Renal Medullary Circulation

Renal Physiology > Integrative Control of Renal Output > Integrative Function

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Thomas L. Pallone, Aurélie Edwards, David L. Mattson

10.1002/cphy.c100036

Source: Volume 2, Issue 1, January 2012

Published online: January 2012

Full Article on Wiley Online Library

Abstract
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Abstract

The renal medullary microcirculation is a distinctive arrangement of blood vessels that serve multiple functions in the renal medulla. This article begins with a description of the unique anatomy of this vascular bed and the role it plays in transport and countercurrent exchange in the medulla. A segment of the review is then devoted to the important role mathematical modeling has played in the understanding of this vascular bed's function. Succeeding sections focus upon the hematocrit in the vasa recta capillaries and methods utilized to assess blood flow in the renal medulla. An extensive portion of the article is then devoted to the regulation of the medullary circulation, from ion channel architecture to neurohormonal signaling. Finally, we discuss the importance of the renal medullary circulation in the regulation of fluid and electrolyte homeostasis and arterial blood pressure regulation. © 2012 American Physiological Society. Compr Physiol 2:97‐140, 2012.

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	Figure 1. Microcirculation of the renal cortex and medulla. Within the renal cortex, interlobular arteries, derived from the arcuate artery, ascend toward the cortical surface. Superficial and midcortical glomeruli arise at obtuse and right angles, while juxtamedullary glomeruli arise at an acute, recurrent angle from the interlobular artery. The majority of blood flow to the medulla arises from juxtamedullary efferent arterioles. A minor fraction might also be derived from periglomerular shunt pathways. In the outer stripe of the outer medulla (OM), juxtamedullary efferent arterioles give rise to descending vasa recta (DVR) that coalesce with ascending vasa recta (AVR), and sometimes, thin descending limbs of Henle, to form vascular bundles. Vascular bundles are the prominent feature of the inner stripe of the OM. DVR on the periphery of vascular bundles perfuse the interbundle capillary plexus that supplies nephrons (thick‐ascending limbs, collecting ducts (CD), long looped thin descending limbs, not shown). DVR in the center of the bundles continue across the inner‐outer medullary junction to perfuse the inner medulla (IM). In some species, thin descending limbs of short‐looped nephrons migrate toward or become associated with vascular bundles. In the inner medulla, vascular bundles disappear and vasa recta become dispersed with thin loops of Henle and CDs. Blood from the interbundle capillary plexus is returned without rejoining vascular bundles. DVR have a continuous endothelium (inset) and are surrounded by contractile pericytes. Like cortical peritubular capillaries, the AVR endothelium is highly fenestrated. As blood flows toward the papillary tip, NaCl and urea diffuse into DVR and out of AVR. Transmural gradients of NaCl and urea drive water efflux across the DVR wall via aquaporin‐1 water channels. Reproduced, with permission, from Pallone et al. 514.
	Figure 2. The intra‐arterial cushion. A longitudinal section through an afferent arteriole shows an intra‐arterial cushion at its origin from the interlobular artery (inset, × 160). The cushion protrudes into the lumen of the parent vessel. Smooth muscle cells of the cushion are embedded in a copious matrix (× 4000). Intra‐arterial cushions might affect the relative volume fraction of RBCs vs plasma (hematocrit) that is directed from intralobular arterioles to juxtamedullary glomeruli and renal medulla. It is also conceivable that they regulate the relative distribution of blood flow between the superficial and juxtamedullary cortex (see text). Reproduced, with permission, from Moffat and Creasey 433.
	Figure 3. Structure and transition of cortical and medullary vessels. The proximal afferent arteriole is composed of at least two layers of smooth muscle cells. The muscularity and size of cortical efferent arterioles differ with location. Note the difference between the superficial and juxtamedullary efferent arterioles. The juxtamedullary efferent arteriole is larger, has a thicker, multilayered media, and its endothelium is composed of more numerous endothelial cells. In the illustration, a descending vas rectum (DVR) in a vascular bundle is adjacent to three fenestrated ascending vasa recta (AVR). The DVR wall is surrounded by a contractile pericyte. At the bottom right, DVR and AVR from the inner medulla are shown. Inner medullary DVR have a continuous endothelium through most of their length as pericytes become scarcer with medullary depth. Terminal DVR and the entire AVR wall are fenestrated. Reproduced, with permission, from Jamison and Kriz 291.
	Figure 4. Distribution of descending vasa recta (DVR) pericytes. (A and B) Immunofluorescent staining of DVR pericytes using anti α‐smooth muscle actin as primary antibody. The pericytes are present on DVR from outer medullary vascular bundles (Panel A) and those from the inner medulla (Panel B) (1000 ×). (C) Low power image of immunofluorescent staining of DVR pericytes using anti α‐smooth muscle actin antibody. Some vessels show pericytes throughout their length to the papillary tip. Black vessels are filled with India ink (× 100). Reproduced, with permission, from Park et al. 529.
	Figure 5. Electron micrograph of descending vasa recta (DVR) and ascending vasa recta (AVR). Electron micrograph of DVR and AVR in rat vascular bundles. DVR have a continuous endothelium and AVR are fenestrated. Note the minimal interstitium that exists between vessels in this region (× 12,400). Reproduced, with permission, from Pallone et al. 516.
	Figure 6. Arterial injection of Psammomys obesus. (A) Photograph of the microvasculature of the desert rodent Psammomys obesus obtained by injecting the arteries of the kidney with Microfil and digesting the tissue. The distinct arteriolar patterns of the cortex, outer and inner medulla are apparent. In Psammomys, the separation of the outer medulla into vascular bundles and the dense capillary plexus of the interbundle region () is striking because vasa recta coalesce into giant vascular bundles. OM, outer medulla; IM, inner medulla. Designations on the original figure are C = cortex, TR = transitional region (outer stripe of the outer medulla), IS = inner stripe of the outer medulla, IZ = inner zone (inner medulla). Reproduced, with permission, from Bankir et al.. (B and C) India ink injection study of vascular bundles in the outer medulla of the rat. In contrast to Psammomys*, individual vascular bundles do not coalesce into giant bundles. The bundles are more evenly dispersed throughout the inner stripe of the outer medulla. This pattern is typical of many mammalian species including the rat, mouse and human. Reproduced, with permission, from Bankir et al., Moffat and Fourman) (29, 33).
