Role of epigenetic modulation for the treatment of sarcoma

Current Treatment Options in Oncology

Volumn 14, Issue 3, 2013, Pages 454-464

  Cote, Gregory M ^a   Choy, Edwin ^a  

^a NONE   (United States)

Author keywords

Chromatin modification; Epigenetics; Ewing sarcoma; EZH2; HDAC inhibitor; Sarcoma

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ABEXINOSTAT; ANTHRACYCLINE; AZACITIDINE; BELINOSTAT; BEVACIZUMAB; BORTEZOMIB; CISPLATIN; CYCLOPHOSPHAMIDE; DNA; DOXORUBICIN; ENTINOSTAT; ETOPOSIDE; GEMCITABINE; HISTONE; HISTONE DEACETYLASE INHIBITOR; IFOSFAMIDE; METHOTREXATE; PANOBINOSTAT; PAZOPANIB; PLACEBO; ROMIDEPSIN; TAXANE DERIVATIVE; TEMOZOLOMIDE; TRANSCRIPTION FACTOR EZH2; UNINDEXED DRUG; VACCINE; VALPROIC ACID; VINCRISTINE; VORINOSTAT;

ADJUVANT CHEMOTHERAPY; CANCER PROGNOSIS; CANCER SURGERY; CENTRAL NERVOUS SYSTEM TUMOR; CHEMOTHERAPY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMBINATION CHEMOTHERAPY; CPG ISLAND; CUTANEOUS T CELL LYMPHOMA; DNA METHYLATION; DNA SEQUENCE; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; DRUG TOLERABILITY; EPIGENETICS; EWING SARCOMA; GASTROINTESTINAL STROMAL TUMOR; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HISTONE MODIFICATION; HUMAN; LYMPHOMA; MALIGNANT MESOTHELIOMA; MENTAL DISEASE; META ANALYSIS (TOPIC); METASTASIS; MIGRAINE; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; MYELODYSPLASTIC SYNDROME; NEUROBLASTOMA; OSTEOSARCOMA; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); RECURRENCE FREE SURVIVAL; REVIEW; RHABDOMYOSARCOMA; SARCOMA; SEIZURE; SOFT TISSUE SARCOMA; SOLID TUMOR; TUMOR VOLUME;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CLINICAL TRIALS AS TOPIC; COMBINED MODALITY THERAPY; EPIGENESIS, GENETIC; HUMANS; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; SARCOMA; SARCOMA, EWING; SEQUENCE ANALYSIS, DNA;

EID: 84884170835     PISSN: 15272729     EISSN: 15346277     Source Type: Journal    
DOI: 10.1007/s11864-013-0239-3     Document Type: Review

