Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer

LINE-1 retrotransposons are abundant repetitive elements of viral origin, which in normal cells are kept quiescent through epigenetic mechanisms. Activation of LINE-1 occurs frequently in cancer and can enable LINE-1 mobilization but also has retrotransposition-independent consequences. We pre...

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Main Authors: Cruickshanks, H.A, Vafadar-Isfahani, N., Dunican, D.S., Lee, A., Sproul, D., Lund, Jonathan N., Meehan, R.R., Tufarelli, C.
Format: Article
Published: Oxford Journals
Online Access:https://eprints.nottingham.ac.uk/2212/
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author Cruickshanks, H.A
Vafadar-Isfahani, N.
Dunican, D.S.
Lee, A.
Sproul, D.
Lund, Jonathan N.
Meehan, R.R.
Tufarelli, C.
author_facet Cruickshanks, H.A
Vafadar-Isfahani, N.
Dunican, D.S.
Lee, A.
Sproul, D.
Lund, Jonathan N.
Meehan, R.R.
Tufarelli, C.
author_sort Cruickshanks, H.A
building Nottingham Research Data Repository
collection Online Access
description LINE-1 retrotransposons are abundant repetitive elements of viral origin, which in normal cells are kept quiescent through epigenetic mechanisms. Activation of LINE-1 occurs frequently in cancer and can enable LINE-1 mobilization but also has retrotransposition-independent consequences. We previously reported that in cancer, aberrantly active LINE-1 promoters can drive transcription of flanking unique sequences giving rise to LINE-1 chimeric transcripts (LCTs). Here, we show that one such LCT, LCT13, is a large transcript (>300 kb) running antisense to the metastasis-suppressor gene TFPI- 2. We have modelled antisense RNA expression at TFPI-2 in transgenic mouse embryonic stem (ES) cells and demonstrate that antisense RNA induces silencing and deposition of repressive histone modifications implying a causal link. Consistent with this, LCT13 expression in breast and colon cancer cell lines is associated with silencing and repressive chromatin at TFPI-2. Furthermore, we detected LCT13 transcripts in 56% of colorectal tumours exhibiting reduced TFPI-2 expression. Our findings implicate activation of LINE-1 elements in subsequent epigenetic remodelling of surrounding genes, thus hinting a novel retrotransposition-independent role for LINE-1 elements in malignancy.
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spelling nottingham-22122020-05-04T20:34:29Z https://eprints.nottingham.ac.uk/2212/ Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer Cruickshanks, H.A Vafadar-Isfahani, N. Dunican, D.S. Lee, A. Sproul, D. Lund, Jonathan N. Meehan, R.R. Tufarelli, C. LINE-1 retrotransposons are abundant repetitive elements of viral origin, which in normal cells are kept quiescent through epigenetic mechanisms. Activation of LINE-1 occurs frequently in cancer and can enable LINE-1 mobilization but also has retrotransposition-independent consequences. We previously reported that in cancer, aberrantly active LINE-1 promoters can drive transcription of flanking unique sequences giving rise to LINE-1 chimeric transcripts (LCTs). Here, we show that one such LCT, LCT13, is a large transcript (>300 kb) running antisense to the metastasis-suppressor gene TFPI- 2. We have modelled antisense RNA expression at TFPI-2 in transgenic mouse embryonic stem (ES) cells and demonstrate that antisense RNA induces silencing and deposition of repressive histone modifications implying a causal link. Consistent with this, LCT13 expression in breast and colon cancer cell lines is associated with silencing and repressive chromatin at TFPI-2. Furthermore, we detected LCT13 transcripts in 56% of colorectal tumours exhibiting reduced TFPI-2 expression. Our findings implicate activation of LINE-1 elements in subsequent epigenetic remodelling of surrounding genes, thus hinting a novel retrotransposition-independent role for LINE-1 elements in malignancy. Oxford Journals Article PeerReviewed Cruickshanks, H.A, Vafadar-Isfahani, N., Dunican, D.S., Lee, A., Sproul, D., Lund, Jonathan N., Meehan, R.R. and Tufarelli, C. Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer. Nucleic Acids Research, 41 (14). pp. 6857-6869. ISSN 0305-1048 http://nar.oxfordjournals.org/content/41/14/6857 doi:10.1093/nar/gkt438 doi:10.1093/nar/gkt438
spellingShingle Cruickshanks, H.A
Vafadar-Isfahani, N.
Dunican, D.S.
Lee, A.
Sproul, D.
Lund, Jonathan N.
Meehan, R.R.
Tufarelli, C.
Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer
title Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer
title_full Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer
title_fullStr Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer
title_full_unstemmed Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer
title_short Expression of a large LINE-1-driven antisense RNA is linked to epigenetic silencing of the metastasis suppressor gene TFPI-2 in cancer
title_sort expression of a large line-1-driven antisense rna is linked to epigenetic silencing of the metastasis suppressor gene tfpi-2 in cancer
url https://eprints.nottingham.ac.uk/2212/
https://eprints.nottingham.ac.uk/2212/
https://eprints.nottingham.ac.uk/2212/