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Volume 272, Number 50, Issue of December 12, 1997
pp. 31213-31216
(Received for publication, August 27, 1997, and in revised form, October 8, 1997)
From the ABSTRACT Immunohistochemistry of porcine pulmonary artery
endothelial cells (PAEC) with antibodies specific for caveolin,
endothelial nitric-oxide synthase (eNOS), and the arginine transporter
(CAT1) demonstrates that all of these proteins co-localize in plasma membrane caveolae. When incubated with solubilized PAEC plasma membrane
proteins, eNOS-specific antibody immunoprecipitates CAT1-mediated arginine transport. These results document the existence of a caveolar
complex between CAT1 and eNOS in PAEC that provides a mechanism for the
directed delivery of substrate arginine to eNOS. Direct transfer of
extracellular arginine to membrane-bound eNOS accounts for the
"arginine paradox" and explains why caveolar localization of eNOS
is required for optimal nitric oxide production by endothelial
cells.
INTRODUCTION Pulmonary endothelial cells are a rich source of nitric oxide
(NO),1 a nitrogen-centered
free radical with multiple and unique physiologic and bioregulatory
activities. Pulmonary endothelial cells generate NO from arginine via
the catalytic action of an NADPH-requiring, Ca2+/calmodulin-dependent NO synthase (referred
to as eNOS, ecNOS, or type III NOS) that is membrane-associated (1-3).
In endothelial cells, eNOS-mediated formation of NO from arginine is
dependent upon an adequate and continuing supply of arginine (4-8).
Several studies have shown that the half-saturating arginine
concentration for eNOS is less than 10 µM (9-11). We
(12) and others (13-16) have reported intracellular arginine
concentrations that range from 0.1 to 0.8 mM in cultured
endothelial cells. Consequently, eNOS should be saturated in these
cells, and therefore increasing the extracellular arginine should not
increase NO production any further. However, a number of in
vitro and in vivo studies indicate that NO production
by vascular endothelial cells under physiological conditions can be
increased by extracellular arginine, despite a saturating intracellular
arginine concentration (4-8, 17). Furthermore, a recent report by
Arnal et al. (18) demonstrates that the intracellular
concentration of arginine in endothelial cells can be varied over
100-fold without changing NO production. This observation,
i.e. that extracellular arginine administration seems to
drive NO production even when intracellular levels of arginine are
available in excess, has been termed the "arginine paradox" and
cannot be explained based on the available data (19). One paradigm that
would explain this observation is that in endothelial cells the
intracellular arginine is sequestered in one or more pools that are
poorly, if at all, accessible to eNOS, whereas extracellular arginine
transported into the cell is preferentially delivered to eNOS. Under
this paradigm, a plasma membrane arginine transporter must be in close
spatial alignment with or directly linked to the eNOS protein.
Arginine transport is mediated by several independent transport
activities in mammalian cells (20-22). The distribution and relative
contribution of each of these transport activities to the total
arginine uptake by a particular cell type varies widely due to
cell-specific expression of the corresponding genes. Arginine transport
into endothelial cells has been investigated by several laboratories
(23-26). Transport into porcine pulmonary artery endothelial cells
(PAEC) is mediated by only two agencies (26-28). System y+
has been extensively characterized in PAEC (28) and is responsible for
60-80% of total carrier-mediated arginine uptake (26, 27). In 1991, two laboratories independently documented that the native biologic
function of the previously cloned murine ecotropic retroviral receptor
was System y+ transport activity (29, 30). The mRNA and
corresponding protein, termed CAT1, are expressed in a wide variety of
cells, with the notable exception of liver (29-32).
Woodard et al. (33) documented the expression of CAT1 within
the plasma membrane of PAEC by immunohistochemistry. Interestingly, that study illustrated that the CAT1 transporter protein was not uniformly distributed over the cell surface but instead was
concentrated in randomly distributed clusters within the plasma
membrane. The CAT1 transporter-containing clusters could be dispersed
by nocodazole-induced disruption of the microtubule network, but they
reformed within a few hours after removal of the drug. Recently,
Kizhatil and Albritton2 have
confirmed the cytoskeletal association of CAT1 and demonstrated that
the clusters are required for retrovirus infectivity. With regard to
micro-domains within the plasma membrane, considerable information has
been published regarding the presence of plasma membrane regions
referred to as caveolae (34-38). This specialized membrane region
contains one of a family of structural proteins called caveolins, as
well as numerous signaling proteins and a high cholesterol content.
Within endothelial cells a significant portion of eNOS is localized to
caveolae (9, 39-42). For example, Garcia-Cardena et al.
(41) showed that caveolin and membrane-bound eNOS co-localize in lung
microvascular endothelial cells and that antibodies against one could
be used to immunoprecipitate the other, strongly suggesting that eNOS
is complexed with caveolin (41). Interestingly, for reasons that were
previously not known, caveolar localization optimizes the ability of
eNOS to produce NO (9, 42). We hypothesize that in PAEC the CAT1
transporter-containing clusters represent plasma membrane caveolae. We
also propose that co-localization of CAT1-mediated arginine transport
and eNOS would provide an efficient mechanism for delivery of substrate
for NO synthesis, perhaps even in a direct manner. The following
experiments document co-localization of CAT1 and eNOS within PAEC
caveolae.
