| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Institute of Pathophysiology, Semmelweis University of Medicine, Budapest 1445, Hungary; and Department of Physiology, New York Medical College, Valhalla, New York 10595
 |
ABSTRACT |
|---|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
Skeletal muscle
arterioles dilate in response to increases in flow velocity/wall shear
stress (WSS). The effect of flow/WSS on the diameter of skeletal muscle
venules and the possible endothelial mediation of the response,
however, have not yet been characterized. Thus changes in diameter of
pressurized (10 mmHg) and norepinephrine-preconstricted venules
(179 ± 8 µm in diameter) to increases in perfusate flow before and after endothelium removal or application of inhibitors of NO
and prostaglandin (PG) synthesis,
N
-nitro-L-arginine
(L-NNA,
104 M) and indomethacin (Indo, 2.8 × 105 M), respectively, were
measured. Increases in perfusate flow [elicited by increases in
the pressure difference (Pdiff)
between proximal and distal cannulas] evoked with a delay of 17 ± 2 s dilations, up to 36 ± 9 µm at the highest flow, a
response that was completely eliminated by removal/disruption of the
venular endothelium. Calculation of WSS indicated that in
endothelium-intact venules, the midpoint of the shear stress-diameter
curve was at ~8 dyn/cm2, whereas
in endothelium-denuded vessels, shear stress increased in a linear
fashion with increases in flow, up to 40 dyn/cm2.
L-NNA significantly reduced
flow-induced dilations (from 38 ± 11 to 17 ± 9 µm at 14 mmHg
Pdiff), whereas in the
additional presence of Indo, flow elicited constriction of venules
decreasing basal diameter (by 21 ± 8 µm at
Pdiff 12 mmHg). Thus in skeletal muscle venules an increase in shear stress due to increases in perfusate flow stimulates the release of endothelium-derived NO and PGs
eliciting dilation, which in turn, regulates WSS, albeit at a lower
value than what is observed in arterioles. In the absence of NO and
PGs, flow-induced constriction is revealed, the cause of which remains
obscure. From these data, we propose that shear stress-related
responses of venules are involved in the regulation of venular
resistance, especially during high flow conditions, such as reactive
and exercise hyperemia.
rat gracilis muscle; venular resistance; endothelium-derived constrictor factors; power dissipation
| |
INTRODUCTION |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
IN ADDITION to the well-described capacitance function of veins (1, 30) recent investigations paid considerable attention to the regulation of venular resistance (1, 3, 5, 6, 8, 9, 13, 19, 25, 33). An increasing amount of evidence supports the view that changes in local hemodynamic forces, by affecting the function of endothelium and/or smooth muscle (5, 8, 9, 12, 19, 27, 28), modulate the diameter of venules. Previous in vitro studies (19) demonstrated that alterations in luminal pressure elicit increases in tone of porcine coronary venules, a response that is weaker than what was found in arterioles of similar size. In bat wing venules, which exhibit spontaneous vasomotion, elevating pressure elicited an increase in contraction frequency and a decrease in contraction amplitude (6). A myogenic response to increases in intraluminal pressure was also demonstrated in rat skeletal muscle venules and was shown to be enhanced by the presence of norepinephrine (NE) (9). Taken together, these studies established that a myogenic mechanism intrinsic to smooth muscle, independent of but modulated by factors released from the endothelium, operates in venules.
In vivo, during changes in blood pressure, blood flow velocity and wall shear stress (WSS) may also change. It was shown that arteriolar endothelium is sensitive to changes in WSS (15-18, 20, 29, 34) and has, in turn, an important role in the regulation of WSS, thereby contributing to optimal power dissipation in the arterial system (16, 18). Changes in the rheological attributes of blood have been recognized as an important modulator of venular resistance (13, 23). Yet, there are only a few studies that made an attempt to assess the effect of flow-shear stress on venular diameter. Falcone and Bohlen (10) showed that endothelium-derived relaxing factor from intestinal venules elicits dilation of adjacent arterioles. Similarly, Boegehold (4), Saito et al. (31), and McKay et al. (26) showed that increases in venular blood flow elicit the release of endothelial factors that affect arteriolar but not venular diameter. In addition, an earlier study showed that the smooth muscle of portal-mesenteric veins is not affected by endothelium-derived relaxing factor(s) (11).
