Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
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
_version_ 1784710305194967040
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
work_keys_str_mv AT leedonnam targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT sunangela targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT patilsnehas targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT liulijun targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT raoaparnav targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT trentparkert targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT aliareeja targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT liucatherine targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT rauschjessical targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT presuttilaurad targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT kaczorowskiadam targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT schneiderfelix targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT amankulorndukam targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT shudamasahiro targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability
AT duensinganette targetingthetranslationalmachineryingastrointestinalstromaltumorsgistanewtherapeuticvulnerability