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Angiotensins

Barbara J. Ballermann, Macaulay A. C. Onuigbo

10.1002/cphy.cp070304

Source: Supplement 22: Handbook of Physiology, The Endocrine System, Endocrine Regulation of Water and Electrolyte Balance

Originally published: 2000

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Angiotensin Generation and Metabolism
1.1 Classic Pathway of Angiotensin II Generation
1.2 Alternative Pathways Generating Angiotensin Peptides
2 Angiotensin Actions in the Kidney
2.1 Regulation of Intrarenal Hemodynamics
2.2 Angiotensin II Actions on Renal Tubule Epithelial Transport
2.3 Coordination of Renal Vascular and Epithelial Angiotensin II Actions
3 Cardiovascular Actions of Angiotensin II
3.1 Effects on Blood Vessels
3.2 Cardiac Actions
4 Adrenal Actions of Angiotensin
4.1 Adrenal Angiotensin II Receptors
4.2 Mechanisms of Angiotensin II‐Stimulated Aldosterone Synthesis
4.3 Mechanisms of Adrenal Glomerulosa Cell Activation
4.4 Trophic Effects on the Adrenal Gland
5 Central Nervous System Actions of Angiotensin II
5.1 Expression of Renin‐Angiotensin System Components
5.2 Angiotensin II‐Mediated Drinking, Vasopressin Release, and Salt Intake
5.3 Centrally Mediated Effects on Blood Pressure
5.4 Cellular Mechanisms
6 Angiotensin II Receptors
6.1 Angiotensin II Receptor Subtypes
6.2 Regulation of Receptor Expression
6.3 Receptor Structure‐Function Relationships
6.4 Receptor Signaling Mechanisms
7 Conclusions
Figure 1. Figure 1.

Generation and metabolism of angiotensin peptides. A: Classic pathway of angiotensin generation and subsequent cleavage steps. B: Generation of Angiotensin III bypassing Angiotensin II. C: Generation of Angiotensin (1–7) from Angiotensin I and subsequent cleavage steps. D: Generation of Angiotensin (1–7) from Angiotensin II.
Figure 2. Figure 2.

Autoregulation of renal blood flow and glomerular filtration rate. In sodium‐depleted dogs, renal perfusion pressure was reduced stepwise from a mean of 130 mm Hg to 70 mm Hg, in the absence or presence of the angiotensin‐converting enzyme inhibitor SQ‐20881. Glomerular filtration rate and efferent arteriolar resistance are dependent on angiotensin II (AII) as perfusion pressure falls. Afferent arteriolar resistance varies steeply with changes in perfusion pressure and is not dependent on AII. [From Hall 624 with permission.]
Figure 3. Figure 3.

Glomerular and peritubular capillary Starling forces. The hydraulic pressure gradient (black arrows) favoring fluid exit from capillaries is opposed by the oncotic pressure gradient (gray arrows). Net pressure gradient (ΔP) is shown below the panels. In glomerular capillaries, oncotic pressure rises as filtration removes protein‐free ultrafiltrate. Reduction of hydraulic pressure between glomerular and peritubular capillaries is due to efferent arteriolar resistance. In the presence of angiotensin II (bottom panel), the pressure profile is changed, resulting in higher end‐glomerular capillary and, hence, peritubular capillary oncotic pressure and reduced peritubular capillary hydraulic pressure.
Figure 4. Figure 4.

Structure of glomerular mesangium. Transmission electron micrograph of rat glomerulus, single glomerular capillary loop. Basement membrane is not circumferential. Mesangial cells are present in the glomerular interstitium. (Photomicrograph kindly provided by W. Kriz Ruprecht‐Karls‐Universitat, Heidelberg, Germany.)
Figure 5. Figure 5.

Effect of a kinin antagonist and enalaprilat on papillary blood flow in anesthetized rats. Each data point represents mean ± SE from eight rats. *P < 0.05 vs. control; C, P < 0.05 vs. kinin antagonist. Hence, angiotensin II has a significant effect on papillary blood flow when the vasodilatory effect of kinins is inhibited. [From Roman et al. 450 with permission.]
Figure 6. Figure 6.

Effect of angiotensin II (AII) on net proximal tubule fluid reabsorption. Angiotensin II (10 pM, left panel; 10 μ, M, right panel was added to the bath of isolated, perfused proximal tubules obtained from rabbits, and net fluid reabsorption (Jv) was measured during control, AII, and recovery periods. Individual data points are shown as line graphs, averaged data as bar graphs. This study was the first to show a direct and bimodal effect of AII on transport functions in isolated tubules. [From Schuster Kokko and Jacobson 491 with permission.]
Figure 7. Figure 7.

