(Hypertension. 2000;35:61.)
© 2000 American Heart Association, Inc.
Scientific Contributions |
Extracellular Signal-Regulated Kinase Pathway Is Involved in Basic Fibroblast Growth Factor Effect on Angiotensin II–Induced Ca2+ Transient in Vascular Smooth Muscle Cell From Wistar-Kyoto and Spontaneously Hypertensive Rats
From INSERM U337 (E.S., H.B., C.P., M.S., G.D.), Faculty Broussais-Hotel Dieu, Paris, France; INSERM U36 (S.M.), Collège de France, Paris, France; and CNRS (J.-F.R.), Marie Lannelongue Hospital, Department of Medical Research, Le Plessis Robinson, France.
Correspondence to Dr Michel Safar, Hopital Broussais, Service de Médecine Interne 1.0, 96 rue Didot, 75014 Paris, France.
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Abstract—We studied the effect of basic fibroblast growth factor (b-FGF) on different Ca2+ mechanisms elicited by angiotensin II (Ang II) in normotensive Wistar-Kyoto (WKY) rats and spontaneously hypertensive rats (SHR). Intracellular Ca2+ (Ca2+i) variations were studied in cultured vascular smooth muscle cells (VSMCs) isolated from the aorta of 5- to 6-week-old WKY rats and SHR. Ca2+i was assessed in Fura-2–loaded cells with fluorescent imaging microscopy. Ang II subtype 1 receptor activation by Ang II (1 µmol/L) induced a transient increase in Ca2+i that was partially attenuated by genistein, a tyrosine kinase inhibitor. Pretreatment of VSMCs with b-FGF for 24 hours markedly stimulated the Ang II–induced Ca2+i release from the internal stores in WKY rats, whereas it was without effect in SHR. This was not consequent to a change in the affinity of Ang II subtype 1 receptors or an increase in their density. Inhibition of mitogen-activated protein kinase with PD 98059 reduced this stimulatory effect of the cytokine in the WKY rats. On the other hand, b-FGF stimulated the Ang II–induced Ca2+ influx in both strains. Similar results were observed when Ca2+ influx was induced with thapsigargin. Genistein and PD 98059 abolished the effect of b-FGF. These results show for the first time that b-FGF regulates Ca2+ mechanisms induced by Ang II and that this regulation is different in SHR than in normotensive control animals. The extracellular signal-regulated kinase cascade is implicated in this cross-regulation with G protein–signaling pathway at 2 levels and possibly more: 1 at the tyrosine kinases and the other downstream of the extracellular signal–regulated kinase family. These results may prove useful in understanding the interaction between these 2 pathways and their implication in genetic hypertension.
Key Words: fibroblast growth factor • angiotensin II • muscle, smooth, vascular • calcium • kinase • hypertension, genetic
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Angiotensin II (Ang II) receptors belong to the superfamily of the G protein–coupled receptors, and 2 subtypes, AT1 and AT2, have been identified. In vascular smooth muscle cells (VSMCs), the binding of Ang II to AT1 receptors is known to release Ca2+i from internal stores and to increase Ca2+ influx, thus resulting in transient Ca2+i increase. Ang II has also been shown to induce hypertrophy of cultured VSMCs and to stimulate replication of VSMCs from different arterial beds.1 On the other hand, basic fibroblast growth factor (b-FGF) has been reported to play an important role in the regulation of arterial cell growth2 3 and in blood pressure homeostasis.4 b-FGF couples to receptor protein tyrosine kinase and activates mitogen-activated protein (MAP) kinases, and numerous studies have shown that this cascade is critical to the mitogenic response, to cellular differentiation, and to the induction of hypertrophy in many cell types. Recently, it has become apparent that G protein signal transduction pathways share common events with those stimulated by growth factors and cytokines. Thus, Ang II induces tyrosine phosphorylation of many proteins5 and stimulates extracellular signal-regulated kinases (ERKs).6 7 8 On the other hand, Ang II–induced inositol phosphate generation is mediated through the tyrosine kinase pathway.9 Recently, Su et al2 showed that mitogenic effect of Ang II on VSMCs after rat carotid injury was dependent on the presence of b-FGF. Calcium signaling could play an important role in this cross-regulation, because tyrosine kinase influences Ang II–induced Ca2+ transient10 and voltage-dependent11 channels in VSMCs. This led us to investigate the effect of b-FGF on Ang II–induced Ca2+i increase in aortic VSMCs. Because a dysfunction in the regulation of VSMC growth and a decrease in endothelial b-FGF content was observed in genetic hypertension,4 we wanted to address this problem in spontaneously hypertensive rats (SHR) compared with normotensive Wistar-Kyoto (WKY) rats.
