Architecture of the rat nephron-arterial network: analysis with micro-computed tomography

Author:

Marsh Donald J.1ORCID,Postnov Dmitry D.2,Rowland Douglas J.3,Wexler Anthony S.4,Sosnovtseva Olga V.2,Holstein-Rathlou Niels-Henrik2

Affiliation:

1. Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, Providence, Rhode Island;

2. Department of Biomedical Sciences, Panum Institute, University of Copenhagen, Copenhagen, Denmark;

3. Department of Biomedical Engineering and Center for Molecular and Genomic Imaging, University of California, Davis, Davis, California; and

4. Department of Mechanical and Aerospace Engineering, University of California, Davis, Davis, California

Abstract

Among solid organs, the kidney’s vascular network stands out, because each nephron has two distinct capillary structures in series and because tubuloglomerular feedback, one of the mechanisms responsible for blood flow autoregulation, is specific to renal tubules. Tubuloglomerular feedback and the myogenic mechanism, acting jointly, autoregulate single-nephron blood flow. Each generates a self-sustained periodic oscillation and an oscillating electrical signal that propagates upstream along arterioles. Similar electrical signals from other nephrons interact, allowing nephron synchronization. Experimental measurements show synchronization over fields of a few nephrons; simulations based on a simplified network structure that could obscure complex interactions predict more widespread synchronization. To permit more realistic simulations, we made a cast of blood vessels in a rat kidney, performed micro-computed tomography at 2.5-μm resolution, and recorded three-dimensional coordinates of arteries, afferent arterioles, and glomeruli. Nonterminal branches of arcuate arteries form treelike structures requiring two to six bifurcations to reach terminal branches at the tree tops. Terminal arterial structures were either paired branches at the tops of the arterial trees, from which 52.6% of all afferent arterioles originated, or unpaired arteries not at the tree tops, yielding the other 22.9%; the other 24.5% originated directly from nonterminal arteries. Afferent arterioles near the corticomedullary boundary were longer than those farther away, suggesting that juxtamedullary nephrons have longer afferent arterioles. The distance separating origins of pairs of afferent arterioles varied randomly. The results suggest an irregular-network tree structure with vascular nodes, where arteriolar activity and local blood pressure interact.

Funder

Lundbeckfonden (Lundbeck Foundation)

University of Copenhagen (Københavns Universitet)

NIH

Publisher

American Physiological Society

Subject

Physiology

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