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Neural Control of Renal Function

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Abstract

The kidney is innervated with efferent sympathetic nerve fibers that directly contact the vasculature, the renal tubules, and the juxtaglomerular granular cells. Via specific adrenoceptors, increased efferent renal sympathetic nerve activity decreases renal blood flow and glomerular filtration rate, increases renal tubular sodium and water reabsorption, and increases renin release. Decreased efferent renal sympathetic nerve activity produces opposite functional responses. This integrated system contributes importantly to homeostatic regulation of sodium and water balance under physiological conditions and to pathological alterations in sodium and water balance in disease. The kidney contains afferent sensory nerve fibers that are located primarily in the renal pelvic wall where they sense stretch. Stretch activation of these afferent sensory nerve fibers elicits an inhibitory renorenal reflex response wherein the contralateral kidney exhibits a compensatory natriuresis and diuresis due to diminished efferent renal sympathetic nerve activity. The renorenal reflex coordinates the excretory function of the two kidneys so as to facilitate homeostatic regulation of sodium and water balance. There is a negative feedback loop in which efferent renal sympathetic nerve activity facilitates increases in afferent renal nerve activity that in turn inhibit efferent renal sympathetic nerve activity so as to avoid excess renal sodium retention. In states of renal disease or injury, there is activation of afferent sensory nerve fibers that are excitatory, leading to increased peripheral sympathetic nerve activity, vasoconstriction, and increased arterial pressure. Proof of principle studies in essential hypertensive patients demonstrate that renal denervation produces sustained decreases in arterial pressure. © 2011 American Physiological Society. Compr Physiol 1:731‐767, 2011.

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Figure 1. Figure 1.

Neural pathways of the efferent renal sympathetic nerves.

Figure 2. Figure 2.

Functional terminations of efferent renal sympathetic innervation within the kidney.

Figure 3. Figure 3.

Neuromodulators of synaptic interaction between efferent renal sympathetic nerve terminal and renal tubular epithelial cell.

Figure 4. Figure 4.

Intracellular trafficking of renin and prorenin.

Figure 5. Figure 5.

Factors involved in the exocytosis of renin from the juxtaglomerular granular cell.

Figure 6. Figure 6.

Effects of intensity of renal sympathetic nerve stimulation on various renal functions.

Figure 7. Figure 7.

Effects of various patterns of renal sympathetic nerve stimulation on renal blood flow.

Figure 8. Figure 8.

Effects of various patterns of renal sympathetic nerve stimulation on urinary sodium excretion at constant renal blood flow and glomerular filtration rate.

Figure 9. Figure 9.

A variety of inputs to the brain participate in the regulation of efferent renal sympathetic nerve activity.

Figure 10. Figure 10.

Integration of peripheral and central pathways in the regulation of efferent renal sympathetic nerve activity.

Figure 11. Figure 11.

Immunofluorescence double‐labeling for CGRP (calcitonin gene‐related peptide, panel a), a marker for sensory nerves, and NE‐t (norepinephrine transporter, panel b), a marker for sympathetic nerves. CGRP‐immunoreactive (ir) fibers (red) and NE‐t‐ir fibers (green) are distributed in both the muscle layer and the subepithelial connective tissue of the renal pelvic wall. The majority of the NE‐t‐ir fibers are close to CGRP‐ir fibers (panel c). Arrows in panels a, b, and c point to same fibers. Higher magnification showed that the NE‐t‐ir and CGRP‐ir fibers are intertwined (arrows, panel d) (adapted from ).

Figure 12. Figure 12.

In volume expanded rats, unilateral denervation of the ipsilateral kidney increases ipsilateral urinary sodium excretion (solid lines) and increases contralateral efferent renal sympathetic nerve activity (ERSNA) (dashed line) that in turn decreases contralateral urinary sodium excretion (dashed line). These findings suggest that the afferent renal nerves exert a tonic inhibition on efferent renal sympathetic nerve activity in the overall goal of maintaining low basal ERSNA during conditions of increased water/sodium load (adapted from ).

Figure 13. Figure 13.

Activation of renal sensory nerves by many stimuli, including increased renal pelvic pressure, renal venous pressure, and renal pelvic administration of substance P, bradykinin or capsaicin, decreases efferent renal sympathetic nerve activity that in turn increases urinary sodium, an inhibitory renorenal reflex response.

Figure 14. Figure 14.

Graded increases in renal pelvic pressure results in graded increases in ipsilateral afferent renal nerve activity (ARNA) (left panel) and contralateral urinary sodium excretion (right panel) in rats fed high (solid lines) and low sodium diet (dashed lines). However, the lines depicting the responses of ARNA and urinary sodium excretion in rats fed the high sodium diet are shifted to the left compared to those in rats fed the low sodium diet. Thus, each increase in renal pelvic pressure results in a greater increase in ipsilateral ARNA and contralateral urinary sodium excretion in high sodium diet rats compared to low sodium diet rats. The threshold for activation of renal mechanosensory nerves was 2.6 mmHg in rats fed high compared to 7.5 mmHg in rats fed low sodium diet. These findings suggest that the afferent renal nerves are tonically active in high sodium dietary conditions (adapted from ).

