© 2000 American Heart Association, Inc.
Cellular Biology |
ADP-Ribosyl Cyclase in Rat Vascular Smooth Muscle Cells
Properties and Regulation
From the Department of Physiology and Biophysics, Division of Nephrology and Internal Medicine (F.G.S.d.T., J.C., M.L., T.P.D.), and Departments of Anesthesiology and Department of Medicine (E.N.C.), Mayo Clinic and Foundation, Mayo Medical School, Rochester, Minn.
Correspondence to Eduardo N. Chini, MD, PhD, Mayo Clinic, 200 First St, SW, Guggenheim 9, Rochester, MN 55905. E-mail chini.eduardo{at}mayo.edu
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Abstract |
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Abstract—We investigated whether ADP-ribosyl cyclase (ADPR-cyclase) in rat vascular smooth muscle cells (VSMCs) has enzymatic properties that differ from the well-characterized CD38-antigen ADPR-cyclase, expressed in HL-60 cells. ADPR-cyclase from VSMCs, but not CD38 ADPR-cyclase from HL-60 cells, was inhibited by gangliosides (10 µmol/L) GT1B, GD1, and GM3. Preincubation of membranes from CD38 HL-60 cells, but not from VSMCs, with anti-CD38 antibodies increased ADPR-cyclase activity; CD38 antigen was detected both in VSMCs and in HL-60 cells. ADPR-cyclase in VSMC membranes was more sensitive than CD38 HL-60 ADPR-cyclase to inactivation by N-endoglycosidase F and to thermal inactivation at 45°C. The specific activity of ADPR-cyclase in membranes from VSMCs was >20-fold higher than in membranes from CD38 HL-60 cells. Most importantly, VSMC ADPR-cyclase was inhibited by Zn2+ and Cu2+ ions; the inhibition by Zn2+ was dose dependent, noncompetitive, and reversible by EDTA. In contrast, Zn2+ stimulated the activity of CD38 HL-60 ADPR-cyclase and other known types of ADPR-cyclases. Retinoids act either via the nuclear receptor retinoic acid receptor or retinoid X receptor, including all-trans retinoic acid (atRA), and panagonist 9-cis-retinoic acid–upregulated VSMC ADPR-cyclase; the stimulatory effect of atRA was blocked by actinomycin D and cycloheximide. 1,25(OH)2–Vitamin D3 (calciferol) stimulated VSMC ADPR-cyclase dose dependently at subnanomolar concentrations (ED50
56 pmol/L).
Oral administration of atRA to rats resulted in an increase of
ADPR-cyclase activity in aorta (+60%) and, to a lesser degree, in
myocardium of left ventricle (+18%), but atRA had no
effect on ADPR-cyclases in lungs, spleen, intestinal smooth muscle,
skeletal muscle, liver, or testis. Administration of
3,5,3'-triiodothyronine (T3) to rats resulted in an
increase of ADPR-cyclase activity in aorta (+89%), but not in liver
or brain. We conclude the following: (1) ADPR-cyclase in VSMCs has
enzymatic properties distinct from "classic" CD38 ADPR-cyclase,
especially sensitivity to inhibition by Zn2+ and
Cu2+; (2) ADPR-cyclase in VSMCs is upregulated by various
retinoids, calcitriol, and T3 in vitro; and (3)
administration of atRA and T3 increases ADPR-cyclase in
aorta in vivo. We suggest that the cADPR signaling system plays an
important role in the regulation of VSMC functions in response to
steroid superfamily hormones.