	Figure 7. Tubular‐vascular relationships in the outer medulla (OM). Organization of the inner stripe of the OM. Top and bottom panels show longitudinal and cross‐sectional views, respectively. The extent to which the thin descending limbs of Henle (tDLH) of short looped nephrons associate with vascular bundles varies between species. In the rabbit, no association exists, whereas in the rat and mouse, the tDLH migrates to the periphery or becomes incorporated within vascular bundles, respectively. Abbreviations: VB, vascular bundle; IB, interbundle region; CD, collecting duct; 1 and 2, thin descending and thick ascending limbs of long‐looped nephrons; 3 and 4, thin descending and thick ascending limbs of short‐looped nephrons. Reproduced, with permission, from Bankir and de Rouffignac 29.
	Figure 8. Renal medullary interstitial cells (RMICs). RMICs appear to be tethered between thin limbs and vasa recta in the inner medulla. Interstitial spaces lie between the cells and the cells are stacked like rungs of a ladder. RMICs are contractile and secrete vasoactive paracrine agents (see text). The stacked arrangement of RMICs in some species has been suggested to help retard axial diffusion that would otherwise tend to dissipate corticomedullary gradients of NaCl and urea. AVR, venous or ascending vasa recta. Arrows point to lipid droplets within RMIC. Reproduced, with permission, from Lemley and Kriz 355.
	Figure 9. Tubular vascular relationships and collecting duct clusters in the inner medulla. (A) A CD cluster (blue) is surrounded by descending vasa recta (DVR) (red) and thin DLH (green). Neither DVR nor thin DLH are incorporated into the center of the cluster. (B) A CD cluster (blue) has both ascending vasa recta (AVR) (red) and thin ALH (green) in its surroundings and within the cluster. (C) Idealized cross‐sectional depiction of a CD cluster (blue) in relationship to AVR (red) and thin ALH (green). AVR and thin ALH are diffusely distributed around and within the CD cluster. (D) Idealized cross‐sectional depiction of thin DLH (purple) and DVR (aqua) surrounding open regions in which CD clusters reside. Reproduced, with permission, from Pannabecker and Dantzler 522.
	Figure 10. Relationships of vasa recta and loops of Henle to collecting duct clusters. (A) Three‐dimensional reconstruction of single CD segment (blue) with multiple ascending vasa recta (AVR) (red). Top: 90° axial rotation of segments shown in adjacent panels. Scale bar, 100 μm. (B) Electron micrographs showing transverse sections of CDs and AVR from 1.5 mm (i, ii, and iv) and 4 mm (iii) below the base of the IM. i: CD surrounded by 4 AVR (*). Other tubular structures surrounding the CD are ATLs. Scale bar, 10 μm. ii: AVR abuts CD with minimal direct contact. Scale bar, 1 μm. iii: AVR abuts CD with microvillus (arrow). IS, interstitium. Scale bar, 1 μm. iv: AVR abuts CD with microvilli (arrows). Scale bar, 1 μm. Reproduced, with permission, from Pannabecker and Dantzler 522.
	Figure 11. Hemodynamic effects on intrarenal oxygenation. Intrarenal oxygen tension (pO2) was measured in the cortex and medulla with a microelectrode. Cortical pO2 falls and medullary pO2 increases during an episode of hypotension induced by either hemorrhage, aortic ligation, or nitroprusside infusion (Panel A). Inhibition of transport in the thick ascending limb of Henle with a loop diuretic (Panel B) increases basal pO2 in the medulla (compare to Panel A) and eliminates the effect of hypotension to raise medullary pO2. Inhibition of vasodilatory prostaglandins and nitric oxide, or blockade of adenosine receptors reduces basal pO2 in the medulla and accentuates the increase in pO2 caused by hypotension (Panel C). Intrarenal tissue pO2 decreases with medullary depth (Panel D). * indicates significance from baseline (P < .001). Reproduced, with permission, from Brezis et al. and Brezis et al. 55,56.
	Figure 12. Vasa recta solute permeabilities. [¹⁴C]urea permeability (P_U, ordinate) vs ²²Na permeability (P_Na, abscissa) is shown for outer medullary descending vasa recta (DVR) (OMDVR) isolated from Sprague‐Dawley rats and perfused in vitro. Results are also shown for inner medullary DVR and ascending vasa recta (AVR) (IMDVR, IMAVR) perfused on the surface of the exposed papilla of Munich‐Wistar rats in vivo. The dashed line is identity. P_U and P_Na are highly correlated and nearly equal in inner medullary vasa recta. In contrast, P_U of outer medullary DVR is always very high and is not correlated with P_Na. The dissociation of P_Na and P_U in OMDVR results (at least in part) from the expression of the UTB‐facilitated urea carrier. In separate experiments (not shown), P_U of OMDVR was inhibited by exposure to urea analogues or phloretin. Data reproduced, with permission, from Pallone et al. 516.
	Figure 13. Osmotic water permeability (P_f) of outer medullary descending vasa recta (DVR). (A) P_f was measured in glutaraldehyde fixed rat DVR by measuring the rate of transmural water flux generated by a bath > lumen NaCl gradient. Sequential measurements in controls were stable. In contrast, exposure to p‐chloromercuribenzene sulfonate (pCMBS, 2 mM), an agent that covalently binds to cysteine residues on aquaporin‐1, reduced P_f to nearly zero. In these experiments, glutaraldehyde fixation was necessary to prevent deterioration of the vessel caused by pCMBS and other harsh conditions of the experiment. (B) P_f was measured in AQP1 null (−/−) or replete (+/+) murine DVR by transmural gradients of NaCl, urea, glucose or raffinose. When NaCl was the solute used to drive water flux, deletion of AQP1 reduced P_f from ∼1100 μm/s to nearly zero. Water flux driven by raffinose (MW 564) was markedly reduced by AQP1 deletion (compare AQP1 −/− to +/+), but remained unexpectedly high. Similarly, glucose (MW 180) and urea (MW 60) gradients drove measurable water flux across AQP1 (−/−) DVR. Reproduced, with permission, from Pallone et al. 501,504.
	Figure 14. UTB and urea recycling in the medulla. Schematic of vascular and tubular urea recycling in the kidney. Short and long loops of Henle and vasa recta are shown. The UTA2 urea transporter is expressed in the thin descending limbs of Henle. The UTB urea transporter is expressed in descending vasa recta (DVR) endothelium and red blood cells (not shown). Thin descending limbs of short‐looped nephrons become associated with vascular bundles (see Fig. 9) so that urea recycling from thin limbs to DVR via UTA2 and UTB is accommodated. UTB is not expressed by the ascending vasa recta (AVR) endothelium but AVR are fenestrated and urea permeability is high. Thus urea in AVR plasma and RBCs can readily recycle back to DVR in vascular bundles using UTB in the RBC membrane and DVR endothelium. The UTA1, A3 and A4 collecting duct urea transporters conduct urea from the lumen to the inner medullary interstitium. C, cortex; OS, outer stripe of outer medulla; IS, inner stripe of outer medulla; IM, inner medulla. Reproduced, with permission, from Yang and Bankir 706.
	Figure 15. Effect of AQP1 deletion on predictions of renal medullary interstitial osmolality. A mathematical simulation of the renal medulla was solved to predict interstitial osmolality. Interstitial osmolality is shown as a function of corticomedullary axis (x/liter = 0 is the corticomedullary junction, x/liter = 1 is the papillary tip). Various curves denote predictions for different values of P_f [descending vasa recta (DVR) osmotic water permeability]. P_f was varied between 0 (equivalent to AQP1 deletion) and 2000 μm/s. AQP1 expression in DVR is predicted to enhance concentrating ability by conducting water flux from DVR to interstitium where it is then taken up by ascending vasa recta. The net result is a secondary reduction of blood flow in the deepest regions of the inner medulla (papillary tip). Reproduced, with permission, from Pallone et al. 501.
