Histone deacetylase inhibitor ITF2357 leads to apoptosis and enhances doxorubicin cytotoxicity in preclinical models of human sarcoma

Oncogenesis

Volumn 7, Issue 2, 2018, Pages

  Di Martile, Marta ^a   Desideri, Marianna ^a   Tupone, Maria Grazia ^a   Buglioni, Simonetta ^a   Antoniani, Barbara ^a   Mastroiorio, Carlotta ^a   Falcioni, Rita ^a   Ferraresi, Virginia ^a   Baldini, Nicola ^b,c   Biagini, Roberto ^a   Milella, Michele ^a   Trisciuoglio, Daniela ^a,d   Del Bufalo, Donatella ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; CASPASE; DOXORUBICIN; GIVINOSTAT; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO4; TRANSCRIPTION FACTOR FOXO6; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIZATION; FEMALE; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SARCOMA; SARCOMA CELL; UPREGULATION;

EID: 85042526779     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/s41389-018-0026-x     Document Type: Article

References (48)

1. HaDuong, J. H., Martin, A. A., Skapek, S. X. & Mascarenhas, L. Sarcomas. Pediatr. Clin. North Am. 62, 179-200 (2015).
2. Zahm, S. H. & Fraumeni, J. F. Jr The epidemiology of soft tissue sarcoma. Semin. Oncol. 24, 504-514 (1997).
3. Walczak, B. E. & Irwin, R. B. Sarcoma chemotherapy. J. Am. Acad. Orthop. Surg. 21, 480-491 (2013).
4. Riedel, R. F. Systemic therapy for advanced soft tissue sarcomas: highlighting novel therapies and treatment approaches. Cancer 118, 1474-1485 (2012).
5. Le Cesne, A. et al. Doxorubicin-based adjuvant chemotherapy in soft tissue sarcoma: pooled analysis of two STBSG-EORTC phase III clinical trials. Ann. Oncol. 25, 2425-2432 (2014).
6. Di Marcotullio, L., Canettieri, G., Infante, P., Greco, A. & Gulino, A. Protected from the inside: endogenous histone deacetylase inhibitors and the road to cancer. Biochim. Biophys. Acta 1815, 241-252 (2011).
7. Lane, A. A. & Chabner, B. A. Histone deacetylase inhibitors in cancer therapy. J. Clin. Oncol. 27, 5459-5468 (2009).
8. Tan, J., Cang, S., Ma, Y., Petrillo, R. L. & Liu, D. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J. Hematol. Oncol. 3, 5 (2010).
9. Choy, E. et al. Phase 1 study of oral abexinostat, a histone deacetylase inhibitor, in combination with doxorubicin in patients with metastatic sarcoma. Cancer 121, 1223-1230 (2015).
10. Chu, Q. S. et al. A phase II study of SB939, a novel pan-histone deacetylase inhibitor, in patients with translocation-associated recurrent/metastatic sarcomas-NCIC-CTG IND 200†. Ann. Oncol. 26, 973-981 (2015).
11. Thomas, S. et al. A phase I trial of panobinostat and epirubicin in solid tumors with a dose expansion in patients with sarcoma. Ann. Oncol. 27, 947-952 (2016).
12. Kayarthodi, S. et al. Anti-epileptic drug targets ewing sarcoma. J. Pharm. Sci. Pharmacol. 1, 87-100 (2014).
13. Sampson V. B. et al. Vorinostat enhances cytotoxicity of SN-38 and temozolomide in ewing sarcoma cells and activates STAT3/AKT/MAPK pathways. PLoS ONE 10, e0142704 (2015).
14. Lopez, G. et al. HDAC inhibition for the treatment of epithelioid sarcoma: novel cross talk between epigenetic components. Mol. Cancer Res. 14, 35-43 (2016).
15. Ou, W. B. et al. HDACi inhibits liposarcoma via targeting of the MDM2-p53 signaling axis and PTEN, irrespective of p53 mutational status. Oncotarget 6, 10510-10520 (2015).
16. Ma, L. et al. SIRT1 and SIRT2 inhibition impairs pediatric soft tissue sarcoma growth. Cell Death Dis. 5, e1483 (2014).
17. Laporte, A. N. et al. HDAC and proteasome inhibitors synergize to activate proapoptotic factors in synovial sarcoma. PLoS ONE 12, e0169407 (2017).
18. Su, L., Cheng, H., Sampaio, A. V., Nielsen, T. O. & Underhill, T. M. EGR1 reactivation by histone deacetylase inhibitors promotes synovial sarcoma cell death through the PTEN tumor suppressor. Oncogene 29, 4352-4361 (2010).
19. Capobianco, E. et al. Separate and combined effects of DNMT and HDAC inhibitors in treating human multi-drug resistant osteosarcoma HosDXR150 cell line. PLoS ONE 9, e95596 (2014).
20. Murahari, S. et al Sensitivity of osteosarcoma cells to HDAC inhibitor AR-42 mediated apoptosis. BMC Cancer 17, 67 (2017).
21. Pettke, A. et al. Suberanilohydroxamic acid (vorinostat) synergistically enhances the cytotoxicity of doxorubicin and cisplatin in osteosarcoma cell lines. Anticancer Drugs 27, 1001-1010 (2016).
22. Thayanithy, V. et al. Combinatorial treatment of DNA and chromatinmodifying drugs cause cell death in human and canine osteosarcoma cell lines. PLoS ONE 7, e43720 (2012).
