Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1783694112202948608 |
---|---|
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. |
format | Online Article Text |
id | pubmed-8128439 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT yesilkanalaliekrem limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT yangdongbo limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT valdespinoandrea limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT tiwaripayal limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT sabinoalanu limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT nguyenlongchi limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT leejiyoung limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT xiexiaohe limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT sunsiqi limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT dannchristopher limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT robinsonmailmanlydia limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT steinbergethan limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT stuhlmillertimothy limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT frankenbergercasey limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT goldsmithelizabeth limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT johnsongaryl limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT ramosalexandref limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis AT rosnermarshar limitedinhibitionofmultiplenodesinadrivernetworkblocksmetastasis |