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Adrenergic Regulation of Vascular Smooth Muscle

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Abstract

The sections in this article are:

1 Morphology of Adrenergic Innervation
2 Adrenergic Transmission: Presynaptic and Synaptic Events
2.1 Transmitter Synthesis, Storage, and Release
2.2 Mode of Transmitter Release
2.3 Feedback Control of Transmitter Release
2.4 Transmitter Distribution and Movement
2.5 Transmitter Concentrations During Neural Activity
2.6 Transmitter Disposition and Termination of Its Effect
3 Adrenergic Transmission: Postsynaptic Events
3.1 Receptor Analysis and Variation
3.2 Bimodal Transmitter Action
3.3 Contractile Properties of Endothelium
4 Functional Consequences of Variation in Vascular Neuroeffector Apparatus
4.1 Synaptic Cleft Width
4.2 Innervation Density
4.3 Innervation Distribution
5 Functional Description of Specific Vessels
6 Adrenergic Neuron in Hypertension
6.1 Changes in Presynaptic Mechanisms
6.2 Neurogenic Transmission and Postsynaptic Function
6.3 Distribution of Adrenergic Transmitter in Hypertensive Arteries
6.4 Plasma Norepinephrine and Dopamine β‐Hydroxylase Levels
6.5 Interpretation of Changes in Adrenergic Mechanisms
7 Development of Adrenergic Control: Trophic Regulation
7.1 Ontogenetic Development of Innervation of Blood Vessels
7.2 Specificity of Adrenergic Innervation of Blood Vessels
7.3 Smooth Muscle Specificity for Nerve
7.4 Interactions of Nerve and Smooth Muscle
7.5 Influence of Adrenergic Nerves on Smooth Muscle
7.6 Influence of Smooth Muscle on Adrenergic Nerves
7.7 Factors Influencing Development and Maturation of Peripheral Sympathetic Nerve Terminals
7.8 Regulation of Sympathetic Function in Adults
7.9 Morphological and Functional Plasticity of Adrenergic Neurons
Figure 1. Figure 1.

Sympathetic innervation patterns in 2 blood vessels of rabbit. Specific catecholamine fluorescence induced by glyoxylic acid method. A: whole mount of distal portion of middle cerebral artery showing network of varicose fibers. B: transverse section of ear artery. Innervation is confined to adventitia. Internal elastic lamina and fine elastic fibers in adventitia are autofluorescent.

Figure 2. Figure 2.

Electron micrograph of human omental vein showing longitudinal section of a sympathetic nerve axon containing neurotubules (n) in parallel with a smooth muscle cell (SMC) with typical pinocytic vesicles (pv). Note presence of a neuronal varicosity containing large (lv) and small (sv) dense‐core vesicles, and mitochondria (m). A possible site of exocytosis is shown by unlabeled arrow. × 45,000.

From A. Thureson‐Klein, unpublished work
Figure 3. Figure 3.

Freeze‐etch study of innervation of mesenteric arteries of rat. A portion of vascular smooth muscle cell (sm) with an axon bundle in the adventitia is shown. Abundant collagen (col) and elastic tissue (el) is present around axon (ao), which is varicose (arrow). × 15,000.

From Devine et al.
Figure 4. Figure 4.

Biosynthesis of norepinephrine from tyrosine.

Figure 5. Figure 5.

Metabolism of norepinephrine. MAO, monoamine oxidase; COMT, catechol‐O‐methyltransferase; NE, norepinephrine; NM, normetanephrine; DHPG, 3,4‐dihydroxyphenylglycol; MHPG, 3‐methoxy‐4‐hydroxy‐phenylglycol; DHMA, 3,4‐dihydroxymandelic acid; VMA, 3‐methoxy‐4‐hydroxymandelic acid; Dehydro, dehydrogenase.

From Takimoto
Figure 6. Figure 6.

