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Basic Research
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Vasopressin Regulates Extracellular Vesicle Uptake by Kidney Collecting Duct Cells

Wilna Oosthuyzen, Kathleen M. Scullion, Jessica R. Ivy, Emma E. Morrison, Robert W. Hunter, Philip J. Starkey Lewis, Eoghan O'Duibhir, Jonathan M. Street, Andrea Caporali, Christopher D. Gregory, Stuart J. Forbes, David J. Webb, Matthew A. Bailey and James W. Dear
JASN November 2016, 27 (11) 3345-3355; DOI: https://doi.org/10.1681/ASN.2015050568
Wilna Oosthuyzen
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Kathleen M. Scullion
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Jessica R. Ivy
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Emma E. Morrison
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Robert W. Hunter
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Philip J. Starkey Lewis
†Medical Research Council Centre for Regenerative Medicine, Scottish Centre for Regenerative Medicine, Edinburgh, United Kingdom; and
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Eoghan O'Duibhir
†Medical Research Council Centre for Regenerative Medicine, Scottish Centre for Regenerative Medicine, Edinburgh, United Kingdom; and
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Jonathan M. Street
‡Renal Diagnostics and Therapeutics Unit, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland
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Andrea Caporali
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Christopher D. Gregory
§Medical Research Council Centre for Inflammation Research, University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh, United Kingdom;
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Stuart J. Forbes
†Medical Research Council Centre for Regenerative Medicine, Scottish Centre for Regenerative Medicine, Edinburgh, United Kingdom; and
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David J. Webb
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Matthew A. Bailey
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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James W. Dear
*British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh and
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Abstract

Extracellular vesicles (ECVs) facilitate intercellular communication along the nephron, with the potential to change the function of the recipient cell. However, it is not known whether this is a regulated process analogous to other signaling systems. We investigated the potential hormonal regulation of ECV transfer and report that desmopressin, a vasopressin analogue, stimulated the uptake of fluorescently loaded ECVs into a kidney collecting duct cell line (mCCDC11) and into primary cells. Exposure of mCCDC11 cells to ECVs isolated from cells overexpressing microRNA-503 led to downregulated expression of microRNA-503 target genes, but only in the presence of desmopressin. Mechanistically, ECV entry into mCCDC11 cells required cAMP production, was reduced by inhibiting dynamin, and was selective for ECVs from kidney tubular cells. In vivo, we measured the urinary excretion and tissue uptake of fluorescently loaded ECVs delivered systemically to mice before and after administration of the vasopressin V2 receptor antagonist tolvaptan. In control-treated mice, we recovered 2.5% of administered ECVs in the urine; tolvaptan increased recovery five-fold and reduced ECV deposition in kidney tissue. Furthermore, in a patient with central diabetes insipidus, desmopressin reduced the excretion of ECVs derived from glomerular and proximal tubular cells. These data are consistent with vasopressin-regulated uptake of ECVs in vivo. We conclude that ECV uptake is a specific and regulated process. Physiologically, ECVs are a new mechanism of intercellular communication; therapeutically, ECVs may be a vehicle by which RNA therapy could be targeted to specific cells for the treatment of kidney disease.

  • exosomes
  • vasopressin
  • vesicles
  • Copyright © 2016 by the American Society of Nephrology
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Journal of the American Society of Nephrology: 27 (11)
Journal of the American Society of Nephrology
Vol. 27, Issue 11
November 2016
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Vasopressin Regulates Extracellular Vesicle Uptake by Kidney Collecting Duct Cells
Wilna Oosthuyzen, Kathleen M. Scullion, Jessica R. Ivy, Emma E. Morrison, Robert W. Hunter, Philip J. Starkey Lewis, Eoghan O'Duibhir, Jonathan M. Street, Andrea Caporali, Christopher D. Gregory, Stuart J. Forbes, David J. Webb, Matthew A. Bailey, James W. Dear
JASN Nov 2016, 27 (11) 3345-3355; DOI: 10.1681/ASN.2015050568

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Vasopressin Regulates Extracellular Vesicle Uptake by Kidney Collecting Duct Cells
Wilna Oosthuyzen, Kathleen M. Scullion, Jessica R. Ivy, Emma E. Morrison, Robert W. Hunter, Philip J. Starkey Lewis, Eoghan O'Duibhir, Jonathan M. Street, Andrea Caporali, Christopher D. Gregory, Stuart J. Forbes, David J. Webb, Matthew A. Bailey, James W. Dear
JASN Nov 2016, 27 (11) 3345-3355; DOI: 10.1681/ASN.2015050568
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More in this TOC Section

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