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Neural Control of Renal Function

Nicholas G. Moss, Romulo E. Colindres, Carl W. Gottschalk

10.1002/cphy.cp080124

Source: Supplement 25: Handbook of Physiology, Renal Physiology

Originally published: 1992

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Current Research
2 Historical Perspective
3 Neuroanatomy and Neurophysiology
3.1 Efferent Renal Innervation
3.2 Afferent Renal Innervation
4 Renal Adrenergic Receptors
4.1 General Concepts
4.2 Prejunctional Renal Receptors
4.3 Post‐ and Extrajunctional Adrenoceptors
4.4 Renal Tubular and Vascular Dopamine Receptors
4.5 Renal Cholinergic Receptors
4.6 Cellular Transduction of Neurotransmitter Effects
5 Sympathetic Nervous System and Renal Hemodynamics
5.1 Vasoconstrictor Responses
5.2 Vasodilatory Responses
6 Sympathetic Nervous System and Renal Tubular Function
6.1 Studies in Anesthetized Animals
6.2 Studies in Conscious Animals
6.3 Effects of Neurotransmitters on Renal Tubular Function
6.4 Cellular Mechanisms in the Renal Tubular Responses to Catecholamines
7 Sympathetic Nervous System and Renin Secretion by the Kidney
7.1 General Concepts
7.2 Effects of Direct and Reflex Stimulation of the Renal Nerves
7.3 Effects of Renal Denervation on Renin Release
7.4 Renal Adrenoceptors Involved in Renin Secretion
7.5 Interactions Between Nerves and Prostaglandins in Renin Release
Figure 1. Figure 1.

Innervated proximal tubule (PT) overlapped by accumulation of autoradiographic grains (arrow) in animal injected with tritiated norepinephrine. Ultrastructural examination of overlap sites disclosed neuroeffector contacts. E, efferent arteriole. × 1,100.

From Barajas et al. 34
Figure 2. Figure 2.

Response of multiunit renal afferent nerve activity (ARNA) and renal blood flow (RBF) as percentage of control levels during progressive reductions in renal perfusion pressure (ABP) in anesthetized Sprague‐Dawley rats. Renal blood flow was measured with pulsed Doppler ultrasonic flowmeter; renal perfusion pressure was reduced by tightening an aortic snare. Closed circles, measurements before cyclooxygenase treatment; open circles, measurements made after inhibition of prostanoid production by cyclooxygenase inhibition with indomethacin.

N. Moss, unpublished observations; see also ref. 42
Figure 3. Figure 3.

Schematic of intracellular events that result from stimulation of α1‐adrenoceptors. PLC, phospholipase C; GP, unknown guanine nucleotide‐binding regulatory protein that is activated by receptor occupancy and that stimulates phospholipase C; PIP2, phosphatidylinositol‐4,5‐bisphosphate; IP3, inositol‐1,4,5‐trisphosphate; IP4, inositol‐1,3,4,5‐tetrakisphosphate; E.R., endoplasmic reticulum; plus sign, stimulatory effect. Stimulation of α1‐adrenoceptors may activate other G proteins and cause release of second messengers other than IP3 and diacylglycerol.

Modified from Timmermans 729
Figure 4. Figure 4.

Schematic of intracellular events resulting from stimulation of α2‐adrenoceptors. Gi, guanine nucleotide‐binding regulatory protein that inhibits adenylate cyclase (AC) upon receptor occupancy; minus sign, inhibition. Stimulation of α2‐adrenoceptors may lead to cellular events unrelated to inhibition of AC.

Modified from Timmermans 729
Figure 5. Figure 5.

Effects of several α‐adrenergic agonists on renal blood flow in 27 anesthetized rats. Composite dose‐response curves were determined from individual dose‐response curves. Increasing dosages of agonists were given directly into renal artery. Changes in renal blood flow were measured with a Doppler flowmeter. Results indicate decrease of renal blood flow from baseline values as function of agonist dosage. Number of individual dose‐response curves and receptor specificity for each agonist are indicated. Selective α2‐adrenoceptor agonists are neither potent nor efficacious renal vasoconstrictors in anesthetized rats, whereas α1‐adrenoceptor agonists can produce a transient cessation of renal blood flow.

