Comprehensive Physiology Wiley Online Library

Cholinergic and Purinergic Regulation of Blood Vessels

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Abstract

The sections in this article are:

1 Neuroeffector Junctions in Blood Vessels
2 Identification of Autonomic Nerves
2.1 Cholinergic Nerves
2.2 Adrenergic Nerves
2.3 Purinergic Nerves
2.4 Other Nerve Profiles
3 Cholinergic Regulation
3.1 Methods of Identifying Cholinergic Vasomotor Nerves
3.2 Electrophysiology of Vasomotor Action of Acetylcholine
3.3 Regional Cholinergic Vasomotor Control
3.4 Comparative Studies in Lower Vertebrates
4 Purinergic Regulation
4.1 Methods of Identifying Purinergic Nerves
4.2 Purinergic Receptors
4.3 Regional Purinergic Vasomotor Control
5 Neuromodulation of Vasomotor Activity
5.1 Modulation of Adrenergic Nerve Activity by Acetylcholine, ATP, and Adenosine
5.2 Modulation of Cholinergic Nerve Activity by Catecholamine, ATP, and Adenosine
6 Summary
Figure 1. Figure 1.

A: schematic representation of control of visceral smooth muscle. B: schematic representation of control of vascular smooth muscle. Connected dots, nerves; arrows, circulating catecholamines.

Adapted from Burnstock and Iwayama and from Burnstock
Figure 2. Figure 2.

A: synaptic cleft and postsynaptic specialization in guinea pig sphincter pupillae. Note the subsurface cisterna (C) beneath the plasma membrane of the muscle cell (M) in the close‐contact (within 20 nm) area between the naked axon (A) and the muscle cell. Cytoplasmic zone between the muscle cell membrane and distal membrane of the cisterna is consistent in width (15–17 nm) and contains a continuous electron‐opaque intermediate layer (arrow). × 142,500. Inset is a high‐power electron micrograph showing the organized cytoplasmic zone containing the intermediate layer (arrow) about 4 nm thick between the plasma membrane of muscle cell (M) and the distal membrane of the cisterna. The intermediate layer is about 8 nm apart from the plasma membrane and about 4 nm from the distal cisternal membrane. A, terminal axon; V, synaptic vesicle. × 300,000. B: relation of axons (A) and smooth muscle (M) at the adventitial‐medial border of the anterior cerebral artery of the rat. Axons are devoid of Schwann cytoplasm (S) on the side facing the muscle, and they approach the muscle surface as close as 80 nm. Basement membrane material is interposed between axonal and smooth muscle membranes. There are many synaptic vesicles and mitochondria in the terminal varicosities. Some small and large granular vesicles are also present.

A from Uehara and Burnstock ; B from Burnstock et al.
Figure 3. Figure 3.

Diagrammatic representation of sections through the terminal varicosities of autonomic nerves.

Adapted from Burnstock and Iwayama
Figure 4. Figure 4.

A: precapillary sphincter region in coronary vascular bed of rat. Note several nerve profiles (asterisks) at the branching site. Cap, capillary; Art, arteriole. Glutaraldehyde‐osmium fixation. B: higher magnification showing axon profiles of at least three types; the profile labeled Ch contains a predominance of small agranular vesicles and is probably cholinergic; the profile labeled S is packed with mitochondria and may be sensory; two of the three remaining profiles contain some granular vesicles and are probably adrenergic. Glutaraldehyde‐osmium fixation.

From I. Yohro and G. Burnstock, unpublished observations
Figure 5. Figure 5.

Axon profiles near the anterior cerebral artery of a rat injected with 6‐hydroxydopamine (250 mg/kg) 1 h before decapitation. Adrenergic axon (Ad) has many small vesicles with distinct electron‐opaque cores and also with large, densely granulated vesicles. Cholinergic axon (Ch) contains no small granular vesicles, but many small agranular vesicles and a few large vesicles with moderately granular cores. Osmium fixation: calibration, 0.5 μm.

From Iwayama, Furness, and Burnstock,
Figure 6. Figure 6.

A: control sample of axon at the periphery of an arteriovenous anastomosis in the carpal skin of sheep. Axon contains many large vesicles whose contents show a gradation in density and that are comparable to large opaque vesicles in purinergic nerves in the gut and lung. B: axons at the periphery of an arteriovenous anastomosis in sheep carpal skin 1 wk after surgical sympathectomy. Degenerated axons are enclosed by Schwann cell cytoplasm, but an unaffected axon containing large opaque vesicles remains.

From Molyneux
Figure 7. Figure 7.

Electron micrographs of an intimal cushion at the orifice of the rat septal artery at its junction with the left coronary artery. A: scanning electron micrograph demonstrating the well‐developed ridge of the cushion around the orifice. ×360. B: transmission electron micrograph through a ridge, showing the complex relationships of smooth muscle cells and the presence of nerves (arrows).

