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The Renal Microcirculation

L Gabriel Navar, William J Arendshorst, Thomas L Pallone, Edward W Inscho, John D Imig, P Darwin Bell

10.1002/cphy.cp020413

Source: Supplement 9: Handbook of Physiology, The Cardiovascular System, Microcirculation

Originally published: 2008

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Introduction
2 Structural‐Functional Aspects Unique to the Renal Microcirculation
2.1 Microvasculature of the renal cortex
2.2 Glomerular and peritubular capillary networks
2.3 Renal interstitium and lymphatics
2.4 Microvasculature of the renal medulla
2.5 Juxtaglomerular complex and macula densa
2.6 Innervation of the renal vascular structures
3 Fluid and Solute Transcapillary Exchange in Renal Microcirculation
3.1 Glomerular ultrafiltration
3.2 Restricted permeability to macromolecules in glomerular capillaries
3.3 Peritubular capillaries and uptake of tubular reabsorbate
3.4 Regulation of the filtration coefficient
3.5 Transport of solutes and water in medullary microvasculature
4 Vascular Activating Mechanisms and Intrinsic Control of Renal Microcirculation
4.1 Membrane activating mechanisms
4.2 Mechanosensitive responses and renal autoregulation
4.3 TGF mechanism
5 Endothelial Interactions with Renal Vasculature
5.1 Endothelial‐derived vasoactive factors
5.2 Nitric oxide
5.3 Endothelin and renal hemodynamics
5.4 Endothelin effects on renal microcirculation
5.5 Heme oxygenase and CO
5.6 Reactive oxygen species
6 Renin‐Angiotensin System
6.1 Intrarenal formation of Ang II
6.2 Intrarenal angiotensin receptors
6.3 Actions of Ang II on renal microvasculature and renal hemodynamics
6.4 Differential activation and signal transduction mechanisms on afferent and efferent arterioles
6.5 Responses to ACE inhibitors and Ang II receptor blockers
6.6 Actions of intrarenally formed Ang II and renal interstitial Ang II
6.7 Modulation of TGF responsiveness by Ang II
6.8 Synergistic interactions between renal vascular and tubular effects of Ang II
7 Arachidonic Acid Related Paracrine Factors: Cyclooxygenase, Lipoxygenase, Cytochrome P450 Pathways
7.1 Enzymes that metabolize eicosanoids
7.2 Renal microcirculatory actions of COX metabolites
7.3 Renal microcirculatory actions of CYP metabolites
7.4 Renal microcirculatory actions of LOX metabolites
7.5 Renal microvascular interactions between hormonal and paracrine factors and eicosanoids
7.6 Role of eicosanoids in renal autoregulation
7.7 Conclusions
8 Purinergic Factors Regulating the Renal Microcirculation
8.1 Overview of purinoceptors
8.2 Purinoceptors and their expression in the kidney
8.3 Purinoceptors and renal hemodynamics
8.4 Purinoceptors and the renal microcirculation: single vessel studies
8.5 Purinoceptors and renal autoregulation and TGF
9 Mechanisms Regulating Medullary Microcirculation
9.1 Introduction
9.2 Reduction of intramedullary hematocrit
9.3 The unique requirements of renal medullary perfusion
9.4 Autoregulation and pressure natriuresis
9.5 Diuresis and vasopressin
9.6 Angiotensin and medullary perfusion
9.7 Nitric oxide
9.8 Reactive oxygen species
9.9 Carbon monoxide
9.10 Endothelial‐derived hyperpolarizing factor
9.11 Arachadonic acid metabolite
9.12 Kinins
9.13 Adenosine
9.14 Endothelins
10 Neural Factors and Catecholamines
10.1 Innervation of the renal vascular structures
10.2 Neural effects on renal hemodynamics and microcirculation
10.3 Segmental vascular resistance and glomerular hemodynamics
10.4 Effects of renal nerves on autoregulation
10.5 Neural interactions with paracrine factors
10.6 Co‐neurotransmitters
10.7 Afferent renal nerves
11 Concluding Comments
Figure 1. Figure 1.

Microvascular anatomy of the kidney. Outer, middle and juxtamedullary nephrovascular units and outer medullary bundles are shown. In the left panel, nephrons are shown without the vascular structures with distal nephron segments in darker color. The center panel shows only the vascular structures with arterial vessels in red and venous vessels in blue. The right panel shows the combined nephro‐vascualr units. Representative efferent and peritubular capillary systems for only a few nephrons are shown to illustrate the different patterns. Peritubular capillary blood vessels in the cortex are derived from superficial and mid‐cortical nephrons, while juxtamedullary nephrons gave rise to descending vasa recta (DVR). DVR from bundle periphery supply the interbundle capillary plexus while those in the center supply blood to the inner medulla. See text for further detail. From Ref. 20. (See page 14 in colour section at the back of the book)
Figure 2. Figure 2.

Renal vasculature filled with red polymer and single juxtamedullary nephron filled with yellow polymer showing a long loop of Henle

(Courtesy of Daniel Casellas). (See page 14 in colour section at the back of the book)
Figure 3. Figure 3.