	Figure 16. Predicted oxygen tension (P_O2) profiles in the rat outer medullary interstitium. The structural organization of the OM is represented by means of four concentric regions centered on a vascular bundle: an innermost region containing the central vascular bundle (R1), where long descending vasa recta are sequestered; a peripheral region of the vascular bundle (R2); a region neighboring the vascular bundle (R3), where most thick ascending limbs reside; and the region most distant from the vascular bundle (R4), where collecting ducts are located. Vertical dotted lines mark the boundary between the outer stripe (OS) and the inner stripe (IS), and x/liter denotes the ratio of the axial coordinate to total length of outer medulla. Model suggests that the OM anatomy has a significant impact on the radial distribution of oxygen. It preserves O₂ delivery to the inner medulla, but limits active Na⁺ reabsorption across medullary thick ascending limbs and thereby decreases the OM urinary concentrating capacity. Reproduced, with permission, from Chen et al. 89.
	Figure 17. Distribution of hematocrit in the kidney. ⁵¹Cr‐RBCs and ¹³¹I‐IgM (plasma volume marker) were simultaneously infused into the kidney. An equilibration period of either 1 or 10 min followed before ligation of the renal artery and vein. The distribution of RBCs and plasma was inferred by measuring activity of the isotopes in tissue and dividing their ratio by the systemic ratio. Results show that the hematocrit of inner medullary blood is lower than that of either whole kidney, cortex, or outer medulla. Data redrawn, with permission, from Rasmussen 561.
	Figure 18. Connexin staining in descending vasa recta. Immunostaining of Cx40. Immunostaining is shown with antibody directed against α‐smooth muscle actin (SMA red) or Cx40 (green). A merged image is shown along with a corresponding white light micrograph. Cx40 showed linear staining confined to the endothelium with very little SMA colocalization. Bar = 10 μm. Reproduced, with permission, from Zhang et al. 725.
	Figure 19. Effect of arginine vasopressin (AVP) on inner medullary blood flow and urine osmolality. To control plasma vasopressin concentrations, decerebrate rats were infused with AVP. Increasing AVP concentration within the physiological range caused a reduction of inner medullary blood flow and an improvement in urinary concentration. * indicates significance from control period (P < .05). Reproduced, with permission, from Franchini and Cowley 189.
	Figure 20. In vitro microperfusion. (A) An afferent arteriole is cannulated with concentric pipettes and perfused toward the glomerulus. Reproduced, with permission, from Hansen et al. (B and C) Perfusion of an isolated descending vasa recta (DVR). Images obtained before (B) and after (C) exposure to angiotensin II (AngII). Compare the thick smooth muscle layer of the afferent arteriole to the sporadically distributed pericyte cell bodies of DVR. Reproduced, with permission, from Hansen et al. and Pallone et al. 233,511.
	Figure 21. Arachidonic acid (AA) metabolites. (A) Abbreviated schematic showing signaling molecules generated from arachadonic acid by cyclo‐oxygenase (COX). Prostaglandins (PG) and thromboxanes (Tx) are vasoactive end products. B. Abbreviated schematic showing signaling molecules generated from the cytochrome P450 metabolism of AA. Hydrolases generate the potent constrictor 20‐hydroxyeicosatetraenoic acid (20‐HETE) and epoxygenases generate the epoxyeicosatrienoic acids that most often function as vasodilators. The lipoxygenase pathway of arachidonic acid metabolism is not shown. Reproduced, with permission, from Pallone and Cao 499.
	Figure 22. Effect of intrarenal infusion of adenosine receptor A1 or A2 subtype agonists. Top and bottom panels show the effect of adenosine agonist infusions on intrarenal blood flow. Cortical and medullary measurements were obtained using laser‐Doppler flowmetry with optical fibers placed on the kidney surface or inserted into the renal parenchyma, respectively. Left and right panels show the respective effects of either A1 or A2 receptor stimulation with subtype‐specific agonists. At time = 0, the A1 agonist N6‐cyclopentyladenosine (left panels) or the A2 agonist CGS‐21680C (right panels) was transiently infused (1 min) into the renal parenchyma. The A1 agonist transiently reduced both cortical and medullary blood flow, while the A2 agonist caused a preferential increase in blood flow to the medulla. Reproduced, with permission, from Agmon et al. 5.
	Figure 23. Autoregulation in different regions of the kidney. An electromagnetic flow device on the renal artery was used to measure total renal blood flow (RBF). Laser‐Doppler flow probes were inserted into the renal parenchyma at various depths to measure regional blood flow in the outer and inner medulla (IM). Total RBF and cortical tissue blood flow shows intact autoregulation (stability of blood flow over a range of perfusion pressure). In contrast, in these volume‐expanded rats (see text), the small fraction of blood flow that reaches the outer or IM is not autoregulated. Reproduced, with permission, from Mattson et al. 410.
	Figure 24. Pressure natriuresis. (A) Medullary blood flow is autoregulated in hydropenic but not volume expanded rats. (B) Renal interstitial hydrostatic pressure (RIHP) is higher and increases to a greater degree with renal perfusion pressure in volume expanded animals. (C) When renal perfusion pressure is increased, urinary sodium excretion (UNaV) increases much more markedly in volume expanded than in hydropenic animals. Reproduced, with permission, from Cowley 108.
	Figure 25. Acute NOS inhibition in the renal medulla. Line graph (left) showing changes in renal cortical and medullary blood flow (measured by laser‐Doppler flowmetry) in response to renal medullary interstitial infusion of the nitric oxide synthase inhibitor NG‐nitro‐l‐arginine methyl ester (L‐NAME, 120 μg/h). Bar graph (right) shows changes in urine volume (UVol) and sodium excretion (UNaV) accompanying medullary interstitial infusion of L‐NAME in the infused kidney and the noninfused contralateral kidney. * indicates significance from control (P < 0.05). Reproduced, with permission, from Mattson et al. 415.
	Figure 26. Chronic influence of renal medullary interstitial infusion of the nitric oxide synthase inhibitor NG‐nitro‐l‐arginine methyl ester (L‐NAME, 8.6 mg/kg/day) on renal medullary blood flow (top), daily sodium balance (middle), and mean arterial blood pressure (bottom) in conscious Sprague Dawley rats. Vertical‐hashed marks indicate the L‐NAME infusion period. * indicates significance from control (P < 0.05). Reproduced, with permission, from Mattson et al. 409.
	Figure 27. Hypothetical mechanisms whereby changes in renal medullary perfusion may lead to an alteration in arterial blood pressure. Reproduced, with permission, from Mattson 404.