MATERIALS AND METHODS PAEC were obtained
from the main pulmonary artery of 6-7-month-old pigs and were cultured
for 3-7 passages as described by Block et al. (12). Cells
were cultured on glass coverslips to a density of approximately 70%
and then subjected to immunohistochemistry using the incubation
conditions and methodology described by Woodard et al. (33).
Mouse monoclonal antibodies against caveolin and eNOS were obtained
from Transduction Laboratory (Lexington, KY). Production and
characterization of a rabbit polyclonal antiserum against a predicted
extracellular loop of the murine CAT1 arginine transporter has been
described previously (33). FITC-labeled goat anti-rabbit IgG (Sigma)
was used to detect anti-CAT1, whereas Texas Red-labeled goat anti-mouse
IgG (ICN Pharmaceuticals, Inc., Aurora, OH) was used to detect
anti-caveolin and anti-eNOS.
Fluorescently stained
cells were analyzed by deconvolution microscopy as described originally
by Agard et al. (43). Three-dimensional light microscopy
(LM) data collection and computational removal of out-of-focus
information used an integrated, cooled CCD-based, fluorescence LM data
collection, processing, and visualization workstation described in
detail elsewhere (Ref. 44; Applied Precision, Inc., Mercer Island, WA).
Three-dimensional data sets were processed as has been described
previously (43, 45). LM images were viewed using an integrated modeling
program (PRISM) specially designed for analyzing complex
three-dimensional biological structures (46).
Plasma membrane
vesides were prepared by sucrose gradient centrifugation as described
by Teitel (47) and modified by Bhat and Block (48, 49). Plasma membrane
proteins were solubilized by the method described by Fafournoux
et al. (50). The solubilized proteins in the supernatant
were precipitated by incubation with 20% polyethylene glycol
(PEG-8000) at 4 °C for 20 min. Immunodepletion of CAT1 transporter
was performed using the protocol of Tamarappoo et al. (51).
Briefly, a 1-ml aliquot of goat anti-mouse IgG covalently liked to
agarose beads (Sigma) was incubated for 1 h with 20 µg of
monoclonal eNOS antibody (Transduction Laboratories) on ice and
centrifuged, after which the supernatant was discarded. The agarose
beads were then washed once with STAB buffer (20% glycerol, 2 mM EDTA, 2 mM dithiothreitol, 0.2% sodium
cholate, 0.25% asolectin, and 10 mM HEPES, pH 7.4) and
mixed with solubilized proteins resuspended in STAB buffer. After
incubation for 1 h on ice, the beads were centrifuged, the
supernatant was removed, and the proteins were reconstituted into
proteoliposomes.
Reconstitution of proteins into proteoliposomes was
performed following the protocol of Fafournoux et al. (50)
and transport assays were performed as described previously (28).
Briefly, plasma membrane vesicles or proteoliposomes (20 µg/30 µl)
were added to 270 µl of external solution containing 140 mM NaSCN, l mM MgSO4, 10 mM HEPES-Tris, pH 7.4, and 50 µM
[3H]L-arginine or 50 µM
[3H]glutamine. After incubation for 3 min at 37 °C,
reactions were terminated by the addition of 5 ml of ice-cold 140 mM NaC1 (stop solution) followed by filtration through
glass fiber Whatman GF/C filters presoaked in 0.3% polyethylenimine to
decrease the nonspecific absorption of
[3H]L-arginine or glutamine. The filters were
washed four times with 5 ml of stop solution, dried, and counted using
liquid scintillation spectrometry. Zero time blank values (membrane
vesicles or proteoliposomes added after stop solution) were subtracted
from all experimental values.
RESULTS AND DISCUSSION Localization of CAT1 in several cell types revealed localized
transporter-containing clusters within the plasma membrane when analyzed by epifluorescence microscopy (33). Fig.
1 illustrates this staining pattern
analyzed at much greater resolution before (Fig. 1A) and
after (Fig. 1B) the use of deconvolution microscopy technology (43-46). As reported previously, the CAT1 transporter is
not uniformly distributed over the entire cell surface. Instead, the
cell surface has discrete regions that contain a high transporter content. Staining with the anti-CAT1 transporter antibody is completely inhibited by preadsorption of the antibody with the corresponding peptide antigen (Fig. 1C), whereas incubation of the
antibody with nonantigen peptide sequences from within the CAT1
transporter does not block cell staining (33).
[View Larger Version of this Image (51K GIF file)]
Immunohistochemistry of the PAEC with antibodies specific for caveolin
also documented intensely staining plasma membrane-associated clusters,
consistent with proposed caveolae structure and localization (Fig.
