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Sleeping beauty genetic screen identifies miR-23b::BTBD7 gene interaction as crucial for colorectal cancer metastasis

Sleeping beauty genetic screen identifies miR-23b::BTBD7 gene interaction as crucial for colorectal cancer metastasis
Sleeping beauty genetic screen identifies miR-23b::BTBD7 gene interaction as crucial for colorectal cancer metastasis

Background: Metastatic colorectal cancer (CRC) remains a deadly disease. Identifying locally advanced CRC patients with high risk of developing metastasis and improving outcome of metastatic CRC patients require discovering master regulators of metastasis. In this context, the non-coding part of the human genome is still largely unexplored. 


Methods: To interrogate the non-coding part of the human genome and disclose regulators of CRC metastasis, we combined a transposon-based forward genetic screen with a novel in vitro assay, which forces cells to grow deprived of cell-substrate and cell-cell contacts (i.e. forced single cell suspension assay - fSCS). 


Findings: We proved that fSCS selects CRC cells with mesenchymal and pro-metastatic traits. Moreover, we found that the transposon insertions conferred CRC cells resistance to fSCS and thus metastatic advantage. Among the retrieved transposon insertions, we demonstrated that the one located in the 3′UTR of BTBD7 disrupts miR-23b::BTBD7 interaction and contributes to pro-metastatic traits. In addition, miR-23b and BTBD7 correlate with CRC metastasis both in preclinical experiments and in clinical samples. 


Interpretation: fSCS is a simple and scalable in vitro assay to investigate pro-metastatic traits and transposon-based genetic screens can interrogate the non-coding part of the human genome (e.g. miRNA::target interactions). Finally, both Btbd7 and miR-23b represent promising prognostic biomarkers and therapeutic targets in CRC. 

Fund: This work was supported by Marie Curie Actions (CIG n. 303877) and Friuli Venezia Giulia region (Grant Agreement n°245574), Italian Association for Cancer Research (AIRC, MFAG n°13589), Italian Ministry of Health (GR-2010-2319387 and PE-2016-02361040) and 5x1000 to CRO Aviano.

Colorectal cancer metastasis, DNA transposons, microRNA target, spleeping beauty
Grisard, Eleonora
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Coan, Michela
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Cesaratto, Laura
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Rigo, Ilenia
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Zandonà, Luigi
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Paulitti, Alice
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Andreuzzi, Eva
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Rampioni Vinciguerra, Gian Luca
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Poletto, Evelina
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Del Ben, Fabio
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Brisotto, Giulia
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Biscontin, Eva
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Turetta, Matteo
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Dassi, Erik
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Mirnezami, Alex
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Canzonieri, Vincenzo
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Vecchione, Andrea
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Baldassarre, Gustavo
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Mongiat, Maurizio
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Spizzo, Riccardo
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Nicoloso, Milena S.
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Grisard, Eleonora
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Coan, Michela
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Cesaratto, Laura
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Rigo, Ilenia
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Zandonà, Luigi
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Paulitti, Alice
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Andreuzzi, Eva
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Rampioni Vinciguerra, Gian Luca
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Poletto, Evelina
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Del Ben, Fabio
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Brisotto, Giulia
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Biscontin, Eva
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Turetta, Matteo
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Dassi, Erik
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Mirnezami, Alex
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Canzonieri, Vincenzo
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Vecchione, Andrea
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Baldassarre, Gustavo
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Mongiat, Maurizio
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Spizzo, Riccardo
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Nicoloso, Milena S.
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Grisard, Eleonora, Coan, Michela, Cesaratto, Laura, Rigo, Ilenia, Zandonà, Luigi, Paulitti, Alice, Andreuzzi, Eva, Rampioni Vinciguerra, Gian Luca, Poletto, Evelina, Del Ben, Fabio, Brisotto, Giulia, Biscontin, Eva, Turetta, Matteo, Dassi, Erik, Mirnezami, Alex, Canzonieri, Vincenzo, Vecchione, Andrea, Baldassarre, Gustavo, Mongiat, Maurizio, Spizzo, Riccardo and Nicoloso, Milena S. (2019) Sleeping beauty genetic screen identifies miR-23b::BTBD7 gene interaction as crucial for colorectal cancer metastasis. EBioMedicine. (doi:10.1016/j.ebiom.2019.06.044).

Record type: Article

Abstract

Background: Metastatic colorectal cancer (CRC) remains a deadly disease. Identifying locally advanced CRC patients with high risk of developing metastasis and improving outcome of metastatic CRC patients require discovering master regulators of metastasis. In this context, the non-coding part of the human genome is still largely unexplored. 


Methods: To interrogate the non-coding part of the human genome and disclose regulators of CRC metastasis, we combined a transposon-based forward genetic screen with a novel in vitro assay, which forces cells to grow deprived of cell-substrate and cell-cell contacts (i.e. forced single cell suspension assay - fSCS). 


Findings: We proved that fSCS selects CRC cells with mesenchymal and pro-metastatic traits. Moreover, we found that the transposon insertions conferred CRC cells resistance to fSCS and thus metastatic advantage. Among the retrieved transposon insertions, we demonstrated that the one located in the 3′UTR of BTBD7 disrupts miR-23b::BTBD7 interaction and contributes to pro-metastatic traits. In addition, miR-23b and BTBD7 correlate with CRC metastasis both in preclinical experiments and in clinical samples. 


Interpretation: fSCS is a simple and scalable in vitro assay to investigate pro-metastatic traits and transposon-based genetic screens can interrogate the non-coding part of the human genome (e.g. miRNA::target interactions). Finally, both Btbd7 and miR-23b represent promising prognostic biomarkers and therapeutic targets in CRC. 

Fund: This work was supported by Marie Curie Actions (CIG n. 303877) and Friuli Venezia Giulia region (Grant Agreement n°245574), Italian Association for Cancer Research (AIRC, MFAG n°13589), Italian Ministry of Health (GR-2010-2319387 and PE-2016-02361040) and 5x1000 to CRO Aviano.

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Accepted/In Press date: 21 June 2019
e-pub ahead of print date: 11 July 2019
Keywords: Colorectal cancer metastasis, DNA transposons, microRNA target, spleeping beauty

Identifiers

Local EPrints ID: 432867
URI: http://eprints.soton.ac.uk/id/eprint/432867
PURE UUID: 6daa73ea-cc6b-4946-a171-860111bd258c

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Date deposited: 31 Jul 2019 16:30
Last modified: 05 Jun 2024 19:56

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Contributors

Author: Eleonora Grisard
Author: Michela Coan
Author: Laura Cesaratto
Author: Ilenia Rigo
Author: Luigi Zandonà
Author: Alice Paulitti
Author: Eva Andreuzzi
Author: Gian Luca Rampioni Vinciguerra
Author: Evelina Poletto
Author: Fabio Del Ben
Author: Giulia Brisotto
Author: Eva Biscontin
Author: Matteo Turetta
Author: Erik Dassi
Author: Alex Mirnezami
Author: Vincenzo Canzonieri
Author: Andrea Vecchione
Author: Gustavo Baldassarre
Author: Maurizio Mongiat
Author: Riccardo Spizzo
Author: Milena S. Nicoloso

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