Microvascular structures of cortex. (A) depicts an isolated renal corpuscle (RC) with attached AA. The groove (asterisk) is the point of attachment to the macula densa. (B) is a vascular cast of a glomerular capillary system. (C) is a scanning EM of a single glomerular capillary revealing all cell types including the endothelium and endothelial fenestrations, the basement membrane and interdigitating podocyte foot processes. A mesangial cell is seen in intercapillary position. (D) shows a peritubular capillary of the outer cortex. Characteristically, the endothelial cells are flattened with many small fenestrae bridged by a diaphragm and an attenuated basement membrane (BM). From Ref. 2.
Figure 4. Figure 4.

Comparison of DVR and AVR wall characteristics. 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.

Reproduced with permission from Ref. 61
Figure 5. Figure 5.

Tubular vascular relationships and collecting duct clusters in the inner medulla. (A) A CD cluster (blue) is surrounded by 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 AVR (red) and thin ALH (green) in its surroundings and within the cluster. (C) Idealized crossectional 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. From Ref. 62,78. See page 15 in colour section at the back of the book)
Figure 6. Figure 6.

Close relationship of ascending vasa recta and collecting ducts in the inner medulla. (A) Four AVR (red) surround a single inner medullary CD (blue). Successive panels show rotations as specified by the idealized depiction above each panel. (B) Transmission electron micrograph of an inner medullary CD surrounded by four AVR that abutt the abluminal surface (AVR lumens identified with asterisks). Bar = 1 micron. From Ref. 62. (See page 15 in colour section at the back of the book)
Figure 7. Figure 7.

In vitro tubuloglomerular feedback visualized using multiphoton laser‐scanning fluorescence image of the living isolated perfused cortical thick ascending limb (cTAL) with attached glomerulus (G) labeled with membrane staining dye TMA‐DPH. Note the macula densa (MD) cells

(Courtesy of P. D. Bell). (See page 15 in colour section at the back of the book)
Figure 8. Figure 8.

Multicolor labeling of the in vitro microperfused juxtaglomerular apparatus with attached glomerulus. Cell membranes of tubular epithelium (cortical thick ascending limb [cTAL] containing the macula densa), vascular endothelium of afferent arteriole (AA), and glomerulus (G) are labeled with R18 (red), renin granules with quinacrine (green), and cell nuclei with Hoechst 33342 (blue). From Ref. 94. (See page 15 in colour section at the back of the book)
Figure 9. Figure 9.

Depiction of the hydraulic and oncotic forces responsible for filtration of fluid of the glomerulus and reabsorption of fluid into the peritubular capillaries. Representative values for humans are provided. Insert shows representative profiles in the net hydrostatic pressure gradient and glomerular plasma colloid osmotic pressure (πg) along the length of the glomerular capillaries. Profile A represents continued filtration throughout glomerular capillaries while profile B represents achievement of filtration pressure equilibrium. Profile C represents the change in response to volume expansion and vasodilation. Revised from Ref. 1.
Figure 10. Figure 10.

Passage of macromolecules across glomerular capillaries. Representative sieving curves for several test molecules in the glomerular circulation. The curve representing neutral molecules is based on data obtained with use of polyvinylpyrrolidone and neutral dextran. The curves for anionic and cationic molecules are based on studies with charged dextrans. Also shown are the sieving values for neutral horseradish peroxidase (neutral HRP) and for albumin. The smaller molecules are shown to have a sieving coefficient of 1.0. Revised from Ref. 1.
Figure 11. Figure 11.

Movement of water NaCl and urea in the renal medullary microcirculation. The majority of blood flow to the medulla arises from juxtamedullary efferent arterioles with a minor fraction from periglomerular shunt pathways. In the outer stripe of the outer medulla, juxtamedullary efferent arterioles give rise to DVR that coalesce with AVR to form vascular bundles which are the prominent feature of the inner stripe of the outer medulla. DVR on the periphery of vascular bundles perfuse the interbundle capillary plexus. DVR in the center of the bundles continue to perfuse the inner medulla. Vascular bundles disappear in the inner medulla and VR because dispersed with thin loops of Henle and collecting ducts. DVR have a continuous endothelium (inset) and are surrounded by contractile pericytes. In contrast, 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 Ref. 86
Figure 12. Figure 12.

Aquaporin‐1 mediated osmotic water permeability (Pf) of DVR. (A) Pf 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 Pf to nearly zero. From Ref. 217. (B) Pf 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 Pf from ∼1100μ/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 Refs. 216,217
Figure 13. Figure 13.

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 DVR endothelium and red blood cells (not shown). Thin descending limbs of short looped nephrons become associated with vascular bundles so that urea recycling from thin limbs to DVR via UTA2 and UTB is accommodated. UTB is not expressed by the AVR endothelium but AVR are fenestrated and urea permeability is high. Thus urea in AVR plasma and RBCs readily recycles back to DVR in vascular bundles using UTB in the RBC membrane and DVR endothelium. The UTAl, 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 Ref. 244
Figure 14. Figure 14.

Characteristic autoregulatory relationships between renal arterial pressure and renal blood flow, glomerular filtration rate, intrarenal pressures and segmental vascular resistances. PG is glomerular capillary pressure, PPT is proximal tubular pressure, PC is parttibular capillary pressure, and Pt is renal interstitial fluid pressure. Revised from Ref. 1.
Figure 15. Figure 15.