2A). Co-staining of the PAEC
with anti-CAT1 (Fig. 2B) and anti-caveolin antibodies
resulted in significant overlap with regard to localization of the two
proteins (Fig. 2C). It is clear from these results that the
majority of the clusters containing the arginine transporter coincide
with caveolae in the PAEC plasma membrane. Furthermore, in PAEC we have
confirmed, as reported previously by others (41, 42), the
co-localization of caveolin and eNOS by immunohistochemistry (data not
shown).
[View Larger Version of this Image (77K GIF file)]
The presence of the CAT1 arginine transporter in plasma membrane
caveolae raised the possibility that CAT1 and eNOS may be co-localized
in a caveolar complex to facilitate NO synthesis. Therefore, PAEC were
subjected to immunohistochemistry to test for co-localization of CAT1
and eNOS. A significant portion of the detectable plasma
membrane-associated eNOS was clustered within random regions over the
cell surface (Fig. 3A). As
mentioned above, these eNOS-containing micro-domains have been
identified as caveolae, and the eNOS present can be
co-immunoprecipitated with anti-caveolin antibodies (41, 42). The CAT1
arginine transporter-containing clusters were similar in distribution
(Fig. 3B), and when the stained regions were analyzed for
co-localization of CAT1 and eNOS, a significant degree of overlap was
clearly revealed (Fig. 3C).
[View Larger Version of this Image (54K GIF file)]
Co-localization of the CAT1 arginine transporter and eNOS within
caveolae is consistent with the proposal that these membrane micro-domains are a site for concentrating proteins involved in signaling (34-38). However, the present observations also raise the
intriguing possibility that the CAT1 arginine transporter and eNOS are
physically associated. Such a complex might provide a mechanism for
directed delivery or even channeling of newly acquired extracellular
arginine to eNOS for NO synthesis. Selective delivery of transported
arginine to membrane-bound eNOS could explain the arginine paradox
discussed above (19). As a more direct test for a complex between CAT1
and eNOS, PAEC plasma membrane arginine transport activity was
detergent solubilized and subjected to immunoprecipitation with
anti-eNOS antibody (50). Using the proteins in the immunoprecipitate
supernatant to reconstitute proteoliposomes (51) provided an assay to
check for anti-eNOS-dependent immunodepletion of arginine
transport. Immunodepletion with control mouse IgG caused no loss of
reconstitutable arginine transport, whereas the anti-eNOS monoclonal
antibody caused immunoprecipitation of 73% of the
Na+-independent arginine transport (Table
I). To establish that the anti-eNOS did
not result in immunodepletion of arginine transport in a nonspecific
manner, glutamine transport was monitored in the reconstituted
proteoliposomes after immunoprecipitation with control and anti-eNOS
IgG (Table I). No immunodepletion of glutamine transport was observed.
These data document that a protein-protein association exists between
the CAT1 arginine transporter and membrane-bound eNOS in PAEC.
Table I.
Immunodepletion of CAT1-mediated arginine transport activity by
anti-eNOS antibody
COMMUNICATION:
A Caveolar Complex between the Cationic Amino Acid
Transporter 1 and Endothelial Nitric-oxide Synthase May Explain the
"Arginine Paradox"*
§,
Department of Biochemistry and Molecular
Biology and the Center for Structural Biology and the ¶ Department
of Medicine and the Gainesville VA Medical Center, University of
Florida College of Medicine, Gainesville, Florida 32610-0245
Fig. 1.
CAT1 amino acid transporter exists in
clusters on the surface of PAEC. The data shown represent analysis
of 1-µm sections through the cell. Deconvolution microscopy
methodology is described in the text. A shows the staining
results prior to deconvolution to reveal the outline of the entire cell
body, whereas the results shown in B and C have
been deconvolved. B illustrates the clustering of CAT1
transporters on the PAEC surface. If the antibody was preadsorbed for
16 h at 4 °C with 50 µg/ml of peptide antigen prior to
incubation with the cells, little or no immunoreactive material is
detected (C). Incubation with other nonantigen peptide sequences from within the CAT1 transporter sequence did not block antibody staining (33). PAEC from more than five independent preparations exhibited the same staining pattern.
Fig. 2.
Caveolin and CAT1 amino acid transporter are
co-localized in plasma membrane clusters in PAEC. Using the
methods described under "Materials and Methods," the PAEC were
subjected to immunohistochemistry with antibodies specific for CAT1
(A), caveolin (B), or both (C). Co-localization of the proteins was assayed by using simultaneously a
rabbit polyclonal antibody against CAT1 (15) detected by FITC-labeled goat anti-rabbit IgG and a mouse monoclonal antibody against caveolin detected by Texas Red-labeled goat anti-mouse IgG (C).
Staining from three independent experiments was analyzed by
deconvolution microscopy and shown to be reproducible.
Fig. 3.