These results leave in doubt the concept that changes in blood flow serve as stimuli for the release of factors from the venular endothelium to affect venular diameter itself. Yet, in vitro studies showed that isolated porcine coronary and bat wing venules exhibit flow-dependent dilation (5, 19). Whereas, in vitro, large conduit veins increase their tone to increases in flow (4), canine femoral veins (27) and venous endothelial cells in a bioassay system (12) respond to increases in flow by the release of nitric oxide, known to dilate veins (14) and venules (8, 19). Interestingly, in the bat wing, venular dilation to flow is mediated by an unknown factor, the nature of which is different from the presently known endothelial mediators (5). The possible role of flow-shear stress-induced responses of venules of skeletal muscle, the nature of factors produced by venular endothelium, and the magnitude of responses, all of which may be quite different from those found in arterioles (8, 11), have not yet been studied. It would be important to clarify these issues in order to better understand the coordination of pre- and postcapillary resistances during various flow conditions.
On the basis of the aforementioned results, we hypothesized that venules of skeletal muscle are sensitive to increases in flow-shear stress but that the characteristics and mediation of flow-induced responses may not be the same as those found in arterioles. Thus we investigated the effects of increases in perfusate flow-shear stress on the diameter of isolated venules of gracilis muscle of rats and aimed to elucidate the nature of the factors responsible for the mediation of responses.
| |
METHODS |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
Eleven-week-old male Wistar rats were anesthetized with pentobarbital sodium (50 mg/kg). The skeletal muscle, gracilis anticus, was exposed by an incision of the skin, isolated from surrounding tissues, and removed and pinned to the Silastic bottom of a petri dish containing cold (0-4°C) physiological salt (PS1) solution (pH 7.4). The PS1 solution contained (in mM) 145 NaCl, 5.0 KCl, 2.0 CaCl2, 1.0 MgSO4, 1.0 NaH2PO4, 5.0 dextrose, 2.0 pyruvate, 0.02 EDTA, and 3.0 3-(N-morpholino)propanesulfonic acid. Then the muscle was allowed to equilibrate for 15 min. With the use of an operating microscope, a 1.5-2 mm long segment of a venule running intramuscularly was isolated and placed into an organ chamber containing two glass micropipettes, and cannulated. The chamber solution (PS2) contained (in mM) 110 NaCl, 5.0 KCl, 2.5 CaCl2, 1.0 MgSO4, 1.0 KH2PO4, 10.0 dextrose, and 24.0 NaHCO3 and was bubbled with 10% O2-5% CO2-balance N2. The micropipettes were filled with PS2 solution and connected with silicone tubing to a pressure-servo control system (Living System Instrumentation, Burlington, VT), which contains two pressure transducers, each connected to a pressure-servo syringe (9, 18).
Experimental protocols. In each series of experiments, before the start of the protocols, venules were equilibrated at 10 mmHg perfusion pressure, at 37°C in order to achieve a steady-state diameter, whereupon the various experimental protocols were performed. In all experiments, responses of venules were obtained in the presence of NE (106 M) in the chamber solution. This concentration of NE was selected because in previous experiments it elicited half-maximal constriction of venules (9). As previously described (18, 20), increases in perfusate flow were established by equal increases in proximal and decreases in distal perfusion pressure from 0 to 14 mmHg pressure difference (Pdiff). Between 0-4 and 4-14 mmHg Pdiff, 1- and 2-mmHg step changes, respectively, were used. The relationship between Pdiff and flow is depicted in Fig. 1.
|
Responses to increases in perfusate flow were obtained after removal of the endothelium. As described previously (8, 9), perfusion of venules with air results in the complete removal of the endothelial cell layer. The vessel was untied from the primary pipette, and the endothelium was removed carefully by injecting 0.3 ml of air into the lumen. It took ~1 min for the bubble to travel through the lumen. Then the endothelium of the venule was flushed out of the lumen with 0.5 ml of PS2, and the free end of the venule was reconnected to the primary pipette.
