2015; 3: 3-8.
15. Schagdarsurengin U, Gimm O, Dralle H, Hoang-Vu C, P. Pfeifer G, Dammann R. CpG island methylation of tumor-related promoters occurs preferentially in undifferentiated carcinoma. Thyroid 2006; 16 (7): 633-42.
16. Itoh F, Ishizaka Y, Tahira T, Yamamoto M, Miya A, Imai K, et al. Identification and analysis of the ret proto-oncogene promoter region in neuroblastoma cell lines and medullary thyroid carcinomas from MEN2A patients. Oncogene 1992; 7(6): 1201-6.
17. Mian C, Pennelli G, Fassan M, Balistreri M, Barollo S, Cavedon E, et al. MicroRNA profiles in familial and sporadic medullary thyroid carcinoma: Preliminary relationships with RET status and outcome. Thyroid 2012; 22(9): 890-96.
18. Angrisano T, Sacchetti S, Natale F, Cerrato A, Pero R, Keller S, et al. Chromatin and DNA methylation dynamics during retinoic acid-induced RET gene transcriptional activation in neuroblastoma cells. Nucleic Acids Res 2011; 39(6): 1993-2006.
19. Rodríguez-Rodero S, Fernández AF, Fernández-Morera JL, Castro-Santos P, Bayon GF, Ferrero C, et al. DNA methylation signatures identify biologically distinct thyroid cancer subtypes. J Clin Endocrinol Metab 2013; 98: 2811-21.
20. Lee SJ, Lee MH, Kim DW, Lee S, Huang S, Ryu MJ, et al. Crossregulation between oncogenic BRAFV600E kinase and the mst1 pathway in papillary thyroid carcinoma. PLoS One 2011; 13: 6(1): e16180.
21. Nakamura N, Carney JA, Jin L, Kajita S, Pallares J, Zhang H, et al. RASSF1A and NORE1A methylation and BRAFV600E mutations in thyroid tumors. Lab Invest 2005; 85: 1065-75.
22. Schagdarsurengin U, Gimm O, Hoang-Vu C, Dralle H, P. Pfeifer G, Dammann R. Frequent epigenetic silencing of the CpG island promoter of RASSF1A in thyroid carcinoma. Cancer Res 2002; 62: 3698.
23. Macià A, Galle P, Vaquero M, Gou-Fabregas M, Santacana M, Maliszewska A, et al. Sprouty1 is a candidate tumor suppressor gene in medullary thyroid carcinoma. Oncogene 2012; 31(35): 3961-72.
24. Macià A, Vaquero M, Gou-Fàbregas M, Castelblanco E, Valdivielso JM, Anerillas C, et al. Sprouty1 induces a senescenceassociated secretory phenotype by regulating NF_B activity: Implications for tumorigenesis. Cell Death Differ 2014; 21(2): 333-43.
25. Sponziello M, Durante C, Boichard A, Dima M, Puppin C, Verrienti A, et al. Epigenetic-related gene expression profile in medullary thyroid cancer revealed the overexpression of the histone methyltransferases EZH2 and SMYD3 in aggressive tumours. Mol Cell Endocrinol 2014; 392: 8-13.
26. Hatzimichael E, Crook T. Cancer epigenetics: New therapies and new challenges. J Drug Deliv 2013; 2013: 529312.
27. Sledziewski, A.Z., deVos, T. Oligonucleotide inhibitors of DNA methyltransferases and their use in treating diseases. US20150038548 (2015).
28. Dicitore A, Gaudenzi G, Misso G, Caraglia M, Borghi MO, Hofland L, et al. Combined treatment with Everolimus and 5-Aza-2-deoxycytidine in the therapy of medullary thyroid cancer. European Thyroid Association 37th Annual Meeting, Leiden, NL, September 7-11, 2013.
29. Maio, M., Covre, A. DNA hypomethylating agents for cancer therapy. WO2014128245 (2014).
30. Stephen, B., Baylin, S.B., Pardoll, D.M., Topalian, S.L. Cancer therapy via a combination of epigenetic modulation and immune modulation. WO2015035112 (2015).
31. Hofland, L.J. Novel composition for tumor growth control. WO2007114697 (2007).
32. Kimura H. Histone modifications for human epigenome analysis. J Hum Genet 2013; 58(7): 439-45.
33. Saetrom P, Snove O Jr, Rossi JJ. Epigenetics and microRNAs. Pediatr Res 2007; 61(5): 17R-23R.
34. Jin B, Li Y, Robertson KD. DNA methylation: Superior or subordinate in the epigenetic hierarchy? Genes Cancer 2011; 2(6): 607-17.