From Burnstock
Figure 8. Figure 8.

Demonstration of functional cholinergic vasodilator fibers to guinea pig uterus in middle and late pregnancy. Responses that the parametrial artery exhibits toward periarterial nerve stimulation at 20 pulses/s (solid circles), showing vasoconstrictor (deflection upwards) and vasodilator (deflection downwards) responses. A, consecutive periods of stimulation before and during infusion of norepinephrine (5 × 10−7 g/ml). B, basal tone, pure constriction. C, blockade of the constriction after bretylium (2 × 10−6 g/ml). D, in a preparation in which the tone was increased with norepinephrine (10−6 g/ml), dilatation to nerve stimulation in the absence of constrictor fiber influence. E, control response to nerve stimulation. F, response in presence of neostigmine (10−6 g/ml). G, response after subsequent addition of hyoscine (2 × 10−6 g/ml). H, response to acetylcholine (ACh) obtained in the presence of norepinephrine (5 × 10−7 g/ml).

Adapted from Bell
Figure 9. Figure 9.

Middle cerebral artery of monkey, with acetylcholinesterase‐positive staining fibers. Section was incubated with acetylthiocholine and a selective inhibitor of pseudocholinesterases.

From Denn and Stone
Figure 10. Figure 10.

Schematic representation of storage, release, and inactivation of ATP at the purinergic neuromuscular junction.

From Burnstock
Figure 11. Figure 11.

Classic and new concepts of sympathetic innervation of blood vessels in skeletal muscle. For convenience, terminal ganglion cells are shown external to vessel; cells actually lie within arteriolar walls. ACH, acetylcholine; NE, norepinephrine.

From Myers et al.
Figure 12. Figure 12.

Schematic hypotheses of the neurogenic basis of reflex vasodilatation in skin vessels. One proposal is that Substance P (Subst. P), a putative transmitter in sensory nerve endings in the spinal cord, is released from sensory nerve collaterals in the skin. Another is that ATP is the transmitter released from these collaterals. Both these substances are powerful vasodilators and can release histamine from mast cells. ATP is also a potent inducer of prostaglandin synthesis. A further possibility is that a peripherally placed purinergic neuron is interposed between the sensory nerve collateral and the effector system; this proposal takes into account histological reports that neurons exist in the skin and provides an alternative explanation for the initiation of the vasodilator reflex by nicotine and the block of the reflex by hexamethonium.

From Burnstock
Figure 13. Figure 13.

After intraneuronal application [3H]adenosine derivatives are transported within dendrites (arrowhead) and are released to the neighboring neuropile. There glial cells (small arrow) as well as cells of the vessel wall (large arrows) are labeled. Autoradiograph counterstained with Toluidine Blue.

From Schubert and Kreutzberg
Figure 14. Figure 14.

The effect of adenosine on saphenous vein strip during electrical stimulation.

From Verhaeghe and Vanhoutte


Figure 1.

A: schematic representation of control of visceral smooth muscle. B: schematic representation of control of vascular smooth muscle. Connected dots, nerves; arrows, circulating catecholamines.

Adapted from Burnstock and Iwayama and from Burnstock


Figure 2.

A: synaptic cleft and postsynaptic specialization in guinea pig sphincter pupillae. Note the subsurface cisterna (C) beneath the plasma membrane of the muscle cell (M) in the close‐contact (within 20 nm) area between the naked axon (A) and the muscle cell. Cytoplasmic zone between the muscle cell membrane and distal membrane of the cisterna is consistent in width (15–17 nm) and contains a continuous electron‐opaque intermediate layer (arrow). × 142,500. Inset is a high‐power electron micrograph showing the organized cytoplasmic zone containing the intermediate layer (arrow) about 4 nm thick between the plasma membrane of muscle cell (M) and the distal membrane of the cisterna. The intermediate layer is about 8 nm apart from the plasma membrane and about 4 nm from the distal cisternal membrane. A, terminal axon; V, synaptic vesicle. × 300,000. B: relation of axons (A) and smooth muscle (M) at the adventitial‐medial border of the anterior cerebral artery of the rat. Axons are devoid of Schwann cytoplasm (S) on the side facing the muscle, and they approach the muscle surface as close as 80 nm. Basement membrane material is interposed between axonal and smooth muscle membranes. There are many synaptic vesicles and mitochondria in the terminal varicosities. Some small and large granular vesicles are also present.

A from Uehara and Burnstock ; B from Burnstock et al.


Figure 3.

Diagrammatic representation of sections through the terminal varicosities of autonomic nerves.

Adapted from Burnstock and Iwayama


Figure 4.