This study provides novel data relating to b-FGF regulation of Ca2+i release and Ca2+ influx. b-FGF stimulates Ang II–induced Ca2+i release from internal stores in the WKY rats but not in the SHR and stimulates Ca2+ influx in both strains. This is mediated in part by tyrosine kinases and in part by ERKs. The present study provides new insights regarding cross-regulation of G protein and ERK signaling pathway that could be of importance in hypertension. Some of these results have been presented previously in abstract form.12
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Cell Isolation and Culture
Male rats of the SHR and WKY strains (5 to 6 weeks old; mean arterial pressure: SHR 136±5 mm Hg [mean±SE], n=25; WKY 98±4 mm Hg, n=20, P<0.05; weight: SHR 153±5 g, n=25; WKY 135±4 g, n=20, P<0.05) were used throughout the study. Young rats were used to avoid the effect of chronic hypertension on cell function. The investigation was conducted under guidelines established by the "Guide for the Care and Use of Laboratory Animals." VSMCs were isolated from aorta through enzymatic digestion as previously described.13 14 Isolated cells were cultured in Dulbecco’s modified Eagle’s medium (Eurobio) supplemented with 10% FCS (Eurobio), 2 mmol/L L-glutamine, 25 mmol/L HEPES, pH 7.4, 10 000 U/L penicillin, and 17 mmol/L streptomycin at 37°C and 5% CO2 in a humidified incubator. Cells at confluence between passages 3 and 9 were incubated in 0.5% FCS medium for 48 hours before experiments.
Cell Ca2+ Measurements
Ca2+i variations
were assessed at the single-cell level with the use of
fluorescence imagery as described previously.14
Cells loaded with Fura-2 (Molecular Probes) and superfused with
Na+-HEPES solution composed of (in mmol/L)
140 NaCl, 4.5 KCl, 0.8 MgCl2, 0.8
KH2PO4, 1.0
CaCl2, 5.6 glucose, and 10 HEPES, pH 7.4, at
37°C, were illuminated alternately at 350 and 380 nm, and the
intensity of emitted light at wavelength of >520 nm was measured. The
ratio of the emitted light at each of the excitation wavelength was
plotted against time for each single cell. Because calibration
procedures are prone to errors,15 no attempt was made to
assess absolute free Ca2+i
concentrations. Therefore, qualitative changes in
Ca2+i are
represented by changes in the ratio of the emitted
fluorescence at 350/380 nm.16
Receptor Binding Studies
Receptors binding assays were performed according to the method
of Conchon et al.17 Briefly, Ang II (Sigma Chemical Co)
was labeled according to the chloramine-T method, and the
monoiodinated product was purified through HPLC. Cells
were incubated for 45 minutes at 22°C with 0.5 nmol/L
125I-Ang II in the presence of increasing amounts
of nonlabeled Ang II in 50 mmol/L Tris-HCl, 6.5 mmol/L
MgCl2, 125 mmol/L NaCl, 1 mmol/L EDTA,
and 0.1% BSA (pH 7.6). Nonspecific binding was determined in the
presence of 1 µmol/L Ang II. Each experiment was carried out in
triplicate. Binding data were analyzed with a nonlinear
regression program (Excel 4.0; Microsoft Corp).
Thymidine and Proline Incorporation
For thymidine or proline incorporation, cells were pulsed with 1
and 10 mCi/L, respectively, for 20 hours. The cells were washed twice
with Dulbecco’s PBS (Eurobio) with 1 mmol/L
CaCl2 and 1 mmol/L
MgCl2, fixed with cold 10% trichloroacetic acid
for 60 minutes, and then washed twice with 10% trichloroacetic acid.
Cells were then scrapped with a rubber policeman, and the cell
suspension was pipetted in Eppendorf tubes and washed once with
distilled water. NaOH (0.5 N) was added to the cell pellet and
incubated for 10 minutes at 37°C. The incorporation of thymidine or
proline was determined through scintillation counting. Experiments were
performed in triplicate.
