Long non-coding RNA TINCR suppresses metastatic melanoma dissemination by preventing ATF4 translation

Transition from proliferative-to-invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down-regulated in meta...

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Veröffentlicht in:	EMBO reports Jg. 22; H. 3; S. e50852 - n/a
Hauptverfasser:	Melixetian, Marine, Bossi, Daniela, Mihailovich, Marija, Punzi, Simona, Barozzi, Iros, Marocchi, Federica, Cuomo, Alessandro, Bonaldi, Tiziana, Testa, Giuseppe, Marine, Jean-Christophe, Leucci, Eleonora, Minucci, Saverio, Pelicci, Pier Giuseppe, Lanfrancone, Luisa
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 03.03.2021 Springer Nature B.V John Wiley and Sons Inc
Schlagworte:	ATF4 Binding Depletion Drug resistance EMBO03 EMBO36 EMBO37 Genotype & phenotype integrated stress response lncRNAs MEK inhibitors Melanoma Metastases Metastasis Non-coding RNA Nutrients Phenotypes Phosphorylation Protein biosynthesis Protein synthesis Proteins Reversion Ribonucleic acid Ribosomes RNA Translation translational reprogramming Tumors lncRNAs melanoma translational reprogramming ATF4 integrated stress response
ISSN:	1469-221X, 1469-3178, 1469-3178
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Abstract	Transition from proliferative-to-invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down-regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR-depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re-expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor-initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient-rich conditions by repressing translation of selected ISR RNAs. SYNOPSIS Long non-coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes. High TINCR levels prevent translational reprogramming and ATF4 translation, maintaining proliferative, epithelial-like states. TINCR downregulation leads to translational reprogramming and ATF4 activation, promoting invasion in nutrient-rich conditions. TINCR interacts with selected integrated stress response RNAs, preventing their binding to the translating ribosomes. Graphical Abstract Long non-coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes.
AbstractList	Transition from proliferative‐to‐invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down‐regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR‐depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re‐expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor‐initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient‐rich conditions by repressing translation of selected ISR RNAs. Transition from proliferative‐to‐invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down‐regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR‐depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re‐expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor‐initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient‐rich conditions by repressing translation of selected ISR RNAs. SYNOPSIS Long non‐coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes. High TINCR levels prevent translational reprogramming and ATF4 translation, maintaining proliferative, epithelial‐like states. TINCR downregulation leads to translational reprogramming and ATF4 activation, promoting invasion in nutrient‐rich conditions. TINCR interacts with selected integrated stress response RNAs, preventing their binding to the translating ribosomes. Long non‐coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes. Transition from proliferative-to-invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down-regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR-depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re-expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor-initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient-rich conditions by repressing translation of selected ISR RNAs.Transition from proliferative-to-invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down-regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR-depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re-expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor-initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient-rich conditions by repressing translation of selected ISR RNAs. Transition from proliferative‐to‐invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down‐regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR‐depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re‐expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor‐initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient‐rich conditions by repressing translation of selected ISR RNAs. Long non‐coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes. Transition from proliferative‐to‐invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down‐regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR‐depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re‐expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor‐initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient‐rich conditions by repressing translation of selected ISR