IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45995-5.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45995-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45995-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Zhiyuan Zheng & Ya-nan Li & Shanfen Jia & Mengting Zhu & Lijuan Cao & Min Tao & Jingting Jiang & Shenghua Zhan & Yongjing Chen & Ping-Jin Gao & Weiguo Hu & Ying Wang & Changshun Shao & Yufang Shi, 2021. "Lung mesenchymal stromal cells influenced by Th2 cytokines mobilize neutrophils and facilitate metastasis by producing complement C3," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Zihan Tang & Yanyan Xu & Yun Tan & Hui Shi & Peipei Jin & Yunqi Li & Jialin Teng & Honglei Liu & Haoyu Pan & Qiongyi Hu & Xiaobing Cheng & Junna Ye & Yutong Su & Yue Sun & Jianfen Meng & Zhuochao Zhou, 2023. "CD36 mediates SARS-CoV-2-envelope-protein-induced platelet activation and thrombosis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Lufei Sui & Suming Wang & Debolina Ganguly & Tyler P. El Rayes & Cecilie Askeland & Astrid Børretzen & Danielle Sim & Ole Johan Halvorsen & Gøril Knutsvik & Jarle Arnes & Sura Aziz & Svein Haukaas & W, 2022. "PRSS2 remodels the tumor microenvironment via repression of Tsp1 to stimulate tumor growth and progression," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Nieves Montenegro-Navarro & Claudia García-Báez & Melissa García-Caballero, 2023. "Molecular and metabolic orchestration of the lymphatic vasculature in physiology and pathology," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Yuchao Xia & Zijie Jin & Chengsheng Zhang & Linkun Ouyang & Yuhao Dong & Juan Li & Lvze Guo & Biyang Jing & Yang Shi & Susheng Miao & Ruibin Xi, 2023. "TAGET: a toolkit for analyzing full-length transcripts from long-read sequencing," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Yi Zhou & Peng Ke & Xiaoyan Bao & Honghui Wu & Yiyi Xia & Zhentao Zhang & Haiqing Zhong & Qi Dai & Linjie Wu & Tiantian Wang & Mengting Lin & Yaosheng Li & Xinchi Jiang & Qiyao Yang & Yiying Lu & Xinc, 2022. "Peptide nano-blanket impedes fibroblasts activation and subsequent formation of pre-metastatic niche," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Yibing Han & Takeshi Tomita & Masayoshi Kato & Norihiro Ashihara & Yumiko Higuchi & Hisanori Matoba & Weiyi Wang & Hikaru Hayashi & Yuji Itoh & Satoshi Takahashi & Hiroshi Kurita & Jun Nakayama & Nobu, 2023. "Citrullinated fibrinogen-SAAs complex causes vascular metastagenesis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Flavia A. Graca & Mamta Rai & Liam C. Hunt & Anna Stephan & Yong-Dong Wang & Brittney Gordon & Ruishan Wang & Giovanni Quarato & Beisi Xu & Yiping Fan & Myriam Labelle & Fabio Demontis, 2022. "The myokine Fibcd1 is an endogenous determinant of myofiber size and mitigates cancer-induced myofiber atrophy," Nature Communications, Nature, vol. 13(1), pages 1-22, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45995-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.