Determination of Cell Volume
After dissociation with trypsin (20 nmol/L), cells were counted
with the use of a hemocytometer, and their volume was assessed with an
FACS apparatus. Experiments were performed in triplicate.
When necessary, b-FGF was added to the FCS-free medium for the final 24
hours.
Statistical Analysis
The results are presented as mean±SE. The values of
parameters used to characterize the variations of cellular
Ca2+ in treated cells are expressed as percent of
values obtained in the control (ie, untreated) cells. The Student
t test for unpaired data was used to compare mean values
obtained in control (nontreated) cells with values obtained in treated
cells and to compare mean values obtained in WKY rats with values
obtained in SHR (StatView 4.5; Abacus Concepts Inc). A comparison of
values obtained in cells from passages 3 to 9 for each strain was
performed with ANOVA with multiple testing according to the Bonferroni
method (SuperAnova; Abacus Concepts Inc). P<0.05 is
considered significant.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Effect of Ang II on Cell Ca2+
The exposure of VSMCs to Ang II induced a transient increase in Ca2+i (Figure 1). The maximal response was observed in both strains for concentrations of Ang II of >0.5 µmol/L, as previously reported (Figure 2).14 18 Therefore, the effect of Ang II was assayed at 1 µmol/L throughout the study. Ca2+i transient was characterized by the amplitude and slope of Ca2+i increase (Figure 1A, a to b) and the total Ca2+i mobilized (area under transient curve; Figure 1A, a to c). The steady-state value of Ca2+i reached after the addition of Ang II was higher than that before the addition of Ang II. Ang II induced a cell receptor desensitization that lasted for up to 30 minutes and precluded the repetitive exposure of the same cells to Ang II.19 Ang II–induced Ca2+i mobilization was not significantly different in cells from the third to the ninth passage in both strains. The blockade of L-type Ca2+ channels with nifedipine (5 µmol/L; Bayer) did not significantly modify the Ang II–induced Ca2+i mobilization in both WKY rats and SHR. As previously described,20 the incubation of cells for 5 minutes with AT1 antagonists CGP-48933 (100 nmol/L; Ciba-Geigy) or CI-996 (100 nmol/L; Parke-Davis) both abolished the effect of Ang II on the Ca2+i (>95% inhibition versus control, P
0.001 for each).
|
|
). Results are expressed as mean±SD of 16 to 25
cells per concentration of Ang II. *P<0.05 SHR vs WKY
rats.Ang II–induced Ca2+i release from internal stores was assessed in Ca2+-free Na+-HEPES medium made without CaCl2 and with the addition of 1 mmol/L EGTA (Figure 1B, e to f). The Ca2+i transient peaked to lower values than that in the presence of external Ca2+.
Ang II–induced Ca2+ influx was estimated from the initial rate of Ca2+i increase on the reintroduction of external Ca2+ (Figure 1B, h to i). The blockade of L-type Ca2+ channels with nifedipine (5 µmol/L) did not significantly modify the Ca2+ influx in either strain (WKY 98±8% of control values, n=73; SHR 93±14% of control values, n=43, P=NS for each). The participation of the Na+-Ca2+ exchanger in Ang II–induced Ca2+ influx was assessed in Ca2+-free medium in the presence or in the absence of external Na+ (replaced with N-methyl-glucamine [NMG]). Ca2+ influx was not significantly different in NMG-HEPES and Na+-HEPES medium in the SHR and WKY rats (Figure 3), suggesting that the reverse mode of the Na+-Ca2+ exchanger is negligible, which is in accord with previous studies.21
|
The incubation of VSMCs for 1 hour at 37°C in the presence of 120 µmol/L genistein (Sigma), a potent inhibitor of tyrosine kinase, significantly decreased Ang II–induced Ca2+ mobilization from internal stores and Ca2+ influx in both WKY rats and SHR (Table 1).