35. Gillette TG, Hill JA. Chromatin as the whiteboard of heart disease. Circ Res 2015; 116: 1245-53.
36. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293: 1074-80.
37. Mitsiades CS, Poulaki V, McMullan C, Negri J, Fanourakis G, Goudopoulou A, et al. Novel histone deacetylase inhibitors in the treatment of thyroid cancer. Clin Cancer Res 2005; 11(10): 15.
38. Bae WK, Hennighausen L. Canonical and non-canonical roles of the histone methyltransferase EZH2 in mammary development and cancer. Mol Cell Endocrinol 2014; 382: 593-7.
39. Hamamoto R, Furukawa Y, Morita M, Iimura Y, Silva FP, Li M, Yagyu R, et al. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat Cell Biol 2004; 6: 731-40.
40. Colón-Bolea P, Crespo P. Lysine methylation in cancer: SMYD3-MAP3K2 teaches us new lessons in the Ras-ERK pathway. Bioessays 2014; 36(12): 1162-9.
41. Kuntz, K.W., Knutson, S.K., Wigle, T.J.N. Inhibitors of human EZH2, and methods of use thereof. US20159175331 (2015).
42. Di Luccio, E., Morishita, M., Lee, T.H. Novel histone methyl transferase inhibitor and use thereof. WO2015152437 (2015).
43. De Souza C, Chatterji BP. HDAC inhibitors as novel anti-cancer therapeutics. Recent Pat Anticancer Drug Discov 2015; 10(2): 145-62.
44. Lin SF, Lin JD, Chou TC, Huang YY, Wong RJ. Utility of a histone deacetylase inhibitor (PXD101) for thyroid cancer treatment. PLoS One 2013; 8(10): e77684.
45. Ning L, Greenblatt DY, Kunnimalaiyaan M, Chen H. Suberoyl bishydroxamic acid activatesvnotch-1 signaling and induces apoptosis in medullary thyroid carcinoma cells. Oncologist 2008; 13(2): 98-104.
46. Greenblatt DY, Cayo MA, Adler JT, Ning L, Haymart MR, Kunnimalaiyaan M, et al. Valproic acid activates notch1 signaling and induces apoptosis in medullary thyroid cancer cells. Ann Surg 2008; 247(6): 1036-40.
47. Ning L, Jaskula-Sztul R, Kunnimalaiyaan M, Chen H. Suberoyl bishydroxamic acid activates notch1 signaling and suppresses tumor progression in an animal model of medullary thyroid carcinoma. Ann Surg Oncol 2008; 15(9): 2600-5.
48. Adler JT, Hottinger DG, Kunnimalaiyaan M, Chen H. Inhibition of growth in medullary thyroid cancer cells with histone deacetylase inhibitors and lithium chloride. J Surg Res 2010; 159(2): 640-4.
49. Jaskula-Sztul R, Pisarnturakit P, Landowski M, Chen H, Kunnimalaiyaan M. Expression of the active Notch1 decreases MTC tumor growth in vivo. J Surg Res 2011; 171(1): 23-7.
50. Jaskula-Sztul R, Eide J, Tesfazghi S, Dammalapati A, Harrison AD, Xiao-Min Yu, et al. Tumor-suppressor role of notch3 in medullary thyroid carcinoma revealed by genetic and pharmacological induction. Mol Cancer Ther 2015; 14: 499-512.
51. Mottamal M, Zheng S, Huang TL, Wang G. Histone deacetylase inhibitors in clinical studies as templates for new anticancer agents. Molecules 2015; 20(3): 3898-941.
52. Woyach JA, Kloos RT, Ringel MD, Arbogast D, Collamore M, Zwiebel JA, et al. Lack of therapeutic effect of the histone deacetylase inhibitor Vorinostat in patients with metastatic radioiodinerefractory thyroid carcinoma. J Clin Endocrinol Metab 2009; 94: 164-170.
53. Kunnimalaiyaan M, Vaccaro AM, Ndiaye MA, Chen H. Inactivation of glycogen synthase kinase-3beta, a downstream target of the raf-1 pathway, is associated with growth suppression in medullary thyroid cancer cells. Mol Cancer Ther 2007; 6: 1151-58.
