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PSMD14-mediated PFKFB2 deubiquitination activates H3K27 lactylation to drive cancer stemness in gastric adenocarcinoma

Cell Death & Differentiation (2025)Cite this article

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Abstract

Deubiquitinases (DUBs) are pivotal in cancer progression, yet their role in metabolic reprogramming in gastric adenocarcinoma (GAC) remains unclear. Here, we discover that highly expressed PSMD14 strengthens tumor stemness and drives tumor progression by increasing glycolysis and lactate accumulation, which activates H3K27 lactylation (H3K27la) and turns to enhance the expression of PSMD14 and SOX9. Mechanistically, PSMD14 deubiquitinates PFKFB2 at K355, facilitating SCYL2-mediated phosphorylation of PFKFB2 at S466/S483, which increases the generation of fructose-2,6-bisphosphate, activating PFK1 and glycolysis. Additionally, the H3K27la/PSMD14/SCYL2/p-PFKFB2 axis correlates with increased glucose metabolic activity and poor prognosis in GAC patients. Notably, high-throughput screening of FDA-approved drugs reveals that Daclatasvir (DCV) exhibits high binding affinity for PSMD14 protein, disrupts the PSMD14-PFKFB2 interaction, reduces PFKFB2 activity and tumor burden. Collectively, our findings are the first to elucidate a positive feedback loop existing between PSMD14 and glycolysis in GAC progression, suggesting that PSMD14 blockade may represent a potential therapeutic approach for GAC.

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Fig. 1: PSMD14 modulates glycolysis and tumor stemness in GAC.
Fig. 2: PSMD14 is epigenetically regulated by glucose homeostasis in GAC.
Fig. 3: PSMD14 augments aerobic glycolysis via an interaction with PFKFB2.
Fig. 4: PSMD14 decreases the K63-linked ubiquitination of PFKFB2.
Fig. 5: PSMD14 deubiquitinates PFKFB2 at K355 to increase PFKFB2 activation.
Fig. 6: SCYL2 binds to and phosphorylates PFKFB2.
Fig. 7: H3K27la-mediated PSMD14 expression was correlated with SCYL2-induced PFKFB2 phosphorylation and poor GAC prognosis.
Fig. 8: Daclatasvir (DCV) binds with PSMD14 counteract GAC progression.

Data availability

Data generated or analyzed in this study are available from the corresponding authors upon reasonable request. LC–MS/MS proteomics for the PSMD14 interactome have been deposited with the ProteomeXchange Consortium via the iProX repository under accession PXD067241. The PFKFB2 ubiquitinomics dataset is provided within the article and Supplementary materials. Public resources used include: TCGA-STAD, ACRG (GSE66229), and GEO (GSE13873).

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Funding

This work was supported in part by the National Natural Science Foundation of China (U24A20720, 82273157, 82473107, 82073114, 82102984); and the Natural Science Foundation of Anhui Province (2408085QH235); and China Postdoctoral Science Foundation (2024M760032); and the Nanjing special foundation for health science and technology development (distinguished young program, JQX22005); and the Health Research Program of Anhui (AHWJ2024Aa20050).

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Author notes

  1. These authors contributed equally: Xiaoya Zhao, Mengmeng Li, Yao Fu, Chen Chen.

Authors and Affiliations

  1. Medical School of Nanjing University, Nanjing, China

    Xiaoya Zhao, Mengmeng Li, Zhuang Ma, Jiawen Xu, Shimeng Zhou, Yun Qian & Shouyu Wang

  2. Department of Pathology, The First Affiliated Hospital of Anhui Medical University, Hefei, China

    Yao Fu

  3. Department of Hepatobiliary Surgery, The First Affiliated Hospital of Anhui Medical University; MOE Innovation Center for Basic Research in Tumor Immunotherapy; Anhui Province Key Laboratory of Tumor Immune Microenvironment and Immunotherapy, Hefei, China

    Chen Chen, Bo Wang, Qiang Wang, Zhangding Wang & Shouyu Wang

  4. STD Clinic, Institute of Dermatology, Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing, China

    Yali Chen

  5. Department of Gastroenterology, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China

    Lei Xu

  6. Division of Gastric Surgery, Department of General Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China

    Linsen Bao & Meng Wang

  7. Department of Nuclear Medicine, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing University, Nanjing, China

    Jian He

  8. Department of Geriatric Oncology, The First Affiliated Hospital of Nanjing Medical University, Nanjing, China

    Qingqing Ding

  9. The Comprehensive Cancer Center, Department of Central Laboratory, The Affiliated Huaian No.1 People’s Hospital of Nanjing Medical University, Huai’an, China

    Qilong Wang

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Contributions

XZ, ML, and YF performed the experiments; CC and LB contributed to the construction of GAC organoids; LX, QD, YC, YQ, SZ and ML evaluated the IHC of TMA; YF was responsible for the pathological staining interpretation; JX, ZM and BW participated in the construction of plasmids; QLW performed protein purification and subsequent SPR assay; JH, QW, MW and ZW analyzed data; XZ and SW wrote the paper; SW designed the project.

Corresponding authors

Correspondence to Meng Wang, Qilong Wang, Zhangding Wang or Shouyu Wang.

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The authors declare no competing interests.

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All animal related experiments were approved by the Animal Care and Use Committee of Nanjing Drum Tower Hospital. All participants were fully aware of the goal and possible risk of this study and provided written informed consent. This study was performed in accordance with the Declaration of Helsinki principles.

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Zhao, X., Li, M., Fu, Y. et al. PSMD14-mediated PFKFB2 deubiquitination activates H3K27 lactylation to drive cancer stemness in gastric adenocarcinoma. Cell Death Differ (2025). https://doi.org/10.1038/s41418-025-01605-5

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