© 1999 American Heart Association, Inc.
Original Contribution |
Expression and Distribution of the Type 1 and Type 3 Inositol 1,4,5-Trisphosphate Receptor in Developing Vascular Smooth Muscle
From the Department of Biomedical Sciences (P.N.T., G.F.N.), Institute of Medical Sciences, University of Aberdeen, Aberdeen, UK, and the School of Biochemistry (F.M.), University of Birmingham, Birmingham, UK.
Correspondence to Graeme F. Nixon, PhD, Department of Biomedical Sciences, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, UK. E-mail g.f.nixon{at}abdn.ac.uk
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Abstract |
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Abstract—The recent discoveries of inositol 1,4,5-trisphosphate (IP3) receptor subtypes with different affinities for IP3 and their potential involvement in development has important consequences for vascular smooth muscle. This study has examined the expression and distribution of the type 1 and type 3 IP3 receptor subtypes in developing rat vascular smooth muscles. Immunoblotting of portal vein and aorta from neonatal (2 to 4 days) and fully developed (6 weeks) rats revealed significantly higher levels of the type 3 IP3 receptor expression in neonatal, compared with developed, vascular smooth muscles. In contrast, expression of the type 1 IP3 receptor in neonates was lower compared with developed vascular smooth muscles. Immunolocalization of the type 3 IP3 receptors in neonatal tissues revealed that staining corresponded to the distribution of the sarcoplasmic reticulum (visualized by osmium ferricyanide staining of thin tissue sections), which suggested localization of the type 3 IP3 receptor throughout the sarcoplasmic reticulum network. We conclude that type 3 IP3 receptors are the predominant subtype in the development of vascular smooth muscle and are distributed throughout the sarcoplasmic reticulum in these cells. The switch in isoforms of the IP3 receptor during development from the type 3 with low affinity for IP3 to the higher-affinity type 1 receptor may play a role in calcium-mediated regulation of developing vascular smooth muscle.
Key Words: receptor • muscle, smooth, vascular • Ins(1,4,5)P3 • development
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Introduction |
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An important step in the vascular smooth muscle contractile process is an increase in the intracellular Ca2+ concentration.1 It is now well established that a major pathway for increasing intracellular Ca2+ in smooth muscle is the activation of phospholipase C via activation of a plasma membrane receptor, which leads to the production of inositol 1,4,5-trisphosphate (IP3).2 IP3 binds to specific IP3 receptors in the smooth muscle cell, which produces a release of Ca2+ from the intracellular stores.3 4 Several investigators have isolated full-length cDNA clones that encode at least 3 distinct IP3 receptors: type 1,5 type 2,6 and type 3.7 8 Type 1 IP3 receptor is expressed in many cell types,9 type 2 IP3 receptor is expressed in brain and heart,10 and type 3 IP3 receptor is expressed predominantly in nonneural tissues.7 Messenger RNA for type 1, 2, and 3 IP3 receptors has been detected in nonvascular smooth muscle,11 12 and in a vascular smooth muscle cell line, only mRNA for type 1 and type 3 receptors was detected.13 In smooth muscle, the type 1 IP3 receptor has been localized to the sarcoplasmic reticulum throughout the cell.14
The role of the different IP3 receptor subtypes in smooth muscle remains to be established, although distinct functions of the type 1 and type 3 IP3 receptors are suggested by their different binding affinities for IP3; type 3 receptor has a 10-fold lower affinity than type 1 receptor.12 In vascular smooth muscle cells, alterations in the IP3 receptor subtype expression and/or localization could have functional implications for Ca2+ homeostasis in blood vessels. To date, no studies have investigated the IP3 receptor subtypes expressed in vascular smooth muscle or examined possible circumstances in which these may be altered. There is evidence that the expression of IP3 receptor subtypes changes during differentiation in some cell types, which suggests a possible involvement in cell development.15 16 Developmentally associated alterations in messenger RNA levels for IP3 receptors have also been observed in the mouse cerebellum.17 These developmental changes may occur in vascular smooth muscle, which given the difference in IP3 affinities of the different subtypes,12 could potentially have functional implications for the regulation of blood vessel development.
