A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity

Cancer metabolism plays an essential role in therapeutic resistance, where significant inter- and intra-tumoral heterogeneity exists. Hypoxia is a prominent driver of metabolic rewiring behaviors and drug responses. Recapitulating the hypoxic landscape in the tumor microenvironment thus offers uniqu...

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Main Authors: Jeong Min Oh, Tianze Guo, Hydari Masuma Begum, Saci-Elodie Marty, Liang Sha, Cem Kilic, Hao Zhou, Yali Dou, Keyue Shen
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-06-01
Series:Bioactive Materials
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Online Access:http://www.sciencedirect.com/science/article/pii/S2452199X25000866
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author Jeong Min Oh
Tianze Guo
Hydari Masuma Begum
Saci-Elodie Marty
Liang Sha
Cem Kilic
Hao Zhou
Yali Dou
Keyue Shen
author_facet Jeong Min Oh
Tianze Guo
Hydari Masuma Begum
Saci-Elodie Marty
Liang Sha
Cem Kilic
Hao Zhou
Yali Dou
Keyue Shen
author_sort Jeong Min Oh
collection DOAJ
description Cancer metabolism plays an essential role in therapeutic resistance, where significant inter- and intra-tumoral heterogeneity exists. Hypoxia is a prominent driver of metabolic rewiring behaviors and drug responses. Recapitulating the hypoxic landscape in the tumor microenvironment thus offers unique insights into heterogeneity in metabolic rewiring and therapeutic responses, to inform better treatment strategies. There remains a lack of scalable tools that can readily interface with imaging platforms and resolve the heterogeneous behaviors in hypoxia-associated metabolic rewiring. Here we present a micro-metabolic rewiring (μMeRe) assay that provides the scalability and resolution needed to characterize the metabolic rewiring behaviors of different cancer cells in the context of hypoxic solid tumors. Our assay generates hypoxia through cellular metabolism without external gas controls, enabling the characterization of cell-specific intrinsic ability to drive hypoxia and undergo metabolic rewiring. We further developed quantitative metrics that measure the metabolic plasticity through phenotypes and gene expression. As a proof-of-concept, we evaluated the efficacy of a metabolism-targeting strategy in mitigating hypoxia- and metabolic rewiring-induced chemotherapeutic resistance. Our study and the scalable platform thus lay the foundation for designing more effective cancer treatments tailored toward specific metabolic rewiring behaviors.
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spelling doaj-art-c856b68bb2b044748d47b4fa08e2abeb2025-08-20T03:14:54ZengKeAi Communications Co., Ltd.Bioactive Materials2452-199X2025-06-014849350910.1016/j.bioactmat.2025.02.030A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneityJeong Min Oh0Tianze Guo1Hydari Masuma Begum2Saci-Elodie Marty3Liang Sha4Cem Kilic5Hao Zhou6Yali Dou7Keyue Shen8Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USADepartment of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, 90033, USADepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USADepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USADepartment of Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, 90033, USA; Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA, 90033, USADepartment of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USA; Norris Comprehensive Cancer Center, University of Southern California, Los Angeles, CA, 90033, USA; USC Stem Cell, University of Southern California, Los Angeles, CA, 90033, USA; Corresponding author. Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, 90089, USA.Cancer metabolism plays an essential role in therapeutic resistance, where significant inter- and intra-tumoral heterogeneity exists. Hypoxia is a prominent driver of metabolic rewiring behaviors and drug responses. Recapitulating the hypoxic landscape in the tumor microenvironment thus offers unique insights into heterogeneity in metabolic rewiring and therapeutic responses, to inform better treatment strategies. There remains a lack of scalable tools that can readily interface with imaging platforms and resolve the heterogeneous behaviors in hypoxia-associated metabolic rewiring. Here we present a micro-metabolic rewiring (μMeRe) assay that provides the scalability and resolution needed to characterize the metabolic rewiring behaviors of different cancer cells in the context of hypoxic solid tumors. Our assay generates hypoxia through cellular metabolism without external gas controls, enabling the characterization of cell-specific intrinsic ability to drive hypoxia and undergo metabolic rewiring. We further developed quantitative metrics that measure the metabolic plasticity through phenotypes and gene expression. As a proof-of-concept, we evaluated the efficacy of a metabolism-targeting strategy in mitigating hypoxia- and metabolic rewiring-induced chemotherapeutic resistance. Our study and the scalable platform thus lay the foundation for designing more effective cancer treatments tailored toward specific metabolic rewiring behaviors.http://www.sciencedirect.com/science/article/pii/S2452199X25000866Metabolic rewiringHypoxiaTumor heterogeneityMetabolism-targeting therapyTumor microenvironment
spellingShingle Jeong Min Oh
Tianze Guo
Hydari Masuma Begum
Saci-Elodie Marty
Liang Sha
Cem Kilic
Hao Zhou
Yali Dou
Keyue Shen
A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity
Bioactive Materials
Metabolic rewiring
Hypoxia
Tumor heterogeneity
Metabolism-targeting therapy
Tumor microenvironment
title A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity
title_full A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity
title_fullStr A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity
title_full_unstemmed A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity
title_short A micro-metabolic rewiring assay for assessing hypoxia-associated cancer metabolic heterogeneity
title_sort micro metabolic rewiring assay for assessing hypoxia associated cancer metabolic heterogeneity
topic Metabolic rewiring
Hypoxia
Tumor heterogeneity
Metabolism-targeting therapy
Tumor microenvironment
url http://www.sciencedirect.com/science/article/pii/S2452199X25000866
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