Architecture of inner medullary descending and ascending vasa recta: pathways for countercurrent exchange

Abstract

Pathways and densities of descending vasa recta (DVR) and ascending vasa recta (AVR) in the outer zone of the inner medulla (IM) were evaluated to better understand medullary countercurrent exchange. Nearly all urea transporter B (UT-B)-positive DVR, those vessels exhibiting a continuous endothelium, descend with little or no branching exclusively through the intercluster region. All DVR have a terminal fenestrated (PV-1-positive) segment that partially overlaps with the UT-B-positive segment. This fenestrated segment descends a distance equal to approximately 15% of the length of the connecting UT-B-positive segment before formation of the first branch. The onset of branching is indicative of vessel entry into the intracluster region. The number density of UT-B-positive DVR at 3,000 mum below the OM-IM boundary is approximately 60% lower than the density at 400 mum below the OM-IM boundary, a result of DVR joining to fenestrated interconnecting vessels and an overall decline in UT-B expression. AVR that lie in the intercluster region (designated AVR(2)) lie distant from CDs and ascend to the OM-IM boundary with little or no branching. AVR(2a) represent a subcategory of AVR(2) that abut DVR. The mean DVR length (combined UT-B- and PV-1-positive segments) nearly equals the mean AVR(2a) length, implying a degree of overall equivalence in fluid and solute countercurrent exchange may exist. The AVR(2)/DVR ratio is approximately 2:1, and the AVR(2a)/DVR ratio is approximately 1:1; however, the AVR/DVR ratio determined for the full complement of fenestrated vessels is approximately 4:1. The excess fenestrated vessels include vessels of the intracluster region (designated AVR(1)). Countercurrent exchange between vasa recta occurs predominantly in the intercluster region. This architecture supports previous functional estimates of capillary fluid uptake in the renal IM.

Fig. 1.

Five vascular bundles from a transverse section at 100 μm below the outer medullary (OM)-inner medullary (IM) boundary [collecting ducts (CDs), aquaporin-2 (AQP2)/blue; descending vasa recta (DVR), urea transporter B (UT-B)/green; vessels of the intracluster region (AVR₁) and in the intercluster region (AVR₂), PV-1/red]. Vascular bundles are located predominantly in the intercluster region, distant from CDs. In the intracluster region, fenestrated vessels abut CDs. Scale bar = 100 μm.

Fig. 2.

Transverse sections that include 2 secondary CD clusters (see results for definition of secondary CD cluster) (CDs, AQP2/blue; DVR, UT-B/green; AVR₁ and AVR₂, PV-1/red). A: 400 μm below the OM-IM boundary. B: 1,500 μm below the OM-IM boundary. Within bundles, DVR descend from, and AVR₂ ascend to, the upper boundary of reconstruction at 400 μm below the OM-IM boundary. Each secondary CD cluster consists of 5 primary clusters; secondary cluster 1, bottom 5 white borders; secondary cluster 2, top 5 white borders (compare with Figs. 1–3 in Ref. 26). Four vascular bundles (VB) are associated with cluster 1, and 5 vascular bundles are associated with cluster 2 (outlined with green). Inset: magnification of vascular bundle 2 from cluster 1 (arrows) (CDs, AQP2/blue; DVR, UT-B/green; AVR₂, PV-1/overdrawn with white; AVR₁, PV-1/red). Scale bars = 100 μm (figure) and 25 μm (inset).

Fig. 3.

Diagram of vasa recta architecture in the outer zone of the IM. UT-B-positive (shaded light, nonfenestrated) DVR descends along the corticopapillary axis. UT-B-positive segment overlaps (small bracket) with PV-1 (shaded dark, fenestrated) and is continuous with a descending PV-1-positive, UT-B-negative DVR (large bracket). This PV-1-positive segment is continuous with AVR₁, which lie within the CD cluster (intracluster region) (8). AVR₁ connect to AVR₂ in vascular bundles of the intercluster region. Arrows denote blood flow direction. AVR₁, PV-1-positive intracluster AVR and interconnecting capillaries that do abut CDs; AVR₂, ascending PV-1-positive intercluster vessels that do not abut CDs, and do or do not abut DVR.

Fig. 4.

Number densities and ratios of IM blood vessels. A: number densities and ratios for UT-B-positive and PV-1-positive vessels that lie within random cross-sectional areas of the IM from 3 kidneys. Values are means ± SE. Ratio means marked with an asterisk are not significantly different from each other (ANOVA; P < 0.05). B: number densities and ratios for reconstructed DVR and AVR that lie within the borders of CD clusters 1 and 2. Tracing UT-B-positive DVR and their fenestrated segments becomes increasingly less accurate beyond 2 mm for technical reasons. Incomplete recognition of fenestrated DVR combined with biological variation probably account for higher AVR/DVR ratios at 2,000 μm below the OM-IM boundary. Compare with Fig. 4 in Ref. .

Fig. 5.

Comparisons between mean lengths of DVR (including PV-1-positive segment) and AVR_2a for vessels of 4 vascular bundles from secondary CD cluster 1 (black circles) and for 5 vascular bundles from secondary CD cluster 2 (white squares). Values are means ± SE. The 2 clusters and 9 bundles are outlined in Fig. 2A. DVR and AVR_2a lie within the reconstructed interval of 400 and 3,200 μm below the OM-IM boundary. Line of identity is shown.

Fig. 6.

Lengths of vessel segments in vascular bundles of the outer zone of the IM. A: secondary CD cluster 1 (n = 4). B: secondary CD cluster 2 (n = 5). Values are means ± SE. Sample means that share a common symbol are not significantly different from each other (ANOVA; P < 0.05).