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1 Experimental Research Department and Institute of Human Physiology, and 2 Faculty of Medicine, Department of Anatomy, Histology, and Embriology, Semmelweis University, 1082 Budapest, Hungary
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The aim of this study
was to quantitate the density of nerve terminals as well as their
synaptic vesicle population in the adventitia of saphenous (SV and SA)
and brachial veins and arteries (BV and BA) obtained from rats
maintained in a horizontal control or a tilted position. Adult animals
were kept individually in tubelike cages in a 45° head-up position.
After 2 wk, both tilted and control animals were anesthetized, and the
whole body was perfused with fixative solution at physiological
pressure. Vessels segments were then excised for electron microscopy
and immunohistochemistry. The nerve terminal density (NTD) of SA was
8.20 ± 1.46 nerve terminals/100 µm2 cross section
of adventitia and that of SV was 4.53 ± 0.61 nerve terminals/100
µm2 cross section of adventitia in control rats. Tilting
caused a significant increase in NTD of both SA (70%) and SV (52%).
The synaptic microvesicle density (SyVD) was larger in SA than SV in
control rats (30.48 ± 4.41 vs. 13.38 ± 2.61 synaptic
vesicles/10 terminal sections), but tilting resulted in more pronounced
changes in SyVD of SV (95%) than SA (54%). No significant changes in
NTD and SyVD of BA were found after tilt (
3.6% relative to 4.99 ± 0.33 compared with 0.4% relative to 24.89 ± 3.7, respectively). Whereas NTD of BV exhibited a tendency to increase
(3.73 ± 0.86 vs. 2.31 ± 0.29 nerve terminals/100
µm2 cross section of adventitia), SyVD did not
change significantly (18.96 ± 2.74 vs. 22.85 ± 3.17 synaptic vesicles/10 terminal sections). A large number of
nerve terminals of all vessels were tyrosine hydroxylase immunoreactive
(containing norepinephrine). These findings support the hypothesis that
long-term gravitational load causes adaptive morphological and
functional remodeling of sympathetic innervation in blood vessels of
the extremities.
innervation of extremity arteries; innervation of extremity veins; neural remodeling; tilting head up; vascular adaptation to gravity
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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CONSIDERABLE EXPERIMENTAL evidence has accumulated in literature related to gravity-dependent short-term sympathetic vasoconstrictor responses in skeletal muscles (3, 8, 9, 11, 12, 20-22, 25-27). There is also evidence for trophic actions of sympathetic innervation on vascular pattern and structure (2, 5, 10), suggesting that such mechanisms should be considered when evaluating the long-term morphological and functional remodeling of blood vessels in response to chronic stimuli such as gravitational stress. There is a paucity of data on this subject, and the venous vasculature has been especially neglected. Adaptation of veins to orthostatic stress is important to understand given the position of our bodies during many conditions such as prolonged standing, prolonged bed rest, conditions of microgravity, and a number of other conditions that expose the veins to long-term changes in mechanical stress and sympathetic tone (23).
To study the adaptive mechanisms of blood vessels in the extremities to prolonged experimental orthostatic body position, rats were placed in special tubelike tiltable transparent cages (45° head-up tilt) as described previously (16). The animals were allowed to move freely along the individual cages in a head-up position, and they could rotate around the longitudinal axis of their body; however, they could not turn back. We have shown that this head-up tilt position resulted in an immediate and permanent doubling of saphenofemoral venous pressure, whereas arterial mean pressure does not significantly change (16). Several studies have been performed to characterize rats living under these conditions. The movement of the rats was studied using a video computer based on an infrared tracking method to continuously record and quantitate the locomotion of these animals, and it has been demonstrated that the circadian pattern of locomotor activity did not differ from that of control rats maintained in horizontal cages (18, 20). However, significant changes in biomechanical and electrophysiological properties of the saphenous vein from rats tilted for 2 wk were observed. These changes included enhancement of acute pressure-induced myogenic responses and an increase in the passive lumen capacity of the vessel without a substantial change in wall thickness. Furthermore, the sympathetic component of the smooth muscle membrane (SMM) potential, measured in vivo, was significantly augmented in the saphenous vein but not in the saphenous artery or in brachial vessels (14-17, 19). Other studies have also indicated that the veins of dependent limbs in humans exhibit significant myogenic responses. Specifically, human saphenous veins react to sudden pressure increases with much larger myogenic responses than tilted rat saphenous veins or canine femoral veins. No substantial myogenic response could be elicited in human brachiocephalic veins and canine femoral veins. Furthermore, we (1, 24) demonstrated that calcium- and voltage-dependent potassium ion channels counterregulate the depolarization associated with the myogenic response in human saphenous vein SMM but not in brachiocephalic vein SMM or in rat saphenous vein SMM. Consistent with these observations, it has also been shown that sympathoadrenergic influences via norepinephrine may substantially augment the venular myogenic response (4).
