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Elevated extracellular matrix protein 1 in circulating extracellular vesicles supports breast cancer progression under obesity conditions

Author

Listed:
  • Keyang Xu

    (Hong Kong Baptist University)

  • Ai Fu

    (Zhejiang Chinese Medical University)

  • Zhaoyi Li

    (Zhejiang Chinese Medical University)

  • Liangbin Miao

    (Zhejiang Chinese Medical University)

  • Zhonghan Lou

    (Zhejiang Chinese Medical University)

  • Keying Jiang

    (Hong Kong Baptist University)

  • Condon Lau

    (City University of Hong Kong)

  • Tao Su

    (Guangzhou University of Chinese Medicine)

  • Tiejun Tong

    (Hong Kong Baptist University)

  • Jianfeng Bao

    (Zhejiang Chinese Medical University)

  • Aiping Lyu

    (Hong Kong Baptist University
    Hong Kong Baptist University)

  • Hiu Yee Kwan

    (Hong Kong Baptist University
    Hong Kong Baptist University
    Hong Kong Baptist University)

Abstract

The cargo content in small extracellular vesicles (sEVs) changes under pathological conditions. Our data shows that in obesity, extracellular matrix protein 1 (ECM1) protein levels are significantly increased in circulating sEVs, which is dependent on integrin-β2. Knockdown of integrin-β2 does not affect cellular ECM1 protein levels but significantly reduces ECM1 protein levels in the sEVs released by these cells. In breast cancer (BC), overexpressing ECM1 increases matrix metalloproteinase 3 (MMP3) and S100A/B protein levels. Interestingly, sEVs purified from high-fat diet-induced obesity mice (D-sEVs) deliver more ECM1 protein to BC cells compared to sEVs from control diet-fed mice. Consequently, BC cells secrete more ECM1 protein, which promotes cancer cell invasion and migration. D-sEVs treatment also significantly enhances ECM1-mediated BC metastasis and growth in mouse models, as evidenced by the elevated tumor levels of MMP3 and S100A/B. Our study reveals a mechanism and suggests sEV-based strategies for treating obesity-associated BC.

Suggested Citation

  • Keyang Xu & Ai Fu & Zhaoyi Li & Liangbin Miao & Zhonghan Lou & Keying Jiang & Condon Lau & Tao Su & Tiejun Tong & Jianfeng Bao & Aiping Lyu & Hiu Yee Kwan, 2024. "Elevated extracellular matrix protein 1 in circulating extracellular vesicles supports breast cancer progression under obesity conditions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45995-5
    DOI: 10.1038/s41467-024-45995-5
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    References listed on IDEAS

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    1. Huijing Yin & Jingshu Wang & Hui Li & Yinjue Yu & Xiaoling Wang & Lili Lu & Cuiting Lv & Bin Chang & Wei Jin & Wenwen Guo & Chunxia Ren & Gong Yang, 2021. "Extracellular matrix protein-1 secretory isoform promotes ovarian cancer through increasing alternative mRNA splicing and stemness," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    2. Rosandra N. Kaplan & Rebecca D. Riba & Stergios Zacharoulis & Anna H. Bramley & Loïc Vincent & Carla Costa & Daniel D. MacDonald & David K. Jin & Koji Shido & Scott A. Kerns & Zhenping Zhu & Daniel Hi, 2005. "VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche," Nature, Nature, vol. 438(7069), pages 820-827, December.
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