Figure 15. Figure 15.

Rats with dorsal rhizotomy (DRX, open circles) and Sham DRX (closed circles) were maintained on normal and high sodium diet for 3 weeks prior to the study. Both groups of rats were in sodium balance on either diet at the time of the study. However, this was achieved at markedly different levels of arterial pressure, as measured chronically in conscious rats. Sham DRX rats were able to excrete a 4‐fold increase in dietary sodium load in the absence of a change in arterial pressure. However, DRX required a significant increase in arterial pressure to achieve external sodium balance. Excretion of an increased dietary sodium load in the absence of a change in arterial pressure requires intact renal innervation. DRX rats are characterized by NaCl‐sensitive hypertension (adapted from ).

Figure 16. Figure 16.

Thermal cutaneous stimulation produced by placing the rat's tail in warm water results in increases in arterial pressure, heart rate (not shown), and efferent renal sympathetic nerve activity (ERSNA). The reflex increase in ERSNA causes an increase in afferent renal nerve activity (ARNA) that is blocked by renal denervation (adapted from ).

Figure 17. Figure 17.

There is an interaction between efferent renal sympathetic nerve activity (ERSNA) and afferent renal nerve activity (ARNA) whereby increases in ERSNA increase ARNA. The increased ARNA exerts a negative feedback control of ERSNA via activation of the renorenal reflexes in the overall goal of maintaining a low level of ERSNA.

Figure 18. Figure 18.

Immunofluorescence for ETA receptors (left panel) and ETB receptors (right panel) in renal pelvic tissue suggests the presence of ETA receptors on smooth muscle cells in the renal pelvic wall and adjacent blood vessels (arrows, left panel) and ETB receptors on or close to sensory nerve fibers (arrows, right panel) among smooth muscle cells (adapted from ).

Figure 19. Figure 19.

In summary, increases in efferent renal sympathetic nerve activity (ERSNA) increase afferent renal nerve activity (ARNA) via release of norepinephrine (NE). NE activates α1 and α2 adrenoceptors on renal pelvic sensory nerves. In rats fed normal or high sodium diet, the ERSNA‐induced release of NE results in increased PGE2 synthesis. PGE2 activates the adenylyl cyclase (AC)/cAMP/PKA signal transduction pathway resulting in release of substance P from the renal sensory nerves by a mechanism involving activation of N‐type Ca2+channels. The increased substance P release increases ARNA that in turn will reduce ERSNA by a negative feedback mechanism involving activation of the renorenal reflexes in the overall goal of maintaining low basal ERSNA in high and normal sodium dietary conditions. In low sodium dietary conditions, increased endogenous angiotensin (ANG) II activity suppresses the PGE2‐mediated activation of AC by a pertussis toxin‐sensitive mechanism resulting in reduced increases in substance P and ARNA leading to no or minimal activation of the renorenal reflex mechanism so as to maintain ERSNA at a higher baseline level to facilitate sodium retention. Endothelin (ET) modulates the activation of renal sensory nerves in a variable manner depending on dietary sodium intake. During high sodium diet, ET enhances the activation of renal sensory nerves by stimulation of ETB receptors (ETB‐R) involving increased PGE2 synthesis/release. In low sodium diet, ET suppresses the activation of renal sensory nerves by stimulation of ETA receptors (ETA‐R) involving steps subsequent to ANG II type 1 receptor (AT1) stimulation.



Figure 1.

Neural pathways of the efferent renal sympathetic nerves.



Figure 2.

Functional terminations of efferent renal sympathetic innervation within the kidney.



Figure 3.

Neuromodulators of synaptic interaction between efferent renal sympathetic nerve terminal and renal tubular epithelial cell.



Figure 4.

Intracellular trafficking of renin and prorenin.



Figure 5.

Factors involved in the exocytosis of renin from the juxtaglomerular granular cell.



Figure 6.

Effects of intensity of renal sympathetic nerve stimulation on various renal functions.



Figure 7.

Effects of various patterns of renal sympathetic nerve stimulation on renal blood flow.



Figure 8.

Effects of various patterns of renal sympathetic nerve stimulation on urinary sodium excretion at constant renal blood flow and glomerular filtration rate.



Figure 9.

A variety of inputs to the brain participate in the regulation of efferent renal sympathetic nerve activity.



Figure 10.

Integration of peripheral and central pathways in the regulation of efferent renal sympathetic nerve activity.



Figure 11.

Immunofluorescence double‐labeling for CGRP (calcitonin gene‐related peptide, panel a), a marker for sensory nerves, and NE‐t (norepinephrine transporter, panel b), a marker for sympathetic nerves. CGRP‐immunoreactive (ir) fibers (red) and NE‐t‐ir fibers (green) are distributed in both the muscle layer and the subepithelial connective tissue of the renal pelvic wall. The majority of the NE‐t‐ir fibers are close to CGRP‐ir fibers (panel c). Arrows in panels a, b, and c point to same fibers. Higher magnification showed that the NE‐t‐ir and CGRP‐ir fibers are intertwined (arrows, panel d) (adapted from ).