Sites of angiotensin II action in proximal tubule cells. Vectorial Na+ transport is accomplished by the restricted location of Na+−K+‐ATPase at the basolateral membrane (facing the interstitium) of polarized epithelia. Entry of Na+ from tubule lumen via the apical Na+−H+ exchanger (NHE) is down an electrochemical gradient generated by Na+−K+‐ATPase. Intracellular H+ is derived from CO2 and H2O through the action of carbonic anhydrase. H+ entering the tubule lumen is buffered by filtered HCO3−. Angiotensin II (large arrows) stimulates both apical NHE‐ and basolateral Na+−HCO3− transport activity.
Figure 8. Figure 8.

Sodium excretion during angiotensin II (AII) infusion is pressure dependent. Mean arterial pressure, cumulative sodium balance, and urinary sodium excretion in a dog (HS‐7) receiving a continuous infusion of AII. During the first 4 days, renal perfusion pressure was prevented from rising by a servocontrol device. Note progressive sodium retention and severe hypertension during this period. When renal pressure was allowed to rise to the level of the systemic pressure, natriuresis promptly ensued and sodium balance was restored. [From Hall, Granger, Hester et al. 200 with permission.]
Figure 9. Figure 9.

Role of angiotensin (AII) in maintaining stable blood pressure when salt intake changes. Sodium intake was varied in dogs given the angiotensin‐converting enzyme inhibitor SQ‐14225 (captopril) or AII (5 ng · kg−1 · min−1). Blood pressure falls significantly on a low‐salt diet when AII production is inhibited. Also, severe hypertension develops on high‐salt diets if circulating AII levels remain high. [From Hall et al. 625 with permission.]
Figure 10. Figure 10.

Vascular smooth muscle cell responses to angiotensin II (AII). A: Time course of AII (100 nM)‐induced aortic contraction. B: Time course of AII‐stimulated rise in cytosolic Ca2+ concentration. Time course of AII‐stimulated inositol 1,4,5‐trisphosphate (IP3) and diacylglycerol (DG) concentrations. D: Time‐course of vascular smooth muscle cell alkalinization in responses to AII. The dissociation between IP3 and diacylglycerol generation is accounted for by a switch from phospholipase Cβ‐dependent to phospholipase D dependent diacylglycerol generation. See text for details. [From Griendling et al. 180 with permission.]
Figure 11. Figure 11.

Aldosterone biosynthetic pathway. Angiotensin stimulates cholesterol transfer from outer mitochondrial membrane to the inner mitochondrial membrane, the rate‐limiting step in aldosterone synthesis. See text for details.
Figure 12. Figure 12.

Angiotensin II (AII) and Ca2+ dependence of cholesterol transfer. Cholesterol content in the outer mitochondrial membrane (OM), inner membrane contact sites (CS), and inner mitochondrial membrane (IM) after CaCl2 or angiotensin II stimulation in the presence or absence of cycloheximide (CHx). Cholesterol content in contact sites and inner mitochondrial membranes increases in response to angiotensin II and Ca2+ in a protein synthesis‐dependent fashion. On Western blots, the abundance of StAR (steroidogenic acute regulatory) protein similarly increases in response to stimulation with angiotensin II and Ca2+. [From Cherradi et al. 87 with permission.]
Figure 13. Figure 13.

Effect of AT2 receptor deficiency on drinking response. Mice deficient in AT2 receptors (−/Y) and wild‐type mice (+/Y) were deprived of water for 40 h, followed by a 3 h period during which they had free access to water. Although all mice lost an equivalent percentage of body weight during the deprivation period, the drinking response of AT2 receptor‐deficient mice was significantly less than that of wild‐type mice. [From Hein et al. 626 with permission.]
Figure 14. Figure 14.

Central effect of angiotensin II (AII) on blood pressure. A: Rate meter records of action potential firing frequency in the area postrema and blood pressure response following systemic administration of angiotensin II (50ng AII). B: Dose‐dependent blood pressure response to angiotensin II microinjection into the area postrema. [From Ferguson and Washburn 155 with permission.]
Figure 15. Figure 15.

Schematic view of AT1 receptor embedded in plasma membrane. The receptor consists of a seven‐transmembrane‐spanning domain, which forms a ring‐like structure. Angiotensin II (AII) is shown in its binding pocket. See text for details. [From Burns et al. 623 with permission.]
Figure 16. Figure 16.

Intracellular signals stimulated by AT1 receptor activation. Pathways dependent on Gq and Gi activation and their downstream effectors are shown. In this cascade, calcium and protein kinase C serve as the central signaling molecules. See text for details. NHE‐3, Na+−H+ exchanger; IP3, inositol 1,4,5‐trisphosphate; PLCβ, phospholipase Cβ; PLA2 phospholipase A2; PLD, phospholipase D; MLC, myosin light chain; DAG, diacylglycerol; PKC, protein kinase C.
Figure 17. Figure 17.