|
Effect of b-FGF on Ang II–Induced
Ca2+i Transient
We assessed the effect of different concentrations of b-FGF
(Sigma) and different times of incubation on Ang II–induced
Ca2+i mobilization. The addition
of b-FGF at concentrations of 0.05 and 0.5 ng ·
5x104 cells-1 ·
cm-2 for either 1 minute, 1 hour, or 24 hours
did not significantly alter
Ca2+i steady state or Ang
II–induced Ca2+ transient in both WKY rats and
SHR. Similarly, no effect on the
Ca2+i steady state or on the Ang
II–induced Ca2+ release could be observed with a
b-FGF concentration of 5 ng · 5x104
cells-1 · cm-2
after 1-minute or 1-hour incubation (results not shown). In contrast,
the incubation of cells for 24 hours with b-FGF (5 ng ·
5x104 cells-1 ·
cm-2) did not modify
Ca2+i steady state (WKY 104±1%
of control values, n=196; SHR 103±1.5% of control values, n=384,
P=NS) but elicited changes in the Ang II–induced
Ca2+ transient. Therefore, this protocol was used
in subsequent experiments.
The effect of b-FGF on the Ang II–induced
Ca2+i mobilization observed in
the presence or in the nominal absence of external
Ca2+ and on Ca2+ influx is
shown in Table 2. In WKY rats, b-FGF
significantly increased the amplitude and slope of
Ca2+i transient, whereas the
total Ca2+i was not modified. In
this strain, the rate of Ca2+i
decrease after the peak of Ca2+ was reached was
increased in cells pretreated with b-FGF (128±7% of control values,
n=384, P0.0009), suggesting that
Ca2+ recovery to internal stores or extrusion to
the external medium was stimulated by b-FGF.
|
Effect of ERK Pathway Inhibitor PD 98059 on Ang
II–Induced Ca2+ Transient
We wanted to explore the implication of ERK pathway in the
modulation by b-FGF of Ang II–induced
Ca2+i mobilization. To this end,
VSMCs were incubated for 24 hours in the presence of PD 98059 (15
µmol/L; Parke-Davis) or incubated for 1 hour with PD 98059 and then
incubated for 24 hours with b-FGF in the presence of PD 98059 before
stimulation with Ang II (1 µmol/L). Preincubation of control
cells from WKY rats and SHR with PD 98059 did not modify either the Ang
II–induced Ca2+i mobilization
from internal stores or the Ca2+ influx values
(Figure 4). Conversely, PD 98059
significantly reduced the stimulation of Ca2+
release from internal stores and Ca2+ influx
elicited by Ang II observed in cells from WKY rats pretreated with
b-FGF (Figure 4). On the other hand, in the SHR, PD 98059
abolished the stimulation of Ca2+ influx observed
in the presence of b-FGF (b-FGF-pretreated cells 157±11% of control
value, n=52; b-FGF-pretreated cells in the presence of PD98059 99±5%
of control value, n=53, P<0.005).
|
, Control cells (n=117); 
,
incubation with PD 98059 for 24 hours (n=75); 
, incubation for 24
hours with b-FGF (n=73); and 
, incubation for 1 hour with PD 98059
and then incubation with b-FGF in presence of PD 98059 (n=64).
*P<0.05 vs control cells. 
P<0.05 vs
b-FGF–pretreated cells.
Effect of Thapsigargin on Cell Ca2+
The addition of thapsigargin (3 µmol/L, Sigma) in the
absence of external Ca2+ induced a transient
Ca2+i increase in cells from
both WKY rats and SHR, followed by a decrease most probably consequent
to Ca2+ extrusion from the cell (Figure 5). The reintroduction of
Ca2+ to the medium induced a
Ca2+ influx of similar magnitude to that observed
after Ang II (WKY 0.552±0.017 ratio U/min, n=58; SHR 1.002± 0.041
ratio U/min, n=62; P0.01 SHR versus WKY rats). The
incubation of VSMCs with thapsigargin during 5 minutes abolished the
response to the subsequent infusion of Ang II in both strains, as
previously reported18 (results not shown). The
addition of ionomycin did not elicit any increase in cell
Ca2+, suggesting that thapsigargin completely
emptied intracellular Ca2+ stores (results not
shown).
|
The pretreatment of VSMCs from both strains for 24 hours with b-FGF (5 ng · 5x104 cells-1 · cm-2) stimulated the thapsigargin-induced Ca2+ influx in both WKY rats (194±10% of control values, n=114, P<0.0001) and SHR (137±4%, n=52, P<0.005).
Effect of b-FGF on Cell Volume, Protein, and DNA Synthesis
Cell number, cell size, and thymidine and proline incorporation
were not significantly altered after the incubation of cells at
confluence with b-FGF for 24 hours in both strains (results not
shown).