Figure 1.

Microcirculation of the renal cortex and medulla. Within the renal cortex, interlobular arteries, derived from the arcuate artery, ascend toward the cortical surface. Superficial and midcortical glomeruli arise at obtuse and right angles, while juxtamedullary glomeruli arise at an acute, recurrent angle from the interlobular artery. The majority of blood flow to the medulla arises from juxtamedullary efferent arterioles. A minor fraction might also be derived from periglomerular shunt pathways. In the outer stripe of the outer medulla (OM), juxtamedullary efferent arterioles give rise to descending vasa recta (DVR) that coalesce with ascending vasa recta (AVR), and sometimes, thin descending limbs of Henle, to form vascular bundles. Vascular bundles are the prominent feature of the inner stripe of the OM. DVR on the periphery of vascular bundles perfuse the interbundle capillary plexus that supplies nephrons (thick‐ascending limbs, collecting ducts (CD), long looped thin descending limbs, not shown). DVR in the center of the bundles continue across the inner‐outer medullary junction to perfuse the inner medulla (IM). In some species, thin descending limbs of short‐looped nephrons migrate toward or become associated with vascular bundles. In the inner medulla, vascular bundles disappear and vasa recta become dispersed with thin loops of Henle and CDs. Blood from the interbundle capillary plexus is returned without rejoining vascular bundles. DVR have a continuous endothelium (inset) and are surrounded by contractile pericytes. Like cortical peritubular capillaries, the AVR endothelium is highly fenestrated. As blood flows toward the papillary tip, NaCl and urea diffuse into DVR and out of AVR. Transmural gradients of NaCl and urea drive water efflux across the DVR wall via aquaporin‐1 water channels.