CAT1 amino acid transporter and eNOS are
co-localized in the PAEC plasma membrane. By the same methodology
outlined in Fig. 1, PAEC were used to detect the plasma membrane
localization of the cationic amino acid transporter CAT1
(A), eNOS (B), or both (C) by
immunohistochemistry. The cells were stained using a rabbit polyclonal
antibody against CAT1 detected by a goat anti-rabbit IgG linked to FITC
and a mouse monoclonal antibody against eNOS detected by a goat
anti-mouse IgG linked to Texas Red. Staining was analyzed by
decovolution microscopy, and cells from three independent experiments
documented the reproducibility of the results.
Immunoprecipitation prior to
reconstitution
Transport velocity
Control
pmol · mg
1 protein · 3 min1%
Arginine transport
No antibody
3511 ± 50
Mouse
IgG
4084 ± 44
100
Anti-eNOS IgG
1113
± 17a
27
Glutamine transport
Mouse IgG
4026
± 176
100
Anti-eNOS IgG
4368 ± 706
109
a
p < 0.001 versus no antibody or
non-immune mouse IgG, n = 3 independent experiments.
ABSTRACTCaveolae are abundant in lung endothelial cells, and they have been implicated in transcytosis, potocytosis, and signal transduction (34-38). Garcia-Cardena et al. (41) have recently reported a protein-protein interaction between eNOS and caveolin, a caveolar coat protein found in endothelial cells. It is likely that this eNOS-caveolin interaction is responsible for positioning eNOS adjacent to other caveolar proteins such as CAT1 to form a highly efficient signal transduction cascade and to optimize production of the vital signaling molecule NO. Our results demonstrate that the CAT1 arginine transporter is localized to plasma membrane caveolae of PAEC and that treatment of PAEC plasma membrane vesicles with an antibody directed against eNOS depletes CAT1-mediated arginine transport. Taken together, these results document the existence of a caveolar complex between the CAT1 arginine transporter and eNOS in PAEC.
Association of the CAT1 arginine transporter and eNOS in PAEC provides a mechanism for the directed delivery of substrate to eNOS and, for mammalian cells, represents the first example of a functional complex between a plasma membrane transport protein and an enzyme. Such directed delivery of extracellular arginine to eNOS would account for the arginine paradox described earlier (19) and would also explain the observation by Liu et al. (9) that caveolar localization of eNOS is required for optimal NO production by eNOS.
FOOTNOTES
§ These authors contributed equally to this work.
To whom correspondence should be addressed: Dept. of
Biochemistry and Molecular Biology, University of Florida College of Medicine, Box 100245, Gainesville, FL 32610-0245. Tel.: 352-392-2711; Fax: 352-392-6511; E-mail: mkilberg{at}biochem.med.ufl.edu.
1 The abbreviations used are: NO, nitric oxide; PAEC, pulmonary artery endothelial cell(s); eNOS, endothelial nitric-oxide synthase; CAT1, cationic amino acid transporter 1 (System y+); FITC, fluorescein isothiocyanate; LM, light microscopy.
2 K. Kizhatil and L. M. Albritton (1997) J. Virol. 71, 7145-7156.
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Volume 272, Number 50,
Issue of December 12, 1997
pp. 31213-31216
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.
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T. A. John, B. O. Ibe, and J. Usha Raj Oxygen alters caveolin-1 and nitric oxide synthase-3 functions in ovine fetal and neonatal lung microvascular endothelial cells Am J Physiol Lung Cell Mol Physiol, November 1, 2006; 291(5): L1079 - L1093. [Abstract] [Full Text] [PDF]
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M. Kakoki, H.-S. Kim, C.-J. S. Edgell, N. Maeda, O. Smithies, and D. L. Mattson Amino acids as modulators of endothelium-derived nitric oxide Am J Physiol Renal Physiol, August 1, 2006; 291(2): F297 - F304. [Abstract] [Full Text] [PDF]
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W.-Z. Zhang, K. Venardos, J. Chin-Dusting, and D. M. Kaye Adverse Effects of Cigarette Smoke on NO Bioavailability: Role of Arginine Metabolism and Oxidative Stress Hypertension, August 1, 2006; 48(2): 278 - 285. [Abstract] [Full Text] [PDF]
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L. A. Holowatz, C. S. Thompson, and W. L. Kenney L-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilatation in aged human skin J. Physiol., July 15, 2006; 574(2): 573 - 581. [Abstract] [Full Text] [PDF]
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O. Feron and J.-L. Balligand Caveolins and the regulation of endothelial nitric oxide synthase in the heart Cardiovasc Res, March 1, 2006; 69(4): 788 - 797. [Abstract] [Full Text] [PDF]
