Transcriptional regulation of autophagy-lysosomal function in BRAF-driven melanoma progression and chemoresistance
Identifieur interne : 000313 ( Main/Merge ); précédent : 000312; suivant : 000314Transcriptional regulation of autophagy-lysosomal function in BRAF-driven melanoma progression and chemoresistance
Auteurs : Shun Li [États-Unis, République populaire de Chine] ; Ying Song [États-Unis] ; Christine Quach [États-Unis] ; Hongrui Guo [États-Unis, République populaire de Chine] ; Gyu-Beom Jang [États-Unis] ; Hadi Maazi [États-Unis] ; Shihui Zhao [États-Unis] ; Nathaniel A. Sands [États-Unis] ; Qingsong Liu [République populaire de Chine] ; Gino K. In [États-Unis] ; David Peng [États-Unis] ; Weiming Yuan [États-Unis] ; Keigo Machida [États-Unis] ; Min Yu [États-Unis] ; Omid Akbari [États-Unis] ; Ashley Hagiya [États-Unis] ; Yongfei Yang [États-Unis] ; Vasu Punj [États-Unis] ; Liling Tang [République populaire de Chine] ; Chengyu Liang [États-Unis]Source :
- Nature Communications [ 2041-1723 ] ; 2019.
Abstract
Autophagy maintains homeostasis and is induced upon stress. Yet, its mechanistic interaction with oncogenic signaling remains elusive. Here, we show that in BRAFV600E-melanoma, autophagy is induced by BRAF inhibitor (BRAFi), as part of a transcriptional program coordinating lysosome biogenesis/function, mediated by the TFEB transcription factor. TFEB is phosphorylated and thus inactivated by BRAFV600E via its downstream ERK independently of mTORC1. BRAFi disrupts TFEB phosphorylation, allowing its nuclear translocation, which is synergized by increased phosphorylation/inactivation of the ZKSCAN3 transcriptional repressor by JNK2/p38-MAPK. Blockade of BRAFi-induced transcriptional activation of autophagy-lysosomal function in melanoma xenografts causes enhanced tumor progression, EMT-transdifferentiation, metastatic dissemination, and chemoresistance, which is associated with elevated TGF-β levels and enhanced TGF-β signaling. Inhibition of TGF-β signaling restores tumor differentiation and drug responsiveness in melanoma cells. Thus, the “BRAF-TFEB-autophagy-lysosome” axis represents an intrinsic regulatory pathway in BRAF-mutant melanoma, coupling BRAF signaling with TGF-β signaling to drive tumor progression and chemoresistance.
Url:
DOI: 10.1038/s41467-019-09634-8
PubMed: 30979895
PubMed Central: 6461621
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PMC:6461621Le document en format XML
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Los Angeles, CA 90033 USA</nlm:aff>
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Chengdu, 611130 China</nlm:aff>
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Los Angeles, CA 90033 USA</nlm:aff>
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<author><name sortKey="Zhao, Shihui" sort="Zhao, Shihui" uniqKey="Zhao S" first="Shihui" last="Zhao">Shihui Zhao</name>
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<author><name sortKey="Sands, Nathaniel A" sort="Sands, Nathaniel A" uniqKey="Sands N" first="Nathaniel A." last="Sands">Nathaniel A. Sands</name>
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Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
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<author><name sortKey="Liu, Qingsong" sort="Liu, Qingsong" uniqKey="Liu Q" first="Qingsong" last="Liu">Qingsong Liu</name>
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<institution>Chinese Academy of Sciences,</institution>
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350 Shushan Hu Road, Hefei, 230031 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
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<placeName><settlement type="city">Hefei</settlement>
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</placeName>
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<author><name sortKey="In, Gino K" sort="In, Gino K" uniqKey="In G" first="Gino K." last="In">Gino K. In</name>
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<institution>Norris Comprehensive Cancer, Division of Oncology,</institution>
<institution>University of Southern California,</institution>
</institution-wrap>
Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
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<author><name sortKey="Peng, David" sort="Peng, David" uniqKey="Peng D" first="David" last="Peng">David Peng</name>
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<institution>Department of Dermatology, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
</institution-wrap>
Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Yuan, Weiming" sort="Yuan, Weiming" uniqKey="Yuan W" first="Weiming" last="Yuan">Weiming Yuan</name>
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<institution-id institution-id-type="GRID">grid.42505.36</institution-id>
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<institution>University of Southern California,</institution>
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Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
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</affiliation>
</author>
<author><name sortKey="Machida, Keigo" sort="Machida, Keigo" uniqKey="Machida K" first="Keigo" last="Machida">Keigo Machida</name>
