Synchronization in renal microcirculation unveiled with high-resolution blood flow imaging

  1. Dmitry Postnov  Is a corresponding author
  2. Donald J Marsh
  3. Will A Cupples
  4. Niels-Henrik Holstein-Rathlou
  5. Olga Sosnovtseva
  1. Aarhus University, Denmark
  2. Brown University, United States
  3. Simon Fraser University, Canada
  4. University of Copenhagen, Denmark

Abstract

Internephron interaction is fundamental for kidney function. Earlier studies have shown that nephrons signal to each other, synchronise over short distances, and potentially form large synchronised clusters. Such clusters would play an important role in renal autoregulation, but due to the technological limitations, their presence is yet to be confirmed. In the present study, we introduce an approach for high-resolution laser speckle imaging of renal blood flow and apply it to estimate frequency and phase differences in rat kidney microcirculation under different conditions. The analysis unveiled spatial and temporal evolution of synchronised blood flow clusters of various sizes, including the formation of large (>90 vessels) long-lived clusters (>10 periods) locked at the frequency of the tubular glomerular feedback mechanism. Administration of vasoactive agents caused significant changes in the synchronisation patterns and, thus, in nephrons' co-operative dynamics. Specifically, infusion of vasoconstrictor angiotensin II promoted stronger synchronisation, while acetylcholine caused complete desynchronisation. The results confirm the presence of the local synchronisation in the renal microcirculatory blood flow and that it changes depending on the condition of the vascular network and the blood pressure, which will have further implications for the role of such synchronisation in pathologies development.

Data availability

The data underlying this article are available at public data repository (Dryad): https://doi.org/10.5061/dryad.g79cnp5r2

The following data sets were generated

Article and author information

Author details

  1. Dmitry Postnov

    Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
    For correspondence
    dpostnov@cfin.au.dk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9708-8453
  2. Donald J Marsh

    Division of Biology and Medicine, Brown University, Rhode Island, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Will A Cupples

    Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Niels-Henrik Holstein-Rathlou

    Biomedical Sciences Institute, University of Copenhagen, Copenhagen, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  5. Olga Sosnovtseva

    Biomedical Sciences Institute, University of Copenhagen, Copenhagen, Denmark
    Competing interests
    The authors declare that no competing interests exist.

Funding

Novo Nordisk Fonden

  • Dmitry Postnov

Lundbeckfonden

  • Dmitry Postnov

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Martin R Pollak, Harvard Medical School, United States

Ethics

Animal experimentation: All experimental protocols were approved by the Danish National Animal Experiments Inspectorate (License 2015-15-0201-00463) and were conducted according to the American Physiological Society guidelines.

Version history

  1. Preprint posted: October 16, 2021 (view preprint)
  2. Received: November 4, 2021
  3. Accepted: May 6, 2022
  4. Accepted Manuscript published: May 6, 2022 (version 1)
  5. Version of Record published: May 17, 2022 (version 2)
  6. Version of Record updated: May 19, 2022 (version 3)

Copyright

© 2022, Postnov et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Dmitry Postnov
  2. Donald J Marsh
  3. Will A Cupples
  4. Niels-Henrik Holstein-Rathlou
  5. Olga Sosnovtseva
(2022)
Synchronization in renal microcirculation unveiled with high-resolution blood flow imaging
eLife 11:e75284.
https://doi.org/10.7554/eLife.75284

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https://doi.org/10.7554/eLife.75284