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USP25 promotes pathological HIF-1-driven metabolic reprogramming and is a potential therapeutic target in pancreatic cancer

USP25 promotes pathological HIF-1-driven metabolic reprogramming and is a potential therapeutic target in pancreatic cancer
USP25 promotes pathological HIF-1-driven metabolic reprogramming and is a potential therapeutic target in pancreatic cancer

Deubiquitylating enzymes (DUBs) play an essential role in targeted protein degradation and represent an emerging therapeutic paradigm in cancer. However, their therapeutic potential in pancreatic ductal adenocarcinoma (PDAC) has not been explored. Here, we develop a DUB discovery pipeline, combining activity-based proteomics with a loss-of-function genetic screen in patient-derived PDAC organoids and murine genetic models. This approach identifies USP25 as a master regulator of PDAC growth and maintenance. Genetic and pharmacological USP25 inhibition results in potent growth impairment in PDAC organoids, while normal pancreatic organoids are insensitive, and causes dramatic regression of patient-derived xenografts. Mechanistically, USP25 deubiquitinates and stabilizes the HIF-1α transcription factor. PDAC is characterized by a severely hypoxic microenvironment, and USP25 depletion abrogates HIF-1α transcriptional activity and impairs glycolysis, inducing PDAC cell death in the tumor hypoxic core. Thus, the USP25/HIF-1α axis is an essential mechanism of metabolic reprogramming and survival in PDAC, which can be therapeutically exploited.

Animals, Carcinoma, Pancreatic Ductal/pathology, Cell Line, Tumor, Glycolysis/genetics, Humans, Mice, Pancreatic Neoplasms/metabolism, Tumor Microenvironment/genetics, Ubiquitin Thiolesterase/genetics
2041-1723
Nelson, Jessica K.
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Thin, May Zaw
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Evan, Theodore
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Howell, Steven
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Wu, Mary
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Almeida, Bruna
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Legrave, Nathalie
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Koenis, Duco S.
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Koifman, Gabriela
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Sugimoto, Yoichiro
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Llorian Sopena, Miriam
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MacRae, James
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Nye, Emma
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Howell, Michael
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Snijders, Ambrosius P.
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Prachalias, Andreas
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Zen, Yoh
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Sarker, Debashis
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Behrens, Axel
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Nelson, Jessica K.
7dc3f0c8-5a67-4467-a332-efd560a0630b
Thin, May Zaw
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Evan, Theodore
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Howell, Steven
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Wu, Mary
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Almeida, Bruna
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Legrave, Nathalie
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Koenis, Duco S.
2fce0429-69b3-4175-8367-dcaa1156d236
Koifman, Gabriela
2385a740-d61e-46ea-b4fa-e712b89eebab
Sugimoto, Yoichiro
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Llorian Sopena, Miriam
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MacRae, James
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Nye, Emma
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Howell, Michael
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Snijders, Ambrosius P.
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Prachalias, Andreas
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Zen, Yoh
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Sarker, Debashis
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Behrens, Axel
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Nelson, Jessica K., Thin, May Zaw, Evan, Theodore, Howell, Steven, Wu, Mary, Almeida, Bruna, Legrave, Nathalie, Koenis, Duco S., Koifman, Gabriela, Sugimoto, Yoichiro, Llorian Sopena, Miriam, MacRae, James, Nye, Emma, Howell, Michael, Snijders, Ambrosius P., Prachalias, Andreas, Zen, Yoh, Sarker, Debashis and Behrens, Axel (2022) USP25 promotes pathological HIF-1-driven metabolic reprogramming and is a potential therapeutic target in pancreatic cancer. Nature Communications, 13 (1), [2070]. (doi:10.1038/s41467-022-29684-9).

Record type: Article

Abstract

Deubiquitylating enzymes (DUBs) play an essential role in targeted protein degradation and represent an emerging therapeutic paradigm in cancer. However, their therapeutic potential in pancreatic ductal adenocarcinoma (PDAC) has not been explored. Here, we develop a DUB discovery pipeline, combining activity-based proteomics with a loss-of-function genetic screen in patient-derived PDAC organoids and murine genetic models. This approach identifies USP25 as a master regulator of PDAC growth and maintenance. Genetic and pharmacological USP25 inhibition results in potent growth impairment in PDAC organoids, while normal pancreatic organoids are insensitive, and causes dramatic regression of patient-derived xenografts. Mechanistically, USP25 deubiquitinates and stabilizes the HIF-1α transcription factor. PDAC is characterized by a severely hypoxic microenvironment, and USP25 depletion abrogates HIF-1α transcriptional activity and impairs glycolysis, inducing PDAC cell death in the tumor hypoxic core. Thus, the USP25/HIF-1α axis is an essential mechanism of metabolic reprogramming and survival in PDAC, which can be therapeutically exploited.

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e-pub ahead of print date: 19 April 2022
Published date: 19 April 2022
Keywords: Animals, Carcinoma, Pancreatic Ductal/pathology, Cell Line, Tumor, Glycolysis/genetics, Humans, Mice, Pancreatic Neoplasms/metabolism, Tumor Microenvironment/genetics, Ubiquitin Thiolesterase/genetics

Identifiers

Local EPrints ID: 505355
URI: http://eprints.soton.ac.uk/id/eprint/505355
ISSN: 2041-1723
PURE UUID: bfc1593d-6bac-420f-8264-e3b527264858
ORCID for Jessica K. Nelson: ORCID iD orcid.org/0000-0003-2866-5170

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Date deposited: 07 Oct 2025 16:43
Last modified: 08 Oct 2025 02:17

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Contributors

Author: Jessica K. Nelson ORCID iD
Author: May Zaw Thin
Author: Theodore Evan
Author: Steven Howell
Author: Mary Wu
Author: Bruna Almeida
Author: Nathalie Legrave
Author: Duco S. Koenis
Author: Gabriela Koifman
Author: Yoichiro Sugimoto
Author: Miriam Llorian Sopena
Author: James MacRae
Author: Emma Nye
Author: Michael Howell
Author: Ambrosius P. Snijders
Author: Andreas Prachalias
Author: Yoh Zen
Author: Debashis Sarker
Author: Axel Behrens

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