This study examined the expression and distribution of the type 1 and type 3 IP3 receptor in vascular smooth muscle from neonatal and fully developed rats. We reveal a significant increase in the expression of type 3 IP3 receptors in neonatal vascular smooth muscle distributed throughout the sarcoplasmic reticulum.
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Materials and Methods |
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Antibody Specificity and Immunoblotting
Polyclonal anti–type 1 IP3 receptor antibody was, as described previously,18 raised in guinea pigs against the COOH-terminal 16 amino acids (residues 2733 to 2749) of the rat type 1 IP3 receptor protein. Polyclonal anti–type 3 antibody was prepared, as described by Blondel et al,7 in rabbits against the COOH-terminal 15 amino acids (residues 2656 to 2670) of the rat type 3 IP3 receptor protein. Characterization of antibody specificity for the IP3 receptor subtypes has been previously performed in other studies.7 18
Adult male Sprague-Dawley rats (6 weeks old, 300 to 350 g) were killed by cervical dislocation followed by exsanguination, neonatal male Sprague-Dawley rats (2 to 4 days old, 6 to 10 g) were killed by destruction of the brain, and the aorta and portal vein were quickly removed from all rats. Blood vessels were carefully cleaned of connective tissue with the use of a dissecting microscope, and the endothelium was removed by gentle rubbing of the lumen. In the case of portal vein, the outer layer of smooth muscle was removed. All procedures performed on animals were in accordance with institutional guidelines. Tissues were homogenized at 4°C in a Braun homogenizing vessel in buffer containing 0.25 mol/L sucrose, 10 mmol/L Tris/HCl (pH 7.4), 1 mmol/L EDTA, 0.1 mmol/L PMSF, and 50 µmol/L leupeptin. In the case of neonatal rats, tissues were pooled from 6 rats to obtain sufficient material. Whole-cell homogenates were used for immunoblotting with anti-calponin and anti–smooth muscle actin antibodies (Dako Ltd) and routinely prepared from the same pooled whole-cell homogenate. For IP3 receptor immunoblots, homogenates were centrifuged twice at 130 000g for 20 minutes and the supernatant was discarded. Forty micrograms of each sample (membrane protein or whole-cell homogenate) was loaded and electrophoresed on 6% SDS-polyacrylamide gel.19 Proteins were transferred onto activated Immobilon-P transfer membrane (Millipore). The membranes were blocked with 5% skim milk and incubated with primary antibody (either anti–type 1 or anti–type 3 IP3 receptor antibody for membrane preparations or either anti-calponin or anti-actin antibodies for whole-cell homogenates) followed by horseradish peroxidase–conjugated secondary antibody. Specific protein bands were visualized with enhanced chemiluminescence (Amersham Life Science). The relative density of protein bands was analyzed with an imaging densitometer (Biorad GS-690). Some gels were not transferred but stained with Coomassie blue to show protein loading between samples (not shown).
Sample Preparation for Confocal Laser Scanning Microscopy
Portal vein and aorta from neonatal rats (2 to 4 days old)
and 6-week-old rats were dissected and treated as previously
described.20 The muscle was fixed in freshly made 3%
paraformaldehyde in 0.1 mol/L phosphate buffer (pH
7.4), encased in 5% gelatin, and infused with sucrose in phosphate
buffer. Tissue blocks were rapidly frozen by plunging them into liquid
N2–cooled Freon-22. Cryosectioning was performed
on a Reichert-Jung cryostat E microtome at -25°C. Sections 8
µm thick were covered with 1% PBS/BSA before incubation with 5%
donkey serum. Sections were incubated with either anti–type 3
IP3 receptor antibody or anti–type 1
IP3 receptor antibody in PBS/BSA overnight at
4°C. Control sections were not exposed to primary antibody but
incubated with either PBS/BSA or nonimmune serum in PBS/BSA. Sections
were incubated with a TRITC-conjugated affinity-purified
F(ab')2 fragment species specific IgG (Jackson
ImmunoResearch Laboratories, Inc) secondary antibody at a dilution of
1:400 in PBS/BSA for 2 hours. Confocal images were obtained with a
Bio-Rad MRC-1024 laser scanning microscope equipped with a
krypton-argon laser and a x40 oil-immersion lens. The laser was fitted
with either a blue (excitation, 488 nm) or a yellow (excitation, 568
nm) filter block.