Intracellular tyrosine phosphorylation cascades activated by AT1 receptor. The precise mechanism whereby the AT1 receptor activates tyrosine kinase activity is not known. Two potential mechanisms (via c‐SRC and/or Pyk2) are described in the text. PKC, protein kinase C; PLCγ, phospholipse Cγ; SOS, son of sevenless; IP3, inositol 1,4,5‐trisphosphate; DAG, diacylglycerol; PI3‐kinase, phosphatidylinositol‐3‐kinase; JNK, Jun N‐terminal kinase; MEK, mitogen activated protein kinase/extracellular signal‐regulated kinase kinase, POSH, “Plenty of SH”; ERK, “extracellular signal‐regulated kinase.”


Figure 1.

Generation and metabolism of angiotensin peptides. A: Classic pathway of angiotensin generation and subsequent cleavage steps. B: Generation of Angiotensin III bypassing Angiotensin II. C: Generation of Angiotensin (1–7) from Angiotensin I and subsequent cleavage steps. D: Generation of Angiotensin (1–7) from Angiotensin II.



Figure 2.

Autoregulation of renal blood flow and glomerular filtration rate. In sodium‐depleted dogs, renal perfusion pressure was reduced stepwise from a mean of 130 mm Hg to 70 mm Hg, in the absence or presence of the angiotensin‐converting enzyme inhibitor SQ‐20881. Glomerular filtration rate and efferent arteriolar resistance are dependent on angiotensin II (AII) as perfusion pressure falls. Afferent arteriolar resistance varies steeply with changes in perfusion pressure and is not dependent on AII. [From Hall 624 with permission.]



Figure 3.

Glomerular and peritubular capillary Starling forces. The hydraulic pressure gradient (black arrows) favoring fluid exit from capillaries is opposed by the oncotic pressure gradient (gray arrows). Net pressure gradient (ΔP) is shown below the panels. In glomerular capillaries, oncotic pressure rises as filtration removes protein‐free ultrafiltrate. Reduction of hydraulic pressure between glomerular and peritubular capillaries is due to efferent arteriolar resistance. In the presence of angiotensin II (bottom panel), the pressure profile is changed, resulting in higher end‐glomerular capillary and, hence, peritubular capillary oncotic pressure and reduced peritubular capillary hydraulic pressure.



Figure 4.

Structure of glomerular mesangium. Transmission electron micrograph of rat glomerulus, single glomerular capillary loop. Basement membrane is not circumferential. Mesangial cells are present in the glomerular interstitium. (Photomicrograph kindly provided by W. Kriz Ruprecht‐Karls‐Universitat, Heidelberg, Germany.)



Figure 5.

Effect of a kinin antagonist and enalaprilat on papillary blood flow in anesthetized rats. Each data point represents mean ± SE from eight rats. *P < 0.05 vs. control; C, P < 0.05 vs. kinin antagonist. Hence, angiotensin II has a significant effect on papillary blood flow when the vasodilatory effect of kinins is inhibited. [From Roman et al. 450 with permission.]



Figure 6.

Effect of angiotensin II (AII) on net proximal tubule fluid reabsorption. Angiotensin II (10 pM, left panel; 10 μ, M, right panel was added to the bath of isolated, perfused proximal tubules obtained from rabbits, and net fluid reabsorption (Jv) was measured during control, AII, and recovery periods. Individual data points are shown as line graphs, averaged data as bar graphs. This study was the first to show a direct and bimodal effect of AII on transport functions in isolated tubules. [From Schuster Kokko and Jacobson 491 with permission.]



Figure 7.

Sites of angiotensin II action in proximal tubule cells. Vectorial Na+ transport is accomplished by the restricted location of Na+−K+‐ATPase at the basolateral membrane (facing the interstitium) of polarized epithelia. Entry of Na+ from tubule lumen via the apical Na+−H+ exchanger (NHE) is down an electrochemical gradient generated by Na+−K+‐ATPase. Intracellular H+ is derived from CO2 and H2O through the action of carbonic anhydrase. H+ entering the tubule lumen is buffered by filtered HCO3−. Angiotensin II (large arrows) stimulates both apical NHE‐ and basolateral Na+−HCO3− transport activity.



Figure 8.

Sodium excretion during angiotensin II (AII) infusion is pressure dependent. Mean arterial pressure, cumulative sodium balance, and urinary sodium excretion in a dog (HS‐7) receiving a continuous infusion of AII. During the first 4 days, renal perfusion pressure was prevented from rising by a servocontrol device. Note progressive sodium retention and severe hypertension during this period. When renal pressure was allowed to rise to the level of the systemic pressure, natriuresis promptly ensued and sodium balance was restored. [From Hall, Granger, Hester et al. 200 with permission.]