On the basis of these observations, we hypothesized that long-term increases in the orthostatic gravitational load to dependent limbs would induce morphological and functional changes in blood vessels including changes of vascular sympathetic innervation. Thus the aim of the present study was to quantitate and compare the nerve terminal density (NTD) and the synaptic vesicle population [synaptic microvesicle density (SyVD)] in the saphenous vein and artery and in the brachial vein and artery obtained from rats maintained in the horizontal or in the tilted (45° head-up tilt) position for 2 wk. Electron microscopy and immunohistochemical techniques were used to determine tyrosine hydroxylase (TH), vasoactive intestinal polypeptide (VIP), and neuronal nitric oxide synthase (NOS). The findings of this study indicate that long-term changes in gravitational load may induce regionally different morphological and functional adaptation of blood vessels including local sympathetic neural mechanisms.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Experimental animals and chronic tilt. Adult male Sprague-Dawley rats of 300-400 g body wt were placed individually in specially designed, 65-cm-long, tubelike tiltable cages fabricated from transparent acrylic plastic and described in earlier studies (16, 18). Rats were kept in either the horizontal or head-up tilted body position. Tilted rats (n = 9) lived in cages set in the 45° oblique position to maintain an experimental orthostatic body posture for 2 wk. The animals could walk up and back down on the metal grid of the cage but they could not turn around. They had free access to food (conventional rat chow) and tap water at the upper end of the cage. Rats (n = 9) kept in the same type of tubular cages but in a horizontal position for 2 wk served as parallel controls. Animals in both groups were removed for 1-h periods each day and allowed free grooming in a traditional rat cage. This time was also used for measurement of body weight, daily food and water intake, and for cleaning of cages. Three tilted and three control animals were studied in parallel simultaneously in an air-conditioned room containing six tubular tilt cages. Studies were approved by the Semmelweis University Committee on the Ethical Use of Experimental Animals (590/99 Rh).
Preparation of tissues for electron microscopy. After 2 wk in the tubular cages, animals were anesthetized with pentobarbital sodium (Nembutal; 4 mg/100 g ip). The vasculature was then perfused and fixed with a solution containing 3% paraformaldehyde and 0.1% glutaraldehyde in 0.2 M phosphate buffer that was delivered into the aorta at a perfusion pressure controlled at 100 mmHg. Vascular segments for electron microscopy were carefully prepared from saphenous and brachial arteries and veins. Small pieces of the specimens were postfixed in the same fixative solution and then treated in 1% osmic acid for 2 h before being embedded into Araldite. Ultrathin tissue sections were prepared and then stained with uranyl acetate and lead citrate. Electron micrographs were taken using an electron microscope (model 100, Jeol; Tokyo, Japan).
Determination of innervation density.
