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Long noncoding RNA DIO3OS induces glycolytic-dominant metabolic reprogramming to promote aromatase inhibitor resistance in breast cancer

Author

Listed:
  • Xueman Chen

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Rong Luo

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Yunmei Zhang

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Shuying Ye

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Xin Zeng

    (Sun Yat-Sen University)

  • Jiang Liu

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Di Huang

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Yujie Liu

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Qiang Liu

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Man-Li Luo

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen Memorial Hospital)

  • Erwei Song

    (Sun Yat-Sen University
    Sun Yat-Sen University)

Abstract

Aromatase inhibition is an efficient endocrine therapy to block ectopic estrogen production for postmenopausal estrogen receptor (ER)-positive breast cancer patients, but many develop resistance. Here, we show that aromatase inhibitor (AI)-resistant breast tumors display features of enhanced aerobic glycolysis with upregulation of long noncoding RNA (lncRNA) DIO3OS, which correlates with poor prognosis of breast cancer patients on AI therapies. Long-term estrogen deprivation induces DIO3OS expression in ER-positive breast tumor cells, which further enhances aerobic glycolysis and promotes estrogen-independent cell proliferation in vitro and in vivo. Mechanistically, DIO3OS interacts with polypyrimidine tract binding protein 1 (PTBP1) and stabilizes the mRNA of lactate dehydrogenase A (LDHA) by protecting the integrity of its 3’UTR, and subsequently upregulates LDHA expression and activates glycolytic metabolism in AI-resistant breast cancer cells. Our findings highlight the role of lncRNA in regulating the key enzyme of glycolytic metabolism in response to endocrine therapies and the potential of targeting DIO3OS to reverse AI resistance in ER-positive breast cancer.

Suggested Citation

  • Xueman Chen & Rong Luo & Yunmei Zhang & Shuying Ye & Xin Zeng & Jiang Liu & Di Huang & Yujie Liu & Qiang Liu & Man-Li Luo & Erwei Song, 2022. "Long noncoding RNA DIO3OS induces glycolytic-dominant metabolic reprogramming to promote aromatase inhibitor resistance in breast cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34702-x
    DOI: 10.1038/s41467-022-34702-x
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    References listed on IDEAS

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    1. Chunqing Wang & Yongmei Li & Shuai Yan & Hao Wang & Xianfeng Shao & Mingming Xiao & Baicai Yang & Guoxuan Qin & Ruirui Kong & Ruibing Chen & Ning Zhang, 2020. "Interactome analysis reveals that lncRNA HULC promotes aerobic glycolysis through LDHA and PKM2," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Sheng Hui & Jonathan M. Ghergurovich & Raphael J. Morscher & Cholsoon Jang & Xin Teng & Wenyun Lu & Lourdes A. Esparza & Tannishtha Reya & Le Zhan & Jessie Yanxiang Guo & Eileen White & Joshua D. Rabi, 2017. "Glucose feeds the TCA cycle via circulating lactate," Nature, Nature, vol. 551(7678), pages 115-118, November.
    3. Jiayin Tang & Tingting Yan & Yujie Bao & Chaoqin Shen & Chenyang Yu & Xiaoqiang Zhu & Xianglong Tian & Fangfang Guo & Qian Liang & Qiang Liu & Ming Zhong & Jinxian Chen & Zhizheng Ge & Xiaobo Li & Xia, 2019. "LncRNA GLCC1 promotes colorectal carcinogenesis and glucose metabolism by stabilizing c-Myc," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
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