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B-cell receptor signaling induces proteasomal degradation of PDCD4 via MEK1/2 and mTORC1 in malignant B cells

B-cell receptor signaling induces proteasomal degradation of PDCD4 via MEK1/2 and mTORC1 in malignant B cells
B-cell receptor signaling induces proteasomal degradation of PDCD4 via MEK1/2 and mTORC1 in malignant B cells
B-cell receptor (BCR) signaling plays a major role in the pathogenesis of B-cell malignancies and is an established target for therapy, including in chronic lymphocytic leukemia cells (CLL), the most common B-cell malignancy. We previously demonstrated that activation of BCR signaling in primary CLL cells downregulated expression of PDCD4, an inhibitor of the translational initiation factor eIF4A and a potential tumor suppressor in lymphoma. Regulation of the PDCD4/eIF4A axis appeared to be important for expression of the MYC oncoprotein as MYC mRNA translation was increased following BCR stimulation and MYC protein induction was repressed by pharmacological inhibition of eIF4A. Here we show that MYC expression is also associated with PDCD4 down-regulation in CLL cells in vivo and characterize the signaling pathways that mediate BCR-induced PDCD4 down-regulation in CLL and lymphoma cells. PDCD4 downregulation was mediated by proteasomal degradation as it was inhibited by proteasome inhibitors in both primary CLL cells and B-lymphoma cell lines. In lymphoma cells, PDCD4 degradation was predominantly dependent on signaling via the AKT pathway. By contrast, in CLL cells, both ERK and AKT pathways contributed to PDCD4 down-regulation and dual inhibition using ibrutinib with either MEK1/2 or mTORC1 inhibition was required to fully reverse PDCD4 down-regulation. Consistent with this, dual inhibition of BTK with MEK1/2 or mTORC1 resulted in the strongest inhibition of BCR-induced MYC expression. This study provides important new insight into the regulation of mRNA translation in B-cell malignancies and a rationale for combinations of kinase inhibitors to target translation control and MYC expression.
0898-6568
Taylor, Joe
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Wilmore, Sarah
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Marriot, Sophie
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Rogers-Broadway, Karly-Rai
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Fell, Rachel
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Minton, Annabel R.
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Branch, Tom
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Ashton-Key, Meg
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Coldwell, Mark
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Stevenson, Freda K.
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Forconi, Francesco
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Steele, Andrew J.
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Packham, Graham
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Yeomans, Alison
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Taylor, Joe
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Wilmore, Sarah
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Marriot, Sophie
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Rogers-Broadway, Karly-Rai
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Fell, Rachel
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Minton, Annabel R.
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Branch, Tom
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Ashton-Key, Meg
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Coldwell, Mark
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Stevenson, Freda K.
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Forconi, Francesco
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Steele, Andrew J.
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Packham, Graham
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Yeomans, Alison
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Taylor, Joe, Wilmore, Sarah, Marriot, Sophie, Rogers-Broadway, Karly-Rai, Fell, Rachel, Minton, Annabel R., Branch, Tom, Ashton-Key, Meg, Coldwell, Mark, Stevenson, Freda K., Forconi, Francesco, Steele, Andrew J., Packham, Graham and Yeomans, Alison (2022) B-cell receptor signaling induces proteasomal degradation of PDCD4 via MEK1/2 and mTORC1 in malignant B cells. Cellular Signalling, 94, [110311]. (doi:10.1016/j.cellsig.2022.110311).

Record type: Article

Abstract

B-cell receptor (BCR) signaling plays a major role in the pathogenesis of B-cell malignancies and is an established target for therapy, including in chronic lymphocytic leukemia cells (CLL), the most common B-cell malignancy. We previously demonstrated that activation of BCR signaling in primary CLL cells downregulated expression of PDCD4, an inhibitor of the translational initiation factor eIF4A and a potential tumor suppressor in lymphoma. Regulation of the PDCD4/eIF4A axis appeared to be important for expression of the MYC oncoprotein as MYC mRNA translation was increased following BCR stimulation and MYC protein induction was repressed by pharmacological inhibition of eIF4A. Here we show that MYC expression is also associated with PDCD4 down-regulation in CLL cells in vivo and characterize the signaling pathways that mediate BCR-induced PDCD4 down-regulation in CLL and lymphoma cells. PDCD4 downregulation was mediated by proteasomal degradation as it was inhibited by proteasome inhibitors in both primary CLL cells and B-lymphoma cell lines. In lymphoma cells, PDCD4 degradation was predominantly dependent on signaling via the AKT pathway. By contrast, in CLL cells, both ERK and AKT pathways contributed to PDCD4 down-regulation and dual inhibition using ibrutinib with either MEK1/2 or mTORC1 inhibition was required to fully reverse PDCD4 down-regulation. Consistent with this, dual inhibition of BTK with MEK1/2 or mTORC1 resulted in the strongest inhibition of BCR-induced MYC expression. This study provides important new insight into the regulation of mRNA translation in B-cell malignancies and a rationale for combinations of kinase inhibitors to target translation control and MYC expression.

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Accepted/In Press date: 13 March 2022
e-pub ahead of print date: 16 March 2022
Published date: 21 March 2022

Identifiers

Local EPrints ID: 488319
URI: http://eprints.soton.ac.uk/id/eprint/488319
ISSN: 0898-6568
PURE UUID: 48152b16-8523-4e49-a899-142bdc56c328
ORCID for Sarah Wilmore: ORCID iD orcid.org/0000-0002-6929-0267
ORCID for Annabel R. Minton: ORCID iD orcid.org/0000-0002-2640-990X
ORCID for Mark Coldwell: ORCID iD orcid.org/0000-0002-6243-3886
ORCID for Freda K. Stevenson: ORCID iD orcid.org/0000-0002-0933-5021
ORCID for Francesco Forconi: ORCID iD orcid.org/0000-0002-2211-1831
ORCID for Andrew J. Steele: ORCID iD orcid.org/0000-0003-0667-1596
ORCID for Graham Packham: ORCID iD orcid.org/0000-0002-9232-5691

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Date deposited: 20 Mar 2024 17:34
Last modified: 21 Mar 2024 02:47

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Contributors

Author: Joe Taylor
Author: Sarah Wilmore ORCID iD
Author: Sophie Marriot
Author: Karly-Rai Rogers-Broadway
Author: Rachel Fell
Author: Annabel R. Minton ORCID iD
Author: Tom Branch
Author: Meg Ashton-Key
Author: Mark Coldwell ORCID iD
Author: Graham Packham ORCID iD
Author: Alison Yeomans

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