References (65)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics. CA Cancer J Clin. 2013;63(1):11-30.
2. Clark MA, Fisher C, Judson I, Thomas JM. Soft-tissue sarcomas in adults. N Engl J Med. 2005;353(7):701-11.
3. O'Sullivan B, Davis AM, Turcotte R, et al. Preoperative versus postoperative radiotherapy in soft-tissue sarcoma of the limbs: a randomised trial. Lancet. 2002;359(9325):2235-41.
4. Woll PJ, Reichardt P, Le Cesne A, et al. Adjuvant chemotherapy with doxorubicin, ifosfamide, and lenograstim for resected soft-tissue sarcoma (EORTC 62931): a multicentre randomised controlled trial. Lancet Oncol. 2012;13(10):1045-54. This is the largest study of modern adjuvant chemotherapy. There was no difference in PFS or OS. This highlights the need for novel therapies to treat this disease.
5. Pervaiz N, Colterjohn N, Farrokhyar F, Tozer R, Figueredo A, Ghert M. A systematic meta-analysis of randomized controlled trials of adjuvant chemotherapy for localized resectable soft-tissue sarcoma. Cancer. 2008;113(3):573-81.
6. Italiano A, Mathoulin-Pelissier S, Cesne AL, et al. Trends in survival for patients with metastatic soft-tissue sarcoma. Cancer. 2011;117(5):1049-54.
7. Karavasilis V, Seddon BM, Ashley S, Al-Muderis O, Fisher C, Judson I. Significant clinical benefit of first-line palliative chemotherapy in advanced soft-tissue sarcoma: retrospective analysis and identification of prognostic factors in 488 patients. Cancer. 2008;112(7):1585-91.
8. Grier HE, Krailo MD, Tarbell NJ, et al. Addition of ifosfamide and etoposide to standard chemotherapy for Ewing's sarcoma and primitive neuroectodermal tumor of bone. N Engl J Med. 2003;348(8):694-701.
9. Goorin AM, Schwartzentruber DJ, Devidas M, et al. Presurgical chemotherapy compared with immediate surgery and adjuvant chemotherapy for nonmetastatic osteosarcoma: Pediatric Oncology Group Study POG-8651. J Clin Oncol. 2003;21(8):1574-80.
10. Holliday R. The inheritance of epigenetic defects. Science. 1987;238(4824):163-70.
11. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev. 2009;23(7):781-3.
12. Hassler MR, Egger G. Epigenomics of cancer - emerging new concepts. Biochimie. 2012;94(1):2219-30.
13. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128(4):683-92.
14. Wilson BG, Roberts CW. SWI/SNF nucleosome remodellers and cancer. Nat Rev Cancer 2011;11:481-92. There is now an emerging understanding of SWI/SNF nucleosome remodeling in malignancy. This review nicely summarizes this disease model and compiles known data on SWI/SNF subunit mutations in cancer.
15. Siddiqi S, Mills J, Matushansky I. Epigenetic remodeling of chromatin architecture: exploring tumor differentiation therapies in mesenchymal stem cells and sarcomas. Curr Stem Cell Res Ther;5(1):63-73.
16. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-54.
17. Costello JF, Fruhwald MC, Smiraglia DJ, et al. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet. 2000;24(2):132-8.
18. Tsuchiya T, Sekine K, Hinohara S, Namiki T, Nobori T, Kaneko Y. Analysis of the p16INK4, p14ARF, p15, TP53, and MDM2 genes and their prognostic implications in osteosarcoma and Ewing sarcoma. Cancer Genet Cytogenet. 2000;120(2):91-8.
19. Hurtubise A, Bernstein ML, Momparler RL. Preclinical evaluation of the antineoplastic action of 5-aza-2'-deoxycytidine and different histone deacetylase inhibitors on human Ewing's sarcoma cells. Cancer Cell Int. 2008;8:16.
20. Nestheide S, Bridge JA, Barnes M, Frayer R, Sumegi J. Pharmacologic inhibition of epigenetic modification reveals targets of aberrant promoter methylation in Ewing Sarcoma. Pediatr Blood Cancer.
21. Sievers S, Fritzsch C, Lehnhardt M, et al. Hypermethylation of the APC promoter but lack of APC mutations in myxoid/round-cell liposarcoma. Int J Cancer. 2006;119(10):2347-52.
22. Luger K. Structure and dynamic behavior of nucleosomes. Curr Opin Genet Dev. 2003;13(2):127-35.
23. Freitas MA, Sklenar AR, Parthun MR. Application of mass spectrometry to the identification and quantification of histone post-translational modifications. J Cell Biochem. 2004;92(4):691-700.
24. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381-95.
25. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 1997;90(4):595-606.
26. Patel JH, Du Y, Ard PG, et al. The c-MYC oncoprotein is a substrate of the acetyltransferases hGCN5/PCAF and TIP60. Mol Cell Biol. 2004;24(24):10826- 34.
27. Ververis K, Hiong A, Karagiannis TC, Licciardi PV. Histone deacetylase inhibitors (HDACIs): multitargeted anticancer agents. Biologics. 2013;7:47-60.
28. Nakagawa M, Oda Y, Eguchi T, et al. Expression profile of class I histone deacetylases in human cancer tissues. Oncol Rep. 2007;18(4):769-74.
29. Kutko MC, Glick RD, Butler LM, et al. Histone deacetylase inhibitors induce growth suppression and cell death in human rhabdomyosarcoma in vitro. Clin Cancer Res. 2003;9(15):5749-55.
30. Maeda T, Nagaoka Y, Kawai Y, et al. Inhibitory effects of cancer cell proliferation by novel histone deacetylase inhibitors involve p21/WAF1 induction and G2/M arrest. Biol Pharm Bull. 2005;28(5):849-53.
31. Yamamoto S, Tanaka K, Sakimura R, et al. Suberoylanilide hydroxamic acid (SAHA) induces apoptosis or autophagy-associated cell death in chondrosarcoma cell lines. Anticancer Res. 2008;28(3A):1585-91.
32. Muhlenberg T, Zhang Y, Wagner AJ, et al. Inhibitors of deacetylases suppress oncogenic KIT signaling, acetylate HSP90, and induce apoptosis in gastrointestinal stromal tumors. Cancer Res. 2009;69(17):6941-50.
33. Liu S, Cheng H, Kwan W, Lubieniecka JM, Nielsen TO. Histone deacetylase inhibitors induce growth arrest, apoptosis, and differentiation in clear cell sarcoma models. Mol Cancer Ther. 2008;7(6):1751-61.
34. Su L, Sampaio AV, Jones KB, et al. Deconstruction of the SS18-SSX fusion oncoprotein complex: insights into disease etiology and therapeutics. Cancer Cell 2012;21:333-47.
35. Wittenburg LA, Bisson L, Rose BJ, Korch C, Thamm DH. The histone deacetylase inhibitor valproic acid sensitizes human and canine osteosarcoma to doxorubicin. Cancer Chemother Pharmacol;67(1):83-92.
36. Yang C, Choy E, Hornicek FJ, et al. Histone deacetylase inhibitor PCI-24781 enhances chemotherapy-induced apoptosis in multidrug-resistant sarcoma cell lines. Anticancer Res 31(4):1115-23.
37. Yang C, Choy E, Hornicek FJ, et al. Histone deacetylase inhibitor (HDACI) PCI-24781 potentiates cytotoxic effects of doxorubicin in bone sarcoma cells. Cancer Chemother Pharmacol;67(2):439-46.
38. Edwin Choy SB, James Butrynski, Jeffrey Morgan, Mint Sirisawad, Chitra Mani, Suzanne George, Andrew Wagner, David Harmon, Yael Rubinstein, Zhenfeng Duan, Francis Hornicek, George Demetri. Massachusetts General Hospital, Boston, MA,. Phase I dose escalation study of abexinostat and doxorubicin in patients with metastatic sarcomas. In: American Association for Cancer Research Annual Meeting; 2013; Washington, D.C.; 2013.
39. Mermoud JE, Rowbotham SP, Varga-Weisz PD. Keeping chromatin quiet: how nucleosome remodeling restores heterochromatin after replication. Cell Cycle. 2011;10(23):4017-25.
40. Jackson EM, Sievert AJ, Gai X, et al. Genomic analysis using high-density single nucleotide polymorphism-based oligonucleotide arrays and multiplex ligation-dependent probe amplification provides a comprehensive analysis of INI1/SMARCB1 in malignant rhabdoid tumors. Clin Cancer Res. 2009;15(6):1923-30.
41. Versteege I, Sevenet N, Lange J, et al. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature. 1998;394(6689):203-6.
42. Biegel JA, Zhou JY, Rorke LB, Stenstrom C, Wainwright LM, Fogelgren B. Germ-line and acquired mutations of INI1 in atypical teratoid and rhabdoid tumors. Cancer Res. 1999;59(1):74-9.
43. Kohashi K, Oda Y, Yamamoto H, et al. SMARCB1/INI1 protein expression in round cell soft tissue sarcomas associated with chromosomal translocations involving EWS: a special reference to SMARCB1/INI1 negative variant extraskeletal myxoid chondrosarcoma. Am J Surg Pathol. 2008;32(8):1168-74.
44. Kohashi K, Izumi T, Oda Y, et al. Infrequent SMARCB1/INI1 gene alteration in epithelioid sarcoma: a useful tool in distinguishing epithelioid sarcoma from malignant rhabdoid tumor. Hum Pathol. 2009;40(3):349-55.