A: precapillary sphincter region in coronary vascular bed of rat. Note several nerve profiles (asterisks) at the branching site. Cap, capillary; Art, arteriole. Glutaraldehyde‐osmium fixation. B: higher magnification showing axon profiles of at least three types; the profile labeled Ch contains a predominance of small agranular vesicles and is probably cholinergic; the profile labeled S is packed with mitochondria and may be sensory; two of the three remaining profiles contain some granular vesicles and are probably adrenergic. Glutaraldehyde‐osmium fixation.

From I. Yohro and G. Burnstock, unpublished observations


Figure 5.

Axon profiles near the anterior cerebral artery of a rat injected with 6‐hydroxydopamine (250 mg/kg) 1 h before decapitation. Adrenergic axon (Ad) has many small vesicles with distinct electron‐opaque cores and also with large, densely granulated vesicles. Cholinergic axon (Ch) contains no small granular vesicles, but many small agranular vesicles and a few large vesicles with moderately granular cores. Osmium fixation: calibration, 0.5 μm.

From Iwayama, Furness, and Burnstock,


Figure 6.

A: control sample of axon at the periphery of an arteriovenous anastomosis in the carpal skin of sheep. Axon contains many large vesicles whose contents show a gradation in density and that are comparable to large opaque vesicles in purinergic nerves in the gut and lung. B: axons at the periphery of an arteriovenous anastomosis in sheep carpal skin 1 wk after surgical sympathectomy. Degenerated axons are enclosed by Schwann cell cytoplasm, but an unaffected axon containing large opaque vesicles remains.

From Molyneux


Figure 7.

Electron micrographs of an intimal cushion at the orifice of the rat septal artery at its junction with the left coronary artery. A: scanning electron micrograph demonstrating the well‐developed ridge of the cushion around the orifice. ×360. B: transmission electron micrograph through a ridge, showing the complex relationships of smooth muscle cells and the presence of nerves (arrows).

From Burnstock


Figure 8.

Demonstration of functional cholinergic vasodilator fibers to guinea pig uterus in middle and late pregnancy. Responses that the parametrial artery exhibits toward periarterial nerve stimulation at 20 pulses/s (solid circles), showing vasoconstrictor (deflection upwards) and vasodilator (deflection downwards) responses. A, consecutive periods of stimulation before and during infusion of norepinephrine (5 × 10−7 g/ml). B, basal tone, pure constriction. C, blockade of the constriction after bretylium (2 × 10−6 g/ml). D, in a preparation in which the tone was increased with norepinephrine (10−6 g/ml), dilatation to nerve stimulation in the absence of constrictor fiber influence. E, control response to nerve stimulation. F, response in presence of neostigmine (10−6 g/ml). G, response after subsequent addition of hyoscine (2 × 10−6 g/ml). H, response to acetylcholine (ACh) obtained in the presence of norepinephrine (5 × 10−7 g/ml).

Adapted from Bell


Figure 9.

Middle cerebral artery of monkey, with acetylcholinesterase‐positive staining fibers. Section was incubated with acetylthiocholine and a selective inhibitor of pseudocholinesterases.

From Denn and Stone


Figure 10.

Schematic representation of storage, release, and inactivation of ATP at the purinergic neuromuscular junction.

From Burnstock


Figure 11.

Classic and new concepts of sympathetic innervation of blood vessels in skeletal muscle. For convenience, terminal ganglion cells are shown external to vessel; cells actually lie within arteriolar walls. ACH, acetylcholine; NE, norepinephrine.

From Myers et al.


Figure 12.

Schematic hypotheses of the neurogenic basis of reflex vasodilatation in skin vessels. One proposal is that Substance P (Subst. P), a putative transmitter in sensory nerve endings in the spinal cord, is released from sensory nerve collaterals in the skin. Another is that ATP is the transmitter released from these collaterals. Both these substances are powerful vasodilators and can release histamine from mast cells. ATP is also a potent inducer of prostaglandin synthesis. A further possibility is that a peripherally placed purinergic neuron is interposed between the sensory nerve collateral and the effector system; this proposal takes into account histological reports that neurons exist in the skin and provides an alternative explanation for the initiation of the vasodilator reflex by nicotine and the block of the reflex by hexamethonium.

From Burnstock


Figure 13.

After intraneuronal application [3H]adenosine derivatives are transported within dendrites (arrowhead) and are released to the neighboring neuropile. There glial cells (small arrow) as well as cells of the vessel wall (large arrows) are labeled. Autoradiograph counterstained with Toluidine Blue.

From Schubert and Kreutzberg


Figure 14.

The effect of adenosine on saphenous vein strip during electrical stimulation.

From Verhaeghe and Vanhoutte
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Geoffrey Burnstock. Cholinergic and Purinergic Regulation of Blood Vessels. Compr Physiol 2011, Supplement 7: Handbook of Physiology, The Cardiovascular System, Vascular Smooth Muscle: 567-612. First published in print 1980. doi: 10.1002/cphy.cp020219