54. Fouladi, M. Histone deacetylase inhibitors in cancer therapy. Cancer Invest. 2006; 24(5): 521-7.
55. Dadu R, Hu MN, Grubbs EG, Gagel RF. Use of tyrosine kinase inhibitors for treatment of medullary thyroid carcinoma. Recent Results Cancer Res 2015; 204: 227-49.
56. Leone A, Roca MS, Ciardiello C, Terranova-Barberio M, Vitagliano C, Ciliberto G, et al. Vorinostat synergizes with EGFR inhibitors in NSCLC cells by increasing ROS via up-regulation of the major mitochondrial porin VDAC1 and modulation of the c-Myc-NRF2-KEAP1 pathway. Free Radic Biol Med 2015; 89: 287-99.
57. Chen MC, Chen CH, Wang JC, Tsai AC, Liou JP, Pan SL, et al. The HDAC inhibitor, MPT0E028, enhances erlotinib-induced cell death in EGFR-TKI-resistant NSCLC cells. Cell Death Dis 2013; 19; 4: e810.
58. Nguyen, A.N., Kyle, J., MacBeth, K.J., Di Martino, J. Inhibition of drug resistant cancer cells. US20159101579 (2015).
59. Quayle, S. N., Jones, S.S., Sotomayor, E.M., Pinilla-Ibarz, J., Sahakian, E. Hdac inhibitors, alone or in combination with btk inhibitors, for treating Non-Hodgkin's Lymphoma. WO2015054197 (2015).
60. Wells SA Jr, Robinson BG, Gage lRF, Dralle H, Fagin JA, Santoro M, et al. Vandetanib in patients with locally advanced or metastatic medullary thyroid cancer: A randomized, double-blind Phase III trial. J Clin Oncol 2012; 30: 134-41.
61. Elisei R, Schlumberger MJ, Müller SP, Schöffski P, Brose MS, Shah MH, et al. Cabozantinib in progressive medullary thyroid cancer. J Clin Oncol 2013; 31: 3639-46.
62. Milano A. New molecular targeted therapies in thyroid cancer. Anticancer Drugs 2006; 17(8): 869-79.
63. Zhou N, Xu W, Zhang Y. Histone deacetylase inhibitors merged with protein tyrosine kinase inhibitors. Drug Discov Ther 2015; 9(3): 147-55.
64. Bing, G.Y., Caixia, W., Haiyan, H., Tao, Y., Xiaohong, L., Jing, Q., Yuhua, L., Shaoqing, J. Novel nitric oxide donor type HDAC (histone deacetylase) inhibitor as well as preparation method and medical application thereof. CN104356087 (2015).
65. Duan W, Li J, Inks ES, Chou CJ, Jia Y, Chu X, et al. Design, synthesis, and antitumor evaluation of novel histone deacetylase inhibitors equipped with a phenylsulfonylfuroxan module as a nitric oxide donor. J Med Chem 2015; 58(10): 4325-38.
66. Soler MN, Bobé P, Benihoud K, Lemaire G, Roos BA, Lausson S. Gene therapy of rat medullary thyroid cancer by naked nitric oxide synthase II DNA injection. J Gene Med 2000; 2(5): 344-52.
67. Ragot T, Provost C, Prignon A, Cohen R, Lepoivre M, Lausson S. Apoptosis induction by combination of drugs or a conjugated molecule associating non-steroidal anti-inflammatory and nitric oxide donor effects in medullary thyroid cancer models: Implication of the tumor suppressor p73. Thyroid Res 2015; 14, 8: 13.
68. Kazuo S, Ahlenstiel C, Marks K, Kelleher AD. Promoter targeting RNAs: Unexpected contributors to the control of HIV-1 transcription. Mol Ther Nucleic Acids 2015; 4: e22.
69. Yarmishyn AA, Kurochkin IV. Long noncoding RNAs: A potential novel class of cancer biomarkers. Front Genet 2015; 6: 145.
70. Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol 2012; 6(6): 590-610.
71. Holley CL, Topkara VK. An introduction to small non-coding RNAs: miRNA and snoRNA. Cardiovasc Drugs Ther 2011; 25(2): 151-9.
72. Morani F, Titone R, Pagano L, Galetto A, Alabiso O, Aimaretti G. Autophagy and thyroid carcinogenesis: Genetic and epigenetic links. Endocr Relat Cancer 2014; 21(1): R13-29.
73. Iorio MV, Croce CM. MicroRNAs in cancer: Small molecules with a huge impact. J Clin Oncol 2009; 27(34): 5848-56.
74. de Oliveira L, Frizzo MN. Evaluation molecular in medullary thyroid carcinoma: IJRRR 2016; 95(3): 90-9.
