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Non-invasive modulation of meningeal lymphatics ameliorates ageing and Alzheimer’s disease-associated pathology and cognition in mice

Author

Listed:
  • Miao Wang

    (School of Biomedical Engineering, Hainan University)

  • Congcong Yan

    (School of Biomedical Engineering, Hainan University)

  • Xi Li

    (School of Biomedical Engineering, Hainan University)

  • Tianhao Yang

    (School of Biomedical Engineering, Hainan University)

  • Shengnan Wu

    (School of Medical Technology, Beijing Institute of Technology)

  • Qian Liu

    (School of Biomedical Engineering, Hainan University)

  • Qingming Luo

    (School of Biomedical Engineering, Hainan University)

  • Feifan Zhou

    (School of Biomedical Engineering, Hainan University)

Abstract

Meningeal lymphatic vessels (mLVs) have been shown to be involved in amyloid beta (Aβ) clearance, which is considered as a potential therapeutic target for Alzheimer’s disease (AD). In this study, based on the superficial spatial distribution of mLVs, a near-infrared light is employed to modulate lymphatic drainage, significantly improving cognition of both aged and AD (5xFAD and APP/PS1) mice, and alleviating AD-associated pathology by reducing Aβ deposition, neuroinflammation and neuronal damage. Furthermore, transmission electron microscopy imaging and RNA sequencing data indicate amelioration of mitochondrial metabolism and cellular junction of meningeal lymphatic endothelial cells (mLECs) by light modulation. These studies collectively suggest that near-infrared light treatment can improve cognitive function by strengthening scavenging ability of mLVs through restoring mLEC function. In conclusion, lymphatic drainage potentiation by light promotes pathological remission and cognitive enhancement in aging and AD mouse models, which offers a potential amelioration strategy for neurodegenerative diseases.

Suggested Citation

  • Miao Wang & Congcong Yan & Xi Li & Tianhao Yang & Shengnan Wu & Qian Liu & Qingming Luo & Feifan Zhou, 2024. "Non-invasive modulation of meningeal lymphatics ameliorates ageing and Alzheimer’s disease-associated pathology and cognition in mice," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45656-7
    DOI: 10.1038/s41467-024-45656-7
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    1. Jinman Chen & Linmei Wang & Hao Xu & Lianping Xing & Zixin Zhuang & Yangkang Zheng & Xuefei Li & Chinyun Wang & Shaohua Chen & Zibin Guo & Qianqian Liang & Yongjun Wang, 2020. "Meningeal lymphatics clear erythrocytes that arise from subarachnoid hemorrhage," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    2. Dongyu Li & Shaojun Liu & Tingting Yu & Zhang Liu & Silin Sun & Denis Bragin & Alexander Shirokov & Nikita Navolokin & Olga Bragina & Zhengwu Hu & Jürgen Kurths & Ivan Fedosov & Inna Blokhina & Alexan, 2023. "Photostimulation of brain lymphatics in male newborn and adult rodents for therapy of intraventricular hemorrhage," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Ashley C. Bolte & Arun B. Dutta & Mariah E. Hurt & Igor Smirnov & Michael A. Kovacs & Celia A. McKee & Hannah E. Ennerfelt & Daniel Shapiro & Bao H. Nguyen & Elizabeth L. Frost & Catherine R. Lammert , 2020. "Meningeal lymphatic dysfunction exacerbates traumatic brain injury pathogenesis," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    4. Antoine Louveau & Igor Smirnov & Timothy J. Keyes & Jacob D. Eccles & Sherin J. Rouhani & J. David Peske & Noel C. Derecki & David Castle & James W. Mandell & Kevin S. Lee & Tajie H. Harris & Jonathan, 2015. "Structural and functional features of central nervous system lymphatic vessels," Nature, Nature, vol. 523(7560), pages 337-341, July.
    5. Sandro Da Mesquita & Antoine Louveau & Andrea Vaccari & Igor Smirnov & R. Chase Cornelison & Kathryn M. Kingsmore & Christian Contarino & Suna Onengut-Gumuscu & Emily Farber & Daniel Raper & Kenneth E, 2018. "Publisher Correction: Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease," Nature, Nature, vol. 564(7734), pages 7-7, December.
    6. Sandro Mesquita & Zachary Papadopoulos & Taitea Dykstra & Logan Brase & Fabiana Geraldo Farias & Morgan Wall & Hong Jiang & Chinnappa Dilip Kodira & Kalil Alves Lima & Jasmin Herz & Antoine Louveau & , 2021. "Meningeal lymphatics affect microglia responses and anti-Aβ immunotherapy," Nature, Nature, vol. 593(7858), pages 255-260, May.
    7. Sandro Mesquita & Antoine Louveau & Andrea Vaccari & Igor Smirnov & R. Chase Cornelison & Kathryn M. Kingsmore & Christian Contarino & Suna Onengut-Gumuscu & Emily Farber & Daniel Raper & Kenneth E. V, 2018. "Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease," Nature, Nature, vol. 560(7717), pages 185-191, August.
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