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Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors

Mitogen-activated protein kinase (MAPK) pathway dysregulation is implicated in >30% of all cancers, rationalizing the development of RAF, MEK and ERK inhibitors. While BRAF and MEK inhibitors improve BRAF mutant melanoma patient outcomes, these inhibitors had limited success in other MAPK dysregu...

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Autores principales: Merchant, Mark, Moffat, John, Schaefer, Gabriele, Chan, Jocelyn, Wang, Xi, Orr, Christine, Cheng, Jason, Hunsaker, Thomas, Shao, Lily, Wang, Stephanie J., Wagle, Marie-Claire, Lin, Eva, Haverty, Peter M., Shahidi-Latham, Sheerin, Ngu, Hai, Solon, Margaret, Eastham-Anderson, Jeffrey, Koeppen, Hartmut, Huang, Shih-Min A., Schwarz, Jacob, Belvin, Marcia, Kirouac, Daniel, Junttila, Melissa R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5628883/
https://www.ncbi.nlm.nih.gov/pubmed/28982154
http://dx.doi.org/10.1371/journal.pone.0185862
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author Merchant, Mark
Moffat, John
Schaefer, Gabriele
Chan, Jocelyn
Wang, Xi
Orr, Christine
Cheng, Jason
Hunsaker, Thomas
Shao, Lily
Wang, Stephanie J.
Wagle, Marie-Claire
Lin, Eva
Haverty, Peter M.
Shahidi-Latham, Sheerin
Ngu, Hai
Solon, Margaret
Eastham-Anderson, Jeffrey
Koeppen, Hartmut
Huang, Shih-Min A.
Schwarz, Jacob
Belvin, Marcia
Kirouac, Daniel
Junttila, Melissa R.
author_facet Merchant, Mark
Moffat, John
Schaefer, Gabriele
Chan, Jocelyn
Wang, Xi
Orr, Christine
Cheng, Jason
Hunsaker, Thomas
Shao, Lily
Wang, Stephanie J.
Wagle, Marie-Claire
Lin, Eva
Haverty, Peter M.
Shahidi-Latham, Sheerin
Ngu, Hai
Solon, Margaret
Eastham-Anderson, Jeffrey
Koeppen, Hartmut
Huang, Shih-Min A.
Schwarz, Jacob
Belvin, Marcia
Kirouac, Daniel
Junttila, Melissa R.
author_sort Merchant, Mark
collection PubMed
description Mitogen-activated protein kinase (MAPK) pathway dysregulation is implicated in >30% of all cancers, rationalizing the development of RAF, MEK and ERK inhibitors. While BRAF and MEK inhibitors improve BRAF mutant melanoma patient outcomes, these inhibitors had limited success in other MAPK dysregulated tumors, with insufficient pathway suppression and likely pathway reactivation. In this study we show that inhibition of either MEK or ERK alone only transiently inhibits the MAPK pathway due to feedback reactivation. Simultaneous targeting of both MEK and ERK nodes results in deeper and more durable suppression of MAPK signaling that is not achievable with any dose of single agent, in tumors where feedback reactivation occurs. Strikingly, combined MEK and ERK inhibition is synergistic in RAS mutant models but only additive in BRAF mutant models where the RAF complex is dissociated from RAS and thus feedback productivity is disabled. We discovered that pathway reactivation in RAS mutant models occurs at the level of CRAF with combination treatment resulting in a markedly more active pool of CRAF. However, distinct from single node targeting, combining MEK and ERK inhibitor treatment effectively blocks the downstream signaling as assessed by transcriptional signatures and phospho-p90RSK. Importantly, these data reveal that MAPK pathway inhibitors whose activity is attenuated due to feedback reactivation can be rescued with sufficient inhibition by using a combination of MEK and ERK inhibitors. The MEK and ERK combination significantly suppresses MAPK pathway output and tumor growth in vivo to a greater extent than the maximum tolerated doses of single agents, and results in improved anti-tumor activity in multiple xenografts as well as in two Kras mutant genetically engineered mouse (GEM) models. Collectively, these data demonstrate that combined MEK and ERK inhibition is functionally unique, yielding greater than additive anti-tumor effects and elucidates a highly effective combination strategy in MAPK-dependent cancer, such as KRAS mutant tumors.