Autoregulatory responses in afferent arteriolar diameter and blood flow to changes in perfusion pressure in in vitro juxtamedullary nephron preparation with intact myogenic and TGF mechanisms and after elimination of TGF mechanism. Control (•) responses were observed with intact flow to macula densa, TGF was interrupted by transection of loops of Henle (papillectomy) (○), and residual myogenic mechanism was then blocked with 10μM diltiazem (▪). *p < 0.05 compared with respective basal value at 100mmHg. p < 0.01 compared with control condition at a similar pressure (Modified from Ref. 292).
Figure 16. Figure 16.

Absolute and relative afferent arteriolar dynamic responses to pressure step from 100 to 150mmHg at differing levels of TGF activity obtained in juxtamedullary nephron preparation. The responses with intact flow to the macula densa are shown as open circles (O). The responses during acetazolamide‐induced enhancement of TGF activity are shown as closed circles (•). The responses after cessation of distal flow imposed by transection of the loops of Henle are shown as closed triangles (▴). (Modified from Ref. 478 and unpublished observations).
Figure 17. Figure 17.

Tubuloglomerular feedback mechanism. Micropuncture procedures used to assess TGF responses (left) and representative relationships between distal nephron volume delivery and single‐nephron GFR responses. Effects of some agents that decrease sensitivity of TGF responses and agents that increase sensitivity of TGF responses are indicated. NOS. nitric oxide synthase; HETE, 20‐hydroxyeico‐satetraenoic acid; PGI2, prostacyclin, Modified from Ref, 473, (See page 16 in colour section at the back of the book)
Figure 18. Figure 18.

Overview of apical and basolateral membrane transport systems in macula densa cell. (Modified from Ref, 521).
Figure 19. Figure 19.

Release of ATP from macula densa cells. PCI2 cells loaded with fura 2 were positioned in close proximity to the basolateral aspect of macula densa cells with attached ascending limb. In response to increases in luminal NaCl concentration the increased fluorescence reflected release of ATP, ATP release was prevented by furosemide in lumen. Suramin in bath was used to block P2 receptors demonstrating specificity of the response, From Ref. 556, Illustrtion by E. Inscho, (See page 16 in colour section at the back of the book)
Figure 20. Figure 20.

(A) Relationships between luminal NaCl, TGF responses and release of ATP, NO and PGE2 from macula densa cells. Increases in luminal NaCl concentration lead to decreases in stop flow pressure (PSF) reflecting predominant afferent arteriolar constriction and leading to increases in ATP causing vasoconstriction partially compensated by increases in nitric oxide. In contrast. PGE2 release is greater at low NaCl concentrations and decreases with increases in luminal NaCl concentration. (B) Cartoon of macula densa cell signaling molecules and actions on adjoining extraglomerular mesangial cells and arteriolar vascular smooth muscle cells (provided by P. D. Bell).
Figure 21. Figure 21.

Effects of NOS inhibition with nitro‐L‐arginine on autoregulatory responses of renal blood flow (RBF), cortical blood flow (CBF), MBF, and glomerular filtration rate (GFR). Control responses are shown as open circles (○). NOS inhibition, shown as closed circles (•), reduced RBF, CBF and MBF without changing GFR, but autoregulatory capability remained intact. The responses to a NO donor, s‐nitroso‐n‐acetylpenicillamine (SNAP) are shown as open triangles and restored the flows back to control levels. From Ref. 680.
Figure 22. Figure 22.

Effects of L‐SMTC (nNOS inhibitor) on afferent arteriolar diameters of juxtamedullary nephron preparation in microns. Arteriolar responses to L‐SMTC were performed using different groups of the kidneys; that is control kidneys (open circle), papillectomized kidneys (open triangle), acetazolamide‐treated kidneys (closed circle), and papillectomized kidneys treated with acetazolamide (closed triangle). nNOS inhibition reduced both afferent and efferent arteriolar diameters and this response was enhanced when distal delivery was increased by acetazolamide. After interruption of distal delivery, the vasoconstriction in response to L‐SMTC was markedly reduced even during treatment with acetazolamide. From Ref. 746.
Figure 23. Figure 23.

(A) Influence of endogenous ET‐1 on renal blood flow in anesthetized Sprague‐Dawley rats. Effect of ET receptor antagonism on basal renal hemodynamics. Blocking ETA receptors increased RBF while blocking ETB receptors decreased RBF. Data from Ref. 735. (B) Acute renal vasoconstriction produced by exogenous ET‐1, ET‐1 + the ETA receptor antagonist BQ123, ET‐1 + the ETB receptor antagonist BQ‐788, and ETB receptor stimulation with the selective agonists S6C or IRL‐1620. All agents were either injected or infused into the renal artery of anesthetized Sprague‐Dawley rats. *p < 0.01 vs. ET‐1 response. Data from Ref. 833.
Figure 24. Figure 24.

Enzymatic cascade of the renin angiotensin system. (Modified from Navar et al., In: Molecular Mechanisms in Hypertension, edited by Re R, DiPette DJ, Schiffrin EL and Sowers JR. Taylor & Francis Group, 2006, p. 3–14).
Figure 25. Figure 25.

Renal vascular actions of AT 1 and AT2 receptors.
Figure 26. Figure 26.

