The insulin and IGF signaling pathway sustains breast cancer stem cells by IRS2/PI3K-mediated regulation of MYC

Despite the strong association of the insulin/insulin-like growth factor (IGF) signaling (IIS) pathway with tumor initiation, recurrence, and metastasis, the mechanism by which this pathway regulates cancer progression is not well understood. Here, we report that IIS supports breast cancer stem cell...

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Published inCell reports (Cambridge) Vol. 41; no. 10; p. 111759
Main Authors Lee, Ji-Sun, Lero, Michael W., Mercado-Matos, Jose, Zhu, Sha, Jo, Minjeong, Tocheny, Claire E., Morgan, Jennifer S., Shaw, Leslie M.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 06.12.2022
Subjects
breast cancer
cancer stem cell
CSC
IGF
Insulin
insulin receptor substrate
insulin-like growth factor
IRS2
MYC
Neoplasms
Neoplastic Stem Cells
Phosphatidylinositol 3-Kinase
Phosphatidylinositol 3-Kinases
PI3K
Signal Transduction
Somatomedins
CSC
insulin
cancer stem cell
PI3K
MYC
CP: Cancer
IGF
breast cancer
insulin-like growth factor
IRS2
insulin receptor substrate
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Abstract Despite the strong association of the insulin/insulin-like growth factor (IGF) signaling (IIS) pathway with tumor initiation, recurrence, and metastasis, the mechanism by which this pathway regulates cancer progression is not well understood. Here, we report that IIS supports breast cancer stem cell (CSC) self-renewal in an IRS2-phosphatidylinositol 3-kinase (PI3K)-dependent manner that involves the activation and stabilization of MYC. IRS2-PI3K signaling enhances MYC expression through the inhibition of GSK3β activity and suppression of MYC phosphorylation on threonine 58, thus reducing proteasome-mediated degradation of MYC and sustaining active pS62-MYC function. A stable T58A-Myc mutant rescues CSC function in Irs2−/− cells, supporting the role of this MYC stabilization in IRS2-dependent CSC regulation. These findings establish a mechanistic connection between the IIS pathway and MYC and highlight a role for IRS2-dependent signaling in breast cancer progression. [Display omitted] •Insulin/IGF signaling (IIS) supports breast cancer stem cell (CSC) self-renewal•IIS regulates stemness in an IRS2- and PI3K-dependent manner•IRS2/PI3K signaling activates and stabilizes MYC to enhance CSC function Lee et al. show that the insulin/IGF signaling pathway regulates breast cancer stem cell (CSC) function in an IRS2- and PI3K-dependent manner. This regulation involves the activation and stabilization of MYC, as shown by the ability of a stable T58A-MYC mutant to restore CSC function in IRS2−/− cells.
AbstractList Despite the strong association of the insulin/insulin-like growth factor (IGF) signaling (IIS) pathway with tumor initiation, recurrence, and metastasis, the mechanism by which this pathway regulates cancer progression is not well understood. Here, we report that IIS supports breast cancer stem cell (CSC) self-renewal in an IRS2-phosphatidylinositol 3-kinase (PI3K)-dependent manner that involves the activation and stabilization of MYC. IRS2-PI3K signaling enhances MYC expression through the inhibition of GSK3β activity and suppression of MYC phosphorylation on threonine 58, thus reducing proteasome-mediated degradation of MYC and sustaining active pS62-MYC function. A stable T58A-Myc mutant rescues CSC function in Irs2 −/− cells, supporting the role of this MYC stabilization in IRS2-dependent CSC regulation. These findings establish a mechanistic connection between the IIS pathway and MYC and highlight a role for IRS2-dependent signaling in breast cancer progression. Lee et al. show that the insulin/IGF signaling pathway regulates breast cancer stem cell (CSC) function in an IRS2- and PI3K-dependent manner. This regulation involves the activation and stabilization of MYC, as shown by the ability of a stable T58A-MYC mutant to restore CSC function in IRS2 −/− cells.