RNAs. image Long non‐coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes. High TINCR levels prevent translational reprogramming and ATF4 translation, maintaining proliferative, epithelial‐like states. TINCR downregulation leads to translational reprogramming and ATF4 activation, promoting invasion in nutrient‐rich conditions. TINCR interacts with selected integrated stress response RNAs, preventing their binding to the translating ribosomes. Transition from proliferative-to-invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is challenged by the poor understanding of mechanisms underlying its maintenance. Here, we report that the lncRNA TINCR is down-regulated in metastatic melanoma and its silencing increases the expression levels of invasive markers, in vitro migration, in vivo tumor growth, and resistance to BRAF and MEK inhibitors. The critical mediator is ATF4, a central player of the integrated stress response (ISR), which is activated in TINCR-depleted cells in the absence of starvation and eIF2α phosphorylation. TINCR depletion increases global protein synthesis and induces translational reprogramming, leading to increased translation of mRNAs encoding ATF4 and other ISR proteins. Strikingly, re-expression of TINCR in metastatic melanoma suppresses the invasive phenotype, reduces numbers of tumor-initiating cells and metastasis formation, and increases drug sensitivity. Mechanistically, TINCR interacts with mRNAs associated with the invasive phenotype, including ATF4, preventing their binding to ribosomes. Thus, TINCR is a suppressor of the melanoma invasive phenotype, which functions in nutrient-rich conditions by repressing translation of selected ISR RNAs. SYNOPSIS Long non-coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes. High TINCR levels prevent translational reprogramming and ATF4 translation, maintaining proliferative, epithelial-like states. TINCR downregulation leads to translational reprogramming and ATF4 activation, promoting invasion in nutrient-rich conditions. TINCR interacts with selected integrated stress response RNAs, preventing their binding to the translating ribosomes. Graphical Abstract Long non-coding RNA TINCR blocks the acquisition of invasive phenotypes in melanoma, including drug resistance and metastasis dissemination. TINCR targets RNAs associated with invasive phenotypes, preventing their interaction with ribosomes.
Author	Cuomo, Alessandro Punzi, Simona Marocchi, Federica Bonaldi, Tiziana Pelicci, Pier Giuseppe Bossi, Daniela Mihailovich, Marija Melixetian, Marine Barozzi, Iros Leucci, Eleonora Minucci, Saverio Marine, Jean-Christophe Lanfrancone, Luisa Testa, Giuseppe
AuthorAffiliation	3 Department of Oncology and Hemato‐oncology University of Milan Milan Italy 2 Department of Surgery and Cancer Imperial College London London UK 6 Laboratory for RNA Cancer Biology Department of Oncology KULeuven Leuven Belgium 5 Center for Cancer Biology VIB Leuven Belgium 8 Present address: Institute of Oncology Research (IOR) Bellinzona Switzerland 9 Present address: Candiolo Cancer Institute—FPO IRCCS Candiolo Torino Italy 1 Department of Experimental Oncology IEO European Institute of Oncology IRCCS Milan Italy 7 Department of Biosciences University of Milan Milan Italy 4 Laboratory for Molecular Cancer Biology Department of Oncology KULeuven Leuven Belgium
AuthorAffiliation_xml	– name: 4 Laboratory for Molecular Cancer Biology Department of Oncology KULeuven Leuven Belgium – name: 5 Center for Cancer Biology VIB Leuven Belgium – name: 6 Laboratory for RNA Cancer Biology Department of Oncology KULeuven Leuven Belgium – name: 2 Department of Surgery and Cancer Imperial College London London UK – name: 1 Department of Experimental Oncology IEO European Institute of Oncology IRCCS Milan Italy – name: 3 Department of Oncology and Hemato‐oncology University of Milan Milan Italy – name: 8 Present address: Institute of Oncology Research (IOR) Bellinzona Switzerland – name: 9 Present address: Candiolo Cancer Institute—FPO IRCCS Candiolo Torino Italy – name: 7 Department of Biosciences University of Milan Milan Italy
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Keywords	lncRNAs melanoma translational reprogramming ATF4 integrated stress response
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Snippet	Transition from proliferative-to-invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is... Transition from proliferative‐to‐invasive phenotypes promotes metastasis and therapy resistance in melanoma. Reversion of the invasive phenotype, however, is...
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SubjectTerms	ATF4 Binding Depletion Drug resistance EMBO03 EMBO36 EMBO37 Genotype & phenotype integrated stress response lncRNAs MEK inhibitors Melanoma Metastases Metastasis Non-coding RNA Nutrients Phenotypes Phosphorylation Protein biosynthesis Protein synthesis Proteins Reversion Ribonucleic acid Ribosomes RNA Translation translational reprogramming Tumors
Title	Long non-coding RNA TINCR suppresses metastatic melanoma dissemination by preventing ATF4 translation
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