Influence of yohimbine on response of rabbit pulmonary artery to transmural sympathetic nerve stimulation. Strips of the artery were preincubated with [3H]NE and then superfused with medium containing 3 × 10−5 M cocaine, 4 × 10−5 M corticosterone, and 4 × 10−6 M propranolol. Each strip was stimulated four times for 3 min each at either 2 (•——•) or 4 (•——•) Hz. Ratio of tritium overflow evoked before and after exposure to yohimbine is shown. Each point is mean ± SEM of 3–7 experiments. Significant differences from controls (yohimbine concentration = 0); *, P < 0.02; **, P < 0.001.

From Starke et al.
Figure 7. Figure 7.

Mean increase in transmitter overflow after treatment with phenoxybenzamine and cocaine in relation to mean width of neuromuscular interval. 1, Guinea pig vas deferens; 2, rabbit atria; 3, portal vein; 4, guinea pig uterine artery; 5, rabbit ear artery; and 6, rabbit pulmonary artery.

1 and 3 from data of Hughes ; 2 from data of Rand et al. ; 4 from data of Bell and Vogt ; 5 from data of Kirpekar and Puig ; 6 from data of McCulloch, Bevan, and Su
Figure 8. Figure 8.

Distribution of 3H in wall of rabbit aorta pretreated with cocaine (10−3 M) for 30 min after exposure of intimal surface of vessel to [3H]norepinephrine (NE) (7.5 × 10−7 M) and cocaine for 20 s, 1 min, and 10 min. After exposure aorta strips were frozen and sections parallel to the intima were cut in a cryostat. Radioactivity in each section was expressed in terms of tissue:medium ratio, i.e., ml bath fluid cleared per gram tissue. Vertical bars represent SEM. Divisions on abscissa are 100 μm.

From Torok and Bevan , © 1971 The Williams & Wilkins Co., Baltimore
Figure 9. Figure 9.

Three‐dimensional representation of changes of transmitter concentration in relation to time after release and to distance from site of release of contents of one storage vesicle. Horizontal plane indicated by light dashed line indicates threshold concentration of a‐adrenergic receptor in most blood vessels. Subthreshold concentration curves are shown as heavy dashed line and dotted line where concentration curves cross diagram planes.

Figure 10. Figure 10.

Isometric force recording in grams from a segment of buccal portion of anterior facial vein of rabbit. Responses to norepinephrine (NE) and to transmural nerve stimulation (0.3 ms pulse duration of varying frequency) were obtained before and after addition of propranolol.

From Pegram, Bevan, and Bevan , by permission of the American Heart Association, Inc
Figure 11. Figure 11.

Isotonic contraction of isolated segments of saphenous vein of the dog in response to different concentrations of several adrenergic agonists. Solid lines show responses to epinephrine (E), norepinephrine (N), phenylephrine (P), and isoproterenol (I) in the presence of cocaine (1.4 × 10−5 M) to inhibit neuronal uptake, and in presence of U‐0521 (10−4 M) to inhibit catechol‐O‐methyltransferase. Broken lines show responses in presence of cocaine and U‐0521 plus propranolol (5 × 10−7 M) to inhibit β‐adrenergic receptors. Values are mean ± SEM.

Adapted from Guimaraes
Figure 12. Figure 12.

Concentration‐response curves showing relaxant effects of several adrenergic agonists in saphenous vein of dog. Tissue had been treated for 30 min with phenoxybenzamine (7.5 × 10−6 M) and was contracted by prostaglandin F (10−4 M). Values are mean ± SEM.

Adapted from Guimaraes
Figure 13. Figure 13.

Differences in relative magnitude of the two phases of response of perfused rabbit ear artery to different frequencies of stimulation or to different concentrations of transmitter. A: continuous nerve stimulation for 3 min at different frequencies. B: infusion of norepinephrine (NE) for 3 min at different concentrations. The same ear artery was used for both nerve stimulation and norepinephrine infusion.

From Steinsland et al. , by permission of the American Heart Association, Inc
Figure 14. Figure 14.