The NTD in the vascular wall was estimated by projecting the cross
section of the vessels onto the screen of the electron microscope
(×38,000-42,000) and measuring by planimetry along the entire
adventitia of a given vascular section. In this way, adventitial areas
of 4,000-6,000 µm2 were examined in each vessel type
of each animal. All of the nerve terminals seen were carefully
identified, including cross sections of both varicosities and
intervaricosity portions (the presence of mitochondria, microfilaments,
and microtubules was also used as markers). The varicosities
characteristically contain synaptic microvesicles, but intervaricosity
terminal portions usually do not (6). All of the
microvesicles were counted in the nerve terminals. NTD was expressed as
the number of terminals per 100 µm2 of adventitia. The
magnitude of the SyVD was characterized in each vessel by calculating
the average number of vesicles per cross section of 10 nerve terminals
from a total of 38-45 terminal cross sections identified in the
whole adventitial area examined. All of the morphological examinations
were done by the same investigator (E. Fehér) following a
"double-blind" design procedure. After the morphological analysis
was completed, several areas were selected for documentation and
photographed, as demonstrated in Fig. 1, a-c.
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Immunohistochemistry. TH (for norepinephrine), neuronal NOS, and VIP were detected in the nerve terminals of the vessel sections utilizing techniques of immunohistochemistry. Whole body fixation of three control and three tilted rats was carried out by perfusion with Zamboni solution (4% paraformaldehyde, 0.1% glutaraldehyde, and 0.19% picric acid in 0.1 M phosphate buffer; pH 7.3). Blood vessels were kept in a glutaraldehyde-free fixative containing 10% sucrose at 4°C overnight. Sections (40 µm thick) were cut on a Vibrotome (TPI; St. Louis, MO) and then rinsed in several changes of phosphate-buffered saline (PBS). Free-floating sections were washed with PBS and treated with 3% H2O2 for 10 min to reduce endogenous peroxidase activity. They were then incubated in 0.1 M PBS containing 10% normal goat serum at room temperature for 1 h. Rabbit anti-rat primary antibodies were used to detect TH at a dilution of 1:10,000 (Institute Jacques Boy; No. C. P. 208020234), NOS (specific for neuronal NOS) at a dilution of 1:1,000 (Affinit Research Products; Nottingham, UK), and VIP at a dilution of 1:10,000 (Amersham, PRN 1852, Lot 17). All antibodies were diluted with 0.1 M PBS containing 1% normal goat serum, 0.3% Triton X-100, and 0.1% sodium azide.
The sections were incubated with a primary antibody for 48 h at 4°C, subsequently rinsed, and then incubated with biotynilated anti-rabbit IgG (dilution, 1:500) for 4 h, followed by avidin-biotin-peroxidase complex (dilution, 1:250; Vector) for 1 h each at room temperature. Between each incubation step, sections were rinsed throughly with three changes of PBS for 15 min each. The tissue-bound peroxidase activity was visualized with 0.02% 3.3-diamino-benzidine in 0.05 M Tris · HCl buffer (pH 7.6) containing 0.6% nickel ammonium sulfate and 0.0021% H2O2. Sections were mounted on gelatinized slides, dehydrated, and coverslipped with Depex. As controls for immunohistochemical specificity, the primary antibody was omitted from the incubation steps or preabsorption of the antibodies with the appropriate synthetic peptides was carried out before immunohistochemical staining. No immunostaining was found in these cases.Statistical analysis. Two-factor ANOVA was used for the final statistical evaluations of the experimental data, with P < 0.05 indicating statistical significance. Results are given as means ± SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Food and water intake. Daily food consumption during the first 3 days averaged 30.1 ± 4.6 g (n = 9) in tilted rats and 35.3 ± 5.6 g (n = 9) in control rats. During the last 3 days of the 2-wk study, tilted rats averaged 40.6 ± 7.5 g and control rats averaged 35.0 ± 5.4 g. Daily water intake of the tilted and control rats for the same periods averaged 29.3 ± 3.2 and 43.4 ± 6.4 ml (P < 0.01) at the start of the 2-wk study and 46.1 ± 6.9 and 54.3 ± 7.1 ml, respectively, at the end of the study. Both daily food and water consumption exhibited a slight initial decline that was followed by a tendency to increase in both groups. Consequently, the average body weight was maintained relatively stable throughout the 2-wk observation period in both tilted and control groups, averaging 344.1 ± 11.7 versus 388.3 ± 18.2 g (P < 0.01) and 332.0 ± 13.3 versus 384.9 ± 20.5 g (P < 0.007), respectively. In an earlier study, daily food and water intake of free-moving control Spague-Dawley rats (n = 12) of the same body weight range (363.3 ± 2.7 g) averaged 25.8 ± 6.7 g and 45.5 ± 4.4 ml, respectively (unpublished data).