To characterize the factors involved in the mediation of flow-induced
responses, N-nitro-L-arginine
(L-NNA,
10
4 M) and indomethacin
(2.8 × 105 M) were
utilized (8). The efficacy and selectivity of inhibitors were tested by
responses to acetylcholine (ACh,
106 M), sodium
nitroprusside (SNP, 106 M),
and arachidonic acid (108
M). Arachidonic acid was first dissolved in ethanol and then further
diluted with PS2 solution. All other drugs were dissolved in PS2
solution. Agonists were added to the vessel chamber, and final
concentrations are reported. The vehicle solution for the various drugs
did not affect the diameter of veins. After responses to an agonist
subsided, the system was flushed with PS2. To obtain the passive
diameter, at the conclusion of each experiment the suffusion solution
was changed to a Ca2+-free
physiological salt solution, which contained SNP
(104 M) and EGTA (1.0 mM).
The vessel was incubated for 20 min, and the passive diameter at 10 mmHg of pressure was obtained. The perfusate flow was measured by a
ball flowmeter (Omega) in the range of 0-0.5 ml/min and calibrated
by a Harvard perfusion pump. From the diameter and flow (Q) data WSS
was calculated according the formula: WSS = 4
Q/
r3,
where is viscosity (0.7 centipoise at 37°C), Q is perfusate flow, and r is the radius (18).
All salts and chemicals were obtained from Sigma or Aldrich Chemical and were prepared on the day of the experiment. In the various protocols, 6-15 venules (only one vessel from each rat) were investigated. The data are presented as means ± SE. GB-Stats statistical program was used to analyze the data. Statistical significance was calculated by analysis of variance, followed by a multiple comparison test (Tukey post hoc test) and paired Student's t-test, as appropriate. Differences were considered significant at P < 0.05.
| |
RESULTS |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
In all experiments 106 M NE
was administered into the bath solution, and the perfusion pressure was
maintained constant at 10 mmHg. In these conditions the basal diameter
of venules (n = 21) was 195 ± 13 µm, which is 47% of passive diameter (412 ± 15 µm) obtained in
Ca2+-free solution. Responses of
venules to agonists in the presence of various inhibitors are
summarized in Table 1.
|
An original record (Fig. 2) demonstrates
that step increases in perfusate flow, elicited by increases in the
difference between inflow and outflow pressures, resulted in
significant increases in venular diameter, from 170 to 220 µm. First
flow increased, and then it was followed by an increase in diameter. On
average, the delay between the increase in flow and the onset of
dilation was 17 ± 2 s (n = 20).
The data obtained in control conditions are summarized in Fig.
3, which shows that in response to
increases in flow, the diameter of venules increased substantially.
This increase was 36 ± 9 µm at
Pdiff 14 mmHg (from 165 ± 12 to 201 ± 16 µm), which corresponds to a 22% increase in basal
diameter. Removal of the endothelium completely eliminated venular
dilations to ACh (106 M),
but SNP (106 M) still
elicited dilation (Table 1). Also, the vessels lacking endothelial
cells did not respond to increases in flow (Fig. 3).
|
|
With the use of diameter and flow data, WSS was calculated and plotted against changes in diameter of venules. The relationship between calculated WSS and diameter indicates that in endothelium-intact venules, the midpoint of the WSS-diameter curve is ~8 dyn/cm2 (Fig. 4).
|
Inhibition of nitric oxide synthesis by L-NNA significantly reduced the response to ACh and inhibited the flow-induced increase in venular diameter (Table 1 and Fig. 5), indicating that nitric oxide participates in the mediation of the response. After the additional administration of indomethacin, an inhibitor of cyclooxygenase, increases in flow not only eliminated flow-dependent dilations but elicited significant constriction of venules, up to 21 ± 8 µm at a Pdiff of 12 mmHg (Fig. 5), corresponding to an ~13% decrease in diameter. Indomethacin also abolished responses to arachidonic acid, the precursor of prostaglandin synthesis (Table 1).
|
To exclude the changes in venular diameter due to the possible miniscule changes in intraluminal pressure during increases in the pressure difference, vessels were also studied in Ca2+-free bath solution. Figure 6 indicates that there were no changes in venular diameter during increases in the pressure difference in passive conditions whether data were obtained in the absence of the endothelium or in the presence of L-NNA or L-NNA plus indomethacin, indicating that dilations and constrictions to flow in the presence of Ca2+ were due to active responses of venules.
|
| |
DISCUSSION |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
The salient finding of the present study is that increases in WSS due to increases in perfusate flow elicit dilations of isolated skeletal muscle venules, thereby regulating venular WSS. An increase in shear stress is coupled with the release of endothelium-derived nitric oxide and prostaglandins, whereas in the absence of these dilator factors, the release of an endothelium-derived constrictor factor in response to increased perfusate flow is also uncovered.