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K. P. Stanley, L. G. Chicoine, T. L. Young, K. M. Reber, C. R. Lyons, Y. Liu, and L. D. Nelin Gene transfer with inducible nitric oxide synthase decreases production of urea by arginase in pulmonary arterial endothelial cells Am J Physiol Lung Cell Mol Physiol, February 1, 2006; 290(2): L298 - L306. [Abstract] [Full Text] [PDF]
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A. R. White, S. Ryoo, D. Li, H. C. Champion, J. Steppan, D. Wang, D. Nyhan, A. A. Shoukas, J. M. Hare, and D. E. Berkowitz Knockdown of Arginase I Restores NO Signaling in the Vasculature of Old Rats Hypertension, February 1, 2006; 47(2): 245 - 251. [Abstract] [Full Text] [PDF]
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B. G. Zani and H. G. Bohlen Transport of extracellular L-arginine via cationic amino acid transporter is required during in vivo endothelial nitric oxide production Am J Physiol Heart Circ Physiol, October 1, 2005; 289(4): H1381 - H1390. [Abstract] [Full Text] [PDF]
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T. Teerlink ADMA metabolism and clearance Vascular Medicine, July 1, 2005; 10(1_suppl): S73 - S81. [Abstract] [PDF]
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T. Teerlink ADMA metabolism and clearance Vascular Medicine, May 1, 2005; 10(2_suppl): S73 - S81. [Abstract] [PDF]
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M. Kakoki, H.-S. Kim, W. J. Arendshorst, and D. L. Mattson L-Arginine uptake affects nitric oxide production and blood flow in the renal medulla Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2004; 287(6): R1478 - R1485. [Abstract] [Full Text] [PDF]
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E. I. Closs, A. Simon, N. Vekony, and A. Rotmann Plasma Membrane Transporters for Arginine J. Nutr., October 1, 2004; 134(10): 2752S - 2759S. [Abstract] [Full Text] [PDF]
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J. Loscalzo L-Arginine and Atherothrombosis J. Nutr., October 1, 2004; 134(10): 2798S - 2800S. [Abstract] [Full Text] [PDF]
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G. Cherla and E. A. Jaimes Role of L-Arginine in the Pathogenesis and Treatment of Renal Disease J. Nutr., October 1, 2004; 134(10): 2801S - 2806S. [Abstract] [Full Text] [PDF]
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G. Hao, L. Xie, and S. S. Gross Argininosuccinate Synthetase is Reversibly Inactivated by S-Nitrosylation in Vitro and in Vivo J. Biol. Chem., August 27, 2004; 279(35): 36192 - 36200. [Abstract] [Full Text] [PDF]
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V. Hadkar, S. Sangsree, S. M. Vogel, V. Brovkovych, and R. A. Skidgel Carboxypeptidase-mediated enhancement of nitric oxide production in rat lungs and microvascular endothelial cells Am J Physiol Lung Cell Mol Physiol, July 1, 2004; 287(1): L35 - L45. [Abstract] [Full Text] [PDF]
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L. G. Chicoine, M. L. Paffett, T. L. Young, and L. D. Nelin Arginase inhibition increases nitric oxide production in bovine pulmonary arterial endothelial cells Am J Physiol Lung Cell Mol Physiol, July 1, 2004; 287(1): L60 - L68. [Abstract] [Full Text] [PDF]
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M. M. Parnell, J. P. F. Chin-Dusting, J. Starr, and D. M. Kaye In vivo and in vitro evidence for ACh-stimulated L-arginine uptake Am J Physiol Heart Circ Physiol, July 1, 2004; 287(1): H395 - H400. [Abstract] [Full Text] [PDF]
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J. H. Newman, B. L. Fanburg, S. L. Archer, D. B. Badesch, R. J. Barst, J. G.N. Garcia, P. N. Kao, J. A. Knowles, J. E. Loyd, M. D. McGoon, et al. Pulmonary Arterial Hypertension: Future Directions: Report of a National Heart, Lung and Blood Institute/Office of Rare Diseases Workshop Circulation, June 22, 2004; 109(24): 2947 - 2952. [Full Text] [PDF]
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C. D. Fike, J. L. Aschner, Y. Zhang, and M. R. Kaplowitz Impaired NO signaling in small pulmonary arteries of chronically hypoxic newborn piglets Am J Physiol Lung Cell Mol Physiol, June 1, 2004; 286(6): L1244 - L1254. [Abstract] [Full Text] [PDF]
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S. I. Zharikov, K. Y. Krotova, L. Belayev, and E. R. Block Pertussis toxin activates L-arginine uptake in pulmonary endothelial cells through downregulation of PKC-{alpha} activity Am J Physiol Lung Cell Mol Physiol, May 1, 2004; 286(5): L974 - L983. [Abstract] [Full Text] [PDF]
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H. Hu, M. Xin, L. L. Belayev, J. Zhang, E. R. Block, and J. M. Patel Autoinhibitory domain fragment of endothelial NOS enhances pulmonary artery vasorelaxation by the NO-cGMP pathway Am J Physiol Lung Cell Mol Physiol, May 1, 2004; 286(5): L1066 - L1074. [Abstract] [Full Text] [PDF]