Binding Studies
In both strains, the specific binding was saturable, and the
Scatchard plot was consistent with the presence of a single
class of binding sites. b-FGF did not significantly alter the count of
cells in each culture tray. The effects of b-FGF on
KD value and on binding site density
(calculated from binding experiments with the same compound as
radioligand and competitor) in cells from both WKY rats and
SHR are shown in Table 3.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Results from the present study demonstrate that b-FGF stimulates (1) Ang II–induced Ca2+i release from internal stores in the WKY rats but not in the SHR and (2) Ang II–induced Ca2+ influx in both strains. Furthermore, our results show for the first time that this effect is mediated by ERKs.
In VSMCs, the binding of Ang II to AT1 receptors is known to release Ca2+i from internal stores and to increase Ca2+ influx, thus resulting in transient Ca2+i increase. The signaling pathways involved in this event have been characterized and involve inositol-1,4,5-triphosphate [Ins(1,4,5)P3] for binding to its receptor on the endoplasmic reticulum. Functional studies also provide evidence of a ryanodine-sensitive Ca2+i pools and that cross-talk exists between these 2 pools.22 An increase in Ca2+ release, like that observed with b-FGF, could be consequent to either an increase in the number of AT1 receptors or a change in their affinity. However, AT1 affinity was not altered, whereas AT1 receptor density decreased with b-FGF pretreatment. This could be consequent to the internalization of AT1 receptors as suggested previously.23 Another likely explanation is an increase in the number of Ins(1,4,5)P3 or ryanodine receptors. In this respect, b-FGF was shown to increase the expression of mRNA encoding for ryanodine receptors.24 Finally, an increase in the sensitivity to Ins(1,4,5)P3 of the Ca2+ release mechanism cannot be excluded, and further studies are required to elucidate this point.
In addition to the stimulation of phospholipase C–mediated Ca2+ signaling pathway, Ang II stimulates protein phosphorylation on tyrosine residues.5 Genistein, a selective tyrosine kinase inhibitor,25 attenuated the response to Ang II, suggesting a contribution of tyrosine kinases in the regulation of Ca2+i release from internal stores, which is in accord with previous results depicting Ca2+ response to Ang II.10 This could be consequent to an inhibition of Ins(1,4,5)P3 synthesis in that tyrosine phosphorylation was shown to be implicated in Ins(1,4,5)P3 formation.9
MAP kinase/ERK kinase inhibition with PD 98059 did not modify the Ca2+i mobilized in response to Ang II stimulation in nontreated cells from both strains. This suggests that it did not interfere with the process, which begins with AT1 binding and continues through G protein coupling to the release of Ca2+ from internal pools. In a recent study, Touyz et al8 reported that PD 98059 attenuated the Ang II–induced Ca2+i response in VSMCs from human resistance arteries. The reason for such a discrepancy is unknown; it could be related to cell type or species specificity of signaling pathways.
A major observation of this study is the possible role of ERK pathway in mediation of the effect of b-FGF on Ang II–induced Ca2+i mobilization. Thus, in the WKY rats, PD 98059 blocked the stimulation by b-FGF of the Ang II–induced Ca2+i release from internal stores. Although the effect of PD 98059 on MAP kinase was not directly assessed in this study, the inhibitory effect of this agent at the concentrations used on MAP kinase activation elicited by Ang II and by various growth factors, including b-FGF, has been previously well documented.26
Findings from the present study suggest a difference between the 2 strains in the cross-regulation between the MAP kinase and the G protein pathways. Thus, in the WKY rats, upregulation of the Ang II–induced Ca2+ release by b-FGF occurs at levels downstream of the MAP kinase, whereas no such interaction could be observed in the SHR.
The possibility that an alteration in signal transduction plays an important role in the pathogenesis of hypertension has been previously suggested.27 28 29 It would be premature to establish a link between the results obtained in cultured cells and the alteration of VSMCs properties observed in hypertension. It is tempting to speculate that it could be in relation to the enhanced cell proliferation and arterial wall thickening observed in hypertension. In this regard, variations in intracellular Ca2+ play an essential role in signaling events within the cells, in particular, in cell proliferation and progression of the cells through the cell cycle.30 On the other hand, the activation of transcription factors seems to be controlled by the amplitude and duration of cell Ca2+ increase,31 as well as by nuclear or cytoplasmic Ca2+ signals.32 These observations suggest that downstream effectors can decode information contained in the amplitude, duration, and localization of Ca2+ signals, which could intervene in the regulation of gene expression. In this respect, this model may prove useful in understanding the interactions between ERK pathway and the G protein–signaling pathway and their specificity in genetic hypertension.