Role of L and T‐type Ca2+ channels in Ang II‐mediated afferent and efferent arteriolar vasoconstriction. The vasoconstrictor effects of Ang II on afferent arterioles are blocked by both L‐type and T‐type Ca2+ channel blockers. In contrast, the efferent vasoconstrictor effects of Ang II are not blocked by L‐type Ca2+ channel blockers, but are blocked by T‐type Ca2+ channel blockers. Data compiled from Refs. 288,295.
Figure 27. Figure 27.

Arachidonic acid metabolism by COX, CYP and LOX pathways. COX enzymes generate PGH2 that can be metabolized by synthases to from TXA2, PGE2 and PGI2. CYP enzymes can generate HETEs and EETs. EETs can be hydrolyzed by SEH to form DHETEs. LOX enzymes generate HETEs, LTs, and LXs.
Figure 28. Figure 28.

Endothelial eicosanoids mediate renal microvascular dilation. Diagram of renal microvessel depicting bradykinin‐mediated endothelial generation of COX and CYP products that lead to relaxation of the adjacent vascular smooth muscle cells. (See page 17 in colour section at the back of the book)
Figure 29. Figure 29.

Renal microvascular eicosanoids mediate constriction. Diagram of renal microvessel depicting vasoconstrictor‐mediated generation of COX, LOX and CYP products that contribute to the vasoconstriction response. (See page 17 in colour section at the back of the book)
Figure 30. Figure 30.

Purinoceptors (P1 and P2 receptors) and postulated intracellular cascades in renal vascular smooth muscle cells. Mechanisms for activation of P1 and P2 purinoceptors by adenosine monophosphate (AMP), adenosine, adenosine triphosphate (ATP) and adenosine diphosphate (ADP), respectively as shown in arrows. Gp, GTP‐binding proteins; Gi, inhibitory G‐protein; Gs, stimulatory G‐protein; IP3, inositol‐1,4,5‐triphosphate: SR, sarcoplasmic reticulum; PLC, phospholipase C; VOC, voltage‐operated calcium channel; ROC, receptor‐operated calcium channel; cAMP, cyclic adenosine monphosphate; ECTO‐5′‐NT, ecto‐5′‐nucleotidase. Symbols (+), stimulation; (−), inhibition. (See page 17 in colour section at the back of the book)
Figure 31. Figure 31.

Afferent and efferent arteriolor responses to ATP in blood‐perfused rat juxtamedullary nephron preparation. The diameter of the afferent arteriole decreases rapidly within a few seconds in response to superfusion with ATP and then increases slightly but remains significantly smaller than control (black circles). The efferent arterioles do not respond even to high concentration of ATP (gray circles). Data taken from Ref. 674.
Figure 32. Figure 32.

Relationships between renal arterial pressure and renal vascular resistance (top left) and renal interstitial fluid ATP concentration (bottom left). Renal interstitial ATP concentrations decrease consistently in response to reductions in RAP. The changes in autoregulatory related changes in renal vascular resistance are positively correlated with the changes in renal interstitial fluid ATP concentrations. These data demonstrate an association between the autoregulatory adjustments in RVR and the interstitial ATP concentration. (From Ref. 1418). Renal interstitial concentrations of ATP were decreased consistently in response to reductions in RAP. Interestingly, changes in ATP concentration were highly correlated with the changes in the autoregulatory associated alterations in renal vascular resistance. Thus, these data demonstrated an association between the autoregulatory adjustments in RVR and the interstitial ATP concentration, and support the hypothesis that RIF ATP is involved in the mechanism of renal autoregulation.
Figure 33. Figure 33.

Effect of the P2X1 receptor blocker, NF279, on afferent arteriolar responses to increases in renal perfusion pressure (RPP). The diameter of the afferent arterioles was significantly decreased in response to increasing RPP during control period (black circles). NF 279 inhibited the pressure‐mediated afferent arteriolar response (grey circles). Each point represents mean vessel diameter measured at 12‐s intervals throughout each pressure period, *p < 0.05 vs. diameter at 100 mmHg. Data taken from Ref. 550.
Figure 34. Figure 34.

Effect of P2X blocker NF279 on the afferent arteriolar response to the A1 agonist N6‐cyclopentyl adenosine (CPA) from P2X1 knockout mouse kidney. Afferent arterioles constricted in response to administration of CPA in the absence (black circles) and presence of NF279 (grey circles). *p < 0.05 vs. diameter at 100 mmHg. Data taken from Ref. 550.
Figure 35. Figure 35.

Intrarenal hematocrit. 51Cr‐RBC's 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 RBC's and plasma were inferred by measuring activity of the isotopes in tissue and dividing their ratio by the systemic ratio. The hematocrit of inner medullary blood is lower than that either whole kidney, cortex or outer medulla. Data redrawn with permission from Ref. 1457. Rasmussen S.N. Intrarenal red cell and plasma volumes in the nondiuretic rat. Pflugers Archives 342: 61–72, 1973.
Figure 36. Figure 36.

Periglomerular shunts. The afferent arteriole (AA) of juxtamedullary glomeruli occasionally give rise to a side branch (AV) which forms descending vasa recta (VR). The efferent arteriole (EA) of the juxtamedullary glomerulus is visible (arrowhead), 16m sphere; bar, 100m. Thus, it is probable that some blood flow that reaches the renal medulla bypasses juxtamedullary glomeruli by shunts such as the one illustrated, but the overall fraction of medullary blood flow derived from shunts is probably small (i.e. < 10%).