Key Words: vascular smooth muscle cells • calciferols • antibodies • ADP-ribose • retinoids
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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It is well established that inositol 1',4',5'-triphosphate (IP3) triggers Ca2+ release, via IP3 receptor/channel, from endocellular stores to cytoplasm.1 Recently,2 3 the nucleotide cyclic ADP-ribose (cADPR) was found to stimulate Ca2+ release from intracellular stores via ryanodine receptor/channel.1 2 3 Enzymatic synthesis and hydrolysis of cADPR are catalyzed by ADP-ribosyl cyclase (ADPR-cyclase) and cADPR-hydrolase, respectively.2 3 4 ADPR-cyclase is regulated by hormones in vitro4 5 6 and in vivo.7 cADP-ribose modulates Ca2+ fluxes in several types of contractile cells,8 9 10 including vascular smooth muscle cells (VSMCs).9 11 12 13 Furthermore, cADPR, alone and/or via interaction within the IP3 signaling system,11 regulates contractility8 10 and possibly other cellular functions.13 We recently observed that ADPR-cyclase present in rat VSMCs14 is upregulated by all-trans retinoic acid (atRA) and by 3,5,3'-triiodothyronine (T3).15 Our observations, and reports on regulatory action of cADPR in muscle cells,8 9 10 11 12 13 prompted us to investigate properties and regulatory responses of ADPR-cyclase of VSMCs to hormones.
To date, most information is available about ADPR-cyclase that is identical with lymphocytic CD38 antigen, a molecule that has not only ADPR-cyclase but also cADPR-hydrolase and NADase activities.2 3 16 17 This ADPR-cyclase (referred to hereafter as CD38 ADPR-cyclase) was found initially in hematopoietic cells,2 3 but was later also detected in several cell types and tissues.16 17 18 However, CD38 was not detected in vessels or in intestinal smooth muscle,18 suggesting that ADPR-cyclase in VSMCs may have properties different from CD38 ADPR-cyclase.3 16 17 Another well-described vertebrate ADPR-cyclase is the CD157 (BST-1/PB-3) antigen.4 17 19
According to a recent report, knockout mice that lack CD3820 are capable of living at least 8 months without abnormalities and suffer only nonlethal impairment of the immune system.20 Similarly, knockout mice that are deficient in BST-1 (CD157) antigen display only limited immune deficiency.21 From these observations, it can be inferred that, besides CD38 ADPR-cyclase and BST-1 ADPR-cyclase, other isozymes (or isoforms) of ADPR-cyclase must exist to sustain cADPR signaling system in diverse cell types, including VSMCs. These considerations prompted us to investigate some fundamental properties and regulation of ADPR-cyclase in rat VSMCs.
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Materials and Methods |
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Cell Culture
VSMCs were isolated from rat abdominal aorta explant outgrowths, as previously described.14 22 Skin fibroblasts were obtained from dermis of rat abdominal skin as described previously.23 Mesangial cells were isolated from rat glomeruli and grown in primary culture as described previously.14 23 24 HL-60 cells (purchased from American Type Culture Collection) were cultured in RPMI 1640 with 20% bovine FCS, 100 U/L penicillin, 100 µg/L streptomycin, and 0.25 µg/L amphotericin B.
Preparation of Subcellular Fractions
The total membrane fraction for each type of cultured cell was
prepared similarly as previously described for VSMCs.15
Cells were rinsed 3 times with ice-cold PBS and scraped into ice-cold
homogenizing buffer containing 40 mmol/L Tris-HCl
(pH 7.2) and 0.25 mol/L sucrose (TSB). Cells were disrupted by and then
centrifuged at 2000g for 10 minutes. The resulting
supernatant was centrifuged at 40 000g for 30
minutes. The pellet, resuspended in TSB, is referred to hereafter as
the membrane fraction. Protein content in the homogenate
was measured by the method of Lowry et al.25 Membrane
fractions from rat tissues were prepared using a procedure similar to
that used for cultured cells. Animal use in the present study was
approved by the Mayo Clinic and Foundation Animal Care Committee.
In Vivo Studies
Studies in vivo were conducted on male Sprague-Dawley rats (200
to 250 g body weight). The rats were treated with atRA 3 mg
(SC)/kg body weight per day for 3 days, and controls received vehicle
(DMSO). Experiments examining the effects of T3
were done on surgically thyroparathyrectomized (TPTX) rats. Rats were
treated with 2 mg (IP) T3/kg body weight per day
for 10 days before euthanization.26 Tissues were
homogenized, and then membrane fraction was prepared as
above.