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B. L. Goodwin, L. P. Solomonson, and D. C. Eichler Argininosuccinate Synthase Expression Is Required to Maintain Nitric Oxide Production and Cell Viability in Aortic Endothelial Cells J. Biol. Chem., April 30, 2004; 279(18): 18353 - 18360. [Abstract] [Full Text] [PDF]
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S.E.S. Miner, A. Al-Hesayen, S. Kelly, T. Benson, J.J. Thiessen, V.R. Young, and J.D. Parker L-Arginine Transport in the Human Coronary and Peripheral Circulation Circulation, March 16, 2004; 109(10): 1278 - 1283. [Abstract] [Full Text] [PDF]
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M. Noris, M. Todeschini, P. Cassis, F. Pasta, A. Cappellini, S. Bonazzola, D. Macconi, R. Maucci, F. Porrati, A. Benigni, et al. L-Arginine Depletion in Preeclampsia Orients Nitric Oxide Synthase Toward Oxidant Species Hypertension, March 1, 2004; 43(3): 614 - 622. [Abstract] [Full Text] [PDF]
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S. Fujii, L. Zhang, J. Igarashi, and H. Kosaka L-Arginine Reverses p47phox and gp91phox Expression Induced by High Salt in Dahl Rats Hypertension, November 1, 2003; 42(5): 1014 - 1020. [Abstract] [Full Text] [PDF]
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D. E. Berkowitz, R. White, D. Li, K. M. Minhas, A. Cernetich, S. Kim, S. Burke, A. A. Shoukas, D. Nyhan, H. C. Champion, et al. Arginase Reciprocally Regulates Nitric Oxide Synthase Activity and Contributes to Endothelial Dysfunction in Aging Blood Vessels Circulation, October 21, 2003; 108(16): 2000 - 2006. [Abstract] [Full Text] [PDF]
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T. Abe, H. Hikiji, W. S. Shin, N. Koshikiya, S.-i. Shima, J. Nakata, T. Susami, T. Takato, and T. Toyo-oka Targeting of iNOS with antisense DNA plasmid reduces cytokine-induced inhibition of osteoblastic activity Am J Physiol Endocrinol Metab, September 1, 2003; 285(3): E614 - E621. [Abstract] [Full Text] [PDF]
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B. C. Kone, T. Kuncewicz, W. Zhang, and Z.-Y. Yu Protein interactions with nitric oxide synthases: controlling the right time, the right place, and the right amount of nitric oxide Am J Physiol Renal Physiol, August 1, 2003; 285(2): F178 - F190. [Abstract] [Full Text] [PDF]
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K. Y. Krotova, S. I. Zharikov, and E. R. Block Classical isoforms of PKC as regulators of CAT-1 transporter activity in pulmonary artery endothelial cells Am J Physiol Lung Cell Mol Physiol, June 1, 2003; 284(6): L1037 - L1044. [Abstract] [Full Text] [PDF]
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J. Lee, H. Ryu, R. J. Ferrante, S. M. Morris Jr., and R. R. Ratan From the Cover: Translational control of inducible nitric oxide synthase expression by arginine can explain the arginine paradox PNAS, April 15, 2003; 100(8): 4843 - 4848. [Abstract] [Full Text] [PDF]
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H. KOSAKA, H. YONEYAMA, L. ZHANG, S. FUJII, A. YAMAMOTO, and J. IGARASHI Induction of LOX-1 and iNOS expressions by ischemia-reperfusion of rat kidney and the opposing effect of L-arginine FASEB J, April 1, 2003; 17(6): 636 - 643. [Abstract] [Full Text] [PDF]
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M. Sabbatini, A. Pisani, F. Uccello, G. Fuiano, R. Alfieri, A. Cesaro, B. Cianciaruso, and V. E. Andreucci Arginase inhibition slows the progression of renal failure in rats with renal ablation Am J Physiol Renal Physiol, April 1, 2003; 284(4): F680 - F687. [Abstract] [Full Text] [PDF]
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D. Schwartz, I. F. Schwartz, E. Gnessin, Y. Wollman, T. Chernichovsky, M. Blum, and A. Iaina Differential regulation of glomerular arginine transporters (CAT-1 and CAT-2) in lipopolysaccharide-treated rats Am J Physiol Renal Physiol, April 1, 2003; 284(4): F788 - F795. [Abstract] [Full Text] [PDF]
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P. I. Nedvetsky, W. C. Sessa, and H. H. H. W. Schmidt There's NO binding like NOS binding: Protein-protein interactions in NO/cGMP signaling PNAS, December 24, 2002; 99(26): 16510 - 16512. [Full Text] [PDF]
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K. Kizhatil and L. M. Albritton System y+ localizes to different membrane subdomains in the basolateral plasma membrane of epithelial cells Am J Physiol Cell Physiol, December 1, 2002; 283(6): C1784 - C1794. [Abstract] [Full Text] [PDF]
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T. Gori and J. D. Parker The Puzzle of Nitrate Tolerance: Pieces Smaller Than We Thought? Circulation, October 29, 2002; 106(18): 2404 - 2408. [Full Text] [PDF]