Figure 12.

In volume expanded rats, unilateral denervation of the ipsilateral kidney increases ipsilateral urinary sodium excretion (solid lines) and increases contralateral efferent renal sympathetic nerve activity (ERSNA) (dashed line) that in turn decreases contralateral urinary sodium excretion (dashed line). These findings suggest that the afferent renal nerves exert a tonic inhibition on efferent renal sympathetic nerve activity in the overall goal of maintaining low basal ERSNA during conditions of increased water/sodium load (adapted from ).



Figure 13.

Activation of renal sensory nerves by many stimuli, including increased renal pelvic pressure, renal venous pressure, and renal pelvic administration of substance P, bradykinin or capsaicin, decreases efferent renal sympathetic nerve activity that in turn increases urinary sodium, an inhibitory renorenal reflex response.



Figure 14.

Graded increases in renal pelvic pressure results in graded increases in ipsilateral afferent renal nerve activity (ARNA) (left panel) and contralateral urinary sodium excretion (right panel) in rats fed high (solid lines) and low sodium diet (dashed lines). However, the lines depicting the responses of ARNA and urinary sodium excretion in rats fed the high sodium diet are shifted to the left compared to those in rats fed the low sodium diet. Thus, each increase in renal pelvic pressure results in a greater increase in ipsilateral ARNA and contralateral urinary sodium excretion in high sodium diet rats compared to low sodium diet rats. The threshold for activation of renal mechanosensory nerves was 2.6 mmHg in rats fed high compared to 7.5 mmHg in rats fed low sodium diet. These findings suggest that the afferent renal nerves are tonically active in high sodium dietary conditions (adapted from ).



Figure 15.

Rats with dorsal rhizotomy (DRX, open circles) and Sham DRX (closed circles) were maintained on normal and high sodium diet for 3 weeks prior to the study. Both groups of rats were in sodium balance on either diet at the time of the study. However, this was achieved at markedly different levels of arterial pressure, as measured chronically in conscious rats. Sham DRX rats were able to excrete a 4‐fold increase in dietary sodium load in the absence of a change in arterial pressure. However, DRX required a significant increase in arterial pressure to achieve external sodium balance. Excretion of an increased dietary sodium load in the absence of a change in arterial pressure requires intact renal innervation. DRX rats are characterized by NaCl‐sensitive hypertension (adapted from ).



Figure 16.

Thermal cutaneous stimulation produced by placing the rat's tail in warm water results in increases in arterial pressure, heart rate (not shown), and efferent renal sympathetic nerve activity (ERSNA). The reflex increase in ERSNA causes an increase in afferent renal nerve activity (ARNA) that is blocked by renal denervation (adapted from ).



Figure 17.

There is an interaction between efferent renal sympathetic nerve activity (ERSNA) and afferent renal nerve activity (ARNA) whereby increases in ERSNA increase ARNA. The increased ARNA exerts a negative feedback control of ERSNA via activation of the renorenal reflexes in the overall goal of maintaining a low level of ERSNA.



Figure 18.

Immunofluorescence for ETA receptors (left panel) and ETB receptors (right panel) in renal pelvic tissue suggests the presence of ETA receptors on smooth muscle cells in the renal pelvic wall and adjacent blood vessels (arrows, left panel) and ETB receptors on or close to sensory nerve fibers (arrows, right panel) among smooth muscle cells (adapted from ).



Figure 19.

In summary, increases in efferent renal sympathetic nerve activity (ERSNA) increase afferent renal nerve activity (ARNA) via release of norepinephrine (NE). NE activates α1 and α2 adrenoceptors on renal pelvic sensory nerves. In rats fed normal or high sodium diet, the ERSNA‐induced release of NE results in increased PGE2 synthesis. PGE2 activates the adenylyl cyclase (AC)/cAMP/PKA signal transduction pathway resulting in release of substance P from the renal sensory nerves by a mechanism involving activation of N‐type Ca2+channels. The increased substance P release increases ARNA that in turn will reduce ERSNA by a negative feedback mechanism involving activation of the renorenal reflexes in the overall goal of maintaining low basal ERSNA in high and normal sodium dietary conditions. In low sodium dietary conditions, increased endogenous angiotensin (ANG) II activity suppresses the PGE2‐mediated activation of AC by a pertussis toxin‐sensitive mechanism resulting in reduced increases in substance P and ARNA leading to no or minimal activation of the renorenal reflex mechanism so as to maintain ERSNA at a higher baseline level to facilitate sodium retention. Endothelin (ET) modulates the activation of renal sensory nerves in a variable manner depending on dietary sodium intake. During high sodium diet, ET enhances the activation of renal sensory nerves by stimulation of ETB receptors (ETB‐R) involving increased PGE2 synthesis/release. In low sodium diet, ET suppresses the activation of renal sensory nerves by stimulation of ETA receptors (ETA‐R) involving steps subsequent to ANG II type 1 receptor (AT1) stimulation.

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Edward J. Johns, Ulla C. Kopp, Gerald F. DiBona. Neural Control of Renal Function. Compr Physiol 2011, 1: 731-767. doi: 10.1002/cphy.c100043