ADPR-Cyclase Activity
Activity was measured using nicotinamide guanine
dinucleotide (NGD) or nicotinamide hypoxanthine
dinucleotide (NHD).6 27 28
Fluorescence was monitored with a 300-nm excitation wavelength
and 410-nm emission wavelength using a Hitachi F-2000
spectrofluorimeter. The 
change in fluorescence was
calibrated from standard curves generated from known concentrations of
cGDPR or cIDPR.7 15 Use of NGD or NHD is explicitly
specified in the Results.
Enzymatic Deglycosylation
Suspended membranes from VSMCs or HL-60 cells (1 to 2 mg/tube)
were incubated without (controls) or with recombinant
N-endoglycosidase F (16 U/mL) in a buffer containing
final concentrations as follows: in mmol/L, EDTA 5, PMSF 0.1, and
Tris-HCl (ph 7.4) 40; 0.5% Triton X-100; 5 µg/mL leupeptin; and 3
µg/mL pepstatin.
The effect of anti-CD38 antibodies (Abs) on ADPR-cyclase in membranes from VSMCs and HL-60 cells was determined with either goat anti-mouse CD38 Abs or goat anti-human CD38 Abs (Santa Cruz Biotechnology), diluted 1:1.
Western Blots for CD38
The cells were homogenized in 20 mmol/L
Tris-HEPES buffer, pH 7.4, containing 1% Triton X-100. The sample of
membranes (30 µg protein per lane) was subjected to 10% SDS-PAGE,
and proteins were transferred onto nitrocellulose membrane and Western
blot analysis using a standard technique. To determine thermal
stability of ADPR-cyclase, membrane preparations were incubated at
either 37°C or 45°C for various time periods indicated in the
Results, and the ADPR-cyclase activity was measured in aliquots.
All values are expressed as mean±SEM. When appropriate, the results were statistically evaluated using the Student t test for paired or group comparisons. The values were considered statistically significant at P<0.05.
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Results |
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The specific activity of ADPR-cyclase activity in membranes of VSMCs was >20-fold higher than the activity of CD38 ADPR-cyclase in membranes from HL-60 cells. Addition of Zn2+ ions significantly increased CD38 ADPR-cyclase activity (Table 1
). In contrast,
Zn2+ inhibited the VSMC ADPR-cyclase >20-fold,
using either NGD or NHD as substrate (Table 1). The inhibition
of VSMC ADPR-cyclase by Zn2+ was dose dependent,
which was similar to that with use of NHD or NGD substrate. Both the
inhibition of VSMC ADPR-cyclase by Zn2+ and
stimulation of CD38 HL-60 ADPR-cyclase by Zn2+
were dose dependent (Figure 1A), and both
effects were reversed by addition of EDTA (Figure 1D). The
inhibition of VSMC ADPR-cyclase by Zn2+ was of a
noncompetitive type (Figure 1B). In contrast to VSMCs (Figure 1A), Zn2+ increased ADPR-cyclase activity
also in homogenates of sea urchin eggs and in Aplysia
californica ovotestis (Table 1).
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=37±4 µmol/L) or with (•)
(Km=39±12 µmol/L) 1 mmol/L
ZnCl2. Vmax with 1 mmol/L
Zn2+ was
Copper ions (Cu2+) had basically a similar effect
as Zn2+. Addition of Cu2+
inhibited the ADPR-cyclase activity in VSMCs and enhanced CD38
ADPR-cyclase activity in membranes from HL-60 cells. Addition of
Mn2+ or Mg2+ had no effect
on ADPR-cyclase activity in membranes from either VSMCs or HL-60 cells
(Figure 1C
).