Reproduced with permission from Ref. 28
Figure 37. Figure 37.

Renal autoregulation in different regions of volume expanded rats. An electromagnetic flow probe on the renal artery was used to measure total renal blood flow. Laser‐Doppler flow probes were inserted into the renal parenchyma at various depths to measure regional blood flow in the outer and inner medulla. (A) Total renal blood flow and cortical tissue blood flow show stability of blood flow over a range of perfusion pressure. In these volume expanded rats (see text), the small fraction of blood flow that reaches the outer or inner medulla is not autoregulated. (B) However, medullary blood flow is autoregulated in hydropenic rats. (C) Renal interstitial hydrostatic pressure (RIHP) is higher and increases to a greater degree with renal perfusion pressure in volume expanded animals. (D) When renal perfusion pressure is increased, urinary sodium excretion (UNaV) increases much more markedly in volume expanded than in hydropenic animals. From Refs 1451,1461.
Figure 38. Figure 38.

Pressure natriuresis and autoregulation of medullary blood flow in dog kidneys. In anesthetized dog kidneys, both outer and inner medullary blood flow exhibit highly efficient autoregulation in response to changes in renal arterial pressure. Pressure natriuresis is observed in the presence of medullary blood flow autoregulation. From Ref. 1469.
Figure 39. Figure 39.

Arginine vasopressin (AVP), 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.

Reproduced with permission from Ref. 1497
Figure 40. Figure 40.

Adenosine vasodilates the renal medulla; effect of intrarenal infusion of adenosine receptor A1 or A2 subtype agonists. Cortical and medullary blood flow 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 Al agonist N6‐cyclopentyladenosine (left panels) or the A2 agonist CGS‐21680C (right panels) were 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 predominant increase in blood flow to the medulla.

Reproduced with permission from Ref. 1634
Figure 41. Figure 41.

Effects of electrical stimulation of renal efferent nerves at 1–5 Hz on single nephron GFR. plasma flow, and resistance of preglomerular vessels and efferent arterioles. Data from Ref. 1710,1711.


Figure 1.

Microvascular anatomy of the kidney. Outer, middle and juxtamedullary nephrovascular units and outer medullary bundles are shown. In the left panel, nephrons are shown without the vascular structures with distal nephron segments in darker color. The center panel shows only the vascular structures with arterial vessels in red and venous vessels in blue. The right panel shows the combined nephro‐vascualr units. Representative efferent and peritubular capillary systems for only a few nephrons are shown to illustrate the different patterns. Peritubular capillary blood vessels in the cortex are derived from superficial and mid‐cortical nephrons, while juxtamedullary nephrons gave rise to descending vasa recta (DVR). DVR from bundle periphery supply the interbundle capillary plexus while those in the center supply blood to the inner medulla. See text for further detail. From Ref. 20. (See page 14 in colour section at the back of the book)



Figure 2.

Renal vasculature filled with red polymer and single juxtamedullary nephron filled with yellow polymer showing a long loop of Henle

(Courtesy of Daniel Casellas). (See page 14 in colour section at the back of the book)


Figure 3.

Microvascular structures of cortex. (A) depicts an isolated renal corpuscle (RC) with attached AA. The groove (asterisk) is the point of attachment to the macula densa. (B) is a vascular cast of a glomerular capillary system. (C) is a scanning EM of a single glomerular capillary revealing all cell types including the endothelium and endothelial fenestrations, the basement membrane and interdigitating podocyte foot processes. A mesangial cell is seen in intercapillary position. (D) shows a peritubular capillary of the outer cortex. Characteristically, the endothelial cells are flattened with many small fenestrae bridged by a diaphragm and an attenuated basement membrane (BM). From Ref. 2.



Figure 4.

Comparison of DVR and AVR wall characteristics. 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.

Reproduced with permission from Ref. 61


Figure 5.

Tubular vascular relationships and collecting duct clusters in the inner medulla. (A) A CD cluster (blue) is surrounded by 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 AVR (red) and thin ALH (green) in its surroundings and within the cluster. (C) Idealized crossectional 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. From Ref. 62,78. See page 15 in colour section at the back of the book)



Figure 6.

Close relationship of ascending vasa recta and collecting ducts in the inner medulla. (A) Four AVR (red) surround a single inner medullary CD (blue). Successive panels show rotations as specified by the idealized depiction above each panel. (B) Transmission electron micrograph of an inner medullary CD surrounded by four AVR that abutt the abluminal surface (AVR lumens identified with asterisks). Bar = 1 micron. From Ref. 62. (See page 15 in colour section at the back of the book)



Figure 7.

In vitro tubuloglomerular feedback visualized using multiphoton laser‐scanning fluorescence image of the living isolated perfused cortical thick ascending limb (cTAL) with attached glomerulus (G) labeled with membrane staining dye TMA‐DPH. Note the macula densa (MD) cells

(Courtesy of P. D. Bell). (See page 15 in colour section at the back of the book)


Figure 8.

Multicolor labeling of the in vitro microperfused juxtaglomerular apparatus with attached glomerulus. Cell membranes of tubular epithelium (cortical thick ascending limb [cTAL] containing the macula densa), vascular endothelium of afferent arteriole (AA), and glomerulus (G) are labeled with R18 (red), renin granules with quinacrine (green), and cell nuclei with Hoechst 33342 (blue). From Ref. 94. (See page 15 in colour section at the back of the book)



Figure 9.