Despite the strong association of the insulin/insulin-like growth factor (IGF) signaling (IIS) pathway with tumor initiation, recurrence, and metastasis, the mechanism by which this pathway regulates cancer progression is not well understood. Here, we report that IIS supports breast cancer stem cell (CSC) self-renewal in an IRS2-phosphatidylinositol 3-kinase (PI3K)-dependent manner that involves the activation and stabilization of MYC. IRS2-PI3K signaling enhances MYC expression through the inhibition of GSK3β activity and suppression of MYC phosphorylation on threonine 58, thus reducing proteasome-mediated degradation of MYC and sustaining active pS62-MYC function. A stable T58A-Myc mutant rescues CSC function in Irs2 cells, supporting the role of this MYC stabilization in IRS2-dependent CSC regulation. These findings establish a mechanistic connection between the IIS pathway and MYC and highlight a role for IRS2-dependent signaling in breast cancer progression.
Despite the strong association of the insulin/insulin-like growth factor (IGF) signaling (IIS) pathway with tumor initiation, recurrence, and metastasis, the mechanism by which this pathway regulates cancer progression is not well understood. Here, we report that IIS supports breast cancer stem cell (CSC) self-renewal in an IRS2-phosphatidylinositol 3-kinase (PI3K)-dependent manner that involves the activation and stabilization of MYC. IRS2-PI3K signaling enhances MYC expression through the inhibition of GSK3β activity and suppression of MYC phosphorylation on threonine 58, thus reducing proteasome-mediated degradation of MYC and sustaining active pS62-MYC function. A stable T58A-Myc mutant rescues CSC function in Irs2−/− cells, supporting the role of this MYC stabilization in IRS2-dependent CSC regulation. These findings establish a mechanistic connection between the IIS pathway and MYC and highlight a role for IRS2-dependent signaling in breast cancer progression. [Display omitted] •Insulin/IGF signaling (IIS) supports breast cancer stem cell (CSC) self-renewal•IIS regulates stemness in an IRS2- and PI3K-dependent manner•IRS2/PI3K signaling activates and stabilizes MYC to enhance CSC function Lee et al. show that the insulin/IGF signaling pathway regulates breast cancer stem cell (CSC) function in an IRS2- and PI3K-dependent manner. This regulation involves the activation and stabilization of MYC, as shown by the ability of a stable T58A-MYC mutant to restore CSC function in IRS2−/− cells.
ArticleNumber 111759
Author Mercado-Matos, Jose
Lee, Ji-Sun
Morgan, Jennifer S.
Zhu, Sha
Lero, Michael W.
Jo, Minjeong
Tocheny, Claire E.
Shaw, Leslie M.
AuthorAffiliation 1 Department of Molecular, Cell & Cancer Biology, University of Massachusetts Chan Medical School, 364 Plantation St., Worcester, MA 01605, USA
2 Lead contact
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Issue 10
Keywords CSC
insulin
cancer stem cell
PI3K
MYC
CP: Cancer
IGF
breast cancer
insulin-like growth factor
IRS2
insulin receptor substrate
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.
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AUTHOR CONTRIBUTIONS
J.-S.L. and L.M.S. were involved in the conception and design of the project and wrote the manuscript; J.-S.L., M.W.L., J.M.-M., S.Z., M.J., C.E.T., and J.S.M. were involved with the development of methodology and the acquisition and analysis of data. All authors reviewed and approved the final version of the manuscript.
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Snippet Despite the strong association of the insulin/insulin-like growth factor (IGF) signaling (IIS) pathway with tumor initiation, recurrence, and metastasis, the...
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SubjectTerms breast cancer
cancer stem cell
CSC
IGF
Insulin
insulin receptor substrate
insulin-like growth factor
IRS2
MYC
Neoplasms
Neoplastic Stem Cells
Phosphatidylinositol 3-Kinase
Phosphatidylinositol 3-Kinases
PI3K
Signal Transduction
Somatomedins
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Title The insulin and IGF signaling pathway sustains breast cancer stem cells by IRS2/PI3K-mediated regulation of MYC
URI https://dx.doi.org/10.1016/j.celrep.2022.111759
https://www.ncbi.nlm.nih.gov/pubmed/36476848
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Volume 41
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