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Limited inhibition of multiple nodes in a driver network blocks metastasis

Metastasis suppression by high-dose, multi-drug targeting is unsuccessful due to network heterogeneity and compensatory network activation. Here, we show that targeting driver network signaling capacity by limited inhibition of core pathways is a more effective anti-metastatic strategy. This princip...

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Autores principales: Yesilkanal, Ali Ekrem, Yang, Dongbo, Valdespino, Andrea, Tiwari, Payal, Sabino, Alan U, Nguyen, Long Chi, Lee, Jiyoung, Xie, Xiao-He, Sun, Siqi, Dann, Christopher, Robinson-Mailman, Lydia, Steinberg, Ethan, Stuhlmiller, Timothy, Frankenberger, Casey, Goldsmith, Elizabeth, Johnson, Gary L, Ramos, Alexandre F, Rosner, Marsha R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8128439/
https://www.ncbi.nlm.nih.gov/pubmed/33973518
http://dx.doi.org/10.7554/eLife.59696
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author Yesilkanal, Ali Ekrem
Yang, Dongbo
Valdespino, Andrea
Tiwari, Payal
Sabino, Alan U
Nguyen, Long Chi
Lee, Jiyoung
Xie, Xiao-He
Sun, Siqi
Dann, Christopher
Robinson-Mailman, Lydia
Steinberg, Ethan
Stuhlmiller, Timothy
Frankenberger, Casey
Goldsmith, Elizabeth
Johnson, Gary L
Ramos, Alexandre F
Rosner, Marsha R
author_facet Yesilkanal, Ali Ekrem
Yang, Dongbo
Valdespino, Andrea
Tiwari, Payal
Sabino, Alan U
Nguyen, Long Chi
Lee, Jiyoung
Xie, Xiao-He
Sun, Siqi
Dann, Christopher
Robinson-Mailman, Lydia
Steinberg, Ethan
Stuhlmiller, Timothy
Frankenberger, Casey
Goldsmith, Elizabeth
Johnson, Gary L
Ramos, Alexandre F
Rosner, Marsha R
author_sort Yesilkanal, Ali Ekrem
collection PubMed
description Metastasis suppression by high-dose, multi-drug targeting is unsuccessful due to network heterogeneity and compensatory network activation. Here, we show that targeting driver network signaling capacity by limited inhibition of core pathways is a more effective anti-metastatic strategy. This principle underlies the action of a physiological metastasis suppressor, Raf Kinase Inhibitory Protein (RKIP), that moderately decreases stress-regulated MAP kinase network activity, reducing output to transcription factors such as pro-metastastic BACH1 and motility-related target genes. We developed a low-dose four-drug mimic that blocks metastatic colonization in mouse breast cancer models and increases survival. Experiments and network flow modeling show limited inhibition of multiple pathways is required to overcome variation in MAPK network topology and suppress signaling output across heterogeneous tumor cells. Restricting inhibition of individual kinases dissipates surplus signal, preventing threshold activation of compensatory kinase networks. This low-dose multi-drug approach to decrease signaling capacity of driver networks represents a transformative, clinically relevant strategy for anti-metastatic treatment.
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spelling pubmed-81284392021-05-19 Limited inhibition of multiple nodes in a driver network blocks metastasis Yesilkanal, Ali Ekrem Yang, Dongbo Valdespino, Andrea Tiwari, Payal Sabino, Alan U Nguyen, Long Chi Lee, Jiyoung Xie, Xiao-He Sun, Siqi Dann, Christopher Robinson-Mailman, Lydia Steinberg, Ethan Stuhlmiller, Timothy Frankenberger, Casey Goldsmith, Elizabeth Johnson, Gary L Ramos, Alexandre F Rosner, Marsha R eLife Cancer Biology Metastasis suppression by high-dose, multi-drug targeting is unsuccessful due to network heterogeneity and compensatory network activation. Here, we show that targeting driver network signaling capacity by limited inhibition of core pathways is a more effective anti-metastatic strategy. This principle underlies the action of a physiological metastasis suppressor, Raf Kinase Inhibitory Protein (RKIP), that moderately decreases stress-regulated MAP kinase network activity, reducing output to transcription factors such as pro-metastastic BACH1 and motility-related target genes. We developed a low-dose four-drug mimic that blocks metastatic colonization in mouse breast cancer models and increases survival. Experiments and network flow modeling show limited inhibition of multiple pathways is required to overcome variation in MAPK network topology and suppress signaling output across heterogeneous tumor cells. Restricting inhibition of individual kinases dissipates surplus signal, preventing threshold activation of compensatory kinase networks. This low-dose multi-drug approach to decrease signaling capacity of driver networks represents a transformative, clinically relevant strategy for anti-metastatic treatment. eLife Sciences Publications, Ltd 2021-05-11 /pmc/articles/PMC8128439/ /pubmed/33973518 http://dx.doi.org/10.7554/eLife.59696 Text en © 2021, Yesilkanal et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cancer Biology
Yesilkanal, Ali Ekrem
Yang, Dongbo
Valdespino, Andrea
Tiwari, Payal
Sabino, Alan U
Nguyen, Long Chi
Lee, Jiyoung
Xie, Xiao-He
Sun, Siqi
Dann, Christopher
Robinson-Mailman, Lydia
Steinberg, Ethan
Stuhlmiller, Timothy
Frankenberger, Casey
Goldsmith, Elizabeth
Johnson, Gary L
Ramos, Alexandre F
Rosner, Marsha R
Limited inhibition of multiple nodes in a driver network blocks metastasis
title Limited inhibition of multiple nodes in a driver network blocks metastasis
title_full Limited inhibition of multiple nodes in a driver network blocks metastasis
title_fullStr Limited inhibition of multiple nodes in a driver network blocks metastasis
title_full_unstemmed Limited inhibition of multiple nodes in a driver network blocks metastasis
title_short Limited inhibition of multiple nodes in a driver network blocks metastasis
title_sort limited inhibition of multiple nodes in a driver network blocks metastasis
topic Cancer Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8128439/
https://www.ncbi.nlm.nih.gov/pubmed/33973518
http://dx.doi.org/10.7554/eLife.59696
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