Skip to main content
Top
Published in: BMC Cancer 1/2017

Open Access 01-12-2017 | Research article

Mechanism of action of trabectedin in desmoplastic small round cell tumor cells

Authors: S. Uboldi, I. Craparotta, G. Colella, E. Ronchetti, L. Beltrame, S. Vicario, S. Marchini, N. Panini, G. Dagrada, F. Bozzi, S. Pilotti, C. M. Galmarini, M. D’Incalci, R. Gatta

Published in: BMC Cancer | Issue 1/2017

Login to get access

Abstract

Background

Desmoplastic small round cell tumor (DSRCT) is a rare and highly aggressive disease, that can be described as a member of the family of small round blue cell tumors. The molecular diagnostic marker is the t(11;22)(p13;q12) translocation, which creates an aberrant transcription factor, EWS-WT1, that underlies the oncogenesis of DSRCT. Current treatments are not very effective so new active drugs are needed. Trabectedin, now used as a single agent for the treatment of soft tissue sarcoma, was reported to be active in some pre-treated DSRCT patients. Using JN-DSRCT-1, a cell line derived from DSRCT expressing the EWS-WT1 fusion protein, we investigated the ability of trabectedin to modify the function of the chimeric protein, as in other sarcomas expressing fusion proteins. After detailed characterization of the EWS-WT1 transcripts structure, we investigated the mode of action of trabectedin, looking at the expression and function of the oncogenic chimera.

Methods

We characterized JN-DSRCT-1 cells using cellular approaches (FISH, Clonogenicity assay) and molecular approaches (Sanger sequencing, ChIP, GEP).

Results

JN-DSRCT-1 cells were sensitive to trabectedin at nanomolar concentrations. The cell line expresses different variants of EWS-WT1, some already identified in patients. EWS-WT1 mRNA expression was affected by trabectedin and chimeric protein binding on its target gene promoters was reduced. Expression profiling indicated that trabectedin affects the expression of genes involved in cell proliferation and apoptosis.