Reproduced, with permission, from Pallone et al. 514.

Figure 2.

The intra‐arterial cushion. A longitudinal section through an afferent arteriole shows an intra‐arterial cushion at its origin from the interlobular artery (inset, × 160). The cushion protrudes into the lumen of the parent vessel. Smooth muscle cells of the cushion are embedded in a copious matrix (× 4000). Intra‐arterial cushions might affect the relative volume fraction of RBCs vs plasma (hematocrit) that is directed from intralobular arterioles to juxtamedullary glomeruli and renal medulla. It is also conceivable that they regulate the relative distribution of blood flow between the superficial and juxtamedullary cortex (see text).

Reproduced, with permission, from Moffat and Creasey 433.

Figure 3.

Structure and transition of cortical and medullary vessels. The proximal afferent arteriole is composed of at least two layers of smooth muscle cells. The muscularity and size of cortical efferent arterioles differ with location. Note the difference between the superficial and juxtamedullary efferent arterioles. The juxtamedullary efferent arteriole is larger, has a thicker, multilayered media, and its endothelium is composed of more numerous endothelial cells. In the illustration, a descending vas rectum (DVR) in a vascular bundle is adjacent to three fenestrated ascending vasa recta (AVR). The DVR wall is surrounded by a contractile pericyte. At the bottom right, DVR and AVR from the inner medulla are shown. Inner medullary DVR have a continuous endothelium through most of their length as pericytes become scarcer with medullary depth. Terminal DVR and the entire AVR wall are fenestrated.

Reproduced, with permission, from Jamison and Kriz 291.

Figure 4.

Distribution of descending vasa recta (DVR) pericytes. (A and B) Immunofluorescent staining of DVR pericytes using anti α‐smooth muscle actin as primary antibody. The pericytes are present on DVR from outer medullary vascular bundles (Panel A) and those from the inner medulla (Panel B) (1000 ×). (C) Low power image of immunofluorescent staining of DVR pericytes using anti α‐smooth muscle actin antibody. Some vessels show pericytes throughout their length to the papillary tip. Black vessels are filled with India ink (× 100).

Reproduced, with permission, from Park et al. 529.

Figure 5.

Electron micrograph of descending vasa recta (DVR) and ascending vasa recta (AVR). Electron micrograph of DVR and AVR in rat vascular bundles. DVR have a continuous endothelium and AVR are fenestrated. Note the minimal interstitium that exists between vessels in this region (× 12,400).

Reproduced, with permission, from Pallone et al. 516.

Figure 6.

Arterial injection of Psammomys obesus. (A) Photograph of the microvasculature of the desert rodent Psammomys obesus obtained by injecting the arteries of the kidney with Microfil and digesting the tissue. The distinct arteriolar patterns of the cortex, outer and inner medulla are apparent. In Psammomys, the separation of the outer medulla into vascular bundles and the dense capillary plexus of the interbundle region (*) is striking because vasa recta coalesce into giant vascular bundles. OM, outer medulla; IM, inner medulla. Designations on the original figure are C = cortex, TR = transitional region (outer stripe of the outer medulla), IS = inner stripe of the outer medulla, IZ = inner zone (inner medulla).