Flow-dependent responses of veins and venules. Previous in vivo and in vitro studies established that skeletal muscle arterioles are sensitive to increases in luminal flow. Increases in flow velocity or viscosity elicit an increase in WSS resulting in arteriolar dilation (15-18), which in turn reduces WSS. In contrast, in vivo studies of venules in skeletal muscle (4, 10, 26, 31) did not provide evidence that increases in blood flow elicit changes in venular diameter, but they showed that under these conditions endothelial factors are released from venules affecting arteriolar tone. Also, changes in blood viscosity which should elicit changes in shear stress did not affect the diameter of venules in cat sartorius muscle (13).
The only evidence heretofore for the existence of a flow-sensitive mechanism in venules was provided by studies of Kuo et al. (19), who showed that increases in perfusate flow due to increases in pressure drop across the isolated porcine coronary venules resulted in dilation, and those of Davis (5), who demonstrated that spontaneous contractions of bat wing venules are inhibited by increases in luminal flow. There are no data extant regarding the effects of intraluminal flow-shear stress on the regulation of diameter of skeletal muscle venules. The present study was conducted in isolated pressurized venules, a condition in which the confounding effect of neural, humoral, and metabolic factors is negligible. We found a substantial (~22%) dilation in response to increased perfusate flow in venules (Fig. 3). Our findings also indicate that the range of WSS in isolated venules that causes changes in diameter is between 0 and 20 dyn/cm2 (Fig. 4), with the midpoint of the diameter-WSS curve at 8 dyn/cm2. In this context, Davis (5) found that in bat wing venules, ~120 µm in diameter, maximum WSS was 2.8 dyn/cm2. Collectively, these studies suggest that perhaps all types of blood vessels are sensitive to forces associated with increases in blood flow. The reason for the findings that in vivo, venular diameter did not change in response to increases in wall shear stress is not clear. We suspect that the experimental conditions, including anesthesia, may have reduced the tone of skeletal muscle venules and therefore increases in flow/shear stress could not further affect their diameter. It is also possible that in conjunction with changes in red blood cell velocity, changes in apparent viscosity offset the changes in wall shear rate resulting in no change in WSS (13, 23).
Release of venular endothelial factors to flow. The present studies indicate that increases in WSS elicit the release of several factors from the endothelium increasing the venular diameter which, in turn regulates WSS. In isolated porcine coronary venules, increases in perfusate flow induced dilations, a response that is endothelium dependent and mediated primarily by the release of a nitrovasodilator (19). Because in this study administration of indomethacin elicited great constriction of porcine venules, the possible role of prostaglandins was not further studied. Interestingly, the authors also observed flow-induced venular constrictions but only after the removal of endothelium. These findings demonstrate that the sensitivity of venules to increases in flow is different from that of arterioles, a finding to which as yet no physiological role has been assigned. Davis et al. (5) also showed that increases in luminal flow can modulate the contractile function of bat wing venules via the release of a transferable substance from the endothelium, which does not appear to be nitric oxide, a prostaglandin, or oxygen radical species, further emphasizing the differences between venules and arterioles.
To characterize the endothelial factors that mediate flow-induced responses in skeletal muscle venules, we have utilized inhibitors interfering with L-arginine and arachidonic acid metabolism. Previously we have found that in arterioles of gracilis muscle L-NNA and indomethacin eliminated dilation to increases in flow/WSS, suggesting that both nitric oxide and prostaglandins are responsible for shear stress-induced responses (17). In the present studies, combined inhibition of nitric oxide and prostaglandin synthesis not only eliminated flow-induced dilations but resulted in constrictions to increases in flow (Fig. 5). We interpret these findings to mean that in addition to nitric oxide, dilator prostaglandins, PGI2 and/or PGE2, are also released in response to increases in WSS. Previous studies suggested that nitric oxide and/or prostaglandins released from venular endothelium only affect the diameter of paired arteriolar segments in skeletal muscle (4, 10, 26, 31); the present study, however, shows that these factors can also affect the diameter of venules.
The present results uncovered constrictions to flow after inhibition of synthesis of nitric oxide and prostaglandins, suggesting the corelease of constrictor and dilator factors from the endothelium in response to increases in flow/shear stress. In the absence of the endothelium, flow induced neither constriction nor dilation. It is unlikely that the constrictor factor is PGH2/thromboxane (TX) A2, shown previously to be released by venules in response to ACh (8), because indomethacin did not block the constrictor response. Also, administration of SQ-29548, a selective PGH2/TXA2 receptor blocker, did not affect the constrictor response to flow (unpublished observation). To identify the nature of this factor(s) is a subject for future studies. Several putative factors, however, including 20-15-hydroxyeicosatetraenoic acid, a p450 metabolite (2), endothelin (28), or reactive oxygen metabolites, (22), shown to be associated with changes in flow in previous studies, could be hypothesized to be responsible for the response. In theory it is also possible that flow elicits the washout of dilator factors from the venular endothelium, a possibility that has been suggested previously (19, 28).
Circulatory role of venular control of WSS. Several important physiological roles can be envisioned for the shear stress mechanism in skeletal muscle venules. It is likely that blood flow velocity increases in venules at the time when flow is high in arterioles; for example, during exercise hyperemia. It seems logical that great increases in blood flow in the arteriolar network of skeletal muscle can only occur if similar increases in venular blood flow due to increased conductance of the venular network take place concurrently. During isotonic exercise, due to the increase in arterial pressure and the presence of an effective muscle pump (32, 35), one can assume that blood flow velocity suddenly increases in venules when skeletal muscle relaxes. This then could increase WSS, resulting in dilation of venules providing for a greater arteriovenous pressure drop, which can further amplify the increase in blood flow on the arteriolar side. At the same time capillary hydrostatic pressure will be reduced, thereby mitigating fluid loss to assist in circulatory adjustments to exercise. Indeed, direct observation of venules during electrical stimulation of skeletal muscle revealed increases in their diameter (25).
It is well known that rheological resistance (i.e., viscosity of the blood, hematocrit, number of white blood cell, etc.) contributes significantly to vascular resistance to flow, which is especially important in venules (13, 23). Thus changes in shear stress, via release of nitric oxide, prostaglandins, and perhaps other factors, affect not only diameter but also aggregation of platelets and other formed elements of the blood (13, 23), as well as adhesion processes (21), thereby also reducing the rheological resistance to flow in venules. Moreover, changes in WSS were shown to have an impact on thrombosis and hemostasis (24), which is especially relevant in venules, indicating the complexity of various venular regulatory mechanisms in circulatory homeostasis.
In summary, our results demonstrate that increases in perfusate flow-shear stress elicit dilation of isolated skeletal muscle venules, providing for regulation of WSS. The response is mediated by endothelium-derived nitric oxide and prostaglandins, but in their absence constrictor factor(s) may become dominant. These findings suggest that the endothelium of venules can be actively involved in the regulation of venular resistance and blood flow, which should be considered when results of studies of skeletal muscle blood flow, during exercise or other conditions leading to hyperemia, are interpreted. Furthermore, these findings suggest that in addition to the arteriolar system (16, 18), regulation of power dissipation could be important in the low-pressure segment of the circulation as well.
| |
ACKNOWLEDGEMENTS |
|---|
We thank Miriam Nunez for excellent secretarial assistance.
| |
FOOTNOTES |
|---|
This work was supported by National Heart, Lung, and Blood Institute Grants P01 HL-43023 and HL-46813; by Hungarian National Scientific Research Grant OTKA T-023863; and by Ministry of Welfare Grant ETT-524.
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. §1734 solely to indicate this fact.
Address for reprint requests: A. Koller, Dept. of Physiology, New York Medical College, Valhalla, NY 10595.
Received 9 February 1998; accepted in final form 21 May 1998.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Methods
Results
Discussion
References
|
|---|
1.
Abdel-Sayed, W. A.,
F. M. Abboud,
and
D. R. Ballard.
Contribution of venous resistance to total vascular resistance in skeletal muscle.
Am. J. Physiol.
218:
1291-1295,
1970.
2.
Alonso-Galicia, M.,
H. A. Drummond,
K. K. Reddy,
J. R. Falck,
and
R. J. Roman.
Inhibition of 20-HETE production contributes to the vascular responses to nitric oxide.
Hypertension
29:
320-325,
1997
3.
Bevan, J. A.,
and
E. H. Joyce.
Saline infusion into lumen of resistance artery and small vein causes contraction.
Am. J. Physiol.
259 (Heart Circ. Physiol. 28):
H23-H28,
1990
4.
Boegehold, M. A.
Shear-dependent release of venular nitric oxide: effect on arteriolar tone in rat striated muscle.
Am. J. Physiol.
271 (Heart Circ. Physiol. 40):
H387-H395,
1996
5.
Davis, M. J.
Spontaneous contractions of isolated bat wing venules are inhibited by luminal flow.
Am. J. Physiol.
264 (Heart Circ. Physiol. 33):
H1174-H1186,
1993
6.
Davis, M. J.,
X. Shi,
and
P. J. Sikes.
Modulation of bat wing venule contraction by transmural pressure changes.
Am. J. Physiol.
262 (Heart Circ. Physiol. 31):
H625-H634,
1992
7.
De Mey, F. G.,
and
P. M. Vanhoutte.
Heterogeneous behavior of the canine arterial and venous wall: importance of the endothelium.
Circ. Res.
51:
439-447,
1982
8.
Dörnyei, G.,
G. Kaley,
and
A. Koller.
Release of nitric oxide and prostaglandin H2 to acetylcholine in skeletal muscle venules.
Am. J. Physiol.
272 (Heart Circ. Physiol. 41):
H2541-H2546,
1997
9.
Dörnyei, G.,
E. Monos,
G. Kaley,
and
A. Koller.
Myogenic responses of isolated rat skeletal muscle venules: modulation by norepinephrine and endothelium.
Am. J. Physiol.
271 (Heart Circ. Physiol. 40):
H267-H272,
1996
10.
Falcone, J. C.,
and
H. G. Bohlen.
EDRF from rat intestine and skeletal muscle venules causes dilation of arterioles.
Am. J. Physiol.
258 (Heart Circ. Physiol. 27):
H1515-H1523,
1990
11.
Feletou, M.,
U. Hoeffner,
and
P. M. Vanhoutte.
Endothelium-dependent relaxing factors do not affect the smooth muscle of portal-mesenteric veins.
Blood Vessels
26:
21-32,
1989[Medline].
12.
Fukaya, Y.,
and
T. Ohhashi.
Acetylcholine-and flow-induced production and release of nitric oxide in arterial and venous endothelial cells.
Am. J. Physiol.
270 (Heart Circ. Physiol. 39):
H99-H106,
1996
13.
House, S. D.,
and
P. C. Johnson.
Diameter and blood flow of skeletal muscle venules during local flow regulation.
Am. J. Physiol.
250 (Heart Circ. Physiol. 19):
H828-H837,
1986.
14.
Ignarro, L. J.
Biological actions and properties of endothelium derived nitric oxide formed and released from artery and vein.
Circ. Res.
65:
1-21,
1989
15.
Koller, A.,
and
G. Kaley.
Flow velocity dependent regulation of microvascular resistance in in vivo.
Microcirc. Endothelium Lymphatics
5:
519-530,
1989[Medline].
16.
Koller, A.,
and
G. Kaley.
Endothelial regulation of wall sheart stress and flow in skeletal muscle microcirculation.
Am. J. Physiol.
260 (Heart Circ. Physiol. 29):
H862-H868,
1991
17.
Koller, A.,
D. Sun,
A. Huang,
and
G. Kaley.
Corelease of nitric oxide and prostaglandins mediates flow-dependent dilation flow of rat gracilis muscle arterioles.
Am. J. Physiol.
266 (Heart Circ. Physiol. 35):
H326-H332,
1994.
18.
Koller, A.,
D. Sun,
and
G. Kaley.
Role of sheart stress and endothelial prostaglandins in flow and viscosity-induced dilation of arterioles in vitro.
Circ. Res.
72:
1276-1284,
1993
19.
Kuo, L.,
F. Arko,
W. M. Chilian,
and
M. J. Davis.
Coronary venular responses to flow and pressure.
Circ. Res.
72:
607-615,
1993
20.
Kuo, L.,
M. J. Davis,
and
W. M. Chilian.
Endothelium-dependent, flow-induced dilation of isolated coronary arterioles.
Am. J. Physiol.
259 (Heart Circ. Physiol. 28):
H1063-H1070,
1990
21.
Kurose, I.,
R. Wolf,
M. B. Grisham,
and
D. N. Granger.
Effects of an endogenous inhibitor of nitric oxide synthesis on postcapillary venules.
Am. J. Physiol.
268 (Heart Circ. Physiol. 37):
H2224-H2231,
1995
22.
Laurindo, F. R. M.,
M. de A Pedro,
H. V. Barbeiro,
F. Pileggi,
M. H. C. Carvalho,
O. Augusto,
and
P. L. da Luz.
Vascular free radical release. Ex vivo and in vivo evidence for a flow-dependent endothelial mechanism.
Circ. Res.
74:
700-709,
1994
23.
Lipowsky, H. H.,
S. Usami,
and
S. Chien.
In vivo measurements of "apparent viscosity" and microvessel hematocrit in the mesentery of the cat.
Microvasc. Res.
19:
297-319,
1980[Medline].
24.
Malek, A. M.,
R. Jackman,
R. D. Rosenberg,
and
S. Izumo.
Endothelial expression of thrombomodulin is reversibly regulated by fluid shear stress.
Circ. Res.
74:
852-860,
1994
25.
Marshall, J. M.,
and
H. C. Tandon.
Direct observations of muscle arterioles and venules following contraction of skeletal muscle fibers in the rat.
J. Physiol. (Lond.)
350:
447-459,
1984
26.
McKay, M. K.,
A. L. Gardner,
D. Boyd,
and
R. L. Hester.
Influence of venular prostaglandin release on arteriolar diameter during functional hyperemia.
Hypertension
31:
213-217,
1998
27.
Miller, V. M.,
and
D. A. Barber.
Modulation of endothelium-derived nitric oxide in canine femoral veins.
Am. J. Physiol.
271 (Heart Circ. Physiol. 40):
H668-H673,
1996
28.
Milner, P.,
P. Bodin,
A. Loesch,
and
G. Burnstock.
Rapid release of endothelin and ATP from isolated aortic endothelial cells exposed to increased flow.
Biochem. Biophys. Res. Commun.
170:
649-656,
1990[Medline].
29.
Pohl, U.,
J. Holtz,
R. Busse,
and
E. Bassenge.
Crucial role of endothelium in the vasodilator response to increases in flow in vivo.
Hypertension
7:
37-44,
1986.
30.
Rothe, C. F.
The venous system. The physiology of the capacitance vessels.
In: Handbook of Physiology. The Cardiovascular System. Peripheral Circulation and Organ Blood Flow. Bethesda, MD: Am. Physiol. Soc., 1983, sect. 2, vol. 3, chapt. 13, p. 397-452.
31.
Saito, Y.,
A. Eraslan,
V. Lockard,
and
R. L. Hester.
Role of venular endothelium in control of arteriolar diameter during functional hyperemia.
Am. J. Physiol.
267 (Heart Circ. Physiol. 36):
H1227-H1231,
1994
32.
Sheriff, Don, D.,
L. B. Rowell,
and
A. M. Scher.
Is rapid rise in vascular conductance at onset of dynamic exercise due to muscle pump.
Am. J. Physiol.
265 (Heart Circ. Physiol. 34):
H1227-H1234,
1993
33.
Shoukas, A. A.,
and
G. Bohlen.
Rat venular pressure-diameter relationships are regulated by sympathetic activity.
Am. J. Physiol.
259 (Heart Circ. Physiol. 28):
H674-H680,
1990
34.
Smiesko, V.,
D. J. Lang,
and
P. C. Johnson.
Dilator response of rat mesenteric arcading arterioles to increased blood flow velocity.
Am. J. Physiol.
256 (Heart Circ. Physiol. 25):
H1958-H1965,
1989.
35.
Leeuwen, B. E.,
G. J. Barendsen,
J. Lubbers,
and
L. De Pater.
Calf blood flow and posture: Doppler ultrasound measurements during and after exercise.
J. Appl. Physiol.
72:
1675-1680,
1992
This article has been cited by other articles:
|
|
 |
|
  B. E. Carlson, J. C. Arciero, and T. W. Secomb Theoretical model of blood flow autoregulation: roles of myogenic, shear-dependent, and metabolic responses Am J Physiol Heart Circ Physiol, October 1, 2008; 295(4): H1572 - H1579. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. M. Lockwood, M. P. Pricher, B. W. Wilkins, L. A. Holowatz, and J. R. Halliwill Postexercise hypotension is not explained by a prostaglandin-dependent peripheral vasodilation J Appl Physiol, February 1, 2005; 98(2): 447 - 453. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Nithipatikom, B. B. Holmes, M. J. McCoy, C. J. Hillard, and W. B. Campbell Chronic administration of nitric oxide reduces angiotensin II receptor type 1 expression and aldosterone synthesis in zona glomerulosa cells Am J Physiol Endocrinol Metab, November 1, 2004; 287(5): E820 - E827. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Cicha, Y. Suzuki, N. Tateishi, and N. Maeda Changes of RBC aggregation in oxygenation-deoxygenation: pH dependency and cell morphology Am J Physiol Heart Circ Physiol, June 1, 2003; 284(6): H2335 - H2342. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. E. Tschakovsky and R. L. Hughson Rapid blunting of sympathetic vasoconstriction in the human forearm at the onset of exercise J Appl Physiol, May 1, 2003; 94(5): 1785 - 1792. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. A. Kingwell, M. Formosa, M. Muhlmann, S. J. Bradley, and G. K. McConell Type 2 Diabetic Individuals Have Impaired Leg Blood Flow Responses to Exercise: Role of endothelium-dependent vasodilation Diabetes Care, March 1, 2003; 26(3): 899 - 904. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. N. Dzeka and J. M. O. Arnold Prostaglandin modulation of venoconstriction to physiological stress in normals and heart failure patients Am J Physiol Heart Circ Physiol, March 1, 2003; 284(3): H790 - H797. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. L. Hester and L. W. Hammer Venular-arteriolar communication in the regulation of blood flow Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2002; 282(5): R1280 - R1285. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. G. Schrage, C. R. Woodman, and M. H. Laughlin Mechanisms of flow and ACh-induced dilation in rat soleus arterioles are altered by hindlimb unweighting J Appl Physiol, March 1, 2002; 92(3): 901 - 911. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. W. Hammer, A. L. Ligon, and R. L. Hester ATP-mediated release of arachidonic acid metabolites from venular endothelium causes arteriolar dilation Am J Physiol Heart Circ Physiol, June 1, 2001; 280(6): H2616 - H2622. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Jagger, R. M. Bateman, M. L. Ellsworth, and C. G. Ellis Role of erythrocyte in regulating local O2 delivery mediated by hemoglobin oxygenation Am J Physiol Heart Circ Physiol, June 1, 2001; 280(6): H2833 - H2839. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. A. W. Broeders, G.-J. Tangelder, D. W. Slaaf, R. S. Reneman, and M. G. A. o. Egbrink Endogenous Nitric Oxide and Prostaglandins Synergistically Counteract Thromboembolism in Arterioles but Not in Venules Arterioscler. Thromb. Vasc. Biol., January 1, 2001; 21(1): 163 - 169. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. J. Bishop, P. R. Nance, A. S. Popel, M. Intaglietta, and P. C. Johnson Diameter changes in skeletal muscle venules during arterial pressure reduction Am J Physiol Heart Circ Physiol, July 1, 2000; 279(1): H47 - H57. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. N. Mbaku, L. Zhang, S. P. Duckles, and J. Buchholz Nitric-Oxide Synthase-Containing Nerves Facilitate Adrenergic Transmitter Release in Sheep Middle Cerebral Arteries J. Pharmacol. Exp. Ther., May 1, 2000; 293(2): 397 - 402. [Abstract] [Full Text]
|
|
|
|
|
|
L. Loufrani, S. Lehoux, A. Tedgui, B. I. Levy, and D. Henrion Stretch Induces Mitogen-Activated Protein Kinase Activation and Myogenic Tone Through 2 Distinct Pathways Arterioscler. Thromb. Vasc. Biol., December 1, 1999; 19(12): 2878 - 2883. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Koller, R. Mizuno, and G. Kaley Flow reduces the amplitude and increases the frequency of lymphatic vasomotion: role of endothelial prostanoids Am J Physiol Regulatory Integrative Comp Physiol, December 1, 1999; 277(6): R1683 - R1689. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
) removal
of endothelium. * Significant differences from E+
(n = 6).