Depiction of the hydraulic and oncotic forces responsible for filtration of fluid of the glomerulus and reabsorption of fluid into the peritubular capillaries. Representative values for humans are provided. Insert shows representative profiles in the net hydrostatic pressure gradient and glomerular plasma colloid osmotic pressure (πg) along the length of the glomerular capillaries. Profile A represents continued filtration throughout glomerular capillaries while profile B represents achievement of filtration pressure equilibrium. Profile C represents the change in response to volume expansion and vasodilation. Revised from Ref. 1.



Figure 10.

Passage of macromolecules across glomerular capillaries. Representative sieving curves for several test molecules in the glomerular circulation. The curve representing neutral molecules is based on data obtained with use of polyvinylpyrrolidone and neutral dextran. The curves for anionic and cationic molecules are based on studies with charged dextrans. Also shown are the sieving values for neutral horseradish peroxidase (neutral HRP) and for albumin. The smaller molecules are shown to have a sieving coefficient of 1.0. Revised from Ref. 1.



Figure 11.

Movement of water NaCl and urea in the renal medullary microcirculation. The majority of blood flow to the medulla arises from juxtamedullary efferent arterioles with a minor fraction from periglomerular shunt pathways. In the outer stripe of the outer medulla, juxtamedullary efferent arterioles give rise to DVR that coalesce with AVR to form vascular bundles which are the prominent feature of the inner stripe of the outer medulla. DVR on the periphery of vascular bundles perfuse the interbundle capillary plexus. DVR in the center of the bundles continue to perfuse the inner medulla. Vascular bundles disappear in the inner medulla and VR because dispersed with thin loops of Henle and collecting ducts. DVR have a continuous endothelium (inset) and are surrounded by contractile pericytes. In contrast, 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 Ref. 86


Figure 12.

Aquaporin‐1 mediated osmotic water permeability (Pf) of DVR. (A) Pf 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 Pf to nearly zero. From Ref. 217. (B) Pf 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 Pf from ∼1100μ/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 Refs. 216,217


Figure 13.

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 DVR endothelium and red blood cells (not shown). Thin descending limbs of short looped nephrons become associated with vascular bundles so that urea recycling from thin limbs to DVR via UTA2 and UTB is accommodated. UTB is not expressed by the AVR endothelium but AVR are fenestrated and urea permeability is high. Thus urea in AVR plasma and RBCs readily recycles back to DVR in vascular bundles using UTB in the RBC membrane and DVR endothelium. The UTAl, 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 Ref. 244


Figure 14.

Characteristic autoregulatory relationships between renal arterial pressure and renal blood flow, glomerular filtration rate, intrarenal pressures and segmental vascular resistances. PG is glomerular capillary pressure, PPT is proximal tubular pressure, PC is parttibular capillary pressure, and Pt is renal interstitial fluid pressure. Revised from Ref. 1.



Figure 15.

Autoregulatory responses in afferent arteriolar diameter and blood flow to changes in perfusion pressure in in vitro juxtamedullary nephron preparation with intact myogenic and TGF mechanisms and after elimination of TGF mechanism. Control (•) responses were observed with intact flow to macula densa, TGF was interrupted by transection of loops of Henle (papillectomy) (○), and residual myogenic mechanism was then blocked with 10μM diltiazem (▪). *p < 0.05 compared with respective basal value at 100mmHg. p < 0.01 compared with control condition at a similar pressure (Modified from Ref. 292).



Figure 16.

Absolute and relative afferent arteriolar dynamic responses to pressure step from 100 to 150mmHg at differing levels of TGF activity obtained in juxtamedullary nephron preparation. The responses with intact flow to the macula densa are shown as open circles (O). The responses during acetazolamide‐induced enhancement of TGF activity are shown as closed circles (•). The responses after cessation of distal flow imposed by transection of the loops of Henle are shown as closed triangles (▴). (Modified from Ref. 478 and unpublished observations).



Figure 17.

Tubuloglomerular feedback mechanism. Micropuncture procedures used to assess TGF responses (left) and representative relationships between distal nephron volume delivery and single‐nephron GFR responses. Effects of some agents that decrease sensitivity of TGF responses and agents that increase sensitivity of TGF responses are indicated. NOS. nitric oxide synthase; HETE, 20‐hydroxyeico‐satetraenoic acid; PGI2, prostacyclin, Modified from Ref, 473, (See page 16 in colour section at the back of the book)



Figure 18.

Overview of apical and basolateral membrane transport systems in macula densa cell. (Modified from Ref, 521).



Figure 19.

Release of ATP from macula densa cells. PCI2 cells loaded with fura 2 were positioned in close proximity to the basolateral aspect of macula densa cells with attached ascending limb. In response to increases in luminal NaCl concentration the increased fluorescence reflected release of ATP, ATP release was prevented by furosemide in lumen. Suramin in bath was used to block P2 receptors demonstrating specificity of the response, From Ref. 556, Illustrtion by E. Inscho, (See page 16 in colour section at the back of the book)



Figure 20.