Conclusions

The JN-DSRCT-1 cell line, in vitro, is sensitive to trabectedin: after drug exposure, EWS-WT1 chimera expression decreases as well as binding on its target promoters. Probably the heterogeneity of chimera transcripts is an obstacle to precisely defining the molecular mode of action of drugs, calling for further cellular models of DSRCT, possibly growing in vivo too, to mimic the biological complexity of this disease.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gerald WL, Rosai J. Desmoplastic small round cell tumor with divergent differentiation. Paediatr Pathol. 1989;9:177–83.CrossRef Gerald WL, Rosai J. Desmoplastic small round cell tumor with divergent differentiation. Paediatr Pathol. 1989;9:177–83.CrossRef
4.
5.
go back to reference Lopez-Gonzalez A, Cantos B, Tejerina E, Provencio M. Activity of trabectedin in desmoplastic small round cell tumor. Med Oncol. 2011;28:S644–6.CrossRefPubMed Lopez-Gonzalez A, Cantos B, Tejerina E, Provencio M. Activity of trabectedin in desmoplastic small round cell tumor. Med Oncol. 2011;28:S644–6.CrossRefPubMed
6.
go back to reference Larsen AK, Galmarini CM, D’Incalci M. Unique features of trabectedin mechanism of action. Cancer Chemother Pharmacol. 2016;77(4):663–71. doi:10.1007/s00280-015-2918-1. Epub 2015Dec 14. Larsen AK, Galmarini CM, D’Incalci M. Unique features of trabectedin mechanism of action. Cancer Chemother Pharmacol. 2016;77(4):663–71. doi:10.​1007/​s00280-015-2918-1. Epub 2015Dec 14.
7.
go back to reference Grosso F, Jones RL, Demetri GD, Judson IR, Blay JY, Le Cesne A, Sanfilippo R, Casieri P, Collini P, Dileo P, Spreafico C, Stacchiotti S, Tamborini E, Tercero JC, Jimeno J, D’Incalci M, Gronchi A, Fletcher JA, Pilotti S, Casali PG. Efficacy of trabectedin (ecteinascidin-743) in advanced pretreated myxoid liposarcomas: a retrospective study. Lancet Oncol. 2007;8(7):595–602.CrossRefPubMed Grosso F, Jones RL, Demetri GD, Judson IR, Blay JY, Le Cesne A, Sanfilippo R, Casieri P, Collini P, Dileo P, Spreafico C, Stacchiotti S, Tamborini E, Tercero JC, Jimeno J, D’Incalci M, Gronchi A, Fletcher JA, Pilotti S, Casali PG. Efficacy of trabectedin (ecteinascidin-743) in advanced pretreated myxoid liposarcomas: a retrospective study. Lancet Oncol. 2007;8(7):595–602.CrossRefPubMed
8.
go back to reference Di Giandomenico S, Frapolli R, Bello E, Uboldi S, Licandro SA, Marchini S, Beltrame L, Brich S, Mauro V, Tamborini E, Pilotti S, Casali PG, Grosso F, Sanfilippo R, Gronchi A, Mantovani R, Gatta R, Galmarini CM, Sousa-Faro JM, D’Incalci M. Mode of action of trabectedin in myxoid liposarcomas. Oncogene. 2014;33(44):5201–10. doi:10.1038/onc.2013.462. Epub 2013 Nov 11.CrossRefPubMed Di Giandomenico S, Frapolli R, Bello E, Uboldi S, Licandro SA, Marchini S, Beltrame L, Brich S, Mauro V, Tamborini E, Pilotti S, Casali PG, Grosso F, Sanfilippo R, Gronchi A, Mantovani R, Gatta R, Galmarini CM, Sousa-Faro JM, D’Incalci M. Mode of action of trabectedin in myxoid liposarcomas. Oncogene. 2014;33(44):5201–10. doi:10.​1038/​onc.​2013.​462. Epub 2013 Nov 11.CrossRefPubMed
9.
go back to reference Nishio J, Iwasaki H, Ishiguro M, Ohjimi Y, Fujita C, Yanai F, Nibu K, Mitsudome A, Kaneko Y, Kikuchi M. Establishment and characterization of a novel human desmoplastic small round cell tumor cell line, JN-DSRCT-1. Lab Invest. 2002;82(9):1175–82.CrossRefPubMed Nishio J, Iwasaki H, Ishiguro M, Ohjimi Y, Fujita C, Yanai F, Nibu K, Mitsudome A, Kaneko Y, Kikuchi M. Establishment and characterization of a novel human desmoplastic small round cell tumor cell line, JN-DSRCT-1. Lab Invest. 2002;82(9):1175–82.CrossRefPubMed
10.
go back to reference Bandopadhayay P, Jabbour AM, Riffkin C, Salmanidis M, Gordon L, Popovski D, Rigby L, Ashley DM, Watkins DN, Thomas DM, Algar E, Ekert PG. The oncogenic properties of EWS/WT1 of desmoplastic small round cell tumors are unmasked by loss of p53 in murine embryonic fibroblasts. BMC Cancer. 2013;13:585. doi:10.1186/1471-2407-13-585.CrossRefPubMedPubMedCentral Bandopadhayay P, Jabbour AM, Riffkin C, Salmanidis M, Gordon L, Popovski D, Rigby L, Ashley DM, Watkins DN, Thomas DM, Algar E, Ekert PG. The oncogenic properties of EWS/WT1 of desmoplastic small round cell tumors are unmasked by loss of p53 in murine embryonic fibroblasts. BMC Cancer. 2013;13:585. doi:10.​1186/​1471-2407-13-585.CrossRefPubMedPubMedCentral
11.
go back to reference Kim J, Lee K, Pelletier J. The desmoplastic small round cell tumor t(11;22) translocation produces EWS/WT1 isoforms with differing oncogenic properties. Oncogene. 1998;16(15):1973–9.CrossRefPubMed Kim J, Lee K, Pelletier J. The desmoplastic small round cell tumor t(11;22) translocation produces EWS/WT1 isoforms with differing oncogenic properties. Oncogene. 1998;16(15):1973–9.CrossRefPubMed
12.