Figure 9.

Role of angiotensin (AII) in maintaining stable blood pressure when salt intake changes. Sodium intake was varied in dogs given the angiotensin‐converting enzyme inhibitor SQ‐14225 (captopril) or AII (5 ng · kg−1 · min−1). Blood pressure falls significantly on a low‐salt diet when AII production is inhibited. Also, severe hypertension develops on high‐salt diets if circulating AII levels remain high. [From Hall et al. 625 with permission.]



Figure 10.

Vascular smooth muscle cell responses to angiotensin II (AII). A: Time course of AII (100 nM)‐induced aortic contraction. B: Time course of AII‐stimulated rise in cytosolic Ca2+ concentration. Time course of AII‐stimulated inositol 1,4,5‐trisphosphate (IP3) and diacylglycerol (DG) concentrations. D: Time‐course of vascular smooth muscle cell alkalinization in responses to AII. The dissociation between IP3 and diacylglycerol generation is accounted for by a switch from phospholipase Cβ‐dependent to phospholipase D dependent diacylglycerol generation. See text for details. [From Griendling et al. 180 with permission.]



Figure 11.

Aldosterone biosynthetic pathway. Angiotensin stimulates cholesterol transfer from outer mitochondrial membrane to the inner mitochondrial membrane, the rate‐limiting step in aldosterone synthesis. See text for details.



Figure 12.

Angiotensin II (AII) and Ca2+ dependence of cholesterol transfer. Cholesterol content in the outer mitochondrial membrane (OM), inner membrane contact sites (CS), and inner mitochondrial membrane (IM) after CaCl2 or angiotensin II stimulation in the presence or absence of cycloheximide (CHx). Cholesterol content in contact sites and inner mitochondrial membranes increases in response to angiotensin II and Ca2+ in a protein synthesis‐dependent fashion. On Western blots, the abundance of StAR (steroidogenic acute regulatory) protein similarly increases in response to stimulation with angiotensin II and Ca2+. [From Cherradi et al. 87 with permission.]



Figure 13.

Effect of AT2 receptor deficiency on drinking response. Mice deficient in AT2 receptors (−/Y) and wild‐type mice (+/Y) were deprived of water for 40 h, followed by a 3 h period during which they had free access to water. Although all mice lost an equivalent percentage of body weight during the deprivation period, the drinking response of AT2 receptor‐deficient mice was significantly less than that of wild‐type mice. [From Hein et al. 626 with permission.]



Figure 14.

Central effect of angiotensin II (AII) on blood pressure. A: Rate meter records of action potential firing frequency in the area postrema and blood pressure response following systemic administration of angiotensin II (50ng AII). B: Dose‐dependent blood pressure response to angiotensin II microinjection into the area postrema. [From Ferguson and Washburn 155 with permission.]



Figure 15.

Schematic view of AT1 receptor embedded in plasma membrane. The receptor consists of a seven‐transmembrane‐spanning domain, which forms a ring‐like structure. Angiotensin II (AII) is shown in its binding pocket. See text for details. [From Burns et al. 623 with permission.]



Figure 16.

Intracellular signals stimulated by AT1 receptor activation. Pathways dependent on Gq and Gi activation and their downstream effectors are shown. In this cascade, calcium and protein kinase C serve as the central signaling molecules. See text for details. NHE‐3, Na+−H+ exchanger; IP3, inositol 1,4,5‐trisphosphate; PLCβ, phospholipase Cβ; PLA2 phospholipase A2; PLD, phospholipase D; MLC, myosin light chain; DAG, diacylglycerol; PKC, protein kinase C.



Figure 17.

Intracellular tyrosine phosphorylation cascades activated by AT1 receptor. The precise mechanism whereby the AT1 receptor activates tyrosine kinase activity is not known. Two potential mechanisms (via c‐SRC and/or Pyk2) are described in the text. PKC, protein kinase C; PLCγ, phospholipse Cγ; SOS, son of sevenless; IP3, inositol 1,4,5‐trisphosphate; DAG, diacylglycerol; PI3‐kinase, phosphatidylinositol‐3‐kinase; JNK, Jun N‐terminal kinase; MEK, mitogen activated protein kinase/extracellular signal‐regulated kinase kinase, POSH, “Plenty of SH”; ERK, “extracellular signal‐regulated kinase.”

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Article Title: Angiotensins
 

How to Cite

Barbara J. Ballermann, Macaulay A. C. Onuigbo. Angiotensins. Compr Physiol 2011, Supplement 22: Handbook of Physiology, The Endocrine System, Endocrine Regulation of Water and Electrolyte Balance: 104-155. First published in print 2000. doi: 10.1002/cphy.cp070304