Reproduced, with permission, from Bankir et al.. (B and C) India ink injection study of vascular bundles in the outer medulla of the rat. In contrast to Psammomys, individual vascular bundles do not coalesce into giant bundles. The bundles are more evenly dispersed throughout the inner stripe of the outer medulla. This pattern is typical of many mammalian species including the rat, mouse and human. Reproduced, with permission, from Bankir et al., Moffat and Fourman) (29, 33).

Figure 7.

Tubular‐vascular relationships in the outer medulla (OM). Organization of the inner stripe of the OM. Top and bottom panels show longitudinal and cross‐sectional views, respectively. The extent to which the thin descending limbs of Henle (tDLH) of short looped nephrons associate with vascular bundles varies between species. In the rabbit, no association exists, whereas in the rat and mouse, the tDLH migrates to the periphery or becomes incorporated within vascular bundles, respectively. Abbreviations: VB, vascular bundle; IB, interbundle region; CD, collecting duct; 1 and 2, thin descending and thick ascending limbs of long‐looped nephrons; 3 and 4, thin descending and thick ascending limbs of short‐looped nephrons.

Reproduced, with permission, from Bankir and de Rouffignac 29.

Figure 8.

Renal medullary interstitial cells (RMICs). RMICs appear to be tethered between thin limbs and vasa recta in the inner medulla. Interstitial spaces lie between the cells and the cells are stacked like rungs of a ladder. RMICs are contractile and secrete vasoactive paracrine agents (see text). The stacked arrangement of RMICs in some species has been suggested to help retard axial diffusion that would otherwise tend to dissipate corticomedullary gradients of NaCl and urea. AVR, venous or ascending vasa recta. Arrows point to lipid droplets within RMIC.

Reproduced, with permission, from Lemley and Kriz 355.

Figure 9.

Tubular vascular relationships and collecting duct clusters in the inner medulla. (A) A CD cluster (blue) is surrounded by descending vasa recta (DVR) (red) and thin DLH (green). Neither DVR nor thin DLH are incorporated into the center of the cluster. (B) A CD cluster (blue) has both ascending vasa recta (AVR) (red) and thin ALH (green) in its surroundings and within the cluster. (C) Idealized cross‐sectional depiction of a CD cluster (blue) in relationship to AVR (red) and thin ALH (green). AVR and thin ALH are diffusely distributed around and within the CD cluster. (D) Idealized cross‐sectional depiction of thin DLH (purple) and DVR (aqua) surrounding open regions in which CD clusters reside.

Reproduced, with permission, from Pannabecker and Dantzler 522.

Figure 10.

Relationships of vasa recta and loops of Henle to collecting duct clusters. (A) Three‐dimensional reconstruction of single CD segment (blue) with multiple ascending vasa recta (AVR) (red). Top: 90° axial rotation of segments shown in adjacent panels. Scale bar, 100 μm. (B) Electron micrographs showing transverse sections of CDs and AVR from 1.5 mm (i, ii, and iv) and 4 mm (iii) below the base of the IM. i: CD surrounded by 4 AVR (*). Other tubular structures surrounding the CD are ATLs. Scale bar, 10 μm. ii: AVR abuts CD with minimal direct contact. Scale bar, 1 μm. iii: AVR abuts CD with microvillus (arrow). IS, interstitium. Scale bar, 1 μm. iv: AVR abuts CD with microvilli (arrows). Scale bar, 1 μm.

Reproduced, with permission, from Pannabecker and Dantzler 522.

Figure 11.

Hemodynamic effects on intrarenal oxygenation. Intrarenal oxygen tension (pO2) was measured in the cortex and medulla with a microelectrode. Cortical pO2 falls and medullary pO2 increases during an episode of hypotension induced by either hemorrhage, aortic ligation, or nitroprusside infusion (Panel A). Inhibition of transport in the thick ascending limb of Henle with a loop diuretic (Panel B) increases basal pO2 in the medulla (compare to Panel A) and eliminates the effect of hypotension to raise medullary pO2. Inhibition of vasodilatory prostaglandins and nitric oxide, or blockade of adenosine receptors reduces basal pO2 in the medulla and accentuates the increase in pO2 caused by hypotension (Panel C). Intrarenal tissue pO2 decreases with medullary depth (Panel D). * indicates significance from baseline (P < .001).

Reproduced, with permission, from Brezis et al. and Brezis et al. 55,56.

Figure 12.

Vasa recta solute permeabilities. [¹⁴C]urea permeability (P_U, ordinate) vs ²²Na permeability (P_Na, abscissa) is shown for outer medullary descending vasa recta (DVR) (OMDVR) isolated from Sprague‐Dawley rats and perfused in vitro. Results are also shown for inner medullary DVR and ascending vasa recta (AVR) (IMDVR, IMAVR) perfused on the surface of the exposed papilla of Munich‐Wistar rats in vivo. The dashed line is identity. P_U and P_Na are highly correlated and nearly equal in inner medullary vasa recta. In contrast, P_U of outer medullary DVR is always very high and is not correlated with P_Na. The dissociation of P_Na and P_U in OMDVR results (at least in part) from the expression of the UTB‐facilitated urea carrier. In separate experiments (not shown), P_U of OMDVR was inhibited by exposure to urea analogues or phloretin.