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J. Sun and J. K. Liao Functional interaction of endothelial nitric oxide synthase with a voltage-dependent anion channel PNAS, October 1, 2002; 99(20): 13108 - 13113. [Abstract] [Full Text] [PDF]
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E. Noiri, H. Satoh, J.-i. Taguchi, S. V. Brodsky, A. Nakao, Y. Ogawa, S. Nishijima, T. Yokomizo, K. Tokunaga, and T. Fujita Association of eNOS Glu298Asp Polymorphism With End-Stage Renal Disease Hypertension, October 1, 2002; 40(4): 535 - 540. [Abstract] [Full Text] [PDF]
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L. Wagner, J. D. Klein, J. M. Sands, and C. Baylis Urea transporters are distributed in endothelial cells and mediate inhibition of L-arginine transport Am J Physiol Renal Physiol, September 1, 2002; 283(3): F578 - F582. [Abstract] [Full Text] [PDF]
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L. C. Pendleton, B. L. Goodwin, B. R. Flam, L. P. Solomonson, and D. C. Eichler Endothelial Argininosuccinate Synthase mRNA 5'-Untranslated Region Diversity. INFRASTRUCTURE FOR TISSUE-SPECIFIC EXPRESSION J. Biol. Chem., July 5, 2002; 277(28): 25363 - 25369. [Abstract] [Full Text] [PDF]
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M. S. Goligorsky, H. Li, S. Brodsky, and J. Chen Relationships between caveolae and eNOS: everything in proximity and the proximity of everything Am J Physiol Renal Physiol, July 1, 2002; 283(1): F1 - F10. [Abstract] [Full Text] [PDF]
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H. Masuda, T. Tsujii, T. Okuno, K. Kihara, M. Goto, and H. Azuma Accumulated endogenous NOS inhibitors, decreased NOS activity, and impaired cavernosal relaxation with ischemia Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2002; 282(6): R1730 - R1738. [Abstract] [Full Text] [PDF]
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C. B. Cymeryng, S. P. Lotito, C. Colonna, C. Finkielstein, Y. Pomeraniec, N. Grion, L. Gadda, P. Maloberti, and E. J. Podesta Expression of Nitric Oxide Synthases in Rat Adrenal Zona Fasciculata Cells Endocrinology, April 1, 2002; 143(4): 1235 - 1242. [Abstract] [Full Text] [PDF]
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R. Sala, B. M. Rotoli, E. Colla, R. Visigalli, A. Parolari, O. Bussolati, G. C. Gazzola, and V. Dall'Asta Two-way arginine transport in human endothelial cells: TNF-alpha stimulation is restricted to system y+ Am J Physiol Cell Physiol, January 1, 2002; 282(1): C134 - C143. [Abstract] [Full Text] [PDF]
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S. Chowdhary, S. L. Nuttall, J. H. Coote, and J. N. Townend L-Arginine Augments Cardiac Vagal Control in Healthy Human Subjects Hypertension, January 1, 2002; 39(1): 51 - 56. [Abstract] [Full Text] [PDF]
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L. D. Nelin, H. E. Nash, and L. G. Chicoine Cytokine treatment increases arginine metabolism and uptake in bovine pulmonary arterial endothelial cells Am J Physiol Lung Cell Mol Physiol, November 1, 2001; 281(5): L1232 - L1239. [Abstract] [Full Text] [PDF]
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C. E. P. de Figueiredo, B. E. P. da Costa, L. Comerlato, E. Micheli, and E. Barros Low dose L-arginine reduces blood pressure and endothelin-1 production in hypertensive uraemic rats Nephrol. Dial. Transplant., October 1, 2001; 16(10): 2110 - 2111. [Full Text] [PDF]
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M. Jayachandran, T. Hayashi, D. Sumi, A. Iguchi, and V. M. Miller Temporal effects of 17{beta}-estradiol on caveolin-1 mRNA and protein in bovine aortic endothelial cells Am J Physiol Heart Circ Physiol, September 1, 2001; 281(3): H1327 - H1333. [Abstract] [Full Text] [PDF]
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S. Xiao, L. Wagner, J. Mahaney, and C. Baylis Uremic levels of urea inhibit L-arginine transport in cultured endothelial cells Am J Physiol Renal Physiol, June 1, 2001; 280(6): F989 - F995. [Abstract] [Full Text] [PDF]
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S. I. Zharikov, A. A. Sigova, S. Chen, M. R. Bubb, and E. R. Block Cytoskeletal regulation of the L-arginine/NO pathway in pulmonary artery endothelial cells Am J Physiol Lung Cell Mol Physiol, March 1, 2001; 280(3): L465 - L473. [Abstract] [Full Text] [PDF]
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H. Li, S. Brodsky, M. Basco, V. Romanov, D. A. De Angelis, and M. S. Goligorsky Nitric Oxide Attenuates Signal Transduction : Possible Role in Dissociating Caveolin-1 Scaffold Circ. Res., February 2, 2001; 88(2): 229 - 236. [Abstract] [Full Text] [PDF]
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R. Govers and T. J. Rabelink Cellular regulation of endothelial nitric oxide synthase Am J Physiol Renal Physiol, February 1, 2001; 280(2): F193 - F206. [Abstract] [Full Text] [PDF]