Effect of b-FGF on Ca2+ Influx
Agonist-stimulated release of
Ca2+i from the intracellular
stores is accompanied by repletion of the store by
Ca2+ influx from the extracellular
space.33 It is now admitted that the action of Ang II in
VSMCs involves both voltage-operating channels and voltage-independent
channels.34 35 The relative contribution of these 2
pathways to either muscle contraction or Ca2+
influx depends on the smooth muscle type and the experimental
conditions.33 36 37 The lack of effect of
nifedipine in this study suggests that
Ca2+ influx is mediated by voltage-independent
channels. This is further supported by our observation that
agonist-independent depletion of intracellular
Ca2+ stores with thapsigargin activated a
Ca2+ entry pathway. This pathway, termed
capacitative Ca2+ entry, was reported in
different cell types (see Parekh and Penner38 for a
review), including VSMCs39 40 41 ; is insensitive to
nifedipine41 ; and contributes to smooth muscle
contraction (see Gibson et al35 for a review). On the
other hand, the role of the
Na+-Ca2+ exchanger in
Ca2+ influx, although well documented in several
cell preparations, remains a subject of controversy in
VSMCs.42 In this study, the participation of this
exchanger in Ang II–induced Ca2+ influx is
negligible. Alternately, Na+ loading may not be
sufficient to elicit a significant influx via the exchanger or
Ca2+ influx may be too small to be detected with
Fura-2.21 42
The inhibition of tyrosine kinase with genistein reduced the Ang II–induced Ca2+ influx in both WKY rats and SHR, which is in accord with previous studies in normotensive rats.10 11
Another major observation of this study was that in both SHR and WKY rats, b-FGF increased a voltage-independent Ca2+ influx elicited by Ang II. Similarly, the release and entry of Ca2+ in response to Ca2+ pool depletion induced by thapsigargin were significantly increased in both strains after treatment with b-FGF. Furthermore, PD 98059 inhibited the stimulatory effect of b-FGF in both strains, suggesting that it is at levels downstream of the MAP kinases. The nature of the signal linking pool depletion to opening of the capacitative Ca2+ influx remains to be determined.
In conclusion, these results show that b-FGF regulates Ca2+ mechanisms elicited with Ang II. This response is mediated in part by tyrosine kinases and in part by elements downstream of the ERK family. This latter interplay seems to be particular to genetic hypertension.
|
Acknowledgments |
|---|
We wish to thank Dr Eric Clauser for support and for stimulating discussion and Dr Pascal Ferré for reading the manuscript.
Received June 1, 1999; first decision June 23, 1999; accepted September 7, 1999.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Geisterfer AA, Peach MJ, Owens GK. Angiotensin II induces hypertrophy, not hyperplasia, of cultured aortic smooth muscle cells. Circ Res. 1988;62:749–756.
2.
Su EJ, Lombardi DM, Wiener J, Daemen MJ, Reidy MA,
Schwartz SM. Mitogenic effects of angiotensin
II on rat carotid arteries and type II or III mesenteric microvessels
but not type I microvessels is mediated by endogenous basic
fibroblast growth factor. Circ Res. 1998;82:321–327.
3. Itoh H, Mukoyama M, Pratt RE, Gibbons GH, Dzau VJ. Multiple autocrine growth factors modulate vascular smooth muscle cell growth response to angiotensin II. J Clin Invest. 1993;91:2268–2274.
4.
Cuevas P, Garcia-Calvo M, Carceller F, Reimers D, Zazo
M, Cuevas B, Munoz-Willery I, Martinez-Coso V, Lamas S, Gimenez-Gallego
G. Correction of hypertension by normalization of
endothelial levels of fibroblast growth factor and
nitric oxide synthase in spontaneously hypertensive rats. Proc
Natl Acad Sci U S A. 1996;93:11996–12001.
5.
Molloy CJ, Taylor DS, Weber H. Angiotensin
II stimulation of rapid protein tyrosine
phosphorylation and protein kinase activation in rat
aortic smooth muscle cells. J Biol Chem. 1993;268:7338–7345.