75. Pallante P, Battista S, Pierantoni GM, Fusco A. Deregulation of microRNA expression in thyroid neoplasias. Nat Rev Endocrinol 2014; 10: 88-101.
76. Nikiforova MN, Tseng C, Steward D, Diorio D, Nikiforov YE. MicroRNA expression profiling of thyroid tumors: Biological significance and diagnostic utility. J Clin Endocrinol Metab 2008; 93(5): 1600-08.
77. Abraham D, Jackson N, Gundara JS, Zhao J, Gill AJ, Delbridge L, et al. MicroRNA profiling of sporadic and hereditary medullary thyroid cancer identifies predictors of nodal metastasis, prognosis, and potential therapeutic targets. Clin Cancer Res 2011; 17(14): 4772-81.
78. van de Bunt M, Gaulton KJ, Parts L, Moran I, Johnson PR, Lindgren CM, et al. The miRNA profile of human pancreatic islets and beta-cells and relationship to type 2 diabetes pathogenesis. PLoS One 2013; 8(1): e55272.
79. Jin Y, Liu Y, Zhang J, Huang W, Jiang H, Hou Y, et al. The expression of miR-375 is associated with carcinogenesis in three subtypes of lung cancer. PLoS One 2015; 10(12): e0144187.
80. Nishikawa E, Osada H, Okazaki Y, Arima C, Tomida S, Tatematsu Y, et al. miR-375 is activated by ASH1 and inhibits YAP1 in a lineage-dependent manner in lung cancer. Cancer Res 2011; 71(19): 6165-73.
81. Pennelli G, Galuppini F, Barollo S, Cavedon E, Bertazza L, Fassan M, et al. The PDCD4/miR-21 pathway in medullary thyroid carcinoma. Hum Pathol 2015; 46(1): 50-7.
82. Shen F, Mo M-H, Chen L, An S, Tan X, Fu Y, et al. MicroRNA-21 Down-regulates Rb1 expression by targeting PDCD4 in retinoblastoma. J Cancer 2014; 5(9): 804-12.
83. Duan L, Hao X, Liu Z, Zhang Y, Zhang G. MiR-129-5p is downregulated and involved in the growth, apoptosis and migration of medullary thyroid carcinoma cells through targeting RET. FEBS Lett 2014; 588(9): 1644-51.
84. Puppin C, Durante C, Sponziello M, Verrienti A, Pecce V, Lavarone E, et al. Overexpression of genes involved in miRNA biogenesis in medullary thyroid carcinomas with RET mutation. Endocrine 2014; 47(2): 528-36.
85. Kentwell J, Gundara JS, Sidhu SB. Noncoding RNAs in endocrine malignancy. Oncologist 2014; 19(5): 483-91.
86. Gundara JS, Robinson BG, Sidhu SB. Evolution of the “autophagamiR”. Autophagy 2011; 7(12): 1553-4.
87. Santarpia L, Jimenez C. miRNAs in medullary thyroid carcinoma: When will they be relevant to the clinic? Int J Endo Oncol 2014; 1(1): 7-10.
88. Santarpia L, Calin GA, Adam L, Ye L, Fusco A, Giunti S, et al. miRNA signature associated with human metastatic medullary thyroid carcinoma. Endocr Relat Cancer 2013; 20(6): 809-23.
89. Schnekenburger M, Diederich M. Epigenetics offer new horizons for colorectal cancer prevention. Curr Colorectal Cancer Rep 2012; 8(1): 66-81.
90. Møller, T. Oligonucleotides for modulation of target RNA activity. US20158951984 (2015).
91. Bhat, B. MicroRNA compounds and methods for modulating MIR-21 activity. US20159181547 (2015).
92. Wójcicka A, Kolanowska M, Jażdżewski K. Mechanisms in endocrinology: MicroRNA in diagnostics and therapy of thyroid cancer. Eur J Endocrinol 2016; 174(3): R89-98.
93. Gundara JS, Zhao J, Gill AJ, Lee JC, Delbridge L, Robinson BG, et al. Noncoding RNA blockade of autophagy is therapeutic in medullary thyroid cancer. Cancer Med 2015; 4(2): 174-82.
94. Xing M. Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer 2013; 13(3): 184-99.
95. Liu H, McDowell TL, Hanson NE, Tang X, Fujimoto J, Rodriguez-Canales J. Laser capture microdissection for the investigative pathologist. Vet Pathol 2014; 51(1): 257-69.