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 L. J. Van Winkle Amino Acid Transport Regulation and Early Embryo Development Biol Reprod, January 1, 2001; 64(1): 1 - 12. [Abstract] [Full Text]
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R. E. Rumbaut, J. Wang, and V. H. Huxley Differential effects of L-NAME on rat venular hydraulic conductivity Am J Physiol Heart Circ Physiol, October 1, 2000; 279(4): H2017 - H2023. [Abstract] [Full Text] [PDF]
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J. P. Cooke Does ADMA Cause Endothelial Dysfunction? Arterioscler. Thromb. Vasc. Biol., September 1, 2000; 20(9): 2032 - 2037. [Abstract] [Full Text] [PDF]
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P. T.-Y. Ayuk, C. P. Sibley, P. Donnai, S. D'Souza, and J. D. Glazier Development and polarization of cationic amino acid transporters and regulators in the human placenta Am J Physiol Cell Physiol, June 1, 2000; 278(6): C1162 - C1171. [Abstract] [Full Text] [PDF]
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 F. H. Guo, S. A. A. Comhair, S. Zheng, R. A. Dweik, N. T. Eissa, M. J. Thomassen, W. Calhoun, and S. C. Erzurum Molecular Mechanisms of Increased Nitric Oxide (NO) in Asthma: Evidence for Transcriptional and Post-Translational Regulation of NO Synthesis J. Immunol., June 1, 2000; 164(11): 5970 - 5980. [Abstract] [Full Text] [PDF]
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 C. D. Fike, M. R. Kaplowitz, L. A. Rehorst-Paea, and L. D. Nelin L-Arginine increases nitric oxide production in isolated lungs of chronically hypoxic newborn pigs J Appl Physiol, May 1, 2000; 88(5): 1797 - 1803. [Abstract] [Full Text] [PDF]
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P. G. Lloyd and C. D. Hardin Sorting of metabolic pathway flux by the plasma membrane in cerebrovascular smooth muscle cells Am J Physiol Cell Physiol, April 1, 2000; 278(4): C803 - C811. [Abstract] [Full Text] [PDF]
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L. Eckmann, F. Laurent, T. D. Langford, M. L. Hetsko, J. R. Smith, M. F. Kagnoff, and F. D. Gillin Nitric Oxide Production by Human Intestinal Epithelial Cells and Competition for Arginine as Potential Determinants of Host Defense Against the Lumen-Dwelling Pathogen Giardia lamblia J. Immunol., February 1, 2000; 164(3): 1478 - 1487. [Abstract] [Full Text] [PDF]
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E. I. Closs, J.-S. Scheld, M. Sharafi, and U. Förstermann Substrate Supply for Nitric-Oxide Synthase in Macrophages and Endothelial Cells: Role of Cationic Amino Acid Transporters Mol. Pharmacol., January 1, 2000; 57(1): 68 - 74. [Abstract] [Full Text]
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A. A. Ogonowski, W. H. Kaesemeyer, L. Jin, V. Ganapathy, F. H. Leibach, and R. W. Caldwell Effects of NO donors and synthase agonists on endothelial cell uptake of L-Arg and superoxide production Am J Physiol Cell Physiol, January 1, 2000; 278(1): C136 - C143. [Abstract] [Full Text] [PDF]
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S. I. Zharikov and E. R. Block Association of L-arginine transporters with fodrin: implications for hypoxic inhibition of arginine uptake Am J Physiol Lung Cell Mol Physiol, January 1, 2000; 278(1): L111 - L117. [Abstract] [Full Text] [PDF]
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M. Teubl, K. Groschner, S. D. Kohlwein, B. Mayer, and K. Schmidt Na+/Ca2+ Exchange Facilitates Ca2+-dependent Activation of Endothelial Nitric-oxide Synthase J. Biol. Chem., October 8, 1999; 274(41): 29529 - 29535. [Abstract] [Full Text] [PDF]
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M. Higaki and K. Shimokado Phosphatidylinositol 3-Kinase Is Required for Growth Factor–Induced Amino Acid Uptake by Vascular Smooth Muscle Cells Arterioscler. Thromb. Vasc. Biol., September 1, 1999; 19(9): 2127 - 2132. [Abstract] [Full Text] [PDF]
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J. Leiper and P. Vallance Biological significance of endogenous methylarginines that inhibit nitric oxide synthases Cardiovasc Res, August 15, 1999; 43(3): 542 - 548. [Abstract] [Full Text] [PDF]
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H. Drexler Nitric oxide and coronary endothelial dysfunction in humans Cardiovasc Res, August 15, 1999; 43(3): 572 - 579. [Full Text] [PDF]
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P. Musialek, D. J Paterson, and B. Casadei Changes in extracellular pH mediate the chronotropic responses to L-arginine Cardiovasc Res, August 15, 1999; 43(3): 712 - 720. [Abstract] [Full Text] [PDF]
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