Staining of the Sarcoplasmic Reticulum for Electron
Microscopy
Portal vein and aorta from neonatal rats (2 to 4 days old) and
6-week-old rats were stained as previously described by Nixon et
al.14 Briefly, strips of smooth muscle were fixed in a 0.1
mol/L sodium cacodylate buffer solution that contained 2%
glutaraldehyde, 4.5% sucrose, and 50 mmol/L
CaCl2. The muscle strips were postfixed in 2%
OsO4 and 0.8% potassium ferricyanide for 2.5
hours at room temperature followed by a buffer wash. Samples were
incubated for 90 minutes in a saturated uranyl acetate and dehydrated
in a graded series of ethanol concentrations up to 100%. The pieces
were placed in a Spurr resin overnight, embedded in resin, and
polymerized at 70°C. Tissue blocks were sectioned on a Jung
Supercut. Sections were cut at <100-nm thickness, mounted on
200-mesh copper grids, and examined on a Jeol electron microscope at 60
keV.
All chemicals and reagents were obtained from Sigma-Aldrich Co unless otherwise stated.
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Results |
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Expression of Calponin and Smooth Muscle Actin in Developing and Fully Developed Vascular Smooth Muscle
Calponin, a marker of differentiated contractile smooth muscle, was expressed in neonatal and fully developed tissues (Figure 1A
). Immunoblotting for
calponin revealed a decreased expression in neonatal portal vein and
aorta compared with developed smooth muscles based on equal protein
loading of whole-cell homogenates. Similarly, smooth muscle
actin, which also increases in expression with postnatal development in
vascular smooth muscle, was lower in neonatal aorta and portal vein
than in fully developed tissues (Figure 1B).
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Expression of Type 1 and Type 3 IP3 Receptor in
Developing and Fully Developed Smooth Muscle
Immunoblotting with anti–type 3
IP3 receptor antibody revealed a substantially
increased expression of the type 3 IP3 receptor
in neonatal aorta compared with fully developed aorta based on equal
membrane-protein loading (Figure 2A).
Similarly, neonatal portal vein showed an increased expression of the
type 3 IP3 receptor compared with developed
portal vein preparations.
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Analysis of type 1 IP3 receptor
expression showed a decrease in the neonatal vascular smooth muscle
(both portal vein and aorta; Figure 2B
) compared with fully
developed smooth muscles which was at, or below, the limits of
detection for equal membrane-protein loading. Other bands observed with
this antibody represent breakdown products and some
nonspecific binding.18 Gels with the same pooled membrane
preparations for both type 1 and type 3 IP3
receptor immunoblotting showed similar quantifiable
changes in both subtypes, which suggested minimal cross-reactivity of
subtype-specific antibodies.
Localization of the Type 3 and Type 1 IP3 Receptor in
Neonatal and Developed Vascular Smooth Muscle
Neonatal rat aorta sections displayed a patchy, bright
staining pattern throughout the cell cytoplasm (Figure 3A). Nuclei were mostly devoid of any
signal. The staining of sections from fully developed rat aorta was
similar in distribution to neonatal aorta although different in
appearance. Fully developed rat aorta sections showed intense staining
of distinct cytoplasmic structures, which were observed throughout the
cytoplasm (Figure 3B) and extended along the axes of the
cell. These stained structures reached from adjacent to the nuclear
membrane to the plasma membrane and did not appreciably stain the
nucleus itself. Immunostaining of neonatal–portal vein
smooth muscle sections for the type 3 IP3
receptor produced a staining pattern that extended throughout the
length of the cell (Figure 4), with
higher-magnification views revealing an apparently continuous network
structure (Figure 4 inset). The fully developed portal vein
showed no staining for type 3 IP3 receptor above
background levels (not shown), which was in agreement with results from
immunoblots. The type 1 IP3 receptor
antibody showed no staining in neonatal tissues as predicted by
immunoblots. Both the fully developed aorta and portal vein
showed staining of the type 1 IP3 receptor
(Figure 5). Staining in both cell types
was observed throughout the cytoplasm. Notably, the localization for
the type 1 IP3 receptor in developed aorta is
similar in distribution but different in staining pattern than the type
3 IP3 receptor in developed aorta. Although
control sections incubated with only TRITC-conjugated secondary
antibody or with nonimmune serum and secondary antibody occasionally
showed autofluorescence of elastin, no significant labeling was
detected when imaged at pinhole and laser conditions similar to those
used in Figures 3, 4, and 5.
