Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth

Summary: Lactate extensively associates with metabolic reprogramming, signal transduction, and immune modulation. Nevertheless, the regulatory role of lactate in immune sensing of cytosolic DNA remains uncertain. Here, we report that lactate serves as an initiator to facilitate proteasomal degradati...

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Main Authors: Keqiang Rao, Xinchao Zhang, Yi Luo, Qiang Xia, Yuting Jin, Jing He
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725002128
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author Keqiang Rao
Xinchao Zhang
Yi Luo
Qiang Xia
Yuting Jin
Jing He
author_facet Keqiang Rao
Xinchao Zhang
Yi Luo
Qiang Xia
Yuting Jin
Jing He
author_sort Keqiang Rao
collection DOAJ
description Summary: Lactate extensively associates with metabolic reprogramming, signal transduction, and immune modulation. Nevertheless, the regulatory role of lactate in immune sensing of cytosolic DNA remains uncertain. Here, we report that lactate serves as an initiator to facilitate proteasomal degradation of cyclic GMP-AMP synthase (cGAS) independent of ubiquitin, thus repressing the production of interferon and contributing to tumor growth. Mechanistically, lactylation of K21 stimulates cGAS translocation from the nucleus to the proteasome for degradation, which is compromised by phosphorylation of PSMA4 S188 via disrupting its association with cGAS. Concurrently, lactylation of K415 rewires PIK3CB activity and impairs ULK1-driven phosphorylation of PSMA4 S188. Physiologically, lactylation of cGAS sustains tumor growth. Expression of cGAS correlates with the antitumor effect of the LDHA inhibitor FX11. Finally, the lactate-cGAS axis indicates a prognostic outcome of lung adenocarcinoma. Collectively, these findings not only put forth a mechanism of cGAS degradation but also unravel the clinical relevance of cGAS lactylation.
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institution Kabale University
issn 2211-1247
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publishDate 2025-04-01
publisher Elsevier
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series Cell Reports
spelling doaj-art-8f8aa99843494201a8cdd81f3ef18ec22025-08-20T03:42:53ZengElsevierCell Reports2211-12472025-04-0144411544110.1016/j.celrep.2025.115441Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growthKeqiang Rao0Xinchao Zhang1Yi Luo2Qiang Xia3Yuting Jin4Jing He5Department of Liver Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200120, China; Shanghai Institute of Transplantation, Shanghai 200120, China; Shanghai Engineering Research Center of Transplantation and Immunology, Shanghai 200120, ChinaDepartment of Pathology, College of Basic Medical Sciences, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, ChinaDepartment of Liver Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200120, China; Shanghai Institute of Transplantation, Shanghai 200120, China; Shanghai Engineering Research Center of Transplantation and Immunology, Shanghai 200120, ChinaDepartment of Liver Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200120, China; Shanghai Institute of Transplantation, Shanghai 200120, China; Shanghai Engineering Research Center of Transplantation and Immunology, Shanghai 200120, China; Corresponding authorDepartment of Liver Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200120, China; Shanghai Institute of Transplantation, Shanghai 200120, China; Shanghai Engineering Research Center of Transplantation and Immunology, Shanghai 200120, China; Corresponding authorDepartment of Liver Surgery, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200120, China; Corresponding authorSummary: Lactate extensively associates with metabolic reprogramming, signal transduction, and immune modulation. Nevertheless, the regulatory role of lactate in immune sensing of cytosolic DNA remains uncertain. Here, we report that lactate serves as an initiator to facilitate proteasomal degradation of cyclic GMP-AMP synthase (cGAS) independent of ubiquitin, thus repressing the production of interferon and contributing to tumor growth. Mechanistically, lactylation of K21 stimulates cGAS translocation from the nucleus to the proteasome for degradation, which is compromised by phosphorylation of PSMA4 S188 via disrupting its association with cGAS. Concurrently, lactylation of K415 rewires PIK3CB activity and impairs ULK1-driven phosphorylation of PSMA4 S188. Physiologically, lactylation of cGAS sustains tumor growth. Expression of cGAS correlates with the antitumor effect of the LDHA inhibitor FX11. Finally, the lactate-cGAS axis indicates a prognostic outcome of lung adenocarcinoma. Collectively, these findings not only put forth a mechanism of cGAS degradation but also unravel the clinical relevance of cGAS lactylation.http://www.sciencedirect.com/science/article/pii/S2211124725002128CP: Cancer
spellingShingle Keqiang Rao
Xinchao Zhang
Yi Luo
Qiang Xia
Yuting Jin
Jing He
Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth
Cell Reports
CP: Cancer
title Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth
title_full Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth
title_fullStr Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth
title_full_unstemmed Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth
title_short Lactylation orchestrates ubiquitin-independent degradation of cGAS and promotes tumor growth
title_sort lactylation orchestrates ubiquitin independent degradation of cgas and promotes tumor growth
topic CP: Cancer
url http://www.sciencedirect.com/science/article/pii/S2211124725002128
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