45. Mobley BC, McKenney JK, Bangs CD, et al. Loss of SMARCB1/INI1 expression in poorly differentiated chordomas. Acta Neuropathol. 2010;120(6):745-53.
46. Kadoch C, Crabtree GR. Reversible Disruption of mSWI/SNF (BAF) Complexes by the SS18-SSX Oncogenic Fusion in Synovial Sarcoma. Cell. 2013;153(1):71-85. In this article by Kodoch and Crabtree they determine for the first time that the translocation product SS18-SSX in Synovial Sarcoma disrupts the function of SWI/SNF. They show evidence that this leads to transcription silencing and as such may drive oncogenesis. If these data hold true, it will be an important step in the search for novel therapies for this disease.
47. Kennison JA. The Polycomb and Trithorax group proteins of Drosophila: trans-regulators of homeotic gene function. Annu Rev Genet. 1995;29:289-303.
48. Shao Z, Raible F, Mollaaghababa R, et al. Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell. 1999;98(1):37-46.
49. Simon JA, Lange CA. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res. 2008;647(1-2):21-9.
50. Staege MS, Hutter C, Neumann I, et al. DNA microarrays reveal relationship of Ewing family tumors to both endothelial and fetal neural crest-derived cells and define novel targets. Cancer Res. 2004;64(22):8213-21.
51. Riggi N, Suva ML, Suva D, et al. EWS-FLI-1 expression triggers a Ewing's sarcoma initiation program in primary human mesenchymal stem cells. Cancer Res. 2008;68(7):2176-85.
52. Richter GH, Plehm S, Fasan A, et al. EZH2 is a mediator of EWS/FLI1 driven tumor growth and metastasis blocking endothelial and neuro-ectodermal differentiation. Proc Natl Acad Sci U S A. 2009;106(13):5324-9.
53. Burdach S, Plehm S, Unland R, et al. Epigenetic maintenance of stemness and malignancy in peripheral neuroectodermal tumors by EZH2. Cell Cycle 2009;8:1991-6.
54. Changchien YC, Tatrai P, Papp G, et al. Poorly differentiated synovial sarcoma is associated with high expression of enhancer of zeste homologue 2 (EZH2). J Transl Med. 2012;10:216.
55. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol. 2009;10(3):223-32.
56. Kantarjian H, Issa JP, Rosenfeld CS, et al. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Cancer. 2006;106(8):1794-803.
57. Straus DJ, Duvic M, Kuzel T, et al. Results of a phase II trial of oral bexarotene (Targretin) combined with interferon alfa-2b (Intron-A) for patients with cutaneous T-cell lymphoma. Cancer 2007;109:1799-803.
58. Olsen EA, Kim YH, Kuzel TM, et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol. 2007;25(21):3109-15.
59. Piekarz RL, Frye R, Prince HM, et al. Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood. 2011;117(22):5827-34.
60. Ryan QC, Headlee D, Acharya M, et al. Phase I and pharmacokinetic study of MS-275, a histone deacetylase inhibitor, in patients with advanced and refractory solid tumors or lymphoma. J Clin Oncol. 2005;23(17):3912-22.
61. Schmitt T, Liu L, Leisen M, Ho AD, Burhenne J, Mikus G, Egerer G. Pharmacokinetic analyses of vorinostat in patients with metastatic soft tissue sarcoma. In: ASCO; 2012; Chicago; 2012.
62. Schelman WR, Schell K, Marnocha R, Eickhoff J, Alberti D, Wilding G, Bailey H. A phase I study of vorinostat in combination with bortezomib in refractory solid tumors. In: ASCO Annual Meeting; 2007; 2007.
63. Attia S, Okuno SH, Adkins D, Ahuja HG, Ducker TP, Maples WJ, Ochs L, Wentworth-Hartung NL, Erlichman C, Bailey HH. A phase II consortium trial of vorinostat and bortezomib for advanced soft tissue sarcomas. In: ASCO Annual Meeting; 2011; Chicago, IL; 2011.
64. Banerji U, van Doorn L, Papadatos-Pastos D, et al. A phase I pharmacokinetic and pharmacodynamic study of CHR-3996, an oral class I selective histone deacetylase inhibitor in refractory solid tumors. Clin Cancer Res. 2012;18(9):2687-94.
65. Muscal JA, Thompson PA, Horton TM, et al. A phase I trial of vorinostat and bortezomib in children with refractory or recurrent solid tumors: a Children's Oncology Group phase I consortium study (ADVL0916). Pediatr Blood Cancer. 2013;60(3):390-5.