go back to reference Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19(2):185–93.CrossRefPubMed Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19(2):185–93.CrossRefPubMed
13.
go back to reference Liu R, Holik AZ, Su S, Jansz N, Chen K, Leong HS, Blewitt ME, Asselin-Labat ML, Smyth GK, Ritchie ME. Why weight? Modelling sample and observational level variability improves power in RNA-seq analyses. Nucleic Acids Res. 2015;43(15):e97. doi:10.1093/nar/gkv412.CrossRefPubMedPubMedCentral Liu R, Holik AZ, Su S, Jansz N, Chen K, Leong HS, Blewitt ME, Asselin-Labat ML, Smyth GK, Ritchie ME. Why weight? Modelling sample and observational level variability improves power in RNA-seq analyses. Nucleic Acids Res. 2015;43(15):e97. doi:10.​1093/​nar/​gkv412.CrossRefPubMedPubMedCentral
15.
go back to reference Grosu P, Townsend JP, Hartl DL, Cavalieri D. Pathway Processor: a tool for integrating whole-genome expression results into metabolic networks. Genome Res. 2002;12(7):1121–6.CrossRefPubMedPubMedCentral Grosu P, Townsend JP, Hartl DL, Cavalieri D. Pathway Processor: a tool for integrating whole-genome expression results into metabolic networks. Genome Res. 2002;12(7):1121–6.CrossRefPubMedPubMedCentral
16.
go back to reference Sales G, Calura E, Martini P, Romualdi C. Graphite Web: Web tool for gene set analysis exploiting pathway topology. Web Server Issue. 2013;41:W89–97. doi:10.1093/nar/gkt386. Epub 2013 May 10. Sales G, Calura E, Martini P, Romualdi C. Graphite Web: Web tool for gene set analysis exploiting pathway topology. Web Server Issue. 2013;41:W89–97. doi:10.​1093/​nar/​gkt386. Epub 2013 May 10.
17.
go back to reference Negri T, Brich S, Conca E, Bozzi F, Orsenigo M, Stacchiotti S, Alberghini M, Mauro V, Gronchi A, Dusio GF, Pelosi G, Picci P, Casali PG, Pierotti MA, Pilotti S. Receptor tyrosine kinase pathway analysis sheds light on similarities between clear-cell sarcoma and metastatic melanoma. Genes Chromosomes Cancer. 2012;51(2):111–26. doi:10.1002/gcc.20933. Epub 2011 Nov 1.CrossRefPubMed Negri T, Brich S, Conca E, Bozzi F, Orsenigo M, Stacchiotti S, Alberghini M, Mauro V, Gronchi A, Dusio GF, Pelosi G, Picci P, Casali PG, Pierotti MA, Pilotti S. Receptor tyrosine kinase pathway analysis sheds light on similarities between clear-cell sarcoma and metastatic melanoma. Genes Chromosomes Cancer. 2012;51(2):111–26. doi:10.​1002/​gcc.​20933. Epub 2011 Nov 1.CrossRefPubMed
18.
go back to reference Tavecchio M, Simone M, Erba E, Chiolo I, Liberi G, Foiani M, D’Incalci M, Damia G. Role of homologous recombination in trabectedin-induced DNA damage. Eur J Cancer. 2008;44:609-–18.CrossRefPubMed Tavecchio M, Simone M, Erba E, Chiolo I, Liberi G, Foiani M, D’Incalci M, Damia G. Role of homologous recombination in trabectedin-induced DNA damage. Eur J Cancer. 2008;44:609-–18.CrossRefPubMed
19.
go back to reference Liu J, Nau MM, Yeh JC, Allegra CJ, Chu E, Wright JJ. Molecular heterogeneity and function of EWS-WT1 fusion transcripts in desmoplastic small round cell tumors. Clin Cancer Res. 2000;6(9):3522–9.PubMed Liu J, Nau MM, Yeh JC, Allegra CJ, Chu E, Wright JJ. Molecular heterogeneity and function of EWS-WT1 fusion transcripts in desmoplastic small round cell tumors. Clin Cancer Res. 2000;6(9):3522–9.PubMed
20.
go back to reference Grohar PJ, Griffin LB, Yeung C, Chen QR, Pommier Y, Khanna C, Khan J, Helman LJ. Ecteinascidin 743 interferes with the activity of EWS-FLI1 in Ewing sarcoma cells. Neoplasia. 2011;13(2):145–53.CrossRefPubMedPubMedCentral Grohar PJ, Griffin LB, Yeung C, Chen QR, Pommier Y, Khanna C, Khan J, Helman LJ. Ecteinascidin 743 interferes with the activity of EWS-FLI1 in Ewing sarcoma cells. Neoplasia. 2011;13(2):145–53.CrossRefPubMedPubMedCentral
21.
go back to reference Ambati SR, Shieh JH, Pera B, Lopes EC, Chaudhry A, Wong EW, Saxena A, Su TL, Moore MA. BO-1055, a novel DNA cross-linking agent with remarkable low myelotoxicity shows potent activity in sarcoma models. Oncotarget. 2016;7:43062–75. doi:10.18632/oncotarget.9657. Ambati SR, Shieh JH, Pera B, Lopes EC, Chaudhry A, Wong EW, Saxena A, Su TL, Moore MA. BO-1055, a novel DNA cross-linking agent with remarkable low myelotoxicity shows potent activity in sarcoma models. Oncotarget. 2016;7:43062–75. doi:10.​18632/​oncotarget.​9657.
Metadata
Title
Mechanism of action of trabectedin in desmoplastic small round cell tumor cells
Authors
S. Uboldi
I. Craparotta
G. Colella
E. Ronchetti
L. Beltrame
S. Vicario
S. Marchini
N. Panini
G. Dagrada
F. Bozzi
S. Pilotti
C. M. Galmarini
M. D’Incalci
R. Gatta
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2017
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-017-3091-1

Other articles of this Issue 1/2017

BMC Cancer 1/2017 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine