(Hypertension. 1997;30:942-947.)
© 1997 American Heart Association, Inc.
Articles |
Impaired Nitric Oxide– and Prostaglandin-Mediated Responses to Flow in Resistance Arteries of Hypertensive Rats
From the Institut National de la Santé et de la Recherche Médicale (INSERM) U141 and U348 (J.M.), IFR Circulation Lariboisière, Université Paris VII, Paris, France.
Correspondence to D. Henrion, PhD, INSERM U141, Hôpital Lariboisière, 41 Bd de la Chapelle, 75475 Paris, Cedex 10, France. E-mail daniel.henrion{at}inserm.lrb.ap-hop-paris.fr
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Abstract |
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Abstract In human and experimental hypertension, flow (shear stress)–induced dilation in large arteries is attenuated and resistant to nitric oxide blockade. We tested the hypothesis that a defect in nitric oxide–and/or prostaglandin-dependent flow-induced dilation might occur in mesenteric resistance arteries from spontaneously hypertensive rats (SHR). We measured resistance mesenteric artery diameter in situ by intravital microscopy and simultaneously measured mesenteric arterial pressure in a collateral artery. The flow-diameter-pressure relationship was established in normotensive Wistar-Kyoto rats (WKY) and in SHR under control conditions and after endothelium removal, inhibition of nitric oxide synthesis with N
-nitro-L-arginine
methyl ester (10 µmol/L), or inhibition of
prostaglandin synthesis with indomethacin
(10 µmol/L). Production of prostaglandins
was determined in the perfusate. Endothelium
removal decreased artery diameter by 14±1.6% in WKY and 5±0.5%
(P<.01 versus WKY) in SHR at a flow rate of 400 µL/min.
In WKY, N-nitro-L-arginine methyl
ester and indomethacin decreased resistance artery
diameter by 12±3% (P<.001) and 5±2%
(P<.01), respectively, at a flow rate of 400 µL/min;
neither substance had any significant effect in SHR. In both strains,
flow induced the production of 6-keto-prostaglandin
F1
, the metabolite of prostacyclin;
prostaglandin F2; and
thromboxane B2, the stable metabolite of
thromboxane A2. Production of
6-keto-prostaglandin F1 and
prostaglandin F2 was
significantly lower in SHR than WKY, and TxB2
production was significantly higher in SHR than WKY. The
present findings suggest that in SHR mesenteric resistance
arteries, dilation in response to increases in flow was
resistant to nitric oxide and prostaglandin
synthesis blockade. A modification of the ratio of vasodilator to
vasoconstrictor prostaglandins might be at least partly
responsible for the decreased dilator response to flow in SHR.
Key Words: blood vessels • nitric oxide • rats, inbred SHR • prostaglandins
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Genetic hypertension is characterized by an increased peripheral vascular resistance, which has been proposed to be a consequence of morphological and/or functional changes within the arterial wall.1 2 Flow-induced vasodilation plays an important role in the control of blood flow.3 4 5 6 7 8 9 10 11 12 Flow (shear stress) induces the release of prostaglandins7 8 13 and NO4 9 10 11 12 by endothelial cells. In hypertension, impaired flow-induced dilation could contribute to the enhanced peripheral resistance.13 14 15 16 We have previously shown that flow-induced dilation in SHR mesenteric conductance arteries was attenuated, compared with that in normotensive WKY, and resistant to NO blockade.14 This resistance of flow-induced dilation to NO blockade in SHR has also been shown in rat gracilis muscle arterioles, in which flow-induced dilation is decreased only by PG synthesis blockade with indomethacin.13
Therefore, we conducted the present study to establish in
mesenteric resistance arteries of WKY and SHR the role of NO and PGs in
response to flow. Flow-induced dilation was measured in both strains
under control conditions and after blockade of the NO and/or PG
synthesis pathway. Furthermore, we quantified the mesenteric vascular
bed production of 6-keto-PGF1, the
stable metabolite of prostacyclin (PGI2);
PGF2; and TxB2, the stable
metabolite of thromboxane A2, in response to
flow.
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Methods |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Experimental Model
Blood pressure was measured once with the tail-cuff method before the following protocol. As rats were not trained to this measurement, pressure was overestimated, but the measurement was done only to test that the two groups had a difference in blood pressure, as usually described. Twelve-week-old WKY and age-matched SHR (Iffa-Credo) were anesthetized with sodium pentobarbital (50 mg/kg IP), and a medial laparotomy was performed. The last loop of the small intestine was exposed and placed in a container allowing the superfusion of the preparation (Fig 1
).
The preparation was irrigated with a PSS of the following composition
(mmol/L): NaCl 130, NaHCO3 14.9, KCl 3.7,
CaCl2(2H2O) 1.6, KH2PO4
1.2, MgSO4(7H2O) 1.2, glucose 11, and HEPES 5.
Albumin (4%) was added to the PSS. Temperature was 37° to
38°C, with pH 7.4. PO2 was maintained at a
value of 160 mm Hg, and PCO2, at 37
mm Hg. A 1.5-mm-long segment of a mesenteric resistance artery
(second-order) was gently dissected free of fat and connective tissues
under a binocular lens (Microcontrol). A video camera (Microcontrol)
mounted on a binocular lens allowed recording and
analysis of the images of the isolated arterial
segment. The total magnification of the optical system was x160. A
polyethylene catheter (external diameter, 0.6 mm; internal
diameter, 0.28 mm) was placed in the first-generation branch of
the mesenteric artery and connected to a syringe infusion pump (Harvard
Apparatus) driving a 10-mL syringe (Becton Dickinson). One
second-order branch was left open, and a 10-cm-long catheter, connected
to a pressure transducer and recorder (Gould P10EZ), was inserted
into an arterial branch located upstream of the observed
segment of artery for recording of mesenteric
arterial pressure. In addition, all other branches were
sutured. Step increases in flow (30 to 400 µL/min) were performed in
the observed mesenteric artery. Each flow rate was maintained for 3
minutes so steady-state arterial diameters and intraluminal
pressures could be obtained. The arterial video images and
mesenteric resistance artery pressures were recorded continuously
during the experiments. Under steady-state conditions, wall shear
stress (
, dyne/cm2) was calculated as =4 
·
Q/
· r3, where is viscosity (poise=dyne
· s · cm-2), Q is flow (mL/s), and r
is radius (cm). At 37°C, viscosity () of the 4% albumin
PSS was 0.02 poise.
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Experimental Protocol
Flow-pressure-diameter relationships were established by
imposing step increases in flow (30 to 400 µL/min) to the mesenteric
arteries. Step increases in flow and diameter measurement were
conducted under control conditions. This was then repeated after
endothelium removal or in the presence of either the NO
synthase inhibitor L-NAME (10 µmol/L) or the
cyclooxygenase inhibitor
indomethacin (10 µmol/L) in the
perfusate. Finally, step increases in flow and diameter
measurement were conducted in the presence of sodium nitroprusside
(1 mmol/L) and EGTA (2 mmol/L) and in the
absence of extracellular calcium to determine mesenteric artery passive
diameter.
Endothelium Removal
The endothelial layer was removed as previously
described.14 17 Briefly, the mesenteric network was
perfused with 1 mL carbon dioxide for 30 seconds. We verified that
topically applied acetylcholine (10 µmol/L) had no more
dilating effect after preconstriction with phenylephrine
(10 µmol/L).
Determination of 6-keto-PGF1,
PGF2 and TxB2 in
Perfusate
In a different series of experiments, the last loop of the small
intestine was exposed and placed in a container that allowed
superfusion of the tissue. The preparation was irrigated with the PSS
at 37° to 38°C. A polyethylene catheter (external diameter,
0.6 mm) was introduced and secured into the first-generation
branch of the mesenteric artery and connected to a syringe infusion
pump (Harvard Apparatus). One first-order branch of the
mesenteric arterial bed was irrigated (corresponding to Fig 1
without the ligatures). The corresponding small intestine was cut,
isolated, washed with PSS, and laid on a glass container. The
preparation was perfused at flow rates of 0.2, 2, and 4 mL/min, and the
effluent from the mesenteric network was collected and stored at
-80°C. Each flow step was maintained for 1 minute, during which the
effluent was collected. Concentrations of
PGF2;
6-keto-PGF1, the stable metabolite of
prostacyclin; and TxB2, the stable metabolite of
thromboxane A2, were determined in the
supernatants by immunoenzymatic assay with acetylcholinesterase-labeled
6-keto-PGF1,
PGF2, or TxB2 as
tracer.18 Results are expressed as picograms per
milliliter.
Drugs
L-NAME, phenylephrine, indomethacin,
sodium nitroprusside, and acetylcholine were purchased from Sigma
Chemical Co.
Statistical Analysis
Results are expressed as mean±SEM. The significance of
differences between the different groups was determined by one-factor
ANOVA. Rat strains (WKY versus SHR) or groups with or without
endothelium were compared using a two-factor ANOVA for
consecutive measurements when the flow rate was increased step by step.
Means were compared using Bonferroni's test. Value of
P<.05 were considered to be significant.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Body weight was 356±47 g (n=21) in WKY and 306±16 g (n=24) in SHR. Systolic blood pressure measured once by the tail-cuff method was 164±9 mm Hg in WKY and 220±3 mm Hg in SHR.
Flow-diameter, flow-pressure, and pressure-diameter relationships
determined in mesenteric resistance arteries under control conditions
in situ are shown in Fig 2. External
diameter (Fig 2, top) and intraluminal pressure (Fig 2, middle)
increased when flow was raised from 30 to 400 µL/min in WKY and SHR.
The pressure-diameter relationship (Fig 2, bottom) shows that in SHR
the diameter was significantly smaller than in WKY for similar
pressures. In both strains, endothelium removal induced
a significant decrease in diameter and significant increase in pressure
at the different flow rates tested. The effect of
endothelium removal was significantly less pronounced
in SHR than WKY (Fig 3).
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Changes in mesenteric resistance artery diameter were positively
correlated with wall shear stress in WKY and SHR (Fig 4). However, the increase in diameter
with increasing shear stress was significantly lower in SHR than WKY.
After endothelium removal, there was a significant
shift to the right of the shear stress–diameter relationship, which
was significantly smaller in SHR than WKY (Fig 4).
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Passive diameter measured in fully dilated vessels was significantly
smaller in SHR than WKY (Fig 5).
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In WKY, perfusion of L-NAME (10 µmol/L) or
indomethacin (10 µmol/L) induced a
significant decrease of flow-induced dilation in mesenteric resistance
arteries (Fig 6). In SHR, L-NAME (10
µmol/L) and indomethacin (10
µmol/L) induced no significant change in mesenteric artery
diameter (Fig 6).
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Phenylephrine-induced tone and acetylcholine-induced dilation were tested at the beginning of the experimental protocol. Phenylephrine (10 µmol/L) induced a significant decrease in artery diameter from 115±4.9 to 59±2.3 µm in WKY and from 88±3.2 to 46±3.4 µm in SHR. After preconstriction with phenylephrine (10 µmol/L), acetylcholine (10 µmol/L) induced a significant increase in artery diameter from 59±2.3 to 116±5.4 µm in WKY and from 46±3.4 to 69±5.9 µm in SHR. In time-control experiments, there was no significant difference in the response of the arteries to successive step increases in flow (data not shown, n=3).
Measurement of PGF1,
PGF2, and TxB2
Increasing flow rate significantly enhanced the production
of 6-keto-PGF1,
PGF2, and TxB2 in the
perfusate of mesenteric beds in both strains (Fig 7). In both strains, this
production was significantly decreased in the absence of
endothelium. The production of TxB2
was significantly higher in SHR than WKY, whereas the
production of PGF1 and
PGF2 was significantly lower in SHR than WKY
(Fig 7). In the presence of indomethacin (10
µmol/L), the production of
PGF1, PGF2, and
TxB2 was reduced to a level similar to that obtained in the
absence of endothelium (not shown).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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In the present study, we showed that flow-induced dilation in resistance mesenteric arteries from SHR was resistant to NO and PG synthesis blockade. In the perfusate of mesenteric arteries, a reversal of the ratio of vasodilator to vasoconstrictor PGs occurred in SHR.
Flow induces dilation3 4 5 6 7 8 9 10 11 12 13 and in some situations constriction.4 19 20 Increases in diameter with increasing flow rates was lower in SHR than WKY, suggesting less flow-induced dilation in SHR. This is in agreement with our previous observation in conductance mesenteric arteries.14 An attenuation of the response to flow in hypertension has been described in human large arteries15 16 and gracilis muscle arteries.13 This decrease in flow-induced dilation could participate in the increased vascular resistance observed in hypertension, together with an increased myogenic tone.21 22 In the same way, we found a smaller diameter in SHR than WKY, which is also in agreement with previous studies.2 13 21 Nevertheless, in resistance arteries, basal tone, mainly of myogenic origin,3 10 11 is much more important than in large arteries. In resistance arteries from SHR, basal tone might be higher than in WKY,22 23 and this could influence flow-induced dilation. The design of our experiments does not allow us to measure basal tone in the absence of flow. Thus, we cannot conclude that flow-induced dilation in resistance arteries from SHR was decreased. But it is clear that flow-induced dilation occurred in both strains and that it was much less sensitive to endothelium removal in SHR than WKY. Endothelium-independent responses to flow have been previously described4 12 20 and might be enhanced in arteries from SHR. But this issue remains to be investigated.
The role of NO production in the response to flow is well documented. Flow or shear stress stimulates the production of NO by the endothelial cells.4 9 10 11 12 We found a significant decrease in the flow-diameter relationship after L-NAME treatment in mesenteric resistance arteries from WKY. However, the response of the arteries to flow was not abolished, suggesting that NO is not solely responsible for flow-induced dilation in this vascular bed. This is consistent with our observation that indomethacin also attenuated the flow-diameter relationship in WKY (discussed below) and with the previous observation that this relationship is strongly attenuated by NO blockade in rat kidney24 and papillary arteries25 or only partly decreased in dog coronary26 and rat renal25 arteries. A participation of NO in flow-induced dilation has also been shown in resistance vessels such as rat renal arterioles,27 28 spinotrapezius muscle arterioles,9 gracilis muscle arteries,13 29 mesenteric arteries,30 and the gastric microcirculation31 as well as in several types of rabbit resistance vessels.4 Thus, the proportion of flow-induced dilation that depends on NO production is variable. This certainly reflects a tissue and species specificity and also some difference in experimental conditions, as previously discussed.9
An alteration of the NO pathway in hypertension has been previously described. Most studies have shown a decrease in the responses to pharmacological stimuli.13 14 15 16 32 33 In line with these studies, we found that acetylcholine-induced dilation was attenuated in mesenteric resistance arteries from SHR. Nevertheless, this point is now becoming controversial,34 and NO production might be normal or increased but less efficient in SHR.35 In response to flow, the proportion of dilation that is sensitive to NO blockade is attenuated or suppressed in hypertension.13 15 16 In the present study, flow-induced dilation was insensitive to NO synthesis blockade in SHR. This is consistent with previous studies13 15 16 and with our previous observation in rat mesenteric large arteries.14
The participation of PGs in the response to flow is also variable, depending on the tissue or species. In the present study, PG-induced dilation represented part of the response to flow in WKY. This is in agreement with results obtained in rat cremaster and gracilis muscle arterioles7 8 13 and in the gastric microcirculation.31 Another study9 has shown, in rat spinotrapezius muscle arteries, that both NO and PGs are involved in baseline vascular tone but that the dilation induced by an increased flow rate is solely dependent on NO. No role for PGs was found in flow-induced dilation in rat cerebral36 37 38 and renal25 28 arteries, in swine mesenteric arteries,30 and in human radial arteries.39
In the hypertensive rat, we found that the indomethacin-sensitive flow-induced dilation was absent. In rat gracilis muscle arterioles,6 13 hypertension is associated with the loss of NO-dependent flow-induced dilation and with an increase in indomethacin-sensitive flow-induced dilation. The difference between these previous results6 13 and our present results could reflect a difference in anatomic localization.
To gain more insight into the role of PGs in flow-induced dilation, we
measured the amounts of cyclo- oxygenase
products in the perfusate of the mesenteric bed. Change in
prostanoid production has been shown in a number of disease
states,40 and mechanical stimulation increases
cyclooxygenase activity.41 In our
study, the amounts of PGF2 and
6-keto-PGF1, reflecting the amount of
PGI2, were decreased and the amount of TxB2 was
increased in SHR. In the perfused isolated mesenteric bed, Soma et
al42 43 found a decreased production of
PGE2, 6-keto-PGF1 (or
PGI2), and TxB2, and as in our study, the ratio
of the vasorelaxant to the vasoconstrictor PGs (ratio of
PGI2 to TxB2) was decreased, reflecting
activity in the favor of the vasoconstrictor TxB2 in SHR.
This change in the balance of vasorelaxant to vasoconstrictor PGs
possibly explains the loss of effect of indomethacin in
SHR. Thus in SHR vasoconstrictor and vasorelaxant prostanoids might
cancel each other out.
In conclusion, this work suggests that in rat resistance mesenteric arteries, hypertension was associated with a loss of the NO- and PG-dependent response to flow, with a lower dependency of flow-induced dilation on the endothelium. A change in the balance of vasorelaxant to vasoconstrictor PGs could partly explain these observations.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This study was supported in part by a grant from "Fondation de France." Khalid Matrougui is a fellow of the "Recherche et Partage" Foundation, Paris, France.
Received October 15, 1996; first decision November 7, 1996; accepted March 24, 1997.
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L. Loufrani, C. Dubroca, D. You, Z. Li, B. Levy, D. Paulin, and D. Henrion Absence of Dystrophin in Mice Reduces NO-Dependent Vascular Function and Vascular Density: Total Recovery After a Treatment with the Aminoglycoside Gentamicin Arterioscler Thromb Vasc Biol, April 1, 2004; 24(4): 671 - 676. [Abstract] [Full Text] [PDF]
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S. Srivastava, R. L. Terjung, and H. T. Yang Basic fibroblast growth factor increases collateral blood flow in spontaneously hypertensive rats Am J Physiol Heart Circ Physiol, August 7, 2003; 285(3): H1190 - H1197. [Abstract] [Full Text] [PDF]
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 L. Loufrani, B. I. Levy, and D. Henrion Defect in Microvascular Adaptation to Chronic Changes in Blood Flow in Mice Lacking the Gene Encoding for Dystrophin Circ. Res., December 13, 2002; 91(12): 1183 - 1189. [Abstract] [Full Text] [PDF]
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 M. Rathaus and J. Bernheim Oxygen species in the microvascular environment: regulation of vascular tone and the development of hypertension Nephrol. Dial. Transplant., February 1, 2002; 17(2): 216 - 221. [Abstract] [Full Text] [PDF]
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D. Henrion, N. Kubis, and B. I. Levy Physiological and Pathophysiological Functions of the AT2 Subtype Receptor of Angiotensin II: From Large Arteries to the Microcirculation Hypertension, November 1, 2001; 38(5): 1150 - 1157. [Abstract] [Full Text] [PDF]
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 H. Suzuki, H. Ikezaki, D. Hong, and I. Rubinstein PGH2-TxA2-receptor blockade restores vasoreactivity in a new rodent model of genetic hypertension J Appl Physiol, June 1, 2000; 88(6): 1983 - 1988. [Abstract] [Full Text] [PDF]
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A. Huang, D. Sun, and A. Koller Shear Stress-Induced Release of Prostaglandin H2 in Arterioles of Hypertensive Rats Hypertension, April 1, 2000; 35(4): 925 - 930. [Abstract] [Full Text] [PDF]
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 L. Loufrani, D. Henrion, D. Chansel, R. Ardaillou, and B. I. Levy Functional Evidence for an Angiotensin IV Receptor in Rat Resistance Arteries J. Pharmacol. Exp. Ther., November 1, 1999; 291(2): 583 - 588. [Abstract] [Full Text]
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A. Koller and A. Huang Development of Nitric Oxide and Prostaglandin Mediation of Shear Stress-Induced Arteriolar Dilation With Aging and Hypertension Hypertension, November 1, 1999; 34(5): 1073 - 1079. [Abstract] [Full Text] [PDF]
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 D. J. Horstman, D. A. McCall, D. U. Frank, and G. F. Rich Inhaled Nitric Oxide and Nifedipine Have Similar Effects on Lung cGMP Levels in Rats Anesth. Analg., October 1, 1999; 89(4): 932 - 932. [Abstract] [Full Text] [PDF]
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K. Matrougui, L. Loufrani, C. Heymes, B. I. Levy, and D. Henrion Activation of AT2 Receptors by Endogenous Angiotensin II Is Involved in Flow-Induced Dilation in Rat Resistance Arteries Hypertension, October 1, 1999; 34(4): 659 - 665. [Abstract] [Full Text] [PDF]
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D. Henrion, M. Iglarz, and B. I. Levy Chronic Endothelin-1 Improves Nitric Oxide–Dependent Flow-Induced Dilation in Resistance Arteries From Normotensive and Hypertensive Rats Arterioscler Thromb Vasc Biol, September 1, 1999; 19(9): 2148 - 2153. [Abstract] [Full Text] [PDF]
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H. Y. Qiu, D. Henrion, J. Benessiano, C. Heymes, B. Tournier, and B. I. Levy Decreased Flow-Induced Dilation and Increased Production of cGMP in Spontaneously Hypertensive Rats Hypertension, December 1, 1998; 32(6): 1098 - 1103. [Abstract] [Full Text] [PDF]
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A. Huang, D. Sun, G. Kaley, and A. Koller Superoxide Released to High Intra-arteriolar Pressure Reduces Nitric Oxide–Mediated Shear Stress– and Agonist-Induced Dilations Circ. Res., November 2, 1998; 83(9): 960 - 965. [Abstract] [Full Text] [PDF]
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M. Iglarz, K. Matrougui, B. I. Levy, and D. Henrion Chronic blockade of endothelin ETA receptors improves flow dependent dilation in resistance arteries of hypertensive rats Cardiovasc Res, September 1, 1998; 39(3): 657 - 664. [Abstract] [Full Text] [PDF]
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K. Matrougui, P. Schiavi, D. Guez, and D. Henrion High Sodium Intake Decreases Pressure-Induced (Myogenic) Tone and Flow-Induced Dilation in Resistance Arteries From Hypertensive Rats Hypertension, July 1, 1998; 32(1): 176 - 179. [Abstract] [Full Text] [PDF]
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