Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation

Abstract Fine particulate matter (PM2.5) exposure has been associated with increased incidence and mortality of lung cancer. However, the molecular mechanisms underlying PM2.5 carcinogenicity remain incompletely understood. Here, we identified that PM2.5 suppressed the expression of tRNA methyltrans...

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Main Authors: Yiling Wang, Yuxin Wen, Qianqian Chen, Yongyi Huang, Duanyang Zhou, Wenhan Yang, Lin Yang, Juan Xiong, Kaiping Gao, Liyuan Sun, Rihong Zhai
Format: Article
Language:English
Published: Nature Publishing Group 2024-12-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-024-07287-0
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author Yiling Wang
Yuxin Wen
Qianqian Chen
Yongyi Huang
Duanyang Zhou
Wenhan Yang
Lin Yang
Juan Xiong
Kaiping Gao
Liyuan Sun
Rihong Zhai
author_facet Yiling Wang
Yuxin Wen
Qianqian Chen
Yongyi Huang
Duanyang Zhou
Wenhan Yang
Lin Yang
Juan Xiong
Kaiping Gao
Liyuan Sun
Rihong Zhai
author_sort Yiling Wang
collection DOAJ
description Abstract Fine particulate matter (PM2.5) exposure has been associated with increased incidence and mortality of lung cancer. However, the molecular mechanisms underlying PM2.5 carcinogenicity remain incompletely understood. Here, we identified that PM2.5 suppressed the expression of tRNA methyltransferase FTSJ1 and Am modification level of tRNA in vitro and in vivo. FTSJ1 downregulation enhanced glycolytic metabolism of non-small cell lung cancer (NSCLC) cells, as indicated by increased levels of lactate, pyruvate, and extracellular acidification rate (ECAR). Whereas treatment with glycolytic inhibitor 2-DG reversed this effect. In contrast, upregulation of FTSJ1 significantly suppressed glycolysis of NSCLC cells. Mechanistically, the silencing of FTSJ1 increased NSCLC cell proliferation and glycolysis through enhancing the expression and translation of PGK1. In human NSCLC tumor samples, FTSJ1 expression was negatively correlated with PGK1 expression level and the SUVmax value of PET/CT scan. In summary, our work reveals a previously unrecognized function of PM2.5-downregulated FTSJ1 on PGK1-mediated glycolysis in NSCLC, suggesting that targeted upregulation of FTSJ1 may represent a potential therapeutic strategy for NSCLC.
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spelling doaj-art-be7eda69db704b2e9c0e552da421707d2025-08-20T02:31:52ZengNature Publishing GroupCell Death and Disease2041-48892024-12-01151211310.1038/s41419-024-07287-0Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translationYiling Wang0Yuxin Wen1Qianqian Chen2Yongyi Huang3Duanyang Zhou4Wenhan Yang5Lin Yang6Juan Xiong7Kaiping Gao8Liyuan Sun9Rihong Zhai10School of Public Health, Shenzhen University Medical SchoolDepartment of Thoracic Surgery, The People’s Hospital of ShenzhenSchool of Public Health, Shenzhen University Medical SchoolSchool of Public Health, Shenzhen University Medical SchoolSchool of Public Health, Shenzhen University Medical SchoolSchool of Public Health, Shenzhen University Medical SchoolDepartment of Thoracic Surgery, The People’s Hospital of ShenzhenSchool of Public Health, Shenzhen University Medical SchoolSchool of Public Health, Shenzhen University Medical SchoolSchool of Nursing, Shenzhen University Medical SchoolSchool of Public Health, Shenzhen University Medical SchoolAbstract Fine particulate matter (PM2.5) exposure has been associated with increased incidence and mortality of lung cancer. However, the molecular mechanisms underlying PM2.5 carcinogenicity remain incompletely understood. Here, we identified that PM2.5 suppressed the expression of tRNA methyltransferase FTSJ1 and Am modification level of tRNA in vitro and in vivo. FTSJ1 downregulation enhanced glycolytic metabolism of non-small cell lung cancer (NSCLC) cells, as indicated by increased levels of lactate, pyruvate, and extracellular acidification rate (ECAR). Whereas treatment with glycolytic inhibitor 2-DG reversed this effect. In contrast, upregulation of FTSJ1 significantly suppressed glycolysis of NSCLC cells. Mechanistically, the silencing of FTSJ1 increased NSCLC cell proliferation and glycolysis through enhancing the expression and translation of PGK1. In human NSCLC tumor samples, FTSJ1 expression was negatively correlated with PGK1 expression level and the SUVmax value of PET/CT scan. In summary, our work reveals a previously unrecognized function of PM2.5-downregulated FTSJ1 on PGK1-mediated glycolysis in NSCLC, suggesting that targeted upregulation of FTSJ1 may represent a potential therapeutic strategy for NSCLC.https://doi.org/10.1038/s41419-024-07287-0
spellingShingle Yiling Wang
Yuxin Wen
Qianqian Chen
Yongyi Huang
Duanyang Zhou
Wenhan Yang
Lin Yang
Juan Xiong
Kaiping Gao
Liyuan Sun
Rihong Zhai
Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation
Cell Death and Disease
title Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation
title_full Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation
title_fullStr Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation
title_full_unstemmed Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation
title_short Downregulation of tRNA methyltransferase FTSJ1 by PM2.5 promotes glycolysis and malignancy of NSCLC via facilitating PGK1 expression and translation
title_sort downregulation of trna methyltransferase ftsj1 by pm2 5 promotes glycolysis and malignancy of nsclc via facilitating pgk1 expression and translation
url https://doi.org/10.1038/s41419-024-07287-0
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