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<institution>University of Southern California,</institution>
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Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Yu, Min" sort="Yu, Min" uniqKey="Yu M" first="Min" last="Yu">Min Yu</name>
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<institution>Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
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Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
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</affiliation>
</author>
<author><name sortKey="Akbari, Omid" sort="Akbari, Omid" uniqKey="Akbari O" first="Omid" last="Akbari">Omid Akbari</name>
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<institution>University of Southern California,</institution>
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Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Hagiya, Ashley" sort="Hagiya, Ashley" uniqKey="Hagiya A" first="Ashley" last="Hagiya">Ashley Hagiya</name>
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<institution-id institution-id-type="GRID">grid.42505.36</institution-id>
<institution>Department of Pathology, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
</institution-wrap>
Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Yang, Yongfei" sort="Yang, Yongfei" uniqKey="Yang Y" first="Yongfei" last="Yang">Yongfei Yang</name>
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<institution-id institution-id-type="GRID">grid.42505.36</institution-id>
<institution>Department of Molecular Microbiology and Immunology, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
</institution-wrap>
Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Punj, Vasu" sort="Punj, Vasu" uniqKey="Punj V" first="Vasu" last="Punj">Vasu Punj</name>
<affiliation wicri:level="2"><nlm:aff id="Aff8"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2156 6853</institution-id>
<institution-id institution-id-type="GRID">grid.42505.36</institution-id>
<institution>Department of Pathology, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
</institution-wrap>
Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
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<affiliation wicri:level="2"><nlm:aff id="Aff9"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2156 6853</institution-id>
<institution-id institution-id-type="GRID">grid.42505.36</institution-id>
<institution>Department of Medicine, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
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Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Tang, Liling" sort="Tang, Liling" uniqKey="Tang L" first="Liling" last="Tang">Liling Tang</name>
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<institution>Key Laboratory of Biorheological Science and Technology, Ministry of Education, College of Bioengineering,</institution>
<institution>Chongqing University,</institution>
</institution-wrap>
Chongqing, 400044 China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>Chongqing</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Liang, Chengyu" sort="Liang, Chengyu" uniqKey="Liang C" first="Chengyu" last="Liang">Chengyu Liang</name>
<affiliation wicri:level="2"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2156 6853</institution-id>
<institution-id institution-id-type="GRID">grid.42505.36</institution-id>
<institution>Department of Molecular Microbiology and Immunology, Keck School of Medicine,</institution>
<institution>University of Southern California,</institution>
</institution-wrap>
Los Angeles, CA 90033 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Los Angeles</wicri:cityArea>
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</author>
</analytic>
<series><title level="j">Nature Communications</title>
<idno type="eISSN">2041-1723</idno>
<imprint><date when="2019">2019</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Autophagy maintains homeostasis and is induced upon stress. Yet, its mechanistic interaction with oncogenic signaling remains elusive. Here, we show that in BRAF<sup>V600E</sup>
-melanoma, autophagy is induced by BRAF inhibitor (BRAFi), as part of a transcriptional program coordinating lysosome biogenesis/function, mediated by the TFEB transcription factor. TFEB is phosphorylated and thus inactivated by BRAF<sup>V600E</sup>
via its downstream ERK independently of mTORC1. BRAFi disrupts TFEB phosphorylation, allowing its nuclear translocation, which is synergized by increased phosphorylation/inactivation of the ZKSCAN3 transcriptional repressor by JNK2/p38-MAPK. Blockade of BRAFi-induced transcriptional activation of autophagy-lysosomal function in melanoma xenografts causes enhanced tumor progression, EMT-transdifferentiation, metastatic dissemination, and chemoresistance, which is associated with elevated TGF-β levels and enhanced TGF-β signaling. Inhibition of TGF-β signaling restores tumor differentiation and drug responsiveness in melanoma cells. Thus, the “BRAF-TFEB-autophagy-lysosome” axis represents an intrinsic regulatory pathway in BRAF-mutant melanoma, coupling BRAF signaling with TGF-β signaling to drive tumor progression and chemoresistance.</p>
</div>
</front>
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