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spelling pubmed-56288832017-10-20 Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors Merchant, Mark Moffat, John Schaefer, Gabriele Chan, Jocelyn Wang, Xi Orr, Christine Cheng, Jason Hunsaker, Thomas Shao, Lily Wang, Stephanie J. Wagle, Marie-Claire Lin, Eva Haverty, Peter M. Shahidi-Latham, Sheerin Ngu, Hai Solon, Margaret Eastham-Anderson, Jeffrey Koeppen, Hartmut Huang, Shih-Min A. Schwarz, Jacob Belvin, Marcia Kirouac, Daniel Junttila, Melissa R. PLoS One Research Article Mitogen-activated protein kinase (MAPK) pathway dysregulation is implicated in >30% of all cancers, rationalizing the development of RAF, MEK and ERK inhibitors. While BRAF and MEK inhibitors improve BRAF mutant melanoma patient outcomes, these inhibitors had limited success in other MAPK dysregulated tumors, with insufficient pathway suppression and likely pathway reactivation. In this study we show that inhibition of either MEK or ERK alone only transiently inhibits the MAPK pathway due to feedback reactivation. Simultaneous targeting of both MEK and ERK nodes results in deeper and more durable suppression of MAPK signaling that is not achievable with any dose of single agent, in tumors where feedback reactivation occurs. Strikingly, combined MEK and ERK inhibition is synergistic in RAS mutant models but only additive in BRAF mutant models where the RAF complex is dissociated from RAS and thus feedback productivity is disabled. We discovered that pathway reactivation in RAS mutant models occurs at the level of CRAF with combination treatment resulting in a markedly more active pool of CRAF. However, distinct from single node targeting, combining MEK and ERK inhibitor treatment effectively blocks the downstream signaling as assessed by transcriptional signatures and phospho-p90RSK. Importantly, these data reveal that MAPK pathway inhibitors whose activity is attenuated due to feedback reactivation can be rescued with sufficient inhibition by using a combination of MEK and ERK inhibitors. The MEK and ERK combination significantly suppresses MAPK pathway output and tumor growth in vivo to a greater extent than the maximum tolerated doses of single agents, and results in improved anti-tumor activity in multiple xenografts as well as in two Kras mutant genetically engineered mouse (GEM) models. Collectively, these data demonstrate that combined MEK and ERK inhibition is functionally unique, yielding greater than additive anti-tumor effects and elucidates a highly effective combination strategy in MAPK-dependent cancer, such as KRAS mutant tumors. Public Library of Science 2017-10-05 /pmc/articles/PMC5628883/ /pubmed/28982154 http://dx.doi.org/10.1371/journal.pone.0185862 Text en © 2017 Merchant et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Merchant, Mark
Moffat, John
Schaefer, Gabriele
Chan, Jocelyn
Wang, Xi
Orr, Christine
Cheng, Jason
Hunsaker, Thomas
Shao, Lily
Wang, Stephanie J.
Wagle, Marie-Claire
Lin, Eva
Haverty, Peter M.
Shahidi-Latham, Sheerin
Ngu, Hai
Solon, Margaret
Eastham-Anderson, Jeffrey
Koeppen, Hartmut
Huang, Shih-Min A.
Schwarz, Jacob
Belvin, Marcia
Kirouac, Daniel
Junttila, Melissa R.
Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors
title Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors
title_full Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors
title_fullStr Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors
title_full_unstemmed Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors
title_short Combined MEK and ERK inhibition overcomes therapy-mediated pathway reactivation in RAS mutant tumors
title_sort combined mek and erk inhibition overcomes therapy-mediated pathway reactivation in ras mutant tumors
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5628883/
https://www.ncbi.nlm.nih.gov/pubmed/28982154
http://dx.doi.org/10.1371/journal.pone.0185862
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