Effect of tilt on innervation density of saphenous blood vessels.
In the control untilted rats, the NTD in saphenous arteries averaged
8.20 ± 1.46 nerve terminals/100 µm2 adventitial
cross section and that of saphenous veins averaged 4.53 ± 0.61 nerve terminals/100 µm2 adventitial cross section
(P < 0.12, with Student's t-test; the difference proved to be statistically significant at level of P < 0.02). Head-up tilt position for 2 wk caused a
substantial increase in NTD of both saphenous arteries (70%;
P < 0.03) and veins (52%; P < 0.05)
(Fig. 2).
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Effect of tilt on innervation density of brachial blood vessels.
The effect of tilt on the innervation density of brachail blood vessels
is shown in Fig. 3. No significant
changes in NTD and SyVD of brachial arteries were found after chronic
tilt (3.6% relative to 4.99 ± 0.33 and 0.4% relative to
24.89 ± 4.2, respectively). Whereas the NTD of brachial veins
exhibited a tendency to increase (from 2.31 ± 0.29 to 3.73 ± 0.86 nerve terminals/100 µm2 of adventitia,
P < 0.1 with ANOVA and P < 0.05 with
Student's t-test), SyVD did not change significantly (18.96 ± 2.74 relative to 22.85 ± 3.17 synaptic vesicles/10 nerve
terminals, P < 0.51).
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Comparison of innervation densities of saphenous and brachial vessels from control animals. It is also shown by the above data that the NTD in the saphenous vein and artery of control rats was significantly larger than that of the brachial vein and artery (by 96%, P < 0.01, and 64%, P < 0.05, respectively). On the other hand, the SyVD of the brachial vein of control rats was larger than that of the saphenous vein by 71% (P < 0.007), but the SyVD did not significantly differ between control saphenous and brachial arteries (P < 0.31).
Qualitative histology.
Immunohistochemical observations revealed immunoreative staining for TH
in a large number of nerve terminals in both veins and arteries,
indicating a dominance of norepinephrine (Fig.
4). Immunoreactive staining appeared to
be more intense in saphenous vessels from tilted animals compared with
those obtained from control animals. Although VIP- and neuronal
NOS-containing nerve terminals (Fig. 5)
were detected in the arteries, most of the synaptic vesicles were small
granulated microvesicles, also suggesting the presence of
norepinephrine (6).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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The most remarkable finding of this study was that 2 wk of exposure to an experimental orthostatic body position caused a striking increase in the innervation density of the adventitia of saphenous veins and arteries. This included both the NTD and their transmitter-containing synaptic vesicles. These results are consistent with the observations of Zhang et al. (28), who studied perivascular innervation density of the hindquarter arterioles in a tail-suspension rat model of microgravity. Both noradrenergic and peptidergic (NPY and CGRP) hypoinnervation of the hindquarter muscle arterioles was observed in rats suspended head down for 4 wk. Despite the absence of quantitative data concerning the innervation density of veins in that study (28), taken together it is evident that vascular innervation demonstrates a substantial degree of plasticity in response to changes in gravitational conditions.
The increase in innervation density of hindlimb blood vessels associated with a prolonged head-up tilt position may enhance the orthostatic tolerance of the organism. The significantly higher values of control NTD found in saphenous blood vessels relative to brachial vessels suggest that the uneven distribution of basal innervation density itself plays an important role in this regard. Increased vascular innervation density would increase the neural vasoconstrictor capacity of blood vessels and potentiate the acute pressure-induced myogenic response (4). Control of veins would contribute importantly to the maintenance of normal levels of venous return and cardiac output, as emphasised by our previous studies (15, 16).
The changes of innervation density observed in blood vessels of the extremities after 2 wk of experimental orthostatic stress clearly depend on the position of the extremity relative to the level of heart. Hindlimb vessels, both veins and arteries, reacted to the head-up tilt in a similar manner, with both exhibiting increases of NTD and SyVD. In contrast, the brachial vessels of the forelimbs exhibited only minimal changes. The striking increase in the number of norepinephrine-containing nerve terminals with a highly elevated count of synaptic vesicles found in the saphenous vein is consistent with our earlier results (16). This study showed an increase in the sympathetic component of SMM potential exclusively in the saphenous vein after a head-up tilt of 2 wk. No changes in the brachial vein or artery were observed. In addition, it has also been shown that the saphenous vein reacts to a long-term orthostatic gravitational load with a significant augmentation of the acute pressure-induced myogenic response (19). This and other studies (17) provided data also demonstrating increases in diameter and wall thickness of vessels subjected to chronic orthostatic loading. We also demonstrated that noradrenergic influences can potentiate the venular myogenic response (4). Taken together, these observations provide consistent evidence that sympathetic efferents participate in both the morphological and functional remodeling that occurs in long-term vascular adaptation in response to gravitational loads. Our results also suggest that innervation remodeling is more reactive to head-up tilt in veins than in arteries of dependent extremities. Namely, in the case of forelimb vessels, only brachial vein NTD exhibited a tendency to increase (SyVD remained "silent"); in addition, the increase in SyVD of hindlimb saphenous veins was significantly more pronounced than in saphenous arteries. Taking into account the importance of veins in maintaining orthostatic tolerance, this kind of adaptive innervation redistribution seems to be physiologically purposeful.
The central neural and regional signaling pathways that control the regional specific innervation density redistribution found in this study remain to be identified. Given the data by others (7, 21, 22, 25, 27) demonstrating the existence of the vestibulosympathetic reflex in both animals and humans, the vestibular system may be importantly involved. It is possible that other receptor systems are also involved, including the baroreceptors and distributed somatic graviceptors (13).
It is unlikely that nonspecific stress-related hormones such as ACTH and corticosterone are responsible for the changes of innervation density in the tilted animal group (16). We found that plasma levels of these two "stress hormones" rise transiently above normal resting values only during the first day of tilting in normal rats studied under the same conditions. In this (16) and in the present study, the rats appeared calm and comfortable in the tube cages after a short orientation reaction observed during the first several hours of the first day only. After daily grooming "sessions," they walked spontaneously back to their individual cages from the palm of the assistant. In an other study, we demonstrated quantitatively that tilted rats maintained the same circadian locomotor rhythm as nontilted control rats with increased night activity in both groups (18). Feeding behavior and body weight exhibited characteristics similar in both tilted and nontilted control groups. The smaller average water intake of the tilted rats relative to the parallel controls during the first 3 days of the tilt period is explained in part by the difference in body weight between the two groups and perhaps by the easier accessibility of the water to control rats in the horizontal cages. Random nonspecific environmental effects on the rats were avoided by the parallel evaluation of nontilted rats to tilted rats in a neighboring tube cage.
In conclusion, this study provides evidence that chronic changes in orthostatic body position induce significant changes in sympathetic innervation density of extremity blood vessels within 2 wk. This response differs according to body region (extremity) and vessel type (artery versus vein), suggesting that its nature is adaptive. The reactions of veins seemed to be less specific in the extremity than that of the arteries.
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ACKNOWLEDGEMENTS |
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We thank Dr. György Nádasy and Sándor Sedlacsek for helpful suggestions during this study as well as Prof. Allen W. Cowley, Jr., for valuable help in editing the manuscript. We also thank Ildikó Murányi for skillful technical assistance and Katalin Juhász and Eszter Erdész for the processing of this manuscript.
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FOOTNOTES |
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This work was supported by Hungarian Grants OTKA T-30245/1999, OTKA C-194, and ETT-149/2000.
Address for reprint requests and other correspondence: E. Monos, Institute of Human Physiology and Experimental Research Dept., Faculty of Medicine, Semmelweis Univ., 1082 Üll
i üt
78/a. (1446 Budapest, POB 448), Budapest, Hungary (E-mail:
monos{at}elet2.sote.hu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 27 November 2000; accepted in final form 18 June 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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