6. Butcher RD, Schollmann C, Marme D. Angiotensin II mediates intracellular signalling in vascular smooth muscle cells by activation of tyrosine-specific protein kinases and c-raf-1. Biochem Biophys Res Commun. 1993;196:1280–1287.[Medline] [Order article via Infotrieve]
7. Duff JL, Marrero MB, Paxton WG, Schieffer B, Bernstein KE, Berk BC. Angiotensin II signal transduction and the mitogen-activated protein kinase pathway. Cardiovasc Res. 1995;30:511–517.[Medline] [Order article via Infotrieve]
8.
Touyz RM, He G, Deng L-Y, Schiffrin EL. Role of
extracellular signal-regulated kinases in angiotensin
II-stimulated contraction of smooth muscle cells from human resistance
arteries. Circulation. 1999;99:392–399.
9.
Marrero MB, Paxton WG, Duff JL, Berk BC, Bernstein KE.
Angiotensin II stimulates tyrosine
phosphorylation of phospholipase C-gamma1 in vascular
smooth muscle cells. J Biol Chem. 1994;269:10935–10939.
10.
Touyz RM, Schiffrin EL. Tyrosine kinase signaling
pathways modulate angiotensin II–induced calcium
([Ca2+]i) transients in vascular smooth muscle
cells. Hypertension. 1996;27:1097–1103.
11. Suzuki A, Shinoda J, Oiso Y, Kozawa O. Tyrosine kinase is involved in angiotensin II–stimulated phospholipase D activation in aortic smooth muscle cells: function of Ca2+ influx. Atherosclerosis. 1996;121:119–127.[Medline] [Order article via Infotrieve]
12. Bouillier H, Samain E, Perret C, Safar M, Dagher G. The effect of b-FGF on the angiotensin II-induced Ca++ mobilization is mediated by the MAP kinase pathway. J Physiol (Lond). 1998;511P:168. Abstract.
13. Pacaud P, Malam-Souley R, Loirand G, Desgranges C. ATP raises [Ca2+]i via different P2-receptor subtypes in freshly isolated and cultured aortic myocytes. Am J Physiol. 1995;269(1 pt 2):H30–H36.
14. Samain E, Bouillier H, Perret C, Safar M, Dagher G. Angiotensin II–induced calcium increase in smooth muscle cells from spontaneous hypertensive rat is regulated by actin and microtubule networks. Am J Physiol. 1999;277:H834–H841.
15. Williams DA, Fay FS. Intracellular calibration of the fluorescent calcium indicator Fura-2. Cell Calcium. 1990;11:75–83.[Medline] [Order article via Infotrieve]
16. Chambers P, Neal DE, Gillespie JI. Ca++ signaling in cultured smooth muscle cells from human bladder. Exp Physiol. 1996;81:553–564.[Abstract]
17. Conchon S, Peltier N, Corvol P, Clauser E. A noninternalized nondesensitized truncated AT1A receptor transduces an amplified ANG II signal. Am J Physiol. 1998;274:E336–E345.
18.
Côrtes SF, Lemos VS, Stoclet JC. Alterations in
calcium stores in aortic myocytes from spontaneously hypertensive rats.
Hypertension. 1997;29:1322–1328.
19. Aboulafia J, Oshiro MEM, Feres T, Shimuta SI, Paiva ACM. Angiotensin II desensitization and Ca++ and Na+ fluxes in vascular smooth muscle cells. Pflügers Arch. 1989;415:230–234.
20. Touyz RM, Tolloczko B, Schiffrin EL. Mesenteric vascular smooth muscle cells from spontaneously hypertensive rats display increased calcium responses to angiotensin II but not to endothelin-1. J Hypertens. 1994;12:663–673.[Medline] [Order article via Infotrieve]
21. Smith JB, Zheng T, Smith L. Relationship between cytosolic free Ca2+ and Na+-Ca2+ exchange in aortic muscle cells. Am J Physiol. 1989;256(1 pt 1):C147–C154.
22. Kraus-Friedmann N. Signal transduction and calcium: a suggested role for the cytoskeleton in inositol 1,4,5-triphosphate action. Cell Motil Cytoskel. 1994;28:279–284.[Medline] [Order article via Infotrieve]
23. Ullian ME, Raymond JR, Willingham MC, Paul RV. Regulation of vascular angiotensin II receptors by EGF. Am J Physiol. 1997;273(4 pt 1):C1241–C1249.
