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Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability
Although KIT-mutant GISTs can be effectively treated with tyrosine kinase inhibitors (TKIs), many patients develop resistance to imatinib mesylate (IM) as well as the FDA-approved later-line agents sunitinib, regorafenib and ripretinib. Resistance mechanisms mainly involve secondary mutations in the...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9117308/ https://www.ncbi.nlm.nih.gov/pubmed/35585158 http://dx.doi.org/10.1038/s41598-022-12000-2 |
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author | Lee, Donna M. Sun, Angela Patil, Sneha S. Liu, Lijun Rao, Aparna V. Trent, Parker T. Ali, Areej A. Liu, Catherine Rausch, Jessica L. Presutti, Laura D. Kaczorowski, Adam Schneider, Felix Amankulor, Nduka M. Shuda, Masahiro Duensing, Anette |
author_facet | Lee, Donna M. Sun, Angela Patil, Sneha S. Liu, Lijun Rao, Aparna V. Trent, Parker T. Ali, Areej A. Liu, Catherine Rausch, Jessica L. Presutti, Laura D. Kaczorowski, Adam Schneider, Felix Amankulor, Nduka M. Shuda, Masahiro Duensing, Anette |
author_sort | Lee, Donna M. |
collection | PubMed |
description | Although KIT-mutant GISTs can be effectively treated with tyrosine kinase inhibitors (TKIs), many patients develop resistance to imatinib mesylate (IM) as well as the FDA-approved later-line agents sunitinib, regorafenib and ripretinib. Resistance mechanisms mainly involve secondary mutations in the KIT receptor tyrosine kinase gene indicating continued dependency on the KIT signaling pathway. The fact that the type of secondary mutation confers either sensitivity or resistance towards TKIs and the notion that secondary mutations exhibit intra- and intertumoral heterogeneity complicates the optimal choice of treatment in the imatinib-resistant setting. Therefore, new strategies that target KIT independently of its underlying mutations are urgently needed. Homoharringtonine (HHT) is a first-in-class inhibitor of protein biosynthesis and is FDA-approved for the treatment of chronic myeloid leukemia (CML) that is resistant to at least two TKIs. HHT has also shown activity in KIT-mutant mastocytosis models, which are intrinsically resistant to imatinib and most other TKIs. We hypothesized that HHT could be effective in GIST through downregulation of KIT expression and subsequent decrease of KIT activation and downstream signaling. Testing several GIST cell line models, HHT led to a significant reduction in nascent protein synthesis and was highly effective in the nanomolar range in IM-sensitive and IM-resistant GIST cell lines. HHT treatment resulted in a rapid and complete abolishment of KIT expression and activation, while KIT mRNA levels were minimally affected. The response to HHT involved induction of apoptosis as well as cell cycle arrest. The antitumor activity of HHT was confirmed in a GIST xenograft model. Taken together, inhibition of protein biosynthesis is a promising strategy to overcome TKI resistance in GIST. |
format | Online Article Text |
id | pubmed-9117308 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-91173082022-05-20 Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability Lee, Donna M. Sun, Angela Patil, Sneha S. Liu, Lijun Rao, Aparna V. Trent, Parker T. Ali, Areej A. Liu, Catherine Rausch, Jessica L. Presutti, Laura D. Kaczorowski, Adam Schneider, Felix Amankulor, Nduka M. Shuda, Masahiro Duensing, Anette Sci Rep Article Although KIT-mutant GISTs can be effectively treated with tyrosine kinase inhibitors (TKIs), many patients develop resistance to imatinib mesylate (IM) as well as the FDA-approved later-line agents sunitinib, regorafenib and ripretinib. Resistance mechanisms mainly involve secondary mutations in the KIT receptor tyrosine kinase gene indicating continued dependency on the KIT signaling pathway. The fact that the type of secondary mutation confers either sensitivity or resistance towards TKIs and the notion that secondary mutations exhibit intra- and intertumoral heterogeneity complicates the optimal choice of treatment in the imatinib-resistant setting. Therefore, new strategies that target KIT independently of its underlying mutations are urgently needed. Homoharringtonine (HHT) is a first-in-class inhibitor of protein biosynthesis and is FDA-approved for the treatment of chronic myeloid leukemia (CML) that is resistant to at least two TKIs. HHT has also shown activity in KIT-mutant mastocytosis models, which are intrinsically resistant to imatinib and most other TKIs. We hypothesized that HHT could be effective in GIST through downregulation of KIT expression and subsequent decrease of KIT activation and downstream signaling. Testing several GIST cell line models, HHT led to a significant reduction in nascent protein synthesis and was highly effective in the nanomolar range in IM-sensitive and IM-resistant GIST cell lines. HHT treatment resulted in a rapid and complete abolishment of KIT expression and activation, while KIT mRNA levels were minimally affected. The response to HHT involved induction of apoptosis as well as cell cycle arrest. The antitumor activity of HHT was confirmed in a GIST xenograft model. Taken together, inhibition of protein biosynthesis is a promising strategy to overcome TKI resistance in GIST. Nature Publishing Group UK 2022-05-18 /pmc/articles/PMC9117308/ /pubmed/35585158 http://dx.doi.org/10.1038/s41598-022-12000-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Lee, Donna M. Sun, Angela Patil, Sneha S. Liu, Lijun Rao, Aparna V. Trent, Parker T. Ali, Areej A. Liu, Catherine Rausch, Jessica L. Presutti, Laura D. Kaczorowski, Adam Schneider, Felix Amankulor, Nduka M. Shuda, Masahiro Duensing, Anette Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability |
title | Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability |
title_full | Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability |
title_fullStr | Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability |
title_full_unstemmed | Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability |
title_short | Targeting the translational machinery in gastrointestinal stromal tumors (GIST): a new therapeutic vulnerability |
title_sort | targeting the translational machinery in gastrointestinal stromal tumors (gist): a new therapeutic vulnerability |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9117308/ https://www.ncbi.nlm.nih.gov/pubmed/35585158 http://dx.doi.org/10.1038/s41598-022-12000-2 |
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