Diagrammatic representation of l‐norepinephrine doseresponse curve of rabbit pulmonary artery. Experimentally derived transmitter concentrations at 1 and 10 Hz at intra‐ (single line) and perisynaptic (double line) sites are shown in relation to this curve; α indicates α‐adrenergic receptor.

From Bevan . Reprinted from Federation Proceedings
Figure 15. Figure 15.

Diagrammatic representation of l‐norepinephrine dose‐response curve of rat portal vein. Experimentally derived transmitter concentrations at 1 and 10 Hz at intra‐ (single line) and perisynaptic (double line) sites are shown in relation to this curve; α indicates α‐adrenergic receptors.

From Bevan . Reprinted from Federation Proceedings
Figure 16. Figure 16.

Rate of change of diameter of dog femoral artery (•——•) and resistance vessels (○—○) induced by homolateral sympathetic trunk stimulation using triangular pulses at supramaximal intensity (5 ms duration at 15 Hz, plotted against duration of stimulation).

From Gero and Gerova , with permission of S. Karger AG, Basel
Figure 17. Figure 17.

Steady‐state neurogenic response of small saphenous and anterior mesenteric veins of rabbit at different stimulation frequencies, expressed as percentage of maximum norepinephrine response. Values are mean ± SEM.

From Bevan . Reprinted from Federation Proceedings
Figure 18. Figure 18.

Relation between steady‐state neurogenic contractile response in grams of cephalic and saphenous vein segments at 10 Hz and carotid arterial pressure of rabbits with partial constriction of abdominal aorta and their sham‐operated controls.

From Bevan, Bevan, et al. with permission of S. Karger AG, Basel
Figure 19. Figure 19.

Relation of mean blood pressure to plasma norepinephrine in 16 quadriplegic humans at rest, and during and after bladder and muscle stimulation.

From Mathias et al. , by permission of the American Heart Association, Inc
Figure 20. Figure 20.

Schematic representation of pattern of development of adrenergic neuroeffector mechanisms in carotid artery from fetal sheep. MAO and COMT are total vessel monoamine oxidase and catechol‐O‐methyltransferase, respectively. Curves labeled α‐receptor, NE uptake, and NE release represent relative size of the experimental in vitro response to exogenous norepinephrine, neuronal uptake of norepinephrine, and neurogenic contractile response to field stimulation, respectively.

From Su, Bevan, et al. , with permission of S. Karger AG, Basel
Figure 21. Figure 21.

A: changes in maximum force developed to norepinephrine (NE), wall thickness, tissue weight, and NE ED50 by standard segment of ear artery from growing rabbit 2 mo after unilateral superior cervical ganglionectomy (n = 8). Denervation was confirmed in each instance by fluorescence microscopy. P values refer to paired comparisons of data. B: passive stress‐length curves of innervated and contralateral denervated segments of rabbit ear arteries. At longer lengths, tangential elastic modulus is greater for denervated compared with innervated arteries (*P < 0.05; **P < 0.01; n = 20).

From Bevan and Tsuru , by permission of the American Heart Association, Inc


Figure 1.

Sympathetic innervation patterns in 2 blood vessels of rabbit. Specific catecholamine fluorescence induced by glyoxylic acid method. A: whole mount of distal portion of middle cerebral artery showing network of varicose fibers. B: transverse section of ear artery. Innervation is confined to adventitia. Internal elastic lamina and fine elastic fibers in adventitia are autofluorescent.



Figure 2.

Electron micrograph of human omental vein showing longitudinal section of a sympathetic nerve axon containing neurotubules (n) in parallel with a smooth muscle cell (SMC) with typical pinocytic vesicles (pv). Note presence of a neuronal varicosity containing large (lv) and small (sv) dense‐core vesicles, and mitochondria (m). A possible site of exocytosis is shown by unlabeled arrow. × 45,000.

From A. Thureson‐Klein, unpublished work


Figure 3.

Freeze‐etch study of innervation of mesenteric arteries of rat. A portion of vascular smooth muscle cell (sm) with an axon bundle in the adventitia is shown. Abundant collagen (col) and elastic tissue (el) is present around axon (ao), which is varicose (arrow). × 15,000.