24.
Marks AR, Taubman MB, Saito A, Dai Y, Fleischer S. The
ryanodine receptor/junctional channel complex is regulated by growth
factors in a myogenic cell line. J Cell Biol. 1991;114:303–312.
25.
Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S,
Itoh N, Shibuya M, Fukami Y. Genistein, a specific
inhibitor of tyrosine-specific protein kinases.
J Biol Chem. 1987;262:5592–5595.
26.
Servant MJ, Giasson E, Meloche S. Inhibition of growth
factor-induced protein synthesis by a selective MEK
inhibitor in aortic smooth muscle cells. J Biol
Chem. 1996;271:16047–16052.
27.
Rosskopf D, Düsing R, Siffert W. Membrane
sodium-proton exchange and primary hypertension.
Hypertension. 1993;21:607–617.
28.
Berk BC, Corson MA. Angiotensin II signal
transduction in vascular smooth muscle. Circ Res. 1997;80:607–616.
29. Bendhack LM, Sharma RV, Bhalla RC. Altered signal transduction in vascular smooth muscle cells from spontaneously hypertensive rats. Hypertension. 1992;19(suppl II):II-142–II-148.
30.
Waldron RT, Short AD, Meadows JJ, Gosh TK, Gill DL.
Endoplasmic reticulum calcium pump expression and control of cell
growth. J Biol Chem. 1994;269:11927–11933.
31. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature. 1997;386:855–858.[Medline] [Order article via Infotrieve]
32. Hardingham GE, Chawla S, Johnson CM, Bading H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature. 1997;385:260–265.[Medline] [Order article via Infotrieve]
33. van Breemen C, Saida K. Cellular mechanisms regulating [Ca2+]i smooth muscle. Annu Rev Physiol. 1989;51:315–329.[Medline] [Order article via Infotrieve]
34. Somlyo AP, Somlyo AV. Signal transduction and regulation in smooth muscle. Nature. 1994;372:231–236.[Medline] [Order article via Infotrieve]
35. Gibson A, McFadzean I, Wallace P, Wayman CP. Capacitative Ca2+ entry and the regulation of smooth muscle tone. Trends Pharmacol Sci. 1998;19:266–269.[Medline] [Order article via Infotrieve]
36. Kuriyama H, Kitamura K, Nabata H. Pharmacological and physiological significance of ion channels and factors that modulate them in vascular tissues. Pharmacol Rev. 1995;47:387–573.[Medline] [Order article via Infotrieve]
37. Hughes AD. Calcium channels in vascular smooth muscle cells. J Vasc Res. 1995;32:353–370.[Medline] [Order article via Infotrieve]
38.
Parekh AB, Penner R. Store depletion and calcium
influx. Physiol Rev. 1997;77:901–930.
39.
Pacaud P, Loirand G, Gregoire G, Mironneau C, Mironneau
J. Noradrenaline-activated heparin-sensitive
Ca2+ entry after depletion of intracellular
Ca2+ store in portal vein smooth muscle cells.
J Biol Chem. 1993;268:3866–3872.
40.
Xuan YT, Wang OL, Whorton AR. Thapsigargin stimulates
Ca2+ entry in vascular smooth muscle cells:
nicardipine-sensitive and -insensitive pathways.
Am J Physiol. 1992;262:C1258–C1265.
41.
Yoshimura M, Oshima T, Matsuura H, Ishida T, Kambe M,
Kajiyama G. Extracellular Mg2+ inhibits
capacitative Ca2+ entry in vascular smooth muscle
cells. Circulation. 1997;95:2567–2572.
42.
Nabel EG, Berk BC, Brock TA, Smith TW.
Na+-Ca2+ exchange in
cultured vascular smooth muscle cells. Circ Res. 1988;62:486–493.
This article has been cited by other articles:
 |
|
 |
|
  D. Liu, D. Yang, H. He, X. Chen, T. Cao, X. Feng, L. Ma, Z. Luo, L. Wang, Z. Yan, et al. Increased Transient Receptor Potential Canonical Type 3 Channels in Vasculature From Hypertensive Rats Hypertension, January 1, 2009; 53(1): 70 - 76. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||