From Wolff et al. 771
Figure 6. Figure 6.

Percent decrease of renal blood flow from baseline values produced by increasing dosages of norepinephrine (NE), phenylephrine (PHE), and guanabenz (GBZ) in five conscious, unrestrained chronically instrumented rats. Changes in renal blood flow were measured with a Doppler flowmeter. Composite dose‐response curves were determined by giving 4–12 doses of agonists as bolus into renal artery. Solid lines, average baseline dose‐response curves; dashed lines, average curves obtained in presence of α2‐adrenoceptor antagonist rauwolscine (RAUW). Symbols in each curve indicate agonist dosage that produces decreases in renal blood flow of 15% and 75%.

From Wolff et al. 770
Figure 7. Figure 7.

Effects of direct renal nerve stimulation on fluid reabsorption along proximal tubule of anesthetized rats with expansion of extracellular fluid volume. Measurements of fluid to plasma inulin concentration ratios (F/P) in late proximal tubule were made in absence of stimulation (C1, C2) and in presence of stimulation at 1 (S1) and 2 (S2) Hz. Each point is mean of two to four measurements. Each line represents one animal. Values are means ± S.E.

From Bello‐Reuss et al. 62
Figure 8. Figure 8.

Response of urine flow rate (top), sodium excretion (middle), and efferent renal nerve activity (bottom) in conscious dogs before, during, and after head‐out immersion in water. Closed circles, dogs with innervated kidneys; open circles, dogs with denervated kidneys.

Modified from Miki et al. 476
Figure 9. Figure 9.

Right atrial pressure (top), integrated efferent renal nerve activity (middle), and urinary sodium excretion (bottom) in conscious rats before and during expansion of extracellular fluid volume with an intravenous infusion of saline equivalent to 10% of body weight. Animals were maintained on high (HNa), normal (NNa), or low (LNa) sodium diet.

From Dibona and Sawin 168
Figure 10. Figure 10.

Changes in urinary sodium excretion (UNa; top), sodium intake (middle), and cumulative sodium balance (bottom) in unrestrained, conscious rats before and after bilateral renal denervation or sham denervation. Animals were first fed a diet with normal sodium content and then a diet with very low sodium content. Arrows, days on which blood was collected.

From Fernandez‐Repollet et al. 206
Figure 11. Figure 11.

Reversal of effects of vasopressin and arachidonic acid on urine volume (top), sodium excretion (UNAV; middle), and fractional excretion of sodium (% FENA; bottom) in isolated rat kidneys by α2‐adrenoceptor stimulation with epinephrine. Yohimbine (α2‐adrenoceptor antagonist) was combined with epinephrine during a fourth experimental period to demonstrate that epinephrine effect was indeed mediated by stimulation of α2‐adrenoceptors. Each column represents data from at least five kidneys. Observations were made 20 min after starting infusions of vasopressin, arachidonic acid, or placebo.

From Pettinger et al. 582
Figure 12. Figure 12.

Effects of indomethacin (INDO) on natriuretic response to acute renal denervation (DNX). Comparison of drug effect before (n = 7) or after (n = 6) denervation. Values are ± S.E. *P < 0.01; † P < 0.05.

From Barber et al. 41
Figure 13. Figure 13.

A: light microscopic autoradiograph revealing nerves (arrow) adjacent to granular cells of afferent arteriole (a). G, glomerulus, × 1,250. B: electron microscopic autoradiograph. Heavily labeled monoaminergic varicosities (V) filled with vesicles and occasional mitochondria are associated with granular cell (GC) and two varicosities (V1, V2) are in contact with it. × 26,500.

(Autoradiographs courtesy of Dr. Luciano Barajas.)
Figure 14. Figure 14.

Mean arterial blood pressure (AP), renal blood flow (RBF), urinary sodium excretion (UNAV), and renin secretion rate (RSR) in ten anesthetized dogs. Measurements were made under control conditions (C), during suprarenal aortic constriction (AC), during very‐low‐frequency renal nerve stimulation (RNS), and during suprarenal aortic constriction while stimulating renal nerves. Observations were also made after recovery (R) from AC. FA, blood pressure measured in femoral artery. Results are from left kidney and are means ± S.E.