From Devine et al.


Figure 4.

Biosynthesis of norepinephrine from tyrosine.



Figure 5.

Metabolism of norepinephrine. MAO, monoamine oxidase; COMT, catechol‐O‐methyltransferase; NE, norepinephrine; NM, normetanephrine; DHPG, 3,4‐dihydroxyphenylglycol; MHPG, 3‐methoxy‐4‐hydroxy‐phenylglycol; DHMA, 3,4‐dihydroxymandelic acid; VMA, 3‐methoxy‐4‐hydroxymandelic acid; Dehydro, dehydrogenase.

From Takimoto


Figure 6.

Influence of yohimbine on response of rabbit pulmonary artery to transmural sympathetic nerve stimulation. Strips of the artery were preincubated with [3H]NE and then superfused with medium containing 3 × 10−5 M cocaine, 4 × 10−5 M corticosterone, and 4 × 10−6 M propranolol. Each strip was stimulated four times for 3 min each at either 2 (•——•) or 4 (•——•) Hz. Ratio of tritium overflow evoked before and after exposure to yohimbine is shown. Each point is mean ± SEM of 3–7 experiments. Significant differences from controls (yohimbine concentration = 0); *, P < 0.02; **, P < 0.001.

From Starke et al.


Figure 7.

Mean increase in transmitter overflow after treatment with phenoxybenzamine and cocaine in relation to mean width of neuromuscular interval. 1, Guinea pig vas deferens; 2, rabbit atria; 3, portal vein; 4, guinea pig uterine artery; 5, rabbit ear artery; and 6, rabbit pulmonary artery.

1 and 3 from data of Hughes ; 2 from data of Rand et al. ; 4 from data of Bell and Vogt ; 5 from data of Kirpekar and Puig ; 6 from data of McCulloch, Bevan, and Su


Figure 8.

Distribution of 3H in wall of rabbit aorta pretreated with cocaine (10−3 M) for 30 min after exposure of intimal surface of vessel to [3H]norepinephrine (NE) (7.5 × 10−7 M) and cocaine for 20 s, 1 min, and 10 min. After exposure aorta strips were frozen and sections parallel to the intima were cut in a cryostat. Radioactivity in each section was expressed in terms of tissue:medium ratio, i.e., ml bath fluid cleared per gram tissue. Vertical bars represent SEM. Divisions on abscissa are 100 μm.

From Torok and Bevan , © 1971 The Williams & Wilkins Co., Baltimore


Figure 9.

Three‐dimensional representation of changes of transmitter concentration in relation to time after release and to distance from site of release of contents of one storage vesicle. Horizontal plane indicated by light dashed line indicates threshold concentration of a‐adrenergic receptor in most blood vessels. Subthreshold concentration curves are shown as heavy dashed line and dotted line where concentration curves cross diagram planes.



Figure 10.

Isometric force recording in grams from a segment of buccal portion of anterior facial vein of rabbit. Responses to norepinephrine (NE) and to transmural nerve stimulation (0.3 ms pulse duration of varying frequency) were obtained before and after addition of propranolol.

From Pegram, Bevan, and Bevan , by permission of the American Heart Association, Inc


Figure 11.

Isotonic contraction of isolated segments of saphenous vein of the dog in response to different concentrations of several adrenergic agonists. Solid lines show responses to epinephrine (E), norepinephrine (N), phenylephrine (P), and isoproterenol (I) in the presence of cocaine (1.4 × 10−5 M) to inhibit neuronal uptake, and in presence of U‐0521 (10−4 M) to inhibit catechol‐O‐methyltransferase. Broken lines show responses in presence of cocaine and U‐0521 plus propranolol (5 × 10−7 M) to inhibit β‐adrenergic receptors. Values are mean ± SEM.

Adapted from Guimaraes


Figure 12.