Immunostaining was completely blocked by the
preincubation of primary antibody with peptides that corresponded to
the amino acid sequence of the antibody.
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Distribution of [Ca2+]i Stores in
Neonatal and Developed Smooth Muscle
Electron microscopy of vascular smooth muscle treated with osmium
ferricyanide revealed a network staining throughout the cytoplasm, with
an interconnecting reticulum that is continuous with the outer nuclear
membrane in all smooth muscle tissues examined (Figure 6). In neonatal rat aorta, the reticulum
network was well developed and abundant, especially around the nucleus.
This is expected in developing smooth muscle cells in which not all of
the intracellular Ca2+ stores are sarcoplasmic
reticulum and in which there is an increased volume of the rough
endoplasmic reticulum network.21 Therefore, in this study
we have used the term "endoplasmic/sarcoplasmic reticulum" to
describe the reticulum in developing smooth muscle cells. Fully
developed rat aorta showed a sarcoplasmic reticulum distribution
proportionately more in central areas of the cytoplasm than in
areas adjacent to the plasma membrane. In neonatal portal vein,
osmium ferricyanide–stained tissue showed the endoplasmic/sarcoplasmic
reticulum network to be concentrated predominantly at the center of the
cell similar to neonatal aorta, with large regions around the nuclear
poles, and a proportionately smaller volume at the periphery of the
cell. In contrast, developed rat portal vein contained sarcoplasmic
reticulum that was located predominantly at the periphery of the cell,
in close apposition to the plasma membrane, with occasional elements in
the central cytoplasm.
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Discussion |
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Morphological studies of development have revealed that at birth, the portal vein in the rat is unusual with respect to structure because the smooth muscle cells are in an undifferentiated state.22 Two to 4 days after birth, the smooth muscle cells are myoblasts, and development is essentially complete at
28
days.22 Morphological studies of aortic
development23 have shown that at birth, the aorta is still
undergoing structural development, including hypertrophy
and hyperplasia.23 This also includes a doubling in vessel
wall thickness produced primarily by the growth of the extracellular
matrix.23 The developmental time points used in this study
were chosen on the basis of these previous studies. Confirmation of a
developing vascular smooth muscle cell phenotype in 2 to 4 day
postnatal portal vein and aorta was verified by the relative expression
of calponin, a thin filament–associated protein,24 and
smooth muscle actin. Calponin is expressed late in the development of
vascular smooth muscle cells and is indicative of a contractile
phenotype.25 In both the developing vascular
smooth muscles studied, the calponin expression was lower (3-fold)
than in the fully developed tissue, which would be expected in a
developing contractile smooth muscle cell. Previous studies have shown
that smooth muscle–specific actin increases throughout postnatal
development of vascular smooth muscle.26 The neonatal
aorta and portal vein both show decreased expression of smooth
muscle–specific actin compared with fully developed smooth muscles.
This is further evidence that the neonatal tissues used in this study
are developing vascular smooth muscles.
This study reveals that the IP3 receptor subtype
expression is altered during postnatal development of neonatal vascular
smooth muscles. The developing smooth muscle has relatively higher
expression of the type 3 IP3 receptor, with low
levels of the type 1 IP3 receptor. In contrast,
the fully developed vascular smooth muscles have low expression levels
of type 3 compared with neonates and relatively higher levels of the
type 1 IP3 receptor. The relative expression of
these proteins as measured by immunoblotting is
semiquantitative because, although the lanes were loaded with equal
membrane protein, samples were prepared at different stages of
development and are likely to have varying levels of expression of many
membrane proteins. Data could be normalizing to the expression of other
proteins, which would alter slightly the quantitative changes. For
example, normalizing to smooth muscle–actin expression (Figure 1B) would increase the quantitative difference between neonatal
and developed tissues with regard to the type 3
IP3 receptor and have no effect on the relative
expression of type 1 IP3 receptor, because the
type 1 receptor is not present in neonatal samples. We are
therefore confident that this reflects a real change in cellular
protein expression levels of IP3 receptors.