23. Blattmann, C. et al. Histone deacetylase inhibition sensitizes osteosarcoma to heavy ion radiotherapy. Radiat. Oncol. 10, 146 (2015).
24. Luo, J., Su, F., Chen, D., Shiloh, A. & Gu, W. Deacetylation of p53modulates its effect on cell growth and apoptosis. Nature 408, 377-381 (2000).
25. Stankov, M. V. et al. Histone deacetylase inhibitors induce apoptosis in myeloid leukemia by suppressing autophagy. Leukemia 28, 577-588 (2014).
26. Zhang, J. et al. Histone deacetylase inhibitors induce autophagy through FOXO1-dependent pathways. Autophagy 11, 629-642 (2015).
27. Di Pompo, G. et al. Novel histone deacetylase inhibitors induce growth arrest, apoptosis, and differentiation in sarcoma cancer stem cells. J. Med. Chem. 58, 4073-4079 (2015).
28. Bauer, S. et al. Phase I study of panobinostat and imatinib in patients with treatment-refractory metastatic gastrointestinal stromal tumors. Br. J. Cancer 110, 1155-1162 (2014).
29. Vitfell-Rasmussen, J. et al. A phase I/II clinical trial of belinostat (PXD101) in combination with doxorubicin in patients with soft tissue sarcomas. Sarcoma 2016, 2090271 (2016).
30. Cassier, P. A. et al. A phase II trial of panobinostat in patients with advanced pretreated soft tissue sarcoma. A study from the French Sarcoma Group. Br. J. Cancer 109, 909-914 (2013).
31. Furlan, A. et al. Pharmacokinetics, safety and inducible cytokine responses during a phase 1 trial of the oral histone deacetylase inhibitor ITF2357 (givinostat). Mol. Med. 17, 353-362 (2011).
32. Rambaldi, A. et al. A pilot study of the histone-deacetylase inhibitor givinostat in patients with JAK2V617F positive chronic myeloproliferative neoplasms. Br. J. Haematol. 150, 446-455 (2010).
33. Zappasodi, R. et al. Pleiotropic antitumor effects of the pan-HDAC inhibitor ITF2357 against c-Myc-overexpressing human B-cell non-Hodgkin lymphomas. Int. J. Cancer 135, 2034-2045 (2014).
34. Golay, J. et al. The histone deacetylase inhibitor ITF2357 has anti-leukemic activity in vitro and in vivo and inhibits IL-6 and VEGF production by stromal cells. Leukemia 21, 1892-1900 (2007).
35. Todoerti, K. et al. Pleiotropic anti-myeloma activity of ITF2357: inhibition of interleukin-6 receptor signaling and repression of miR-19a and miR-19b. Haematologica 95, 260-269 (2010).
36. Angeletti, F. et al. Inhibition of the autophagy pathway synergistically potentiates the cytotoxic activity of givinostat (ITF2357) on human glioblastoma cancer stem cells. Front. Mol. Neurosci. 9, 107 (2016).
37. Del Bufalo, D. et al. Histone deacetylase inhibition synergistically enhances pemetrexed cytotoxicity through induction of apoptosis and autophagy in non-small cell lung cancer. Mol. Cancer 13, 230 (2014).
38. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12, 1-222 (2016).
39. Coomans de Brachene, A. & Demoulin, J. B. FOXO transcription factors in cancer development and therapy. Cell. Mol. Life Sci. 73, 1159-1172 (2016).
40. Rodrigues, M., Kalinowska, W., Zielinski, C. & Sinzinger, H. Verapamil decreases accumulation of 99Tcm-MIBI and 99Tcm-tetrofosmin in human breast cancer and soft tissue sarcoma cell lines. Nucl. Med. Commun. 22, 645-650 (2001).
41. Pistritto, G., Trisciuoglio, D., Ceci, C., Garufi, A. & D'Orazi, G. Apoptosis as anticancer mechanism: function and dysfunction of its modulators and targeted therapeutic strategies. Aging 8, 603-619 (2016).
42. Ferraiuolo, M., Di Agostino, S., Blandino, G. & Strano, S. Oncogenic intra-p53 family member interactions in human cancers. Front. Oncol. 6, 77 (2016).
43. Koeneke, E., Witt, O. & Oehme, I. HDAC family members intertwined in the regulation of autophagy: a druggable vulnerability in aggressive tumor entities. Cells 4, 135-168 (2015).
44. Fulda, S. & Kogel, D. Cell death by autophagy: emerging molecular mechanisms and implications for cancer therapy. Oncogene 34, 5105-5113 (2015).
45. Schmitt-Ney, M. & Camussi, G. The PAX3-FOXO1 fusion protein present in rhabdomyosarcoma interferes with normal FOXO activity and the TGF-beta pathway. PLoS ONE 10, e0121474 (2015).
46. Guan, H. et al. FOXO1 inhibits osteosarcoma oncogenesis via Wnt/betacatenin pathway suppression. Oncogenesis 4, e166 (2015).
47. Lopez, G. et al. Combining PCI-24781, a novel histone deacetylase inhibitor, with chemotherapy for the treatment of soft tissue sarcoma. Clin. Cancer Res. 15, 3472-3483 (2009).
48. Ragazzoni, Y. et al. The thiazole derivative CPTH6 impairs autophagy. Cell Death Dis. 4, e524 (2013).