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Caveolae in CNS arterioles mediate neurovascular coupling

Author

Listed:
  • Brian W. Chow

    (Harvard Medical School)

  • Vicente Nuñez

    (Harvard Medical School)

  • Luke Kaplan

    (Harvard Medical School)

  • Adam J. Granger

    (Harvard Medical School
    Harvard Medical School)

  • Karina Bistrong

    (Harvard Medical School)

  • Hannah L. Zucker

    (Harvard Medical School)

  • Payal Kumar

    (Harvard Medical School)

  • Bernardo L. Sabatini

    (Harvard Medical School
    Harvard Medical School)

  • Chenghua Gu

    (Harvard Medical School)

Abstract

Proper brain function depends on neurovascular coupling: neural activity rapidly increases local blood flow to meet moment-to-moment changes in regional brain energy demand1. Neurovascular coupling is the basis for functional brain imaging2, and impaired neurovascular coupling is implicated in neurodegeneration1. The underlying molecular and cellular mechanisms of neurovascular coupling remain poorly understood. The conventional view is that neurons or astrocytes release vasodilatory factors that act directly on smooth muscle cells (SMCs) to induce arterial dilation and increase local blood flow1. Here, using two-photon microscopy to image neural activity and vascular dynamics simultaneously in the barrel cortex of awake mice under whisker stimulation, we found that arteriolar endothelial cells (aECs) have an active role in mediating neurovascular coupling. We found that aECs, unlike other vascular segments of endothelial cells in the central nervous system, have abundant caveolae. Acute genetic perturbations that eliminated caveolae in aECs, but not in neighbouring SMCs, impaired neurovascular coupling. Notably, caveolae function in aECs is independent of the endothelial NO synthase (eNOS)-mediated NO pathway. Ablation of both caveolae and eNOS completely abolished neurovascular coupling, whereas the single mutants exhibited partial impairment, revealing that the caveolae-mediated pathway in aECs is a major contributor to neurovascular coupling. Our findings indicate that vasodilation is largely mediated by endothelial cells that actively relay signals from the central nervous system to SMCs via a caveolae-dependent pathway.

Suggested Citation

  • Brian W. Chow & Vicente Nuñez & Luke Kaplan & Adam J. Granger & Karina Bistrong & Hannah L. Zucker & Payal Kumar & Bernardo L. Sabatini & Chenghua Gu, 2020. "Caveolae in CNS arterioles mediate neurovascular coupling," Nature, Nature, vol. 579(7797), pages 106-110, March.
  • Handle: RePEc:nat:nature:v:579:y:2020:i:7797:d:10.1038_s41586-020-2026-1
    DOI: 10.1038/s41586-020-2026-1
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    Cited by:

    1. Ying Zhao & Wusheng Zhu & Ting Wan & Xiaohao Zhang & Yunzi Li & Zhenqian Huang & Pengfei Xu & Kangmo Huang & Ruidong Ye & Yi Xie & Xinfeng Liu, 2022. "Vascular endothelium deploys caveolin-1 to regulate oligodendrogenesis after chronic cerebral ischemia in mice," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    2. Adam Institoris & Milène Vandal & Govind Peringod & Christy Catalano & Cam Ha Tran & Xinzhu Yu & Frank Visser & Cheryl Breiteneder & Leonardo Molina & Baljit S. Khakh & Minh Dang Nguyen & Roger J. Tho, 2022. "Astrocytes amplify neurovascular coupling to sustained activation of neocortex in awake mice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Brandon R. Munn & Eli J. Müller & Gabriel Wainstein & James M. Shine, 2021. "The ascending arousal system shapes neural dynamics to mediate awareness of cognitive states," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    4. Karolina Jezierska & Anna Sękowska-Namiotko & Bartłomiej Pala & Danuta Lietz-Kijak & Helena Gronwald & Wojciech Podraza, 2022. "Searching for the Mechanism of Action of Extremely Low Frequency Electromagnetic Field—The Pilot fNIRS Research," IJERPH, MDPI, vol. 19(7), pages 1-9, March.

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