Data reproduced, with permission, from Pallone et al. 516.

Figure 13.

Osmotic water permeability (P_f) of outer medullary descending vasa recta (DVR). (A) P_f was measured in glutaraldehyde fixed rat DVR by measuring the rate of transmural water flux generated by a bath > lumen NaCl gradient. Sequential measurements in controls were stable. In contrast, exposure to p‐chloromercuribenzene sulfonate (pCMBS, 2 mM), an agent that covalently binds to cysteine residues on aquaporin‐1, reduced P_f to nearly zero. In these experiments, glutaraldehyde fixation was necessary to prevent deterioration of the vessel caused by pCMBS and other harsh conditions of the experiment. (B) P_f was measured in AQP1 null (−/−) or replete (+/+) murine DVR by transmural gradients of NaCl, urea, glucose or raffinose. When NaCl was the solute used to drive water flux, deletion of AQP1 reduced P_f from ∼1100 μm/s to nearly zero. Water flux driven by raffinose (MW 564) was markedly reduced by AQP1 deletion (compare AQP1 −/− to +/+), but remained unexpectedly high. Similarly, glucose (MW 180) and urea (MW 60) gradients drove measurable water flux across AQP1 (−/−) DVR.

Reproduced, with permission, from Pallone et al. 501,504.

Figure 14.

UTB and urea recycling in the medulla. Schematic of vascular and tubular urea recycling in the kidney. Short and long loops of Henle and vasa recta are shown. The UTA2 urea transporter is expressed in the thin descending limbs of Henle. The UTB urea transporter is expressed in descending vasa recta (DVR) endothelium and red blood cells (not shown). Thin descending limbs of short‐looped nephrons become associated with vascular bundles (see Fig. 9) so that urea recycling from thin limbs to DVR via UTA2 and UTB is accommodated. UTB is not expressed by the ascending vasa recta (AVR) endothelium but AVR are fenestrated and urea permeability is high. Thus urea in AVR plasma and RBCs can readily recycle back to DVR in vascular bundles using UTB in the RBC membrane and DVR endothelium. The UTA1, A3 and A4 collecting duct urea transporters conduct urea from the lumen to the inner medullary interstitium. C, cortex; OS, outer stripe of outer medulla; IS, inner stripe of outer medulla; IM, inner medulla.

Reproduced, with permission, from Yang and Bankir 706.

Figure 15.

Effect of AQP1 deletion on predictions of renal medullary interstitial osmolality. A mathematical simulation of the renal medulla was solved to predict interstitial osmolality. Interstitial osmolality is shown as a function of corticomedullary axis (x/liter = 0 is the corticomedullary junction, x/liter = 1 is the papillary tip). Various curves denote predictions for different values of P_f [descending vasa recta (DVR) osmotic water permeability]. P_f was varied between 0 (equivalent to AQP1 deletion) and 2000 μm/s. AQP1 expression in DVR is predicted to enhance concentrating ability by conducting water flux from DVR to interstitium where it is then taken up by ascending vasa recta. The net result is a secondary reduction of blood flow in the deepest regions of the inner medulla (papillary tip).

Reproduced, with permission, from Pallone et al. 501.

Figure 16.

Predicted oxygen tension (P_O2) profiles in the rat outer medullary interstitium. The structural organization of the OM is represented by means of four concentric regions centered on a vascular bundle: an innermost region containing the central vascular bundle (R1), where long descending vasa recta are sequestered; a peripheral region of the vascular bundle (R2); a region neighboring the vascular bundle (R3), where most thick ascending limbs reside; and the region most distant from the vascular bundle (R4), where collecting ducts are located. Vertical dotted lines mark the boundary between the outer stripe (OS) and the inner stripe (IS), and x/liter denotes the ratio of the axial coordinate to total length of outer medulla. Model suggests that the OM anatomy has a significant impact on the radial distribution of oxygen. It preserves O₂ delivery to the inner medulla, but limits active Na⁺ reabsorption across medullary thick ascending limbs and thereby decreases the OM urinary concentrating capacity.

Reproduced, with permission, from Chen et al. 89.

Figure 17.

Distribution of hematocrit in the kidney. ⁵¹Cr‐RBCs and ¹³¹I‐IgM (plasma volume marker) were simultaneously infused into the kidney. An equilibration period of either 1 or 10 min followed before ligation of the renal artery and vein. The distribution of RBCs and plasma was inferred by measuring activity of the isotopes in tissue and dividing their ratio by the systemic ratio. Results show that the hematocrit of inner medullary blood is lower than that of either whole kidney, cortex, or outer medulla.

Data redrawn, with permission, from Rasmussen 561.

Figure 18.

Connexin staining in descending vasa recta. Immunostaining of Cx40. Immunostaining is shown with antibody directed against α‐smooth muscle actin (SMA red) or Cx40 (green). A merged image is shown along with a corresponding white light micrograph. Cx40 showed linear staining confined to the endothelium with very little SMA colocalization. Bar = 10 μm.