According to a recent report, some gangliosides inhibit or stimulate
CD38 ADPR-cyclase from different species.29 At
concentrations >10 µmol/L gangliosides,
GT1B, GM3, and
GD1a inhibited ADPR-cyclase in membranes from
VSMCs, but not in HL-60 cells (Figure 2A). The most potent ganglioside
GT1b at concentrations >10 µmol/L
inhibited also CD38 HL-60 ADPR-cyclase, but to a much lesser degree
than the VSMC ADPR-cyclase (Figure 2B). On the other hand,
nicotinamide, a known general inhibitor of
ADPR-cyclase,2 3 4 inhibited to the same degree
ADPR-cyclase activity in VSMC membranes
(IC50=3.1±0.5 mmol/L; n=3) and in membranes
from CD38 HL-60 cells (IC502.1±0.4
mmol/L; n=3).
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) or HL-60 cell membranes (
Inhibition significantly less (P<0.05,
t test) than with GT1B. B, Dose-dependent
inhibition by trisialoganglioside GT1b of VSMC ADPR-cyclase
(
) (IC50=9.8±0.6 µmol/L; n=3), (maximum
inhibition=94%), and of CD38 HL-60 ADPR-cyclase (•)
(IC50=33±3 µmol/L; n=3, maximum inhibition=-54%).
*Values significantly (P<0.05, t test)
different, VSMCs (
The catalytic site of CD38 ADPR-cyclase is situated close to the C
terminus.17 30 Therefore, we tested whether
protein-protein interaction with anti-CD38 Abs, directed against the
C-terminal 20 amino acids of CD38,17 may influence
ADPR-cyclase activity.30 In membranes from VSMCs
preincubated with murine anti-CD38 Abs, the Abs had no effect on
ADPR-cyclase activity (Figure 2C). However, incubation of
membranes from CD38 HL-60 cells with the same Abs significantly
increased the ADPR-cyclase activity (Figure 2C). Incubation of
CD38 HL-60 membranes with human anti-CD38 Abs (C-19) had a similar
effect (data not shown). Western blot analysis shows that rat
anti-CD38 Abs react well with VSMC membranes (45-kDa band), but only
slightly with a 45-kDa band in HL-60 membranes (Figure 2E).
Conversely, human anti-CD38 Abs reacted strongly with membranes from
the HL-60 cell and, to a lesser degree, with VSMC membranes (Figure 2E).
Incubation with N-glycosidase F caused a minor reduction of
ADPR-cyclase activity in membranes from CD38 HL-60 cells, but markedly
diminished ADPR-cyclase in membranes from VSMCs (Figure D).
Furthermore, ADPR-cyclase from VSMCs was more sensitive than the HL-60
cell enzyme to thermal inactivation. When incubated at 45°C, the rate
of inactivation of ADPR-cyclase in VSMCs
(t1/2=26±3 minutes, n=2) was 
5-fold
faster than the decline of CD38 HL-60 ADPR-cyclase activity
(t1/2=125±25 minutes, n=2).
With respect to some VSMC-related cell types and tissues, we examined
the effect of Zn2+ on ADPR-cyclase in rat
fibroblasts and mesangial cells grown in cell culture
(Table 1). ADPR-cyclase activities from rat
mesangial cells and rat skin fibroblasts were inhibited by
Zn2+ in a way similar to that in VSMCs (Table 1).
Effect of Hormones
In accordance with our previous study, incubation of VSMCs with
atRA and T3 enhanced ADPR-cyclase,15
and the upregulatory effect of atRA was blocked by actinomycin D and
cycloheximide (Figure 3). We examined
whether such an upregulating effect is also shared with retinoids that
have a similar mechanism of action.31 The retinoid
panagonist 9-cis–retinoic acid stimulated the activity on
ADPR-cyclase (Table 2). A survey of the
action of several retinoids that act through either of the nuclear
receptors retinoic acid receptor (RAR) or retinoid X receptor (RXR),
which are both present in VSMCs, indicates
that all tested compounds can upregulate activity of VSMC ADPR-cyclase
(Table 2). However, unlike in VSMCs, ADPR-cyclase in rat
fibroblasts grown in primary culture was not stimulated by atRA (data
not shown). Finally, we found that the
1,25(OH)2–vitamin D3
(calcitriol) does upregulate ADPR-cyclase in a dose-dependent manner
(Figure 4); however, its precursor with
low biologic activity, 25(OH)–vitamin D3, was
inactive (data not shown).