(A) Relationships between luminal NaCl, TGF responses and release of ATP, NO and PGE2 from macula densa cells. Increases in luminal NaCl concentration lead to decreases in stop flow pressure (PSF) reflecting predominant afferent arteriolar constriction and leading to increases in ATP causing vasoconstriction partially compensated by increases in nitric oxide. In contrast. PGE2 release is greater at low NaCl concentrations and decreases with increases in luminal NaCl concentration. (B) Cartoon of macula densa cell signaling molecules and actions on adjoining extraglomerular mesangial cells and arteriolar vascular smooth muscle cells (provided by P. D. Bell).



Figure 21.

Effects of NOS inhibition with nitro‐L‐arginine on autoregulatory responses of renal blood flow (RBF), cortical blood flow (CBF), MBF, and glomerular filtration rate (GFR). Control responses are shown as open circles (○). NOS inhibition, shown as closed circles (•), reduced RBF, CBF and MBF without changing GFR, but autoregulatory capability remained intact. The responses to a NO donor, s‐nitroso‐n‐acetylpenicillamine (SNAP) are shown as open triangles and restored the flows back to control levels. From Ref. 680.



Figure 22.

Effects of L‐SMTC (nNOS inhibitor) on afferent arteriolar diameters of juxtamedullary nephron preparation in microns. Arteriolar responses to L‐SMTC were performed using different groups of the kidneys; that is control kidneys (open circle), papillectomized kidneys (open triangle), acetazolamide‐treated kidneys (closed circle), and papillectomized kidneys treated with acetazolamide (closed triangle). nNOS inhibition reduced both afferent and efferent arteriolar diameters and this response was enhanced when distal delivery was increased by acetazolamide. After interruption of distal delivery, the vasoconstriction in response to L‐SMTC was markedly reduced even during treatment with acetazolamide. From Ref. 746.



Figure 23.

(A) Influence of endogenous ET‐1 on renal blood flow in anesthetized Sprague‐Dawley rats. Effect of ET receptor antagonism on basal renal hemodynamics. Blocking ETA receptors increased RBF while blocking ETB receptors decreased RBF. Data from Ref. 735. (B) Acute renal vasoconstriction produced by exogenous ET‐1, ET‐1 + the ETA receptor antagonist BQ123, ET‐1 + the ETB receptor antagonist BQ‐788, and ETB receptor stimulation with the selective agonists S6C or IRL‐1620. All agents were either injected or infused into the renal artery of anesthetized Sprague‐Dawley rats. *p < 0.01 vs. ET‐1 response. Data from Ref. 833.



Figure 24.

Enzymatic cascade of the renin angiotensin system. (Modified from Navar et al., In: Molecular Mechanisms in Hypertension, edited by Re R, DiPette DJ, Schiffrin EL and Sowers JR. Taylor & Francis Group, 2006, p. 3–14).



Figure 25.

Renal vascular actions of AT 1 and AT2 receptors.



Figure 26.

Role of L and T‐type Ca2+ channels in Ang II‐mediated afferent and efferent arteriolar vasoconstriction. The vasoconstrictor effects of Ang II on afferent arterioles are blocked by both L‐type and T‐type Ca2+ channel blockers. In contrast, the efferent vasoconstrictor effects of Ang II are not blocked by L‐type Ca2+ channel blockers, but are blocked by T‐type Ca2+ channel blockers. Data compiled from Refs. 288,295.



Figure 27.

Arachidonic acid metabolism by COX, CYP and LOX pathways. COX enzymes generate PGH2 that can be metabolized by synthases to from TXA2, PGE2 and PGI2. CYP enzymes can generate HETEs and EETs. EETs can be hydrolyzed by SEH to form DHETEs. LOX enzymes generate HETEs, LTs, and LXs.



Figure 28.

Endothelial eicosanoids mediate renal microvascular dilation. Diagram of renal microvessel depicting bradykinin‐mediated endothelial generation of COX and CYP products that lead to relaxation of the adjacent vascular smooth muscle cells. (See page 17 in colour section at the back of the book)



Figure 29.

Renal microvascular eicosanoids mediate constriction. Diagram of renal microvessel depicting vasoconstrictor‐mediated generation of COX, LOX and CYP products that contribute to the vasoconstriction response. (See page 17 in colour section at the back of the book)



Figure 30.

Purinoceptors (P1 and P2 receptors) and postulated intracellular cascades in renal vascular smooth muscle cells. Mechanisms for activation of P1 and P2 purinoceptors by adenosine monophosphate (AMP), adenosine, adenosine triphosphate (ATP) and adenosine diphosphate (ADP), respectively as shown in arrows. Gp, GTP‐binding proteins; Gi, inhibitory G‐protein; Gs, stimulatory G‐protein; IP3, inositol‐1,4,5‐triphosphate: SR, sarcoplasmic reticulum; PLC, phospholipase C; VOC, voltage‐operated calcium channel; ROC, receptor‐operated calcium channel; cAMP, cyclic adenosine monphosphate; ECTO‐5′‐NT, ecto‐5′‐nucleotidase. Symbols (+), stimulation; (−), inhibition. (See page 17 in colour section at the back of the book)



Figure 31.