Although this study has not examined a role for the type 2
IP3 receptor, a previous study has shown that an
embryonic-aortic smooth muscle cell line contains no detectable amounts
of mRNA for the type 2 receptor.13 Therefore, in neonatal
vascular smooth muscle cells, the type 3 IP3
receptor has a predominant role in intracellular
Ca2+ release. Evidence that neonatal portal vein
has an IP3-releasable intracellular
Ca2+ store was demonstrated in a recent
study.27 The localization of the type 3
IP3 receptor in neonatal portal vein and aorta
was consistent with the distribution of the sarcoplasmic
reticulum, although immunostaining patterns were
apparently more widespread than the sarcoplasmic reticulum distribution
observed in electron micrographs. This discrepancy arises because
electron micrographs are taken from ultrathin sections (<0.1 µm
thick), whereas sections obtained for confocal microscopy are 8
µm thick. The thicker sections contain proportionately more
sarcoplasmic reticulum than the 80 times thinner sections used for
electron microscopy. This correlation is therefore a qualitative one
and not quantitative. In adult aorta, the type 3 receptor also appeared
to be localized throughout the sarcoplasmic reticulum, although the
staining was of a different appearance compared with neonatal aorta.
This difference is probably the result of a difference in distribution
of the reticulum in neonatal aorta compared with developed aorta (see
Figure 6). The type 1 IP3 receptor was
also localized throughout the sarcoplasmic reticulum in developed aorta
and portal vein, in agreement with the previous study,14
but was not detected in neonatal vascular smooth muscles. It is
noteworthy that the distribution of the type 3
IP3 receptor was not only at discrete locations
in the cell such as the extended poles of the cell or only at the
plasma membrane. This may indicate a more general role in
Ca2+ homeostasis rather than a specific function
such as localized initiation of Ca2+
waves28 or a purely Ca2+ influx
mechanism.29
The observed changes in IP3 receptor subtypes
presumably represents an important switch in expression during
the normal development of vascular smooth muscle cells; however, the
functional relevance of these findings and the role of type 3 receptor
in development is still unclear. The type 3 receptor has an 10-fold
lower affinity than the type 1 IP3
receptor.12 The increased expression of the type 3
IP3 receptor would presumably alter intracellular
Ca2+ release profiles that may regulate some
developmental processes. During development, the cells are in a
proliferative state and have important synthetic
functions,30 and the type 3 IP3
receptor may therefore play a role in proliferation or synthesis,
although this remains to be determined.
The remodeling of the intima of blood vessels that occurs with restenosis and in atherosclerotic lesions involves a change in the phenotype of the vascular smooth muscle cell.31 32 These cells undergo a phenotypic modulation from a differentiated-contractile phenotype to a synthetic phenotype. This synthetic and proliferative phenotype has many similarities, although it is not identical, to a developing vascular smooth muscle cell. Both developing cells and those that have undergone a phenotypic modulation have a decreased myofilament content and a prominent, rough endoplasmic reticulum and Golgi complex.31 33 If the type 3 IP3 receptor is involved in regulating the development of blood vessels, it seems likely that smooth muscle cells that are of a modulated synthetic phenotype will also show increased expression of the type 3 IP3 receptor. No studies to date have examined IP3 receptor subtype expression in vascular smooth muscle cells that have undergone a phenotypic modulation.
In conclusion, this study presents evidence that the predominant IP3 receptor subtype expressed in developing vascular smooth muscle is the type 3 IP3 receptor. Developed smooth muscle cells expressed proportionately more type 1 than type 3 IP3 receptor, which indicated a switch in subtype expression through development. The type 3 IP3 receptor expression in both developing and adult cells was located in areas consistent with the distribution of the endoplasmic/sarcoplasmic reticulum. The increased type 3 IP3 receptor expression and widespread subcellular distribution observed in developing cells indicates a general role in Ca2+ homeostasis during vascular smooth muscle development.