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CHX). Data are mean±SEM; n=4. *Significant difference
(P<0.05, t test) from controls.
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In Vivo Studies
To determine whether ADPR-cyclase in VSMCs is upregulated by
hormones in vivo, rats were treated with atRA 3 mg (SC)/kg body weight
per 24 hours for 3 days, and ADPR-cyclase activity was determined in
homogenates and in membrane fractions from harvested
tissues.
There was no significant difference between control rats and
atRA-administered rats in ADPR-cyclase activities from spleen, lung,
intestinal smooth muscle, hind-limb skeletal muscle, or liver (Table 3). In atRA-treated rats, ADPR-cyclase
activity was higher in myocardium of left ventricle (+
18%; P<0.05) compared with controls (Table 3).
ADPR-cyclase activity, both in homogenates and membrane
fractions, from aorta was higher (%60%; P<0.05)
than in controls (Figure 5). In another
experiment, TPTX rats were treated with 2 mg (IP)
T3/kg body weight per day for 10 days. The
ADPR-cyclase in homogenates of aorta from
T3-treated rats was higher (+89%;
P<0.05) than in controls, whereas ADPR-cyclase activities
in homogenates from brain and in liver were not different
between control and T3-treated rats (Figure 5).
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) and rats treated with atRA 3 mg/kg body
weight per 3 days (atRA, |
Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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We demonstrate that ADPR-cyclase in rat VSMCs has distinct properties and is sensitive to regulation by several hormones both in vitro and in vivo. According to a recent report of an immunohistochemical study, the commonly occurring CD38 antigen that has ADPR-cyclase activity was not found in vasculature or other smooth muscles,18 thus suggesting that ADPR-cyclase in VSMCs differs from the well-characterized CD38 ADPR-cyclase.2 3 16 17
Indeed, specific activity of ADPR-cyclase in membranes of VSMCs is many
times (>20) higher than CD38 ADPR-cyclase in membranes of HL-60 cells
(Table 1) and was more sensitive to inactivation by
N-glycosidase F (Figure 2D), to thermal inactivation,
and to inhibitory effects of gangliosides (Figures 2A and 2B). Although the molecular basis of these differences
remains to be elucidated, the findings clearly show that VSMC
ADPR-cyclase differs in structure of enzyme-glycoprotein
and/or its insertion into the membrane. Western blot analysis
showed the presence of CD38 both in membranes from HL-60 cells and in
membranes from VSMCs (Figure 2E). Interestingly, unlike CD38
HL-60 ADPR-cyclase, the VSMC ADPR-cyclase was not influenced by
interaction with anti-CD38 Abs directed against C-terminal part of CD38
molecule (Figure 2C) that contains ADPR-cyclase
activity.16 17 28 32
Conceivably, because VSMC ADPR-cyclase is 20-fold more active than CD38
ADPR-cyclase (Table 1), CD38 ADPR-cyclase may well coexist
within rat VSMC membranes with another, distinct VSMC ADPR-cyclase, but
probably constitutes only a minute portion of overall ADPR-cyclase
activity. The most prominent unique property of VSMC ADPR-cyclase is
its sensitivity to inhibition by Zn2+, a property
that is in contrast to all hitherto-described ADPR-cyclases, including
CD38 ADPR-cyclase,33 BST-1 ADPR-cyclase,19 34
Aplysia ADPR-cyclase,34 and ADPR-cyclase
from sea urchin eggs (Table 2, Figure 4); all of these
enzymes are stimulated, rather than inhibited, by
Zn2+.
We propose the presence of a novel variety of ADPR-cyclase in VSMCs
that is distinct from enzymes described to date. The results
presented herein show that VSMC ADPR-cyclase is upregulated by
hormones. The mechanism by which studied hormones/agents upregulated
ADPR-cyclase in VSMCs was not analyzed in the present
study. However, it might be at least assumed that the studied hormones,
ie, retinoids, T3, and vitamin
D3, also exert their upregulatory effect on
ADPR-cyclase by binding to requisite nuclear receptors and via
transcriptional control mechanisms that are typical for hormones of
steroid superfamily.31 Inhibition of the upregulatory
effect of atRA on ADPR-cyclase by actinomycin D and cycloheximide
indeed suggests that regulation of ADPR-cyclase requires ongoing DNA
and protein synthesis (Figure 3).