Concentration‐response curves showing relaxant effects of several adrenergic agonists in saphenous vein of dog. Tissue had been treated for 30 min with phenoxybenzamine (7.5 × 10−6 M) and was contracted by prostaglandin F (10−4 M). Values are mean ± SEM.

Adapted from Guimaraes


Figure 13.

Differences in relative magnitude of the two phases of response of perfused rabbit ear artery to different frequencies of stimulation or to different concentrations of transmitter. A: continuous nerve stimulation for 3 min at different frequencies. B: infusion of norepinephrine (NE) for 3 min at different concentrations. The same ear artery was used for both nerve stimulation and norepinephrine infusion.

From Steinsland et al. , by permission of the American Heart Association, Inc


Figure 14.

Diagrammatic representation of l‐norepinephrine doseresponse curve of rabbit pulmonary artery. Experimentally derived transmitter concentrations at 1 and 10 Hz at intra‐ (single line) and perisynaptic (double line) sites are shown in relation to this curve; α indicates α‐adrenergic receptor.

From Bevan . Reprinted from Federation Proceedings


Figure 15.

Diagrammatic representation of l‐norepinephrine dose‐response curve of rat portal vein. Experimentally derived transmitter concentrations at 1 and 10 Hz at intra‐ (single line) and perisynaptic (double line) sites are shown in relation to this curve; α indicates α‐adrenergic receptors.

From Bevan . Reprinted from Federation Proceedings


Figure 16.

Rate of change of diameter of dog femoral artery (•——•) and resistance vessels (○—○) induced by homolateral sympathetic trunk stimulation using triangular pulses at supramaximal intensity (5 ms duration at 15 Hz, plotted against duration of stimulation).

From Gero and Gerova , with permission of S. Karger AG, Basel


Figure 17.

Steady‐state neurogenic response of small saphenous and anterior mesenteric veins of rabbit at different stimulation frequencies, expressed as percentage of maximum norepinephrine response. Values are mean ± SEM.

From Bevan . Reprinted from Federation Proceedings


Figure 18.

Relation between steady‐state neurogenic contractile response in grams of cephalic and saphenous vein segments at 10 Hz and carotid arterial pressure of rabbits with partial constriction of abdominal aorta and their sham‐operated controls.

From Bevan, Bevan, et al. with permission of S. Karger AG, Basel


Figure 19.

Relation of mean blood pressure to plasma norepinephrine in 16 quadriplegic humans at rest, and during and after bladder and muscle stimulation.

From Mathias et al. , by permission of the American Heart Association, Inc


Figure 20.

Schematic representation of pattern of development of adrenergic neuroeffector mechanisms in carotid artery from fetal sheep. MAO and COMT are total vessel monoamine oxidase and catechol‐O‐methyltransferase, respectively. Curves labeled α‐receptor, NE uptake, and NE release represent relative size of the experimental in vitro response to exogenous norepinephrine, neuronal uptake of norepinephrine, and neurogenic contractile response to field stimulation, respectively.

From Su, Bevan, et al. , with permission of S. Karger AG, Basel


Figure 21.

A: changes in maximum force developed to norepinephrine (NE), wall thickness, tissue weight, and NE ED50 by standard segment of ear artery from growing rabbit 2 mo after unilateral superior cervical ganglionectomy (n = 8). Denervation was confirmed in each instance by fluorescence microscopy. P values refer to paired comparisons of data. B: passive stress‐length curves of innervated and contralateral denervated segments of rabbit ear arteries. At longer lengths, tangential elastic modulus is greater for denervated compared with innervated arteries (*P < 0.05; **P < 0.01; n = 20).

From Bevan and Tsuru , by permission of the American Heart Association, Inc
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John A. Bevan, Rosemary D. Bevan, Sue P. Duckles. Adrenergic Regulation of Vascular Smooth Muscle. Compr Physiol 2011, Supplement 7: Handbook of Physiology, The Cardiovascular System, Vascular Smooth Muscle: 515-566. First published in print 1980. doi: 10.1002/cphy.cp020218