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Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling

Multiple myeloma is an incurable plasma cell malignancy with only a 53% 5-year survival rate. There is a critical need to find new multiple myeloma vulnerabilities and therapeutic avenues. Herein, we identified and explored a novel multiple myeloma target: the fatty acid binding protein (FABP) famil...

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Autores principales: Farrell, Mariah, Fairfield, Heather, Karam, Michelle, D'Amico, Anastasia, Murphy, Connor S, Falank, Carolyne, Pistofidi, Romanos Sklavenitis, Cao, Amanda, Marinac, Catherine R, Dragon, Julie A, McGuinness, Lauren, Gartner, Carlos G, Iorio, Reagan Di, Jachimowicz, Edward, DeMambro, Victoria, Vary, Calvin, Reagan, Michaela R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9995119/
https://www.ncbi.nlm.nih.gov/pubmed/36880649
http://dx.doi.org/10.7554/eLife.81184
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author Farrell, Mariah
Fairfield, Heather
Karam, Michelle
D'Amico, Anastasia
Murphy, Connor S
Falank, Carolyne
Pistofidi, Romanos Sklavenitis
Cao, Amanda
Marinac, Catherine R
Dragon, Julie A
McGuinness, Lauren
Gartner, Carlos G
Iorio, Reagan Di
Jachimowicz, Edward
DeMambro, Victoria
Vary, Calvin
Reagan, Michaela R
author_facet Farrell, Mariah
Fairfield, Heather
Karam, Michelle
D'Amico, Anastasia
Murphy, Connor S
Falank, Carolyne
Pistofidi, Romanos Sklavenitis
Cao, Amanda
Marinac, Catherine R
Dragon, Julie A
McGuinness, Lauren
Gartner, Carlos G
Iorio, Reagan Di
Jachimowicz, Edward
DeMambro, Victoria
Vary, Calvin
Reagan, Michaela R
author_sort Farrell, Mariah
collection PubMed
description Multiple myeloma is an incurable plasma cell malignancy with only a 53% 5-year survival rate. There is a critical need to find new multiple myeloma vulnerabilities and therapeutic avenues. Herein, we identified and explored a novel multiple myeloma target: the fatty acid binding protein (FABP) family. In our work, myeloma cells were treated with FABP inhibitors (BMS3094013 and SBFI-26) and examined in vivo and in vitro for cell cycle state, proliferation, apoptosis, mitochondrial membrane potential, cellular metabolism (oxygen consumption rates and fatty acid oxidation), and DNA methylation properties. Myeloma cell responses to BMS309403, SBFI-26, or both, were also assessed with RNA sequencing (RNA-Seq) and proteomic analysis, and confirmed with western blotting and qRT-PCR. Myeloma cell dependency on FABPs was assessed using the Cancer Dependency Map (DepMap). Finally, MM patient datasets (CoMMpass and GEO) were mined for FABP expression correlations with clinical outcomes. We found that myeloma cells treated with FABPi or with FABP5 knockout (generated via CRISPR/Cas9 editing) exhibited diminished proliferation, increased apoptosis, and metabolic changes in vitro. FABPi had mixed results in vivo, in two pre-clinical MM mouse models, suggesting optimization of in vivo delivery, dosing, or type of FABP inhibitors will be needed before clinical applicability. FABPi negatively impacted mitochondrial respiration and reduced expression of MYC and other key signaling pathways in MM cells in vitro. Clinical data demonstrated worse overall and progression-free survival in patients with high FABP5 expression in tumor cells. Overall, this study establishes the FABP family as a potentially new target in multiple myeloma. In MM cells, FABPs have a multitude of actions and cellular roles that result in the support of myeloma progression. Further research into the FABP family in MM is warrented, especially into the effective translation of targeting these in vivo.
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spelling pubmed-99951192023-03-09 Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling Farrell, Mariah Fairfield, Heather Karam, Michelle D'Amico, Anastasia Murphy, Connor S Falank, Carolyne Pistofidi, Romanos Sklavenitis Cao, Amanda Marinac, Catherine R Dragon, Julie A McGuinness, Lauren Gartner, Carlos G Iorio, Reagan Di Jachimowicz, Edward DeMambro, Victoria Vary, Calvin Reagan, Michaela R eLife Cancer Biology Multiple myeloma is an incurable plasma cell malignancy with only a 53% 5-year survival rate. There is a critical need to find new multiple myeloma vulnerabilities and therapeutic avenues. Herein, we identified and explored a novel multiple myeloma target: the fatty acid binding protein (FABP) family. In our work, myeloma cells were treated with FABP inhibitors (BMS3094013 and SBFI-26) and examined in vivo and in vitro for cell cycle state, proliferation, apoptosis, mitochondrial membrane potential, cellular metabolism (oxygen consumption rates and fatty acid oxidation), and DNA methylation properties. Myeloma cell responses to BMS309403, SBFI-26, or both, were also assessed with RNA sequencing (RNA-Seq) and proteomic analysis, and confirmed with western blotting and qRT-PCR. Myeloma cell dependency on FABPs was assessed using the Cancer Dependency Map (DepMap). Finally, MM patient datasets (CoMMpass and GEO) were mined for FABP expression correlations with clinical outcomes. We found that myeloma cells treated with FABPi or with FABP5 knockout (generated via CRISPR/Cas9 editing) exhibited diminished proliferation, increased apoptosis, and metabolic changes in vitro. FABPi had mixed results in vivo, in two pre-clinical MM mouse models, suggesting optimization of in vivo delivery, dosing, or type of FABP inhibitors will be needed before clinical applicability. FABPi negatively impacted mitochondrial respiration and reduced expression of MYC and other key signaling pathways in MM cells in vitro. Clinical data demonstrated worse overall and progression-free survival in patients with high FABP5 expression in tumor cells. Overall, this study establishes the FABP family as a potentially new target in multiple myeloma. In MM cells, FABPs have a multitude of actions and cellular roles that result in the support of myeloma progression. Further research into the FABP family in MM is warrented, especially into the effective translation of targeting these in vivo. eLife Sciences Publications, Ltd 2023-03-07 /pmc/articles/PMC9995119/ /pubmed/36880649 http://dx.doi.org/10.7554/eLife.81184 Text en © 2023, Farrell 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
Farrell, Mariah
Fairfield, Heather
Karam, Michelle
D'Amico, Anastasia
Murphy, Connor S
Falank, Carolyne
Pistofidi, Romanos Sklavenitis
Cao, Amanda
Marinac, Catherine R
Dragon, Julie A
McGuinness, Lauren
Gartner, Carlos G
Iorio, Reagan Di
Jachimowicz, Edward
DeMambro, Victoria
Vary, Calvin
Reagan, Michaela R
Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling
title Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling
title_full Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling
title_fullStr Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling
title_full_unstemmed Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling
title_short Targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and MYC signaling
title_sort targeting the fatty acid binding proteins disrupts multiple myeloma cell cycle progression and myc signaling
topic Cancer Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9995119/
https://www.ncbi.nlm.nih.gov/pubmed/36880649
http://dx.doi.org/10.7554/eLife.81184
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