In conclusion, we report that VSMCs are endowed with highly active ADPR-cyclase and differ in a number of properties from the widespread CD38-antigen ADPR-cyclase.17 18 The VSMC ADPR-cyclase activity is most likely upregulated by retinoids that act through either RAR or RXR, or via heterodimers, and by 2 other hormones, calcitriol and T3. We found the presence of a unique ADPR-cyclase in VSMCs that is subject to regulation by several hormones. The role of this novel cADPR-Ca2+ signaling system in the regulation of VSMC functions is still an open question.
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Acknowledgments |
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This work was supported by National Institute of Diabetes and Digestive and Kidney Diseases Grant DK-30759 and by the Mayo Foundation. F.G.S.d.T., J.C., and E.N.C. were postdoctoral research fellows supported by the Mayo Foundation. E.N.C. was also supported by the National Kidney Foundation. We acknowledge Michael A. Thompson and Henry Walker for providing excellent technical assistance.
Received February 2, 2000; accepted April 12, 2000.
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  S. K. Fellner and W. J. Arendshorst Complex interactions of NO/cGMP/PKG systems on Ca2+ signaling in afferent arteriolar vascular smooth muscle Am J Physiol Heart Circ Physiol, January 1, 2010; 298(1): H144 - H151. [Abstract] [Full Text] [PDF]
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 T. L. Thai and W. J. Arendshorst Mice lacking the ADP ribosyl cyclase CD38 exhibit attenuated renal vasoconstriction to angiotensin II, endothelin-1, and norepinephrine Am J Physiol Renal Physiol, July 1, 2009; 297(1): F169 - F176. [Abstract] [Full Text] [PDF]
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 R. Gul, J.-H. Park, S.-Y. Kim, K. Y. Jang, J.-K. Chae, J.-K. Ko, and U.-H. Kim Inhibition of ADP-ribosyl cyclase attenuates angiotensin II-induced cardiac hypertrophy Cardiovasc Res, February 15, 2009; 81(3): 582 - 591. [Abstract] [Full Text] [PDF]
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T. L. Thai and W. J. Arendshorst ADP-ribosyl cyclase and ryanodine receptors mediate endothelin ETA and ETB receptor-induced renal vasoconstriction in vivo Am J Physiol Renal Physiol, August 1, 2008; 295(2): F360 - F368. [Abstract] [Full Text] [PDF]
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 F. Malavasi, S. Deaglio, A. Funaro, E. Ferrero, A. L. Horenstein, E. Ortolan, T. Vaisitti, and S. Aydin Evolution and Function of the ADP Ribosyl Cyclase/CD38 Gene Family in Physiology and Pathology Physiol Rev, July 1, 2008; 88(3): 841 - 886. [Abstract] [Full Text] [PDF]
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R. Gul, S.-Y. Kim, K.-H. Park, B.-J. Kim, S.-J. Kim, M.-J. Im, and U.-H. Kim A novel signaling pathway of ADP-ribosyl cyclase activation by angiotensin II in adult rat cardiomyocytes Am J Physiol Heart Circ Physiol, July 1, 2008; 295(1): H77 - H88. [Abstract] [Full Text] [PDF]
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S.-Y. Kim, R. Gul, S.-Y. Rah, S. H. Kim, S. K. Park, M.-J. Im, H. J. Kwon, and U.-H. Kim Molecular mechanism of ADP-ribosyl cyclase activation in angiotensin II signaling in murine mesangial cells Am J Physiol Renal Physiol, April 1, 2008; 294(4): F982 - F989. [Abstract] [Full Text] [PDF]
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 M. Liang and J. L. Pietrusz Thiol-Related Genes in Diabetic Complications: A Novel Protective Role for Endogenous Thioredoxin 2 Arterioscler Thromb Vasc Biol, January 1, 2007; 27(1): 77 - 83. [Abstract] [Full Text] [PDF]