Modified from Thames and DiBona 723
Figure 15. Figure 15.

Renal blood flow (RBF), glomerular filtration rate (GFR), urinary sodium excretion (UNAV), and renin secretion rate (RSR) in anesthetized dogs. Measurements were made under control conditions (C), during low‐frequency electrical stimulation of renal nerves (RNS, 0.5 Hz), and after recovery (R) from RNS. Observations were also made during β‐adrenoceptor blockade with either the β1‐adrenoceptor antagonist atenolol (ATN) or the β2‐adrenoceptor antagonist butoxamine (BUT). Numbers of animals studied in each group are indicated. Results are from left kidney and are means ± S.E.

Modified from Osborn et al. 541


Figure 1.

Innervated proximal tubule (PT) overlapped by accumulation of autoradiographic grains (arrow) in animal injected with tritiated norepinephrine. Ultrastructural examination of overlap sites disclosed neuroeffector contacts. E, efferent arteriole. × 1,100.

From Barajas et al. 34


Figure 2.

Response of multiunit renal afferent nerve activity (ARNA) and renal blood flow (RBF) as percentage of control levels during progressive reductions in renal perfusion pressure (ABP) in anesthetized Sprague‐Dawley rats. Renal blood flow was measured with pulsed Doppler ultrasonic flowmeter; renal perfusion pressure was reduced by tightening an aortic snare. Closed circles, measurements before cyclooxygenase treatment; open circles, measurements made after inhibition of prostanoid production by cyclooxygenase inhibition with indomethacin.

N. Moss, unpublished observations; see also ref. 42


Figure 3.

Schematic of intracellular events that result from stimulation of α1‐adrenoceptors. PLC, phospholipase C; GP, unknown guanine nucleotide‐binding regulatory protein that is activated by receptor occupancy and that stimulates phospholipase C; PIP2, phosphatidylinositol‐4,5‐bisphosphate; IP3, inositol‐1,4,5‐trisphosphate; IP4, inositol‐1,3,4,5‐tetrakisphosphate; E.R., endoplasmic reticulum; plus sign, stimulatory effect. Stimulation of α1‐adrenoceptors may activate other G proteins and cause release of second messengers other than IP3 and diacylglycerol.

Modified from Timmermans 729


Figure 4.

Schematic of intracellular events resulting from stimulation of α2‐adrenoceptors. Gi, guanine nucleotide‐binding regulatory protein that inhibits adenylate cyclase (AC) upon receptor occupancy; minus sign, inhibition. Stimulation of α2‐adrenoceptors may lead to cellular events unrelated to inhibition of AC.

Modified from Timmermans 729


Figure 5.

Effects of several α‐adrenergic agonists on renal blood flow in 27 anesthetized rats. Composite dose‐response curves were determined from individual dose‐response curves. Increasing dosages of agonists were given directly into renal artery. Changes in renal blood flow were measured with a Doppler flowmeter. Results indicate decrease of renal blood flow from baseline values as function of agonist dosage. Number of individual dose‐response curves and receptor specificity for each agonist are indicated. Selective α2‐adrenoceptor agonists are neither potent nor efficacious renal vasoconstrictors in anesthetized rats, whereas α1‐adrenoceptor agonists can produce a transient cessation of renal blood flow.

From Wolff et al. 771


Figure 6.

Percent decrease of renal blood flow from baseline values produced by increasing dosages of norepinephrine (NE), phenylephrine (PHE), and guanabenz (GBZ) in five conscious, unrestrained chronically instrumented rats. Changes in renal blood flow were measured with a Doppler flowmeter. Composite dose‐response curves were determined by giving 4–12 doses of agonists as bolus into renal artery. Solid lines, average baseline dose‐response curves; dashed lines, average curves obtained in presence of α2‐adrenoceptor antagonist rauwolscine (RAUW). Symbols in each curve indicate agonist dosage that produces decreases in renal blood flow of 15% and 75%.

From Wolff et al. 770


Figure 7.