Afferent and efferent arteriolor responses to ATP in blood‐perfused rat juxtamedullary nephron preparation. The diameter of the afferent arteriole decreases rapidly within a few seconds in response to superfusion with ATP and then increases slightly but remains significantly smaller than control (black circles). The efferent arterioles do not respond even to high concentration of ATP (gray circles). Data taken from Ref. 674.



Figure 32.

Relationships between renal arterial pressure and renal vascular resistance (top left) and renal interstitial fluid ATP concentration (bottom left). Renal interstitial ATP concentrations decrease consistently in response to reductions in RAP. The changes in autoregulatory related changes in renal vascular resistance are positively correlated with the changes in renal interstitial fluid ATP concentrations. These data demonstrate an association between the autoregulatory adjustments in RVR and the interstitial ATP concentration. (From Ref. 1418). Renal interstitial concentrations of ATP were decreased consistently in response to reductions in RAP. Interestingly, changes in ATP concentration were highly correlated with the changes in the autoregulatory associated alterations in renal vascular resistance. Thus, these data demonstrated an association between the autoregulatory adjustments in RVR and the interstitial ATP concentration, and support the hypothesis that RIF ATP is involved in the mechanism of renal autoregulation.



Figure 33.

Effect of the P2X1 receptor blocker, NF279, on afferent arteriolar responses to increases in renal perfusion pressure (RPP). The diameter of the afferent arterioles was significantly decreased in response to increasing RPP during control period (black circles). NF 279 inhibited the pressure‐mediated afferent arteriolar response (grey circles). Each point represents mean vessel diameter measured at 12‐s intervals throughout each pressure period, *p < 0.05 vs. diameter at 100 mmHg. Data taken from Ref. 550.



Figure 34.

Effect of P2X blocker NF279 on the afferent arteriolar response to the A1 agonist N6‐cyclopentyl adenosine (CPA) from P2X1 knockout mouse kidney. Afferent arterioles constricted in response to administration of CPA in the absence (black circles) and presence of NF279 (grey circles). *p < 0.05 vs. diameter at 100 mmHg. Data taken from Ref. 550.



Figure 35.

Intrarenal hematocrit. 51Cr‐RBC's 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 RBC's and plasma were inferred by measuring activity of the isotopes in tissue and dividing their ratio by the systemic ratio. The hematocrit of inner medullary blood is lower than that either whole kidney, cortex or outer medulla. Data redrawn with permission from Ref. 1457. Rasmussen S.N. Intrarenal red cell and plasma volumes in the nondiuretic rat. Pflugers Archives 342: 61–72, 1973.



Figure 36.

Periglomerular shunts. The afferent arteriole (AA) of juxtamedullary glomeruli occasionally give rise to a side branch (AV) which forms descending vasa recta (VR). The efferent arteriole (EA) of the juxtamedullary glomerulus is visible (arrowhead), 16m sphere; bar, 100m. Thus, it is probable that some blood flow that reaches the renal medulla bypasses juxtamedullary glomeruli by shunts such as the one illustrated, but the overall fraction of medullary blood flow derived from shunts is probably small (i.e. < 10%).

Reproduced with permission from Ref. 28


Figure 37.

Renal autoregulation in different regions of volume expanded rats. An electromagnetic flow probe on the renal artery was used to measure total renal blood flow. Laser‐Doppler flow probes were inserted into the renal parenchyma at various depths to measure regional blood flow in the outer and inner medulla. (A) Total renal blood flow and cortical tissue blood flow show stability of blood flow over a range of perfusion pressure. In these volume expanded rats (see text), the small fraction of blood flow that reaches the outer or inner medulla is not autoregulated. (B) However, medullary blood flow is autoregulated in hydropenic rats. (C) Renal interstitial hydrostatic pressure (RIHP) is higher and increases to a greater degree with renal perfusion pressure in volume expanded animals. (D) When renal perfusion pressure is increased, urinary sodium excretion (UNaV) increases much more markedly in volume expanded than in hydropenic animals. From Refs 1451,1461.



Figure 38.

Pressure natriuresis and autoregulation of medullary blood flow in dog kidneys. In anesthetized dog kidneys, both outer and inner medullary blood flow exhibit highly efficient autoregulation in response to changes in renal arterial pressure. Pressure natriuresis is observed in the presence of medullary blood flow autoregulation. From Ref. 1469.



Figure 39.

Arginine vasopressin (AVP), 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.

Reproduced with permission from Ref. 1497


Figure 40.

Adenosine vasodilates the renal medulla; effect of intrarenal infusion of adenosine receptor A1 or A2 subtype agonists. Cortical and medullary blood flow 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 Al agonist N6‐cyclopentyladenosine (left panels) or the A2 agonist CGS‐21680C (right panels) were 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 predominant increase in blood flow to the medulla.

Reproduced with permission from Ref. 1634


Figure 41.

Effects of electrical stimulation of renal efferent nerves at 1–5 Hz on single nephron GFR. plasma flow, and resistance of preglomerular vessels and efferent arterioles. Data from Ref. 1710,1711.

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Article Title: The Renal Microcirculation
 

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L Gabriel Navar, William J Arendshorst, Thomas L Pallone, Edward W Inscho, John D Imig, P Darwin Bell. The Renal Microcirculation. Compr Physiol 2011, Supplement 9: Handbook of Physiology, The Cardiovascular System, Microcirculation: 550-683. First published in print 2008. doi: 10.1002/cphy.cp020413