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Acknowledgments |
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This study was funded by the Wellcome Trust and the Nuffield Foundation. The authors would like to thank Dr Graeme I. Bell for the generous gift of anti–type 3 IP3 receptor antibody and peptide. The authors gratefully acknowledge A. McKinnon for technical assistance on EM studies.
Received August 7, 1998; accepted January 3, 1999.
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 F. Coussin, R. H. Scott, A. Wise, and G. F. Nixon Comparison of Sphingosine 1-Phosphate-Induced Intracellular Signaling Pathways in Vascular Smooth Muscles: Differential Role in Vasoconstriction Circ. Res., July 26, 2002; 91(2): 151 - 157. [Abstract] [Full Text] [PDF]
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S. M. Nauli, J. M. Williams, S. E. Akopov, L. Zhang, and W. J. Pearce Developmental changes in ryanodine- and IP3-sensitive Ca2+ pools in ovine basilar artery Am J Physiol Cell Physiol, December 1, 2001; 281(6): C1785 - C1796. [Abstract] [Full Text] [PDF]
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Y. Wang, J. Chen, Y. Wang, C. W. Taylor, Y. Hirata, H. Hagiwara, K. Mikoshiba, T. Toyo-oka, M. Omata, and Y. Sakaki Crucial Role of Type 1, but Not Type 3, Inositol 1,4,5-Trisphosphate (IP3) Receptors in IP3-Induced Ca2+ Release, Capacitative Ca2+ Entry, and Proliferation of A7r5 Vascular Smooth Muscle Cells Circ. Res., February 2, 2001; 88(2): 202 - 209. [Abstract] [Full Text] [PDF]
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 D. M. Angeles, J. Williams, R. E. Purdy, L. Zhang, and W. J. Pearce Effects of maturation and acute hypoxia on receptor-IP3 coupling in ovine common carotid arteries Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2001; 280(2): R410 - R417. [Abstract] [Full Text] [PDF]
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 Y. Xu, A. S. Clanachan, and B. I. Jugdutt Enhanced Expression of Angiotensin II Type 2 Receptor, Inositol 1,4,5-Trisphosphate Receptor, and Protein Kinase C{epsilon} During Cardioprotection Induced by Angiotensin II Type 2 Receptor Blockade Hypertension, October 1, 2000; 36(4): 506 - 510. [Abstract] [Full Text] [PDF]
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W. Long, L. Zhang, and L. D. Longo Cerebral artery sarcoplasmic reticulum Ca2+ stores and contractility: changes with development Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2000; 279(3): R860 - R873. [Abstract] [Full Text] [PDF]
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 Yi Xu, V. Menon, and B. I Jugdutt Cardioprotection after angiotensin II type 1 blockade involves angiotensin II type 2 receptor expression and activation of protein kinase C-{varepsilon} in acutely reperfused myocardial infarction in the dog: Effect of UP269-6 and losartan on AT1- and AT2-receptor expression and IP3 receptor and PKC{varepsilon} proteins Journal of Renin-Angiotensin-Aldosterone System, June 1, 2000; 1(2): 184 - 195. [Abstract] [PDF]
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O. Vallot, L. Combettes, P. Jourdon, J. Inamo, I. Marty, M. Claret, and A.-M. Lompre Intracellular Ca2+ Handling in Vascular Smooth Muscle Cells Is Affected by Proliferation Arterioscler Thromb Vasc Biol, May 1, 2000; 20(5): 1225 - 1235. [Abstract] [Full Text] [PDF]
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 B. I. Jugdutt, Yi Xu, M. Balghith, R. Moudgil, and V. Menon Cardioprotection Induced by AT1R Blockade After Reperfused Myocardial Infarction: Association With Regional Increase in AT2R, IP3R and PKC{varepsilon} Proteins and cGMP Journal of Cardiovascular Pharmacology and Therapeutics, January 1, 2000; 5(4): 301 - 311. [Abstract] [PDF]
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