Effects of direct renal nerve stimulation on fluid reabsorption along proximal tubule of anesthetized rats with expansion of extracellular fluid volume. Measurements of fluid to plasma inulin concentration ratios (F/P) in late proximal tubule were made in absence of stimulation (C1, C2) and in presence of stimulation at 1 (S1) and 2 (S2) Hz. Each point is mean of two to four measurements. Each line represents one animal. Values are means ± S.E.

From Bello‐Reuss et al. 62


Figure 8.

Response of urine flow rate (top), sodium excretion (middle), and efferent renal nerve activity (bottom) in conscious dogs before, during, and after head‐out immersion in water. Closed circles, dogs with innervated kidneys; open circles, dogs with denervated kidneys.

Modified from Miki et al. 476


Figure 9.

Right atrial pressure (top), integrated efferent renal nerve activity (middle), and urinary sodium excretion (bottom) in conscious rats before and during expansion of extracellular fluid volume with an intravenous infusion of saline equivalent to 10% of body weight. Animals were maintained on high (HNa), normal (NNa), or low (LNa) sodium diet.

From Dibona and Sawin 168


Figure 10.

Changes in urinary sodium excretion (UNa; top), sodium intake (middle), and cumulative sodium balance (bottom) in unrestrained, conscious rats before and after bilateral renal denervation or sham denervation. Animals were first fed a diet with normal sodium content and then a diet with very low sodium content. Arrows, days on which blood was collected.

From Fernandez‐Repollet et al. 206


Figure 11.

Reversal of effects of vasopressin and arachidonic acid on urine volume (top), sodium excretion (UNAV; middle), and fractional excretion of sodium (% FENA; bottom) in isolated rat kidneys by α2‐adrenoceptor stimulation with epinephrine. Yohimbine (α2‐adrenoceptor antagonist) was combined with epinephrine during a fourth experimental period to demonstrate that epinephrine effect was indeed mediated by stimulation of α2‐adrenoceptors. Each column represents data from at least five kidneys. Observations were made 20 min after starting infusions of vasopressin, arachidonic acid, or placebo.

From Pettinger et al. 582


Figure 12.

Effects of indomethacin (INDO) on natriuretic response to acute renal denervation (DNX). Comparison of drug effect before (n = 7) or after (n = 6) denervation. Values are ± S.E. *P < 0.01; † P < 0.05.

From Barber et al. 41


Figure 13.

A: light microscopic autoradiograph revealing nerves (arrow) adjacent to granular cells of afferent arteriole (a). G, glomerulus, × 1,250. B: electron microscopic autoradiograph. Heavily labeled monoaminergic varicosities (V) filled with vesicles and occasional mitochondria are associated with granular cell (GC) and two varicosities (V1, V2) are in contact with it. × 26,500.

(Autoradiographs courtesy of Dr. Luciano Barajas.)


Figure 14.

Mean arterial blood pressure (AP), renal blood flow (RBF), urinary sodium excretion (UNAV), and renin secretion rate (RSR) in ten anesthetized dogs. Measurements were made under control conditions (C), during suprarenal aortic constriction (AC), during very‐low‐frequency renal nerve stimulation (RNS), and during suprarenal aortic constriction while stimulating renal nerves. Observations were also made after recovery (R) from AC. FA, blood pressure measured in femoral artery. Results are from left kidney and are means ± S.E.

Modified from Thames and DiBona 723


Figure 15.

Renal blood flow (RBF), glomerular filtration rate (GFR), urinary sodium excretion (UNAV), and renin secretion rate (RSR) in anesthetized dogs. Measurements were made under control conditions (C), during low‐frequency electrical stimulation of renal nerves (RNS, 0.5 Hz), and after recovery (R) from RNS. Observations were also made during β‐adrenoceptor blockade with either the β1‐adrenoceptor antagonist atenolol (ATN) or the β2‐adrenoceptor antagonist butoxamine (BUT). Numbers of animals studied in each group are indicated. Results are from left kidney and are means ± S.E.

Modified from Osborn et al. 541
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Article Title: Neural Control of Renal Function
 

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Nicholas G. Moss, Romulo E. Colindres, Carl W. Gottschalk. Neural Control of Renal Function. Compr Physiol 2011, Supplement 25: Handbook of Physiology, Renal Physiology: 1061-1128. First published in print 1992. doi: 10.1002/cphy.cp080124