Reproduced, with permission, from Zhang et al. 725.

Figure 19.

Effect of arginine vasopressin (AVP) on inner medullary blood flow and urine osmolality. To control plasma vasopressin concentrations, decerebrate rats were infused with AVP. Increasing AVP concentration within the physiological range caused a reduction of inner medullary blood flow and an improvement in urinary concentration. * indicates significance from control period (P < .05).

Reproduced, with permission, from Franchini and Cowley 189.

Figure 20.

In vitro microperfusion. (A) An afferent arteriole is cannulated with concentric pipettes and perfused toward the glomerulus.

Reproduced, with permission, from Hansen et al. (B and C) Perfusion of an isolated descending vasa recta (DVR). Images obtained before (B) and after (C) exposure to angiotensin II (AngII). Compare the thick smooth muscle layer of the afferent arteriole to the sporadically distributed pericyte cell bodies of DVR. Reproduced, with permission, from Hansen et al. and Pallone et al. 233,511.

Figure 21.

Arachidonic acid (AA) metabolites. (A) Abbreviated schematic showing signaling molecules generated from arachadonic acid by cyclo‐oxygenase (COX). Prostaglandins (PG) and thromboxanes (Tx) are vasoactive end products. B. Abbreviated schematic showing signaling molecules generated from the cytochrome P450 metabolism of AA. Hydrolases generate the potent constrictor 20‐hydroxyeicosatetraenoic acid (20‐HETE) and epoxygenases generate the epoxyeicosatrienoic acids that most often function as vasodilators. The lipoxygenase pathway of arachidonic acid metabolism is not shown.

Reproduced, with permission, from Pallone and Cao 499.

Figure 22.

Effect of intrarenal infusion of adenosine receptor A1 or A2 subtype agonists. Top and bottom panels show the effect of adenosine agonist infusions on intrarenal blood flow. Cortical and medullary measurements were obtained using laser‐Doppler flowmetry with optical fibers placed on the kidney surface or inserted into the renal parenchyma, respectively. Left and right panels show the respective effects of either A1 or A2 receptor stimulation with subtype‐specific agonists. At time = 0, the A1 agonist N6‐cyclopentyladenosine (left panels) or the A2 agonist CGS‐21680C (right panels) was transiently infused (1 min) into the renal parenchyma. The A1 agonist transiently reduced both cortical and medullary blood flow, while the A2 agonist caused a preferential increase in blood flow to the medulla.

Reproduced, with permission, from Agmon et al. 5.

Figure 23.

Autoregulation in different regions of the kidney. An electromagnetic flow device on the renal artery was used to measure total renal blood flow (RBF). Laser‐Doppler flow probes were inserted into the renal parenchyma at various depths to measure regional blood flow in the outer and inner medulla (IM). Total RBF and cortical tissue blood flow shows intact autoregulation (stability of blood flow over a range of perfusion pressure). In contrast, in these volume‐expanded rats (see text), the small fraction of blood flow that reaches the outer or IM is not autoregulated.

Reproduced, with permission, from Mattson et al. 410.

Figure 24.

Pressure natriuresis. (A) Medullary blood flow is autoregulated in hydropenic but not volume expanded rats. (B) Renal interstitial hydrostatic pressure (RIHP) is higher and increases to a greater degree with renal perfusion pressure in volume expanded animals. (C) When renal perfusion pressure is increased, urinary sodium excretion (UNaV) increases much more markedly in volume expanded than in hydropenic animals.

Reproduced, with permission, from Cowley 108.

Figure 25.

Acute NOS inhibition in the renal medulla. Line graph (left) showing changes in renal cortical and medullary blood flow (measured by laser‐Doppler flowmetry) in response to renal medullary interstitial infusion of the nitric oxide synthase inhibitor NG‐nitro‐l‐arginine methyl ester (L‐NAME, 120 μg/h). Bar graph (right) shows changes in urine volume (UVol) and sodium excretion (UNaV) accompanying medullary interstitial infusion of L‐NAME in the infused kidney and the noninfused contralateral kidney. * indicates significance from control (P < 0.05).

Reproduced, with permission, from Mattson et al. 415.

Figure 26.

Chronic influence of renal medullary interstitial infusion of the nitric oxide synthase inhibitor NG‐nitro‐l‐arginine methyl ester (L‐NAME, 8.6 mg/kg/day) on renal medullary blood flow (top), daily sodium balance (middle), and mean arterial blood pressure (bottom) in conscious Sprague Dawley rats. Vertical‐hashed marks indicate the L‐NAME infusion period. * indicates significance from control (P < 0.05).

Reproduced, with permission, from Mattson et al. 409.

Figure 27.

Hypothetical mechanisms whereby changes in renal medullary perfusion may lead to an alteration in arterial blood pressure.

Reproduced, with permission, from Mattson 404.

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Article Title:	Renal Medullary Circulation
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Thomas L. Pallone, Aurélie Edwards, David L. Mattson. Renal Medullary Circulation. Compr Physiol 2012, 2: 97-140. doi: 10.1002/cphy.c100036

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