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 S. Soares, M. Thompson, T. White, A. Isbell, M. Yamasaki, Y. Prakash, F. E. Lund, A. Galione, and E. N. Chini NAADP as a second messenger: neither CD38 nor base-exchange reaction are necessary for in vivo generation of NAADP in myometrial cells Am J Physiol Cell Physiol, January 1, 2007; 292(1): C227 - C239. [Abstract] [Full Text] [PDF]
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S. K. Fellner and W. J. Arendshorst Angiotensin II, reactive oxygen species, and Ca2+ signaling in afferent arterioles Am J Physiol Renal Physiol, November 1, 2005; 289(5): F1012 - F1019. [Abstract] [Full Text] [PDF]
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 N. Fritz, N. Macrez, J. Mironneau, L. H. Jeyakumar, S. Fleischer, and J.-L. Morel Ryanodine receptor subtype 2 encodes Ca2+ oscillations activated by acetylcholine via the M2 muscarinic receptor/cADP-ribose signalling pathway in duodenum myocytes J. Cell Sci., May 15, 2005; 118(10): 2261 - 2270. [Abstract] [Full Text] [PDF]
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 D. A. Deshpande, T. A. White, S. Dogan, T. F. Walseth, R. A. Panettieri, and M. S. Kannan CD38/cyclic ADP-ribose signaling: role in the regulation of calcium homeostasis in airway smooth muscle Am J Physiol Lung Cell Mol Physiol, May 1, 2005; 288(5): L773 - L788. [Abstract] [Full Text] [PDF]
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S. K. Fellner and W. J. Arendshorst Angiotensin II Ca2+ signaling in rat afferent arterioles: stimulation of cyclic ADP ribose and IP3 pathways Am J Physiol Renal Physiol, April 1, 2005; 288(4): F785 - F791. [Abstract] [Full Text] [PDF]
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 S. K. Fellner and L. Parker Endothelin-1, superoxide and adeninediphosphate ribose cyclase in shark vascular smooth muscle J. Exp. Biol., March 15, 2005; 208(6): 1045 - 1052. [Abstract] [Full Text] [PDF]
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 R. Laporte, A. Hui, and I. Laher Pharmacological Modulation of Sarcoplasmic Reticulum Function in Smooth Muscle Pharmacol. Rev., December 1, 2004; 56(4): 439 - 513. [Abstract] [Full Text] [PDF]
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 H. Barata, M. Thompson, W. Zielinska, Y. S. Han, C. B. Mantilla, Y. S. Prakash, S. Feitoza, G. Sieck, and E. N. Chini The Role of Cyclic-ADP-Ribose-Signaling Pathway in Oxytocin-Induced Ca2+ Transients in Human Myometrium Cells Endocrinology, February 1, 2004; 145(2): 881 - 889. [Abstract] [Full Text] [PDF]
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E. N. Chini and F. G. S. De Toledo Nicotinic acid adenine dinucleotide phosphate: a new intracellular second messenger? Am J Physiol Cell Physiol, June 1, 2002; 282(6): C1191 - C1198. [Abstract] [Full Text] [PDF]
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 S. Dogan, T. A. White, D. A. Deshpande, M. P. Murtaugh, T. F. Walseth, and M. S. Kannan Estrogen Increases CD38 Gene Expression and Leads to Differential Regulation of Adenosine Diphosphate (ADP)-Ribosyl Cyclase and Cyclic ADP-Ribose Hydrolase Activities in Rat Myometrium Biol Reprod, March 1, 2002; 66(3): 596 - 602. [Abstract] [Full Text] [PDF]
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 E. N. Chini Signal Transduction in Smooth Muscle: Selected Contribution: Effect of volatile anesthetics on cADP-ribose-induced Ca2+ release system J Appl Physiol, July 1, 2001; 91(1): 516 - 521. [Abstract] [Full Text] [PDF]
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